Transcriptional pausing at +62 of the HIV-1 nascent RNA modulates formation of the TAR RNA structure

Molecular Cell

Volumn 1, Issue 7, 1998, Pages 1033-1042

  Palangat, Murali ^a   Meier, Timothy I ^b,c   Keene, Richard G ^b,d   Landick, Robert ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c ELI LILLY AND COMPANY   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENERAL TRANSCRIPTION FACTOR; GUANOSINE TRIPHOSPHATE; HETERODUPLEX; PYROPHOSPHATE; RNA POLYMERASE II; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR S II; TRANSCRIPTION FACTOR S-II; TUMOR PROTEIN; VIRUS RNA;

ARTICLE; BINDING SITE; CHEMISTRY; CONFORMATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HELA CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; METHODOLOGY; NUCLEOTIDE SEQUENCE; STRUCTURE ACTIVITY RELATION;

BASE SEQUENCE; BINDING SITES; DIPHOSPHATES; GENE EXPRESSION REGULATION, VIRAL; GUANOSINE TRIPHOSPHATE; HELA CELLS; HIV-1; HUMANS; NEOPLASM PROTEINS; NUCLEIC ACID CONFORMATION; NUCLEIC ACID HETERODUPLEXES; RESEARCH DESIGN; RNA POLYMERASE II; RNA, VIRAL; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS, GENERAL; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 0032087891     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80103-3     Document Type: Article

References (59)

