Pituitary adenylate cyclase-activating polypeptide (PACAP)
Binge eating
C57BL/6 J
Cre
DREADDs
Ensure
PACAP
PCR
PVT
Sex differences
mRNA
Journal
Psychopharmacology
ISSN: 1432-2072
Titre abrégé: Psychopharmacology (Berl)
Pays: Germany
ID NLM: 7608025
Informations de publication
Date de publication:
28 Sep 2024
28 Sep 2024
Historique:
received:
17
06
2024
accepted:
14
09
2024
medline:
28
9
2024
pubmed:
28
9
2024
entrez:
28
9
2024
Statut:
aheadofprint
Résumé
Both the paraventricular nucleus of the thalamus (PVT) and the neuropeptide, pituitary adenylate cyclase-activating polypeptide (PACAP), are thought to be involved in food intake. Importantly, PACAP is expressed in cells of the PVT. To determine if PACAP in cells of the PVT might mediate some of the involvement of the PVT with palatable food intake. In male and female C57BL/6 J mice and PACAP-Cre transgenic mice on a C57BL/6 J background, limited access to Milk Chocolate Ensure Plus® was used to establish a model of binge-type eating. Next, using quantitative real-time PCR, gene expression of PACAP in the PVT was measured in relation to this binge-type eating. Finally, using chemogenetics in PACAP-Cre transgenic mice, the effect of activation of PVT PACAP Males and females both engaged in binge-type eating with Ensure, although females engaged in this behavior to a greater degree than males. While females also had a higher baseline level of PVT PACAP mRNA than males, only males showed an increase in levels of PACAP after a history of exposure to Ensure, and only males showed a reduction in levels of PACAP immediately prior to a binge session. Conversely, activation of PACAP The present findings indicate that PVT PACAP
Identifiants
pubmed: 39340653
doi: 10.1007/s00213-024-06692-9
pii: 10.1007/s00213-024-06692-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIAAA NIH HHS
ID : R01AA028218
Pays : United States
Organisme : NIAAA NIH HHS
ID : F31AA031427
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
Allen Institute for Brain Science (2004) Allen Mouse Brain Atlas. Available online at: https://mouse.brain-map.org/search/index?fbclid=IwAR1f_D-imYpQaLkfrUVO9afEtQUx38-AtVl3JHh5CxZD0cKHDdt5P3St65E . Accessed 1 Sep 2024
American Psychiatric Association (2022) Binge-eating disorder. In Diagnostic and Statistical Manual of Mental Disorders (5th edn, text rev). https://doi.org/10.1176/appi.books.9780890425787
Babbs RK, Wojnicki FH, Corwin RL (2012) Assessing binge eating. An analysis of data previously collected in bingeing rats. Appetite 59:478–482. https://doi.org/10.1016/j.appet.2012.05.022
doi: 10.1016/j.appet.2012.05.022
pubmed: 22641146
pmcid: 3428474
Bake T, Morgan DG, Mercer JG (2014) Feeding and metabolic consequences of scheduled consumption of large, binge-type meals of high fat diet in the Sprague-Dawley rat. Physiol Behav 128:70–79. https://doi.org/10.1016/j.physbeh.2014.01.018
doi: 10.1016/j.physbeh.2014.01.018
pubmed: 24518863
pmcid: 3989043
Barson JR, Ho HT, Leibowitz SF (2015) Anterior thalamic paraventricular nucleus is involved in intermittent access ethanol drinking: role of orexin receptor 2. Addict Biol 20:469–481. https://doi.org/10.1111/adb.12139
doi: 10.1111/adb.12139
pubmed: 24712379
