PACAP in the BNST produces anorexia and weight loss in male and female rats

Neuropsychopharmacology

Volumn 39, Issue 7, 2014, Pages 1614-1623

  Kocho Schellenberg, Margaret ^a   Lezak, Kimberly R ^a   Harris, Olivia M ^a   Roelke, Erin ^a   Gick, Niklas ^a   Choi, Inyop ^a   Edwards, Shaquille ^a   Wasserman, Emily ^a   Toufexis, Donna J ^a   Braas, Karen M ^b   May, Victor ^b   Hammack, Sayamwong E ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

bed nucleus of the stria terminalis; Extended amygdala; pituitary adenylate cyclase activating polypeptide

Indexed keywords

ESTRADIOL; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANOREXIA; ARTICLE; BED NUCLEUS OF THE STRIA TERMINALIS; BODY WEIGHT; BRAIN NUCLEUS; CONTROLLED STUDY; DOSE RESPONSE; ESTRADIOL BLOOD LEVEL; FEMALE; FLUID INTAKE; FOOD INTAKE; LATERAL BRAIN VENTRICLE; MALE; NONHUMAN; POTENTIAL DIFFERENCE; PRIORITY JOURNAL; RAT; STRIA TERMINALIS; WEIGHT CHANGE; WEIGHT GAIN; WEIGHT REDUCTION; ANALYSIS OF VARIANCE; ANIMAL; CHEMICALLY INDUCED; DRUG ADMINISTRATION ROUTE; DRUG EFFECTS; EATING; OVARIECTOMY; PHYSIOLOGY; SEPTUM NUCLEUS; SEX DIFFERENCE; SPRAGUE DAWLEY RAT; TOXICITY;

ANALYSIS OF VARIANCE; ANIMALS; ANOREXIA; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; EATING; ESTRADIOL; FEMALE; MALE; NEUROTRANSMITTER AGENTS; OVARIECTOMY; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RATS; RATS, SPRAGUE-DAWLEY; SEPTAL NUCLEI; SEX FACTORS; WEIGHT LOSS;

EID: 84900557248     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.8     Document Type: Article

References (67)

