GHSR controls food deprivation-induced activation of CRF neurons of the hypothalamic paraventricular nucleus in a LEAP2-dependent manner.


Journal

Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402

Informations de publication

Date de publication:
04 May 2022
Historique:
received: 11 03 2022
accepted: 10 04 2022
revised: 08 04 2022
entrez: 3 5 2022
pubmed: 4 5 2022
medline: 6 5 2022
Statut: epublish

Résumé

Prolonged fasting is a major challenge for living organisms. An appropriate metabolic response to food deprivation requires the activation of the corticotropin-releasing factor-producing neurons of the hypothalamic paraventricular nucleus (PVH We estimated the activation of the PVH We found that food deprivation results in the activation of the PVH Food deprivation-induced activation of the PVH

Identifiants

pubmed: 35504998
doi: 10.1007/s00018-022-04302-5
pii: 10.1007/s00018-022-04302-5
doi:

Substances chimiques

Antimicrobial Cationic Peptides 0
Ghrelin 0
Ghsr1a protein, mouse 0
Leap2 protein, mouse 0
Receptors, Ghrelin 0
Corticotropin-Releasing Hormone 9015-71-8

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

277

Subventions

Organisme : Fondo para la Investigación Científica y Tecnológica
ID : PICT2016-1084
Organisme : Fondo para la Investigación Científica y Tecnológica
ID : PICT2017-3196
Organisme : Fondo para la Investigación Científica y Tecnológica
ID : PICT2019-3054
Organisme : Conicet
ID : PUE105
Organisme : The National Qatar Research Foundation
ID : NPRP13S-0209-200315

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature Switzerland AG.

