Activation of α-tropomyosin exon 2 is regulated by the SR protein 9G8 and heterogeneous nuclear ribonucleoproteins H and F

Molecular and Cellular Biology

Volumn 26, Issue 23, 2006, Pages 8791-8802

  Crawford, J Barrett ^a   Patton, James G ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TROPOMYOSIN; ARGININE; CIS ACTING ELEMENT; DIPEPTIDE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; PROTEIN; PROTEIN 9G8; PROTEIN SR; PURINE; PYRIMIDINE; SERINE; SMALL INTERFERING RNA; TROPONE DERIVATIVE; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; CELL TYPE; CONTROLLED STUDY; CROSS LINKING; CROSS LINKING COMPETITION ASSAY; DNA FLANKING REGION; ENHANCER REGION; EXON; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RNA AFFINITY CHROMATOGRAPHY; RNA SPLICING; SMOOTH MUSCLE FIBER; TISSUE SPECIFICITY;

ALTERNATIVE SPLICING; CELL LINE; EXONS; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP F-H; HUMANS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RNA-BINDING PROTEINS; TROPOMYOSIN;

EID: 33845213293     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01677-06     Document Type: Article

References (83)

1. Allerson, C. R., A. Martinez, E. Yikilmaz, and T. A. Rouault. 2003. A high capacity RNA affinity column for the purification of human IRP1 and IRP2 overexpressed in Pichia pastoris. RNA 9:364-374.
2. Black, D. L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72:291-336.
3. Black, D. L., and P. J. Grabowski. 2003. Alternative pre-mRNA splicing and neuronal function. Prog. Mol. Subcell. Biol. 31:187-216.
4. Buratti, E., M. Baralle, L. De Conti, D. Baralle, M. Romano, Y. M. Ayala, and F. E. Baralle. 2004. hnRNP H binding at the 5′ splice site correlates with the pathological effect of two intronic mutations in the NF-1 and TSH-β genes. Nucleic Acids Res. 32:4224-4236.
5. Buvoli, M., S. A. Mayer, and J. G. Patton. 1997. Functional crosstalk between exon enhancers, polypyrimidine tracts, and branchpoint sequences. EMBO J. 16:7174-7183.
6. 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.
7. Caputi, M., and A. M. Zahler. 2001. Determination of the RNA binding specificity of the heterogeneous nuclear ribonucleoprotein (hnRNP) H/H′/ F/2H9 family. J. Biol. Chem. 276:43850-43859.
8. Caputi, M., and A. M. Zahler. 2002. SR proteins and hnRNP H regulate the splicing of the HIV-1 tev-specific exon 6D. EMBO J. 21:845-855.
9. Cartegni, L., S. Chew, and A. Krainer. 2002. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Gen. 3:285-298.
10. Charlet-B, N., P. Logan, G. Singh, and T. A. Cooper. 2002. Dynamic antagonism between ETR-3 and PTB regulates cell type-specific alternative splicing. Mol. Cell 9:649-658.
11. Chen, C. D., R. Kobayashi, and D. M. Helfman. 1999. Binding of hnRNP H to an exonic splicing enhancer is involved in the regulation of alternative splicing of the rat β-tropomyosin gene. Genes Dev. 13:593-606.
12. Chou, M.-Y., N. Rooke, C. W. Turck, and D. L. Black. 1999. hnRNP H is a component of a splicing enhancer complex that activates a c-src alternative exon in neuronal cells. Mol. Cell. Biol. 19:69-77.
13. Conway, G., J. Wooley, T. Bibring, and W. LeStourgeon. 1988. Ribonucleoproteins package 700 nucleotides of pre-mRNA into a repeating array of regular particles. Mol. Cell. Biol. 8:2884-2895.
14. Cooley, B. C., and G. Bergtrom. 2001. Multiple combinations of alternatively spliced exons in rat tropomyosin-alpha gene mRNA: evidence for 20 new isoforms in adult tissues and cultured cells. Arch. Biochem. Biophys. 390:71-77.
15. Cáceres, J. F., S. Stamm, D. M. Helfman, and A. R. Krainer. 1994. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265:1706-1708.
16. Dansithong, W., S. Paul, L. Comai, and S. Reddy. 2005. MBNL1 is the primary determinant of focus formation and aberrant insulin receptor splicing in DM1. J. Biol. Chem. 280:5773-5780.
