Calcium-dependent mitochondrial cAMP production enhances aldosterone secretion

Molecular and Cellular Endocrinology

Volumn 412, Issue , 2015, Pages 196-204

  Katona, Dávid ^a   Rajki, Anikó ^b   Di Benedetto, Giulietta ^c,d   Pozzan, Tullio ^c,d   Spät, András ^a  

^a SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c CNR   (Italy)

^d VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

Author keywords

Aldosterone; Angiotensin II; Ca2 + signal, glomerulosa cell; Cyclic AMP; Mitochondria; Soluble adenylyl cyclase

Indexed keywords

2 HYDROXYESTRADIOL; ADENYLATE CYCLASE; ALDOSTERONE; ANGIOTENSIN II; BICARBONATE; CALCIUM BINDING PROTEIN; CALCIUM ION; CYCLIC AMP; PHOSPHODIESTERASE; PROTEIN PDE2A; PROTEIN S100G; RNA; UNCLASSIFIED DRUG; ADCY10 PROTEIN, HUMAN;

ADRENAL CORTEX CELL; ALDOSTERONE RELEASE; ARTICLE; CALCIUM MOBILIZATION; CELL FUNCTION; CELL SPECIFICITY; HETEROLOGOUS EXPRESSION; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA INTERFERENCE; BIOSYNTHESIS; CALCIUM SIGNALING; CELL LINE; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

ADENYLYL CYCLASES; ALDOSTERONE; ANGIOTENSIN II; CALCIUM SIGNALING; CELL LINE; CYCLIC AMP; HUMANS; MITOCHONDRIA;

EID: 84939571861     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.05.002     Document Type: Article

References (52)

