Pituitary adenylate cyclase-activating peptide enhances electrical coupling in the mouse adrenal medulla

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 3, 2012, Pages

  Hill, Jacqueline ^a   Lee, Seong Ki ^a   Samasilp, Prattana ^a   Smith, Corey ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acute stress; Catecholamine; Connexin 36; Connexin 43; Gap junction

Indexed keywords

ACETYLCHOLINE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE;

ACTION POTENTIAL; ADRENAL MEDULLA; ADRENERGIC SYSTEM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATECHOLAMINE RELEASE; CELL STRESS; CHROMAFFIN CELL; EXCITATION CONTRACTION COUPLING; GAP JUNCTION; MALE; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; SPLANCHNIC NERVE; SYNAPSE;

ACTION POTENTIALS; ADRENAL MEDULLA; ANIMALS; CHROMAFFIN CELLS; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; GAP JUNCTIONS; MALE; MICE; MICE, INBRED C57BL; NEUROTRANSMITTER AGENTS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE;

EID: 84864503958     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00119.2012     Document Type: Article

References (50)

1. 2+ channels are coupled to the rapid component of secretion in mouse adrenal slice chromaffin cells. J Neurosci 20: 8323-8330, 2000.
2. Aunis D. Exocytosis in chromaffin cells of the adrenal medulla. Int Rev Cytol 181: 213-320, 1998.
3. Benninger RK, Head WS, Zhang M, Satin LS, Piston DW. Gap junctions and other mechanisms of cell-cell communication regulate basal insulin secretion in the pancreatic islet. J Physiol 589: 5453-5466, 2011.
4. Bevington A, Radda GK. Declining catecholamine secretion in adrenal medulla on prolonged stimulation with acetylcholine. Biochem Pharmacol 34: 1497-1500, 1985.
5. +, agents that stimulate catecholamine secretion, in isolated adrenal chromaffin cells. J Neurochem 42: 607-617, 1984.
6. Cao F, Eckert R, Elfgang C, Nitsche JM, Snyder SA, Hu DF, Willecke K, Nicholson BJ. A quantitative analysis of connexin-specific permeability differences of gap junctions expressed in HeLa transfectants and Xenopus oocytes. J Cell Sci 1: 31-43, 1998.
7. Chan SA, Polo-Parada L, Smith C. Action potential stimulation reveals an increased role for P/Q-calcium channel-dependent exocytosis in mouse adrenal tissue slices. Arch Biochem Biophys 435: 65-73, 2005.
8. Charpantier E, Cancela J, Meda P. Beta cells preferentially exchange cationic molecules via connexin 36 gap junction channels. Diabetologia 50: 2332-2341, 2007.
9. Colomer C, Desarmenien MG, Guerineau NC. Revisiting the stimulussecretion coupling in the adrenal medulla: role of gap junction-mediated intercellular communication. Mol Neurobiol 40: 87-100, 2009.
10. Colomer C, Martin AO, Desarmenien MG, Guerineau NC. Gap junction-mediated intercellular communication in the adrenal medulla: An additional ingredient of stimulus-secretion coupling regulation. Biochim Biophys Acta 1818: 1937-1951, 2011.
11. Colomer C, Olivos-Ore LA, Vincent A, McIntosh JM, Artalejo AR, Guerineau NC. Functional characterization of alpha9-containing cholinergic nicotinic receptors in the rat adrenal medulla: implication in stressinduced functional plasticity. J Neurosci 30: 6732-6742, 2010.
12. Colomer C, Olivos Ore LA, Coutry N, Mathieu MN, Arthaud S, Fontanaud P, Iankova I, Macari F, Thouennon E, Yon L, Anouar Y, Guerineau NC. Functional remodeling of gap junction-mediated electrical communication between adrenal chromaffin cells in stressed rats. J Neurosci 28: 6616-6626, 2008.
