Expression of a dominant negative PKA mutation in the kidney elicits a diabetes insipidus phenotype

American Journal of Physiology - Renal Physiology

Volumn 308, Issue 6, 2015, Pages F627-F638

  Gilbert, Merle L ^a   Yang, Linghai ^a   Su, Thomas ^a   McKnight, G Stanley ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Aquaporin 2; Arginine vasopressin; cAMP; Principal cell; Protein kinase A

Indexed keywords

AQUAPORIN 2; ARGIPRESSIN; CRE RECOMBINASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; MESSENGER RNA; PHOSPHOTRANSFERASE; PROTEIN RIALPHAB; UNCLASSIFIED DRUG; VASOPRESSIN V2 RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; VASOPRESSIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CONTROLLED STUDY; DIABETES INSIPIDUS; DIURESIS; ENZYME INHIBITION; FEMALE; GENE; HOMEOSTASIS; HORMONE RELEASE; HYPOTHALAMUS; MALE; MOUSE; MUTATION; NONHUMAN; PHENOTYPE; POLYURIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SIM1 GENE; TRANSCRIPTION REGULATION; WATER ABSORPTION; ANIMAL; DISEASE MODEL; ELECTROLYTE BALANCE; GENETICS; KIDNEY; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; AQUAPORIN 2; ARGININE VASOPRESSIN; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIALPHA SUBUNIT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIABETES INSIPIDUS; DISEASE MODELS, ANIMAL; HYPOTHALAMUS; KIDNEY; MICE; MICE, TRANSGENIC; PHENOTYPE; RECEPTORS, VASOPRESSIN; WATER-ELECTROLYTE BALANCE;

EID: 84930894642     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00222.2014     Document Type: Article

References (64)

