Puf1p acts in combination with other yeast Puf proteins to control mRNA stability

RNA

Volumn 14, Issue 2, 2008, Pages 246-262

  Ulbricht, Randi J ^a   Olivas, Wendy M ^a  

^a UNIVERSITY OF MISSOURI ST LOUIS   (United States)

Author keywords

3 UTR; Decay; mRNA; Puf; Stability; Yeast

Indexed keywords

FUNGAL PROTEIN; HEXOKINASE; MESSENGER RNA; PROTEIN HXK1; PROTEIN PUF1; PROTEIN PUF1P; PROTEIN PUF3P; PROTEIN PUF5; PROTEIN PUF5P; PROTEIN TIF1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; RNA STABILITY; RNA TRANSCRIPTION; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; UPREGULATION; YEAST;

3' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; BASE SEQUENCE; CELL CYCLE PROTEINS; EUKARYOTIC INITIATION FACTOR-4F; GENE EXPRESSION REGULATION, FUNGAL; HEXOKINASE; MOLECULAR SEQUENCE DATA; REPRESSOR PROTEINS; RNA STABILITY; RNA, FUNGAL; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 38649087012     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.847408     Document Type: Article

References (57)

1. Adams, C.D. and Gross, D.S. 1991. The yeast heat shock response is induced by conversion of cells to spheroplasts and by potent transcriptional inhibitors. J. Bacteriol. 173: 7429-7435.
2. Aragon, A.D., Quinones, G.A., Thomas, E.V., Roy, S., and Werner-Washburne, M. 2006. Release of extraction-resistant mRNA in stationary phase Saccharomyces cerevisiae produces a massive increase in transcript abundance in response to stress. Genome Biol. 7: R9. doi: 10.1186/gb-2006-7-2-r9.
3. Bachorik, J.L. and Kimble, J. 2005. Redundant control of the Caenorhabditis elegans sperm/oocyte switch by PUF-8 and FBF-1, two distinct Puf RNA-binding proteins. Proc. Natl. Acad. Sci. 102: 10893-10897.
4. Bernstein, D., Hook, B., Hajarnavis, A., Opperman, L., and Wickens, M. 2005. Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1. RNA 11: 447-458.
5. Boy-Marcotte, E., Perrot, M., Bussereau, F., Boucherie, H., and Jacquet, M. 1998. Msn2p and Msn4p control a large number of genes induced at the diauxic transition which are repressed by cyclic AMP in Saccharomyces cerevisiae. J. Bacteriol. 180: 1044-1052.
6. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., and Boeke, J.D. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
7. Caponigro, G., Muhlrad, D., and Parker, R. 1993. A small segment of the MATa1 transcript promotes mRNA decay in Saccharomyces cerevisiae: A stimulatory role for rare codons. Mol. Cell. Biol. 13: 5141-5148.
8. Crittenden, S.L., Bernstein, D.S., Bachorik, J.L., Thompson, B.E., Gallegos, M., Petcherski, A.G., Moulder, G., Barstead, R., Wickens, M., and Kimble, J. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417: 660-663.
9. Curtis, D., Treiber, D.K., Tao, F., Zamore, P.D., Williamson, J.R., and Lehmann, R. 1997. A CCHC metal-binding domain in Nanos is essential for translation regulation. EMBO J. 16: 834-843.
10. Decker, C.J. and Parker, R. 1993. A turnover pathway for both stable and unstable mRNAs in yeast: Evidence for a requirement for deadenylation. Genes & Dev. 7: 1632-1643.
11. Derrigo, M., Cestelli, A., Savettieri, G., and Di Liegro, I. 2000. RNA-protein interactions in the control of stability and localization of messenger RNA. Int. J. Mol. Med. 5: 111-123.
12. Edwards, T.A., Pyle, S.E., Wharton, R.P., and Aggarwal, A.K. 2001. Structure of Pumilio reveals similarity between RNA and peptide binding motifs. Cell 105: 281-289.
13. Fehrenbacher, K.L., Boldogh, I.R., and Pon, L.A. 2005. A role for Jsn1p in recruiting the Arp2/3 complex to mitochondria in budding yeast. Mol. Biol. Cell 16: 5094-5102.
