The TRIM-NHL protein LIN-41 and the OMA RNA-binding proteins antagonistically control the prophase-to-metaphase transition and growth of caenorhabditis elegans oocytes

Genetics

Volumn 198, Issue 4, 2014, Pages 1535-1558

  Spike, Caroline A ^a   Coetzee, Donna ^a   Eichten, Carly ^a   Wang, Xin ^b   Hansen, Dave ^b   Greenstein, David ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CDC25.3 PHOSPHATASE; CYCLIN DEPENDENT KINASE 1; LIN 41 PROTEIN; OMA 1 PROTEIN; OMA 2 PROTEIN; PROTEIN TYROSINE PHOSPHATASE; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CARRIER PROTEIN; LIN-41 PROTEIN, C ELEGANS; OMA-1 PROTEIN, C ELEGANS; OMA-2 PROTEIN, C ELEGANS; TRANSCRIPTION FACTOR;

ADULT; ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL MATURATION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DIPLOTENE; EMBRYO; ENZYME ACTIVATION; FEMALE; GENETIC ANALYSIS; GERM LINE; HERMAPHRODITE; M PHASE CELL CYCLE CHECKPOINT; METAPHASE; NONHUMAN; OOCYTE CELLULARIZATION; OOCYTE DEVELOPMENT; PACHYTENE; PHENOTYPE; PROPHASE; TRANSLATION REGULATION; YOUNG ADULT; ANIMAL; CELL CYCLE; CHEMISTRY; FERTILITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE ORDER; GENETICS; GENOTYPE; MALE; MEIOSIS; METABOLISM; MUTATION; NONDISJUNCTION; OOCYTE; PROTEIN DOMAIN; RNA SPLICING; SPERMATOGENESIS;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CDC2 PROTEIN KINASE; CELL CYCLE; FEMALE; FERTILITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE ORDER; GENETIC LOCI; GENOTYPE; MALE; MEIOSIS; METAPHASE; MUTATION; NONDISJUNCTION, GENETIC; OOCYTES; OOGENESIS; PROPHASE; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA SPLICING; RNA-BINDING PROTEINS; SPERMATOGENESIS; TRANSCRIPTION FACTORS;

EID: 84915745497     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.168831     Document Type: Article

References (119)

1. Abrahante, J. E., A. L. Daul, M. Li, M. L. Volk, J. M. Tennessen et al., 2003 The Caenorhabditis elegans hunchback-like gene lin-57/ hbl-1 controls developmental time and is regulated by micro- RNAs. Dev. Cell 4: 625-637.
2. Albertson, D. G., and J. N. Thomson, 1993 Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1: 15-26.
3. Altun-Gultekin, Z., Y. Andachi, E. L. Tsalik, D. Pilgrim, Y. Kohara et al., 2001 A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128: 1951- 1969.
4. Amini, R., E. Goupil, S. Labella, M. Zetka, A. S. Maddox et al., 2014 C. elegans Anillin proteins regulate intercellular bridge stability and germline syncytial organization. J. Cell Biol. 206: 129-143.
5. Ashcroft, N., and A. Golden, 2002 CDC-25.1 regulates germline proliferation in Caenorhabditis elegans. Genesis 33: 1-7.
6. Ashcroft, N. R., M. Srayko, M. E. Kosinski, P. E. Mains, and A. Golden, 1999 RNA-mediated interference of a cdc25 homolog in Caenorhabditis elegans results in defects in embryonic cortical membrane, meiosis, and mitosis. Dev. Biol. 206: 15-32.
7. Austin, J., and J. Kimble, 1987 glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51: 589-599.
8. Bagga, S., J. Bracht, S. Hunter, K. Massirer, J. Holtz et al., 2005 Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122: 553-563.
9. Bettinger, J. C., K. Lee, and A. E. Rougvie, 1996 Stage-specific accumulation of the terminal differentiation factor LIN-29 during Caenorhabditis elegans development. Development 122: 2517-2527.
