Acute and chronic hyperglycemic effects of vasopressin in normal rats: Involvement of V1A receptors

American Journal of Physiology - Endocrinology and Metabolism

Volumn 312, Issue 3, 2017, Pages E127-E135

  Taveau, Christopher ^a,b,c   Chollet, Catherine ^a,b,c   Bichet, Daniel G ^d   Velho, Gilberto ^a   Guillon, Gilles ^e,f   Corbani, Maithe ^e,f   Roussel, Ronan ^a,c,g   Bankir, Lise ^a,b,c   Melander, Olle ^h,i   Bouby, Nadine ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

^e INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^f UNIV MONTPELLIER   (France)

^g BICHAT HOSPITAL   (France)

^h LUND UNIVERSITY   (Sweden)

ⁱ LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Glucagon; Glycemia; Insulin; Vasopressin V1A receptor; Vasopressin V1B receptor

Indexed keywords

ARGIPRESSIN; GLUCAGON; GLUCOSE; INSULIN; NELIVAPTAN; RELCOVAPTAN; VASOPRESSIN V1A RECEPTOR; VASOPRESSIN V1B RECEPTOR; WATER; 1-(5-CHLORO-1-((2,4-DIMETHOXYPHENYL)SULFONYL)-3-(2-METHOXYPHENYL)-2-OXO-2,3-DIHYDRO-1H-INDOL-3-YL)-4-HYDROXY-N,N-DIMETHYL-2-PYRROLIDINECARBOXAMIDE; CYCLOPEPTIDE; FE 201874; GLUCOSE BLOOD LEVEL; INDOLE DERIVATIVE; PYRROLIDINE DERIVATIVE; V1A VASOPRESSIN RECEPTOR, RAT; VASOPRESSIN RECEPTOR; VASOPRESSIN RECEPTOR ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; FLUID INTAKE; GLUCAGON RELEASE; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HYPERGLYCEMIA; INSULIN RELEASE; MALE; NONHUMAN; PRESSOR RESPONSE; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; ZUCKER RAT; AGONISTS; ANIMAL; BLOOD; DRUG EFFECTS; FLUORESCENCE IMAGING; GENE TARGETING; HYPERINSULINISM; METABOLISM; PANCREAS;

ANIMALS; ANTIDIURETIC HORMONE RECEPTOR ANTAGONISTS; ARGININE VASOPRESSIN; BLOOD GLUCOSE; GENE KNOCK-IN TECHNIQUES; GLUCAGON; HYPERGLYCEMIA; HYPERINSULINISM; INDOLES; INSULIN; MALE; OPTICAL IMAGING; PANCREAS; PEPTIDES, CYCLIC; PYRROLIDINES; RATS; RATS, SPRAGUE-DAWLEY; RATS, ZUCKER; RECEPTORS, VASOPRESSIN;

EID: 85014540994     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00269.2016     Document Type: Article

References (62)

