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. 1985 Aug;76(2):779–788. doi: 10.1172/JCI112035

Importance of amino acids on vasopressin-stimulated water flow.

C P Carvounis, G Carvounis, B J Wilk
PMCID: PMC423900  PMID: 2863287

Abstract

The presence of several naturally occurring amino acids in the serosal bath of toad urinary bladder significantly alters the hydrosmotic response of this tissue to vasopressin. We found that histidine, glutamate, and lysine increase vasopressin-stimulated water flow by 75%, 60%, and 43%, respectively. In contrast, alanine did not alter vasopressin-stimulated water flow, whereas glutamine decreased it by 25%. The effect of each amino acid represents intracellular events because their effects on theophylline-stimulated water flow were similar to those found with vasopressin. However, the site of action of amino acids varied, with some operating at steps before and others at steps after cyclic AMP generation. The fact that the metabolically inactive D-histidine and D-glutamate are as effective as their metabolically active L-counterparts suggests that the action of amino acids depends upon some physicochemical properties of their molecules. The ability of amino acids to influence the hydrosmotic effects of vasopressin was shown to be independent of prostaglandin generation, ionic composition, and molecular charge. In the case of histidine, we were able to obtain some understanding of the mechanism responsible for its action. We first showed that the effect of histidine does not depend upon its metabolism. In addition to D-histidine being as effective as the metabolically active L-histidine, we also showed that histidine is effective when its metabolism is abolished by low ambient temperature and also when its incorporation into proteins was prevented by cycloheximide. These findings suggest that histidine operates through some physicochemical property localized on its molecule. We were able to show that this property resides on the imidazole part of histidine. Imidazole, similar to histidine, increases vasopressin-stimulated water flow. Methylation of histidine on the imidazole ring completely abolished its effectiveness in increasing vasopressin-stimulated water flow. In contrast, methylation of histidine at the side chain increased vasopressin action similar to that found for histidine. We provide evidence that the physicochemical property of the imidazole ring of histidine is that of chelating Zn++ intracellularly, and that the intracellular site of action of histidine is closely linked to microtubules formation and/or action.

