Neisseria meningitidis opc invasin binds to the sulphated tyrosines of activated vitronectin to attach to and invade human brain endothelial cells

PLoS Pathogens

Volumn 6, Issue 5, 2010, Pages 1-18

  Cunha, Claudia Sa E ^a   Griffiths, Natalie J ^a   Virji, Mumtaz ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; FIBRONECTIN; HEPARIN; INVASIN; MONOCLONAL ANTIBODY; PEPTIDE DERIVATIVE; PROTEIN OPC; SULFUR DERIVATIVE; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG; VITRONECTIN;

ARTICLE; BINDING AFFINITY; BRAIN CELL; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIUM CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MICROBIAL ACTIVITY; NEISSERIA MENINGITIDIS; NONHUMAN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING;

ANIMALS; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BLOOD-BRAIN BARRIER; BRAIN; CATTLE; CELL LINE; ENDOTHELIAL CELLS; FIBRONECTINS; HEPARIN; HUMANS; MICE; NEISSERIA MENINGITIDIS, SEROGROUP A; NEISSERIA MENINGITIDIS, SEROGROUP B; PHOSPHORYLATION; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; SPECIES SPECIFICITY; SULFATES; TYROSINE; VITRONECTIN;

BACTERIA (MICROORGANISMS); HARNESS; NEISSERIA MENINGITIDIS;

EID: 77954067912     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000911     Document Type: Article

References (65)