10. 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.
11. Boxem, M., D. G. Srinivasan, and S. van den Heuvel, 1999 The Caenorhabditis elegans gene ncc-1 encodes a cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase. Development 126: 2227-2239.
12. Brodigan, T. M., J. Liu, M. Park, E. T. Kipreos, and M. Krause, 2003 Cyclin E expression during development in Caenorhabditis elegans. Dev. Biol. 254: 102-115.
13. Burrows, A. E., B. K. Sceurman, M. E. Kosinski, C. T. Richie, P. L. Sadler et al., 2006 The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 133: 697- 709.
14. Chase, D., C. Serafinas, N. Ashcroft, M. Kosinski, D. Longo et al., 2000 The polo-like kinase PLK-1 is required for nuclear envelope breakdown and the completion of meiosis in Caenorhabditis elegans. Genesis 26: 26-41.
15. Cheeseman, I. M., and A. Desai, 2005 A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci. STKE 2005: pl1.
16. Clucas, C., J. Cabello, I. Büssing, R. Schnabel, and I. L. Johnstone, 2002 Oncogenic potential of a C. elegans cdc25 gene is demonstrated by a gain-of-function allele. EMBO J. 21: 665-674.
17. Colaiácovo, M., A. J. MacQueen, E. Martinez-Perez, K. McDonald, A. Adamo et al., 2003 Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell 5: 463-474.
18. Del Rio-Albrechtsen, T., K. Kiontke, S. Y. Chiou, and D. H. Fitch, 2006 Novel gain-of-function alleles demonstrate a role for the heterochronic gene lin-41 in C. elegans male tail tip morphogenesis. Dev. Biol. 297: 74-86.
19. Detwiler, M. R., M. Reuben, X. Li, E. Rogers, and R. Lin, 2001 Two zinc finger proteins, OMA-1 and OMA-2, are redundantly required for oocyte maturation in C. elegans. Dev. Cell 1: 187-199.
20. Dickinson, D. J., J. D. Ward, D. J. Reiner, and B. Goldstein, 2013 Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods 10: 1028-1034.
21. Downs, S. M., 2010 Regulation of the G2/M transition in rodent oocytes. Mol. Reprod. Dev. 77: 566-585.
22. Ecsedi, M., and H. Grosshans, 2013 LIN-41/TRIM71: emancipation of a miRNA target. Genes Dev. 27: 581-589.
23. Ellis, R., and T. Schedl, 2007 Sex determination in the germ line (March 5, 2007), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.82.2, http:// www.wormbook.org.
24. Ellis, R. E., and G. M. Stanfield, 2014 The regulation of spermatogenesis and sperm function in nematodes. Semin. Cell Dev. Biol. 29C: 17-30.
25. Fox, P. M., V. E. Vought, M. Hanazawa, M. H. Lee, E. M. 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.
26. Francis, R., E. Maine, and T. Schedl, 1995a 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.
27. Francis, R., M. K. Barton, J. Kimble, and T. Schedl, 1995b gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139: 579-606.
28. Friedland, A. E., Y. B. Tzur, K. M. Esvelt, M. P. Colaiácovo, G. M. Church et al., 2013 Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat. Methods 10: 741-743.
29. Furuta, T., S. Tuck, J. Kirchner, B. Koch, R. Auty et al., 2000 EMB- 30: an APC4 homologue required for metaphase-to-anaphase transitions during meiosis and mitosis in Caenorhabditis elegans. Mol. Biol. Cell 11: 1401-1419.
30. Gartner, A., S. Milstein, S. Ahmed, J. Hodgkin, and M. O. Hengartner, 2000 A conserved checkpoint pathway mediates DNA damageinduced apoptosis and cell cycle arrest in C. elegans. Mol. Cell 5: 435-443.