1. Abu-Basha EA, Yibchok-Anun S, Hsu WH. Glucose dependency of arginine vasopressin-induced insulin and glucagon release from the perfused rat pancreas. Metabolism 51: 1184-1190, 2002. doi:10.1053/meta.2002.34052.
2. Aguilera G. Regulation of the hypothalamic-pituitary-adrenal axis by neuropeptides. Horm Mol Biol Clin Investig 7: 327-336, 2011. doi:10.1515/HMBCI.2011.123.
3. Aoyagi T, Birumachi J, Hiroyama M, Fujiwara Y, Sanbe A, Yamauchi J, Tanoue A. Alteration of glucose homeostasis in V1A vasopressin receptor-deficient mice. Endocrinology 148: 2075-2084, 2007. doi:10.1210/en.2006-1315.
4. Bankir L, Bardoux P, Ahloulay M. Vasopressin and diabetes mellitus. Nephron 87: 8-18, 2001. doi:10.1159/000045879.
5. Bardoux P, Bichet DG, Martin H, Gallois Y, Marre M, Arthus MF, Lonergan M, Ruel N, Bouby N, Bankir L. Vasopressin increases urinary albumin excretion in rats and humans: involvement of V2 receptors and the renin-angiotensin system. Nephrol Dial Transplant 18: 497-506, 2003. doi:10.1093/ndt/18.3.497.
6. Baylis PH, Heath DA. Plasma-arginine-vasopressin response to insulininduced hypoglycaemia. Lancet 310: 428-430, 1977. doi:10.1016/S0140-6736(77)90610-9.
7. Baylis PH, Zerbe RL, Robertson GL. Arginine vasopressin response to insulin-induced hypoglycemia in man. J Clin Endocrinol Metab 53: 935-940, 1981. doi:10.1210/jcem-53-5-935.
8. Boertien WE, Meijer E, de Jong PE, ter Horst GJ, Renken RJ, van der Jagt EJ, Kappert P, Ouyang J, Engels GE, van Oeveren W, Struck J, Czerwiec FS, Oberdhan D, Krasa HB, Gansevoort RT. Short-term effects of tolvaptan in individuals with autosomal dominant polycystic kidney disease at various levels of kidney function. Am J Kidney Dis 65: 833-841, 2015. doi:10.1053/j.ajkd.2014.11.010.
9. Bouby N, Bachmann S, Bichet D, Bankir L. Effect of water intake on the progression of chronic renal failure in the 5/6 nephrectomized rat. Am J Physiol Renal Physiol 258: F973-F979, 1990.
10. Canivell S, Ponte B, Pruijm M, Ackermann D, Guessous I, Ehret G, Paccaud F, Pechere-Bertschi A, Mohaupt M, Vogt B, Burnier M, Devuyst O, Martin PY, Bochud M. 4b.05: Plasma copeptin is associated with insulin resistance in a swiss population-based study. J Hypertens 33, Suppl 1: e54, 2015. doi:10.1097/01.hjh.0000467489.06977.50.
11. Caraty A, Grino M, Locatelli A, Guillaume V, Boudouresque F, Conte-Devolx B, Oliver C. Insulin-induced hypoglycemia stimulates corticotropin-releasing factor and arginine vasopressin secretion into hypophysial portal blood of conscious, unrestrained rams. J Clin Invest 85: 1716-1721, 1990. doi:10.1172/JCI114626.
12. Edgerton DS, Jacobson PB, Opgenorth TJ, Zinker B, Beno D, von Geldern T, Ohman L, Scott M, Neal D, Cherrington AD. Selective antagonism of the hepatic glucocorticoid receptor reduces hepatic glucose production. Metabolism 55: 1255-1262, 2006. doi:10.1016/j.metabol.2006.05.011.
13. Enhörning S, Bankir L, Bouby N, Struck J, Hedblad B, Persson M, Morgenthaler NG, Nilsson PM, Melander O. Copeptin, a marker of vasopressin, in abdominal obesity, diabetes and microalbuminuria: the prospective Malmö Diet and Cancer Study cardiovascular cohort. Int J Obes 37: 598-603, 2013. doi:10.1038/ijo.2012.88.
14. Enhörning S, Leosdottir M, Wallström P, Gullberg B, Berglund G, Wirfält E, Melander O. Relation between human vasopressin 1A gene variance, fat intake, and diabetes. Am J Clin Nutr 89: 400-406, 2009. doi:10.3945/ajcn.2008.26382.
15. Enhörning S, Wang TJ, Nilsson PM, Almgren P, Hedblad B, Berglund G, Struck J, Morgenthaler NG, Bergmann A, Lindholm E, Groop L, Lyssenko V, Orho-Melander M, Newton-Cheh C, Melander O. Plasma copeptin and the risk of diabetes mellitus. Circulation 121: 2102-2108, 2010. doi:10.1161/CIRCULATIONAHA.109.909663.
