A mutation in teg-4, which encodes a protein homologous to the SAP130 pre-mRNA splicing factor, disrupts the balance between proliferation and differentiation in the C. elegans germ line

Mechanisms of Development

Volumn 126, Issue 5-6, 2009, Pages 417-429

  Mantina, Pallavi ^a   MacDonald, Lindsay ^a   Kulaga, Adam ^a   Zhao, Lina ^a   Hansen, Dave ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Germline development; Meiotic entry; Notch signaling; Pre mRNA splicing; Proliferation; SAP130; Stem cells; tag 203; teg 4; Tumor

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; MESSENGER RNA PRECURSOR; MESSENGER RNA PRECURSOR SAP130; NOTCH RECEPTOR; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE; GENE FUNCTION; GENE MUTATION; GENETIC EPISTASIS; GERM LINE; LOSS OF FUNCTION MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA SPLICING; SEQUENCE HOMOLOGY; STEM CELL; TEG4 GENE;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO, NONMAMMALIAN; EPISTASIS, GENETIC; GERM CELLS; LARVA; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PROTEIN SUBUNITS; RECEPTORS, NOTCH; RNA PRECURSORS; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TEMPERATURE;

CAENORHABDITIS ELEGANS;

EID: 67349184010     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2009.01.006     Document Type: Article

References (79)

