Phosphorylation regulates human T-cell leukemia virus type 1 Rex function

Retrovirology

Volumn 6, Issue , 2009, Pages

  Kesic, Matthew ^a   Doueiri, Rami ^a   Ward, Michael ^c   Semmes, O John ^c   Green, Patrick L ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REX 1 PROTEIN; REX PROTEIN; SERINE; THREONINE; UNCLASSIFIED DRUG; PHOSPHOSERINE; PHOSPHOTHREONINE; REX PROTEIN, HUMAN T LYMPHOTROPIC VIRUS 1; REX PROTEIN, HUMAN T-LYMPHOTROPIC VIRUS 1;

AMINO ACID ANALYSIS; ARTICLE; CONTROLLED STUDY; GENE FUNCTION; GENE MAPPING; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; LIQUID CHROMATOGRAPHY; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; REPORTER GENE; RESIDUE ANALYSIS; SITE DIRECTED MUTAGENESIS; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION;

DELTARETROVIRUS; HUMAN T-LYMPHOTROPIC VIRUS 1;

AMINO ACID SEQUENCE; CELL LINE; GENE EXPRESSION REGULATION, VIRAL; GENE PRODUCTS, REX; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PHOSPHOSERINE; PHOSPHOTHREONINE;

EID: 71049160847     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-6-105     Document Type: Article

References (61)