1. Amir S, Lamont EW, Robinson B, Stewart J (2004). A circadian rhythm in the expression of PERIOD2 protein reveals a novel SCN-controlled oscillator in the oval nucleus of the bed nucleus of the stria terminalis. J Neurosci 24: 781-790.
2. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E et al (2005). Strategies and methods for rese arch on sex differences in brain and behavior. Endocrinology 146: 1650-1673.
3. Bingham B, Myung C, Innala L, Gray M, Anonuevo A, Viau V (2011). Androgen receptors in the posterior bed nucleus of the s tria terminalis increase neuropeptiDe expression and the stress-induced activation of the paraventricular nucleus of the hypothalamus. Neuropsychopharmacology 36: 1433-1443.
4. Carvalho-Netto EF, Myers B, Jones K, Solomon MB, Herman JP (2011). Sex differences in synaptic plasticity in stress-responsive brain regions following chronic variable stress. Physiol Behav 104: 242-247.
5. Chance WT, Thompson H, Thomas I, Fischer JE (1995). Anorectic and neurochemical effects of pituitary aDenylate-cyclase activating polypeptiDe in rats. PeptiDes 16: 1511-1516.
6. Cho JH, Zushida K, Shumyatsky GP, Carlezon WA Jr., Meloni EG, Bolshakov VY (2012). Pituitary aDenylate cyclase-activating polypeptiDe induces postsynaptically expressed potentiation in the intra-amygdala circuit. J Ne urosci 32: 14165-14177.
7. Choi DC, Evanson NK, Furay AR, Ulrich-Lai YM, OstranDer MM, Herman JP (2008a ). The anteroventral bed nucleus of the stria terminalis differentially regulates hypothalamic-pitu itary-adrenocortical axis responses to acute and chronic stress. Endocrinology 149: 818-826.
8. Choi DC, Furay AR, Evanson NK, OstranDer MM, Ulrich-Lai YM, Herman JP (2007). Bed nucleus of the stri a terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: Implications for the integration of limbic inputs. J Neurosci 27: 2025-2034.
9. Choi DC, Furay AR, Evanson NK, Ulrich-Lai YM, Nguyen MM, OstranDer MM et al (2008b ). The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamicpituitary-adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendoc rinology 33: 659-669.
10. Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O?Donohue TL (1985). The anatomy of neuropeptiDe-Ycontaining neurons in rat brain. Neuroscience 15: 1159-1181.
11. Ciccocioppo R, FeDeli A, Economidou D, Policani F, Weiss F, Massi M (2003). The bed nucleus is a neuroanatomical substrate for the anorectic effect of corticotropin-releasing factor and for its rev ersal by nociceptin/orphanin FQ. J Neurosci 23: 9445-9451.
12. Coburn-Litvak PS, Pothakos K, Tata DA, McCloskey DP, AnDerson BJ (2003). Chronic administration of corticosterone impairs spatial reference memory before spatial working memory in rats. Neurobiol Learn Mem 80: 11-23.
13. Del Abril A, Segovia S, Guillamon A (1987). The bed nucleus of the stria terminalis in the rat: Regional sex differences control led by gonadal steroids early after birth. Brain Res 429: 295-300.
14. Dong HW, Petrovich GD, Watts AG, Swanson LW (2001). Basic organization of projections from the oval and fusiform nuclei of the bed nucl ei of the stria terminalis in adult rat brain. J Comp Neurol 436: 430-455.
15. Dong HW, Swanson LW (2004). Projections from bed nuclei of the stria terminalis, posterior division: Implications for cerebral hemisphe re regulation of Defensive and reproductive behaviors. J Comp Neurol 471: 396-433.
16. Dore R, Iemolo A, Smith KL, Wang X, Cottone P, Sabino V (2013). CRF mediates the anxiogenic and anti-rewarding, but not the anorectic effects of PACAP. Neuropsychopharmacology 38: 2160-2169.
17. Gelez H, Poirier S, Facchinetti P, Allers KA, Wayman C, Bernabe J et al (2010). Neuroanatomical distribution of the me lanocortin-4 receptors in male and female roDent brain. J Chem Neuroanat 40: 310-324.
18. Hammack SE, Cheung J, RhoDes KM, Schutz KC, Falls WA, Braas KM et al (2009). Chronic stress increases pi tuitary 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: 83 3-843.
19. Hammack SE,Roman CW,Lezak KR,Kocho-Shellenberg M,Grimmig B,Falls WA,et al (2010, Roles for pituitary aDenylate cyclase-activating peptiDe (PACAP) expression and signaling in the bed nucleus of the st ria terminalis (BNST) in mediating the behavioral consequences of chronic stress , J Mol Neurosci ,42, 327-340.
20. Hannibal J, Mikkelsen JD, Clausen H, Holst JJ, Wulff BS, Fahrenkrug J (1995). Gene e xpression of pituitary aDenylate cyclase activating polypeptiDe (PACAP) in the rat hypothalamus. Regul Pept 55: 133-148.
21. Harmar AJ (2003). An essential role for peptiDergic signalling in the control of circadian rhythms in the suprachiasmatic nuclei. J Neuroendocrinol 15: 335-338.
