Calcium/calmodulin and cAMP/protein kinase-A pathways regulate sperm motility in the stallion

Animal Reproduction Science

Volumn 132, Issue 3-4, 2012, Pages 169-177

  Lasko, Jodi ^a   Schlingmann, Karen ^a   Klocke, Ann ^a   Mengel, Grace Ann ^a   Turner, Regina ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Calcium; Motility; Protein kinase A; Signaling; Sperm; Stallion

Indexed keywords

CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ISOQUINOLINE DERIVATIVE; N (2 (4 BROMOCINNAMYLAMINO)ETHYL) 5 ISOQUINOLINESULFONAMIDE; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; N-(2-(4-BROMOCINNAMYLAMINO)ETHYL)-5-ISOQUINOLINESULFONAMIDE; SULFONAMIDE;

ANIMAL; ARTICLE; DRUG ANTAGONISM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HORSE; MALE; METABOLISM; PHYSIOLOGY; SPERMATOZOON; SPERMATOZOON MOTILITY;

ANIMALS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALMODULIN; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION REGULATION; HORSES; ISOQUINOLINES; MALE; SPERM MOTILITY; SPERMATOZOA; SULFONAMIDES;

MAMMALIA;

EID: 84863213950     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2012.05.007     Document Type: Article

References (69)

