Meningococcus hijacks a β2-adrenoceptor/β-arrestin pathway to cross brain microvasculature endothelium

Cell

Volumn 143, Issue 7, 2010, Pages 1149-1160

  Coureuil, Mathieu ^a,b   Lécuyer, Hervé ^a,b,c   Scott, Mark G H ^a,d,e   Boularan, Cédric ^a,d,e   Enslen, Hervé ^a,d,e   Soyer, Magali ^a,f   Mikaty, Guillain ^a,b   Bourdoulous, Sandrine ^a,d,e   Nassif, Xavier ^a,b,c   Marullo, Stefano ^a,d,e  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b INSERM   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d CNRS   (France)

^e INSTITUT COCHIN   (France)

^f PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; BETA ARRESTIN; GAP JUNCTION PROTEIN; PROTEIN TYROSINE KINASE;

ARTICLE; BACTERIUM ADHERENCE; BACTERIUM COLONY; BETA ADRENERGIC STIMULATION; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CELL JUNCTION; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; ENDOCYTOSIS; ENDOTHELIUM CELL; HOST CELL; HUMAN; HUMAN CELL; MENINGOCOCCOSIS; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

BACTERIA (MICROORGANISMS); NEISSERIA MENINGITIDIS;

EID: 78650476918     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.11.035     Document Type: Article

References (44)