1. Lairmore M, Franchini G. Human T-Cell Leukemia Virus Types 1 and 2. Fields Virology. Volume 5th 2007, Chapter 56:2071-2106. Philadelphia, PA USA.: Lippincott Williams, and Wilkins, Fields B, Knipe D, Howley P, Chanock R, Monath T, Melnick J, Roizman B, Straus S.
2. Wolfe ND, Heneine W, Carr JK, Garcia AD, Shanmugam V, Tamoufe U, Torimiro JN, Prosser AT, Lebreton M, Mpoudi-Ngole E. Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. Proc Natl Acad Sci USA 2005, 102:7994-7999. 10.1073/pnas.0501734102, 1142377, 15911757.
3. Calattini S, Chevalier SA, Duprez R, Bassot S, Froment A, Mahieux R, Gessain A. Discovery of a new human T-cell lymphotropic virus (HTLV-3) in Central Africa. Retrovirology 2005, 2:30. 10.1186/1742-4690-2-30, 1142341, 15882466.
4. Switzer WM, Salemi M, Qari SH, Jia H, Gray RR, Katzourakis A, Marriott SJ, Pryor KN, Wolfe ND, Burke DS. Ancient, independent evolution and distinct molecular features of the novel human T-lymphotropic virus type 4. Retrovirology 2009, 6:9. 10.1186/1742-4690-6-9, 2647524, 19187529.
5. Ferreira OJ, Planelles V, Rosenblatt J. Human T-cell leukemia viruses: epidemiology, biology, and pathogenesis. Blood Rev 1997, 11:91-104. 10.1016/S0268-960X(97)90015-1, 9242992.
6. Osame M, Igata A, Matsumoto M, Usuku K, Izumo S, Kosaka K. HTLV-I associated myelopathy: A report of 85 cases. Ann Neurol 1987, 22:116.
7. Yoshida M. Discovery of HTLV-1, the first human retrovirus, its unique regulatory mechanisms, and insights into pathogenesis. Oncogene 2005, 24:5931-5937. 10.1038/sj.onc.1208981, 16155600.
8. Rosenblatt JD, Giorgi JV, Golde DW, Ezra JB, Wu A, Winberg CD, Glaspy J, Wachsman W, Chen IS. Integrated human T-cell leukemia virus II genome in CD8 + T cells from a patient with "atypica" hairy cell leukemia: evidence for distinct T and B cell lymphoproliferative disorders. Blood 1988, 71:363-369.
9. Berger JR, Svenningsson A, Raffanti S, Resnick L. Tropical spastic paraparesis-like illness occurring in a patient dually infected with HIV-1 and HTLV-II. Neurology 1991, 41:5-7.
10. Hjelle B, Appenzeller O, Mills R, Alexander S, Torrez-Martinez N, Jahnke R, Ross G. Chronic neurodegenerative disease associated with HTLV-II infection. Lancet 1992, 339:645-646. 10.1016/0140-6736(92)90797-7, 1347339.
11. Harrington WJ, Sheremata W, Hjelle B, Dube DK, Bradshaw P, Foung SK, Snodgrass S, Toedter G, Cabra L, Poiesz B. Spastic ataxia associated with human T-cell lymphotropic virus type II infection. Annals Neurol 1993, 7:1031-1034.
12. Poiesz B, Dube D, Dube S, Love J, Papsidero L, Uner A, Hutchinson R. HTLV-II-associated cutaneous T-cell lymphoma in a patient with HIV-1 infection. N Engl J Med 2000, 342:930-936. 10.1056/NEJM200003303421304, 10738051.
13. Cann AJ, Rosenblatt JD, Wachsman W, Shah NP, Chen ISY. Identification of the gene responsible for human T-cell leukemia virus transcriptional regulation. Nature 1985, 318:571-574. 10.1038/318571a0, 2999613.
14. Felber BK, Paskalis H, Kleinman-Ewing C, Wong-Staal F, Pavlakis GN. The pX protein of HTLV-I is a transcriptional activator of its long terminal repeats. Science 1985, 229:675-679. 10.1126/science.2992082, 2992082.
15. Inoue JI, Yoshida M, Seiki M. Transcriptional (p40x) and post-transcriptional (p27xIII) regulators are required for the expression and replication of human T-cell leukemia virus type I genes. Proc Natl Acad Sci USA 1987, 84:3653-3657. 10.1073/pnas.84.11.3653, 304933, 3035544.
16. Mulloy JC, Kislyakova T, Cereseto A, Casareto L, LoMonico A, Fullen J, Lorenzi MV, Cara A, Nicot C, Giam C, Franchini G. Human T-cell lymphotropic/leukemia virus type 1 Tax abrogates p53- induced cell cycle arrest and apoptosis through its CREB/ATF functional domain. J Virol 1998, 72:8852-8860. 110302, 9765430.
17. Ressler S, Morris GF, Marriott SJ. Human T-cell leukemia virus type 1 Tax transactivates the human proliferating cell nuclear antigen promoter. J Virol 1997, 71:1181-1190. 191171, 8995640.
18. Schmitt I, Rosin O, Rohwer P, Gossen M, Grassmann R. Stimulation of cyclin-dependent kinase activity and G1 to S phase transition in human lymphocytes by the human T-cell leukemia/lymphotropic virus type 1 tax protein. J Virol 1998, 72:633-640. 109417, 9420268.
19. Boxus M, Twizere JC, Legros S, Dewulf JF, Kettmann R, Willems L. The HTLV-1 Tax interactome. Retrovirology 2008, 5:76. 10.1186/1742-4690-5-76, 2533353, 18702816.
