Aquaporin-2 downregulation in kidney medulla of aging rats is posttranscriptional and is abolished by water deprivation

American Journal of Physiology - Renal Physiology

Volumn 294, Issue 6, 2008, Pages

  Combet, S ^a,b,c   Gouraud, S ^a,b,g   Gobin, R ^a,b   Berthonaud, V ^a,b   Geelen, G ^d,e   Corman, B ^a,f   Verbavatz, J M ^a,b,c  

^a SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c CEA SACLAY   (France)

^d UNIVERSITÉ LYON 1   (France)

^e CROIX ROUSSE HOSPITAL   (France)

^f Successful aging database   (France)

^g WAKAYAMA MEDICAL UNIVERSITY   (Japan)

Author keywords

Aquaporins; AVP; cAMP; cGMP; Phosphorylated AQP2; Urine concentration

Indexed keywords

AQUAPORIN 2; ARGIPRESSIN; AQP2 PROTEIN, RAT; CYCLIC AMP; CYCLIC GMP; MESSENGER RNA;

AGING; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; FLUID BALANCE; KIDNEY MEDULLA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; URINE FLOW RATE; URINE OSMOLALITY; WATER DEPRIVATION; ANIMAL; DOWN REGULATION; ELECTROLYTE BALANCE; GENETICS; KIDNEY CONCENTRATING CAPACITY; METABOLISM; OSMOLARITY; PHOSPHORYLATION; PHYSIOLOGY; RAT STRAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING;

AGING; ANIMALS; AQUAPORIN 2; CYCLIC AMP; CYCLIC GMP; DOWN-REGULATION; FEMALE; KIDNEY CONCENTRATING ABILITY; KIDNEY MEDULLA; OSMOLAR CONCENTRATION; PHOSPHORYLATION; RATS; RATS, INBRED STRAINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; WATER DEPRIVATION; WATER-ELECTROLYTE BALANCE;

EID: 48249126472     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00437.2007     Document Type: Article

References (50)