1. Virji M, Makepeace K, Moxon ER (1994) Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells; the role of integrins in apical interactions. Mol Microbiol 14: 173-184.
2. Virji M, Makepeace K, Peak IR, Ferguson DJ, Jennings MP, et al. (1995) Opcand pilus-dependent interactions of meningococci with human endothelial cells: molecular mechanisms and modulation by surface polysaccharides. Mol Microbiol 18: 741-754.
3. Virji M, Makepeace K, Ferguson DJ, Achtman M, Sarkari J, et al. (1992) Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol 6: 2785-2795.
4. Unkmeir A, Latsch K, Dietrich G, Wintermeyer E, Schinke B, et al. (2002) Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol Microbiol 46: 933-946.
5. Lambotin M, Hoffmann I, Laran-Chich MP, Nassif X, Couraud PO, et al. (2005) Invasion of endothelial cells by Neisseria meningitidis requires cortactin recruitment by a phosphoinositide-3-kinase/Rac1 signalling pathway triggered by the lipo-oligosaccharide. J Cell Sci 118: 3805-3816.
6. Griffiths NJ, Bradley CJ, Heyderman RS, Virji M (2007) IFN-gamma amplifies NFkappaB-dependent Neisseria meningitidis invasion of epithelial cells via specific upregulation of CEA-related cell adhesion molecule 1. Cell Microbiol 9: 2968-2983.
7. 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. Cell Microbiol 7: 1490-1503.
8. Rowe HA, Griffiths NJ, Hill DJ, Virji M (2007) Co-ordinate action of bacterial adhesins and human carcinoembryonic antigen receptors in enhanced cellular invasion by capsulate serum resistant Neisseria meningitidis. Cell Microbiol 9: 154-168.
9. Carbonnelle E, Hill DJ, Morand P, Griffiths NJ, Bourdoulous S, et al. (2009) Meningococcal interactions with the host. Vaccine 27 Suppl 2: B78-89.
10. Virji M, Makepeace K, Ferguson DJ, Achtman M, Moxon ER (1993) Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol 10: 499-510.
11. Seiler A, Reinhardt R, Sarkari J, Caugant DA, Achtman M (1996) Allelic polymorphism and site-specific recombination in the opc locus of Neisseria meningitidis. Mol Microbiol 19: 841-856.
12. 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. Mol Microbiol 13: 207-217.
13. Whalen CM, Hockin JC, Ryan A, Ashton F (1995) The changing epidemiology of invasive meningococcal disease in Canada, 1985 through 1992. Emergence of a virulent clone of Neisseria meningitidis. JAMA 273: 390-394.
14. Kriz P, Vlckova J, Bobak M (1995) Targeted vaccination with meningococcal polysaccharide vaccine in one district of the Czech Republic. Epidemiol Infect 115: 411-418.
15. Caugant DA (2008) Genetics and evolution of Neisseria meningitidis: importance for the epidemiology of meningococcal disease. Infect Genet Evol 8: 558-565.
16. Prince SM, Feron C, Janssens D, Lobet Y, Achtman M, et al. (2001) Expression, refolding and crystallization of the OpcA invasin from Neisseria meningitidis. Acta Crystallogr D Biol Crystallogr 57: 1164-1166.
17. Prince SM, Achtman M, Derrick JP (2002) Crystal structure of the OpcA integral membrane adhesin from Neisseria meningitidis. Proc Natl Acad Sci USA 99: 3417-3421.
18. Moore J, Bailey SE, Benmechernene Z, Tzitzilonis C, Griffiths NJ, et al. (2005) Recognition of saccharides by the OpcA, OpaD, and OpaB outer membrane proteins from Neisseria meningitidis. J Biol Chem 280: 31489-31497.
19. Bond PJ, Derrick JP, Sansom MS (2007) Membrane simulations of OpcA: gating in the loops? Biophys J 92: L23-25.
20. de Vries FP, Cole R, Dankert J, Frosch M, van Putten JP (1998) Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 27: 1203-1212.
21. Underwood PA, Kirkpatrick A, Mitchell SM (2002) New insights into heparin binding to vitronectin: studies with monoclonal antibodies. Biochem J 365: 57-67.
22. Seiffert D (1995) Evidence that conformational changes upon the transition of the native to the modified form of vitronectin are not limited to the heparin binding domain. FEBS Lett 368: 155-159.
23. Preissner KT, Seiffert D (1998) Role of vitronectin and its receptors in haemostasis and vascular remodeling. Thromb Res 89: 1-21.
24. de Kleijn ED, Hazelzet JA, Kornelisse RF, de Groot R (1998) Pathophysiology of meningococcal sepsis in children. Eur J Pediatr 157: 869-880.
25. Hazelzet JA, de Groot R, van Mierlo G, Joosten KF, van der Voort E, et al. (1998) Complement activation in relation to capillary leakage in children with septic shock and purpura. Infect Immun 66: 5350-5356.
26. Schvartz I, Seger D, Shaltiel S (1999) Vitronectin. Int J Biochem Cell Biol 31: 539-544.
27. Lynn GW, Heller WT, Mayasundari A, Minor KH, Peterson CB (2005) A model for the three-dimensional structure of human plasma vitronectin from small-angle scattering measurements. Biochemistry 44: 565-574.
28. Hogasen K, Mollnes TE, Brandtzaeg P (1994) Low levels of vitronectin and clusterin in acute meningococcal disease are closely associated with formation of the terminal-complement complex and the vitronectin-thrombin-antithrombin complex. Infect Immun 62: 4874-4880.
29. Jenne D, Hille A, Stanley KK, Huttner WB (1989) Sulfation of two tyrosineresidues in human complement S-protein (vitronectin). Eur J Biochem 185: 391-395.
30. Okumura Y, Kamikubo Y, Curriden SA, Wang J, Kiwada T, et al. (2002) Kinetic analysis of the interaction between vitronectin and the urokinase receptor. J Biol Chem 277: 9395-9404.
31. Yu Y, Hoffhines AJ, Moore KL, Leary JA (2007) Determination of the sites of tyrosine O-sulfation in peptides and proteins. Nat Methods 4: 583-588.
32. Seiffert D, Smith JW (1997) The cell adhesion domain in plasma vitronectin is cryptic. J Biol Chem 272: 13705-13710.
33. Izumi M, Yamada KM, Hayashi M (1989) Vitronectin exists in two structurally and functionally distinct forms in human plasma. Biochim Biophys Acta 990: 101-108.