1. Ajuh P., Kuster B., Panov K., Zomerdijk J.C., Mann M., and Lamond A.I. Functional analysis of the human CDC5L complex and identification of its components by mass spectrometry. Embo. J. 19 (2000) 6569-6581
2. Ashcroft N., and Golden A. CDC-25.1 regulates germline proliferation in Caenorhabditis elegans. Genesis 33 (2002) 1-7
3. Austin J., and Kimble J. Glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51 (1987) 589-599
4. Bayne E.H., Portoso M., Kagansky A., Kos-Braun I.C., Urano T., Ekwall K., Alves F., Rappsilber J., and Allshire R.C. Splicing factors facilitate RNAi-directed silencing in fission yeast. Science 322 (2008) 602-606
5. Belfiore M., Pugnale P., Saudan Z., and Puoti A. Roles of the C. elegans cyclophilin-like protein MOG-6 in MEP-1 binding and germline fates. Development 131 (2004) 2935-2945
6. Berry L.W., Westlund B., and Schedl T. Germ-line tumor formation caused by activation of glp-1, a Caenorhabditis elegans member of the Notch family of receptors. Development 124 (1997) 925
7. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
8. Burns C.G., Ohi R., Krainer A.R., and Gould K.L. Evidence that Myb-related CDC5 proteins are required for pre-mRNA splicing. Proc. Natl. Acad. Sci. USA 96 (1999) 13789-13794
9. Caspary F., Shevchenko A., Wilm M., and Seraphin B. Partial purification of the yeast U2 snRNP reveals a novel yeast pre-mRNA splicing factor required for pre-spliceosome assembly. Embo. J. 18 (1999) 3463-3474
10. Chen E.J., Frand A.R., Chitouras E., and Kaiser C.A. A link between secretion and pre-mRNA processing defects in Saccharomyces cerevisiae and the identification of a novel splicing gene, RSE1. Mol. Cell. Biol. 18 (1998) 7139-7146
11. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T.J., Higgins D.G., and Thompson J.D. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31 (2003) 3497-3500
12. Christensen S., Kodoyianni V., Bosenberg M., Friedman L., and Kimble J. Lag-1, a gene required for lin-12 and glp-1 signaling in Caenorhabditis elegans, is homologous to human CBF1 and Drosophila Su(H). Development 122 (1996) 1373-1383
13. Crittenden S.L., Bernstein D.S., Bachorik J.L., Thompson B.E., and Gallegos M. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417 (2002) 660
14. Das B.K., Xia L., Palandjian L., Gozani O., Chyung Y., and Reed R. Characterization of a protein complex containing spliceosomal proteins SAPs 49, 130, 145 and 155. Mol. Cell. Biol. 19 (1999) 6796-6802
15. Ding W.Q., Kuntz S.M., and Miller L.J. A misspliced form of the cholecystokinin-B/gastrin receptor in pancreatic carcinoma: role of reduced sellular U2AF35 and a suboptimal 3′-splicing site leading to retention of the fourth intron. Cancer Res. 62 (2002) 947-952
16. Doyle T.G., Wen C., and Greenwald I. SEL-8, a nuclear protein required for LIN-12 and GLP-1 signaling in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 97 (2000) 7877-7881
17. Dziembowski A., Ventura A.P., Rutz B., Caspary F., Faux C., Halgand F., Laprevote O., and Seraphin B. Proteomic analysis identifies a new complex required for nuclear pre-mRNA retention and splicing. Embo. J. 23 (2004) 4847-4856
18. Eckmann C.R., Kraemer B., Wickens M., and Kimble J. GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in Caenorhabditis elegans. Dev Cell 3 (2002) 697-710
19. Eckmann C., Crittenden S.L., Suh N., and Kimble J. GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168 (2004) 147
20. Ferguson E.L., and Horvitz H.R. Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics 110 (1985) 17-72
21. Francis R., Maine E., and Schedl T. Analysis of the multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signaling pathway. Genetics 139 (1995) 607-630
22. Fraser A.G., Kamath R.S., Zipperlen P., Martinez-Campos M., Sohrmann M., and Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408 (2000) 325-330
23. Graham P.L., and Kimble J. The mog-1 gene is required for the switch from spermatogenesis to oogenesis in Caenorhabditis elegans. Genetics 133 (1993) 919-931
24. Graham P.L., Schedl T., and Kimble J. More mog genes that influence the switch from spermatogenesis to oogenesis in the hermaphrodite germ line of Caenorhabditis elegans. Dev. Genet. 14 (1993) 471-484
25. Greenwald I., Sternberg P.W., and Horvitz H.R. The lin-12 locus specifies cell fate in Caenorhabditis elegans. Cell 34 (1983) 435-444
