The carboxyl-terminal SH3 domain of the mammalian adaptor CrkII promotes internalization of Listeria monocytogenes through activation of host phosphoinositide 3-kinase

Cellular Microbiology

Volumn 9, Issue 10, 2007, Pages 2497-2516

  Dokainish, Hatem ^a   Gavicherla, Balramakrishna ^b   Shen, Yang ^a   Ireton, Keith ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN CRKII; COAT PROTEIN; F ACTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN INIB; PROTEIN SH3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CERCOPITHECIDAE; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME REGULATION; GENE OVEREXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTERNALIZATION; LISTERIA MONOCYTOGENES; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN TRANSPORT; RNA INTERFERENCE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTINS; BACTERIAL PROTEINS; CELL MEMBRANE; CHROMONES; ENDOCYTOSIS; ENZYME ACTIVATION; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; LISTERIA MONOCYTOGENES; MEMBRANE PROTEINS; MORPHOLINES; PROTO-ONCOGENE PROTEINS C-CRK; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS;

BACTERIA (MICROORGANISMS); LISTERIA; LISTERIA MONOCYTOGENES; MAMMALIA;

EID: 34548431321     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.00976.x     Document Type: Article

References (67)

1. Akagi, T., Shishido, T., Murata, K., and Hanafusa, H. (2000) V-Crk activates the phosphoinositide 3-kinase Akt pathway in transformation. Proc Natl Acad Sci USA 97: 7290-7295.
2. Akakura, S., Kar, B., Singh, S., Cho, L., Tibrewal, N., Sanokawa-Akakura, R., et al. (2005) C-terminal SH3 domain of CrkII regulates the assembly and function of the Dock180/ELMO Rac-GEF. J Cell Physiol 204: 344-351.
3. Allen, L.A., Algood, J.A., Han, X., and Wittine, L.M. (2005) Phosphoinositide 3-kinase regulates actin polymerization during delayed phagocytosis of Helicobacter pylori. J Leukoc Biol 78: 220-230.
4. Araki, N., Johnson, M.T., and Swanson, J.A. (1996) A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 135: 1249-1260.
5. Basar, T., Shen, Y., and Ireton, K. (2005) Redundant roles for Met docking site tyrosines and the Gab1 PH domain in InlB-mediated entry of Listeria monocytogenes. Infect Immun 73: 2061-2074.
6. Benard, V., Bohl, B.P., and Bokoch, G.M. (1999) Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J Biol Chem 274: 13198-13204.
7. Bierne, H., Gouin, E., Roux, P., Caroni, P., Yin, H.L., and Cossart, P. (2001) A role for cofilin and LIM kinase in Listeria -induced phagocytosis. J Cell Biol 155: 101-112.
8. Bierne, H., Miki, H., Innocenti, M., Scita, G., Gertler, F.B., Takenawa, T., and Cossart, P. (2005) WASP-related proteins, Abi1 and Ena/VASP are required for Listeria invasion induced by the Met receptor. J Cell Sci 118: 1537-1547.
9. Birchmeier, C., Birchmeier, W., Gherardi, E., and Vande Woude, G.F. (2003) Met, metastasis, motility, and more. Nat Rev Mol Cell Biol 4: 915-925.
10. Bompard, B., and Caron, E. (2004) Regulation of WASP/WAVE proteins: making a long story short. J Cell Biol 166: 957-962.
11. Bougneres, L., Girardin, S.E., Weed, S.A., Karginov, A.V., Olivo-Marin, J.-C., Parsons, J.T., et al. (2004) Cortactin and Crk cooperate to trigger actin polymerization during Shigella invasion of epithelial cells. J Cell Biol 166: 225-235.
12. Braun, L., Dramsi, S., Dehoux, P., Bierne, H., Lindahl, G., and Cossart, P. (1997) InlB: An invasion protein of Listeria monocytogenes with a novel type of surface association. Mol Microbiol 25: 285-294.
