Hormone-induced assembly and activation of V-ATPase in blowfly salivary glands is mediated by protein kinase A

American Journal of Physiology - Cell Physiology

Volumn 294, Issue 1, 2008, Pages

  Rein, Julia ^a,b   Voss, Martin ^a   Blenau, Wolfgang ^a   Walz, Bernd ^a   Baumann, Otto ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Adenosine 3 ,5 cyclic monophosphate; Exchange protein directly activated by adenosine 3 ,5 cyclic monophosphate; Insect; Vacuolar H+ adenosine 5 triphosphatase

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ANTIPORTER; CYCLIC AMP DEPENDENT PROTEIN KINASE; EPAC PROTEIN; HOLOENZYME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SEROTONIN; UNCLASSIFIED DRUG;

ACIDIFICATION; ARTICLE; BLOWFLY; CALLIPHORA VICINA; CATION TRANSPORT; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; FLY; HORMONAL REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SALIVARY GLAND; SEROTONIN RELEASE; VOLTAGE CLAMP;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; DIPTERA; ENZYME ACTIVATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HYDROGEN-ION CONCENTRATION; INSECT PROTEINS; MEMBRANE POTENTIALS; MOLECULAR SEQUENCE DATA; PROTEIN KINASE INHIBITORS; PROTEIN SUBUNITS; PROTEIN TRANSPORT; SALIVARY GLANDS; SEROTONIN; SIGNAL TRANSDUCTION; TIME FACTORS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

CALLIPHORA VICINA; HEXAPODA;

EID: 38349084073     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00041.2007     Document Type: Article

References (74)

