505
Views
2
CrossRef citations to date
0
Altmetric
Review

Elucidating Gene Regulatory Mechanisms for Sperm Function Through the Integration of Classical and Systems Approaches in C. elegans

, , &
Pages 222-235 | Received 18 Nov 2009, Accepted 16 Jan 2010, Published online: 10 Jun 2010

REFERENCES

  • Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., et al. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442:203–207.
  • Aravin, A. A., Hannon, G. J. and Brennecke, J. (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318:761–764.
  • Bamps, S. and Hope, I. A. (2008) Large-scale gene expression pattern analysis, in situ, in Caenorhabditis elegans. Brief Funct Genomic Proteomic 7:175–183.
  • Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297.
  • Barton, M. K. and Kimble, J. (1990) fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 125:29–39.
  • Barton, M. K., Schedl, T. B. and Kimble, J. (1987) Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics 115:107–119.
  • Batista, P. J., Ruby, J. G., Claycomb, J. M., Chiang, R., Fahlgren, N., Kasschau, K. D., et al. (2008) PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell 31:67–78.
  • Bean, C. J., Schaner, C. E. and Kelly, W. G. (2004) Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nat Genet 36:100–105.
  • Beanan, M. J. and Strome, S. (1992) Characterization of a germ-line proliferation mutation in C. elegans. Development 116:755–766.
  • Birney, E., Stamatoyannopoulos, J. A., Dutta, A., Guigo, R., Gingeras, T. R., Margulies, et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447:799–816.
  • Boutros, M. and Ahringer, J. (2008) The art and design of genetic screens: RNA interference. Nat Rev Genet 9:554–566.
  • Braun, R. E. (2001) Packaging paternal chromosomes with protamine. Nat Genet 28:10–12.
  • Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R. and Hannon, G. J. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103.
  • Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94.
  • Byrd, D. T. and Kimble, J. (2009) Scratching the niche that controls Caenorhabditis elegans germline stem cells. Semin Cell Dev Biol.
  • C. elegans Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–2018.
  • Celniker, S. E., Dillon, L. A., Gerstein, M. B., Gunsalus, K. C., Henikoff, S., Karpen, G. H., et al. (2009) Unlocking the secrets of the genome. Nature 459:927–930.
  • Chen, N., Harris, T. W., Antoshechkin, I., Bastiani, C., Bieri, T., Blasiar, D., et al. (2005) WormBase: a comprehensive data resource for Caenorhabditis biology and genomics. Nucleic Acids Res 33:D383–389.
  • Chu, D. S., Liu, H., Nix, P., Wu, T. F., Ralston, E. J., Yates, J. R., 3rd and Meyer, B. J. (2006) Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature 443:101–105.
  • Church, D. L., Guan, K. L. and Lambie, E. J. (1995) Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 121:2525–2535.
  • Ciccone, D. N., Su, H., Hevi, S., Gay, F., Lei, H., Bajko, J., et al. (2009) KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461:415–418.
  • Dadoune, J. P., Siffroi, J. P. and Alfonsi, M. F. (2004) Transcription in haploid male germ cells. Int Rev Cytol 237:1–56.
  • Das, P. P., Bagijn, M. P., Goldstein, L. D., Woolford, J. R., Lehrbach, N. J., Sapetschnig, A., et al. (2008) Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline. Mol Cell 31:79–90.
  • del Castillo-Olivares, A., Kulkarni, M. and Smith, H. E. (2009) Regulation of sperm gene expression by the GATA factor ELT-1. Dev Biol 333:397–408.
  • Deng, W. and Lin, H.. (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2:819–830.
  • Drysdale, R. (2008) FlyBase: a database for the Drosophila research community. Methods Mol Biol 420:45–59.
  • Ellis, R and Schedl, T. (2007) Sex determination in the germ line. WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.7.1, http://www.wormbook.org.
  • Feil, R. (2009) Epigenetic asymmetry in the zygote and mammalian development. Int J Dev Biol 53:191–201.
  • Findlay, G. D., MacCoss, M. J. and Swanson, W. J. (2009) Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. Genome Res 19:886–896.
  • Findlay, G. D., Yi, X., Maccoss, M. J. and Swanson, W. J. (2008) Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol 6:e178.
  • Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811.
