Egg jelly proteins stimulate directed motility in Xenopus laevis sperm

Molecular Reproduction and Development

Volumn 78, Issue 6, 2011, Pages 450-462

  Burnett, Lindsey A ^a   Sugiyama, Hitoshi ^c   Bieber, Allan L ^b   Chandler, Douglas E ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Allurin; Amphibian egg jelly; Crisp proteins; Directed sperm motility; Fertilization

Indexed keywords

ALLURIN; EGG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; EGG WATER GRADIENT; FEMALE; MALE; MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SPERMATOZOON MOTILITY; VELOCITY; VIDEORECORDING; XENOPUS LAEVIS;

ANIMALS; CARRIER PROTEINS; CHEMOTACTIC FACTORS; EGG PROTEINS; FEMALE; MALE; OOCYTES; SPERM MOTILITY; SPERM-OVUM INTERACTIONS; SPERMATOZOA; XENOPUS LAEVIS;

AMPHIBIA; XENOPUS LAEVIS;

EID: 79959476702     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.21325     Document Type: Article

References (64)

1. Al-Anzi B, Chandler D. 1998. Xenopus laevis egg jelly releases a sperm chemoattractant during spawning. Dev Biol 198: 366-375.
2. Bernardini G, Stipini R, Melone G. 1986. The ultrastructure of Xenopus spermatozoon. J Ultrastruct Mol Struct Res 94: 188-194.
3. Bernardini G, Andreitti F, Camatini M, Cosson M. 1988. Xenopus spermatozoon: Correlation between shape and motility. Gamete Res 20: 165-175.
4. 2+ spikes in the flagellum control chemotactic behavior of sperm. EMBO J 24: 2741-2752.
5. Burnett LA, Xiang X, Bieber AL, Chandler DE. 2008a. Crisp proteins and sperm chemotaxis: Discovery in amphibians and explorations in mammals. Int J Dev Biol 52: 489-501.
6. Burnett LA, Boyles S, Spencer C, Bieber AL, Chandler DE. 2008b. Xenopus tropicalis allurin: Expression, purification and characterization of a sperm chemoattractant that exhibits cross-species activity. Dev Biol 316: 408-416.
7. Cardullo RA, Herrick SB, Peterson MJ, Dangott LJ. 1994. Speract receptors are localized on sea urchin sperm flagella using a fluorescent peptide analog. Dev Biol 162: 600-607.
8. Carlson AE, Burnett LA, del Camino D, Quill TA, Hill B, Chong JA, Moran MM, Babcock DF. 2009. Pharmacological targeting of native CatSper channels reveals a required role in maintenance of sperm hyperactivation. PLoS ONE 4: e6844.
9. Chang H, Suarez SS. 2010. Rethinking the relationship between hyperactivation and chemotaxis in mammalian sperm. Biol Reprod 83: 507-513.
10. Cohen DJ, Busso D, Da Ros V, Ellerman DA, Maldera JA, Goldweic N, Cuasnicu PS. 2008. Participation of cysteine-rich secretory proteins (CRISP) in mammalian sperm-egg interaction. Int J Dev Biol 52: 737-742.
11. Costello S, Michelangeli F, Nash K, Lefivre L, Morris J, Machado-Oliveira G, Barratt C, Kirkman-Brown J, Publicover S. 2009. Calcium stores in sperm: Their identities and functions. Reproduction 138: 425-437.
12. Darszon A, Acevedo JJ, Galindo BE, Hernández-González EO, Nishigaki T, Treviño CL, Wood C, Beltrán C. 2006. Sperm channel diversity and functional multiplicity. Reproduction 131: 977-988.
13. Dangott LJ, Garbers DL. 1984. Identification and partial characterization of the receptor for speract. J Biol Chem 259: 13712-13716.
14. Eisenbach M, Giojalas L. 2006. Sperm guidance in mammals-An unpaved road to the egg. Nat Rev Mol Cell Biol 7: 276-285.
15. Ellerman DA, Cohen DJ, Da Ros VG, Morgenfeld MM, Busso D, Cuasnicu PS. 2006. Sperm protein "DE" mediates gamete fusion through an evolutionarily conserved site of the CRISP family. Dev Biol 297: 228-237.
16. Fabro G, Rovasio RA, Civalero S, Frenkel A, Caplan SR, Eisenbach M, Giojalas LC. 2002. Chemotaxis of capacitated rabbit spermatozoa to follicular fluid revealed by a novel directionality-based assay. Biol Reprod 67: 1565-1571.
17. Garbers DL. 1989. Guanylate cyclase, a cell surface receptor. J Biol Chem 264: 9103-9106.
18. Gibbs GM, Roelants K, O'Bryan MK. 2008. The CAP superfamily: Cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins-Roles in reproduction, cancer, and immune defense. Endocr Rev 29: 865-897.