1. Berridge MJ. Cyclic AMP, calcium and fluid secretion. In: Transport of Ions and Water, edited by Gupta BL, Moreton RB, Oschman JL, and Wall BW. New York, NY: Academic, 1977, p. 225-238.
2. Berridge MJ. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem J 212: 849-858, 1983.
3. Berridge MJ, Heslop JP. Separate 5-hydroxytryptamine receptors on the salivary gland of the blowfly are linked to the generation of either cyclic adenosine 3′,5′-monophosphate or calcium signals. Br J Pharmacol 73: 729-738, 1981.
4. Berridge MJ, Patel NG. Insect salivary glands: stimulation of fluid secretion by 5-hydroxytryptamine and adenosine-3′,5′- monophosphate. Science 162: 462-463, 1968.
5. Berridge MJ, Lindley BD, Prince WT. Studies on the mechanism of fluid secretion by isolated salivary glands of Calliphora. J Exp Biol 64: 311-322, 1976.
6. + ATPase: molecular structure and function, physiological roles and regulation. J Exp Biol 209: 577-589, 2006.
7. Bos JL. Epac: a new cAMP target and new avenues in cAMP research. Nat Rev Mol Cell Biol 4: 733-738, 2003.
8. +-ATPase activity in murine peritoneal macrophages. J Biol Chem 271: 2005-2011, 1996.
9. +V-ATPase-dependent luminal acidification in the kidney collecting duct and the epididymis/vas deferens: vesicle recycling and transcytotic pathways. J Exp Biol 203: 137-145, 2000.
10. Cheung U, Atwood HL, Zucker RS. Presynaptic effectors contributing to cAMP-induced synaptic potentiation in Drosophila. J Neurobiol 66: 273-280, 2006.
11. Chijiwa T, Mishima A, Hagiwara M, Sano M, Hayashi K, Inoue T, Naito K, Toshioka T, Hidaka H. Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino) ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J Biol Chem 265: 5267-5272, 1990.
12. Christensen AE, Selheim F, deRooij J, Dremier S, Schwede F, Khanh KD, Martinez A, Maenhaut C, Bos JL, Genieser HG, Døskeland SO. cAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J Biol Chem 278: 35394-35402, 2003.
13. Coast GM, Webster SG, Schegg KM, Tobe SS, Schooley DA. The Drosophila melanogaster homologue of an insect calcitonin-like diuretic peptide stimulates V-ATPase activity in fruit fly Malpighian tubules. J Exp Biol 204: 1795-1804, 2001.
14. +-ATPase assembly and activity in blowfly salivary glands. Proc Natl Acad Sci USA 103: 3926-3931, 2006.
15. Dao KK, Teigen K, Kopperud R, Hodneland E, Schwede F, Christensen AE, Martinez A, Døskeland SO. Epac1 and cAMP-dependent protein kinase holoenzyme have similar cAMP affinity, but their cAMP domains have distinct structural features and cyclic nucleotide recognition. J Biol Chem 281: 21500-21511, 2006.
16. De Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A, Bos JL. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396: 474-477, 1998.
17. Døskeland SO, Øgreid D. Binding proteins for cyclic AMP in mammalian tissues. Int J Biochem 13: 1-19, 1981.
18. Dostmann WR, Taylor SS, Genieser HG, Jastorff B, Døskeland SO, Øgreid D. Probing the cyclic nucleotide binding sites of cAMP-dependent protein kinases I and II with analogs of adenosine 3′,5′-cyclic phosphorothioates. J Biol Chem 265: 10484-10491, 1990.
19. Dröse S, Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 200: 1-8, 1997.
20. Enserink JM, Christensen AE, de Rooij J, van Triest M, Schwede F, Genieser HG, Doskeland SO, Blank JL, Bos JL. A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat Cell Biol 4: 901-906, 2002.
21. Fain JN, Berridge MJ. Relationship between hormonal activation of phosphatidylinositol hydrolysis, fluid secretion and calcium flux in the blowfly salivary gland. Biochem J 178: 45-58, 1979.
22. Filippova M, Ross LS, Gill SS. Cloning of the V-ATPase B subunit cDNA from Culex quinquefasciatus and expression of the B and C subunits in mosquitoes. Insect Mol Biol 7: 223-232, 1998.
23. Genz AK, von Engelhardt W, Busche R. Maintenance and regulation of the pH microclimate at the luminal surface of the distal colon of guinea-pig. J Physiol 517: 507-519, 1999.
24. Gluck SL, Underhill DM, Iyori M, Holliday LS, Kostrominova TY, Lee BS. Physiology and biochemistry of the kidney vacuolar H′-ATPase. Annu Rev Physiol 58: 427-445, 1996.
25. Gluck SL, Lee BS, Wang SP, Underhill D, Nemoto J, Holliday LS. Plasma membrane V-ATPases in proton-transporting cells of the mammalian kidney and osteoclast. Acta Physiol Scand Suppl 643: 203-213, 1998.
26. 1-ATPase. J Biol Chem 271: 20908-20913, 1996.
27. Hattori M, Minato N. Rap1 GTPase: functions, regulation, and malignancy. J Biochem (Tokyo) 134: 479-484, 2003.
28. Heslop JP, Berridge MJ. Changes in cyclic AMP and cyclic GMP concentrations during the action of 5-hydroxytryptamine on an insect salivary gland. Biochem J 192: 247-255, 1980.
29. Hong-Hermesdorf A, Brux A, Gruber A, Gruber G, Schuhmacher K. A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett 580: 932-939, 2006.
30. 0 domain. J Biol Chem 280: 27896-27903, 2005.
31. +-ATPase in vivo. J Biol Chem 270: 17025-17032, 1995.
32. +-ATPase. J Bioenerg Biomembr 35: 313-321, 2003.
33. Kawasaki H, Springett GM, Mochizuki N, Toki S, Nakaya M, Matsuda M, Housman DE, Graybiel AM. A family of cAMP-binding proteins that directly activate Rap1. Science 282: 2275-2279, 1998.
34. Li YP, Chen W, Liang Y, Li E, Stashenko P. Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast-mediated extracellular acidification. Nat Genet 23: 447-451, 1999.
