Chapter 1 Regulation of HIV-1 Alternative RNA Splicing and Its Role in Virus Replication

Advances in Virus Research

Volumn 74, Issue , 2009, Pages 1-40

  Martin Stoltzfus, C ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; VIRUS RNA;

ALTERNATIVE RNA SPLICING; CELL LINE; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REVIEW; VIRUS REPLICATION;

ALTERNATIVE SPLICING; BASE SEQUENCE; CELL LINE; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, VIRAL; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; RNA, VIRAL; VIRUS REPLICATION;

EID: 68649095173     PISSN: 00653527     EISSN: 15578399     Source Type: Book Series    
DOI: 10.1016/S0065-3527(09)74001-1     Document Type: Review

References (103)

1. Abbink T.E., and Berkhout B. RNA structure modulates splicing efficiency at the human immunodeficiency virus type 1 major splice donor. J. Virol. 82 (2008) 3090-3098
2. Adachi A., Gendelman H.E., Koenig S., Folks T., Willey R., Rabson A., and Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59 (1986) 284-291
3. Aldovini A., and Young R.A. Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus. J. Virol. 64 (1990) 1920-1926
4. Amendt B.A., Hesslein D., Chang L.-J., and Stoltzfus C.M. Presence of negative and positive cis-acting RNA splicing elements within and flanking the first tat coding exon of the human immunodeficiency virus type 1. Mol. Cell. Biol. 14 (1994) 3960-3970
5. Amendt B.A., Si Z.-H., and Stoltzfus C.M. Presence of exon splicing silencers within HIV-1 tat exon 2 and tat/rev exon 3: Evidence for inhibition mediated by cellular factors. Mol. Cell. Biol. 15 (1995) 4606-4615
6. Asang C., Hauber I., and Schaal H. Insights into the selective activation of alternatively used splice acceptors by the human immunodeficiency virus type-1 bidirectional splicing enhancer. Nucl. Acids Res. 36 (2008) 1450-1463
7. Ashe M.P., Griffin P., James W., and Proudfoot N.J. Poly(A) site selection in the HIV-1 provirus: Inhibition of promoter-proximal polyadenylation by the downstream major splice donor site. Genes Dev. 9 (1995) 3008-3025
8. Ashe M.P., Pearson L.H., and Proudfoot N.J. The HIV-1 5′ LTR poly(A) site is inactivated by U1 snRNP interaction with the downstream major splice donor site. EMBO J. 16 (1997) 5752-5763
9. Ashe M.P., Furger A., and Proudfoot N.J. Stem-loop 1 of the U1 snRNP plays a critical role in the suppression of HIV-1 polyadenylation. RNA 6 (2000) 170-177
10. Asparuhova M.B., Marti G., Liu S., Serhan F., Trono D., and Schumperli D. Inhibition of HIV-1 multiplication by a modified U7 snRNA inducing Tat and Rev exon skipping. J. Gene Med. 9 (2007) 323-334
11. Benko D.M., Schwartz S., Pavlakis G.N., and Felber B.K. A novel human immunodeficiency virus type 1 protein, tev, shares sequences with tat, env, and rev proteins. J. Virol. 64 (1990) 2505-2518
12. Berro R., Kehn K., de la Fuente C., Pumfery A., Adair R., Wade J., Colberg-Poley A.M., Hiscott J., and Kashanchi F. Acetylated Tat regulates human immunodeficiency virus type 1 splicing through its interaction with the splicing regulator p32. J. Virol. 80 (2006) 3189-3204
13. Berro R., Pedati C., Kehn-Hall K., Wu W., Klase Z., Even Y., Geneviere A.M., Ammosova T., Nekhai S., and Kashanchi F. CDK13, a new potential human immunodeficiency virus type 1 inhibitory factor regulating viral mRNA splicing. J. Virol. 82 (2008) 7155-7166
14. Bilodeau P.S., Domsic J.K., and Stoltzfus C.M. Splicing regulatory elements within tat exon 2 of human immunodeficiency virus type 1 (HIV-1) are characteristic of group M but not group O HIV-1 strains. J. Virol. 73 (1999) 9764-9772
