Pathogenesis of Various Bacterial Agents in CSF during Meningitis

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Research Paper 10/08/2022
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Pathogenesis of Various Bacterial Agents in CSF during Meningitis

Syeda Ayesha Ali, Muhammad Kamran Taj, Safa Farooqi, Ashiq Hussain, Saima Azam, Syeda Hafsa Ali
Int. J. Biosci.21( 2), 80-120, August 2022.
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Abstract

The human central nervous system (CNS) infections remain the leading cause of intensified morbidity and mortality rates around the world. Vanquish the barriers that protect the brain from pathogens is a prerequisite to develop meningitis. The commonest pathogens, pneumococcus, meningococcus, E. coli, H. influenzae are main causative agents in children and adults; are associated with high morbidity and mortality. Bacteria have evolved a variety of different strategies for breaching the blood–brain barrier (BBB), evade the immune system and enter CNS. For this purpose, they use a variety of different virulence factors, allowing them to adhere to and overcome these barriers. These virulence factors arbitrate adhesion host cell invasion, intracellular survival, host cell signaling and induction of inflammation. The CNS will ultimately be invaded by the bacteria, causing inflammation of meninges, increased permeability of BBB, and pleocytosis in cerebrospinal fluid (CSF) as well as nervous tissue infiltration. Some of these mechanisms are different, but others are shared by some pathogens. Supplementary understanding of these processes, especially, differences between the blood-brain barrier and the blood-cerebrospinal fluid barrier, and Virulence factors used by pathogens are still required.

VIEWS 177

Aguilar J, Urday-Cornejo V, Donabedian S, Perri M, Tibbetts R, Zervos M. 2010. Staphylococcus aureus meningitis: case series and literature review. Medicine 89(2), 117-125.

Al-Obaidi MMJ, Desa MNM. 2018. Mechanisms of blood brain barrier disruption by different types of bacteria, and bacterial–host interactions facilitate the bacterial pathogen invading the brain. Cellular and molecular neurobiology, 38(7), 1349-1368.

Alexander HE. 1965. The haemophilus group. Bacterial and mycotic infections of man 724-741.

Amagai M, Matsuyoshi N, Wang Z, Andl C, Stanley J. 2000. Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1. Nature medicine 6(11), 1275-1277.

Anderson P, Pichichero M, Connor E. 1985. Enhanced nasopharyngeal colonization of rats by piliated Haemophilus influenzae type b. Infection and immunity 48(2), 565-568.

Andersson B, Dahmen J, Frejd T, Leffler H, Magnusson G, Noori G, Eden CS. 1983. Identification of an active disaccharide unit of a glycoconjugate receptor for pneumococci attaching to human pharyngeal epithelial cells. The Journal of experimental medicine 158(2), 559-570.

Bachman MA, Breen P, Deornellas V, Mu Q, Zhao L, Wu W, Mobley HL. 2015. Genome-wide identification of Klebsiella pneumoniae fitness genes during lung infection. MBio 6(3), e00775-00715.

Bagley ST. 1985. Habitat association of Klebsiella species. Infection Control & Hospital Epidemiology, 6(2), 52-58.

Barichello T, dos Santos I, Savi GD, Simões LR, Silvestre T, Comim CM, Quevedo J. 2010. TNF-α, IL-1β, IL-6, and cinc-1 levels in rat brain after meningitis induced by Streptococcus pneumoniae. Journal of neuroimmunology 221(1-2), 42-45.

Bergmann S, Lang A, Rohde M, Agarwal V, Rennemeier C, Grashoff C, Hammerschmidt S. 2009. Integrin-linked kinase is required for vitronectin-mediated internalization of Streptococcus pneumoniae by host cells. Journal of cell science, 122(2), 256-267.

Bernard SC, Simpson N, Join-Lambert O, Federici C, Laran-Chich MP, Maïssa N, Taouji S. 2014. Pathogenic Neisseria meningitidis utilizes CD147 for vascular colonization. Nature medicine, 20(7), 725-731.

Bialek-Davenet S, Criscuolo A, Ailloud F, Passet V, Jones L, Delannoy-Vieillard A.-S, Nicolas-Chanoine MH. 2014. Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerging infectious diseases 20(11), 1812.

Bloch O, Papadopoulos MC, Manley GT, Verkman A. 2005. Aquaporin‐4 gene deletion in mice increases focal edema associated with staphylococcal brain abscess. Journal of neurochemistry 95(1), 254-262.

Bonacorsi S, Clermont O, Houdouin V, Cordevant C, Brahimi N. Marecat A, Bingen, E. 2003. Molecular analysis and experimental virulence of French and North American Escherichia coli neonatal meningitis isolates: identification of a new virulent clone. The Journal of infectious diseases 187(12), 1895-1906.

Bradley CJ, Griffiths NJ, Rowe HA, Heyderman RS, Virji M. 2005. Critical determinants of the interactions of capsule‐expressing Neisseria meningitidis with host cells: the role of receptor density in increased cellular targeting via the outer membrane Opa proteins. Cellular microbiology 7(10), 1490-1503.

Bricker J, Mulks M, Moxon E, Plaut A, Wright A. 1985. Physical and genetic analysis of DNA regions encoding the immunoglobulin A proteases of different specificities produced by Haemophilus influenzae. Infection and immunity 47(2), 370-374.

Bricker J, Mulks M, Plaut A, Moxon E, Wright A. 1983. IgA1 proteases of Haemophilus influenzae: cloning and characterization in Escherichia coli K-12. Proceedings of the national academy of sciences, 80(9), 2681-2685.

Brinton Jr CC, Carter MJ, Derber DB, Kar S, Kramarik JA, To Acc, Wood SW. 1989. Design and development of pilus vaccines for Haemophilus influenzae diseases. The Pediatric infectious disease journal 8(1), S62.

Brown DR, Helaine S, Carbonnelle E, Pelicic V. 2010. Systematic functional analysis reveals that a set of seven genes is involved in fine-tuning of the multiple functions mediated by type IV pili in Neisseria meningitidis. Infection and immunity, 78(7), 3053-3063.

Capecchi B, AduBobie J, Di Marcello F, Ciucchi L, Masignani V, Taddei A, Aricò B. 2005. Neisseria meningitidis NadA is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells. Molecular microbiology, 55(3), 687-698.

Caporarello N, Olivieri M, Cristaldi M, Scalia M, Toscano M, Genovese C, Anfuso C. 2018. Blood–brain barrier in a Haemophilus influenzae type a in vitro infection: role of adenosine receptors A2A and A2B. Molecular neurobiology 55(6), 5321-5336.

Carbonnelle E, Helaine S, Nassif X, Pelicic V. 2006. A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Molecular microbiology, 61(6), 1510-1522.

Caugant DA, Maiden MC. 2009. Meningococcal carriage and disease—population biology and evolution. Vaccine, 27, B64-B70.

Chang WN, Huang CR, Lu CH, Chien CC. (2012). Adult Klebsiella pneumoniae meningitis in Taiwan: an overview. Acta Neurol Taiwan 21(2), 87-96.

Chang WN, Lu CH, Huang CR, Tsai NW, Chuang YC, Chang CC, Chien CC. 2008. Changing epidemiology of adult bacterial meningitis in southern Taiwan: a hospital-based study. Infection, 36(1), 15-22.

Chanyangam M, Smith A, MoseleyS, Kuehn M, Jenny P. 1991. Contribution of a 28-kilodalton membrane protein to the virulence of Haemophilus influenzae. Infection and immunity 59(2), 600-608.

Chen YT, Chang HY, Lai YC, Pan CC, Tsai SF, Peng HL. 2004. Sequencing and analysis of the large virulence plasmid pLVPK of Klebsiella pneumoniae CG43. Gene, 337, 189-198.

Chen YT, Lai YC, Tan MC, Hsieh LY, Wang JT, Shiau YR, Huang IW. 2017. Prevalence and characteristics of pks genotoxin gene cluster-positive clinical Klebsiella pneumoniae isolates in Taiwan. Scientific reports 7(1), 1-10.

Cheng H, Chen Y, Wu C, Chang H, Lai Y, Peng HL. 2010. RmpA regulation of capsular polysaccharide biosynthesis in Klebsiella pneumoniae CG43. Journal of bacteriology 192(12), 3144-3158.

Cherubin CE, Marr JS, Sierra MF, Becker S. 1981. Listeria and gram-negative bacillary meningitis in New York City, 1972–1979: frequent causes of meningitis in adults. The American journal of medicine 71(2), 199-209.