35. +-ATPase to basolateral ion transport in Malpighian tubules of Drosophila melanogaster. J Exp Biol 202: 1561-1570, 1999.
36. +-ATPase: evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J Biol Chem 276: 30407-30413, 2001.
37. +-ATPase. J Biol Chem 279: 8732-8739, 2004.
38. Merzendorfer H, Gräf R, Huss M, Harvey WR, Wieczorek H. Regulation of proton-translocating V-ATPases. J Exp Biol 200: 225-235, 1997.
39. Merzendorfer H, Reineke S, Zhao XF, Jacobmeier B, Harvey WR, Wieczorek H. The multigene family of the tobacco hornworm V-ATPase: novel subunits a, C, D, H, and putative isoforms. Biochim Biophys Acta 1467: 369-379, 2000.
40. +-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.
41. Nelson N, Harvey WR. Vacuolar and plasma membrane proton-adenosinetriphosphatases. Physiol Rev 79: 361-385, 1999.
42. +-ATPases - nature's most versatile proton pumps. Nat Rev Mol Cell Biol 3: 94-103, 2002.
43. O'Donnell MJ, Dow JAT, Huesmann GR, Tublitz NJ, Maddrell SHP. Separate control of anion and cation transport in Malpighian tubules of Drosophila melanogaster. J Exp Biol 199: 1163-1175, 1996.
44. 3-cAMP. FEBS Lett 150: 161-166, 1982.
45. Øgreid D, Døskeland SO, Miller JP. Evidence that cyclic nucleotides activating rabbit muscle protein kinase I interact with both types of cAMP binding sites associated with the enzyme. J Biol Chem 258: 1041-1049, 1983.
46. Øgreid D, Ekanger R, Suva RH, Miller JP, Døskeland SO. Comparison of the two classes of binding sites (A and B) of type I and type II cyclic-AMP-dependent protein kinases by using cyclic nucleotide analogs. Eur J Biochem 181: 19-31, 1989.
47. Onken H, Schöbel A, Kraft I, Putzenlechner M. Active NaCl absorption across split lamellae of posterior gills of the Chinese crab Eriocheir sinensis: stimulation by eyestalk extract. J Exp Biol 203: 1373-1382, 2000.
48. Oschmann JL, Berridge MJ. Structural and functional aspects of fluid secretion in Calliphora. Tissue Cell 2: 281-310, 1970.
49. Otten AD, Parenteau LA, Døskeland SO, McKnight GS. Hormonal activation of gene transcription in ras-transformed NIH3T3 cells overexpressing RIIα and RIIβ subunits of the cAMP-dependent protein kinase. J Biol Chem 266: 23074-23082, 1991.
50. 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.
51. Prince WT, Berridge MJ. The effects of 5-hydroxytryptamine and cyclic AMP on the potential profile across isolated salivary glands. J Exp Biol 56: 323-333, 1972.
52. Rehmann H, Schwede F, Døskeland SO, Wittinghofer A, Bos JL. Ligand-mediated activation of the cAMP-responsive guanine nucleotide exchange factor Epac. J Biol Chem 278: 38548-38556, 2003.
53. Rein J, Zimmermann B, Hille C, Lang I, Walz B, Baumann O Fluorescence measurements of serotonin-induced V-ATPase-dependent pH changes at the luminal surface in salivary glands of the blowfly Calliphora vicina. J Exp Biol 209: 1716-1724, 2006.
54. Robinson-Steiner AM, Corbin JD. Probable involvement of both intrachain cAMP binding sites in activation of protein kinase. J Biol Chem 258: 1032-1040, 1983.
55. +-ATPase in rat submandibular gland and adaptive changes induced by acid-base disturbances. J Histochem Cytochem 46: 91-100, 1998.
56. +-ATPase assembly, translocation, and acidification of intracellular compartments in renal epithelial cells. Mol Cell Biol 25: 575-589, 2005.
57. Schoonderwoert VT, Martens GJ. Proton pumping in the secretory pathway. J Membr Biol 182: 159-169, 2001.
58. Seol JH, Shevchenko A, Shevchenko A, Deshaies RJ. Skp1 forms multiple protein complexes, including RAVE, a regulator of V-ATPase assembly. Nat Cell Biol 3: 384-391, 2001.
59. +-ATPase. J Biol Chem 282: 26185-26194, 2007.
60. Smardon AM, Tarsio M, Kane PM. The RAVE complex is essential for stable assembly of the yeast V-ATPase. J Biol Chem 277: 13831-13839, 2002.
61. +)-ATPase. Annu Rev Cell Dev Biol 13: 779-808, 1997.
62. +-ATPase interacts with phosphofructokinase-1 in humans. J Biol Chem 278: 20013-20018, 2003.
63. Sumner JP, Dow JA, Earley FG, Klein U, Jager D, Wieczorek H. Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J Biol Chem 270: 5649-5653, 1995.
64. Taylor SS, Buechler JA, Yonemoto W. cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu Rev Biochem 59: 971-1005, 1990.
65. Trombetta ES, Ebersold M, Garrett W, Pypaert M, Mellman I. Activation of lysosomal function during dendritic cell maturation. Science 299: 1400-1403, 2003.
66. Voss M, Vitavska O, Walz B, Wieczorek H, Baumann O. Stimulus-induced phosphorylation of V-ATPase by protein kinase A. J Biol Chem 282: 33735-33742, 2007.
67. +-ATPase. Physiol Rev 84: 1263-1314, 2004.
68. Walsh DA, van Patten SM. Multiple pathway signal transduction by the cAMP-dependent protein kinase. FASEB J 8: 1227-1236, 1994.
69. + antiport in an animal plasma membrane. J Biol Chem 266: 15340-15347, 1991.
70. +V-ATPase. J Exp Biol 203: 127-135, 2000.
71. +-ATPase. J Biol Chem 267: 9773-9778, 1992.
72. Zhong N, Zucker RS. cAMP acts on exchange protein activated by cAMP/cAMP-regulated guanine nucleotide exchange protein to regulate transmitter release at the crayfish neuromuscular junction. J Neurosci 25: 208-214, 2005.
73. Zimmermann B, Walz B. Serotonin-induced intercellular calcium waves in salivary glands of the blowfly Calliphora erythrocephala. J Physiol 500: 17-28, 1997.
74. +-ATPase in the salivary glands of the blowfly Calliphora vicina. J Exp Biol 206: 1867-1876, 2003.