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Escherichia coli K1 Meningitis and Heat Shock Protein, gp96

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Moonlighting Cell Stress Proteins in Microbial Infections

Part of the book series: Heat Shock Proteins ((HESP,volume 7))

Abstract

Evidence is emerging rapidly that heat shock protein, gp96, plays a critical role in various infectious diseases. Herein, I emphasize the role of gp96 in the pathogenesis of E. coli K1 meningitis. E. coli K1 is the most common neonatal meningitis-causing Gram-negative bacterium, which interacts with gp96 via outer membrane protein A (OmpA) on both neutrophils and human brain microvascular endothelial cells (HBMEC). E. coli K1 infection induces the surface expression of gp96 in neutrophils, using it as a receptor for entering cells and suppressing the production of reactive oxygen species. Thus, the bacterium survives and multiplies inside neutrophils to achieve high-grade bacteremia. E. coli K1 subsequently interacts with HBMEC gp96 (Ecgp96), to induce a variety of signaling pathways for bacterial invasion of the blood–brain barrier and temporarily disrupts the tight junctions between the cells. Of note, E. coli K1 attachment to HBMEC promotes the interaction of Ecgp96 with TLR2 to form a complex, Ecgp96/TLR2, which then translocates to the cell surface. The binding of E. coli K1 OmpA to Ecgp96/TLR2 enhances the production of inducible nitric oxide, which is, in turn, responsible for more Ecgp96 expression at the cell surface and subsequent tight junction disruption.

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References

  • Abdelsadik A, Trad A (2011) Toll-like receptors on the fork roads between innate and adaptive immunity. Hum Immunol 72:1188–1193

    Article  PubMed  CAS  Google Scholar 

  • Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615

    Article  PubMed  CAS  Google Scholar 

  • Andreishcheva EN, Vann WF (2006) Gene products required for de novo synthesis of polysialic acid in Escherichia coli K1. J Bacteriol 188:1786–1797

    Article  PubMed  CAS  Google Scholar 

  • Arora A, Abildgaard F, Bushweller JH, Tamm LK (2001) Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat Struct Biol 8:334–338

    Article  PubMed  CAS  Google Scholar 

  • Arruda MA, Barja-Fidalgo C (2009) NADPH oxidase activity: in the crossroad of neutrophil life and death. Front Biosci 14:4546–4556

    Article  PubMed  CAS  Google Scholar 

  • Azumagawa K, Suzuki S, Tanabe T, Wakamiya E, Kawamura N, Tamai H (2003) Neopterin, biopterin, and nitric oxide concentrations in the cerebrospinal fluid of children with central nervous system infections. Brain Dev 25:200–2

    Article  PubMed  Google Scholar 

  • Bamberger DM (2010) Diagnosis, initial management, and prevention of meningitis. Am Fam Physician 82:1491149–8

    Google Scholar 

  • Banerjee PP, Vinay DS, Mathew A, Raje M, Parekh V, Prasad DV, Kumar A, Mitra D, Mishra GC (2002) Evidence that glycoprotein 96 (B2), a stress protein, functions as a Th2-specific costimulatory molecule. J Immunol 169:3507–3518

    PubMed  CAS  Google Scholar 

  • Bierne H, Dramsi S, Gratacap MP, Randriamampita C, Carpenter G, Payrastre B, Cossart P (2000) The invasion protein InIB from Listeria monocytogenes activates PLC-gamma1 downstream from PI 3-kinase. Cell Microbiol 2:465–476

    Article  PubMed  CAS  Google Scholar 

  • Bogdan C (2001) Nitric oxide and the immune response. Nat Immunol 2:907–916

    Article  PubMed  CAS  Google Scholar 

  • Bond PJ, Faraldo-Gomez JD, Sansom MS (2002) Water in ion channels and pores simulation studies. Biophys J 83:763–775

    Article  PubMed  CAS  Google Scholar 

  • Cabanes D, Sousa S, Cebriá A, Lecuit M, García-del Portillo F, Cossart P (2005) Gp96 is a receptor for a novel Listeria monocytogenes virulence factor, Vip, a surface protein. EMBO J 24:2827–2838

    Article  PubMed  CAS  Google Scholar 

  • Chakravortty D, Hensel M (2003) Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microbes Infect 5:621–627

    Article  PubMed  CAS  Google Scholar 

  • Cole ST, Chen-Schmeisser U, Hindennach I, Henning U (1983) Apparent bacteriophage-binding region of an Escherichia coli K-12 outer membrane protein. J Bacteriol 153:581–587

