Novel vasotocin-regulated aquaporins expressed in the ventral skin of semiaquatic anuran amphibians: Evolution of cutaneous water-absorbing mechanisms

Endocrinology

Volumn 155, Issue 6, 2014, Pages 2166-2177

  Saitoh, Yasunori ^a   Ogushi, Yuji ^a   Shibata, Yuki ^a   Okada, Reiko ^a   Tanaka, Shigeyasu ^a   Suzuki, Masakazu ^a  

^a SHIZUOKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; ARGIPRESTOCIN; COMPLEMENTARY DNA; ISOPRENALINE; PROPRANOLOL; PROTEIN AQP RJ3A; PROTEIN AQP RJ3B; UNCLASSIFIED DRUG; MESSENGER RNA; WATER;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANURA; ARTICLE; BULLFROG; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HINDLIMB; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANA JAPONICA; RANA NIGROMACULATA; SEQUENCE ANALYSIS; SKIN PERMEABILITY; TISSUE DISTRIBUTION; WATER ABSORPTION; AMPHIBIA; ANIMAL; GENETICS; METABOLISM; PHYLOGENY; SKIN; WESTERN BLOTTING;

AMPHIBIANS; ANIMALS; AQUAPORINS; BLOTTING, WESTERN; DNA, COMPLEMENTARY; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; PHYLOGENY; RNA, MESSENGER; SKIN; VASOTOCIN; WATER;

EID: 84901433666     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1928     Document Type: Article

References (51)