19. Guerrero A, Nishigaki T, Carneiro J, Tatsu Y, Wood CD, Darszon A. 2010. Tuning sperm chemotaxis by calcium burst timing. Dev Biol 344: 52-65.
20. Guidobaldi HA, Teves ME, Uñates DR, Anastasía A, Giojalas LC. 2008. Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex. PLoS ONE 3: e3040.
21. Ho HC, Suarez SS. 2001. An inositol 1, 4, 5-trisphosphate receptor-gated intracellular Ca(2+) store is involved in regulating sperm hyperactivated motility. Biol Reprod 65: 1606-1615.
22. Ho HC, Suarez SS. 2003. Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility. Biol Reprod 68: 1590-1596.
23. Jang S, Yi LSH. 2005. Identification of a 71kDa protein as a putative nongenomic membrane progesterone receptor in boar spermatozoa. J Endocrinol 184: 417-425.
24. Kaupp UB, Kashikar ND, Weyand I. 2008. Mechanisms of sperm chemotaxis. Annu Rev Physiol 70: 93-117.
25. Koppers AJ, Reddy T, O'Bryan MK. 2011. The role of cysteine-rich secretory proteins in male fertility. Asian J Androl 13: 111-117.
26. Krug PJ, Riffell JA, Zimmer RK. 2009. Endogenous signaling pathways and chemical communication between sperm and egg. J Exp Biol 212: 1092-1100.
27. Lishko PV, Botchkina IL, Kirichok Y. 2011. Progesterone activates the principal Ca2+ channel of human sperm. Nature 471: 387-391.
28. Luconi M, Bonaccorsi L, Maggi M, Pecchioli P, Krausz C, Forti G, Baldi E. 1998. Identification and characterization of functional nongenomic progesterone receptors on human sperm membrane. J Clin Endocrinol Metab 83: 877-885.
29. Morita M, Kitamura M, Nakajima A, Susilo E, Takemura A, Okuno M. 2009. Regulation of sperm flagellar motility activation and chemotaxis caused by egg-derived substance(s) in sea cucumber. Cell Motil Cytoskeleton 66: 202-214.
30. Nishigaki T, Chiba K, Hoshi M. 2000. A 130-kDa membrane protein of sperm flagella is the receptor for asterosaps, sperm-activating peptides of starfish Asterias amurensis Dev Biol 219: 154-162.
31. Olson J, Xiang X, Ziegert T, Kittleson A, Rawls A, Bieber A, Chandler DE. 2001. Allurin, a 21kD sperm chemoattractant from Xenopus egg jelly, is homologous to mammalian sperm-binding proteins. Proc Natl Acad Sci USA 98: 11205-11210.
32. Oren-Benaroya R, Orvieto R, Gakamsky A, Pinchasov M, Eisenbach M. 2008. The sperm chemoattractant secreted from human cumulus cells is progesterone. Hum Reprod 23: 2339-2345.
33. Publicover SJ, Giojalas LC, Teves ME, de Oliveira GS, Garcia AA, Barratt CL, Harper CV. 2008. Ca2+ signalling in the control of motility and guidance in mammalian sperm. Front Biosci 13: 5623-5637.
34. i signaling in sperm-Making the most of what you've got. Nat Cell Biol 9: 235-242.
35. Reinhart D, Ridgway J, Chandler DE. 1998. Xenopus laevis fertilisation: Analysis of sperm motility in egg jelly using video light microscopy. Zygote 6: 173-182.
36. Riffell JA, Krug PJ, Zimmer RK. 2004. The ecological and evolutionary consequences of sperm chemoattraction. Proc Natl Acad Sci USA 101: 4501-4506.
37. Roberts KP, Johnston DS, Nolan MA, Wooters JL, Waxmonsky NC, Piehl LB, Ensrud-Bowlin KM, Hamilton DW. 2007. Structure and function of epididymal protein cysteine-rich secretory protein-1. Asian J Androl 9: 508-514.
38. Roberts KP, Ensrud KM, Hamilton D. 2002. A comparative analysis of expression and processing of the rat epididymal fluid and sperm-bound forms of proteins D and E. Biol Reprod 67: 525-533.
39. Rochwerger L, Cuasnicu PS. 1992. Redistribution of a rat sperm epididymal glycoprotein after in vivo and in vitro capacitation. Mol Reprod Dev 31: 34-41.
40. Rochwerger L, Cohen DJ, Cuasnicu PS. 1992. Mammalian sperm-egg fusion: The rat egg has complementary sites for a sperm protein that mediates gamete fusion. Dev Biol 153: 83-90.
41. Sabeur K, Edwards DP, Meizel S. 1996. Human sperm plasma membrane progesterone receptor(s) and the acrosome reaction. Biol Reprod 54: 993-1001.
42. Shiba K, Baba SA, Inoue T, Yoshida M. 2008. Ca2+ bursts occur around a local minimal concentration of attractant and trigger sperm chemotactic response. Proc Natl Acad Sci USA 105: 19312-19317.