31. Gartner, A., A. J. MacQueen, and A. Villeneuve, 2004 Methods for analyzing checkpoint responses in Caenorhabditis elegans. Methods Mol. Biol. 280: 257-274.
32. Gibert, M. A., J. Starck, and B. Beguet, 1984 Role of the gonad cytoplasmic core during oogenesis of the nematode Caenorhabditis elegans. Biol. Cell 50: 77-85.
33. Govindan, J. A., H. Cheng, J. E. Harris, and D. Greenstein, 2006 Galphao/i and Galphas signaling function in parallel with the MSP/Eph receptor to control meiotic diapause in C. elegans. Curr. Biol. 16: 1257-1268.
34. Govindan, J. A., S. Nadarajan, S. Kim, T. A. Starich, and D. Greenstein, 2009 Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in C. elegans. Development 136: 2211-2221.
35. Grant, B., and D. Hirsh, 1999 Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10: 4311- 4326.
36. Gumienny, T. L., E. Lambie, E. Hartwieg, H. R. Horvitz, and M. O. Hengartner, 1999 Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126: 1011-1022.
37. Hansen, D., and T. Schedl, 2013 Stem cell proliferation versus meiotic fate decision in Caenorhabditis elegans. Adv. Exp. Med. Biol. 757: 71-99.
38. Hansen, D., E. J. Hubbard, and T. Schedl, 2004a Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev. Biol. 268: 342-357.
39. Hansen, D., L. Wilson-Berry, T. Dang, and T. Schedl, 2004b Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131: 93-104.
40. Harris, D. T., and H. R. Horvitz, 2011 MAB-10/NAB acts with LIN- 29/EGR to regulate terminal differentiation and the transition from larva to adult in C. elegans. Development 138: 4051-4062.
41. Harris, J. E., J. A. Govindan, I. Yamamoto, J. Schwartz, I. Kaverina et al., 2006 Major sperm protein signaling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans. Dev. Biol. 299: 105-121.
42. Hirsh, D., D. Oppenheim, and M. Klass, 1976 Development of the reproductive system of Caenorhabditis elegans. Dev. Biol. 49: 200-219.
43. Hodgkin, J., H. R. Horvitz, and S. Brenner, 1979 Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91: 67-94.
44. Hsu, J. Y., Z. W. Sun, X. Li, M. Reuben, K. Tatchell et al., 2000 Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102: 279-291.
45. Italiano, J. E., T. M. Roberts, M. Stewart, and C. A. Fontana, 1996 Reconstitution in vitro of the motile apparatus from the amoeboid sperm of Ascaris shows that filament assembly and bundling move membranes. Cell 84: 105-114.
46. Ito, K., and J. D. McGhee, 1987 Parental DNA strands segregate randomly during embryonic development of Caenorhabditis elegans. Cell 48: 329-336.
47. Jaramillo-Lambert, A., Y. Harigaya, J. Vitt, A. Villeneuve, and J. Engebrecht, 2010 Meiotic errors activate checkpoints that improve gamete quality without triggering apoptosis in male germ cells. Curr. Biol. 20: 2078-2089.
48. Jones, A. R., and T. Schedl, 1995 Mutations in gld-1, a female germ cell-specific tumor suppressor gene in Caenorhabditis elegans, affects a conserved domain also found in Src-associated protein Sam68. Genes Dev. 9: 1491-1504.
49. 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: 165-183.
50. Kadyk, L. C., and J. Kimble, 1998 Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125: 1803- 1813.
51. Karashima, T., A. Sugimoto, and M. Yamamoto, 2000 Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127: 1069-1079.
52. Kelly, W. G., C. E. Schaner, A. F. Dernburg, M. H. Lee, S. K. Kim et al., 2002 X-chromosome silencing in the germline of C. elegans. Development 129: 479-492.
53. Kim, J., A. R. Lee, I. Kawasaki, S. Strome, and Y. H. Shim, 2009 A mutation of cdc-25.1 causes defects in germ cells but not in somatic tissues in C. elegans. Mol. Cells 28: 43-48.
