AMP-activated protein kinase regulates the vacuolar H+-ATPase via direct phosphorylation of the A subunit (ATP6V1A) in the kidney

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 7, 2013, Pages

  Alzamora, Rodrigo ^a   Al Bataineh, Mohammad M ^a   Liu, Wen ^d   Gong, Fan ^a   Li, Hui ^a   Thali, Ramon F ^b   Joho Auchli, Yolanda ^e   Brunisholz, René A ^e   Satlin, Lisa M ^d   Neumann, Dietbert ^b,c   Hallows, Kenneth R ^a   Pastor Soler, Núria M ^a  

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

^b ETH ZURICH   (Switzerland)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

AMPK; Intercalated cells; Kidney; Mass spectrometry; V ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ACID SECRETION; ACIDIFICATION; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL PH; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; EPIFLUORESCENCE MICROSCOPY; FLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; KIDNEY; KIDNEY COLLECTING TUBULE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; RABBIT; REGULATORY MECHANISM; STEADY STATE; WILD TYPE;

EID: 84884930855     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00303.2013     Document Type: Article

References (57)

1. Al-Awqati Q, Gao XB. Differentiation of intercalated cells in the kidney. Physiology (Bethesda) 26: 266-272, 2011.
2. +-ATPase localization and activity via direct phosphorylation of the A subunit in kidney cells. J Biol Chem 285: 24676-24685, 2010.
3. Bens M, Vallet V, Cluzeaud F, Pascual-Letallec L, Kahn A, Rafestin-Oblin ME, Rossier BC, Vandewalle A. Corticosteroid-dependent sodium transport in a novel immortalized mouse collecting duct principal cell line. J Am Soc Nephrol 10: 923-934, 1999.
4. + channel through functional regulation of the ubiquitin ligase Nedd4-2. J Biol Chem 281: 26159-26169, 2006.
5. Bouley R, Pastor-Soler N, Cohen O, McLaughlin M, Breton S, Brown D. Stimulation of AQP2 membrane insertion in renal epithelial cells in vitro and in vivo by the cGMP phosphodiesterase inhibitor sildenafil citrate (Viagra). Am J Physiol Renal Physiol 288: F1103-F1112, 2005.
6. Bowman EJ, Siebers A, Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci USA 85: 7972-7976, 1988.
7. Carattino MD, Edinger RS, Grieser HJ, Wise R, Neumann D, Schlattner U, Johnson JP, Kleyman TR, Hallows KR. Epithelial sodium channel inhibition by AMP-activated protein kinase in oocytes and polarized renal epithelial cells. J Biol Chem 280: 17608-17616, 2005.
8. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano PR, Kemp BE. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 443: 285-289, 1999.
9. Constantinescu A, Silver RB, Satlin LM. H-K-ATPase activity in PNA-binding intercalated cells of newborn rabbit cortical collecting duct. Am J Physiol Renal Physiol 272: F167-F177, 1997.
10. Dale S, Wilson WA, Edelman AM, Hardie DG. Similar substrate recognition motifs for mammalian AMP-activated protein kinase, higher plant HMG-CoA reductase kinase-A, yeast SNF1, and mammalian calmodulin-dependent protein kinase I. FEBS Lett 361: 191-195, 1995.
11. Djouder N, Tuerk RD, Suter M, Salvioni P, Thali RF, Scholz R, Vaahtomeri K, Auchli Y, Rechsteiner H, Brunisholz RA, Viollet B, Makela TP, Wallimann T, Neumann D, Krek W. PKA phosphorylates and inactivates AMPKalpha to promote efficient lipolysis. EMBO J 29: 469-481, 2010.
12. Dobyan DC, Magill LS, Friedman PA, Hebert SC, Bulger RE. Carbonic anhydrase histochemistry in rabbit and mouse kidneys. Anat Rec 204: 185-197, 1982.
