Pathogenic Neisseria meningitidis utilizes CD147 for vascular colonization

Nature Medicine

Volumn 20, Issue 7, 2014, Pages 725-731

  Bernard, Sandra C ^a,b,c   Simpson, Nandi ^a,b,c,n   Join Lambert, Olivier ^b,c,d,e   Federici, Christian ^c   Laran Chich, Marie Pierre ^a,b,c   Maïssa, Nawal ^a,b,c   Bouzinba Ségard, Haniaa ^a,b,c   Morand, Philippe C ^a,b,c   Chretien, Fabrice ^f,g,h   Taouji, Saïd ⁱ   Chevet, Eric ⁱ   Janel, Sébastien ^j,k,l,m   Lafont, Frank ^j,k,l,m   Coureuil, Mathieu ^b,c,d   Segura, Audrey ^b,c,d   Niedergang, Florence ^a,b,c   Marullo, Stefano ^a,b,c   Couraud, Pierre Olivier ^a,b,c   Nassif, Xavier ^b,c,d,e   Bourdoulous, Sandrine ^a,b,c  

^a INSTITUT COCHIN   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INSTITUT NECKER ENFANTS MALADES   (France)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f INSTITUT PASTEUR   (France)

^g LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^h RAYMOND POINCARÉ HOSPITAL   (France)

ⁱ UNIVERSITÉ DE BORDEAUX   (France)

^j INSTITUT PASTEUR DE LILLE   (France)

^k CNRS UM8204   (France)

^l INSERM U1019   (France)

^m UNIV LILLE   (France)

ⁿ UNIVERSITY COLLEGE LONDON   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CD147 ANTIGEN; DACTINOMYCIN; EPIDERMAL GROWTH FACTOR; INTERCELLULAR ADHESION MOLECULE 1; PHORBOL 13 ACETATE 12 MYRISTATE; PILINS PILE PROTEIN; PILINS PILV PROTEIN; SIALIC ACID BINDING IMMUNOGLOBULIN LIKE LECTIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BRAIN CAPILLARY; BRAIN TISSUE; CELL ADHESION; CELL JUNCTION; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; MENINGOCOCCOSIS; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; UPREGULATION; VASCULAR COLONIZATION; VASCULAR DISEASE;

BACTERIA (MICROORGANISMS); MUS; NEISSERIA MENINGITIDIS;

ANTIGENS, CD147; BACTERIAL ADHESION; BLOOD VESSELS; FIMBRIAE, BACTERIAL; HUMANS; NEISSERIA MENINGITIDIS;

EID: 84904049840     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3563     Document Type: Article

References (57)

