Phospholipase C-ε defines a PACAP-stimulated pathway for secretion in the chromaffin cell.


Journal

Journal of neuroendocrinology
ISSN: 1365-2826
Titre abrégé: J Neuroendocrinol
Pays: United States
ID NLM: 8913461

Informations de publication

Date de publication:
Nov 2023
Historique:
revised: 15 02 2023
received: 30 12 2022
accepted: 08 03 2023
medline: 23 11 2023
pubmed: 28 3 2023
entrez: 27 3 2023
Statut: ppublish

Résumé

Adrenomedullary chromaffin cells respond to splanchnic (sympathetic) nerve stimulation by releasing stress hormones into the circulation. The signal for hormone secretion is encoded in the neurotransmitters - especially acetylcholine (ACh) and pituitary adenylate cyclase activating polypeptide (PACAP) - that are released into the splanchnic-chromaffin cell synapse. However, functional differences in the effects of ACh and PACAP on the chromaffin cell secretory response are not well defined. Here, selective agonists of PACAP receptors or nicotinic and muscarinic acetylcholine receptors were applied to chromaffin cells. The major differences in the effects of these agents were not on exocytosis, per se, but rather on the steps upstream of exocytosis. In almost every respect, the properties of individual fusion events triggered by PACAP and cholinergic agonists were similar. On the other hand, the properties of the Ca

Identifiants

pubmed: 36970756
doi: 10.1111/jne.13255
doi:

Substances chimiques

Acetylcholine N9YNS0M02X
Catecholamines 0
Cholinergic Agonists 0
Guanine Nucleotide Exchange Factors 0
Hormones 0
Pituitary Adenylate Cyclase-Activating Polypeptide 0
phospholipase C epsilon EC 3.1.4.11
Receptors, Cholinergic 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13255

Subventions

Organisme : NIGMS NIH HHS
ID : R35 GM127303
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS122534
Pays : United States
Organisme : NINDS NIH HHS
ID : R01NS122534
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01GM106569
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35GM127303
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01GM106569
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35GM127303
Pays : United States
Organisme : NINDS NIH HHS
ID : R01NS122534
Pays : United States

Informations de copyright

© 2023 The Authors. Journal of Neuroendocrinology published by John Wiley & Sons Ltd on behalf of British Society for Neuroendocrinology.