15. Bilodeau P.S., Domsic J.K., Mayeda A., Krainer A.R., and Stoltzfus C.M. 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 (2001) 8487-8497
16. Black D.L. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72 (2003) 291-336
17. Bohne J., and Krausslich H.G. Mutation of the major 5′ splice site renders a CMV-driven HIV-1 proviral clone Tat-dependent: Connections between transcription and splicing. FEBS Lett. 563 (2004) 113-118
18. Bohne J., Wodrich H., and Krausslich H.-G. Splicing of human immunodeficiency virus RNA is position-dependent suggesting sequential removal of introns from the 5′ end. Nucl. Acids Res. 33 (2005) 825-837
19. Buratti E., and Baralle F.E. Influence of RNA secondary structure on the pre-mRNA splicing process. Mol. Cell. Biol. 24 (2004) 10505-10514
20. Buratti E., Muro A.F., Giombi M., Gherbassi D., Iaconcig A., and Baralle F.E. RNA folding affects the recruitment of SR proteins by mouse and human polypurinic enhancer elements in the fibronectin EDA exon. Mol. Cell. Biol. 24 (2004) 1387-1400
21. Caputi M., and Zahler A.M. SR proteins and hnRNP H regulate the splicing of the HIV-1 tev-specific exon 6D. EMBO J. 21 (2002) 845-855
22. Caputi M., Mayeda A., Krainer A.R., and Zahler A.M. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 18 (1999) 4060-4067
23. Caputi M., Freund M., Kammler S., Asang C., and Schaal H. A bidirectional SF2/ASF- and SRp40-dependent splicing enhancer regulates HIV-1 rev, env, vpu, and nef gene expression. J. Virol. 78 (2004) 6517-6526
24. - human immunodeficiency viruses: Genetic analyses of LTR and tat mutations in primary and long-term human lymphoid cells. Virology 211 (1995) 157-169
25. Chen C.D., Kobayashi R., and Helfman D.M. Binding of hnRNP H to an exonic splicing silencer is involved in the regulation of alternative splicing of the rat β-tropomyosin gene. Genes Dev. 13 (1999) 593-606
26. Cullen B.R. Nuclear mRNA export: Insights from virology. Trends Biochem. Sci. 28 (2003) 419-424
27. Damgaard C.K., Tange T.O., and Kjems J. 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 (2002) 1401-1415
28. Damier L., Domenjoud L., and Branlant C. The D1-A2 and D2-A2 pairs of splice sites from human immunodeficiency virus type 1 are highly efficient in vitro, in spite of an unusual branch site. Biochem. Biophys. Res. Commun. 237 (1997) 182-187
29. Dehart J.L., and Planelles V. Human immunodeficiency virus type 1 Vpr links proteasomal degradation and checkpoint activation. J. Virol. 82 (2008) 1066-1072
30. DelGatto-Konczak F., Olive M., Gesnel M.-C., and Breathnach R. hnRNP A1 recruited to an exon in vivo can function as an exon splicing silencer. Mol. Cell. Biol. 19 (1999) 251-260
31. Domsic J.K., Wang Y., Mayeda A., Krainer A.R., and Stoltzfus C.M. Human immunodeficiency virus type 1 hnRNP A/B-dependent exonic splicing silencer ESSV antagonizes binding of U2AF65 to viral polypyrimidine tracts. Mol. Cell. Biol. 23 (2003) 8762-8772
32. Dowling D., Nasr-Esfahani S., Tan C.H., O'Brien K., Howard J.L., Jans D.A., Purcell D.F., Stoltzfus C.M., and Sonza S. HIV-1 infection induces changes in expression of cellular splicing factors that regulate alternative viral splicing and virus production in macrophages. Retrovirology 5 (2008) 18
33. Dyhr-Mikkelsen H., and Kjems J. Inefficient spliceosome assembly and abnormal branch site selection in splicing of an HIV-1 transcript in vitro. J. Biol. Chem. 270 (1995) 24060-24066
