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Catestatin regulates vesicular quanta through modulation of cholinergic and peptidergic (PACAPergic) stimulation in PC12 cells

Sahu, Bhavani Shankar and Mahata, Sumana and Bandyopadhyay, Keya and Mahata, Manjula and Avolio, Ennio and Pasqua, Teresa and Sahu, Chinmayi and Bandyopadhyay, Gautam K. and Bartolomucci, Alessandro and Webster, Nicholas J. G. and Van Den Bogaart, Geert and Fischer-Colbrie, Reiner and Corti, Angelo and Eiden, Lee E. and Mahata, Sushil K. (2019) Catestatin regulates vesicular quanta through modulation of cholinergic and peptidergic (PACAPergic) stimulation in PC12 cells. Cell and Tissue Research, 376 (1). pp. 51-70. ISSN 0302-766X. https://resolver.caltech.edu/CaltechAUTHORS:20181204-075246416

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Abstract

We have previously shown that the chromogranin A (CgA)-derived peptide catestatin (CST: hCgA_(352–372)) inhibits nicotine-induced secretion of catecholamines from the adrenal medulla and chromaffin cells. In the present study, we seek to determine whether CST regulates dense core (DC) vesicle (DCV) quanta (catecholamine and chromogranin/secretogranin proteins) during acute (0.5-h treatment) or chronic (24-h treatment) cholinergic (nicotine) or peptidergic (PACAP, pituitary adenylyl cyclase activating polypeptide) stimulation of PC12 cells. In acute experiments, we found that both nicotine (60 μM) and PACAP (0.1 μM) decreased intracellular norepinephrine (NE) content and increased ^3H‐NE secretion, with both effects markedly inhibited by co-treatment with CST (2 μM). In chronic experiments, we found that nicotine and PACAP both reduced DCV and DC diameters and that this effect was likewise prevented by CST. Nicotine or CST alone increased expression of CgA protein and together elicited an additional increase in CgA protein, implying that nicotine and CST utilize separate signaling pathways to activate CgA expression. In contrast, PACAP increased expression of CgB and SgII proteins, with a further potentiation by CST. CST augmented the expression of tyrosine hydroxylase (TH) but did not increase intracellular NE levels, presumably due to its inability to cause post-translational activation of TH through serine phosphorylation. Co-treatment of CST with nicotine or PACAP increased quantal size, plausibly due to increased synthesis of CgA, CgB and SgII by CST. We conclude that CST regulates DCV quanta by acutely inhibiting catecholamine secretion and chronically increasing expression of CgA after nicotinic stimulation and CgB and SgII after PACAPergic stimulation.


Item Type:Article
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https://doi.org/10.1007/s00441-018-2956-1DOIArticle
https://rdcu.be/bcrJbPublisherFree ReadCube access
Additional Information:© 2018 Springer-Verlag GmbH Germany, part of Springer Nature. Received: 27 July 2018; Accepted: 30 October 2018; First Online: 22 November 2018. The electron micrographs were taken in the Cellular and Molecular Medicine Electron microscopy core facility at UCSD, which is supported in part by National Institutes of Health Award number S10OD023527. This research was supported by a grant from the Department of Veterans Affairs (I01BX000323 to S.K.M.; I01BX002709 and an SRCS award to N.J.G.W) and the National Institutes of Health (NIH/NIDDK DK102496 to A.B. and MH002386 to L.E.E.). JCSTF-180217 travelling research fellowship to B.S.S. from company of biologists (Cambridge, UK). The Noland Scholarship from the California Institute of Technology supported S.M. Compliance with ethical standards. The authors declare that they have no conflict of interest.
Funders:
Funding AgencyGrant Number
NIHS10OD023527
Department of Veterans AffairsI01BX000323
Department of Veterans AffairsI01BX002709
NIHDK102496
NIHMH002386
Company of BiologistsJCSTF-180217
CaltechUNSPECIFIED
Issue or Number:1
Record Number:CaltechAUTHORS:20181204-075246416
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20181204-075246416
Official Citation:Sahu, B.S., Mahata, S., Bandyopadhyay, K. et al. Cell Tissue Res (2019) 376: 51. https://doi.org/10.1007/s00441-018-2956-1
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:91418
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:04 Dec 2018 19:24
Last Modified:03 Oct 2019 20:35

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