13. Edwards JC, van Adelsberg J, Rater M, Herzlinger D, Lebowitz J, al-Awqati Q. Conditional immortalization of bicarbonate-secreting intercalated cells from rabbit. Am J Physiol Cell Physiol 263: C521-C529, 1992.
14. Estilo G, Liu W, Pastor-Soler N, Mitchell P, Carattino MD, Kleyman TR, Satlin LM. Effect of aldosterone on BK channel expression in mammalian cortical collecting duct. Am J Physiol Renal Physiol 295: F780-F788, 2008.
15. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 8: 917-929, 2007.
16. +-ATPase apical accumulation in kidney intercalated cells is regulated by PKA and AMP-activated protein kinase. Am J Physiol Renal Physiol 298: F1162-F1169, 2010.
17. Hallows KR. Emerging role of AMP-activated protein kinase in coupling membrane transport to cellular metabolism. Curr Opin Nephrol Hypertens 14: 464-471, 2005.
18. +-ATPase accumulation in epididymal clear cells. Am J Physiol Cell Physiol 296: C672-C681, 2009.
19. Hallows KR, McCane JE, Kemp BE, Witters LA, Foskett JK. Regulation of channel gating by AMP-activated protein kinase modulates cystic fibrosis transmembrane conductance regulator activity in lung submucosal cells. J Biol Chem 278: 998-1004, 2003.
20. Hamm LL, Hering-Smith KS. Acid-base transport in the collecting duct. Semin Nephrol 13: 246-255, 1993.
21. Hamm LL, Nakhoul NL. Renal acidification. In: Brenner and Rector's The Kidney (8th ed.), edited by Brenner BM. Philadelphia, PA: Saunders Elsevier, 2008, p. 248-279.
22. Hardie DG, Scott JW, Pan DA, Hudson ER. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 546: 113-120, 2003.
23. +-ATPase. Microbiol Mol Biol Rev 70: 177-191, 2006.
24. +-ATPase cause renal tubular acidosis with sensorineural deafness. Nat Genet 21: 84-90, 1999.
25. +-ATPase in human embryonic kidney (HEK) cells. Cell Physiol Biochem 13: 257-262, 2003.
26. + transport regulation by AMP-activated protein kinase in kidney collecting duct and its role in ischemia (Abstract). J Am Soc Nephrol 22: 524A, 2011.
27. +-ATPase activity in the cortical collecting duct (CCD). Am J Physiol Renal Physiol 302: F205-F215, 2012.
28. +-ATPase is essential for the assembly and activity of the proton pump. J Biol Chem 282: 24495-24503, 2007.
29. +-ATPase: evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J Biol Chem 276: 30407-30413, 2001.
30. +-ATPase. J Biol Chem 279: 8732-8739, 2004.
31. Marshansky V, Ausiello DA, Brown D. Physiological importance of endosomal acidification: potential role in proximal tubulopathies. Curr Opin Nephrol Hypertens 11: 527-537, 2002.
32. Marsin AS, Bertrand L, Rider MH, Deprez J, Beauloye C, Vincent MF, Van den Berghe G, Carling D, Hue L. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol 10: 1247-1255, 2000.
33. Mount PF, Hill RE, Fraser SA, Levidiotis V, Katsis F, Kemp BE, Power DA. Acute renal ischemia rapidly activates the energy sensor AMPK but does not increase phosphorylation of eNOS-Ser1177. Am J Physiol Renal Physiol 289: F1103-F1115, 2005.
34. Munton RP, Tweedie-Cullen R, Livingstone-Zatchej M, Weinandy F, Waidelich M, Longo D, Gehrig P, Potthast F, Rutishauser D, Gerrits B, Panse C, Schlapbach R, Mansuy IM. Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Mol Cell Proteomics 6: 283-293, 2007.
35. Nelson N, Harvey WR. Vacuolar and plasma membrane proton-adenosinetriphosphatases. Physiol Rev 79: 361-385, 1999.