22. Hashimoto R, Hashimoto H, Shintani N, Chiba S, Hattori S, Okada T et al (2007). Pituitary aDenylate cyclase-activating pol ypeptiDe is associated with schizophrenia. Mol Psychiatry 12: 1026-1032.
23. Hashimoto R, Hashimoto H, Shintani N, Ohi K, Hori H, Saitoh O et al (2010). Possible association between the pituitary ad enylate cyclase-activating polypeptiDe (PACAP) gene and major Depressive disorDer. Neurosci Lett 468: 300-302.
24. Haskell-Luevano C, Chen P, Li C, Chang K, Smith MS, Cameron JL et al (1999). Ch aracterization of the neuroanatomical distribution of agouti-related protein immunoreactivity in the rhesus monkey and the rat. Endocrinology 140: 1408-1415.
25. Herman JP, OstranDer MM, Mueller NK, Figueiredo H (2005). Limbic system mechanisms of stress regulation: Hypothalamopituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29: 1201-1213.
26. Hines M, Allen LS, Gorski RA (1992). Sex diffe rences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res 579: 321-326.
27. Jennings JH, Rizzi G, Stamatakis AM, Ung RL, Stuber GD (2013). The inhibitory circuit architecture of the lateral hypothalamus orchestrates feeding. Science 341: 1517-1521.
28. Kalin NH, Shelton SE, Fox AS, Oakes TR, Davidson RJ (2005). Brain regions associated wit h the expression and contextual regulation of anxiety in primates. Biol Psychiatry 58: 796-804.
29. Kessler RC, Berglund P, Demler O, Jin R, Walters EE (2005). Lifetime prevalence and age-of-onset distributionsof DSM-IV disorDers in the national comorbidity survey replication. Arch Gen Psychiatry 62: 593-602.
30. Kozicz T, Vigh S, Arimura A (1997). Axon terminals containing PACAP-and VIP-immunoreactivity fo rm synapses with CRFimmunoreactive neurons in the dorsolateral division of the bed nucleus of the stria terminalis in the rat. Brain Res 767: 109-119.
31. Kozicz T, Vigh S, Arimura A (1998). Immunohistochemical eviDence for PACAP and VIP interaction with met-enkephalin and CRF containing neurons in the bed nucleus of the stria terminalis. Ann N Y Acad Sci 865: 523-528.
32. Krahn DD, Gosnell BA, Majchrzak MJ (1990). The anorectic effects of CRH and restraint stress Decrease with repeated exposures. Biol Psychiatry 27: 1094-1102.
33. Krawczyk M, Sharma R, Mason X, Debacker J, Jones AA, Dumont EC (2011). A switch in t he neuromodulatory effects of dopamine in the oval bed nucleus of the stria terminalis associated with cocaine self-administration in rats. J Neurosci 31: 8928-8935.
34. Lim MM, Tsivkovskaia NO, Bai Y, Young LJ, Ryabinin AE (2006). Distribution of corticotropin-releasing factor and urocortin 1 in the vole brain. Brain Behav Evol 68: 229-240.
35. Marti O, Ar mario A (1997). Influence of regularity of exposure to chronic stress on the pattern of habituation of pituitary-adrenal hormones, prolactin and glucose. Stress 1: 179-189.
36. Marti O, Marti J, Armario A ( 1994). Effects of chronic stress on food intake in rats: Influence of stressor intensity and duration of daily exposure. Physiol Behav 55: 747-753.
37. Masuo Y, Suzuki N, Matsumoto H, Tokito F, Matsumoto Y, Tsuda M et al (1993). Regional distribution of pituitary aDenylate cyclase activating polypeptiDe (PACAP) in the rat central nervous system as Determined by sandwich-enzyme immunoassay. Brain Res 602: 57-63.
38. Matsuda K, Maruyama K, Miura T, Uchiyama M, Shioda S (2005a ). Anorexigenic action of pituitary aDenylate cyclase-activating polypeptiDe (PACAP) in the goldfish: Feeding-induced changes in the expression of mRNAs for PACAP and it s receptors in the brain, and locomotor response to central injection. Neurosci Lett 386: 9-13.
39. Matsuda K, Maruyama K, Nakamachi T, Miura T, Uchiyama M, Shioda S (2005b ). Inhibitory effects of p ituitary aDenylate cyclase-activating polypeptiDe (PACAP) and vasoactive intestinal peptiDe (VIP) on food intake in the goldfish, Carassius auratus. PeptiDes 26: 1611-1616.
40. McLean CP, Asnaani A, Litz BT, Hofmann SG (2011). GenDer differences in anxiety disorDers: Prevalence, course of illness, comorbidity and burDen of illness. J Psychiatr Res 45: 1027-1035.
41. Mertens I,Husson SJ,Janssen T,LinDemans M,Schoofs L,2007, PACAP and PDF signaling in the regulation of mammalian and insect circadian rhythms, PeptiDes,28, 1775-1783.
42. Michopoulos V, Higgins M, Toufexis D, Wilson ME (2012). Social subordination produces distinct stress-related phenotypes in female rhesus monkeys. Psychoneuroendocrinology 37: 1071-1085.
43. Mizuno Y, Kondo K, Terashima Y, Arima H, Murase T, Oiso Y (1998). Anorectic effect of pituitary aDenylate cyclase activating polypeptiDe (PACAP) in rats: Lack of eviDence for involvement of hypothalamic neuropeptiDe gene expression. J Neuroendocrinol 10: 611-616.