1. Bentley, D.L. (1995). Regulation of transcriptional elongation by RNA polymerase II. Curr. Opin. Genet. Dev. 5, 210-216.
2. Berkhout, B., Silverman, R.H., and Jeang, K.T. (1989). Tat trans-activates the human immunodeficiency virus through a nascent RNA target. Cell 59, 273-282.
3. Chan, C., Wang, D., and Landick, R. (1997). Spacing from the transcript 3′ end determines whether a nascent RNA hairpin interacts with RNA polymerase to prolong pausing or triggers termination. J. Mol. Biol. 268, 54-68.
4. Chan, C.L., and Landick, R. (1993). Dissection of the his leader pause site by base substitution reveals a multipartite signal that includes a pause RNA hairpin. J. Mol. Biol. 233, 25-42.
5. Chan, C.L., and Landick, R. (1994). New perspectives on RNA chain elongation and termination by E coli RNA polymerase. In Transcription: Mechanisms and Regulation, R.C. Conaway and J.W. Conaway, eds. (New York: Raven Press), pp. 297-321.
6. Churcher, M.J., Lamont, C., Hamy, F., Dingwall, C., Green, S.M., Lowe, A.D., Butler, JG, Gait, M.J., and Karn, J. (1993). High affinity binding of TAR RNA by the human immunodeficiency virus type-1 tat protein requires base-pairs in the RNA stem and amino acid residues flanking the basic region. J. Mol. Biol. 230, 90-110.
7. Cujec, T., Okamoto, H., Fujinaga, K., Meyer, J., Chamberlin, H., Morgan, D., and Peterlin, B. (1997). The HIV transactivator TAT binds to the CDK-activating kinase and activates the phosphoyrlation of the carboxy-terminal domain of RNA polmyerase II. Genes Dev. 11, 2645-2657.
8. Feng, G., Lee, D.N., Wang, D., Chan, C.L., and Landick, R. (1994). GreA-induced transcript cleavage in transcription complexes containing Escherichia coli RNA polymerase is controlled by multiple factors, including nascent transcript location and structure. J. Biol. Chem. 269, 22282-22294.
9. Garcia-Martinez, L.F., Mavankal, G., Neveu, J.M., Lane, W.S., Ivanov, D., and Gaynor, R.B. (1997). Purification of a Tat-associated kinase reveals a TFIIH complex that modulates HIV-1 transcription. EMBO J. 16, 2836-2850.
10. Graeble, M.A., Churcher, M.J., Lowe, A.D., Gait, M.J., and Karn, J. (1993). Human immunodeficiency virus type 1 transactivator protein, tat, stimulates transcriptional read-through of distal terminator sequences in vitro. Proc. Natl. Acad. Sci. USA 90, 6184-6188.
11. Gu, W., Powell, W., Mote, J., Jr., and Reines, D. (1993). Nascent RNA cleavage by arrested RNA polymerase II does not require upstream translocation of the elongation complex on DNA. J. Biol. Chem. 268, 25604-25616.
12. Gu, W., Wind, M., and Reines, D. (1996). Increased accommodation of nascent RNA in a product site on RNA polymerase II during arrest. Proc. Natl. Acad. Sci. USA 93, 6935-6940.
13. Guajardo, R., and Sousa, R. (1997). A model for the mechanism of polymerase translocation. J. Mol. Biol. 265, 8-19.
14. Izban, M.G., and Luse, D.S. (1991). Transcription on nucleosomal templates by RNA polymerase II in vitro: inhibition of elongation with enhancement of sequence-specific pausing. Genes Dev. 5, 683-696.
15. Jeang, K.T., and Berkhout, B. (1992). Kinetics of HIV-1 long terminal repeat trans-activation. Use of intragenic ribozyme to assess rate-limiting steps. J. Biol. Chem. 267, 17891-17899.
16. Jeong, S.W., Lang, W.H., and Reeder, R.H. (1996). The yeast transcription terminator for RNA polymerase I is designed to prevent polymerase slippage. J. Biol. Chem. 271, 16104-16110.
17. Jones, K.A. (1997). Taking a new TAK on Tat transactivation. Genes Dev. 11, 2593-2599.
18. 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.
19. Kadesch, T.R., and Chamberlin, M.J. (1982). Studies of in vitro transcription by calf thymus RNA polymerase II using a novel duplex DNA template. J. Biol. Chem. 257, 5286-5295.
20. Kamine, J., Subramanian, T., and Chinnadurai, G. (1991). Sp1-dependent activation of a synthetic promoter by human immunodeficiency virus type 1 Tat protein. Proc. Natl. Acad. Sci. USA 88, 8510-8514.
21. Kashlev, M., Martin, E., Polyakov, A., Severinov, K., Nikiforov, V., and Goldfarb, A. (1993). Histidine-tagged RNA polymerase: dissection of the transcription cycle using immobilized enzyme. Gene 130, 9-14.
22. 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.
23. Keen, N., Churcher, M., and Karn, J. (1997). Transfer of Tat and release of TAR RNA during the activation of the human immunodeficiency virus type-1 transcription elongation complex. EMBO J. 16, 5260-5272.
24. Kessler, M., and Mathews, M.B. (1992). Premature termination and processing of human immunodeficiency virus type 1-promoted transcripts. J. Virol. 66, 4488-4496.
25. Komissarova, N., and Kashlev, M. (1997). RNA polymerase switches between inactivated and activated states by translocating back and forth along the DNA and the RNA. J. Biol. Chem. 272, 15329-15338.
26. 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.
27. Landick, R. (1997). RNA polymerase slides home: pause and termination site recognition. Cell 88, 741-744.
28. Landick, R., Turnbough, C., Jr., and Yanofsky, C. (1996a).Transcription attenuation. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd Edition, F. Neidhardt, R. Curtiss, III, J. Ingraham, E. Lin, K. Low, B. Magasanik, W. Reznikoff, M. Riley, M. Schaechter, and H. Umbarger, eds. (Washington, DC: ASM Press), pp. 1263-1286.
