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The Physiological Role and Regulation of Aquaporins in Teleost Germ Cells

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Aquaporins

Abstract

The unicellular germ cells and gametes of oviparous teleosts lack the osmoregulatory organs present in juveniles and adults, yet during development and particularly at spawning, they face tremendous osmotic challenges when released into the external aquatic environment. Increasing evidence suggests that transmembrane water channels (aquaporins) evolved to play vital adaptive roles that mitigate the osmotic and oxidative stress problems of the developing oocytes , embryos and spermatozoa. In this chapter, we provide a short overview of the diversity of the aquaporin superfamily in teleosts, and summarize the findings that uncovered a highly specific molecular regulation of aquaporins during oogenesis and spermatogenesis. We further review the multiple functions that these channels play during the establishment of egg buoyancy and the activation and detoxification of spermatozoa in the marine environment.

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Abbreviations

AQP /Aqp:

aquaporin

CNGK:

cyclic nucleotide-gated K+ channel

FAA:

free amino acid

IgG:

immunoglobulin

LvH:

lipovitellin heavy chain

LvL:

lipovitellin light chain

MAPK:

mitogen activated protein kinase

PKA:

protein kinase A

ROS:

reactive oxygen species

SAC:

stretch-activated channel

Sox:

Sry-related high mobility group [HMG]-box

TEA:

tetraethylammonium

TRPV:

transient receptor potential cation channel subfamily V

Vtg:

vitellogenin

References

  1. Marshall WS, Grosell M (2006) Ion transport, osmoregulation and acid-base balance. In: Evans DH, Claiborne JB (eds) The physiology of fishes, 3rd edn. CRC Press, BocaRaton, pp 177–230

    Google Scholar 

  2. Cerdà J, Finn RN (2010) Piscine aquaporins: an overview of recent advances. J Exp Zool A Ecol Genet Physiol 313:623–650

    Article  PubMed  CAS  Google Scholar 

  3. Madsen SS, Engelund MB, Cutler CP (2015) Water transport and functional dynamics of aquaporins in osmoregulatory organs of fishes. Biol Bull 229:70–92

    Article  CAS  PubMed  Google Scholar 

  4. 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 10:38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Finn RN, Cerdà J (2011) Aquaporin evolution in fishes. Front Physiol 2:44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Engelund MB, Chauvigné F, Chrstensen BM, Finn RN, Cerdà J, Madsen SS (2013) Differential expression and novel permeability properties of three aquaporin 8 paralogs from seawater-challenged Atlantic salmon smolts. J Exp Biol 216:3873–3885

    Article  CAS  PubMed  Google Scholar 

  7. Finn RN, Chauvigné F, Hlidberg JB, Cutler CP, Cerdà J (2014) The lineage-specific evolution of aquaporin gene clusters facilitated tetrapod terrestrial adaptation. PLoS One 9:e113686

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Stavang JA, Chauvigné F, Kongshaug H, Cerdà J, Nilsen F, Finn RN (2015) Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda. BMC Genomics 16:618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Finn RN, Cerdà J (2015) Evolution and functional diversity of aquaporins. Biol Bull 229:6–23

    Article  CAS  PubMed  Google Scholar 

  10. Xu P, Zhang X, Wang X, Li J, Liu G, Kuang Y et al (2014) Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet 46:1212–1219

    Article  CAS  PubMed  Google Scholar 

  11. Tine M, Kuhl H, Gagnaire PA, Louro B, Desmarais E, Martins RST et al (2014) European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nat Commun 10:1038

    Google Scholar 

  12. Zapater C, Chauvigné F, Norberg B, Finn RN, Cerdà J (2011) Dual neofunctionalization of a rapidly evolving aquaporin-1 paralog resulted in constrained and relaxed traits controlling channel function during meiosis resumption in teleosts. Mol Biol Evol 28:3151–3169

