Social defeat leads to changes in the endocannabinoid system: An overexpression of calreticulin and motor impairment in mice

Behavioural Brain Research

Volumn 303, Issue , 2016, Pages 34-43

  Tomas Roig, J ^a,b   Piscitelli, F ^c   Gil, V ^d   del Rio J A ^d   Moore, T P ^a,b   Agbemenyah, H ^e,f   Salinas Riester, G ^g   Pommerenke, C ^g   Lorenzen, S ^h,i   Beissbarth T ^h   Hoyer Fender, S ^a   Di Marzo, V ^c   Havemann Reinecke, U ^a,b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b Center for Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB)   (Germany)

^c CNR   (Italy)

^d UNIVERSITY OF BARCELONA   (Spain)

^e EUROPEAN NEUROSCIENCE INSTITUTE   (Germany)

^f UNIVERSITY OF HEALTH AND ALLIED SCIENCES   (Ghana)

^g Dept of Developmental Biochemistry ^*  (Germany)

^h UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

ⁱ BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

Author keywords

Behavior; Calreticulin; Cerebellum; Endocannabinoid system; Psychosocial stress; RNA seq

Indexed keywords

2 ARACHIDONOYLGLYCEROL; CALRETICULIN; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; MESSENGER RNA; TRANSCRIPTOME; ACYLGLYCEROL; ARACHIDONIC ACID DERIVATIVE; GLYCERYL 2-ARACHIDONATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CALRETICULIN GENE; CANNABINOID 1 RECEPTOR GENE; CEREBELLUM; CONTROLLED STUDY; GENE EXPRESSION; LEARNING; LOCOMOTION; MALE; MENTAL STRESS; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOTOR LEARNING; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOCIAL STRESS; ANIMAL; C57BL MOUSE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; ROTAROD TEST; SOCIAL BEHAVIOR;

ANIMALS; ARACHIDONIC ACIDS; CALRETICULIN; CEREBELLUM; ENDOCANNABINOIDS; GENE EXPRESSION PROFILING; GLYCERIDES; LEARNING; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PSYCHOMOTOR PERFORMANCE; RECEPTOR, CANNABINOID, CB1; RNA, MESSENGER; ROTAROD PERFORMANCE TEST; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84961379137     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2016.01.036     Document Type: Article

References (98)

