Transformation: how do nematode sperm become activated and crawl?

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

References

[1] Abbas, M., and Cain, G.D. (1979). In vitro Activation and Behavior of Ameboid Sperm of Ascaris suum (Nematoda). Cell Tissue Res 200, 273-284 .10.1007/BF00236419
[2] Arduengo, P.M., Appleberry, O.K., Chuang, P., and L'Hernault, S.W. (1998). 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 111, 3645-3654 .
[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.,. (2002). Calcineurin, a calcium/calmodulin-dependent protein phosphatase, is involved in movement, fertility, egg laying, and growth in Caenorhabditis elegans. Mol Biol Cell 13, 3281-3293 10.1091/mbc.E02-01-0005
[4] Buck, J., Sinclair, M.L., Schapal, L., Cann, M.J., and Levin, L.R. (1999). Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci U S A 96, 79-84 .10.1073/pnas.96.1.79
[5] Buttery, S.M., Ekman, G.C., Seavy, M., Stewart, M., and Roberts, T.M. (2003). Dissection of the Ascaris sperm motility machinery identifies key proteins involved in major sperm protein-based amoeboid locomotion. Mol Biol Cell 14, 5082-5088 .10.1091/mbc.E03-04-0246
[6] Chen, Y., Cann, M.J., Litvin, T.N., Iourgenko, V., Sinclair, M.L., Levin, L.R., and Buck, J. (2000). Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289, 625-628 .10.1126/science.289.5479.625
[7] Edmonds, J.W., McKinney, S.L., Prasain, J.K., and Miller, M.A. (2011). The gap junctional protein INX-14 functions in oocyte precursors to promote C. elegans sperm guidance. Dev Biol 359, 47-58 .10.1016/j.ydbio.2011.08.014
[8] 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, 1417-1426 .10.1371/journal.pbio.0060178
[9] Fraire-zamora, J.J., and Cardullo, R.A. (2010). The Physiological Acquisition of Ameboid Motility in Nematode Sperm: Is the Tail the Only Thing the Sperm Lost? Mol Reprod Dev 77, 739-750 .10.1002/mrd.21193
[10] Fraser, L.R. (2010). The "switching on" of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation. Mol Reprod Dev 77, 197-208 .
[11] Geldziler, B., Chatterjee, I., and Singson, A.(2005). The genetic and molecular analysis of spe-19, a gene required for sperm activation in Caenorhabditis elegans. Dev Biol 283, 424-436 .10.1016/j.ydbio.2005.04.036
[12] Italiano, J.E., Roberts, T.M., Stewart, M., and Fontana, C.A. (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 .10.1016/S0092-8674(00)80997-6
[13] Kubagawa, H.M., Watts, J.L., Corrigan, C., Edmonds, J.W., Sztul, E., Browse, J., and Miller, M.A. (2006). Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nature Cell Biol 8, 1143-U1183 .10.1038/ncb1476
[14] L'Hernault, S.W. (2006). Spermatogenesis. In Wormbook (The C. elegans Research Community) .10.1895/wormbook.1.85.1
[15] L'Hernault, S.W. (2009). The genetics and cell biology of spermatogenesis in the nematode C. elegans. Mol Cell Endocrinol 306, 59-65 .10.1016/j.mce.2009.01.008
[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)10.1371/journal.pgen.1002435
[17] LeClaire, L.L., Stewart, M., and Roberts, T.M. (2003). A 48 kDa integral membrane phosphoprotein orchestrates the cytoskeletal dynamics that generate amoeboid cell motility in Ascaris sperm. J Cell Sci 116, 2655-2663 .10.1242/jcs.00469
[18] Machaca, K., DeFelice, L.J., and Lhernault, S.W. (1996). A novel chloride channel localizes to Caenorhabditis elegans spermatids and chloride channel blockers induce spermatid differentiation. Dev Biol 176, 1-16 .10.1006/dbio.1996.9999
[19] Miao, L., Vanderlinde, O., Stewart, M., and Roberts, T.M. (2003). Retraction in amoeboid cell motility powered by cytoskeletal dynamics. Science 302, 1405-1407 .10.1126/science.1089129
[20] Minniti, A.N., Sadler, C., and Ward, S. (1996). Genetic and molecular analysis of spe-27, a gene required for spermiogenesis in Caenorhabditis elegans hermaphrodites213-223 .
[21] Mogilner, A., and Oster, G. (2003). Cell biology. Shrinking gels pull cells. Science 302, 1340-1341 .10.1126/science.1092041
[22] Murer, V., Spetz, J.F., Hengst, U., Altrogge, L.M., de Agostini, A., and Monard, D. (2001). Male fertility defects in mice lacking the serine protease inhibitor protease nexin-1. Proc Natl Acad Sci U S A 98, 3029-3033 .10.1073/pnas.051630698
[23] Nance, J., Davis, E.B., and Ward, S. (2000). spe-29 encodes a small predicted membrane protein required for the initiation of sperm activation in Caenorhabditis elegans. Genetics 156, 1623-1633 .
[24] Nance, J., Minniti, A.N., Sadler, C., and Ward, S. (1999). spe-12 encodes a sperm cell surface protein that promotes spermiogenesis in Caenorhabditis elegans. Genetics 152, 209-220 .
[25] Nelson, G.A., and Ward, S. (1980). Vesicle fusion, pseudopod extension and ameboid motility are induced in nematode spermatids by the inophore monensin. Cell 19, 457-464 .10.1016/0092-8674(80)90520-6
[26] Nishimura, H., and L'Hernault, S.W. (2010). Spermatogenesis-defective (spe) mutants of the nematode Caenorhabditis elegans provide clues to solve the puzzle of male germline functions during reproduction. Dev Dynamics 239, 1502-1514 .
[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.,. (2001). Calreticulin, a calcium-binding molecular chaperone, is required for stress response and fertility in Caenorhabditis elegans. Mol Biol Cell 12, 2835-2845 .
[28] Ram, K.R., and Wolfner, M.F. (2007). Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integrat Comp Biol 47, 427-445 .10.1093/icb/icm046
[29] 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 .10.1242/dev.00914
[30] Roberts, T.M., and King, K.L. (1991). Centripeta Flow and Directed Reassembly of the Major Sperm Protein (MSP) Cytoskeleton in the Ameboid Sperm of the Nematode, Ascaris suum. Cell Motil Cytoskel 20, 228-241 10.1002/cm.970200306
[31] Sepsenwol, S., and Taft, S.J. (1990).In vitro Induction of Crawling in the Ameboid Sperm of the Parasite, Ascaris suum . Cell Motil Cytoskel 15, 99-110 .10.1002/cm.970150206
[32] Shakes, D.C., and Ward, S. (1989). Initiation of Spermiogenesis in C. elegans: a Pharmacological and Genetic Analysis. Dev Biol 134, 189-200 .10.1016/0012-1606(89)90088-2
[33] Shimabukuro, K., Noda, N., Stewart, M., and Roberts, T.M. (2011). Reconstitution of Amoeboid Motility In Vitro Identifies a Motor-Independent Mechanism for Cell Body Retraction. Curr Biol 21, 1727-1731 10.1016/j.cub.2011.08.047
[34] Singson, A. (2006). Sperm activation: Time and tide wait for no sperm. Curr Biol 16, R160-R162 .10.1016/j.cub.2006.02.039
[35] Smith, J.R., and Stanfield, G.M. (2011). TRY-5 Is a Sperm-Activating Protease in Caenorhabditis elegans Seminal Fluid. Plos Genet 7.10.1371/journal.pgen.1002375
[36] Stanfield, G.M., and Villeneuve, A.M. (2006). Regulation of sperm activation by SWM-1 is required for reproductive success of C. elegans males. Curr Biol 16, 252-263 .10.1016/j.cub.2005.12.041
[37] Vanfleteren, J.R., Van De Peer, Y., Blaxter, M.L., Tweedie, S.A.R., Trotman, C., Lu, L., Van Hauwaert, M.-L., and Moens, L. (1994). Molecular genealogy of some nematode taxa as based on cytochrome c and globin amino acid sequence. Mol Phylogenet Evol 3, 92-101 .10.1006/mpev.1994.1012
[38] Varkey, J.P., Jansma, P.L., Minniti, A.N., and Ward, S. (1993). The Caenorhabditis elegans Spe-6 Gene Is Required for Major Sperm Protein Assembly and Shows 2nd Site Noncomplementation with an Unlinked Deficiency. Genetics 133, 79-86 .
[39] Ward, S., Hogan, E., and Nelson, G.A. (1983). The initiation of spermiogenesis in the nematode Caenorhabditis elegans. Dev Biol 98, 70-79 .10.1016/0012-1606(83)90336-6
[40] Washington, N.L., and Ward, S. (2006). FER-1 regulates Ca2⁺-mediated membrane fusion during C. elegans spermatogenesis. J Cell Sci 119, 2552-2562 .10.1242/jcs.02980
[41] Wu, J.-c., Go, A.C., Samson, M., Cintra, T., Mirsoian, S., Wu, T.F., Jow, M.M., Routman, E.J., and Chu, D.S. (2012). Sperm development and motility are regulated by PP1 phosphatases in Caenorhabditis elegans. Genetics 190, 143-157 .10.1534/genetics.111.135376
[42] Yi, K.X., Buttery, S.M., Stewart, M., and Roberts, T.M. (2007). 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 18, 1816-1825 .10.1091/mbc.E06-08-0741
[43] Yi, K.X., Wang, X., Emmett, M.R., Marshall, A.G., Stewart, M., and Roberts, T.M. (2009). 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 20, 3200-3208 .10.1091/mbc.E09-03-0240
[44] Zhao, Y., Sun, W., Zhang, P., Chi, H., Zhang, M.-J., Song, C.-Q., Ma, X., Shang, Y., Wang, B., Hu, Y.,. (2012). Nematode sperm maturation triggered by protease involves sperm-secreted serine protease inhibitor (Serpin). Proc Natl Acad Sci U S A 109, 1542-1547 .10.1073/pnas.1109912109
[45] Zhu, G.D., Salazar, G., Zlatic, S.A., Fiza, B., Doucette, M.M., Heilman, C.J., Levey, A.I., Faundez, V., and L'Hernault, S.W. (2009). SPE-39 family proteins interact with the HOPS complex and function in lysosomal delivery. Mol Biol Cell 20, 1223-1240 .10.1091/mbc.E08-07-0728