Aquaporin3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration

Cell Research

Volumn 21, Issue 6, 2011, Pages 922-933

  Chen, Qi ^a,b   Peng, Hongying ^a   Lei, Li ^a,b   Zhang, Ying ^a,b   Kuang, Haibin ^a,b   Cao, Yujing ^a   Shi, Qi Xian ^c   Ma, Tonghui ^d   Duan, Enkui ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF MATERIA MEDICA   (China)

^d THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

Author keywords

aquaporin3; osmoregulation; postcopulation; sperm

Indexed keywords

AQUAPORIN 3;

ADAPTATION; ANIMAL; ANIMAL EMBRYO; ARTICLE; CHEMISTRY; COITUS; COPULATION; CYTOLOGY; FEMALE; FERTILIZATION; GENETICS; HUMAN; MALE; MALE INFERTILITY; METABOLISM; MOUSE; MOUSE MUTANT; OSMOTIC PRESSURE; PHYSIOLOGY; SPERMATOZOON; SPERMATOZOON MOTILITY; SPERMATOZOON TAIL; TESTIS; ULTRASTRUCTURE; UTERUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AQUAPORIN 3; COITUS; COPULATION; EMBRYO, MAMMALIAN; FEMALE; FERTILIZATION; HUMANS; INFERTILITY, MALE; MALE; MICE; MICE, KNOCKOUT; OSMOTIC PRESSURE; SPERM MOTILITY; SPERM TAIL; SPERMATOZOA; TESTIS; UTERUS;

MAMMALIA; MUS;

EID: 79960038352     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2010.169     Document Type: Article

References (45)

