PUF-8, a pumilio homolog, inhibits the proliferative fate in the caenorhabditis elegans germline

G3: Genes, Genomes, Genetics

Volumn 2, Issue 10, 2012, Pages 1197-1205

  Racher, Hilary ^a   Hansen, Dave ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Germline stem cells; Notch signaling; Proliferative fate; PUF; Puf 8; Pumilio

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; GLP 1 PROTEIN, C ELEGANS; GLP-1 PROTEIN, C ELEGANS; MEMBRANE PROTEIN; NOTCH RECEPTOR; PUF 8 PROTEIN, C ELEGANS; PUF-8 PROTEIN, C ELEGANS; RNA BINDING PROTEIN;

ALLELE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; CHROMOSOME MAP; GENE EXPRESSION REGULATION; GENETICS; GERM CELL; METABOLISM; MITOSIS; PHENOTYPE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; STEM CELL;

ALLELES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL PROLIFERATION; CHROMOSOME MAPPING; GENE EXPRESSION REGULATION; GERM CELLS; MEMBRANE GLYCOPROTEINS; MITOSIS; MODELS, BIOLOGICAL; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, NOTCH; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84883203689     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.003350     Document Type: Article

References (50)

1. Ariz, M., R. Mainpal, and K. Subramaniam, 2009 C. elegans RNA-binding proteins PUF-8 and MEX-3 function redundantly to promote germline stem cell mitosis. Dev. Biol. 326: 295-304.
2. Austin, J., and J. Kimble, 1989 Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell 58: 565-571.
3. Bachorik, J. L., and J. Kimble, 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. USA 102: 10893-10897.
4. Barker, D. D., C. Wang, J. Moore, L. K. Dickinson, and R. Lehmann, 1992 Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev. 6: 2312-2326.
5. Beadell, A. V., Q. Liu, D. M. Johnson, and E. S. Haag, 2011 Independent recruitments of a translational regulator in the evolution of self-fertile nematodes. Proc. Natl. Acad. Sci. USA 108: 19672-19677.
6. Biedermann, B., J. Wright, M. Senften, I. Kalchhauser, G. Sarathy et al., 2009 Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Dev. Cell 17: 355-364.
7. Brenner, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71- 94.
8. Ciosk, R., M. DePalma, and J. R. Priess, 2006 Translational regulators maintain totipotency in the Caenorhabditis elegans germline. Science 311: 851-853.
9. Crittenden, S. L., E. R. Troemel, T. C. Evans, and J. Kimble, 1994 GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 120: 2901.
10. Crittenden, S. L., D. S. Bernstein, J. L. Bachorik, B. E. Thompson, andM.Gallegos, 2002 A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417: 660.
11. Eckmann, C., S. L. Crittenden, N. Suh, and J. Kimble, 2004 GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168: 147.
12. Forbes, A., and R. Lehmann, 1998 Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125: 679-690.
13. Fox, P. M., V. E. Vought, M. Hanazawa, M. H. Lee, E. Maine et al., 2011 Cyclin E and CDK-2 regulate proliferative cell fate and cell cycle progression in the C. elegans germline. Development 138: 2223-2234.
14. Francis, R., M. K. Barton, J. Kimble, and T. Schedl, 1995a gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139: 579-606.
15. Francis, R., E. Maine, and T. Schedl, 1995b 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: 607-630.
16. Frokjaer-Jensen, C., M. W. Davis, C. E. Hopkins, B. J. Newman, J. M. Thummel et al., 2008 Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40: 1375-1383.
17. Hansen, D., and T. Schedl, 2006 The regulatory network controlling the proliferation-meiotic entry decision in the Caenorhabditis elegans germ line. Curr. Top. Dev. Biol. 76: 185-215.
18. Hansen, D., and T. Schedl, 2013 Stem cell proliferation vs. meiotic fate decision in Caenorhabditis elegans. Adv. Exp. Med. Biol. 757: 71-99.
19. Hansen, D., E. J. Hubbard, and T. Schedl, 2004a Multi-pathway control of the proliferation vs. meiotic development decision in the Caenorhabditis elegans germline. Dev. Biol. 268: 342-357.
20. Hansen, D., L. Wilson-Berry, T. Dang, and T. Schedl, 2004b Control of the proliferation vs. meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131: 93-104.
21. Horton, R. M., 1993 In vitro recombination and mutagenesis of DNA: SOEing together tailor-made genes. Methods Mol. Biol. 15: 251-261.
22. Hubstenberger, A., S. L. Noble, C. Cameron, R. Shtofman, S. Gutman et al., 2012 A network of PUF proteins and Ras signaling promote mRNA repression and oogenesis in C. elegans. Dev. Biol. 366: 218-231.