17. Del Gatto-Konczak, F., C. F. Bourgeois, C. Le Guiner, L. Kister, M. C. Gesnel, J. Stevenin, and R. Breathnach. 2000. The RNA-binding protein TIA-1 is a novel mammalian splicing regulator acting through intron sequences adjacent to a 5′ splice site. Mol. Cell. Biol. 20:6287-6299.
18. Del Gatto-Konczak, F., M. Olive, M.-C. Gesnel, and R. Breathnach. 1999. hnRNP A1 recruited to an exon in vivo can function as an exon splicing silencer. Mol. Cell. Biol. 19:251-260.
19. Domsic, J. K., Y. Wang, A. Mayeda, A. R. Krainer, and C. M. Stoltzfus. 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.
20. Dye, B. T., M. Buvoli, S. A. Mayer, C.-H. Lin, and J. G. Patton. 1998. Enhancer elements activate the weak 3′ splice site of α-tropomyosin exon 2. RNA 4:1523-1536.
21. Ellis, P. D., C. W. Smith, and P. Kemp. 2004. Regulated tissue-specific alternative splicing of enhanced green fluorescent protein transgenes conferred by α-tropomyosin regulatory elements in transgenic mice. J. Biol. Chem. 279:36660-36669.
22. Eperon, I. C., O. V. Makarova, A. Mayeda, S. H. Munroe, J. F. Caceres, D. G. Hayward, and A. R. Krainer. 2000. Selection of alternative 5′ splice sites: role of U1 snRNP and models for the antagonistic effects of SF2/ASF and hnRNP A1. Mol. Cell. Biol. 20:8303-8318.
23. Fairbrother, W. G., R. F. Yeh, P. A. Sharp, and C. B. Burge. 2002. Predictive identification of exonic splicing enhancers in human genes. Science 297:1007-1013.
24. Forch, P., O. Puig, N. Kedersha, C. Martinez, S. Granneman, B. Seraphin, P. Anderson, and J. Valcarcel. 2000. The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing. Mol. Cell 6:1089-1098.
25. Fu, X.-D. 1995. The superfamily of arginine/serine-rich splicing factors. RNA 1:663-680.
26. Garneau, D., T. Revil, J. F. Fisette, and B. Chabot. 2005. Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J. Biol. Chem. 280:22641-22650.
27. Gooding, C., G. C. Roberts, G. Moreau, B. Nadal-Ginard, and C. W. J. Smith. 1994. Smooth muscle specific switching of α-tropomyosin mutually exclusive exon selection by specific inhibition of the strong default exon. EMBO J. 13:3861-3872.
28. Gooding, C., G. C. Roberts, and C. W. J. Smith. 1998. Role of an inhibitory pyrimidine element and polypyrimidine tract binding protein in repression of a regulated α-tropomyosin exon. RNA 4:85-100.
29. Goodwin, L. O., J. P. Lees-Miller, M. A. Leonard, S. B. Cheley, and D. M. Helfman. 1991. Four fibroblast tropomyosin isoforms are expressed from the rat α-tropomyosin gene via alternative RNA splicing and the use of two promoters. J. Biol. Chem. 266:8408-8415.
30. Graveley, B. R. 2001. Alternative splicing: increasing diversity in the proteomic world. Trends Genet. 17:100-107.
31. Graveley, B. R. 2000. Sorting out the complexity of SR protein functions. RNA 6:1197-1211.
32. Gromak, N., A. Rideau, J. Southby, A. Scadden, C. Gooding, S. Huttelmaier, R. Singer, and C. Smith. 2003. The PTB interacting protein raver1 regulates α-tropomyosin alternative splicing. EMBO J. 22:6356-6364.
33. Gromak, N., and C. W. Smith. 2002. A splicing silencer that regulates smooth muscle specific alternative splicing is active in multiple cell types. Nucleic Acids Res. 30:3548-3557.
34. Hamon, S., C. Le Sommer, A. Mereau, M. R. Allo, and S. Hardy. 2004. Polypyrimidine tract-binding protein is involved in vivo in repression of a composite internal/3′-terminal exon of the Xenopus α-tropomyosin Pre-mRNA. J. Biol. Chem. 279:22166-22175.
35. Ho, T. H., B. N. Charlet, M. G. Poulos, G. Singh, M. S. Swanson, and T. A. Cooper. 2004. Muscleblind proteins regulate alternative splicing. EMBO J. 23:3103-3112.
36. Honore, B., U. Baandrup, and H. Vorum. 2004. Heterogeneous nuclear ribonucleoproteins F and H/H′ show differential expression in normal and selected cancer tissues. Exp. Cell Res. 294:199-209.
37. Huang, Y., and J. A. Steitz, 2005. SRprises along a messenger's journey. Mol. Cell 17:613-615.
