Novel exploitation of a nuclear function by influenza virus: The cellular SF2/ASF splicing factor controls the amount of the essential viral M2 ion channel protein in infected cells

EMBO Journal

Volumn 15, Issue 19, 1996, Pages 5415-5427

  Shih, Shin Ru ^a,b   Krug, Robert M ^a  

^a RUTGERS UNIVERSITY   (United States)

^b Chang Jung Coll Med and Technol   (Taiwan)

Author keywords

Alternative splicing; Influenza virus; M2 ion channel protein; SF2 (ASF) splicing factor; Splicing enhancer sequence

Indexed keywords

ION CHANNEL; MEMBRANE PROTEIN; MESSENGER RNA; NUCLEAR PROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL NUCLEUS; HUMAN; HUMAN CELL; INFLUENZA; INFLUENZA VIRUS; PRIORITY JOURNAL; RNA SPLICING;

HUMAN INFLUENZA VIRUS; INFLUENZA VIRUS;

EID: 0029815612     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00925.x     Document Type: Article

References (52)

1. Alonso-Caplen, F.V., Nemeroff, M.E., Qiu, Y. and Krug, R.M. (1992) Nuclear-cytoplasmic transport: the influenza virus NS1 protein regulates the transport of spliced NS2 mRNA and its precursor NS1 mRNA. Genes Dev., 6, 255-267.
2. Amerin, H., Hedley, M.L. and Maniatis, T. (1994) The role of specific protein-RNA and protein-protein interactions in positive and negative control of pre-mRNA splicing by transformer 2. Cell, 76, 735-746.
3. Birney, E., Kumar, S. and Krainer, A.R. (1993) Analysis of the RNA recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res., 21, 5803-5816.
4. Bogerd, H.P., Fridell, R.A., Madore, S. and Cullen, B.R. (1995) Identification of a novel cellular cofactor for the Rev/Rex class of retroviral regulatory proteins. Cell, 82, 485-494.
5. Dirksen, W.P., Sun, Q. and Rottman, F.M. (1995) Multiple splicing signals control alternative intron retention of bovine growth hormone pre-mRNA. J. Biol Chem., 270, 5346-5352.
6. Eperon, I.C., Ireland, D.C., Smith, R.A., Mayeda, A. and Krainer, A.R. (1993) Pathways for selection of 5′ splice sites by U1 snRNPs and SF2/ASF. EMBO J., 12, 3607-3617.
7. Felber, B.K., Hadzopoulou-Cladaras, M., Cladaras, C., Copeland, T. and Pavlakis, G.N. (1989) Rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc. Natl Acad. Sci. USA, 86, 1495-1499.
8. Fortes, P., Beloso, A. and Ortin, J. (1994) Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J., 13, 704-714.
9. Fritz, C.C., Zapp, M.L. and Green, M.R. (1995) A human nucleoporin-like protein that specifically interacts with HIV Rev. Nature, 376, 530-533.
10. Fu, X.D. (1993) Specific commitment of different pre-mRNAs to splicing by single SR proteins. Nature, 365, 82-85.
11. Fu, X.D. (1995) The superfamily of arginine/serine-rich splicing factors. RNA, 1, 663-680.
12. Ge, H. and Manley, J.L. (1990) A protein factor, ASF, controls cell-specific alternative splicing of SV40 early pre-mRNA in vitro. Cell, 62, 25-34.
13. Ge, H., Zuo, P. and Manley, J.L. (1991) Primary structure of human splicing factor ASF reveals similarities with Drosophila regulators. Cell, 66, 373-382.
14. Hadzopoulou-Caldaras, M., Felber, B.K., Cladaras, C., Athahassopoulos, A., Tse, A. and Pavlakis, G.N. (1989) The rev (trs/art) protein of human immunodeficiency virus type 1 affects viral mRNA and protein expression via a cis-acting sequence in the env region. J. Virol., 63, 1265-1274.
15. Himmelspach, M., Cavaloc, Y., Chebli, K. Stevenin J. and Gattoni, R. (1995) Titration of serine/arginine (SR) splicing factors during adenoviral infection mudulates E1A pre-mRNA alternative splicing. RNA, 8, 794-806.