1. M. Audet, and M. Bouvier Insights into signaling from the beta2-adrenergic receptor structure Nat. Chem. Biol. 4 2008 397 403
2. M. Azzi, P.G. Charest, S. Angers, G. Rousseau, T. Kohout, M. Bouvier, and G. Pineyro Beta-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors Proc. Natl. Acad. Sci. USA 100 2003 11406 11411
3. W.G. Barnes, E. Reiter, J.D. Violin, X.R. Ren, G. Milligan, and R.J. Lefkowitz beta-Arrestin 1 and Galphaq/11 coordinately activate RhoA and stress fiber formation following receptor stimulation J. Biol. Chem. 280 2005 8041 8050
4. A. Benmerah, M. Bayrou, N. Cerf-Bensussan, and A. Dautry-Varsat Inhibition of clathrin-coated pit assembly by an Eps15 mutant J. Cell Sci. 112 1999 1303 1311
5. M. Bhattacharya, P.H. Anborgh, A.V. Babwah, L.B. Dale, T. Dobransky, J.L. Benovic, R.D. Feldman, J.M. Verdi, R.J. Rylett, and S.S. Ferguson Beta-arrestins regulate a Ral-GDS Ral effector pathway that mediates cytoskeletal reorganization Nat. Cell Biol. 4 2002 547 555
6. C.C. Bleul, M. Farzan, H. Choe, C. Parolin, I. Clark-Lewis, J. Sodroski, and T.A. Springer The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry Nature 382 1996 829 833
7. H. Choe, M. Farzan, Y. Sun, N. Sullivan, B. Rollins, P.D. Ponath, L. Wu, C.R. Mackay, G. LaRosa, and W. Newman The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates Cell 85 1996 1135 1148
8. M. Coureuil, G. Mikaty, F. Miller, H. Lecuyer, C. Bernard, S. Bourdoulous, G. Dumenil, R.M. Mege, B.B. Weksler, and I.A. Romero Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium Science 325 2009 83 87
9. L. Craig, M.E. Pique, and J.E. Tainer Type IV pilus structure and bacterial pathogenicity Nat. Rev. Microbiol. 2 2004 363 378
10. K.A. DeFea, J. Zalevsky, M.S. Thoma, O. Dery, R.D. Mullins, and N.W. Bunnett beta-arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2 J. Cell Biol. 148 2000 1267 1281
11. R.W. Doms, and J.P. Moore HIV-1 membrane fusion. Targets of opportunity J. Cell Biol. 151 2000 F9 F14
12. E. Eugene, I. Hoffmann, C. Pujol, P.O. Couraud, S. Bourdoulous, and X. Nassif Microvilli-like structures are associated with the internalization of virulent capsulated Neisseria meningitidis into vascular endothelial cells J. Cell Sci. 115 2002 1231 1241
13. N.J. Freedman, and R.J. Lefkowitz Desensitization of G protein-coupled receptors Recent Prog. Horm. Res. 51 1996 319 351 discussion 352-353
14. J. Gavard, and J.S. Gutkind VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin Nat. Cell Biol. 8 2006 1223 1234
15. I. Hoffmann, E. Eugene, X. Nassif, P.O. Couraud, and S. Bourdoulous Activation of ErbB2 receptor tyrosine kinase supports invasion of endothelial cells by Neisseria meningitidis J. Cell Biol. 155 2001 133 143
16. M. Lambotin, I. Hoffmann, M.P. Laran-Chich, X. Nassif, P.O. Couraud, and S. Bourdoulous Invasion of endothelial cells by Neisseria meningitidis requires cortactin recruitment by a phosphoinositide-3-kinase/Rac1 signaling pathway triggered by the lipo-oligosaccharide J. Cell Sci. 118 2005 3805 3816
17. S.A. Laporte, R.H. Oakley, J. Zhang, J.A. Holt, S.S. Ferguson, M.G. Caron, and L.S. Barak The beta2-adrenergic receptor/beta-arrestin complex recruits the clathrin adaptor AP-2 during endocytosis Proc. Natl. Acad. Sci. USA 96 1999 3712 3717
18. L.M. Luttrell, S.S. Ferguson, Y. Daaka, W.E. Miller, S. Maudsley, G.J. Della Rocca, F. Lin, H. Kawakatsu, K. Owada, and D.K. Luttrell Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes Science 283 1999 655 661
19. L.M. Luttrell, F.L. Roudabush, E.W. Choy, W.E. Miller, M.E. Field, K.L. Pierce, and R.J. Lefkowitz Activation and targeting of extracellular signal-regulated kinases by beta-arrestin scaffolds Proc. Natl. Acad. Sci. USA 98 2001 2449 2454
20. E. Mairey, A. Genovesio, E. Donnadieu, C. Bernard, F. Jaubert, E. Pinard, J. Seylaz, J.C. Olivo-Marin, X. Nassif, and G. Duménil Cerebral microcirculation shear stress levels determine Neisseria meningitidis attachment sites along the blood-brain barrier J. Exp. Med. 203 2006 1939 1950
21. M.C. Martín, F. Pérez, A. Moreno, A. Moral, M.A. Alvarez, F.J. Méndez, and F. Vázquez Neisseria gonorrhoeae meningitis in pregnant adolescent Emerg. Infect. Dis. 14 2008 672 674
22. A.J. Merz, C.A. Enns, and M. So Type IV pili of pathogenic Neisseriae elicit cortical plaque formation in epithelial cells Mol. Microbiol. 32 1999 1316 1332
23. G. Mikaty, M. Soyer, E. Mairey, N. Henry, D. Dyer, K.T. Forest, P. Morand, S. Guadagnini, M.C. Prevost, X. Nassif, and G. Dumenil Extracellular bacterial pathogen induces host cell surface reorganization to resist shear stress PLoS Pathog. 5 2009 e1000314
