Aquaporin isoforms involved in physiological volume regulation of murine spermatozoa

Biology of Reproduction

Volumn 80, Issue 2, 2009, Pages 350-357

  Yeung, Ching Hei ^a   Callies, Chiara ^a   Rojek, Aleksandra ^b   Nielsen, Søren ^b   Cooper, Trevor G ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

AQP7 knockout; AQP8; Aquaporin mRNA; Cell volume regulation; Epididymis; Gamete biology; Sperm; Sperm regulatory volume decrease; Sperm water channels

Indexed keywords

AQUAPORIN; AQUAPORIN 7; AQUAPORIN 8; AQUAPORIN 9; MERCURIC CHLORIDE; POTASSIUM CHANNEL; QUININE; VALINOMYCIN;

ANIMAL CELL; ARTICLE; CELL SIZE; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; EPIDIDYMIS; FERTILIZATION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OSMOLALITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SPERMATOZOON; TRANSGENIC MOUSE; WATER TRANSPORT; WESTERN BLOTTING;

ANIMALS; AQUAPORINS; CELL SIZE; CELLS, CULTURED; EJACULATION; FERTILIZATION; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; SPERMATOZOA; WATER;

MURINAE; MUS; MUS MUSCULUS;

EID: 59949083707     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.071928     Document Type: Article

References (51)