54. Kim, J., I. Kawasaki, and Y. H. Shim, 2010a cdc-25.2, a C. elegans ortholog of cdc25, is required to promote oocyte maturation. J. Cell Sci. 123: 993-1000.
55. Kim, K. W., T. L. Wilson, and J. Kimble, 2010b GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program. Proc. Natl. Acad. Sci. USA 107: 17445-17450.
56. Kim, S., C. Spike, and D. Greenstein, 2013 Control of oocyte growth and meiotic maturation in Caenorhabditis elegans. Adv. Exp. Med. Biol. 757: 277-320.
57. Kosinski, M., K. McDonald, J. Schwartz, I. Yamamoto, and D. Greenstein, 2005 C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes. Development 132: 3357-3369.
58. Kumsta, C., and M. Hansen, 2012 C. elegans rrf-1 mutations maintain RNAi efficiency in the soma in addition to the germline. PLoS ONE 7: e35428.
59. Lancman, J. J., N. C. Caruccio, B. D. Harfe, A. E. Pasquinelli, J. J. Schageman et al., 2005 Analysis of the regulation of lin-41 during chick and mouse limb development. Dev. Dyn. 234: 948-960.
60. Lau, N. C., L. P. Lim, E. G. Weinstein, and D. P. Bartel, 2001 An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294: 858-862.
61. Lee, M. H., and T. Schedl, 2001 Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev. 15: 2408- 2420.
62. Lee, M. H., and T. Schedl, 2004 Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans. Genes Dev. 18: 1047-1059.
63. Lee, M. H., M. Ohmachi, S. Arur, S. Nayak, R. Francis et al., 2007 Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development. Genetics 177: 2039-2062.
64. Leidel, S., M. Delattre, L. Cerutti, K. Baumer, and P. Gönczy, 2005 SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nat. Cell Biol. 7: 115-125.
65. Lesch, B. J., and D. C. Page, 2012 Genetics of germ cell development. Nat. Rev. Genet. 13: 781-794.
66. Liu, J., T. Rolef Ben-Shahar, D. Riemer, M. Treinin, P. Spann et al., 2000 Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol. Biol. Cell 11: 3937- 3947.
67. Liu, Z. C., and V. Ambros, 1991 Alternative temporal control systems for hypodermal cell differentiation in Caenorhabditis elegans. Nature 350: 162-165.
68. Loedige, I., D. Gaidatzis, R. Sack, G. Meister, and W. Filipowicz, 2013 The mammalian TRIM-NHL protein TRIM71/LIN-41 is a repressor of mRNA function. Nucleic Acids Res. 41: 518-532.
69. Loedige, I., M. Stotz, S. Qamar, K. Kramer, J. Hennig et al., 2014 The NHL domain of BRAT is an RNA-binding domain that directly contacts the hunchback mRNA for regulation. Genes Dev. 28: 749-764.
70. MacQueen, A. J., M. P. Colaiácovo, K. McDonald, and A. M. Villeneuve, 2002 Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 16: 2428-2442.
71. Maddox, A. S., B. Habermann, A. Desai, and K. Oegema, 2005 Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 132: 2837-2848.
72. Maduro, M., and D. Pilgrim, 1995 Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141: 977-988.
73. Maller Schulman, B. R., X. Liang, C. Stahlhut, C. DelConte, G. Stefani et al., 2008 The let-7 microRNA target gene, Mlin41/ Trim71, is required for mouse embryonic survival and neural tube closure. Cell Cycle 7: 3935-3942.
74. Maruyama, R., S. Endo, A. Sugimoto, and M. Yamamoto, 2005 Caenorhabditis elegans DAZ-1 is expressed in proliferating germ cells and directs proper nuclear organization and cytoplasmic core formation during oogenesis. Dev. Biol. 277: 142-154.
