Purification of a Tat-associated kinase reveals a TFIIH complex that modulates HIV-1 transcription

EMBO Journal

Volumn 16, Issue 10, 1997, Pages 2836-2850

  García Martínez, León F ^b   Mavankal, Gopinath ^b   Neveu, John M ^a   Lane, William S ^a   Ivanov, Dmitri ^b   Gaynor, Richard B ^b  

^a HARVARD UNIVERSITY   (United States)

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

Author keywords

HIV 1; Kinase; RNA polymerase II; Tat; TFIIH

Indexed keywords

PROTEIN KINASE; RNA POLYMERASE II; TRANSACTIVATOR PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; TRANSCRIPTION INITIATION;

CYCLIN-DEPENDENT KINASES; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; GENE EXPRESSION REGULATION, VIRAL; GENE PRODUCTS, TAT; HIV-1; NEOPLASM PROTEINS; NUCLEIC ACID SYNTHESIS INHIBITORS; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RNA POLYMERASE II; SEQUENCE ANALYSIS; TRANSCRIPTION FACTOR TFIIH; TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS, TFII; TRANSCRIPTION, GENETIC;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0039243885     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.10.2836     Document Type: Article

References (83)

1. Akoulitchev, S., Makela, T.P., Weinberg, R.A. and Reinberg, D. (1995) Requirement for TFIIH kinase activity in transcription by RNA polymerase II. Nature, 377, 557-560.
2. Blau, J., Xiao, H., McCracken, S., O'Hare, P., Greenblatt, J. and Bentley, D. (1996) Three functional classes of transcriptional activation domains. Mol. Cell. Biol., 16, 2044-2055.
3. Cadena, D. and Dahmus, M.J. (1987) Messenger RNA synthesis in mammalian cells is catalyzed by the phosphorylated form of RNA polymerase II. J. Biol. Chem., 262, 12468-12474.
4. Chao, D.M., Gadbois, E.L., Murray, P.J., Anderson, S.F., Sonu, M.S., Parvin, J.D. and Young, R.A. (1996) A mammalian SRB protein associated with an RNA polymerase II holoenzyme. Nature, 380, 82-85.
5. Chodosh, L.A., Fire, A., Samuels, M. and Sharp, P.A. (1989) 5,6-Dichloro1-beta-D-ribofuranosylbenzimidazole inhibits transcription elongation by RNA polymerase II in vitro. J. Biol. Chem., 264, 2250-2257.
6. Dignam, J.D., Lebovitz, R.M. and Roeder, R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
7. Dingwall, C., Ernberg, I., Gait, M.J., Green, S.M., Heaphy, S., Karn, J., Lowe, A.D., Singh, M. and Skinner, M.A. (1990) HIV-1 Tat protein stimulates transcription by binding to a U-rich bulge in the stem of the TAR RNA structure. EMBO J., 9, 4145-1153.
8. Drapkin, R., Reardon, J.T., Ansari, A., Huang, J.-C., Zawel, L., Ahn, K., Sancar, A. and Reinberg, D. (1994) Dual role of TFIIH in DNA excision repair and in transcription by RNA polymerase II. Nature, 368, 769-772.
9. Drapkin, R., Roy, G.L., Cho, H., Akoulitchev, S. and Reinberg, D. (1996) Human cyclin-dependent kinase-activating kinase exists in three distinct complexes. Proc. Natl Acad. Sci. USA, 93, 6488-6493.
10. Elroy-Stein, O., Fuerst, T.R. and Moss, B. (1989) Cap-independent translation of mRNA conferred by encephalomyocarditis virus 5′ sequence improves the performance of the vaccinia virus/bacteriophage T7 hybrid expression system. Proc. Natl Acad. Sci. USA, 86, 6126-6130.
11. Feaver, W.J., Svejstrup, J.Q., Henry, N.L. and Kornberg, R.D. (1994) Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK. Cell. 79, 1103-1109.
12. Feinberg, M.B., Baltimore, D. and Frankel, A.D. (1991) The role of Tat in the human immunodeficiency virus life cycle indicates a primary effect on transcriptional elongation. Proc. Natl Acad. Sci. USA, 88, 4045-4049.