Références

Luque RM, Park S, Kineman RD (2007) Severity of the catabolic condition differentially modulates hypothalamic expression of growth hormone-releasing hormone in the fasted mouse: potential role of neuropeptide Y and corticotropin-releasing hormone. Endocrinology 148(1):300–309. https://doi.org/10.1210/en.2006-0592
doi: 10.1210/en.2006-0592 pubmed: 17038558
Muglia L, Jacobson L, Dikkes P, Majzoub JA (1995) Corticotropin-releasing hormone deficiency reveals major fetal but not adult glucocorticoid need. Nature 373(6513):427–432. https://doi.org/10.1038/373427a0
doi: 10.1038/373427a0 pubmed: 7830793
Howard AD, Feighner SD, Cully DF, Arena JP, Liberator PA, Rosenblum CI et al (1996) A receptor in pituitary and hypothalamus that functions in growth hormone release. Science 273(5277):974–977. https://doi.org/10.1126/science.273.5277.974
doi: 10.1126/science.273.5277.974 pubmed: 8688086
Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402(6762):656–660. https://doi.org/10.1038/45230
doi: 10.1038/45230 pubmed: 10604470
Fernandez G, Cabral A, Andreoli MF, Labarthe A, M’Kadmi C, Ramos JG et al (2018) Evidence supporting a role for constitutive ghrelin receptor signaling in fasting-induced hyperphagia in male mice. Endocrinology 159(2):1021–1034. https://doi.org/10.1210/en.2017-03101
doi: 10.1210/en.2017-03101 pubmed: 29300858
Cabral A, Suescun O, Zigman JM, Perello M (2012) Ghrelin indirectly activates hypophysiotropic CRF neurons in rodents. PLoS ONE 7(2):e31462. https://doi.org/10.1371/journal.pone.0031462
doi: 10.1371/journal.pone.0031462 pubmed: 22363652 pmcid: 3282735
Tolle V, Zizzari P, Tomasetto C, Rio MC, Epelbaum J, Bluet-Pajot MT (2001) In vivo and in vitro effects of ghrelin/motilin-related peptide on growth hormone secretion in the rat. Neuroendocrinology 73(1):54–61. https://doi.org/10.1159/000054620
doi: 10.1159/000054620 pubmed: 11174017
Cornejo MP, Mustafa ER, Cassano D, Baneres JL, Raingo J, Perello M (2021) The ups and downs of growth hormone secretagogue receptor signaling. FEBS J. https://doi.org/10.1111/febs.15718
doi: 10.1111/febs.15718 pubmed: 33460513
Henry FE, Sugino K, Tozer A, Branco T, Sternson SM (2015) Cell type-specific transcriptomics of hypothalamic energy-sensing neuron responses to weight-loss. Elife. https://doi.org/10.7554/eLife.09800
doi: 10.7554/eLife.09800 pubmed: 26609809 pmcid: 4755750
Yasrebi A, Hsieh A, Mamounis KJ, Krumm EA, Yang JA, Magby J et al (2016) Differential gene regulation of GHSR signaling pathway in the arcuate nucleus and NPY neurons by fasting, diet-induced obesity, and 17beta-estradiol. Mol Cell Endocrinol 422:42–56. https://doi.org/10.1016/j.mce.2015.11.007
doi: 10.1016/j.mce.2015.11.007 pubmed: 26577678
Atasoy D, Betley JN, Su HH, Sternson SM (2012) Deconstruction of a neural circuit for hunger. Nature 488(7410):172–177. https://doi.org/10.1038/nature11270
doi: 10.1038/nature11270 pubmed: 22801496 pmcid: 3416931
Campbell JN, Macosko EZ, Fenselau H, Pers TH, Lyubetskaya A, Tenen D et al (2017) A molecular census of arcuate hypothalamus and median eminence cell types. Nat Neurosci 20(3):484–496. https://doi.org/10.1038/nn.4495
doi: 10.1038/nn.4495 pubmed: 28166221 pmcid: 5323293
Cornejo MP, Denis RGP, Garcia Romero G, Fernandez G, Reynaldo M, Luquet S et al (2021) Ghrelin treatment induces rapid and delayed increments of food intake: a heuristic model to explain ghrelin’s orexigenic effects. Cell Mol Life Sci 78(19–20):6689–6708. https://doi.org/10.1007/s00018-021-03937-0
doi: 10.1007/s00018-021-03937-0 pubmed: 34559253
Wang Q, Liu C, Uchida A, Chuang JC, Walker A, Liu T et al (2014) Arcuate AgRP neurons mediate orexigenic and glucoregulatory actions of ghrelin. Mol Metab 3(1):64–72. https://doi.org/10.1016/j.molmet.2013.10.001
doi: 10.1016/j.molmet.2013.10.001 pubmed: 24567905
Willesen MG, Kristensen P, Romer J (1999) Co-localization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology 70(5):306–316. https://doi.org/10.1159/000054491
doi: 10.1159/000054491 pubmed: 10567856
Sun Y, Butte NF, Garcia JM, Smith RG (2008) Characterization of adult ghrelin and ghrelin receptor knockout mice under positive and negative energy balance. Endocrinology 149(2):843–850. https://doi.org/10.1210/en.2007-0271