1. Yazdankhah, S.P. & Caugant, D.A. Neisseria meningitidis: an overview of the carriage state. J. Med. Microbiol. 53, 821-832 (2004).
2. Stephens, D.S., Greenwood, B. & Brandtzaeg, P. Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 369, 2196-2210 (2007).
3. Virji, M. Pathogenic neisseriae: surface modulation, pathogenesis and infection control. Nat. Rev. Microbiol. 7, 274-286 (2009).
4. Brandtzaeg, P. & van Deuren, M. Classification and pathogenesis of meningococcal infections. Methods Mol. Biol. 799, 21-35 (2012).
5. Lemichez, E., Lecuit, M., Nassif, X. & Bourdoulous, S. Breaking the wall: targeting of the endothelium by pathogenic bacteria. Nat. Rev. Microbiol. 8, 93-104 (2010).
6. Melican, K. & Dumenil, G. Vascular colonization by Neisseria meningitidis. Curr. Opin. Microbiol. 15, 50-56 (2012).
7. Doulet, N. et al. Neisseria meningitidis infection of human endothelial cells interferes with leukocyte transmigration by preventing the formation of endothelial docking structures. J. Cell Biol. 173, 627-637 (2006).
8. Coureuil, M. et al. Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science 325, 83-87 (2009).
9. Coureuil, M. et al. Meningococcus hijacks a β2-adrenoceptor/β- arrestin pathway to cross brain microvasculature endothelium. Cell 143, 1149-1160 (2010).
10. Dupin, N. et al. Chronic meningococcemia cutaneous lesions involve meningococcal perivascular invasion through the remodeling of endothelial barriers. Clin. Infect. Dis. 54, 1162-1165 (2012).
11. Craig, L. & Li, J. Type IV pili: paradoxes in form and function. Curr. Opin. Struct. Biol. 18, 267-277 (2008).
12. Hélaine, S. et al. Pil X, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol. Microbiol. 55, 65-77 (2005).
13. Mikaty, G. et al. Extracellular bacterial pathogen induces host cell surface reorganization to resist shear stress. PLo S Pathog. 5, e1000314 (2009).
14. Brown, D.R., Helaine, S., Carbonnelle, E. & Pelicic, V. 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. Infect. Immun. 78, 3053-3063 (2010).
15. Stephens, D.S., Whitney, A.M., Rothbard, J. & Schoolnik, G.K. Pili of Neisseria meningitidis. Analysis of structure and investigation of structural and antigenic relationships to gonococcal pili. J. Exp. Med. 161, 1539-1553 (1985).
16. Virji, M. et al. Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status of pilin. Mol. Microbiol. 10, 1013-1028 (1993).
17. Nassif, X. et al. Roles of pilin and Pil C in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc. Natl. Acad. Sci. USA 91, 3769-3773 (1994).
18. Winther-Larsen, H.C. et al. Neisseria gonorrhoeae Pil V, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc. Natl. Acad. Sci. USA 98, 15276-15281 (2001).
19. Lécuyer, H., Nassif, X. & Coureuil, M. Two strikingly different signaling pathways are induced by meningococcal type IV pili on endothelial and epithelial cells. Infect. Immun. 80, 175-186 (2012).
20. Iacono, K.T., Brown, A.L., Greene, M.I. & Saouaf, S.J. CD147 immunoglobulin superfamily receptor function and role in pathology. Exp. Mol. Pathol. 83, 283-295 (2007).
21. Sameshima, T. et al. Expression of EMMPRIN (CD147), a cell surface inducer of matrix metalloproteinases, in normal human brain and gliomas. Int. J. Cancer 88, 21-27 (2000).
22. Bertossi, M. et al. Developmental changes of HT7 expression in the microvessels of the chick embryo brain. Anat. Embryol. (Berl.) 205, 229-233 (2002).
23. Kimberley, F.C., Sivasankar, B. & Paul Morgan, B. Alternative roles for CD59. Mol. Immunol. 44, 73-81 (2007).
24. Weksler, B., Romero, I.A. & Couraud, P.O. The hCMEC/D3 cell line as a model of the human blood brain barrier. Fluids Barriers CNS 10, 16 (2013).
25. Schweitzer, K.M. et al. Characterization of a newly established human bone marrow endothelial cell line: distinct adhesive properties for hematopoietic progenitors compared with human umbilical vein endothelial cells. Lab. Invest. 76, 25-36 (1997).
26. Chen, Y. et al. Upregulation of HAb18G/CD147 in activated human umbilical vein endothelial cells enhances the angiogenesis. Cancer Lett. 278, 113-121 (2009).
27. Yu, X.L. et al. Crystal structure of HAb18G/CD147: implications for immunoglobulin superfamily homophilic adhesion. J. Biol. Chem. 283, 18056-18065 (2008).
28. Mairey, E. et al. Cerebral microcirculation shear stress levels determine Neisseria meningitidis attachment sites along the blood-brain barrier. J. Exp. Med. 203, 1939-1950 (2006).
29. Helm, R.A. & Seifert, H.S. Frequency and rate of pilin antigenic variation of Neisseria meningitidis. J. Bacteriol. 192, 3822-3823 (2010).
