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Vol 56, No 3 (2018)
Original paper
Submitted: 2016-11-16
Accepted: 2018-07-24
Published online: 2018-07-31
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Study of the hydromineral regulation of Typhlonectes compressicauda according to the seasonal variation

Mohammad Yousef1, Elara N. Moudilou1, Hafsa Djoudad-Kadji2, Jean-Marie Exbrayat1
·
Pubmed: 30070682
·
Folia Histochem Cytobiol 2018;56(3):172-183.
Affiliations
  1. University of Lyon, UMRS 449, Laboratory of General Biology, Lyon Catholic University; Laboratory of Reproduction and Comparative Development, Lyon, France
  2. Laboratoire de Zoologie Appliquée et d’Ecophysiologie Animale, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Algérie

open access

Vol 56, No 3 (2018)
ORIGINAL PAPERS
Submitted: 2016-11-16
Accepted: 2018-07-24
Published online: 2018-07-31

Abstract

Introduction. Typhlonectes compressicauda is a viviparous gymnophionan amphibian living in tropical areas of South America. This lengthened amphibian is submitted to seasonal variations characterized by the rainy season (from January to June) and the dry season (from July to December). The mineral homeostasis in amphibians is partly ensured by the neurohormones arginine-vasotocin (AVT), and mesotocin (MST). These two hormones were localized in the hypothalamus, and their receptors, mesotocin receptors (MTR) and vasotocin receptors (VTR2) in the kidney. The aim of the study was to better understand the physiology of the hydromineral regulation of the studied species.

Material and methods. The specimens of T. compressicauda male and female adult were divided into 6 groups: males in the rainy season, males in the dry season, females pregnant in the rainy season, females pregnant in the dry season, females not pregnant in the rainy season, females not pregnant in the dry season. We studied the expression of hormones (AVT, MST) and their receptors (MTR, VTR2) in the hypothalamus and the kidney, respectively, by immunohistochemical and histological techniques. We also studied the expression of aquaporin-2 (AQP2), a water-channel protein in the kidney.

Results. We found that the MST (diuretic hormone) and its receptor were more intensively expressed during the rainy season, whereas the period of maximal AVT (anti-diuretic hormone) and VTR2 expression was the dry season. A quantitative analysis showed significant differences in the number of labeled cells in the hypothalamus depending on the seasonal variation. The expression of AQP2 was observed in renal tubules during both seasons with an increased intensity during the dry season.

Conclusion. The expression of the MST/AVT in brain, their receptors MTRs/VTR2, and AQP2 in kidney changed in T. compressicauda according to the seasonal variations. A direct relationship between the seasonal cycle and reproduction cycle was demonstrated in this species.

Abstract

Introduction. Typhlonectes compressicauda is a viviparous gymnophionan amphibian living in tropical areas of South America. This lengthened amphibian is submitted to seasonal variations characterized by the rainy season (from January to June) and the dry season (from July to December). The mineral homeostasis in amphibians is partly ensured by the neurohormones arginine-vasotocin (AVT), and mesotocin (MST). These two hormones were localized in the hypothalamus, and their receptors, mesotocin receptors (MTR) and vasotocin receptors (VTR2) in the kidney. The aim of the study was to better understand the physiology of the hydromineral regulation of the studied species.

Material and methods. The specimens of T. compressicauda male and female adult were divided into 6 groups: males in the rainy season, males in the dry season, females pregnant in the rainy season, females pregnant in the dry season, females not pregnant in the rainy season, females not pregnant in the dry season. We studied the expression of hormones (AVT, MST) and their receptors (MTR, VTR2) in the hypothalamus and the kidney, respectively, by immunohistochemical and histological techniques. We also studied the expression of aquaporin-2 (AQP2), a water-channel protein in the kidney.

Results. We found that the MST (diuretic hormone) and its receptor were more intensively expressed during the rainy season, whereas the period of maximal AVT (anti-diuretic hormone) and VTR2 expression was the dry season. A quantitative analysis showed significant differences in the number of labeled cells in the hypothalamus depending on the seasonal variation. The expression of AQP2 was observed in renal tubules during both seasons with an increased intensity during the dry season.

