Abstract
The discovery of the role of a teleost-specific aquaporin (Aqp1ab) during the process of oocyte hydration in marine fish producing pelagic (floating) eggs, recently confirmed by molecular approaches, has revealed that this mechanism is more sophisticated than initially thought. Recent phylogenetic and genomic studies suggest that Aqp1ab likely evolved by tandem duplication from a common ancestor and further neofunctionalized in oocytes for water transport. Investigations into the regulation of Aqp1ab during oogenesis indicate that the mRNA and protein product are highly accumulated during early oocyte growth, possibly through the transcriptional activation of the aqp1ab promoter by the classical nuclear progesterone receptor and perhaps by Sry-related high mobility group [HMG]-box (Sox) transcription factors. During oocyte growth and maturation, Aqp1ab intracellular trafficking may be regulated by phosphorylation and/or dephosphorylation of specific C-terminal residues in Aqp1ab, as well as by signal-mediated sorting processes. These mechanisms possibly regulate the temporal insertion of Aqp1ab into the oocyte plasma membrane during oocyte hydration, although the intracellular signaling pathways involved are yet unknown. Interestingly, in some freshwater species that spawn partially hydrated eggs, high accumulation of transcripts encoding functional Aqp1ab channels have also been found in the ovary. These findings suggest that the Aqp1ab-mediated mechanism for oocyte hydration is likely conserved in teleosts. The tight regulation of Aqp1ab during oogenesis, at both the transcriptional and posttranslational levels, highlights the essential physiological role of this water channel and opens new research avenues for understanding the molecular basis of egg formation in fish.
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References
Allendorf FW, Thorgaard G (1984) Tetraploidy and the evolution of salmonid fishes. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum Press, New York, pp 1–45
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
Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Ann Rev Biochem 72:395–447
Cerdà J (2009) Molecular pathways during marine fish egg hydration: the role of aquaporins. J Fish Biol 75:2175–2196
Cerdà J, Finn RN (2010) Piscine aquaporins: an overview of recent advances. J Exp Zool 313A:623–650
Cerdà J, Fabra M, Raldúa D (2007) Physiological and molecular basis of fish oocyte hydration. In: Babin PJ, Cerdà J, Lubzens E (eds) The fish oocyte: from basic studies to biotechnological applications. Springer, Dordrecht, pp 349–396
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
Eppig JJ, Viveiros MM, Marin-Bivens C, de La Fuente R (2004) Regulation of mammalian oocyte maturation. In: Leung PCK, Adashi EY (eds) The Ovary, 2nd edn. Elsevier/Academic Press, San Diego, pp 113–129
Fabra M, Raldúa D, Power DM, Deen PM, Cerdà J (2005) Marine fish egg hydration is aquaporin-mediated. Science 307:545
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
Finn RN (2007a) 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
Finn RN (2007b) Vertebrate yolk complexes and the functional implications of phosvitins and other subdomains in vitellogenins. Biol Reprod 76:926–935
Finn RN, Cerdà J (2011) Aquaporin evolution in fishes. Front Physio 2:44
Finn RN, Fyhn HJ (2010) Requirement for amino acids in ontogeny of fish. Aquacult Res 41:684–716
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
Finn RN, Østby GC, Norberg B, Fyhn HJ (2002) In vivo oocyte hydration in Atlantic halibut (Hippoglossus hippoglossus): Proteolytic liberation of free amino acids, and ion transport, are driving forces for osmotic water influx. J Exp Biol 205:211–224
Fulton TW (1898) On the growth and maturation of the ovarian eggs of teleostean fishes. Fish Board Scotland, 16th Annual Report, Part 3:83–134
Fyhn HJ, Finn RN, Reith M, Norberg B (1999) Yolk protein hydrolysis and oocyte free amino acids as key features in the adaptive evolution of teleost fishes to seawater. Sarsia 84:451–456
Hanna RN, Zhu Y (2011) Controls of meiotic signaling by membrane or nuclear progestin receptor in zebrafish follicle-enclosed oocytes. Mol Cell Endocrinol 337:80–88
Hanna RN, Daly SC, Pang Y, Anglade I, Kah O, Thomas P, Zhu Y (2010) Characterization and expression of the nuclear progestin receptor in zebrafish gonads and brain. Biol Reprod 82:112–122