1. Acin-Perez R., Salazar E., Brosel S., Yang H., Schon E.A., Manfredi G. Modulation of mitochondrial protein phosphorylation by soluble adenylyl cyclase ameliorates cytochrome oxidase defects. EMBO Mol. Med 2009, 1:392-406.
2. Acin-Perez R., Salazar E., Kamenetsky M., Buck J., Levin L.R., Manfredi G. Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab 2009, 9:265-276.
3. Acin-Perez R., Russwurm M., Gunnewig K., Gertz M., Zoidl G., Ramos L., et al. A phosphodiesterase 2A isoform localized to mitochondria regulates respiration. J. Biol. Chem 2011, 286:30423-30432.
4. Andersen K. Aldosterone synthase inhibition in hypertension. Curr. Hypertens. Rep 2013, 15:484-488.
5. Baukal A.J., Hunyady L., Catt K.J., Balla T. Evidence for participation of calcineurin in potentiation of agonist-stimulated cyclic AMP formation by the calcium- mobilizing hormone, angiotensin II. J. Biol. Chem 1994, 269:24546-24549.
6. Begeot M., Langlois D., Penhoat A., Saez J.M. Variations in guanine-binding proteins (Gs, Gi) in cultured bovine adrenal cells. Consequences on the effects of phorbol ester and angiotensin II on adrenocorticotropin-induced and cholera-toxin-induced cAMP production. Eur. J. Biochem 1988, 174:317-321.
7. Bell J.B.G., Tait J.F., Tait S.A.S., Barnes G.D., Brown B.L. Lack of effect of angiotensin on levels of cyclic AMP in isolated adrenal zona glomerulosa cells from the rat. J. Endocrinol 1981, 91:145-154.
8. Bird I.M., Hanley N.A., Word R.A., Mathis J.M., McCarthy J.L., Mason J.I., et al. Human NCI-H295 adrenocortical carcinoma cells: a model for angiotensin-II-responsive aldosterone secretion. Endocrinology 1993, 133:1555-1561.
9. Bolton T.B., Prestwich S.A., Zholos A.V., Gordienko D.V. Excitation-contraction coupling in gastrointestinal and other smooth muscles. Annu. Rev. Physiol 1999, 61:85-115.
10. Brandenburger Y., Kennedy E.D., Python C.P., Rossier M.F., Vallotton M.B., Wollheim C.B., et al. Possible role for mitochondrial calcium in angiotensin II- and potassium-stimulated steroidogenesis in bovine adrenal glomerulosa cells. Endocrinology 1996, 137:5544-5551.
11. Braun T., Dods R.F. Development of a Mn-2+-sensitive, "soluble" adenylate cyclase in rat testis. Proc. Natl. Acad. Sci. U.S.A. 1975, 72:1097-1101.
12. Briet M., Schiffrin E.L. Aldosterone: effects on the kidney and cardiovascular system. Nat. Rev. Nephrol 2010, 6:261-273.
13. Buck J., Sinclair M.L., Schapal L., Cann M.J., Levin L.R. Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:79-84.
14. Burnay M.M., Vallotton M.B., Capponi A.M., Rossier M.F. Angiotensin II potentiates adrenocorticotrophic hormone- induced cAMP formation in bovine adrenal glomerulosa cells through a capacitative calcium influx. Biochem. J. 1998, 330:21-27.
15. Cano Abad M.F., Di Benedetto G., Magalhaes P.J., Filippin L., Pozzan T. Mitochondrial pH monitored by a new engineered green fluorescent protein mutant. J. Biol. Chem 2004, 279:11521-11529.
16. Cote M., Guillon G., Payet M.D., Gallo-Payet N. Expression and regulation of adenylyl cyclase isoforms in the human adrenal gland. J. Clin. Endocrinol. Metab 2001, 86:4495-4503.
17. 2+ uptake induces cyclic AMP generation in the matrix and modulates organelle ATP levels. Cell Metab 2013, 17:965-975.
18. Enyedi P., Mucsi I., Hunyady L., Catt K.J., Spät A. The role of guanyl nucleotide binding proteins in the formation of inositol phosphates in adrenal glomerulosa cells. Biochem. Biophys. Res. Commun 1986, 140:941-947.
19. 2+ signaling. PLoS ONE 2011, 6. e25199.
20. Gomez-Sanchez C.E. Non renal effects of aldosterone. Steroids 2014, 91:1-2.
21. Hattangady N.G., Olala L.O., Bollag W.B., Rainey W.E. Acute and chronic regulation of aldosterone production. Mol. Cell. Endocrinol 2011, 10.1016/j.mce.2011.07.034.
22. Hausdorff W.P., Sekura R.D., Aguilera G., Catt K.J. Control of aldosterone production by angiotensin II is mediated by two guanine nucleotide regulatory proteins. Endocrinology 1987, 120:1668-1678.
23. + on the steroidogenesis of rat zona glomerulosa cells of the adrenal cortex: role of cyclic AMP. Proc. R. Soc. Lond. B Biol Sci 1986, 227:21-42.
24. Jaiswal B.S., Conti M. Identification and functional analysis of splice variants of the germ cell soluble adenylyl cyclase. J. Biol. Chem 2001, 276:31698-31708.