13. de Diego AM. Electrophysiological and morphological features underlying neurotransmission efficacy at the splanchnic nerve-chromaffin cell synapse of bovine adrenal medulla. Am J Physiol Cell Physiol 298: C397-C405, 2010.
14. de Groot JR, Veenstra T, Verkerk AO, Wilders R, Smits JP, Wilms-Schopman FJ, Wiegerinck RF, Bourier J, Belterman CN, Coronel R, Verheijck EE. Conduction slowing by the gap junctional uncoupler carbenoxolone. Cardiovasc Res 60: 288-297, 2003.
15. Degen J, Meier C, Van Der Giessen RS, Sohl G, Petrasch-Parwez E, Urschel S, Dermietzel R, Schilling K, De Zeeuw CI, Willecke K. Expression pattern of lacZ reporter gene representing connexin36 in transgenic mice. J Comp Neurol 473: 511-525, 2004.
16. Duquesnes N, Derangeon M, Metrich M, Lucas A, Mateo P, Li L, Morel E, Lezoualc'h F, Crozatier B. Epac stimulation induces rapid increases in connexin43 phosphorylation and function without preconditioning effect. Pflügers Arch 460: 731-741, 2010.
17. Elfgang C, Eckert R, Lichtenberg-Frate H, Butterweck A, Traub O, Klein RA, Hulser DF, Willecke K. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J Cell Biol 129: 805-817, 1995.
18. Garcia de Diego AM, Arnaiz JJ, Gandia L, Hernandez-Guijo JM, Garcia AG. A comparison between acetylcholine-like action potentials and square depolarizing pulses in triggering calcium entry and exocytosis in bovine chromaffin cells. J Mol Neurosci 30: 57-58, 2006.
19. Goodenough DA, Goliger JA, Paul DL. Connexins, connexons, and intercellular communication. Annu Rev Biochem 65: 475-502, 1996.
20. Grynszpan-Wynograd O, Nicolas G. Intercellular junctions in the adrenal medulla: a comparative freeze-fracture study. Tissue Cell 12: 661-672, 1980.
21. Gulinello M, Etgen AM. Sexually dimorphic hormonal regulation of the gap junction protein, CX43, in rats and altered female reproductive function in CX43+/-mice. Brain Res 1045: 107-115, 2005.
22. Guo X, Wakade AR. Differential secretion of catecholamines in response to peptidergic and cholinergic transmitters in rat adrenals. J Physiol 475: 539-545, 1994.
23. Head WS, Orseth ML, Nunemaker CS, Satin LS, Piston DW, Benninger RK. Connexin-36 gap junctions regulate in vivo first-and secondphase insulin secretion dynamics and glucose tolerance in the conscious mouse. Diabetes 2012 Apr 17. [Epub ahead of print]
24. Hill J, Chan SA, Kuri B, Smith C. Pituitary adenylate cyclase-activating peptide (PACAP) recruits low voltage-activated T-type calcium influx under acute sympathetic stimulation in mouse adrenal chromaffin cells. J Biol Chem 286: 42459-42469, 2011.
25. Klevans LR, Gebber GL. Comparison of differential secretion of adrenal catecholamines by splanchnic nerve stimulation and cholinergic agents. J Pharmacol Exp Ther 172: 69-76, 1970.
26. Kuri BA, Chan SA, Smith CB. PACAP regulates immediate catecholamine release from adrenal chromaffin cells in an activity-dependent manner through a protein kinase C-dependent pathway. J Neurochem 110: 1214-1225, 2009.
27. Kwak BR, van Veen TA, Analbers LJ, Jongsma HJ. TPA increases conductance but decreases permeability in neonatal rat cardiomyocyte gap junction channels. Exp Cell Res 220: 456-463, 1995.
28. Livezey GT, Miller JM, Vogel WH. Plasma norepinephrine, epinephrine and corticosterone stress responses to restraint in individual male and female rats, and their correlations. Neurosci Lett 62: 51-56, 1985.
29. Marley PD. Desensitization of the nicotinic secretory response of adrenal chromaffin cells. Trends Pharmacol Sci 9: 102-107, 1988.
30. Martin AO, Alonso G, Guerineau NC. Agrin mediates a rapid switch from electrical coupling to chemical neurotransmission during synaptogenesis. J Cell Biol 169: 503-514, 2005.