    Article  CAS  PubMed  Google Scholar 

  13. Froger A, Clemens D, Kalman K, Németh-Cahalan KL, Schilling TF, Hall JE (2010) Two distinct aquaporin 0s required for development and transparency of the zebraish lens. Invest Ophthalmol Vis Sci 51:6582–6592

    Article  PubMed  PubMed Central  Google Scholar 

  14. Clemens DM, Németh-Cahalan KL, Trinh L, Zhang T, Schilling TF, Hall JE (2013) In vivo analysis of aquaporin 0 function in zebraish: permeability regulation is required for lens transparency. Invest Ophthalmol Vis Sci 54:5136–5143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Hall JE, Mathias RT (2014) The aquaporin zero puzzle. Biophys Rev 107:10–15

    CAS  Google Scholar 

  16. Chauvigné F, Zapater C, Stavang JA, Taranger GL, Cerdà J, Finn RN (2015) The pH sensitivity of Aqp0 channels in tetraploid and diploid teleosts. FASEB J 29:2172–2184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Chauvigné F, Fjelldal OG, Cerdà J, Finn RN (2016) Auto-adhesion potential of extraocular Aqp0 during teleost development. PLoS One 11(5):e0154592

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Amores A, Force A, Yan YL, Joly L, Amemiya C (1998) Zebrash hox clusters and vertebrate genome evolution. Science 282:1711–1714

    Article  CAS  PubMed  Google Scholar 

  19. Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH (2011) Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188:799–808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. McLysaght A, Hokamp K, Wolfe KH (2002) Extensive genomic duplication during early chordate evolution. Nat Genet 31:200–204

    Article  CAS  PubMed  Google Scholar 

  21. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N et al (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957

    Article  PubMed  Google Scholar 

  22. Vandepoele K, De Vos W, Taylor JS, Meyer A, Van der Peer Y (2004) Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci U S A 101:1638–1643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3(10):e314

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Finn RN, Kristoffersen BA (2007) Vertebrate vitellogenin gene duplication in relation to the “3R hypothesis”: correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS One 2:e169

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Braasch I, Gehrke AR, Smith JJ, Kawasaki K, Manousaki T et al (2016) The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat Genet 48:427–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  CAS  PubMed  Google Scholar 

  27. Wolfe KH (2001) Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet 2:333–341

    Article  CAS  PubMed  Google Scholar 

  28. Furlong RF, Holland PWH (2002) Were vertebrates octoploid? Philos Trans R Soc Lond B Biol Sci 357:531–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lien S, Koop BF, Sandve SR, Miller JR, Kent MP, Nome T et al (2016) The Atlantic salmon genome provides insights into rediploidization. Nature 533:200–205

    Article  CAS  PubMed  Google Scholar 

  30. Braasch I, Postlethwait JH (2012) Polyploidy in fish and the teleost genome duplication. Chapter 17. In: Soltis PS, Soltis DE (eds) Polyploidy and genome evolution. Springer, Berlin, pp 341–383

    Chapter  Google Scholar 

  31. Deen PM, Verdijk MA, Knoers NV, Wieringa B, Monnens LA, van Os CH, van Oost BA (1994) Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 264:92–95

    Article  CAS  PubMed  Google Scholar 

  32. Müller C, Sendler M, Hildebrandt JP (2006) Downregulation of aquaporins 1 and 5 in nasal gland by osmotic stress in ducklings, Anas platyrhynchos: implications for the production of hypertonic fluid. J Exp Biol 209:4067–4076

    Article  PubMed  CAS  Google Scholar 

  33. Nishimura H (2008) Urine concentration and avian aquaporin water channels. Eur J Physiol 456:755–768

    Article  CAS  Google Scholar 

  34. Lau KK, Yang Y, Cook GA, Wyatt RJ, Nishimura H (2009) Control of aquaporin 2 expression in collecting ducts of quail kidneys. Gen Comp Endocrinol 160:288–294

    Article  CAS  PubMed  Google Scholar 

  35. Suzuki M, Shibata Y, Ogushi Y, Okada R (2015) Molecular machinery for vasotocin-dependent transepithelial water movement in amphibians: aquaporins and evolution. Biol Bull 229:109–119