Cho JS, Pietras EM, Garcia NC, Ramos RI, Farzam DM, Monroe HR, Cheung AL. 2010. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. The Journal of Clinical Investigation 120(5), 1762-1773.

Comanducci M, Bambini S, Brunelli B, Adu-Bobie J, Aricò B, Capecchi B, Savino S. 2002. NadA, a novel vaccine candidate of Neisseria meningitidis. The Journal of experimental medicine, 195(11), 1445-1454.

Cope LD, Yogev R, Mertsola J, Argyle JC, McCracken Jr G, Hansen E. 1990. Effect of mutations in lipooligosaccharide biosynthesis genes on virulence of Haemophilus influenzae type b. Infection and immunity 58(7), 2343-2351.

Cortés G, Borrell N, de Astorza B, Gómez C, Sauleda J, Albertí S. 2002. Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infection and immunity 70(5), 2583-2590.

Coulton J, Wan D. 1983. The outer membrane of Haemophilus influenzae type b: cell envelope associations of major proteins. Canadian Journal of Microbiology 29(2), 280-287.

Coureuil M, Bourdoulous S, Marullo S, Nassif X. 2014. Invasive meningococcal disease: a disease of the endothelial cells. Trends in Molecular Medicine, 20(10), 571-578.

Coureuil M, Lécuyer H, Scott MG, Boularan C, Enslen H, Soyer M, Marullo S. 2010. Meningococcus hijacks a β2-adrenoceptor/β-arrestin pathway to cross brain microvasculature endothelium. Cell, 143(7), 1149-1160.

Coureuil M, Mikaty G, Miller F, Lécuyer H, Bernard C, Bourdoulous S, Romero IA. 2009. Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science, 325(5936), 83-87.

Courtney HS, Von Hunolstein C, Dale JB, Bronze MS, Beachey EH, Hasty DL. 1992. Lipoteichoic acid and M protein: dual adhesins of group A streptococci. Microbial pathogenesis 12(3), 199-208.

Coutinho LG, Grandgirard D, Leib SL, Agnez-Lima LF. 2013. Cerebrospinal-fluid cytokine and chemokine profile in patients with pneumococcal and meningococcal meningitis. BMC infectious diseases, 13(1), 1-9.

Cundell DR, Gerard NP, Gerard C, Idanpaan-Heikkila I, Tuomanen EI. 1995. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature, 377(6548), 435-438.

Cundell DR, Weiser JN, Shen J, Young A, Tuomanen EI. 1995. Relationship between colonial morphology and adherence of Streptococcus pneumoniae. Infection and immunity 63(3), 757-761.

Dacey RG, Sande MA. 1974. Effect of probenecid on cerebrospinal fluid concentrations of penicillin and cephalosporin derivatives. Antimicrobial agents and chemotherapy 6(4), 437-441.

Dajani AS, Asmar BI, Thirumoorthi M. 1979. Systemic Haemophilus influenzae disease: an overview. The Journal of pediatrics 94(3), 355-364.

Dao TT, Liebenthal D, Tran TK, Ngoc Thi Vu, B., Ngoc Thi Nguyen, D., Thi Tran, H. K, Horby P. 2014. Klebsiella pneumoniae oropharyngeal carriage in rural and urban Vietnam and the effect of alcohol consumption. PloS one, 9(3), e91999.

de Astorza B, Cortés G, Crespí C, Saus C, Rojo, JM, Albertí S. 2004. C3 promotes clearance of Klebsiella pneumoniae by A549 epithelial cells. Infection and immunity 72(3), 1767-1774.

de Lorenzo V. 1984. Isolation and characterization of microcin E 492 fromKlebsiella pneumoniae. Archives of microbiology 139(1), 72-75.

Decker CF. 2008. Pathogenesis of MRSA infections. Disease-a-month, 12(54), 774-779.

Diep BA, Otton M. 2008. The role of virulence determinants in community-associated MRSA pathogenesis. Trends in microbiology 16(8), 361-369.

Dietzman DE, Fischer GW, Schoenknecht F. D. 1974. Neonatal Escherichia coli septicemia—bacterial counts in blood. The Journal of pediatrics, 85(1), 128-130.

Dixon GLJ. 2000. The influence of bacterial structure on the host inflammatory response to Neisseria meningitidis: University of London, University College London (United Kingdom).

Doran KS, Banerjee A, Disson O, Lecuit M. 2013. Concepts and mechanisms: crossing host barriers. Cold Spring Harbor perspectives in medicine 3(7), a010090.

Doran KS, Fulde M, Gratz N, Kim BJ, Nau R, Prasadarao N, Valentin-Weigand P. 2016. Host–pathogen interactions in bacterial meningitis. Acta neuropathologica 131(2), 185-209.

Drevets DA, Leenen PJ. 2000. Leukocyte-facilitated entry of intracellular pathogens into the central nervous system. Microbes and Infection, 2(13), 1609-1618.

Durand ML, Calderwood SB, Weber DJ, Miller SI, Southwick FS, Caviness Jr, VS, Swartz MN. 1993. Acute bacterial meningitis in adults–A review of 493 episodes. New England Journal of Medicine, 328(1), 21-28.

Edwards MS, Rench MA, Haffar AA, Murphy, MA, Desmond MM, Baker CJ. 1985. Long-term sequelae of group B streptococcal meningitis in infants. The Journal of pediatrics 106(5), 717-722.

Eugène E, Hoffmann I, Pujol C, Couraud PO, Bourdoulous S, Nassif X. 2002. Microvilli-like structures are associated with the internalization of virulent capsulated Neisseria meningitidis into vascular endothelial cells. Journal of cell science 115(6), 1231-1241.

Fagan RP, Lambert MA, Smith SG. 2008. The hek outer membrane protein of Escherichia coli strain RS218 binds to proteoglycan and utilizes a single extracellular loop for adherence, invasion, and autoaggregation. Infection and immunity 76(3), 1135-1142.

Fang CT, Chen YC, Chang SC, Sau WY, Luh KT. 2000. Klebsiella pneumoniae meningitis: timing of antimicrobial therapy and prognosis. Qjm, 93(1), 45-53.

Fang CT, Chuang YP, Shun CT, Chang SC, Wang JT. 2004. A novel virulence gene in Klebsiella pneumoniae strains causing primary liver abscess and septic metastatic complications. The Journal of experimental medicine 199(5), 697-705.

Fang CT, Lai SY, Yi WC, Hsueh PR, Liu KL, Chang SC. 2007. Klebsiella pneumoniae genotype K1: an emerging pathogen that causes septic ocular or central nervous system complications from pyogenic liver abscess. Clinical infectious diseases 45(3), 284-293.

Fazili T, Sharngoe C, Endy T, Kiska D, Javaid W, Polhemus M. 2016. Klebsiella pneumoniae liver abscess: an emerging disease. The American journal of the medical sciences 351(3), 297-304.

Fedtke I, Mader D, Kohler T, Moll H, Nicholson G, Biswas R, Peschel A. 2007. A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity. Molecular microbiology 65(4), 1078-1091.

Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Merrick JM. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269(5223), 496-512.

Foster TJ, Geoghegan JA, Ganesh VK, Höök M. 2014. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nature Reviews Microbiology 12(1), 49-62.

Fraser D. 1982. Haemophilus influenzae in the community and the home. Haemophilus influenzae: epidemiology, immunology, and prevention of disease. New York: Elsevier Biomedical, 11-22.

Furyk J, Swann O, Molyneux E. 2011. Systematic review: neonatal meningitis in the developing world. Tropical Medicine & International Health 16(6), 672-679.

Gordon RJ, Lowy FD. 2008. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clinical infectious diseases 46(5), S350-S359.

Gosink KK., Mann ER, Guglielmo C, Tuomanen EI, Masure HR. 2000. Role of novel choline binding proteins in virulence of Streptococcus pneumoniae. Infection and immunity 68(10), 5690-5695.

Grandgirard D, Gäumann R, Coulibaly B, Dangy JP, Sie A, Junghanss T, Leib SL. 2013. The causative pathogen determines the inflammatory profile in cerebrospinal fluid and outcome in patients with bacterial meningitis. Mediators of inflammation, 2013.

Grassmé H, Becker KA. 2013. Bacterial infections and ceramide. Sphingolipids in disease 305-320.

Gratz N, Loh LN, Tuomanen E. 2015. Pneumococcal invasion: development of bacteremia and meningitis. In Streptococcus Pneumoniae (p 433-451) Elsevier.

