Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis.
- Authors
- Patel, Sachin; Roelke, Craig T; Rademacher, David J; Cullinan, William E; Hillard, Cecilia J
- Year
- 2004
- Journal
- Endocrinology
- PMID
- 15331569
- DOI
- 10.1210/en.2004-0638
Activation of the hypothalamic-pituitary-adrenal (HPA) axis is critical for the adaptation and survival of animals upon exposure to stressful stimuli, and data suggest that endocannabinoid (eCB) signaling modulates neuroendocrine function. We have explored the role of eCB signaling in the modulation of stress-induced HPA axis activation. Administration of the CB1 receptor antagonist/inverse agonist SR141716 (0.01, 0.1, 1, and 5 mg/kg, i.p.) to male mice produced a small, dose-dependent increase in the serum corticosterone (CORT) concentration. Despite this effect, the highest dose of SR141716 did not significantly increase neuronal activity within the paraventricular nucleus of the hypothalamus, as measured by the induction of Fos protein. Similarly, exposure of mice to 30 min of restraint increased serum CORT concentrations, but did not produce a consistent, statistically significant increase in Fos expression within the PVN. However, pretreatment of mice with SR141716 before restraint stress robustly potentiated restraint-induced CORT release and Fos expression within the PVN. Pretreatment of mice with either the CB1 receptor agonist CP55940, the eCB transport inhibitor AM404, or the fatty acid amide hydrolase inhibitor URB597 significantly decreased or eliminated restraint-induced CORT release. Upon exposure to acute restraint, hypothalamic 2-arachidonylglycerol content was reduced compared with the control value; however, after 5 d of restraint exposure (which resulted in an attenuated CORT response), the hypothalamic 2-arachidonylglycerol content was increased compared with the control value. These data indicate that eCB signaling negatively modulates HPA axis function in a context-dependent manner and suggest that pharmacological augmentation of eCB signaling could serve as a novel approach to the treatment of anxiety-related disorders.
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| Cannabinoid receptor type 1 antagonism significantly modulates basal and loud noise induced neural and hypothalamic-pituitary-adrenal axis responses in male Sprague-Dawley rats. | Newsom RJ et al. | β | 2012 | β |
| Cannabinoid-related agents in the treatment of anxiety disorders: current knowledge and future perspectives. | Tambaro S et al. | β | 2012 | β |
| Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress. | Ganon-Elazar E et al. | β | 2012 | β |
| CB1 receptor-deficient mice as a model for depression. | Valverde O et al. | β | 2012 | β |
| Differences in spontaneously avoiding or approaching mice reflect differences in CB1-mediated signaling of dorsal striatal transmission. | Laricchiuta D et al. | β | 2012 | β |
| Differential effects of single versus repeated alcohol withdrawal on the expression of endocannabinoid system-related genes in the rat amygdala. | Serrano A et al. | β | 2012 | β |
| Endocannabinoids and the cardiovascular response to stress. | O'Sullivan SE et al. | β | 2012 | β |
| Endocannabinoid signaling, glucocorticoid-mediated negative feedback, and regulation of the hypothalamic-pituitary-adrenal axis. | Hill MN et al. | β | 2012 | β |
| Endocannabinoid signaling in the amygdala: anatomy, synaptic signaling, behavior, and adaptations to stress. | Ramikie TS et al. | β | 2012 | β |
| Introduction to the special issue on stress, emotional behavior, and the endocannabinoid system: a decade of research. | Hill MN | β | 2012 | β |
| Maternal separation and proclivity for ethanol intake: a potential role of the endocannabinoid system in rats. | Romano-LΓ³pez A et al. | β | 2012 | β |
| N-arachidonoyl-serotonin in the basolateral amygdala increases anxiolytic behavior in the elevated plus maze. | John CS et al. | β | 2012 | β |