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Selected References

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  1. Arnauld J., Lachance P. A. Basic amino acid accumulation in potassium-depleted rat muscle. J Nutr. 1980 Dec;110(12):2480–2489. doi: 10.1093/jn/110.12.2480. [DOI] [PubMed] [Google Scholar]
  2. BENTLEY P. J. The effects of neurohypophysial extracts on the water transfer across the wall of the isolated urinary bladder of the toad Bufo marinus. J Endocrinol. 1958 Sep;17(3):201–209. doi: 10.1677/joe.0.0170201. [DOI] [PubMed] [Google Scholar]
  3. BRANDT I. K., MATALKA V. A., COMBS J. T. Amino acids in muscle and kidney of potassium-deficient rats. Am J Physiol. 1960 Jul;199:39–42. doi: 10.1152/ajplegacy.1960.199.1.39. [DOI] [PubMed] [Google Scholar]
  4. Bentley P. J. Mechanism of action of neurohypophysial hormones: actions of manganese and zinc on the permeability of the toad bladder. J Endocrinol. 1967 Dec;39(4):493–506. doi: 10.1677/joe.0.0390493. [DOI] [PubMed] [Google Scholar]
  5. Bentley P. J. Mechanism of action of neurohypophysial hormones: actions of manganese and zinc on the permeability of the toad bladder. J Endocrinol. 1967 Dec;39(4):493–506. doi: 10.1677/joe.0.0390493. [DOI] [PubMed] [Google Scholar]
  6. Bernardi G., Floris V., Marciani M. G., Morocutti C., Stanzione P. The action of acetylcholine and L-glutamic acid on rat caudate neurons. Brain Res. 1976 Sep 10;114(1):134–138. doi: 10.1016/0006-8993(76)91014-3. [DOI] [PubMed] [Google Scholar]
  7. Bisordi J. E., Schlondorff D., Hays R. M. Interaction of vasopressin and prostaglandins in the toad urinary bladder. J Clin Invest. 1980 Dec;66(6):1200–1210. doi: 10.1172/JCI109971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Burch R. M., Knapp D. R., Halushka P. V. Vasopressin stimulates thromboxane synthesis in the toad urinary bladder: effects of imidazole. J Pharmacol Exp Ther. 1979 Sep;210(3):344–348. [PubMed] [Google Scholar]
  9. Burg M., Patlak C., Green N., Villey D. Organic solutes in fluid absorption by renal proximal convoluted tubules. Am J Physiol. 1976 Aug;231(2):627–637. doi: 10.1152/ajplegacy.1976.231.2.627. [DOI] [PubMed] [Google Scholar]
  10. Carvounis C. P., Levine S. D., Hays R. M. pH-Dependence of water and solute transport in toad urinary bladder. Kidney Int. 1979 May;15(5):513–519. doi: 10.1038/ki.1979.66. [DOI] [PubMed] [Google Scholar]
  11. Curtis D. R., Duggan A. W., Felix D., Johnston G. A., Teb ecis A. K., Watkins J. C. Excitation of mammalian central neurones by acidic amino acids. Brain Res. 1972 Jun 22;41(2):283–301. doi: 10.1016/0006-8993(72)90503-3. [DOI] [PubMed] [Google Scholar]
  12. DICKERMAN H. W., WALKER W. G. EFFECT OF CATIONIC AMINO ACID INFUSION ON POTASSIUM METABOLISM IN VIVO. Am J Physiol. 1964 Feb;206:403–408. doi: 10.1152/ajplegacy.1964.206.2.403. [DOI] [PubMed] [Google Scholar]
  13. DeFeudis F. V. Amino acids as central neurotransmitters. Annu Rev Pharmacol. 1975;15:105–130. doi: 10.1146/annurev.pa.15.040175.000541. [DOI] [PubMed] [Google Scholar]
  14. ECKEL R. E., NORRIS J. E., POPE C. E., 2nd Basic amino acids as intracellular cations in K deficiency. Am J Physiol. 1958 Jun;193(3):644–652. doi: 10.1152/ajplegacy.1958.193.3.644. [DOI] [PubMed] [Google Scholar]
  15. Epstein F. H., Brosnan J. T., Tange J. D., Ross B. D. Improved function with amino acids in the isolated perfused kidney. Am J Physiol. 1982 Sep;243(3):F284–F292. doi: 10.1152/ajprenal.1982.243.3.F284. [DOI] [PubMed] [Google Scholar]
  16. Finn A. L., Handler J. S., Orloff J. Relation between toad bladder potassium content and permeability response to vasopressin. Am J Physiol. 1966 Jun;210(6):1279–1284. doi: 10.1152/ajplegacy.1966.210.6.1279. [DOI] [PubMed] [Google Scholar]