13. Feng, S. and Holland, E.C. (1988) HIV-1 Tat trans-activation requires the loop sequence within TAR. Nature, 334, 165-167.
14. Fernandez, J.L., Andrews, L. and Mische, S.M. (1994) An improved procedure for enzymatic digestion of poly vinylidene difluoride-bound proteins for internal sequence analysis. Anal. Biochem., 218, 113-117.
15. Field, J., Nikawa, J., Broek, D., MacDonald, B., Rodgers, L., Wilson, I.A., Lerner, R.A. and Wigler, M. (1988) Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell Biol., 8, 2159-2165.
16. Fischer, L., Gerard, M., Chalut, C., Lutz, Y., Humbert, S., Kanno, M., Chambon, P. and Egly, J.M. (1992) Cloning of the 62-kilodalton component of basic transcription factor BTF2. Science, 257 1392-1395.
17. Fisher, R.P. and Morgan, D.O. (1994) A novel cyclin associates with M015/CDK7 to form the CDK-activating kinase. Cell, 78, 713-724.
18. Fisher, R.P., Jin, P., Chamberlin, H.M. and Morgan, D.O. (1995) Alternative mechanisms of CAK assembly require an assembly factor or an activating kinase. Cell, 83, 47-57.
19. Flores, O., Lu, H. and Reinberg, D. (1992) Factors involved in specific transcription by mammalian RNA polymerase II. Identification and characterization of factor IIH. J. Biol. Chem., 267, 2786-2793.
20. García-Martínez, L.F., Mavankal, G., Peters, P., Wu-Baer, F. and Gaynor, R.B. (1995) Tat functions to stimulate the elongation properties of transcription complexes paused by the duplicated TAR RNA element of human immunodeficiency virus 2. J. Mol. Biol., 254, 350-363.
21. Gerard, M., Fischer, L., Moncollin, V., Chipoulet, J.M., Chambon, P. and Egly, J.M. (1991) Purification and interaction properties of the human RNA polymerase B (II) general transcription factor BTF2. J. Biol. Chem., 266, 20940-20945.
22. Gerber, H.P., Hagmann, M., Seipel, K., Georgiev, O., West, M.A., Litingtung, Y., Schaffner, W. and Cordan, J.L. (1995) RNA polymerase II C-terminal domain required for enhancer-driven transcription. Nature, 374, 660-662.
23. Goodrich, J.A. and Tjian, R. (1994) Transcription factors IIE and IIIH and ATP hydrolysis direct promoter clearance by RNA polymerase II. Cell, 77, 145-156.
24. Graeble, M.A., Churcher, M.J., Lowe, A.D., Gait, M.J. and Karn, J. (1993) Human immunodeficiency virus type-1 trans-activator protein, tat, stimulates transcriptional read-through of distal terminator sequences in vitro. Proc. Natl Acad. Sci. USA, 90, 6184-6188.
25. Herrmann, C.H. and Rice, A.P. (1995) Lentivirus Tat proteins specifically associate with a cellular protein kinase, TAK, that hyperphosphorylates the carboxyl-terminal domain of the large subunit of RNA polymerase II: candidate for a Tat cofactor. J. Virol., 69, 1612-1620.
26. Herrmann, C.H., Gold, M.O. and Rice, A.P. (1996) Viral transactivators specifically target distinct cellular protein kinases that phosphorylate the RNA polymerase II C-terminal domain. Nucleic Acids Res., 24, 501-508.
27. Hodo, H.G. and Blatti, S.P. (1977) Purification using polyethylemmine precipitation and low molecular weight subunit analysis of calf thymus and wheat germ DNA-dependent RNA polymerase. Biochemistry, 16, 2334-23433.
28. Humbert, S., van Vuuren, H., Lutz, Y., Hoeijmakers, J.H.J., Egly, J.-M. and Moncollin, V. (1994) p44 and p34 subunits of the BTF2/TFIIH transcription factor have homologies with SSL1, a yeast protein involved in DNA repair. EMBO J., 13, 2393-2398.
