HIV-1 Vpr protein inhibits telomerase activity via the EDD-DDB1-VPRBP E3 ligase complex

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15474-15480

  Wang, Xin ^a   Singh, Shailbala ^b   Jung, Hae Yun ^a   Yang, Guojun ^b   Jun, Sohee ^a   Sastry, K Jagannadha ^b   Park, Jae Il ^a,b,c  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER CELLS; CATALYTIC SUBUNITS; CELL SENESCENCES; MOLECULAR MECHANISM; TELOMERASE ACTIVITY; TELOMERIC SEQUENCES; UBIQUITINATION; VIRAL PROTEINS;

MACHINERY;

PROTEINS;

ADAPTOR PROTEIN; BINDING PROTEIN; MUTANT PROTEIN; PROTEIN DDB1; PROTEIN EDD; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIRUS PROTEIN; VPR BINDING PROTEIN; VPR PROTEIN;

ARTICLE; CANCER CELL; CATALYSIS; CHROMOSOME; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME STABILITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; STEM CELL; UBIQUITINATION;

DYRK2; EDD; HIV-1; PROTEIN DEGRADATION; TELOMERASE; TELOMERES; TERT; UBIQUITINATION; VPR; VPRBP;

CARRIER PROTEINS; DNA-BINDING PROTEINS; HELA CELLS; HIV INFECTIONS; HIV-1; HUMANS; JURKAT CELLS; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; PROTEOLYSIS; TELOMERASE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84878386878     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.416735     Document Type: Article

References (41)

