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Post-Transcriptional Regulation by STAR Proteins pp 106–122Cite as

C. Elegans Star Proteins, Gld-1 And Asd-2, Regulate Specific RNA Targets to Control Development

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 693))

Abstract

A comprehensive understanding of the C. elegans STAR proteins GLD-1 and ASD-2 is emerging from a combination of studies. Those employing genetic analysis reveal in vivo function, others involving biochemical approaches pursue the identification of mRNA targets through which these proteins act. Lastly, mechanistic studies provide the molecular pathway of target mRNA regulation.

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References

  1. Francis R, Barton MK, Kimble J et al. gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 1995a; 139:579–606.

    CAS  PubMed  Google Scholar 

  2. Zarkower D. Somatic sex determination. WormBook 2006; 1–12.

    Google Scholar 

  3. Ellis R, Schedl T. Sex determination in the germ line. WormBook 2007; 1–13.

    Google Scholar 

  4. Gibert MA, Starck J, Beguet B. Role of the gonad cytoplasmic core during oogenesis of the nematode Caenorhabditis elegans. Biol Cell 1984; 50(1):77–85.

    CAS  PubMed  Google Scholar 

  5. Wolke U, Jezuit EA, Priess JR. Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 2007; 134(12):2227–2236.

    Article  CAS  PubMed  Google Scholar 

  6. Gumienny TL, Lambie E, Hartwieg E et al. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 1999; 126(5):1011–1022.

    CAS  PubMed  Google Scholar 

  7. Gartner A, Milstein S, Ahmed S et al. A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 2000; 5(3):435–443.

    Article  CAS  PubMed  Google Scholar 

  8. Francis R, Maine E, Schedl T. Analysis of multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signaling pathway. Genetics 1995b; 139:607–630.

    CAS  PubMed  Google Scholar 

  9. Jones AR, Francis R, Schedl T. GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage-and sex-specific expression during Caenorhabditis elegans germline development. Dev Biol 1996; 180:165–183.

    Article  CAS  PubMed  Google Scholar 

  10. Ciosk R, DePalma M, Priess JR. Translational regulators maintain totipotency in the Caenorhabditis elegans germline. Science 2006; 311(5762):851–853.

    Article  CAS  PubMed  Google Scholar 

  11. Biedermann B, Wright J, Senften M et al. Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Developmental Cell 2009; 17(3):355–364.

    Article  CAS  PubMed  Google Scholar 

  12. Schumacher B, Hanazawa M, Lee MH et al. Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis. Cell 2005; 120(3):357–368.

    Article  CAS  PubMed  Google Scholar 

  13. Kadyk LC, Kimble J. Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 1998; 125(10):1803–1813.

    CAS  PubMed  Google Scholar 

  14. Eckmann CR, Crittenden SL, Suh N et al. GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 2004; 168(1):147–160.

    Article  CAS  PubMed  Google Scholar 

  15. Hansen D, Wilson-Berry L, Dang T et al. Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 2004a; 131(1):93–104.

    Article  CAS  PubMed  Google Scholar 

  16. Austin J, Kimble J. glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 1987; 51(4):589–599.

    Article  CAS  PubMed  Google Scholar 

  17. Hansen D, Schedl T. The regulatory network controlling the proliferation-meiotic entry decision in the Caenorhabditis elegans germ line. Curr Top Dev Biol 2006; 76:185–215.

    Article  CAS  PubMed  Google Scholar 

  18. Kimble J, Crittenden SL. Controls of germline stem cells, entry into meiosis and the sperm/oocyte decision in Caenorhabditis elegans. Annu Rev Cell Dev Biol 2007; 23:405–433.

    Article  CAS  PubMed  Google Scholar 

  19. Jones AR, Schedl T. Mutations in gld-1, a female germ cell-specific tumor suppressor gene in Caenorhabditis elegans, affect a conserved domain also found in Src-associated protein Sam68. Genes Dev 1995; 9:1491–1504.

    Article  CAS  PubMed  Google Scholar 

  20. Gibson TJ, Rice PM, Thompson JD et al. KH domains within the FMR1 sequence suggest that fragile X syndrome stems from a defect in RNA metabolism. Trends Biochem Sci 1993; 18(9):331–333.

    Article  CAS  PubMed  Google Scholar 

  21. Musco G, Stier G, Joseph C et al. Three-dimensional structure and stability of the KH domain: molecular insights into the fragile X syndrome. Cell 1996; 85(2):237–245.

    Article  CAS  PubMed  Google Scholar 

  22. Lewis HA, Musunuru K, Jensen KB et al. Sequence-specific RNA binding by a Nova KH domain: implications for paraneoplastic disease and the fragile X syndrome. Cell 2000; 100(3):323–332.