29. Landick, R., Wang, D., and Chan, C. (1996b). Quantitative analysis of transcriptional pausing by RNA polymerase: the his leader pause site as a paradigm. Methods Enzymol. 274, 334-352.
30. Lang, W.H., Morrow, B.E., Ju, Q., Warner, J.R., and Reeder, R.H. (1994). A model for transcription termination by RNA polymerase I. Cell 79, 527-534.
31. Lee, D.N., and Landick, R. (1992). Structure of RNA and DNA chains in paused transcription complexes containing Escherichia coli RNA polymerase. J. Mol. Biol. 228, 759-777.
32. Linn, S.C., and Luse, D.S. (1991). RNA polymerase II elongation complexes paused after the synthesis of 15-or 35-base transcripts have different structures. Mol. Cell. Biol. 11, 1508-1522.
33. 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.
34. 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.
35. Mavankal, G., Ignatius Ou, S.H., Oliver, H., Sigman, D., and Gaynor, R.B. (1996). Human immunodeficiency virus type 1 and 2 Tat proteins specifically interact with RNA polymerase II. Proc. Natl. Acad. Sci. USA 93, 2089-2094.
36. Nudler, E., Mustaev, A., Lukhtanov, E., and Goldfarb, E. (1997). The RNA:DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell 89, 33-41.
37. O'Brien, T., and Lis, J.T. (1991). RNA polymerase II pauses at the 5′ end of the transcriptionally induced Drosophila hsp 70 gene. Mol. Cell. Biol. 11, 5285-5290.
38. Parada, C.A., and Roeder, R.G. (1996). Enhanced processivity of RNA polymerase II triggered by Tat-induced phosphorylation of its carboxy-terminal domain. Nature 384, 375-378.
39. Parada, C.A., Yoon, J.B., and Roeder, R.G. (1995). A novel LBP-1-mediated restriction of HIV-1 transcription at the level of elongation in vitro. J. Biol. Chem. 270, 2274-2283.
40. Reeder, T., and Hawley, D. (1996). Promoter proximal sequences modulate RNA polymerase II elongation by a novel mechanism. Cell 87, 767-777.
41. Reines, D., Conaway, J.W., and Conaway, R.C. (1996). The RNA polymerase II general elongation factors. Trends Biochem. Sci. 21, 351-355.
42. Rice, G.A., Kane, C.M., and Chamberlin, M.J. (1991). Footprinting analysis of mammalian RNA polymerase II along its transcript as an alternate view of transcription elongation. Proc. Natl. Acad. Sci. USA 88, 1245-1249.
43. 70 in promoter-proximal pausing. Cell 86, 485-493.
44. Ring, B.Z., and Roberts, J.W. (1994). Function of a nontranscribed DNA strand site in transcription elongation. Cell 78, 317-324.
45. Rougvie, A., and Lis, J. (1990). Postinitiation transcriptional control in Drosophila melanogaster. Mol. Cell. Biol. 10, 6041-6045.
46. Selby, M.J., and Peterlin, B.M. (1990). Trans-activation by HIV-1 Tat via a heterologous RNA binding protein. Cell 62, 769-776.
47. Shapiro, D., Wahli, W., and Keller, M. (1988). A high-efficiency HeLa cell nuclear transcription system. DNA 7, 47-55.
48. Southgate, C., Zapp, M.L., and Green, M.R. (1990). Activation of transcription by HIV-1 Tat protein tethered to nascent RNA through another protein. Nature 345, 640-642.
49. 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.
50. Sugimoto, N., Nakano, S., Katoh, M., Matsumura, A., Nakamuta, H., Ohmichi, T., Yoneyama, M., and Sasaki, M. (1995). Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes. Biochemistry 34, 11211-11216.
51. Thompson, N.E., and Burgess, R.R. (1996). Immunoaffinity purification of RNA polymerase II and transcription factors using polyol-responsive monoclonal antibodies. Methods Enzymol. 274, 513-526.
52. Tuerk, C., Gauss, P., Thermes, C., Groebe, D.R., Gayle, M., Guild, N., Stormo, G., d'Aubenton-Carafa, Y., Uhlenbeck, O.C., Tinoco, I.J., Brody, E.N., and Gold, L. (1988). CUUCGG hairpins: extraordinarily stable RNA secondary structures associated with various biochemical processes. Proc. Natl. Acad. Sci. USA 85, 1364-1368.
53. Valegard, K., Murray, J.B., Stockley, P.G., Stonehouse, N.J., and Liljas, L. (1994). Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature 371, 623-626.
54. Wang, D., and Landick, R. (1997). A nascent RNA hairpin that stimulates transcriptional pausing interacts with RNA polymerase near amino acid 900 of the β subunit. Proc. Natl. Acad. Sci. USA 94, 8433-8438.
55. Wei, P., Garber, M., Fang, S.-M., Fischer, W., and Jones, K. (1998). A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates in high-affinity, loop-specific binding to TAR RNA. Cell 92, 451-462.
56. Wu, F., Garcia, J., Sigman, D., and Gaynor, R. (1991). Tat regulates binding of the human immunodeficiency virus trans-activating region RNA loop-binding protein TRP-185. Genes Dev. 5, 2128-2140.
57. Yoo, O.J., Yoon, H.S., Baek, K.H., Jeon, C.J., Miyamoto, K., Ueno, A., and Agarwal, K. (1991). Cloning, expression and characterization of the human transcription elongation factor, TFIIS. Nucleic Acids Res. 19, 1073-1079.
58. Zhu, Y., Pe'ery, T., Peng, J., Ramanathan, Y., Marshall, N., Marshall, T., Amendt, B., Mathews, M., and Price, D. (1997). Transcription elongation factor P-TEFb is required for HIV-1 Tat transactivation in vitro. Genes Dev. 11, 2622-2632.
59. Zuker, M., and Stiegler, P. (1981). Optimal computer folding of large RNA sequences using thermodynamics and auxilliary information. Nucleic Acids Res. 9, 133-148.