| Neural Regulation of the Stress Response: The Many Faces of Feedback. | Myers B et al. | β | 2012 | β |
| Neuronal populations mediating the effects of endocannabinoids on stress and emotionality. | HΓ€ring M et al. | β | 2012 | β |
| Pharmacological inhibition of endocannabinoid degradation modulates the expression of inflammatory mediators in the hypothalamus following an immunological stressor. | Kerr DM et al. | β | 2012 | β |
| Role of leaky neuronal ryanodine receptors in stress-induced cognitive dysfunction. | Liu X et al. | β | 2012 | β |
| Salivary cortisol, heart rate, and blood lactate responses during elite downhill mountain bike racing. | Sperlich B et al. | β | 2012 | β |
| Serum contents of endocannabinoids are correlated with blood pressure in depressed women. | Ho WS et al. | β | 2012 | β |
| Short- and long-term cognitive effects of chronic cannabinoids administration in late-adolescence rats. | Abush H et al. | β | 2012 | β |
| The intricate link between glucocorticoids and endocannabinoids at stress-relevant synapses in the hypothalamus. | Crosby KM et al. | β | 2012 | β |
| Timing is everything: evidence for a role of corticolimbic endocannabinoids in modulating hypothalamic-pituitary-adrenal axis activity across developmental periods. | Lee TT et al. | β | 2012 | β |
| Alterations in corticolimbic dendritic morphology and emotional behavior in cannabinoid CB1 receptor-deficient mice parallel the effects of chronic stress. | Hill MN et al. | β | 2011 | β |
| Chronic stress induces changes in the structure of interneurons and in the expression of molecules related to neuronal structural plasticity and inhibitory neurotransmission in the amygdala of adult mice. | Gilabert-Juan J et al. | β | 2011 | β |
| Determination of endocannabinoids in nematodes and human brain tissue by liquid chromatography electrospray ionization tandem mass spectrometry. | Lehtonen M et al. | β | 2011 | β |
| Early exposure to environmental enrichment alters the expression of genes of the endocannabinoid system. | El Rawas R et al. | β | 2011 | β |
| Endocannabinoid influence in drug reinforcement, dependence and addiction-related behaviors. | Serrano A et al. | β | 2011 | β |
| Endocannabinoid-mediated synaptic plasticity and addiction-related behavior. | Sidhpura N et al. | β | 2011 | β |
| Endocannabinoids and stress. | Riebe CJ et al. | β | 2011 | β |
| Enhancement of endocannabinoid signaling with JZL184, an inhibitor of the 2-arachidonoylglycerol hydrolyzing enzyme monoacylglycerol lipase, produces anxiolytic effects under conditions of high environmental aversiveness in rats. | Sciolino NR et al. | β | 2011 | β |
| Evaluation of the emotional phenotype and serotonergic neurotransmission of fatty acid amide hydrolase-deficient mice. | Cassano T et al. | β | 2011 | β |
| Interactions between endocannabinoid and serotonergic systems in mood disorders caused by nicotine withdrawal. | Mannucci C et al. | β | 2011 | β |
| Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic-pituitary-adrenal axis. | Tasker JG et al. | β | 2011 | β |
| Modulation of the serotonin system by endocannabinoid signaling. | Haj-Dahmane S et al. | β | 2011 | β |
| Overexpression of CB2 cannabinoid receptors decreased vulnerability to anxiety and impaired anxiolytic action of alprazolam in mice. | GarcΓa-GutiΓ©rrez MS et al. | β | 2011 | β |
| Pre-training anandamide infusion within the basolateral amygdala impairs plus-maze discriminative avoidance task in rats. | Munguba H et al. | β | 2011 | β |
| Putative role of endocannabinoid signaling in the etiology of depression and actions of antidepressants. | Gorzalka BB et al. | β | 2011 | β |
| Recruitment of prefrontal cortical endocannabinoid signaling by glucocorticoids contributes to termination of the stress response. | Hill MN et al. | β | 2011 | β |
| Regulatory role of cannabinoid receptor 1 in stress-induced excitotoxicity and neuroinflammation. | Zoppi S et al. | β | 2011 | β |