    PubMed  CAS  Google Scholar 

  • Datta D, Vaidehi N, Floriano WB, Kim KS, Prasadarao NV, Goddard WA 3rd (2003) Atomistic simulation models of E. coli OmpA interaction with GlcNAc1, 4GlcNAc epitopes. Proteins 50:213–221

    Article  PubMed  CAS  Google Scholar 

  • El Bashir H, Laundy M, Booy R (2003) Diagnosis and treatment of bacterial meningitis. Arch Dis Child 88:615–620

    Article  PubMed  CAS  Google Scholar 

  • Ferrieri P, Burke B, Nelson J (1980) Production of bacteremia and meningitis in infant rats with group B streptococcal serotypes. Infect Immun 27:1023–1032

    PubMed  CAS  Google Scholar 

  • Finlay BB, Bonas U (2011) Host-microbe interactions: ever increasing complexity. Curr Opin Microbiol 14:1–2

    Article  PubMed  Google Scholar 

  • Finne J, Leinonen M, Mäkelä PH (1983) Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet 13:8346–8355

    Google Scholar 

  • Grandgirard D, Steiner O, Tauber MG, Leib SL (2007) Apoptosis of hippocampal neurons in organotypic slice culture models: direct effect of bacteria revisited. Acta Neuropathol 114:609–617

    Article  PubMed  Google Scholar 

  • Harding CV (2007) Gp96 leads the way for toll-like receptors. Immunity 26:141–143

    Article  PubMed  CAS  Google Scholar 

  • Harris ES, Nelson WJ (2010) VE-cadherin: at the front, center, and sides of endothelial cell organization and function. Curr Opin Cell Biol 22:651–658

    Article  PubMed  CAS  Google Scholar 

  • Hauser B, Bracht H, Matejovic M, Radermacher P, Venkatesh B (2005) Nitric oxide synthase inhibition in sepsis? Lessons learned from large-animal studies. Anesth Analg 101:488–98

    Article  PubMed  CAS  Google Scholar 

  • Hsu HE, Shutt KA, Moore MR, Beall BW, Bennett NM, Craig AS, Farley MM, Jorgensen JH, Lexau CA, Petit S, Reingold A, Schaffner W, Thomas A, Whitney CG, Harrison LH (2009) Effect of pneumococcal conjugate vaccine on pneumococcal meningitis. N Engl J Med 360:244–56

    Article  PubMed  CAS  Google Scholar 

  • Kim KS (2003) Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat Rev Neurosci 4:376–385

    Article  PubMed  CAS  Google Scholar 

  • 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. J Clin Invest 90:897–905

    Article  PubMed  CAS  Google Scholar 

  • Krishnan S, Chen S, Turcatel G, Arditi M, Prasadarao NV (2012) Regulation of Toll-like receptor 2 interaction with EcGp96 controls Escherichia coli K1 invasion of brain endothelial cells. Cell Microbiol. doi:10.1111/cmi.12026

    Google Scholar 

  • Linscheid P, Schaffner A, Schoedon G (1998) Modulation of inducible nitric oxide synthase mRNA stability by tetrahydrobiopterin in vascular smooth muscle cells. Biochem Biophys Res Commun 243:137–141

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Mittal R, Solis NV, Prasadarao NV, Filler SG (2011) Mechanisms of Candida albicans trafficking to the brain. PLoS Pathog 7:e1002305

    Article  PubMed  CAS  Google Scholar 

  • Manoil C, Rosenbusch JP (1982) Conjugation-deficient mutants of Escherichia coli distinguish classes of functions of the outer membrane OmpA protein. Mol Gen Genet 187(148–1):56

    Google Scholar 

  • Maruvada R, Blom AM, Prasadarao NV (2008a) Effects of complement regulators bound to Escherichia coli k1 and group b streptococcus on the interaction with host cells. Immunology 124:265–276

    Article  PubMed  CAS  Google Scholar 

  • Maruvada R, Argon Y, Prasadarao N (2008b) Escherichia coli K1 interaction with human brain microvascular endothelial cells induces stat3 association with the c-terminal domain of Ec-Gp96, the outer membrane protein a receptor for invasion. Cell Microbiol 10:2326–2338

    Article  PubMed  CAS  Google Scholar 

  • Mittal R, Prasadarao NV (2010) Nitric oxide/cGMP signaling induces Escherichia coli K1 receptor expression and modulates the permeability in human brain endothelial cell monolayers during invasion. Cell Microbiol 12:67–83

    Article  PubMed  CAS  Google Scholar 

  • Mittal R, Prasadarao NV (2011) Gp96 expression in neutrophils is critical for the onset of Escherichia coli K1 (RS218) meningitis. Nat Commun 2:552. doi:10.1038/ncomms1554