34. Exline C.M., Feng Z., and Stoltzfus C.M. Negative and positive mRNA splicing elements act competitively to regulate human immunodeficiency virus type 1 vif gene expression. J. Virol. 82 (2008) 3921-3931
35. Fukuhara T., Hosoya T., Shimizu S., Sumi K., Oshiro T., Yoshinaka Y., Suzuki M., Yamamoto N., Herzenberg L.A., Herzenberg L.A., and Hagiwara M. Utilization of host SR protein kinases and RNA-splicing machinery during viral replication. Proc. Natl. Acad. Sci. USA 103 (2006) 11329-11333
36. Goila-Gaur R., and Strebel K. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5 (2008) 51
37. Goodchild J., Agrawal S., Civeira M.P., Sarin P.S., Sun D., and Zamecnik P.C. Inhibition of human immunodeficiency virus replication by antisense oligodeoxynucleotides. Proc. Natl. Acad. Sci. USA 85 (1988) 5507-5511
38. Graveley B.R. Sorting out the complexity of SR protein functions. RNA 6 (2000) 1197-1211
39. Hallay H., Locker N., Ayadi L., Ropers D., Guittet E., and Branlant C. Biochemical and NMR study on the competition between proteins SC35, SRp40, and heterogeneous nuclear ribonucleoprotein A1 at the HIV-1 Tat exon 2 splicing site. J. Biol. Chem. 281 (2006) 37159-37174
40. Han K., Yeo G., An P., Burge C.B., and Grabowski P.J. A combinatorial code for splicing silencing: UAGG and GGGG motifs. PLoS Biol. 3 (2005) e158
41. Hoffman B.E., and Grabowski P.J. U1 snRNP targets an essential splicing factor, U2AF65, to the 3′ splice site by a network of interactions spanning the exon. Genes Dev. 6 (1992) 2554-2568
42. Jablonski J.A., and Caputi M. Role of cellular RNA processing factors in human immunodeficiency virus type 1 mRNA metabolism, replication, and infectivity. J. Virol. 83 (2009) 981-992
43. Jacquenet S., Mereau A., Bilodeau P.S., Damier L., Stoltzfus C.M., and Branlant C. A second exon splicing silencer within human immunodeficiency virus type 1 tat exon 2 represses splicing of Tat mRNA and binds protein hnRNP H. J. Biol. Chem. 276 (2001) 40464-40475
44. Jacquenet S., Decimo D., Muriaux D., and Darlix J.-L. Dual effect of the SR proteins ASF/SF2, SC35, and 9G8 on HIV-1 RNA splicing and virion production. Retrovirology 2 (2005) 33
45. Kammler S., Leurs C., Freund M., Krummheuer J., Seidel K., Tange T.O., Lund M.K., Kjems J., Scheid A., and Schaal H. 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 (2001) 421-434
46. Kammler S., Otte M., Hauber I., Kjems J., Hauber J., and Schaal H. The strength of the HIV-1 3′ splice sites affects Rev function. Retrovirology 3 (2006) 89
47. Karkare S., and Bhatnagar D. Promising nucleic acid analogs and mimics: Characteristic features and applications of PNA, LNA, and morpholino. Appl. Microbiol. Biotechnol. 71 (2006) 575-586
48. Kim S., Byrn R., Groopman J., and Baltimore D. Temporal aspects of DNA and RNA synthesis during human immunodeficiency virus infection: Evidence for differential gene expression. J. Virol. 63 (1989) 3708-3713
49. Klotman M.E., Kim S., Buchbinder A., DeRossi A., Baltimore D., and Wong-Staal F. Kinetics of expression of multiply spliced RNA in early human immunodeficiency virus type 1 infection of lymphocytes and monocytes. Proc. Natl. Acad. Sci. USA 88 (1991) 5011-5015
50. Kornblihtt A.R., Mata M.D.L., Fededa J.P., Munoz M.J., and Nogues G. Multiple links between transcription and splicing. RNA 10 (2004) 1489-1498
51. Krummheuer J., Lenz C., Kammler S., Scheid A., and Schaal H. Influence of the small leader exons 2 and 3 on human immunodeficiency virus type 1 gene expression. Virology 286 (2001) 276-289