Conclusion. The expression of the MST/AVT in brain, their receptors MTRs/VTR2, and AQP2 in kidney changed in T. compressicauda according to the seasonal variations. A direct relationship between the seasonal cycle and reproduction cycle was demonstrated in this species.

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Keywords

Amphibian, gymnophiona; Typhlonectes compressicauda; mesotocin; vasotocin; vasotocin receptors; aquaporin; IHC

About this article
Title

Study of the hydromineral regulation of Typhlonectes compressicauda according to the seasonal variation

Journal

Folia Histochemica et Cytobiologica

Issue

Vol 56, No 3 (2018)

Article type

Original paper

Pages

172-183

Published online

2018-07-31

Page views

2392

Article views/downloads

1559

DOI

10.5603/FHC.a2018.0016

Pubmed

30070682

Bibliographic record

Folia Histochem Cytobiol 2018;56(3):172-183.

Keywords

Amphibian
gymnophiona
Typhlonectes compressicauda
mesotocin
vasotocin
vasotocin receptors
aquaporin
IHC

Authors

Mohammad Yousef
Elara N. Moudilou
Hafsa Djoudad-Kadji
Jean-Marie Exbrayat

References (73)
  1. Wake M. The comparative morphology and evolution of the eyes of caecilians (Amphibia, Gymnophiona). Zoomorphology. 1985; 105(5): 277–295.
  2. Exbrayat JM, Laurent MT. Quelques observations sur la reproduction en élevage de deux amphibiens apodes: Typhlonectes compressicaudus et un Ichthyophis. Possibilité de rythmes endogènes. Bulletin de la Société Herpétologique de France. 1986; 40: 52–62.
  3. Exbrayat JM. Les Gymnophiones, ces curieux Amphibiens. Paris: Boubée. ; 2000.
  4. Wake M. The Spermatogenic Cycle of Dermophis mexicanus (Amphibia: Gymnophiona). Journal of Herpetology. 1995; 29(1): 119.
  5. Exbrayat JM. Premières observations sur le cycle annuel de l’ovaire de Typhlonectes compressicaudus (Duméril et Bibron, 1841), Batracien Apode vivipare. CR Acad Sci. 1983; 296: 493–498.
  6. Exbrayat JM, Estabel J. Anatomy with particular reference to the reproductive system. Pp. 79–155. In J.M. Exbrayat (Ed.) Reproductive Biology and Phylogeny of Gymnophiona Caecilians). Science Publishers, U K. 2006; 5: 79–155.
  7. Measey GJ, Smitam M, Beyor RS, et al. Year-round spermatogenic activity in an oviparous subterranean Caecilian, Boulengurula taitanus Loveridge 1935 (Amphibia Gymnophiona Caeciliidae). Tropical Zoology. 2008; 21: 109–122.
  8. Raquet MA, Measey GJ, Exbrayat JM. Annual variation of ovarian structures ofBoulengerula taitana(Loveridge 1935), a Kenyan caecilian. African Journal of Herpetology. 2015; 64(2): 116–134.
  9. Moodie G. Observations on the life history of the caecilian Typhlonectes compressicaudus (Dumeril and Bibron) in the Amazon basin. Canadian Journal of Zoology. 1978; 56(4): 1005–1008.
  10. Exbrayat JM, Delsol M, Flatin J. Typhlonectes compressicaudus Amphibien vivipare de Guyane. Le Littoral Guyanais, Fragilité de l'Environnement. Nature Guyanaise. 1er congrès régional SEPANGUY, 10éme coll. SEPANRI. Edited by SEPANGUY, Cayenne, SEPANRIT, Bordeaux. ; 1986: 119–124.
  11. Exbrayat JM, Morel G. Prolactin (PRL)-coding mRNA in Typhlonectes compressicaudus, a viviparous gymnophionan amphibian: an in situ hybridization study. Cell and Tissue Research. 1995; 280(1): 133–138.
  12. Acher R. Chemistry of the neurohypophysial hormones: an example of molecular evolution. Handbook of physiology. 1974; 4: 119–130.
  13. Oksche A. The neuroanatomical basis of comparative neuroendocrinology. Gen Comp Endocrinol. 1976; 29(2): 225–239.