36. Neumann D, Woods A, Carling D, Wallimann T, Schlattner U. Mammalian AMP-activated protein kinase: functional, heterotrimeric complexes by co-expression of subunits in Escherichia coli. Protein Expr Purif 30: 230-237, 2003.
37. 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.
38. Pastor-Soler NM, Alzamora R, Naveed S, Smolak C, Gong F, Hallows KR. Novel regulation of V-ATPase by PKA and AMPK in kidney intercalated cells. FASEB J 23: 602.13, 2009.
39. Pastor-Soler NM, Hallows KR. AMP-activated protein kinase regulation of kidney tubular transport. Curr Opin Nephrol Hypertens 21: 523-533, 2012.
40. 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.
41. Paunescu TG, Ljubojevic M, Russo LM, Winter C, McLaughlin MM, Wagner CA, Breton S, Brown D. Cyclic AMP stimulates apical V-ATPase accumulation, microvillar elongation and proton extrusion in kidney collecting duct A-intercalated cells. Am J Physiol Renal Physiol 298: F643-F654, 2010.
42. Rein J, Voss M, Blenau W, Walz B, Baumann O. Hormone-induced assembly and activation of V-ATPase in blowfly salivary glands is mediated by protein kinase A. Am J Physiol Cell Physiol 294: C56-C65, 2008.
43. +-ATPase assembly, translocation, and acidification of intracellular compartments in renal epithelial cells. Mol Cell Biol 25: 575-589, 2005.
44. + pumps in isolated perfused proximal and collecting tubules. J Clin Invest 75: 1638-1644, 1985.
45. Shao E, Forgac M. Involvement of the nonhomologous region of subunit A of the yeast V-ATPase in coupling and in vivo dissociation. J Biol Chem 279: 48663-48670, 2004.
46. Shao E, Nishi T, Kawasaki-Nishi S, Forgac M. Mutational analysis of the non-homologous region of subunit A of the yeast V-ATPase. J Biol Chem 278: 12985-12991, 2003.
47. Smith AN, Skaug J, Choate KA, Nayir A, Bakkaloglu A, Ozen S, Hulton SA, Sanjad SA, Al-Sabban EA, Lifton RP, Scherer SW, Karet FE. Mutations in ATP6N1B, encoding a new kidney vacuolar proton pump 116-kD subunit, cause recessive distal renal tubular acidosis with preserved hearing. Nat Genet 26: 71-75, 2000.
48. Steinmetz PR. Cellular organization of urinary acidification. Am J Physiol Renal Fluid Electrolyte Physiol 251: F173-F187, 1986.
49. +-ATPase interacts with phosphofructokinase-1 in humans. J Biol Chem 278: 20013-20018, 2003.
50. 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.
51. 32 P-labeled phosphopeptides in liquid chromatography matrix-assisted laser desorption/ionization mass spectrometry. Anal Biochem 390: 141-148, 2009.
52. Tuerk RD, Thali RF, Auchli Y, Rechsteiner H, Brunisholz RA, Schlattner U, Wallimann T, Neumann D. New candidate targets of AMP-activated protein kinase in murine brain revealed by a novel multidimensional substrate-screen for protein kinases. J Proteome Res 6: 3266-3277, 2007.
53. van Adelsberg J, Edwards JC, Takito J, Kiss B, al-Awqati Q. An induced extracellular matrix protein reverses the polarity of band 3 in intercalated epithelial cells. Cell 76: 1053-1061, 1994.
54. +-ATPase by protein kinase A. J Biol Chem 282: 33735-33742, 2007.
55. Wagner CA, Finberg KE, Breton S, Marshansky V, Brown D, Geibel JP. Renal vacuolar-ATPase. Physiol Rev 84: 1263-1314, 2004.
56. Weiner ID, Hamm LL. Use of fluorescent dye BCECF to measure intracellular pH in cortical collecting tubule. Am J Physiol Renal Fluid Electrolyte Physiol 256: F957-F964, 1989.
57. 3-responsive soluble adenylyl cyclase as a putative metabolic sensor. Trends Endocrinol Metab 12: 366-370, 2001.