Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala
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Psychosocial stress is a risk factor for development and exacerbation of neuropsychiatric illness. Repeated stress causes biochemical adaptations in endocannabinoid (eCB) signaling that contribute to stress-response habituation, however, the synaptic correlates of these adaptations have not been examined. Here, we show that the synthetic enzyme for the eCB 2-arachidonoylglycerol (2-AG), diacylglycerol (DAG) lipase alpha, is heterogeneously expressed in the amygdala, and that levels of 2-AG and precursor DAGs are increased in the basolateral amygdala (BLA) after 10 days, but not 1 day, of restraint stress. In contrast, arachidonic acid was decreased after both 1 and 10 days of restraint stress. To examine the synaptic correlates of these alterations in 2-AG metabolism, we used whole-cell electrophysiology to determine the effects of restraint stress on depolarization-induced suppression of inhibition (DSI) in the BLA. A single restraint stress exposure did not alter DSI compared with control mice. However, after 10 days of restraint stress, DSI duration, but not magnitude, was significantly prolonged. Inhibition of 2-AG degradation with MAFP also prolonged DSI duration; the effects of repeated restraint stress and MAFP were mutually occlusive. These data indicate that exposure to repeated, but not acute, stress produces neuroadaptations that confer BLA neurons with an enhanced capacity to elevate 2-AG content and engage in 2-AG-mediated short-term retrograde synaptic signaling. We suggest stress-induced enhancement of eCB-mediated suppression of inhibitory transmission in the BLA could contribute to affective dysregulation associated with chronic stress.
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Stress produces divergent effects on AEA and 2-AG levels in the BLA, with an elevation in 2-AG levels and a rapid induction of FAAH activity and resultant decline in the AEA pool following exposure to various types of stress.
“Interestingly, stress appears to produce divergent effects on AEA and 2-AG levels in the BLA – with an elevation in 2-AG levels [57], but a rapid induction of FAAH activity and a resultant decline in the pool of AEA [58–60] were reported following exposure to various types of stress.”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [57]
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Cites
Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., et al. (2003) · Science · doi:10.1126/science.1083968 · Cited by 8,120 · see citing works
Hammen, C. (2005) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.1.102803.143938 · Cited by 2,979 · see citing works
The molecular logic of endocannabinoid signalling
Piomelli, D. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1247 · Cited by 1,957 · see citing works
Stress, Depression, and Neuroplasticity: A Convergence of Mechanisms
Pittenger, C., & Duman, R. S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301574 · Cited by 1,795 · see citing works
The Amygdaloid Complex: Anatomy and Physiology
SAH, P., FABER, E. S. L., LOPEZ DE ARMENTIA, M., & POWER, J. (2003) · Physiological Reviews · doi:10.1152/physrev.00002.2003 · Cited by 1,745 · see citing works
The endogenous cannabinoid system controls extinction of aversive memories
Marsicano, G., Wotjak, C. T., Azad, S. C., Bisogno, T., Rammes, G., Cascio, M. G., Hermann, H., Tang, J., Hofmann, C., Zieglgänsberger, W., et al. (2002) · Nature · doi:10.1038/nature00839 · Cited by 1,728 · see citing works
Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses
Wilson, R. I., & Nicoll, R. A. (2001) · Nature · doi:10.1038/35069076 · Cited by 1,607 · see citing works
Endocannabinoid-Mediated Control of Synaptic Transmission
Kano, M., Ohno‐Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009) · Physiological Reviews · doi:10.1152/physrev.00019.2008 · Cited by 1,529 · see citing works
Yamagata, K., Andreasson, K. I., Kaufmann, W. E., Barnes, C. A., & Worley, P. F. (1993) · Neuron · doi:10.1016/0896-6273(93)90192-t · Cited by 1,224 · see citing works
A Comprehensive Profile of Brain Enzymes that Hydrolyze the Endocannabinoid 2-Arachidonoylglycerol
Blankman, J. L., Simon, G. M., & Cravatt, B. F. (2007) · Chemistry & Biology · doi:10.1016/j.chembiol.2007.11.006 · Cited by 1,177 · see citing works
Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects
Long, J. Z., Li, W., Booker, L., Burston, J. J., Kinsey, S. G., Schlosburg, J. E., Pavón, F. J., Serrano, A., Selley, D. E., Parsons, L. H., et al. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.129 · Cited by 938 · see citing works
Work stress precipitates depression and anxiety in young, working women and men
MELCHIOR, M., CASPI, A., MILNE, B. J., DANESE, A., POULTON, R., & MOFFITT, T. E. (2007) · Psychological Medicine · doi:10.1017/s0033291707000414 · Cited by 691 · see citing works
Katona, I., Rancz, E. A., Acsády, L., Ledent, C., Mackie, K., Hájos, N., & Freund, T. F. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09506.2001 · Cited by 668 · cited 4× · see citing works
“We focused our electrophysiological studies on the BLA given the high level of both DAGLp and CB1 receptor expression in this subregion (Katona et al, 2001).”