  14. Dierickx K. Immunocytochemical localization of the vertebrate cyclic nonapeptide neurohypophyseal hormones and neurophysins. Int Rev Cytol. 1980; 62: 119–185.
  15. Acher R, Chauvet J. The neurohypophysial endocrine regulatory cascade: precursors, mediators, receptors, and effectors. Front Neuroendocrinol. 1995; 16(3): 237–289.
  16. Moore FL, Lowry CA. Comparative neuroanatomy of vasotocin and vasopressin in amphibians and other vertebrates. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 1998; 119(3): 251–260.
  17. Acher R. Neurohypophysial peptide systems: processing machinery, hydroosmotic regulation, adaptation and evolution. Regul Pept. 1993; 45(1-2): 1–13.
  18. Dantzler WH, Braun EJ. Comparative nephron function in reptiles, birds, and mammals. Am J Physiol. 1980; 239(3): R197–R213.
  19. Rice GE. Plasma arginine vasotocin concentrations in the lizard Varanus gouldii (Gray) following water loading, salt loading, and dehydration. Gen Comp Endocrinol. 1982; 47(1): 1–6.
  20. Takei Y. Comparative physiology of body fluid regulation in vertebrates with special reference to thirst regulation. Jpn J Physiol. 2000; 50(2): 171–186.
  21. Akhundova A, Getmanova E, Gorbulev V, et al. Cloning and functional characterization of the amphibian mesotocin receptor, a member of the oxytocin/vasopressin receptor superfamily. Eur J Biochem. 1996; 237(3): 759–767.
  22. Zardoya R. Phylogeny and evolution of the major intrinsic protein family. Biol Cell. 2005; 97(6): 397–414.
  23. Fu D, Lu M. The structural basis of water permeation and proton exclusion in aquaporins. Mol Membr Biol. 2007; 24(5-6): 366–374.
  24. Boyd SK. Arginine vasotocin facilitation of advertisement calling and call phonotaxis in bullfrogs. Horm Behav. 1994; 28(3): 232–240.
  25. Goodson JL, Bass AH. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Brain Res Rev. 2001; 35(3): 246–265.
  26. Do-Rego JL, Acharjee S, Seong JY, et al. Vasotocin and mesotocin stimulate the biosynthesis of neurosteroids in the frog brain. J Neurosci. 2006; 26(25): 6749–6760.
  27. Acharjee S, Do-Rego JL, Oh DY, et al. Identification of amino acid residues that direct differential ligand selectivity of mammalian and nonmammalian V1a type receptors for arginine vasopressin and vasotocin. Insights into molecular coevolution of V1a type receptors and their ligands. J Biol Chem. 2004; 279(52): 54445–54453.
  28. 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(3): 485–498.
  29. Acharjee S. Molecular cloning, pharmacological characterization, and histochemical distribution of frog vasotocin and mesotocin receptors. Journal of Molecular Endocrinology. 2004; 33(1): 293–313.
  30. Bentley PJ. Endocrines and osmoregulation: a comparative account in vertebrates. Springer Science & Business Media. ; 2002.
  31. Bentley AJ, Yorio T. Do Frogs Drinks? Journal of Experimental Biology. 1979; 79(1): 41–46.
  32. Hillyard SD. Behavioral, molecular and integrative mechanisms of amphibian osmoregulation. J Exp Zool. 1999; 283(7): 662–674.
  33. Uchiyama M, Konno N. Hormonal regulation of ion and water transport in anuran amphibians. Gen Comp Endocrinol. 2006; 147(1): 54–61.
  34. Suzuki M, Tanaka S. Molecular diversity of vasotocin-dependent aquaporins closely associated with water adaptation strategy in anuran amphibians. J Neuroendocrinol. 2010; 22(5): 407–412.
  35. Tanii H, Hasegawa T, Hirakawa N, et al. Molecular and cellular characterization of a water-channel protein, AQP-h3, specifically expressed in the frog ventral skin. J Membr Biol. 2002; 188(1): 43–53.