13. Braun, L., Ohayon, H., and Cossart, P. (1998) The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol Microbiol 27: 1077-1087.
14. Braun, L., Nato, F., Payrastre, B., Mazie, J.-C., and Cossart, P. (1999) The 213 amino-acid leucine-rich repeat region of the Listeria monocytogenes InlB protein is sufficient for entry into mammalian cells, stimulation of PI 3 kinase, and membrane ruffling. Mol Microbiol 34: 10-23.
15. Burton, E.A., Plattner, R., and Pendergrast, A.M. (2003) Abl tyrosine kinases are required for infection by Shigella flexneri. EMBO J 22: 5471-5479.
16. Cote, J.F., Motoyama, A.B., Bush, J.A., and Vuori, K. (2005) A novel and evolutionarily conserved PtdIns(3,4,5)P3- binding domain is necessary for Dock180 signaling. Nat Cell Biol 7: 797-806.
17. Cox, D., Tseng, C.C., Bjekic, G., and Greenberg, S. (1999) A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J Biol Chem 274: 1240-1247.
18. D'Souza-Schorey, C., and Chavrier, P. (2006) ARF proteins: Roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7: 347-358.
19. Dalgarno, D.C., Botfield, M.C., and Rickles, R.J. (1997) SH3 domains and drug design: Ligands, structure, and biological function. Biopoly 43: 383-400.
20. Dramsi, S., Biswas, I., Maguin, E., Braun, L., Mastroeni, P., and Cossart, P. (1995) Entry of L. monocytogenes into hepatocytes requires expression of InlB, a surface protein of the internalin multigene family. Mol Microbiol 16: 251-261.
21. Feller, S.M. (2001) Crk family adaptors-signalling complex formation and biological roles. Oncogene 20: 6348-6371.
22. Gaillard, J.L., Berche, P., Mounier, J., Richard, S., and Sansonetti, P.J. (1987) In vitro model of penetration and intracellular growth of L. monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun 55: 2822-2829.
23. Gelkop, S., Baichev, Y., and Isakov, N. (2001) T cell activation induces direct binding of the Crk adaptor protein to the regulatory subunit of phosphatidylinositol 3-kinase (p85) via a complex mechanism involving the Cbl protein. J Biol Chem 276: 36174-36182.
24. Giardini, P.A., and Theriot, J.A. (2001) Effects of intermediate filaments on actin-based motility of Listeria monocytogenes. Biophys J 81: 3193-3203.
25. Goh, E.L.K., Zhu, T., Yakar, S., LeRoith, D., and Lobie, P.E. (2000) CrkII participation in the cellular effects of growth hormone and insulin-like growth factor-1. J Biol Chem 275: 17683-17692.
26. Gouin, E., Dehoux, P., Mengaud, J., Kocks, C., and Cossart, P. (1995) iactA of Listeria ivanovii, although distantly related to Listeria monocytogenes actA, restores actin tail formation in an L. monocytogenes actA mutant. Infect Immun 63: 2729-2737.
27. Haugh, J.M., Codazzi, F., Truel, M., and Meyer, T. (2000) Spatial sensing in fibroblasts mediated by 3′ phosphoinositides. J Cell Biol 151: 1269-1279.
28. Heidi, C.E., Welch, W., Coadwell, J., Stephens, L.R., and Hawkins, P.T. (2003) Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett 546: 93-97.
29. Hirai, T., and Chida, K. (2003) Protein kinase Cζ (PKCζ) activation mechanisms and cellular functions. J Biochem 133: 1-7.
30. Insall, R.H., and Weiner, O.D. (2001) PIP3, PIP2, and cell movement -similar messages, different meanings? Dev Cell 1: 743-747.
31. Ireton, K. (2006) Listeria monocytogenes. In Bacterial Genomes and Infectious Diseases. Chan, V.L., Sherman, P.M., and Bourke, B. (eds). Totowa, NJ: Humana Press, pp. 125-149.