InfluentialEnzymatic pathways that regulate endocannabinoid signaling in the nervous system
Ahn, K., McKinney, M. K., & Cravatt, B. F. (2008) · Chemical Reviews · doi:10.1021/cr0782067 · Cited by 529 · see citing works
Molecular Composition of the Endocannabinoid System at Glutamatergic Synapses
Katona, I., Urbán, G. M., Wallace, M., Ledent, C., Jung, K.-M., Piomelli, D., Mackie, K., & Freund, T. F. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0309-06.2006 · Cited by 511 · see citing works
Endocannabinoid system and stress and anxiety responses
VIVEROS, M., MARCO, E., & FILE, S. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.01.029 · Cited by 485 · see citing works
Uchigashima, M., Narushima, M., Fukaya, M., Katona, I., Kano, M., & Watanabe, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0448-07.2007 · Cited by 375 · see citing works
Cerebellar Depolarization-Induced Suppression of Inhibition Is Mediated by Endogenous Cannabinoids
Kreitzer, A. C., & Regehr, W. G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-20-j0005.2001 · Cited by 353 · see citing works
Inhibition of the Amygdala: Key to Pathological States?
Quirk, G. J., & Gehlert, D. R. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07087.x · Cited by 308 · see citing works
Patel, S., Roelke, C. T., Rademacher, D. J., & Hillard, C. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03916.x · Cited by 297 · see citing works
Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling
Azad, S. C., Monory, K., Marsicano, G., Cravatt, B. F., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2134-04.2004 · Cited by 263 · cited 2× · see citing works
“It is also not because of a general impairment in 2-AG signaling because receptor-driven eCB release initiated by 50 mM dihydroxyphenylglycine (B50% eIPSC suppression) is comparable to that observed in BLA and other brain regions (Patel and Winder, unpublished data; (Azad et al, 2004)).”
Rademacher, D. J., Meier, S. E., Shi, L., Vanessa Ho, W.-S., Jarrahian, A., & Hillard, C. J. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.06.012 · Cited by 233 · see citing works
The endocannabinoid system: emotion, learning and addiction
Moreira, F. A., & Lutz, B. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00104.x · Cited by 222 · see citing works
A single in-vivo exposure to Δ9THC blocks endocannabinoid-mediated synaptic plasticity
Mato, S., Chevaleyre, V., Robbe, D., Pazos, Á., Castillo, P. E., & Manzoni, O. J. (2004) · Nature Neuroscience · doi:10.1038/nn1251 · Cited by 220 · see citing works
Azad, S. C., Eder, M., Marsicano, G., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2003) · Learning & Memory · doi:10.1101/lm.53303 · Cited by 220 · see citing works
Cannabinoid CB1 Receptor Mediates Fear Extinction via Habituation-Like Processes
Kamprath, K., Marsicano, G., Tang, J., Monory, K., Bisogno, T., Marzo, V. D., Lutz, B., & Wotjak, C. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0153-06.2006 · Cited by 217 · see citing works
Hammen, C. L., Brennan, P. A., & Shih, J. H. (2004) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000127588.57468.f6 · Cited by 198 · see citing works
Jung, K., Mangieri, R. A., Stapleton, C. J., Kim, J., Fegley, D., Wallace, M., Mackie, K., & Piomelli, D. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.013961 · Cited by 197 · see citing works
Hill, M. N., & Gorzalka, B. B. (2005) · Behavioural Pharmacology · doi:10.1097/00008877-200509000-00006 · Cited by 193 · see citing works
Hashimotodani, Y., Ohno‐Shosaku, T., & Kano, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4159-06.2007 · Cited by 186 · see citing works
Jung, K., Astarita, G., Zhu, C., Wallace, M., Mackie, K., & Piomelli, D. (2007) · Molecular Pharmacology · doi:10.1124/mol.107.037796 · Cited by 170 · see citing works
Juhász, G., Chase, D. S., Pegg, E., Downey, D., Toth, Z. G., Stones, K., Platt, H., Mekli, K., Payton, A., Elliott, R., et al. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.19 · Cited by 166 · see citing works