16. Fisher BM, Baylis PH, Frier BM. Plasma oxytocin, arginine vasopressin and atrial natriuretic peptide responses to insulin-induced hypoglycaemia in man. Clin Endocrinol (Oxf) 26: 179-185, 1987. doi:10.1111/j.1365-2265.1987.tb00775.x.
17. Folny V, Raufaste D, Lukovic L, Pouzet B, Rochard P, Pascal M, Serradeil-Le Gal C. Pancreatic vasopressin V1B receptors: characteriza-tion in In-R1-G9 cells and localization in human pancreas. Am J Physiol Endocrinol Metab 285: E566-E576, 2003. doi:10.1152/ajpendo.00148.2003.
18. Fujiwara Y, Hiroyama M, Sanbe A, Aoyagi T, Birumachi J, Yamauchi J, Tsujimoto G, Tanoue A. Insulin hypersensitivity in mice lacking the V1B vasopressin receptor. J Physiol 584: 235-244, 2007. doi:10.1113/jphysiol.2007.136481.
19. Gao ZY, Gérard M, Henquin JC. Glucose-and concentration-dependence of vasopressin-induced hormone release by mouse pancreatic islets. Regul Pept 38: 89-98, 1992. doi:10.1016/0167-0115(92)90075-6.
20. Gibbs DM. Dissociation of oxytocin, vasopressin and corticotropin secretion during different types of stress. Life Sci 35: 487-491, 1984. doi:10.1016/0024-3205(84)90241-8.
21. Gillies GE, Linton EA, Lowry PJ. Corticotropin releasing activity of the new CRF is potentiated several times by vasopressin. Nature 299: 355-357, 1982. doi:10.1038/299355a0.
22. Hems DA, Rodrigues LM, Whitton PD. Rapid stimulation by vasopressin, oxytocin and angiotensin II of glycogen degradation in hepatocyte suspensions. Biochem J 172: 311-317, 1978. doi:10.1042/bj1720311.
23. Hems DA, Whitton PD. Stimulation by vasopressin of glycogen breakdown and gluconeogenesis in the perfused rat liver. Biochem J 136: 705-709, 1973. doi:10.1042/bj1360705.
24. Hems DA, Whitton PD, Ma GY. Metabolic actions of vasopressin, glucagon and adrenalin in the intact rat. Biochim Biophys Acta 411: 155-164, 1975. doi:10.1016/0304-4165(75)90294-9.
25. Lee B, Yang C, Chen TH, al-Azawi N, Hsu WH. Effect of AVP and oxytocin on insulin release: involvement of V1B receptors. Am J Physiol Endocrinol Metab 269: E1095-E1100, 1995.
26. Manning M, Misicka A, Olma A, Bankowski K, Stoev S, Chini B, Durroux T, Mouillac B, Corbani M, Guillon G. Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J Neuroendocrinol 24: 609-628, 2012. doi:10.1111/j.1365-2826.2012.02303.x.
27. Marir R, Virsolvy A, Wisniewski K, Mion J, Haddou D, Galibert E, Meraihi Z, Desarménien MG, Guillon G. Pharmacological characterization of FE 201874, the first selective high affinity rat V1A vasopressin receptor agonist. Br J Pharmacol 170: 278-292, 2013. doi:10.1111/bph.12249.
28. Méchaly I, Macari F, Laliberté MF, Lautier C, Serrano JJ, Cros G, Grigorescu F. Identification by RT-PCR and immunolocalization of arginine vasopressin in rat pancreas. Diabetes Metab 25: 498-501, 1999. DM-11-1999-25-6-1262-3636-101019-ART98.
29. Morel A, O’Carroll AM, Brownstein MJ, Lolaft SJ. Molecular cloning and expression of a rat V1A arginine vasopressin receptor. Nature 356: 523-526, 1992. doi:10.1038/356523a0.
30. Morgenthaler NG, Struck J, Alonso C, Bergmann A. Assay for the measurement of copeptin, a stable peptide derived from the precursor of vasopressin. Clin Chem 52: 112-119, 2006. doi:10.1373/clinchem.2005.060038.
31. Murat B, Devost D, Andrés M, Mion J, Boulay V, Corbani M, Zingg HH, Guillon G. V1B and CRHR1 receptor heterodimerization mediates synergistic biological actions of vasopressin and CRH. Mol Endocrinol 26: 502-520, 2012. doi:10.1210/me.2011-1202.
32. Nakamura K, Aoyagi T, Hiroyama M, Kusakawa S, Mizutani R, Sanbe A, Yamauchi J, Kamohara M, Momose K, Tanoue A. Both V1A and V1B vasopressin receptors deficiency result in impaired glucose tolerance. Eur J Pharmacol 613: 182-188, 2009. doi:10.1016/j.ejphar.2009.04.008.