32. Ireton, K., Payrastre, B., Chap, H., Ogawa, W., Sakaue, H., Kasuga, M., and Cossart, P. (1996) A role for phosphoinositide 3-kinase in bacterial invasion. Science 274: 780-782.
33. Ireton, K., Payrastre, B., and Cossart, P. (1999) The Listeria monocytogenes protein InlB is an agonist of mammalian Phosphoinositide 3-kinase. J Biol Chem 274: 17025-17032.
34. Kim, D., and Chung, J. (2002) Akt: Versatile mediator of cell survival and beyond. J Biochem Mol Biol 35: 106-115.
35. Kizaka-Kondoh, S., Matsuda, M., and Okayama, H. (1996) CrkII signals from epidermal growth factor receptor to ras. Proc Natl Acad Sci USA 93: 12177-12182.
36. Kontos, C.D., Stauffer, P.T., Yang, W.P., York, J.D., Huang, L., Blanar, M.A., et al. (1998) Tyrosine 1101 of Tie2 is the major site of association of p85 and is required for activation of phosphatidylinositol 3-kinase and Akt. Mol Cell Biol 18: 4131-4140.
37. Larson, S.M., and Davidson, A.R. (2000) The identification of conserved interactions within the SH3 domain by alignment of sequences and structures. Protein Sci 9: 2170-2180.
38. Marshall, J.G., Booth, J.W., Stambolic, V., Mak, T., Balla, T., Schrieber, A.D., et al. (2001) Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fc gamma receptor-mediated phagocytosis. J Cell Biol 153: 1369-1380.
39. Matsuda, M., Tanaka, S., Nagata, S., Kojima, A., Kurata, T., and Shibuya, M. (1992) Two species of human CRK cDNA encode proteins with distinct biological activities. Mol Cell Biol 12: 3482-3489.
40. Mengaud, J., Ohayon, H., Gounon, P., Mège, R.M., and Cossart, P. (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of Listeria monocytogenes into epithelial cells. Cell 84: 923-932.
41. Muralidharan, V., Dutta, K., Cho, J., Vila-Perello, M., Raleigh, D.P., Cowburn, D., and Muir, T.W. (2006) Solution structure and folding characteristics of he C-terminal SH3 domain of c-CrkII. Biochemistry 45: 8874-8884.
42. Ninomiya, N., Hazeki, K., Fukui, Y., Seya, T., Okada, T., Hazeki, O., and Ui, M. (1994) Involvment of phosphatidylinositol 3-kinase in Fcγ receptor signaling. J Biol Chem 269: 22732-22737.
43. Nobes, C.D., Hawkins, P., Stephens, L., and Hall, A. (1995) Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J Cell Sci 108: 225-233.
44. Ogawa, S., Toyoshima, H., Kozutsumi, H., Hagiwara, K., Sakai, R., Tanaka, T., et al. (1994) The C-terminal SH3 domain of the mouse c-Crk protein negatively regulates tyrosine-phosphorylation of Crk associated p130 in rat 3Y1 cells. Oncogene 9: 1669-1678.
45. Ota, S., Kizaka-Kondoh, S., Hashimoto, Y., Nishihara, H., Nagashima, K., Kurata, T., et al. (1998) Constitutive association of EGF receptor with the CrkII-23 mutant that inhibits transformation of NRK cells by EGF and TGF-beta. Cell Signal 10: 283-290.
46. Pizarro-Cerda, J., and Cossart, P. (2006) Bacterial Adhesion and Entry into Host cells. Cell 124: 715-727.
47. Pizarro-Cerda, J., Jonquieres, R., Gouin, E., Vandekerckhove, J., Garin, J., and Cossart, P. (2002) Distinct protein patterns associated with Listeria monocytogenes InlA- or InlB-phagosomes. Cell Microbiol 4: 101-115.
48. Powner, D.J., and Wakelam, M.J.O. (2002) The regulation of phospholipase D by inositol phospholipids and small GTPases. FEBS Lett 531: 62-64.
49. Reichman, C., Singh, K., Liu, Y., Singh, S., Li, H., Fajardo, J.E., et al. (2005) Transactivation of Abl with the CrkII adapter protein requires a PNAY sequence in the Crk C-terminal SH3 domain. Oncogene 24: 8187-8199.
