Tra2-mediated recognition of HIV-1 5' splice site D3 as a key factor in the processing of vpr mRNA

Journal of Virology

Volumn 87, Issue 5, 2013, Pages 2721-2734

  Erkelenz, Steffen ^a   Poschmann, Gereon ^b   Theiss, Stephan ^a   Stefanski, Anja ^b   Hillebrand, Frank ^a   Otte, Marianne ^a   Stühler, Kai ^b   Schaal, Heiner ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; REGULATOR PROTEIN; SMALL NUCLEAR RNA; TRANSFORMER 2 PROTEIN; UNCLASSIFIED DRUG; VPR PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; EXON; GENETIC TRANSFECTION; HELA CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MASS SPECTROMETRY; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN ISOLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA BINDING; RNA PROCESSING; RNA SPLICING; SITE DIRECTED MUTAGENESIS;

ALTERNATIVE SPLICING; ANTIGENS, CD46; CELL LINE; HEK293 CELLS; HELA CELLS; HIV-1; HUMANS; REGULATORY SEQUENCES, NUCLEIC ACID; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA SPLICE SITES; RNA, MESSENGER; RNA, SMALL NUCLEAR; RNA, VIRAL; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84874741127     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02756-12     Document Type: Article

References (47)

1. Frankel AD, Young JA. 1998. HIV-1: fifteen proteins and an RNA. Annu. Rev. Biochem. 67:1-25.
2. Kozak M. 2002. Pushing the limits of the scanning mechanism for initiation of translation. Gene 299:1-34.
3. Anderson JL, Johnson AT, Howard JL, Purcell DF. 2007. Both linear and discontinuous ribosome scanning are used for translation initiation from bicistronic human immunodeficiency virus type 1 env mRNAs. J. Virol. 81:4664-4676.
4. Krummheuer J, Johnson AT, Hauber I, Kammler S, Anderson JL, Hauber J, Purcell DF, Schaal H. 2007. A minimal uORF within the HIV-1 vpu leader allows efficient translation initiation at the downstream env AUG. Virology 363:261-271.
5. Purcell DF, Martin MA. 1993. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J. Virol. 67:6365- 6378.
6. Stoltzfus CM. 2009. Chapter 1. Regulation of HIV-1 alternative RNA splicing and its role in virus replication. Adv. Virus Res. 74:1- 40.
7. Kim SY, Byrn R, Groopman J, Baltimore D. 1989. Temporal aspects of DNA and RNA synthesis during human immunodeficiency virus infection: evidence for differential gene expression. J. Virol. 63:3708 -3713.
8. Klotman ME, Kim S, Buchbinder A, DeRossi A, Baltimore D, Wong- Staal F. 1991. Kinetics of expression of multiply spliced RNA in early human immunodeficiency virus type 1 infection of lymphocytes and monocytes. Proc. Natl. Acad. Sci. U. S. A. 88:5011-5015.
9. Cullen BR. 1991. Regulation of human immunodeficiency virus replication. Annu. Rev. Microbiol. 45:219 -250.
10. Hoffmann D, Schwarck D, Banning C, Brenner M, Mariyanna L, Krepstakies M, Schindler M, Millar DP, Hauber J. 2012. Formation oftrans-activation competent HIV-1 Rev:RRE complexes requires the recruitment of multiple protein activation domains. PLoS One 7:e38305.
11. Bilodeau PS, Domsic JK, Mayeda A, Krainer AR, Stoltzfus CM. 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.
12. Domsic JK, Wang Y, Mayeda A, Krainer AR, Stoltzfus CM. 2003. Human immunodeficiency virus type 1 hnRNP A/B-dependent exonic splicing silencer ESSV antagonizes binding of U2AF65 to viral polypyrimidine tracts. Mol. Cell. Biol. 23:8762- 8772.
13. Madsen JM, Stoltzfus CM. 2005. An exonic splicing silencer downstream of the 3' splice site A2 is required for efficient human immunodeficiency virus type 1 replication. J. Virol. 79:10478 -10486.
14. Kammler S, Otte M, Hauber I, Kjems J, Hauber J, Schaal H. 2006. The strength of the HIV-1 3' splice sites affects Rev function. Retrovirology 3:89.
15. Tange TO, Damgaard CK, Guth S, Valcarcel J, Kjems J. 2001. The hnRNP A1 protein regulates HIV-1 tat splicing via a novel intron silencer element. EMBO J. 20:5748 -5758.
16. Caputi M, Freund M, Kammler S, Asang C, Schaal H. 2004. A bidirectional SF2/ASF- and SRp40-dependent splicing enhancer regulates human immunodeficiency virus type 1 rev, env, vpu, and nef gene expression. J. Virol. 78:6517- 6526.
17. Kammler S, Leurs C, Freund M, Krummheuer J, Seidel K, Tange TO, Lund MK, Kjems J, Scheid A, Schaal H. 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.
18. Goncalves J, Jallepalli P, Gabuzda DH. 1994. Subcellular localization of the Vif protein of human immunodeficiency virus type 1. J. Virol. 68:704- 712.
19. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98:5116 -5121.
20. Otte M. 2006. Identifizierung von cis-wirkenden Sequenzen in den alternativen HIV-1 Leaderexons und ihre funktionelle Bedeutung fÜr die Spleißregulation. Ph.D. dissertation. Heinrich-Heine-Universität, Düsseldorf, Germany.