Références

Goldstein DS. Adrenal responses to stress. Cell Mol Neurobiol. 2010;30(8):1433-1440. doi:10.1007/s10571-010-9606-9
Goldstein DS, Kopin IJ. Evolution of concepts of stress. Stress. 2007;10(2):109-120. doi:10.1080/10253890701288935
Cannon WB. The adrenal medulla. Bull N Y Acad Med. 1940;16(1):3-13. https://www.ncbi.nlm.nih.gov/pubmed/19312138
De Robertis E, Ferreira AV. Submicroscopic changes of the nerve endings in the adrenal medulla after stimulation of the splanchnic nerve. J Biophys Biochem Cytol. 1957;3(4):611-614. doi:10.1083/jcb.3.4.611
Grynszpan-Winograd O. Adrenaline and noradrenaline cells in the adrenal medulla of the hamster: a morphological study of their innervation. J Neurocytol. 1974;3(3):341-361. doi:10.1007/bf01097918
Feldberg W, Minz B, Tsudzimura H. The mechanism of the nervous discharge of adrenaline. J Physiol. 1934;81(3):286-304. doi:10.1113/jphysiol.1934.sp003136
Guerineau NC. Cholinergic and peptidergic neurotransmission in the adrenal medulla: a dynamic control of stimulus-secretion coupling. IUBMB Life. 2019;72:553-567. doi:10.1002/iub.2117
Carbone E, Borges R, Eiden LE, Garcia AG, Hernandez-Cruz A. Chromaffin cells of the adrenal medulla: physiology, pharmacology, and disease. Compr Physiol. 2019;9(4):1443-1502. doi:10.1002/cphy.c190003
Eiden LE, Emery AC, Zhang L, Smith CB. PACAP signaling in stress: insights from the chromaffin cell. Pflugers Arch. 2018;470(1):79-88. doi:10.1007/s00424-017-2062-3
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. 2009;110(4):1214-1225. doi:10.1111/j.1471-4159.2009.06206.x
Stroth N, Kuri BA, Mustafa T, Chan SA, Smith CB, Eiden LE. PACAP controls adrenomedullary catecholamine secretion and expression of catecholamine biosynthetic enzymes at high splanchnic nerve firing rates characteristic of stress transduction in male mice. Endocrinology. 2013;154(1):330-339. doi:10.1210/en.2012-1829
Criado M. Acetylcholine nicotinic receptor subtypes in chromaffin cells. Pflugers Arch. 2018;470(1):13-20. doi:10.1007/s00424-017-2050-7
Zhou Z, Neher E. Calcium permeability of nicotinic acetylcholine receptor channels in bovine adrenal chromaffin cells. Pflugers Arch. 1993;425(5-6):511-517. http://www.ncbi.nlm.nih.gov/pubmed/7510879
Fenwick EM, Marty A, Neher E. Sodium and calcium channels in bovine chromaffin cells. J Physiol. 1982a;331:599-635. http://www.ncbi.nlm.nih.gov/pubmed/6296372
Garcia AG, Garcia-De-Diego AM, Gandia L, Borges R, Garcia-Sancho J. Calcium signaling and exocytosis in adrenal chromaffin cells. Physiol Rev. 2006;86(4):1093-1131. doi:10.1152/physrev.00039.2005
Inoue M, Matsuoka H, Harada K, Kao LS. Muscarinic receptors in adrenal chromaffin cells: physiological role and regulation of ion channels. Pflugers Arch. 2018;470(1):29-38. doi:10.1007/s00424-017-2047-2
Harada K, Matsuoka H, Miyata H, Matsui M, Inoue M. Identification of muscarinic receptor subtypes involved in catecholamine secretion in adrenal medullary chromaffin cells by genetic deletion. Br J Pharmacol. 2015;172(5):1348-1359. doi:10.1111/bph.13011
Fisher SK, Holz RW, Agranoff BW. Muscarinic receptors in chromaffin cell cultures mediate enhanced phospholipid labeling but not catecholamine secretion. J Neurochem. 1981;37:491-497.
Olivos L, Artalejo AR. Muscarinic excitation-secretion coupling in chromaffin cells. Acta Physiol. 2008;192(2):213-220. doi:10.1111/j.1748-1716.2007.01816.x
Holman ME, Tonta MA, Coleman HA, Parkington HC. Muscarinic receptor activation in Guinea-pig chromaffin cells causes decreased membrane conductance and depolarization. J Auton Nerv Syst. 1998;68(3):140-144. doi:10.1016/s0165-1838(97)00122-7
Inoue M, Harada K, Matsuoka H, Nakamura J, Warashina A. Mechanisms and roles of muscarinic activation in Guinea-pig adrenal medullary cells. Am J Physiol Cell Physiol. 2012;303(6):C635-C644. doi:10.1152/ajpcell.00147.2012
Morales A, Mohan R, Chen X, et al. J Gen Physiol. 2023;155(2):1-22. doi:10.1085/jgp.202213180
Smith CB, Eiden LE. Is PACAP the major neurotransmitter for stress transduction at the adrenomedullary synapse? J Mol Neurosci. 2012;48(2):403-412. doi:10.1007/s12031-012-9749-x
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. 2011;286(49):42459-42469. doi:10.1074/jbc.M111.289389
Shigetomi E, Kracun S, Sofroniew MV, Khakh BS. A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nat Neurosci. 2010;13(6):759-766. doi:10.1038/nn.2557
Gubernator NG, Zhang H, Staal RG, et al. Fluorescent false neurotransmitters visualize dopamine release from individual presynaptic terminals. Science. 2009;324(5933):1441-1444. doi:10.1126/science.1172278
Wightman RM, Jankowski JA, Kennedy RT, et al. Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc Natl Acad Sci U S A. 1991;88:10754-10758.
Atchison DK, O'Connor CL, Menon R, et al. Hypertension induces glomerulosclerosis in phospholipase C-epsilon1 deficiency. Am J Physiol Renal Physiol. 2020;318(5):F1177-F1187. doi:10.1152/ajprenal.00541.2019
Wang H, Oestreich EA, Maekawa N, et al. Phospholipase C epsilon modulates beta-adrenergic receptor-dependent cardiac contraction and inhibits cardiac hypertrophy. Circ Res. 2005;97(12):1305-1313. doi:10.1161/01.RES.0000196578.15385.bb