29. Jones, K.A. and Peterlin, B.M. (1994) Control of RNA initiation and elongation at the HIV-1 promoter. Annu. Rev. Biochem., 63, 717-743.
30. Kao, S.Y., Calnan, A.F., Luciw, P.A. and Peterlin, B.M. (1987) Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature, 330, 489-493.
31. Kato, H., Sumimoto, H., Pognonec, P., Chen, C.H., Rosen, C.A. and Roeder, R.G. (1992) HIV-1 Tat acts as a processivity factor in vitro in conjunction with cellular elongation factors. Genes Dev., 6, 655-666.
32. Keen, N.J., Gait, M.J. and Karn, J. (1996) Human immunodeficiency virus type-1 Tat is an integral component of the activated transcription-elongation complex. Proc. Natl Acad. Sci. USA, 93, 2505-2510.
33. Kim, Y.-J., Bjorklund, S., Li, Y., Sayre, M.H. and Kornberg, R.D. (1994) A multiprotein mediator of transcriptional activation and its interaction with the C terminal repeat domain of RNA polymerase II. Cell, 77, 599-608.
34. Koleske, A.J. and Young, R.A. (1994) An RNA polymerase II holoenzyme responsive to activators. Nature, 368, 466-469.
35. Koleske, A.J. and Young, R.A. (1995) The RNA polymerase II holoenzyme and its implications for gene regulation. Trends Biochem. Sci., 20, 113-116.
36. Krumm, A., Hickey, L.B. and Groudine, M. (1995) Promoter-proximal pausing of RNA polymerase II defines a general rate-limiting step after transcription initiation. Genes Dev., 9, 559-572.
37. Lane, W.S., Galat, A., Harding, M.W. and Schreiber, S.L. (1991) Complete amino acid sequence of the FK506 and rapamycin binding protein, FKBP, isolated from calf thymus. J. Protein Chem., 10, 151-160.
38. Laspia, M.F., Rice, A.P. and Mathews, M.B. (1989) HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell, 59, 283-292.
39. Lu, H., Flores, O., Weinmann, R. and Reinberg, D. (1991) The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. Proc. Natl Acad. Sci. USA, 88, 10004-10008.
40. Lu, H., Zawel, L., Fisher, L., Egly, J.-M. and Reinberg, D. (1992) Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature, 358, 641-645.
41. Makela, T.P., Parvin, J.D., Kim, J., Huber, L.J., Sharp, P.A. and Weinberg, R.A. (1995) A kinase-deficient transcription factor TFIIH is functional in basal and activated transcription. Proc. Natl Acad. Sci. USA, 92, 5174-5178.
42. Maldonado, E. et al. (1996) A human RNA polymerase II complex associated with SRB and DNA-repair proteins. Nature, 381, 86-89.
43. Marciniak, R.A. and Sharp, P.A. (1991) HIV-1 Tat protein promotes formation of more-processive elongation complexes. EMBO J., 10, 4189-4196.
44. Marciniak, R.A., Calnan, B.J., Frankel, A.D. and Sharp, P.A. (1990) HIV-1 Tat protein trans-activates transcription in vitro. Cell, 63, 791-802.
45. Marinoni, J.C. et al. (1996) Cloning and characterization of p52 the fifth subunit of the core of the transcription/DNA repair factor TFIIH. DDBJ/EMBL/GenBank Accession No. Y07595.
46. Mavankal, G., Ou, S.H.I., Oliver, H., Sigman, D. and Gaynor, R.B. (1996) HIV-1 and HIV-2 Tat proteins specifically interact with RNA polymerase II. Proc. Natl Acad. Sci. USA, 93, 2089-2094.
47. Maxon, E., Goodrich, J.A. and Tjian, R.M. (1994) Transcription factor IIE binds preferentially to RNA polymerase IIa and recruits TFIIH: a model for promoter clearance. Genes Dev., 8, 515-524.
48. O'Brian, T., Hardin, S., Greenleaf, A. and Lis, J.T. (1994) Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature, 370, 75-77.
