Arginine methylation facilitates the nuclear export of hnRNP proteins

Genes and Development

Volumn 12, Issue 5, 1998, Pages 679-691

  Shen, Elisa C ^a   Henry, Michael F ^a,b   Weiss, Valerie H ^a   Valentini, Sandro R ^a   Silver, Pamela A ^a   Lee, Margaret S ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

Arginine methylation; CBP80; Heterogeneous ribonucleoprotein (hnRNP); HMT1; HRP1; mRNA export; NPL3

Indexed keywords

RIBONUCLEOPROTEIN;

ARTICLE; CELL NUCLEUS; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN TRANSPORT; RNA PROCESSING; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 0032030939     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.5.679     Document Type: Article

References (60)

1. +, which encodes a 115-kD protein preferentially localized in the nucleus and its periphery. J. Cell Biol. 108: 1195-1207.
2. Baudin, A., O. Ozier-Kalogeropoulou, A. Denouel, F. Lacroute, and C. Cullin. 1993. A simple and efficient method of direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids. Res. 21: 3329-3330.
3. Beyer, A.L., M.E. Christensen, B.W. Walker, and W.M. LeStourgeon. 1977. Identification and characterization of the packaging proteins of core 40S hnRNP particles. Cell 11: 127-138.
4. Birney, E., S. Kumar, and A.R. Krainer. 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.
5. G-dimethylarginine in nuclear protein fractions. Biochem. Biophys. Res. Commun. 74: 969-976.
6. Bossie, M.A., C. DeHoratius, G. Barcelo, and P. Silver. 1992. A mutant nuclear protein with similarity to RNA binding proteins interferes with nuclear import in yeast. Mol. Biol. Cell 3: 875-893.
7. Calnan, B.J., B. Tidor, S. Biancalana, D. Hudson, and A.D. Frankel. 1991. Arginine-mediated RNA recognition: The arginine fork. Science 252: 1167-1171.
8. Cobianchi, F., C. Calvio, M. Stoppin, M. Buvoli, and S. Riva. 1993. Phosphorylation of human hnRNP protein A1 abrogates in vitro strand annealing activity. Nucleic Acids Res. 21: 949-955.
9. Colot, H., F. Stutz, and M. Rosbash. 1996. The yeast splicing factor Mud13p is a commitment complex component and corresponds to CBP20, the small subunit of the nuclear cap binding complex. Genes & Dev. 10: 1699-1708.
10. Doye, V., R. Wepf, and E.C. Hurt. 1994. A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution. EMBO J. 13: 6062-6075.
11. Dreyfuss, G., M.J. Matunis, S. Piñol-Roma, and C.G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62: 289-321.
12. Fischer, U., M. Michael, R. Luhrmann, and G. Dreyfuss. 1996. Signal-mediated nuclear export pathways of proteins and RNAs. Trends Cell Biol. 6: 290-293.
13. Flach, J., M. Bossie, J. Vogel, A. Corbett, T. Jinks, D.A. Willins, and P.A. Silver. 1994. A yeast RNA-binding protein shuttles between the nucleus and the cytoplasm. Mol. Cell Biol. 14: 8399-8407.
14. Fornerod, M., M. Ohno, M. Yoshida, and I.W. Mattaj. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90: 1051-1060.
15. Gary, J.D., W.J. Lin, M.C. Yang, H.R. Herschman, and S. Clarke. 1996. The predominant protein-arginine methyltransferase from Saccharomyces cerevisiae. J. Biol Chem. 271: 12585-12594.
16. Ghosh, S.K., W.K. Paik, and S. Kim. 1988. Purification and molecular identification of two protein methylases I from calf brain. Myelin basic protein and histone specific enzyme. J. Biol. Chem. 263: 19024-19033.
17. Gorlich, D., R. Kraft, S. Kostka, F. Vogel, E. Hartmann, R.A. Laskey, I.W. Mattaj, and E. Izaurralde. 1996. Importin provides a link between nuclear protein import and U snRNA export. Cell 87: 21-32.
18. Hamm, J. and I.W. Mattaj. 1990. Monomethylated cap structures facilitate RNA export from the nucleus. Cell 63: 109-118.