  17. Gaskin F., Kress Y. Zinc ion-induced assembly of tubulin. J Biol Chem. 1977 Oct 10;252(19):6918–6924. [PubMed] [Google Scholar]
  18. Gilles R. Métabolisme des acides aminés et contrôle du volume cellulaire. Arch Int Physiol Biochim. 1974 Aug;82(3):423–589. doi: 10.3109/13813457409070480. [DOI] [PubMed] [Google Scholar]
  19. Giroux E. L., Henkin R. I. Competition for zinc among serum albumin and amino acids. Biochim Biophys Acta. 1972 Jun 26;273(1):64–72. doi: 10.1016/0304-4165(72)90191-2. [DOI] [PubMed] [Google Scholar]
  20. HANDLER J. S., ORLOFF J. CYSTEINE EFFECT ON TOAD BLADDER RESPONSE TO VASOPRESSIN, CYCLIC AMP, AND THEOPHYLLINE. Am J Physiol. 1964 Mar;206:505–509. doi: 10.1152/ajplegacy.1964.206.3.505. [DOI] [PubMed] [Google Scholar]
  21. HAYS R. M., LEAF A. The problem of clinical vasopressin resistance: in vitro studies. Ann Intern Med. 1961 Apr;54:700–709. doi: 10.7326/0003-4819-54-4-700. [DOI] [PubMed] [Google Scholar]
  22. Hallman P. S., Perrin D. D., Watt A. E. The computed distribution of copper(II) and zinc(II) ions among seventeen amino acids present in human blood plasma. Biochem J. 1971 Feb;121(3):549–555. doi: 10.1042/bj1210549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Harris D. I., Sass-Kortsak A. The influence of amino acids on copper uptake by rat liver slices. J Clin Invest. 1967 Apr;46(4):659–667. doi: 10.1172/JCI105567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Harvey P. W., Hunsaker H. A., Allen K. G. Dietary L-histidine-induced hypercholesterolemia and hypocupremia in the rat. J Nutr. 1981 Apr;111(4):639–647. doi: 10.1093/jn/111.4.639. [DOI] [PubMed] [Google Scholar]
  25. Havener L. J., Toback F. G. Amino acid modulation of renal phosphatidylcholine biosynthesis in the rat. J Clin Invest. 1980 Mar;65(3):741–745. doi: 10.1172/JCI109721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hendil K. B., Hoffmann E. K. Cell volume regulation in Ehrlich ascites tumor cells. J Cell Physiol. 1974 Aug;84(1):115–125. doi: 10.1002/jcp.1040840113. [DOI] [PubMed] [Google Scholar]
  27. Hertz P., Richardson J. A. Arginine-induced hyperkalemia in renal failure patients. Arch Intern Med. 1972 Nov;130(5):778–780. [PubMed] [Google Scholar]
  28. IACOBELLIS M., GRIFFIN G. E., MUNTWYLER E. Free amino acid patterns of certain tissues from potassium-deficient dogs. Proc Soc Exp Biol Med. 1957 Oct;96(1):64–66. doi: 10.3181/00379727-96-23394. [DOI] [PubMed] [Google Scholar]
  29. IACOBELLIS M., MUNTWYLER E., DODGEN C. L. Free amino acid patterns of certain tissues from potassium and/or protein-deficient rats. Am J Physiol. 1956 May;185(2):275–278. doi: 10.1152/ajplegacy.1956.185.2.275. [DOI] [PubMed] [Google Scholar]
  30. LEVINSKY N. G., TYSON I., MILLER R. B., RELMAN A. S. The relation between amino acids and potassium in isolated rat muscle. J Clin Invest. 1962 Mar;41:480–487. doi: 10.1172/JCI104501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Larsson H., Wallin M., Edström A. Induction of a sheet polymer of tubulin by Zn2+. Exp Cell Res. 1976 Jun;100(1):104–110. doi: 10.1016/0014-4827(76)90332-3. [DOI] [PubMed] [Google Scholar]
  32. Lau S. J., Sarkar B. Ternary coordination complex between human serum albumin, copper (II), and L-histidine. J Biol Chem. 1971 Oct 10;246(19):5938–5943. [PubMed] [Google Scholar]
  33. Neumann P. Z., Sass-Kortsak A. The state of copper in human serum: evidence for an amino acid-bound fraction. J Clin Invest. 1967 Apr;46(4):646–658. doi: 10.1172/JCI105566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Olney J. W., Cicero T. J., Meyer E. R., de Gubareff T. Acute glutamate-induced elevations in serum testosterone and luteinizing hormone. Brain Res. 1976 Aug 13;112(2):420–424. doi: 10.1016/0006-8993(76)90298-5. [DOI] [PubMed] [Google Scholar]