1. Ahmad K., Bracho G.E., Wolf D.P., Tash J.S. Regulation of human sperm motility and hyperactivation components by calcium, calmodulin, and protein phosphatases. Arch. Androl. 1995, 35:187-208.
2. Bellve A.R., Cavicchia J.C., Millette C.F., O'Brien D.A., Bhatnagar Y.M., Dym M. Spermatogenic cells of the prepuberal mouse: isolation and morphological characterization. J. Cell Biol. 1977, 74:68-71.
3. Bendahmane M., Lynch C., 2nd, Tulsiani D.R. Calmodulin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa. Arch. Biochem. Biophys. 2001, 390:1-8.
4. Brokaw C.J. Calcium sensors in sea urchin sperm flagella. Cell Motil. Cytoskeleton 1991, 18:123-130.
5. Bunch D.O., Welch J.E., Magyar P.L., Eddy E.M., O'Brien D.A. Glyceraldehyde 3-phosphate dehydrogenase-S protein distribution during mouse spermatogenesis. Biol. Reprod. 1998, 58:834-841.
6. Carr D.W., Fujita A., Stentz C.L., Liberty G.A., Olson G.E., Narumiya S. Identification of sperm-specific proteins that interact with A-kinase anchoring proteins in a manner similar to the type II regulatory subunit of PKA. J. Biol. Chem. 2001, 276:17332-17338.
7. Carrera A., Gerton G.L., Moss S.B. The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev. Biol. 1994, 165:272-284.
8. Chang B.H., Mukherji S., Soderling T.R. Calcium/calmodulin-dependent protein kinase II inhibitor protein: localization of isoforms in rat brain. Neuroscience 2001, 102:767-777.
9. 2+ signaling pathways modulate sperm flagellar beating patterns in mice. Biol. Reprod. 2011, 85:296-305.
10. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 2000, 351:95-105.
11. 2+-calmodulin-dependent protein kinase II in dorsal root ganglion neurons. J. Neurosci. 2001, 21:6694-6705.
12. Esposito G., Jaiswal B.S., Xie F., Krajnc-Franken M.A., Robben T.J., Strik A.M., Kuil C., Philipsen R.L., van Duin M., Conti M., Gossen J.A. Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2993-2998.
13. 2+/calmodulin-dependent protein kinase CaM kinase-Gr, in rat thymus. J. Biol. Chem. 1991, 266:17592-17596.
14. Fujita A., Nakamura K., Kato T., Watanabe N., Ishizaki T., Kimura K., Mizoguchi A., Narumiya S. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J. Cell Sci. 2000, 113:103-112.
15. Galantino-Homer H.L., Visconti P.E., Kopf G.S. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3'5'-monophosphate-dependent pathway. Biol. Reprod. 1997, 56:707-719.
16. Gardner H.P., Rajan J.V., Ha S.I., Copeland N.G., Gilbert D.J., Jenkins N.A., Marquis S.T., Chodosh L.A. Cloning, characterization, and chromosomal localization of Pnck, a Ca(2+)/calmodulin-dependent protein kinase. Genomics 2000, 63:279-288.
17. Heffner L.J., Storey B.T. The role of calcium in maintaining motility in mouse spermatozoa. J. Exp. Zool. 1981, 218:427-434.
18. Hidaka H., Kobayashi R. Pharmacology of protein kinase inhibitors. Annu. Rev. Pharmacol. Toxicol. 1992, 32:377-397.
19. 2+ and not cAMP. Dev. Biol. 2002, 250:208-217.
20. Ignotz G.G., Suarez S.S. Calcium/calmodulin and calmodulin kinase II stimulate hyperactivation in demembranated bovine sperm. Biol. Reprod. 2005, 73:519-526.
21. Jaiswal B.S., Conti M. Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10676-10681.
22. Johnson L., Foster J.A., Haig-Ladewig L., VanScoy H., Moss S.M., Gerton G.L. Assembly of AKAP82, a protein kinase A anchor protein, into the fibrous sheath of mouse sperm. Dev. Biol. 1997, 192:340-350.
23. 2+/calmodulin-dependent protein kinase IV gene. FEBS Lett. 1991, 289:105-109.
24. 2+/calmodulin-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:945-949.
25. Lindemann C.B., Goltz J.S. Calcium regulation of flagellar curvature and swimming pattern in Triton X-100 extracted rat sperm. Cell Motil. Cytoskeleton 1988, 10:420-431.
26. Lishko P.V., Botchkina I.L., Fedorenko A., Kirichok Y. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell 2010, 140:327-337.
27. 2+ channel of human sperm. Nature 2011, 471:387-391.
28. Lishko P.V., Kirichok Y. The role of Hv1 and CatSper channels in sperm activation. J. Physiol. 2010, 588:4667-4672.
29. Litvin T.N., Kamenetsky M., Zarifyan A., Buck J., Levin L.R. Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate. J. Biol. Chem. 2003, 278:15922-15926.
30. Marin-Briggiler C.I., Jha K.N., Chertihin O., Buffone M.G., Herr J.C., Vazquez-Levin M.H., Visconti P.E. Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation. J. Cell Sci. 2005, 118:2013-2022.
31. McPartlin L.A., Bedford-Guaus S.J. Soluble adenylate cyclase generated cAMP acts via protein kinase-A and not Epac 1/2 to direct capacitation-associated protein tyrosine phosphorylation in stallion sperm. Annual Conference of the Society for Theriogenology 2008, 589.
32. McPartlin L.A., Littell J., Mark E., Nelson J.L., Travis A.J., Bedford S.J. Successful in vitro capacitation of stallion sperm in a defined medium. Anim. Reprod. Sci. 2006, 94:168-169.
33. McPartlin L.A., Littell J., Mark E., Nelson J.L., Travis A.J., Bedford-Guaus S.J. A defined medium supports changes consistent with capacitation in stallion sperm, as evidenced by increases in protein tyrosine phosphorylation and high rates of acrosomal exocytosis. Theriogenology 2008, 69:639-650.
34. McPartlin L.A., Suarez S.S., Czaya C.A., Hinrichs K., Bedford-Guaus S.J. Hyperactivation of stallion sperm is required for successful in vitro fertilization of equine oocytes. Biol. Reprod. 2009, 81:199-206.
35. Miki K., Eddy E.M. Identification of tethering domains for protein kinase A type I alpha regulatory subunits on sperm fibrous sheath protein FSC1. J. Biol. Chem. 1998, 273:34384-34390.
36. Mori C., Nakamura N., Welch J.E., Gotoh H., Goulding E.H., Fujioka M., Eddy E.M. Mouse spermatogenic cell-specific type 1 hexokinase (mHk1-s) transcripts are expressed by alternative splicing from the mHk1 gene and the HK1-S protein is localized mainly in the sperm tail. Mol. Reprod. Dev. 1998, 49:374-385.