Gross R, Ward LR, Threlfall E, Cheasty T, Rowe B. 1983. Drug resistance among Escherichia coil strains isolated from cerebrospinal fluid. Epidemiology & Infection 90(2), 195-198.

Gründling A, Schneewind O. 2007. Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus. Journal of bacteriology 189(6), 2521-2530.

Grundy F, Plaut A, Wright A. 1990. Localization of the cleavage site specificity determinant of Haemophilus influenzae immunoglobulin A1 protease genes. Infection and immunity 58(2), 320-331.

Gu D, Dong N, Zheng Z, Lin D, Huang M, Wang L, Zhang R. 2018. A fatal outbreak of ST11 carbapenem-resistant hypervirulent Klebsiella pneumoniae in a Chinese hospital: a molecular epidemiological study. The Lancet infectious diseases, 18(1), 37-46.

Gulig PA, Hansen EJ. 1985. Coprecipitation of lipopolysaccharide and the 39,000-molecular-weight major outer membrane protein of Haemophilus influenzae type b by lipopolysaccharide-directed monoclonal antibody. Infection and immunity 49(3), 819-827.

Haas PJ, de Haas CJ, Kleibeuker W, Poppelier MJJG, Van Kessel KPM, Kruijtzer JAW, Van Strijp JAG. 2004. N-Terminal Residues of the Chemotaxis Inhibitory Protein of <em>Staphylococcus aureus</em> Are Essential for Blocking Formylated Peptide Receptor but Not C5a Receptor. The Journal of Immunology 173(9), 5704-5711. http://dx.doi.org/10.4049/jimmunol.173.9.5704.

Hadi HA, Wooldridge KG, Robinson K, Ala’Aldeen DA. 2001. Identification and characterization of App: an immunogenic autotransporter protein of Neisseria meningitidis. Molecular microbiology 41(3), 611-623.

Hauck CR, Agerer F, Muenzner P, Schmitter T. 2006. Cellular adhesion molecules as targets for bacterial infection. European journal of cell biology 85(3-4), 235-242.

Häuser S, Wegele C, Stump-Guthier C, Borkowski J, Weiss C, Rohde M, Adam R. 2018. Capsule and fimbriae modulate the invasion of Haemophilus influenzae in a human blood-cerebrospinal fluid barrier model. International Journal of Medical Microbiology 308(7), 829-839.

Hoegen T, Tremel N, Klein M, Angele B, Wagner H, Kirschning C, Koedel U. 2011. The NLRP3 inflammasome contributes to brain injury in pneumococcal meningitis and is activated through ATP-dependent lysosomal cathepsin B release. The Journal of Immunology 187(10), 5440-5451.

Hornick DB, Allen BL, Horn MA, Clegg S. 1992. Adherence to respiratory epithelia by recombinant Escherichia coli expressing Klebsiella pneumoniae type 3 fimbrial gene products. Infection and immunity 60(4), 1577-1588.

Hsieh PF, Lin HH, Lin TL, Wang JT. 2010. CadC regulates cad and tdc operons in response to gastrointestinal stresses and enhances intestinal colonization of Klebsiella pneumoniae. The Journal of infectious diseases 202(1), 52-64.

Hsieh PF, Lin TL, Lee CZ, Tsai SF, Wang JT. 2008. Serum-induced iron-acquisition systems and TonB contribute to virulence in Klebsiella pneumoniae causing primary pyogenic liver abscess. Journal of Infectious Diseases 197(12), 1717-1727.

Hsieh PF, Lin TL, Yang FL, Wu MC, Pan YJ, Wu SH, Wang JT. 2012. Lipopolysaccharide O1 antigen contributes to the virulence in Klebsiella pneumoniae causing pyogenic liver abscess. PLoS One 7(3), e33155.

Hsu CR, Chang IW, Hsieh PF, Lin TL, Liu PY, Huang CH, Wang JT. 2019. A novel role for the Klebsiella pneumoniae Sap (sensitivity to antimicrobial peptides) transporter in intestinal cell interactions, innate immune responses, liver abscess, and virulence. The Journal of infectious diseases, 219(8), 1294-1306.

Humphries HE, Triantafilou M, Makepeace BL, Heckels JE, Triantafilou K, Christodoulides M. 2005. Activation of human meningeal cells is modulated by lipopolysaccharide (LPS) and non‐LPS components of Neisseria meningitidis and is independent of Toll‐like receptor (TLR) 4 and TLR2 signalling. Cellular microbiology, 7(3), 415-430.

Idänpään-Heikkilä I, Simon PM, Zopf D, Vullo T, Cahill P, Sokol K. 1997. Oligosaccharides interfere with the establishment and progression of experimental pneumococcal pneumonia Journal of  Infectious Diseases 176(3), 704-712.

Iovino F, Molema G, Bijlsma JJ. 2014. Platelet endothelial cell adhesion molecule-1, a putative receptor for the adhesion of Streptococcus pneumoniae to the vascular endothelium of the blood-brain barrier. Infection and immunity 82(9), 3555-3566.

Iovino F, Orihuela CJ, Moorlag HE, Molema G, Bijlsma JJ. 2013. Interactions between blood-borne Streptococcus pneumoniae and the blood-brain barrier preceding meningitis. PloS one 8(7), e68408.

Jacobsson G, Gustafsson E, Andersson R. 2008. Outcome for invasive Staphylococcus aureus infections. European journal of clinical microbiology & infectious diseases 27(9), 839-848.

Jen FE, Warren MJ, Schulz BL, Power PM, Swords WE, Weiser JN, Jennings MP. 2013. Dual pili post-translational modifications synergize to mediate meningococcal adherence to platelet activating factor receptor on human airway cells. PLoS pathogens 9(5), e1003377.

Jonquieres R, Bierne H, Fiedler F, Gounon P, Cossart P. 1999. Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: a novel mechanism of protein association at the surface of Gram‐positive bacteria. Molecular microbiology 34(5), 902-914.

KällströmH, Liszewski MK, Atkinson JP, Jonsson AB. 1997. Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Molecular microbiology 25(4), 639-647.

Kidd TJ, Mills G, SáPessoa J, Dumigan A, Frank CG, Insua JL, Bengoechea JA. 2017. A Klebsiella pneumoniae antibiotic resistance mechanism that subdues host defences and promotes virulence. EMBO molecular medicine 9(4), 430-447.

Kielian T, Hickey WF. 2000. Proinflammatory cytokine, chemokine, and cellular adhesion molecule expression during the acute phase of experimental brain abscess development. The American journal of pathology 157(2), 647-658.

Kilian M, Mestecky J, Russell M. 1988. Defense mechanisms involving Fc-dependent functions of immunoglobulin A and their subversion by bacterial immunoglobulin A proteases. Microbiological reviews 52(2), 296-303.

Kilian M, Reinholdt J, Lomholt H, Poulsen K, Frandsen EVG. 1996. Biological significance of IgA1 proteases in bacterial colonization and pathogenesis: critical evaluation of experimental evidence. Apmis, 104(16), 321-338.

Kim KS. 2001. Escherichia coli translocation at the blood-brain barrier. Infection and immunity, 69(9), 5217-5222.

Kim KS. 2002. Strategy of Escherichia coli for crossing the blood-brain barrier. The Journal of infectious diseases 186(2), S220-S224.

Kim KS. 2003. Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nature Reviews Neuroscience 4(5), 376-385.

Kim KS. 2008. Mechanisms of microbial traversal of the blood–brain barrier. Nature Reviews Microbiology 6(8), 625-634.

Kim KS. 2014. How pathogens penetrate the blood-brain barrier: To reach the central nervous system, meningitis-causing strains of E. coli and other pathogens exploit microbial and host factors. Microbe, 9(12), 487-492.

Kim KS, Itabashi H, Gemski P, Sadoff J, Warren RL, Cross AS. 1992. The K1 capsule is the critical determinant in the development of Escherichia coli meningitis in the rat. The Journal of Clinical Investigation, 90(3), 897-905.

Kim KS, Kang JH, Cross AS, Kaufman B, Zollinger W, Sadoff J. 1988. Functional activities of monoclonal antibodies to the O side chain of Escherichia coli lipopolysaccharides in vitro and in vivo. Journal of Infectious Diseases 157(1), 47-53.

Klauser T, Pohlner J, Meyer F. 1993. The secretion pathway of IgA protease‐type proteins in gram‐negative bacteria. Bioessays 15(12), 799-805.