23. Jones, A. R., and T. Schedl, 1995 Mutations in gld-1, a female germ cellspecific tumor suppressor gene in Caenorhabditis elegans, affect a conserved domain also found in Src-associated protein Sam68. Genes Dev. 9: 1491-1504.
24. Jones, A. R., R. Francis, and T. Schedl, 1996 GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 180: 165.
25. Kadyk, L. C., and J. Kimble, 1998 Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125: 1803-1813.
26. Kerins, J. A., M. Hanazawa, M. Dorsett, and T. Schedl, 2010 PRP-17 and the pre-mRNA splicing pathway are preferentially required for the proliferation vs. meiotic development decision and germline sex determination in Caenorhabditis elegans. Dev. Dyn. 239: 1555-1572.
27. Killian, D. J., and E. J. Hubbard, 2005 Caenorhabditis elegans germline patterning requires coordinated development of the somatic gonadal sheath and the germ line. Dev. Biol. 279: 322-335.
28. Kimble, J., and S. L. Crittenden, 2007 Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 23: 405-433.
29. Lamont, L. B., S. L. Crittenden, D. Bernstein, M. Wickens, and J. Kimble, 2004 FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev. Cell 7: 697-707.
30. Lin, H., and A. C. Spradling, 1997 A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124: 2463-2476.
31. Lublin, A. L., and T. C. Evans, 2007 The RNA-binding proteins PUF-5, PUF-6, and PUF-7 reveal multiple systems for maternal mRNA regulation during C. elegans oogenesis. Dev. Biol. 303: 635-649.
32. Macdonald, P. M., 1992 The Drosophila pumilio gene: an unusually long transcription unit and an unusual protein. Development 114: 221-232.
33. Mainpal, R., A. Priti, and K. Subramaniam, 2011 PUF-8 suppresses the somatic transcription factor PAL-1 expression in C. elegans germline stem cells. Dev. Biol. 360: 195-207.
34. Mantina, P., L. Macdonald, A. Kulaga, L. Zhao, and D. Hansen, 2009 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. Mech. Dev. 126: 417-429.
35. Murata, Y., and R. P. Wharton, 1995 Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80: 747-756.
36. Pasierbek, P., M. Jantsch, M. Melcher, A. Schleiffer, D. Schweizer et al., 2001 A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev. 15: 1349-1360.
37. Quenault, T., T. Lithgow, and A. Traven, 2011 PUF proteins: repression, activation and mRNA localization. Trends Cell Biol. 21: 104-112.
38. Spassov, D. S., and R. Jurecic, 2003 Mouse Pum1 and Pum2 genes, members of the Pumilio family of RNA-binding proteins, show differential expression in fetal and adult hematopoietic stem cells and progenitors. Blood Cells Mol. Dis. 30: 55-69.
39. Stumpf, C. R., J. Kimble, and M. Wickens, 2008 A Caenorhabditis elegans PUF protein family with distinct RNA binding specificity. RNA 14: 1550-1557.
40. Subramaniam, K., and G. Seydoux, 2003 Dedifferentiation of primary spermatocytes into germ cell tumors in C. elegans lacking the pumilio-like protein PUF-8. Curr. Biol. 13: 134-139.
41. Suh, N., S. L. Crittenden, A. Goldstrohm, B. Hook, B. Thompson et al., 2009 FBF and its dual control of gld-1 expression in the Caenorhabditis elegans germline. Genetics 181: 1249-1260.
42. Tautz, D., 1988 Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature 332: 281-284.
43. Varkey, J. P., P. L. Jansma, A. N. Minniti, and S. Ward, 1993 The Caenorhabditis elegans spe-6 gene is required for major sperm protein assembly and shows second site non-complementation with an unlinked deficiency. Genetics 133: 79-86.
44. Walser, C. B., G. Battu, E. F. Hoier, and A. Hajnal, 2006 Distinct roles of the Pumilio and FBF translational repressors during C. elegans vulval development. Development 133: 3461-3471.
45. Wang, C., L. Wilson-Berry, T. Schedl, and D. Hansen, 2012 TEG-1 CD2BP2 regulates stem cell proliferation and sex determination in the C. elegans germ line and physically interacts with the UAF-1 U2AF65 splicing factor. Dev. Dyn. 241: 505-521.
46. Wickens, M., D. S. Bernstein, J. Kimble, and R. Parker, 2002 A PUF family portrait: 39UTR regulation as a way of life. Trends Genet. 18: 150-157.
47. Xu, E. Y., R. Chang, N. A. Salmon, and R. A. Reijo Pera, 2007 A gene trap mutation of a murine homolog of the Drosophila stem cell factor Pumilio results in smaller testes but does not affect litter size or fertility. Mol. Reprod. Dev. 74: 912-921.
48. Yochem, J., and I. Greenwald, 1989 glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. Cell 58: 553-563.
49. Zetka, M. C., I. Kawasaki, S. Strome, and F. Muller, 1999 Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev. 13: 2258-2270.
50. Zhang, B., M. Gallegos, A. Puoti, E. Durkin, S. Fields et al., 1997 A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390: 477-484.