  35. Parisi M., Piccinni Z. F. Regulation of the permeability to water in toad urinary bladder: the effect of copper. J Endocrinol. 1972 Oct;55(1):1–9. doi: 10.1677/joe.0.0550001. [DOI] [PubMed] [Google Scholar]
  36. Pitts R. F. Production of CO2 by the intact functioning kidney of the dog. Med Clin North Am. 1975 May;59(3):507–522. doi: 10.1016/s0025-7125(16)32004-1. [DOI] [PubMed] [Google Scholar]
  37. Prasad A. S., Oberleas D. Binding of zinc to amino acids and serum proteins in vitro. J Lab Clin Med. 1970 Sep;76(3):416–425. [PubMed] [Google Scholar]
  38. Rodriguez H. J., Yates J. T. Studies on amino acid incorporation in isolated toad bladder epithelial cells. Seasonal changes in protein synthesis. Biochim Biophys Acta. 1980 Feb 15;596(1):64–80. doi: 10.1016/0005-2736(80)90171-6. [DOI] [PubMed] [Google Scholar]
  39. Roth E., Muhlbacher F., Rauhs R., Huk I., Soderland K., Funovics J. Free amino acids in plasma and muscle in fulminant hepatic coma during an extracorporeal liver perfusion. JPEN J Parenter Enteral Nutr. 1982 May-Jun;6(3):240–244. doi: 10.1177/0148607182006003240. [DOI] [PubMed] [Google Scholar]
  40. Schlondorff D., Carvounis C. P., Jacoby M., Satriano J. A., Levine S. D. Multiple sites for interaction of prostaglandin and vasopressin in toad urinary bladder. Am J Physiol. 1981 Dec;241(6):F625–F631. doi: 10.1152/ajprenal.1981.241.6.F625. [DOI] [PubMed] [Google Scholar]
  41. Schmidt M. J., Thornberry J. F., Molloy B. B. Effects of kainate and other glutamate analogues on cyclic nucleotide accumulation in slices of rat cerebellum. Brain Res. 1977 Jan 31;121(1):182–189. doi: 10.1016/0006-8993(77)90450-4. [DOI] [PubMed] [Google Scholar]
  42. Shimizu H., Ichishita H., Odagiri H. Stimulated formation of cyclic adenosine 3':5'-monophosphate by aspartate and glutamate in cerebral cortical slices of guinea pig. J Biol Chem. 1974 Sep 25;249(18):5955–5962. [PubMed] [Google Scholar]
  43. Steiner D. F., Kemmler W., Tager H. S., Peterson J. D. Proteolytic processing in the biosynthesis of insulin and other proteins. Fed Proc. 1974 Oct;33(10):2105–2115. [PubMed] [Google Scholar]
  44. Tannen R. L. Control of acid excretion by the kidney. Annu Rev Med. 1980;31:35–49. doi: 10.1146/annurev.me.31.020180.000343. [DOI] [PubMed] [Google Scholar]
  45. Taylor A., Mamelak M., Golbetz H., Maffly R. Evidence for involvement of microtubules in the action of vasopressin in toad urinary bladder. I. Functional studies on the effects of antimitotic agents on the response to vasopressin. J Membr Biol. 1978 May 3;40(3):213–235. doi: 10.1007/BF02002969. [DOI] [PubMed] [Google Scholar]
  46. Thier S. O. Amino acid accumulation in the toad bladder. Relationship to transepithelial sodium transport. Biochim Biophys Acta. 1968 Mar 1;150(2):253–262. doi: 10.1016/0005-2736(68)90168-5. [DOI] [PubMed] [Google Scholar]
  47. WALKER W. G., DICKERMAN H., JOST L. J. MECHANISM OF LYSINE-INDUCED KALIURESIS. Am J Physiol. 1964 Feb;206:409–414. doi: 10.1152/ajplegacy.1964.206.2.409. [DOI] [PubMed] [Google Scholar]
  48. Yuasa S., Urakabe S., Kimura G., Shirai D., Takamitsu Y. Effect of colchicine on the osmotic water flow across the toad urinary bladder. Biochim Biophys Acta. 1975 Dec 1;413(2):277–282. doi: 10.1016/0005-2736(75)90112-1. [DOI] [PubMed] [Google Scholar]
  49. Yunice A. A., King R. W., Jr, Kraikitpanitch S., Haygood C. C., Lindeman R. D. Urinary zinc excretion following infusions of zinc sulfate, cysteine, histidine, or glycine. Am J Physiol. 1978 Jul;235(1):F40–F45. doi: 10.1152/ajprenal.1978.235.1.F40. [DOI] [PubMed] [Google Scholar]
  50. Zusman R. M., Keiser H. R., Handler J. S. Vasopressin-stimulated prostaglandin E biosynthesis in the toad urinary bladder. Effect of water flow. J Clin Invest. 1977 Dec;60(6):1339–1347. doi: 10.1172/JCI108893. [DOI] [PMC free article] [PubMed] [Google Scholar]

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