doi: 10.1210/en.2007-0271 pubmed: 18006636
Wortley KE, Anderson KD, Garcia K, Murray JD, Malinova L, Liu R et al (2004) Genetic deletion of ghrelin does not decrease food intake but influences metabolic fuel preference. Proc Natl Acad Sci USA 101(21):8227–8232. https://doi.org/10.1073/pnas.0402763101
doi: 10.1073/pnas.0402763101 pubmed: 15148384 pmcid: 419585
Ge X, Yang H, Bednarek MA, Galon-Tilleman H, Chen P, Chen M et al (2018) LEAP2 is an endogenous antagonist of the ghrelin receptor. Cell Metab 27(2):461–469. https://doi.org/10.1016/j.cmet.2017.10.016
doi: 10.1016/j.cmet.2017.10.016 pubmed: 29233536
M’Kadmi C, Cabral A, Barrile F, Giribaldi J, Cantel S, Damian M et al (2019) N-terminal liver-expressed antimicrobial peptide 2 (LEAP2) region exhibits inverse agonist activity toward the ghrelin receptor. J Med Chem 62(2):965–973. https://doi.org/10.1021/acs.jmedchem.8b01644
doi: 10.1021/acs.jmedchem.8b01644 pubmed: 30543423
Wang JH, Li HZ, Shao XX, Nie WH, Liu YL, Xu ZG et al (2019) Identifying the binding mechanism of LEAP2 to receptor GHSR1a. FEBS J 286(7):1332–1345. https://doi.org/10.1111/febs.14763
doi: 10.1111/febs.14763 pubmed: 30666806
Shankar K, Metzger NP, Singh O, Mani BK, Osborne-Lawrence S, Varshney S et al (2021) LEAP2 deletion in mice enhances ghrelin’s actions as an orexigen and growth hormone secretagogue. Mol Metab 53:101327. https://doi.org/10.1016/j.molmet.2021.101327
doi: 10.1016/j.molmet.2021.101327 pubmed: 34428557 pmcid: 8452786
Arvat E, Maccario M, Di Vito L, Broglio F, Benso A, Gottero C et al (2001) Endocrine activities of ghrelin, a natural growth hormone secretagogue (GHS), in humans: comparison and interactions with hexarelin, a nonnatural peptidyl GHS, and GH-releasing hormone. J Clin Endocrinol Metab 86(3):1169–1174. https://doi.org/10.1210/jcem.86.3.7314
doi: 10.1210/jcem.86.3.7314 pubmed: 11238504
Cabral A, Portiansky E, Sanchez-Jaramillo E, Zigman JM, Perello M (2016) Ghrelin activates hypophysiotropic corticotropin-releasing factor neurons independently of the arcuate nucleus. Psychoneuroendocrinology 67:27–39. https://doi.org/10.1016/j.psyneuen.2016.01.027
doi: 10.1016/j.psyneuen.2016.01.027 pubmed: 26874559 pmcid: 4808343
Zigman JM, Nakano Y, Coppari R, Balthasar N, Marcus JN, Lee CE et al (2005) Mice lacking ghrelin receptors resist the development of diet-induced obesity. J Clin Invest 115(12):3564–3572. https://doi.org/10.1172/JCI26002
doi: 10.1172/JCI26002 pubmed: 16322794 pmcid: 1297251
Hassouna R, Zizzari P, Tomasetto C, Veldhuis JD, Fiquet O, Labarthe A et al (2014) An early reduction in GH peak amplitude in preproghrelin-deficient male mice has a minor impact on linear growth. Endocrinology 155(9):3561–3571. https://doi.org/10.1210/en.2014-1126
doi: 10.1210/en.2014-1126 pubmed: 24949662
Cabral A, Fernandez G, Tolosa MJ, Rey Moggia A, Calfa G, De Francesco PN et al (2020) Fasting induces remodeling of the orexigenic projections from the arcuate nucleus to the hypothalamic paraventricular nucleus, in a growth hormone secretagogue receptor-dependent manner. Mol Metab 32:69–84. https://doi.org/10.1016/j.molmet.2019.11.014
doi: 10.1016/j.molmet.2019.11.014 pubmed: 32029231
Cabral A, Valdivia S, Fernandez G, Reynaldo M, Perello M (2014) Divergent neuronal circuitries underlying acute orexigenic effects of peripheral or central ghrelin: critical role of brain accessibility. J Neuroendocrinol 26(8):542–554. https://doi.org/10.1111/jne.12168
doi: 10.1111/jne.12168 pubmed: 24888783 pmcid: 4108543
Els S, Schild E, Petersen PS, Kilian TM, Mokrosinski J, Frimurer TM et al (2012) An aromatic region to induce a switch between agonism and inverse agonism at the ghrelin receptor. J Med Chem 55(17):7437–7449. https://doi.org/10.1021/jm300414b
doi: 10.1021/jm300414b pubmed: 22920150
Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K et al (2001) A role for ghrelin in the central regulation of feeding. Nature 409(6817):194–198. https://doi.org/10.1038/35051587
doi: 10.1038/35051587 pubmed: 11196643
Uriarte M, De Francesco PN, Fernandez G, Cabral A, Castrogiovanni D, Lalonde T et al (2019) Evidence supporting a role for the blood-cerebrospinal fluid barrier transporting circulating ghrelin into the brain. Mol Neurobiol 56(6):4120–4134. https://doi.org/10.1007/s12035-018-1362-8