30. Lancellotti, M. et al. Conserved virulence of C to B capsule switched Neisseria meningitidis clinical isolates belonging to ET-37/ST-11 clonal complex. Microbes Infect. 8, 191-196 (2006).
31. Yurchenko, V., Constant, S., Eisenmesser, E. & Bukrinsky, M. Cyclophilin-CD147 interactions: a new target for anti-inflammatory therapeutics. Clin. Exp. Immunol. 160, 305-317 (2010).
32. Join-Lambert, O. et al. Meningococcal interaction to microvasculature triggers the tissular lesions of purpura fulminans. J. Infect. Dis. 208, 1590-1597 (2013).
33. Melican, K., Michea Veloso, P., Martin, T., Bruneval, P. & Dumenil, G. Adhesion of Neisseria meningitidis to dermal vessels leads to local vascular damage and purpura in a humanized mouse model. PLo S Pathog. 9, e1003139 (2013).
34. Gray, F. & Alonso, J.M. in Greenfield's Neuropathology 6th edn. (eds. Graham, D.I. & Lantos, P.L.) Ch. 3, 151-189 (2002).
35. Trust, T.J., Gillespie, R.M., Bhatti, A.R. & White, L.A. Differences in the adhesive properties of Neisseria meningitidis for human buccal epithelial cells and erythrocytes. Infect. Immun. 41, 106-113 (1983).
36. Pinner, R.W., Spellman, P.A. & Stephens, D.S. Evidence for functionally distinct pili expressed by Neisseria meningitidis. Infect. Immun. 59, 3169-3175 (1991).
37. Chen, Z. et al. Function of HAb18G/CD147 in invasion of host cells by severe acute respiratory syndrome coronavirus. J. Infect. Dis. 191, 755-760 (2005).
38. Watanabe, A. et al. CD147/EMMPRIN acts as a functional entry receptor for measles virus on epithelial cells. J. Virol. 84, 4183-4193 (2010).
39. Till, A. et al. A role for membrane-bound CD147 in NOD2-mediated recognition of bacterial cytoinvasion. J. Cell Sci. 121, 487-495 (2008).
40. Gabison, E.E., Hoang-Xuan, T., Mauviel, A. & Menashi, S. EMMPRIN/CD147, an MMP modulator in cancer, development and tissue repair. Biochimie 87, 361-368 (2005).
41. Crosnier, C. et al. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480, 534-537 (2011).
42. Harrison, T. et al. Erythrocyte G protein-coupled receptor signaling in malarial infection. Science 301, 1734-1736 (2003).
43. Nassif, X. et al. Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol. Microbiol. 8, 719-725 (1993).
44. Hoffmann, I., Eugene, E., Nassif, X., Couraud, P.O. & Bourdoulous, S. Activation of Erb B2 receptor tyrosine kinase supports invasion of endothelial cells by Neisseria meningitidis. J. Cell Biol. 155, 133-143 (2001).
45. Achtman, M. et al. Purification and characterization of eight class 5 outer membrane protein variants from a clone of Neisseria meningitidis serogroup A. J. Exp. Med. 168, 507-525 (1988).
46. Tettelin, H. et al. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287, 1809-1815 (2000).
47. Dyer, D.W., Mc Kenna, W., Woods, J.P. & Sparling, P.F. Isolation by streptonigrin enrichment and characterization of a transferrin-specific iron uptake mutant of Neisseria meningitidis. Microb. Pathog. 3, 351-363 (1987).
48. Pron, B. et al. Interaction of Neisseria meningitidis with the components of the blood- brain barrier correlates with an increased expression of Pil C. J. Infect. Dis. 176, 1285-1292 (1997).
49. Prudhomme, J.G. et al. Studies of Plasmodium falciparum cytoadherence using immortalized human brain capillary endothelial cells. Int. J. Parasitol. 26, 647-655 (1996).
50. Angers, S. et al. Detection of β 2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc. Natl. Acad. Sci. USA 97, 3684-3689 (2000).
51. Virlon, B. et al. Serial microanalysis of renal transcriptomes. Proc. Natl. Acad. Sci. USA 96, 15286-15291 (1999).
52. Lambotin, M. et al. Invasion of endothelial cells by Neisseria meningitidis requires cortactin recruitment by a PI3-kinase/Rac1 signalling pathway triggered by the lipo-oligosaccharide. J. Cell Sci. 118, 3805-3816 (2005).
53. Steffen, A. et al. MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr. Biol. 18, 926-931 (2008).
54. Chevalier, S. et al. Creating biomimetic surfaces through covalent and oriented binding of proteins. Langmuir 26, 14707-14715 (2010).
55. Roduit, C. et al. Elastic membrane heterogeneity of living cells revealed by stiff nanoscale membrane domains. Biophys. J. 94, 1521-1532 (2008).
56. Yersin, A. et al. Elastic properties of the cell surface and trafficking of single AMPA receptors in living hippocampal neurons. Biophys. J. 92, 4482-4489 (2007).
57. Kasas, S., Riederer, B.M., Catsicas, S., Cappella, B. & Dietler, G. Fuzzy logic algorithm to extract specific interaction forces from atomic force microscopy data. Rev. Sci. Instrum. 71, 2082-2086 (2000).