Osmoregulation in fish sperm
Jazyk angličtina Země Nizozemsko Médium print-electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
LM2018099
Ministerstvo Školství, Mládeže a Tělovýchovy (CZ)
CZ.02.1.01./0.0/0.0/16_025/0007370
Ministerstvo Školství, Mládeže a Tělovýchovy
125/2016/Z
Grantová Agentura JU (CZ)
18-12465Y
Grantová Agentura České Republiky (CZ)
PubMed
34076793
DOI
10.1007/s10695-021-00958-1
PII: 10.1007/s10695-021-00958-1
Knihovny.cz E-zdroje
- Klíčová slova
- Aquaporins, Motility, Osmoresistance,·Water transport,
- MeSH
- akvaporiny fyziologie MeSH
- kryoprezervace MeSH
- lidé MeSH
- lipidy fyziologie MeSH
- osmoregulace * MeSH
- ryby fyziologie MeSH
- spermie fyziologie MeSH
- uchování spermatu MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- akvaporiny MeSH
- lipidy MeSH
In most fish exhibiting external fertilization, spermatozoa become motile after release into water, triggered by differences between intracellular and extracellular conditions such as osmotic pressure, ion composition, and pH. The rapid change in osmolarity initiating spermatozoon motility induces osmotic pressure, resulting in active water movement across the cell membrane. Mechanisms of ion and water transport across the plasma membrane and cell volume regulation are important in maintaining structure and functional integrity of the cell. The capacity of the fish spermatozoon plasma membrane to adapt to dramatic environmental changes is an essential prerequisite for motility and successful fertilization. Adaptation to change in external osmolality may be the basis of spermatozoon function and an indicator of sperm quality. The involvement of specific water channels (aquaporins) in cell volume regulation and motility is highly likely. The goal of this review is to describe basic mechanisms of water transport and their role in fish spermatozoon physiology, focusing on osmoresistance, cell volume regulation, motility, and survival.
Zobrazit více v PubMed
Abascal FJ, Cosson J, Fauvel C (2007) Characterization of sperm motility in sea bass: the effect of heavy metals and physicochemical variables on sperm motility. J Fish Biol 70:509–522. https://doi.org/10.1111/j.1095-8649.2007.01322.x DOI
Agre P, King LS, Yasui M et al (2002) Aquaporin water channels–from atomic structure to clinical medicine. J Physiol 542:3–16. https://doi.org/10.1113/jphysiol.2002.020818 PubMed DOI PMC
Alavi SMH, Cosson J (2006) Sperm motility in fishes. (II) Effects of ions and osmolality: a review. Cell Biol Int 30:1–14 DOI
Alavi SMH, Gela D, Rodina M, Linhart O (2011) Roles of osmolality, calcium-potassium antagonist and calcium in activation and flagellar beating pattern of sturgeon sperm. Comp Biochem Physiol A Mol Integr Physiol. https://doi.org/10.1016/j.cbpa.2011.05.026 PubMed DOI
Alavi SMH, Matsumura N, Shiba K et al (2014) Roles of extracellular ions and pH in 5-HT-induced sperm motility in marine bivalve. Reproduction 147:331–345. https://doi.org/10.1530/REP-13-0418 PubMed DOI
Alavi SMH, Cosson J, Bondarenko O, Linhart O (2019) Sperm motility in fishes: (III) diversity of regulatory signals from membrane to the axoneme. Theriogenology 136:143–165. https://doi.org/10.1016/j.theriogenology.2019.06.038 PubMed DOI
Arena S, Arena F, Maisano D et al (2011) Aquaporin-9 immunohistochemistry in varicocele testes as a consequence of hypoxia in the sperm production site. Andrologia 43:34–37. https://doi.org/10.1111/j.1439-0272.2009.01009.x PubMed DOI
Baeza R, Mazzeo I, Vílchez MC et al (2015) Relationship between sperm quality parameters and the fatty acid composition of the muscle, liver and testis of European eel. Comp Biochem Physiol A Mol Integr Physiol 181:79–86. https://doi.org/10.1016/j.cbpa.2014.11.022 PubMed DOI