1. AmphibiaWeb: Information on amphibian biology and conservation, http://amphibiaweb.org/. Updated March 27, 2014. Accessed March 27, 2014.
2. Pough FH. Amphibian biology and husbandry. ILAR J. 2007;48: 203-213.
3. Lillywhite HB. Water relations of tetrapod integument. J Exp Biol. 2006;209: 202-226.
4. Bentley AJ, Yorio T. Do frogs drink? J Exp Biol. 1979;79: 41-46.
5. Bentley PJ. The Amphibia. In: Bradshaw SD, Burggren W, Heller HC, et al, eds. Endocrines and Osmoregulation: A Comparative Account in Vertebrates. Berlin, Germany: Springer; 2002: 155-186.
6. Hillyard SD. Behavioral, molecular and integrative mechanisms of amphibian osmoregulation. J Exp Zool. 1999;283: 662-674.
7. Jorgensen CB. 200 years of amphibian water economy: from Robert Townson to the present. Biol Rev Camb Philos Soc. 1997;72: 153-237.
8. Hillman SS, Withers PC, Drewes RC, Hillyard SD. Specialized physiological characteristics of Amphibia. In. Ecological and Environmental Physiology of Amphibians. New York, NY: Oxford University Press; 2009.
9. Agre P, Preston GM, Smith BL, et al. Aquaporin CHIP: the archetypal molecular water channel.Am J Physiol. 1993;265: F463-F476.
10. Zardoya R. Phylogeny and evolution of the major intrinsic protein family. Biol Cell. 2005;97: 397-414.
11. Benga G. Water channel proteins (later called aquaporins) and relatives: past, present, and future. IUBMB Life. 2009;61: 112-133.
12. Ishibashi K, Kondo S, Hara S, Morishita Y. The evolutionary aspects of aquaporin family. Am J Physiol Regul Integr Comp Physiol. 2011;300: R566-R576.
13. Suzuki M, Hasegawa T, Ogushi Y, Tanaka S. Amphibian aquaporins and adaptation to terrestrial environments: a review. Comp Biochem Physiol A Mol Integr Physiol. 2007;148: 72-81.
14. Suzuki M, Tanaka S. Molecular diversity of vasotocin-dependent aquaporins closely associated with water adaptation strategy in anuran amphibians. J Neuroendocrinol. 2010;22: 407-412.
15. Suzuki M, Tanaka S. Molecular and cellular regulation of water homeostasis in anuran amphibians by aquaporins. Comp Biochem Physiol A Mol Integr Physiol. 2009;153: 231-241.
16. Ogushi Y, Akabane G, Hasegawa T, et al. Water adaptation strategy in anuran amphibians: molecular diversity of aquaporin. Endocrinology. 2010;151: 165-173.
17. Hasegawa T, Tanii H, Suzuki M, Tanaka S. Regulation of water absorption in the frog skins by two vasotocin-dependent waterchannel aquaporins, AQP-h2 and AQP-h3. Endocrinology. 2003; 144: 4087-4096.
18. Voute CL, Ussing HH. Some morphological aspects of active sodium transport. The epithelium of the frog skin. J Cell Biol. 1968; 36: 625-638.
19. Ogushi Y, Tsuzuki A, Sato M, et al. The water-absorption region of ventral skin of several semiterrestrial and aquatic anuran amphibians identified by aquaporins. Am J Physiol Regul Integr Comp Physiol. 2010;299: R1150-R1162.
20. The Center for Biological Sequence Analysis, the Technical University of Denmark, TMHMM Server v. 2.0, http://www.cbs. dtu.dk/services/TMHMM/. Accessed October 7, 2013.
21. Suzuki M, Hyodo S, Kobayashi M, Aida K, Urano A. Characterization and localization ofmRNAencoding the salmon-type gonadotrophin-releasing hormone precursor of the masu salmon. J Mol Endocrinol. 1992;9: 73-82.
22. Zhang RB, Logee KA, Verkman AS. Expression of mRNA coding for kidney and red cell water channels in Xenopus oocytes. J Biol Chem. 1990;265: 15375-15378.
23. Ogushi Y, Mochida H, Nakakura T, Suzuki M, Tanaka S. Immunocytochemical and phylogenetic analyses of an arginine vasotocindependent aquaporin, AQP-h2K, specifically expressed in the kidney of the tree frog, Hyla japonica. Endocrinology. 2007;148: 5891-5901.
24. Tanii H, Hasegawa T, Hirakawa N, SuzukiM, Tanaka S. Molecular and cellular characterization of a water-channel protein, AQP-h3, specifically expressed in the frog ventral skin. J Membr Biol. 2002; 188: 43-53.
25. Ogushi Y, Kitagawa D, Hasegawa T, Suzuki M, Tanaka S. Correlation between aquaporin and water permeability in response to vasotocin, hydrin and β-adrenergic effectors in the ventral pelvic skin of the tree frog Hyla japonica. J Exp Biol. 2010;213: 288-294.
26. The Institut Pasteur Biology IT Center and the Ressource Parisienne en Bioinformatique Structurale, ClustalW 2.0.12, http://bioweb. pasteur.fr/seqanal/interfaces/clustalw.html. Accessed October 7, 2013.
27. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22: 4673-4680.
28. Hall BG. Phylogenetic Trees Made Easy: A How-to Manual. Sunderland, Massachusetts: Sinauer Associates, Inc; 2011.
29. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4: 406-425.
30. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39: 783-791.
31. de Groot BL, Grubmuller H. The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr Opin Struct Biol. 2005;15: 176-183.
32. Hirano Y, Okimoto N, Kadohira I, Suematsu M, Yasuoka K, Yasui M. Molecular mechanisms of how mercury inhibits water permeation through aquaporin-1: understanding by molecular dynamics simulation. Biophys J. 2010;98: 1512-1519.
33. Bentley PJ. The Amphibia. In: Hoar WS, Jacobs J, Langer H, Lindauer M, eds. Endocrines and Osmoregulation. A Comparative Account of the Regulation of Water and Salt in Vertebrates. Berlin, Germany: Springer-Verlag; 1971: 161-197.
34. Bentley PJ Actions of neurohypophysial peptide in amphibians, replies, and birds. In: Geiger SR, ed. Handbook of Physiology. Endocrinology IV. Vol part 1. Washington, DC: American Physiological Society; 1974: 545-563.
35. Hillman SS, Withers PC, Drewes RC, Hillyard SD. Habitats and morphotypes. In: Ecological and Environmental Physiology of Amphibians. New York, NY: Oxford University Press; 2009: 23-59.
36. Hillyard SD. The effect of isoproterenol on the anuran water balance response. Comp Biochem Physiol C. 1979;62C: 93-95.
37. Yokota SD, Hillman SS. Adrenergic control of the anuran cutaneous hydroosmotic response. GenCompEndocrinol. 1984;53: 309-314.
38. Viborg AL, Rosenkilde P. Water potential receptors in the skin regulate blood perfusion in the ventral pelvic patch of toads. Physiol Biochem Zool. 2004;77: 39-49.
39. Hillyard SD, Willumsen NJ. Chemosensory function of amphibian skin: integrating epithelial transport, capillary blood flow and behaviour. Acta Physiol (Oxf). 2011;202: 533-548.
40. Kohno S, Kamishima Y, Iguchi T. Molecular cloning of an anuran V(2) type [Arg(8)] vasotocin receptor and mesotocin receptor: functional characterization and tissue expression in the Japanese tree frog (Hyla japonica). Gen Comp Endocrinol. 2003;132: 485-498.
41. Stiles GL, Caron MG, Lefkowitz RJ. β-Adrenergic receptors: biochemical mechanisms of physiological regulation. Physiol Rev. 1984;64: 661-743.
42. De Sousa RC, Grosso A. Osmotic water flow across the abdominal skin of the toad Bufo marinus: effect of vasopressin and isoprenaline. J Physiol. 1982;329: 281-296.
43. Christensen CU. Effect of arterial perfusion on net water flux and active sodium transport across the isolated skin of Bufo bufo bufo (L.). J Comp Physiol. 1974;93: 93-104.
44. Viborg AL, Hillyard SD. Cutaneous blood flow and water absorption by dehydrated toads. Physiol Biochem Zool. 2005;78: 394-404.
45. Flicek P, Amode MR, Barrell D, et al. Ensembl 2014. Nucleic Acids Res. 2014;42: D749-D755.
46. San Mauro D, Vences M, Alcobendas M, Zardoya R, Meyer A. Initial diversification of living amphibians predated the breakup of Pangaea. Am Nat. 2005;165: 590-599.
47. Frost DR, Grant T, Faivovich J, et al. The amphibian tree of life.Am Mus Nat Hist. 2006;297: 1-370.
48. Fu D, Lu M. The structural basis of water permeation and proton exclusion in aquaporins. Mol Membr Biol. 2007;24: 366-374.
49. Hub JS, Grubmuller H, de Groot BL. Dynamics and energetics of permeation through aquaporins. What do we learn from molecular dynamics simulations? Handb Exp Pharmacol. 2009;190: 57-76.
50. Sasaki S. Aquaporin 2: from its discovery to molecular structure and medical implications. Mol Aspects Med. 2012;33: 535-546.
51. Shibata Y, Takeuchi H, Hasegawa T, et al. Localization of water channels in the skin of two species of desert toads, Anaxyrus (Bufo) punctatus and Incilius (Bufo) alvarius. Zool Sci. 2011;28: 664-670.