Barson JR, Poon K, Ho HT, Alam MI, Sanzalone L, Leibowitz SF (2017) Substance P in the anterior thalamic paraventricular nucleus: promotion of ethanol drinking in response to orexin from the hypothalamus. Addict Biol 22:58–69. https://doi.org/10.1111/adb.12288
doi: 10.1111/adb.12288
pubmed: 26223289
Barson JR, Mack NR, Gao WJ (2020) The paraventricular nucleus of the thalamus is an important node in the emotional processing network. Front Behav Neurosci 14:598469. https://doi.org/10.3389/fnbeh.2020.598469
doi: 10.3389/fnbeh.2020.598469
pubmed: 33192373
pmcid: 7658442
Ben-Ari Y, Brody Y, Kinor N, Mor A, Tsukamoto T, Spector DL, Singer RH, Shav-Tal Y (2010) The life of an mRNA in space and time. J Cell Sci 123:1761–1774. https://doi.org/10.1242/jcs.062638
doi: 10.1242/jcs.062638
pubmed: 20427315
pmcid: 2864715
Berner LA, Avena NM, Hoebel BG (2008) Bingeing, self-restriction, and increased body weight in rats with limited access to a sweet-fat diet. Obesity (Silver Spring) 16:1998–2002. https://doi.org/10.1038/oby.2008.328
doi: 10.1038/oby.2008.328
pubmed: 19186326
Boggiano MM, Artiga AI, Pritchett CE, Chandler-Laney PC, Smith ML, Eldridge AJ (2007) High intake of palatable food predicts binge-eating independent of susceptibility to obesity: an animal model of lean vs obese binge-eating and obesity with and without binge-eating. Int J Obes (Lond) 31:1357–1367. https://doi.org/10.1038/sj.ijo.0803614
doi: 10.1038/sj.ijo.0803614
pubmed: 17372614
Corwin RL, Wojnicki FH, Fisher JO, Dimitriou SG, Rice HB, Young MA (1998) Limited access to a dietary fat option affects ingestive behavior but not body composition in male rats. Physiol Behav 65:545–553. https://doi.org/10.1016/s0031-9384(98)00201-7
doi: 10.1016/s0031-9384(98)00201-7
pubmed: 9877422
Curtis GR, Coudriet JM, Sanzalone L, Mack NR, Stein LM, Hayes MR, Barson JR (2019) Short- and long-access palatable food self-administration results in different phenotypes of binge-type eating. Physiol Behav 212:112700. https://doi.org/10.1016/j.physbeh.2019.112700
doi: 10.1016/j.physbeh.2019.112700
pubmed: 31614159
pmcid: 6858592
Curtis GR, Oakes K, Barson JR (2020) Expression and distribution of neuropeptide-expressing cells throughout the rodent paraventricular nucleus of the thalamus. Front Behav Neurosci 14:634163. https://doi.org/10.3389/fnbeh.2020.634163
doi: 10.3389/fnbeh.2020.634163
pubmed: 33584216
Curtis GR, Gargiulo AT, Carpenter BA, Pirino BE, Hawks A, Coleman SA, Syed NA, Gupta A, Barson JR (2023) Sex-related differences in endogenous pituitary adenylate cyclase-activating polypeptide (PACAP) in the thalamic paraventricular nucleus: Implications for addiction neuroscience. Addict Neurosci 5 https://doi.org/10.1016/j.addicn.2022.100058
Dimitriou SG, Rice HB, Corwin RL (2000) Effects of limited access to a fat option on food intake and body composition in female rats. Int J Eat Disord 28:436–445. https://doi.org/10.1002/1098-108x(200012)28:4%3c436::aid-eat12%3e3.0.co;2-p
doi: 10.1002/1098-108x(200012)28:4<436::aid-eat12>3.0.co;2-p
pubmed: 11054791
Do-Monte FH, Minier-Toribio A, Quinones-Laracuente K, Medina-Colon EM, Quirk GJ (2017) Thalamic regulation of sucrose seeking during unexpected reward omission. Neuron 94(388–400):e4. https://doi.org/10.1016/j.neuron.2017.03.036
doi: 10.1016/j.neuron.2017.03.036