Bobe J, Labbé C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165:535–548. https://doi.org/10.1016/j.ygcen.2009.02.011 PubMed DOI
Bondarenko O, Dzyuba B, Cosson J et al (2013) Volume changes during the motility period of fish spermatozoa: interspecies differences. Theriogenology 79:872–881. https://doi.org/10.1016/j.theriogenology.2013.01.005 PubMed DOI
Bondarenko O, Dzyuba B, Cosson J et al (2014) The role of Ca2+ and Na+ membrane transport in brook trout (Salvelinus fontinalis) spermatozoa motility. Fish Physiol Biochem. https://doi.org/10.1007/s10695-014-9936-5 PubMed DOI
Bonilla-Correal S, Noto F, Garcia-Bonavila E et al (2017) First evidence for the presence of aquaporins in stallion sperm. Reprod Domest Anim 52:61–64. https://doi.org/10.1111/rda.13059 PubMed DOI
Boryshpolets S, Dzyuba B, Rodina M et al (2009) Freeze-thawing as the factor of spontaneous activation of spermatozoa motility in common carp (Cyprinus carpio L.). Cryobiology 59:291–296. https://doi.org/10.1016/j.cryobiol.2009.08.005 PubMed DOI
Boulais M, Suquet M, Arsenault-Pernet EJ et al (2018) pH controls spermatozoa motility in the Pacific oyster (Crassostrea gigas). Biol Open 7:bio031427. https://doi.org/10.1242/bio.031427 PubMed DOI PMC
Cabrita E, Robles V, Rebordinos L et al (2005) Evaluation of DNA damage in rainbow trout (Oncorhynchus mykiss) and gilthead sea bream (Sparus aurata) cryopreserved sperm. Cryobiology 50:144–153. https://doi.org/10.1016/j.cryobiol.2004.12.003 PubMed DOI
Caldwell RA, Clemo HF, Baumgarten CM (1998) Using gadolinium to identify stretch-activated channels: technical considerations. Am J Physiol Cell Physiol 275:C619–C621. https://doi.org/10.1152/ajpcell.1998.275.2.c619 DOI
Cejko BI, Horváth Á, Kollár T et al (2018) Optimisation of sodium and potassium concentrations and pH in the artificial seminal plasma of common carp Cyprinus carpio L. Fish Physiol Biochem 44:1435–1442. https://doi.org/10.1007/s10695-018-0491-3 PubMed DOI PMC
Chen Q, Duan EK (2011) Aquaporins in sperm osmoadaptation: an emerging role for volume regulation. Acta Pharmacol Sin 32:721–724 DOI
Christen R, Schackmann RW, Dahlquist FW, Shapiro BM (1983a) 31P-NMR analysis of sea urchin sperm activation. Reversible formation of high energy phosphate compounds by changes in intracellular pH. Exp Cell Res 149:289–294 DOI
Christen R, Schackmann RW, Shapiro BM (1983b) Metabolism of sea urchin sperm. Interrelationships between intracellular pH, ATPase activity, and mitochondrial respiration. J Biol Chem 258:5392–5399 DOI
Cosson J, Dreanno C, Billard R, Suquet M, Cibert C (1999) Ionic factors regulating the motility of fish sperm. In: Cagnon C (ed) The male gamete: from basic science to clinical applications. Cache River Press, Montreal, pp 161–186
Cosson J, Groison AL, Suquet M, Fauvel C, Dreanno C, Billard R (2008) Studying sperm motility in marine fish: an overview on the state of the art. J Appl Ichthyol 24(4):460–486. https://doi.org/10.1111/j.1439-0426.2008.01151.x
Cutler CP, Martinez AS, Cramb G (2007) The role of aquaporin 3 in teleost fish. Comp Biochem Physiol A Mol Integr Physiol 148:82–91. https://doi.org/10.1016/j.cbpa.2006.09.022 PubMed DOI
Dadras H, Sampels S, Golpour A et al (2017) Analysis of common carp Cyprinus carpio sperm motility and lipid composition using different in vitro temperatures. Anim Reprod Sci 180:37–43. https://doi.org/10.1016/j.anireprosci.2017.02.011 PubMed DOI
Danziger J, Zeidel ML (2015) Osmotic homeostasis. Clin J Am Soc Nephrol 10:852–862. https://doi.org/10.2215/CJN.10741013 PubMed DOI
Dawaliby R, Trubbia C, Delporte C et al (2016) Phosphatidylethanolamine is a key regulator of membrane fluidity in eukaryotic cells. J Biol Chem 291:3658–3667. https://doi.org/10.1074/jbc.M115.706523 PubMed DOI