16. Holsinger, L.J. and Lamb, R.A. (1991) Influenza virus M2 integral membrane protein is a homotetramer stablized by formation of disulfide bonds. Virology, 183, 32-43.
17. Hughey, P.G., Roberts, P.C., Holsinger, L.J., Zebedee, S.L., Lamb, R.A. and Compans, R.W. (1995) Effects of antibody to the influenza A virus M2 protein on M2 surface expression and assembly. Virology, 212, 411-421.
18. Inglis, S.C. and Brown, C.M. (1984) Differences in the control of virus RNA splicing during permissive or abortive infection with influenza (Fowl Plaque) virus. J. Gen. Virol., 65, 153-164.
19. Inoue, K., Hoshijima, K., Sakamoto, H. and Shimura, Y. (1990) Binding of the Drosophila sex-lethal gene product to the alternative splice site of transformer primary transcript. Nature, 344, 461-463.
20. Kohtz, J.D., Jamison, S.F., Will, C.L., Zuo, P., Luhrmann, R., Garcia-Blanco, M.A. and Manley, J.L. (1994) Protein-protein interactions and 5′ splice site recognition in mammalian mRNA precursors. Nature, 368, 119-124.
21. Krainer, A.R., Conway, G.C. and Kozak, D. (1990a) Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev., 4, 1158-1171.
22. Krainer, A.R., Conway, G.C. and Kozak, D. (1990b) The essential pre-mRNA splicing factor SF2 influences 5′ splice site selection by activating proximal sites. Cell, 62, 35-42.
23. Krainer, A.R., Mayeda, A., Kozak, D. and Binns, G. (1991) Functional expression of cloned human splicing factor SF2 : homology to RNA-binding proteins, U1-70K, and Drosophila splicing regulators. Cell, 66, 383-394.
24. Krug, R.M., Alonso-Caplen, F.V., Julkunen, I. and Katze, M. (1989) Expression and replication of the influenza virus genome. In Krug, R.M. (ed), The Influenza Viruses. Plenum Press, New York, pp. 89-152.
25. Lamb, R.A. and Lai, C.J. (1982) Spliced and unspliced messenger RNAs synthesized from cloned influenza virus M DNA in an SV40 vector: expression of the influenza virus membrane protein (M1). Virology, 123, 237-256.
26. Lamb, R.A., Zebedee, S.L. and Richardson, C.D. (1985) Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell, 40, 627-633.
27. Lau, S.C. and Scholtissek, C. (1995) Abortive infection of Vero cells by an influenza A virus (FPV). Virology, 212, 225-231.
28. Lavigueur, A., Branche, H.L., Kornblihtt, A.R. and Chabot, B. (1993) A splicing enhancer in the human fibronectin alternate ED1 exon interacts with SR proteins and stimulates U2 snRNP binding. Genes Dev., 7, 2405-2417.
29. Malim, M.H., Hauber, J., Le, S.-Y., Maizel, J.V. and Cullen, B.R. (1989a) The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature, 338, 254-257.
30. Malim, M.H., Bohnlein, S., Hauber, J. and Cullen, B.R. (1989b) Functional dissection of the HIV-1 Rev trans-activator: derivation of of a trans-dominant repressor of Rev function. Cell, 58, 205-214.
31. Nemeroff, M.E., Utans, U., Kramer, A. and Krug, R.M. (1992) Identification of cis-acting intron and exon regions in influenza virus NS1 mRNA that inhibit splicing and cause the formation of aberrantly sedimenting presplicing complexes. Mol. Cell. Biol., 2, 962-970.
32. Noonan, K.E. et al. (1990) Quantitative analysis of MDR1 (multidrug resistance) gene expression in human tumors by polymerase chain reaction. Proc. Natl Acad. Sci. USA, 87, 7160-7164.
33. O'Reilly, M.M., McNally, M.T. and Beemon, K.L. (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.