52. Kuramitsu M., Hashizume C., Yamamoto N., Asuma A., Kamata M., Yamamoto N., Tanaka Y., and Aida Y. A novel role for Vpr of human immunodeficiency virus type 1 as a regulator of splicing of cellular pre-mRNA. Microbes Infect. 7 (2005) 1150-1160
53. Lever A., Gottlinger H., Haseltine W., and Sodroski J. Identification of a sequence required for efficient packaging of human immunodeficiency virus type 1 RNA into virions. J. Virol. 63 (1989) 4085-4087
54. Lu X., Heimer J., Rekosh D., and Hammarskjold M.-L. U1 small nuclear RNA plays a direct role in the formation of a rev-regulated human immunodeficiency virus env mRNA that remains unspliced. Proc. Natl. Acad. Sci. USA 87 (1990) 7598-7602
55. Lu R., Ghory H.Z., and Engelman A. Genetic analyses of conserved residues in the carboxyl-terminal domain of human immunodeficiency virus type 1 integrase. J. Virol. 79 (2005) 10356-10368
56. Luo Y., Yu H., and Peterlin B.M. Cellular protein modulates effects of human immunodeficiency virus type 1 Rev. J. Virol. 68 (1994) 3850-3856
57. Lutzelberger M., Reinert L.S., Das A.T., Berkhout B., and Kjems J. A novel splice donor site in the gag-pol gene is required for HIV-1 RNA stability. J. Biol. Chem. 281 (2006) 18644-18651
58. Madsen J.M., and Stoltzfus C.M. An exonic splicing silencer downstream of 3′ splice site A2 is required for efficient human immunodeficiency virus type 1 replication. J. Virol. 79 (2005) 10478-10486
59. Madsen J.M., and Stoltzfus C.M. A suboptimal 5′ splice site downstream of HIV-1 splice site A1 is required for unspliced viral mRNA accumulation and efficient virus replication. Retrovirology 3 (2006) 10
60. Maldarelli F., Xiang C., Chamoun G., and Zeichner S.L. The expression of the essential nuclear splicing factor SC35 is altered by human immunodeficiency virus infection. Virus Res. 53 (1998) 39-51
61. Mandal D., Feng Z., and Stoltzfus C.M. Gag-processing defect of human immunodeficiency virus type 1 integrase E246 and G247 mutants is caused by activation of an overlapping 5′ splice site. J. Virol. 82 (2008) 1600-1604
62. Mandal D., Exline C.M., Feng Z., and Stoltzfus C.M. Regulation of vif mRNA splicing by human immunodeficiency virus type 1 requires 5′ splice site D2 and an exonic splicing enhancer to counteract cellular restriction factor APOBEC3G. J. Virol. 83 (2009) 6067-6078
63. Marchand V., Mereau A., Jacquenet S., Thomas D., Mougin A., Gattoni R., Stevenin J., and Branlant C. A Janus splicing regulatory element modulates HIV-1 tat and rev mRNA production by coordination of hnRNP A1 cooperative binding. J. Mol. Biol. 323 (2002) 629-652
64. Matlin A.J., Clark F., and Smith C.W. Understanding alternative splicing: Towards a cellular code. Nat. Rev. Mol. Cell Biol. 6 (2005) 386-398
65. Mayeda A., Screaton G.R., Chandler S.D., Fu X.-D., and Krainer A.R. Substrate specificities of SR proteins in constitutive splicing are determined by their RNA recognition motifs and composite pre-mRNA exonic elements. Mol. Cell. Biol. 19 (1999) 1853-1863
66. Michael N.L., Morrow P., Mosca J., Vahey M., Burke D.S., and Redfield R.R. Induction of human immunodeficiency virus type 1 expression in chronically infected cells is associated primarily with a shift in RNA splicing patterns. J. Virol. 65 (1991) 1291-1303
67. Muesing M.A., Smith D.H., and Capon D.J. Regulation of mRNA accumulation by a human immunodeficiency virus transactivator protein. Cell 48 (1987) 691-701
