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Stress
The International Journal on the Biology of Stress
Volume 19, 2016 - Issue 4: Smolenice Symposium
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Original Article

Activation of the HPA axis and depression of feeding behavior induced by restraint stress are separately regulated by PACAPergic neurotransmission in the mouse

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Pages 374-382 | Received 26 Dec 2015, Accepted 02 Apr 2016, Published online: 26 May 2016

References

  • Agarwal A, Halvorson LM, Legradi G. (2005). Pituitary adenylate cyclase-activating polypeptide (PACAP) mimics neuroendocrine and behavioral manifestations of stress: evidence for PKA-mediated expression of the corticotropin-releasing hormone (CRH) gene. Brain Res Mol Brain Res 138:45–57.
  • Arimura A. (1992). Pituitary adenylate cyclase-activating polypeptide (PACAP): discovery and current status of research. Regul Peptides 37:287–303.
  • Arimura A, Somogyvari-Vigh A, Miyata A, Mizuno K, Coy DH, Kitada C. (1991). Tissue distribution of PACAP as determined by RIA: highly abundant in the rat brain and testes. Endocrinology 129:2787–9.
  • Das M, Vihlen CS, Legradi G. (2007). Hypothalamic and brainstem sources of pituitary adenylate cyclase-activating polypeptide nerve fibers innervating the hypothalamic paraventricular nucleus in the rat. J Comp Neurol 500:761–76.
  • 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 38:2160–9.
  • Dun NJ, Miyazaki T, Tang H, Dun EC. (1996). Pituitary adenylate cyclase activating polypeptide immunoreactivity in the rat spinal cord and medulla: implication of sensory and autonomic functions. Neuroscience 73:677–86.
  • Gaszner B, Kormos V, Kozicz T, Hashimoto H, Reglodi D, Helyes Z. (2012). The behavioral phenotype of pituitary adenylate-cyclase activating polypeptide-deficient mice in anxiety and depression tests is accompanied by blunted c-Fos expression in the bed nucleus of the stria terminalis, central projecting Edinger-Westphal nucleus, ventral lateral septum, and dorsal raphe nucleus. Neuroscience 202:283–99.
  • Geerling JC, Shin JW, Chimenti PC, Loewy AD. (2010). Paraventricular hypothalamic nucleus: axonal projections to the brainstem. J Comp Neurol 518:1460–99.
  • Grinevich V, Fournier A, Pelletier G. (1997). Effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on corticotropin-releasing hormone (CRH) gene expression in the rat hypothalamic paraventricular nucleus. Brain Res 773:190–6.
  • Hamelink C, Tjurmina O, Damadzic R, Young WS, Weihe E, Lee H-W, Eiden LE. (2002). Pituitary adenylate cyclase activating polypeptide is a sympathoadrenal neurotransmitter involved in catecholamine regulation and glucohomeostasis. Proc Natl Acad Sci USA 99:461–6.
  • 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 34:833–43.
  • Hammack SE, May V. (2015). Pituitary adenylate cyclase activating polypeptide in stress-related disorders: data convergence from animal and human studies. Biol Psychiatry 78:167–77.
  • Hammack SE, Roman CW, Lezak KR, Kocho-Shellenberg M, Grimmig B, Falls WA, Braas K, May V. (2010). Roles for pituitary adenylate cyclase-activating peptide (PACAP) expression and signaling in the bed nucleus of the stria terminalis (BNST) in mediating the behavioral consequences of chronic stress. J Mol Neurosci 42:327–40.
  • Hannibal J. (2002). Pituitary adenylate cyclase-activating peptide in the rat central nervous system: an immunohistochemical and in situ hybridization study. J Comp Neurol 453:389–417.
  • Herman JP, Cullinan WE. (1997). Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78–84.
  • Herman JP, Ostrander MM, Mueller NK, Figueiredo H. (2005). Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29:1201–13.
  • Jiang SZ, Eiden LE. (in press). PACAPergic synaptic signaling and circuitry mediating mammalian responses to psychogenic and systemic stressors. In: Reglodi D, Tamas A, editors. Pituitary adenylate cyclase activating polypeptide – PACAP. New York: Springer Nature.
  • Kocho-Schellenberg M, Lezak KR, Harris OM, Roelke E, Gick N, Choi I, Edwards S, et al. (2014). PACAP in the BNST produces anorexia and weight loss in male and female rats. Neuropsychopharmacology 39:1614–23.
  • Kozicz T, Vigh S, Arimura A. (1997). Axon terminals containing PACAP- and VIP-immunoreactivity form synapses with CRF-immunoreactive neurons in the dorsolateral division of the bed nucleus of the stria terminalis in the rat. Brain Res 767:109–19.
  • Legradi G, Das M, Giunta B, Hirani K, Mitchell EA, Diamond DM. (2007). Microinfusion of pituitary adenylate cyclase-activating polypeptide into the central nucleus of amygdala of the rat produces a shift from an active to passive mode of coping in the shock-probe fear/defensive burying test. Neural Plasticity 2007:79102–13.
  • Legradi G, Hannibal J, Lechan RM. (1998). Pituitary adenylate cyclase-activating polypeptide-nerve terminals densely innervate corticotropin-releasing hormone-neurons in the hypothalamic paraventricular nucleus of the rat. Neurosci Lett 246:145–8.
  • Lehmann ML, Mustafa T, Eiden AM, Herkenham M, Eiden LE. (2013). PACAP-deficient mice show attenuated corticosterone secretion and fail to develop depressive behavior during chronic social defeat stress. Psychoneuroendocrinology 38:702–15.
  • 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 54:477–84.
  • Mustafa T, Eiden LE. (2006). The secretin superfamily: PACAP, VIP and related peptides. In: Lim R, editor. Handbook of neurochemistry and molecular neurobiology: XIII neuroactive peptides and proteins. Heidelberg: Springer. p. 1–36.
  • Mustafa T, Jiang SZ, Eiden AM, Weihe E, Thistlethwaite I, Eiden LE. (2015). Impact of PACAP and PAC1 receptor deficiency on the neurochemical and behavioral effects of acute and chronic restraint stress in male C57BL/6 mice. Stress 18:408–18.
  • Norrholm SD, Das M, Legradi G. (2005). Behavioral effects of local microinfusion of pituitary adenylate cyclase activating polypeptide (PACAP) into the paraventricular nucleus of the hypothalamus (PVN). Regul Pept 128:33–41.
  • Piggins HD, Stamp JA, Burns J, Rusak B, Semba K. (1996). Distribution of pituitary adenylate cyclase activating polypeptide (PACAP) immunoreactivity in the hypothalamus and extended amygdala of the rat. J Comp Neurol 376:278–94.
  • Radley JJ. (2012). Toward a limbic cortical inhibitory network: implications for hypothalamic-pituitary-adrenal responses following chronic stress. Front Behav Neurosci 6:7.
  • Radley JJ, Arias CM, Sawchenko PE. (2006). Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 26:12967–76.
  • Resch JM, Maunze B, Phillips KA, Choi S. (2014). Inhibition of food intake by PACAP in the hypothalamic ventromedial nuclei is mediated by NMDA receptors. Physiol Behav 133:230–5.
  • Ressler KJ, Mercer KB, Bradley B, Jovanovic T, Mahan A, Kerley K, Norrholm SD, et al. (2011). Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 470:492–7.
  • 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 47:151–65.
  • Schafer MK, Mahata SK, Stroth N, Eiden LE, Weihe E. (2010). Cellular distribution of chromogranin A in excitatory, inhibitory, aminergic and peptidergic neurons of the rodent central nervous system. Regul Pept 165:36–44.
  • Seiglie MP, Smith KL, Blasio A, Cottone P, Sabino V. (2015). Pituitary adenylate cyclase-activating polypeptide induces a depressive-like phenotype in rats. Psychopharmacology (Berl) 232:3821–31.
  • Stroth N, Eiden LE. (2010). Stress hormone synthesis in mouse hypothalamus and adrenal gland triggered by restraint is dependent on pituitary adenylate cyclase-activating polypeptide signaling. Neuroscience 165:1025–30.
  • Stroth N, Holighaus Y, Ait-Ali D, Eiden LE. (2011a). PACAP: a master regulator of neuroendocrine stress circuits and the cellular stress response. Ann N Y Acad Sci 1220:49–59.
  • Stroth N, Kuri BA, Mustafa T, Chan SA, Smith CB, Eiden LE. (2013). 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 154:330–9.
  • Stroth N, Liu Y, Aguilera G, Eiden LE. (2011b). Pituitary adenylate cyclase-activating polypeptide (PACAP) controls stimulus-transcription coupling in the hypothalamic-pituitary-adrenal axis to mediate sustained hormone secretion during stress. J Neuroendocrinol 23:944–55.
  • Tsukiyama N, Saida Y, Kakuda M, Shintani N, Hayata A, MoritaY, Tanida M, et al. (2011). PACAP centrally mediates emotional stress-induced corticosterone responses in mice. Stress 14:368–75.
  • Ulrich-Lai YM, Herman JP. (2009). Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397–409.
  • Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, Vaudry H. (2000). Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Revs 52:269–324.
  • Vigh S, Arimura A, Koves K, Somogyvari-Vigh A, Sitton J, Fermin CD. (1991). Immunohistochemical localization of the neuropeptide, pituitary adenylate cyclase activating polypeptide (PACAP), in human and primate hypothalamus. Peptides 12:313–18.

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