1. Margottin, F., Bour, S. P., Durand, H., Selig, L., Benichou, S., Richard, V., Thomas, D., Strebel, K., and Benarous, R. (1998) A novel human WD protein, h-βTrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1, 565-574 (Pubitemid 128374692)
2. Yu, X., Yu, Y., Liu, B., Luo, K., Kong, W., Mao, P., and Yu, X. F. (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302, 1056-1060 (Pubitemid 37386201)
3. Marin, M., Rose, K. M., Kozak, S. L., and Kabat, D. (2003) HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9, 1398-1403 (Pubitemid 37466189)
4. Sheehy, A. M., Gaddis, N. C., and Malim, M. H. (2003) The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 9, 1404-1407 (Pubitemid 37466190)
5. Mariani, R., Chen, D., Schröfelbauer, B., Navarro, F., König, R., Bollman, B., Münk, C., Nymark-McMahon, H., and Landau, N. R. (2003) Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114, 21-31 (Pubitemid 36859838)
6. Jäger, S., Kim, D. Y., Hultquist, J. F., Shindo, K., LaRue, R. S., Kwon, E., Li, M., Anderson, B. D., Yen, L., Stanley, D., Mahon, C., Kane, J., Franks-Skiba, K., Cimermancic, P., Burlingame, A., Sali, A., Craik, C. S., Harris, R. S., Gross, J. D., and Krogan, N. J. (2012) Vif hijacks CBF-β to degrade APOBEC3G and promote HIV-1 infection. Nature 481, 371-375
7. Hrecka, K., Hao, C., Gierszewska, M., Swanson, S. K., Kesik-Brodacka, M., Srivastava, S., Florens, L., Washburn, M. P., and Skowronski, J. (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474, 658-661
8. Laguette, N., Sobhian, B., Casartelli, N., Ringeard, M., Chable-Bessia, C., Ségéral, E., Yatim, A., Emiliani, S., Schwartz, O., and Benkirane, M. (2011) SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474, 654-657
9. Kogan, M., and Rappaport, J. (2011) HIV-1 accessory protein Vpr: relevance in the pathogenesis of HIV and potential for therapeutic intervention. Retrovirology 8, 25
10. Zhao, L. J., Mukherjee, S., and Narayan, O. (1994) Biochemical mechanism of HIV-I Vpr function. Specific interaction with a cellular protein. J. Biol. Chem. 269, 15577-15582
11. Cech, T. R. (2004) Beginning to understand the end of the chromosome. Cell 116, 273-279
12. Shippen-Lentz, D., and Blackburn, E. H. (1990) Functional evidence for an RNA template in telomerase. Science 247, 546-552
13. Autexier, C., and Lue, N. F. (2006) The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75, 493-517 (Pubitemid 44118041)
14. Meyerson, M., Counter, C. M., Eaton, E. N., Ellisen, L. W., Steiner, P., Caddle, S. D., Ziaugra, L., Beijersbergen, R. L., Davidoff, M. J., Liu, Q., Bacchetti, S., Haber, D. A., and Weinberg, R. A. (1997) hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90, 785-795 (Pubitemid 27357969)
15. Bodnar, A. G., Ouellette, M., Frolkis, M., Holt, S. E., Chiu, C. P., Morin, G. B., Harley, C. B., Shay, J. W., Lichtsteiner, S., and Wright, W. E. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279, 349-352 (Pubitemid 28063364)
16. Harley, C. B., Futcher, A. B., and Greider, C. W. (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460
17. Ballon, G., Ometto, L., Righetti, E., Cattelan, A. M., Masiero, S., Zanchetta, M., Chieco-Bianchi, L., and De Rossi, A. (2001) Human immunodeficiency virus type 1 modulates telomerase activity in peripheral blood lymphocytes. J. Infect. Dis. 183, 417-424 (Pubitemid 32105601)
18. Bostik, P., Dodd, G. L., Patel, S. S., Kadivar, H., and Ansari, A. A. (2002) Effect of productive in vitro human immunodeficiency virus or simian immunodeficiency virus infection on telomerase activity in lymphoid and nonlymphoid cells. J. Infect. Dis. 185, 999-1001; author reply 1001-1002
19. + T lymphocytes infected with human immunodeficiency virus type 1 (HIV-1). J. Med. Virol. 79, 639-646
20. Reynoso, R., Minces, L., Salomon, H., and Quarleri, J. (2006) HIV-1 infection downregulates nuclear telomerase activity on lymphoblastoic cells without affecting the enzymatic components at the transcriptional level. AIDS Res. Hum. Retroviruses 22, 425-429 (Pubitemid 43787767)
21. + T lymphocytes. J. Immunol. 181, 7400-7406
22. Maddika, S., and Chen, J. (2009) Protein kinase DYRK2 is a scaffold that facilitates assembly of an E3 ligase. Nat. Cell Biol. 11, 409-419
23. Huang, J., and Chen, J. (2008) VprBP targets Merlin to the Roc1-Cul4ADDB1 E3 ligase complex for degradation. Oncogene 27, 4056-4064 (Pubitemid 351931990)