Patel, S., Cravatt, B. F., & Hillard, C. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300535 · Cited by 164 · see citing works
Patel, S., & Hillard, C. J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06266.x · Cited by 162 · see citing works
Self-citationZhu, P., & Lovinger, D. M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1148-05.2005 · Cited by 125 · see citing works
Rossi, S., Chiara, V. D., Musella, A., Kusayanagi, H., Mataluni, G., Bernardi, G., Usiello, A., & Centonze, D. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5346-07.2008 · Cited by 112 · see citing works
Monoacylglycerol lipase regulates 2-arachidonoylglycerol action and arachidonic acid levels
Nomura, D. K., Hudak, C. S. S., Ward, A. M., Burston, J. J., Issa, R. S., Fisher, K. J., Abood, M. E., Wiley, J. L., Lichtman, A. H., & Casida, J. E. (2008) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2008.08.007 · Cited by 88 · see citing works
Hashimotodani, Y., Ohno‐Shosaku, T., & Kano, M. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.03.012 · Cited by 84 · see citing works
Carter, E., & Wang, X.-J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm103 · Cited by 62 · see citing works
Cannabinoid-induced Fos expression within A10 dopaminergic neurons
Patel, S., & Hillard, C. J. (2003) · Brain Research · doi:10.1016/s0006-8993(02)03797-6 · Cited by 61 · see citing works
Metaplastic control of the endocannabinoid system at inhibitory synapses in hippocampus
Edwards, D. A., Zhang, L., & Alger, B. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803558105 · Cited by 59 · see citing works
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Endocannabinoid Signaling and Synaptic Function
Castillo, P. E., Younts, T. J., Chávez, A. E., & Hashimotodani, Y. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.020 · Cited by 1,126 · see citing works
Neurobiological Interactions Between Stress and the Endocannabinoid System
Morena, M., Patel, S., Bains, J. S., & Hill, M. N. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.166 · Cited by 663 · see citing works
The endocannabinoid system in guarding against fear, anxiety and stress
Lutz, B., Marsicano, G., Maldonado, R., & Hillard, C. J. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4036 · Cited by 506 · see citing works
Dendritic Spines in Depression: What We Learned from Animal Models
Qiao, H., Li, M.-X., Xu, C. S., Chen, H.-B., An, S.-C., & Ma, X. (2016) · Neural Plasticity · doi:10.1155/2016/8056370 · Cited by 442 · see citing works
Endogenous cannabinoid signaling is essential for stress adaptation
Hill, M. N., McLaughlin, R. J., Bingham, B., Shrestha, L., Lee, T. T. Y., Gray, J. M., Hillard, C. J., Gorzalka, B. B., & Viau, V. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914661107 · Cited by 349 · see citing works
Gunduz-Cinar, O., MacPherson, K. P., Cinar, R., Gamble-George, J., Sugden, K., Williams, B., Godlewski, G., Ramikie, T. S., Gorka, A. X., Alapafuja, S. O., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.72 · Cited by 307 · see citing works
Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic–pituitary–adrenal axis
Tasker, J. G., & Herman, J. P. (2011) · Stress · doi:10.3109/10253890.2011.586446 · Cited by 277 · see citing works
Hill, M. N., Patel, S., Campolongo, P., Tasker, J. G., Wotjak, C. T., & Bains, J. S. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4283-10.2010 · Cited by 255 · see citing works
Corticotropin-releasing hormone drives anandamide hydrolysis in the amygdala to promote anxiety
Gray, J. M., Vecchiarelli, H. A., Morena, M., Lee, T. T. Y., Hermanson, D. J., Kim, A. B., McLaughlin, R. J., Hassan, K. I., Kühne, C., Wotjak, C. T., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2737-14.2015 · Cited by 246 · see citing works
Self-citationEndocannabinoid-mediated retrograde modulation of synaptic transmission
Ohno‐Shosaku, T., & Kano, M. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.017 · Cited by 244 · see citing works
Neurodevelopment, GABA System Dysfunction, and Schizophrenia