Bolte S, Cordeliers FP. A guided tour into subcellular colocalization analysis in light microscopy. Journal of Microscopy. 2006;224(3): 213-232. doi:10.1111/j.1365-2818.2006.01706.x
Brindley RL, Bauer MB, Blakely RD, Currie KPM. An interplay between the serotonin transporter (SERT) and 5-HT receptors controls stimulus-secretion coupling in sympathoadrenal chromaffin cells. Neuropharmacology. 2016;110(Pt A):438-448. doi:10.1016/j.neuropharm.2016.08.015
Mosharov EV, Sulzer D. Analysis of exocytotic events recorded by amperometry. Nat Methods. 2005;2(9):651-658. doi:10.1038/nmeth782
Colliver TL, Hess EJ, Ewing AG. Amperometric analysis of exocytosis at chromaffin cells from genetically distinct mice. J Neurosci Methods. 2001;105(1):95-103. doi:10.1016/s0165-0270(00)00359-9
Dwivedi AK, Mallawaarachchi I, Alvarado LA. Analysis of small sample size studies using nonparametric bootstrap test with pooled resampling method. Stat Med. 2017;36(14):2187-2205. doi:10.1002/sim.7263
Akerboom J, Chen TW, Wardill TJ, et al. Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci. 2012;32(40):13819-13840. doi:10.1523/JNEUROSCI.2601-12.2012
Chow RH, von Ruden L, Neher E. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature. 1992;356(6364):60-63. doi:10.1038/356060a0
Wightman RM, Schroeder TJ, Finnegan JM, Ciolkowski EL, Pihel K. Time course of release of catecholamines from individual vesicles during exocytosis at adrenal medullary cells. BiophysicalJ. 1995;68(1):383-390.
Chang CW, Chiang CW, Jackson MB. Fusion pores and their control of neurotransmitter and hormone release. J Gen Physiol. 2017;149(3):301-322. doi:10.1085/jgp.201611724
Zhou Z, Misler S, Chow RH. Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys J. 1996;70(3):1543-1552. doi:10.1016/S0006-3495(96)79718-7
Lewis MJ, Pelham HR. Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum. Cell. 1992;68(2):353-364. doi:10.1016/0092-8674(92)90476-s
Oestreich EA, Malik S, Goonasekera SA, et al. Epac and phospholipase Cepsilon regulate Ca2+ release in the heart by activation of protein kinase Cepsilon and calcium-calmodulin kinase II. J Biol Chem. 2009;284(3):1514-1522. doi:10.1074/jbc.M806994200
Saternos HC, Almarghalani DA, Gibson HM, et al. Distribution and function of the muscarinic receptor subtypes in the cardiovascular system. Physiol Genomics. 2018;50(1):1-9. doi:10.1152/physiolgenomics.00062.2017
Ohta T, Wakade AR, Nakazato Y, Ito S. Ca(2+)-dependent K(+) current and exocytosis in responses to caffeine and muscarine in voltage-clamped Guinea-pig adrenal chromaffin cells. J Neurochem. 2001;78(6):1243-1255. doi:10.1046/j.1471-4159.2001.00502.x
Dzhura I, Chepurny OG, Kelley GG, et al. Epac2-dependent mobilization of intracellular Ca(2)+ by glucagon-like peptide-1 receptor agonist exendin-4 is disrupted in beta-cells of phospholipase C-epsilon knockout mice. J Physiol. 2010;588(Pt 24):4871-4889. doi:10.1113/jphysiol.2010.198424
Nash CA, Brown LM, Malik S, Cheng X, Smrcka AV. Compartmentalized cyclic nucleotides have opposing effects on regulation of hypertrophic phospholipase Cepsilon signaling in cardiac myocytes. J Mol Cell Cardiol. 2018;121:51-59. doi:10.1016/j.yjmcc.2018.06.002
Wakade AR. Noncholinergic transmitter(s) maintains secretion of catecholamines from rat adrenal medulla for several hours of continuous stimulation of splanchnic neurons. J Neurochem. 1988;50(4):1302-1308. doi:10.1111/j.1471-4159.1988.tb10608.x
Chowdhury PS, Guo X, Wakade TD, Przywara DA, Wakade AR. Exocytosis from a single rat chromaffin cell by cholinergic and peptidergic neurotransmitters. Neuroscience. 1994;59(1):1-5. doi:10.1016/0306-4522(94)90092-2
Cropper EC, Jing J, Vilim FS, Weiss KR. Peptide Cotransmitters as dynamic, intrinsic modulators of network activity. Front Neural Circuits. 2018;12:78. doi:10.3389/fncir.2018.00078
Verhage M, McMahon HT, Ghijsen WE, et al. Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron. 1991;6(4):517-524. doi:10.1016/0896-6273(91)90054-4

Auteurs

Xiaohuan Chen (X)

Department of Neurosciences, University of Toledo, Toledo, Ohio, 43606, USA.

Breanna L Coffman (BL)

Department of Neurosciences, University of Toledo, Toledo, Ohio, 43606, USA.

Rebecca L Brindley (RL)

Department of Biomedical Sciences, Cooper Medical School of Rowan University, Camden, New Jersey, 08103, USA.

Jason D Galpin (JD)

Department of Molecular Physiology and Biophysics, University of Iowa College of Medicine, Iowa City, Iowa, 52246, USA.

Christopher A Ahern (CA)

Department of Molecular Physiology and Biophysics, University of Iowa College of Medicine, Iowa City, Iowa, 52246, USA.

Kevin P M Currie (KPM)

Department of Biomedical Sciences, Cooper Medical School of Rowan University, Camden, New Jersey, 08103, USA.

Alan V Smrcka (AV)

Department of Pharmacology, University of Michigan, Ann Arbor, Michigan, 48109, USA.

Daniel Axelrod (D)

Department of Physics and LSA Biophysics, University of Michigan, Ann Arbor, Michigan, 48109, USA.

Arun Anantharam (A)

Department of Neurosciences, University of Toledo, Toledo, Ohio, 43606, USA.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH