cAMP stimulates apical V-ATPase accumulation, microvillar elongation, and proton extrusion in kidney collecting duct A-intercalated cells

American Journal of Physiology - Renal Physiology

Volumn 298, Issue 3, 2010, Pages

  Pǎunescu, Teodor G ^a   Ljubojevic, Marija ^a   Russo, Leileata M ^a   Winter, Christian ^b   McLaughlin, Margaret M ^a   Wagner, Carsten A ^b   Breton, Sylvie ^a   Brown, Dennis ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Acid base sensing; Immunocytochemistry; Membrane trafficking; Phosphorylation; Proton pump

Indexed keywords

CYCLIC AMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ACID BASE BALANCE; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME LOCALIZATION; FLUORESCENCE MICROSCOPY; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD ELECTRON MICROSCOPY; KIDNEY COLLECTING TUBULE; KIDNEY TUBULE EPITHELIUM; MALE; MICROVILLUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

EID: 77649131946     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00584.2009     Document Type: Article

References (70)

1. Al-Awqati Q. Terminal differentiation of intercalated cells: the role of hensin. Annu Rev Physiol 65: 567-583, 2003.
2. Alper SL. Genetic diseases of acid-base transporters. Annu Rev Physiol 64: 899-923, 2002.
3. +-ATPase. Proc Natl Acad Sci USA 86: 5429-5433, 1989.
4. Bagnis C, Marshansky V, Breton S, Brown D. Remodeling the cellular profile of collecting ducts by chronic carbonic anhydrase inhibition. Am J Physiol Renal Physiol 280: F437-F448, 2001.
5. Bastani B, Haragsim L. Immunocytochemistry of renal H-ATPase. Miner Electrolyte Metab 22: 382-395, 1996.
6. Bastani B, Purcell H, Hemken P, Trigg D, Gluck S. Expression and distribution of renal vacuolar proton-translocating adenosine triphosphatase in response to chronic acid and alkali loads in the rat. J Clin Invest 88: 126-136, 1991.
7. +-ATPase recycling. J Biol Chem 280: 8452-8463, 2005.
8. Breton S, Alper SL, Gluck SL, Sly WS, Barker JE, Brown D. Depletion of intercalated cells from collecting ducts of carbonic anhydrase II-deficient (CAR2 null) mice. Am J Physiol Renal Fluid Electrolyte Physiol 269: F761-F774, 1995.
9. Breton S, Brown D. New insights into the regulation of V-ATPasedependent proton secretion. Am J Physiol Renal Physiol 292: F1-F10, 2007.
10. +ATPase is a PDZ domain-binding protein. Colocalization with NHE-RF in renal B-intercalated cells. J Biol Chem 275: 18219-18224, 2000.
11. Brown D. Analysis of protein expression by immunocytochemistry. In: Gene Probes: A Practical Approach, edited by Hames BD and Higgins S. Oxford, UK: Oxford University Press, 1996, p. 267-311.
12. Brown D, Breton S. Mitochondria-rich, proton-secreting epithelial cells. J Exp Biol 199: 2345-2358, 1996.
13. +-ATPase in opposite plasma membrane domains in kidney epithelial cell subpopulations. Nature 331: 622-624, 1988.
14. Brown D, Hirsch S, Gluck S. Localization of a proton-pumping ATPase in rat kidney. J Clin Invest 82: 2114-2126, 1988.
15. Brown D, Lydon J, McLaughlin M, Stuart-Tilley A, Tyszkowski R, Alper S. Antigen retrieval in cryostat tissue sections and cultured cells by treatment with sodium dodecyl sulfate (SDS). Histochem Cell Biol 105: 261-267, 1996.
16. Brown D, Pǎunescu TG, Breton S, Marshansky V. Regulation of the V-ATPase in kidney epithelial cells: dual role in acid-base homeostasis and vesicle trafficking. J Exp Biol 212: 1762-1772, 2009.
17. +-phosphate cotransporter NaPi-IIa in Nherf1-deficient mice. Am J Physiol Cell Physiol 292: C927-C934, 2007.
18. Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289: 625-628, 2000.
19. Gekle M, Wunsch S, Oberleithner H, Silbernagl S. Characterization of two MDCK-cell subtypes as a model system to study principal cell and intercalated cell properties. Pflügers Arch 428: 157-162, 1994.
20. +-ATPase accumulation in epididymal clear cells. Am J Physiol Cell Physiol 296: C672-C681, 2009.
