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Expression and localization of aquaporin-1 on the apical membrane of enterocytes in the small intestine of bottlenose dolphins

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Abstract

The small and large intestines are primary sites for water intake in mammals. To reveal how water is absorbed in the intestines of cetaceans, histological and molecular-biological studies were performed on the small intestine of the bottlenose dolphin, Tursiops truncatus. In histological studies using fresh specimens, obvious villi and deep crypts of Lieberkühn, lined by abundant enterocytes with microvilli and goblet cells, were observed in the mucosa. Expressions and immunolocalizations of aquaporin-1 (AQP1), a member of the water-selective channel termed AQP, were also investigated in the intestine. By reverse transcriptional polymerase chain reaction and rapid amplification of cDNA ends using RNA extracted from the dolphins’ small intestines, the full length of mRNA for AQP1 was sequenced. The deductive amino acid sequence for an open reading frame showed high homologies with other mammals’ AQP1, and water permeability of the protein was certified by cRNA injection to Xenopus oocytes. Immunohistochemistry showed AQP1 distribution on the apical membrane of the enterocytes, especially in the crypts. These data suggest that AQP1 is a channel protein responsible for water absorption in the small intestine of dolphins.

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References

  • Agre P, Kozono D (2003) Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 555:72–78

    Article  CAS  PubMed  Google Scholar 

  • Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S (2002) Aquaporin water channels—from atomic structure to clinical medicine. J Physiol 542:3–16

    Article  CAS  PubMed  Google Scholar 

  • Aoki M, Kaneko T, Katoh F, Hasegawa S, Tsutsui N, Aida K (2003) Intestinal water absorption through aquaporin 1 expressed in the apical membrane of mucosal epithelial cells in seawater-adapted Japanese eel. J Exp Biol 206:3495–3505

    Article  PubMed  Google Scholar 

  • Barrett KE (2005) Water and electrolyte absorption and recretion. In: Barrett KE (ed) Gastrointestinal physiology. The McGraw-Hill Companies, Inc., New York, pp 79–100

    Google Scholar 

  • Calamita G, Mazzone A, Bizzoca A, Cavalier A, Cassano G, Thomas D, Svelto M (2001) Expression and immunolocalization of the aquaporin-8 water channel in rat gastrointestinal tract. Eur J Cell Biol 80:711–719

    Article  CAS  PubMed  Google Scholar 

  • Elkjær ML, Nejsum LN, Gresz V, Kwon TH, Jensen UB, Frøkiær J, Nielsen S (2001) Immunolocalization of aquaporin-8 in raft kidney, gastrointestinal tract, testis, and airways. Am J Physiol Renal Physiol 281:F1047–F1057

    PubMed  Google Scholar 

  • Elsner R (1999) Living in water: solution to physiological problems. In: Reynolds JE III, Rommel SA (eds) Biology of marine mammals. Smithsonian Institution Press, Washington, DC, pp 73–116

    Google Scholar 

  • Gallardo P, Olea N, Sepulveda V (2002) Distribution of aquaporins in the colon of Octodon degus, a South American desert rodent. J Physiol Regul Integr Comp Physiol 283:R779–R788

    CAS  Google Scholar 

  • Gaskin DE (1978) Form and function in the digestive tract and associated organs in cetacea, with a consideration of metabolic rates and specific energy budgets. Orceangr Mar Biol Ann Rev 16:313–345

    Google Scholar 

  • Giffard-Mena I, Buolo V, Aujoulat F, Fowden H, Castille R, Charmantier G, Cramb G (2007) Aquaporin molecular characterization in the sea-bass (Dicentrarchus labrax): the effect of salinity on AQP1 and AQP3 expression. Comp Biochem Physiol A 148:430–444

    Article  Google Scholar 

  • Gordon JI, Hermiston ML (1994) Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr Opin Cell Biol 6:795–803

    Article  CAS  PubMed  Google Scholar 

  • Harrison RJ, Johnson FR, Young BA (1977) The small intestine of dolphins (Tursiops, Delphinus, Stenella). In: Harrison RJ (ed) Functional anatomy of marine mammals. Academic Press, New York, pp 297–331

    Google Scholar 

  • Hatakeyama S, Yoshida Y, Tani T, Koyama Y, Nihei K, Ohshiro K, Kamiie J, Yaoita E, Suda T, Hayakeyama K, Yamamoto T (2001) Cloning of a new aquaporin (AQP10) abundantly expressed in duodenum and jejunum. Biochem Biophys Res Commun 287:814–819