34. Pinto, L.H., Holsinger, L.J. and Lamb, R.A. (1992) Influenza virus M2 protein has ion channel activity. Cell, 69, 517-528.
35. Qian, X.Y., Alonso-Caplen, F. and Krug, R.M. (1994) Two functional domains of the influenza virus NS1 protein are required for regulation of nuclear export of mRNA. J. Virol., 68, 2433-2441.
36. Qiu, Y. and Krug, R.M. (1994) The influenza virus NS1 protein is a poly(A)-binding protein that inhibits nuclear export of mRNAs containing poly(A). J. Virol., 68, 2425-2432.
37. Salomon, R.N., Underwood, R., Doyle, M., Wang, A. and Libby, P. (1992) Increased apolipoprotein E and c-fms fene expression without elevated interleukin 1 or 6 mRNA levels indicated selective activation of macrophage functions in advanced human atheroma. Proc. Natl Acad. Sci. USA, 89, 2814-2818.
38. Shih, S.R., Nemeroff, M.E. and Krug, R.M. (1995) The choice of alternative 5′ splice sites in influenza virus M1 mRNA is regulated by the viral polymerase complex. Proc. Natl Acad. Sci. USA, 92, 6324-6328.
39. SosnoOlki, B.A., Belote, J.M. and McKeown, M. (1989) Sex-specific alternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage. Cell, 58, 449-459.
40. Staknis, D. and Reed, R. (1994) SR proteins promote the first specific recognition of pre-mRNA and are present together with the U1 small nuclear ribonucleoprotein particle in a general splicing enhancer complex. Mol. Cell. Biol., 14, 7670-7682.
41. Stutz, F., Neville, M. and Rosbash, M. (1995) Identification of a novel nuclear pore-associated protein as a functional target of the HIV-1 rev protein in yeast. Cell, 82, 495-506.
42. Sun, Q., Mayeda, A., Hampson, R.K., Krainer, A.R. and Rottman, F.M. (1993a) General splicing factor SF2/ASF promotes alternative splicing by binding to an exonic splicing enhancer. Genes Dev., 7, 2598-2608.
43. Sun, Q., Hampson, P.K. and Rottman, F.M. (1993b) In vitro analysis of bovine growth hormone pre-mRNA splicing : involvement of exon sequence and transacting factor(s). J. Biol. Chem., 268, 15659-15666.
44. Tacke, R. and Manley, J. (1995) The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities. EMBO J., 14, 3540-3551.
45. Tian, M. and Maniatis, T. (1993) A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell, 74, 105-114.
46. Valcarcel, J., Singh, R., Zamore, P.D. and Green, M.R. (1993) The protein sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature, 362, 171-175.
47. Wu, J. and Maniatis, T. (1993) Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell, 75, 1061-1070.
48. Zahler, A.M. and Roth, M.B. (1995) Distinct functions of SR proteins in recruitment of U1 small nuclear ribonucleoprotein to alternative 5′ splice sites. Proc. Natl Acad. Sci. USA, 92, 2642-2646.
49. Zahler, A.M., Lane, W.S., Stolk, J.A.S. and Roth, M.B. (1992) SR proteins : a conserved family of pre-mRNA splicing factors. Genes Dev., 6, 837-847.
50. Zahler, A.M., Neugebauer, K.M., Lane, W.S. and Roth, M.B. (1993) Distinct functions of SR proteins in alternative pre-mRNA splicing. Science, 260, 219-222.
51. Zebedee, S.L. and Lamb, R.A. (1988) Influenza A virus M2 protein: Monoclonal antibody restriction of virus growth and detection of M2 in virions. J. Virol., 62, 2762-2772.
52. Zuo, P. and Manley, J.L. (1994) The human splicing factor ASF/SF2 can specifically recognize pre-mRNA 5′ splice sites. Proc. Natl Acad. Sci. USA, 91, 3363-3367.