14. Felici, F., Cesareni, G., and Hughes, J.M.X. 1989. The most abundant small cytoplasmic RNA of Saccharomyces cerevisiae has an important function required for normal cell growth. Mol. Cell. Biol. 9: 3260-3268.
15. Foat, B.C., Houshmandi, S.S., Olivas, W.M., and Bussemaker, H.J. 2005. Profiling condition-specific, genome-wide regulation of mRNA stability in yeast. Proc. Natl. Acad. Sci. 102: 17675-17680.
16. Forbes, A. and Lehmann, R. 1998. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125: 679-690.
17. Gamberi, C., Peterson, D.S., He, L., and Gottlieb, E. 2002. An anterior function for the Drosophila posterior determinant Pumilio. Development 129: 2699-2710.
18. Gancedo, J.M., Clifton, D., and Fraenkel, D.G. 1977. Yeast hexokinase mutants. J. Biol. Chem. 252: 4443-4444.
19. Garcia-Rodriguez, L.J., Gay, A.C., and Pon, L.A. 2007. Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast. J. Cell Biol. 176: 197-207.
20. Gerber, A.P., Herschlag, D., and Brown, P.O. 2004. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2: 342-354. doi: 10.1371/journal.pbio.0020079.
21. Gietz, R.D. and Schiestl, R.H. 1995. Transforming yeast with DNA. Methods Mol. Cell. Biol. 5: 255-269.
22. Goldstrohm, A.C., Hook, B.A., Seay, D.J., and Wickens, M. 2006. PUF proteins bind Pop2p to regulate messenger RNAs. Nat. Struct. Mol. Biol. 13: 533-539.
23. Grigull, J., Mnaimneh, S., Pootoolal, J., Robinson, M.D., and Hughes, T.R. 2004. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24: 5534-5547.
24. Grzybowska, E.A., Wilczynska, A., and Siedlecki, J.A. 2001. Regulatory functions of 3′ UTRs. Biochem. Biophys. Res. Commun. 288: 291-295.
25. Gu, W., Deng, Y., Zenklusen, D., and Singer, R.H. 2004. A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes & Dev. 18: 1452-1465.
26. Guhaniyogi, J. and Brewer, G. 2001. Regulation of mRNA stability in mammalian cells. Gene 265: 11-23.
27. Hatfield, L., Beelman, C.A., Stevens, A., and Parker, R. 1996. Mutations in trans-acting factors affecting mRNA decapping in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 5830-5838.
28. Heaton, B., Decker, C., Muhlrad, D., Donahue, J., Jacobson, A., and Parker, R. 1992. Analysis of chimeric mRNAs derived from the STE3 mRNA identifies multiple regions within yeast mRNAs that modulate mRNA decay. Nucleic Acids Res. 20: 5365-5373. doi: 10.1093/nar/20.20.5365.
29. Herrick, D., Parker, R., and Jacobson, A. 1990. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 10: 2269-2284.
30. Hook, B.A., Goldstrohm, A.C., Saeu, D.J., and Wickens, M. 2007. Two yeast Puf proteins negatively regulate a single mRNA. J. Biol. Chem. 282: 15430-15438.
31. Houshmandi, S.S. and Olivas, W.M. 2005. Yeast Puf3 mutants reveal the complexity of Puf-RNA binding and identify a loop required for regulation of mRNA decay. RNA 11: 1655-1666.
32. Jackson, J.S., Houshmandi, S.S., Leban, F.L., and Olivas, W.M. 2004. Recruitment of the Puf3 protein to its mRNA target for regulation of mRNA decay in yeast. RNA 10: 1625-1636.
33. Kawasaki, G. and Fraenkel, D.G. 1982. Cloning of yeast glycolysis genes by complementation. Biochem. Biophys. Res. Commun. 108: 1107-1112.
34. Kraemer, B., Crittenden, S., Gallegos, M., Moulder, G., Barstead, R., Kimble, J., and Wickens, M. 1999. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr. Biol. 9: 1009-1018.
35. Lidder, P., Gutierrez, R.A., Salome, P.A., McClung, C.R., and Green, P.J. 2005. Circadian control of messenger RNA stability. Association with a sequence-specific messenger RNA decay pathway. Plant Physiol. 138: 2374-2385.