Klein M, Paul R, Angele B, Popp B, Pfister HW, Koedel U. 2006. Protein expression pattern in experimental pneumococcal meningitis. Microbes and Infection 8(4), 974-983.

Klein RS, Garber C, Howard N. 2017. Infectious immunity in the central nervous system and brain function. Nature immunology 18(2), 132-141.

Koedel U, Frankenberg T, Kirschnek S, Obermaier B, Häcker H, Paul R, Häcker G. 2009. Apoptosis is essential for neutrophil functional shutdown and determines tissue damage in experimental pneumococcal meningitis. PLoS pathogens, 5(5), e1000461.

Könnecke H, Bechmann I. 2013. The role of microglia and matrix metalloproteinases involvement in neuroinflammation and gliomas. Clinical and Developmental Immunology, 2013.

Koppe U, Suttorp N, Opitz B. 2012. Recognition of Streptococcus pneumoniae by the innate immune system. Cellular microbiology 14(4), 460-466.

Korhonen TK, Valtonen MV, Parkkinen J, Väisänen-Rhen V, Finne J, Orskov F, Mäkelä, PH. 1985. Serotypes, hemolysin production, and receptor recognition of Escherichia coli strains associated with neonatal sepsis and meningitis. Infection and immunity 48(2), 486-491.

Kostyanev TS, Sechanova LP. 2012. Virulence factors and mechanisms of antibiotic resistance of Haemophilus influenzae. Folia Med (Plovdiv) 54(1), 19-23.

Kostyukova N, Volkova M, Ivanova V, Kvetnaya A. 1995. A study of pathogenic factors of Streptococcus pneumoniae strains causing meningitis. FEMS Immunology & Medical Microbiology 10(2), 133-137.

Krishnan S, Chen S, Turcatel G, Arditi M, Prasadarao NV. 2013. Regulation of T oll‐like receptor 2 interaction with Ecgp96 controls E scherichia coli K 1 invasion of brain endothelial cells. Cellular microbiology 15(1), 63-81.

Krishnan S, Liu F, Abrol R, Hodges J, Goddard WA, Prasadarao NV. 2014. The Interaction of N-Glycans in Fcγ Receptor I α-Chain with Escherichia coli K1 Outer Membrane Protein A for Entry into Macrophages. Journal of Biological Chemistry 289(45), 30937-30949.

Krishnan S, Prasadarao NV. 2012. Outer membrane protein A and OprF: versatile roles in Gram‐negative bacterial infections. The FEBS journal, 279(6), 919-931.

Krishnan S, Prasadarao NV. 2014. Identification of minimum carbohydrate moiety in N-glycosylation sites of brain endothelial cell glycoprotein 96 for interaction with Escherichia coli K1 outer membrane protein A. Microbes and Infection 16(7), 540-552.

Krishnan S, Shanmuganathan MV, Behenna, D, Stoltz BM, Prasadarao NV. 2014. Angiotensin II receptor type 1—a novel target for preventing neonatal meningitis in mice by Escherichia coli K1. The Journal of infectious diseases 209(3), 409-419.

Krogfelt KA. 1991. Bacterial adhesion: genetics, biogenesis, and role in pathogenesis of fimbrial adhesins of Escherichia coli. Reviews of infectious diseases 13(4), 721-735.

Lagos R, Baeza M, Corsini G, Hetz C, Strahsburger E, Castillo JA, Monasterio O. 2001. Structure, organization and characterization of the gene cluster involved in the production of microcin E492, a channel‐forming bacteriocin. Molecular microbiology 42(1), 229-243.

Lai YC, Lin AC, Chiang MK, Dai YH, Hsu CC, Lu MC, Chen YT. 2014. Genotoxic Klebsiella pneumoniae in Taiwan. PloS one 9(5), e96292.

Lai YC, Peng HL, Chang HY. 2003. RmpA2, an activator of capsule biosynthesis in Klebsiella pneumoniae CG43, regulates K2 cps gene expression at the transcriptional level. Journal of bacteriology, 185(3), 788-800.

Lam M, Wyres KL, Duchêne S, Wick RR, Judd LM, Gan YH, Kalimuddin S. 2018. Population genomics of hypervirulent Klebsiella pneumoniae clonal-group 23 reveals early emergence and rapid global dissemination. Nature communications 9(1), 1-10.

Lane JR, Tata M, Briles DE, Orihuela CJ. 2022. A Jack of All Trades: The Role of Pneumococcal Surface Protein A in the Pathogenesis of Streptococcus pneumoniae. Frontiers in Cellular and Infection Microbiology, 12. http://dx.doi.org/10.3389/fcimb.2022.826264

Lécuyer H, Nassif X,Coureuil M. 2012. Two strikingly different signaling pathways are induced by meningococcal type IV pili on endothelial and epithelial cells. Infection and immunity 80(1), 175-186.

Lee CH, Chuah SK, Tai WC, Chang CC, Chen FJ. 2017. Delay in human neutrophil constitutive apoptosis after infection with Klebsiella pneumoniae serotype K1. Frontiers in cellular and infection microbiology 7, 87.

Leib SL, Leppert D, Clements J, Täuber MG. 2000. Matrix metalloproteinases contribute to brain damage in experimental pneumococcal meningitis. Infection and immunity 68(2), 615-620.

Leppert D, Leib S, Grygar C, Miller K, Schaad U, Holländer G. 2000. Matrix metalloproteinase (MMP)-8 and MMP-9 in cerebrospinal fluid during bacterial meningitis: association with blood-brain barrier damage and neurological sequelae. Clinical infectious diseases 31(1), 80-84.

Liechti FD, Grandgirard D, Leppert D, Leib S. L. 2014. Matrix metalloproteinase inhibition lowers mortality and brain injury in experimental pneumococcal meningitis. Infection and immunity, 82(4), 1710-1718.

Lin CT, Chen YC, Jinn TR, Wu CC, Hong YM, Wu WH. 2013. Role of the cAMP-dependent carbon catabolite repression in capsular polysaccharide biosynthesis in Klebsiella pneumoniae. PLoS One, 8(2), e54430.

Lin CT, Huang TY, Liang WC, Peng HL. 2006. Homologous response regulators KvgA, KvhA and KvhR regulate the synthesis of capsular polysaccharide in Klebsiella pneumoniae CG43 in a coordinated manner. Journal of biochemistry, 140(3), 429-438.

Lin CT, Wu CC, Chen YS, Lai YC, Chi C, Lin JC, Peng HL. 2011. Fur regulation of the capsular polysaccharide biosynthesis and iron-acquisition systems in Klebsiella pneumoniae CG43. Microbiology 157(2), 419-429.

Lin JC, Chang FY, Fung CP, Yeh KM, Chen CT, TsaiYK, Siu LK. 2010. Do neutrophils play a role in establishing liver abscesses and distant metastases caused by Klebsiella pneumoniae? PLoS One 5(11), e15005.

Lin TL, Lee CZ, Hsieh PF, Tsai SF, Wang JT. 2008. Characterization of integrative and conjugative element ICE Kp1-associated genomic heterogeneity in a Klebsiella pneumoniae strain isolated from a primary liver abscess. Journal of bacteriology 190(2), 515-526.

Lindsay JA, Holden MT. 2004. Staphylococcus aureus: superbug, super genome? Trends in microbiology  12(8), 378-385.

Liu X, Chauhan VS, Young AB,  Marriott I. 2010. NOD2 mediates inflammatory responses of primary murine glia to Streptococcus pneumoniae. Glia  58(7), 839-847.

Liu YC, Yen MY, Wang RS. 1991. Septic metastatic lesions of pyogenic liver abscess: their association with Klebsiella pneumoniae bacteremia in diabetic patients. Archives of internal medicine 151(8), 1557-1559.

Llobet E, Martínez Moliner V, Moranta D, Dahlström KM, Regueiro V, Tomás A, Fernández Carrasco H. 2015. Deciphering tissue-induced Klebsiella pneumoniae lipid A structure. Proceedings of the National Academy of Sciences 112(46), E6369-E6378.

Loeb M, Zachary  A,  Smith D. 1981. Isolation and partial characterization of outer and inner membranes from encapsulated Haemophilus influenzae type b. Journal of bacteriology  145(1), 596-604.

Lowy FD. 1998. Staphylococcus aureus infections. New England Journal of Medicine 339(8), 520-532.

Lu CH, Chang, WN, Chang HW. 2000. Adult bacterial meningitis in southern Taiwan: epidemiologic trend and prognostic factors. Journal of the neurological sciences  182(1), 36-44.

