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Epithelial remodeling and claudin mRNA abundance in the gill and kidney of puffer fish (Tetraodon biocellatus) acclimated to altered environmental ion levels

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Abstract

In water of varying ion content, the gills and kidney of fishes contribute significantly to the maintenance of salt and water balance. However, little is known about the molecular architecture of the tight junction (TJ) complex and the regulation of paracellular permeability characteristics in these tissues. In the current studies, puffer fish (Tetraodon biocellatus) were acclimated to freshwater (FW), seawater (SW) or ion-poor freshwater (IPW) conditions. Following acclimation, alterations in systemic endpoints of hydromineral status were examined in conjunction with changes in gill and kidney epithelia morphology/morphometrics, as well as claudin TJ protein mRNA abundance. T. biocellatus were able to maintain endpoints of hydromineral status within relatively tight limits across the broad range of water ion content examined. Both gill and kidney tissue exhibited substantial alterations in morphology as well as claudin TJ protein mRNA abundance. These responses were particularly pronounced when comparing fish acclimated to SW versus those acclimated to IPW. TEM observations of IPW-acclimated fish gills revealed the presence of cells that exhibited the typical characteristics of gill mitochondria-rich cells (e.g. voluminous, Na+-K+-ATPase-immunoreactive, exposed to the external environment at the apical surface), but were not mitochondria-rich. To our knowledge, this type of cell has not previously been described in hyperosmoregulating fish gills. Furthermore, modifications in the morphometrics and claudin mRNA abundance of kidney tissue support the notion that spatial alterations in claudin TJ proteins along the nephron of fishes will likely play an important role in the regulation of salt and water balance in these organisms.

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References

  • Angelow S, Kim KJ, Yu ASL (2006) Claudin-8 modulates paracellular permeability to acidic and basic ions in MDCK II cells. J Physiol 571:15–26

    Article  CAS  PubMed  Google Scholar 

  • Angelow S, Schneeberger EE, Yu ASL (2007) Claudin-8 expression in renal epithelial cells augments the paracellular barrier by replacing endogenous claudin-2. J Membr Biol 215:147–159

    Article  CAS  PubMed  Google Scholar 

  • Avella M, Masoni A, Bornancin M, Mayer-Gostan N (1987) Gill morphology and sodium influx in the rainbow trout (Salmo gairdneri) acclimated to artificial freshwater environments. J Exp Zool 241:159–169

    Article  CAS  Google Scholar 

  • Bagherie-Lachidan M, Wright SI, Kelly SP (2008) Claudin-3 tight junction proteins in Tetraodon nigroviridis: cloning, tissue specific expression and a role in hydromineral balance. Am J Physiol Integr Comp Physiol 294:R1638–R1647

    CAS  Google Scholar 

  • Bagherie-Lachidan M, Wright SI, Kelly SP (2009) Claudin-8 and -27 expression in puffer fish (Tetraodon nigroviridis). J Comp Physiol B 179:419–431

    Article  CAS  PubMed  Google Scholar 

  • Bui P, Bagherie Lachidan M, Kelly SP (2010) Cortisol differentially alters claudin isoform mRNA abundance in a cultured gill epithelium from puffer fish (Tetraodon nigroviridis). Mol Cell Endocrinol 317:120–126

    Article  CAS  PubMed  Google Scholar 

  • Chasiotis H, Kelly SP (2008) Occludin immunolocalization and protein expression in goldfish. J Exp Biol 211:1524–1534

    Article  CAS  PubMed  Google Scholar 

  • Chasiotis H, Kelly SP (2009) Occludin and hydromineral balance in Xenopus laevis. J Exp Biol 212:287–296

    Article  CAS  PubMed  Google Scholar 

  • Chasiotis H, Effendi JC, Kelly SP (2009) Occludin expression in goldfish held in ion poor water. J Comp Physiol B 179:145–154

    Article  CAS  PubMed  Google Scholar 

  • Chasiotis H, Wood CM, Kelly SP (2010) Cortisol reduces paracellular permeability and increases occludin abundance in cultured trout gill epithelia. Mol Cell Endocrinol 323:232–238

    Article  CAS  PubMed  Google Scholar 

  • Chiba H, Osanai M, Murata M, Kojima T, Sawada N (2008) Transmembrane proteins of tight junctions. Biochim Biophys Acta 1778:588–600

    Article  CAS  PubMed  Google Scholar 

  • Claude P, Goodenough DA (1973) Fracture faces of zonulae occludentes from “tight” and “leaky” epithelia. J Cell Biol 58:390–400

    Article  CAS  PubMed  Google Scholar 

  • Clelland ES, Bui P, Bagherie Lachidan M, Kelly SP (2010) Spatial and salinity-induced alterations in claudin-3 isoform mRNA along the gastrointestinal tract of the puffer fish Tetraodon nigroviridis. Comp Biochem Physiol 155A:154–163

