Bacterial cyclomodulin Cif blocks the host cell cycle by stabilizing the cyclin-dependent kinase inhibitors p21waf1 and p27kip1

Cellular Microbiology

Volumn 10, Issue 12, 2008, Pages 2496-2508

  Samba louaka, Ascel ^a,b   Nougayrède, Jean Philippe ^a,b   Watrin, Claude ^a,b   Jubelin, Grégory ^a,b   Oswald, Eric ^a,b   Taieb, Frédéric ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLE INHIBITING FACTOR; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; PROTEIN P53; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL STRAIN; CONTROLLED STUDY; CORRELATION ANALYSIS; ENTEROPATHOGENIC ESCHERICHIA COLI; HUMAN; HUMAN CELL; INTESTINE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

CDC2 PROTEIN KINASE; CELL CYCLE; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 55749091664     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01224.x     Document Type: Article

References (54)

1. Abramovitch, R.B., Janjusevic, R., Stebbins, C.E., and Martin, G.B. (2006) Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Natl Acad Sci USA 103: 2851-2856.
2. Alevizopoulos, K., Catarin, B., Vlach, J., and Amati, B. (1998) A novel function of adenovirus E1A is required to overcome growth arrest by the CDK2 inhibitor p27 (Kip1). EMBO J 17: 5987-5997.
3. Amini, S., Saunders, M., Kelley, K., Khalili, K., and Sawaya, B.E. (2004) Interplay between HIV-1 Vpr and Sp1 modulates p21 (WAF1) gene expression in human astrocytes. J Biol Chem 279: 46046-46056.
4. Azuma, A., Matsuo, A., Suzuki, T., Kurosawa, T., Zhang, X., and Aida, Y. (2006) Human immunodeficiency virus type 1 Vpr induces cell cycle arrest at the G(1) phase and apoptosis via disruption of mitochondrial function in rodent cells. Microbes Infect 8: 670-679.
5. Blagosklonny, M.V., Wu, G.S., Omura, S., and el-Deiry, W.S. (1996) Proteasome-dependent regulation of p21WAF1/CIP1 expression. Biochem Biophys Res Commun 227: 564-569.
6. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J.P., et al. (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
7. Cayrol, C., and Ducommun, B. (1998) Interaction with cyclin-dependent kinases and PCNA modulates proteasome-dependent degradation of p21. Oncogene 17: 2437-2444.
8. Cayrol, C., Knibiehler, M., and Ducommun, B. (1998) p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells. Oncogene 16: 311-320.
9. Charpentier, X., and Oswald, E. (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186: 5486-5495.
10. Chowdhury, I.H., Wang, X.F., Landau, N.R., Robb, M.L., Polonis, V.R., Birx, D.L., and Kim, J.H. (2003) HIV-1 Vpr activates cell cycle inhibitor p21/Waf1/Cip1: A potential mechanism of G2/M cell cycle arrest. Virology 305: 371-377.
11. el-Deiry, W.S., Tokino, T., Velculescu, V.E., Levy, D.B., Parsons, R., Trent, J.M., et al. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817-825.
12. Dulic, V., Beney, G.E., Frebourg, G., Drullinger, L.F., and Stein, G.H. (2000) Uncoupling between phenotypic senescence and cell cycle arrest in aging p21-deficient fibroblasts. Mol Cell Biol 20: 6741-6754.
13. Evers, B.M. (1999) Intestinal cell differentiation: Cellular mechanisms and the search for the perfect model focus on 'involvement of p21 (WAF1/ Cip1) and p27 (Kip1) in intestinal epithelial cell differentiation'. Am J Physiol 276: C1243-C1244.
14. Fenteany, G., Standaert, R.F., Lane, W.S., Choi, S., Corey, E.J., and Schreiber, S.L. (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268: 726-731.
15. de La Fuente, C., Santiago, F., Chong, S.Y., Deng, L., Mayhood, T., Fu, P., et al. (2000) Overexpression of p21(waf1) in human T-cell lymphotropic virus type 1-infected cells and its association with cyclin A/cdk2. J Virol 74: 7270-7283.