33. Nakamura K, Yamashita T, Fujiki H, Aoyagi T, Yamauchi J, Mori T, Tanoue A. Enhanced glucose tolerance in the Brattleboro rat. Biochem Biophys Res Commun 405: 64-67, 2011. doi:10.1016/j.bbrc.2010.12.126.
34. O’Carroll AM, Howell GM, Roberts EM, Lolait SJ. Vasopressin potentiates corticotropin-releasing hormone-induced insulin release from mouse pancreatic -cells. J Endocrinol 197: 231-239, 2008. doi:10.1677/JOE-07-0645.
35. Ohnishi A, Orita Y, Takagi N, Fujita T, Toyoki T, Ihara Y, Yamamura Y, Inoue T, Tanaka T. Aquaretic effect of a potent, orally active, nonpeptide V2 antagonist in men. J Pharmacol Exp Ther 272: 546-551, 1995.
36. Oshikawa S, Tanoue A, Koshimizu TA, Kitagawa Y, Tsujimoto G. Vasopressin stimulates insulin release from islet cells through V1B receptors: a combined pharmacological/knockout approach. Mol Pharmacol 65: 623-629, 2004. doi:10.1124/mol.65.3.623.
37. Pena A, Murat B, Trueba M, Ventura MA, Bertrand G, Cheng LL, Stoev S, Szeto HH, Wo N, Brossard G, Serradeil-Le Gal C, Manning M, Guillon G. Pharmacological and physiological characterization of d[Leu4, Lys8]vasopressin, the first V1B-selective agonist for rat vasopressin/ oxytocin receptors. Endocrinology 148: 4136-4146, 2007. doi:10.1210/en.2006-1633.
38. Perucca J, Bichet DG, Bardoux P, Bouby N, Bankir L. Sodium excretion in response to vasopressin and selective vasopressin receptor antagonists. J Am Soc Nephrol 19: 1721-1731, 2008. doi:10.1681/ASN.2008010021.
39. Perucca J, Bouby N, Valeix P, Bankir L. Sex difference in urine concentration across differing ages, sodium intake, and level of kidney disease. Am J Physiol Regul Integr Comp Physiol 292: R700-R705, 2007. doi:10.1152/ajpregu.00500.2006.
40. Ravier MA, Leduc M, Richard J, Linck N, Varrault A, Pirot N, Roussel MM, Bockaert J, Dalle S, Bertrand G. Arrestin2 plays a key role in the modulation of the pancreatic -cell mass in mice. Diabetologia 57: 532-541, 2014. doi:10.1007/s00125-013-3130-7.
41. Robertson GL. The regulation of vasopressin function in health and disease. Recent Prog Horm Res 33: 333-385, 1976.
42. Rofe AM, Williamson DH. Metabolic effects of vasopressin infusion in the starved rat. Reversal of ketonaemia. Biochem J 212: 231-239, 1983. doi:10.1042/bj2120231.
43. Roussel R, El Boustany R, Bouby N, Potier L, Fumeron F, Mohammedi K, Balkau B, Tichet J, Bankir L, Marre M, Velho G. Plasma copeptin, AVP gene variants, and incidence of Type 2 diabetes in a cohort from the community. J Clin Endocrinol Metab 101: 2432-2439, 2016. doi:10.1210/jc.2016-1113.
44. Roussel R, Fezeu L, Bouby N, Balkau B, Lantieri O, Alhenc-Gelas F, Marre M, Bankir L; D.E.S.I.R. Study Group. Low water intake and risk for new-onset hyperglycemia. Diabetes Care 34: 2551-2554, 2011. doi:10.2337/dc11-0652.
45. Roussel R, Fezeu L, Marre M, Velho G, Fumeron F, Jungers P, Lantieri O, Balkau B, Bouby N, Bankir L, Bichet DG. Comparison between copeptin and vasopressin in a population from the community and in people with chronic kidney disease. J Clin Endocrinol Metab 99: 4656-4663, 2014. doi:10.1210/jc.2014-2295.
46. Saleem U, Khaleghi M, Morgenthaler NG, Bergmann A, Struck J, Mosley TH Jr, Kullo IJ. Plasma carboxy-terminal provasopressin (copeptin): a novel marker of insulin resistance and metabolic syndrome. J Clin Endocrinol Metab 94: 2558-2564, 2009. doi:10.1210/jc.2008-2278.
47. Schrier RW, Gross P, Gheorghiade M, Berl T, Verbalis JG, Czerwiec FS, Orlandi C; SALT Investigators. Tolvaptan, a selective oral vasopressin V2-receptor antagonist, for hyponatremia. N Engl J Med 355: 2099-2112, 2006. doi:10.1056/NEJMoa065181.
48. Seelig E, Bilz S, Keller U, Meienberg F, Christ-Crain M. Concentrations of the stress hormone copeptin increase upon hypoglycaemia in patients with type 1 diabetes dependent of hypoglycaemia awareness. PLoS One 8: e72876, 2013. doi:10.1371/journal.pone.0072876.