26. Grosso A.R., Martins S., and Carmo-Fonseca M. The emerging role of splicing factors in cancer. EMBO Rep. 9 (2008) 1087-1093
27. Habara Y., Urushiyama S., Shibuya T., Ohshima Y., and Tani T. Mutation in the prp12+ 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 (2001) 671-681
28. Hansen D., Hubbard E.J., and Schedl T. Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev. Biol. 268 (2004) 342-357
29. Hansen D., and Schedl T. The regulatory network controlling the proliferation-meiotic entry decision in the Caenorhabditis elegans germ line. Curr. Top Dev. Biol. 76 (2006) 185-215
30. Hansen D., Wilson-Berry L., Dang T., and Schedl T. Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131 (2004) 93-104
31. Hebeisen M., Drysdale J., and Roy R. 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 14 (2008) 2618-2633
32. Henderson S.T., Gao D., Lambie E.J., and Kimble J. Lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 120 (1994) 2913-2924
33. Hirsh D., Oppenheim D., and Klass M. Development of the reproductive system of Caenorhabditis elegans. Dev. Biol. 49 (1976) 200-219
34. Horowitz D.S., Kobayashi R., and Krainer A.R. A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4/U6 snRNPs. RNA 3 (1997) 1374-1387
35. Horowitz D.S., Lee E.J., Mabon S.A., and Misteli T. A cyclophilin functions in pre-mRNA splicing. Embo. J. 21 (2002) 470-480
36. Ingelfinger D., Gothel S.F., Marahiel M.A., Reidt U., Ficner R., Luhrmann R., and Achsel T. Two protein-protein interaction sites on the spliceosome-associated human cyclophilin CypH. Nucleic Acids Res. 31 (2003) 4791-4796
37. Jakubowski J., and Kornfeld K. A local, high-density, single-nucleotide polymorphism map used to clone Caenorhabditis elegans cdf-1. Genetics 153 (1999) 743-752
38. Jones A.R., Francis R., and Schedl T. GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 180 (1996) 165
39. Jurica M.S., and Moore M.J. Pre-mRNA splicing: awash in a sea of proteins. Mol. Cell 12 (2003) 5-14
40. Kadyk L.C., and Kimble J. Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125 (1998) 1803-1813
41. Kambach C., Walke S., and Nagai K. Structure and assembly of the spliceosomal small nuclear ribonucleoprotein particles. Curr. Opin. Struct. Biol. 9 (1999) 222-230
42. Kim E., Goren A., and Ast G. Insights into the connection between cancer and alternative splicing. Trends Genet. 24 (2008) 7-10
43. Kim J.K., Gabel H.W., Kamath R.S., Tewari M., Pasquinelli A., Rual J.F., Kennedy S., Dybbs M., Bertin N., Kaplan J.M., Vidal M., and Ruvkun G. Functional genomic analysis of RNA interference in C. elegans. Science 308 (2005) 1164-1167
44. Kimble J., and Crittenden S.L. Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 23 (2007) 405-433
45. Kimble J.E., and Hirsh D.I. Post-embryonic cell lineages of the hermaphrodite and male gonads in C. elegans. Dev. Biol. 70 (1979) 396-417
46. Kimble J.E., and White J.G. On the control of germ cell development in Caenorhabditis elegans. Dev. Biol. 81 (1981) 208-219
47. Konishi T., Uodome N., and Sugimoto A. The Caenorhabditis elegans DDX-23, a homolog of yeast splicing factor PRP28, is required for the sperm-oocyte switch and differentiation of various cell types. Dev. Dyn. 237 (2008) 2367-2377
48. Kotake Y., Sagane K., Owa T., Mimori-Kiyosue Y., Shimizu H., Uesugi M., Ishihama Y., Iwata M., and Mizui Y. Splicing factor SF3b as a target of the antitumor natural product pladienolide. Nat. Chem. Biol. 3 (2007) 570-575
49. Kraemer B., Crittenden S., Gallegos M., Moulder G., Barstead R., Kimble J., and Wickens M. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr. Biol 9 (1999) 1009-1018
50. Lamont L.B., Crittenden S.L., Bernstein D., Wickens M., and Kimble J. FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev. Cell. 7 (2004) 697-707
51. MacDonald L.D., Knox A., and Hansen D. Proteasomal regulation of the proliferation vs. meiotic entry decision in the C. elegans germ line. Genetics 180 (2008) 905-920
52. McDonald W.H., Ohi R., Smelkova N., Frendewey D., and Gould K.L. Myb-related fission yeast cdc5p is a component of a 40S snRNP-containing complex and is essential for pre-mRNA splicing. Mol. Cell. Biol. 19 (1999) 5352-5362
53. Mumm J.S., and Kopan R. Notch signaling: from the outside in. Dev. Biol. 228 (2000) 151-165