16. Gabastou, J.M., Kerneis, S., Bernet-Camard, M.F., Barbat, A., Coconnier, M.H., Kaper, J.B., and Servin, A.L. (1995) Two stages of enteropathogenic Escherichia coli intestinal pathogenicity are up and down-regulated by the epithelial cell differentiation. Differentiation 59: 127-134.
17. Gartel, A.L. (2006) Is p21 an oncogene? Mol Cancer Ther 5: 1385-1386.
18. Gartel, A.L., and Tyner, A.L. (2002) The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Ther 1: 639-649.
19. Gartel, A.L., Goufman, E., Najmabadi, F., and Tyner, A.L. (2000) Sp1 and Sp3 activate p21 (WAF1/CIP1) gene transcription in the Caco-2 colon adenocarcinoma cell line. Oncogene 19: 5182-5188.
20. Han, J.W., Ahn, S.H., Park, S.H., Wang, S.Y., Bae, G.U., Seo, D.W., etal. (2000) Apicidin, a histone deacetylase inhibitor, inhibits proliferation of tumor cells via induction of p21WAF1/Cip1 and gelsolin. Cancer Res 60: 6068-6074.
21. Harper, J.W., Elledge, S.J., Keyomarsi, K., Dynlacht, B., Tsai, L.H., Zhang, P., et al. (1995) Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell 6: 387-400.
22. He, J., Choe, S., Walker, R., Di Marzio, P., Morgan, D.O., and Landau, N.R. (1995) Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J Virol 69: 6705-6711.
23. Heron-Milhavet, L., Franckhauser, C., Rana, V., Berthenet, C., Fisher, D., Hemmings, B.A., et al. (2006) Only Akt1 is required for proliferation, while Akt2 promotes cell cycle exit through p21 binding. Mol Cell Biol 26: 8267-8280.
24. Hsieh, F.F., Barnett, L.A., Green, W.F., Freedman, K., Matushansky, I., Skoultchi, A.I., and Kelley, L.L. (2000) Cell cycle exit during terminal erythroid differentiation is associated with accumulation of p27 (Kip1) and inactivation of cdk2 kinase. Blood 96: 2746-2754.
25. Iwai, H., Kim, M., Yoshikawa, Y., Ashida, H., Ogawa, M., Fujita, Y., et al. (2007) A bacterial effector targets Mad2L2, an APC inhibitor, to modulate host cell cycling. Cell 130: 611-623.
26. Kim, D.W., Lenzen, G., Page, A.L., Legrain, P., Sansonetti, P.J., and Parsot, C. (2005a) The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci USA 102: 14046-14051.
27. Kim, H., Kokkotou, E., Na, X., Rhee, S.H., Moyer, M.P., Pothoulakis, C., and Lamont, J.T. (2005b) Clostridium difficile toxin A-induced colonocyte apoptosis involves p53-dependent p21 (WAF1/CIP1) induction via p38 mitogen-activated protein kinase. Gastroenterology 129: 1875-1888.
28. Koff, A., and Polyak, K. (1995) p27KIP1, an inhibitor of cyclin-dependent kinases. Prog Cell Cycle Res 1: 141-147.
29. Lee, D.H., and Goldberg, A.L. (1998) Proteasome inhibitors: Valuable new tools for cell biologists. Trends Cell Biol 8: 397-403.
30. Marches, O., Ledger, T.N., Boury, M., Ohara, M., Tu, X., Goffaux, F., et al. (2003) Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol 50: 1553-1567.
31. Mueller, P.R., Coleman, T.R., and Dunphy, W.G. (1995) Cell cycle regulation of a Xenopus Wee1-like kinase. Mol Biol Cell 6: 119-134.
32. Niculescu, A.B., 3rd, Chen, X., Smeets, M., Hengst, L., Prives, C., and Reed, S.I. (1998) Effects of p21 (Cip1/Waf1) at both the G1/S and the G2/ M cell cycle transitions: PRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol Cell Biol 18: 629-643.
33. Nougayrede, J.P., Boury, M., Tasca, C., Marches, O., Milon, A., Oswald, E., and De Rycke, J. (2001) Type III secretion-dependent cell cycle block caused in HeLa cells by enteropathogenic Escherichia coli O103. Infect Immun 69: 6785-6795.
34. Nougayrede, J.P., Taieb, F., De Rycke, J., and Oswald, E. (2005) Cyclomodulins: Bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 13: 103-110.