  36. Tanaka S, Hasegawa T, Tanii H, et al. Immunocytochemical and phylogenetic distribution of aquaporins in the frog ventral skin and urinary bladder. Ann N Y Acad Sci. 2005; 1040: 483–485.
  37. Ogushi Y, Mochida H, Nakakura T, et al. Immunocytochemical and phylogenetic analyses of an arginine vasotocin-dependent aquaporin, AQP-h2K, specifically expressed in the kidney of the tree frog, Hyla japonica. Endocrinology. 2007; 148(12): 5891–5901.
  38. Sasaki S, Noda Y. Aquaporin-2 protein dynamics within the cell. Curr Opin Nephrol Hypertens. 2007; 16(4): 348–352.
  39. Wake, M.H. Evolutionary morphology of the caecilian urogenital system. Part II: the kidneys and urogenital ducts. Acta Anatomica. 1970; 75: 321–358.
  40. Sakai T, Billo R, Kriz W. The structural organization of the kidney of Typhlonectes compressicaudus (Amphibia, Gymnophiona). Anat Embryol (Berl). 1986; 174(2): 243–252.
  41. Sakai T, Billo R, Nobiling R, et al. Ultrastructure of the kidney of a South American caecilian, Typhlonectes compressicaudus (Amphibia, Gymnophiona). Cell and Tissue Research. 1988; 252(3): 589–600.
  42. Sakai T, Billo R, Kriz W. Ultrastructure of the kidney of a South American caecilian, Typhlonectes compressicaudus (Amphibia, Gymnophiona). II. Distal tubule, connecting tubule, collecting duct and Wolffian duct. Cell Tissue Res. 1988; 252(3): 601–610.
  43. Korte GE, Rosenbluth J. Ependymal astrocytes in the frog cerebellum. Anat Rec. 1981; 199(2): 267–279.
  44. Leclercq B. Martin- Bouyer L, Exbrayat JM. . Embryonic development of pineal organ in Typhlonectes compressicauda, a viviparous Gymnophionan Amphibia. Scientia Herpetologica. 1995; 1995: 107–111.
  45. Clairambault P, Christophe N, Pairault C, et al. Organization of the serotoninergic system in the brain of two amphibian species, Ambystoma mexicanum (Urodela) and Typhlonectes compressicauda (Gymnophiona). Anat Embryol (Berl). 1994; 190(1): 87–99.
  46. Estabel J, Exbrayat JM. Brain development of Typhlonectes compressicaudus. Journal of herpetology. ; 1998: 1–10.
  47. Exbrayat JM. The cytological modifications of the distal lobe of the hypophysis in Typhlonectes compressicaudus (Duméril and Bibron, 1841), amphibian gymnophiona, during the cycles of seasonal activity. I: In adult males. Archives d'anatomie microscopique et de morphologie expérimentale. 1989; 2(4): 117–123.
  48. Exbrayat JM, Morel G. The cytological modifications of the distal lobe of the hypophysis in Typhlonectes compressicaudus (Dumeril and Bibron, 1841), amphibia gymnophiona, during the cycles of seasonal activity. II: In adult females. Biological structures and morphogenesis. 1990; 3(4): 129–138.
  49. Estabel J, Exbrayat JM. Brain Development of Typhlonectes compressicaudus. Journal of Herpetology. 1998; 32(1): 1.
  50. Wake WH. Kidney morphology in terrestrial and aquatic caecilians. Anat Rec. 1969; 163(2): 331.
  51. Stiffler D, DeRuyter M, Talbot C. Osmotic and Ionic Regulation in the Aquatic Caecilian Typhlonectes compressicauda and the Terrestrial Caecilian Ichthyophis kohtaoensis. Physiological Zoology. 1990; 63(4): 649–668.
  52. Warburg MR. Hormonal effect on the osmotic, electrolyte and nitrogen balance in terrestrial Amphibia. Zoolog Sci. 1995; 12(1): 1–11.
  53. Eggena P, Schwartz IL, Walter R. A sensitive hydroosmotic toad bladder assay. Affinity and intrinsic activity of neurohypophyseal peptides. J Gen Physiol. 1968; 52(3): 465–481.
  54. Shoemaker V, Bickler P. Kidney and bladder function in a uricotelic treefrog (Phyllomedusa sauvagei). Journal of Comparative Physiology ? B. 1979; 133(3): 211–218.
