Suppressors of the cdc-25.1(gf)-associated intestinal hyperplasia reveal important maternal roles for prp-8 and a subset of splicing factors in C. elegans

RNA

Volumn 14, Issue 12, 2008, Pages 2618-2633

  Hebeisen, Michaël ^a   Drysdale, John ^a   Roy, Richard ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

cdc 25.1; Cell cycle; Maternal contribution; prp 8; Retinitis pigmentosa; Splicing factors; Tissue specificity

Indexed keywords

PROTEIN TYROSINE PHOSPHATASE; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; GENE; GENE MAPPING; GENE MUTATION; GENE REPRESSION; GENETIC SCREENING; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HYPERPLASIA; INTESTINAL HYPERPLASIA; LINKAGE ANALYSIS; MOLECULAR CLONING; MOTHER CHILD RELATION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROTEIN TYROSINE PHOSPHATASE GENE; PRP 8 GENE; RETINITIS PIGMENTOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA SPLICING; SPLICEOSOME; STEADY STATE; TISSUE SPECIFICITY; WILD TYPE; ZYGOTE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CDC25 PHOSPHATASES; HUMANS; INTESTINES; RNA, MESSENGER, STORED;

CAENORHABDITIS ELEGANS;

EID: 57049174563     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1168408     Document Type: Article

References (90)