| Reversible gating of endocannabinoid plasticity in the amygdala by chronic stress: a potential role for monoacylglycerol lipase inhibition in the prevention of stress-induced behavioral adaptation. | Sumislawski JJ et al. | β | 2011 | β |
| Safety evaluation and treatment affect of LY2190416, a CB-1 antagonist/inverse agonist in growing beagle dogs. | Nunamaker E et al. | β | 2011 | β |
| Social encounter with a novel partner in adolescent rats: activation of the central endocannabinoid system. | Marco EM et al. | β | 2011 | β |
| The CBβ receptor antagonist SR141716A reverses adult male mice overweight and metabolic alterations induced by early stress. | Valenzuela CA et al. | β | 2011 | β |
| The Role of the Endocannabinoids in Suppression of the Hypothalamic-pituitary-adrenal Axis Activity by Doxepin. | Hassanzadeh P et al. | β | 2011 | β |
| The synthetic cannabinoid WIN 55212-2 differentially modulates thigmotaxis but not spatial learning in adolescent and adult animals. | Acheson SK et al. | β | 2011 | β |
| Activation of the hypothalamic-pituitary-adrenal axis by addictive drugs: different pathways, common outcome. | Armario A | β | 2010 | β |
| Additive actions of the cannabinoid and neuropeptide Y systems on adiposity and lipid oxidation. | Zhang L et al. | β | 2010 | β |
| Anandamide prior to sensitization increases cell-mediated immunity in mice. | Ribeiro A et al. | β | 2010 | β |
| Cannabinoids and their interactions with diazepam on modulation of serum corticosterone concentration in male mice. | Saber-Tehrani A et al. | β | 2010 | β |
| Central oxytocin is involved in restoring impaired gastric motility following chronic repeated stress in mice. | Babygirija R et al. | β | 2010 | β |
| Deficiency in endocannabinoid signaling in the nucleus accumbens induced by chronic unpredictable stress. | Wang W et al. | β | 2010 | β |
| Dietary lecithin source affects growth potential and gene expression in Sparus aurata larvae. | Alves Martins D et al. | β | 2010 | β |
| Endocannabinoid-mediated modulation of stress responses: physiological and pathophysiological significance. | Finn DP | β | 2010 | β |
| Endocannabinoid signalling: has it got rhythm? | Vaughn LK et al. | β | 2010 | β |
| Endogenous cannabinoid signaling is essential for stress adaptation. | Hill MN et al. | β | 2010 | β |
| Facilitation of endocannabinoid effects in the ventral hippocampus modulates anxiety-like behaviors depending on previous stress experience. | Campos AC et al. | β | 2010 | β |
| Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. | Evanson NK et al. | β | 2010 | β |
| Functional interactions between stress and the endocannabinoid system: from synaptic signaling to behavioral output. | Hill MN et al. | β | 2010 | β |
| Glucocorticoids, stress and obesity. | Pasquali R et al. | β | 2010 | β |
| Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. | Hill MN et al. | β | 2010 | β |
| Localization and function of the cannabinoid CB1 receptor in the anterolateral bed nucleus of the stria terminalis. | Puente N et al. | β | 2010 | β |
| Maternal dietary fat determines metabolic profile and the magnitude of endocannabinoid inhibition of the stress response in neonatal rat offspring. | D'Asti E et al. | β | 2010 | β |
| More aroused, less fatigued: fatty acid amide hydrolase gene polymorphisms influence acute response to amphetamine. | Dlugos AM et al. | β | 2010 | β |
| Motion sickness, stress and the endocannabinoid system. | ChoukΓ¨r A et al. | β | 2010 | β |
| Nongenomic actions of adrenal steroids in the central nervous system. | Evanson NK et al. | β | 2010 | β |
| Preservation of striatal cannabinoid CB1 receptor function correlates with the antianxiety effects of fatty acid amide hydrolase inhibition. | Rossi S et al. | β | 2010 | β |
| Quantification of brain endocannabinoid levels: methods, interpretations and pitfalls. | Buczynski MW et al. | β | 2010 | β |
