Endogenous cannabinoid signaling is essential for stress adaptation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 20, 2010, Pages 9406-9411

  Hill, Matthew N ^a   McLaughlin, Ryan J ^a   Bingham, Brenda ^a   Shrestha, Lalita ^b   Lee, Tiffany T Y ^a   Gray, J Megan ^a   Hillard, Cecilia J ^b   Gorzalka, Boris B ^a   Viau, Victor ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Amygdala; Corticosterone; Endocannabinoid; Habituation; Hypothalamic pituitary adrenal axis

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ANANDAMIDE; CANNABINOID 1 RECEPTOR ANTAGONIST; CORTICOSTERONE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE RELEASE; HABITUATION; HORMONE RESPONSE; HYDROLYSIS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; LIMBIC SYSTEM; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STRESS;

ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; ARACHIDONIC ACIDS; BENZAMIDES; CARBAMATES; CORTICOSTERONE; ENDOCANNABINOIDS; MALE; PIPERIDINES; POLYUNSATURATED ALKAMIDES; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 77952717194     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0914661107     Document Type: Article

References (42)

1. Chrousos GP (2009) Stress anddisorders of the stress system. Nat Rev Endocrinol 5:374-381.
2. McEwen BS (2005) Glucocorticoids, depression, and mood disorders: Structural remodeling in the brain. Metabolism 54(5, Suppl 1)20-23.
3. Feder A, Nestler EJ, Charney DS (2009) Psychobiology and molecular genetics of resilience. Nat Rev Neurosci 10:446-457.
4. Girotti M, et al. (2006) Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain. Neuroscience 138:1067-1081. (Pubitemid 43363525)
5. Jaferi A, Bhatnagar S (2006) Corticosterone can act at the posterior paraventricular thalamus to inhibit hypothalamic-pituitary-adrenal activity in animals that habituate to repeated stress. Endocrinology 147:4917-4930. (Pubitemid 44402199)
6. Dallman MF (2007) Modulation of stress responses: How we cope with excess glucocorticoids. Exp Neurol 206:179-182.
7. Hill MN, McEwen BS (2009) Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog Neuropsychopharmacol Biol Psychiatry, in press.
8. Patel S, Hillard CJ (2008) Adaptations in endocannabinoid signaling in response to repeated homotypic stress: A novel mechanism for stress habituation. Eur J Neurosci 27:2821-2829. (Pubitemid 351832221)
9. Ahn K, McKinney MK, Cravatt BF (2008) Enzymatic pathways that regulate endocannabinoid signaling in the nervous system. Chem Rev 108:1687-1707. (Pubitemid 351796405)
10. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066. (Pubitemid 36828930)
11. Gorzalka BB, Hill MN, Hillard CJ (2008) Regulation of endocannabinoid signaling by stress: Implications for stress-related affective disorders. Neurosci Biobehav Rev 32:1152-1160.
12. Steiner MA, Wotjak CT (2008) Role of the endocannabinoid system in regulation of the hypothalamic-pituitary-adrenocortical axis. Prog Brain Res 170:397-432. (Pubitemid 352010245)
13. Patel S, Roelke CT, Rademacher DJ, Cullinan WE, Hillard CJ (2004) Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamicpituitary- adrenal axis. Endocrinology 145:5431-5438. (Pubitemid 39564580)
14. Cota D, et al. (2007) Requirement of cannabinoid receptor type1 for the basal modulation of hypothalamic-pituitary-adrenal axis function. Endocrinology 148:1574-1581. (Pubitemid 46457104)
15. Steiner MA, Marsicano G, Wotjak CT, Lutz B (2008) Conditional cannabinoid receptor type 1 mutants reveal neuron subpopulation-specific effects on behavioral and neuroendocrine stress responses. Psychoneuroendocrinology 33:1165-1170.
16. Patel S, Roelke CT, Rademacher DJ, Hillard CJ (2005) Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Eur J Neurosci 21:1057-1069. (Pubitemid 40461057)
17. Kamprath K, et al. (2006) Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci 26:6677-6686. (Pubitemid 44315229)