68. O'Reilly M.M., McNally M.T., and Beemon K.L. Two strong 5′ splice sites and competing suboptimal 3′ splice sites involved in alternative splicing of human immunodeficiency virus type 1 RNA. Virology 213 (1995) 373-385
69. Pandit S., Wang D., and Fu X.D. Functional integration of transcriptional and RNA processing machineries. Curr. Opin. Cell Biol. 20 (2008) 260-265
70. Peng G., Lei K.J., Jin W., Greenwell-Wild T., and Wahl S.M. Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV activity. J. Exp. Med. 203 (2006) 41-46
71. Petersen-Mahrt S.K., Estmer C., Ohrmalm C., Matthews D.A., Russell W.C., and Akusjarvi G. The splicing factor-associated protein, p32, regulates RNA splicing by inhibiting ASF/SF2 RNA binding and phosphorylation. EMBO J. 18 (1999) 1014-1024
72. Pollard V.W., and Malim M.H. The HIV-1 Rev protein. Annu. Rev. Microbiol. 52 (1998) 491-532
73. Pongoski J., Asai K., and Cochrane A. Positive and negative modulation of human immunodeficiency virus type 1 Rev function by cis and trans regulators of viral RNA splicing. J. Virol. 76 (2002) 5108-5120
74. Price D.H. P-TEFb, a cyclin-dependent kinase controlling degradation by RNA polymerase II. Mol. Cell. Biol. 20 (2000) 2629-2634
75. Purcell D.F.J., and Martin M.A. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication and infectivity. J. Virol. 67 (1993) 6365-6378
76. Riggs N.L., Little S.J., Richman D.D., and Guatelli J.C. Biological importance and cooperativity of HIV-1 regulatory gene splice acceptors. Virology 202 (1994) 264-271
77. Robberson B.L., Cote G.J., and Berget S.M. Exon definition may facilitate splice site selection in RNAs with multiple exons. Mol. Cell. Biol. 10 (1990) 84-94
78. Ropers D., Ayadi L., Gattoni R., Jacquenet S., Damier L., Branlant C., and Stevenin J. Differential effects of the SR proteins 9G8, SC35, ASF/SF2, and SRp40 on the utilization of the A1 to A5 splicing sites of HIV-1 RNA. J. Biol. Chem. 279 (2004) 29963-29973
79. Rose K.M., Marin M., Kozak S.L., and Kabat D. Transcriptional regulation of APOBEC3G, a cytidine deaminase that hypermutates human immunodeficiency virus. J. Biol. Chem. 279 (2004) 41744-41749
80. Ryo A., Suzuki Y., Arai M., Kondoh N., Wakatsuki T., Hada A., Shuda M., Tanaka K., Sato C., Yamamoto M., and Yamamoto N. Identification and characterization of differentially expressed mRNAs in HIV type 1-infected human T cells. AIDS Res. Hum. Retroviruses 16 (2000) 995-1005
81. Salfeld J., Gottlinger H., Sia R., Park R., Sodroski J., and Haseltine W. A tripartite HIV-1 tat-env-rev fusion protein. EMBO J. 9 (1990) 965-970
82. Saliou J.M., Bourgeois C.F., Ayadi-Ben Mena L., Ropers D., Jacquenet S., Marchand V., Stevenin J., and Branlant C. Role of RNA structure and protein factors in the control of HIV-1 splicing. Front Biosci. 14 (2009) 2714-2729
83. Schwartz S., Felber B.K., Benko D.M., Fenyo E.-M., and Pavlakis G.N. Cloning and functional analysis of multiply spliced mRNA species of human immunodeficiency virus type 1. J. Virol. 64 (1990) 2519-2529
84. Sharp P.M., Bailes E., Chaudhuri R.R., Rodenburg C.M., Santiago M.O., and Hahn B.H. The origins of acquired immune deficiency syndrome viruses: Where and when?. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356 (2001) 867-876
85. Si Z.-H., Amendt B.A., and Stoltzfus C.M. 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. Nucl. Acids Res. 25 (1997) 861-867
86. Si Z.-H., Rauch D., and Stoltzfus C.M. 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 (1998) 5404-5413