Hasegawa T, Tanii H, Suzuki M, Tanaka S (2003) Regulation of water absorption in the frog skins by two vasotocin-dependent water-channel aquaporins, AQPh2 and AQP-h3. Endocrinology 144:4087–4096
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 Ecol Genet Physiol 311A:752–762
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
King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Natl Rev Mol Cell Biol 5:687–698
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
Kristoffersean BA, Finn RN (2008) Major osmolyte changes during oocyte hydration of a clupeocephalan marine benthophil: Atlantic herring. Mar Biol 154:683–692
Kristoffersen BA, Nerland A, Nilsen F, Kolarevic J, Finn RN (2009) Genomic and proteomic analyses reveal non-neofunctionalized 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
Lubzens E, Young G, Bobe J, Cerdà J (2010) Oogenesis in teleosts: how eggs are formed. Gen Comp Endocrinol 165:367–389
Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ 50(Suppl. 1):S195–S219
Nedvetsky PI, Tamma G, Beulshausen S, Valenti G, Rosenthal W, Klussmann E (2009) Regulation of aquaporin-2 trafficking. Handb Exp Pharmacol 190:133–157
Norberg N, Valknera V, Husea J, Karlsena I, Grung GL (1991) Ovulatory rhythms and egg viability in the Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 97:365–371
Perdiguero E, Nebreda AR (2004) Use of Xenopus oocytes and early embryos to study MAPK signaling. Methods Mol Biol 250:299–314
Philpott A, Yew PR (2008) The Xenopus cell cycle: an overview. Mol Biotechnol 39:9–19
Robert J, Clauser E, Petit PX, Ventura MA (2005) A novel C-terminal motif is necessary for the export of the vasopressin V1b/V3 receptor to the plasma membrane. J Biol Chem 280:2300–2308
Rodríguez-Marí A, Yan YL, Bremiller RA, Wilson C, Cañestro C, Postlethwait JH (2005) Characterization and expression pattern of zebrafish Anti-Müllerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns 5:655–667
Selman K, Wallace RA, Cerdà J (2001) Bafilomycin A1 inhibits proteolytic cleavage and hydration but not yolk crystal disassembly or meiosis during maturation of sea bass oocytes. J Exp Zool 290:265–278
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
Sun Y, Zhang Q, Qi J, Yu Y, Li S, Li C, Zhong Q (2009) Cloning, expression and analysis of two Aquaporin-1 paralogous genes in Cynoglossus semilaevis. J Wuhan University (Natural Science Edition) 55:335–339 (in Chinese with English summary)
Sun Y, Zhang Q, Qi J, Chen Y, Zhong Q, Li C, Yu Y, Li S, Wang Z (2010) Identification of differential genes in the ovary relative to the testis and their expression patterns in half-smooth tongue sole (Cynoglossus semilaevis). J Genet Genomics 37:137–145
Tian J, Kim S, Heilig E, Ruderman JV (2000) Identification of XPR-1, a progesterone receptor required for Xenopus oocyte activation. Proc Natl Acad Sci USA 97:14358–14363
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
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
Törnroth-Horsefield S, Hedfalk K, Fischer G, Lindkvist-Petersson K, Neutze R (2010) Structural insights into eukaryotic aquaporin regulation. FEBS Lett 584:2580–2588
Virkki LV, Franke C, Somieski P, Boron WF (2002) Cloning and functional characterization of a novel aquaporin from Xenopus laevis oocytes. J Biol Chem 277:40610–40616
Yao B, Zhou L, Wang Y, Xia W, Gui JF (2007) Differential expression and dynamic changes of SOX3 during gametogenesis and sex reversal in protogynous hermaphroditic fish. J Exp Zool A Ecol Genet Physiol 307:207–219
Yokoi H, Kobayashi T, Tanaka M, Nagahama Y, Wakamatsu Y, Takeda H, Araki K, Morohashi K, Ozato K (2002) Sox9 in a teleost fish, medaka (Oryzias latipes): evidence for diversified function of Sox9 in gonad differentiation. Mol Reprod Dev 63:5–16
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
Zhu Y, Rice CD, Pang Y, Pace M, Thomas P (2003) Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc Natl Acad Sci USA 100:2231–2236
Acknowledgments
The authors are grateful to the Spanish Ministry of Science and Innovation (MICINN) and the Research Council of Norway FriBio (204813) programme for the continuous financial support. C. Z. and F. C. were supported by predoctoral (FPI) and postdoctoral (Juan de la Cierva Programme) fellowships, respectively, from MICINN.
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Cerdà, J., Zapater, C., Chauvigné, F. et al. 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 (2013). https://doi.org/10.1007/s10695-012-9608-2
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DOI: https://doi.org/10.1007/s10695-012-9608-2