31. 2+ increases between chromaffin cells in adrenal slices: A role in catecholamine release. J Neurosci 21: 5397-5405, 2001.
32. Martin AO, Mathieu MN, Guerineau NC. Evidence for long-lasting cholinergic control of gap junctional communication between adrenal chromaffin cells. J Neurosci 23: 3669-3678, 2003.
33. Moser T. Low-conductance intercellular coupling between mouse chromaffin cells in situ. J Physiol 506: 195-205, 1998.
34. Murray SA, Pharrams SY. Comparison of gap junction expression in the adrenal gland. Microsc Res Tech 36: 510-519, 1997.
35. Mustafa T, Walsh J, Grimaldi M, Eiden LE. PAC1hop receptor activation facilitates catecholamine secretion selectively through 2-APBsensitive Ca(2+) channels in PC12 cells. Cell Signal 22: 1420-1426, 2010.
36. Nassar-Gentina V, Pollard HB, Rojas E. Electrical activity in chromaffin cells of intact mouse adrenal gland. Am J Physiol Cell Physiol 254: C675-C683, 1988.
37. Sala F, Nistri A, Criado M. Nicotinic acetylcholine receptors of adrenal chromaffin cells. Acta Physiol (Oxf) 192: 203-212, 2008.
38. Stroth N, Eiden LE. Stress hormone synthesis in mouse hypothalamus and adrenal gland triggered by restraint is dependent on pituitary adenylate cyclase-activating polypeptide signaling. Neuroscience 165: 1025-1030, 2010.
39. 2+ entry via protein kinase C and A pathways in melanotrophs of the pituitary pars intermedia of rats. Endocrinology 138: 4086-4095, 1997.
40. TenBroek EM, Lampe PD, Solan JL, Reynhout JK, Johnson RG. Ser364 of connexin43 and the upregulation of gap junction assembly by cAMP. J Cell Biol 155: 1307-1318, 2001.
41. Tonshoff C, Hemmick L, Evinger MJ. Pituitary adenylate cyclase activating polypeptide (PACAP) regulates expression of catecholamine biosynthetic enzyme genes in bovine adrenal chromaffin cells. J Mol Neurosci 9: 127-140, 1997.
42. Valiunas V, Beyer EC, Brink PR. Cardiac gap junction channels show quantitative differences in selectivity. Circ Res 91: 104-111, 2002.
43. van Veen TA, van Rijen HV, Jongsma HJ. Electrical conductance of mouse connexin45 gap junction channels is modulated by phosphorylation. Cardiovasc Res 46: 496-510, 2000.
44. Wakade AR. Multiple transmitter control of catecholamine secretion in rat adrenal medulla. Adv Pharmacol 42: 595-598, 1998.
45. Wakade AR, Wakade TD. Contribution of nicotinic and muscarinic receptors in the secretion of catecholamines evoked by endogenous and exogenous acetylcholine. Neuroscience 10: 973-978, 1983.
46. Walcott B, Moore LC, Birzgalis A, Claros N, Valiunas V, Ott T, Willecke K, Brink PR. Role of gap junctions in fluid secretion of lacrimal glands. Am J Physiol Cell Physiol 282: C501-C507, 2002.
47. Watanabe T, Masuo Y, Matsumoto H, Suzuki N, Ohtaki T, Masuda Y, Kitada C, Tsuda M, Fujino M. Pituitary adenylate cyclase activating polypeptide provokes cultured rat chromaffin cells to secrete adrenaline. Biochem Biophys Res Commun 182: 403-411, 1992.
48. Weinstock M, Razin M, Schorer-Apelbaum D, Men D, McCarty R. Gender differences in sympathoadrenal activity in rats at rest and in response to footshock stress. Int J Dev Neurosci 16: 289-295, 1998.
49. Wong DL, Anderson LJ, Tai TC. Cholinergic and peptidergic regulation of phenylethanolamine N-methyltransferase gene expression. Ann NY Acad Sci 971: 19-26, 2002.
50. Zhou CJ, Yada T, Kohno D, Kikuyama S, Suzuki R, Mizushima H, Shioda S. PACAP activates PKA, PKC and Ca(2+) signaling cascades in rat neuroepithelial cells. Peptides 22: 1111-1117, 2001.