doi: 10.1007/s12035-018-1362-8 pubmed: 30276663
Greenblatt DJ, Koch-Weser J (1975) Clinical pharmacokinetics (second of two parts). N Engl J Med 293(19):964–970. https://doi.org/10.1056/NEJM197511062931905
doi: 10.1056/NEJM197511062931905 pubmed: 1101062
Greenblatt DJ, Kock-Weser J (1975) Drug therapy clinical pharmacokinetics (first of two parts). N Engl J Med 293(14):702–705. https://doi.org/10.1056/NEJM197510022931406
doi: 10.1056/NEJM197510022931406 pubmed: 1160938
Perello M, Chacon F, Cardinali DP, Esquifino AI, Spinedi E (2006) Effect of social isolation on 24-h pattern of stress hormones and leptin in rats. Life Sci 78(16):1857–1862. https://doi.org/10.1016/j.lfs.2005.08.029
doi: 10.1016/j.lfs.2005.08.029 pubmed: 16289237
Cornejo MP, Castrogiovanni D, Schioth HB, Reynaldo M, Marie J, Fehrentz JA et al (2019) Growth hormone secretagogue receptor signalling affects high-fat intake independently of plasma levels of ghrelin and LEAP2, in a 4-day binge eating model. J Neuroendocrinol 31(10):e12785. https://doi.org/10.1111/jne.12785
doi: 10.1111/jne.12785 pubmed: 31469195
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676–682. https://doi.org/10.1038/nmeth.2019
doi: 10.1038/nmeth.2019 pubmed: 22743772
Paxinos G, Franklin KBJ, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic Press, San Diego
Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247. https://doi.org/10.1002/ar.1090940210
doi: 10.1002/ar.1090940210 pubmed: 21015608
Zhao TJ, Liang G, Li RL, Xie X, Sleeman MW, Murphy AJ et al (2010) Ghrelin O-acyltransferase (GOAT) is essential for growth hormone-mediated survival of calorie-restricted mice. Proc Natl Acad Sci USA 107(16):7467–7472. https://doi.org/10.1073/pnas.1002271107
doi: 10.1073/pnas.1002271107 pubmed: 20231469 pmcid: 2867684
Mani BK, Puzziferri N, He Z, Rodriguez JA, Osborne-Lawrence S, Metzger NP et al (2019) LEAP2 changes with body mass and food intake in humans and mice. J Clin Invest 129(9):3909–3923. https://doi.org/10.1172/JCI125332
doi: 10.1172/JCI125332 pubmed: 31424424 pmcid: 6715358
Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R et al (2016) Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol 6(2):603–621. https://doi.org/10.1002/cphy.c150015
doi: 10.1002/cphy.c150015 pubmed: 27065163 pmcid: 4867107
Ahima RS, Prabakaran D, Mantzoros C, Qu D, Lowell B, Maratos-Flier E et al (1996) Role of leptin in the neuroendocrine response to fasting. Nature 382(6588):250–252. https://doi.org/10.1038/382250a0
doi: 10.1038/382250a0 pubmed: 8717038
Perello M, Gaillard RC, Chisari A, Spinedi E (2003) Adrenal enucleation in MSG-damaged hyperleptinemic male rats transiently restores adrenal sensitivity to leptin. Neuroendocrinology 78(3):176–184. https://doi.org/10.1159/000072799
doi: 10.1159/000072799 pubmed: 14512710
Chuang JC, Perello M, Sakata I, Osborne-Lawrence S, Savitt JM, Lutter M et al (2011) Ghrelin mediates stress-induced food-reward behavior in mice. J Clin Invest 121(7):2684–2692. https://doi.org/10.1172/JCI57660
doi: 10.1172/JCI57660 pubmed: 21701068 pmcid: 3223843
Ciofi P, Garret M, Lapirot O, Lafon P, Loyens A, Prevot V et al (2009) Brain-endocrine interactions: a microvascular route in the mediobasal hypothalamus. Endocrinology 150(12):5509–5519. https://doi.org/10.1210/en.2009-0584
doi: 10.1210/en.2009-0584 pubmed: 19837874 pmcid: 2819742
Schaeffer M, Langlet F, Lafont C, Molino F, Hodson DJ, Roux T et al (2013) Rapid sensing of circulating ghrelin by hypothalamic appetite-modifying neurons. Proc Natl Acad Sci USA 110(4):1512–1517. https://doi.org/10.1073/pnas.1212137110
doi: 10.1073/pnas.1212137110 pubmed: 23297228 pmcid: 3557016
Broberger C, Johansen J, Johansson C, Schalling M, Hokfelt T (1998) The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc Natl Acad Sci U S A 95(25):15043–15048. https://doi.org/10.1073/pnas.95.25.15043
doi: 10.1073/pnas.95.25.15043 pubmed: 9844012 pmcid: 24572
Yulyaningsih E, Rudenko IA, Valdearcos M, Dahlen E, Vagena E, Chan A et al (2017) Acute lesioning and rapid repair of hypothalamic neurons outside the blood-brain barrier. Cell Rep 19(11):2257–2271. https://doi.org/10.1016/j.celrep.2017.05.060
