Human Immunodeficiency Virus Type 1 hnRNP A/B-Dependent Exonic Splicing Silencer ESSV Antagonizes Binding of U2AF65 to Viral Polypyrimidine Tracts

Molecular and Cellular Biology

Volumn 23, Issue 23, 2003, Pages 8762-8772

  Domsic, Jeffrey K ^a,d   Wang, Yibin ^a   Mayeda, Akila ^b   Krainer, Adrian R ^c   Stoltzfus, C Martin ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RNA; RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; VPR PROTEIN;

ARTICLE; BINDING COMPETITION; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN SYNTHESIS REGULATION; RNA BINDING; RNA SPLICING; VIRUS REPLICATION;

BASE SEQUENCE; EXONS; GENE SILENCING; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HIV-1; HUMANS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PROTEIN BINDING; RETROVIRIDAE PROTEINS; RIBONUCLEOPROTEINS; RNA SPLICING; RNA, SMALL NUCLEAR; RNA, VIRAL; SPLICEOSOMES;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

EID: 0242637344     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.23.8762-8772.2003     Document Type: Article

References (52)

1. Abdul-Manan, N., and K. R. Williams. 1996. hnRNP A1 binds promiscuously to oligoribonucleotides: utilization of random and homo-oligonucleotides to discriminate sequence from base-specific binding. Nucleic Acids Res. 24:4063-4070.
2. Amendt, B. A., D. Hesslein, L.-J. Chang, and C. M. Stoltzfus. 1994. Presence of negative and positive cis-acting RNA splicing elements within and flanking the first tat coding exon of human immunodeficiency virus type 1. Mol. Cell Biol. 14:3960-3970.
3. Amendt, B. A., Z.-H. Si, and C. M. Stoltzfus. 1995. Presence of exon splicing silencers within human immunodeficiency virus type 1 tat exon 2 and tat-rev exon 3: evidence for inhibition mediated by cellular factors. Mol. Cell Biol. 15:4606-4615.
4. Arrigo, S. J., S. Weitsman, J. A. Zack, and I. S. Chen. 1990. Characterization and expression of novel singly spliced RNA species of human immunodeficiency virus type 1. J. Virol. 64:4585-4588.
5. Ashe, M. P., A. Furger, and N. J. Proudfoot. 2000. Stem-loop 1 of the U1 snRNP plays a critical role in the suppression of HIV-1 polyadenylation. RNA 6:170-177.
6. Ashe, M. P., L. H. Pearson, and N. J. Proudfoot. 1997. The HIV-1 5′ LTR poly(A) site is inactivated by U1 snRNP interaction with the downstream major splice donor site. EMBO J. 16:5752-5763.
7. Berglund J. A., N. Abovich, and M. Rosbash. 1998. A cooperative interaction between U2AF65 and mBBP/SF1 facilitates branchpoint region recognition. Genes Dev. 12:858-867.
8. Bilodeau, P. S., J. K. Domsic, A. Mayeda, A. R. Krainer, and C. M. Stoltzfus. 2001. RNA splicing at human immunodeficiency virus type 1 3′ splice site A2 is regulated by binding of hnRNP A/B proteins to an exonic splicing silencer element. J. Virol. 75:8487-8497.
9. Black, D. L., B. Chabot, and J. A. Steitz. 1985. U2 as well as U1 small nuclear ribonucleoproteins are involved in premessenger RNA splicing. Cell 42:737-750.
10. Burd, C. G., and G. Dreyfuss. 1994. RNA binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J. 13:1197-1204.
11. Butsch, M., and K. Boris-Lawrie. 2000. Translation is not required to generate virion precursor RNA in human immunodeficiency virus type 1-infected T cells. J. Virol. 74:11531-11537.
12. Caputi, M., A. Mayeda, A. R. Krainer, and A. M. Zahler. 1999. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 18:4060-4067.
13. Cartegni, L., M. Maconi, E. Morandi, F. Cobianchi, S. Riva, and G. Biamonti. 1996. hnRNP A1 selectively interacts through its Gly-rich domain with different RNA-binding proteins. J. Mol. Biol. 259:337-348.