Lu MC, Chen YT, Chiang MK, Wang YC, Hsiao, PY, Huang YJ,  Lai YC. 2017. Colibactin contributes to the hypervirulence of pks+ K1 CC23 Klebsiella pneumoniae in mouse meningitis infections. Frontiers in Cellular and Infection Microbiology 7, 103.

Ma LC, Fang CT, Lee CZ, Shun CT,  Wang JT. 2005. Genomic heterogeneity in Klebsiella pneumoniae strains is associated with primary pyogenic liver abscess and metastatic infection. The Journal of infectious diseases 192(1), 117-128.

Mahdi LK, Wang H, Van der Hoek MB, Paton, JC, Ogunniyi AD. 2012. Identification of a novel pneumococcal vaccine antigen preferentially expressed during meningitis in mice. The Journal of Clinical Investigation 122(6), 2208-2220.

Mairey E, Genovesio A, Donnadieu E, Bernard C, Jaubert F, Pinardm E, Duménil G. 2006. Cerebral microcirculation shear stress levels determine Neisseria meningitidis attachment sites along the blood–brain barrier. The Journal of experimental medicine 203(8), 1939-1950.

Mangi RJ, Quintiliani R,  Andriole VT. 1975. Gram-negative bacillary meningitis. The American journal of medicine 59(6), 829-836.

March C, Cano V, Moranta D, Llobet  E, Pérez Gutiérrez C, Tomás JM, Bengoechea JA. (2013). Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. PLoS One 8(2), e56847.

Martin RM, Bachman MA. 2018. Colonization, infection, and the accessory genome of Klebsiella pneumoniae. Frontiers in Cellular and Infection Microbiology 8(4).

Martin RM, Cao J, Wu W, Zhao L, Manthei DM, Pirani A, Bachman MA. 2018. Identification of pathogenicity-associated loci in Klebsiella pneumoniae from hospitalized patients. Msystems 3(3), e00015-00018.

Maruvada R, Argon Y,  Prasadarao NV. 2008. Escherichia coli interaction with human brain microvascular endothelial cells induces signal transducer and activator of transcription 3 association with the C‐terminal domain of Ec‐gp96, the outer membrane protein A receptor for invasion. Cellular microbiology  10(11), 2326-2338.

McCormick JK,  JMY, Schlievert PM. 2001. Toxic Shock Syndrome and Bacterial Superantigens: An Update. Annual review of microbiology  55(1), 77-104. http://dx.doi.org/10.1146/annurev.micro.55.1.77

McLoughlin A, Rochfort KD, McDonnell CJ, Kerrigan S.W, Cummins PM. 2017. Staphylococcus aureus‐mediated blood–brain barrier injury: an in vitro human brain microvascular endothelial cell model. Cellular microbiology 19(3), e12664.

Mills G, Dumigan A, Kidd T, Hobley L, Bengoechea JA. 2017. Identification and characterization of two Klebsiella pneumoniae lpxL lipid A late acyltransferases and their role in virulence. Infection and immunity 85(9), e00068-00017.

Mitchell L, Smith SH, Braun JS, Herzog KH., Weber JR,  Tuomanen EI. 2004. Dual phases of apoptosis in pneumococcal meningitis. The Journal of infectious diseases 190(11), 2039-2046.

Mittal R, Gonzalez Gomez I, Goth KA,  Prasadarao NV. 2010. Inhibition of inducible nitric oxide controls pathogen load and brain damage by enhancing phagocytosis of Escherichia coli K1 in neonatal meningitis. The American journal of pathology  176(3), 1292-1305.

Mittal R, Gonzalez Gomez I, Panigrahy A, Goth K, Bonnet R, Prasadarao NV. 2010. IL-10 administration reduces PGE-2 levels and promotes CR3-mediated clearance of Escherichia coli K1 by phagocytes in meningitis. Journal of Experimental Medicine 207(6), 1307-1319.

Mittal R, Prasadarao NV. 2011. gp96 expression in neutrophils is critical for the onset of Escherichia coli K1 (RS218) meningitis. Nature communications 2(1), 1-11.

Mombelli G, Klastersky J, Coppens L, Daneau D,  Nubourgh Y. 1983. Gram-negative bacillary meningitis in neurosurgical patients. Journal of neurosurgery 59(4), 634-641.

Montgomerie JZ. 1979. Epidemiology of Klebsiella and hospital-associated infections. Reviews of infectious diseases  1(5), 736-753.

Mook Kanamori B, Geldhoff M, Troost  D, van Der Poll T, van de Beek D. 2012. Characterization of a pneumococcal meningitis mouse model. BMC infectious diseases  12(1), 1-10.

Mook  Kanamori  BB, Geldhoff  M, van der Poll T,  van de Beek D. 2011. Pathogenesis and pathophysiology of pneumococcal meningitis. Clinical microbiology reviews 24(3), 557-591.

Moon SY,  Chung D,  Kim  SW, Chang H,  Lee H, Jung D,  Heo S. 2010. Changing etiology of community-acquired bacterial meningitis in adults: a nationwide multicenter study in Korea. European journal of clinical microbiology & infectious diseases 29(7), 793-800.

Moranta D, Regueiro V, March C, Llobet E, Margareto J, Larrate E, Bengoechea JA. 2010. Klebsiella pneumoniae capsule polysaccharide impedes the expression of β-defensins by airway epithelial cells. Infection and immunity 78(3), 1135-1146.

Moxon E, Smith A, Averill D, Smith D. 1974. Haemophilus influenzae meningitis in infant rats after intranasal inoculation. Journal of Infectious Diseases 129(2), 154-162.

Moxon ER. 1997. Haemophilus influenzae. Principles and Practice of Infectious Disease.

Moxon ER, Ostrow PT. 1977. Haemophilus influenzae meningitis in infant rats: role of bacteremia in pathogenesis of age-dependent inflammatory responses in cerebrospinal fluid. Journal of Infectious Diseases 135(2), 303-307.

Murphy TF, Dudas KC, Mylotte JM,  Apicella MA. 1983. A subtyping system for nontypable Haemophilus influenzae based on outer-membrane proteins. Journal of Infectious Diseases 147(5), 838-846.

Naber CK. 2009. Staphylococcus aureus bacteremia: epidemiology, pathophysiology, and management strategies. Clinical infectious diseases 48(4), S231-S237.

Nandi A, Dey S, Biswas J, Jaiswal P, Naaz S, Yasmin T, Bishayi B. 2015. Differential induction of inflammatory cytokines and reactive oxygen species in murine peritoneal macrophages and resident fresh bone marrow cells by acute staphylococcus aureus infection: contribution of toll-like receptor 2 (TLR2). Inflammation 38(1), 224-244.

Nau R,  Brück W. 2002. Neuronal injury in bacterial meningitis: mechanisms and implications for therapy. Trends in neurosciences 25(1), 38-45.

Orihuela CJ, Mahdavi J, Thornton J, Mann B, Wooldridge KG, Abouseada N, Tuomanen EI. 2009. Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. The Journal of Clinical Investigation 119(6), 1638-1646.

Østergaard C, Benfield T, Gesser B, Kharazmi A, Frimodt Møller N, Espersen F,  Lundgren  JD. 1999. Pretreatment with granulocyte colony-stimulating factor attenuates the inflammatory response but not the bacterial load in cerebrospinal fluid during experimental pneumococcal meningitis in rabbits. Infection and immunity 67(7), 3430-3436.

Otto M. 2004. Quorum-sensing control in Staphylococci – a target for antimicrobial drug therapy? FEMS microbiology letters 241(2), 135-141. http://dx.doi.org/10.1016/j.femsle.2004.11.016

Otto M. 2010. Looking toward basic science for potential drug discovery targets against community‐associated MRSA. Medicinal research reviews 30(1), 1-22.

Paczosa MK,  Mecsas J. 2016. Klebsiella pneumoniae: going on the offense with a strong defense. Microbiology and Molecular Biology Reviews 80(3), 629-661.

Pan YJ, Lin TL, Hsu CR,  Wang JT. 2011. Use of a Dictyostelium model for isolation of genetic loci associated with phagocytosis and virulence in Klebsiella pneumoniae. Infection and immunity 79(3), 997-1006.

Parisi DN,  Martinez LR. 2014. Intracellular Haemophilus influenzae invades the brain: is zyxin a critical blood brain barrier component regulated by TNF-α? Virulence 5(6), 645-647.