38. Huang, Y., T. A. Yario, and J. A. Steitz. 2004. A molecular link between SR protein dephosphorylation and mRNA export. Proc. Natl. Acad. Sci. USA 101:9666-9670.
39. Jensen, K. B., B. K. Dredge, G. Stefani, R. Zhong, R. J. Buckanovich, H. J. Okano, Y. Y. L. Yang, and R. B. Darnell. 2000. Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25:359-371.
40. Jiang, Z.-H., W. J. Zhang, Y. Rao, and J. Y. Wu. 1998. Regulation of Ich-1 pre-mRNA alternative splicing and apoptosis by mammalian splicing factors. Proc. Natl. Acad. Sci. USA 95:9155-9160.
41. Jin, Y., H. Suzuki, S. Maegawa, H. Endo, S. Sugano, K. Hashimoto, K. Yasuda, and K. Inoue. 2003. A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG. EMBO J. 22:905-912.
42. Johnson, J., J. Castle, P. Garrett-Engele, Z. Kan, P. Loerch, C. Armour, R. Santos, E. Schadt, R. Stoughton, and D. Shoemaker. 2003. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302:2141-2144.
43. Kashima, T., and J. L. Manley. 2003. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat. Genet. 34:460-463.
44. Krecic, A. M., and M. S. Swanson. 1999. hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11:363-371.
45. Ladd, A. N., N. Charlet, and T. A. Cooper. 2001. The CELF family of RNA binding proteins is implicated in cell-specific and developmentally regulated alternative splicing. Mol. Cell. Biol. 21:1285-1296.
46. Lai, M. C., and W. Y. Tarn. 2004. Hypophosphorylated ASF/SF2 binds TAP and is present in messenger ribonucleoproteins. J. Biol. Chem. 279:31745-31749.
47. Lam, B. J., A. Bakshi, F. Y. Ekinci, J. Webb, B. R. Graveley, and K. J. Hertel. 2003. Enhancer-dependent 5′-splice site control of fruitless pre-mRNA splicing. J. Biol. Chem. 278:22740-22747.
48. Lam, B. J., and K. J. Hertel. 2002. A general role for splicing enhancers in exon definition. RNA 8:1233-1241.
49. Lin, C.-H., and J. G. Patton. 1995. Regulation of alternative 3′ splice site selection by constitutive splicing factors. RNA 1:234-245.
50. Lin, S., R Xiao, P. Sun, X. Xu, and X. D. Fu. 2005. Dephosphorylation- dependent sorting of SR splicing factors during mRNP maturation. Mol. Cell 20:413-425.
51. Liu, J., S. Beqaj, Y. Yang, B. Honore, and L. Schuger. 2001. Heterogeneous nuclear ribonucleoprotein-H plays a suppressive role in visceral myogenesis. Mech. Dev. 104:79-87.
52. Lynch, K. W., and T. Maniatis. 1996. Assembly of specific SR protein complexes on distinct regulatory elements of the Drosophila doublesex splicing enhancer. Genes Dev. 10:2089-2101.
53. Markovtsov, V., J. M. Nikolic, J. A. Goldman, C. W. Turck, M.-Y. Chou, and D. L. Black. 2000. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol. Cell. Biol. 20:7463-7479.
54. Matlin, A., F. Clark, and C. Smith. 2005. Understanding alternative splicing: toward a cellular code. Nat. Rev. Mol. Cell. Biol. 6:386-398.
55. Matunis, M. J., J. Xing, and G. Dreyfuss. 1994. The hnRNP F protein: unique primary structure, nucleic acid-binding properties, and subcellular localization. Nucleic Acids Res. 22:1059-1067.
56. Mayeda, A., and A. R. Krainer. 1992. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68:365-375.
57. Min, H., R. C. Chan, and D. L. Black. 1995. The generally expressed hnRNP F is involved in a neural-specific pre-mRNA splicing event. Genes Dev. 9:2659-2671.
58. Mullen, M. P., C. W. J. Smith, J. G. Patton, and B. Nadal-Ginard. 1991. α-Tropomyosin mutually exclusive exon selection: competition between branch point/polypyrimidine tracts determines exon choice. Genes Dev. 5:642-655.
59. Patton, J. G., S. A. Mayer, P. Tempst, and B. Nadal-Ginard. 1991. Characterization and molecular cloning of polypyrimidine tract binding protein: a component of a complex necessary for pre-mRNA splicing. Genes Dev. 5:1237-1251.
60. Patton, J. G., E. B. Porro, J. Galceran, P. Tempst, and B. Nadal-Ginard. 1993. Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev. 7:393-406.