34. Cunha CS, Griffiths NJ, Murillo I, Virji M (2009) Neisseria meningitidis Opc invasin binds to the cytoskeletal protein alpha-actinin. Cell Microbiol 11: 389-405.
35. Virji M, Kayhty H, Ferguson DJ, Alexandrescu C, Heckels JE, et al. (1991) The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol Microbiol 5: 1831-1841.
36. Tomasini BR, Mosher DF (1988) Conformational states of vitronectin: preferential expression of an antigenic epitope when vitronectin is covalently and noncovalently complexed with thrombin-antithrombin III or treated with urea. Blood 72: 903-912.
37. Hayashi M, Akama T, Kono I, Kashiwagi H (1985) Activation of vitronectin (serum spreading factor) binding of heparin by denaturing agents. J Biochem 98: 1135-1138.
38. Bale MD, Wohlfahrt LA, Mosher DF, Tomasini B, Sutton RC (1989) Identification of vitronectin as a major plasma protein adsorbed on polymer surfaces of different copolymer composition. Blood 74: 2698-2706
39. Seger D, Gechtman Z, Shaltiel S (1998) Phosphorylation of vitronectin by casein kinase II. Identification of the sites and their promotion of cell adhesion and spreading. J Biol Chem 273: 24805-24813.
40. Rodriguez FA, Contreras C, Bolanos-Garcia V, Allende JE (2008) Protein kinase CK2 as an ectokinase: the role of the regulatory CK2 beta subunit. Proc Natl Acad Sci USA 105: 5693-5698.
41. Stepanova V, Jerke U, Sagach V, Lindschau C, Dietz R, et al. (2002) Urokinasedependent human vascular smooth muscle cell adhesion requires selective vitronectin phosphorylation by ectoprotein kinase CK2. J Biol Chem 277: 10265-10272.
42. Bylund DB, Huang TS (1976) Decomposition of phosphoserine and phosphothreonine during acid hydrolysis. Anal Biochem 73: 477-485.
43. Bailin G (1979) Phosphorylation of a bovine cardiac actin complex. Am J Physiol 236: C41-46.
44. Merker P, Tommassen J, Kusecek B, Virji M, Sesardic D, et al. (1997) Twodimensional structure of the Opc invasin from Neisseria meningitidis. Mol Microbiol 23: 281-293.
45. Gibson AD, Lamerdin JA, Zhuang P, Baburaj K, Serpersu EH, et al. (1999) Orientation of heparin-binding sites in native vitronectin. Analyses of ligand binding to the primary glycosaminoglycan-binding site indicate that putative secondary sites are not functional. J Biol Chem 274: 6432-6442.
46. Duensing TD, Wing JS, van Putten JP (1999) Sulfated polysaccharide-directed recruitment of mammalian host proteins: a novel strategy in microbial pathogenesis. Infect Immun 67: 4463-4468.
47. van Putten JP, Hayes SF, Duensing TD (1997) Natural proteoglycan receptor analogs determine the dynamics of Opa adhesin-mediated gonococcal infection of Chang epithelial cells. Infect Immun 65: 5028-5034.
48. Sinha B, Francois PP, Nusse O, Foti M, Hartford OM, et al. (1999) Fibronectinbinding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol 1: 101-117.
49. Schwarz-Linek U, Hook M, Potts JR (2004) The molecular basis of fibronectinmediated bacterial adherence to host cells. Mol Microbiol 52: 631-641.
50. Rostand KS, Esko JD (1997) Microbial adherence to and invasion through proteoglycans. Infect Immun 65: 1-8.
51. Dabo SM, Confer AW, Saliki JT, Anderson BE (2006) Binding of Bartonella henselae to extracellular molecules: identification of potential adhesins. Microb Pathog 41: 10-20.
52. Eberhard T, Virkola R, Korhonen T, Kronvall G, Ullberg M (1998) Binding to human extracellular matrix by Neisseria meningitidis. Infect Immun 66: 1791-1794.
53. Tomasini-Johansson BR, Ruoslahti E, Pierschbacher MD (1993) A 30 kD sulfated extracellular matrix protein immunologically cross reactive with vitronectin. Matrix 13: 203-214.
54. Huttner WB (1988) Tyrosine sulfation and the secretory pathway. Annu Rev Physiol 50: 363-376.
55. Liu J, Louie S, Hsu W, Yu KM, Nicholas HB, Jr., et al. (2008) Tyrosine sulfation is prevalent in human chemokine receptors important in lung disease. Am J Respir Cell Mol Biol 38: 738-743.
56. Farzan M, Vasilieva N, Schnitzler CE, Chung S, Robinson J, et al. (2000) A tyrosine-sulfated peptide based on the N terminus of CCR5 interacts with a CD4-enhanced epitope of the HIV-1 gp120 envelope glycoprotein and inhibits HIV-1 entry. J Biol Chem 275: 33516-33521.
57. Peake PW, Greenstein JD, Pussell BA, Charlesworth JA (1996) The behaviour of human vitronectin in vivo: effects of complement activation, conformation and phosphorylation. Clin Exp Immunol 106: 416-422.
58. Griffiths NJ, Cunha CS, Murillo I, Youssef A-R, Borodina E, Hill DJ, Virji M (2009) Dynamics of Neisseria meningitidis interactions with human cellular barriers and immune effectors. VacciMonitor (proceedings of NeisseriaVaccines 2009, Cuba) 18: 88-90.
59. Duensing TD, Putten JP (1998) Vitronectin binds to the gonococcal adhesion OpaA through a glycosaminoglycan molecular bridge. Biochem J 334: 133-139.
60. Stins MF, Gilles F, Kim KS (1997) Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 76: 81-90.
61. Achtman M, Neibert M, Crowe BA, Strittmatter W, Kusecek B, et al. (1988) 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.
62. Rosenqvist E, Hoiby EA, Wedege E, Bryn K, Kolberg J, et al. (1995) Human antibody responses to meningococcal outer membrane antigens after three doses of the Norwegian group B meningococcal vaccine. Infect Immun 63: 4642-4652.
63. Hill DJ, Virji M (2003) A novel cell-binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: specific targeting of the N-domain of carcinoembryonic antigen-related cell adhesion molecules by UspA1. Mol Microbiol 48: 117-129.
64. Liang OD, Preissner KT, Chhatwal GS (1997) The hemopexin-type repeats of human vitronectin are recognized by Streptococcus pyogenes. Biochem Biophys Res Commun 234: 445-449.
65. Liang OD, Flock JI, Wadstrom T (1995) Isolation and characterisation of a vitronectin-binding surface protein from Staphylococcus aureus. Biochim Biophys Acta 1250: 110-116.