Cell invasion by neisseria meningitidis requires a functional interplay between the focal adhesion kinase, Src and cortactin

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Slanina, Heiko ^a   Hebling, Sabrina ^a   Hauck, Christoph R ^b   Schubert Unkmeir, Alexandra ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; CORTACTIN; DYNAMIN; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE INHIBITOR; MEMBRANE PROTEIN; PF 573228; PROTEIN OPC; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; BRAIN; CELL INVASION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; ENZYME INHIBITION; FIBROBLAST; GENE MUTATION; GENE SILENCING; HUMAN; HUMAN CELL; INTERNALIZATION; MICROVASCULAR ENDOTHELIAL CELL; MUTANT; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE;

ACTIN CYTOSKELETON; ANIMALS; BRAIN; CORTACTIN; ENDOCYTOSIS; ENDOTHELIAL CELLS; FIBROBLASTS; FOCAL ADHESION KINASE 1; HOST-PATHOGEN INTERACTIONS; HUMANS; INTEGRINS; MICE; MICROVESSELS; NEISSERIA MENINGITIDIS; PHOSPHORYLATION; PHOSPHOTYROSINE; SRC-FAMILY KINASES;

EUKARYOTA; NEISSERIA MENINGITIDIS;

EID: 84863111001     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039613     Document Type: Article

References (72)

