Urinary Excretion of Aquaporin-2 and Inappropriate Secretion of Vasopressin in Hyponatremic Patients after Cerebral Infarction

 

 Buy Article Permissions and Reprints

Abstract

Aquaporin-2, a water-channel protein, is known to increase water permeability due to vasopressin binding to V2 receptors at the renal collecting duct and is excreted into the urine. It is still unclear whether a hyponatremic state is caused by vasopressin-dependent aquaporin-2 in patients clinically diagnosed with the syndrome of inappropriate secretion of antidiuretic hormone. To determine this, we measured urinary aquaporin-2 and vasopressin by radioimmunoassay in normonatremic or hyponatremic patients after cerebral infarction and in healthy controls. In the normonatremia group, urinary aquaporin-2 and plasma AVP levels were higher than in controls. In the hyponatremia group, plasma AVP was relatively high despite low plasma osmolality in each patient. However, urinary aquaporin-2 in hyponatremia was significantly increased when compared with the other two groups. In conclusion, AQP-2 increment does not directly reflect non-osmotic AVP secretion in a hyponatremic state. This result indicates that the urinary excretion of AQP-2 is not only AVP-dependent in hyponatremic states.

References

• 1 Sasaki S, Fushimi K, Saito H, Saito F, Uchida S, Ishibashi K, Kuwahara M, Ikeuchi T, Inui K, Nakajima K, Watanabe T X, Marumo F. Cloning characterization and chromosomal mapping of human aquaporin of collecting duct.  J Clin Invest. 1994;  93 1250-1256
  PubMedGoogle Scholar
• 2 Fushimi K, Uchida S, Hara Y, Hirata Y, Marumo F, Sasaki S. Cloning and expression of apical membrane water channel of rat kidney collecting tubule.  Nature. 1993;  361 549-552
  CrossrefPubMedGoogle Scholar
• 3 Hayashi M, Sasaki S, Tsuganezawa H, Monkawa T, Kitajima W, Konishi K, Fushimi K, Marumo F, Saruta T. Expression and distribution of aquaporin of collecting duct are regulated by vasopressin V2 receptor in rat kidney.  J Clin Invest. 1999;  94 1778-1783
  PubMedGoogle Scholar
• 4 Hochberg Z, van Lieburg A, Even L, Brenner B, Lanir N, van Oost B A, Knoers N V. Autosomal recessive nephrogenic insipidus caused by aquaporin-2 mutation.  J Clin Endocr Metab. 1997;  82 686-689
  CrossrefPubMedGoogle Scholar
• 5 Deen P MT, Verdijk M AJ, Knoers N VAM, Wieringa B, Monnens L AH, van Os C H, van Oost B A. Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine.  Science. 1994;  264 92-95
  PubMedGoogle Scholar
• 6 van Lieburg A F, Verdijk M AJ, Knoers N VAM, van Essen A J, Proesmans W, Mallmann R, Monnens L AH, van Oost B A, van Os C H, Deen P MT. Patients with autosomal nephrogenic diabetes insipidus homozygous for mutations in the aquaporin 2 water-channel gene.  Am J Hum Genet. 1994;  55 648-652
  PubMedGoogle Scholar
• 7 Mulders S M, Bichet D G, Rijss J PL, Kamsteeg E-J, Françoise M-F, Lonergan M, Fujiwara M, Morgan K, Leijendekker R, van der Sluijs P, van Os C H, Deen P MT. An aquaporin-2 water channel mutant which causes autosomal dominant nephrogenic diabetes insipidus is retained in the Golgi complex.  J Clin Invest. 1998;  102 57-66
  PubMedGoogle Scholar
• 8 Kanno K, Sasaki S, Hirata Y, Ishikawa S, Fushimi K, Nakanishi S , Bichet D G, Marumo F. Urinary excretion of AQP-2 in patients with diabetes insipidus.  New Engl J Med. 1995;  332 1540-1545
  CrossrefPubMedGoogle Scholar
• 9 Saito T, Ishikawa S, Sasaki S, Nakamura T, Rokkaku K, Kawakami A, Honda K, Marumo F, Saito T. Urinary excretion of aquaporin-2 in the diagnosis of central diabetes insipidus.  J Clin Endocr Metab. 1997;  82 1823-1827
  CrossrefPubMedGoogle Scholar
• 10 Fujita N, Ishikawa S, Sasaki S, Fujisawa G, Fushimi K, Marumo F, Saito T. Role of water channel AQP-CD in water retention in SIADH and cirrhotic rats.  Am J Physiol. 1995;  269 F926-931
  PubMedGoogle Scholar
