The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion

Journal of Experimental Medicine

Volumn 206, Issue 9, 2009, Pages 1845-1852

  Uchiyama, Satoshi ^a   Carlin, Aaron F ^a,b   Khosravi, Arya ^a   Weiman, Shannon ^a,b   Banerjee, Anirban ^e   Quach, Darin ^a   Hightower, George ^a,b   Mitchell, Tim J ^d   Doran, Kelly S ^a,e   Nizet, Victor ^a,c,f  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e SAN DIEGO STATE UNIVERSITY   (United States)

^f RADY CHILDREN'S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; PROTEIN; PROTEIN NANA; SIALIC ACID; SIALIDASE; SIALIDASE INHIBITOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL MENINGITIS; BACTERIAL STRAIN; BLOOD BRAIN BARRIER; BRAIN; CELL ADHESION; CELL INTERACTION; CELL INVASION; CELL SURFACE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HETEROLOGOUS EXPRESSION; HOST CELL; HUMAN; HUMAN CELL; MORTALITY; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BLOOD-BRAIN BARRIER; CELL ADHESION; DNA PRIMERS; ENDOTHELIAL CELLS; HUMANS; MALE; MENINGITIS, BACTERIAL; MICE; MICE, INBRED BALB C; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PLASMIDS; STREPTOCOCCUS PNEUMONIAE;

EID: 69549095908     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20090386     Document Type: Article

References (37)