Demoy-Schneider M, Levêque A, Schmitt N et al (2012) Motility activation and metabolism characteristics of spermatozoa of the black-lip-pearl oyster Pinctada margaritifera var: Cumingii (Jameson, 1901). Theriogenology 77:53–64. https://doi.org/10.1016/j.theriogenology.2011.07.014 PubMed DOI
Dong Q, Huang C, Tiersch TR (2007) Control of sperm concentration is necessary for standardization of sperm cryopreservation in aquatic species: evidence from sperm agglutination in oysters. Cryobiology 54:87–98. https://doi.org/10.1016/j.cryobiol.2006.11.007 PubMed DOI
Drokin SI, Ii O, Rrsour L et al (1993) Phospholipid distribution and fatty acid composition of phosphatidylcholine and phosphatidylethanolamine in sperm of some freshwater and marine species of fish. Aquat Living Resour 6:49–56. https://doi.org/10.1051/alr:1993005 DOI
Dumorné K, Valdebenito I, Risopatron J et al (2018) Morphology and ultrastructure of pink cusk-eel (Genypterus blacodes, Schneider 1801) spermatozoa by scanning and transmission electron microscopy. Tissue Cell 54:26–29. https://doi.org/10.1016/j.tice.2018.07.005 PubMed DOI
Dzuba BB, Kopeika EF (2002) Relationship between the changes in cellular volume of fish spermatozoa and their cryoresistance. Cryo-Letters 23:353–360 PubMed
Dzyuba V, Sampels S, Ninhaus-Silveira A et al (2019) Sperm motility and lipid composition in internally fertilizing ocellate river stingray Potamotrygon motoro. Theriogenology 130:26–35. https://doi.org/10.1016/j.theriogenology.2019.02.029 PubMed DOI
Elliott GD, Wang S, Fuller BJ (2017) Cryoprotectants: a review of the actions and applications of cryoprotective solutes that modulate cell recovery from ultra-low temperatures. Cryobiology 76:74–91. https://doi.org/10.1016/j.cryobiol.2017.04.004 PubMed DOI
Engel KM, Sampels S, Dzyuba B et al (2019) Swimming at different temperatures: the lipid composition of sperm from three freshwater fish species determined by mass spectrometry and nuclear magnetic resonance spectroscopy. Chem Phys Lipids 221:65–72. https://doi.org/10.1016/j.chemphyslip.2019.03.014 PubMed DOI
Faure C, Devauchelle N, Girard JP (1994) Ionic factors affecting motility, respiration and fertilization rate of the sperm of the bivalve Pecten maximus (L.). J Comp Physiol B 164:444–450. https://doi.org/10.1007/BF00714581 DOI
Giffard-Mena I, Boulo V, Aujoulat F et al (2007) Aquaporin molecular characterization in the sea-bass (Dicentrarchus labrax): the effect of salinity on AQP1 and AQP3 expression. Comp Biochem Physiol A Mol Integr Physiol 148:430–444. https://doi.org/10.1016/j.cbpa.2007.06.002 PubMed DOI
Hazel JR, Eugene Williams E (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227 DOI
Hille B (1978) Ionic channels in excitable membranes. Current problems and biophysical approaches. Biophys J 22:283–294. https://doi.org/10.1016/S0006-3495(78)85489-7 PubMed DOI PMC
Horokhovatskyi Y, Sampels S, Cosson J et al (2016) Lipid composition in common carp (Cyprinus carpio) sperm possessing different cryoresistance. Cryobiology 73:282–285. https://doi.org/10.1016/j.cryobiol.2016.08.005 PubMed DOI
Hu J, Zhang Y, Zhou R, Zhang Y (2009) Changes in extracellular osmolality initiate sperm motility in freshwater teleost rosy barb Puntius conchonius. Theriogenology 72:704–710. https://doi.org/10.1016/j.theriogenology.2009.05.009 PubMed DOI
Ito J, Kawabe M, Ochiai H et al (2008) Expression and immunodetection of aquaporin 1 (AQP1) in canine spermatozoa. Cryobiology 57:312–314. https://doi.org/10.1016/j.cryobiol.2008.09.012 PubMed DOI
John Morris G, Acton E, Murray BJ, Fonseca F (2012) Freezing injury: the special case of the sperm cell. Cryobiology 64:71–80. https://doi.org/10.1016/j.cryobiol.2011.12.002 PubMed DOI