1. Szabo S., Tache Y., Somogyi A. The legacy of Hans Selye and the origins of stress research: a retrospective 75 years after his landmark brief "letter" to the editor# of nature. Stress 2012, 15:472-478. 10.3109/10253890.2012.710919.
2. Sapolsky R. Taming stress. Sci. Am. 2003, 289:86-95. 10.1038/scientificamerican0903-86.
3. Buwalda B., Kole M.H., Veenema A.H., Huininga M., de Boer S.F., Korte S.M., et al. Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci. Biobehav. Rev. 2005, 29:83-97. 10.1016/j.neubiorev.2004.05.005.
4. Miczek K.A., Yap J.J., Covington H.E. Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol. Ther. 2008, 120:102-128. 10.1016/j.pharmthera.2008.07.006.
5. Huhman K.L. Social conflict models: can they inform us about human psychopathology?. Horm. Behav. 2006, 50:640-646. 10.1016/j.yhbeh.2006.06.022.
6. Dubreucq S., Kambire S., Conforzi M., Metna-Laurent M., Cannich A., Soria-Gomez E., et al. Cannabinoid type 1 receptors located on single-minded 1-expressing neurons control emotional behaviors. Neuroscience 2012, 204:230-244. 10.1016/j.neuroscience.2011.08.049.
7. Mizoguchi K., Yuzurihara M., Ishige A., Sasaki H., Tabira T. Chronic stress impairs rotarod performance in rats: implications for depressive state. Pharmacol. Biochem. Behav. 2002, 71:79-84. 10.1016/S0091-3057(01)00636-0.
8. Cooper D.W. The physiology and pathology of the cerebellum. Yale J. Biol. Med. 1958, 31:108. 10.1212/WNL.9.3.199-a.
9. Ito M. Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning. Ann. N. Y. Acad. Sci. 2002, 978:273-288.
10. Swinny J.D., van der Want J.J.L., Gramsbergen A. Cerebellar development and plasticity: perspectives for motor coordination strategies, for motor skills, and for therapy. Neural Plast. 2005, 12:153-160. 10.1155/NP.2005.153.
11. Thach W.T., Goodkin H.P., Keating J.G. The cerebellum and the adaptive coordination of movement. Annu. Rev. Neurosci. 1992, 15:403-442. 10.1146/annurev.neuro.15.1.403.
12. Zhang L., Chung S.K., Chow B.K.C. The knockout of secretin in cerebellar Purkinje cells impairs mouse motor coordination and motor learning. Neuropsychopharmacology 2014, 39:1460-1468. 10.1038/npp.2013.344.
13. Heath R.G., Franklin D.E., Shraberg D. Gross pathology of the cerebellum in patients diagnosed and treated as functional psychiatric disorders. J. Nerv. Ment. Dis. 1979, 167:585-592.
14. Weinberger D.R., Torrey E.F., Wyatt R.J. Cerebellar atrophy in chronic schizophrenia. Lancet 1979, 1:718-719.
15. Weinberger D.R., Kleinman J.E., Luchins D.J., Bigelow L.B., Wyatt R.J. Cerebellar pathology in schizophrenia: a controlled postmortem study. Am. J. Psychiatry 1980, 137:359-361.
16. Pollack I.F. Posterior fossa syndrome. Int. Rev. Neurobiol. 1997, S0074-S7742. 10.1016/S0074-7742(08)60362-1.
17. van Dongen H.R., Catsman-Berrevoets C.E., van Mourik M. The syndrome of cerebellar mutism and subsequent dysarthria. Neurology 1994, 10.1212/WNL.44.11.2040.
18. Silveri M.C., Leggio M.G., Molinari M. The cerebellum contributes to linguistic production: a case of agrammatic speech following a right cerebellar lesion. Neurology 1994, 10.1212/WNL.44.11.2047.
19. Hill M.N., McEwen B.S. Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:791-797. 10.1016/j.pnpbp.2009.11.001.
20. Herkenham M., Lynn A.B., Little M.D., Johnson M.R., Melvin L.S., de Costa B.R., et al. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:1932-1936.
21. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 1991, 11:563-583. http://www.ncbi.nlm.nih.gov/pubmed/1992016.