20. Ramadan E, Ward M, Guo X, Durkin SS, Sawyer A, Vilela M, Osgood C, Pothen A, Semmes OJ. Physical and in silico approaches identify DNA-PK in a Tax DNA-damage response interactome. Retrovirology 2008, 5:92. 10.1186/1742-4690-5-92, 2576351, 18922151.
21. Robek MD, Ratner L. Immortalization of CD4+ and CD8+ T-lymphocytes by human T-cell leukemia virus type 1 Tax mutants expressed in a functional molecular clone. J Virol 1999, 73:4856-4865. 112529, 10233947.
22. Ross TM, Narayan M, Fang ZY, Minella AC, Green PL. Tax transactivation of both NFκB and CREB/ATF is essential for Human T-cell leukemia virus type 2-mediated transformation of primary human T-cells. J Virol 2000, 74:2655-2662. 10.1128/JVI.74.6.2655-2662.2000, 111754, 10684280.
23. Wycuff DR, Marriott SJ. The HTLV-1 Tax Oncoprotein:Hypertasking at the molecular level. Front Biosci 2005, 10:620-642. 10.2741/1558, 15569604.
24. Ballaun C, Farrington GR, Dobrovnik M, Rusche J, Hauber J, Bohnlein E. Functional analysis of human T-cell leukemia virus type I Rex-response element: Direct RNA binding of Rex protein correlates with in vivo binding activity. J Virol 1991, 65:4408-4413. 248880, 2072457.
25. Kusuhara K, Anderson M, Pettiford SM, Green PL. Human T-cell leukemia virus type 2 Rex protein increases stability and promotes nuclear to cytoplasmic transport of gag/pol and env RNAs. J Virol 1999, 73:8112-8119. 112827, 10482560.
26. Narayan M, Kusuhara K, Green PL. Phosphorylation of two serine residues regulates human T-cell leukemia virus type 2 Rex function. J Virol 2001, 75:8440-8448. 10.1128/JVI.75.18.8440-8448.2001, 115089, 11507189.
27. Younis I, Green PL. The human T-cell leukemia virus Rex protein. Frontiers in Biosciences 2005, 10:431-445.
28. Xie L, Kesic M, Yamamoto B, Li M, Younis I, Lairmore MD, Green PL. HTLV-2 Rex carboxy terminus is an inhibitory/stability domain that regulates Rex functional activity and viral replication. J Virol 2009, 83:5232-5243. 10.1128/JVI.02271-08, 2682101, 19279097.
29. Bogerd H, Greene WC. Dominant negative mutants of human T-cell leukemia virus type I Rex and human immunodeficiency virus type 1 Rev fail to multimerize in vivo. J Virol 1993, 67:2496-2502. 237568, 8474155.
30. Bogerd HP, Huckaby GL, Ahmed YF, Hanly SM, Greene WC. The type 1 human T-cell leukemia virus (HTLV-I) Rex trans-activator binds directly to the HTLV-I Rex and the type 1 human immunodeficiency virus Rev RNA response elements. Proc Natl Acad Sci USA 1991, 88:5704-5708. 10.1073/pnas.88.13.5704, 51946, 1905815.
31. Hammes SR, Green WC. Multiple arginine residues within the basic domian of HTLV-1 Rex are required for specific RNA binding and function. Virology 1993, 193:41-49. 10.1006/viro.1993.1101, 8438577.
32. Hope TJ, Bond BL, McDonald B, Klein NP, Parslow TG. Effector domains of human immunodeficiency virus type 1 Rev and human T-cell leukemia virus type I Rex are functionally interchangeable and share an essential peptide motif. J Virol 1991, 65:6001-6007. 250265, 1920623.
33. Narayan M, Younis I, D'Agostino DM, Green PL. Functional domain structure of human T-cell leukemia virus type 2 Rex. J Virol 2003, 77:12829-12840. 10.1128/JVI.77.23.12829-12840.2003, 262564, 14610204.
34. Palmeri D, Malim MH. The human T-cell leukemia virus type 1 post-transcriptional trans-activator Rex contains a nuclear export signal. J Virol 1996, 70:6442-6445. 190676, 8709278.
35. Rimsky L, Duc Dodon M, Dixon EP, Greene WC. Trans-dominant inactivation of HTLV-I and HIV-1 gene expression by mutation of the HTLV-I Rex transactivator. Nature 1989, 341:453-456. 10.1038/341453a0, 2677743.
36. Siomi H, Shida H, Nam SH, Nosaka T, Maki M, Hatanaka M. Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing. Cell 1988, 55:197-209. 10.1016/0092-8674(88)90043-8, 3048703.
37. Weichselbraun I, Farrington GK, Rusche JR, Bohnlein E, Hauber J. Definition of human immunodeficiency virus type 1 Rev and human T-cell leukemia virus type 1 Rex protein activation domain by functional exchange. J Virol 1992, 66:2583-2587. 289062, 1548784.
38. Tootle TL, Rebay I. Post-translational modifications influence transcription factor activity: a view from the ETS superfamily. Bioessays 2005, 27:285-298. 10.1002/bies.20198, 15714552.
39. Adachi Y, Copeland TD, Takahashi C, Nosaka T, Ahmed A, Oroszlan S, Hatanaka M. Phosphorylation of the Rex protein of human T-cell leukemia virus type I. J Biol Chem 1992, 267:21977-21981.