1. Apostol E, Ecelbarger CA, Terris J, Bradford AD, Andrews P, Knepper MA. Reduced renal medullary water channel expression in puromycin aminonucleoside-induced nephrotic syndrome. J Am Soc Nephrol 8: 15-24, 1997.
2. Baylis C, Corman B. The aging kidney: insights from experimental studies. J Am Soc Nephrol 9: 699-709, 1998.
3. Bengele HH, Mathias RS, Perkins JH, Alexander EA. Urinary concentrating defect in the aged rat. Am J Physiol Renal Fluid Electrolyte Physiol 240: F147-F150, 1981.
4. Bia MJ, Dewitt S, Forrest JN Jr. Dissociation between plasma, urine, and renal papillary cyclic AMP content following vasopressin and DDAVP. Am J Physiol Renal Fluid Electrolyte Physiol 237: F218-F225, 1979.
5. Bouley R, Breton S, Sun T, McLaughlin M, Nsumu NN, Lin HY, Ausiello DA, Brown D. Nitric oxide and atrial natriuretic factor stimulate cGMP-dependent membrane insertion of aquaporin 2 in renal epithelial cells. J Clin Invest 106: 1115-1126, 2000.
6. Brockmann R, Beyer A, Heinisch JJ, Wilhelm T. Posttranscriptional expression regulation: what determines translation rates? PLoS Comput Biol 3: 531-539, 2007.
7. Catudioc-Vallero J, Sands JM, Klein JD, Sidorowicz HE, Sladek CD. Effect of age and testosterone on the vasopressin and aquaporin responses to dehydration in Fischer 344/Brown-Norway F1 rats. J Gerontol A Biol Sci Med Sci 55: B26-B34, 2000.
8. 2-receptor agonist/antagonist treatment. Am J Physiol Renal Physiol 278: F29-F42, 2000.
9. Christensen S. Dissociation between antidiuretic response and renal medullary cyclic AMP levels in the rat. Pflügers Arch 374: 229-234, 1978.
10. Coller J, Parker R. General translational repression by activators of mRNA decapping. Cell 122: 875-886, 2005.
11. Combet S, Teillet L, Geelen G, Pitrat B, Gobin R, Nielsen S, Trinh-Trang-Tan MM, Corman B, Verbavatz JM. Food restriction prevents age-related polyuria by vasopressin-dependent recruitment of aquaporin-2. Am J Physiol Renal Physiol 281: F1123-F1131, 2001.
12. Combet S, Geffroy N, Berthonaud V, Dick B, Teillet L, Verbavatz JM, Corman B, Trinh-Trang-Tan MM. Correction of age-related polyuria by dDAVP: molecular analysis of aquaporins and urea transporters. Am J Physiol Renal Physiol 284: F199-F208, 2003.
13. Corman B, Michel JB. Glomerular filtration, renal blood flow, and solute excretion in conscious aging rats. Am J Physiol Regul Integr Comp Physiol 253: R555-R560, 1987.
14. Donahue JL, Lowenthal DT. Nocturnal polyuria in the elderly person. Am J Med Sci 314: 232-238, 1997.
15. Eikmans M, Baelde HJ, de Heer E, Bruijn JA. Effect of age and biopsy site on extracellular matrix mRNA and protein levels in human kidney biopsies. Kidney Int 60: 974-981, 2001.
16. Furuno M, Uchida S, Marumo F, Sasaki S. Repressive regulation of the aquaporin-2 gene. Am J Physiol Renal Fluid Electrolyte Physiol 271: F854-F860, 1996.
17. Geelen G, Corman B. Relationship between vasopressin and renal concentrating ability in aging rats. Am J Physiol Regul Integr Comp Physiol 262: R826-R833, 1992.
18. Gouraud SS, Heesom K, Yao ST, Qiu J, Paton JF, Murphy D. Dehydration-induced proteome changes in the rat hypothalamo-neurohypophyseal system. Endocrinology 148: 3041-3052, 2007.
19. Gouraud SS, Yao ST, Heesom KJ, Paton JF, Murphy D. 14-3-3 Proteins within the hypothalamic-neurohypophyseal system of the osmotically stressed rat: transcriptomic and proteomic studies. J Neuroendocrinol 19: 913-922, 2007.
20. Hasler U, Mordasini D, Bens M, Bianchi M, Cluzeaud F, Rousselot M, Vandewalle A, Feraille E, Martin PY. Long term regulation of aquaporin-2 expression in vasopressin-responsive renal collecting duct principal cells. J Biol Chem 277: 10379-10386, 2002.
21. Hasler U, Vinciguerra M, Vandewalle A, Martin PY, Feraille E. Dual effects of hypertonicity on aquaporin-2 expression in cultured renal collecting duct principal cells. J Am Soc Nephrol 16: 1571-1582, 2005.
22. Hasler U, Nielsen S, Feraille E, Martin PY. Posttranscriptional control of aquaporin-2 abundance by vasopressin in renal collecting duct principal cells. Am J Physiol Renal Physiol 290: F177-F187, 2006.
23. Ideker T, Thorsson V, Ranish JA, Christmas R, Buhler J, Eng JK, Bumgarner R, Goodlett DR, Aebersold R, Hood L. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292: 929-934, 2001.
24. Keil LC, Severs WB. Reduction in plasma vasopressin levels of dehydrated rats following acute stress. Endocrinology 100: 30-38, 1977.
25. Klingler C, Preisser L, Barrault MB, Lluel P, Horgen L, Teillet L, Ancellin N, Corman B. Vasopressin V2 receptor mRNA expression and cAMP accumulation in aging rat kidney. Am J Physiol Regul Integr Comp Physiol 272: R1775-R1782, 1997.