1. Schmitt C, Turner D, Boesl M, Abele M, Frosch M, et al. (2007) A functional two-partner secretion system contributes to adhesion of Neisseria meningitidis to epithelial cells. J Bacteriol 189: 7968-7976.
2. Comanducci M, Bambini S, Brunelli B, Adu-Bobie J, Arico B, et al. (2002) NadA, a novel vaccine candidate of Neisseria meningitidis. J Exp Med 195: 1445-1454.
3. Turner DP, Marietou AG, Johnston L, Ho KK, Rogers AJ, et al. (2006) Characterization of MspA, an immunogenic autotransporter protein that mediates adhesion to epithelial and endothelial cells in Neisseria meningitidis. Infect Immun 74: 2957-2964.
4. Scarselli M, Serruto D, Montanari P, Capecchi B, Adu-Bobie J, et al. (2006) Neisseria meningitidis NhhA is a multifunctional trimeric autotransporter adhesin. Mol Microbiol 61: 631-644.
5. Virji M, (2009) Pathogenic neisseriae: surface modulation, pathogenesis and infection control. Nat Rev Microbiol 7: 274-286.
6. Achtman M, (1995) Epidemic spread and antigenic variability of Neisseria meningitidis. Trends Microbiol 3: 186-192.
7. Zhu P, Morelli G, Achtman M, (1999) The opcA and (psi)opcB regions in Neisseria: genes, pseudogenes, deletions, insertion elements and DNA islands. Mol Microbiol 33: 635-650.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. Sa ECC, Griffiths NJ, Virji M, (2010) Neisseria meningitidis Opc invasin binds to the sulphated tyrosines of activated vitronectin to attach to and invade human brain endothelial cells. PLoS Pathog 6: e1000911.
16. Preissner KT, (1991) Structure and biological role of vitronectin. Annu Rev Cell Biol 7: 275-310.
17. Sawaya R, Cummins CJ, Smith BH, Kornblith PL, (1985) Plasma fibronectin in patients with brain tumors. Neurosurgery 16: 161-165.
18. Slanina H, Konig A, Hebling S, Hauck CR, Frosch M, et al. (2010) Entry of Neisseria meningitidis into mammalian cells requires the Src family protein tyrosine kinases. Infect Immun 78: 1905-1914.
19. Hynes RO, (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25.
20. Sinha B, Francois PP, Nusse O, Foti M, Hartford OM, et al. (1999) Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol 1: 101-117.
21. Fowler T, Wann ER, Joh D, Johansson S, Foster TJ, et al. (2000) Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur J Cell Biol 79: 672-679.
22. Isberg RR, Leong JM, (1990) Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60: 861-871.
23. Bergmann S, Lang A, Rohde M, Agarwal V, Rennemeier C, et al. (2009) Integrin-linked kinase is required for vitronectin-mediated internalization of Streptococcus pneumoniae by host cells. J Cell Sci 122: 256-267.
24. Miyamoto S, Teramoto H, Coso OA, Gutkind JS, Burbelo PD, et al. (1995) Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol 131: 791-805.
25. Miyamoto S, Akiyama SK, Yamada KM, (1995) Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267: 883-885.
26. Zamir E, Geiger B, (2001) Molecular complexity and dynamics of cell-matrix adhesions. J Cell Sci 114: 3583-3590.
27. Zaidel-Bar R, Ballestrem C, Kam Z, Geiger B, (2003) Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J Cell Sci 116: 4605-4613.
28. Hauck CR, Hsia DA, Schlaepfer DD, (2002) The focal adhesion kinase-a regulator of cell migration and invasion. IUBMB Life 53: 115-119.
29. Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA, (2002) Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420: 89-93.
30. Wickstrom SA, Lange A, Montanez E, Fassler R, (2010) The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase! Embo J 29: 281-291.
31. Schubert-Unkmeir A, Konrad C, Slanina H, Czapek F, Hebling S, et al. (2010) Neisseria meningitidis induces brain microvascular endothelial cell detachment from the matrix and cleavage of occludin: a role for MMP-8. PLoS Pathog 6: e1000874.
32. Schlaepfer DD, Mitra SK, Ilic D, (2004) Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim Biophys Acta 1692: 77-102.
33. Schlaepfer DD, Hauck CR, Sieg DJ, (1999) Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71: 435-478.
34. Mitra SK, Hanson DA, Schlaepfer DD, (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6: 56-68.
35. Uruno T, Liu J, Zhang P, Fan Y, Egile C, et al. (2001) Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat Cell Biol 3: 259-266.
36. Sokolova O, Heppel N, Jagerhuber R, Kim KS, Frosch M, et al. (2004) 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: 1153-1166.
37. Ridley AJ, Hall A, (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389-399.
38. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, et al. (2007) Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 282: 14845-14852.
39. Schaller MD, Borgman CA, Parsons JT, (1993) Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK. Mol Cell Biol 13: 785-791.
40. Klinghoffer RA, Sachsenmaier C, Cooper JA, Soriano P, (1999) Src family kinases are required for integrin but not PDGFR signal transduction. 18: 2459-2471.
41. Cosen-Binker LI, Kapus A, (2006) Cortactin: the gray eminence of the cytoskeleton. Physiology (Bethesda) 21: 352-361.