54. Nagai K., Muto Y., Pomeranz Krummel D.A., Kambach C., Ignjatovic T., Walke S., and Kuglstatter A. Structure and assembly of the spliceosomal snRNPs. Novartis Medal Lecture. Biochem. Soc. Trans. 29 (2001) 15-26
55. Nasmyth K., and Nurse P. Cell division cycle mutants altered in DNA replication and mitosis in the fission yeast Schizosaccharomyces pombe. Mol. Gen. Genet. 182 (1981) 119-124
56. Oh J.J., Razfar A., Delgado I., Reed R.A., Malkina A., Boctor B., and Slamon D.J. 3p21.3 tumor suppressor gene H37/Luca15/RBM5 inhibits growth of human lung cancer cells through cell cycle arrest and apoptosis. Cancer Res. 66 (2006) 3419-3427
57. Ohi R., McCollum D., Hirani B., Den Haese G.J., Zhang X., Burke J.D., Turner K., and Gould K.L. The Schizosaccharomyces pombe cdc5+ gene encodes an essential protein with homology to c-Myb. Embo. J. 13 (1994) 471-483
58. Pacheco T.R., Moita L.F., Gomes A.Q., Hacohen N., and Carmo-Fonseca M. RNA interference knockdown of hU2AF35 impairs cell cycle progression and modulates alternative splicing of Cdc25 transcripts. Mol. Biol. Cell 17 (2006) 4187-4199
59. Pasierbek P., Jantsch M., Melcher M., Schleiffer A., Schweizer D., and Loidl J. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev. 15 (2001) 1349-1360
60. Pepper A.S., Killian D.J., and Hubbard E.J. Genetic analysis of Caenorhabditis elegans glp-1 mutants suggests receptor interaction or competition. Genetics 163 (2003) 115-132
61. Petcherski A.G., and Kimble J. LAG-3 is a putative transcriptional activator in the C. elegans Notch pathway. Nature 405 (2000) 364-368
62. Puoti A., and Kimble J. The Caenorhabditis elegans sex determination gene mog-1 encodes a member of the DEAH-Box protein family. Mol. Cell. Biol. 19 (1999) 2189-2197
63. Puoti A., and Kimble J. The hermaphrodite sperm/oocyte switch requires the Caenorhabditis elegans homologs of PRP2 and PRP22. Proc. Natl. Acad. Sci. USA 97 (2000) 3276-3281
64. Qiao L., Lissemore J.L., Shu P., Smardon A., Gelber M.B., and Maine E.M. Enhancers of glp-1, a gene required for cell-signaling in Caenorhabditis elegans, define a set of genes required for germline development. Genetics 141 (1995) 551-569
65. Reidt U., Wahl M.C., Fasshauer D., Horowitz D.S., Luhrmann R., and Ficner R. Crystal structure of a complex between human spliceosomal cyclophilin H and a U4/U6 snRNP-60K peptide. J. Mol. Biol. 331 (2003) 45-56
66. Ritchie W., Granjeaud S., Puthier D., and Gautheret D. Entropy measures quantify global splicing disorders in cancer. PLoS Comput. Biol. 4 (2008) e1000011
67. Roychoudhury, P., Chaudhuri, K. 2007. Evidence for heterogeneous nuclear ribonucleoprotein K overexpression in oral squamous cell carcinoma. Br. J. Cancer 97, 574-575; (author reply 576).
68. Shitashige M., Naishiro Y., Idogawa M., Honda K., Ono M., Hirohashi S., and Yamada T. Involvement of splicing factor-1 in beta-catenin/T-cell factor-4-mediated gene transactivation and pre-mRNA splicing. Gastroenterology 132 (2007) 1039-1054
69. Shitashige M., Satow R., Honda K., Ono M., Hirohashi S., and Yamada T. Increased susceptibility of Sf1(+/-) mice to azoxymethane-induced colon tumorigenesis. Cancer Sci. 98 (2007) 1862-1867
70. Srebrow A., and Kornblihtt A.R. The connection between splicing and cancer. J. Cell. Sci. 119 (2006) 2635-2641
71. Staley J.P., and Guthrie C. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92 (1998) 315-326
72. Sternberg, P.W. 2005. Vulval development. In: T.C.e.R. (Ed.), Community, WormBook, WormBook.
73. Tax F.E., Yeargers J.J., and Thomas J.H. Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature 368 (1994) 150-154
74. Teigelkamp S., Achsel T., Mundt C., Gothel S.F., Cronshagen U., Lane W.S., Marahiel M., and Luhrmann R. The 20 kD protein of human [U4/U6.U5] tri-snRNPs is a novel cyclophilin that forms a complex with the U4/U6-specific 60 kD and 90 kD proteins. RNA 4 (1998) 127-141
75. Timmons L., and Fire A. Specific interference by ingested dsRNA. Nature 395 (1998) 854
76. Venables J.P. Unbalanced alternative splicing and its significance in cancer. Bioessays 28 (2006) 378-386
77. Wang G.S., and Cooper T.A. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat. Rev. Genet. 8 (2007) 749-761
78. Wicks S.R., Yeh R.T., Gish W.R., Waterston R.H., and Plasterk R.H. Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28 (2001) 160-164
79. Zetka M.C., Kawasaki I., Strome S., and Muller F. Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev. 13 (1999) 2258-2270