1. Alphey, L., Jimenez, J., White-Cooper, H., Dawson, I., Nurse, P., and Glover, D.M. 1992. twine, a cdc25 homolog that functions in the male and female germ line of Drosophila. Cell 69: 977-988.
2. Aroian, R.V., Levy, A.D., Koga, M., Ohshima, Y., Kramer, J.M., and Sternberg, P.W. 1993. Splicing in Caenorhabditis elegans does not require an AG at the 3′ splice acceptor site. Mol. Cell. Biol. 13: 626-637.
3. Ashcroft, N. and Golden, A. 2002. CDC-25.1 regulates germ line proliferation in Caenorhabditis elegans. Genesis 33: 1-7.
4. Ashcroft, N.R., Kosinski, M.E., Wickramasinghe, D., Donovan, P.J., and Golden, A. 1998. The four cdc25 genes from the nematode Caenorhabditis elegans. Gene 214: 59-66.
5. Bao, Z., Zhao, Z., Boyle, T.J., Murray, J.I., and Waterston, R.H. 2008. Control of cell cycle timing during C. elegans embryogenesis. Dev. Biol. 318: 65-72.
6. Behzadnia, N., Golas, M.M., Hartmuth, K., Sander, B., Kastner, B., Deckert, J., Dube, P., Will, C.L., Urlaub, H., Stark, H., et al. 2007. Composition and three-dimensional EM structure of double affinity-purified, human prespliceosomal A complexes. EMBO J. 26: 1737-1748.
7. Bejsovec, A. and Anderson, P. 1988. Myosin heavy-chain mutations that disrupt Caenorhabditis elegans thick filament assembly. Genes & Dev. 2: 1307-1317.
8. Ben-Yehuda, S., Dix, I., Russell, C.S., McGarvey, M., Beggs, J.D., and Kupiec, M. 2000a. Genetic and physical interactions between factors involved in both cell cycle progression and pre-mRNA splicing in Saccharomyces cerevisiae. Genetics 156: 1503-1517.
9. Ben-Yehuda, S., Russell, C.S., Dix, I., Beggs, J.D., and Kupiec, M. 2000b. Extensive genetic interactions between PRP8 and PRP17/CDC40, two yeast genes involved in pre-mRNA splicing and cell cycle progression. Genetics 154: 61-71.
10. Bessonov, S., Anokhina, M., Will, C.L., Urlaub, H., and Luhrmann, R. 2008. Isolation of an active step I spliceosome and composition of its RNP core. Nature 452: 846-850.
11. Boon, K.L., Grainger, R.J., Ehsani, P., Barrass, J.D., Auchynnikava, T., Inglehearn, C.F., and Beggs, J.D. 2007. prp8 mutations that cause human retinitis pigmentosa lead to a U5 snRNP maturation defect in yeast. Nat. Struct. Mol. Biol. 14: 1077-1083.
12. Bowerman, B. 1998. Maternal control of pattern formation in early Caenorhabditis elegans embryos. Curr. Top. Dev. Biol. 39: 73-117.
13. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
14. Burns, C.G., Ohi, R., Mehta, S., O'Toole, E.T., Winey, M., Clark, T.A., Sugnet, C.W., Ares Jr., M., and Gould, K.L. 2002. Removal of a single α-tubulin gene intron suppresses cell cycle arrest phenotypes of splicing factor mutations in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 801-815.
15. Busino, L., Donzelli, M., Chiesa, M., Guardavaccaro, D., Ganoth, D., Dorrello, N.V., Hershko, A., Pagano, M., and Draetta, G.F. 2003. Degradation of Cdc25A by β-TrCP during S phase and in response to DNA damage. Nature 426: 87-91.
16. Busino, L., Chiesa, M., Draetta, G.F., and Donzelli, M. 2004. Cdc25A phosphatase: Combinatorial phosphorylation, ubiquitylation, and proteolysis. Oncogene 23: 2050-2056.
17. Chakarova, C.F., Hims, M.M., Bolz, H., Abu-Safieh, L., Patel, R.J., Papaioannou, M.G., Inglehearn, C.F., Keen, T.J., Willis, C., Moore, A.T., et al. 2002. Mutations in HPRP3, a third member of pre-mRNA splicing factor genes, implicated in autosomal dominant retinitis pigmentosa. Hum. Mol. Genet. 11: 87-92.
18. Clucas, C., Cabello, J., Bussing, I., Schnabel, R., and Johnstone, I.L. 2002. Oncogenic potential of a C.elegans cdc25 gene is demonstrated by a gain-of-function allele. EMBO J. 21: 665-674.
19. Coelho, C.M., Kolevski, B., Walker, C.D., Lavagi, I., Shaw, T., Ebert, A., Leevers, S.J., and Marygold, S.J. 2005. A genetic screen for dominant modifiers of a small-wing phenotype in Drosophila melanogaster identifies proteins involved in splicing and translation. Genetics 171: 597-614.
20. Courtot, C., Fankhauser, C., Simanis, V., and Lehner, C.F. 1992. The Drosophila cdc25 homolog twine is required for meiosis. Development 116: 405-416.