Park WB, Kim SH, Cho JH, Bang JH, Kim H. B, Kim NJ, Choe KW. 2007. Effect of salicylic acid on invasion of human vascular endothelial cells by Staphylococcus aureus. FEMS Immunology & Medical Microbiology 49(1), 56-61.

Patel R. 2005. Biofilms and antimicrobial resistance. Clinical Orthopaedics and Related Research® 437, 41-47.

Paul R, Koedel U, Pfister HW. 2003. Using knockout mice to study experimental meningitis. Archivum immunologiae et therapiae experimentalis-english edition  51(5), 315-326.

Pautsch A, Schulz GE. 2000. High-resolution structure of the OmpA membrane domain. Journal of molecular biology 298(2), 273-282.

Pedersen M, Benfield TL, Skinhoej P,  Jensen AG. 2006. Haematogenous Staphylococcus aureus meningitis. A 10-year nationwide study of 96 consecutive cases. BMC infectious diseases 6(1), 1-7.

Pelicic V. 200. Type IV pili: e pluribus unum? Molecular microbiology 68(4), 827-837.

Peltola H. 2000. Worldwide Haemophilus influenzae type b disease at the beginning of the 21st century: global analysis of the disease burden 25 years after the use of the polysaccharide vaccine and a decade after the advent of conjugates. Clinical microbiology reviews 13(2), 302-317.

Petersdorf RG, Swarner DR,  Garcia M. 1962. Studies on the pathogenesis of meningitis. II. Development of meningitis during pneumococcal bacteremia. The Journal of clinical investigation 41(2), 320-327.

Pfeiffer R. 1892. Vorläufige mittheilungen über die erreger der influenza. DMW-Deutsche Medizinische Wochenschrift 18(02), 28-28.

Pittman M. 1931. Variation and type specificity in the bacterial species Hemophilus influenzae. Journal of Experimental Medicine 53(4), 471-492.

Pizza M,  Rappuoli R. 2015. Neisseria meningitidis: pathogenesis and immunity. Current opinion in microbiology 23, 68-72.

Plaut AG. 1983. The IgA1 proteases of pathogenic bacteria. Annual review of microbiology 37(1), 603-622.

Podschun R,  Ullmann U. 1998. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clinical microbiology reviews 11(4), 589-603.

Pohlner J, Halter  R, Beyreuther K,  Meyer TF. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325(6103), 458-462.

Pomakova D, Hsiao C, Beanan J, Olson R, MacDonald U, Keynan Y,  Russo T. 2012. Clinical and phenotypic differences between classic and hypervirulent Klebsiella pneumonia: an emerging and under-recognized pathogenic variant. European journal of clinical microbiology & infectious diseases 31(6), 981-989.

Prasadarao NV, Blom AM, Villoutreixm BO,  Linsangan LC. 2002. A novel interaction of outer membrane protein A with C4b binding protein mediates serum resistance of Escherichia coli K1. The Journal of Immunology 169(11), 6352-6360.

Prasadarao NV, Srivastava PK, Rudrabhatla RS, Kim KS, Huang Sh,  Sukumaran SK. 2003. Cloning and expression of the Escherichia coli K1 outer membrane protein A receptor, a gp96 homologue. Infection and immunity 71(4), 1680-1688.

Prasadarao NV, Wass CA,  Kim KS. 1996. Endothelial cell GlcNAc beta 1-4GlcNAc epitopes for outer membrane protein A enhance traversal of Escherichia coli across the blood-brain barrier. Infection and immunity 64(1), 154-160.

Prasadarao NV, Wass CA, Weiser JN, Stins MF, Huang SH,  Kim KS. 1996. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infection and immunity 64(1), 146-153.

Proctor RA, Kahl B, von Eiff C, Vaudaux PE, Lew DP,  Peters G. 1998. Staphylococcal Small Colony Variants Have Novel Mechanisms for Antibiotic Resistance. Clinical infectious diseases 27(1), S68-S74. http://dx.doi.org/10.1086/514906

Pron B, Taha MK, Rambaud C, Fournet JC, Pattey N, Monnet JP, Nassif X. 1997. Interaction of Neisseria meningitidis with the components of the blood-brain barrier correlates with an increased expression of PilC. Journal of Infectious Diseases 176(5), 1285-1292.

Quagliarello V, Scheld WM. 1992. Bacterial meningitis: pathogenesis, pathophysiology, and progress. New England Journal of Medicine 327(12), 864-872.

Radin JN, Orihuela CJ, Murti G, Guglielmo C, Murray PJ,  Tuomanen EI. 2005. β-Arrestin 1 participates in platelet-activating factor receptor-mediated endocytosis of Streptococcus pneumoniae. Infection and immunity 73(12), 7827-7835.

Raisch J, Buc E, Bonnet M, Sauvanet P, Vazeille E, de Vallée A, Bonnet R. 2014. Colon cancer-associated B2 Escherichia coli colonize gut mucosa and promote cell proliferation. World Journal of Gastroenterology: WJG, 20(21), 6560.

Read  RC, Wilson R, Rutman A, Lund V, Todd HC, Brain AP, Cole PJ. 1991. Interaction of nontypable Haemophilus influenzae with human respiratory mucosa in vitro. Journal of Infectious Diseases 163(3), 549-558.

Reddy  MA, Prasadarao NV, Wass CA, Kim KS. 2000. Phosphatidylinositol 3-kinase activation and interaction with focal adhesion kinase in Escherichia coli K1 invasion of human brain microvascular endothelial cells. Journal of Biological Chemistry 275(47), 36769-36774.

Reddy MA,  Wass CA, Kim KS, Schlaepfer  DD,  Prasadarao NV. 2000. Involvement of focal adhesion kinase in Escherichia coli invasion of human brain microvascular endothelial cells. Infection and immunity 68(11), 6423-6430.

Reinholdt J,  Kilian M. 1997. Comparative analysis of immunoglobulin A1 protease activity among bacteria representing different genera, species, and strains. Infection and immunity 65(11), 4452-4459.

Rochfort KD, Collins LE, McLoughlin A,  Cummins PM. 2016. Tumour necrosis factor‐α‐mediated disruption of cerebrovascular endothelial barrier integrity in vitro involves the production of proinflammatory interleukin‐6. Journal of neurochemistry 136(3), 564-572.

Rochfort KD,  Cummins PM. 2015. Cytokine-mediated dysregulation of zonula occludens-1 properties in human brain microvascular endothelium. Microvascular research 100, 48-53.

Rock C, Thom KA, Masnick M, Johnson JK, Harris AD,  Morgan DJ. 2014. Frequency of Klebsiella pneumoniae carbapenemase (KPC)–producing and non-KPC-producing Klebsiella species contamination of healthcare workers and the environment. Infection Control & Hospital Epidemiology 35(4), 426-429.

Ropes MW. 1958. 1958 revision of diagnostic criteria for rheumatoid arthritis. Bull Rheum Dis 9, 175-176.

Rosen DA, Pinkner JS, Jones JM, Walker JN, Clegg S,  Hultgren SJ. 2008. Utilization of an intracellular bacterial community pathway in Klebsiella pneumoniae urinary tract infection and the effects of FimK on type 1 pilus expression. Infection and immunity 76(7), 3337-3345.

Rosenow C, Ryan P, Weiser JN, Johnson S, Fontan P, Ortqvist A,  Masure HR. 1997. Contribution of novel choline‐binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Molecular microbiology 25(5), 819-829.

Rosenstein NE, Perkins BA, Stephens DS, Popovic T,  Hughes JM. 2001. Meningococcal disease. New England journal of medicine 344(18), 1378-1388.

Roth TL. 2013. Epigenetic mechanisms in the development of behavior: advances, challenges, and future promises of a new field. Development and psychopathology 25(4pt2), 1279-1291.

Rubinstein E. 2008. Staphylococcus aureus bacteraemia with known sources. International journal of antimicrobial agents 32, S18-S20.

Russo TA, Olson R, Fang CT, Stoesser N, Miller M, MacDonald U,  Johnson JR. 2018. Identification of biomarkers for differentiation of hypervirulent Klebsiella pneumoniae from classical K. pneumoniae. Journal of clinical microbiology 56(9), e00776-00718.

Russo TA, Shon AS, Beanan JM, Olson R, MacDonald U, Pomakov AO, Visitacion MP. 2011. Hypervirulent K. pneumoniae secretes more and more active iron-acquisition molecules than “classical” K. pneumoniae thereby enhancing its virulence. PLoS One 6(10), e26734.