22. Cristino L., de Petrocellis L., Pryce G., Baker D., Guglielmotti V., Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 2006, 139:1405-1415. 10.1016/j.neuroscience.2006.02.074.
23. Kreitzer A.C., Regehr W.G. Retrograde signaling by endocannabinoids. Curr. Opin. Neurobiol. 2002, 12:324-330.
24. Freund T.F., Katona I., Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol. Rev. 2003, 83:1017-1066. 10.1152/physrev.00004.2003.
25. Szabo B., Schlicker E. Effects of cannabinoids on neurotransmission. Handbook of Experimental Pharmacology 2005, 327-365. Springer, Berlin, Heidelberg. 10.1007/b137831.
26. Lovinger D.M., Davis M.I. Handbook of Basal Ganglia Structure and Function 2010, Academic Press London, London.
27. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258:1946-1949.
28. Sugiura T., Kondo S., Sukagawa A., Nakane S., Shinoda A., Itoh K., et al. 2-Arachidonoylgylcerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 1995, 215:89-97. 10.1006/bbrc.1995.2437.
29. Pugh P.L., Ahmed S.F., Smith M.I., Upton N., Hunter A.J. A behavioural characterisation of the FVB/N mouse strain. Behav. Brain Res. 2004, 155:283-289. 10.1016/j.bbr.2004.04.021.
30. Rygula R., Abumaria N., Flugge G., Fuchs E., Ruther E., Havemann-Reinecke U. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav. Brain Res. 2005, 162:127-134. 10.1016/j.bbr.2005.03.009.
31. Krugers H.J., Koolhaas J.M., Bohus B., Korf J. A single social stress-experience alters glutamate receptor-binding in rat hippocampal CA3 area. Neurosci. Lett. 1993, 154:73-77.
32. Tornatzky W., Miczek K.A. Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol. Behav. 1993, 53:983-993.
33. Adamcio B., Havemann-Reinecke U., Ehrenreich H. Chronic psychosocial stress in the absence of social support induces pathological pre-pulse inhibition in mice. Behav. Brain Res. 2009, 204:246-249. 10.1016/j.bbr.2009.05.030.
34. Bartolomucci A., Pederzani T., Sacerdote P., Panerai A.E., Parmigiani S., Palanza P. Behavioral and physiological characterization of male mice under chronic psychosocial stress. Psychoneuroendocrinology 2004, 29:899-910. 10.1016/j.psyneuen.2003.08.003.
35. Brzozka M.M., Fischer A., Falkai P., Havemann-Reinecke U. Acute treatment with cannabinoid receptor agonist WIN55212.2 improves prepulse inhibition in psychosocially stressed mice. Behav. Brain Res. 2011, 218:280-287. 10.1016/j.bbr.2010.11.003.
36. Golub M.S., Germann S.L., Lloyd K.C. Behavioral characteristics of a nervous system-specific erbB4 knock-out mouse. Behav. Brain Res. 2004, 153:159-170. 10.1016/j.bbr.2003.11.010.
37. Franco-Pons N., Torrente M., Colomina M.T., Vilella E. Behavioral deficits in the cuprizone-induced murine model of demyelination/remyelination. Toxicol. Lett. 2007, 169:205-213.
38. Matias I., Petrosino S., Racioppi A., Capasso R., Izzo A.A., Di Marzo V. Dysregulation of peripheral endocannabinoid levels in hyperglycemia and obesity: effect of high fat diets. Mol. Cell. Endocrinol. 2008, 286.
39. Di Marzo V., Goparaju S.K., Wang L., Liu J., Batkai S., Jarai Z., et al. Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 2001, 410:822-825. 10.1038/35071088.
40. Bisogno T., Martire A., Petrosino S., Popoli P., Di Marzo V. Symptom-related changes of endocannabinoid and palmitoylethanolamide levels in brain areas of R6/2 mice, a transgenic model of Huntington's disease. Neurochem. Int. 2008, 52:307-313.
41. Hunt D., Mason M.R.J., Campbell G., Coffin R., Anderson P.N. Nogo receptor mRNA expression in intact and regenerating CNS neurons. Mol. Cell. Neurosci. 2002, 20:537-552.