21. Dahan, O. and Kupiec, M. 2002. Mutations in genes of Saccharomyces cerevisiae encoding pre-mRNA splicing factors cause cell cycle arrest through activation of the spindle checkpoint. Nucleic Acids Res. 30: 4361-4370.
22. Dahan, O. and Kupiec, M. 2004. The Saccharomyces cerevisiae gene CDC40/PRP17 controls cell cycle progression through splicing of the ANC1 gene. Nucleic Acids Res. 32: 2529-2540.
23. Deckert, J., Hartmuth, K., Boehringer, D., Behzadnia, N., Will, C.L., Kastner, B., Stark, H., Urlaub, H., and Luhrmann, R. 2006. Protein composition and electron microscopy structure of affinity-purified human spliceosomal B complexes isolated under physiological conditions. Mol. Cell. Biol. 26: 5528-5543.
24. DeRenzo, C. and Seydoux, G. 2004. A clean start: Degradation of maternal proteins at the oocyte-to-embryo transition. Trends Cell Biol. 14: 420-426.
25. Dibb, N.J., Brown, D.M., Karn, J., Moerman, D.G., Bolten, S.L., and Waterston, R.H. 1985. Sequence analysis of mutations that affect the synthesis, assembly and enzymatic activity of the unc-54 myosin heavy chain of Caenorhabditis elegans. J. Mol. Biol. 183: 543-551.
26. Edgar, B.A. 1994. Cell-cycle control in a developmental context. Curr. Biol. 4: 522-524.
27. Edgar, L.G. and McGhee, J.D. 1988. DNA synthesis and the control of embryonic gene expression in C. elegans. Cell 53: 589-599.
28. Edgar, B.A. and Datar, S.A. 1996. Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program. Genes & Dev. 10: 1966-1977.
29. Edgar, B.A. and Lehner, C.F. 1996. Developmental control of cell cycle regulators: A fly's perspective. Science 274: 1646-1652.
30. Evsikov, A.V., Graber, J.H., Brockman, J.M., Hampl, A., Holbrook, A.E., Singh, P., Eppig, J.J., Solter, D., and Knowles, B.B. 2006. Cracking the egg: Molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo. Genes & Dev. 20: 2713-2727.
31. Falck, J., Mailand, N., Syljuasen, R.G., Bartek, J., and Lukas, J. 2001. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410: 842-847.
32. Faustino, N.A. and Cooper, T.A. 2003. Pre-mRNA splicing and human disease. Genes & Dev. 17: 419-437.
33. Fukushige, T., Hendzel, M.J., Bazett-Jones, D.P., and McGhee, J.D. 1999. Direct visualization of the elt-2 gut-specific GATA factor binding to a target promoter inside the living Caenorhabditis elegans embryo. Proc. Natl. Acad. Sci. 96: 11883-11888.
34. Galaktionov, K. and Beach, D. 1991. Specific activation of cdc25 tyrosine phosphatases by B-type cyclins: Evidence for multiple roles of mitotic cyclins. Cell 67: 1181-1194.
35. Gonczy, P., Echeverri, C., Oegema, K., Coulson, A., Jones, S.J., Copley, R.R., Duperon, J., Oegema, J., Brehm, M., Cassin, E., et al. 2000. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408: 331-336.
36. Gonzalez-Santos, J.M., Cao, H., Duan, R.C., and Hu, J. 2008. Mutation in the splicing factor Hprp3p linked to retinitis pigmentosa impairs interactions within the U4/U6 snRNP complex. Hum. Mol. Genet. 17: 225-239.
37. Grainger, R.J. and Beggs, J.D. 2005. Prp8 protein: At the heart of the spliceosome. RNA 11: 533-557.
38. + gene encoding a homolog of SAP130/SF3b130 causes differential inhibition of pre-mRNA splicing and arrest of cell-cycle progression in Schizosaccharomyces pombe. RNA 7: 671-681.
39. Hartwell, L.H. 1967. Macromolecule synthesis in temperature-sensitive mutants of yeast. J. Bacteriol. 93: 1662-1670.
40. Heasman, J. 2006. Patterning the early Xenopus embryo. Development 133: 1205-1217.
41. Hebeisen, M. and Roy, R. 2008. CDC-25.1 stability is regulated by distinct domains to restrict cell division during embryogenesis in C. elegans. Development 135: 1259-1269.
42. Hodges, P.E., Jackson, S.P., Brown, J.D., and Beggs, J.D. 1995. Extraordinary sequence conservation of the PRP8 splicing factor. Yeast 11: 337-342.
43. Hodgkin, J. and Doniach, T. 1997. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146: 149-164.
44. Hodgkin, J., Papp, A., Pulak, R., Ambros, V., and Anderson, P. 1989. A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 123: 301-313.
45. Jin, J., Shirogane, T., Xu, L., Nalepa, G., Qin, J., Elledge, S.J., and Harper, J.W. 2003. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes & Dev. 17: 3062-3074.