    Article  CAS  PubMed  Google Scholar 

  • Hines OJ, Whang EE, Bilchik AJ, Zinner MJ, Welton ML, Lane J, McFadden DW, Ashley SW (2000) Role of Na+-glucose cotransport in jejunal meal-induced absorption. Digest Dis Sci 45:1–6

    Article  CAS  PubMed  Google Scholar 

  • Jin SY, Lie YL, Xu LN, Jiang Y, Wang Y, Yang BX, Yang H, Ma TH (2006) Cloning and characterization of porcine aquaporin 1 water channel expressed extensively in gastrointestinal system. World J Gastroenterol 12:1091–1097

    Google Scholar 

  • Koyama Y, Yamamoto T, Tani T, Nihei K, Kondo D, Funkai H, Yaoita E, Kawasaki K, Sato N, Hatakeyama K, Kihara I (1999) Expression and localization of aquaporins in rat gastrointestinal tract. Am J Physiol 276:C621–C627

    CAS  PubMed  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  CAS  PubMed  Google Scholar 

  • Laforenza U, Gastaldi G, Grazioli M, Cova E, Tritto S, Faelli A, Calamita G, Ventura U (2005) Expression and immunolocalization of aquaporin-7 in rat gastrointestinal tract. Biol Cell 97:605–613

    Article  CAS  PubMed  Google Scholar 

  • Li HP, Kamiie J, Morishita Y, Yoshida Y, Yaoita E, Ishibashi K, Yamamoto T (2005a) Expression and localization of two isoforms of AQP10 in human small intestine. Biol Cell 97:823–829

    Article  CAS  PubMed  Google Scholar 

  • Li C, Hirooka Y, Honda R, Morikawa R, Yatoh M, Gotoh M, Nogimori T (2005b) Distribution of aquaporin-9 in the rat: an immunohistochemical study. Int J Tissue React 27:51–58

    PubMed  Google Scholar 

  • Loo DDF, Wright EM, Zeuthen T (2002) Water pumps. J Physiol Lond 42:53–60

    Article  Google Scholar 

  • Ma T, Verkman AS (1999) Aquaporin water channels in gastrointestinal physiology. J Physiol Lond 517:317–326

    Article  CAS  PubMed  Google Scholar 

  • Martinez AS, Cutler CP, Wilson GD, Phillips C, Hazon N, Cramb G (2005) Regulation of expression of two aquaporin homologs in the intestine of the European eel: effects of seawater acclimation and cortisol treatment. Am J Physiol Regul Integr Comp Physiol 288:R1733–R1743

    CAS  PubMed  Google Scholar 

  • Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K (1999) Water channel protein AQP3 is present in epithelia exposed to the environment of possible water loss. J Histochem Cytochem 47:1275–1286

    CAS  PubMed  Google Scholar 

  • Matthee CA, Burzlaff JD, Taylor JF, Davis SK (2001) Mining the mammalian genome for artiodactyl systematics. Syst Biol 50:367–390

    Article  CAS  PubMed  Google Scholar 

  • Mobasheri A, Shakibaei M, Marples D (2004) Immunohistochemical localization of aquaporin 10 in the apical membranes of the human ileum: a potential pathway for luminal water and small solute absorption. Histochem Cell Biol 121:463–471

    Article  CAS  PubMed  Google Scholar 

  • Mobasheri A, Wray S, Marples D (2005) Distribution of AQP2 and AQP3 water channels in human tissue mycroarrays. J Mol Histol 36:1–14

    Article  CAS  PubMed  Google Scholar 

  • Naftalin RJ, Pedley KC (1999) Regional crypt function in rat large intestine in relation to fluid absorption and growth of the pericryptal sheath. J Physiol Lond 514:211–227

    Article  CAS  PubMed  Google Scholar 

  • Nagahama M, Ma N, Semba R, Naruse S (2006) Aquaporin 1 immunoreactive enteric neurons in the rat ileum. Neurosci Lett 395:206–210

    Article  CAS  PubMed  Google Scholar 

  • Nielsen S, Smith BL, Christensen EI, Agre P (1993) Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. PNAS 90:7275–7279

    Article  CAS  PubMed  Google Scholar 

  • Nielsen S, Frøkiær J, Marples D, Kwon TH, Agre P, Knepper MA (2002) Aquaporins in the kidney: from molecules to medicine. Physiol Rev 82:205–244

    CAS  PubMed  Google Scholar 

  • Nikaido M, Rooney AP, Okada N (1999) Phylogenetic relationships among cetartiodactyls based on insertions of short and long interpersed elements: Hippopotamuses are the closest extant relatives of whales. PNAS 96:10261–10266

