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Comparison of natural and artificial vasopressin deficiency: why the latter is lethal?

https://doi.org/10.18699/VJ16.142

Abstract

The transgenic mouse technology is widespread, however, untill now 22.0 % of tested null mutations was found to be lethal. The complete lack of vasopressin (AVP) resulted also in preweaning lethality. It is surprising take into consideration the viability of the AVP mutant Brattleboro rats. Thus, AVP is essential for survival, but which of its ubiquiter role is the most important. AVP exerts its effect through specific plasma membrane receptors. V1a receptors can induce vasoconstriction maintaining blood pressure during hypovolemia. The V1b receptor on the anterior pituitary has a role in stress adaptation. The V2 subtype is located in the kidney and contributes to the antidiuresis. The avp gene consists of a signal peptide, AVP, neurophysin 2 and a C-terminal glycopeptide. The naturally occuring AVP-deficient Brattleboro rat has a framshift mutation in the neurophysin portion resulting in cental diabetes insipidus. In its hypothalamus AVP is not produced, while in certain peripheral tissues it may be expressed, suggesting the existence of a different synthetic pathway. The avp knockout mice can also be produced, they will be born, but without peripheral AVP administration they will not survive. Comparing available knockout models we can conclude that the combined V1a and V2 receptor mediated effects, namely hypotension and water lost together may led to lethality. As in Brattleboro and targetted knockout mice the local synthesis of AVP in the heart can be maintained and AVP can be released into the general circulation. Thus, in these animals vasoconstriction can compensate the hypovolemia.

About the Author

D. Zelena
Institute of Experimental Medicine, Budapest, Hungary
Russian Federation


References

1. Babey M., Kopp P., Robertson G.L. Familial forms of diabetes insipidus: clinical and molecular characteristics. Nature Rev. Endocrinol. 2011;7:701-714.

2. Bielsky I.F., Hu S.B., Szegda K.L., Westphal H., Young L.J. Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology. 2004;29:483-493.

3. Carrazana E.J., Pasieka K.B., Majzoub J.A. The vasopressin mRNA poly(A) tract is unusually long and increases during stimulation of vasopressin gene expression in vivo. Mol. Cell. Biol. 1988;8: 2267-2274.

4. Chen J., Aguilera G. Vasopressin protects hippocampal neurones in culture against nutrient deprivation or glutamate-induced apoptosis. J. Neuroendocrinol. 2010;22:1072-1081.

5. Chen Q., Patel R., Sales A., Oji G., Kim J., Monreal A.W., Brinton R.D. Vasopressin- induced neurotrophism in cultured neurons of the cerebral cortex: dependency on calcium signaling and protein kinase C activity. Neuroscience. 2000;101:19-26.

6. Egashira N., Tanoue A., Higashihara F., Mishima K., Fukue Y., Takano Y., Tsujimoto G., Iwasaki K., Fujiwara M. V1a receptor knockout mice exhibit impairment of spatial memory in an eight-arm radial maze. Neurosci. Lett. 2004;356:195-198.

7. Ermisch A., Ruhle H.J., Landgraf R., Hess J. Blood-brain barrier and peptides. J. Cerebr. Blood Flow Metab. 1985;5:350-357.

8. Forti F.L., Armelin H.A. Arginine vasopressin controls p27(Kip1) protein expression by PKC activation and irreversibly inhibits the proliferation of K-Ras-dependent mouse Y1 adrenocortical malignant cells. Biochim. Biophys. Acta. 2011;1813:1438- 1445.

9. Friedmann A.S., Memoli V.A., Cheng S.W., Yu X., North W.G. Vasopressin and vasopressin-associated neurophysin are present in gastric and duodenal cells of Brattleboro and Long – Evans rats. Ann. N.Y. Acad. Sci. 1993a;689:522-525.

10. Friedmann A.S., Memoli V.A., Yu X.M., North W.G. Biosynthesis of vasopressin by gastrointestinal cells of Brattleboro and Long – Evans rats. Peptides. 1993b;14:607- 612.

11. Furuse M. Knockout animals and natural mutations as experimental and diagnostic tool for studying tight junction functions in vivo. Biochim. Biophys. Acta. 2009;1788:813-819.

12. Ganong W.F. Neuropeptides in cardiovascular control. J. Hypertension. 1984;2:S15- S23.

13. Grant F.D., Reventos J., Kawabata S., Miller M., Gordon J.W., Majzoub J.A. Transgenic mouse models of vasopressin expression. Hypertension. 1993;22:640-645.