46. Kamath, R.S., Fraser, A.G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M., et al. 2003. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
47. Kaplan, Y. and Kupiec, M. 2007. A role for the yeast cell cycle/splicing factor Cdc40 in the G1/S transition. Curr. Genet. 51: 123-140.
48. Kennan, A., Aherne, A., and Humphries, P. 2005. Light in retinitis pigmentosa. Trends Genet. 21: 103-110.
49. Kim, S.H., Li, C., and Maller, J.L. 1999. A maternal form of the phosphatase Cdc25A regulates early embryonic cell cycles in Xenopus laevis. Dev. Biol. 212: 381-391.
50. Kipreos, E.T. 2005. C. elegans cell cycles: Invariance and stem cell divisions. Nat. Rev. Mol. Cell Biol. 6: 766-776.
51. Kostic, I. and Roy, R. 2002. Organ-specific cell division abnormalities caused by mutation in a general cell cycle regulator in C. elegans. Development 129: 2155-2165.
52. Lecuyer, E., Yoshida, H., Parthasarathy, N., Alm, C., Babak, T., Cerovina, T., Hughes, T.R., Tomancak, P., and Krause, H.M. 2007. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131: 174-187.
53. Lin, R. 2003. A gain-of-function mutation in oma-1, a C. elegans gene required for oocyte maturation, results in delayed degradation of maternal proteins and embryonic lethality. Dev. Biol. 258: 226-239.
54. Longman, D., Plasterk, R.H., Johnstone, I.L., and Caceres, J.F. 2007. Mechanistic insights and identification of two novel factors in the C. elegans NMD pathway. Genes & Dev. 21: 1075-1085.
55. + and encodes an RNA-dependent ATPase/helicase. Mol. Biol. Cell 7: 1083-1094.
56. Maduro, M.F., Hill, R.J., Heid, P.J., Newman-Smith, E.D., Zhu, J., Priess, J.R., and Rothman, J.H. 2005. Genetic redundancy in endoderm specification within the genus Caenorhabditis. Dev. Biol. 284: 509-522.
57. Maita, H., Kitaura, H., Keen, T.J., Inglehearn, C.F., Ariga, H., and Iguchi-Ariga, S.M. 2004. PAP-1, the mutated gene underlying the RP9 form of dominant retinitis pigmentosa, is a splicing factor. Exp. Cell Res. 300: 283-296.
58. Maita, H., Kitaura, H., Ariga, H., and Iguchi-Ariga, S.M. 2005. Association of PAP-1 and Prp3p, the products of causative genes of dominant retinitis pigmentosa, in the tri-snRNP complex. Exp. Cell Res. 302: 61-68.
59. Makarov, E.M., Makarova, O.V., Urlaub, H., Gentzel, M., Will, C.L., Wilm, M., and Lührmann, R. 2002. Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 298: 2205-2208.
60. Makarova, O.V., Makarov, E.M., Liu, S., Vornlocher, H.P., and Lührmann, R. 2002. Protein 61K, encoded by a gene (PRPF31) linked to autosomal dominant retinitis pigmentosa, is required for U4/U6*U5 tri-snRNP formation and pre-mRNA splicing. EMBO J. 21: 1148-1157.
61. Marone, M., Mozzetti, S., De Ritis, D., Pierelli, L., and Scambia, G. 2001. Semiquantitative RT-PCR analysis to assess the expression levels of multiple transcripts from the same sample. Biol. Proced. Online 3: 19-25.
62. Mata, J., Curado, S., Ephrussi, A., and Rorth, P. 2000. Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101: 511-522.
63. McKie, A.B., McHale, J.C., Keen, T.J., Tarttelin, E.E., Goliath, R., van Lith-Verhoeven, J.J., Greenberg, J., Ramesar, R.S., Hoyng, C.B., Cremers, F.P., et al. 2001. Mutations in the pre-mRNA splicing factor gene PRPC8 in autosomal dominant retinitis pigmentosa (RP13). Hum. Mol. Genet. 10: 1555-1562.
64. Mordes, D., Luo, X., Kar, A., Kuo, D., Xu, L., Fushimi, K., Yu, G., Sternberg Jr., P., and Wu, J.Y. 2006. Pre-mRNA splicing and retinitis pigmentosa. Mol. Vis. 12: 1259-1271.
65. Mueller, P.R., Coleman, T.R., Kumagai, A., and Dunphy, W.G. 1995. Myt1: A membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science 270: 86-90.
66. Myer, D.L., Bahassi, E.M., and Stambrook, P.J. 2005. The Plk3-Cdc25 circuit. Oncogene 24: 299-305.
67. Newport, J. and Kirschner, M. 1982. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 30: 675-686.
68. Nishi, Y. and Lin, R. 2005. DYRK2 and GSK-3 phosphorylate and promote the timely degradation of OMA-1, a key regulator of the oocyte-to-embryo transition in C. elegans. Dev. Biol. 288: 139-149.
69. O'Farrell, P.H., Edgar, B.A., Lakich, D., and Lehner, C.F. 1989. Directing cell division during development. Science 246: 635-640.