87. Sonza S., Mutimer H.P., O'Brien K., Ellery P., Howard J.L., Axelrod J.H., Deacon N.J., Crowe S.M., and Purcell D.F. Selectively reduced tat mRNA heralds the decline in productive human immunodeficiency virus type 1 infection in monocyte-derived macrophages. J. Virol. 76 (2002) 12611-12621
88. Soret J., Bakkour N., Maire S., Durand S., Zekri L., Gabut M., Fic W., Divita G., Rivalle C., Dauzonne D., Nguyen C.H., Jeanteur P., and Tazi J. Selective modification of alternative splicing by indole derivatives that target serine-arginine-rich protein splicing factors. Proc. Natl. Acad. Sci. USA 102 (2005) 8764-8769
89. Staffa A., and Cochrane A. Identification of positive and negative splicing regulatory elements within the terminal tat/rev exon of HIV-1. Mol. Cell. Biol. 15 (1995) 4597-4605
90. Stoltzfus C.M., and Madsen J.M. Role of viral splicing elements and cellular RNA binding proteins in regulation of HIV-1 alternative RNA splicing. Curr. HIV Res. 4 (2006) 43-55
91. Stopak K.S., Chiu Y.L., Kropp J., Grant R.M., and Greene W.C. Distinct patterns of cytokine regulation of APOBEC3G expression and activity in primary lymphocytes, macrophages, and dendritic cells. J. Biol. Chem. 282 (2007) 3539-3546
92. Swanson A.K., and Stoltzfus C.M. Overlapping cis sites used for splicing of HIV-1 env/nef and rev mRNAs. J. Biol. Chem. 273 (1998) 34551-34557
93. Tange T.O., and Kjems J. SF2/ASF binds to a splicing enhancer in the third HIV-1 tat exon and stimulates U2AF binding independently of the RS domain. J. Mol. Biol. 312 (2001) 649-662
94. Tange T.O., Jensen T.H., and Kjems J. In vitro interaction between human immunodeficiency virus type 1 Rev protein and splicing factor ASF/SF2-associated protein, p32. J. Biol. Chem. 271 (1996) 10066-10072
95. Terada Y., and Yasuda Y. Human immunodeficiency virus type 1 Vpr induces G2 checkpoint activation by interacting with the splicing factor SAP145. Mol. Cell. Biol. 26 (2006) 8149-8158
96. Varani L., Hasegawa M., Spillantini M.G., Smith M.J., Murrell J.R., Ghetti B., Klug A., Goedert M., and Varani G. Structure of tau exon 10 splicing regulatory element RNA and destabilization by mutations of frontotemporal dementia and parkinsonism linked to chromosome 17. Proc. Natl. Acad. Sci. USA 96 (1999) 8229-8234
97. Wang Z., and Burge C.B. Splicing regulation: From a parts list of regulatory elements to an integrated splicing code. RNA 14 (2008) 802-813
98. Wentz M.P., Moore B.E., Cloyd M.W., Berget S.M., and Donehower L.A. A naturally arising mutation of a potential silencer of exon splicing in human immunodeficiency virus type 1 induces dominant aberrant splicing and arrests virus production. J. Virol. 71 (1997) 8542-8551
99. Zahler A.M., Damgaard C.K., Kjems J., and Caputi M. SC35 and heterogeneous nuclear ribonucleoprotein A/B proteins bind to a juxtaposed exonic splicing enhancer/exonic splicing silencer element to regulate HIV-1 tat exon 2 splicing. J. Biol. Chem. 279 (2004) 10077-10084
100. Zhang G., Zapp M.L., Yan G., and Green M.R. Localization of HIV-1 RNA in mammalian nuclei. J. Cell Biol. 135 (1996) 9-18
101. Zheng Z.-M. Regulation of alternative RNA splicing by exon definition and exon sequences in viral and mammalian gene expression. J. Biomed. Sci. 11 (2004) 278-294
102. Zheng Y.H., Yu H.F., and Peterlin B.M. Human p32 protein relieves a post-transcriptional block to HIV replication in murine cells. Nat. Cell Biol. 5 (2003) 611-618
103. Zhu J., Mayeda A., and Krainer A.R. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol. Cell 8 (2001) 1351-1361