26. Knepper MA. Proteomics and the kidney. J Am Soc Nephrol 13: 1398-1408, 2002.
27. Marples D, Knepper MA, Christensen EI, Nielsen S. Redistribution of aquaporin-2 water channels induced by vasopressin in rat kidney inner medullary collecting duct. Am J Physiol Cell Physiol 269: C655-C664, 1995.
28. Marples D, Christensen BM, Frokiær J, Knepper MA, Nielsen S. Dehydration reverses vasopressin antagonist-induced diuresis and aquaporin-2 downregulation in rats. Am J Physiol Renal Physiol 275: F400-F409, 1998.
29. Michimata M, Nogae S, Ohta M, Kaizuma S, Imai Y, Ito S, Matsubara M. Topographic distribution of aquaporin 2 mRNA in the kidney of dehydrated rats. Exp Nephrol 8: 28-36, 2000.
30. Miller M. Nocturnal polyuria in older people: pathophysiology and clinical implications. J Am Geriatr Soc 48: 1321-1329, 2000.
31. Murillo-Carretero MI, Ilundain AA, Echevarria M. Regulation of aquaporin mRNA expression in rat kidney by water intake. J Am Soc Nephrol 10: 696-703, 1999.
32. Parker R, Sheth U. P bodies and the control of mRNA translation and degradation. Mol Cell 25: 635-646, 2007.
33. Pisitkun T, Bieniek J, Tchapyjnikov D, Wang G, Wu WW, Shen RF, Knepper MA. High-throughput identification of IMCD proteins using LC-MS/MS. Physiol Genomics 25: 263-276, 2006.
34. Pradelles P, Grassi J, Chabardes D, Guiso N. Enzyme immunoassays of adenosine cyclic 3′,5′-monophosphate and guanosine cyclic 3′,5′-monophosphate using acetylcholinesterase. Anal Chem 61: 447-453, 1989.
35. Preisser L, Teillet L, Aliotti S, Gobin R, Berthonaud V, Chevalier J, Corman B, Verbavatz JM. Downregulation of aquaporin-2 and -3 in aging kidney is independent of V2 vasopressin receptor. Am J Physiol Renal Physiol 279: F144-F152, 2000.
36. Preisser L, Houot L, Teillet L, Kortulewski T, Morel A, Tronik-Le Roux D, Corman B. Gene expression in aging kidney and pituitary. Biogerontology 5: 39-47, 2004.
37. Puliyanda DP, Ward DT, Baum MA, Hammond TG, Harris HW Jr. Calpain-mediated AQP2 proteolysis in inner medullary collecting duct. Biochem Biophys Res Commun 303: 52-58, 2003.
38. Rowe JW, Shock NW, DeFronzo RA. The influence of age on the renal response to water deprivation in man. Nephron 17: 270-278, 1976.
39. Roxas B, Farjah M, Danziger RS. Aquaporin-2 transcript is differentially regulated by dietary salt in Sprague-Dawley and Dahl SS/Jr rats. Biochem Biophys Res Commun 296: 755-778, 2002.
40. Sands JM, Flores FX, Kato A, Baum MA, Brown EM, Ward DT, Hebert SC, Harris HW. Vasopressin-elicited water and urea permeabilities are altered in IMCD in hypercalcemic rats. Am J Physiol Renal Physiol 274: F978-F985, 1998.
41. Singh K, Prasad S. Differential expression of Fmr-1 mRNA and FMRP in female mice brain during aging. Mol Biol Rep Sept. 2007 (online).
42. Storm R, Klussmann E, Geelhaar A, Rosenthal W, Maric K. Osmolality and solute composition are strong regulators of AQP2 expression in renal principal cells. Am J Physiol Renal Physiol 284: F189-F198, 2003.
43. Swenson KL, Sands JM, Jacobs JD, Sladek CD. Effect of aging on vasopressin and aquaporin responses to dehydration in Fischer 344-brown-Norway F1 rats. Am J Physiol Regul Integr Comp Physiol 273: R35-R40, 1997.
44. Terris J, Ecelbarger CA, Nielsen S, Knepper MA. Long-term regulation of four renal aquaporins in rats. Am J Physiol Renal Fluid Electrolyte Physiol 271: F414-F422, 1996.
45. Terwel D, ten Haaf JA, Markerink M, Jolles J. Changes in plasma vasopressin concentration and plasma osmolality in relation to age and time of day in the male Wistar rat. Acta Endocrinol 126: 357-362, 1992.
46. Tian Y, Serino R, Verbalis JG. Downregulation of renal vasopressin V2 receptor and aquaporin-2 expression parallels age-associated defects in urine concentration. Am J Physiol Renal Physiol 287: F797-F805, 2004.
47. Trinh-Trang-Tan MM, Geelen G, Teillet L, Corman B. Urea transporter expression in aging kidney and brain during dehydration. Am J Physiol Regul Integr Comp Physiol 285: R1355-R1365, 2003.
48. Umenishi F, Narikiyo T, Schrier RW. Effect on stability, degradation, expression, and targeting of aquaporin-2 water channel by hyperosmolality in renal epithelial cells. Biochem Biophys Res Commun 338: 1593-1599, 2005.
49. Wang KK, Villalobo A, Roufogalis BD. Calmodulin-binding proteins as calpain substrates. Biochem J 262: 693-706, 1989.
50. Wilson PD, Dillingham MA. Age-associated decrease in vasopressin-induced renal water transport: a role for adenylate cyclase and G protein malfunction. Gerontology 38: 315-321, 1992.