C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes

Development

Volumn 132, Issue 15, 2005, Pages 3357-3369

  Kosinki, Mary ^a   McDonald, Kent ^b   Schwartz, Joel ^a   Yamamoto, Ikuko ^a   Greenstein, David ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gamete interactions; Major sperm protein signaling; Meiotic maturation; Oogenesis; Unconventional protein secretion; Vesicle budding

Indexed keywords

ACTIN; CYTOPLASM PROTEIN; MAJOR SPERMATOZOON PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL BUDDING; CELL COMMUNICATION; CELL MATURATION; CELL MEMBRANE; CELL STRUCTURE; CELL SURFACE; CELL VACUOLE; CONTROLLED STUDY; CYTOSKELETON; ENDOPLASMIC RETICULUM; FEMALE; GOLGI COMPLEX; MALE; MEIOSIS; MUSCLE CONTRACTION; NEMATODE; NONHUMAN; OOCYTE; OOCYTE MATURATION; OUTER MEMBRANE; OVARY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN TRANSPORT; REPRODUCTION; RIBOSOME; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOZOON; SPERMATOZOON MOTILITY;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CELL MEMBRANE; FEMALE; GENITALIA, MALE; HELMINTH PROTEINS; MALE; MEIOSIS; MOLECULAR SEQUENCE DATA; MUSCLE CONTRACTION; MUSCLE, SMOOTH; OOCYTES; OVARY; SIGNAL TRANSDUCTION; SPERMATOZOA;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 24344463993     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01916     Document Type: Article

References (48)

