A cell-intrinsic inhibitor of HIV-1 reverse transcription in CD4 + T cells from elite controllers

Cell Host and Microbe

Volumn 15, Issue 6, 2014, Pages 717-728

  Leng, Jin ^a,b   Ho, Hsin Pin ^c   Buzon, Maria J ^a,b   Pereyra, Florencia ^b,d   Walker, Bruce D ^b,e   Yu, Xu G ^b   Chang, Emmanuel J ^c   Lichterfeld, Mathias ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR; HOST FACTOR; PROTEIN P21; RNA DIRECTED DNA POLYMERASE; RNA DIRECTED DNA POLYMERASE INHIBITOR; THREONINE; CDK2 PROTEIN, HUMAN; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; REVERSE TRANSCRIPTASE, HUMAN IMMUNODEFICIENCY VIRUS 1;

ARTICLE; CD4+ T LYMPHOCYTE; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION; UPREGULATION; VIRUS REPLICATION; AMINO ACID SEQUENCE; CASE CONTROL STUDY; ENZYME STABILITY; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY; VIROLOGY;

AMINO ACID SEQUENCE; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ENZYME STABILITY; HIV REVERSE TRANSCRIPTASE; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; REVERSE TRANSCRIPTION; UP-REGULATION; VIRUS REPLICATION;

EID: 84902463597     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.05.011     Document Type: Article

References (42)