42. 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.
43. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, et al. (2001) Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11: 370-374.
44. Weed SA, Karginov AV, Schafer DA, Weaver AM, Kinley AW, et al. (2000) Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J Cell Biol 151: 29-40.
45. Weed SA, Parsons JT, (2001) Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20: 6418-6434.
46. Pendergrass W, Wolf N, Poot M, (2004) Efficacy of MitoTracker Green and CMXrosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry A 61: 162-169.
47. Reddy MA, Wass CA, Kim KS, Schlaepfer DD, Prasadarao NV, (2000) Involvement of focal adhesion kinase in Escherichia coli invasion of human brain microvascular endothelial cells. Infect Immun 68: 6423-6430.
48. Eitel J, Heise T, Thiesen U, Dersch P, (2005) Cell invasion and IL-8 production pathways initiated by YadA of Yersinia pseudotuberculosis require common signalling molecules (FAK, c-Src, Ras) and distinct cell factors. Cell Microbiol 7: 63-77.
49. Agerer F, Lux S, Michel A, Rohde M, Ohlsen K, et al. (2005) Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J Cell Sci 118: 2189-2200.
50. Cho BA, Cho NH, Seong SY, Choi MS, Kim IS, (2010) Intracellular invasion by Orientia tsutsugamushi is mediated by integrin signaling and actin cytoskeleton rearrangements. Infect Immun 78: 1915-1923.
51. Alrutz MA, Isberg RR, (1998) Involvement of focal adhesion kinase in invasin-mediated uptake. Proc Natl Acad Sci U S A 95: 13658-13663.
52. Alrutz MA, Srivastava A, Wong KW, D'Souza-Schorey C, Tang M, et al. (2001) Efficient uptake of Yersinia pseudotuberculosis via integrin receptors involves a Rac1-Arp 2/3 pathway that bypasses N-WASP function. Mol Microbiol 42: 689-703.
53. Isberg RR, Hamburger Z, Dersch P, (2000) Signaling and invasin-promoted uptake via integrin receptors. Microbes Infect 2: 793-801.
54. Agerer F, Michel A, Ohlsen K, Hauck CR, (2003) Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J Biol Chem 278: 42524-42531.
55. Kim KS, (2008) Mechanisms of microbial traversal of the blood-brain barrier. Nat Rev Microbiol 6: 625-634.
56. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B, (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 9: 858-867.
57. Selbach M, Backert S, (2005) Cortactin: an Achilles' heel of the actin cytoskeleton targeted by pathogens. Trends Microbiol 13: 181-189.
58. Hoffmann I, Eugene E, Nassif X, Couraud PO, Bourdoulous S, (2001) Activation of ErbB2 receptor tyrosine kinase supports invasion of endothelial cells by Neisseria meningitidis. J Cell Biol 155: 133-143.
59. Higgs HN, Pollard TD, (2001) Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 70: 649-676.
60. Tegtmeyer N, Wittelsberger R, Hartig R, Wessler S, Martinez-Quiles N,et al. Serine phosphorylation of cortactin controls focal adhesion kinase activity and cell scattering induced by Helicobacter pylori. Cell Host Microbe 9: 520-531.
61. Cantarelli VV, Takahashi A, Akeda Y, Nagayama K, Honda T, (2000) Interaction of enteropathogenic or enterohemorrhagic Escherichia coli with HeLa cells results in translocation of cortactin to the bacterial adherence site. Infect Immun 68: 382-386.
62. Cantarelli VV, Takahashi A, Yanagihara I, Akeda Y, Imura K, et al. (2002) Cortactin is necessary for F-actin accumulation in pedestal structures induced by enteropathogenic Escherichia coli infection. Infect Immun 70: 2206-2209.
63. Dehio C, Prevost MC, Sansonetti PJ, (1995) Invasion of epithelial cells by Shigella flexneri induces tyrosine phosphorylation of cortactin by a pp60c-src-mediated signalling pathway. Embo J 14: 2471-2482.
64. Chen XM, Huang BQ, Splinter PL, Cao H, Zhu G, et al. (2003) Cryptosporidium parvum invasion of biliary epithelia requires host cell tyrosine phosphorylation of cortactin via c-Src. Gastroenterology 125: 216-228.
65. Frischknecht F, Moreau V, Rottger S, Gonfloni S, Reckmann I, et al. (1999) Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401: 926-929.
66. Zaidel-Bar R, Cohen M, Addadi L, Geiger B, (2004) Hierarchical assembly of cell-matrix adhesion complexes. Biochem Soc Trans 32: 416-420.
67. McGuinness BT, Clarke IN, Lambden PR, Barlow AK, Heckels JE, et al. (1991) Point mutation in meningococcal por A gene associated with increased endemic disease. The Lancet 337: 514-517.
68. Stins MF, Gilles F, Kim KS, (1997) Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 76: 81-90.
69. Sieg DJ, Hauck CR, Schlaepfer DD, (1999) Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci 112 (Pt 16): 2677-2691.
70. Schlaepfer DD, Hunter T, (1996) Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol Cell Biol 16: 5623-5633.
71. Agerer F, Waeckerle S, Hauck CR, (2004) Microscopic quantification of bacterial invasion by a novel antibody-independent staining method. J Microbiol Methods 59: 23-32.
72. Tehrani S, Faccio R, Chandrasekar I, Ross FP, Cooper JA, (2006) Cortactin has an essential and specific role in osteoclast actin assembly. Mol Biol Cell 17: 2882-2895.