1. Morisawa M, Suzuki K. Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts. Science 1980; 210:1145-1147. (Pubitemid 11166027)
2. Cosson J, Groison AL, Suquet M, et al. Marine fish spermatozoa: racing ephemeral swimmers. Reproduction 2008; 136:277-294.
3. Johnson AL, Howards SS. Hyperosmolality in intraluminal fluids from hamster testis and epididymis: a micropuncture study. Science 1977; 195:492-493.
4. Cooper TG, Yeung CH. Acquisition of volume regulatory response of sperm upon maturation in the epididymis and the role of the cytoplasmic droplet. Microsc Res Tech 2003; 61:28-38. (Pubitemid 36457544)
5. Rossato M, Di Virgilio F, Foresta C. Involvement of osmo-sensitive calcium infux in human sperm activation. Mol Hum Reprod 1996; 2:903-909. (Pubitemid 126715950)
6. Zanetti N, Mayorga LS. Acrosomal swelling and membrane docking are required for hybrid vesicle formation during the human sperm acrosome reaction. Biol Reprod 2009; 81:396-405.
7. Willoughby CE, Mazur P, Peter AT, Critser JK. Osmotic tolerance limits and properties of murine spermatozoa. Biol Re-prod 1996; 55:715-727. (Pubitemid 26295074)
8. Drevius LO, Eriksson H. Osmotic swelling of mammalian spermatozoa. Exp Cell Res 1966; 42:136-156.
9. Drevius LO. Spiralization in tails of mammalian spermatozoa in hypotonic media. Nature 1963; 197:1123-1124.
10. Yeung CH, Barfield JP, Cooper TG. Physiological volume regulation by spermatozoa. Mol Cell Endocrinol 2006; 250:98-105.
11. Curry MR, Redding BJ, Watson PF. Determination of water permeability coefficient and its activation energy for rabbit spermatozoa. Cryobiology 1995; 32:175-181.
12. Noiles EE, Mazur P, Watson PF, Kleinhans FW, Critser JK. Determination of water permeability coefficient for human spermatozoa and its activation energy. Biol Reprod 1993; 48:99-109. (Pubitemid 23005214)
13. Drevius LO. Permeability coeffcients of bull spermatozoa for water and polyhydric alcohols. Exp Cell Res 1971; 69:212-216.
14. Callies C, Cooper TG, Yeung CH. Channels for water effux and infux involved in volume regulation of murine spermatozoa. Reproduction 2008; 136:401-410.
15. Yeung CH, Barfeld JP, Cooper TG. The role of anion channels and Ca2+ in addition to K+ channels in the physiological volume regulation of murine spermatozoa. Mol Reprod Dev 2005; 71:368-379. (Pubitemid 40770391)
16. Petrunkina AM, Harrison RA, Ekhlasi-Hundrieser M, Topfer-Petersen E. Role of volume-stimulated osmolyte and anion channels in volume regulation by mammalian sperm. Mol Hum Reprod 2004; 10:815-823. (Pubitemid 40045014)
17. King LS, Kozono D, Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 2004; 5:687-698. (Pubitemid 39208179)
18. Curry MR, Millar JD, Watson PF. The presence of water channel proteins in ram and human sperm membranes. J Re-prod Fertil 1995; 104:297-303.
19. Ishibashi K, Kuwahara M, Kageyama Y, et al. Cloning and functional expression of a second new aquaporin abundantly expressed in testis. Biochem Biophys Res Commun 1997; 237:714-718. (Pubitemid 27434753)
20. Ishibashi K, Kuwahara M, Gu Y, et al. Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. J Biol Chem 1997; 272:20782-20786. (Pubitemid 27355645)
21. Yeung CH, Callies C, Rojek A, Nielsen S, Cooper TG. Aqua-porin isoforms involved in physiological volume regulation of murine spermatozoa. Biol Reprod 2009; 80:350-357.
22. Sohara E, Ueda O, Tachibe T, et al. Morphologic and functional analysis of sperm and testes in Aquaporin 7 knockout mice. Fertil Steril 2007; 87:671-676. (Pubitemid 46385954)
23. Yang B, Song Y, Zhao D, Verkman AS. Phenotype analysis of aquaporin-8 null mice. Am J Physiol Cell Physiol 2005; 288:C1161-C1170. (Pubitemid 40559391)
24. Ma T, Song Y, Yang B, et al. Nephrogenic diabetes insipidus in mice lacking aquaporin-3 water channels. Proc Natl Acad Sci USA 2000; 97:4386-4391. (Pubitemid 30226142)
25. Yeung CH, Callies C, Tuttelmann F, Kliesch S, Cooper TG. Aquaporins in the human testis and spermatozoa-identifca-tion, involvement in sperm volume regulation and clinical relevance. Int J Androl 2009; 33:629-641.
26. Yeung CH, Wagenfeld A, Nieschlag E, Cooper TG. The cause of infertility of male c-ros tyrosine kinase receptor knockout mice. Biol Reprod 2000; 63:612-618. (Pubitemid 30639954)
27. Yeung CH, Anapolski M, Cooper TG. Measurement of volume changes in mouse spermatozoa using an electronic sizing analyzer and a fow cytometer: validation and application to an infertile mouse model. J Androl 2002; 23:522-528. (Pubitemid 34655085)
28. Sutton KA, Jungnickel MK, Florman HM. A polycystin-1 controls postcopulatory reproductive selection in mice. Proc Natl Acad Sci USA 2008; 105:8661-8666. (Pubitemid 351987737)
29. Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev 2009; 89:193-277.
30. Hill AE, Shachar-Hill B, Shachar-Hill Y. What are aquaporins for? J Membr Biol 2004; 197:1-32. (Pubitemid 38221960)
31. Kuang K, Yiming M, Wen Q, et al. Fluid transport across cultured layers of corneal endothelium from aquaporin-1 null mice. Exp Eye Res 2004; 78:791-798. (Pubitemid 38252955)
32. Ford P, Rivarola V, Chara O, et al. Volume regulation in cortical collecting duct cells: role of AQP2. Biol Cell 2005; 97:687-697. (Pubitemid 41335162)
33. Liu X, Bandyopadhyay BC, Nakamoto T, et al. A role for AQP5 in activation of TRPV4 by hypotonicity: concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem 2006; 281:15485-15495. (Pubitemid 43855141)
34. Kida H, Miyoshi T, Manabe K, et al. Roles of aquaporin-3 water channels in volume-regulatory water fow in a human epithelial cell line. J Membr Biol 2005; 208:55-64.
35. Gadsby DC. Ion channels versus ion pumps: the principal difference, in principle. Nat Rev Mol Cell Biol 2009; 10:344-352.
36. Waight AB, Love J, Wang DN. Structure and mechanism of a pentameric formate channel. Nat Struct Mol Biol 2010; 17:31-37.
37. Wang Y, Huang Y, Wang J, et al. Structure of the formate transporter FocA reveals a pentameric aquaporin-like channel. Nature 2009; 462:467-472.
38. Cooper TG. Cytoplasmic droplets: the good, the bad or just confusing? Hum Reprod 2005; 20:9-11.
39. Lishko PV, Botchkina IL, Fedorenko A, Kirichok Y. Acid extrusion from human spermatozoa is mediated by fagellar voltage-gated proton channel. Cell 2010; 140:327-337.
40. Kirichok Y, Navarro B, Clapham DE. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature 2006; 439:737-740. (Pubitemid 43237621)
41. Miyamoto H, Chang MC. Effect of osmolality on fertilization of mouse and golden hamster eggs in vitro. J Reprod Fertil 1973; 33:481-487.
42. Kuang H, Chen Q, Fan X, et al. CXCL14 inhibits trophoblast outgrowth via a paracrine/autocrine manner during early pregnancy in mice. J Cell Physiol 2009; 221:448-457.
43. Sipila P, Cooper TG, Yeung CH, et al. Epididymal dysfunction initiated by the expression of simian virus 40 T-antigen leads to angulated sperm fagella and infertility in transgenic mice. Mol Endocrinol 2002; 16:2603-2617. (Pubitemid 35266078)
44. Xu WM, Shi QX, Chen WY, et al. Cystic fibrosis trans-membrane conductance regulator is vital to sperm fertilizing capacity and male fertility. Proc Natl Acad Sci USA 2007; 104:9816-9821.
45. Baibakov B, Gauthier L, Talbot P, Rankin TL, Dean J. Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis. Development 2007; 134:933-943. (Pubitemid 46795684)