  • Gatewood, J. M., Cook, G. R., Balhorn, R., Schmid, C. W. and Bradbury, E. M. (1990) Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J Biol Chem 265:20662–20666.
  • Gent, J. I., Schvarzstein, M., Villeneuve, A. M., Gu, S. G., Jantsch, V., Fire, A. Z. and Baudrimont, A. (2009) A Caenorhabditis elegans RNA-directed RNA Polymerase in Sperm Development and Endogenous RNAi. Genetics.
  • Greenstein, D. (2005) Control of oocyte meiotic maturation and fertilization. WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.7.1, http://www.wormbook.org.
  • Grivna, S. T., Beyret, E., Wang, Z. and Lin, H. (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20:1709–1714.
  • Gunawardane, L. S., Saito, K., Nishida, K. M., Miyoshi, K., Kawamura, Y., Nagami, T., et al. (2007) A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315:1587–1590.
  • Han, T., Manoharan, A. P., Harkins, T. T., Bouffard, P., Fitzpatrick, C., Chu, D. S., et al. (2009) 26G endo-siRNAs regulate spermatogenic and zygotic gene expression in Caenorhabditis elegans. Proc Natl Acad Sci USA 106:18674–18679.
  • Harris, T. W., Lee, R., Schwarz, E., Bradnam, K., Lawson, D., Chen, W., et al. (2003) WormBase: a cross-species database for comparative genomics. Nucleic Acids Res 31:133–137.
  • Houwing, S., Kamminga, L. M., Berezikov, E., Cronembold, D., Girard, A., van den Elst, H., et al. (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129:69–82.
  • Joshua-Tor, L. (2006) The Argonautes. Cold Spring Harb Symp Quant Biol 71:67–72.
  • Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231–237.
  • Karr, T. L. (2007) Fruit flies and the sperm proteome. Hum Mol Genet 16 Spec No. 2:R124–133.
  • Kato, M., de Lencastre, A., Pincus, Z. and Slack, F. J. (2009) Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol 10:R54.
  • Katz, D. J., Edwards, T. M., Reinke, V. and Kelly, W. G. (2009) A C. elegans LSD1 demethylase contributes to germline immortality by reprogramming epigenetic memory. Cell 137:308–320.
  • Kelleher, E. S., Watts, T. D., LaFlamme, B. A., Haynes, P. A. and Markow, T. A. (2009) Proteomic analysis of Drosophila mojavensis male accessory glands suggests novel classes of seminal fluid proteins. Insect Biochem Mol Biol 39:366–371.
  • Kelly, W. G. and Aramayo, R. (2007) Meiotic silencing and the epigenetics of sex. Chromosome Res 15:633–651.
  • Kelly, W. G., Schaner, C. E., Dernburg, A. F., Lee, M. H., Kim, S. K., Villeneuve, A. M. and Reinke, V. (2002) X chromosome silencing in the germline of C. elegans. Development 129:479–492.
  • Kennedy, S., Wang, D. and Ruvkun, G. (2004) A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427:645–649.
  • Ketola, I., Pentikainen, V., Vaskivuo, T., Ilvesmaki, V., Herva, R., Dunkel, L., et al. (2000) Expression of transcription factor GATA-4 during human testicular development and disease. J Clin Endocrinol Metab 85:3925–3931.
  • Ketola, I., Rahman, N., Toppari, J., Bielinska, M., Porter-Tinge, S. B., Tapanainen, J. S., et al. (1999) Expression and regulation of transcription factors GATA-4 and GATA-6 in developing mouse testis. Endocrinology 140:1470–1480.
  • Kimble, J. and Crittenden, S. L. (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.
  • Klass, M., Ammons, D. and Ward, S. (1988) Conservation in the 5′ flanking sequences of transcribed members of the Caenorhabditis elegans major sperm protein gene family. J Mol Biol 199:15–22.
  • Klattenhoff, C. and Theurkauf, W. (2008) Biogenesis and germline functions of piRNAs. Development 135:3–9.
  • Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T. W., Isobe, T., Asada, N., Fujita, Y., et al. (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131:839–849.
  • L'Hernault, S. W. (2006) Spermatogenesis. WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.7.1, http://www.wormbook.org.
