Inhibition of NF-κB activity by HIV-1 Vpr is dependent on Vpr binding protein

Journal of Cellular Physiology

Volumn 228, Issue 4, 2013, Pages 781-790

  Kogan, Michael ^a   Deshmane, Satish ^a   Sawaya, Bassel E ^a   Gracely, Edward J ^b   Khalili, Kamel ^a   Rappaport, Jay ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; HEAT SHOCK PROTEIN 27; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; VIRUS PROTEIN;

ADENOVIRUS; ARTICLE; BONE MARROW CELL; CELL TYPE; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE FUNCTION TEST; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS INFECTION; VIRUS REPLICATION;

CARRIER PROTEINS; CELLS, CULTURED; HIV INFECTIONS; HIV-1; HSP27 HEAT-SHOCK PROTEINS; HUMANS; I-KAPPA B PROTEINS; LEUKOCYTES, MONONUCLEAR; MYELOID CELLS; NF-KAPPA B; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; VIRUS REPLICATION; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

ADENOVIRIDAE; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84871699358     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24226     Document Type: Article

References (52)

1. Asin S, Taylor JA, Trushin S, Bren G, Paya CV. 1999. Ikappakappa mediates NF-kappaB activation in human immunodeficiency virus-infected cells. J Virol 73:3893-3903.
2. Ayyavoo V, Mahboubi A, Mahalingam S, Ramalingam R, Kudchodkar S, Williams WV, Green DR, Weiner DB. 1997. HIV-1 Vpr suppresses immune activation and apoptosis through regulation of nuclear factor kappa B. Nat Med 3:1117-1123.
3. Ayyavoo V, Muthumani K, Kudchodkar S, Zhang D, Ramanathan P, Dayes NS, Kim JJ, Sin JI, Montaner LJ, Weiner DB. 2002. HIV-1 viral protein R compromises cellular immune function in vivo. Int Immunol 14:13-22.
4. Balotta C, Lusso P, Crowley R, Gallo RC, Franchini G. 1993. Antisense phosphorothioate oligodeoxynucleotides targeted to the vpr gene inhibit human immunodeficiency virus type 1 replication in primary human macrophages. J Virol 67:4409-4414.
5. Belzile JP, Richard J, Rougeau N, Xiao Y, Cohen EA. 2010. HIV-1 Vpr induces the K48-linked polyubiquitination and proteasomal degradation of target cellular proteins to activate ATR and promote G2 arrest. J Virol 84:3320-3330.
6. Bour S, Perrin C, Akari H, Strebel K. 2001. The human immunodeficiency virus type 1 Vpu protein inhibits NF-kappa B activation by interfering with beta TrCP-mediated degradation of Ikappa B. J Biol Chem 276:15920-15928.
7. Brown JN, Kohler JJ, Coberley CR, Sleasman JW, Goodenow MM. 2008. HIV-1 activates macrophages independent of Toll-like receptors. PLoS ONE 3:e3664.
8. Bukrinsky M, Zhao Y. 2004. Heat-shock proteins reverse the G2 arrest caused by HIV-1 viral protein R. DNA Cell Biol 23:223-225.
9. Carlson R, Vavricka S, Eloranta J, Musch M, Arvans D, Kles K, Walsh-Reitz M, Kullak-Ublick G, Chang E. 2007. fMLP induces Hsp27 expression, attenuates NF-kappaB activation, and confers intestinal epithelial cell protection. Am J Physiol Gastrointest Liver Physiol 292:G1070-G1078.
10. Chang HK, Gallo RC, Ensoli B. 1995. Regulation of cellular gene expression and function by the human immunodeficiency virus type 1 Tat protein. J Biomed Sci 2:189-202.
11. Choe W, Volsky DJ, Potash MJ. 2002. Activation of NF-kappaB by R5 and X4 human immunodeficiency virus type 1 induces macrophage inflammatory protein 1alpha and tumor necrosis factor alpha in macrophages. J Virol 76:5274-5277.
12. Cohen EA, Terwilliger EF, Jalinoos Y, Proulx J, Sodroski JG, Haseltine WA. 1990. Identification of HIV-1 vpr product and function. J Acquir Immune Defic Syndr 3:11-18.
13. Collins SJ. 1987. The HL-60 promyelocytic leukemia cell line: Proliferation, differentiation, and cellular oncogene expression. Blood 70:1233-1244.
14. Demarchi F, d'Adda di Fagagna F, Falaschi A, Giacca M. 1996. Activation of transcription factor NF-kappaB by the Tat protein of human immunodeficiency virus type 1. J Virol 70:4427-4437.