Sa E Cunha C, Griffiths  NJ,  Virji M. 2010. Neisseria meningitidis Opc invasin binds to the sulphated tyrosines of activated vitronectin to attach to and invade human brain endothelial cells. PLoS pathogens 6(5), e1000911.

Sadarangani M, Pollard AJ,  Gray Owen SD. 2011. Opa proteins and CEACAMs: pathways of immune engagement for pathogenic Neisseria. FEMS microbiology reviews 35(3), 498-514.

Saginur R,  Suh KN. 2008. Staphylococcus aureus bacteraemia of unknown primary source: where do we stand? International journal of antimicrobial agents 32, S21-S25.

Sahly H, Podschun R, Oelschlaeger TA, Greiwe M, Parolis H, Hasty D, Sela S. 2000. Capsule impedes adhesion to and invasion of epithelial cells by Klebsiella pneumoniae. Infection and immunity 68(12), 6744-6749.

Sarff L, Mccracken G, Schiffer M, Glode M, Robbins J, Ørskov I,  Ørskov F. 1975. Epidemiology of Escherichia coli K1 in healthy and diseased newborns. The Lancet 305(7916), 1099-1104.

Sarkari J, Pandit N, Moxon ER,  Achtman M. 1994. Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly‐cytidine. Molecular microbiology 13(2), 207-217.

Scarborough  M,  Thwaites GE. 2008. The diagnosis and management of acute bacterial meningitis in resource-poor settings. The Lancet Neurology 7(7), 637-648.

Scarselli M, Serruto D, Montanari P, Capecchi B, Adu Bobie J, Veggi D, Aricò B. 2006. Neisseria meningitidis NhhA is a multifunctional trimeric autotransporter adhesin. Molecular microbiology  61(3), 631-644.

Schubert Unkmeir A, Konrad C, Slanina H, Czapek F, Hebling S,  Frosch M. 2010. Neisseria meningitidis induces brain microvascular endothelial cell detachment from the matrix and cleavage of occludin: a role for MMP-8. PLoS pathogens 6(4), e1000874.

Selvaraj SK, Periandythevar  P,  Prasadarao NV. 2007. Outer membrane protein A of Escherichia coli K1 selectively enhances the expression of intercellular adhesion molecule-1 in brain microvascular endothelial cells. Microbes and Infection 9(5), 547-557.

Selvaraj SK,  Prasadarao NV. 2005. Escherichia coli K1 inhibits proinflammatory cytokine induction in monocytes by preventing NF‐κB activation. Journal of leukocyte biology 78(2), 544-554.

Serruto D, Adu Bobie J, Scarselli M, Veggi D, Pizza M, Rappuoli R,  Aricò B. 2003. Neisseria meningitidis App, a new adhesin with autocatalytic serine protease activity. Molecular microbiology 48(2), 323-334.

Shanmuganathan MV, Krishnan S, Fu X,  Prasadarao NV. 2013. Attenuation of biopterin synthesis prevents Escherichia coli K1 invasion of brain endothelial cells and the development of meningitis in newborn mice. The Journal of infectious diseases  207(1), 61-71.

Shanmuganathan MV, Krishnan S, Fu X,  Prasadarao NV. 2014. Escherichia coli K1 induces pterin production for enhanced expression of Fcγ receptor I to invade RAW 264.7 macrophages. Microbes and Infection  16(2), 134-141.

Sheen TR, Ebrahimi CM, Hiemstra IH, Barlow SB, Peschel A,  Doran  KS. 2010. Penetration of the blood–brain barrier by Staphylococcus aureus: contribution of membrane-anchored lipoteichoic acid. Journal of molecular medicine 88(6), 633-639.

Shon AS, Bajwa RP,  Russo TA. 2013. Hypervirulent (hypermucoviscous) Klebsiella pneumoniae: a new and dangerous breed. Virulence 4(2), 107-118.

Simberkoff  MS, Moldover  NH,  Rahal JJ. 1980. Absence of detectable bactericidal and opsonic activities in normal and infected human cerebrospinal fluids: a regional host defense deficiency. The Journal of laboratory and clinical medicine 95(3), 362-372.

Simonis A, Hebling S, Gulbins E, Schneider Schaulies S,  Schubert Unkmeir A. 2014. Differential activation of acid sphingomyelinase and ceramide release determines invasiveness of Neisseria meningitidis into brain endothelial cells. PLoS pathogens 10(6), e1004160.

Sjölinder H, Eriksson J, Maudsdotter L, Aro H,  Jonsson AB. 2008. Meningococcal outer membrane protein NhhA is essential for colonization and disease by preventing phagocytosis and complement attack. Infection and immunity 76(11), 5412-5420.

Smith A, Roberts M, Haas J, Stull T,  Mendelman P. 1985. Mechanisms of Haemophilus influenzae type b meningitis. Contemp. issues infect. dis. 1985.

Smith H, Bannister B,  O’shea M. 1973. Cerebrospinal-fluid immunoglobulins in meningitis. The Lancet 302(7829), 591-593.

Smith SG, Mahon V, Lambert MA,  Fagan RP. 2007. A molecular Swiss army knife: OmpA structure, function and expression. FEMS microbiology letters, 273(1), 1-11.

Spivack AP, Eisenberg GM, Weiss W,  Flippin, HF. 1957. Klebsiella meningitis. The American journal of medicine  22(6), 865-871.

Sprong T, Møller  ASW, Bjerre A, Wedege E, Kierulf P, van der Meer JW, Mollnes T. 2004. Complement activation and complement-dependent inflammation by Neisseria meningitidis are independent of lipopolysaccharide. Infection and immunity 72(6), 3344-3349.

Sprong T, Stikkelbroeck N, van der Ley P, Steeghs L, van Alphen L, Klein N,  Van Deuren M. 2001. Contributions of Neisseria meningitidis LPS and non‐LPS to proinflammatory cytokine response. Journal of leukocyte biology 70(2), 283-288.

Stahel PF,  Nadal D. 1997. Complement C3 and factor B cerebrospinal fluid concentrations in bacterial and aseptic meningitis. The Lancet 349(9069), 1886-1887.

Stins MF, Prasadarao NV, Ibric L, Wass CA, Luckett P,  Kim KS. 1994. Binding characteristics of S fimbriated Escherichia coli to isolated brain microvascular endothelial cells. The American journal of pathology 145(5), 1228.

Struve C, Roe CC, Stegger  M, Stahlhut SG, Hansen DS, Engelthaler DM,  Krogfelt KA. 2015. Mapping the evolution of hypervirulent Klebsiella pneumoniae. MBio 6(4), e00630-00615.

Sukumaran SK, McNamara G,  Prasadarao NV. 2003. Escherichia coli K-1 interaction with human brain micro-vascular endothelial cells triggers phospholipase C-γ1 activation downstream of phosphatidylinositol 3-kinase. Journal of Biological Chemistry 278(46), 45753-45762.

Sukumaran SK,  Prasadarao NV. 2003. Escherichia coli K1 invasion increases human brain microvascular endothelial cell monolayer permeability by disassembling vascular-endothelial cadherins at tight junctions. The Journal of infectious diseases 188(9), 1295-1309.

Sukumaran SK, Quon MJ, Prasadarao NV. 2002. Escherichia coli K1 internalization via caveolae requires caveolin-1 and protein kinase Cα interaction in human brain microvascular endothelial cells. Journal of Biological Chemistry 277(52), 50716-50724.

Sukumaran SK, Selvaraj SK,  Prasadarao NV. 2004. Inhibition of apoptosis by Escherichia coli K1 is accompanied by increased expression of BclXL and blockade of mitochondrial cytochrome c release in macrophages. Infection and immunity 72(10), 6012-6022.

Sukumaran SK, Shimada H,  Prasadarao NV. 2003. Entry and intracellular replication of Escherichia coli K1 in macrophages require expression of outer membrane protein A. Infection and immunity 71(10), 5951-5961.

Swords WE, Ketterer MR, Shao J, Campbell CA, Weiser JN,  Apicella  MA. 2001. Binding of the non-typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cellular microbiology 3(8), 525-536. https://doi.org/10.1046/j.1462-5822.2001.00132.x

Swords WE, Ketterer MR, Shao J, Campbell  CA, Weiser JN,  Apicella MA. 2001. Binding of the non‐typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cellular microbiology 3(8), 525-536.

Teng CH, Cai M, Shin S, Xie Y, Kim KJ, Khan NA,  Kim KS. 2005. Escherichia coli K1 RS218 interacts with human brain microvascular endothelial cells via type 1 fimbria bacteria in the fimbriated state. Infection and immunity 73(5), 2923-2931.