• 11 Xu L, Martin P-Y, Ohara M, John J, Pattison T, Meng X, Morris K, Kim J K, Schrier R W. Upregulation of aquaporin-2 water channel expression in chronic heart failure rat.  J Clin Invest. 1997;  99 1500-1505
  PubMedGoogle Scholar
• 12 Murase T, Ecelbarger C A, Baker E A, Tian Y, Knepper M A, Verbalis J G. Kidney aquaporin-2 expression during escape from antidiuresis is not related to plasma or tissue osmolality.  J Am Soc Nephrol. 1999;  10 2067-2075
  PubMedGoogle Scholar
• 13 Kamoi K, Toyama M, Ishibashi M, Yamaji T. Hyponatremia and osmotic regulation of vasopressin secretion in patients with intracranial bleeding.  J Clin Endocr Metab. 1995;  80 2906-2911
  CrossrefPubMedGoogle Scholar
• 14 Kamoi K, Toyoma M, Takagi M, Nishiyama K, Takahashi K, Sasaki H, Muto T. Osmoregulation of vasopressin secretion in patients with the syndrome of inappropriate antidiuresis associated with central nervous system disorders.  Endocr J. 1999;  46 269-277
  PubMedGoogle Scholar
• 15 Schwartz W B, Bennett W, Curelop S, Bartter F C. A syndrome of renal sodium loss and hyponatremia probably resulting from inappropriate secretion of antidiuretic hormone.  Am J Med. 1987;  23 529-542
  PubMedGoogle Scholar
• 16 Mitsuma T, Takagi J, Otake K, Kayama Y, Adachi T, Nogimori T, Sakai J, Hirooka Y. Radioimmunoassay for aquaporin-2.  Endocr Regul. 1998;  32 141-144
  PubMedGoogle Scholar
• 17 Rai T, Sekine K, Kanno K, Hata K, Miura M, Mizushima A, Marumo F, Sasaki S. Urinary excretion of aquaporin-2 water channel protein in human and rat.  J Am Soc Nephrol. 1997;  8 1357-1362
  PubMedGoogle Scholar
• 18 Elliot S, Goldsmith P, Knepper M, Haughey M, Olsen B. Urinary excretion of aquaporin-2 in humans: A potential marker of collecting duct responsiveness to vasopressin.  J Am Soc Nephrol. 1996;  7 403-409
  PubMedGoogle Scholar
• 19 Martin P-Y, Abraham W T, Xu L, Olson B R, Oren R M, Ohara M, Shrier R W. Selective V2-receptor vasopressin antagonism decreases urinary aquaporin-2 excretion in patients with chronic heart failure.  J Am Soc Nephrol. 1999;  10 2165-2170
  PubMedGoogle Scholar
• 20 Olsson J-E, Forsling M L, Lindvall B, Åkerlund M. Cerebrospinal fluid arginine vasopressin in Parkinson's disease, dementia, and other degenerative disorders.  Adv Neurol. 1986;  45 239-242
  PubMedGoogle Scholar
• 21 Joint R J, Feibel J H, Sladek C M. Antidiuretic hormone levels in stroke patients.  Ann Neurol. 1981;  9 182-184
  CrossrefPubMedGoogle Scholar
• 22 Zbigniew M R, Jolanta C M. Vasopressin concentration in the blood during acute short-term intracranial hypertension in cats.  Adv Neurol. 1978;  20 381-388
  PubMedGoogle Scholar
• 23 Sørensen P S, Gjerris A, Hammer M. Cerebrospinal fluid vasopressin in neurological and psychiatric disorders.  J Neurol Neurosurg Psychiat. 1985;  48 50-57
  PubMedGoogle Scholar
• 24 Gaufin L, Skowsky W R, Goodman S J. Release of antidiuretic hormone during mass-induced elevation of intracranial pressure.  J Neurosurg. 1977;  46 627-637
  PubMedGoogle Scholar
• 25 Schrier R W, Berl T, Anderson R J. Osmotic and non-osmotic control of vasopressin release.  Am J Physiol. 1979;  236 F321-F332
  PubMedGoogle Scholar
• 26 Saito T, Ishikawa S, Sasaki S, Fujita N, Fushimi K, Okada K, Takeuchi K, Sakamoto A, Ookawara S, Kaneko T, Marumo F, Saito T. Alteration in water channel AQP-2 by removal of AVP stimulation in collecting duct cells of dehydrated rats.  Am J Physiol. 1997;  272 F183-F191
  PubMedGoogle Scholar
• 27 Nielsen S, Chou C-L, Marples D, Christensen E I, Kishore B K, Knepper M A. Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane.  Proc Natl Acad Sci USA. 1995;  92 1013-1017
  PubMedGoogle Scholar
• 28 DiGiovanni S R, Nielsen S, Christensen E I, Knepper M A. Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat.  Proc Natl Acad Sci USA. 1994;  91 8984-8988
  PubMedGoogle Scholar