    Article  CAS  PubMed  Google Scholar 

  36. Fyhn HJ, Finn RN, Reith M, Norberg B (1999) Yolk protein hydrolysis and oocyte free amino acids as key features in the adaptative evolution of teleost fishes to sea water. Sarsia 84:451–456

    Article  Google Scholar 

  37. Cerdà J, Fabra M, Raldúa D (2007) Physiological and molecular basis of fish oocyte hydration. In: Babin P, Cerdà J, Lubzens E (eds) The fish oocyte: from basic studies to biotechnological applications. Springer, Dordrecht, pp 349–396

    Chapter  Google Scholar 

  38. Podrabsky J, Tingaud-Sequeira A, Cerdà J (2010) Metabolic dormancy and responses to environmental desiccation in fish embryos. In: Lubzens E, Cerdà J, Clark M (eds) Dormancy and resistance in harsh environments, topics in current genetics, vol 21. Springer, Berlin, pp 203–226

    Chapter  Google Scholar 

  39. Craik JCA, Harvey SM (1987) The causes of buoyancy in eggs of marine teleosts. J Mar Biol Ass UK 67:169–182

    Article  Google Scholar 

  40. Finn RN, Fyhn HJ (2010) Requirement for aminoacids in ontogeny of fish. Aquac Res 41:684–716

    Article  CAS  Google Scholar 

  41. Babin PJ, Carnevali O, Lubzens E, Schneider WJ (2007) Molecular aspects of oocyte vitellogenesis in fish. In: Babin PJ, Cerdà J, Lubzens E (eds) The fish oocyte: from basic studies to biotechnological applications. Springer, Dordrecht, pp 39–76

    Chapter  Google Scholar 

  42. Finn RN (2007) Vertebrate yolk complexes and the functional implications of phosvitins and other subdomains in vitellogenins. Biol Reprod 76:926–935

    Article  CAS  PubMed  Google Scholar 

  43. Hiramatsu N, Todo T, Sullivan CV, Schilling J, Reading BJ, Matsubara T et al (2015) Ovarian yolk formation in fishes: Molecular mechanisms underlying formation of lipid droplets and vitellogenin-derived yolk proteins. Gen Comp Endocrinol 221:9–15

    Article  CAS  PubMed  Google Scholar 

  44. Hara A, Hiramatsu N, Fujita T (2016) Vitellogenesis and choriogenesis in fishes. Fish Sci 82:187–202

    Article  CAS  Google Scholar 

  45. Matsubara T, Nagae M, Ohkubo N, Andoh T, Sawaguchi S, Hiramatsu N, Sullivan CV, Hara A (2003) Multiple vitellogenins and their unique roles in marine teleosts. Fish Physiol Biochem 28:295–299

    Article  CAS  Google Scholar 

  46. Finn RN (2007) The maturational disassembly and differential proteolysis of paralogous vitellogenins in a marine pelagophil teleost: a conserved mechanism of oocyte hydration. Biol Reprod 76:936–948

    Article  CAS  PubMed  Google Scholar 

  47. Kristofersen BA, Nerland A, Nilsen F, Kolarevic J, Finn RN (2009) Genomic and proteomic analyses reveal nonneofunctionalized vitellogenins in a basal clupeocephalan, the Atlantic herring, and point to the origin of maturational yolk proteolysis in marine teleosts. Mol Biol Evol 26:1029–1044

    Article  CAS  Google Scholar 

  48. Matsubara T, Ohkubo N, Andoh T, Sullivan CV, Hara A (1999) Two forms of vitellogenin, yielding two distinct lipovitellins, play different roles during oocyte maturation and early development of barfin flounder, Verasper moseri, a marine teleost that spawns pelagic eggs. Dev Biol 213:18–32