61. Polydorides, A. D., H. J. Okano, Y. Y. L. Yang, G. Stefani, and R. B. Darnell. 2000. A brain-enriched polypyrimidine tract-binding protein antagonizes the ability of Nova to regulate neuron-specific alternative splicing. Proc. Natl. Acad. Sci. USA 97:6350-6355.
62. Pérez, I., C.-H. Lin, J. G. McAfee, and J. G. Patton. 1997. Mutation of PTB binding sites causes misregulation of α-tropomyosin alternative 3′ splice site selection in vivo. RNA 3:764-778.
63. Reuter, S. M., C. M. Burns, S. A. Coode, P. Mookherjee, and R. B. Emeson. 1995. Glutamate receptor RNA editing by enzymatic conversion of adenosine to inosine. Science 267:1491-1494.
64. Robberson, B. L., G. Cote, and S. M. Berget. 1990. Exon definition may facilitate splice site selection in RNAs with multiple exons. Mol. Cell. Biol. 10:84-94.
65. Rooke, N., V. Markovtsov, E. Cagavi, and D. L. Black. 2003. Roles for SR proteins and hnRNP A1 in the regulation of c-src exon N1. Mol. Cell. Biol. 23:1874-1884.
66. Rothman, A., T. J. Kulik, M. B. Taubman, B. C. Berk, C. W. J. Smith, and B. Nadal-Ginard. 1992. Characterization of a newly established rat pulmonary arterial smooth muscle cell line. Circulation 86:1977-1986.
67. Smith, C. W. J., and B. Nadal-Ginard. 1989. Mutually exclusive splicing of α-tropomyosin exons enforced by an unusual lariat branch point location; implications for constitutive splicing. Cell 56:749-758.
68. Spellman, R., A. Rideau, A. Matlin, C. Gooding, F. Robinson, N. McGlincy, S. N. Grellscheid, J. Southby, M. Wollerton, and C. W. Smith. 2005. Regulation of alternative splicing by PTB and associated factors. Biochem. Soc. Trans. 33:457-460.
69. Spellman, R., and C. W. Smith. 2006. Novel modes of splicing repression by PTB. Trends Biochem. Sci. 31:73-76.
70. Tian, M., and T. Maniatis. 1992, Positive control of pre-mRNA splicing in vitro. Science 256:237-240.
71. Wagner, E. J., and M. A. Garcia-Blanco. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol. 21:3281-3288.
72. Wang, J., P. J. Smith, A. R. Krainer, and M. Q. Zhang. 2005. Distribution of SR protein exonic splicing enhancer motifs in human protein-coding genes. Nucleic Acids Res. 33:5053-5062.
73. Wang, Z., M. E. Rolish, G. Yeo, V. Tung, M. Mawson, and C. B. Burge. 2004. Systematic identification and analysis of exonic splicing silencers. Cell 119:831-845.
74. Weighardt, F., G. Biamonti, and S. Riva. 1996. The roles of heterogeneous nuclear ribonucleoproteins (hnRNP) in RNA metabolism. Bioessays 18:747-756.
75. Wieczorek, D., C. W. J. Smith, and B. Nadal-Ginard. 1988. The rat α-tropomyosin gene generates a minimum of six different mRNAs coding for striated, smooth, and non-muscle isoforms by alternative splicing. Mol. Cell. Biol. 8:679-694.
76. Wollerton, M. C., C. Gooding, F. Robinson, E. C. Brown, R. J. Jackson, and C. W. J. Smith. 2001. Differential alternative splicing activity of isoforms of polypyrimidine tract binding protein (PTB). RNA 7:819-832.
77. Wollerton, M. C., C. Gooding, E. J. Wagner, M. A. Garcia-Blanco, and C. W. Smith. 2004. Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol. Cell 13:91-100.
78. Wu, J. Y., and T. Maniatis. 1993. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75:1061-1070.
79. Xie, J., J. A. Lee, T. L. Kress, K. L. Mowry, and D. L. Black. 2003. Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein. Proc. Natl. Acad. Sci. USA 100:8776-8781.
80. Yamamoto, H., K. Tsukahara, Y. Kanaoka, S. Jinno, and H. Okayama. 1999. Isolation of a mammalian homologue of a fission yeast differentiation regulator. Mol. Cell. Biol. 19:3829-3841.
81. Zahler, A. M., C. K. Damgaard, J. Kjems, and M. Caputi. 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.
82. Zahler, A. M., W. S. Lane, J. A. Stolk, and M. B. Roth. 1992. SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev. 6:837-847.
83. 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.