Schmidt, M. J., & Mirnics, K. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.95 · Cited by 239 · see citing works
Amygdala FAAH and anandamide: mediating protection and recovery from stress
Gunduz-Cinar, O., Hill, M. N., McEwen, B. S., & Holmes, A. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.08.008 · Cited by 229 · see citing works
Hill, M. N., Kumar, S. A., Filipski, S. B., Iverson, M., Stuhr, K. L., Keith, J. M., Cravatt, B. F., Hillard, C. J., Chattarji, S., & McEwen, B. S. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.90 · Cited by 222 · see citing works
The impact of chronic stress on the rat brain lipidome
Oliveira, T. G., Chan, R., Bravo, F. V., Miranda, A. M., Caridade-Silva, R., Zhou, B., Marques, F., Pinto, V., Cerqueira, J., Paolo, G. D., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.14 · Cited by 219 · see citing works
Endocannabinoid system, stress and HPA axis
Micale, V., & Drago, F. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2018.07.039 · Cited by 189 · see citing works
McPartland, J. M., Guy, G. W., & Marzo, V. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089566 · Cited by 161 · see citing works
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
Dubreucq, S., Matias, I., Cardinal, P., Häring, M., Lutz, B., Marsicano, G., & Chaouloff, F. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.36 · Cited by 147 · see citing works
Repeated Stress Impairs Endocannabinoid Signaling in the Paraventricular Nucleus of the Hypothalamus
Cusulin, J. I. W., Kuzmiski, J. B., & Bains, J. S. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1046-10.2010 · Cited by 145 · see citing works
Riebe, C. J. N., & Wotjak, C. T. (2011) · Stress · doi:10.3109/10253890.2011.586753 · Cited by 144 · see citing works
Wang, M., Hill, M. N., Zhang, L., Gorzalka, B. B., Hillard, C. J., & Alger, B. E. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111409606 · Cited by 137 · see citing works
Endocannabinoid signalling modulates susceptibility to traumatic stress exposure
Bluett, R. J., Báldi, R., Haymer, A., Gaulden, A. D., Hartley, N. D., Parrish, W. P., Baechle, J. J., Marcus, D. J., Bey, R. M., Shonesy, B. C., et al. (2017) · Nature Communications · doi:10.1038/ncomms14782 · Cited by 136 · see citing works
Control of synaptic function by endocannabinoid-mediated retrograde signaling
Kano, M. (2014) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.90.235 · Cited by 129 · see citing works
Substrate-selective COX-2 inhibition decreases anxiety via endocannabinoid activation
Hermanson, D. J., Hartley, N. D., Gamble-George, J., Brown, N., Shonesy, B. C., Kingsley, P. J., Colbran, R. J., Reese, J., Marnett, L. J., & Patel, S. (2013) · Nature Neuroscience · doi:10.1038/nn.3480 · Cited by 126 · see citing works
Sumislawski, J. J., Ramikie, T. S., & Patel, S. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.166 · Cited by 124 · see citing works
Wang, W., Sun, D., Pan, B., Roberts, C. J., Sun, X., Hillard, C. J., & Liu, Q.-S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.99 · Cited by 124 · see citing works
Di, S., Itoga, C. A., Fisher, M. O., Solomonow, J., Roltsch, E. A., Gilpin, N. W., & Tasker, J. G. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2279-15.2016 · Cited by 120 · see citing works
Gorzalka, B. B., & Hill, M. N. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.11.021 · Cited by 118 · see citing works
Yoshida, T., Uchigashima, M., Yamasaki, M., Katona, I., Yamazaki, M., Sakimura, K., Kano, M., Yoshioka, M., & Watanabe, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012875108 · Cited by 116 · see citing works
Hill, M. N., & Patel, S. (2013) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-3-19 · Cited by 117 · see citing works
Spagnolo, P. A., Ramchandani, V. A., Schwandt, M. L., Kwako, L. E., George, D. T., Mayo, L. M., Hillard, C. J., & Heilig, M. A. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13210 · Cited by 104 · see citing works
Endocannabinoid Signaling Collapse Mediates Stress-Induced Amygdalo-Cortical Strengthening