75. Masui, Y., 2001 From oocyte maturation to the in vitro cell cycle: the history of discoveries of maturation-promoting factor (MPF) and cytostatic factor (CSF). Differentiation 69: 1-17.
76. Masui, Y., and H. J. Clarke, 1979 Oocyte maturation. Int. Rev. Cytol. 57: 185-282.
77. McCarter, J., B. Bartlett, T. Dang, and T. Schedl, 1999 On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205: 111-128.
78. McNally, K., A. Audhya, K. Oegema, and F. J. McNally, 2006 Katanin controls mitotic and meiotic spindle length. J. Cell Biol. 175: 881-891.
79. Mikeladze-Dvali, T., L. von Tobel, P. Strnad, G. Knott, H. Leonhardt et al., 2012 Analysis of centriole elimination during C. elegans oogenesis. Development 139: 1670-1679.
80. Miller, M. A., V. Q. Nguyen, M. H. Lee, M. Kosinski, T. Schedl et al., 2001 A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291: 2144-2147.
81. Nabeshima, K., A. M. Villeneuve, and M. P. Colaiácovo, 2005 Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J. Cell Biol. 168: 683-689.
82. Nadarajan, S., J. A. Govindan, M. McGovern, E. J. A. Hubbard, and D. Greenstein, 2009 MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans. Development 136: 2223-2234.
83. Nurse, P., 1990 Universal control mechanism regulating onset of M-phase. Nature 344: 503-508.
84. Otori, M., T. Karashima, and M. Yamamoto, 2006 The Caenorhabditis elegans homologue of deleted in azoospermia is involved in the sperm/oocyte switch. Mol. Biol. Cell 17: 3147-3155.
85. 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.
86. Pellettieri, J., V. Reinke, S. K. Kim, and G. Seydoux, 2003 Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev. Cell 5: 451- 462.
87. Reinhart, B. J., F. J. Slack, M. Basson, A. E. Pasquinelli, J. C. Bettinger et al., 2000 The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403: 901-906.
88. Robertson, S., and R. Lin, 2013 The oocyte-to-embryo transition. Adv. Exp. Med. Biol. 757: 351-372.
89. Rose, A. M., and D. L. Baillie, 1979 The effect of temperature and parental age on recombination and nondisjunction in Caenorhabditis elegans. Genetics 92: 409-418.
90. Rose, K. L., V. P. Winfrey, L. H. Hoffman, D. H. Hall, T. Furuta et al., 1997 The POU gene ceh-18 promotes gonadal sheath cell differentiation and function required for meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 192: 59-77.
91. Rougvie, A. E., and V. Ambros, 1995 The heterochronic gene lin- 29 encodes a zinc finger protein that controls a terminal differentiation event in Caenorhabditis elegans. Development 121: 2491-2500.
92. Rougvie, A. E., and E. G. Moss, 2013 Developmental transitions in C. elegans larval stages. Curr. Top. Dev. Biol. 105: 153-180.
93. Rybak, A., H. Fuchs, K. Hadian, L. Smirnova, E. A. Wulczyn et al., 2009 The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nat. Cell Biol. 11: 1411-1420.
94. Schedl, T., and J. Kimble, 1988 fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119: 43-61.
95. Schisa, J. A., J. N. Pitt, and J. R. Priess, 2001 Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 128: 1287-1298.
96. Schulman, B. R., A. Esquela-Kerscher, and F. J. Slack, 2005 Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis. Dev. Dyn. 234: 1046-1054.
97. Schumacher, B., M. Hanazawa, M. H. Lee, S. Nayak, K. Volkmann et al., 2005 Translational repression of C. elegans p53 by GLD- 1 regulates DNA damage-induced apoptosis. Cell 120: 357-368.
98. Sijen, T., J. Fleenor, F. Simmer, K. L. Thijssen, S. Parrish et al., 2001 On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107: 465-476.