| Rapid alteration of stress-induced hypothalamic-pituitary-adrenal hormone secretion in the rat: a comparison of glucocorticoids and cannabinoids. | Ginsberg AB et al. | β | 2010 | β |
| Regulation of the hypothalamic-pituitary-adrenal axis circadian rhythm by endocannabinoids is sexually diergic. | Atkinson HC et al. | β | 2010 | β |
| Selective alterations of the CB1 receptors and the fatty acid amide hydrolase in the ventral striatum of alcoholics and suicides. | Vinod KY et al. | β | 2010 | β |
| The endocannabinoid system and psychiatric disorders. | Parolaro D et al. | β | 2010 | β |
| Adaptations of striatal endocannabinoid system during stress. | Rossi S et al. | β | 2009 | β |
| Alcohol extract of Echinacea pallida reverses stress-delayed wound healing in mice. | Zhai Z et al. | β | 2009 | β |
| Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. | Ganon-Elazar E et al. | β | 2009 | β |
| Central side-effects of therapies based on CB1 cannabinoid receptor agonists and antagonists: focus on anxiety and depression. | Moreira FA et al. | β | 2009 | β |
| Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. | Campolongo P et al. | β | 2009 | β |
| Endocannabinoids mediate anxiolytic-like effect of acetaminophen via CB1 receptors. | Umathe SN et al. | β | 2009 | β |
| Endocannabinoid system and fear conditioning. | Resstel LB et al. | β | 2009 | β |
| Estrogen impairs glucocorticoid dependent negative feedback on the hypothalamic-pituitary-adrenal axis via estrogen receptor alpha within the hypothalamus. | Weiser MJ et al. | β | 2009 | β |
| From endocannabinoid profiling to 'endocannabinoid therapeutics'. | Ligresti A et al. | β | 2009 | β |
| Genetics of PTSD: Fear Conditioning as a Model for Future Research. | Amstadter AB et al. | β | 2009 | β |
| Glucocorticoid-regulated crosstalk between arachidonic acid and endocannabinoid biochemical pathways coordinates cognitive-, neuroimmune-, and energy homeostasis-related adaptations to stress. | Malcher-Lopes R et al. | β | 2009 | β |
| Integration of endocannabinoid signaling into the neural network regulating stress-induced activation of the hypothalamic-pituitary-adrenal axis. | Gorzalka BB et al. | β | 2009 | β |
| Interactions between environmental aversiveness and the anxiolytic effects of enhanced cannabinoid signaling by FAAH inhibition in rats. | Haller J et al. | β | 2009 | β |
| Monoaminergic neurotransmission contributes to cannabinoid-induced activation of the hypothalamic-pituitary-adrenal axis. | McLaughlin RJ et al. | β | 2009 | β |
| New approaches to the pharmacological management of major depressive disorder. | Witkin JM et al. | β | 2009 | β |
| Reciprocal changes in vanilloid (TRPV1) and endocannabinoid (CB1) receptors contribute to visceral hyperalgesia in the water avoidance stressed rat. | Hong S et al. | β | 2009 | β |
| Repeated novel cage exposure-induced improvement of early Alzheimer's-like cognitive and amyloid changes in TASTPM mice is unrelated to changes in brain endocannabinoids levels. | Pardon MC et al. | β | 2009 | β |
| Role of endocannabinoid signaling in anxiety and depression. | Patel S et al. | β | 2009 | β |
| Role of endocannabinoid system in the ventral hippocampus of rats in the modulation of anxiety-like behaviours. | Roohbakhsh A et al. | β | 2009 | β |
| Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic-pituitary-adrenal axis. | Hill MN et al. | β | 2009 | β |
| The endocannabinoid system as a target for novel anxiolytic and antidepressant drugs. | Gaetani S et al. | β | 2009 | β |
| Adaptations in endocannabinoid signaling in response to repeated homotypic stress: a novel mechanism for stress habituation. | Patel S et al. | β | 2008 | β |
| Anandamide and neutrophil function in patients with fibromyalgia. | Kaufmann I et al. | β | 2008 | β |
| An endocannabinoid signaling system modulates anxiety-like behavior in male Syrian hamsters. | Moise AM et al. | β | 2008 | β |