Marcus, D. J., Bedse, G., Gaulden, A. D., Ryan, J. D., Kondev, V., Winters, N. D., Rosas-Vidal, L. E., Altemus, M., Mackie, K., Lee, F. S., et al. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.024 · Cited by 104 · see citing works
Self-citationTchantchou, F., Tucker, L. B., Fu, A. H., Bluett, R. J., McCabe, J. T., Patel, S., & Zhang, Y. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.06.006 · Cited by 101 · see citing works
Functional Relevance of Endocannabinoid-Dependent Synaptic Plasticity in the Central Nervous System
Augustin, S. M., & Lovinger, D. M. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00508 · Cited by 97 · see citing works
Endocannabinoid-mediated synaptic plasticity and addiction-related behavior
Sidhpura, N., & Parsons, L. H. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.05.034 · Cited by 92 · see citing works
Kamprath, K., Romo-Parra, H., Häring, M., Gaburro, S., Doengi, M., Lutz, B., & Pape, H.-C. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.196 · Cited by 86 · see citing works
Holleran, K. M., Wilson, H. H., Fetterly, T. L., Bluett, R. J., Centanni, S. W., Gilfarb, R. A., Rocco, L. E. R., Patel, S., & Winder, D. G. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.3 · Cited by 83 · see citing works
Serrano, A., Pavon, F. J., Buczynski, M. W., Schlosburg, J., Natividad, L. A., Polis, I. Y., Stouffer, D. G., Zorrilla, E. P., Roberto, M., Cravatt, B. F., et al. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0055-3 · Cited by 83 · see citing works
Ramikie, T. S., Nyilas, R., Bluett, R. J., Gamble‐George, J., Hartley, N. D., Mackie, K., Watanabe, M., Katona, I., & Patel, S. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.012 · Cited by 80 · see citing works
CaMKII regulates diacylglycerol lipase-α and striatal endocannabinoid signaling
Shonesy, B. C., Wang, X., Rose, K. L., Ramikie, T. S., Cavener, V. S., Rentz, T. J., Baucum, A. J., Jalan‐Sakrikar, N., Mackie, K., Winder, D. G., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3353 · Cited by 77 · see citing works
Zhang, W., & Rosenkranz, J. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.051 · Cited by 77 · see citing works
Bedse, G., Hill, M. N., & Patel, S. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.01.015 · Cited by 75 · see citing works
Lee, T. T. ‐., & Gorzalka, B. B. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.10.006 · Cited by 75 · see citing works
Neuronal populations mediating the effects of endocannabinoids on stress and emotionality
Häring, M., Guggenhuber, S., & Lutz, B. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.12.035 · Cited by 70 · see citing works
Morena, M., Castro, V. D., Gray, J. M., Palmery, M., Trezza, V., Roozendaal, B., Hill, M. N., & Campolongo, P. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1983-15.2015 · Cited by 70 · see citing works
Lee, T. T. Y., & Hill, M. N. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.017 · Cited by 67 · see citing works
Campolongo, P., Morena, M., Scaccianoce, S., Trezza, V., Chiarotti, F., Schelling, G., Cuomo, V., & Roozendaal, B. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.26 · Cited by 68 · see citing works
Meet Your Stress Management Professionals: The Endocannabinoids
deRoon‐Cassini, T. A., Stollenwerk, T. M., Beatka, M. J., & Hillard, C. J. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.07.002 · Cited by 66 · see citing works
Luchsinger, J. R., Fetterly, T. L., Williford, K. M., Salimando, G. J., Doyle, M. A., Maldonado, J. A., Simerly, R. B., Winder, D. G., & Centanni, S. W. (2021) · Nature Communications · doi:10.1038/s41467-021-23674-z · Cited by 61 · see citing works
Bowles, N. P., Hill, M. N., Bhagat, S. M., Karatsoreos, I. N., Hillard, C. J., & McEwen, B. S. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.048 · Cited by 63 · see citing works
Cannabinoid Modulation of the Stressed Hippocampus
Scarante, F. F., Vila-Verde, C., Lopes, V. D., Ferreira‐Junior, N. C., Guimarães, F. S., & Campos, A. C. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00411 · Cited by 64 · see citing works