99. Slack, F. J., M. Basson, Z. Liu, V. Ambros, H. R. Horvitz et al., 2000 The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell 5: 659-669.
100. Spike, C. A., D. Coetzee, Y. Nishi, T. Guven-Ozkan, M. Oldenbroek et al., 2014 Translational control of the oogenic program by components of OMA ribonucleoprotein particles in Caenorhabditis elegans. Genetics 198: 1513-1533.
101. Starck, J., 1977 Radioautographic study of RNA synthesis in Caenorhabditis elegans (Bergerac variety) oogenesis. Biol. Cell. 30: 181-182.
102. Stinchcomb, D. T., J. E. Shaw, S. H. Carr, and D. Hirsh, 1985 Extrachromosomal DNA transformation of Caenorhabditis elegans. Mol. Cell. Biol. 5: 3484-3496.
103. 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.
104. Timmons, L., and A. Fire, 1998 Specific interference by ingested dsRNA. Nature 395: 854.
105. Tocchini, C., J. J. Keusch, S. B. Miller, S. Finger, H. Gut et al., 2014 The TRIM-NHL protein LIN-41 controls the onset of developmental plasticity in Caenorhabditis elegans. PLoS Genet. 10: e1004533.
106. Tursun, B., L. Cochella, I. Carrera, and O. Hobert, 2009 A toolkit and robust pipeline for the generation of fosmid-based reporter genes in C. elegans. PLoS ONE 4(3): e4625.
107. Tzur, Y. B., A. E. Friedland, S. Nadarajan, G. M. Church, J. A. Calarco et al., 2013 Heritable custom genomic modifications in Caenorhabditis elegans via a CRISPR-Cas9 system. Genetics 195: 1181-1185.
108. Vella, M. C., E. Y. Choi, S. Y. Lin, K. Reinert, and F. J. Slack, 2004 The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 39UTR. Genes Dev. 18: 132-137.
109. Vladia, B., K. Kemper, J. Alaimo, C. Heine, and E. G. Moss, 2012 lin-28 controls the succession of cell fate choices via two distinct activities. PLoS Genet. 8: e1002588.
110. Walker, A. K., P. R. Boag, and T. K. Blackwell, 2007 Transcription reactivation steps stimulated by oocyte maturation in C. elegans. Dev. Biol. 304: 382-393.
111. Wang, L., C. R. Eckmann, L. C. Kadyk, M. Wickens, and J. Kimble, 2002 A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419: 312-316.
112. Ward, S., and J. S. Carrel, 1979 Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev. Biol. 73: 304- 321.
113. Warming, S., N. Costantino, D. L. Court, N. A. Jenkins, and N. G. Copeland, 2005 Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 33: e36.
114. Wolke, U., E. A. Jezuit, and J. R. Priess, 2007 Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 134: 2227-2236.
115. Worringer, K. A., T. A. Rand, Y. Hayashi, S. Sami, K. Takahashi et al., 2014 The let-7/LIN-41 pathway regulates reprogramming to human induced pluripotent stem cells by controlling expression of prodifferentiation genes. Cell Stem Cell 14: 40- 52.
116. Wright, J. E., D. Gaidatzis, M. Senften, B. M. Farley, E. Westhof et al., 2011 A quantitative RNA code for mRNA target selection by the germline fate determinant GLD-1. EMBO J. 30: 533- 545.
117. Yoon, S., I. Kawasaki, and Y. H. Shim, 2012 CDC-25.1 controls the rate of germline mitotic cell cycle by counteracting WEE-1.3 and by positively regulating CDK-1 in Caenorhabditis elegans. Cell Cycle 11: 1354-1363.
118. Zetka, M. C., I. Kawasaki, S. Strome, and F. Müller, 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.
119. Zou, Y., H. Chiu, A. Zinovyeva, V. Ambros, C. F. Chuang et al., 2013 Developmental decline in neuronal regeneration by the progressive change in two intrinsic timers. Science 340: 372- 376.