35. Nougayrede, J.P., Homburg, S., Taieb, F., Boury, M., Brzuszkiewicz, E., Gottschalk, G., et al. (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313: 848-851.
36. Oswald, E., Nougayrede, J.P., Taieb, F., and Sugai, M. (2005) Bacterial toxins that modulate host cell-cycle progression. Curr Opin Microbiol 8: 83-91.
37. Peres, S.Y., Marches, O., Daigle, F., Nougayrede, J.P., Herault, F., Tasca, C., et al. (1997) A new cytolethal distending toxin (CDT) from Escherichia coli producing CNF2 blocks HeLa cell division in G2/M phase. Mol Microbiol 24: 1095-1107.
38. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: E45.
39. Philipp-Staheli, J., Kim, K.H., Liggitt, D., Gurley, K.E., Longton, G., and Kemp, C.J. (2004) Distinct roles for p53, 27Kip1, and p21Cip1 during tumor development. Oncogene 23: 905-913.
40. Polyak, K., Kato, J.Y., Solomon, M.J., Sherr, C.J., Massague, J., Roberts, J.M., and Koff, A. (1994) p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 8: 9-22.
41. Re, F., Braaten, D., Franke, E.K., and Luban, J. (1995) Human immunodeficiency virus type 1 Vpr arrests the cell cycle in G2 by inhibiting the activation of p34cdc2-cyclin B. J Virol 69: 6859-6864.
42. Rytkonen, A., and Holden, D.W. (2007) Bacterial interference of ubiquitination and deubiquitination. Cell Host Microbe 1: 13-22.
43. Rytkonen, A., Poh, J., Garmendia, J., Boyle, C., Thompson, A., Liu, M., etal. (2007) SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci USA 104: 3502-3507.
44. Sert, V., Cans, C., Tasca, C., Bret-Bennis, L., Oswald, E., Ducommun, B., and De Rycke, J. (1999) The bacterial cytolethal distending toxin (CDT) triggers a G2 cell cycle checkpoint in mammalian cells without preliminary induction of DNA strand breaks. Oncogene 18: 6296-6304.
45. Steinhilb, M.L., Turner, R.S., and Gaut, J.R. (2001) The protease inhibitor, MG132, blocks maturation of the amyloid precursor protein Swedish mutant preventing cleavage by beta-Secretase. J Biol Chem 276: 4476-4484.
46. Taieb, F., Nougayrede, J.P., Watrin, C., Samba-Louaka, A., and Oswald, E. (2006) Escherichia coli cyclomodulin Cif induces G arrest of the host cell cycle without activation of the DNA-damage checkpoint-signalling pathway. Cell Microbiol 8: 1910-1921.
47. Tian, J.Q., and Quaroni, A. (1999) Involvement of p21 (WAF1/Cip1) and p27 (Kip1) in intestinal epithelial cell differentiation. Am J Physiol 276: C1245-C1258.
48. Waldman, T., Kinzler, K.W., and Vogelstein, B. (1995) p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 55: 5187-5190.
49. Watanabe, N., Broome, M., and Hunter, T. (1995) Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J 14: 1878-1891.
50. Watanabe, N., Arai, H., Nishihara, Y., Taniguchi, M., Hunter, T., and Osada, H. (2004) M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP. Proc Natl Acad Sci USA 101: 4419-4424.
51. Watanabe, N., Arai, H., Iwasaki, J., Shiina, M., Ogata, K., Hunter, T., and Osada, H. (2005) Cyclin-dependent kinase (CDK) phosphorylation destabilizes somatic Wee1 via multiple pathways. Proc Natl Acad Sci USA 102: 11663-11668.
52. Yokoyama, K., Higashi, H., Ishikawa, S., Fujii, Y., Kondo, S., Kato, H., etal. (2005) Functional antagonism between Helicobacter pylori CagA and vacuolating toxin VacA in control of the NFAT signaling pathway in gastric epithelial cells. Proc Natl Acad Sci USA 102: 9661-9666.
53. Zhou, B.B., and Elledge, S.J. (2000) The DNA damage response: Putting checkpoints in perspective. Nature 408: 433-439.
54. Zhou, H., Monack, D.M., Kayagaki, N., Wertz, I., Yin, J., Wolf, B., and Dixit, V.M. (2005) Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J Exp Med 202: 1327-1332.