21. Hays S, Kokko JP, Jacobson HR. Hormonal regulation of proton secretion in rabbit medullary collecting duct. J Clin Invest 78: 1279-1286, 1986.
22. Hong-Hermesdorf A, Brux A, Gruber A, Gruber G, Schumacher K. A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett 580: 932-939, 2006.
23. Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada GH, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 8: 124-136, 2006.
24. Iino Y, Troy JL, Brenner BM. Effects of catecholamines on electrolyte transport in cortical collecting tubule. J Membr Biol 61: 67-73, 1981.
25. Kamenetsky M, Middelhaufe S, Bank EM, Levin LR, Buck J, Steegborn C. Molecular details of cAMP generation in Mammalian cells: a tale of two systems. J Mol Biol 362: 623-639, 2006.
26. Klengel T, Liang WJ, Chaloupka J, Ruoff C, Schroppel K, Naglik JR, Eckert SE, Mogensen EG, Haynes K, Tuite MF, Levin LR, Buck J, Muhlschlegel FA. Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15: 2021-2026, 2005.
27. Kyllonen MS, Parkkila S, Rajaniemi H, Waheed A, Grubb JH, Shah GN, Sly WS, Kaunisto K. Localization of carbonic anhydrase XII to the basolateral membrane of H+-secreting cells of mouse and rat kidney. J Histochem Cytochem 51: 1217-1224, 2003.
28. Li S, Sato S, Yang X, Preisig PA, Alpern RJ. Pyk2 activation is integral to acid stimulation of sodium/hydrogen exchanger 3. J Clin Invest 114: 1782-1789, 2004.
29. Litvin TN, Kamenetsky M, Zarifyan A, Buck J, Levin LR. Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate. J Biol Chem 278: 15922-15926, 2003.
30. Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE, Junker U, Hofstetter H, Wolf RM, Seuwen K. Proton-sensing G-protein-coupled receptors. Nature 425: 93-98, 2003.
31. +-secreting epithelia. Fed Proc 44: 2704-2709, 1985.
32. + exchanger regulatory factor 2 directs parathyroid hormone 1 receptor signalling. Nature 417: 858-861, 2002.
33. Mellman I. The importance of being acid: the role of acidification in intracellular membrane traffic. J Exp Biol 172: 39-45, 1992.
34. Miller RL, Zhang P, Smith M, Beaulieu V, Pǎunescu TG, Brown D, Breton S, Nelson RD. V-ATPase B1-subunit promoter drives expression of EGFP in intercalated cells of kidney, clear cells of epididymis and airway cells of lung in transgenic mice. Am J Physiol Cell Physiol 288: C1134-C1144, 2005.
35. 3. Am J Physiol Renal Physiol 274: F1086-F1094, 1998.
36. Mogensen EG, Janbon G, Chaloupka J, Steegborn C, Fu MS, Moyrand F, Klengel T, Pearson DS, Geeves MA, Buck J, Levin LR, Muhlschlegel FA. Cryptococcus neoformans senses CO2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot Cell 5: 103-111, 2006.
37. Morel F, Chabardes D, Imbert M. Functional segmentation of the rabbit distal tubule by microdetermination of hormone-dependent adenylate cyclase activity. Kidney Int 9: 264-277, 1976.
38. Morel F, Doucet A. Hormonal control of kidney functions at the cell level. Physiol Rev 66: 377-468, 1986.
39. +)-ATPase associates with and is phosphorylated by the 50-kDa polypeptide of the clathrin assembly protein AP-2. J Biol Chem 268: 9184-9186, 1993.
40. +-ATPase 56-kilodalton subunit in renal intercalated cells. Proc Natl Acad Sci USA 89: 3541-3545, 1992.
41. Owegi MA, Carenbauer AL, Wick NM, Brown JF, Terhune KL, Bilbo SA, Weaver RS, Shircliff R, Newcomb N, Parra-Belky KJ. Mutational analysis of the stator subunit E of the yeast V-ATPase. J Biol Chem 280: 18393-18402, 2005.
42. Pastor-Soler N, Beaulieu V, Litvin TN, Da Silva N, Chen Y, Brown D, Buck J, Levin LR, Breton S. Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J Biol Chem 278: 49523-49529, 2003.
43. Pastor-Soler NM, Hallows KR, Smolak C, Gong F, Brown D, Breton S. Alkaline pH- and cAMP-induced V-ATPase membrane accumulation is mediated by protein kinase A in epididymal clear cells. Am J Physiol Cell Physiol 294: C488-C494, 2008.
44. +-ATPase in proton-secreting cells of the kidney and epididymis. Am J Physiol Cell Physiol 287: C149-C162, 2004.