    Article  CAS  PubMed  Google Scholar 

  49. LaFleur GJ Jr, Raldúa D, Fabra M, Carnevali O, Denslow N, Wallace RA, Cerdà J (2005) Derivation of major yolk proteins from parental vitellogenins and alternative processing during oocyte maturation in Fundulus heteroclitus. Biol Reprod 73:815–824

    Article  CAS  PubMed  Google Scholar 

  50. Sawaguchi S, Kagawa H, Ohkubo N, Hiramatsu N, Sullivan CV, Matsubara T (2006) Molecular characterization of three forms of vitellogenin and their yolk protein products during oocyte growth and maturation in red seabream (Pagrus major), a marine teleost spawning pelagic eggs. Mol Reprod Dev 73:719–736

    Article  CAS  PubMed  Google Scholar 

  51. Amano H, Fujita T, Hiramatsu N, Kagawa H, Matsubara T, Sullivan CV, Hara A (2008) Multiple vitellogenin-derived yolk proteins in gray mullet (Mugil cephalus): Disparate proteolytic patterns associated with ovarian follicle maturation. Mol Reprod Dev 75:1307–1317

    Article  CAS  PubMed  Google Scholar 

  52. Kolarevic J, Nerland A, Nilsen F, Finn RN (2008) Goldsinny wrasse (Ctenolabrus rupestris) is an extreme vtgAa-type pelagophil teleost. Mol Reprod Dev 75:1011–1020

    Article  CAS  PubMed  Google Scholar 

  53. Williams VN, Reading BJ, Hiramatsu N, Amano H, Glassbrook N, Hara A, Sullivan CV (2014) Multiple vitellogenins and product yolk proteins in striped bass, Morone saxatilis: molecular characterization and processing during oocyte growth and maturation. Fish Physiol Biochem 40:395–415

    Article  CAS  PubMed  Google Scholar 

  54. Yilmaz O, Prat F, Ibáñez AJ, Köksoy S, Amano H, Sullivan CV (2016) Multiple vitellogenins and product yolk proteins in European sea bass (Dicentrarchus labrax): molecular characterization, quantification in plasma, liver and ovary, and maturational proteolysis. Comp Biochem Physiol 194–195:71–86

    Article  CAS  Google Scholar 

  55. Finn RN, Wamboldt M, Fyhn HJ (2002) Differential processing of yolk proteins during hydration in marine fishes (Labridae) that spawn benthic and pelagic eggs. Mar Ecol Prog Ser 237:217–226

    Article  CAS  Google Scholar 

  56. Sawaguchi S, Ohkubo N, Matsubara T (2006) Identification of two forms of vitellogenin-derived phosvitin and elucidation of their fate and roles during oocyte maturation in the barfin flounder, Verasper moseri. Zool Sci 23:1021–1029

    Article  CAS  PubMed  Google Scholar 

  57. Kristoffersen BA, Finn RN (2008) Major osmolyte changes during oocyte hydration of a clupeocephalan marine benthophil: Atlantic herring (Clupea harengus). Mar Biol 154:683–692

    Article  CAS  Google Scholar 

  58. Fabra M, Raldúa D, Power DM, Deen PM, Cerdà J (2005) Marine fish egg hydration is aquaporin-mediated. Science 307:545

    Article  CAS  PubMed  Google Scholar 

  59. Fabra M, Raldúa D, Bozzo MG, Deen PM, Lubzens E, Cerdà J (2006) Yolk proteolysis and aquaporin-1o play essential roles to regulate fish oocyte hydration during meiosis resumption. Dev Biol 295:250–262

    Article  CAS  PubMed  Google Scholar 

  60. Kagawa H, Kishi T, Gen K, Kazeto Y, Tosaka R, Matsubara H, Matsubara T, Sawaguchi S (2011) Expression and localization of aquaporin 1b during oocyte development in the Japanese eel (Anguilla japonica). Reprod Biol Endocrinol 9:71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Zapater C, Chauvigné F, Tingaud-Sequeira A, Finn RN, Cerdà J (2013) Primary oocyte transcriptional activation of aqp1ab by the nuclear progestin receptor determines the pelagic egg phenotype of marine teleosts. Dev Biol 377:345–362