21. Fairbrother WG, Yeh RF, Sharp PA, Burge CB. 2002. Predictive identification of exonic splicing enhancers in human genes. Science 297:1007- 1013.
22. Daoud R, Mies G, Smialowska A, Olah L, Hossmann KA, Stamm S. 2002. Ischemia induces a translocation of the splicing factor tra2-beta 1 and changes alternative splicing patterns in the brain. J. Neurosci. 22: 5889-5899.
23. Glatz DC, Rujescu D, Tang Y, Berendt FJ, Hartmann AM, Faltraco F, Rosenberg C, Hulette C, Jellinger K, Hampel H, Riederer P, Moller HJ, Andreadis A, Henkel K, Stamm S. 2006. The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and Tra2-beta1 changes in sporadic Alzheimer's disease. J. Neurochem. 96:635- 644.
24. Sciabica KS, Hertel KJ. 2006. The splicing regulators Tra and Tra2 are unusually potent activators of pre-mRNA splicing. Nucleic Acids Res. 34:6612- 6620.
25. Watermann DO, Tang Y, Zur Hausen A, Jager M, Stamm S, Stickeler E. 2006. Splicing factor Tra2-beta1 is specifically induced in breast cancer and regulates alternative splicing of the CD44 gene. Cancer Res. 66:4774- 4780.
26. Mandal D, Feng Z, Stoltzfus CM. 2010. Excessive RNA splicing and inhibition of HIV-1 replication induced by modified U1 small nuclear RNAs. J. Virol. 84:12790 -12800.
27. Asang C, Hauber I, Schaal H. 2008. Insights into the selective activation of alternatively used splice acceptors by the human immunodeficiency virus type-1 bidirectional splicing enhancer. Nucleic Acids Res. 36:1450- 1463.
28. Hoffman BE, Grabowski PJ. 1992. U1 snRNP targets an essential splicing factor, U2AF65, to the 3' splice site by a network of interactions spanning the exon. Genes Dev. 6:2554 -2568.
29. Mandal D, Exline CM, Feng Z, Stoltzfus CM. 2009. 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. 83:6067- 6078.
30. Lim SR, Hertel KJ. 2004. Commitment to splice site pairing coincides with A complex formation. Mol. Cell 15:477- 483.
31. Widera M, Erkelenz S, Hillebrand F, Krikoni A, Widera D, Kaisers W, Deenen R, Gombert M, Dellen R, Pfeiffer T, Kaltschmidt B, Münk C, Bosch V, Köhrer K, Schaal H. 2013. An intronic G run within HIV-1 intron 2 is critical for splicing regulation of vif mRNA. J. Virol. 87:2707- 2720.
32. Schneider M, Will CL, Anokhina M, Tazi J, Urlaub H, Luhrmann R. 2010. Exon definition complexes contain the tri-snRNP and can be directly converted into B-like precatalytic splicing complexes. Mol. Cell 38: 223-235.
33. Sharma S, Kohlstaedt LA, Damianov A, Rio DC, Black DL. 2008. Polypyrimidine tract binding protein controls the transition from exon definition to an intron defined spliceosome. Nat. Struct. Mol. Biol. 15: 183-191.
34. Tsuruno C, Ohe K, Kuramitsu M, Kohma T, Takahama Y, Hamaguchi Y, Hamaguchi I, Okuma K. 2011. HMGA1a is involved in specific splice site regulation of human immunodeficiency virus type 1. Biochem. Biophys. Res. Commun. 406:512-517.
35. Asang C, Erkelenz S, Schaal H. 2012. The HIV-1 major splice donor D1 is activated by splicing enhancer elements within the leader region and the p17-inhibitory sequence. Virology 432:133-145.
36. Exline CM, Feng Z, Stoltzfus CM. 2008. Negative and positive mRNA splicing elements act competitively to regulate human immunodeficiency virus type 1 vif gene expression. J. Virol. 82:3921-3931.
37. Jacquenet S, Mereau A, Bilodeau PS, Damier L, Stoltzfus CM, Branlant C. 2001. 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. 276:40464-40475.
38. Hallay H, Locker N, Ayadi L, Ropers D, Guittet E, Branlant C. 2006. 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. 281:37159 -37174.
39. Zahler AM, Damgaard CK, Kjems J, Caputi M. 2004. 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. 279:10077-10084.
40. Amendt BA, Hesslein D, Chang LJ, Stoltzfus CM. 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.
41. Caputi M, Mayeda A, Krainer AR, Zahler AM. 1999. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 18:4060-4067.
42. Si Z, Amendt BA, Stoltzfus CM. 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. Staffa A, Cochrane A. 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.
44. Amendt BA, Si ZH, Stoltzfus CM. 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.
45. Si ZH, Rauch D, Stoltzfus CM. 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.
46. Stoltzfus CM, Madsen JM. 2006. Role of viral splicing elements and cellular RNA binding proteins in regulation of HIV-1 alternative RNA splicing. Curr. HIV Res. 4:43-55.
47. Schaal H, Pfeiffer P, Klein M, Gehrmann P, Scheid A. 1993. Use of DNA end joining activity of a Xenopus laevis egg extract for construction of deletions and expression vectors for HIV-1 Tat and Rev proteins. Gene 124:275-280.