    Article  CAS  PubMed  Google Scholar 

  23. Di Fruscio M, Chen T, Bonyadi S et al. The identification of two Drosophila KH domain proteins: KEP1 and SAM are members of the Sam68 family of GSG domain proteins. J Biol Chem 1998; 273:30122–30130.

    Article  PubMed  Google Scholar 

  24. Vernet C, Artzt K. STAR, a gene family involved in signal transduction and activation of RNA. Trends Genet 1997; 13(12):479–484.

    Article  CAS  PubMed  Google Scholar 

  25. Lehmann-Blount KA, Williamson JR. Shape-specific nucleotide binding of single-stranded RNA by the GLD-1 STAR domain. J Mol Biol 2005; 346(1):91–104.

    Article  CAS  PubMed  Google Scholar 

  26. Lee MH, Schedl T. Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev 2001; 15(18):2408–2420.

    Article  CAS  PubMed  Google Scholar 

  27. Lee MH, Schedl T. Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans. Genes Dev 2004; 18(9):1047–1059.

    Article  CAS  PubMed  Google Scholar 

  28. Jan E, Motzny CK, Graves LE et al. The STAR protein, GLD-1, is a translational regulator of sexual identity in C. elegans. EMBO J 1999; 18:258–269.

    Article  CAS  PubMed  Google Scholar 

  29. Xu L, Paulsen J, Yoo Y et al. Caenorhabditis elegans MES-3 is a target of GLD-1 and functions epigenetically in germline development. Genetics 2001; 159(3):1007–1017.

    CAS  PubMed  Google Scholar 

  30. Marin VA, Evans TC. Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 2003; 130(12):2623–2632.

    Article  CAS  PubMed  Google Scholar 

  31. Mootz D, Ho DM, Hunter CP. The STAR/Maxi-KH domain protein GLD-1 mediates a developmental switch in the translational control of C. elegans PAL-1. Development 2004; 131(14):3263–3272.

    Article  CAS  PubMed  Google Scholar 

  32. Evans TC, Hunter CP. Translational control of maternal RNAs. WormBook 2005; 1–11.

    Google Scholar 

  33. Lublin AL, Evans TC. The RNA-binding proteins PUF-5, PUF-6 and PUF-7 reveal multiple systems for maternal mRNA regulation during C. elegans oogenesis. Dev Biol 2007; 303(2):635–649.

    Article  CAS  PubMed  Google Scholar 

  34. Detwiler MR, Reuben M, Li X et al. Two zinc finger proteins, OMA-1 and OMA-2, are redundantly required for oocyte maturation in C. elegans. Dev Cell 2001; 1(2):187–199.

    Article  CAS  PubMed  Google Scholar 

  35. Nayak S, Goree J, Schedl T. fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 2005; 3(1):e6.

    Article  PubMed  Google Scholar 

  36. Hwang HC, Clurman BE. Cyclin E in normal and neoplastic cell cycles. Oncogene 2005; 24(17):2776–2786.

    Article  CAS  PubMed  Google Scholar 

  37. Lee MH, Ohmachi M, Arur S et al. Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development. Genetics 2007; 177(4):2039–2062.

    Article  CAS  PubMed  Google Scholar 

  38. Clifford R, Lee MH, Nayak S et al. FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development 2000; 127(24):5265–5276.

    CAS  PubMed  Google Scholar 

  39. Stebbins-Boaz B, Cao Q, de Moor CH et al. Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol Cell 1999; 4(6):1017–1027.

    Article  CAS  PubMed  Google Scholar 

  40. Olsen PH, Ambros V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 1999; 216(2):671–680.

    Article  CAS  PubMed  Google Scholar 

  41. Clark IE, Wyckoff D, Gavis ER. Synthesis of the posterior determinant Nanos is spatially restricted by a novel co-translational regulatory mechanism. Curr Biol 2000; 10(20):1311–1314.

    Article  CAS  PubMed  Google Scholar 

  42. Seggerson K, Tang L, Moss EG. Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev Biol 2002; 243(2):215–225.

    Article  CAS  PubMed  Google Scholar 

  43. Goodwin EB, Okkema PG, Evans TC et al. Translational regulation of tra-2 by its 3′ untranslated region controls sexual identity in C. elegans. Cell 1993; 75(2):329–339.

    Article  CAS  PubMed  Google Scholar 

  44. Kuersten S, Goodwin EB. The power of the 3′ UTR: translational control and development. Nat Rev Genet 2003; 4(8):626–637.

    Article  CAS  PubMed  Google Scholar 

  45. Zhang L, Ding L, Cheung TH et al. Systematic identification of C. elegans miRISC proteins, miRNAs and mRNA targets by their interactions with GW182 proteins AIN-1 and AIN-2. Mol Cell 2007; 28(4):598–613.