Freeman LR, Bentzley BS, James MH, Aston-Jones G (2021) Sex differences in demand for highly palatable foods: Role of the orexin system. Int J Neuropsychopharmacol 24:54–63. https://doi.org/10.1093/ijnp/pyaa040
doi: 10.1093/ijnp/pyaa040
pubmed: 32496559
Gao C, Gohel CA, Leng Y, Ma J, Goldman D, Levine AJ, Penzo MA (2023) Molecular and spatial profiling of the paraventricular nucleus of the thalamus. Elife 12 https://doi.org/10.7554/eLife.81818
Gargiulo AT, Badve PS, Curtis GR, Prino BE, Barson JR (2022) Inactivation of the thalamic paraventricular nucleus promotes place preference and sucrose seeking in male rats. Psychopharmacology 239:2659–2671. https://doi.org/10.1007/s00213-022-06160-2
doi: 10.1007/s00213-022-06160-2
pubmed: 35524009
pmcid: 9296579
Gupta A, Gargiulo AT, Curtis GR, Badve PS, Pandey S, Barson JR (2018) Pituitary adenylate cyclase-activating polypeptide-27 (PACAP-27) in the thalamic paraventricular nucleus is stimulated by ethanol drinking. Alcohol Clin Exp Res 42:1650–1660. https://doi.org/10.1111/acer.13826
doi: 10.1111/acer.13826
pubmed: 29969146
pmcid: 6120804
Hammack SE, Cheung J, Rhodes KM, Schutz KC, Falls WA, Braas KM, May V (2009) Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology 34:833–843. https://doi.org/10.1016/j.psyneuen.2008.12.013
doi: 10.1016/j.psyneuen.2008.12.013
pubmed: 19181454
pmcid: 2705919
Harris JA, Hirokawa KE, Sorensen SA, Gu H, Mills M, Ng LL, Bohn P, Mortrud M, Ouellette B, Kidney J, Smith KA, Dang C, Sunkin S, Bernard A, Oh SW, Madisen L, Zeng H (2014) Anatomical characterization of Cre driver mice for neural circuit mapping and manipulation. Front Neural Circuits 8:76. https://doi.org/10.3389/fncir.2014.00076
doi: 10.3389/fncir.2014.00076
pubmed: 25071457
pmcid: 4091307
Hawke Z, Ivanov TR, Bechtold DA, Dhillon H, Lowell BB, Luckman SM (2009) PACAP neurons in the hypothalamic ventromedial nucleus are targets of central leptin signaling. J Neurosci 29:14828–14835. https://doi.org/10.1523/JNEUROSCI.1526-09.2009
doi: 10.1523/JNEUROSCI.1526-09.2009
pubmed: 19940178
pmcid: 6666015
Hildebrandt BA, Fisher H, Ahmari SE (2023) Examination of onset trajectories and persistence of binge-like eating behavior in mice after intermittent palatable food exposure. Behav Neurosci 137:170–177. https://doi.org/10.1037/bne0000550
doi: 10.1037/bne0000550
pubmed: 36821355
pmcid: 10191968
Iglesias AG, Flagel SB (2021) The paraventricular thalamus as a critical node of motivated behavior via the hypothalamic-thalamic-striatal circuit. Front Integr Neurosci 15:706713. https://doi.org/10.3389/fnint.2021.706713
doi: 10.3389/fnint.2021.706713
pubmed: 34220458
pmcid: 8250420
Kelley AE, Baldo BA, Pratt WE (2005) A proposed hypothalamic-thalamic-striatal axis for the integration of energy balance, arousal, and food reward. J Comp Neurol 493:72–85. https://doi.org/10.1002/cne.20769
doi: 10.1002/cne.20769
pubmed: 16255002
Kessler RC, Berglund PA, Chiu WT, Deitz AC, Hudson JI, Shahly V, Aguilar-Gaxiola S, Alonso J, Angermeyer MC, Benjet C, Bruffaerts R, de Girolamo G, de Graaf R, Maria Haro J, Kovess-Masfety V, O’Neill S, Posada-Villa J, Sasu C, Scott K, Viana MC, Xavier M (2013) The prevalence and correlates of binge eating disorder in the World Health Organization World Mental Health Surveys. Biol Psychiatry 73:904–914. https://doi.org/10.1016/j.biopsych.2012.11.020
doi: 10.1016/j.biopsych.2012.11.020
pubmed: 23290497
pmcid: 3628997
Kooiker CL, Chen Y, Birnie MT, Baram TZ (2023) Genetic Tagging Uncovers a Robust, Selective Activation of the Thalamic Paraventricular Nucleus by Adverse Experiences Early in Life. Biol Psychiatry Glob Open Sci 3:746–755. https://doi.org/10.1016/j.bpsgos.2023.01.002
doi: 10.1016/j.bpsgos.2023.01.002
pubmed: 37881549
pmcid: 10593902
Kovacs KJ (2008) Measurement of immediate-early gene activation- c-fos and beyond. J Neuroendocrinol 20:665–672. https://doi.org/10.1111/j.1365-2826.2008.01734.x
doi: 10.1111/j.1365-2826.2008.01734.x
pubmed: 18601687
Kreisler AD, Garcia MG, Spierling SR, Hui BE, Zorrilla EP (2017) Extended vs. brief intermittent access to palatable food differently promote binge-like intake, rejection of less preferred food, and weight cycling in female rats. Physiol Behav 177:305–316. https://doi.org/10.1016/j.physbeh.2017.03.039
doi: 10.1016/j.physbeh.2017.03.039
pubmed: 28366814
Kreisler AD, Mattock M, Zorrilla EP (2018) The duration of intermittent access to preferred sucrose-rich food affects binge-like intake, fat accumulation, and fasting glucose in male rats. Appetite 130:59–69. https://doi.org/10.1016/j.appet.2018.07.025
doi: 10.1016/j.appet.2018.07.025
pubmed: 30063959
pmcid: 6168430
Labouebe G, Boutrel B, Tarussio D, Thorens B (2016) Glucose-responsive neurons of the paraventricular thalamus control sucrose-seeking behavior. Nat Neurosci 19:999–1002. https://doi.org/10.1038/nn.4331
doi: 10.1038/nn.4331
pubmed: 27322418
pmcid: 4964931
Le N, Hernandez J, Gastelum C, Perez L, Vahrson I, Sayers S, Wagner EJ (2021) Pituitary adenylate cyclase activating polypeptide inhibits A(10) dopamine neurons and suppresses the binge-like consumption of palatable food. Neuroscience 478:49–64. https://doi.org/10.1016/j.neuroscience.2021.09.016
doi: 10.1016/j.neuroscience.2021.09.016
pubmed: 34597709
Lezak KR, Roman CW, Braas KM, Schutz KC, Falls WA, Schulkin J, May V, Hammack SE (2014) Regulation of bed nucleus of the stria terminalis PACAP expression by stress and corticosterone. J Mol Neurosci 54:477–484. https://doi.org/10.1007/s12031-014-0269-8
doi: 10.1007/s12031-014-0269-8
pubmed: 24614974
pmcid: 4162870
Li S, Dong X, Kirouac GJ (2021) Extensive divergence of projections to the forebrain from neurons in the paraventricular nucleus of the thalamus. Brain Struct Funct 226:1779–1802. https://doi.org/10.1007/s00429-021-02289-6
doi: 10.1007/s00429-021-02289-6
pubmed: 34032911
pmcid: 8203552
MacLaren DA, Browne RW, Shaw JK, Krishnan Radhakrishnan S, Khare P, Espana RA, Clark SD (2016) Clozapine N-Oxide administration produces behavioral effects in Long-Evans rats: Implications for designing DREADD experiments. eNeuro 3 https://doi.org/10.1523/ENEURO.0219-16.2016
McGinty JF, Otis JM (2020) Heterogeneity in the paraventricular thalamus: The traffic light of motivated behaviors. Front Behav Neurosci 14:590528. https://doi.org/10.3389/fnbeh.2020.590528
doi: 10.3389/fnbeh.2020.590528
pubmed: 33177999
pmcid: 7596164
Miles OW, Thrailkill EA, Linden AK, May V, Bouton ME, Hammack SE (2018) Pituitary adenylate cyclase-activating peptide in the bed nucleus of the stria terminalis mediates stress-induced reinstatement of cocaine seeking in rats. Neuropsychopharmacology 43:978–986. https://doi.org/10.1038/npp.2017.135
doi: 10.1038/npp.2017.135
pubmed: 28656976
Millan EZ, Ong Z, McNally GP (2017) Paraventricular thalamus: Gateway to feeding, appetitive motivation, and drug addiction. Prog Brain Res 235:113–137. https://doi.org/10.1016/bs.pbr.2017.07.006
doi: 10.1016/bs.pbr.2017.07.006
pubmed: 29054285
Miyata A, Jiang L, Dahl RD, Kitada C, Kubo K, Fujino M, Minamino N, Arimura A (1990) Isolation of a neuropeptide corresponding to the N-terminal 27 residues of the pituitary adenylate cyclase activating polypeptide with 38 residues (PACAP38). Biochem Biophys Res Commun 170:643–648. https://doi.org/10.1016/0006-291x(90)92140-u
doi: 10.1016/0006-291x(90)92140-u
pubmed: 2383262
Morley JE, Horowitz M, Morley PM, Flood JF (1992) Pituitary adenylate cyclase activating polypeptide (PACAP) reduces food intake in mice. Peptides 13:1133–1135. https://doi.org/10.1016/0196-9781(92)90019-y
doi: 10.1016/0196-9781(92)90019-y
pubmed: 1494495
Mounien L, Do Rego JC, Bizet P, Boutelet I, Gourcerol G, Fournier A, Brabet P, Costentin J, Vaudry H, Jegou S (2009) Pituitary adenylate cyclase-activating polypeptide inhibits food intake in mice through activation of the hypothalamic melanocortin system. Neuropsychopharmacology 34:424–435. https://doi.org/10.1038/npp.2008.73
doi: 10.1038/npp.2008.73
pubmed: 18536705
Muller JM, Moos K, Baar T, Maier KC, Zumer K, Tresch A (2024) Nuclear export is a limiting factor in eukaryotic mRNA metabolism. PLoS Comput Biol 20:e1012059. https://doi.org/10.1371/journal.pcbi.1012059
doi: 10.1371/journal.pcbi.1012059
pubmed: 38753883
pmcid: 11135743
National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals (2011) Guide for the Care and Use of Laboratory Animals, 8th edn. National Academies Press, Washington (DC)
Paniccia JE, Vollmer KM, Green LM, Grant RI, Winston KT, Buchmaier S, Westphal AM, Clarke RE, Doncheck EM, Bordieanu B, Manusky LM, Martino MR, Ward AL, Rinker JA, McGinty JF, Scofield MD, Otis JM (2024) Restoration of a paraventricular thalamo-accumbal behavioral suppression circuit prevents reinstatement of heroin seeking. Neuron 112(772–785):e9. https://doi.org/10.1016/j.neuron.2023.11.024
doi: 10.1016/j.neuron.2023.11.024
Pauli JL, Chen JY, Basiri ML, Park S, Carter ME, Sanz E, McKnight GS, Stuber GD, Palmiter RD (2022) Molecular and anatomical characterization of parabrachial neurons and their axonal projections. Elife 11 https://doi.org/10.7554/eLife.81868
Paxinos G, Franklin KBJ (2004) The mouse brain in stereotaxic coordinates. 2nd ed., Compact ed. Boston: Academic Press
Perez-Ortin JE (2007) Genomics of mRNA turnover. Brief Funct Genomic Proteomic 6:282–291. https://doi.org/10.1093/bfgp/elm029
doi: 10.1093/bfgp/elm029
pubmed: 18216027
Rodriguez-Ortega E, Alcaraz-Iborra M, de la Fuente L, de Amo E, Cubero I (2019) Environmental enrichment during adulthood reduces sucrose binge-like intake in a high drinking in the dark phenotype (HD) in C57BL/6J mice. Front Behav Neurosci 13:27. https://doi.org/10.3389/fnbeh.2019.00027
doi: 10.3389/fnbeh.2019.00027
pubmed: 30828291
pmcid: 6384528