15. Deshmane SL, Mukerjee R, Fan S, Del Valle L, Michiels C, Sweet T, Rom I, Khalili K, Rappaport J, Amini S, Sawaya BE. 2009. Activation of the oxidative stress pathway by HIV-1 Vpr leads to induction of hypoxia-inducible factor 1alpha expression. J Biol Chem 284:11364-11373.
16. Dodd S, Hain B, Senf S, Judge A. 2009. Hsp27 inhibits IKKbeta-induced NF-kappaB activity and skeletal muscle atrophy. FASEB J 23:3415-3423.
17. Emerman M. 1996. HIV-1, Vpr and the cell cycle. Curr Biol 6:1096-1103.
18. Emiliani S, Fischle W, Ott M, Van Lint C, Amella CA, Verdin E. 1998. Mutations in the tat gene are responsible for human immunodeficiency virus type 1 postintegration latency in the U1 cell line. J Virol 72:1666-1670.
19. Gendelman HE, Orenstein JM, Martin MA, Ferrua C, Mitra R, Phipps T, Wahl LA, Lane HC, Fauci AS, Burke DS, Meltzer MS. 1988. Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes. J Exp Med 167:1428-1441.
20. Genois N, Robichaud GA, Tremblay MJ. 2000. Mono Mac 1: A new in vitro model system to study HIV-1 infection in human cells of the mononuclear phagocyte series. J Leukoc Biol 68:854-864.
21. Guo K, Kang N, Li Y, Sun L, Gan L, Cui F, Gao M, Liu K. 2009. Regulation of HSP27 on NF-kappaB pathway activation may be involved in metastatic hepatocellular carcinoma cells apoptosis. BMC Cancer 9:100.
22. Hoshino S, Konishi M, Mori M, Shimura M, Nishitani C, Kuroki Y, Koyanagi Y, Kano S, Itabe H, Ishizaka Y. 2010. HIV-1 Vpr induces TLR4/MyD88-mediated IL-6 production and reactivates viral production from latency. J Leukoc Biol 87:1133-1143.
23. Karin M, Cao Y, Greten FR, Li ZW. 2002. NF-kappaB in cancer: From innocent bystander to major culprit. Nat Rev Cancer 2:301-310.
24. Kogan M, Rappaport J. 2011. HIV-1 accessory protein Vpr: Relevance in the pathogenesis of HIV and potential for therapeutic intervention. Retrovirology 8:25.
25. Lenardo MJ, Baltimore D. 1989. NF-kappa B: A pleiotropic mediator of inducible and tissue-specific gene control. Cell 58:227-229.
26. Levy DN, Refaeli Y, MacGregor RR, Weiner DB. 1994. Serum Vpr regulates productive infection and latency of human immunodeficiency virus type 1. Proc Natl Acad Sci USA 91:10873-10877.
27. Levy DN, Refaeli Y, Weiner DB. 1995. Extracellular Vpr protein increases cellular permissiveness to human immunodeficiency virus replication and reactivates virus from latency. J Virol 69:1243-1252.
28. Liang D, Benko Z, Agbottah E, Bukrinsky M, Zhao RY. 2007. Anti-vpr activities of heat shock protein 27. Mol Med 13:229-239.
29. Mahajan DK, London SN. 1997. Mifepristone (RU486): A review. Fertil Steril 68:967-976.
30. Majumder B, Janket ML, Schafer EA, Schaubert K, Huang XL, Kan-Mitchell J, Rinaldo CR, Jr., Ayyavoo V. 2005. Human immunodeficiency virus type 1 Vpr impairs dendritic cell maturation and T-cell activation: Implications for viral immune escape. J Virol 79:7990-8003.
31. Mariani R, Rasala BA, Rutter G, Wiegers K, Brandt SM, Krausslich HG, Landau NR. 2001. Mouse-human heterokaryons support efficient human immunodeficiency virus type 1 assembly. J Virol 75:3141-3151.
32. Miller Sanders C, Cruse JM, Lewis RE. 2010. Toll-like receptor and chemokine receptor expression in HIV-infected T lymphocyte subsets. Exp Mol Pathol 88:26-31.
33. Mirani M, Elenkov I, Volpi S, Hiroi N, Chrousos GP, Kino T. 2002. HIV-1 protein Vpr suppresses IL-12 production from human monocytes by enhancing glucocorticoid action: Potential implications of Vpr coactivator activity for the innate and cellular immunity deficits observed in HIV-1 infection. J Immunol 169:6361-6368.
34. Muthumani K, Kudchodkar S, Papasavvas E, Montaner LJ, Weiner DB, Ayyavoo V. 2000. HIV-1 Vpr regulates expression of beta chemokines in human primary lymphocytes and macrophages. J Leukoc Biol 68:366-372.