14. Cullen, B. R. 1998. Retroviruses as model systems for the study of nuclear RNA export pathways. Virology 249:203-210.
15. Damgaard, C. K., T. O. Tange, and J. Kjems. 2002. hnRNP A1 controls HIV-1 mRNA splicing through cooperative binding to intron and exon splicing silencers in the context of a conserved secondary structure. RNA 8:1401-1415.
16. Das, R., and R. Reed. 1999. Resolution of the mammalian E complex and the ATP-dependent spliceosomal complexes on native agarose mini-gels. RNA 5:1504-1508.
17. Das, R., Z. Zhou, and R. Reed. 2000. Functional association of U2 snRNP with the ATP-independent spliceosomal complex E. Mol. Cell 5:779-787.
18. Del Gatto, F., M. C. Gesnel, and R. Breathnach. 1996. The exon sequence TAGG can inhibit splicing. Nucleic Acids Res. 24:2017-2021.
19. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
20. Freed, E. O. 2001. HIV-1 replication. Somat. Cell Mol. Genet. 26:13-33.
21. Furger, A., J. Monks, and N. J. Proudfoot. 2001. The retroviruses human immunodeficiency virus type 1 and Moloney murine leukemia virus adopt radically different strategies to regulate promoter-proximal polyadenylation. J. Virol. 75:11735-11746.
22. Furtado, M. R., R. Balachandran, P. Gupta, and S. M. Wolinsky. 1991. Analysis of alternatively spliced human immunodeficiency virus type-1 mRNA species, one of which encodes a novel tat-env fusion protein. Virology 185:258-270.
23. Gama-Carvalho, M., R. D. Krauss, L. Chiang, J. Valcarcel, M. R. Green, and M. Carmo-Fonseca. 1997. Targeting of U2AF65 to sites of active splicing in the nucleus. J. Cell Biol. 137:975-987.
24. Graveley, B. R., K. J. Hertel, and T. Maniatis. 2001. The role of U2AF35 and U2AF65 in enhancer-dependent splicing. RNA 7:806-818.
25. Guatelli, J. C., T. R. Gingeras, and D. D. Richman. 1990. Alternative splice acceptor utilization during human immunodeficiency virus type 1 infection of cultured cells. J. Virol. 64:4093-4098.
26. Guth, S., T. O. Tange, E. Kellenberger, and J. Valcarcel. 2001. Dual function for U2AF(35) in AG-dependent pre-mRNA splicing. Mol. Cell. Biol. 21:7673-7681.
27. Hou, V. C., R. Lersch, S. L. Gee, J. L. Ponthier, A. J. Lo, M. Wu, C. W. Turck, M. Koury A. R. Krainer, A. Mayeda, and J. G. Conboy. 2002. Decrease in hnRNP A/B expression during erythropoiesis mediates a pre-mRNA splicing switch. EMBO J. 21:6195-6204.
28. Jacquenet, S., D. Ropers, P. S. Bilodeau, L. Damier, A. Mougin, C. M. Stoltzfus, and C. Branlant. 2001. Conserved stem-loop structures in the HIV-1 RNA region containing the A3 3′ splice site and its cis-regulatory element: possible involvement in RNA splicing. Nucleic Acids Res. 29:464-478.
29. Kammler, S., C. Leurs, M. Freund, J. Krummheuer, K. Seidel, T. O. Tange, M. K. Lund, J. Kjems, A. Scheid, and H. Schaal. 2001. The sequence complementarity between HIV-1 5′ splice site SD4 and U1 snRNA determines the steady-state level of an unstable env pre-mRNA. RNA 7:421-434.
30. Konarska, M. M. 1989. Analysis of splicing complexes and small nuclear ribonucleoprotein particles by native gel electrophoresis. Methods Enzymol. 180:442-453.
31. Krainer, A. R., T. Maniatis, B. Ruskin, and M. R. Green. 1984. Normal and mutant human beta-globin pre-mRNAs are faithfully and efficiently spliced in vitro. Cell 36:993-1005.
32. Marchand, V., A. Mereau, S. Jacquenet, D. Thomas, A. Mougin, R. Gattoni, J. Stevenin, and C. Branlant. 2002. A Janus splicing regulatory element modulates HIV-1 tat and rev mRNA production by coordination of hnRNP A1 cooperative binding. J. Mol. Biol. 323:629-652.