1. Achanzar, W. E. and Ward, S. (1997). A nematode gene required for sperm vesicle fusion. J. Cell Sci. 110, 1073-1081.
2. Bottino, D., Mogilner, A., Roberts, T., Stewart, M. and Oster, G. (2002). How nematode sperm crawl. J. Cell Sci. 115, 367-384.
3. 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.
4. Chang, H. C., Samaniego, F., Nair, B. C., Buonaguro, L. and Ensoli, B. (1997). HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. AIDS 11, 1421-1431.
5. Chernomordik, L. V. and Kozlov, M. M. (2003). Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72, 175-207.
6. Cooper, D. N. and Barondes, S. H. (1990). Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J. Cell Biol. 110, 1681-1691.
7. De Ley, P., Geraert, E. and Coomans, A. (1990). Seven cephalobids from Senegal. J. Afr. Zool. 104, 287-304.
8. Eisenbach, M. and Tur-Kaspa, I. (1999). Do human eggs attract spermatozoa? BioEssays 21, 203-210.
9. Grant, B. and Hirsh, D. (1999). Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326.
10. Hall, D. H., Winfrey, V. P., Blaeuer, G., Hoffman, L. H., Furuta, T., Rose, K. L., Hobert, O. and Greenstein, D. (1999). Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev. Biol. 212, 101-123.
11. Hardy, D. M. (ed.) (2002). Fertilization. San Diego: Academic Press.
12. Harlow, E. and Lane, D. (1988). Antibodies: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
13. Hill, K. L. and L'Hernault, S. W. (2001). Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Dev. Biol. 232, 105-114.
14. Howe, M., McDonald, K. L., Albertson, D. G. and Meyer, B. J. (2001). HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J. Cell Biol. 153, 1227-1238.
15. Hubbard, E. J. and Greenstein, D. (2000). The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev. Dyn. 218, 2-22.
16. Italiano, J. E., Jr, 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.
17. Iwasaki, K., McCarter, J., Francis, R. and Schedl, T. (1996). emo-1, a Caenorhabditis elegans Sec61p gamma homologue, is required for oocyte development and ovulation. J. Cell Biol. 134, 699-714.
18. Kamath, R. S., Martinez-Campos, M., Zipperlen, P., Fraser, A. G. and Ahringer, J. (2001). Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, 1-10.
19. Klass, M. R. and Hirsh, D. (1981). Sperm isolation and biochemical analysis of the major sperm protein from C. elegans. Dev. Biol. 84, 299-312.
20. L'Hernault, S. (1997). Spermatogenesis. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), pp. 271-294. New York: Cold Spring Harbor Laboratory Press.
21. L'Hernault, S. W., Shakes, D. C. and Ward, S. (1988). Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 120, 435-452.
22. Lonsdale, J. E., McDonald, K. L. and Jones, R. L. (1999). High pressure freezing and freeze substitution reveal new aspects of fine structure and maintain protein antigenicity in barley aleurone cells. Plant J. 17, 221-229.
23. Lonsdale, J. E., McDonald, K. L. and Jones, R. L. (2001). Microwave polymerization in thin layers of LR white allows selection of specimens for immunogold labeling. In Microwave Techniques and Protocols (ed. R. T. Giberson and R. S. Demaree, Jr), pp. 139-153. New Jersey: Humana Press.
24. MacKenzie, A., Wilson, H. L., Kiss-Toth, E., Dower, S. K., North, R. A. and Surprenant, A. (2001). Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 15, 825-835.
25. Masui, Y. (1985). Meiotic arrest in animal oocytes. In Biology of Fertilization (ed. C. B. Metz and A. Monroy), pp. 189-219. Florida: Academic Press.
26. 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.
27. McDonald, K. (1999). High-pressure freezing for preservation of high resolution fine structure and antigenicity for immunolabeling. Methods Mol. Biol. 117, 77-97.
28. Miao, L., Vanderlinde, O., Stewart, M. and Roberts, T. M. (2003). Retraction in amoeboid cell motility powered by cytoskeletal dynamics. Science 302, 1405-1407.
29. Miller, M. A., Nguyen, V. Q., Lee, M. H., Kosinski, M., Schedl, T., Caprioli, R. M. and Greenstein, D. (2001). A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291, 2144-2147.
30. Miller, M. A., Ruest, P. J., Kosinski, M., Hanks, S. K. and Greenstein, D. (2003). An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev. 17, 187-200.
31. Mignatti, P., Morimoto, T. and Rifkin, D. B. (1992). Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J. Cell Physiol. 151, 81-93.
32. Müller-Reichert, T., O'Toole, E. T., Hohenberg, H. and McDonald, K. L. (2003). Cryoimmobilization and three-dimensional visualization of C. elegans ultrastructure. J. Microsc. 212, 71-80.
33. Neill, A. T. and Vacquier, V. D. (2004). Ligands and receptors mediating signal transduction in sea urchin spermatozoa. Reproduction 127, 141-149.
34. Nickel, W. (2003). The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur. J. Biochem. 270, 2109-2119.
35. Nishimura, A. L., Mitne-Neto, M., Silva, H. C. A., Richieri-Costa, A., Middleton, S., Cascio, D., Kok, F., Oliveira, J. R. M., Gillingwater, T., Webb, J., Skehel, P. and Zatz, M. (2004). A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Genet. 75, 822-831.
36. Nonet, M. L., Staunton, J. E., Kilgard, M. P., Fergestad, T., Hartwieg, E., Horvitz, H. R., Jorgensen, E. M. and Meyer, B. J. (1997). Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 17, 8061-8073.
37. Pennetta, G., Hiesinger, P., Fabian-Fine, R., Meinertzhagen, I. and Bellen, H. J. (2002). Drosophila VAP-33A directs bouton formation at neuromuscular junctions in a dosage-dependent manner. Neuron 32, 291-306.
38. Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R. (eds) (1997). C. elegans II. New York: Cold Spring Harbor Laboratory Press.
39. Rose, K. L., Winfrey, V. P., Hoffman, L. H., Hall, D. H., Furuta, T. and Greenstein, D. (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.
40. Spehr, M., Gisselmann, G., Poplawski, A., Riffell, J. A., Wetzel, C. H., Zimmer, R. K. and Hatt, H. (2003). Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299, 2054-2058.
41. Stinchcombe, J., Bossi, G. and Griffiths, G. M. (2004). Linking albinism and immunity: the secrets of secretory lysosomes. Science 305, 55-59.
42. Thorne, G. (1925). The genus Acrobeles von Linstow, 1877. Trans Am. Microsc. Soc. 44, 171-209.
43. Ward, G. E., Brokaw, C. J., Garbers, D. L. and Vacquier, V. D. (1985). Chemotaxis of Arbacia punctulata spermatozoa to resact, a peptide from the egg jelly layer. J. Cell Biol. 101, 2324-2329.
44. Ward, S. and Carrel, J. S. (1979). Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev. Biol. 73, 304-321.
45. Ward, S. and Klass, M. (1982). The location of the major protein in C. elegans sperm and spermatocytes. Dev. Biol. 92, 203-208.
46. 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 C. elegans sperm-specific proteins. J. Cell Biol. 102, 1778-1786.
47. Wassarman, P. M., Jovine, L. and Litscher, E. S. (2001). A profile of fertilization in mammals. Nat. Cell Biol. 3, E59-E64.
48. Xu, X. Z. and Sternberg, P. W. (2003). A C. elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114, 285-297.