40. Adachi Y, Nosaka T, Hatanaka M. Protein kinase inhibitor H-7 blocks accumulation of unspliced mRNA of human T-cell leukemia virus type I (HTLV-II). Biochem Biophys Res Comm 1990, 169:469-475. 10.1016/0006-291X(90)90355-Q, 2357216.
41. Green PL, Xie Y, Chen ISY. The Rex proteins of human T-cell leukemia virus type-II differ by serine phosphorylation. J Virol 1991, 65:546-550. 240555, 1898667.
42. Green PL, Yip MT, Xie Y, Chen ISY. Phosphorylation regulates RNA binding by the human T-cell leukemia virus rex protein. J Virol 1992, 66:4325-4330. 241238, 1602546.
43. Durkin SS, Ward MD, Fryrear KA, Semmes OJ. Site-specific phosphorylation differentiates active from inactive forms of the human T-cell leukemia virus type 1 Tax oncoprotein. J Biol Chem 2006, 281:31705-31712. 10.1074/jbc.M607011200, 16923801.
44. Ross TM, Minella AC, Fang ZY, Pettiford SM, Green PL. Mutational analysis of human T-cell leukemia virus type 2 Tax. J Virol 1997, 71:8912-8917. 192364, 9343258.
45. Ye J, Sileverman L, Lairmore MD, Green PL. HTLV-1 Rex is required for viral spread and persistence in vivo but is dispensable for cellular immortalization in vitro. Blood 2003, 102:3963-3969. 10.1182/blood-2003-05-1490, 12907436.
46. Kim JS, Raines RT. Ribonuclease S-peptide as a carrier in fusion proteins. Protein Science 1993, 2:348-356. 2142386, 8453373.
47. Joseph JD, Yeh ES, Swenson KI, Means AR, Winkler. The peptidyl-prolyl isomerase Pin1. Prog Cell Cycle Res 2003, 5:477-487.
48. Lu KP, Zhou XZ. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat Rev Mol Cell Biol 2007, 8:904-916. 10.1038/nrm2261, 17878917.
49. Kesic M, Ward MD, Semmes OJ, Green PL. Site-specific phosphorylation regulates human T-cell leukemia virus type 2 Rex function in vivo. J Virol 83(17):8859-68. 10.1128/JVI.00908-09, 19553333.
50. Hofer L, Weichselbraun I, Quick S, Farrington GK, Bohnlein E, Hauber J. Mutational analysis of the human T-cell leukemia virus type I trans-acting rex gene product. J Virol 1991, 65:3379-3383. 241001, 2033676.
51. Böhnlein SF, Pirker FP, Hofer L, Bachmayer H, Böhnlein E, Hauber J. Transdominant repressors for human T-cell leukeina virus type I Rex and human immunodeficiency virus type 1 Rev function. J Virol 1991, 65:81-88. 240491, 1985219.
52. Malim MH, Bohnlein S, Hauber J, Cullen BR. Functional dissection of the HIV-1 Rev transactivator-derivation of trans-dominant repressor of Rev function. Cell 1989, 58:205-214. 10.1016/0092-8674(89)90416-9, 2752419.
53. Venkatesh LK, Chinnadurai G. Mutants in a conserved region near the carboxy-terminus of HIV-1 Rev identify functionally important residues and exhibit a dominant negative phenotype. Virology 1990, 178:327-330. 10.1016/0042-6822(90)90414-M, 2202148.
54. Hakata Y, Umemoto T, Matsushita S, Shida H. Involvement of human CRM1 (exportin 1) in the export and multimerization of the Rex protein of human T-cell leukemia virus type 1. J Virol 1998, 72:6602-6607. 109841, 9658105.
55. Neubauer G, Mann M. Mapping of phosphorylation sites of gel-isolated proteins by nanoelectrospray tandem mass spectrometry: potentials and limitations. Anal Chem 1999, 71:235-242. 10.1021/ac9804902, 9921130.
56. Loyet KM, Stults JT, Arnott D. Mass spectrometric contributions to the practice of phosphorylation site mapping through 2003: a literature review. Mol Cell Proteomics 2005, 4:235-245. 10.1074/mcp.R400011-MCP200, 15640519.
57. Arnott D, Gawinowicz MA, Grant RA, Neubert TA, Packman LC, Speicher KD, Stone K, Turck CW. ABRF-PRG03: phosphorylation site determination. J Biomol Tech 2003, 14:205-215. 2279948, 13678151.
58. McLachlin DT, Chait BT. Analysis of phosphorylated proteins and peptides by mass spectrometry. Curr Opin Chem Biol 2001, 5:591-602. 10.1016/S1367-5931(00)00250-7, 11578935.
59. Ye J, Xie L, Green PL. Tax and overlapping Rex sequences do not confer the distinct transformation tropisms of HTLV-1 and HTLV-2. J Virol 2003, 77:7728-7735. 10.1128/JVI.77.14.7728-7735.2003, 161933, 12829812.
60. Ross TM, Pettiford SM, Green PL. The tax gene of human T-cell leukemia virus type 2 is essential for transformation of human T lymphocytes. J Virol 1996, 70:5194-5202. 190475, 8764028.
61. Voss OH, Batra S, Kolattukudy SJ, Gonzalez-Mejia ME, Smith JB, Doseff AI. Binding of caspase-3 prodomain to heat shock protein 27 regulates monocyte apoptosis by inhibiting caspase-3 proteolytic activation. J Biol Chem 2007, 282:25088-25099. 10.1074/jbc.M701740200, 17597071.