The role of Hv1 and CatSper channels in sperm activation

Journal of Physiology

Volumn 588, Issue 23, 2010, Pages 4667-4672

  Lishko, Polina V ^a   Kirichok, Yuriy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL CATSPER; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL HV1;

CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL PH; FLAGELLUM; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPERM; SPERMATOZOON; SPERMATOZOON MOTILITY;

ANIMALS; CALCIUM CHANNELS; CALCIUM SIGNALING; HUMANS; ION CHANNEL GATING; ION CHANNELS; MALE; SPERMATOZOA;

EID: 78649702915     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.194142     Document Type: Review

References (58)

1. Acott TS & Carr DW (1984). Inhibition of bovine spermatozoa by caudal epididymal fluid: II. Interaction of pH and a quiescence factor. Biol Reprod 30, 926-935.
2. Austin CR (1951). Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res Ser 4, 581-596.
3. Avenarius MR, Hildebrand MS, Zhang Y, Meyer NC, Smith LL, Kahrizi K, Najmabadi H & Smith RJ (2009). Human male infertility caused by mutations in the CATSPER1 channel protein. Am J Hum Genet 84, 505-510.
4. Avidan N, Tamary H, Dgany O, Cattan D, Pariente A, Thulliez M, Borot N, Moati L, Barthelme A, Shalmon L, Krasnov T, Ben-Asher E, Olender T, Khen M, Yaniv I, Zaizov R, Shalev H, Delaunay J, Fellous M, Lancet D & Beckmann JS (2003). CATSPER2, a human autosomal nonsyndromic male infertility gene. Eur J Hum Genet 11, 497-502.
5. Babcock DF, Rufo GA Jr & Lardy HA (1983). Potassium-dependent increases in cytosolic pH stimulate metabolism and motility of mammalian sperm. Proc Natl Acad Sci U S A 80, 1327-1331.
6. Cai X & Clapham DE (2008). Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperβ PloS One 3, e3569.
7. 2+ acts upstream of adenylyl cyclase SACY in the bicarbonate signaled activation of sperm motility. Dev Biol 312, 183-192.
8. Carlson AE, Quill TA, Westenbroek RE, Schuh SM, Hille B & Babcock DF (2005). Identical phenotypes of CatSper1 and CatSper2 null sperm. J Biol Chem 280, 32238-32244.
9. 2+ entry and control of flagellar function in sperm. Proc Natl Acad Sci U S A 100, 14864-14868.
10. Carr DW & Acott TS (1989). Intracellular pH regulates bovine sperm motility and protein phosphorylation. Biol Reprod 41, 907-920.
11. Chang MC (1951). Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168, 697-698.
12. Cummins J (2009). Sperm Biology: An Evolutionary Perspective, p. 195. Elsevier, Burlington, MA, USA
13. DeCoursey TE (2008). Voltage-gated proton channels: what's next? J Physiol 586, 5305-5324.
14. Ehrenwald E, Foote RH & Parks JE (1990). Bovine oviductal fluid components and their potential role in sperm cholesterol efflux. Mol Reprod Dev 25, 195-204.
15. El-Talatini MR, Taylor AH, Elson JC, Brown L, Davidson AC & Konje JC (2009). Localisation and function of the endocannabinoid system in the human ovary. PloS One 4, e4579.
16. Eroglu C, Allen NJ, Susman MW, O'Rourke NA, Park CY, Ozkan E, Chakraborty C, Mulinyawe SB, Annis DS, Huberman AD, Green EM, Lawler J, Dolmetsch R, Garcia KC, Smith SJ, Luo ZD, Rosenthal A, Mosher DF & Barres BA (2009). Gabapentin receptor α 2δ -1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139, 380-392.
17. Florman HM, Jungnickel MK & Sutton KA (2010). Shedding light on sperm pHertility. Cell 140, 310-312.
18. Fraser LR (2010). The "switching on" of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation. Mol Reprod Dev 77, 197-208.
19. Gunn SA & Gould TC (1958). Role of zinc in fertility and fecundity in the rat. Am J Physiol 193, 505-508.
20. Hamamah S & Gatti JL (1998). Role of the ionic environment and internal pH on sperm activity. Hum Reprod 13(Suppl 4), 20-30.
21. Hammar JA (1897). Uber Secretionserscheinungen im Nebenhoden des Hundes. Zugleich ein Beitrag zur Physiologie des Zellenkerns. Arch Anat Phys Anat Abth Suppl, 1-42.
22. Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS, Suarez SS, Levin LR, Williams CJ, Buck J & Moss SB (2005). The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev Cell 9, 249-259.
23. Ho K, Wolff CA & Suarez SS (2009). CatSper-null mutant spermatozoa are unable to ascend beyond the oviductal reservoir. Reprod Fertil Dev 21, 345-350.
24. Kaupp UB, Kashikar ND & Weyand I (2008). Mechanisms of sperm chemotaxis. Annu Rev Physiol 70, 93-117.
25. 2+ channel. Nature 439, 737-740.
26. Koch HP, Kurokawa T, Okochi Y, Sasaki M, Okamura Y & Larsson HP (2008). Multimeric nature of voltage-gated proton channels. Proc Natl Acad Sci U S A 105, 9111-9116.
27. Lee SY, Letts JA & Mackinnon R (2008). Dimeric subunit stoichiometry of the human voltage-dependent proton channel Hv1. Proc Natl Acad Sci U S A 105, 7692-7695.