1. Amieux PS, Cummings DE, Motamed K, Brandon EP, Wailes LA, Le K, Idzerda RL, McKnight GS. Compensatory regulation of RIalpha protein levels in protein kinase A mutant mice. J Biol Chem 272: 3993–3998, 1997.
2. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, Williams T, Ferreira M, Tang V, McGovern RA, Kenny CD, Christiansen LM, Edelstein E, Choi B, Boss O, Aschkenasi C, Zhang CY, Mountjoy K, Kishi T, Elmquist JK, Lowell BB. Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123: 493–505, 2005.
3. Bouley R, Hasler U, Lu HA, Nunes P, Brown D. Bypassing vasopressin receptor signaling pathways in nephrogenic diabetes insipidus. Semin Nephrol 28: 266–278, 2008.
4. Bouley R, Lu HA, Nunes P, Da Silva N, McLaughlin M, Chen Y, Brown D. Calcitonin has a vasopressin-like effect on aquaporin-2 trafficking and urinary concentration. J Am Soc Nephrol 22: 59–72, 2011.
5. Bourque CW. Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 9: 519–531, 2008.
6. Brown RL, August SL, Williams CJ, Moss SB. AKAP7α is a nuclear RI-binding AKAP. Biochem Biophys Res Commun 306: 394–401, 2003.
7. Burton KA, Johnson BD, Hausken ZE, Westenbroek RE, Idzerda RL, Scheuer T, Scott JD, Catterall WA, McKnight GS. Type II regulatory subunits are not required for the anchoring-dependent modulation of Ca2+ channel activity by cAMP-dependent protein kinase. Proc Natl Acad Sci USA 94: 11067–11072, 1997.
8. Carter DA, Murphy D. Cyclic nucleotide dynamics in the rat hypothalamus during osmotic stimulation: in vivo and in vitro studies. Brain Res 487: 350–356, 1989.
9. Chiappini F, Cunha LL, Harris JC, Hollenberg AN. Lack of cAMPresponse element-binding protein 1 in the hypothalamus causes obesity. J Biol Chem 286: 8094–8105, 2011.
10. Chou CL, Yip KP, Michea L, Kador K, Ferraris JD, Wade JB, Knepper MA. Regulation of aquaporin-2 trafficking by vasopressin in the renal collecting duct. Roles of ryanodine-sensitive Ca2+ stores and calmodulin. J Biol Chem 275: 36839–36846, 2000.
11. Clegg CH, Correll LA, Cadd GG, McKnight GS. Inhibition of intracellular cAMP-dependent protein kinase using mutant genes of the regulatory type I subunit. J Biol Chem 262: 13111–13119, 1987.
12. Cowley MA, Pronchuk N, Fan W, Dinulescu DM, Colmers WF, Cone RD. Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus: evidence of a cellular basis for the adipostat. Neuron 24: 155–163, 1999.
13. Cummings DE, Brandon EP, Planas JV, Motamed K, Idzerda RL, McKnight GS. Genetically lean mice result from targeted disruption of the RII β subunit of protein kinase A. Nature 382: 622–626, 1996.
14. Day ME, Gaietta GM, Sastri M, Koller A, Mackey MR, Scott JD, Perkins GA, Ellisman MH, Taylor SS. Isoform-specific targeting of PKA to multivesicular bodies. J Cell Biol 193: 347–363, 2011.
15. DiGiovanni SR, Nielsen S, Christensen EI, Knepper MA. Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat. Proc Natl Acad Sci USA 91: 8984–8988, 1994.
16. Ema M, Morita M, Ikawa S, Tanaka M, Matsuda Y, Gotoh O, Saijoh Y, Fujii H, Hamada H, Kikuchi Y, Fujii-Kuriyama Y. Two new members of the murine Sim gene family are transcriptional repressors and show different expression patterns during mouse embryogenesis. Mol Cell Biol 16: 5865–5875, 1996.
17. Fenton RA, Knepper MA. Mouse models and the urinary concentrating mechanism in the new millennium. Physiol Rev 87: 1083–1112, 2007.
18. Frokiaer J, Marples D, Valtin H, Morris JF, Knepper MA, Nielsen S. Low aquaporin-2 levels in polyuric DI +/+ severe mice with constitutively high cAMP-phosphodiesterase activity. Am J Physiol Renal Physiol 276: F179–F190, 1999.
19. Fushimi K, Sasaki S, Marumo F. Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J Biol Chem 272: 14800–14804, 1997.
20. Greenwood M, Bordieri L, Greenwood MP, Rosso Melo M, Colombari DS, Colombari E, Paton JF, Murphy D. Transcription factor CREB3L1 regulates vasopressin gene expression in the rat hypothalamus. J Neurosci 34: 3810–3820, 2014.
21. 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 94: 1778–1783, 1994.
22. Henn V, Edemir B, Stefan E, Wiesner B, Lorenz D, Theilig F, Schmitt R, Vossebein L, Tamma G, Beyermann M, Krause E, Herberg FW, Valenti G, Bachmann S, Rosenthal W, Klussmann E. Identification of a novel A-kinase anchoring protein 18 isoform and evidence for its role in the vasopressin-induced aquaporin-2 shuttle in renal principal cells. J Biol Chem 279: 26654–26665, 2004.