19. Henry, M., C.Z. Borland, M. Bossie, and P.A. Silver. 1996. Potential RNA binding proteins in Saccharomyces cerevisiae identified as suppressors of temperature-sensitive mutations in NPL3. Genetics 142: 103-115.
20. Henry, M.F. and P.A. Silver. 1996. A novel methyltransferase (Hmt1p) modifies poly(A)+ RNA binding proteins. Mol. Cell. Biol. 16: 3668-3678.
21. Izaurralde, E., J. Lewis, C. McGuigan, M. Jankowska, E. Darzynkiewicz, and I.W. Mattaj. 1994. A nuclear cap binding protein complex involved in pre-mRNA splicing. Cell 78: 657-668.
22. Izaurralde, E., J. Lewis, C. Gamberi, A. Jarmolowski, C. McGuigan, and I.W. Mattaj. 1995. A cap-binding protein complex mediating U snRNA export. Nature 376: 709-712.
23. Izaurralde, E., A. Jarmolowski, C. Beisel, I.W. Mattaj, and G. Dreyfuss. 1997. A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J. Cell Biol. 137: 27-35.
24. Katsanis, N., M.L. Yaspo, and E.M. Fisher. 1997. Identification and mapping of a novel human gene, HRMT1L1, homologous to the rat protein arginine N-methyltransferase 1 (PRMT1) gene. Mammal. Genome 8: 526-529.
25. Kessler, M.M., M.F. Henry, E. Shen, J. Zhao, S. Gross, P.A. Silver, and C.L. Moore. 1997. Hrp1, a sequence-specific RNA-binding protein that shuttles between the nucleus and the cytoplasm, is required for mRNA 3′-end formation in yeast. Genes & Dev. 11: 2545-2556.
26. Kiledjian, M., C.G. Burd, D.S. Portman, and G. Dreyfuss. 1994. Structure and function of hnRNP proteins. In RNA-protein interactions: Frontiers in molecular biology (ed. K. Nagai and I.W. Mattaj), pp. 127-149. IRL Press, Oxford, UK.
27. Koepp, D.M., D.H. Wong, A.H. Corbett, and P.A. Silver. 1996. Dynamic localization of the nuclear import receptor and its interactions with transport factors. J. Cell Biol. 133: 1163-1176.
28. Krainer, A.R., A. Mayeda, D. Kozak, and G. Binns. 1991. Functional expression of cloned human splicing factor SF2: Homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell 66: 383-394.
29. Kranz, J.E. and C. Holm. 1990. Cloning by function: An alternative approach for identifying yeast homologs from other organisms. Proc. Natl. Acad. Sci. 87: 6629-6633.
30. Lee, M.S. and P.A. Silver. 1997. RNA movement between the nucleus and the cytoplasm. Curr. Opin. 7: 212-219.
31. Lee, M.S., M. Henry, and P.A. Silver. 1996. A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes & Dev. 10: 1233-1246.
32. Lewis, J.D., and E. Izaurralde. 1997. The role of the cap structure in RNA processing and nuclear export. Eur. J. Biochem. 247: 461-469.
33. Lewis, J.D., D. Gorlich, and I.W. Mattaj. 1996. A yeast cap-binding protein complex (yCBC) acts as an early step in pre-mRNA splicing. Nucleic Acids Res. 24: 3332-3336.
34. Lin, W.J., J.D. Gary, M.C. Yang, S. Clarke, and H.R. Herschman. 1996. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J. Biol. Chem. 271: 15034-15044.
35. Liu, Q. and G. Dreyfuss. 1995. In vivo and in vitro arginine methylation of RNA-binding proteins. Mol.Cell. Biol. 15: 2800-2808.
36. Mears, W.E. and S.A. Rice. 1996. The RGG box motif of the herpes simplex virus ICP27 protein mediates an RNA-binding activity and determines in vivo methylation. J. Virol. 70: 7445-7453.
37. Michael, W.M., M. Choi, and G. Dreyfuss. 1995. A nuclear export signal in hnRNP A1: A signal-mediated, temperature-dependent nuclear protein export pathway. Cell 83: 415-422.
38. Najbauer, J., B.A. Johnson, A.L. Young, and D.W. Aswad. 1993. Peptides with sequences similar to glycine, arginine-rich motifs in proteins interacting with RNA are efficiently recognized by methyltransferase(s) modifying arginine in numerous proteins. J. Biol. Chem. 268: 10501-10509.