42. Mingorance A., Fontana X., Sole M., Burgaya F., Urena J.M., Teng F.Y., et al. Regulation of Nogo and Nogo receptor during the development of the entorhino-hippocampal pathway and after adult hippocampal lesions. Mol. Cell. Neurosci. 2004, 26:34-49. 10.1016/j.mcn.2004.01.001.
43. Pruitt K.D., Brown G.R., Hiatt S.M., Thibaud-Nissen F., Astashyn A., Ermolaeva O., et al. RefSeq: an update on mammalian reference sequences. Nucleic Acids Res. 2014, 42:D756-D763. 10.1093/nar/gkt1114.
44. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
45. Anders S., Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010, 11:R106.
46. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 1995, 57:289-300. http://www.jstor.org/stable/2346101.
47. Hoshida Y., Villanueva A., Sangiovanni A., Sole M., Hur C., Andersson K.L., et al. Prognostic gene expression signature for patients with hepatitis C-related early-stage cirrhosis. Gastroenterology 2013, 144:1024-1030.
48. Prostko C.R., Dholakia J.N., Brostrom M.A., Brostrom C.O. Activation of the double-stranded RNA-regulated protein kinase by depletion of endoplasmic reticular calcium stores. J. Biol. Chem. 1995, 270:6211-6215. 10.1074/jbc.270.11.6211.
49. Jeffery J., Kendall J.M., Campbell A.K. Apoaequorin monitors degradation of endoplasmic reticulum (ER) proteins initiated by loss of ER Ca(2+). Biochem. Biophys. Res. Commun. 2000, 268:711-715. 10.1006/bbrc.2000.2194.
50. Liu H., Han F., Shi Y. Effect of calreticulin on Ca/CaM kinaseIIalpha and endoplasmic reticulum stress in hippocampal in a rat model of post-traumatic stress disorder. Neurochem. Res. 2013, 10.1007/s11064-013-1038-8.
51. Ozawa K., Kondo T., Hori O., Kitao Y., Stern D.M., Eisenmenger W., et al. Expression of the oxygen-regulated protein ORP150 accelerates wound healing by modulating intracellular VEGF transport. J. Clin. Invest. 2001, 108:41-50.
52. Zhao L., Rosales C., Seburn K., Ron D., Ackerman S.L. Alteration of the unfolded protein response modifies neurodegeneration in a mouse model of Marinesco-Sjögren syndrome. Hum. Mol. Genet. 2009, 19:25-35.
53. Agus D.B., Gambhir S.S., Pardridge W.M., Spielholz C., Baselga J., Vera J.C., et al. Vitamin C crosses the blood-brain barrier in the oxidized form through the glucose transporters. J. Clin. Invest. 1997, 100:2842-2848.
54. Saeki K., Zhu M., Kubosaki A., Xie J., Lan M.S., Notkins A.L. Targeted disruption of the protein tyrosine phosphatase-like molecule IA-2 results in alterations in glucose tolerance tests and insulin secretion. Diabetes 2002, 51:1842-1850. 10.2337/diabetes.51.6.1842.
55. Kubosaki A., Gross S., Miura J., Saeki K., Zhu M., Nakamura S., et al. Targeted disruption of the IA-2 beta gene causes glucose intolerance and impairs insulin secretion but does not prevent the development of diabetes in NOD mice. Diabetes 2004, 53:1684-1691. ://000222397000008.
56. Wang S., Kaufman R.J. The impact of the unfolded protein response on human disease. J. Cell Biol. 2012, 197:857-867. 10.1083/jcb.201110131.
57. Cornejo V.H., Pihán P., Vidal R.L., Hetz C. Role of the unfolded protein response in organ physiology: lessons from mouse models. IUBMB Life 2013, 65:962-975.
58. Valdés P., Mercado G., Vidal R.L., Molina C., Parsons G., Court F.A., et al. Control of dopaminergic neuron survival by the unfolded protein response transcription factor XBP1. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:6804-6809. 10.1073/pnas.1321845111.
59. Anlar B., Gunel-Ozcan A. Tenascin-R: role in the central nervous system. Int. J. Biochem. Cell Biol. 2012, 44:1385-1389. 10.1016/j.biocel.2012.05.009.