50. Reuther, G.W., and Der, C.J. (2000) The Ras brance of small GTPases: Ras family members don't fall far from the tree. Curr Opin Cell Biol 12: 157-165.
51. Rodriguez-Viciana, P., Warne, P.H., Vanhaesebroeck, B., Waterfield, M.D. and Downward, J. (1996) Activation of phosphoinositide 3-kinase by interaction with Ras and by point mutation. EMBO J 15: 2442-2451.
52. Sarkar, P., Reichman, C., Saleh, T., Birge, R.B., and Kalodimos, C.G. (2007) Proline cis-trans isomerization controls autoinhibition of a signaling protein. Mol Cell 25: 413-426.
53. Sattler, M., Salgia, R., Shrikhande, G., Verma, S., Pisick, E., Prasad, K.V.S., and Griffin, J.D. (1997) Steel factor induces tyrosine phosphorylation of CrkL and binding of CrkL to a complex containing c-Kit, phosphatidylinositol 3-kinase, and p120Cbl. J Biol Chem 272: 10248-10253.
54. Schmidt, A., and Hall, A. (2002) Guanine nucleotide exchange factors for Rho GTPases: Turning on the switch. Genes Dev 16: 1587-1609.
55. Senechal, D., Heaney, C., Druker, B., and Sawyers, C.L. (1998) Strutural requirements for function of the CrkL adapter protein in fibroblasts and hematopoietic cells. Mol Cell Biol 18: 5082-5090.
56. Servant, G., Weiner, O.D., Hezmark, P., Balla, T., Sedat, J.W., and Bourne, H.R. (2000) Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287: 1037-1040.
57. Seveau, S., Tham, T.N., Payrastre, B., Hoppe, A.D., Swanson, J.A., and Cossart, P. (2007) A FRET analysis to unravel the role of cholesterol in Rac1 and PI 3 kinase activation in the InlB/Met signalling pathway. Cell Microbiol 9: 790-803.
58. Shen, Y., Naujokas, M., Park, M., and Ireton, K. (2000) InlB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103: 501-510.
59. Sousa, S., Lecuit, M., and Cossart, P. (2005) Microbial strategies to target, cross, or disrupt epithelia. Curr Opin Cell Biol 17: 489-498.
60. Sun, H., Shen, Y., Dokainish, H., Holgado-Madruga, M., Wong, A., and Ireton, K. (2005) Host adaptor proteins Gab1 and CrkII promote InlB-dependent entry of Listeria monocytogenes. Cell Microbiol 7: 443-457.
61. Suzuki, M., Mimuro, H., Suzuki, T., Park, M., Yamamoto, T., and Sasakawa, C. (2005) Interaction of CagA with Crk plays an important role in Helicobacter pylori -induced loss of gastric epithelial cell adhesion. J Exp Med 202: 1235-1247.
62. Tanaka, M., Gupta, R., and Mayer, B.J. (1995) Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins. Mol Cell Biol 15: 6829-6837.
63. Vazquez-Boland, J.A., Kuhn, M., Berche, P., Charkraborty, T., Dominguez-Bernal, G., Goebel, W., et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
64. Veiga, E., and Cossart, P. (2005) Listeria hijacks the clathriin-dependent endocytic machinery to invade mammalian cells. Nat Cell Biol 7: 894-900.
65. Watton, S.J., and Downward, J. (1999) Akt/PKB localization and 3′ phosphoinositide generation at sites of epithelial cell-matrix and cell-cell interaction. Curr Biol 9: 433-436.
66. Wymann, M.P., Zvelebil, M., and Laffargue, M. (2003) Phosphoinositide 3-kinase signalling -which way to target? Trends Pharmacol Sci 24: 366-376.
67. Zvara, A., Fajardo, J.E., Escalante, M., Cotton, G., Muir, T., Kirsch, K.H., and Birge, R.B. (2001) Activation of the focal adhesion kinase signaling pathway by structural alterations in the carboxyl-terminal region of c-CrkII. Oncogene 20: 951-961.