18. Fride E, Suris R, Weidenfeld J, Mechoulam R (2005) Differential response to acute and repeated stress in cannabinoid CB1 receptor knockout newborn and adult mice. Behav Pharmacol 16:431-440. (Pubitemid 41404815)
19. Kathuria S, et al. (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9:76-81.
20. Alvarez-Jaimes L, Stouffer DG, Parsons LH (2009) Chronic ethanol treatment potentiates ethanol-induced increases in interstitial nucleus accumbens endocannabinoid levels in rats. J Neurochem 111:37-48.
21. Hill MN, et al. (2009) Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology 34:2733-2745.
22. Dhabhar FS, McEwen BS, Spencer RL (1997) Adaptation to prolonged or repeated stress - comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroendocrinology 65:360-368.
23. Cole MA, et al. (2000) Selective blockade of the mineralocorticoid receptor impairs hypothalamic-pituitary-adrenal axis expression of habituation. J Neuroendocrinol 12: 1034-1042.
24. Bechtold AG, Patel G, Hochhaus G, Scheuer DA (2009) Chronic blockade of hindbrain glucocorticoid receptors reduces blood pressure responses to novel stress and attenuates adaptation to repeated stress. Am J Physiol Regul Integr Comp Physiol 296: R1445-R1454.
25. Ottenweller JE, Servatius RJ, Natelson BH (1994) Repeated stress persistently elevates morning, but not evening, plasma corticosterone levels in male rats. Physiol Behav 55: 337-340.
26. Bhatnagar S, et al. (2000) A cholecystokinin-mediated pathway to the paraventricular thalamus is recruited in chronically stressed rats and regulates hypothalamicpituitary- adrenal function. J Neurosci 20:5564-5573. (Pubitemid 30457753)
27. Patel S, Kingsley PJ, Mackie K, Marnett LJ, Winder DG (2009) Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala. Neuropsychopharmacology 34: 2699-2709.
28. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397-409.
29. French SJ, Hailstone JC, Totterdell S (2003) Basolateral amygdala efferents to the ventral subiculum preferentially innervate pyramidal cell dendritic spines. Brain Res 981:160-167.
30. Wright CI, Beijer AV, Groenewegen HJ (1996) Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J Neurosci 16:1877-1893.
31. McDonald AJ (1991) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44:1-14.
32. Evanson NK, Ulrich-Lai YM, Furay AR, Tasker JG, Herman JP (2007) Hypothalamic paraventricular cannabinoid receptor signaling in fast feedback inhibition of the hypothalamus-pituitary-adrenal axis response to acute restraint stress. Soc Neurosci Abs 197:195.
33. Di S, Malcher-Lopes R, Halmos KC, Tasker JG (2003) Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: A fast feedback mechanism. J Neurosci 23:4850-4857.
34. Brown AJ, Robin Hiley C (2009) Is GPR55 an anandamide receptor? Vitam Horm 81: 111-137.
35. Tóth A, Blumberg PM, Boczán J (2009) Anandamide and the vanilloid receptor (TRPV1). Vitam Horm 81:389-419.
36. McIntyre CK, Power AE, Roozendaal B, McGaugh JL (2003) Role of the basolateral amygdala in memory consolidation. Ann N Y Acad Sci 985:273-293. (Pubitemid 36521121)
37. Campolongo P, et al. (2009) Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc Natl Acad Sci USA 106:4888-4893.
38. Ganon-Elazar E, Akirav I (2009) Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. J Neurosci 29:11078-11088.
39. Bingham B, Viau V (2008) Neonatal gonadectomy and adult testosterone replacement suggest an involvement of limbic arginine vasopressin and androgen receptors in the organization of the hypothalamic-pituitary-adrenal axis. Endocrinology 149:3581-3591.
40. Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates (Academic, San Diego), 4th Ed.
41. Hill MN, et al. (2006) Involvement of the endocannabinoid system in the ability of long-term tricyclic antidepressant treatment to suppress stress-induced activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology 31:2591-2599.
42. Patel S, et al. (2005) The postmortal accumulation of brain N-arachidonylethanolamine (anandamide) is dependent upon fatty acid amide hydrolase activity. J Lipid Res 46: 342-349. (Pubitemid 40271098)