Johnston SD, Lever J, McLeod R et al (2014) Semen collection and seminal characteristics of the Australian saltwater crocodile (Crocodylus porosus). Aquaculture 422–423:25–35. https://doi.org/10.1016/j.aquaculture.2013.11.002 DOI
Krasznai Z, Márián T, Balkay L et al (1995) Potassium channels regulate hypo-osmotic shock-induced motility of common carp (Cyprinus carpio) sperm. Aquaculture 129:123–128. https://doi.org/10.1016/0044-8486(94)00234-F DOI
Krasznai Z, Morisawa M, Krasznai ZT et al (2003a) Gadolinium, a mechano-sensitive channel blocker, inhibits osmosis-initiated motility of sea- and freshwater fish sperm, but does not affect human or ascidian sperm motility. Cell Motil Cytoskeleton 55:232–243. https://doi.org/10.1002/cm.10125 PubMed DOI
Krasznai ZT, Morisawa M, Morisawa S et al (2003b) Role of ion channels and membrane potential in the initiation of carp sperm motility. Aquat Living Resour 16:445–449. https://doi.org/10.1016/S0990-7440(03)00054-8 DOI
Kulbacka J, Choromoanske A, Rossowska J, Wezgowiec J, Saczko J, Rols M-P (2017) Cell membrane transport mechanisms: ion channels and electrical properties of cell membranes. In: Kulbacka J, Satkauskas S (eds) Advances in anatomy, embryology and cell biology, transport across natural and modified biological membranes and its implications in physiology and therapy. Springer, Switzerland. Retrieved from https://www.springer.com/series/102
Kunkitti P, Chatdarong K, Suwimonteerabutr J et al (2017) Osmotic tolerance of feline epididymal spermatozoa. Anim Reprod Sci 185:148–153. https://doi.org/10.1016/j.anireprosci.2017.08.014 PubMed DOI
Labbe C, Maisse G, Muller K et al (1995) Thermal acclimation and dietary lipids alter the composition, but not fluidity, of trout sperm plasma membrane. Lipids 30:23–33. https://doi.org/10.1007/BF02537038 PubMed DOI
Lahnsteiner F, Mansour N, McNiven MA, Richardson GF (2009) Fatty acids of rainbow trout (Oncorhynchus mykiss) semen: composition and effects on sperm functionality. Aquaculture 298:118–124. https://doi.org/10.1016/j.aquaculture.2009.08.034 DOI
Lee HC, Johnson C, Epel D (1983) Changes in internal pH associated with initiation of motility and acrosome reaction of sea urchin sperm. Dev Biol 95:31–45 DOI
Legendre M, Cosson J, Hadi Alavi SM, Linhart O (2008) Activation of sperm motility in the euryhaline tilapia Sarotherodon melanotheron heudelotii (Dumeril, 1859) acclimatized to fresh, sea and hypersaline waters. French Ichthyological Society - Cybium. https://sfi-cybium.fr/en/node/854
Li YH, Eto K, Horikawa S et al (2009) Aquaporin-2 regulates cell volume recovery via tropomyosin. Int J Biochem Cell Biol 41:2466–2476. https://doi.org/10.1016/j.biocel.2009.07.017 PubMed DOI
Linhart O, Walford J, Sivaloganathan B, Lam TJ (1999) Effects of osmolality and ions on the motility of stripped and testicular sperm of freshwater- and seawater-acclimated tilapia, Oreochromis mossambicus. J Fish Biol 55:1344–1358. https://doi.org/10.1006/jfbi.1999.1133 DOI
Liu DY, Liu ML, Baker HWG (2013) Defective protein kinase A and C pathways are common causes of disordered zona pellucida (ZP)-induced acrosome reaction in normozoospermic infertile men with normal sperm-ZP binding. Fertil Steril 99:86–91. https://doi.org/10.1016/j.fertnstert.2012.08.040 PubMed DOI
Lodish H, Berk A, Kaiser CA, Krieger M (2004) Molecular cell biology. W H Free, New York, p 973
Lovett DL, Tanner CA, Glomski K et al (2006) The effect of seawater composition and osmolality on hemolymph levels of methyl farnesoate in the green crab Carcinus maenas. Comp Biochem Physiol A Mol Integr Physiol 143:67–77. https://doi.org/10.1016/j.cbpa.2005.10.025 PubMed DOI