1. Avery, O.T., C.M. Macleod, and M. Mccarty. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: inductions of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 79:137-158.
2. 2) mediate brain cell apoptosis during meningitis. J. Clin. Invest. 109:19-27.
3. Buschiazzo, A., M.F. Amaya, M.L. Cremona, A.C. Frasch, and P.M. Alzari. 2002. The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Mol. Cell. 10:757-768. (Pubitemid 35339437)
4. Cámara, M., G.J. Boulnois, P.W. Andrew, and T.J. Mitchell. 1994. A neuraminidase from Streptococcus pneumoniae has the features of a surface protein. Infect. Immun. 62:3688-3695. (Pubitemid 24264308)
5. Chuenkova, M.V., and M.A. Pereira. 2000. A trypanosomal protein synergizes with the cytokines ciliary neurotrophic factor and leukemia inhibitory factor to prevent apoptosis of neuronal cells. Mol. Biol. Cell. 11:1487-1498.
6. Chuenkova, M.V., and M. PereiraPerrin. 2004. Chagas' disease parasite promotes neuron survival and differentiation through TrkA nerve growth factor receptor. J. Neurochem. 91:385-394.
7. Crennell, S., E. Garman, G. Laver, E. Vimr, and G. Taylor. 1994. Crystal structure of Vibrio cholerae neuraminidase reveals dual lectin-like domains in addition to the catalytic domain. Structure. 2:535-544. (Pubitemid 2100410)
8. Doran, K.S., E.J. Engelson, A. Khosravi, H.C. Maisey, I. Fedtke, O. Equils, K.S. Michelsen, M. Arditi, A. Peschel, and V. Nizet. 2005. Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J. Clin. Invest. 115:2499-2507.
9. Gao, W., H.H. Wortis, and M.A. Pereira. 2002. The Trypanosoma cruzi trans-sialidase is a T cell-independent B cell mitogen and an inducer of non-specific Ig secretion. Int. Immunol. 14:299-308. (Pubitemid 34213641)
10. Holzer, C.T., M. von Itzstein, B. Jin, M.S. Pegg, W.P. Stewart, and W.Y. Wu. 1993. Inhibition of sialidases from viral, bacterial and mammalian sources by analogues of 2-deoxy-2,3-didehydro-N-acetylneuraminic acid modified at the C-4 position. Glycoconj. J. 10:40-44.
11. Huang, S.H., C. Wass, Q. Fu, N.V. Prasadarao, M. Stins, and K.S. Kim. 1995. Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infect. Immun. 63:4470-4475.
12. Kim, K.S. 2003. Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat. Rev. Neurosci. 4:376-385. (Pubitemid 37280176)
13. Kim, K.S. 2006. Microbial translocation of the blood-brain barrier. Int. J. Parasitol. 36:607-614.
14. King, S.J., K.R. Hippe, and J.N. Weiser. 2006. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol. Microbiol. 59:961-974.
15. Koedel, U., W.M. Scheld, and H.W. Pfister. 2002. Pathogenesis and pathophysiology of pneumococcal meningitis. Lancet Infect. Dis. 2:721-736.
16. Lanie, J.A., W.L. Ng, K.M. Kazmierczak, T.M. Andrzejewski, T.M. Davidsen, K.J. Wayne, H. Tettelin, J.I. Glass, and M.E. Winkler. 2007. Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J. Bacteriol. 189:38-51.
17. Lock, R.A., J.C. Paton, and D. Hansman. 1988. Purification and immunological characterization of neuraminidase produced by Streptococcus pneumoniae. Microb. Pathog. 4:33-43.
18. Manco, S., F. Hernon, H. Yesilkaya, J.C. Paton, P.W. Andrew, and A. Kadioglu. 2006. Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect. Immun. 74:4014-4020. (Pubitemid 43993333)
19. Nizet, V., K.S. Kim, M. Stins, M. Jonas, E.Y. Chi, D. Nguyen, and C.E. Rubens. 1997. Invasion of brain microvascular endothelial cells by group B streptococci. Infect. Immun. 65:5074-5081. (Pubitemid 27513552)
20. O'Toole, R.D., L. Goode, and C. Howe. 1971. Neuraminidase activity in bacterial meningitis. J. Clin. Invest. 50:979-985.
21. Orihuela, C.J., G. Gao, K.P. Francis, J. Yu, and E.I. Tuomanen. 2004. Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J. Infect. Dis. 190:1661-1669. (Pubitemid 39411017)
22. Orihuela, C.J., J. Mahdavi, J. Thornton, B. Mann, K.G. Wooldridge, N. Abouseada, N.J. Oldfield, T. Self, D.A. Ala-Adeen, and E.I. Tuomanen. 2009. Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. J. Clin. Invest. 119:1638-1646
23. Pettigrew, M.M., K.P. Fennie, M.P. York, J. Daniels, and F. Ghaffar. 2006. Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types. Infect. Immun. 74:3360-3365.
24. Pracht, D., C. Elm, J. Gerber, S. Bergmann, M. Rohde, M. Seiler, K.S. Kim, H.F. Jenkinson, R. Nau, and S. Hammerschmidt. 2005. PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infect. Immun. 73:2680-2689. (Pubitemid 40570332)
25. Ring, A., J.N. Weiser, and E.I. Tuomanen. 1998. Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway. J. Clin. Invest. 102:347-360. (Pubitemid 28335194)
26. Saavedra, E., M. Herrera, W. Gao, H. Uemura, and M.A. Pereira. 1999. The Trypanosoma cruzi trans-sialidase, through its COOH-terminal tandem repeat, upregulates interleukin 6 secretion in normal human intestinal microvascular endothelial cells and peripheral blood mononuclear cells. J. Exp. Med. 190:1825-1836. (Pubitemid 30013848)
27. Scanlon, K.L., W.F. Diven, and R.H. Glew. 1989. Purification and properties of Streptococcus pneumoniae neuraminidase. Enzyme. 41:143-150.
28. Shakhnovich, E.A., S.J. King, and J.N. Weiser. 2002. Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae: a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect. Immun. 70:7161-7164.
29. Tong, H.H., X. Liu, Y. Chen, M. James, and T. Demaria. 2002. Effect of neuraminidase on receptor-mediated adherence of Streptococcus pneumoniae to chinchilla tracheal epithelium. Acta Otolaryngol. 122:413-419.
30. Tong, H.H., D. Li, S. Chen, J.P. Long, and T.F. DeMaria. 2005. Immunization with recombinant Streptococcus pneumoniae neuraminidase NanA protects chinchillas against nasopharyngeal colonization. Infect. Immun. 73:7775-7778.
31. Tuomanen, E. 1996. Entry of pathogens into the central nervous system. FEMS Microbiol. Rev. 18:289-299. (Pubitemid 26241883)
32. van de Beek, D., J. de Gans, L. Spanjaard, M. Weisfelt, J.B. Reitsma, and M. Vermeulen. 2004. Clinical features and prognostic factors in adults with bacterial meningitis. N. Engl. J. Med. 351:1849-1859.
33. Weber, J.R., and E.I. Tuomanen. 2007. Cellular damage in bacterial meningitis: an interplay of bacterial and host driven toxicity. J. Neuroimmunol. 184:45-52.
34. Weisfelt, M., D. van de Beek, L. Spanjaard, J.B. Reitsma, and J. de Gans. 2006. Clinical features, complications, and outcome in adults with pneumococcal meningitis: a prospective case series. Lancet Neurol. 5:123-129. (Pubitemid 43107848)
35. Wellmer, A., G. Zysk, J. Gerber, T. Kunst, M. Von Mering, S. Bunkowski, H. Eiffert, and R. Nau. 2002. Decreased virulence of a pneumolysin-deficient strain of Streptococcus pneumoniae in murine meningitis. Infect. Immun. 70:6504-6508. (Pubitemid 35192751)
36. Winter, A.J., S.D. Comis, M.P. Osborne, M.J. Tarlow, J. Stephen, P.W. Andrew, J. Hill, and T.J. Mitchell. 1997. A role for pneumolysin but not neuraminidase in the hearing loss and cochlear damage induced by experimental pneumococcal meningitis in guinea pigs. Infect. Immun. 65:4411-4418.
37. Yesilkaya, H., S. Soma-Haddrick, S.J. Crennell, and P.W. Andrew. 2006. Identification of amino acids essential for catalytic activity of pneumococcal neuraminidase A. Res. Microbiol. 157:569-574. (Pubitemid 44067431)