doi: 10.1016/j.celrep.2017.05.060 pubmed: 28614713 pmcid: 5651178
M’Kadmi C, Leyris JP, Onfroy L, Gales C, Sauliere A, Gagne D et al (2015) Agonism, antagonism, and inverse agonism bias at the ghrelin receptor signaling. J Biol Chem 290(45):27021–27039. https://doi.org/10.1074/jbc.M115.659250
doi: 10.1074/jbc.M115.659250 pubmed: 26363071 pmcid: 4646384
Petersen PS, Woldbye DP, Madsen AN, Egerod KL, Jin C, Lang M et al (2009) In vivo characterization of high Basal signaling from the ghrelin receptor. Endocrinology 150(11):4920–4930. https://doi.org/10.1210/en.2008-1638
doi: 10.1210/en.2008-1638 pubmed: 19819980
Henriques ST, Tan CC, Craik DJ, Clark RJ (2010) Structural and functional analysis of human liver-expressed antimicrobial peptide 2. ChemBioChem 11(15):2148–2157. https://doi.org/10.1002/cbic.201000400
doi: 10.1002/cbic.201000400 pubmed: 20845358
Shirley JL, de Jong YP, Terhorst C, Herzog RW (2020) Immune responses to viral gene therapy vectors. Mol Ther 28(3):709–722. https://doi.org/10.1016/j.ymthe.2020.01.001
doi: 10.1016/j.ymthe.2020.01.001 pubmed: 31968213 pmcid: 7054714
Luckman SM, Rosenzweig I, Dickson SL (1999) Activation of arcuate nucleus neurons by systemic administration of leptin and growth hormone-releasing peptide-6 in normal and fasted rats. Neuroendocrinology 70(2):93–100. https://doi.org/10.1159/000054463
doi: 10.1159/000054463 pubmed: 10461023
Lopez Soto EJ, Agosti F, Cabral A, Mustafa ER, Damonte VM, Gandini MA et al (2015) Constitutive and ghrelin-dependent GHSR1a activation impairs CaV2.1 and CaV2.2 currents in hypothalamic neurons. J Gen Physiol 146(3):205–219. https://doi.org/10.1085/jgp.201511383
doi: 10.1085/jgp.201511383 pubmed: 26283199 pmcid: 4555474
Fuzesi T, Wittmann G, Liposits Z, Lechan RM, Fekete C (2007) Contribution of noradrenergic and adrenergic cell groups of the brainstem and agouti-related protein-synthesizing neurons of the arcuate nucleus to neuropeptide-y innervation of corticotropin-releasing hormone neurons in hypothalamic paraventricular nucleus of the rat. Endocrinology 148(11):5442–5450. https://doi.org/10.1210/en.2007-0732
doi: 10.1210/en.2007-0732 pubmed: 17690163
Li C, Chen P, Smith MS (2000) Corticotropin releasing hormone neurons in the paraventricular nucleus are direct targets for neuropeptide Y neurons in the arcuate nucleus: an anterograde tracing study. Brain Res 854(1–2):122–129. https://doi.org/10.1016/s0006-8993(99)02324-0
doi: 10.1016/s0006-8993(99)02324-0 pubmed: 10784113
Liposits Z, Sievers L, Paull WK (1988) Neuropeptide-Y and ACTH-immunoreactive innervation of corticotropin releasing factor (CRF)-synthesizing neurons in the hypothalamus of the rat an immunocytochemical analysis at the light and electron microscopic levels. Histochemistry 88(3–6):227–234. https://doi.org/10.1007/BF00570278
doi: 10.1007/BF00570278 pubmed: 2835333
Dimitrov EL, DeJoseph MR, Brownfield MS, Urban JH (2007) Involvement of neuropeptide Y Y1 receptors in the regulation of neuroendocrine corticotropin-releasing hormone neuronal activity. Endocrinology 148(8):3666–3673. https://doi.org/10.1210/en.2006-1730
doi: 10.1210/en.2006-1730 pubmed: 17463058
Sarkar S, Lechan RM (2003) Central administration of neuropeptide Y reduces alpha-melanocyte-stimulating hormone-induced cyclic adenosine 5’-monophosphate response element binding protein (CREB) phosphorylation in pro-thyrotropin-releasing hormone neurons and increases CREB phosphorylation in corticotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology 144(1):281–291. https://doi.org/10.1210/en.2002-220675
doi: 10.1210/en.2002-220675 pubmed: 12488356
Spencer SJ, Emmerzaal TL, Kozicz T, Andrews ZB (2015) Ghrelin’s role in the hypothalamic-pituitary-adrenal axis stress response: implications for mood disorders. Biol Psychiatry 78(1):19–27. https://doi.org/10.1016/j.biopsych.2014.10.021
doi: 10.1016/j.biopsych.2014.10.021 pubmed: 25534754
Hagemann CA, Zhang C, Hansen HH, Jorsal T, Rigbolt KTG, Madsen MR et al (2021) Identification and metabolic profiling of a novel human gut-derived LEAP2 fragment. J Clin Endocrinol Metab 106(2):e966–e981. https://doi.org/10.1210/clinem/dgaa803
doi: 10.1210/clinem/dgaa803 pubmed: 33135737