  • L'Hernault, S. W. (2009) The genetics and cell biology of spermatogenesis in the nematode C. elegans. Mol Cell Endocrinol 306:59–65.
  • L'Hernault, S. W. and Roberts, T. M. (1995) Cell biology of nematode sperm. Methods Cell Biol 48:273–301.
  • LaMunyon, C. W. and Ward, S. (1998) Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc R Soc Lond B Biol Sci 265:1997–2002.
  • Lee, T. L., Alba, D., Baxendale, V., Rennert, O. M. and Chan, W. Y. (2006) Application of transcriptional and biological network analyses in mouse germ-cell transcriptomes. Genomics 88:18–33.
  • Lercher, M. J., Blumenthal, T. and Hurst, L. D. (2003) Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes. Genome Res 13:238–243.
  • Li, S., Armstrong, C. M., Bertin, N., Ge, H., Milstein, S., Boxem, M., et al. (2004) A map of the interactome network of the metazoan C. elegans. Science 303:540–543.
  • Maeda, I., Kohara, Y., Yamamoto, M. and Sugimoto, A. (2001) Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 11:171–176.
  • McCarter, J., Bartlett, B., Dang, T. and Schedl, T. (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205:111–128.
  • Mello, C. C. and Conte, D., Jr. (2004) Revealing the world of RNA interference. Nature 431:338–342.
  • Merritt, C., Rasoloson, D., Ko, D. and Seydoux, G. (2008) 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 18:1476–1482.
  • Michalak, P. (2008) Coexpression, coregulation, and cofunctionality of neighboring genes in eukaryotic genomes. Genomics 91:243–248.
  • Miller, M. A. (2006) Sperm and oocyte isolation methods for biochemical and proteomic analysis. Methods Mol Biol 351:193–201.
  • Mitani, S. (2009) Nematode, an experimental animal in the national BioResource project. Exp Anim 58:351–356.
  • Moerman, D. G. and Barstead, R. J. (2008) Towards a mutation in every gene in Caenorhabditis elegans. Brief Funct Genomic Proteomic 7:195–204.
  • Nelson, G. A., Lew, K. K. and Ward, S. (1978) Intersex, a temperature-sensitive mutant of the nematode Caenorhabditis elegans. Dev Biol 66:386–409.
  • Nelson, G. A. and Ward, S. (1980) Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 19:457–464.
  • Pavelec, D. M., Lachowiec, J., Duchaine, T. F., Smith, H. E. and Kennedy, S. (2009) Requirement for ERI/DICER Complex in Endogenous RNAi and Sperm Development in Caenorhabditis elegans. Genetics.
  • Reinke, V. and Cutter, A. D. (2009) Germline expression influences operon organization in the Caenorhabditis elegans genome. Genetics 181:1219–1228.
  • Reinke, V., Gil, I. S., Ward, S. and Kazmer, K. (2004) Genome wide germline enriched and sex biased expression profiles in Caenorhabditis elegans. Development 131:311–323.
  • Reinke, V., Smith, H. E., Nance, J., Wang, J., Van Doren, C., Begley, R., et al. (2000) A global profile of germline gene expression in C. elegans. Mol Cell 6:605–616.
  • Reuben, M. and Lin, R. (2002) Germline X chromosomes exhibit contrasting patterns of histone H3 methylation in Caenorhabditis elegans. Dev Biol 245:71–82.
  • Ruby, J. G., Jan, C., Player, C., Axtell, M. J., Lee, W., Nusbaum, C., et al. (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127:1193–1207.
  • Sassone-Corsi, P. (2002) Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296:2176–2178.
  • Schaner, C. E. and Kelly, W. G. (2006) Germline Chromatin. WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.7.1, http://www.wormbook.org.
  • Sepsenwol, S., Ris, H. and Roberts, T. M. (1989) A unique cytoskeleton associated with crawling in the amoeboid sperm of the nematode, Ascaris suum. J Cell Biol 108:55–66.
  • Seydoux, G. and Schedl, T. (2001) The germline in C. elegans: origins, proliferation, and silencing. Int Rev Cytol 203:139–185.
  • Sha, K. and Fire, A. (2005) Imprinting capacity of gamete lineages in Caenorhabditis elegans. Genetics 170:1633–1652.