Ramikie, T. S., & Patel, S. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.037 · Cited by 62 · see citing works
Roles of multiple lipid mediators in stress and depression
Furuyashiki, T., Akiyama, S., & Kitaoka, S. (2019) · International Immunology · doi:10.1093/intimm/dxz023 · Cited by 59 · see citing works
The Endocannabinoid System and Anxiety
Lisboa, S. F. D. S., Gomes, F. V., Terzian, A. L. B., de Aguiar, D. C., Moreira, F. A., Resstel, L. B. M., & Guimarães, F. S. (2016) · Vitamins and hormones · doi:10.1016/bs.vh.2016.09.006 · Cited by 56 · see citing works
Ratano, P., Petrella, C., Forti, F., Passeri, P. P., Morena, M., Palmery, M., Trezza, V., Severini, C., & Campolongo, P. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.05.030 · Cited by 51 · see citing works
Endogenous cannabinoid signaling at inhibitory interneurons
Younts, T. J., & Castillo, P. E. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.12.006 · Cited by 50 · see citing works
Cannabis in Veterinary Medicine: Cannabinoid Therapies for Animals
Hartsel, J. A., Boyar, K., Pham, A., Silver, R. J., & Makriyannis, A. (2019) · Springer eBooks · doi:10.1007/978-3-030-04624-8_10 · Cited by 51 · see citing works
GABAA(δ) receptor hypofunction in the amygdala-hippocampal circuit underlies stress-induced anxiety
Qin, X., Pan, H., Huang, S.-H., Zou, J., Zheng, Z.-H., Liu, X., You, W.-J., Liu, Z.-P., Cao, J., Zhang, W.-H., et al. (2021) · 中国科学通报：英文版 · doi:10.1016/j.scib.2021.09.007 · Cited by 47 · see citing works
Hu, W., Zhang, M., Czéh, B., Zhang, W., & Flügge, G. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.04.005 · Cited by 48 · see citing works
Rieger, N. S., Varela, J. A., Ng, A. J., Granata, L. E., Djerdjaj, A., Brenhouse, H. C., & Christianson, J. P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01292-7 · Cited by 47 · see citing works
Fluoxetine Facilitates Fear Extinction Through Amygdala Endocannabinoids
Gunduz‐Cinar, O., Flynn, S., Brockway, E. T., Kaugars, K. E., Báldi, R., Ramikie, T. S., Çınar, R., Kunos, G., Patel, S., & Holmes, A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.318 · Cited by 47 · see citing works
Role of the Endocannabinoid System in Depression: from Preclinical to Clinical Evidence
Micale, V., Tabiová, K., Kučerová, J., & Drago, F. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_5 · Cited by 47 · see citing works
Reich, C. G., Mihalik, G. R., Iskander, A. N., Seckler, J. C., & Weiss, M. S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.066 · Cited by 46 · see citing works
Carey, C. E., Agrawal, A., Zhang, B., Conley, E. D., Degenhardt, L. J., Heath, A. C., Li, D., Lynskey, M. T., Martin, N. G., Montgomery, G. W., et al. (2015) · Journal of Abnormal Psychology · doi:10.1037/abn0000079 · Cited by 45 · see citing works
Inhibition of Diacylglycerol Lipase Impairs Fear Extinction in Mice
Cavener, V. S., Gaulden, A. D., Pennipede, D., Jagasia, P., Uddin, J., Marnett, L. J., & Patel, S. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00479 · Cited by 41 · see citing works
Locci, A., & Pinna, G. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.12.014 · Cited by 42 · see citing works
Molecular Alterations of the Endocannabinoid System in Psychiatric Disorders
Navarro, D., Gasparyan, A., Navarrete, F., Torregrosa, A. B., Rubio, G., Marín, M., Acosta, G. B., García‐Gutiérrez, M. S., & Manzanares, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094764 · Cited by 45 · see citing works
Changing the tune: plasticity and adaptation of retrograde signals
Iremonger, K. J., Cusulin, J. I. W., & Bains, J. S. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.04.007 · Cited by 42 · see citing works
Crosby, K. M., & Bains, J. S. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.049 · Cited by 41 · see citing works
Haj‐Dahmane, S., & Shen, R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1310-14.2014 · Cited by 38 · see citing works
The endocannabinoid system in the amygdala and modulation of fear
Gunduz‐Cinar, O. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110116 · Cited by 38 · see citing works