• 29 Saito T, Ishikawa S, Sasaki S, Higashiyama M, Nagasaki S, Fujita N, Fushimi K, Marumo F, Saito T. Lack of vasopressin upregulation of AQP-2 gene expression in homozygous Brattleboro rats.  Am J Physiol. 1999;  277 R427-433
  PubMedGoogle Scholar
• 30 Wen H, Frøkiaer J, Kwon T H, Nielsen S. Urinary excretion of aquaporin-2 in rat is mediated by vasopressin-dependent apical pathway.  J Am Soc Nephrol. 1999;  10 1416-1429
  PubMedGoogle Scholar
• 31 Baumgarten R, van de Pol M HJ, Deen P MT, van Os C H, Werzels J FM. Dissociation between urinary excretion of aquaporin-2 and vasopressin action in healthy volunteers.  J Am Nephrol Soc Abstract A0077. 1998;  9 15A
  PubMedGoogle Scholar
• 32 Buemi M, Corica F, di Pasquale G, Aloisi C, Sofi M, Casuscelli T, Floccari F, Senatore M, Corsonello A, Frisina N. Water immersion increase urinary excretion of aquaporin-2 in healthy humans.  Nephron. 2000;  85 20-26
  CrossrefPubMedGoogle Scholar
• 33 Conte G, Bellizzi V, Cianciaruso B, Minutolo R, Fuiano G, de Nicola L. Physiologic role and diuretic efficacy of atrial natriuretic peptide in health and chronic renal disease.  Kidney Int. 1997;  51 S28-32
  PubMedGoogle Scholar
• 34 Nonoguchi H, Sands J M, Knepper M A. Atrial natriuretic factor inhibits vasopressin-stimulated osmotic water permeability in rat inner medullary collecting duct.  J Clin Invest. 1988;  88 1383-1390
  PubMedGoogle Scholar
• 35 Naruse S, Aoki Y, Takei R, Horikawa Y, Ueda S. Effect of atrial natriuretic peptide on ischemic brain edema in rats evaluated by proton magnetic resonance method.  Stroke. 1991;  22 61-65
  PubMedGoogle Scholar
• 36 Estrada V, Tellez M J, Moya J, Fernandez-Durango R, Egido J, Cruz A F. High plasma levels of endothelin-1 and atrial natriuretic peptide in patients with acute ischemic stroke.  Am J Hypertension. 1994;  7 1085-1089
  PubMedGoogle Scholar
• 37 Weinand M E, O'Boynick P L, Goetz K L. A study of serum antidiuretic hormone and atrial natriuretic peptide levels in series of patients with intracranial disease and hyponatremia.  Neurosurgery. 1989;  25 781-785
  PubMedGoogle Scholar
• 38 Kamoi K, Ebe T, Kobayashi O, Ishida M, Sato F, Arai O, Tamura T, Takagi A, Yamada A, Ishibashi M, Yamaji T. Atrial natriuretic peptide in patients with the syndrome of inappropriate antidiuretic hormone secretion and with diabetes insipidus.  J Clin Endocrinol Metab. 1990;  70 1385-1390
  PubMedGoogle Scholar
• 39 Frigeri A, Gropper M A, Umenishi F, Kawashima M, Brown D, Verkman A S. Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial, and glandular tissues.  J Cell Sci. 1995;  108 2993-3002
  PubMedGoogle Scholar
• 40 Terris J, Ecelbarger C A, Nielsen S, Knepper M A. Long-term regulation of four renal aquaporins in rats.  Am J Physiol. 1996;  271 F414-422
  PubMedGoogle Scholar
• 41 Ecelbarger C A, Terris J, Frindt G, Echevarria M, Marples D, Nielsen S, Knepper M A. Aquaporin-3 water channel localization and regulation in rat kidney.  Am J Physiol. 1995;  269 F663-672
  PubMedGoogle Scholar
• 42 Fernandez-Llama P, Turner R, Dibona G, Knepper M A. Renal expression of aquaporins in liver cirrhosis induced by chronic common bile duct ligation in rats.  J Am Soc Nephrol. 1999;  10 1950-1957
  PubMedGoogle Scholar
• 43 Tsuboi Y, Ishikawa S, Fujisawa G, Okada K, Saito T. Therapeutic efficacy of the non-peptide AVP antagonist OPC-31 260 in cirrhotic rats.  Kidney Int. 1994;  46 237-244
  PubMedGoogle Scholar
• 44 O'Neill P A, Davies I, Fullerton K J, Bennett D. Fluid balance in elderly patients following acute stroke.  Age Ageing. 1992;  21 280-285
  PubMedGoogle Scholar
• 45 Ayus J C, Krothapalli R, Arieff A I. Treatment of symptomatic hyponatremia and its relation to brain damage.  New Engl J Med. 1987;  317 1190-1195
  PubMedGoogle Scholar

J. Takagi

Department of Laboratory Medicine · Aichi Medical University ·

21-Karimata, Nagakute · Aichi 480-1195 · Japan ·

Phone: + 81 (561) 62-3311 (ext. 2115) ·

Fax: + 81 (561) 62-3075

Email: jutakagi@aichi-med-u.ac.jp