24. Jung, H.-Y., Wang, X., Jun, S., and Park, J.-I. (2013) Dyrk2-associated EDD-DDB1-VprBP E3 ligase inhibits telomerase by TERT degradation. J. Biol. Chem. 288, 7252-7262
25. Roshal, M., Kim, B., Zhu, Y., Nghiem, P., and Planelles, V. (2003) Activation of the ATR-mediated DNA damage response by the HIV-1 viral protein R. J. Biol. Chem. 278, 25879-25886 (Pubitemid 36835349)
26. VPRBP E3 ubiquitin ligase. PLoS Pathog. 3, e85
27. Tan, L., Ehrlich, E., and Yu, X. F. (2007) DDB1 and Cul4A are required for human immunodeficiency virus type 1 Vpr-induced G2 arrest. J. Virol. 81, 10822-10830 (Pubitemid 47463356)
28. DCAF1 ubiquitin ligase protects HIV-1 Vpr from proteasomal degradation. J. Biol. Chem. 283, 21686-21692
29. Zhang, L., Huang, Y., Yuan, H., Tuttleton, S., and Ho, D. D. (1997) Genetic characterization of vif, vpr, and vpu sequences from long-term survivors of human immunodeficiency virus type 1 infection. Virology 228, 340-349 (Pubitemid 27238801)
30. Wang, B., Ge, Y. C., Palasanthiran, P., Xiang, S. H., Ziegler, J., Dwyer, D. E., Randle, C., Dowton, D., Cunningham, A., and Saksena, N. K. (1996) Gene defects clustered at the C-terminus of the vpr gene of HIV-1 in long-term nonprogressing mother and child pair: in vivo evolution of vpr quasispecies in blood and plasma. Virology 223, 224-232 (Pubitemid 26302062)
31. Lum, J. J., Cohen, O. J., Nie, Z., Weaver, J. G., Gomez, T. S., Yao, X. J., Lynch, D., Pilon, A. A., Hawley, N., Kim, J. E., Chen, Z., Montpetit, M., Sanchez-Dardon, J., Cohen, E. A., and Badley, A. D. (2003) Vpr R77Q is associated with long-term nonprogressive HIV infection and impaired induction of apoptosis. J. Clin. Invest. 111, 1547-1554 (Pubitemid 38063287)
32. Morellet, N., Bouaziz, S., Petitjean, P., and Roques, B. P. (2003) NMR structure of the HIV-1 regulatory protein VPR. J. Mol. Biol. 327, 215-227 (Pubitemid 36293314)
33. Le Rouzic, E., Belaïdouni, N., Estrabaud, E., Morel, M., Rain, J. C., Transy, C., and Margottin-Goguet, F. (2007) HIV1 Vpr arrests the cell cycle by recruiting DCAF1/VprBP, a receptor of the Cul4-DDB1 ubiquitin ligase. Cell Cycle 6, 182-188 (Pubitemid 46232499)
34. Deeks, S. G. (2011) HIV infection, inflammation, immunosenescence, and aging. Annu. Rev. Med. 62, 141-155
35. Park, J.-I., Venteicher, A. S., Hong, J. Y., Choi, J., Jun, S., Shkreli, M., Chang, W., Meng, Z., Cheung, P., Ji, H., McLaughlin, M., Veenstra, T. D., Nusse, R., McCrea, P. D., and Artandi, S. E. (2009) Telomerase modulates Wnt signalling by association with target gene chromatin. Nature 460, 66-72
36. Artandi, S. E., Alson, S., Tietze, M. K., Sharpless, N. E., Ye, S., Greenberg, R. A., Castrillon, D. H., Horner, J. W., Weiler, S. R., Carrasco, R. D., and DePinho, R. A. (2002) Constitutive telomerase expression promotes mammary carcinomas in aging mice. Proc. Natl. Acad. Sci. U.S.A. 99, 8191-8196 (Pubitemid 34651028)
37. González-Suárez, E., Flores, J. M., and Blasco, M. A. (2002) Cooperation between p53 mutation and high telomerase transgenic expression in spontaneous cancer development. Mol. Cell. Biol. 22, 7291-7301
38. Stewart, S. A., Hahn, W. C., O'Connor, B. F., Banner, E. N., Lundberg, A. S., Modha, P., Mizuno, H., Brooks, M. W., Fleming, M., Zimonjic, D. B., Popescu, N. C., and Weinberg, R. A. (2002) Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc. Natl. Acad. Sci. U.S.A. 99, 12606-12611
39. Armstrong, L., Saretzki, G., Peters, H., Wappler, I., Evans, J., Hole, N., von Zglinicki, T., and Lako, M. (2005) Overexpression of telomerase confers growth advantage, stress resistance, and enhanced differentiation of ESCs toward the hematopoietic lineage. Stem Cells 23, 516-529 (Pubitemid 40478491)
40. Imamura, S., Uchiyama, J., Koshimizu, E., Hanai, J., Raftopoulou, C., Murphey, R. D., Bayliss, P. E., Imai, Y., Burns, C. E., Masutomi, K., Gagos, S., Zon, L. I., Roberts, T. M., and Kishi, S. (2008) A non-canonical function of zebrafish telomerase reverse transcriptase is required for developmental hematopoiesis. PLoS ONE 3, e3364
41. Yang, C., Przyborski, S., Cooke, M. J., Zhang, X., Stewart, R., Anyfantis, G., Atkinson, S. P., Saretzki, G., Armstrong, L., and Lako, M. (2008) A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells 26, 850-863