Madsen SS, Engelund MB, Cutler CP (2015) Water transport and functional dynamics of aquaporins in osmoregulatory organs of fishes. Biol Bull 229:70–92. https://doi.org/10.1086/BBLv229n1p70 PubMed DOI
Morisawa M, Suzuki K (1980) Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts. Science 210:1145–1147 DOI
Morisawa M, Suzuki K, Shimizu H et al (1983) Effects of osmolality and potassium on motility of spermatozoa from freshwater cyprinid fishes. J Exp Biol 107:95–103 DOI
Morita M, Takemura A, Okuno M (2003) Requirement of Ca2+ on activation of sperm motility in euryhaline tilapia Oreochromis mossambicus. J Exp Biol 206:913–921 DOI
Morris J (2000) Asymptote cool guide to cryopreservation. Asymptote Ltd 44:1–42
Nozaki K, Ishii D, Ishibashi K (2008) Intracellular aquaporins: clues for intracellular water transport? Pflugers Arch Eur J Physiol 456:701–707. https://doi.org/10.1007/s00424-007-0373-5 DOI
Oda S, Morisawa M (1993) Rises of intracellular Ca2+ and pH mediate the initiation of sperm motility by hyperosmolality in marine teleosts. Cell Motil Cytoskeleton 25:171–178. https://doi.org/10.1002/cm.970250206 PubMed DOI
Ohta H, Ikeda K, Izawa T (1997) Increases in concentrations of potassium and bicarbonate ions promote acquisition of motility in vitro by Japanese eel spermatozoa. J Exp Zool 277. https://doi.org/10.1002/(SICI)1097-010X(19970201)277:2
Perchec Poupard G, Gatti JL, Cosson J, Fierville F (1997) Effects of extracellular environment on the osmotic signal transduction involved in activation of motility of carp spermatozoa. J Reprod Fertil 110:315–327 DOI
Petrunkina AM, Waberski D, Günzel-Apel AR, Töpfer-Petersen E (2007) Determinants of sperm quality and fertility in domestic species. Reproduction 134:3–17. https://doi.org/10.1530/REP-07-0046 PubMed DOI
Perez LM (2020) Fish sperm maturation, capacitation, and motility activation. In: Yoshida M, Asturiano JF (eds) Reproduction in aquatic animals: from basic biology to aquaculture technology (1st ed). Springer, Singapore, pp 47–67. https://doi.org/10.1007/978-981-15-2290-1
Prokopchuk G, Dzyuba B, Bondarenko O et al (2015) Motility initiation of sterlet sturgeon (Acipenser ruthenus) spermatozoa: describing the propagation of the first flagellar waves. Theriogenology 84:51–61. https://doi.org/10.1016/j.theriogenology.2015.02.011 PubMed DOI
Quinn PJ, Joo F, Vigh L (1989) The role of unsaturated lipids in membrane structure and stability. Prog Biophys Mol Biol 53:71–103. https://doi.org/10.1016/0079-6107(89)90015-1 PubMed DOI
Rana KJ, McAndrew BJ (1989) The viability of cryopreserved tilapia spermatozoa. Aquaculture 76:335–345. https://doi.org/10.1016/0044-8486(89)90085-9 DOI
Rurangwa E, Roelants I, Huyskens G et al (1998) The minimum effective spermatozoa:egg ratio for artificial insemination and the effects of mercury on sperm motility and fertilization ability in Clarias gariepinus. J Fish Biol 53:402–413. https://doi.org/10.1006/jfbi.1998.0711 DOI
Saito K, Kageyama Y, Okada Y et al (2004) Localization of aquaporin-7 in human testis and ejaculated sperm: possible involvement in maintenance of sperm quality. J Urol 172:2073–2076 DOI
Santymire RM, Marinari PE, Kreeger JS et al (2006) Sperm viability in the black-footed ferret (Mustela nigripes) is influenced by seminal and medium osmolality. Cryobiology 53:37–50. https://doi.org/10.1016/j.cryobiol.2006.03.009 PubMed DOI
Shaliutina A, Hulak M, Gazo I et al (2013) Effect of short-term storage on quality parameters, DNA integrity, and oxidative stress in Russian (Acipenser gueldenstaedtii) and Siberian (Acipenser baerii) sturgeon sperm. Anim Reprod Sci 139:127–135. https://doi.org/10.1016/j.anireprosci.2013.03.006 PubMed DOI
Shaliutina-Kolešová A, Gazo I, Cosson J, Llnhart O (2013) Comparison of oxidant and antioxidant status of seminal plasma and spermatozoa of several fish species. Czech J Anim Sci 58:313–320 DOI
Shim AL, Kamkin AG, Kamkina OV et al (2019) Gadolinium as an inhibitor of ionic currents in isolated rat ventricular cardiomyocytes. Bull Exp Biol Med 168:187–192. https://doi.org/10.1007/s10517-019-04672-0 PubMed DOI
Sohara E, Ueda O, Tachibe T et al (2007) Morphologic and functional analysis of sperm and testes in aquaporin 7 knockout mice. Fertil Steril 87:671–676. https://doi.org/10.1016/J.FERTNSTERT.2006.07.1522 PubMed DOI
Stubbs CD, Smith AD (1984) The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta Rev Biomembr 779:89–137. https://doi.org/10.1016/0304-4157(84)90005-4 DOI
Takei GL, Mukai C, Okuno M (2015) Regulation of salmonid fish sperm motility by osmotic shock-induced water influx across the plasma membrane. Comp Biochem Physiol A Mol Integr Physiol 182:84–92. https://doi.org/10.1016/j.cbpa.2014.12.013 PubMed DOI
Tanaka S, Utoh T, Yamada Y et al (2004) Role of sodium bicarbonate on the initiation of sperm motility in the Japanese eel. Fish Sci 70:780–787. https://doi.org/10.1111/j.1444-2906.2004.00871.x DOI
Tingaud-Sequeira A, Calusinska M, Finn RN, Chauvigné F, Lozano J, Cerdà J (2010) The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals. BMC Evol Biol 10(1). https://doi.org/10.1186/1471-2148-10-38
Trigo P, Merino O, Figueroa E et al (2015) Effect of short-term semen storage in salmon (Oncorhynchus mykiss) on sperm functional parameters evaluated by flow cytometry. Andrologia 47:407–411. https://doi.org/10.1111/and.12276 PubMed DOI
Verkman AS, Shi LB, Frigeri A et al (1995) Structure and function of kidney water channels. Kidney Int 48:1069–1081 DOI
Vílchez MC, Morini M, Peñaranda DS et al (2016) Sodium affects the sperm motility in the European eel. Comp Biochem Physiol A Mol Integr Physiol 198:51–58. https://doi.org/10.1016/j.cbpa.2016.04.008 PubMed DOI
Vílchez MC, Morini M, Peñaranda DS et al (2017) Role of potassium and pH on the initiation of sperm motility in the European eel. Comp Biochem Physiol A Mol Integr Physiol 203:210–219. https://doi.org/10.1016/j.cbpa.2016.09.024 PubMed DOI
Yeste M, Morató R, Rodríguez-Gil JE et al (2017) Aquaporins in the male reproductive tract and sperm: functional implications and cryobiology. Reprod Domest Anim 52:12–27 DOI
Yeung CH, Anapolski M, Depenbusch M et al (2003) Human sperm volume regulation. Response to physiological changes in osmolality, channel blockers and potential sperm osmolytes. Hum Reprod 18:1029–1036. https://doi.org/10.1093/humrep/deg204 PubMed DOI
Yeung CH, Barfield JP, Cooper TG (2006) Physiological volume regulation by spermatozoa. Mol Cell Endocrinol 250:98–105. https://doi.org/10.1016/j.mce.2005.12.030 PubMed DOI
Yeung CH, Callies C, Tüttelmann F et al (2010) Aquaporins in the human testis and spermatozoa-identification, involvement in sperm volume regulation and clinical relevance. Int J Androl 33:629–641. https://doi.org/10.1111/j.1365-2605.2009.00998.x PubMed DOI
Zilli L, Schiavone R, Storelli C, Vilella S (2008) Molecular mechanisms determining sperm motility initiation in two sparids (Sparus aurata and Lithognathus mormyrus). Biol Reprod 79:356–366. https://doi.org/10.1095/biolreprod.108.068296 PubMed DOI
Zilli L, Schiavone R, Chauvigné F et al (2009) Evidence for the involvement of aquaporins in sperm motility activation of the teleost gilthead sea bream (Sparus aurata)1. Biol Reprod. https://doi.org/10.1095/biolreprod.109.077933 PubMed DOI
Zilli L, Beirão J, Schiavone R et al (2011) Aquaporin inhibition changes protein phosphorylation pattern following sperm motility activation in fish. Theriogenology 76:737–744. https://doi.org/10.1016/j.theriogenology.2011.04.006 PubMed DOI