23. Hoffert JD, Fenton RA, Moeller HB, Simons B, Tchapyjnikov D, McDill BW, Yu MJ, Pisitkun T, Chen F, Knepper MA. Vasopressinstimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J Biol Chem 283: 24617–24627, 2008.
24. Homma S, Gapstur SM, Coffey A, Valtin H, Dousa TP. Role of cAMP-phosphodiesterase isozymes in pathogenesis of murine nephrogenic diabetes insipidus. Am J Physiol Renal Fluid Electrolyte Physiol 261: F345–F353, 1991.
25. Howe DG, Clarke CM, Yan H, Willis BS, Schneider DA, McKnight GS, Kapur RP. Inhibition of protein kinase A in murine enteric neurons causes lethal intestinal pseudo-obstruction. J Neurobiol 66: 256–272, 2006.
26. Hozawa S, Holtzman EJ, Ausiello DA. cAMP motifs regulating transcription in the aquaporin 2 gene. Am J Physiol Cell Physiol 270: C1695–C1702, 1996.
27. Iwasaki Y, Oiso Y, Saito H, Majzoub JA. Positive and negative regulation of the rat vasopressin gene promoter. Endocrinology 138: 5266–5274, 1997.
28. Jo I, Ward DT, Baum MA, Scott JD, Coghlan VM, Hammond TG, Harris HW. AQP2 is a substrate for endogenous PP2B activity within an inner medullary AKAP-signaling complex. Am J Physiol Renal Physiol 281: F958–F965, 2001.
29. Klussmann E, Maric K, Wiesner B, Beyermann M, Rosenthal W. Protein kinase A anchoring proteins are required for vasopressin-mediated translocation of aquaporin-2 into cell membranes of renal principal cells. J Biol Chem 274: 4934–4938, 1999.
30. Lam AK, Ko BC, Tam S, Morris R, Yang JY, Chung SK, Chung SS. Osmotic response element-binding protein (OREBP) is an essential regulator of the urine concentrating mechanism. J Biol Chem 279: 48048–48054, 2004.
31. Lande MB, Jo I, Zeidel ML, Somers M, Harris HW Jr. Phosphorylation of aquaporin-2 does not alter the membrane water permeability of rat papillary water channel-containing vesicles. J Biol Chem 271: 5552–5557, 1996.
32. Lankford SP, Chou CL, Terada Y, Wall SM, Wade JB, Knepper MA. Regulation of collecting duct water permeability independent of cAMPmediated AVP response. Am J Physiol Renal Fluid Electrolyte Physiol 261: F554–F566, 1991.
33. Li JH, Chou CL, Li B, Gavrilova O, Eisner C, Schnermann J, Anderson SA, Deng CX, Knepper MA, Wess J. A selective EP4 PGE2 receptor agonist alleviates disease in a new mouse model of X-linked nephrogenic diabetes insipidus. J Clin Invest 119: 3115–3126, 2009.
34. Li SZ, McDill BW, Kovach PA, Ding L, Go WY, Ho SN, Chen F. Calcineurin-NFATc signaling pathway regulates AQP2 expression in response to calcium signals and osmotic stress. Am J Physiol Cell Physiol 292: C1606–C1616, 2007.
35. Lubelski D, Ponzio TA, Gainer H. Effects of A-CREB, a dominant negative inhibitor of CREB, on the expression of c-fos and other immediate early genes in the rat SON during hyperosmotic stimulation in vivo. Brain Res 1429: 18–28, 2012.
36. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133–140, 2010.
37. Matsumura Y, Uchida S, Rai T, Sasaki S, Marumo F. Transcriptional regulation of aquaporin-2 water channel gene by cAMP. J Am Soc Nephrol 8: 861–867, 1997.
38. McDill BW, Li SZ, Kovach PA, Ding L, Chen F. Congenital progressive hydronephrosis (cph) is caused by an S256L mutation in aquaporin-2 that affects its phosphorylation and apical membrane accumulation. Proc Natl Acad Sci USA 103: 6952–6957, 2006.
39. McKnight GS. Cyclic AMP second messenger systems. Curr Opin Cell Biol 3: 213–217, 1991.
40. Michaud JL, Rosenquist T, May NR, Fan CM. Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. Genes Dev 12: 3264–3275, 1998.
41. Moeller HB, Praetorius J, Rutzler MR, Fenton RA. Phosphorylation of aquaporin-2 regulates its endocytosis and protein-protein interactions. Proc Natl Acad Sci USA 107: 424–429, 2010.
42. Murakami T, Kondo S, Ogata M, Kanemoto S, Saito A, Wanaka A, Imaizumi K. Cleavage of the membrane-bound transcription factor OASIS in response to endoplasmic reticulum stress. J Neurochem 96: 1090–1100, 2006.