Reich, C. G., Iskander, A. N., & Weiss, M. S. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881113499207 · Cited by 38 · see citing works
A synaptocentric view of the neuroendocrine response to stress
Cusulin, J. I. W., & Bains, J. S. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07513.x · Cited by 37 · see citing works
Scheyer, A. F., Yasmin, F., Naskar, S., & Patel, S. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01438-7 · Cited by 36 · see citing works
Drug discovery strategies that focus on the endocannabinoid signaling system in psychiatric disease
Wyrofsky, R. R., McGonigle, P., & Bockstaele, E. J. V. (2014) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2014.966680 · Cited by 35 · see citing works
Endocannabinoids, stress signaling, and the locus coeruleus-norepinephrine system
Wyrofsky, R. R., Reyes, B. A. S., Zhang, X.-Y., Bhatnagar, S., Kirby, L. G., & Bockstaele, E. J. V. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2019.100176 · Cited by 31 · see citing works
Anandamide deficiency and heightened neuropathic pain in aged mice
Bishay, P., Häußler, A., Lim, H., Oertel, B. G., Galve‐Roperh, I., Ferreirós, N., & Tegeder, I. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.021 · Cited by 31 · see citing works
Shonesy, B. C., Winder, D. G., Patel, S., & Colbran, R. J. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.026 · Cited by 29 · see citing works
Clarke, D. J., Stuart, J. M., McGregor, I. S., & Arnold, J. C. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.08.006 · Cited by 26 · see citing works
Tong, J., Liu, X.-J., Vickstrom, C. R., Li, Y., Yu, L., Lu, Y.-M., Smrcka, A., & Liu, Q.-S. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2810-16.2017 · Cited by 25 · see citing works
Talani, G., & Lovinger, D. (2015) · Alcohol · doi:10.1016/j.alcohol.2015.08.006 · Cited by 25 · see citing works
Tomàs-Roig, J., Piscitelli, F., Gil, V., del Rı́o, J. A., Moore, T. P., Agbemenyah, H. Y., Salinas, G., Pommerenke, C., Lorenzen, S., Beißbarth, T., et al. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.01.036 · Cited by 24 · see citing works
Synaptic effects of cannabinoids
Benarroch, E. E. (2014) · Neurology · doi:10.1212/wnl.0000000000001013 · Cited by 25 · see citing works
Effects of the LPA1 Receptor Deficiency and Stress on the Hippocampal LPA Species in Mice
Tabbai, S., Moreno‐Fernández, R. D., Zambrana-Infantes, E. N., Nieto-Quero, A., Chun, J. J. M., Garcia‐Fernandez, M. I., Estivill‐Torrús, G., de Fonseca, F. R., Santín, L. J., Oliveira, T. G., et al. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00146 · Cited by 22 · see citing works
Long-Term Aberrations To Cerebellar Endocannabinoids Induced By Early-Life Stress
Moussa‐Tooks, A. B., Larson, E. R., Gimeno, A. F., Leishman, E., Bartolomeo, L. A., Bradshaw, H. B., Green, J. T., O’Donnell, B. F., Mackie, K., & Hetrick, W. P. (2020) · Scientific Reports · doi:10.1038/s41598-020-64075-4 · Cited by 22 · see citing works
Ross, J. A., & Bockstaele, E. J. V. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14714 · Cited by 19 · see citing works
Reemst, K., Broos, J. Y., Abbink, M. R., Cimetti, C., Giera, M. A., Kooij, G., & Kőrösi, A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.967437 · Cited by 22 · see citing works
G6PC2 Modulates Fasting Blood Glucose In Male Mice in Response to Stress
Boortz, K. A., Syring, K. E., Dai, C., Pound, L. D., Oeser, J. K., Jacobson, D. A., Wang, J.-C., McGuinness, O. P., Powers, A. C., & O’Brien, R. M. (2016) · Endocrinology · doi:10.1210/en.2016-1245 · Cited by 21 · see citing works
Cannabinoids in Health and Disease
Meccariello, R., & Chianese, R. (2016) · InTech eBooks · doi:10.5772/61595 · Cited by 21 · see citing works
G6PC2 Modulates the Effects of Dexamethasone on Fasting Blood Glucose and Glucose Tolerance
Boortz, K. A., Syring, K. E., Lee, R. A., Dai, C., Oeser, J. K., McGuinness, O. P., Wang, J.-C., & O’Brien, R. M. (2016) · Endocrinology · doi:10.1210/en.2016-1678 · Cited by 20 · see citing works