1. 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.
2. 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.
3. Cooper TG, Yeung CH, Wagenfeld A, Nieschlag E, Poutanen M, Huhtaniemi I, Sipila P. Mouse models of infertility due to swollen spermatozoa. Mol Cell Endocrin 2004; 216:55-63.
4. Yeung CH, Cooper TG. Effects of the ion-channel blocker quinine on human sperm volume, kinematics and mucus penetration, and the involvement of potassium channels. Mol Hum Reprod 2001; 7:819-828.
5. Petrunkina AM, Petzoldt R, Stahlberg S, Pfeilsticker J, Beyerbach M, Bader H, Topfer-Petersen E. Sperm-cell volumetric measurements as parameters in bull semen function evaluation: correlation with nonreturn rate. Andrologia 2001; 33:360-367.
6. Fetic S, Yeung CH, Sonntag B, Nieschlag E, Cooper TG. Relationship of cytoplasmic droplets to motility, migration in mucus, and volume regulation of human spermatozoa. J Androl 2006; 27:294-301.
7. Yeung CH, Cooper TG. Potassium channels involved in human sperm volume regulation-quantitative studies at the protein and mRNA levels. Mol Reprod Dev 2008; 75:659-668.
8. Lang F. Mechanisms and significance of cell volume regulation. J Am Coll Nutr 2007; 26:613S-623S.
9. Yeung CH, Barfield JP, Cooper TG. Chloride channels in physiological volume regulation of human spermatozoa. Biol Reprod 2005; 73:1057-1063.
10. Cooper TG, Yeung CH. Involvement of potassium and chloride channels and other transporters in volume regulation by spermatozoa. Curr Pharm Des 2007; 13:3222-3230.
11. Curry MR, Millar JD, Watson PE. The presence of water channel proteins in ram and human sperm membranes. J Reprod Fertil 1995; 104:297-303.
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.
13. Noiles EE, Thompson KA, Storey BT. Water permeability, L-p, of the mouse sperm plasma membrane and its activation energy are strongly dependent on interaction of the plasma membrane with the sperm cytoskeleton. Cryobiology 1997; 35:79-92.
14. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S. Aquaporin water channels-from atomic structure to clinical medicine. J Physiol 2002; 542:3-16.
15. Shima JE, McLean DJ, McCarrey JR, Griswold MD. The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 2004; 71:319-330.
16. Schultz N, Hamra FK, Garbers DL. A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci USA 2003; 100:12201-12206.
17. Verkman AS. More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 2005; 118:3225-3232.
18. Castle NA. Aquaporins as targets for drug discovery. Drug Discov Today 2005; 10:485-493.
19. Morinaga T, Nakakoshi M, Hirao A, Imai M, Ishibashi K. Mouse aquaporin 10 gene (AQP10) is a pseudogene. Biochem Biophys Res Commun 2002; 294:630-634.
20. Calamita G, Mazzone A, Bizzoca A, Svelto M. Possible involvement of aquaporin-7 and -8 in rat testis development and spermatogenesis. Biochem Biophys Res Commun 2001; 288:619-625.
21. Saito K, Kageyama Y, Okada Y, Kawakami S, Kihara K, Ishibashi K, Sasaki S. Localization of aquaporin-7 in human testis and ejaculated sperm: possible involvement in maintenance of sperm quality. J Urol 2004; 172:2073-2076.
22. Skowronski MT, Lebeck J, Rojek A, Praetorius J, Fuchtbauer EM, Frokiaer J, Nielsen S. AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism. Am J Physiol Renal Physiol 2007; 292:F956-F965.
23. Suzuki-Toyota F, Ishibashi K, Yuasa S. Immunohistochemical localization of a water channel, aquaporin 7 (AQP7), in the rat testis. Cell Tissue Res 1999; 295:279-285.
24. + channels in the physiological volume regulation of murine spermatozoa. Mol Reprod Dev 2005; 71:368-379.
25. Yeung CH, Anapolski M, Sipilä P, Wagenfeld A, Poutanen M, Huhtaniemi I, Nieschlag E, Cooper TG. Sperm volume regulation- maturational changes in fertile and infertile transgenic mice and association with kinematics and tail angulation. Biol Reprod 2002; 67: 269-275.
26. Yeung CH, Anapolski M, Cooper TG. Measurement of volume changes in mouse spermatozoa using an electronic sizing analyser and a flow cytometer-validation and application to an infertile mouse model. J Androl 2002; 23:522-528.
27. Ishibashi K, Kuwahara M, Gu Y, Kageyama Y, Tohsaka A, Suzuki F, Marumo F, Sasaki S. 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.
28. Biggers JD, Whitten WK, Whittingham DG. The culture of mouse embryos in vitro. In: Daniel JC (ed.), Methods in Mammalian Embryology. San Francisco: Freeman; 1971:86-116.
29. Yeung CH, Sonnenberg-Riethmacher E, Cooper TG. Infertile spermatozoa of c-ros tyrosine kinase receptor knockout mice show flagellar angulation and maturational defects in cell volume regulatory mechanisms. Biol Reprod 1999; 61:1062-1069.
30. Klein T, Cooper TG, Yeung CH. The role of potassium chloride cotransporters in murine and human sperm volume regulation. Biol Reprod 2006; 75:853-858.
31. O'Shaughnessy PJ, Willerton L, Baker PJ. Changes in Leydig cell gene expression during development in the mouse. Biol Reprod 2002; 66:966-975.
32. Yeung CH, Anapolski M, Setiawan I, Lang F, Cooper TG. Effects of putative epididymal osmolytes on sperm volume regulation of fertile and infertile c-ros transgenic mice. J Androl 2004; 25:216-223.
33. Pastor-Soler N, Bagnis C, Sabolic I, Tyszkowski R, McKee M, Van Hoek A, Breton S, Brown D. Aquaporin 9 expression along the male reproductive tract. Biol Reprod 2001; 65:384-393.
34. Oliveira CA, Carnes K, Franca LR, Hermo L, Hess RA. Aquaporin-1 and -9 are differentially regulated by oestrogen in the efferent ductule epithelium and initial segment of the epididymis. Biol Cell 2005; 97:385-395.
35. Tsukaguchi H, Shayakul C, Berger UV, Mackenzie B, Devidas S, Guggino WB, van Hoek AN, Hediger MA. Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem 1998; 273:24737-24743.
36. Badran HH, Hermo LS. Expression and regulation of aquaporins 1, 8 and 9 in the testis, efferent ducts, and epididymis of adult rats and during postnatal development. J Androl 2002; 23:358-373.
37. Da Silva N, Silberstein C, Beaulieu V, Pietrement C, Van Hoek AN, Brown D, Breton S. Postnatal expression of aquaporins in epithelial cells of the rat epididymis. Biol Reprod 2006; 74:427-438.
38. Yang B, Song Y, Zhao D, Verkman AS. Phenotype analysis of aquaporin- 8 null mice. Am J Physiol Cell Physiol 2005; 288:C1161-C1170.
39. Calamita G, Mazzone A, Cho YS, Valenti G, Svelto M. Expression and localization of the aquaporin-8 water channel in rat testis. Biol Reprod 2001; 64:1660-1666.
40. Elkjaer ML, Nejsum LN, Gresz V, Kwon TH, Jensen UB, Frokiaer J, Nielsen S. Immunolocalization of aquaporin-8 in rat kidney, gastrointestinal tract, testis, and airways. Am J Physiol Renal Physiol 2001; 281: F1047-F1057.
41. Ishibashi K, Kuwahara M, Kageyama Y, Tohsaka A, Marumo F, Sasaki S. Cloning and functional expression of a second new aquaporin abundantly expressed in testis. Biochem Biophys Res Commun 1997; 237:714-718.
42. Kageyama Y, Ishibashi K, Hayashi T, Xia G, Sasaki S, Kihara K. Expression of aquaporins 7 and 8 in the developing rat testis. Andrologia 2001; 33:165-169.
43. Kerr JB, Loveland KL, O'Bryan MK, de Kretser DM. Cytology of the testis and intrinsic control mechanisms. In: Knobil E, Neill JD (eds.), Physiology of Reproduction. New York: Elsevier; 2006:827-948.
44. Sohara E, Ueda O, Tachibe T, Hani T, Jishage K, Rai T, Sasaki S, Uchida S. Morphologic and functional analysis of sperm and testes in Aquaporin 7 knockout mice. Fertil Steril 2007; 87:671-676.
45. Kleene KC. A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech Dev 2001; 106:3-23.
46. Elliott D. Pathways of post-transcriptional gene regulation in mammalian germ cell development. Cytogenet Genome Res 2003; 103:210-216.
47. Miller D, Ostermeier GC. Towards a better understanding of RNA carriage by ejaculate spermatozoa. Hum Reprod Update 2006; 12:757-767.
48. Kuang K, Yiming M, Wen Q, Li Y, Ma L, Iserovich P, Verkman AS, Fischbarg J. Fluid transport across cultured layers of corneal endothelium from aquaporin-1 null mice. Exp Eye Res 2004; 78:791-798.
49. Krane CM, Melvin JE, Nguyen HV, Richardson L, Towne JE, Doetsch- man T, Menon AG. Salivary acinar cells from aquaporin 5-deficient mice have decreased membrane water permeability and altered cell volume regulation. J Biol Chem 2001; 276:23413-23420.
50. Hansen AK, Galtung HK. Aquaporin expression and cell volume regulation in the SV40 immortalized rat submandibular acinar cell line. Pflugers Arch 2007; 453:787-796.
51. Benfenati V, Nicchia GP, Svelto M, Rapisarda C, Frigeri A, Ferroni S. Functional down-regulation of volume-regulated anion channels in AQP4 knockdown cultured rat cortical astrocytes. J Neurochem 2007; 100:87-104.