    Article  PubMed  Google Scholar 

  • 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. J Exp Med 207:1307–1319

    Article  PubMed  CAS  Google Scholar 

  • Mittal R, Krishnan S, Gonzalez-Gomez I, Prasadarao NV (2011) Deciphering the roles of outer membrane protein A domains in the pathogenesis of Escherichia coli meningitis. J Biol Chem 286:2183–2193

    Article  PubMed  CAS  Google Scholar 

  • Morona R, Klose M, Henning U (1984) Escherichia coli K-12 outer membrane protein (OmpA) as a bacteriophage receptor: analysis of mutant genes expressing altered proteins. J Bacteriol 159:570–578

    PubMed  CAS  Google Scholar 

  • Multhoff G (2006) Heat shock proteins in immunity. Handb Exp Pharmacol 172:279–304

    Article  PubMed  CAS  Google Scholar 

  • Murr C, Widner B, Wirleitner B, Fuchs D (2002) Neopterin as a marker for immune system activation. Curr Drug Metab 3:175–187

    Article  PubMed  CAS  Google Scholar 

  • Na X, Kim H, Moyer MP, Pothoulakis C, LaMont JT (2008) Gp96 is a human colonocyte plasma membrane binding protein for Clostridium difficile toxin A. Infect Immun 76:2862–2871

    Article  PubMed  CAS  Google Scholar 

  • Nauseef WM (2007) How human neutrophils kill and degrade microbes: an integrated view. Immunol Rev 219:88–102

    Article  PubMed  CAS  Google Scholar 

  • Ni M, Lee AS (2007) ER chaperones in mammalian development and human diseases. FEBS Lett 581:3641–3651

    Article  PubMed  CAS  Google Scholar 

  • Parkkinen J, Korhonen TK, Pere A, Hacker J, Soinila S (1988) Binding sites in the rat brain for Escherichia coli S fimbriae associated with neonatal meningitis. J Clin Invest 81:860–865

    Article  PubMed  CAS  Google Scholar 

  • Pascal TA, Abrol R, Mittal R, Wang Y, Prasadarao NV, Goddard WA 3rd (2010) Studies of the efficiency of Escherichia coli K1 invasion into human brain microvascular endothelial cells from both theory and experiment. J Biol Chem 285:37753–37761. doi:10.1074/jbc.M110.122804

    Article  PubMed  CAS  Google Scholar 

  • Pautsch A, Schulz GE (1998) Structure of the outer membrane protein A transmembrane domain. Nat Struct Biol 5:1013–1017

    Article  PubMed  CAS  Google Scholar 

  • Pautsch A, Schulz GE (2000) High-resolution structure of the OmpA membrane domain. J Mol Biol 298:273–282

    Article  PubMed  CAS  Google Scholar 

  • Prasadarao NV (2002) Identification of E. coli outer membrane protein A receptor on human brain microvascular endothelial cells. Infect Immun 70:4556–4563

    Article  PubMed  CAS  Google Scholar 

  • Prasadarao NV, Wass CA, Hacker J, Jann K, Kim KS (1993) Adhesion of S-fimbriated E. coli to brain glycolipids mediated by sfaA gene encoded protein of S-fimbriae. J Biol Chem 268:10356–10363

    PubMed  CAS  Google Scholar 

  • Prasadarao NV, Wass CA, Weiser JN, Stins MF, Huang SH, Kim KS (1996a) Outer membrane protein A (OmpA) contributes to E. coli invasion of brain microvascular endothelial cells. Infect Immun 64:146–153

    PubMed  CAS  Google Scholar 

  • Prasadarao NV, Wass CA, Kim KS (1996b) Endothelial cell GlcNAc1-4GlcNAc epitope interaction with OmpA of E. coli is responsible for crossing of the bacteria across the blood–brain barrier. Infect Immun 64:154–160

    PubMed  CAS  Google Scholar 

  • Prasadarao NV, Stins MF, Shimada H, Wass CA, Kim KS (1999) Outer membrane protein A promoted actin condensation of brain microvascular endothelial cells is required for E. coli invasion. Infect Immun 67:5775–5783

    PubMed  CAS  Google Scholar 

  • Prasadarao NV, Blom AM, Villoutreix BO, Linsangan LC (2002) A novel interaction of OmpA with C4b-binding protein contributes to serum resistance of E. coli K1. J Immunol 169:6352–6360