44. Morley JE, Horowitz M, Morley PM, Flood JF (1992). Pituitary aDenylate cyclase activating polypeptiDe (PACAP) reduces food intake in mice. PeptiDes 13: 1133-1135.
45. Mounien L, Do Rego JC, Bizet P, Boutelet I, Gourcerol G, Fournier A et al (2009). Pituitary aDenylate cyclase-activating polypeptiDe inhibits food intake in mice through activation of the hypothalamic m elanocortin system. Neuropsychopharmacology 34: 424-435.
46. Pego JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OFX, Sousa N (2008). Dissociation of the morphological correlates of stressinduced an xiety and fear. Eur J Neurosci 27: 1503-1516.
47. Piggins HD, Stamp JA, Burns J, Rusak B, Semba K (1996). Distribution of pituitary aDenylate cyclase activating polypeptiDe (PACAP) immunoreactivity in t he hypothalamus and extenDed amygdala of the rat. J Comp Neurol 376: 278-294.
48. Radley JJ, Gosselink KL, Sawchenko PE (2009). A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J Neurosci 29: 7330-7340.
49. Radley JJ, Sawchenko PE (2011). A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response. J Neurosci 31: 9683-9695.
50. Resch JM, Maunze B, Gerhardt AK, Magnuson SK, Phillips KA, Choi S (2013). Intrahypothalamic pituitary aDenylate cyclaseactivating polype ptiDe regulates energy balance via site-specific actions on feeding and metabolism. Am J Physiol Endocrinol Metab 305: E1452-E1463.
51. Ressler KJ, Mercer KB, Bradley B, Jovanovic T, Mahan A, Kerley K et al (2011). Post-traumatic stress disorDer is associated with PACAP and the PAC1 receptor. Nature 470: 492-497.
52. Richard S, Martinez-Garcia F, Lanuza E, Davies DC (2004). Distribution of corticotrop in-releasing factor-immunoreactive neurons in the central nervous system of the domestic chicken and Japanese quail. J Comp Neurol 469: 559-580.
53. Roman CW, Lezak KR, Kocho-Schellenberg M, Garret MA, Braas K, May V et al (2012). Excitotoxic lesions of the bed nucleus of the stria terminalis (BNST) attenuate the effects of repeated stress on weight gain: EviDence for the recruitment of BNST activity by repeated, but not acute, stress. Behav Br ain Res 227: 300-304.
54. Shioda S, Shuto Y, Somogyvari-Vigh A, Legradi G, Onda H, Coy DH et al (1997). Localization and gene expression of the receptor for pituitary aDenylate cyclase-activating poly peptiDe in the rat brain. Neurosci Res 28: 345-354.
55. Shughrue PJ, Lane MV, Merchenthaler I (1997). Comparative distribution of estrogen receptor-alpha and-beta mRNA in the rat central nervous system. J Comp Neurol 388: 507-525.
56. Simerly RB (1993). Distribution and regulation of steroid hormone receptor gene expression in the central nervous system. Adv Neurol 59: 207-226.
57. Somerville LH, Whalen PJ, Kelley WM (2010). Human bed nucleus of the stria terminalis inDexes hypervigilant threat monitoring. Biol Psychiatry 68: 416-424.
58. Straube T, Mentzel HJ, Miltner WHR (2007). Waiting for spiDers: Brain activation during anticipatory anxiety in spiDer phobics. Neuroimage 37: 1427-1436.
59. Strom JO, Theodorsson E, Theodorsson A (2008). OrDer of magnituDe differences between methods for maint aining physiological 17beta-oestradiol concentrations in ovariectomized rats. Scand J Clin Lab Invest 68: 814-822.
60. Stroth N, Holighaus Y, Ait-Ali D, EiDen LE (2011). PACAP: A master regulator of neuroendocrine stress circuits and the cellular stress response. Ann N Y Acad Sci 1220: 49-59.
61. Tachibana T, Saito S, Tomonaga S, Takagi T, Saito ES, Boswell T et al (2003a ). Intracerebroventricular inj ection of vasoactive intestinal peptiDe and pituitary aDenylate cyclase-activating polypeptiDe inhibits feeding in chicks. Neurosci Lett 339: 203-206.
62. Tachibana T,Tomonaga S,Oikawa D,Saito S,Takagi T,Saito ES,et al, 2003, Pituitary aDenylate cyclase activating polypeptiDe and vasoactive intestinal peptiDe inhibit feeding in the chick brain by different mec hanisms, Neurosci Lett,348, 25-28.
63. Turner SW, Wen C, Li M, Fraser TB, Whitworth JA (1998). Adrenocorticotrophin dose-response relationships in the rat: Haemodynamic, metabolic and hormonal effects. J Hypertens 16: 593-600.
64. Valassi E, Scacchi M, Cavagnini F (2008). Neuroendocrine control of food intake. Nutr Metab Cardiovasc Dis 18: 158-168.
65. Vyas A, Bernal S, Ch attarji S (2003). Effects of chronic stress on Dendritic arborization in the central and extenDed amygdala. Brain Res 965: 290-294.
66. WadDell J, Morris RW, Bouton ME (2006). Effects of bed nucleus of the stria terminalis lesions on conditioned anxiety: Aversive conditioning with long-duration conditional stimuli and reinstatement of extinguished fear. Behav Neurosci 120: 324-336.
67. Walker DL, Toufexis DJ, Davis M (2003). Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463: 199-216.