25. Jaiswal B.S., Conti M. Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10676-10681.
26. Lalevee N., Resin V., Arnaudeau S., Demaurex N., Rossier M.F. Intracellular transport of calcium from plasma membrane to mitochondria in adrenal H295R cells: implication for steroidogenesis. Endocrinology 2003, 144:4575-4585.
27. Lefkimmiatis K., Leronni D., Hofer A.M. The inner and outer compartments of mitochondria are sites of distinct cAMP/PKA signaling dynamics. J. Cell Biol 2013, 202:453-462.
28. Litvin T.N., Kamenetsky M., Zarifyan A., Buck J., Levin L.R. Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate. J. Biol. Chem 2003, 278:15922-15926.
29. i. Am. J. Physiol. Cell Physiol 1996, 271:C1340-C1349.
30. Marie J., Jard S. Angiotensin II inhibits adenylate cyclase from adrenal cortex glomerulosa zone. FEBS Lett 1983, 159:97-101.
31. Maturana A.D., Casal A.J., Demaurex N., Vallotton M.B., Capponi A.M., Rossier M.F. Angiotensin II negatively modulates L-type calcium channels through a pertussis toxin-sensitive G protein in adrenal glomerulosa cells. J. Biol. Chem 1999, 274:19943-19948.
32. McCormack J.G., Halestrap A.P., Denton R.M. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev 1990, 70:391-425.
33. Nishimoto K., Rainey W.E., Bollag W.B., Seki T. Lessons from the gene expression pattern of the rat zona glomerulosa. Mol. Cell. Endocrinol 2013, 371:107-113.
34. Nussdorfer G.G. Cytophysiology of the adrenal zona glomerulosa. Int. Rev. Cytol 1980, 64:307-368.
35. Ponsioen B., Zhao J., Riedl J., Zwartkruis F., van der Krogt G., Zaccolo M., et al. Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: epac as a novel cAMP indicator. EMBO Rep 2004, 5:1176-1180.
36. Pralong W.F., Hunyady L., Várnai P., Wollheim C.B., Spät A. Pyridine nucleotide redox state parallels production of aldosterone in potassium-stimulated adrenal glomerulosa cells. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:132-136.
37. 2. J. Biol. Chem 1994, 269:27310-27314.
38. Rainey W.E., Bird I.M., Mason J.I. The NCI-H295 cell line: a pluripotent model for human adrenocortical studies. Mol. Cell. Endocrinol 1994, 100:45-50.
39. Rocco S., Ambroz C., Aguilera G. Interaction between serotonin and other regulators of aldosterone secretion in rat adrenal glomerulosa cells. Endocrinology 1990, 127:3103-3110.
40. +, angiotensin II and vasopressin. Biochem. J. 1997, 322:785-792.
41. Schaub M.C., Kunz B. Regulation of contraction in cardiac and smooth muscles. J. Cardiovasc. Pharmacol 1986, 8(Suppl. 8):S117-S123.
42. Shen T., Suzuki Y., Poyard M., Best-Belpomme M., Defer N., Hanoune J. Localization and differential expression of adenylyl cyclase messenger ribonucleic acids in rat adrenal gland determined by in situ hybridization. Endocrinology 1997, 138:4591-4598.
43. Spät A., Hunyady L. Control of aldosterone secretion: a model for convergence in cellular signaling pathways. Physiol. Rev 2004, 84:489-539.
44. 2+ signal on the redox state of mitochondrial pyridine nucleotides. Mol. Cell. Endocrinol 2004, 215:115-118.
45. 2+ and NAD(P)H in the control of aldosterone secretion. Cell Calcium 2012, 52:64-72.
46. Sperelakis N. Properties of calcium channels in cardiac muscle and vascular smooth muscle. Mol. Cell. Biochem 1990, 99:97-109.
47. Steegborn C., Litvin T.N., Hess K.C., Capper A.B., Taussig R., Buck J., et al. A novel mechanism for adenylyl cyclase inhibition from the crystal structure of its complex with catechol estrogen. J. Biol. Chem 2005, 280:31754-31759.
48. Steegborn C., Litvin T.N., Levin L.R., Buck J., Wu H. Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment. Nat. Struct. Mol. Biol 2005, 12:32-37.
49. Tomaschitz A., Pilz S., Ritz E., Obermayer-Pietsch B., Pieber T.R. Aldosterone and arterial hypertension. Nat. Rev. Endocrinol 2010, 6:83-93.
50. Wiederkehr A., Szanda G., Akhmedov D., Mataki C., Heizmann C.W., Schoonjans K., et al. Mitochondrial matrix calcium is an activating signal for hormone secretion. Cell Metab 2011, 13:601-611.
51. Woodcock E.A., Johnston C.I. Inhibition of adenylate cyclase in rat adrenal glomerulosa cells by angiotensin II. Endocrinology 1984, 115:337-341.
52. Zippin J.H., Chen Y., Nahirney P., Kamenetsky M., Wuttke M.S., Fischman D.A., et al. Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J. 2003, 17:82-84.