    PubMed  CAS  Google Scholar 

  • Prasadarao NV, Srivastava PK, Rudrabhatla RS, Kim KS, Huang SH, Sukumaran SK (2003) Cloning and expression of OmpA receptor gene, a Gp96 homolog. Infect Immun 71:1680–1688

    Article  PubMed  CAS  Google Scholar 

  • Randow F, Seed B (2001) Endoplasmic reticulum chaperone Gp96 is required for innate immunity but not cell viability. Nat Cell Biol 3:891–896

    Article  PubMed  CAS  Google Scholar 

  • Reddy MA, Wass CA, Kim KS, Sclaepfer DD, Prasadarao NV (2000a) Involvement of focal adhesion kinase in E. coli invasion of human brain microvascular endothelial cells. Infect Immun 68:6423–6430

    Article  PubMed  CAS  Google Scholar 

  • Reddy MA, Prasadarao NV, Wass CA, Kim KS (2000b) Phosphatidyl inositol Kinase activation and its interaction with focal adhesion kinase is required for E. coli invasion of human brain endothelial cells. J Biol Chem 275:36769–74

    Article  PubMed  CAS  Google Scholar 

  • Reyland ME (2009) Protein kinase C isoforms: multi-functional regulators of cell life and death. Front Biosci 14:2386–2399

    Article  PubMed  CAS  Google Scholar 

  • Rolhion N, Barnich N, Bringer MA, Glasser AL, Ranc J, Hébuterne X, Hofman P, Darfeuille-Michaud A (2010) Abnormally expressed ER stress response chaperone Gp96 in CD favours adherent-invasive Escherichia coli invasion. Gut 59:1355–1362

    Article  PubMed  CAS  Google Scholar 

  • Rudrabhatla SR, Selvaraj SK, Prasadarao NV (2006) Role of Rac1 in E. coli K1 invasion of HBMEC. Microbes Infect 8:460–469

    Article  PubMed  CAS  Google Scholar 

  • Saitoh S, Miyake K (2006) Mechanism regulating cell surface expression and activation of Toll-like receptor 4. Chem Rec 6:311–319

    Article  PubMed  CAS  Google Scholar 

  • Sal-Man N, Croxen MA, Finlay BB (2011) Translocation of effectors: revisiting the injectosome model. Future Microbiol 6:483–484

    Article  PubMed  Google Scholar 

  • Scheld WM, Koedel U, Nathan B, Pfister HW (2002) Pathophysiology of bacterial meningitis: mechanism(s) of neuronal injury. J Infect Dis 186(Suppl 2):S225–233

    Article  PubMed  CAS  Google Scholar 

  • Schuchat A, Robinson K, Wenger JD, Harrison LH, Farley M, Reingold AL, Lefkowitz L, Perkins BA (1997) Bacterial meningitis in the United States in 1995. Active Surveillance Team. N Engl J Med 337:970–976

    Article  PubMed  CAS  Google Scholar 

  • Schut ES, de Gans J, van de Beek D (2008) Community-acquired bacterial meningitis in adults. Pract Neurol 8:8–23

    Article  PubMed  Google Scholar 

  • Selvaraj SK, Parameswaran P, Prasadarao NV (2007) Up-regulation of ICAM-1 expression in human brain microvascular endothelial cells by OmpA + E. coli infection. Microbes Infect 9:547–557

    Article  PubMed  CAS  Google Scholar 

  • Seveau S, Pizarro-Cerda J, Cossart P (2007) Molecular mechanisms exploited by Listeria monocytogenes during host cell invasion. Microbes Infect 9:1167–1175

    Article  PubMed  CAS  Google Scholar 

  • Shanmuganathan M, Krishnan S, Fu X, Prasadarao NV (2013) Attenuation of pterin synthesis prevents Escherichia coli K1 invasion of brain endothelial cells and the development of meningitis in newborn mice. J Infect Dis 207:61–71

    Article  PubMed  CAS  Google Scholar 

  • Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2:a000414

    Article  PubMed  Google Scholar 

  • Silver RP, Finn CW, Vann WF, Aaronson W, Schneerson R, Kretschmer PJ, Garon CF (1981) Molecular cloning of the K1 capsular polysaccharide genes of E. coli. Nature 289:696–698

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Stahlhut SG, Tchesnokova V, Struve C, Weissman SJ, Chattopadhyay S, Yakovenko O, Aprikian P, Sokurenko EV, Krogfelt KA (2009) Comparative structure-function analysis of mannose-specific FimH adhesins from Klebsiella pneumoniae and Escherichia coli. J Bacteriol 191:6592–6601