    Article  CAS  PubMed  Google Scholar 

  46. Ryder SP, Frater LA, Abramovitz DL et al. RNA target specificity of the STAR/GSG domain post-transcriptional regulatory protein GLD-1. Nat Struct Mol Biol 2004; 11(1):20–28.

    Article  CAS  PubMed  Google Scholar 

  47. Galarneau A, Richard S. The STAR RNA binding proteins GLD-1, QKI, SAM68 and SLM-2 bind bipartite RNA motifs. BMC Mol Biol 2009; 10:47.

    Article  PubMed  Google Scholar 

  48. Zhang B, Gallegos M, Puoti A et al. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 1997; 390(6659):477–484.

    Article  CAS  PubMed  Google Scholar 

  49. Crittenden SL, Bernstein DS, Bachorik JL et al. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 2002; 417(6889):660–663.

    Article  CAS  PubMed  Google Scholar 

  50. Lamont LB, Crittenden SL, Bernstein D et al. FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev Cell 2004; 7(5):697–707.

    Article  CAS  PubMed  Google Scholar 

  51. Eckmann CR, Kraemer B, Wickens M et al. GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans. Dev Cell 2002; 3(5):697–710.

    Article  CAS  PubMed  Google Scholar 

  52. Suh N, Jedamzik B, Eckmann CR et al. The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. Proc Natl Acad Sci USA 2006; 103(41):15108–15112.

    Article  CAS  PubMed  Google Scholar 

  53. Schmid M, Kuchler B, Eckmann CR. Two conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev 2009; 23(7):824–836.

    Article  CAS  PubMed  Google Scholar 

  54. Ohno G, Hagiwara M, Kuroyanagi H. STAR family RNA-binding protein ASD-2 regulates developmental switching of mutually exclusive alternative splicing in vivo. Genes Dev 2008; 22(3):360–374.

    Article  CAS  PubMed  Google Scholar 

  55. Sibley MH, Johnson JJ, Mello CC et al. Genetic identification, sequence and alternative splicing of the Caenorhabditis elegans alpha 2(IV) collagen gene. J Cell Biol 1993; 123(1):255–264.

    Article  CAS  PubMed  Google Scholar 

  56. Graham PL, Johnson JJ, Wang S et al. Type IV collagen is detectable in most, but not all, basement membranes of Caenorhabditis elegans and assembles on tissues that do not express it. J Cell Biol 1997; 137(5):1171–1183.

    Article  CAS  PubMed  Google Scholar 

  57. Grant B, Hirsh D. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 1999; 10(12):4311–4326.

    CAS  PubMed  Google Scholar 

  58. Derry WB, Putzke AP, Rothman JH. Caenorhabditis elegans p53: role in apoptosis, meiosis and stress resistance. Science 2001; 294(5542):591–595.

    Article  CAS  PubMed  Google Scholar 

  59. Shimada M, Kawahara H, Doi H. Novel family of CCCH-type zinc-finger proteins, MOE-1,-2 and-3, participates in C. elegans oocyte maturation. Genes Cells 2002; 7(9):933–947.

    Article  CAS  PubMed  Google Scholar 

  60. Johnston WL, Krizus A, Dennis JW. The eggshell is required for meiotic fidelity, polar-body extrusion and polarization of the C. elegans embryo. BMC Biol 2006; 4:35.

    Article  PubMed  Google Scholar 

  61. Olson SK, Bishop JR, Yates JR et al. Identification of novel chondroitin proteoglycans in Caenorhabditis elegans: embryonic cell division depends on CPG-1 and CPG-2. J Cell Biol 2006; 173(6):985–994.

    Article  CAS  PubMed  Google Scholar 

  62. Hansen D, Hubbard EJ, Schedl T. Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev Biol 2004b; 268(2):342–357.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, University at Albany, SUNY, Albany, New York, 12222

    Min-Ho Lee & Tim Schedl

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  1. Min-Ho Lee
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  2. Tim Schedl
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Correspondence to Min-Ho Lee .

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Editors and Affiliations

  1. Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel

    Talila Volk BSc, MSc, PhD

  2. Department of Molecular Genetics and Microbiology, Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, Texas, USA

    Karen Artzt BA, PhD

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Lee, MH., Schedl, T. (2010). C. Elegans Star Proteins, Gld-1 And Asd-2, Regulate Specific RNA Targets to Control Development. In: Volk, T., Artzt, K. (eds) Post-Transcriptional Regulation by STAR Proteins. Advances in Experimental Medicine and Biology, vol 693. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-7005-3_8

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