    CAS  Google Scholar 

  • Cliff WH, Beyenbach KW (1992) Secretory renal proximal tubules in seawater- and freshwater-adapted killifish. Am J Physiol Renal Physiol 262(1):F108–F116

    CAS  Google Scholar 

  • Coyne CB, Gambling TM, Boucher RC, Carson JL, Johnson LG (2003) Role of claudin interactions in airway tight junctional permeability. Am J Physiol Lung Cell Mol Physiol 285:L1166–L1178

    CAS  PubMed  Google Scholar 

  • Cuthbert AW, Maetz J (1972) The effects of calcium and magnesium on sodium fluxes through gills of Carassius auratus, L. J Physiol 221:633–643

    CAS  PubMed  Google Scholar 

  • Dantzler WH (2003) Regulation of renal proximal and distal tubule transport: sodium, chloride and organic anions. Comp Biochem Physiol A136:453–478

    Google Scholar 

  • Ernst SA, Dobson WC, Karnaky KJ (1980) Structural diversity of occluding junctions in the low resistance chloride-secreting opercular epithelium of seawater-adapted killifish (Fundulus heteroclitus). J Cell Biol 87:488–497

    Article  CAS  PubMed  Google Scholar 

  • Ernst SA, Hootman SR, Schreiber JH, Riddle CV (1981) Freeze-fracture and morphometric analysis of occluding junctions in rectal gland of elasmobranch fish. J Membr Biol 58:101–114

    Article  CAS  PubMed  Google Scholar 

  • Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177

    Article  CAS  PubMed  Google Scholar 

  • Freda J, Sanchez DA, Bergman HL (1991) Shortening of branchial tight junctions in acid-exposed rainbow trout (Onchorhynchus mykiss). Can J Fish Aquat Sci 48:2028–2033

    Article  Google Scholar 

  • González-Mariscal L, Namorado MC, Martin D, Luna J, Alarcon L, Islas S, Valencia L, Muriel P, Ponce L, Reyes JL (2000) Tight junction proteins ZO-1, ZO-2, and occludin along isolated renal tubules. Kidney Int 57:2386–2402

    Article  PubMed  Google Scholar 

  • González-Mariscal L, Betanzos A, Nava P, Jaramillo BE (2003) Tight junction proteins. Prog Biophys Mol Biol 81:1–44

    Article  PubMed  Google Scholar 

  • Greco AM, Fenwick JC, Perry SF (1996) The effects of soft-water acclimation on gill structure in the rainbow trout Oncorhynchus mykiss. Cell Tissue Res 285:75–82

    Article  CAS  PubMed  Google Scholar 

  • Hickman CP Jr, Trump BF (1969) The kidney. In: Hoar WS, Randall DJ (eds) Fish physiology, volume I. Excretion, ionic regulation, and metabolism. Academic Press, New York

    Google Scholar 

  • Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biémont C, Skalli Z, Cattolico L, Poulain J, de Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigó R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quétier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Crollius HR (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957

    Article  PubMed  Google Scholar 

  • Kalujnaia S, McWilliam IS, Zaguinaiko VA, Feilen AL, Nicholson J, Hazon N, Cutler CP, Cramb G (2007) Transcriptomic approach to the study of osmoregulation in the European eel Anguilla anguilla. Physiol Genomics 31:385–401

    Article  CAS  PubMed  Google Scholar 

  • Kelly SP, Wood CM (2001) Effect of cortisol on the physiology of cultured pavement cell epithelia from freshwater trout gills. Am J Physiol Integr Comp Physiol 281:R811–R820

    CAS  Google Scholar 

  • Kelly SP, Wood CM (2002) Cultured gill epithelia from freshwater tilapia (Oreochromis niloticus): effect of cortisol and homologous serum supplements from stressed and unstressed fish. J Membr Biol 190:29–42

    Article  CAS  PubMed  Google Scholar 

  • Kelly SP, Wood CM (2008) Cortisol stimulates calcium transport across cultured gill epithelia from freshwater rainbow trout. In Vitro Cell Dev Biol Anim 44:96–104

    Article  CAS  PubMed  Google Scholar 

  • Kelly SP, Chow INK, Woo NYS (1999) Alterations in Na+-K+-ATPase activity and gill chloride cell morphometrics of juvenile black sea bream (Mylio macrocephalus) in response to salinity and ration size. Aquaculture 172:351–367

    Article  CAS  Google Scholar 

  • Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S (2002) Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13:875–886

    CAS  PubMed  Google Scholar 

  • Kwon O, Myers BD, Sibley R, Dafoe D, Alfrey E, Nelson WJ (1998) Distribution of cell membrane-associated proteins along the human nephron. J Histochem Cytochem 46:1423–1434

    CAS  PubMed  Google Scholar 

  • Lin CH, Tsai RS, Lee TH (2004) Expression and distribution of Na, K-ATPase in gill and kidney of the spotted green pufferfish, Tetraodon nigroviridis, in response to salinity challenge. Comp Biochem Physiol A138:287–295