43. Shimomura H, Dangott LJ, Garbers DL. 1986. Covalent coupling of a resact analogue to guanylate cyclase. J Biol Chem 261: 15778-15782.
44. Smith DJ, Gaffney EA, Gadêlha H, Kapur N, Kirkman-Brown JC. 2009. Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity. Cell Motil Cytoskeleton 66: 220-236.
45. Spehr M, Schwane K, Riffell JA, Barbour J, Zimmer RK, Neuhaus EM, Hatt H. 2004. Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. J Biol Chem 279: 40194-40203.
46. Spehr M, Schwane K, Riffell JA, Zimmer RK, Hatt H. 2006. Odorant receptors and olfactory-like signaling mechanisms in mammalian sperm. Mol Cell Endocrinol 250: 128-136.
47. Strünker T, Weyand I, Bönigk W, Van Q, Loogen A, Brown JE, Kashikar N, Hagen V, Krause E, Kaupp UB. 2006. A K+-selective cGMP-gated ion channel controls chemosensation of sperm. Nat Cell Biol 8: 1149-1154.
48. Strünker T, Goodwin N, Brenker C, Kashikar ND, Weyand I, Seifert R, Kaupp UB. 2011. The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 471: 382-386.
49. Sugiyama H, Al-Anzi B, McGaughey R, Chandler DE. 2004. Assays for vertebrate sperm chemotaxis. In: Schatten H, editor. Germ cell protocols: Sperm and oocyte analysis: Methods in molecular biology. Totowa, NJ: Humana Press, pp 27-48.
50. Sugiyama H, Burnett L, Xiang X, Olson J, Willis S, Miao A, Akema T, Bieber AL, Chandler DE. 2009. Purification and multimer formation of allurin, a sperm chemoattractant from Xenopus laevis egg jelly. Mol Reprod Dev 76: 527-536.
51. Sun F, Bahat A, Gakamsky A, Girsh E, Katz N, Giojalas LC, Tur-Kaspa I, Eisenbach M. 2005. Human sperm chemotaxis: Both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants. Hum Reprod 20: 761-767.
52. Sun F, Giojolas LC, Rovasio RA, Tur-Kaspa I, Sanchez R, Eisenbach M. 2003. Lack of species-specificity in mammalian sperm chemotaxis. Dev Biol 255: 423-427.
53. Suzuki N, Kurita M, Yoshino K, Yamaguchi M. 1987. Speract binds exclusively to sperm tails and causes an electrophoretic mobility shift in a major sperm tail protein of sea urchins. Zool Sci 4: 641-648.
54. Teves ME, Guiobaldi HA, Unates D, Sanchez R, Miska W, Publicover SJ, Morales-Garcia AA, Giojalas LC. 2009. Molecular mechanism for human sperm chemotaxis mediated by progesterone. PLoS ONE 4: e8211.
55. Ward GE, Brokaw CJ, Garbers DL, Vacquier VD. 1985. Chemotaxis of Arbacia punctulata spermatozoa to resact, a peptide from the egg jelly layer. J Cell Biol 101: 2324-2329.
56. Watanabe T, Kubo H, Takeshima S, Nakagawa M, Ohta M, Kamimura S, Takayama-Watanabe E, Watanabe A, Onitake K. 2010. Identification of the sperm motility-initiating substance in the newt, Cynops pyrrhogaster, and its possible relationship with the acrosome reaction during internal fertilization. Int J Dev Biol 54: 591-597.
57. Wood CD, Darszon A, Whitaker M. 2003. Speract induces calcium oscillations in the sperm tail. J Cell Biol 161: 89-101.
58. Wood CD, Nishigaki T, Furuta T, Baba SA, Darszon A. 2005. Real-time analysis of the role of Ca(2+) in flagellar movement and motility in single sea urchin sperm. J Cell Biol 169: 725-731.
59. 2+ spikes regulates their kinetics and sea urchin sperm motility. Dev Biol 306: 525-537.
60. Wu JT, Chiang KC, Cheng FP. 2006. Expression of progesterone receptor(s) during capacitation and incidence of acrosome reaction induced by progesterone and zona proteins in boar spermatozoa. Anim Reprod Sci 93: 34-45.
61. Xiang X, Burnett LA, Rawls A, Bieber AL, Chandler DE. 2004. The sperm chemoattractant "allurin" is expressed and secreted from the Xenopus oviduct in a hormone regulated manner. Dev Biol 275: 343-355.
62. Xiang X, Kittelson A, Olson J, Bieber AL, Chandler DE. 2005. Allurin, a 21kD sperm chemoattractant, is rapidly released from the outermost jelly layer of the Xenopus egg by diffusion and medium convection. Mol Reprod Dev 70: 344-360.
63. Yoshida M, Murata M, Inaba K, Morisawa M. 2002. A chemoattractant for ascidian spermatozoa is a sulfated steroid. Proc Natl Acad Sci USA 99: 14831-14836.
64. Zigmond SH. 1977. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol 75: 606-616.