Skip to main content
Protein & Cell logoLink to Protein & Cell
. 2012 Aug 18;3(10):755–761. doi: 10.1007/s13238-012-2936-2

Transformation: how do nematode sperm become activated and crawl?

Xuan Ma 1, Yanmei Zhao 1, Wei Sun 1,2, Katsuya Shimabukuro 3,, Long Miao 1,
PMCID: PMC4875351  PMID: 22903434

Abstract

Nematode sperm undergo a drastic physiological change during spermiogenesis (sperm activation). Unlike mammalian flagellated sperm, nematode sperm are amoeboid cells and their motility is driven by the dynamics of a cytoskeleton composed of major sperm protein (MSP) rather than actin found in other crawling cells. This review focuses on sperm from Caenorhabditis elegans and Ascaris suum to address the roles of external and internal factors that trigger sperm activation and power sperm motility. Nematode sperm can be activated in vitro by several factors, including Pronase and ionophores, and in vivo through the TRY-5 and SPE-8 pathways. Moreover, protease and protease inhibitors are crucial regulators of sperm maturation. MSP-based sperm motility involves a coupled process of protrusion and retraction, both of which have been reconstituted in vitro. Sperm motility is mediated by phosphorylation signals, as illustrated by identification of several key components (MPOP, MFPs and MPAK) in Ascaris and the characterization of GSP-3/4 in C. elegans.

Keywords: spermiogenesis, major sperm protein, sperm motility

Contributor Information

Katsuya Shimabukuro, Email: kshimabu@ube-k.ac.jp.

Long Miao, Email: lmiao@moon.ibp.ac.cn.

References

  1. Abbas M., Cain G.D. In vitro Activation and Behavior of Ameboid Sperm of Ascaris suum (Nematoda) Cell Tissue Res. 1979;200:273–284. doi: 10.1007/BF00236419. [DOI] [PubMed] [Google Scholar]
  2. Arduengo P.M., Appleberry O.K., Chuang P., L’Hernault S.W. The presenilin protein family member SPE-4 localizes to an ER/Golgi derived organelle and is required for proper cytoplasmic partitioning during Caenorhabditis elegans spermatogenesis. J Cell Sci. 1998;111:3645–3654. doi: 10.1242/jcs.111.24.3645. [DOI] [PubMed] [Google Scholar]
  3. Bandyopadhyay J., Lee J., Il Lee J., Yu J.R., Jee C., Cho J.H., Jung S., Lee M.H., Zannoni S., Singson A., et al. Calcineurin, a calcium/calmodulin-dependent protein phosphatase, is involved in movement, fertility, egg laying, and growth in Caenorhabditis elegans. Mol Biol Cell. 2002;13:3281–3293. doi: 10.1091/mbc.E02-01-0005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buck J., Sinclair M.L., Schapal L., Cann M.J., Levin L.R. Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci U S A. 1999;96:79–84. doi: 10.1073/pnas.96.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buttery S.M., Ekman G.C., Seavy M., Stewart M., Roberts T.M. Dissection of the Ascaris sperm motility machinery identifies key proteins involved in major sperm protein-based amoeboid locomotion. Mol Biol Cell. 2003;14:5082–5088. doi: 10.1091/mbc.E03-04-0246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen Y., Cann M.J., Litvin T.N., Iourgenko V., Sinclair M.L., Levin L.R., Buck J. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science. 2000;289:625–628. doi: 10.1126/science.289.5479.625. [DOI] [PubMed] [Google Scholar]
  7. Edmonds J.W., McKinney S.L., Prasain J.K., Miller M.A. The gap junctional protein INX-14 functions in oocyte precursors to promote C. elegans sperm guidance. Dev Biol. 2011;359:47–58. doi: 10.1016/j.ydbio.2011.08.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Findlay G.D., Yi X., MacCoss M.J., Swanson W.J. Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. Plos Biol. 2008;6:1417–1426. doi: 10.1371/journal.pbio.0060178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fraire-zamora J.J., Cardullo R.A. The Physiological Acquisition of Ameboid Motility in Nematode Sperm: Is the Tail the Only Thing the Sperm Lost? Mol Reprod Dev. 2010;77:739–750. doi: 10.1002/mrd.21193. [DOI] [PubMed] [Google Scholar]
  10. Fraser L.R. The “switching on” of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation. Mol Reprod Dev. 2010;77:197–208. doi: 10.1002/mrd.21124. [DOI] [PubMed] [Google Scholar]
  11. Geldziler B., Chatterjee I., Singson A. The genetic and molecular analysis of spe-19, a gene required for sperm activation in Caenorhabditis elegans. Dev Biol. 2005;283:424–436. doi: 10.1016/j.ydbio.2005.04.036. [DOI] [PubMed] [Google Scholar]
  12. Italiano J.E., Roberts T.M., Stewart M., Fontana C.A. Reconstitution in vitro of the motile apparatus from the amoeboid sperm of Ascaris shows that filament assembly and bundling move membranes. Cell. 1996;84:105–114. doi: 10.1016/S0092-8674(00)80997-6. [DOI] [PubMed] [Google Scholar]
  13. Kubagawa H.M., Watts J.L., Corrigan C., Edmonds J.W., Sztul E., Browse J., Miller M.A. Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nature Cell Biol. 2006;8:1143–U1183. doi: 10.1038/ncb1476. [DOI] [PubMed] [Google Scholar]
  14. L’Hernault, S.W. (2006). Spermatogenesis. In Wormbook (The C. elegans Research Community).
  15. L’Hernault S.W. The genetics and cell biology of spermatogenesis in the nematode C. elegans. Mol Cell Endocrinol. 2009;306:59–65. doi: 10.1016/j.mce.2009.01.008. [DOI] [PubMed] [Google Scholar]
  16. LaFlamme, B.A., Ram, K.R., and Wolfner, M.F. (2012). The Drosophila melanogaster seminal fluid protease “seminase” regulates proteolytic and post-mating reproductive processes. Plos Genet 8. (In Press) [DOI] [PMC free article] [PubMed]
  17. LeClaire L.L., Stewart M., Roberts T.M. A 48 kDa integral membrane phosphoprotein orchestrates the cytoskeletal dynamics that generate amoeboid cell motility in Ascaris sperm. J Cell Sci. 2003;116:2655–2663. doi: 10.1242/jcs.00469. [DOI] [PubMed] [Google Scholar]
  18. Machaca K., DeFelice L.J., Lhernault S.W. A novel chloride channel localizes to Caenorhabditis elegans spermatids and chloride channel blockers induce spermatid differentiation. Dev Biol. 1996;176:1–16. doi: 10.1006/dbio.1996.9999. [DOI] [PubMed] [Google Scholar]
  19. Miao L., Vanderlinde O., Stewart M., Roberts T.M. Retraction in amoeboid cell motility powered by cytoskeletal dynamics. Science. 2003;302:1405–1407. doi: 10.1126/science.1089129. [DOI] [PubMed] [Google Scholar]
  20. Minniti A.N., Sadler C., Ward S. Genetic and molecular analysis of spe-27, a gene required for spermiogenesis in Caenorhabditis elegans hermaphrodites. Genetics. 1996;143:213–223. doi: 10.1093/genetics/143.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mogilner A., Oster G. Cell biology. Shrinking gels pull cells. Science. 2003;302:1340–1341. doi: 10.1126/science.1092041. [DOI] [PubMed] [Google Scholar]
  22. Murer V., Spetz J.F., Hengst U., Altrogge L.M., de Agostini A., Monard D. Male fertility defects in mice lacking the serine protease inhibitor protease nexin-1. Proc Natl Acad Sci U S A. 2001;98:3029–3033. doi: 10.1073/pnas.051630698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nance J., Davis E.B., Ward S. spe-29 encodes a small predicted membrane protein required for the initiation of sperm activation in Caenorhabditis elegans. Genetics. 2000;156:1623–1633. doi: 10.1093/genetics/156.4.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nance J., Minniti A.N., Sadler C., Ward S. spe-12 encodes a sperm cell surface protein that promotes spermiogenesis in Caenorhabditis elegans. Genetics. 1999;152:209–220. doi: 10.1093/genetics/152.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nelson G.A., Ward S. Vesicle fusion, pseudopod extension and ameboid motility are induced in nematode spermatids by the inophore monensin. Cell. 1980;19:457–464. doi: 10.1016/0092-8674(80)90520-6. [DOI] [PubMed] [Google Scholar]
  26. Nishimura H., L’Hernault S.W. Spermatogenesis-defective (spe) mutants of the nematode Caenorhabditis elegans provide clues to solve the puzzle of male germline functions during reproduction. Dev Dynamics. 2010;239:1502–1514. doi: 10.1002/dvdy.22271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Park B.J., Lee D.G., Yu J.R., Jung S.K., Choi K., Lee J., Kim Y.S., Il Lee J., Kwon J.Y., Singson A., et al. Calreticulin, a calcium-binding molecular chaperone, is required for stress response and fertility in Caenorhabditis elegans. Mol Biol Cell. 2001;12:2835–2845. doi: 10.1091/mbc.12.9.2835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ram K.R., Wolfner M.F. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integrat Comp Biol. 2007;47:427–445. doi: 10.1093/icb/icm046. [DOI] [PubMed] [Google Scholar]
  29. Reinke V., Gil I.S., Ward S., Kazmer K. Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development. 2004;131:311–323. doi: 10.1242/dev.00914. [DOI] [PubMed] [Google Scholar]
  30. Roberts T.M., King K.L. Centripetal Flow and Directed Reassembly of the Major Sperm Protein (MSP) Cytoskeleton in the Ameboid Sperm of the Nematode, Ascaris suum. Cell Motil Cytoskel. 1991;20:228–241. doi: 10.1002/cm.970200306. [DOI] [PubMed] [Google Scholar]
  31. Sepsenwol S., Taft S.J. In vitro Induction of Crawling in the Ameboid Sperm of the Parasite, Ascaris suum. Cell Motil Cytoskel. 1990;15:99–110. doi: 10.1002/cm.970150206. [DOI] [PubMed] [Google Scholar]
  32. Shakes D.C., Ward S. Initiation of Spermiogenesis in C. elegans: a Pharmacological and Genetic Analysis. Dev Biol. 1989;134:189–200. doi: 10.1016/0012-1606(89)90088-2. [DOI] [PubMed] [Google Scholar]
  33. Shimabukuro K., Noda N., Stewart M., Roberts T.M. Reconstitution of Amoeboid Motility In Vitro Identifies a Motor-Independent Mechanism for Cell Body Retraction. Curr Biol. 2011;21:1727–1731. doi: 10.1016/j.cub.2011.08.047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Singson A. Sperm activation: Time and tide wait for no sperm. Curr Biol. 2006;16:R160–R162. doi: 10.1016/j.cub.2006.02.039. [DOI] [PubMed] [Google Scholar]
  35. Smith, J.R., and Stanfield, G.M. (2011). TRY-5 Is a Sperm-Activating Protease in Caenorhabditis elegans Seminal Fluid. Plos Genet 7. [DOI] [PMC free article] [PubMed]
  36. Stanfield G.M., Villeneuve A.M. Regulation of sperm activation by SWM-1 is required for reproductive success of C. elegans males. Curr Biol. 2006;16:252–263. doi: 10.1016/j.cub.2005.12.041. [DOI] [PubMed] [Google Scholar]
  37. Vanfleteren J.R., Van De Peer Y., Blaxter M.L., Tweedie S.A.R., Trotman C., Lu L., Van Hauwaert M.-L., Moens L. Molecular genealogy of some nematode taxa as based on cytochrome c and globin amino acid sequence. Mol Phylogenet Evol. 1994;3:92–101. doi: 10.1006/mpev.1994.1012. [DOI] [PubMed] [Google Scholar]
  38. Varkey J.P., Jansma P.L., Minniti A.N., Ward S. The Caenorhabditis elegans Spe-6 Gene Is Required for Major Sperm Protein Assembly and Shows 2nd Site Noncomplementation with an Unlinked Deficiency. Genetics. 1993;133:79–86. doi: 10.1093/genetics/133.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ward S., Hogan E., Nelson G.A. The initiation of spermiogenesis in the nematode Caenorhabditis elegans. Dev Biol. 1983;98:70–79. doi: 10.1016/0012-1606(83)90336-6. [DOI] [PubMed] [Google Scholar]
  40. Washington N.L., Ward S. FER-1 regulates Ca2+-mediated membrane fusion during C. elegans spermatogenesis. J Cell Sci. 2006;119:2552–2562. doi: 10.1242/jcs.02980. [DOI] [PubMed] [Google Scholar]
  41. Wu J.-c., Go A.C., Samson M., Cintra T., Mirsoian S., Wu T.F., Jow M.M., Routman E.J., Chu D.S. Sperm development and motility are regulated by PP1 phosphatases in Caenorhabditis elegans. Genetics. 2012;190:143–157. doi: 10.1534/genetics.111.135376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yi K.X., Buttery S.M., Stewart M., Roberts T.M. A Ser/Thr kinase required for membrane-associated assembly of the major sperm protein motility apparatus in the amoeboid sperm of Ascaris. Mol Biol Cell. 2007;18:1816–1825. doi: 10.1091/mbc.E06-08-0741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Yi K.X., Wang X., Emmett M.R., Marshall A.G., Stewart M., Roberts T.M. Dephosphorylation of major sperm protein (MSP) fiber protein 3 by protein phosphatase 2a during cell body retraction in the MSP-based amoeboid motility of ascaris sperm. Mol Biol Cell. 2009;20:3200–3208. doi: 10.1091/mbc.E09-03-0240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zhao Y., Sun W., Zhang P., Chi H., Zhang M.-J., Song C.-Q., Ma X., Shang Y., Wang B., Hu Y., et al. Nematode sperm maturation triggered by protease involves sperm-secreted serine protease inhibitor (Serpin) Proc Natl Acad Sci U S A. 2012;109:1542–1547. doi: 10.1073/pnas.1109912109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zhu G.D., Salazar G., Zlatic S.A., Fiza B., Doucette M.M., Heilman C.J., Levey A.I., Faundez V., L’Hernault S.W. SPE-39 family proteins interact with the HOPS complex and function in lysosomal delivery. Mol Biol Cell. 2009;20:1223–1240. doi: 10.1091/mbc.E08-07-0728. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Protein & Cell are provided here courtesy of Oxford University Press

RESOURCES