    Article  CAS  PubMed  Google Scholar 

  62. Finn RN, Ostby GC, Norberg B, Fyhn HJ (2002) In vivo oocyte hydration in Atlantic halibut (Hippoglossus hipoglossus): proteolytic liberation of free amino acids, and ion transport, are driving forces for osmotic water influx. J Exp Biol 205:211–224

    CAS  PubMed  Google Scholar 

  63. Tingaud-Sequeira A, Chauvigné F, Fabra M, Lozano J, Raldúa D, Cerdà J (2008) Structural and functional divergence of two fish aquaporin-1 water channels following teleost-specific gene duplication. BMC Evol Biol 8:259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Kagawa H, Horiuchi Y, Kasuga Y, Kishi T (2009) Oocyte hydration in the Japanese eel (Anguilla japonica) during meiosis resumption and ovulation. J Exp Zool A Ecol Genet Physiol 311:752–762

    Article  PubMed  Google Scholar 

  65. Brooks HL, Regan JW, Yool AJ (2000) Inhibition of aquaporin-1 water permeability by tetraethylammonium: involvement of the loop E pore region. Mol Pharmacol 57:1021–1026

    CAS  PubMed  Google Scholar 

  66. Singh V, Joy KP (2010) An involvement of vasotocin in oocyte hydration in the catfish Heteropneustes fossilis: a comparison with effects of isotocin and hCG. Gen Comp Endocrinol 166:504–512

    Article  CAS  PubMed  Google Scholar 

  67. Chaube R, Chauvigné F, Tingaud-Sequeira A, Joy KP, Acharjee A, Singh V, Cerdà J (2011) Molecular and functional characterization of catfish (Heteropneustes fossilis) aquaporin-1b: changes in expression during ovarian development and hormone-induced follicular maturation. Gen Comp Endocrinol 170:162–171

    Article  CAS  PubMed  Google Scholar 

  68. Greeley MS Jr, Hols H, Wallace RA (1991) Changes in size, hydra- tion and low molecular weight osmotic effectors during meiotic maturation of Fundulus oocytes in vivo. Comp Biochem Physiol 100A:639–647

    Article  CAS  Google Scholar 

  69. Milla S, Jalabert B, Rime H, Prunet P, Bobe J (2006) Hydration of rainbow trout oocyte during meiotic maturation and in vitro regulation by 17,20β-dihydroxy-4-pregnen-3-one and cortisol. J Exp Biol 209:1147–1156

    Article  CAS  PubMed  Google Scholar 

  70. Bobe J, Montfort J, Nguyen T, Fostier A (2006) Identification of new participants in the rainbow trout (Oncorhynchus mykiss) oocyte maturation and ovulation processes using cDNA microarrays. Reprod Biol Endocrinol 4:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Balment RJ, Lu W, Weybourne E, Warne JM (2006) Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. Gen Comp Endocrinol 147:9–16

    Article  CAS  PubMed  Google Scholar 

  72. Boone M, Deen PM (2008) Physiology and pathophysiology of the vasopressin-regulated renal water reabsorption. Eur J Physiol 456:1005–1024

    Article  CAS  Google Scholar 

  73. Moeller HB, Fenton RA, Zeuthen T, Macaulay N (2009) Vasopressin-dependent short-term regulation of aquaporin 4 expressed in Xenopus oocytes. Neuroscience 164:1674–1684

    Article  CAS  PubMed  Google Scholar 

  74. Zapater C, Chauvigné F, Scott AP, Gómez A, Katsiadaki I, Cerdà J (2012) Piscine follicle-stimulating hormone triggers progestin production in gilthead seabream primary ovarian follicles. Biol Reprod 87:111