35. Muthumani K, Bagarazzi M, Conway D, Hwang DS, Ayyavoo V, Zhang D, Manson K, Kim J, Boyer J, Weiner DB. 2002. Inclusion of Vpr accessory gene in a plasmid vaccine cocktail markedly reduces Nef vaccine effectiveness in vivo resulting in CD4 cell loss and increased viral loads in rhesus macaques. J Med Primatol 31:179-185.
36. Muthumani K, Desai BM, Hwang DS, Choo AY, Laddy DJ, Thieu KP, Rao RG, Weiner DB. 2004. HIV-1 Vpr and anti-inflammatory activity. DNA Cell Biol 23:239-247.
37. Muthumani K, Choo AY, Zong WX, Madesh M, Hwang DS, Premkumar A, Thieu KP, Emmanuel J, Kumar S, Thompson CB, Weiner DB. 2006. The HIV-1 Vpr and glucocorticoid receptor complex is a gain-of-function interaction that prevents the nuclear localization of PARP-1. Nat Cell Biol 8:170-179.
38. Parcellier A, Schmitt E, Gurbuxani S, Seigneurin-Berny D, Pance A, Chantôme A, Plenchette S, Khochbin S, Solary E, Garrido C. 2003. HSP27 is a ubiquitin-binding protein involved in I-kappaBalpha proteasomal degradation. Mol Cell Biol 23:5790-5802.
39. Planelles V, Jowett JB, Li QX, Xie Y, Hahn B, Chen IS. 1996. Vpr-induced cell cycle arrest is conserved among primate lentiviruses. J Virol 70:2516-2524.
40. Poli G, Kinter A, Justement JS, Kehrl JH, Bressler P, Stanley S, Fauci AS. 1990. Tumor necrosis factor alpha functions in an autocrine manner in the induction of human immunodeficiency virus expression. Proc Natl Acad Sci USA 87:782-785.
41. Richard J, Sindhu S, Pham TN, Belzile JP, Cohen EA. 2010. HIV-1 Vpr up-regulates expression of ligands for the activating NKG2D receptor and promotes NK cell-mediated killing. Blood 115:1354-1363.
42. Roulston A, Lin R, Beauparlant P, Wainberg MA, Hiscott J. 1995. Regulation of human immunodeficiency virus type 1 and cytokine gene expression in myeloid cells by NF-kappa B/Rel transcription factors. Microbiol Rev 59:481-505.
43. Roux P, Alfieri C, Hrimech M, Cohen E, Tanner J. 2000. Activation of transcription factors NF-kappaB and NF-IL-6 by human immunodeficiency virus type 1 protein R (Vpr) induces interleukin-8 expression. J Virol 74:4658-4665.
44. Schweitzer K, Bozko P, Dubiel W, Naumann M. 2007. CSN controls NF-kappaB by deubiquitinylation of IkappaBalpha. EMBO J 26:1532-1541.
45. Siddiqui K, Del Valle L, Morellet N, Cui J, Ghafouri M, Mukerjee R, Urbanska K, Fan S, Pattillo CB, Deshmane SL, Kiani MF, Ansari R, Khalili K, Roques BP, Reiss K, Bouaziz S, Amini S, Srinivasan A, Sawaya BE. 2008. Molecular mimicry in inducing DNA damage between HIV-1 Vpr and the anticancer agent, cisplatin. Oncogene 27:32-43.
46. Sundstrom C, Nilsson K. 1976. Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int J Cancer 17:565-577.
47. Tristem M, Marshall C, Karpas A, Hill F. 1992. Evolution of the primate lentiviruses: Evidence from vpx and vpr. EMBO J 11:3405-3412.
48. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, Tada K. 1980. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 26:171-176.
49. Varin A, Decrion A, Sabbah E, Quivy V, Sire J, Van Lint C, Roques B, Aggarwal B, Herbein G. 2005. Synthetic Vpr protein activates activator protein-1, c-Jun N-terminal kinase, and NF-kappaB and stimulates HIV-1 transcription in promonocytic cells and primary macrophages. J Biol Chem 280:42557-42567.
50. Ward J, Davis Z, DeHart J, Zimmerman E, Bosque A, Brunetta E, Mavilio D, Planelles V, Barker E. 2009. HIV-1 Vpr triggers natural killer cell-mediated lysis of infected cells through activation of the ATR-mediated DNA damage response. PLoS Pathog 5:e1000613.
51. Yuan X, Matsuda Z, Matsuda M, Essex M, Lee TH. 1990. Human immunodeficiency virus vpr gene encodes a virion-associated protein. AIDS Res Hum Retroviruses 6:1265-1271.
52. Zhao LJ, Mukherjee S, Narayan O. 1994. Biochemical mechanism of HIV-I Vpr function. Specific interaction with a cellular protein. J Biol Chem 269:15577-15582.