60. Curley J.P., Pinnock S.B., Dickson S.L., Thresher R., Miyoshi N., Surani M.A., et al. Increased body fat in mice with a targeted mutation of the paternally expressed imprinted gene Peg3. FASEB J. 2005, 19:1302-1304. 10.1096/fj.04-3216fje.
61. Thiaville M.M., Huang J.M., Kim H., Ekram M.B., Roh T.Y., Kim J. DNA-binding motif and target genes of the imprinted transcription factor PEG3. Gene 2013, 512:314-320.
62. Goebel M., Fleming S.M., Million M., Stengel A., Taché Y., Wang L. Mice overexpressing corticotropin-releasing factor show brain atrophy and motor dysfunctions. Neurosci. Lett. 2010, 473:11-15.
63. Parker C.C., Ponicsan H., Spencer R.L., Holmes A., Johnson T.E. Restraint stress and exogenous corticosterone differentially alter sensitivity to the sedative-hypnotic effects of ethanol in inbred long-sleep and inbred short-sleep mice. Alcohol 2008, 42:477-485. 10.1016/j.alcohol.2008.05.004.
64. Green B., Kavanagh D., Young R. Being stoned: a review of self-reported cannabis effects. Drug Alcohol Rev. 2003, 22:453-460. 10.1080/09595230310001613976.
65. 1 receptor blockade. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:4786-4791. 10.1073/pnas.1218573110.
66. Friemel C.M., Zimmer A., Schneider M. The CB1 receptor as an important mediator of hedonic reward processing. Neuropsychopharmacology 2014, 39:2387-2396. 10.1038/npp.2014.86.
67. Haller J., Varga B., Ledent C., Freund T.F. CB1 cannabinoid receptors mediate anxiolytic effects: convergent genetic and pharmacological evidence with CB1-specific agents. Behav. Pharmacol. 2004, 15:299-304. 10.1097/01.fbp.0000135704.56422.40.
68. Marsicano G., Wotjak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., et al. The endogenous cannabinoid system controls extinction of aversive memories. Nature 2002, 418:530-534. 10.1038/nature00839.
69. Patel S., Roelke C.T., Rademacher D.J., Cullinan W.E., Hillard C.J. Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 2004, 145:5431-5438. 10.1210/en.2004-0638.
70. Sanchis-Segura C., Cline B.H., Marsicano G., Lutz B., Spanagel R. Reduced sensitivity to reward in CB1 knockout mice. Psychopharmacology (Berl.) 2004, 176:223-232. 10.1007/s00213-004-1877-8.
71. Santucci V., Storme J.J., Soubrié P., Le Fur G. Arousal-enhancing properties of the CB1 cannabinoid receptor antagonist SR 141716A in rats as assessed by electroencephalographic spectral and sleep-waking cycle analysis. Life Sci. 1996, 58. 10.1016/0024-3205(95)02319-4.
72. Shonesy S., Bluett B.C., Ramikie R.J., Báldi T.S., Hermanson R., Kingsley D.J., Marnett P.J., Winder L.J., Colbran D.G., Patel R.J. Genetic disruption of 2-arachidonoylglycerol synthesis reveals a key role for endocannabinoid signaling in anxiety modulation. Cell Rep. 2014, 9:1644-1653. 10.1016/j.celrep.2014.11.001.
73. Tallett A.J., Blundell J.E., Rodgers R.J. Grooming, scratching and feeding: role of response competition in acute anorectic response to rimonabant in male rats. Psychopharmacology (Berl.) 2007, 195:27-39. 10.1007/s00213-007-0880-2.
74. Varvel S.A., Lichtman A.H. Evaluation of CB1 receptor knockout mice in the Morris water maze. J. Pharmacol. Exp. Ther. 2002, 301:915-924. 10.1124/jpet.301.3.915.
75. Morena M., Patel S., Bains Jaideep S., Hill M.N. Neurobiological interactions between stress and the endocannabinoid system. Neuropsychopharmacology 2015, 10.1038/npp.2015.166.
76. Steiner M.A., Wanisch K., Monory K., Marsicano G., Borroni E., Bächli H., et al. Impaired cannabinoid receptor type 1 signaling interferes with stress-coping behavior in mice. Pharmacogenomics J. 2008, 8:196-208. 10.1038/sj.tpj.6500466.