Bedse, G., Centanni, S. W., Winder, D. G., & Patel, S. (2019) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14159 · Cited by 19 · see citing works
Dietary Omega-6/Omega-3 and Endocannabinoids: Implications for Brain Health and Diseases
Bosch‐Bouju, C., & Layé, S. (2016) · InTech eBooks · doi:10.5772/62498 · Cited by 18 · see citing works
Endogenous cannabinoids are required for MC4R-mediated control of energy homeostasis
Yong, Y., Çakır, I., Pan, P. L., Biddinger, J. E., Bluett, R. J., Mackie, K., Bingham, N. C., Patel, S. H., & Ghamari‐Langroudi, M. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2015990118 · Cited by 18 · see citing works
Lee, T. T.-Y., & Gorzalka, B. B. (2015) · International review of neurobiology · doi:10.1016/bs.irn.2015.09.002 · Cited by 21 · see citing works
Swim stress differentially affects limbic contents of 2-arachidonoylglycerol and 2-oleoylglycerol
Roberts, C. J., Stuhr, K. L., & Hillard, C. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.065 · Cited by 17 · see citing works
The endocannabinoid system in the brain undergoes long-lasting changes following neuropathic pain
Zhang, M., Wang, T., Meng, F., Jiang, M., Wu, S., & Xu, H. (2024) · iScience · doi:10.1016/j.isci.2024.111409 · Cited by 16 · see citing works
2-AG-Mediated Control of GABAergic Signaling Is Impaired in a Model of Epilepsy
Colangeli, R., Morena, M., Werner, A. C., Thompson, R. J., van der Stelt, M., Pittman, Q., Hill, M., & Teskey, G. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0541-22.2022 · Cited by 12 · see citing works
Zhai, Q., Islam, A., Chen, B., Zhang, H., Chi, D. H., Mamun, M. A., Takahashi, Y., Sato, N., Yamasue, H., Nakajima, Y., et al. (2023) · Cells · doi:10.3390/cells12030393 · Cited by 15 · see citing works
Türker‐Kaya, S., Mutlu, O., Celikyurt, I. K., Akar, F., & Ulak, G. (2016) · Spectrochimica Acta Part A Molecular and Biomolecular Spectroscopy · doi:10.1016/j.saa.2016.02.038 · Cited by 15 · see citing works
Circadian regulation of memory under stress: Endocannabinoids matter
Morena, M., Santori, A., & Campolongo, P. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104712 · Cited by 14 · see citing works
- Authors
- Patel, S., Kingsley, P. J., Mackie, K., Marnett, L. J., & Winder, D. G.
- Affiliations
- Vanderbilt University (US)
- Indiana University Bloomington (US)
- Corresponding author
- Patel, Sachin
- Venue
- Neuropsychopharmacology
- Published
- 2009-08-12
- Volume
- 34
- Issue
- 13
- Pages
- 2699-2709
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC2881681
- OpenAlex
- W1963850092
- Cited by
- 153
- References
- 41
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 2 · 2023: 4 · 2022: 11 · 2021: 9 · 2020: 9 · 2019: 9 · 2018: 8 · 2017: 7 · 2016: 15 · 2015: 13 · 2014: 14 · 2013: 11 · 2012: 10
- FWCI
- 7.19
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Vanderbilt University
- Vanderbilt Institute for Clinical and Translational Research
- National Institutes of Health (GM 15431)
- National Institute on Alcohol Abuse and Alcoholism (AA15635, U01AA015635)
- National Institute on Drug Abuse (DA21696, DA11322, DA 19112, R01DA011322, R01DA019112, K05DA021696)
- National Institute of General Medical Sciences (GM 15431, P50GM015431, P01GM015431)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- repeated restraint stress, 2-arachidonoylglycerol, endocannabinoid signaling, basolateral amygdala, diacylglycerol lipase alpha, diacylglycerol, arachidonic acid, depolarization-induced suppression of inhibition, inhibitory synapses, chronic stress, emotional dysregulation
- MeSH terms
- Amygdala, Animals, Arachidonic Acids, Diglycerides, Glycerides, Lipoprotein Lipase, Male, Mice, Inbred ICR, Morpholines, Naphthalenes, Neural Inhibition, Synaptic Transmission, Restraint, Physical, Stress, Physiological, Stress, Psychological, Synapses, Receptor, Cannabinoid, CB1, Benzoxazines, Mice, Inhibitory Postsynaptic Potentials, Organophosphonates, Cannabinoid Receptor Modulators, Endocannabinoids
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