1. M. Abdel-Mohsen, R.A. Raposo, X. Deng, M. Li, T. Liegler, E. Sinclair, M.S. Salama, Hel.-D. Ghanem, R. Hoh, and J.K. Wong et al. Expression profile of host restriction factors in HIV-1 elite controllers Retrovirology 10 2013 106
2. A. Allouch, A. David, S.M. Amie, H. Lahouassa, L. Chartier, F. Margottin-Goguet, F. Barré-Sinoussi, B. Kim, A. Sáez- Cirión, and G. Pancino p21-mediated RNR2 repression restricts HIV-1 replication in macrophages by inhibiting dNTP biosynthesis pathway Proc. Natl. Acad. Sci. USA 110 2013 E3997 E4006
3. T. Ammosova, R. Berro, M. Jerebtsova, A. Jackson, S. Charles, Z. Klase, W. Southerland, V.R. Gordeuk, F. Kashanchi, and S. Nekhai Phosphorylation of HIV-1 Tat by CDK2 in HIV-1 transcription Retrovirology 3 2006 78
4. A. Bergamaschi, A. David, E. Le Rouzic, S. Nisole, F. Barré-Sinoussi, and G. Pancino The CDK inhibitor p21Cip1/WAF1 is induced by FcgammaR activation and restricts the replication of human immunodeficiency virus type 1 and related primate lentiviruses in human macrophages J. Virol. 83 2009 12253 12265
5. A.L. Brass, D.M. Dykxhoorn, Y. Benita, N. Yan, A. Engelman, R.J. Xavier, J. Lieberman, and S.J. Elledge Identification of host proteins required for HIV infection through a functional genomic screen Science 319 2008 921 926
6. D. Breuer, A. Kotelkin, T. Ammosova, N. Kumari, A. Ivanov, A.V. Ilatovskiy, M. Beullens, P.R. Roane, M. Bollen, and M.G. Petukhov et al. CDK2 regulates HIV-1 transcription by phosphorylation of CDK9 on serine 90 Retrovirology 9 2012 94
7. P.P. Chamberlain, J. Ren, C.E. Nichols, L. Douglas, J. Lennerstrand, B.A. Larder, D.I. Stuart, and D.K. Stammers Crystal structures of Zidovudine- or Lamivudine-resistant human immunodeficiency virus type 1 reverse transcriptases containing mutations at codons 41, 184, and 215 J. Virol. 76 2002 10015 10019
8. H. Chen, C. Li, J. Huang, T. Cung, K. Seiss, J. Beamon, M.F. Carrington, L.C. Porter, P.S. Burke, and Y. Yang et al. CD4+ T cells from elite controllers resist HIV-1 infection by selective upregulation of p21 J. Clin. Invest. 121 2011 1549 1560
9. A. Ciuffi, G. Bleiber, M. Muñoz, R. Martinez, C. Loeuillet, M. Rehr, M. Fischer, H.F. Günthard, A. Oxenius, and P. Meylan et al. Entry and transcription as key determinants of differences in CD4 T-cell permissiveness to human immunodeficiency virus type 1 infection J. Virol. 78 2004 10747 10754
10. A. Cribier, B. Descours, A.L. Valadão, N. Laguette, and M. Benkirane Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1 Cell Rep 3 2013 1036 1043
11. L. Deng, T. Ammosova, A. Pumfery, F. Kashanchi, and S. Nekhai HIV-1 Tat interaction with RNA polymerase II C-terminal domain (CTD) and a dynamic association with CDK2 induce CTD phosphorylation and transcription from HIV-1 promoter J. Biol. Chem. 277 2002 33922 33929
12. L.O. Durand, and B. Roizman Role of cdk9 in the optimization of expression of the genes regulated by ICP22 of herpes simplex virus 1 J. Virol. 82 2008 10591 10599
13. S. Elahi, T. Niki, M. Hirashima, and H. Horton Galectin-9 binding to Tim-3 renders activated human CD4+ T cells less susceptible to HIV-1 infection Blood 119 2012 4192 4204
14. B. Emu, E. Sinclair, H. Hatano, A. Ferre, B. Shacklett, J.N. Martin, J.M. McCune, and S.G. Deeks HLA class I-restricted T-cell responses may contribute to the control of human immunodeficiency virus infection, but such responses are not always necessary for long-term virus control J. Virol. 82 2008 5398 5407
15. O. Flores, G. Lee, J. Kessler, M. Miller, W. Schlief, J. Tomassini, and D. Hazuda Host-cell positive transcription elongation factor b kinase activity is essential and limiting for HIV type 1 replication Proc. Natl. Acad. Sci. USA 96 1999 7208 7213
16. A.C. Francis, C. Di Primio, A. Allouch, and A. Cereseto Role of phosphorylation in the nuclear biology of HIV-1 Curr. Med. Chem. 18 2011 2904 2912
17. R.S. Harris, J.F. Hultquist, and D.T. Evans The restriction factors of human immunodeficiency virus J. Biol. Chem. 287 2012 40875 40883
18. J. Jäger, S.J. Smerdon, J. Wang, D.C. Boisvert, and T.A. Steitz Comparison of three different crystal forms shows HIV-1 reverse transcriptase displays an internal swivel motion Structure 2 1994 869 876
19. L.A. Kohlstaedt, J. Wang, J.M. Friedman, P.A. Rice, and T.A. Steitz Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor Science 256 1992 1783 1790
20. R. König, Y. Zhou, D. Elleder, T.L. Diamond, G.M. Bonamy, J.T. Irelan, C.Y. Chiang, B.P. Tu, P.D. De Jesus, and C.E. Lilley et al. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication Cell 135 2008 49 60