    Google Scholar 

  • Loh YH, Christoffels A, Brenner S, Hunziker W, Venkatesh B (2004) Extensive expansion of the claudin gene family in the teleost fish, Fugu rubripes. Genome Res 14:1248–1257

    Article  CAS  PubMed  Google Scholar 

  • Marshall WS, Grosell M (2006) Ion transport, osmoregulation, and acid-base balance. In: Evans DH, Claiborne JB (eds) The physiology of fishes, 3rd edn. Taylor and Francis Group, Boca Raton, pp 177–210

    Google Scholar 

  • McCormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na+, K+-ATPase activity. Can J Fish Aquat Sci 50:656–658

    Article  CAS  Google Scholar 

  • McDonald DG, Freda J, Cavdek V, Gonzalez R, Zia S (1991) Interspecific differences in gill morphology of freshwater fish in relation to tolerance of low-pH environments. Physiol Zool 64(1):124–144

    Google Scholar 

  • Moron SE, Oba ET, De Andrade CA, Fernandes MN (2003) Chloride cell responses to ion challenge in two tropical freshwater fish, the Erythrininds Hoplias malabaricus and Hoplerythrinus unitaeniatus. J Exp Zool 298A:93–104

    Article  Google Scholar 

  • Nishimura H, Fan Z (2003) Regulation of water movement across vertebrate renal tubules. Comp Biochem Physiol 136A:479–498

    CAS  Google Scholar 

  • Perry SF, Laurent P (1989) Adaptational responses of rainbow trout to lowered external NaCl concentration-contribution of the branchial chloride cell. J Exp Biol 147:147–168

    CAS  Google Scholar 

  • Perry SF, Wood CM (1985) Kinetics of branchial calcium uptake in the rainbow trout: effects of acclimation to various calcium levels. J Exp Biol 116:411–433

    Google Scholar 

  • Reyes JL, Lamas M, Martin D, Del Carmen Namorado M, Islas S, Luna J, Tauc M, Gonzalez-Mariscal L (2002) The renal segmental distribution of claudins changes with development. Kidney Int 62:476–487

    Article  CAS  PubMed  Google Scholar 

  • Sloman KA, Desforges PR, Gilmour KM (2001) Evidence for a mineralocorticoid-like receptor linked to branchial chloride cell proliferation in freshwater rainbow trout. J Exp Biol 204:3953–3961

    Google Scholar 

  • Tipsmark CK, Kiilerich P, Nilsen TO, Ebbesson LO, Stefansson SO, Madsen SS (2008) Branchial expression patterns of claudin isoforms in Atlantic salmon during seawater acclimation and smoltification. Am J Physiol Integr Comp Physiol 294:R1563–R1574

    CAS  Google Scholar 

  • Tipsmark CK, Sørensen KJ, Hulgard K, Madsen SS (2010) Claudin-15 and -25b expression in the intestinal tract of Atlantic salmon in response to seawater acclimation, smoltification and hormone treatment. Comp Biochem Physiol 155A:361–370

    CAS  Google Scholar 

  • van der Heijden AJH, van der Meij JCA, Flik G, Wendelaar Bonga SE (1999) Ultrastructure and distribution dynamics of chloride cells in tilapia larvae in fresh water and sea water. Cell Tissue Res 297:119–130

    Article  PubMed  Google Scholar 

  • Van Itallie CM, Anderson JM (2006) Claudins and epithelial paracellular transport. Annu Rev Physiol 68:403–429

    Article  PubMed  CAS  Google Scholar 

  • Wilson JM, Laurent P (2002) Fish gill morphology: inside out. J Exp Zool 293:192–213

    Article  PubMed  Google Scholar 

  • Yu ASL, Enck AH, Lencer WI, Schneeberher EE (2003) Claudin-8 expression in madin-darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem 278:17350–17359

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by an NSERC Discovery Grant, NSERC Discovery Accelerator Supplement, CFI New Opportunities Fund and an Ontario Early Researcher Award to SPK. The monoclonal antibody (α5) developed by D.M. Fambrough was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biological Sciences, Iowa City, IA, 52242, USA. All procedures conformed to the guidelines of the Canadian Council of Animal Care. We extend our thanks to Karen Rethoret for technical assistance.

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  1. Department of Biology, York University, 4700 Keele Street, Toronto, ON, M3J 1P3, Canada

    Nicole M. Duffy, Phuong Bui, Mazdak Bagherie-Lachidan & Scott P. Kelly

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  1. Nicole M. Duffy
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  2. Phuong Bui
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  3. Mazdak Bagherie-Lachidan
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Correspondence to Scott P. Kelly.

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Communicated by H.V. Carey.

N. M. Duffy and P. Bui contributed equally to this work.

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Duffy, N.M., Bui, P., Bagherie-Lachidan, M. et al. Epithelial remodeling and claudin mRNA abundance in the gill and kidney of puffer fish (Tetraodon biocellatus) acclimated to altered environmental ion levels. J Comp Physiol B 181, 219–238 (2011). https://doi.org/10.1007/s00360-010-0517-3

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