24. X. Nassif, J. Lowy, P. Stenberg, P. O'Gaora, A. Ganji, and M. So Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells Mol. Microbiol. 8 1993 719 725
25. X. Nassif, J.L. Beretti, J. Lowy, P. Stenberg, P. O'Gaora, J. Pfeifer, S. Normark, and M. So Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells Proc. Natl. Acad. Sci. USA 91 1994 3769 3773
26. X. Nassif, S. Bourdoulous, E. Eugene, and P.O. Couraud How do extracellular pathogens cross the blood-brain barrier? Trends Microbiol. 10 2002 227 232
27. B. Poller, H. Gutmann, S. Krahenbuhl, B. Weksler, I. Romero, P.O. Couraud, G. Tuffin, J. Drewe, and J. Huwyler The human brain endothelial cell line hCMEC/D3 as a human blood-brain barrier model for drug transport studies J. Neurochem. 107 2008 1358 1368
28. B. Pron, M.K. Taha, C. Rambaud, J.C. Fournet, N. Pattey, J.P. Monnet, M. Musilek, J.L. Beretti, and X. Nassif Interaction of Neisseria maningitidis with the components of the blood-brain barrier correlates with an increased expression of PilC J. Infect. Dis. 176 1997 1285 1292
29. A. Ring, J.N. Weiser, and E.I. Tuomanen Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway J. Clin. Invest. 102 1998 347 360
30. M.G.H. Scott, V. Pierotti, H. Storez, E. Lindberg, A. Thuret, O. Muntaner, C. Labbé-Jullié, J.A. Pitcher, and S. Marullo Cooperative regulation of ERK activation and cell shape change by Filamin A and β-arrestins Mol. Cell. Biol. 26 2006 3432 3445
31. O. Sokolova, N. Heppel, R. Jagerhuber, K.S. Kim, M. Frosch, M. Eigenthaler, and A. Schubert-Unkmeir Interaction of Neisseria meningitidis with human brain microvascular endothelial cells: role of MAP- and tyrosine kinases in invasion and inflammatory cytokine release Cell. Microbiol. 6 2004 1153 1166
32. H. Storez, M.G. Scott, H. Issafras, A. Burtey, A. Benmerah, O. Muntaner, T. Piolot, M. Tramier, M. Coppey-Moisan, and M. Bouvier Homo- and hetero-oligomerization of beta-arrestins in living cells J. Biol. Chem. 280 2005 40210 40215
33. J.D. Violin, and R.J. Lefkowitz Beta-arrestin-biased ligands at seven-transmembrane receptors Trends Pharmacol. Sci. 28 2007 416 422
34. M. Virji, H. Kayhty, D.J. Ferguson, C. Alexandrescu, J.E. Heckels, and E.R. Moxon The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells Mol. Microbiol. 5 1991 1831 1841
35. M. Virji, S.M. Watt, S. Barker, K. Makepeace, and R. Doyonnas The N-domain of the human CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae Mol. Microbiol. 22 1996 929 939
36. B.B. Weksler, E.A. Subileau, N. Perriere, P. Charneau, K. Holloway, M. Leveque, H. Tricoire-Leignel, A. Nicotra, S. Bourdoulous, and P. Turowski Blood-brain barrier-specific properties of a human adult brain endothelial cell line FASEB J. 19 2005 1872 1874
37. Achour, L., Scott, M.G.H., Shirvani, H., Thuret, A., Bismuth, G., Labbé-Jullié, C., and Marullo, S. (2009). CD4 - CCR5 interaction in intracellular compartments contributes to receptor expression at the cell surface. Blood 113, 1938-1947.
38. Angers, S., Salahpour, A., Joly, E., Hilairet, S., Chelsky, D., Dennis, M., and Bouvier, M. (2000). Detection of beta 2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc. Natl. Acad. Sci. USA 97, 3684-3689.
39. Boularan, C., Scott, M.G., Bourougaa, K., Bellal, M., Esteve, E., Thuret, A., Benmerah, A., Tramier, M., Coppey-Moisan, M., Labbé-Jullié, C., et al. (2007). Beta-arrestin 2 oligomerization controls the Mdm2-dependent inhibition of p53. Proc. Natl. Acad. Sci. USA 104, 18061-18066.
40. Bornstein, M.B., and Murray, M.R. (1958). Serial observations on patterns of growth, myelin formation, maintenance and degeneration in cultures of new-born rat and kitten cerebellum. J. Biophys. Biochem. Cytol. 4, 499-504.
41. Helaine, S., Dyer, D.H., Nassif, X., Pelicic, V., and Forest, K.T. (2007). 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. Proc. Natl. Acad. Sci. USA 104, 15888-15893.
42. Scott, M.G., Benmerah, A., Muntaner, O., and Marullo, S. (2002a). Recruitment of activated G protein-coupled receptors to pre-existing clathrin-coated pits in living cells. J. Biol. Chem. 277, 3552-3559.
43. Scott, M.G., Le Rouzic, E., Perianin, A., Pierotti, V., Enslen, H., Benichou, S., Marullo, S., and Benmerah, A. (2002b). Differential nucleocytoplasmic shuttling of beta-arrestins. Characterization of a leucine-rich nuclear export signal in beta-arrestin2. J. Biol. Chem. 277, 37693-37701.
44. Virji, M., Watt, S.M., Barker, S., Makepeace, K., and Doyonnas, R. (1996). The N-domain of the human CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae. Mol. Microbiol. 22, 929-939.