49. Ohkuma, Y. and Roeder, R.G. (1994) Regulation of TFIIH ATPase and kinase activities by TFIIE during active initiation complex formation. Nature, 368, 160-163.
50. Ossipow, V., Tassan, J.-P., Nigg, E.A. and Schibler, U. (1995) A mammalian RNA polymerase II holoenzyme containing all components required for promoter-specific transcription initiation. Cell, 83, 137-146.
51. Parvin, J. and Sharp, P.A. (1993) DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell, 73, 533-540.
52. Payne, J.M. and Dahmus, M.E. (1993) Partial purification and characterization of two distinct protein kinases that differentially phosphorylate the carboxyl-terminal domain of RNA polymerase subunit IIa. J. Biol. Chem., 268, 80-87.
53. Payne, J.M., Laybourn, P.J. and Dahmus, M.E. (1989) The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxyl-terminal domain of subunit IIa. J. Biol. Chem., 264, 19621-19629.
54. Peterson, S.R., Dvir, A., Anderson, C.W. and Dynan, W.S. (1992) DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapetide repeats. Genes Dev., 6, 426-438.
55. Ratnasabapathy, R., Sheldon, M., Johal, L. and Hernandez, N. (1990) The HIV-1 long terminal repeat contains an unusual element that induces the synthesis of short RNAs from various mRNA and snRNA promoters. Genes Dev., 4, 2061-2074.
56. Reardon, J.T., Ge, H., Gibbs, E., Sancar, A., Hurwitz, J. and Pan, Z.-Q. (1996) Isolation and characterization of two human transcription factor IIH (TFIIH)-related complexes: ERCC2/CAK and TFIIH. Proc. Natl Acad. Sci. USA, 93, 6482-6487.
57. Reinberg, D. and Roeder, R.G. (1987) Factors involved in specific transcription by mammalian RNA polymerase II. Purification and functional analysis of initiation factors IIB and IIE. J. Biol. Chem., 262, 3310-3321.
58. Rosen, C.A., Sodoroski, J.G. and Haseltine, W.A. (1985) The location of cis-acting regulatory sequences in the human T cell lymphotropic virus type III (HTLV-III/LAV) long terminal repeat. Cell, 41, 813-823.
59. Roy, R., Adamczewski, J.P., Seroz, T., Vermeulen, W., Tassan, J.P., Schaeffer, L., Nigg, E.A., Hoeijmakers, J.H.J. and Egly, J.-M. (1994) The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor. Cell, 79, 1093-1101.
60. Schaeffer, L., Roy, R., Humber, S., Moncollin, V. Vermeulen, W., Hoeijmakers, J.H.J., Chambon, P. and Egly, J.-M. (1993) DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science, 260, 58-63.
61. Schaeffer, L., Moncolin, V., Roy, R., Staub, A., Mezzina, M., Sarasin, A., Weeda, G., Hoeijmaker, J.H.J. and Egly, J.-M. (1994) The ERCC2/DNA repair protein is associated with the class II BTF2/TFIIH transcription factor. EMBO J., 13, 2388-2392.
62. Serizawa, H., Conaway, J.W. and Conaway, R.C. (1993) Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature, 363, 371-374.
63. Serizawa, H., Makela, T.P., Conaway, J.W., Conaway, R.C., Weinberg, R.A. and Young, R.A. (1995) Association of Cdk-activating kinase subunits with transcription factor TFIIH. Nature, 374, 280-282.
64. Shiekhattar, R., Mermelstein, F., Fisher, R.D., Drapkin, R., Dynlacht, B., Wessling, H.C., Morgan, D.O. and Reinberg, D. (1995) Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature, 374, 283-287.
65. Smith, D.B. and Johnson, K.S. (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione 5-transferase. Gene, 67, 31-40.
66. Southgate, C.D. and Green, M.R. (1991) The HIV-1 Tat protein activates transcription from an upstream DNA-binding site: implications for Tat function. Genes Dev., 5, 2496-2507.
