Multiple and specific mRNA processing targets for the major human hnRNP proteins

Molecular and Cellular Biology

Volumn 28, Issue 19, 2008, Pages 6033-6043

  Venables, Julian P ^a   Koh, Chu Shin ^a   Froehlich, Ulrike ^a   Lapointe, Elvy ^a   Couture, Sonia ^a   Inkel, Lyna ^a   Bramard, Anne ^a   Paquet, Éric R ^a   Watier, Valérie ^a   Durand, Mathieu ^a   Lucier, Jean François ^a   Gervais Bird, Julien ^a   Tremblay, Karine ^a   Prinos, Panagiotis ^a   Klinck, Roscoe ^a   Elela, Sherif Abou ^a   Chabot, Benoit ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN K; MESSENGER RNA; MESSENGER RNA PRECURSOR; RNA BINDING PROTEIN;

ALTERNATIVE RNA SPLICING; APOPTOSIS; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN RNA BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA PROCESSING;

ALTERNATIVE SPLICING; AMINO ACID MOTIFS; CELL LINE, TUMOR; DOWN-REGULATION; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; POLYMERASE CHAIN REACTION; RNA PRECURSORS;

EID: 52649110671     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00726-08     Document Type: Article

References (62)

1. An, P., and P. J. Grabowski. 2007. Exon silencing by UAGG motifs in response to neuronal excitation. PLoS Biol. 5:e36.
2. Auboeuf, D., E. Batsche, M. Dutertre, C. Muchardt, and B. W. O'Malley. 2007. Coregulators: transducing signal from transcription to alternative splicing. Trends Endocrinol. Metab. 18:122-129.
3. Batsche, E., M. Yaniv, and C. Muchardt. 2006. The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat. Struct. Mol. Biol. 13:22-29.
4. 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.
5. Black, D. L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annual Rev. Biochem. 72:291-336.
6. Blanchette, M., R. E. Green, S. E. Brenner, and D. C. Rio. 2005. Global analysis of positive and negative pre-mRNA splicing regulators in Drosophila. Genes Dev. 19:1306-1314.
7. Blencowe, B. J. 2006. Alternative splicing: new insights from global analyses. Cell 126:37-47.
8. Boutz, P. L., P. Stoilov, Q. Li, C. H. Lin, G. Chawla, K. Ostrow, L. Shiue, M. Ares, Jr., and D. L. Black. 2007. A posttranscriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev. 21:1636-1652.
9. 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.
10. 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.
11. 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.
12. Chabot, B., C. LeBel, S. Hutchison, F. H. Nasim, and M. J. Simard. 2003. Heterogeneous nuclear ribonucleoprotein particle A/B proteins and the control of alternative splicing of the mammalian heterogeneous nuclear ribonucleoprotein particle A1 pre-mRNA. Prog. Mol. Subcell. Biol. 31:59-88.
13. Choi, Y. D., P. J. Grabowski, P. A. Sharp, and G. Dreyfuss. 1986. Heterogeneous nuclear ribonucleoproteins: role in RNA splicing. Science 231:1534-1539.
14. Cote, J., S. Dupuis, and J. Y. Wu. 2001. Polypyrimidine track-binding protein binding downstream of caspase-2 alternative exon 9 represses its inclusion. J. Biol. Chem. 276:8535-8543.
15. Del Gatto, F., M. C. Gesnel, and R. Breathnach. 1996. The exon sequence TAGG can inhibit splicing. Nucleic Acids Res. 24:2017-2021.
16. Dobi, A., M. Szemes, C. Lee, M. Palkovits, F. Lim, A. B. Gyorgy, M. A. Mahan, and D. V. Agoston. 2006. AUF1 is expressed in the developing brain, binds to at-rich dsDNA and regulates enkephalin gene expression. J. Biol. Chem.
17. Dreyfuss, G., M. J. Matunis, S. Pinol-Roma, and C. G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
18. Expert-Bezancon, A., J. P. Le Caer, and J. Marie. 2002. Heterogeneous nuclear ribonucleoprotein (hnRNP) K is a component of an intronic splicing enhancer complex that activates the splicing of the alternative exon 6A from chicken beta-tropomyosin pre-mRNA. J. Biol. Chem. 277:16614-16623.
19. Fagnani, M., Y. Barash, J. Y. Ip, C. Misquitta, Q. Pan, A. L. Saltzman, O. Shai, L. Lee, A. Rozenhek, N. Mohammad, S. Willaime-Morawek, T. Babak, W. Zhang, T. R. Hughes, D. van der Kooy, B. J. Frey, and B. J. Blencowe. 2007. Functional coordination of alternative splicing in the mammalian central nervous system. Genome Biol. 8:R108.