21. C.V. Kuny, K. Chinchilla, M.R. Culbertson, and R.F. Kalejta Cyclin-dependent kinase-like function is shared by the beta- and gamma- subset of the conserved herpesvirus protein kinases PLoS Pathog. 6 2010 e1001092
22. M.H. Malim, and P.D. Bieniasz HIV Restriction Factors and Mechanisms of Evasion Cold Spring Harb Perspect Med 2 2012 a006940
23. H.S. Mancebo, G. Lee, J. Flygare, J. Tomassini, P. Luu, Y. Zhu, J. Peng, C. Blau, D. Hazuda, D. Price, and O. Flores P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro Genes Dev. 11 1997 2633 2644
24. L. Manganaro, M. Lusic, M.I. Gutierrez, A. Cereseto, G. Del Sal, and M. Giacca Concerted action of cellular JNK and Pin1 restricts HIV-1 genome integration to activated CD4+ T lymphocytes Nat. Med. 16 2010 329 333
25. J.L. Mbisa, K.A. Delviks-Frankenberry, J.A. Thomas, R.J. Gorelick, and V.K. Pathak Real-time PCR analysis of HIV-1 replication post-entry events Methods Mol. Biol. 485 2009 55 72
26. E.A. Nigg Cellular substrates of p34(cdc2) and its companion cyclin-dependent kinases Trends Cell Biol. 3 1993 296 301
27. H. Nishi, K. Hashimoto, and A.R. Panchenko Phosphorylation in protein-protein binding: effect on stability and function Structure 19 2011 1807 1815
28. F. Pereyra, X. Jia, P.J. McLaren, A. Telenti, P.I. de Bakker, B.D. Walker, S. Ripke, C.J. Brumme, S.L. Pulit, M. Carrington International HIV Controllers Study The major genetic determinants of HIV-1 control affect HLA class I peptide presentation Science 330 2010 1551 1557
29. M. Rotger, C. Bayard, P. Taffé, R. Martinez, M. Cavassini, E. Bernasconi, M. Battegay, B. Hirschel, H. Furrer, A. Witteck Swiss HIV Cohort Study Contribution of genome-wide significant single-nucleotide polymorphisms and antiretroviral therapy to dyslipidemia in HIV-infected individuals: a longitudinal study Circ Cardiovasc Genet 2 2009 621 628
30. A. Sáez-Cirión, and G. Pancino HIV controllers: a genetically determined or inducible phenotype? Immunol. Rev. 254 2013 281 294
31. A. Sáez-Cirión, C. Hamimi, A. Bergamaschi, A. David, P. Versmisse, A. Mélard, F. Boufassa, F. Barré-Sinoussi, O. Lambotte, C. Rouzioux, G. Pancino ANRS CO18 Cohort Restriction of HIV-1 replication in macrophages and CD4+ T cells from HIV controllers Blood 118 2011 955 964
32. A. Sáez-Cirión, C. Bacchus, L. Hocqueloux, V. Avettand-Fenoel, I. Girault, C. Lecuroux, V. Potard, P. Versmisse, A. Melard, T. Prazuck ANRS VISCONTI Study Group Post-treatment HIV-1 controllers with a long-term virological remission after the interruption of early initiated antiretroviral therapy ANRS VISCONTI Study PLoS Pathog. 9 2013 e1003211
33. O. Schwartz, V. Maréchal, B. Friguet, F. Arenzana-Seisdedos, and J.M. Heard Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1 J. Virol. 72 1998 3845 3850
34. L. Serrano, J. Avila, and R.B. Maccioni Controlled proteolysis of tubulin by subtilisin: localization of the site for MAP2 interaction Biochemistry 23 1984 4675 4681
35. X. Tu, K. Das, Q. Han, J.D. Bauman, A.D. Clark Jr., X. Hou, Y.V. Frenkel, B.L. Gaffney, R.A. Jones, and P.L. Boyer et al. Structural basis of HIV-1 resistance to AZT by excision Nat. Struct. Mol. Biol. 17 2010 1202 1209
36. F. Vigneault, M. Woods, M.J. Buzon, C. Li, F. Pereyra, S.D. Crosby, J. Rychert, G. Church, J. Martinez-Picado, and E.S. Rosenberg et al. Transcriptional profiling of CD4 T cells identifies distinct subgroups of HIV-1 elite controllers J. Virol. 85 2011 3015 3019
37. B.D. Walker, and X.G. Yu Unravelling the mechanisms of durable control of HIV-1 Nat. Rev. Immunol. 13 2013 487 498
38. D. Wang, C. de la Fuente, L. Deng, L. Wang, I. Zilberman, C. Eadie, M. Healey, D. Stein, T. Denny, and L.E. Harrison et al. Inhibition of human immunodeficiency virus type 1 transcription by chemical cyclin-dependent kinase inhibitors J. Virol. 75 2001 7266 7279
39. T.E. White, A. Brandariz-Nuñez, J.C. Valle-Casuso, S. Amie, L.A. Nguyen, B. Kim, M. Tuzova, and F. Diaz-Griffero The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation Cell Host Microbe 13 2013 441 451
40. J. Zhang, D.T. Scadden, and C.S. Crumpacker Primitive hematopoietic cells resist HIV-1 infection via p21 J. Clin. Invest. 117 2007 473 481
41. H. Zhou, M. Xu, Q. Huang, A.T. Gates, X.D. Zhang, J.C. Castle, E. Stec, M. Ferrer, B. Strulovici, D.J. Hazuda, and A.S. Espeseth Genome-scale RNAi screen for host factors required for HIV replication Cell Host Microbe 4 2008 495 504
42. M. Zydek, C. Hagemeier, and L. Wiebusch Cyclin-dependent kinase activity controls the onset of the HCMV lytic cycle PLoS Pathog. 6 2010 e1001096