    Article  PubMed  CAS  Google Scholar 

  75. Harwood BN, Cross SK, Radford EE, Haac BE, De Vries WN (2008) Members of the WNT signaling pathways are widely expressed in mouse ovaries, oocytes, and cleavage stage embryos. Dev Dyn 237:1099–1111

    Article  CAS  PubMed  Google Scholar 

  76. Paul D, Bridoux L, Rezsöhazy R, Donnay I (2011) HOX genes are expressed in bovine and mouse oocytes and early embryos. Mol Reprod Dev 78:436–449

    Article  CAS  PubMed  Google Scholar 

  77. Senthilkumaran B, Sreenivasulu G, Wang DS, Sudhakumari CC, Kobayashi T, Nagahama Y (2015) Expression patterns of CREBs in oocyte growth and maturation of fish. PLoS One 10:e0145182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Zapater C, Chauvigné F, Fernández-Gómez B, Finn RN, Cerdà J (2013) Alternative splicing of the nuclear progestin receptor in a perciform teleost generates novel mechanisms of dominant-negative transcriptional regulation. Gen Comp Endocrinol 182:24–40

    Article  CAS  PubMed  Google Scholar 

  79. Cerdà J, Zapater C, Chauvigné F, Finn RN (2013) Water homeostasis in the fish oocyte: new insights into the role and molecular regulation of a teleost-specific aquaporin. Fish Physiol Biochem 39:19–27

    Article  PubMed  CAS  Google Scholar 

  80. Perdiguero E, Nebreda AR (2004) Use of Xenopus oocytes and early embryos to study MAPK signaling. Methods Mol Biol 250:299–314

    CAS  PubMed  Google Scholar 

  81. Wilson JL, Miranda CA, Knepper MA (2013) Vasopressin and the regulation of aquaporin-2. Clin Exp Nephrol 17:751–764

    Article  CAS  PubMed  Google Scholar 

  82. Joy KP, Chaube R (2015) Vasotocin-A new player in the control of oocyte maturation and ovulation in fish. Gen Comp Endocrinol 221:54–63

    Article  CAS  PubMed  Google Scholar 

  83. Morisawa M, Suzuki K (1980) Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts. Science 210:1145–1147

    Article  CAS  PubMed  Google Scholar 

  84. Morisawa M, Suzuki K, Morisawa S (1983) Effects of potassium and osmolality on spermatozoan motility of salmonid fishes. J Exp Biol 107:105–113

    CAS  PubMed  Google Scholar 

  85. Cosson MP, Billard R, Letellier L (1989) Rise of internal Ca2+ accompanies the initiation of trout sperm motility. Cell Motil Cytoskeleton 14:3424–3434

    Article  Google Scholar 

  86. Tanimoto S, Kudo Y, Nakazawa T, Morisawa M (1994) Implication that potassium flux and increase in intracellular calcium are necessary for the initiation of sperm motility in salmonid fishes. Mol Reprod Dev 39:409–414

    Article  CAS  PubMed  Google Scholar 

  87. Hayashi H, Yamamoto K, Yonekawa H, Morisawa M (1987) Involvement of tyrosine protein kinase in the initiation of flagellar movement in rainbow trout spermatozoa. J Biol Chem 262:16692–16698

    CAS  PubMed  Google Scholar 

  88. Inaba K, Kagami O, Ogawa K (1999) Tctex2-related outer arm dynein light chain is phosphorylated at activation of sperm motility. Biochem Biophys Res Commun 256:177–183

    Article  CAS  PubMed  Google Scholar 

  89. Dzyuba V, Cosson J (2014) Motility of fish spermatozoa: from external signaling to flagella response. Reprod Biol 14:165–175

    Article  PubMed  Google Scholar 

  90. Fechner S, Alvarez L, Bönigk W, Müller A, Berger TK, Pascal R et al (2015) A K(+)-selective CNG channel orchestrates Ca(2+) signaling in zebrafish sperm. eLife 9:4