20. Fededa, J. P., E. Petrillo, M. S. Gelfand, A. D. Neverov, S. Kadener, G. Nogues, F. Pelisch, F. E. Baralle, A. F. Muro, and A. R. Kornblihtt. 2005. A polar mechanism coordinates different regions of alternative splicing within a single gene. Mol. Cell 19:393-404.
21. 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.
22. Gorlach, M., C. G. Burd, and G. Dreyfuss. 1994. The determinants of RNA-binding specificity of the heterogeneous nuclear ribonucleoprotein C proteins. J. Biol. Chem. 269:23074-23078.
23. Habelhah, H., K. Shah, L. Huang, A. Ostareck-Lederer, A. L. Burlingame, K. M. Shokat, M. W. Hentze, and Z. Ronai. 2001. ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nat. Cell Biol. 3:325-330.
24. House, A. E., and K. W. Lynch. 2006. An exonic splicing silencer represses spliceosome assembly after ATP-dependent exon recognition. Nat. Struct. Mol. Biol. 13:937-944.
25. Hovhannisyan, R. H., and R. P. Carstens. 2007. Heterogeneous ribonucleoprotein m is a splicing regulatory protein that can enhance or silence splicing of alternatively spliced exons. J. Biol. Chem. 282:36265-36274.
26. Hui, J., L. H. Hung, M. Heiner, S. Schreiner, N. Neumuller, G. Reither, S. A. Haas, and A. Bindereif. 2005. Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing. EMBO J. 24:1988-1998.
27. Hui, J., K. Stangl, W. S. Lane, and A. Bindereif. 2003. HnRNP L stimulates splicing of the eNOS gene by binding to variable-length CA repeats. Nat. Struct. Biol. 10:33-37.
28. Hung, L. H., M. Heiner, J. Hui, S. Schreiner, V. Benes, and A. Bindereif. 2008. Diverse roles of hnRNP L in mammalian mRNA processing: a combined microarray and RNAi analysis. RNA 14:284-296.
29. Hutchison, S., C. LeBel, M. Blanchette, and B. Chabot. 2002. Distinct sets of adjacent heterogeneous nuclear ribonucleoprotein (hnRNP) A1/A2 binding sites control 5′ splice site selection in the hnRNP A1 mRNA precursor. J. Biol. Chem. 277:29745-29752.
30. Ishikawa, F., M. J. Matunis, G. Dreyfuss, and T. R. Cech. 1993. Nuclear proteins that bind the pre-mRNA 3′ splice site sequence r(UUAG/G) and the human telomeric DNA sequence d(TTAGGG)n. Mol. Cell. Biol. 13:4301-4310.
31. Izquierdo, J. M., N. Majos, S. Bonnal, C. Martinez, R. Castelo, R. Guigo, D. Bilbao, and J. Valcarcel. 2005. Regulation of Fas alternative splicing by antagonistic effects of TIA-1 and PTB on exon definition. Mol. Cell 19:475-484.
32. Klinck, R., A. Bramard, L. Inkel, G. Dufresne-Martin, J. Gervais-Bird, R. Madden, E. R. Paquet, C. Koh, J. P. Venables, P. Prinos, M. Jilaveanu-Pelmus, R. Wellinger, C. Rancourt, B. Chabot, and S. Abou Elela. 2008. Multiple alternative splicing markers for ovarian cancer. Cancer Res. 68:657-663.
33. Kreahling, J. M., and B. R. Graveley. 2005. The iStem, a long-range RNA secondary structure element required for efficient exon inclusion in the Drosophila Dscam pre-mRNA. Mol. Cell. Biol. 25:10251- 10260.
34. Krecic, A. M., and M. S. Swanson. 1999. hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11:363-371.
35. Laroia, G., R. Cuesta, G. Brewer, and R. J. Schneider. 1999. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284:499-502.
36. Li, C., M. Kato, L. Shiue, J. E. Shively, M. Ares, Jr., and R. J. Lin. 2006. Cell type and culture condition-dependent alternative splicing in human breast cancer cells revealed by splicing-sensitive microarrays. Cancer Res. 66:1990-1999.
37. Mahajan, M. C., G. J. Narlikar, G. Boyapaty, R. E. Kingston, and S. M. Weissman. 2005. Heterogeneous nuclear ribonucleoprotein C1/C2, MeCP1, and SWI/SNF form a chromatin remodeling complex at the beta-globin locus control region. Proc. Natl. Acad. Sci. USA 102:15012-15017.
38. Martinez-Contreras, R., P. Cloutier, L. Shkreta, J. F. Fisette, T. Revil, and B. Chabot. 2007. hnRNP proteins and splicing control, p. 123-147. In B. J. Blencowe and B. R. Graveley (ed.), Alternative splicing in the postgenomic era. Landes Bioscience, Austin, TX.
39. Martinez-Contreras, R., J. F. Fisette, F. U. Nasim, R. Madden, M. Cordeau, and B. Chabot. 2006. Intronic binding sites for hnRNP A/B and hnRNP F/H proteins stimulate pre-mRNA splicing. PLoS Biol. 4:e21.