| Antidepressant-like behavioral effects of impaired cannabinoid receptor type 1 signaling coincide with exaggerated corticosterone secretion in mice. | Steiner MA et al. | β | 2008 | β |
| BDNF impairment in the hippocampus is related to enhanced despair behavior in CB1 knockout mice. | Aso E et al. | β | 2008 | β |
| Bidirectional roles of the brain 2-arachidonoyl-sn-glycerol in the centrally administered vasopressin-induced adrenomedullary outflow in rats. | Shimizu T et al. | β | 2008 | β |
| Chronic psychoemotional stress impairs cannabinoid-receptor-mediated control of GABA transmission in the striatum. | Rossi S et al. | β | 2008 | β |
| Chronic unpredictable stress enhances cocaine-conditioned place preference in type 1 cannabinoid receptor knockout mice. | Miller LL et al. | β | 2008 | β |
| Conditional cannabinoid receptor type 1 mutants reveal neuron subpopulation-specific effects on behavioral and neuroendocrine stress responses. | Steiner MA et al. | β | 2008 | β |
| Cross-sensitization and cross-tolerance between exogenous cannabinoid antinociception and endocannabinoid-mediated stress-induced analgesia. | Suplita RL et al. | β | 2008 | β |
| Differential effects of the antidepressants tranylcypromine and fluoxetine on limbic cannabinoid receptor binding and endocannabinoid contents. | Hill MN et al. | β | 2008 | β |
| Effects of acute and repeated restraint stress on endocannabinoid content in the amygdala, ventral striatum, and medial prefrontal cortex in mice. | Rademacher DJ et al. | β | 2008 | β |
| Endocannabinoid modulation of male rat sexual behavior. | Gorzalka BB et al. | β | 2008 | β |
| Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. | Bitencourt RM et al. | β | 2008 | β |
| Interaction between cannabinoid compounds and diazepam on anxiety-like behaviour of mice. | Naderi N et al. | β | 2008 | β |
| Multiple-dose pharmacokinetics, pharmacodynamics, and safety of taranabant, a novel selective cannabinoid-1 receptor inverse agonist, in healthy male volunteers. | Addy C et al. | β | 2008 | β |
| Partial cloning of CB1 cDNA and CB1 mRNA changes in stress responses in the Solea solea. | Palermo FA et al. | β | 2008 | β |
| Prolonged glucocorticoid treatment decreases cannabinoid CB1 receptor density in the hippocampus. | Hill MN et al. | β | 2008 | β |
| Regional alterations in the endocannabinoid system in an animal model of depression: effects of concurrent antidepressant treatment. | Hill MN et al. | β | 2008 | β |
| Regulation of endocannabinoid signaling by stress: implications for stress-related affective disorders. | Gorzalka BB et al. | β | 2008 | β |
| Role of cannabinoids and endocannabinoids in cerebral ischemia. | Hillard CJ | β | 2008 | β |
| Targeting the endocannabinoid system: to enhance or reduce? | Di Marzo V | β | 2008 | β |
| The cannabinoid CB1 receptor and the endocannabinoid anandamide: possible antidepressant targets. | Bambico FR et al. | β | 2008 | β |
| The rat pineal gland comprises an endocannabinoid system. | Koch M et al. | β | 2008 | β |
| The role of the endocannabinoid system in the regulation of hypothalamic-pituitary-adrenal axis activity. | Cota D | β | 2008 | β |
| 5-HT1A receptors are involved in the anxiolytic effect of Delta9-tetrahydrocannabinol and AM 404, the anandamide transport inhibitor, in Sprague-Dawley rats. | Braida D et al. | β | 2007 | β |
| Antidepressant-like activity of the fatty acid amide hydrolase inhibitor URB597 in a rat model of chronic mild stress. | Bortolato M et al. | β | 2007 | β |
| Delta9-tetrahydrocannabinol (THC) and AM 404 protect against cerebral ischaemia in gerbils through a mechanism involving cannabinoid and opioid receptors. | Zani A et al. | β | 2007 | β |
| Endocannabinoid system and synaptic plasticity: implications for emotional responses. | Viveros MP et al. | β | 2007 | β |