33. Mayeda, A., and A. R. Krainer. 1992. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68:365-375.
34. Mayeda, A., S. H. Munroe, J. F. Caceres, and A. R. Krainer. 1994. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J. 13:5483-5495.
35. Merendino, L., S. Guth, D. Bilbao, C. Martinez, and J. Valcarcel. 1999. Inhibition of msl-2 splicing by Sex-lethal reveals interaction between U2AF35 and the 3′ splice site AG. Nature 402:838-841.
36. O'Reilly, M. M., M. T. McNally, and K. L. Beemon. 1995. Two strong 5′ splice sites and competing, suboptimal 3′ splice sites involved in alternative splicing of human immunodeficiency virus type 1 RNA. Virology 213:373-385.
37. Purcell, D. F., and M. A. Martin. 1993. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J. Virol. 67:6365-6378.
38. Reed, R. 2000. Mechanisms of fidelity in pre-mRNA splicing. Curr. Opin. Cell Biol. 12:340-345.
39. Reed, R. 1989. The organization of 3′ splice-site sequences in mammalian introns. Genes Dev. 3:2113-2123.
40. Robert-Guroff, M., M. Popovic, S. Gartner, P. Markham, R. C. Gallo, and M. S. Reitz. 1990. Structure and expression of tat-, rev-, and nef-specific transcripts of human immunodeficiency virus type 1 in infected lymphocytes and macrophages. J. Virol. 64:3391-3398.
41. Schwartz, S., B. K. Felber, D. M. Benko, E. M. Fenyo, and G. N. Pavlakis, 1990. Cloning and functional analysis of multiply spliced mRNA species of human immunodeficiency virus type 1. J. Virol. 64:2519-2529.
42. Si, Z., B. A. Amendt, and C. M. Stoltzfus. 1997. Splicing efficiency of human immunodeficiency virus type 1 tat RNA is determined by both a suboptimal 3′ splice site and a 10 nucleotide exon splicing silencer element located within tat exon 2. Nucleic Acids Res. 25:861-867.
43. Si, Z.-H., D. Rauch, and C. M. Stoltzfus. 1998. The exon splicing silencer in human immunodeficiency virus type 1 Tat exon 3 is bipartite and acts early in spliceosome assembly. Mol. Cell. Biol. 18:5404-5413.
44. Singh, R., J. Valcarcel, and M. R. Green. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268:1173-1176.
45. Staffa, A., and A. Cochrane. 1995. Identification of positive and negative splicing regulatory elements within the terminal tat-rev exon of human immunodeficiency virus type 1. Mol. Cell Biol. 15:4597-4605.
46. Staffa, A., and A. Cochrane. 1994. The tat/rev intron of human immunodeficiency virus type 1 is inefficiently spliced because of suboptimal signals in the 3′ splice site. J. Virol. 68:3071-3079.
47. Tange, T. O., C. K. Damgaard, S. Guth, J. Valcarcel, and J. Kjems. 2001. The hnRNP A1 protein regulates HIV-1 tat splicing via a novel intron silencer element. EMBO J. 20:5748-5758.
48. Valcarcel, J., R. Singh, P. D. Zamore, and M. R. Green. 1993. The protein Sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature 362:171-175.
49. Wu, S., C. M. Romfo, T. W. Nilsen, and M. R. Green. 1999. Functional recognition of the 3′ splice site AG by the splicing factor U2AF35. Nature 402:832-835.
50. Zamore, P. D., and M. R. Green. 1991. Biochemical characterization of U2 snRNP auxiliary factor: an essential pre-mRNA splicing factor with a novel intranuclear distribution. EMBO J. 10:207-214.
51. Zhu, J., A. Mayeda, and A. R. Krainer. 2001. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol. Cell 8:1351-1361.
52. Zorio, D. A., and T. Blumenthal. 1999. Both subunits of U2AF recognize the 3′ splice site in Caenorhabditis elegans. Nature 402:835-838.