14. Habener J.F., Cwikel B.J., Hermann H., Hammer R.E., Palmiter R.D., Brinster R.L. Metallothionein-vasopressin fusion gene expression in transgenic mice. Nephrogenic diabetes insipidus and brain transcripts localized to magnocellular neurons. J. Biol. Chem. 1989;264: 18844-18852.

15. Hanahan D., Wagner E.F., Palmiter R.D. The origins of oncomice: a history of the first transgenic mice genetically engineered to develop cancer. Genes Developm. 2007;21:2258-2270.

16. Hiroyama M., Wang S., Aoyagi T., Oikawa R., Sanbe A., Takeo S., Tanoue A. Vasopressin promotes cardiomyocyte hypertrophy via the vasopressin V1A receptor in neonatal mice. Eur. J. Pharmacol. 2007; 559:89-97.

17. Hosoda K., Hammer R.E., Richardson J.A., Baynash A.G., Cheung J.C., Giaid A., Yanagisawa M. Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce megacolon associated with spotted coat color in mice. Cell. 1994;79:1267-1276.

18. Hupf H., Grimm D., Riegger G.A., Schunkert H. Evidence for a vasopressin system in the rat heart. Circulation Res. 1999;84:365-370.

19. Ivell R., Schmale H., Krisch B., Nahke P., Richter D. Expression of a mutant vasopressin gene: differential polyadenylation and readthrough of the mRNA 3’ end in a frame-shift mutant. EMBO J. 1986; 5:971-977.

20. Iwasaki Y., Oiso Y., Saito H., Majzoub J.A. Effects of various mutations in the neurophysin/glycopeptide portion of the vasopressin gene on vasopressin expression in vitro. Tohoku J. Exp. Med. 2000;191: 187-202.

21. Izumi Y., Miura K., Iwao H. Therapeutic potential of vasopressin-receptor antagonists in heart failure. J. Pharmacol. Sci. 2014;124:1-6.

22. Koufaris C., Alexandrou A., Sismani C., Skordis N. Identification of an AVP-NPII mutation within the AVP moiety in a family with neurohypophyseal diabetes insipidus: review of the literature. Hormones. 2015;14:442-446.

23. Landgraf R., Kessler M.S., Bunck M., Murgatroyd C., Spengler D., Zimbelmann M., Nussbaumer M., Czibere L., Turck C.W., Singewald N., Rujescu D., Frank E. Candidate genes of anxiety-related behavior in HAB/LAB rats and mice: focus on vasopressin and glyoxalase- I. Neurosci. Biobehav. Rev. 2007;31:89-102.

24. Landgraf R., Wigger A. Born to be anxious: neuroendocrine and genetic correlates of trait anxiety in HAB rats. Stress. 2003;6:111-119.

25. Lim A.T., Lolait S.J., Barlow J.W., Autelitano D.J., Toh B.H., Boublik J., Abraham J., Johnston C.I., Funder J.W. Immunoreactive argininevasopressin in Brattleboro rat ovary. Nature. 1984;310:61-64.

26. Majzoub J.A., Carrazana E.J., Shulman J.S., Baker K.J., Emanuel R.L. Defective regulation of vasopressin gene expression in Brattleboro rats. Amer. J. Physiol. 1987;252:E637-E642.

27. Miller M., Kawabata S., Wiltshire-Clement M., Reventos J., Gordon J.W. Increased vasopressin secretion and release in mice transgenic for the rat arginine vasopressin gene. Neuroendocrinology. 1993;57:621-625.

28. Montero S., Mendoza H., Valles V., Lemus M., Alvarez-Buylla R., de Alvarez-Buylla E.R. Arginine-vasopressin mediates central and peripheral glucose regulation in response to carotid body receptor stimulation with Na-cyanide. J. Appl. Physiol. 2006;100:1902-1909.

29. Nakamura K., Aoyagi T., Hiroyama M., Kusakawa S., Mizutani R., Sanbe A., Yamauchi J., Kamohara M., Momose K., Tanoue A. Both V(1A) and V(1B) vasopressin receptors deficiency result in impaired glucose tolerance. Eur. J. Pharmacol. 2009;613:182- 188.

30. Neumann I.D., Landgraf R. Advances in vasopressin and oxytocin – from genes to behaviour to disease. Preface. Progr. Brain Res. 2008; 170:XI-XIII.