Roman CW, Lezak KR, Hartsock MJ, Falls WA, Braas KM, Howard AB, Hammack SE, May V (2014) PAC1 receptor antagonism in the bed nucleus of the stria terminalis (BNST) attenuates the endocrine and behavioral consequences of chronic stress. Psychoneuroendocrinology 47:151–165. https://doi.org/10.1016/j.psyneuen.2014.05.014
doi: 10.1016/j.psyneuen.2014.05.014
pubmed: 25001965
pmcid: 4342758
Scarpa LL, Bello NT (2023) Dietary-induced binge-like eating impairs acoustic startle responses to acute nisoxetine in male mice. Behav Pharmacol 34:411–423. https://doi.org/10.1097/FBP.0000000000000748
doi: 10.1097/FBP.0000000000000748
pubmed: 37578423
Schipper L, Harvey L, van der Beek EM, van Dijk G (2018) Home alone: a systematic review and meta-analysis on the effects of individual housing on body weight, food intake and visceral fat mass in rodents. Obes Rev 19:614–637. https://doi.org/10.1111/obr.12663
doi: 10.1111/obr.12663
pubmed: 29334694
Schreiber-Gregory DN, Lavender JM, Engel SG, Wonderlich SA, Crosby RD, Peterson CB, Simonich H, Crow S, Durkin N, Mitchell JE (2013) Examining duration of binge eating episodes in binge eating disorder. Int J Eat Disord 46:810–814. https://doi.org/10.1002/eat.22164
doi: 10.1002/eat.22164
pubmed: 23881639
pmcid: 3889648
Solmi M, Radua J, Stubbs B, Ricca V, Moretti D, Busatta D, Carvalho AF, Dragioti E, Favaro A, Monteleone AM, Shin JI, Fusar-Poli P, Castellini G (2021) Risk factors for eating disorders: an umbrella review of published meta-analyses. Braz J Psychiatry 43:314–323. https://doi.org/10.1590/1516-4446-2020-1099
doi: 10.1590/1516-4446-2020-1099
pubmed: 32997075
Spierling SR, Kreisler AD, Williams CA, Fang SY, Pucci SN, Kines KT, Zorrilla EP (2018) Intermittent, extended access to preferred food leads to escalated food reinforcement and cyclic whole-body metabolism in rats: Sex differences and individual vulnerability. Physiol Behav 192:3–16. https://doi.org/10.1016/j.physbeh.2018.04.001
doi: 10.1016/j.physbeh.2018.04.001
pubmed: 29654812
pmcid: 6019212
Stratford TR, Wirtshafter D (2013) Injections of muscimol into the paraventricular thalamic nucleus, but not mediodorsal thalamic nuclei, induce feeding in rats. Brain Res 1490:128–133. https://doi.org/10.1016/j.brainres.2012.10.043
doi: 10.1016/j.brainres.2012.10.043
pubmed: 23111346
Udo T, Grilo CM (2018) Prevalence and correlates of DSM-5-defined eating disorders in a nationally representative sample of U.S. adults. Biol Psychiatry 84:345–354. https://doi.org/10.1016/j.biopsych.2018.03.014
doi: 10.1016/j.biopsych.2018.03.014
pubmed: 29859631
pmcid: 6097933
Vertes RP, Hoover WB (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508:212–237. https://doi.org/10.1002/cne.21679
doi: 10.1002/cne.21679
pubmed: 18311787
Vu JP, Goyal D, Luong L, Oh S, Sandhu R, Norris J, Parsons W, Pisegna JR, Germano PM (2015) PACAP intraperitoneal treatment suppresses appetite and food intake via PAC1 receptor in mice by inhibiting ghrelin and increasing GLP-1 and leptin. Am J Physiol Gastrointest Liver Physiol 309:G816–G825. https://doi.org/10.1152/ajpgi.00190.2015
doi: 10.1152/ajpgi.00190.2015
pubmed: 26336928
pmcid: 4652141
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134. https://doi.org/10.1186/1471-2105-13-134
doi: 10.1186/1471-2105-13-134
pubmed: 22708584
pmcid: 3412702