    Article  PubMed  CAS  Google Scholar 

  • Sugawara E, Steiert M, Rouhani S, Nikaido H (1996) Secondary structure of the outer membrane proteins OmpA of Escherichia coli and OprF of Pseudomonas aeruginosa. J Bacteriol 178:6067–6069

    PubMed  CAS  Google Scholar 

  • Sukumaran SK, Quon MJ, Prasadarao NV (2002) E. coli internalization via caveolae requires protein kinase C and caveolin-1 interaction in human brain microvascular endothelial cells. J Biol Chem 277:12253–12262

    Article  PubMed  CAS  Google Scholar 

  • Sukumaran SK, Shimada H, Prasadarao NV (2003a) Entry and intracellular multiplication of E. coli K1 in macrophages require the expression of OmpA. Infect Immun 71:5951–5961

    Article  PubMed  CAS  Google Scholar 

  • Sukumaran SK, Shimada H, Prasadarao NV (2003b) Escherichia coli K1 invasion increases HBMEC monolayer permeability by disassembling VE-cadherins at the tight junctions. J Infect Dis 188:1295–1309

    Article  PubMed  CAS  Google Scholar 

  • Swick L, Kapatos G (2006) A yeast 2-hybrid analysis of human GTP cyclohydrolase I protein interactions. J Neurochem 97:1447–1455

    Article  PubMed  CAS  Google Scholar 

  • Thigpen MC, Whitney CG, Messonnier NE, Zell ER, Lynfield R, Hadler JL, Harrison LH, Farley MM, Reingold A, Bennett NM, Craig AS, Schaffner W, Thomas A, Lewis MM, Scallan E, Schuchat A, Network EIP (2011) Bacterial meningitis in the United States, 1998–2007. N Engl J Med 364:2016–2025

    Article  PubMed  CAS  Google Scholar 

  • Thony B, Auerbach G, Blau N (2000) Tetrahydrobiopterin biosynthesis, regeneration and functions. Biochem J 347(Pt 1):1–16

    Article  PubMed  CAS  Google Scholar 

  • Tomar A, Schlaepfer DD (2009) Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 21:676–683

    Article  PubMed  CAS  Google Scholar 

  • Tsan MF, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85:905–910

    Article  PubMed  CAS  Google Scholar 

  • Tunkel AR, Scheld WM (1993) Pathogenesis and pathophysiology of bacterial meningitis. Clin Microbiol Rev 6:118–136

    PubMed  CAS  Google Scholar 

  • Vabulas RM, Wagner H, Schild H (2002) Heat shock proteins as ligands of toll-like receptors. Curr Top Microbiol Immunol 270:169–84

    Article  PubMed  CAS  Google Scholar 

  • Wells JM, Rossi O, Meijerink M, van Baarlen P (2011) Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci U S A 108:4607–4614

    Article  PubMed  CAS  Google Scholar 

  • Wooster DG, Maruvada R, Blom AM, Prasadarao NV (2006) Logarithmic phase Escherichia coli K1 efficiently avoids serum resistance by promoting C4b degradation. Immunology 117:482–493

    Article  PubMed  CAS  Google Scholar 

  • Yam PT, Theriot JA (2004) Repeated cycles of rapid actin assembly and disassembly on epithelial cell phagosomes. Mol Biol Cell 15:5647–5658

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Liu B, Dai J, Srivastava PK, Zammit DJ, Lefrançois L, Li Z (2007) Heat shock protein Gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26:215–226

    Article  PubMed  Google Scholar 

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Acknowledgments

I sincerely thank my past and current members of the lab for their contribution to gp96 research. I also thank Krishna Nemani for critical reading of this chapter. The funding for my research is provided by Public Health Service grants (AI40567, NS73115, HD43550 and NS70112) from the National Institutes of Health, USA, American Heart Association grants, and by the Children’s Hospital Los Angeles Research Fellowships.

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  1. Division of Infectious Diseases, Departments of Pediatrics and Surgery, The Saban Research Institute, Children’s Hospital Los Angeles – Keck School of Medicine, University of Southern California, Los Angeles, CA, 90027, USA

    Nemani V. Prasadarao

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Correspondence to Nemani V. Prasadarao .

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  1. Eastman Dental Institute, Div. Microbial Diseases, University College, London, Gray's Inn Road 256, London, WC1X 8LD, United Kingdom

    Brian Henderson

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Prasadarao, N.V. (2013). Escherichia coli K1 Meningitis and Heat Shock Protein, gp96. In: Henderson, B. (eds) Moonlighting Cell Stress Proteins in Microbial Infections. Heat Shock Proteins, vol 7. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6787-4_23

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