36. Menon, K.P., Sanyal, S., Habara, Y., Sanchez, R., Wharton, R.P., Ramaswami, M., and Zinn, K. 2004. The translational repressor Pumilio regulates presynaptic morphology and controls postsynaptic accumulation of translation factor eIF-4E. Neuron 44: 663-676.
37. Moore, F.L., Jaruzelska, J., Fox, M.S., Urano, J., Firpo, M.T., Turek, P.J., Dorfman, D.M., and Pera, R.A. 2003. Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (deleted in AZoospermia) and DAZ-like proteins. Proc. Natl. Acad. Sci. 100: 538-543.
38. Murata, Y. and Wharton, R. 1995. Binding of Pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80: 747-756.
39. Nakahata, S., Kotani, T., Mita, K., Kawasaki, T., Katsu, Y., Nagahama, Y., and Yamashita, M. 2003. Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech. Dev. 120: 865-880.
40. Olivas, W. and Parker, R. 2000. The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast. EMBO J. 19: 6602-6611.
41. Parisi, M. and Lin, H. 1999. The Drosophila Pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis, and embryogenesis. Genetics 153: 235-250.
42. Parker, R. and Song, H. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11: 121-127.
43. Penelova, A., Richman, L., Neupert, B., Simanis, V., and Kuhn, L.C. 2005. Analysis of the contribution of changes in mRNA stability to the changes in steady-state levels of cyclin mRNA in the mammalian cell cycle. FEBS J. 272: 5217-5229.
44. Rodriguez, A., De La Cera, T., Herrero, P., and Moreno, F. 2001. The hexokinase 2 protein regulates the expression of the GLK1, HXK1, and HXK2 genes of Saccharomyces cerevisiae. Biochem. J. 355: 625-631.
45. Shim, J. and Karin, M. 2002. The control of mRNA stability in response to extracellular stimuli. Mol. Cells 14: 323-331.
46. Sonoda, J. and Wharton, R.P. 1999. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes & Dev. 13: 2704-2712.
47. Sonoda, J. and Wharton, R.P. 2001. Drosophila brain tumor is a translational repressor. Genes & Dev. 15: 762-773.
48. Tadauchi, T., Matsumoto, K., Herskowitz, I., and Irie, K. 2001. Post-transcriptional regulation through the HO 3′-UTR by Mpt5, a yeast homolog of Pumilio and FBF. EMBO J. 20: 552-561.
49. Taylor, R., Kebaara, B.W., Nazarenus, T., Jones, A., Yamanaka, R., Uhrenholdt, R., Wendler, J.P., and Atkin, A.L. 2005. Gene set coregulated by the Saccharomyces cerevisiae nonsense-mediated mRNA decay pathway. Eukaryot. Cell 4: 2066-2077.
50. Walsh, R.B., Clifton, D., Horak, J., and Fraenkel, D.G. 1991. Saccharomyces cerevisiae null mutants in glucose phosphorylation: Metabolism and invertase expression. Genetics 128: 521-527.
51. Wang, X., McLachlan, J., Zamore, P.D., and Tanaka Hall, T.M. 2002. Modular recognition of RNA by a human Pumilio-homology domain. Cell 110: 501-512.
52. Wharton, R.P. and Struhl, G. 1991. RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell 67: 955-967.
53. Wharton, R.P., Sonoda, J., Lee, T., Patterson, M., and Murata, Y. 1998. The Pumilio RNA-binding domain is also a translational regulator. Mol. Cell 1: 863-872.
54. Wickens, M., Bernstein, D.S., Kimble, J., and Parker, R. 2002. A PUF family portrait: 3′ UTR regulation as a way of life. Trends Genet. 18: 150-157.
55. Wreden, C., Verrotti, A.C., Schisa, J.A., Lieberfarb, M.E., and Strickland, S. 1997. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development 124: 3015-3023.
56. Ye, B., Petritsch, C., Clark, I.E., Gavis, E.R., Jan, L.Y., and Jan, Y.N. 2004. Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons. Curr. Biol. 14: 314-321.
57. Zhang, B., Gallegos, M., Puoti, A., Durkin, E., Fields, S., Kimble, J., and Wickens, M.P. 1997. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390: 477-484.