39. Neville, M., F. Stutz, L. Lee, L.I. Davis, and M. Rosbash. 1997. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 7: 767-775.
40. Nigg, E. 1997. Nucleocytoplasmic transport: Signals, mechanisms and regulation. Nature 386: 779-787.
41. Nikawa, J., H. Nakano, and N. Ohi. 1996. Structural and functional conservation of human and yeast HCP1 genes which can suppress the growth defect of the Saccharomyces cerevisiae ire15 mutant. Gene 171: 107-111.
42. Nonet, M., C. Scafe, J. Sexton, and R. Young. 1987. Eukaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol. Cell. Biol. 7: 1602-1611.
43. Ossareh-Nazari, B., F. Bachelerie, and C. Dargemont. 1997. Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278: 141-144.
44. Philippsen, P., K. Kleine, R. Pohlmann, A. Dusterhoft, K. Hamberg, J.H. Hegemann, B. Obermaier, L.A. Urrestarazu, R. Aert, K. Albermann et al. 1997. The nucleotide sequence of Saccharomyces cerevisiae chromosome XIV and its evolutionary implications. Nature 387: 93-98.
45. Piñol-Roma, S. 1997. HnRNP proteins and the nuclear export of mRNA. Sem. Cell Dev. Biol. 8: 57-63.
46. Piñol-Roma, S. and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355: 730-732.
47. _. 1993. Cell cycle-regulated phosphorylation of the pre-mRNA binding (heterogeneous nuclear ribonucleoprotein) C proteins. Mol. Cell. Biol. 13: 5762-5770.
48. Pintucci, G., N. Quarto, and D.B. Rifkin. 1996. Methylation of high molecular weight fibroblast growth factor-2 determines post-translational increases in molecular weight and affects its intracellular distribution. Mol. Biol. Cell 7: 1249-1258.
49. Rajpurohit, R., W.K. Paik, and S. Kim. 1994. Effect of enzymic methylation of heterogeneous ribonucleoprotein particle A1 on its nucleic-acid binding and controlled proteolysis. Biochem. J. 304: 903-909.
50. Rawal, N., R. Rajpurohit, W.K. Paik, and S. Kim. 1994. Purification and characterization of S-adenosylmethionine protein arginine N-methyltransferase from rat liver. Biochem J. 300: 483-489.
51. Russell, I.D., and D. Tollervey. 1992. NOP3 is an essential yeast protein which is required for pre-rRNA processing. J. Cell Biol. 119: 737-747.
52. Siebel, C.W. and C. Guthrie. 1996. The essential yeast RNA binding protein Np13p is methylated. Proc. Natl. Acad. Sci. 93: 13641-13646.
53. Singleton, D.R., S. Chen, M. Hitomi, C. Kumagai, and A.M. Tartakoff. 1995. A yeast protein that bidirectionally affects nucleocytoplasmic transport. J. Cell. Sci. 108: 265-272.
54. Soulard, M., D.V. Veronique, M.C. Siomi, S. Piñol-Roma, P. Codogno, C. Bauvy, M. Bellini, J.C. Lacroix, G. Monod, G. Dreyfuss, et al. 1993. hnRNP G: Sequence and characterization of a glycosylated RNA-binding protein. Nucleic Acids Res. 21: 4210-4217.
55. Stade, K., C.S. Ford, C. Guthrie, and K. Weis. 1997. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90: 1041-1050.
56. Uemera, H. and Y. Jigami. 1992. GCR3 encodes an acidic protein that is required for expression of glycolytic genes in Saccharomyces cerevisiae. J. Bacteriol. 174: 5526-5532.
57. Ullman, K.S., M.A. Powers, and D.J. Forbes. 1997. Nuclear export receptors: From importin to exportin. Cell 90: 967-970.
58. Visa, N., A.T. Alzhanova-Ericsson, X. Sun, E. Kiseleva, B. Bjorkroth, T. Wurtz, and B. Daneholt. 1996a. A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes. Cell 84: 253-264.
59. Visa, N., E. Izaurralde, J. Ferreira, B. Daneholt, and I.W. Mattaj. 1996b. A nuclear cap-binding complex binds Balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export. J. Cell Biol. 133: 5-14.
60. Wilson, S.M., K.V. Datar, M.R. Paddy, J.R. Swedlow, and M. Swanson. 1994. Characterization of nuclear polyadenylated RNA-binding proteins in Saccharomyces cerevisiae. J. Cell Biol. 127: 1173-1184.