70. Pena, V., Liu, S., Bujnicki, J.M., Luhrmann, R., and Wahl, M.C. 2007. Structure of a multipartite protein-protein interaction domain in splicing factor prp8 and its link to retinitis pigmentosa. Mol. Cell 25: 615-624.
71. Perdiguero, E. and Nebreda, A.R. 2004. Regulation of Cdc25C activity during the meiotic G2/M transition. Cell Cycle 3: 733-737.
72. Potashkin, J., Kim, D., Fons, M., Humphrey, T., and Frendewey, D. 1998. Cell-division-cycle defects associated with fission yeast pre-mRNA splicing mutants. Curr. Genet. 34: 153-163.
73. Praitis, V., Casey, E., Collar, D., and Austin, J. 2001. Creation of lowcopy integrated transgenic lines in Caenorhabditis elegans. Genetics 157: 1217-1226.
74. Rasheva, V.I., Knight, D., Bozko, P., Marsh, K., and Frolov, M.V. 2006. Specific role of the SR protein splicing factor B52 in cell cycle control in Drosophila. Mol. Cell. Biol. 26: 3468-3477.
75. Reese, K.J., Dunn, M.A., Waddle, J.A., and Seydoux, G. 2000. Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Mol. Cell 6: 445-455.
76. Rio Frio, T., Wade, N.M., Ransijn, A., Berson, E.L., Beckmann, J.S., and Rivolta, C. 2008. Premature termination codons in PRPF31 cause retinitis pigmentosa via haploinsufficiency due to nonsense-mediated mRNA decay. J. Clin. Invest. 118: 1519-1531.
77. Rushforth, A.M. and Anderson, P. 1996. Splicing removes the Caenorhabditis elegans transposon Tc1 from most mutant premRNAs. Mol. Cell. Biol. 16: 422-429.
78. Russell, P. and Nurse, P. 1987. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell 49: 559-567.
79. Russell, C.S., Ben-Yehuda, S., Dix, I., Kupiec, M., and Beggs, J.D. 2000. Functional analyses of interacting factors involved in both pre-mRNA splicing and cell cycle progression in Saccharomyces cerevisiae. RNA 6: 1565-1572.
80. Shea, J.E., Toyn, J.H., and Johnston, L.H. 1994. The budding yeast U5 snRNP Prp8 is a highly conserved protein which links RNA splicing with cell cycle progression. Nucleic Acids Res. 22: 5555-5564.
81. Shimuta, K., Nakajo, N., Uto, K., Hayano, Y., Okazaki, K., and Sagata, N. 2002. Chk1 is activated transiently and targets Cdc25A for degradation at the Xenopus midblastula transition. EMBO J. 21: 3694-3703.
82. Shirayama, M., Soto, M.C., Ishidate, T., Kim, S., Nakamura, K., Bei, Y., van den Heuvel, S., and Mello, C.C. 2006. The conserved kinases CDK-1, GSK-3, KIN-19, and MBK-2 promote OMA-1 destruction to regulate the oocyte-to-embryo transition in C. elegans. Curr. Biol. 16: 47-55.
83. Sorensen, C.S., Syljuasen, R.G., Falck, J., Schroeder, T., Ronnstrand, L., Khanna, K.K., Zhou, B.B., Bartek, J., and Lukas, J. 2003. Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 3: 247-258.
84. Stitzel, M.L., Pellettieri, J., and Seydoux, G. 2006. The C. elegans DYRK kinase MBK-2 marks oocyte proteins for degradation in response to meiotic maturation. Curr. Biol. 16: 56-62.
85. Teigelkamp, S., Newman, A.J., and Beggs, J.D. 1995. Extensive interactions of PRP8 protein with the 5′ and 3′ splice sites during splicing suggest a role in stabilization of exon alignment by U5 snRNA. EMBO J. 14: 2602-2612.
86. Vijayraghavan, U., Company, M., and Abelson, J. 1989. Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes & Dev. 3: 1206-1216.
87. Vithana, E.N., Abu-Safieh, L., Allen, M.J., Carey, A., Papaioannou, M., Chakarova, C., Al-Maghtheh, M., Ebenezer, N.D., Willis, C., Moore, A.T., et al. 2001. A human homolog of yeast pre-mRNA splicing gene, PRP31, underlies autosomal dominant retinitis pigmentosa on chromosome 19q13.4 (RP11). Mol. Cell 8: 375-381.
88. Wang, Q.T., Piotrowska, K., Ciemerych, M.A., Milenkovic, L., Scott, M.P., Davis, R.W., and Zernicka-Goetz, M. 2004. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev. Cell 6: 133-144.
89. Wicks, S.R., Yeh, R.T., Gish, W.R., Waterston, R.H., and Plasterk, R.H. 2001. Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28: 160-164.
90. Zhang, L., Shen, J., Guarnieri, M.T., Heroux, A., Yang, K., and Zhao, R. 2007. Crystal structure of the C-terminal domain of splicing factor Prp8 carrying retinitis pigmentosa mutants. Protein Sci. 16: 1024-1031.