28. Linares-Hernandez L, Guzman-Grenfell AM, Hicks-Gomez JJ & Gonzalez-Martinez MT (1998). Voltage-dependent calcium influx in human sperm assessed by simultaneous optical detection of intracellular calcium and membrane potential. Biochim Biophys Acta 1372, 1-12.
29. Lishko PV, Botchkina IL, Fedorenko A & Kirichok Y (2010). Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell 140, 327-337.
30. Liu J, Xia J, Cho KH, Clapham DE & Ren D (2007). CatSperβ , a novel transmembrane protein in the CatSper channel complex. J Biol Chem 282, 18945-18952.
31. Lobley A, Pierron V, Reynolds L, Allen L & Michalovich D (2003). Identification of human and mouse CatSper3 and CatSper4 genes: characterisation of a common interaction domain and evidence for expression in testis. Reprod Biol Endocrinol 1, 53.
32. Lu J, Stewart AJ, Sadler PJ, Pinheiro TJ & Blindauer CA (2008). Albumin as a zinc carrier: properties of its high-affinity zinc-binding site. Biochem Soc Trans 36, 1317-1321.
33. Mahi CA & Yanagimachi R (1973). The effects of temperature, osmolality and hydrogen ion concentration on the activation and acrosome reaction of golden hamster spermatozoa. J Reprod Fertil 35, 55-66.
34. 2+ to regulation of sperm motility: Release of intracellular stores can hyperactivate CatSper1 and CatSper2 null sperm. Dev Biol 303, 214-221.
35. Navarro B, Kirichok Y, Chung JJ & Clapham DE (2008). Ion channels that control fertility in mammalian spermatozoa. Int J Dev Biol 52, 607-613.
36. Nixon B & Aitken RJ (2009). The biological significance of detergent-resistant membranes in spermatozoa. J Reprod Immunol 83, 8-13.
37. Okochi Y, Sasaki M, Iwasaki H & Okamura Y (2009). Voltage-gated proton channel is expressed on phagosomes. Biochem Biophys Res Commun 382, 274-279.
38. Qi H, Moran MM, Navarro B, Chong JA, Krapivinsky G, Krapivinsky L, Kirichok Y, Ramsey IS, Quill TA & Clapham DE (2007). All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci U S A 104, 1219-1223.
39. + permeation pathway in the voltage-gated proton channel Hv1. Nat Struct Mol Biol 17, 869-875.
40. Ramsey IS, Moran MM, Chong JA & Clapham DE (2006). A voltage-gated proton-selective channel lacking the pore domain. Nature 440, 1213-1216.
41. Ramsey IS, Ruchti E, Kaczmarek JS & Clapham DE (2009). Hv1 proton channels are required for high-level NADPH oxidase-dependent superoxide production during the phagocyte respiratory burst. Proc Natl Acad Sci U S A 106, 7642-7647.
42. Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tilly JL & Clapham DE (2001). A sperm ion channel required for sperm motility and male fertility. Nature 413, 603-609.
43. Saaranen M, Suistomaa U, Kantola M, Saarikoski S & Vanha-Perttula T (1987). Lead, magnesium, selenium and zinc in human seminal fluid: comparison with semen parameters and fertility. Hum Reprod 2, 475-479.
44. Sasaki M, Takagi M & Okamura Y (2006). A voltage sensor-domain protein is a voltage-gated proton channel. Science 312, 589-592.
45. Stauss CR, Votta TJ & Suarez SS (1995). Sperm motility hyperactivation facilitates penetration of the hamster zona pellucida. Biol Reprod 53, 1280-1285.
46. Suarez SS (2008). Control of hyperactivation in sperm. Hum Reprod Update 14, 647-657.
47. Suarez SS & Ho HC (2003). Hyperactivated motility in sperm. Reprod Domest Anim 38, 119-124.
48. Suarez SS & Pacey AA (2006). Sperm transport in the female reproductive tract. Hum Reprod Update 12, 23-37.
49. Thomas RC & Meech RW (1982). Hydrogen ion currents and intracellular pH in depolarized voltage-clamped snail neurones. Nature 299, 826-828.
50. Tombola F, Ulbrich MH & Isacoff EY (2008). The voltage-gated proton channel Hv1 has two pores, each controlled by one voltage sensor. Neuron 58, 546-556.
51. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P & Kopf GS (1995a). Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121, 1129-1137.
52. Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P & Kopf GS (1995b). Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121, 1139-1150.
53. + exchanger (sNHE) is critical for expression and in vivo bicarbonate regulation of the soluble adenylyl cyclase (sAC). Proc Natl Acad Sci U S A 104, 9325-9330.
54. + exchanger required for sperm motility and fertility. Nat Cell Biol 5, 1117-1122.
55. Wang H, Liu J, Cho KH & Ren D (2009). A novel, single, transmembrane protein CATSPERG is associated with CATSPER1 channel protein. Biol Reprod 81, 539-544.
56. Yanagimachi R (1969). In vitro capacitation of hamster spermatozoa by follicular fluid. J Reprod Fertil 18, 275-286.
57. Yanagimachi R (1970). The movement of golden hamster spermatozoa before and after capacitation. J Reprod Fertil 23, 193-196.
58. --dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev Biol 173, 510-520.