37. 2+/calmodulin-dependent protein phosphorylation. Cell Motil. Cytoskeleton 2006, 63:459-470.
38. Moriya M., Katagiri C., Ikebe M., Yagi K. Immunohistochemical detection of calmodulin and calmodulin-dependent protein kinase II in the mouse testis. Zygote 2000, 8:303-314.
39. Naito Y., Watanabe Y., Yokokura H., Sugita R., Nishio M., Hidaka H. Isoform-specific activation and structural diversity of calmodulin kinase I. J. Biol. Chem. 1997, 272:32704-32708.
40. Nakamura K., Fujita A., Murata T., Watanabe G., Mori C., Fujita J., Watanabe N., Ishizaki T., Yoshida O., Narumiya S. Rhophilin, a small GTPase Rho-binding protein, is abundantly expressed in the mouse testis and localized in the principal piece of the sperm tail. FEBS Lett. 1999, 445:9-13.
41. Navarro B., Kirichok Y., Clapham D.E. KSper, a pH-sensitive K+ current that controls sperm membrane potential. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:7688-7692.
42. Nolan M.A., Babcock D.F., Wennemuth G., Brown W., Burton K.A., McKnight G.S. Sperm-specific protein kinase A catalytic subunit Calpha2 orchestrates cAMP signaling for male fertility. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13483-13488.
43. Nomura M., Yoshida M., Morisawa M. Calmodulin/calmodulin-dependent protein kinase II mediates SAAF-induced motility activation of ascidian sperm. Cell Motil. Cytoskeleton 2004, 59:28-37.
44. Quill T.A., Sugden S.A., Rossi K.L., Doolittle L.K., Hammer R.E., Garbers D.L. Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14869-14874.
45. Quill T.A., Wang D., Garbers D.L. Insights into sperm cell motility signaling through sNHE and the CatSpers. Mol. Cell. Endocrinol. 2006, 250:84-92.
46. Ren D., Navarro B., Perez G., Jackson A.C., Hsu S., Shi Q., Tilly J.L., Clapham D.E. A sperm ion channel required for sperm motility and male fertility. Nature 2001, 413:603-609.
47. Romrell L.J., Bellvé A.R., Fawcett D.W. Separation of mouse spermatogenic cells by sedimentation velocity. Dev. Biol. 1976, 49:119-131.
48. Schlingmann K., Michaut M.A., McElwee J.L., Wolff C.A., Travis A.J., Turner R.M. Calmodulin and CaMKII in the sperm principal piece: evidence for a motility-related calcium/calmodulin pathway. J. Androl. 2007, 28:706-716.
49. 2+/calmodulin-dependent protein kinase II in cultures of hippocampal pyramidal neurons and astrocytes. J. Neurosci. 1988, 8:1039-1051.
50. Si Y., Olds-Clarke P. Evidence for the involvement of calmodulin in mouse sperm capacitation. Biol. Reprod. 2000, 62:1231-1239.
51. Storey B.T. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int. J. Dev. Biol. 2008, 52:427-437.
52. 2+ influx in human sperm. Nature 2011, 471:382-386.
53. Suarez S.S. Control of hyperactivation in sperm. Hum. Reprod. Update 2008, 14:647-657.
54. Suarez S.S., Ho H.C. Hyperactivated motility in sperm. Reprod. Domest. Anim. 2003, 38:119-124.
55. Suarez S.S., Vincenti L., Ceglia M.W. Hyperactivated motility induced in mouse sperm by calcium ionophore A23187 is reversible. J. Exp. Zool. 1987, 244:331-336.
56. Tamblyn T.M., Singh J.P., Lorton S.P., First N.L. Mechanisms controlling motility of stallion spermatozoa. J. Reprod. Fertil. Suppl. 1979, 31-37.
57. 2+ regulation of sperm axonemal motility. Methods Enzymol. 1987, 139:808-823.
58. Travis A.J., Foster J.A., Rosenbaum N.A., Visconti P.E., Gerton G.L., Kopf G.S., Moss S.B. Targeting of a germ cell-specific type 1 hexokinase lacking a porin-binding domain to the mitochondria as well as to the head and fibrous sheath of murine spermatozoa. Mol. Biol. Cell 1998, 9:263-276.
59. Travis A.J., Jorgez C.J., Merdiushev T., Jones B.H., Dess D.M., Diaz-Cueto L., Storey B.T., Kopf G.S., Moss S.B. Functional relationships between capacitation-dependent cell signaling and compartmentalized metabolic pathways in murine spermatozoa. J. Biol. Chem. 2001, 276:7630-7636.
60. Turner R.M., Johnson L.J., Haig-Ladewig L., Gerton G.L., Moss S.B. An X-linked gene encodes a major human sperm fibrous sheath protein, hAKAP82. Genomic organization, protein kinase A-RII binding, and distribution of the precursor in the sperm tail. J. Biol. Chem. 1998, 273:32135-32141.
61. Visconti P., Johnson L., Oyaski M., Fornes M., Moss S., Gerton G., Kopf G. Regulation localization and anchoring of protein kinase A subunits during mouse sperm capacitation. Dev. Biol. 1997, 192:351-363.
62. Visconti P.E., Bailey J.L., Moore G.D., Pan D., Olds-Clarke P., Kopf G.S. Capacitation of mouse spermatozoa I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 1995, 121:1129-1137.
63. Visconti P.E., Moore G.D., Bailey J.L., Leclerc P., Connors S.A., Pan D., Olds-Clarke P., Kopf G.S. Capacitation of mouse spermatozoa II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 1995, 121:1139-1150.
64. Westhoff D., Kamp G. Glyceraldehyde 3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa. J. Cell Sci. 1997, 110:1821-1829.
65. White D.R., Aitken R.J. Relationship between calcium, cyclic AMP, ATP, and intracellular pH and the capacity of hamster spermatozoa to express hyperactivated motility. Gamete Res. 1989, 22:163-177.
66. Yanagimachi R. Mammalian ferilization. The Physiology of Reproduction 1994, 189-317. Raven Press, Ltd., New York. E. Knobil, J.D. Neill (Eds.).
67. Yang P., Diener D.R., Rosenbaum J.L., Sale W.S. Localization of calmodulin and dynein light chain LC8 in flagellar radial spokes. J. Cell Biol. 2001, 153:1315-1326.
68. + current in mouse spermatozoa. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:5879-5884.
69. 3(-)-dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev. Biol. 1996, 173:510-520.