45. Pǎunescu TG, Da Silva N, Russo LM, McKee M, Lu HA, Breton S, Brown D. Association of soluble adenylyl cyclase with the V-ATPase in renal epithelial cells. Am J Physiol Renal Physiol 294: F130-F138, 2008.
46. Pǎunescu TG, Russo LM, Da Silva N, Kovacikova J, Mohebbi N, Van Hoek AN, McKee M, Wagner CA, Breton S, Brown D. Compensatory membrane expression of the V-ATPase B2 subunit isoform in renal medullary intercalated cells of B1-deficient mice. Am J Physiol Renal Physiol 293: F1915-F1926, 2007.
47. Pech V, Zheng W, Pham TD, Verlander JW, Wall SM. Angiotensin II activates H+-ATPase in type A intercalated cells. J Am Soc Nephrol 19: 84-91, 2008.
48. +-ATPase subunit are PDZ motifs involved in their interaction. Am J Physiol Cell Physiol 284: C667-C673, 2003.
49. Roth J, Brown D, Norman AW, Orci L. Localization of the vitamin D-dependent calcium-binding protein in mammalian kidney. Am J Physiol Renal Fluid Electrolyte Physiol 243: F243-F252, 1982.
50. +-ATPase activity in renal acidsecretory intercalated cells from the outer medullary collecting duct. J Am Soc Nephrol 18: 2085-2093, 2007.
51. Royaux IE, Wall SM, Karniski LP, Everett LA, Suzuki K, Knepper MA, Green ED. Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretion. Proc Natl Acad Sci USA 98: 4221-4226, 2001.
52. Russo LM, McKee M, Brown D. Methyl-beta-cyclodextrin induces vasopressin-independent apical accumulation of aquaporin-2 in the isolated, perfused rat kidney. Am J Physiol Renal Physiol 291: F246-F253, 2006.
53. +-ATPase in rat cortex by acute metabolic acidosis and alkalosis. Kidney Int 51: 125-137, 1997.
54. + pumps in isolated perfused proximal and collecting tubules. J Clin Invest 75: 1638-1644, 1985.
55. + transport by exocytosis and endocytosis. Annu Rev Physiol 48: 153-161, 1986.
56. Schwartz GJ, Barasch J, Al-Awqati Q. Plasticity of functional epithelial polarity. Nature 318: 368-371, 1985.
57. Seuwen K, Ludwig MG, Wolf RM. Receptors for protons or lipid messengers or both? J Recept Signal Transduct Res 26: 599-610, 2006.
58. Shum WW, Da Silva N, McKee M, Smith PJ, Brown D, Breton S. Transepithelial projections from basal cells are luminal sensors in pseudostratified epithelia. Cell 135: 1108-1117, 2008.
59. Thomas JA, Buchsbaum RN, Zimniak A, Racker E. Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18: 2210-2218, 1979.
60. Tobo M, Tomura H, Mogi C, Wang JQ, Liu JP, Komachi M, Damirin A, Kimura T, Murata N, Kurose H, Sato K, Okajima F. Previously postulated "ligand-independent" signaling of GPR4 is mediated through proton-sensing mechanisms. Cell Signal 19: 1745-1753, 2007.
61. +-ATPases. J Cell Biol 102: 1638-1645, 1986.
62. Verlander JW, Miller RT, Frank AE, Royaux IE, Kim YH, Weiner ID. Localization of the ammonium transporter proteins RhBG and RhCG in mouse kidney. Am J Physiol Renal Physiol 284: F323-F337, 2003.
63. +-ATPase by protein kinase A. J Biol Chem 282: 33735-33742, 2007.
64. Wagner CA, Finberg KE, Breton S, Marshansky V, Brown D, Geibel JP. Renal vacuolar-ATPase. Physiol Rev 84: 1263-1314, 2004.
65. Wagner CA, Lukewille U, Valles P, Breton S, Brown D, Giebisch GH, Geibel JP. A rapid enzymatic method for the isolation of defined kidney tubule fragments from mouse. Pflügers Arch 446: 623-632, 2003.
66. Wall SM, Fischer MP, Glapion DM, De La Calzada M. ANG II reduces net acid secretion in rat outer medullary collecting duct. Am J Physiol Renal Physiol 285: F930-F937, 2003.
67. Wieczorek H, Brown D, Grinstein S, Ehrenfeld J, Harvey WR. Animal plasma membrane energization by proton-motive V-ATPases. Bioessays 21: 637-648, 1999.
68. +-ATPases in intercalated renal tubule cells by aldosterone. Proc Natl Acad Sci USA 101: 2636-2641, 2004.
69. Zippin JH, Chen Y, Nahirney P, Kamenetsky M, Wuttke MS, Fischman DA, Levin LR, Buck J. Compartmentalization of bicarbonatesensitive adenylyl cyclase in distinct signaling microdomains. FASEB J 17: 82-84, 2003.
70. - -responsive soluble adenylyl cyclase as a putative metabolic sensor. Trends Endocrinol Metab 12: 366-370, 2001.