Auteurs

Gimena Fernandez (G)

Laboratory of Neurophysiology, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina.

Agustina Cabral (A)

Laboratory of Neurophysiology, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina.

Pablo N De Francesco (PN)

Laboratory of Neurophysiology, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina.

Maia Uriarte (M)

Laboratory of Neurophysiology, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina.

Mirta Reynaldo (M)

Laboratory of Neurophysiology, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina.

Daniel Castrogiovanni (D)

Cell Culture Facility, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina.

Guillermina Zubiría (G)

Laboratory of Neuroendocrinology, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina.

Andrés Giovambattista (A)

Laboratory of Neuroendocrinology, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina.

Sonia Cantel (S)

Institut Des Biomolécules Max Mousseron, UMR 5247 CNRS-Université Montpellier-ENSCM, Montpellier, France.

Severine Denoyelle (S)

Institut Des Biomolécules Max Mousseron, UMR 5247 CNRS-Université Montpellier-ENSCM, Montpellier, France.

Jean-Alain Fehrentz (JA)

Institut Des Biomolécules Max Mousseron, UMR 5247 CNRS-Université Montpellier-ENSCM, Montpellier, France.

Virginie Tolle (V)

Institute of Psychiatry and Neuroscience of Paris, Université de Paris, UMR-S 1266 INSERM, Paris, France.

Helgi B Schiöth (HB)

Department of Surgical Sciences, Functional Pharmacology and Neuroscience, Uppsala University, Uppsala, Sweden.
Institute for Translational Medicine and Biotechnology, I. M. Sechenov First Moscow State Medical University, Moscow, Russia.

Mario Perello (M)

Laboratory of Neurophysiology, Multidisciplinary Institute of Cell Biology [IMBICE, Argentine Research Council (CONICET) and Scientific Research Commission, Province of Buenos Aires (CIC-PBA), National University of La Plata (UNLP)], Calle 526 S/N entre 10 y 11, La Plata, Buenos Aires, 1900, Argentina. mperello@imbice.gov.ar.
Department of Surgical Sciences, Functional Pharmacology and Neuroscience, Uppsala University, Uppsala, Sweden. mperello@imbice.gov.ar.

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