PP2A-dependent disruption of centrosome replication and cytoskeleton organization in Drosophila by SV40 small tumor antigen

Oncogene

Volumn 27, Issue 49, 2008, Pages 6334-6346

  Kotadia, S ^a   Kao, L R ^a   Comerford, S A ^a   Jones, R T ^a   Hammer, R E ^a   Megraw, T L ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Aneuploidy; Centriole; Centrosome; Cyclin E; PP2A; SV40 ST

Indexed keywords

CYCLIN E; PHOSPHOPROTEIN PHOSPHATASE 2A; TUMOR ANTIGEN;

ANTIGEN EXPRESSION; ARTICLE; CENTROSOME; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; GENE INTERACTION; GENE MUTATION; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SIMIAN VIRUS 40;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, POLYOMAVIRUS TRANSFORMING; CELL LINE; CENTROSOME; CYTOSKELETON; DROSOPHILA; EMBRYO, NONMAMMALIAN; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLUTATHIONE TRANSFERASE; HETEROZYGOTE; IMMUNOHISTOCHEMISTRY; MUTATION; PROTEIN PHOSPHATASE 2; RECOMBINANT FUSION PROTEINS; SIMIAN VIRUS 40;

SIMIAN VIRUS 40; VERTEBRATA;

EID: 54549104698     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.254     Document Type: Article

References (66)

1. Ahuja D, Saenz-Robles MT, Pipas JM. (2005). SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 24: 7729-7745.
2. Arroyo JD, Hahn WC. (2005). Involvement of PP2A in viral and cellular transformation. Oncogene 24: 7746-7755.
3. Brinkley BR. (2001). Managing the centrosome numbers game: from chaos to stability in cancer cell division. Trends Cell Biol 11: 18-21.
4. Brumby AM, Richardson HE. (2003). Scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J 22: 5769-5779.
5. Callaini G, Riparbelli MG. (1990). Centriole and centrosome cycle in the early Drosophila embryo. J Cell Sci 97(Part 3): 539-543.
6. Chen F, Archambault V, Kar A, Lio P, D'Avino PP, Sinka R et al. (2007a). Multiple protein phosphatases are required for mitosis in Drosophila. Curr Biol 17: 293-303.
7. Chen W, Possemato R, Campbell KT, Plattner CA, Pallas DC, Hahn WC. (2004). Identification of specific PP2A complexes involved in human cell transformation. Cancer Cell 5: 127-136.
8. Chen Y, Xu Y, Bao Q, Xing Y, Li Z, Lin Z et al. (2007b). Structural and biochemical insights into the regulation of protein phosphatase 2A by small t antigen of SV40. Nat Struct Mol Biol 14: 527-534.
9. Cho US, Morrone S, Sablina AA, Arroyo JD, Hahn WC, Xu W. (2007). Structural basis of PP2A inhibition by small t antigen. PLoS Biol 5: e202.
10. Cho US, Xu W. (2007). Crystal structure of a protein phosphatase 2A heterotrimeric holoenzyme. Nature 445: 53-57.
11. Comerford SA, Clouthier DE, Hinnant EA, Hammer RE. (2003). Induction of hepatocyte proliferation and death by modulation of T-Antigen expression. Oncogene 22: 2515-2530.
12. Crawford JM, Harden N, Leung T, Lim L, Kiehart DP. (1998). Cellularization in Drosophila melanogaster is disrupted by the inhibition of rho activity and the activation of Cdc42 function. Dev Biol 204: 151-164.
13. De Luca A, Mangiacasale R, Severino A, Malquori L, Baldi A, Palena A et al. (2003). E1A deregulates the centrosome cycle in a Ran GTPase-dependent manner. Cancer Res 63: 1430-1437.
14. Duensing A, Liu Y, Perdreau SA, Kleylein-Sohn J, Nigg EA, Duensing S. (2007). Centriole overduplication through the concurrent formation of multiple daughter centrioles at single maternal templates. Oncogene 26: 6280-6288.
15. Duensing S, Duensing A, Lee DC, Edwards KM, Piboonniyom SO, Manuel E et al. (2004). Cyclin-dependent kinase inhibitor indirubin-3′-oxime selectively inhibits human papillomavirus type 16 E7-induced numerical centrosome anomalies. Oncogene 23: 8206-8215.
16. Duensing S, Munger K. (2003). Human papillomavirus type 16 E7 oncoprotein can induce abnormal centrosome duplication through a mechanism independent of inactivation of retinoblastoma protein family members. J Virol 77: 12331-12335.
17. Frost JA, Alberts AS, Sontag E, Guan K, Mumby MC, Feramisco JR. (1994). Simian virus 40 small t antigen cooperates with mitogen-activated kinases to stimulate AP-1 activity. Mol Cell Biol 14: 6244-6252.
18. Fujii R, Zhu C, Wen Y, Marusawa H, Bailly-Maitre B, Matsuzawa S et al. (2006). HBXIP, cellular target of hepatitis B virus oncoprotein, is a regulator of centrosome dynamics and cytokinesis. Cancer Res 66: 9099-9107.
19. Fukasawa K. (2007). Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 7: 911-924.
20. Gaillard S, Fahrbach KM, Parkati R, Rundell K. (2001). Overexpression of simian virus 40 small-T antigen blocks centrosome function and mitotic progression in human fibroblasts. J Virol 75: 9799-9807.
21. Goetz F, Tzeng YJ, Guhl E, Merker J, Graessmann M, Graessmann A. (2001). The SV40 small t-antigen prevents mammary gland differentiation and induces breast cancer formation in transgenic mice; truncated large T-antigen molecules harboring the intact p53 and pRb binding region do not have this effect. Oncogene 20: 2325-2332.
22. Hannus M, Feiguin F, Heisenberg CP, Eaton S. (2002). Planar cell polarization requires Widerborst, a B′ regulatory subunit of protein phosphatase 2A. Development 129: 3493-3503.
23. Hong S, Wang LC, Gao X, Kuo YL, Liu B, Merling R et al. (2007). Heptad repeats regulate protein phosphatase 2a recruitment to I-kappaB kinase gamma/NF-kappaB essential modulator and are targeted by human T-lymphotropic virus type 1 tax. J Biol Chem 282: 12119-12126.
24. Horn V, Thelu J, Garcia A, Albiges-Rizo C, Block MR, Viallet J. (2007). Functional interaction of Aurora-A and PP2A during mitosis. Mol Biol Cell 18: 1233-1241.
25. Janssens V, Goris J. (2001). Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417-439.
26. Kleylein-Sohn J, Westendorf J, Le Clech M, Habedanck R, Stierhof YD, Nigg EA. (2007). Plk4-induced centriole biogenesis in human cells. Dev Cell 13: 190-202.
27. Lavia P, Mileo AM, Giordano A, Paggi MG. (2003). Emerging roles of DNA tumor viruses in cell proliferation: new insights into genomic instability. Oncogene 22: 6508-6516.
28. Liao Y, Hung MC. (2004). A new role of protein phosphatase 2a in adenoviral E1A protein-mediated sensitization to anticancer drug-induced apoptosis in human breast cancer cells. Cancer Res 64: 5938-5942.
29. Lingle WL, Barrett SL, Negron VC, D'Assoro AB, Boeneman K, Liu W et al. (2002). Centrosome amplification drives chromosomal instability in breast tumor development. Proc Natl Acad Sci USA 99: 1978-1983.
30. Mateer SC, Fedorov SA, Mumby MC. (1998). Identification of structural elements involved in the interaction of simian virus 40 small tumor antigen with protein phosphatase 2A. J Biol Chem 273: 35339-35346.
31. Mayer-Jaekel RE, Ohkura H, Gomes R, Sunkel CE, Baumgartner S, Hemmings BA et al. (1993). The 55 kd regulatory subunit of Drosophila protein phosphatase 2A is required for anaphase. Cell 72: 621-633.
32. Mumby M. (2007). PP2A: unveiling a reluctant tumor suppressor. Cell 130: 21-24.
33. Mungre S, Enderle K, Turk B, Porras A, Wu YQ, Mumby MC et al. (1994).Mutations which affect the inhibition of protein phosphatase 2A by simian virus 40 small-t antigen in vitro decrease viral transformation. J Virol 68: 1675-1681.
34. Nigg EA. (2002). Centrosome aberrations: cause or consequence of cancer progression? Nat Rev Cancer 2: 815-825.
35. Nigg EA. (2007). Centrosome duplication: of rules and licenses. Trends Cell Biol 17: 215-221.
36. Nitta T, Kanai M, Sugihara E, Tanaka M, Sun B, Nagasawa T et al. (2006). Centrosome amplification in adult T-cell leukemia and human T-cell leukemia virus type 1 Tax-induced human T cells. Cancer Sci 97: 836-841.
37. Nunbhakdi-Craig V, Craig L, Machleidt T, Sontag E. (2003). Simian virus 40 small tumor antigen induces deregulation of the actin cytoskeleton and tight junctions in kidney epithelial cells. J Virol 77: 2807-2818.
38. Pagliarini RA, Xu T. (2003). A genetic screen in Drosophila for metastatic behavior. Science 302: 1227-1231.
39. Pihan GA, Purohit A, Wallace J, Malhotra R, Liotta L, Doxsey SJ. (2001). Centrosome defects can account for cellular and genetic changes that characterize prostate cancer progression. Cancer Res 61: 2212-2219.
40. Pim D, Massimi P, Dilworth SM, Banks L. (2005). Activation of the protein kinase B pathway by the HPV-16 E7 oncoprotein occurs through a mechanism involving interaction with PP2A. Oncogene 24: 7830-7838.
41. Porras A, Bennett J, Howe A, Tokos K, Bouck N, Henglein B et al. (1996). A novel simian virus 40 early-region domain mediates transactivation of the cyclin A promoter by small-t antigen and is required for transformation in small-t antigen-dependent assays. J Virol 70: 6902-6908.
42. Raff JW, Glover DM. (1989). Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos. Cell 57: 611-619.
43. 1/S transition. Cancer Surv 29: 7-23.
44. Rothwell WF, Sullivan W. (2000). The centrosome in early Drosophila embryogenesis. Curr Top Dev Biol 49: 409-447.
45. Saenz-Robles MT, Sullivan CS, Pipas JM. (2001). Transforming functions of simian virus 40. Oncogene 20: 7899-7907.
46. Schuchner S, Wintersberger E. (1999). Binding of polyomavirus small T antigen to protein phosphatase 2A is required for elimination of p27 and support of S-phase induction in concert with large T antigen. J Virol 73: 9266-9273.
47. Schuh M, Lehner CF, Heidmann S. (2007). Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17: 237-243.
48. Skoczylas C, Fahrbach KM, Rundell K. (2004). Cellular targets of the SV40 small-t antigen in human cell transformation. Cell Cycle 3: 606-610.
49. Skoczylas C, Henglein B, Rundell K. (2005). PP2A-dependent transactivation of the cyclin A promoter by SV40 ST is mediated by a cell cycle-regulated E2F site. Virology 332: 596-601.
50. Sluder G, Nordberg JJ. (2004). The good, the bad and the ugly: the practical consequences of centrosome amplification. Curr Opin Cell Biol 16: 49-54.
51. Snaith HA, Armstrong CG, Guo Y, Kaiser K, Cohen PT. (1996). Deficiency of protein phosphatase 2A uncouples the nuclear and centrosome cycles and prevents attachment of microtubules to the kinetochore in Drosophila microtubule star (mts)embryos. J Cell Sci 109(Part 13): 3001-3012.
52. Sontag E. (2001). Protein phosphatase 2A: the Trojan horse of cellular signaling. Cell Signal 13: 7-16.
53. Sontag E, Fedorov S, Kamibayashi C, Robbins D, Cobb M, Mumby M. (1993). The interaction of SV40 small tumor antigen with protein phosphatase 2A stimulates the map kinase pathway and induces cell proliferation. Cell 75: 887-897.
54. Sontag E, Nunbhakdi-Craig V, Bloom GS, Mumby MC. (1995). A novel pool of protein phosphatase 2A is associated with microtubules and is regulated during the cell cycle. J Cell Biol 128: 1131-1144.
55. Sontag JM, Sontag E. (2006). Regulation of cell adhesion by PP2A and SV40 small tumor antigen: an important link to cell transformation. Cell Mol Life Sci 63: 2979-2991.
56. Sullivan CS, Cantalupo P, Pipas JM. (2000). The molecular chaperone activity of simian virus 40 large T antigen is required to disrupt Rb-E2F family complexes by an ATP-dependent mechanism. Mol Cell Biol 20: 6233-6243.
57. Sullivan CS, Pipas JM. (2002). T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol Mol Biol Rev 66: 179-202.
58. Tournebize R, Andersen SS, Verde F, Doree M, Karsenti E, Hyman AA. (1997). Distinct roles of PP1 and PP2A-like phosphatases in control of microtubule dynamics during mitosis. EMBO J 16: 5537-5549.
59. Tsou MF, Stearns T. (2006). Controlling centrosome number: licenses and blocks. Curr Opin Cell Biol 18: 74-78.
60. Viquez NM, Li CR, Wairkar YP, DiAntonio A. (2006). The B′ protein phosphatase 2A regulatory subunit well-rounded regulates synaptic growth and cytoskeletal stability at the Drosophila neuromuscular junction. J Neurosci 26: 9293-9303.
61. Watanabe G, Howe A, Lee RJ, Albanese C, Shu IW, Karnezis AN et al. (1996). Induction of cyclin D1 by simian virus 40 small tumor antigen. Proc Natl Acad Sci USA 93: 12861-12866.
62. Wiese C, Zheng Y. (2006). Microtubule nucleation: gamma-tubulin and beyond. J Cell Sci 119: 4143-4153.
63. Xu Y, Xing Y, Chen Y, Chao Y, Lin Z, Fan E et al. (2006). Structure of the protein phosphatase 2A holoenzyme. Cell 127: 1239-1251.
64. Yang CS, Vitto MJ, Busby SA, Garcia BA, Kesler CT, Gioeli D et al. (2005). Simian virus 40 small t antigen mediates conformation-dependent transfer of protein phosphatase 2A onto the androgen receptor. Mol Cell Biol 25: 1298-1308.
65. Yang SI, Lickteig RL, Estes R, Rundell K, Walter G, Mumby MC. (1991). Control of protein phosphatase 2A by simian virus 40 small-t antigen. Mol Cell Biol 11: 1988-1995.
66. Zhang J, Megraw TL. (2007). Proper recruitment of gamma-tubulin and D-TACC/Msps to embryonic Drosophila centrosomes requires centrosomin motif 1. Mol Biol Cell 18: 4037-4049.