    Article  CAS  PubMed  Google Scholar 

  • Okada S, Misaka T, Matsumoto I, Watanabe H, Abe K (2003) Aquaporin-9 is expressed in a mucus-secreting goblet cell subset in the small intestine. FEBS Lett 540:157–162

    Article  CAS  PubMed  Google Scholar 

  • Ortiz RM (2001) Osmoregulation in marine mammals. J Exp Biol 204:1831–1844

    CAS  PubMed  Google Scholar 

  • Parvin MN, Tsumura K, Akamatsu T, Kanamori N, Hosoi K (2002) Expression and localization of AQP5 in the stomach and duodenum of the rat. BBA-Mol Cel Res 1542:116–124

    CAS  Google Scholar 

  • Preston GM, Agre P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel. PNAS 88:11110–11114

    Article  CAS  PubMed  Google Scholar 

  • Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387

    Article  CAS  PubMed  Google Scholar 

  • Ramírez-Lorca R, Vizuete ML, Venero JL, Revuelta M, Cano J, Ilundáin AA, Echevarría M (1999) Localization of aquaporin-3 mRNA and protein along the gastrointestinal tract of Wistar rats. Pflugers Arch Eur J Phy 438:94–100

    Article  Google Scholar 

  • Rice DW (1998) Marine mammals of the world: systematics and distribution. In: Wartzok E (ed) The society of marine mammalogy. Lawrence, CK, pp 51–125

  • Schenk AD, Werten PJL, Scheuring S, de Groot BL, Müller SA, Stahlberg H, Philippsen A, Engel A (2005) The 4.5 Å structure of human AQP2. J Mol Biol 350:278–289

    Article  CAS  PubMed  Google Scholar 

  • Smith BL, Agre P (1991) Erythrocyte Mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J Biol Chem 266:6407–6415

    CAS  PubMed  Google Scholar 

  • Suzuki M, Endo N, Nakano Y, Kato H, Kishiro T, Asahina K (2008) Localization of aquaporin-2, renal morphology and urine composition in the bottlenose dolphin and the Baird’s beaked whale. J Comp Physiol B 178:149–156

    Article  CAS  PubMed  Google Scholar 

  • Takata K, Matsuzaki T, Tajika Y (2004) Aquaporins: water channel proteins in the cell membrane. Prog Histochem Cytochem 39:1–83

    Article  CAS  PubMed  Google Scholar 

  • Telfer N, Cornell LH, Prescott JH (1970) Do dolphins drink water? J Am Vet Med Assoc 157:555–558

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Tritto S, Gastaldi G, Zelenin S, Grazioli M, Orsenigo MN, Ventura U, Laforenza U, Zelenina M (2007) Osmotic water permeability of rat intestinal brush border membrane vesicles: involvement of aquaporin-7 and aquaporin-8 and effect of metal ions. Biochem Cell Biol 85:675–684

    Article  CAS  PubMed  Google Scholar 

  • Tsujikawa T, Itoh A, Fukunaga T, Satoh J, Yasuoka T, Fujiyama Y (2003) Alteration of aquaporin mRNA expression after small bowel resection in the rat residual ileum and colon. J Gastroenterol Hepatol 18:803–808

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Song Y, Zhao D, Verkman AS (2005) Phenotype analysis of aquaporin-8 null mice. Am J Physiol Cell Physiol 288:C1161–C1170

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

I want to show my appreciation to the Taiji Fisheries Cooperative Union, Wakayama, Japan, Dr. T. Iwasaki and Mr. T. Hara of the Fisheries Research Agency, Kanagawa, Japan, Dr. T. Mori, Associated Professor of Nihon University, Kanagawa, Japan, for their cooperation in this study. I sincerely wish to thank Dr. A. Shimizu of the National Research Institute of Fisheries Science, the Fisheries Research Agency, Kanagawa, Japan, Dr. S. Watanabe of The University of Tokyo, Tokyo, Japan, and Dr. T. Moritomo, Associate Professor of Nihon University, Kanagawa, Japan, for their helpful and useful advices on experiments. This work was supported by the Grant-in-Aid for Young Scientists from the Japan Society for the Promotion of Science (#18880027 and #20780143), and Nihon University Individual Research Grant (2007).

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Correspondence to Miwa Suzuki.

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Communicated by H. V. Carey.

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Suzuki, M. Expression and localization of aquaporin-1 on the apical membrane of enterocytes in the small intestine of bottlenose dolphins. J Comp Physiol B 180, 229–238 (2010). https://doi.org/10.1007/s00360-009-0397-6

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  • DOI: https://doi.org/10.1007/s00360-009-0397-6

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