43. Nedvetsky PI, Tabor V, Tamma G, Beulshausen S, Skroblin P, Kirschner A, Mutig K, Boltzen M, Petrucci O, Vossenkamper A, Wiesner B, Bachmann S, Rosenthal W, Klussmann E. Reciprocal regulation of aquaporin-2 abundance and degradation by protein kinase A and p38-MAP kinase. J Am Soc Nephrol 21: 1645–1656, 2010.
44. Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA. Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92: 1013–1017, 1995.
45. Noda Y, Horikawa S, Kanda E, Yamashita M, Meng H, Eto K, Li Y, Kuwahara M, Hirai K, Pack C, Kinjo M, Okabe S, Sasaki S. Reciprocal interaction with G-actin and tropomyosin is essential for aquaporin-2 trafficking. J Cell Biol 182: 587–601, 2008.
46. Nonoguchi H, Owada A, Kobayashi N, Takayama M, Terada Y, Koike J, Ujiie K, Marumo F, Sakai T, Tomita K. Immunohistochemical localization of V2 vasopressin receptor along the nephron and functional role of luminal V2 receptor in terminal inner medullary collecting ducts. J Clin Invest 96: 1768–1778, 1995.
47. Okutsu R, Rai T, Kikuchi A, Ohno M, Uchida K, Sasaki S, Uchida S. AKAP220 colocalizes with AQP2 in the inner medullary collecting ducts. Kidney Int 74: 1429–1433, 2008.
48. Rieg T, Pothula K, Schroth J, Satriano J, Osswald H, Schnermann J, Insel PA, Bundey RA, Vallon V. Vasopressin regulation of inner medullary collecting ducts and compensatory changes in mice lacking adenosine A1 receptors. Am J Physiol Renal Physiol 294: F638–F644, 2008.
49. Rieg T, Tang T, Murray F, Schroth J, Insel PA, Fenton RA, Hammond HK, Vallon V. Adenylate cyclase 6 determines cAMP formation and aquaporin-2 phosphorylation and trafficking in inner medulla. J Am Soc Nephrol 21: 2059–2068, 2010.
50. Rood BD, De Vries GJ. Vasopressin innervation of the mouse (Mus musculus) brain and spinal cord. J Comp Neurol 519: 2434–2474, 2011.
51. Sanz E, Evanoff R, Quintana A, Evans E, Miller JA, Ko C, Amieux PS, Griswold MD, McKnight GS. RiboTag analysis of actively translated mRNAs in Sertoli and Leydig cells in vivo. PLos One 8: e66179, 2013.
52. Sanz E, Yang L, Su T, Morris DR, McKnight GS, Amieux PS. Cell-type-specific isolation of ribosome-associated mRNA from complex tissues. Proc Natl Acad Sci USA 106: 13939–13944, 2009.
53. Simon H, Gao Y, Franki N, Hays RM. Vasopressin depolymerizes apical F-actin in rat inner medullary collecting duct. Am J Physiol Cell Physiol 265: C757–C762, 1993.
54. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70–71, 1999.
55. Spandidos A, Wang X, Wang H, Seed B. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38: D792–D799, 2010.
56. Steinberg RA, Russell JL, Murphy CS, Yphantis DA. Activation of type I cyclic AMP-dependent protein kinases with defective cyclic AMPbinding sites. J Biol Chem 262: 2664–2671, 1987.
57. 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.
58. Tamma G, Klussmann E, Maric K, Aktories K, Svelto M, Rosenthal W, Valenti G. Rho inhibits cAMP-induced translocation of aquaporin-2 into the apical membrane of renal cells. Am J Physiol Renal Physiol 281: F1092–F1101, 2001.
59. Tamma G, Klussmann E, Procino G, Svelto M, Rosenthal W, Valenti G. cAMP-induced AQP2 translocation is associated with RhoA inhibition through RhoA phosphorylation and interaction with RhoGDI. J Cell Sci 116: 1519–1525, 2003.
60. Willis BS, Niswender CM, Su T, Amieux PS, McKnight GS. Cell-type specific expression of a dominant negative PKA mutation in mice. PLos One 6: e18772, 2011.
61. Wong LF, Harding T, Uney J, Murphy D. cAMP-dependent protein kinase A mediation of vasopressin gene expression in the hypothalamus of the osmotically challenged rat. Mol Cell Neurosci 24: 82–90, 2003.
62. Woodford TA, Correll LA, McKnight GS, Corbin JD. Expression and characterization of mutant forms of the type I regulatory subunit of cAMP-dependent protein kinase. The effect of defective cAMP binding on holoenzyme activation. J Biol Chem 264: 13321–13328, 1989.
63. Yano Y, Cesar KR, Araujo M, Rodrigues AC Jr, Andrade LC, Magaldi AJ. Aquaporin 2 expression increased by glucagon in normal rat inner medullary collecting ducts. Am J Physiol Renal Physiol 296: F54–F59, 2009.
64. Yasui M, Zelenin SM, Celsi G, Aperia A. Adenylate cyclase-coupled vasopressin receptor activates AQP2 promoter via a dual effect on CRE and AP1 elements. Am J Physiol Renal Physiol 272: F443–F450, 1997.