  • Shakes, D. C., Wu, J. C., Sadler, P. L., Laprade, K., Moore, L. L., Noritake, A. and Chu, D. S. (2009) Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet 5:e1000611.
  • Shim, Y. H., Bonner, J. J. and Blumenthal, T. (1995) Activity of a C. elegans GATA transcription factor, ELT-1, expressed in yeast. J Mol Biol 253:665–676.
  • Shim, Y. H. and Paik, Y. K. (2009) Caenorhabditis elegans proteomics comes of age. Proteomics.
  • Shiu, P. K., Raju, N. B., Zickler, D. and Metzenberg, R. L. (2001) Meiotic silencing by unpaired DNA. Cell 107:905–916.
  • Simmer, F., Tijsterman, M., Parrish, S., Koushika, S. P., Nonet, M. L., Fire, A., et al. (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol 12:1317–1319.
  • Simpson, V. J., Johnson, T. E. and Hammen, R. F. (1986) Caenorhabditis elegans DNA does not contain 5-methylcytosine at any time during development or aging. Nucleic Acids Res 14:6711–6719.
  • Singson, A. (2006) Sperm activation: time and tide wait for no sperm. Curr Biol 16:R160–162.
  • Spieth, J., Shim, Y. H., Lea, K., Conrad, R. and Blumenthal, T. (1991) elt-1, an embryonically expressed Caenorhabditis elegans gene homologous to the GATA transcription factor family. Mol Cell Biol 11:4651–4659.
  • Strome, S. (2005) Specification of the germ line. WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.7.1, http://www.wormbook.org.
  • Tanaka, H. and Baba, T. (2005) Gene expression in spermiogenesis. Cell Mol Life Sci 62:344–354.
  • Tevosian, S. G., Albrecht, K. H., Crispino, J. D., Fujiwara, Y., Eicher, E. M. and Orkin, S. H. (2002) Gonadal differentiation, sex determination and normal Sry expression in mice require direct interaction between transcription partners GATA4 and FOG2. Development 129:4627–4634.
  • Timmons, L., Tabara, H., Mello, C. C. and Fire, A. Z. (2003) Inducible systemic RNA silencing in Caenorhabditis elegans. Mol Biol Cell 14:2972–2983.
  • Turner, J. M. (2007) Meiotic sex chromosome inactivation. Development 134:1823–1831.
  • Walhout, A. J., Reboul, J., Shtanko, O., Bertin, N., Vaglio, P., Ge, H., et al. (2002) Integrating Interactome, Phenome, and Transcriptome Mapping Data for the C. elegans Germline. Curr Biol 12:1952–1958.
  • Wang, G. and Reinke, V. (2008) A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Curr Biol 18:861–867.
  • Wang, X., Zhao, Y., Wong, K., Ehlers, P., Kohara, Y., Jones, S. J., et al. (2009) Identification of genes expressed in the hermaphrodite germ line of C. elegans using SAGE. BMC Genomics 10:213.
  • Ward, S. and Carrel, J. S. (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73:304–321.
  • Ward, S., Hogan, E. and Nelson, G. A. (1983) The initiation of spermiogenesis in the nematode Caenorhabditis elegans. Dev Biol 98:70–79.
  • Ward, S. and Klass, M. (1982) The location of the major protein in Caenorhabditis elegans sperm and spermatocytes. Dev Biol 92:203–208.
  • Ward, S., Roberts, T. M., Strome, S., Pavalko, F. M. and Hogan, E. (1986) Monoclonal antibodies that recognize a polypeptide antigenic determinant shared by multiple Caenorhabditis elegans sperm-specific proteins. J Cell Biol 102:1778–1786.
  • Waterston, R. and Sulston, J. (1995) The genome of Caenorhabditis elegans. Proc Natl Acad Sci USA 92:10836–10840.
  • Wu, T. F. and Chu, D. S. (2008) Epigenetic processes implemented during spermatogenesis distinguish the paternal pronucleus in the embryo. Reprod Biomed Online 16:13–22.
  • Yamamoto, I., Kosinski, M. E. and Greenstein, D. (2006) Start me up: cell signaling and the journey from oocyte to embryo in C. elegans. Dev Dyn 235:571–585.
  • Zetka, M. and Rose, A. (1995) The genetics of meiosis in Caenorhabditis elegans. Trends Genet 11:27–31.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.