    Google Scholar 

  91. Majhi RK, Kumar A, Yadav M, Swain N, Kumari S, Saha A et al (2013) Thermosensitive ion channel TRPV1 is endogenously expressed in the sperm of a fresh water teleost fish (Labeo rohita) and regulates sperm motility. Channels (Austin) 7:483–492

    Article  CAS  Google Scholar 

  92. Zilli L, Schiavone R, Storelli C, Vilella S (2012) Molecular mechanism regulating axoneme activation in marine fish: a review. Int Aquat Res 4:2

    Article  Google Scholar 

  93. Pérez L, Vílchez MC, Gallego V, Morini M, Peñaranda DS, Asturiano JF (2016) Role of calcium on the initiation of sperm motility in the European eel. Comp Biochem Physiol A Mol Integr Physiol 191:98–106

    Article  PubMed  CAS  Google Scholar 

  94. Vines CA, Yoshida K, Griffin FJ, Pillai MC, Morisawa M, Yanagimachi R, Cherr GN (2002) Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange. Proc Natl Acad Sci U S A 99:2026–2031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Cosson J, Groison AL, Suquet M, Fauvel C, Dreanno C, Billard R (2008) Marine fish spermatozoa: racing ephemeral swimmers. Reproduction 136:277–294

    Article  CAS  PubMed  Google Scholar 

  96. Cosson J, Billard R, Cibert C, Dreanno C, Suquet M (1999) Regulation of axonemal wave parameters of fish spermatozoa by ionic factors. In: Gagnon C (ed) The male gamete: from basic knowledge to clinical applications. Cache River Press, Vienna, pp 161–186

    Google Scholar 

  97. Zilli L, Schiavone R, Chauvigné F, Cerdà J, Storelli C, Vilella S (2009) Evidence for the involvement of aquaporins in sperm motility activation of the teleost gilthead sea bream (Sparus aurata). Biol Reprod 81:880–888

    Article  CAS  PubMed  Google Scholar 

  98. Chauvigné F, Boj M, Vilella S, Finn RN, Cerdà J (2013) Subcellular localization of selectively permeable aquaporins in the male germ line of a marine teleost reveals spatial redistribution in activated spermatozoa. Biol Reprod 89:37

    Article  PubMed  CAS  Google Scholar 

  99. Boj M, Chauvigné F, Cerdà J (2015) Aquaporin biology of spermatogenesis and sperm physiology in mammals and teleosts. Biol Bull 229:93–108

    Article  CAS  PubMed  Google Scholar 

  100. 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

    Article  CAS  PubMed  Google Scholar 

  101. Labbe C, Maisse G (2001) Characteristics and freezing tolerance of brown trout spermatozoa according to rearing water salinity. Aquaculture 201:287–299

    Article  Google Scholar 

  102. Boj M, Chauvigné F, Zapater C, Cerdà J (2015) Gonadotropin-activated androgen-dependent and independent pathways regulate aquaporin expression during teleost (Sparus aurata) spermatogenesis. PLoS One 10:e0142512

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Chauvigné F, Boj M, Finn RN, Cerdà J (2015) Mitochondrial aquaporin-8-mediated hydrogen peroxide transport is essential for teleost spermatozoon motility. Sci Rep 14:7789

    Article  CAS  Google Scholar 

  104. Boj M, Chauvigné F, Cerdà J (2015) Coordinated action of aquaporins regulates sperm motility in a marine teleost. Biol Reprod 93(2):40

    Article  PubMed  CAS  Google Scholar 

  105. Santos CR, Estêvaõ MD, Fuentes J, Cardoso JC, Fabra M, Passos AL et al (2004) Isolation of a novel aquaglyceroporin from a marine teleost (Sparus auratus): function and tissue distribution. J Exp Biol 207:1217–1227

    Article  CAS  PubMed  Google Scholar 

  106. 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

    Article  CAS  PubMed  Google Scholar 

  107. Bienert GP, Chaumont F (1840) Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta 2014:1596–1604

    Google Scholar 

  108. Almasalmeh A, Krenc D, Wu B, Beitz E (2014) Structural determinants of the hydrogen peroxide permeability of aquaporins. FEBS J 281:647–656