31. Nussey S.S., Ang V.T., Jenkins J.S., Chowdrey H.S., Bisset G.W. Brattleboro rat adrenal contains vasopressin. Nature. 1984;310:64-66.

32. Oba Y., Lone N.A. Mortality benefit of vasopressor and inotropic agents in septic shock: a Bayesian network meta-analysis of randomized controlled trials. J. Crit. Care. 2014;29:706-710.

33. Quintanar-Stephano A., Organista-Esparza A., Chavira-Ramirez R., Kovacs K., Berczi I. Effects of neurointermediate pituitary lobectomy and desmopressin on acute experimental autoimmune encephalomyelitis in lewis rats. Neuroimmunomodulation. 2012;19:148-157.

34. Ring R.H. The central vasopressinergic system: examining the opportunities for psychiatric drug development. Curr. Pharm. Design. 2005;11:205-225.

35. Roper J.A., Craighead M., O’Carroll A.M., Lolait S.J. Attenuated stress response to acute restraint and forced swimming stress in arginine vasopressin 1b receptor subtype (Avpr1b) receptor knockout mice and wild-type mice treated with a novel Avpr1b receptor antagonist. J. Neuroendocrinol. 2010;22:1173-1180.

36. Schmale H., Ivell R., Breindl M., Darmer D., Richter D. The mutant vasopressin gene from diabetes insipidus (Brattleboro) rats is transcribed but the message is not efficiently translated. EMBO J. 1984;3:3289-3293.

37. Schmale H., Richter D. Single base deletion in the vasopressin gene is the cause of diabetes insipidus in Brattleboro rats. Nature. 1984;308:705-709.

38. Serradeil-Le Gal C., Bourrie B., Raufaste D., Carayon P., Garcia C., Maffrand J.P., Le Fur G., Casellas P. Effect of a new, potent, nonpeptide V1a vasopressin antagonist, SR 49059, on the binding and the mitogenic activity of vasopressin on Swiss 3T3 cells. Biochem. Pharmacol. 1994;47:633-641.

39. Serriere V., Tran D., Stelly N., Claret M., Alonso G., Tordjmann T., Guillon G. Vasopressin-induced morphological changes in polarized rat hepatocyte multiplets: dual calcium-dependent effects. Cell Calcium. 2008;43:95-104.

40. Somova L., Ivanova E., Zaharieva S., Machuganska A. Changes of adrenal vasopressin during hemorrhagic shock in rats with hereditary diabetes insipidus (Brattleboro strain). Acta Physiol. Pharmacol. Bulgarica. 1986;12:70-75.

41. Tahara A., Tsukada J., Tomura Y., Yatsu T., Shibasaki M. Vasopressin regulates rat mesangial cell growth by inducing autocrine secretion of vascular endothelial growth factor. J. Physiol. Sci. 2011;61: 115-122.

42. Tamma R., Sun L., Cuscito C., Lu P., Corcelli M., Li J., Colaianni G., Moonga S.S., Di Benedetto A., Grano M., Colucci S., Yuen T., New M.I., Zallone A., Zaidi M. Regulation of bone remodeling by vasopressin explains the bone loss in hyponatremia. Proc. Natl Acad. Sci. USA. 2013;110:18644-18649.

43. Tanoue A., Ito S., Honda K., Oshikawa S., Kitagawa Y., Koshimizu T.A., Mori T., Tsujimoto G. The vasopressin V1b receptor critically regulates hypothalamic- pituitary-adrenal axis activity under both stress and resting conditions. J. Clin. Invest. 2004;113:302-309.

44. Valtin H. The discovery of the Brattleboro rat, recommended nomenclature, and the question of proper controls. Ann. N.Y. Acad. Sci. 1982;394:1-9.

45. Young W.S., 3rd, Kovacs K., Lolait S.J. The diurnal rhythm in vasopressin V1a receptor expression in the suprachiasmatic nucleus is not dependent on vasopressin. Endocrinology. 1993;133:585-590.

46. Zelena D. Vasopressin in health and disease with a focus on affective disorders. Central Nervous Syst. Agents Med. Chem. 2012;12: 286-303.

47. Zhu W., Tilley D.G., Myers V.D., Coleman R.C., Feldman A.M. Arginine vasopressin enhances cell survival via a G protein-coupled receptor kinase 2/beta- arrestin1/extracellular-regulated kinase 1/2-dependent pathway in H9c2 cells. Mol. Pharmacol. 2013;84:227-235.


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