Thompson AJ, Williams EB, Williams ED,  Anderson JM. 1952. Klebsiella pneumoniae meningitis: review of the literature and report of a case with bacteremia and pneumonia, with recovery. AMA Archives of Internal Medicine 89(3), 405-420.

Thornton JA, Durick Eder K,  Tuomanen EI. 2010. Pneumococcal pathogenesis:“innate invasion” yet organ-specific damage. Journal of molecular medicine 88(2), 103-107.

Tong H, Blue L, James M,  DeMaria T. 2000. Evaluation of the virulence of a Streptococcus pneumoniae neuraminidase-deficient mutant in nasopharyngeal colonization and development of otitis media in the chinchilla model. Infection and immunity 68(2), 921-924.

Tosi M, Anderson D, Barrish J, Mason Jr  E, Kaplan S. 1985. Effect of piliation on interactions of Haemophilus influenzae type b with human polymorphonuclear leukocytes. Infection and immunity 47(3), 780-785.

Tu YC, Lu MC, Chiang MK, Huang SP, Peng HL, Chang HY, Lai YC. 2009. Genetic requirements for Klebsiella pneumoniae-induced liver abscess in an oral infection model. Infection and immunity 77(7), 2657-2671.

Tuomanen E. 1996. Entry of pathogens into the central nervous system. FEMS microbiology reviews 18(4), 289-299.

Tuomanen E, Liu H, Hengstler B, Zak O, Tomasz A. 1985. The induction of meningeal inflammation by components of the pneumococcal cell wall. Journal of Infectious Diseases 151(5), 859-868.

Turk, D. 1982. Clinical importance of Haemophilus influenzae. H. influenzae epidemiology, immnology, and prevention of disease 3-9.

Turk DC, May JR. 1967. Haemophilus influenzae: its clinical importance: English Universities Press.

Uchiyama S, Carlin AF, Khosravi A, Weiman S, Banerjee A, Quach D, Nizet V. 2009. The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. Journal of Experimental Medicine, 206(9), 1845-1852.

Unkmeir A, Latsch K, Dietrich G, Wintermeyer E, Schinke B, Schwender S,  Frosch M. 2002. Fibronectin mediates Opc‐dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Molecular microbiology 46(4), 933-946.

Van Alphen L, Geelen-Van Den Broek L, Blaas L, Van Ham M, Dankert J. 1991) Blocking of fimbria-mediated adherence of Haemophilus influenzae by sialyl gangliosides. Infection and immunity 59(12), 4473-4477.

Van Alphen L, Poole J, Overbeeke M. 1986. The Anton blood group antigen is the erythrocyte receptor for Haemophilus influenzae. FEMS microbiology letters 37(1), 69-71.

Van der Ley P, Steeghs L. 2003. Lessons from an LPS-deficient Neisseria meningitidis mutant. Journal of endotoxin research 9(2), 124-128.

Van Putten J, Paul S. 1995. Binding of syndecan‐like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. The EMBO journal 14(10), 2144-2154.

Vartzelis G, Theodoridou M, Daikos G, Dellagrammaticas H, Syriopoulou V. 2005. Brain abscesses complicating Staphylococcus aureus sepsis in a premature infant. Infection, 33(1), 36-38.

Vercellotti G, McCarthy J, Lindholm P, Peterson P, Jacob HS, Furcht L. 1985. Extracellular matrix proteins (fibronectin, laminin, and type IV collagen) bind and aggregate bacteria. The American journal of pathology 120(1), 13.

Vijay K. 2018. Toll-like receptors in immunity and inflammatory diseases: Past, present, and future. International immunopharmacology 59, 391-412.

Virji M. 2009. Pathogenic neisseriae: surface modulation, pathogenesis and infection control. Nature Reviews Microbiology 7(4), 274-286.

Waage A, Brandtzaeg P, Halstensen A, Kierulf P, Espevik T. 1989. The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. The Journal of experimental medicine 169(1), 333-338.

Wang L, Shen D, Wu H, MaY. 2017. Resistance of hypervirulent Klebsiella pneumoniae to both intracellular and extracellular killing of neutrophils. PLoS One, 12(3), e0173638.

Wang ZQ, Orlikowsky T, Dudhane A, Trejo V, Dannecker G, Pernis B, Hoffmann M. (1998). Staphylococcal enterotoxin B‐induced T‐cell anergy is mediated by regulatory T cells. Immunology 94(3), 331-339.

Ward JI, Zangwill KM. 1998. Haemophilus influenzae. In Textbook of Pediatric Infectious Diseases (4th ed., 1, p 1464–1482). Philadelphia: W. B. Saunders Co.

Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, Gross M, Peschel A. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nature medicine 10(3), 243-245.

Weintraub A. 2003. Immunology of bacterial polysaccharide antigens. Carbohydrate research, 338(23), 2539-2547.

Wispelwey B, Hansen EJ, Scheld WM. 1989. Haemophilus influenzae outer membrane vesicle-induced blood-brain barrier permeability during experimental meningitis. Infection and immunity, 57(8), 2559-2562.

Wispelwey B, Lesse A, Hansen E, Scheld W. 1988. Haemophilus influenzae lipopolysaccharide-induced blood brain barrier permeability during experimental meningitis in the rat. The Journal of Clinical Investigation 82(4), 1339-1346.

Wizemann TM, Heinrichs JH, Adamou JE, Erwin AL, Kunsch C, Choi GH, Tuomanen E. 2001. Use of a whole genome approach to identify vaccine molecules affording protection against Streptococcus pneumoniae infection. Infection and immunity 69(3), 1593-1598.

Wooster DG, Maruvada R, Blom AM, Prasadarao NV. 2006. Logarithmic phase Escherichia coli K1 efficiently avoids serum killing by promoting C4bp‐mediated C3b and C4b degradation. Immunology 117(4), 482-493.

Wu CC, Lin CT, Cheng Y, Huang CJ, Wang ZC, Peng HL. 2012. Fur-dependent MrkHI regulation of type 3 fimbriae in Klebsiella pneumoniae CG43. Microbiology 158(4), 1045-1056.

Wu MC, Chen YC, Lin TL, Hsieh PF, Wang JT. 2012. Cellobiose-specific phosphotransferase system of Klebsiella pneumoniae and its importance in biofilm formation and virulence. Infection and immunity 80(7), 2464-2472.

Wu MC, Lin TL, Hsieh PF, Yang HC,  Wang JT. 2011. Isolation of genes involved in biofilm formation of a Klebsiella pneumoniae strain causing pyogenic liver abscess. PloS one 6(8), e23500.

Yagupsky P, Nolte FS. 1990. Quantitative aspects of septicemia. Clinical microbiology reviews 3(3), 269-279.

Yau B, Hunt NH, Mitchell AJ, Too LK. 2018. Blood‒Brain Barrier Pathology and CNS Outcomes in Streptococcus pneumoniae Meningitis. International journal of molecular sciences 19(11), 3555.

Yau B, Mitchell AJ, Too LK, Ball HJ, Hunt N. H. 2016. Interferon-γ-induced nitric oxide synthase-2 contributes to blood/brain barrier dysfunction and acute mortality in experimental Streptococcus pneumoniae meningitis. Journal of Interferon & Cytokine Research 36(2), 86-99.

Yu V, Hansen D, Ko W, Sagnimeni A, Klugman K, Von Gottberg A, Benedi V. 2007. International Klebseilla Study Group: Virulence characteristics of Klebsiella and clinical manifestations of K. pneumoniae bloodstream infections. Emerg Infect Dis 13, 986-993.

Yu WL, Chan KS, Ko WC, Lee CC, Chuang YC. 2007. Lower prevalence of diabetes mellitus in patients with Klebsiella pneumoniae primary liver abscess caused by isolates of K1/K2 than with non-K1/K2 capsular serotypes. Clinical infectious diseases, 45(11), 1529-1530.

Zhang JR, Mostov KE, Lamm ME, Nanno M, Shimida SI, Ohwaki M, Tuomanen E. 2000. The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell, 102(6), 827-837.

Zysk G, Schneider-Wald BK, Hwang JH, Bejo L, Kim KS, Mitchell TJ, Heinz HP. 2001. Pneumolysin is the main inducer of cytotoxicity to brain microvascular endothelial cells caused by Streptococcus pneumoniae. Infection and immunity, 69(2), 845-852.