40. Massiello, A., and C. E. Chalfant. 2006. SRp30a (ASF/SF2) regulates the alternative splicing of caspase-9 pre-mRNA and is required for ceramide-responsiveness. J. Lipid Res. 47:892-897.
41. Matlin, A. J., F. Clark, and C. W. Smith. 2005. Understanding alternative splicing: toward a cellular code. Nat. Rev. Mol. Cell. Biol. 6:386-398.
42. 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.
43. Mirza, M., E. Shaughnessy, J. K. Hurley, K. A. Vanpatten, G. A. Pestano, B. He, and G. F. Weber. 2008. Osteopontin-c is a selective marker of breast cancer. Int. J. Cancer 122:889-897.
44. Mourelatos, Z., L. Abel, J. Yong, N. Kataoka, and G. Dreyfuss. 2001. SMN interacts with a novel family of hnRNP and spliceosomal proteins. EMBO J. 20:5443-5452.
45. Nasim, M. T., T. K. Chernova, H. M. Chowdhury, B. G. Yue, and I. C. Eperon. 2003. HnRNP G and Tra2β: opposite effects on splicing matched by antagonism in RNA binding. Hum. Mol. Genet. 12:1337-1348.
46. Paradis, C., P. Cloutier, L. Shkreta, J. Toutant, K. Klarskov, and B. Chabot. 2007. hnRNP I/PTB can antagonize the splicing repressor activity of SRp30c. RNA. 13:1287-1300.
47. Park, J. W., K. Parisky, A. M. Celotto, R. A. Reenan, and B. R. Graveley. 2004. Identification of alternative splicing regulators by RNA interference in Drosophila. Proc. Natl. Acad. Sci. USA
48. Paronetto, M. P., T. Achsel, A. Massiello, C. E. Chalfant, and C. Sette. 2007. The RNA-binding protein Sam68 modulates the alternative splicing of Bcl-x. J. Cell Biol. 176:929-939.
49. Patry, C., L. Bouchard, P. Labrecque, D. Gendron, B. Lemieux, J. Toutant, E. Lapointe, R. Wellinger, and B. Chabot. 2003. Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparticule A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines. Cancer Res. 63:7679-7688.
50. Revil, T., J. Toutant, L. Shkreta, D. Garneau, P. Cloutier, and B. Chabot. 2007. Protein kinase C-dependent control of Bcl-x alternative splicing. Mol. Cell. Biol. 27:8431-8441.
51. Schwerk, C., and K. Schulze-Osthoff. 2005. Regulation of apoptosis by alternative pre-mRNA splicing. Mol. Cell 19:1-13.
52. Sierakowska, H., W. Szer, P. J. Furdon, and R. Kole. 1986. Antibodies to hnRNP core proteins inhibit in vitro splicing of human beta-globin pre-mRNA. Nucleic Acids Res. 14:5241-5254.
53. Singh, R., and J. Valcarcel. 2005. Building specificity with nonspecific RNA-binding proteins. Nat. Struct. Mol. Biol. 12:645-653.
54. 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.
55. Thisted, T., D. L. Lyakhov, and S. A. Liebhaber. 2001. Optimized RNA targets of two closely related triple KH domain proteins, heterogeneous nuclear ribonucleoprotein K and αCP-2KL, suggest distinct modes of RNA recognition. J. Biol. Chem. 276:17484-17496.
56. Ule, J., G. Stefani, A. Mele, M. Ruggiu, X. Wang, B. Taneri, T. Gaasterland, B. J. Blencowe, and R. B. Darnell. 2006. An RNA map predicting Nova-dependent splicing regulation. Nature 444:580-586.
57. Ule, J., A. Ule, J. Spencer, A. Williams, J. S. Hu, M. Cline, H. Wang, T. Clark, C. Fraser, M. Ruggiu, B. R. Zeeberg, D. Kane, J. N. Weinstein, J. Blume, and R. B. Darnell. 2005. Nova regulates brain-specific splicing to shape the synapse. Nat. Genet. 37:844-852.
58. van der Houven van Oordt, W., M. T. Diaz-Meco, J. Lozano, A. R. Krainer, J. Moscat, and J. F. Caceres. 2000. The MKK(3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J. Cell Biol. 149:307-316.
59. Wagner, E. J., and M. A. Garcia-Blanco. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol. 21:3281-3288.
60. Wang, J., Q. S. Gao, Y. Wang, R. Lafyatis, S. Stamm, and A. Andreadis. 2004. Tau exon 10, whose missplicing causes frontotemporal dementia, is regulated by an intricate interplay of cis elements and trans factors. J. Neurochem. 88:1078-1090.
61. 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.
62. Xu, N., C. Y. Chen, and A. B. Shyu. 2001. Versatile role for hnRNP D isoforms in the differential regulation of cytoplasmic mRNA turnover. Mol. Cell. Biol. 21:6960-6971.