    Article  CAS  PubMed  Google Scholar 

  109. Collins Y, Chouchani ET, James AM, Menger KE, Cochemé HM, Murphy MP (2012) Mitochondrial redox signalling at a glance. J Cell Sci 125:801–806

    Article  CAS  PubMed  Google Scholar 

  110. McCarthy MJ, Baumber J, Kass PH, Meyers SA (2010) Osmotic stress induces oxidative cell damage to rhesus macaque spermatozoa. Biol Reprod 82:644–651

    Article  CAS  PubMed  Google Scholar 

  111. Zilli L, Beiraõ J, Schiavone R, Herraez MP, Cabrita E, Storelli C, Vilella S (2011) Aquaporin inhibition changes protein phosphorylation pattern following sperm motility activation in fish. Theriogenology 76:737–744

    Article  CAS  PubMed  Google Scholar 

  112. Chen Q, Peng H, Lei L, Zhang Y, Kuang H, Cao Y, Shi QX, Ma T, Duan E (2011) Aquaporin 3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration. Cell Res 21:922–933

    Article  CAS  PubMed  Google Scholar 

  113. Yeung CH, Callies C, Rojek A, Nielsen S, Cooper TG (2009) Aquaporin isoforms involved in physiological volume regulation of murine spermatozoa. Biol Reprod 80:350–357

    Article  CAS  PubMed  Google Scholar 

  114. Chen Q, Duan EK (2011) Aquaporins in sperm osmoadaptation: an emerging role for volume regulation. Acta Pharmacol Sin 32:721–724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Liu X, Bandyopadhyay BC, Nakamoto T, Singh B, Liedtke W, Melvin JE et al (2006) 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 281:15485–15495

    Article  CAS  PubMed  Google Scholar 

  116. Benfenati V, Caprini M, Dovizio M, Mylonakou MN, Ferroni S, Ottersen OP et al (2011) An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proc Natl Acad Sci U S A 108:2563–2568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Noda Y, Sasaki S (1758) Regulation of aquaporin-2 trafficking and its binding protein complex. Biochim Biophys Acta 2006:1117–1125

    Google Scholar 

  118. Maccarrone M, Barboni B, Paradisi A, Bernabo N, Gasperi V, Pistilli MG et al (2005) Characterization of the endocannabinoid system in boar spermatozoa and implications for sperm capacitation and acrosome reaction. J Cell Sci 118:4393–4404

    Article  CAS  PubMed  Google Scholar 

  119. Botto L, Bernabo N, Palestini P, Barboni B (2010) Bicarbonate induces membrane reorganization and CBR1 and TRPV1 endocannabinoid receptor migration in lipid microdomains in capacitating boar spermatozoa. J Membr Biol 238:33–41

    Article  CAS  PubMed  Google Scholar 

  120. Maricchiolo G, Genovese L, Laurà R, Micale V, Muglia U (2007) Fine structure of spermatozoa in the gilthead sea bream (Sparus aurata Linnaeus, 1758) (Perciformes, Sparidae). Histol Histopathol 22:79–83

    CAS  PubMed  Google Scholar 

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Acknowledgements

Research in the author’s laboratories is supported by grants from the Spanish Ministry of Economy and Competitivity (AGL2004-00316, AGL2007-60262, AGL2010-15597 and AGL2013-41196-R), Generalitat de Catalunya (2009 SGR 01050 and 2014 SGR 1351), and the Research Council of Norway (204813/F20, 224816/E40 and 254872/E40).

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Correspondence to Joan Cerdà Ph.D. .

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Cerdà, J., Chauvigné, F., Finn, R.N. (2017). The Physiological Role and Regulation of Aquaporins in Teleost Germ Cells. In: Yang, B. (eds) Aquaporins. Advances in Experimental Medicine and Biology, vol 969. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-1057-0_10

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