67. Sung, P. Guzder, S.N., Prakash, L. and Prakash, S. (1996) Reconstitution of TFIIH and requirement of its DNA helicase subunits. Rad3 and Rad25, in the incision step of nucleotide excision repair. J. Biol. Chem., 271, 10821-10826.
68. Svejstrup, J.Q., Wang, Z., Feaver, W.J., Wu, X., Bushnell, D.A., Donahue, T.F., Friedberg, E.C. and Kornberg, R.D. (1995) Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nucleotide excision repairosome. Cell, 80, 21-28.
69. Tassan, J.-P., Jaquenoud, M., Fry, A.M., Frutiger, S., Hughes, G.J. and Nigg, E.A. (1995a) In vitro assembly of a functional human CDK7-cyclin H complex requires MAT1, a novel 36 kDa RING finger protein. EMBO J., 14, 5608-5617.
70. Tassan, J.-P., Jaquenoud, M., Leopold, P., Schultz, S.J. and Nigg, E.A. (1995b) Identification of human cyclin-dependent kinase 8, a putative protein kinase partner for cyclin C. Proc. Natl Acad. Sci. USA, 92, 8871-8875.
71. Thompson, C.M., Koleske, A.J., Chao, D.M. and Young, R.A. (1993) A multisubunit complex associated with the RNA polymerase II CTD and TATA-binding protein in yeast. Cell, 73, 1361-1375.
72. Usheva, A., Maldonado, E., Goldring, A., Lu, H., Houbavi, C., Reinberg, D. and Aloni, Y. (1992) Specific interaction between the nonphosphorylated form of RNA polymerase II and the TATA-binding protein. Cell, 69, 871-881.
73. Weber, C.A., Salazar, E.R. Stewart, S.A. and Thompson, L.H. (1990) ERCC2: cDNA cloning and molecular characterization of a human nucleotide excision repair gene with high homology to yeast RAD3. EMBO J., 9, 1437-1447.
74. Weeks, J.R., Hardin, S.E., Shen, J., Lee, J.M. and Greenleaf, A.L. (1993) Locus-specific variation in phosphorylation state of RNA polymerase II in vivo: correlations with gene activity and transcript processing. Genes Dev., 7, 2329-2344.
75. Wu-Baer, F., Sigman, D. and Gaynor, R.B. (1995a) Specific binding of RNA polymerase II to the human immunodeficiency virus trans-activating region RNA is regulated by cellular cofactors and Tat. Proc. Natl Acad. Sci. USA. 92, 6213-6217.
76. Wu-Baer, F., Lane, W. and Gaynor, R.B. (1995b) The cellular factor TRP-185 regulates RNA polymerase II binding to HIV-1 TAR RNA. EMBO J., 14, 5995-6009.
77. Xiao, H. et al. (1994) Binding of basal transcription factor TFIIH to the acidic activation domains of VP16 and p53. Mol. Cell. Biol., 14, 7013-7024.
78. Yang, X., Herrmann, C.H. and Rice, A.P. (1996) The human immunodeficiency virus Tat proteins specifically associate with TAK in vivo and require the carboxyl-terminal domain of RNA polymerase II for function. J. Virol., 70, 4576-4584.
79. Yankulov, K., Blau, J., Purton, T., Roberts, S. and Bentley, D.L. (1994) Transcriptional elongation by RNA polymerase II is stimulated by transactivators. Cell, 77, 749-759.
80. Yankulov, K., Yamashita, K., Roy, R., Egly, J.-M. and Bentley, D.L. (1995) The transcriptional elongation inhibitor 5,6-dichloro-1-β-D-ribofuranosylbenzimidazole inhibits transcription factor IIH-associated protein kinase. J. Biol. Chem., 270, 23922-23925.
81. Zawel, L. and Reinberg, D. (1995) Common themes in assembly and function of eukaryotic transcription complexes. Annu. Rev. Biochem., 64, 533-561.
82. Zawel, L., Kumar, K.P. and Reinberg, D. (1995) Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev., 9, 1479-1490.
83. Zhou, Q. and Sharp, P.A. (1995) Novel mechanism and factor for regulation by HIV-1 Tat. EMBO J., 14, 321-328.