  55. Yorio T, Bentley PJ. Asymmetrical permeability of the integument of tree frogs (Hylidae). J Exp Biol. 1977; 67: 197–204.
  56. Pang PK, Sawyer WH. Renal and vascular responses of the bullfrog (Rana catesbeiana) to mesotocin. American Journal of Physiology-Renal Physiology. 1978; 235(2): F151–F155.
  57. Zoeller RT, Moore FL. Brain arginine vasotocin concentrations related to sexual behaviors and hydromineral balance in an amphibian. Horm Behav. 1988; 22(1): 66–75.
  58. González A, Smeets WJ. Comparative analysis of the vasotocinergic and mesotocinergic cells and fibers in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. J Comp Neurol. 1992; 315(1): 53–73.
  59. González A, Mun˜oz A, Mun˜oz M, et al. Ontogeny of vasotocinergic and mesotocinergic systems in the brain of the South African clawed frog Xenopus laevis. Journal of Chemical Neuroanatomy. 1995; 9(1): 27–40.
  60. González A, Smeets W. Distribution of vasotocin- and mesotocin-like immunoreactivities in the brain of Typhlonectes compressicauda (Amphibia, Gymnophiona): further assessment of primitive and derived traits of amphibian neuropeptidergic systems. Cell and Tissue Research. 1997; 287(2): 305–314.
  61. Mahlmann S, Meyerhof W, Hausmann H, et al. Structure, function, and phylogeny of [Arg8]vasotocin receptors from teleost fish and toad. Proc Natl Acad Sci U S A. 1994; 91(4): 1342–1345.
  62. Takahashi T, Kawashima M, Yasuoka T, et al. Mesotocin receptor binding of cortical and medullary kidney tissues of the hen. Poult Sci. 1997; 76(9): 1302–1306.
  63. Warne JM. Cloning and characterization of an arginine vasotocin receptor from the euryhaline flounder Platichthys flesus. Gen Comp Endocrinol. 2001; 122(3): 312–319.
  64. Schoepf I, Schradin C. Arginine vasopressin plasma levels change seasonally in African striped mice but do not differ between alternative reproductive tactics. Gen Comp Endocrinol. 2014; 204: 43–48.
  65. Lumpkin MD, Samson WK, McCann SM. Hypothalamic and pituitary sites of action of oxytocin to alter prolactin secretion in the rat. Endocrinology. 1983; 112(5): 1711–1717.
  66. Kennett JE, McKee DT. Oxytocin: an emerging regulator of prolactin secretion in the female rat. J Neuroendocrinol. 2012; 24(3): 403–412.
  67. Vega C, Moreno-Carranza B, Zamorano M, et al. Prolactin promotes oxytocin and vasopressin release by activating neuronal nitric oxide synthase in the supraoptic and paraventricular nuclei. Am J Physiol Regul Integr Comp Physiol. 2010; 299(6): R1701–R1708.
  68. Gimpl G, Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol Rev. 2001; 81(2): 629–683.
  69. Zingg HH, Grazzini E, Breton C, et al. Genomic and non-genomic mechanisms of oxytocin receptor regulation. Adv Exp Med Biol. 1998; 449: 287–295.
  70. Zingg HH, Laporte SA. Laporte SA. The oxytocin receptor Trends Endocrinology Metabolis 2003; 14: 222-227 doi: 10 1016/S1043. 2760; 03: 00080–8.
  71. Rzasa J, Ewy Z. The effect of ovarian steroids on the response of the hen uterus to neurohypophysial hormones. Acta Physiol Pol. 1982; 33(4): 249–255.
  72. Sharma D, Chaturvedi CM. Testosterone modulates pituitary vasotocin receptor expression and adrenal activity in osmotically stressed chicken. Comp Biochem Physiol A Mol Integr Physiol. 2011; 158(1): 87–93.
  73. Fink JoW, McLeod BJ, Assinder SJ, et al. Seasonal changes in mesotocin and localization of its receptor in the prostate of the brushtail possum (Trichosurus vulpecula). Biol Reprod. 2005; 72(2): 470–478.

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