49. Serradeil-Le Gal C, Raufaste D, Derick S, Blankenstein J, Allen J, Pouzet B, Pascal M, Wagnon J, Ventura MA. Biological characterization of rodent and human vasopressin V1B receptors using SSR-149415, a nonpeptide V1B receptor ligand. Am J Physiol Regul Integr Comp Physiol 293: R938-R949, 2007. doi:10.1152/ajpregu.00062.2007.
50. Serradeil-Le Gal C, Wagnon J, Garcia C, Lacour C, Guiraudou P, Christophe B, Villanova G, Nisato D, Maffrand JP, Le Fur G. Biochemical and pharmacological properties of SR 49059, a new, potent, nonpeptide antagonist of rat and human vasopressin V1A receptors. J Clin Invest 92: 224-231, 1993. doi:10.1172/JCI116554.
51. Serradeil-Le Gal C, Wagnon J, Simiand J, Griebel G, Lacour C, Guillon G, Barberis C, Brossard G, Soubrié P, Nisato D, Pascal M, Pruss R, Scatton B, Maffrand JP, Le Fur G. Characterization of (2S,4R)-1-[5-chloro-1-[(2,4-dimethoxyphenyl)sulfonyl]-3-(2-methoxy-phenyl)-2-oxo-2,3-dihydro-1H-indol-3-yl]-4-hydroxy-N,Ndimethyl-2-pyrrolidine carboxamide (SSR149415), a selective and orally active vasopressin V1B receptor antagonist. J Pharmacol Exp Ther 300: 1122-1130, 2002. doi:10.1124/jpet.300.3.1122.
52. Serradeil-Le Gal C, Wagnon J, Valette G, Garcia G, Pascal M, Maffrand JP, Le Fur G. Nonpeptide vasopressin receptor antagonists: development of selective and orally active V1A, V2 and V1B receptor ligands. Prog Brain Res 139: 197-210, 2002. doi:10.1016/S0079-6123(02)39017-4.
53. Spruce BA, McCulloch AJ, Burd J, Orskov H, Heaton A, Baylis PH, Alberti KG. The effect of vasopressin infusion on glucose metabolism in man. Clin Endocrinol (Oxf) 22: 463-468, 1985. doi:10.1111/j.1365-2265.1985.tb00145.x.
54. Taveau C, Chollet C, Waeckel L, Desposito D, Bichet DG, Arthus MF, Magnan C, Philippe E, Paradis V, Foufelle F, Hainault I, Enhorning S, Velho G, Roussel R, Bankir L, Melander O, Bouby N. Vasopressin and hydration play a major role in the development of glucose intolerance and hepatic steatosis in obese rats. Diabetologia 58: 1081-1090, 2015. doi:10.1007/s00125-015-3496-9.
55. Tsuboi Y, Ishikawa S, Fujisawa G, Okada K, Saito T. In vivo diuretic effect of a new non-peptide arginine vasopressin antagonist, OPC-31260, in conscious rats. J Endocrinol 143: 227-234, 1994. doi:10.1677/joe.0.1430227.
56. Vahl TP, Ulrich-Lai YM, Ostrander MM, Dolgas CM, Elfers EE, Seeley RJ, D’Alessio DA, Herman JP. Comparative analysis of ACTH and corticosterone sampling methods in rats. Am J Physiol Endocrinol Metab 289: E823-E828, 2005. doi:10.1152/ajpendo.00122.2005.
57. Whitton PD, Rodrigues LM, Hems DA. Stimulation by vasopressin, angiotensin and oxytocin of gluconeogenesis in hepatocyte suspensions. Biochem J 176: 893-898, 1978. doi:10.1042/bj1760893.
58. Wideman CH, Murphy HM. Modulatory effects of vasopressin on glucose and protein metabolism during food-restriction stress. Peptides 14: 259-261, 1993. doi:10.1016/0196-9781(93)90039-J.
59. Yibchok-anun S, Abu-Basha EA, Yao CY, Panichkriangkrai W, Hsu WH. The role of arginine vasopressin in diabetes-associated increase in glucagon secretion. Regul Pept 122: 157-162, 2004. doi:10.1016/j.regpep.2004.06.010.
60. Yibchok-anun S, Hsu WH. Effects of arginine vasopressin and oxytocin on glucagon release from clonal α-cell line In-R1-G9: involvement of V1B receptors. Life Sci 63: 1871-1878, 1998. doi:10.1016/S0024-3205(98)00463-9.
61. Zerbe RL, Miller JZ, Robertson GL. The reproducibility and heritability of individual differences in osmoregulatory function in normal human subjects. J Lab Clin Med 117: 51-59, 1991.
62. Zerbe RL, Vinicor F, Robertson GL. Plasma vasopressin in uncontrolled diabetes mellitus. Diabetes 28: 503-508, 1979. doi:10.2337/diab.28.5.503.