| Influences of an acoustic signal with ultrasound components on the acquisition of a defensive conditioned reflex in Wistar rats. | Loseva EV et al. | β | 2007 | β |
| Interactions between endocannabinoids and stress-induced decreased sensitivity to natural reward. | Rademacher DJ et al. | β | 2007 | β |
| Local enhancement of cannabinoid CB1 receptor signalling in the dorsal hippocampus elicits an antidepressant-like effect. | McLaughlin RJ et al. | β | 2007 | β |
| Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamic-pituitary-adrenal axis function. | Cota D et al. | β | 2007 | β |
| Short- and long-term plasticity of the endocannabinoid system in neuropsychiatric and neurological disorders. | Bisogno T et al. | β | 2007 | β |
| The endocannabinoid system and gut-brain signalling. | Storr MA et al. | β | 2007 | β |
| The role of the hippocampus in mediating emotional responses to nicotine and cannabinoids: a possible neural substrate for functional interactions. | Viveros MP et al. | β | 2007 | β |
| The toxicology of cannabis and cannabis prohibition. | Grotenhermen F | β | 2007 | β |
| WIN-55,212-2 chronically implanted into the CA3 region of the dorsal hippocampus impairs learning: a novel method for studying chronic, brain-area-specific effects of cannabinoids. | Barna I et al. | β | 2007 | β |
| Anxiolytic-like properties of the anandamide transport inhibitor AM404. | Bortolato M et al. | β | 2006 | β |
| Cannabinoid CB1 receptor antagonism modulates plasma corticosterone in rodents. | Wade MR et al. | β | 2006 | β |
| Effects of rimonabant (SR141716) on fasting-induced hypothalamic-pituitary-adrenal axis and neuronal activation in lean and obese Zucker rats. | Doyon C et al. | β | 2006 | β |
| Endocannabinoids modulate stress-induced suppression of hippocampal cell proliferation and activation of defensive behaviours. | Hill MN et al. | β | 2006 | β |
| Increased sensitivity to restraint stress and novelty-induced emotionality following long-term, high dose cannabinoid exposure. | Hill MN et al. | β | 2006 | β |
| 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. | Hill MN et al. | β | 2006 | β |
| Pharmacological evaluation of cannabinoid receptor ligands in a mouse model of anxiety: further evidence for an anxiolytic role for endogenous cannabinoid signaling. | Patel S et al. | β | 2006 | β |
| Role of the endocannabinoid system in depression and suicide. | Vinod KY et al. | β | 2006 | β |
| The effects of cannabinoids on contextual conditioned fear in CB1 knockout and CD1 mice. | Mikics E et al. | β | 2006 | β |
| The emerging role of the endocannabinoid system in endocrine regulation and energy balance. | Pagotto U et al. | β | 2006 | β |
| The endocannabinoid system as an emerging target of pharmacotherapy. | Pacher P et al. | β | 2006 | β |
| The endocannabinoid system as a target for the treatment of visceral obesity and metabolic syndrome. | Kyrou I et al. | β | 2006 | β |
| Antidepressant-like activity and modulation of brain monoaminergic transmission by blockade of anandamide hydrolysis. | Gobbi G et al. | β | 2005 | β |
| A role for cannabinoid CB1 receptors in mood and anxiety disorders. | Witkin JM et al. | β | 2005 | β |
| Differential response to acute and repeated stress in cannabinoid CB1 receptor knockout newborn and adult mice. | Fride E et al. | β | 2005 | β |
| Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. | Patel S et al. | β | 2005 | β |
| Is there a role for the endocannabinoid system in the etiology and treatment of melancholic depression? | Hill MN et al. | β | 2005 | β |
| Nutritional aspects modulating brain development and the responses to stress in early neonatal life. | Walker CD | β | 2005 | β |
| Provocation of kainic acid receptor mRNA changes in the rat paraventricular nucleus by insulin-induced hypoglycaemia. | Koenig JI et al. | β | 2005 | β |
| The endocannabinoid system in the brain of Carassius auratus and its possible role in the control of food intake. | Valenti M et al. | β | 2005 | β |