77. Hill M.N., McLaughlin R.J., Bingham B., Shrestha L., Lee T.T.Y., Gray J.M., et al. Endogenous cannabinoid signaling is essential for stress adaptation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9406-9411. 10.1073/pnas.0914661107.
78. Patel S., Kingsley P.J., Mackie K., Marnett L.J., Winder D.G. Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala. Neuropsychopharmacology 2009, 34:2699-2709. 10.1038/npp.2009.101.
79. Patel S., Roelke C.T., Rademacher D.J., Hillard C.J. Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Eur. J. Neurosci. 2005, 21:1057-1069. 10.1111/j.1460-9568.2005.03916.x.
80. Rademacher D.J., Hillard C.J. Interactions between endocannabinoids and stress-induced decreased sensitivity to natural reward. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31:633-641. 10.1016/j.pnpbp.2006.12.013.
81. Hill M.N., Carrier E.J., Ho W.-S.V., Shi L., Patel S., Gorzalka B.B., et al. Prolonged glucocorticoid treatment decreases cannabinoid CB1 receptor density in the hippocampus. Hippocampus 2008, 18:221-226. 10.1002/hipo.20386.
82. Hill M.N., Patel S., Carrier E.J., Rademacher D.J., Ormerod B.K., Hillard C.J., et al. Downregulation of endocannabinoid signaling in the hippocampus following chronic unpredictable stress. Neuropsychopharmacology 2005, 30:508-515. 10.1038/sj.npp.1300601.
83. Hu W., Zhang M., Czéh B., Zhang W., Flügge G. Chronic restraint stress impairs endocannabinoid mediated suppression of GABAergic signaling in the hippocampus of adult male rats. Brain Res. Bull. 2011, 85:374-379. 10.1016/j.brainresbull.2011.04.005.
84. Lee T.T.Y., Hill M.N. Age of stress exposure modulates the immediate and sustained effects of repeated stress on corticolimbic cannabinoid CB1 receptor binding in male rats. Neuroscience 2013, 249:106-114. 10.1016/j.neuroscience.2012.11.017.
85. Reich C.G., Taylor M.E., McCarthy M.M. Differential effects of chronic unpredictable stress on hippocampal CB1 receptors in male and female rats. Behav. Brain Res. 2009, 203:264-269. 10.1016/j.bbr.2009.05.013.
86. Wamsteeker J.I., Kuzmiski J.B., Bains J.S. Repeated stress impairs endocannabinoid signaling in the paraventricular nucleus of the hypothalamus. J. Neurosci. 2010, 30:11188-11196. 10.1523/JNEUROSCI. 1046-10.2010.
87. Wamsteeker Cusulin J.I., Senst L., Teskey G.C., Bains J.S. Experience salience gates endocannabinoid signaling at hypothalamic synapses. J. Neurosci. 2014, 34:6177-6181. 10.1523/JNEUROSCI.0163-14.2014.
88. Rossi S., De Chiara V., Musella A., Kusayanagi H., Mataluni G., Bernardi G., et al. Chronic psychoemotional stress impairs cannabinoid-receptor-mediated control of GABA transmission in the striatum. J. Neurosci. 2008, 28:7284-7292. 10.1523/JNEUROSCI.5346-07.2008.
89. Rossi S., De Chiara V., Musella A., Sacchetti L., Cantarella C., Castelli M., et al. Preservation of striatal cannabinoid CB1 receptor function correlates with the antianxiety effects of fatty acid amide hydrolase inhibition. Mol. Pharmacol. 2010, 78:260-268. 10.1124/mol.110.064196.
90. Wang W., Sun D., Pan B., Roberts C.J., Sun X., Hillard C.J., et al. Deficiency in endocannabinoid signaling in the nucleus accumbens induced by chronic unpredictable stress. Neuropsychopharmacology 2010, 35:2249-2261. 10.1038/npp.2010.99.
91. Hong S., Zheng G., Wu X., Snider N.T., Owyang C., Wiley J.W. Corticosterone mediates reciprocal changes in CB 1 and TRPV1 receptors in primary sensory neurons in the chronically stressed rat. Gastroenterology 2011, 140:627-637. 10.1053/j.gastro.2010.11.003.
92. Bowles N.P., Hill M.N., Bhagat S.M., Karatsoreos I.N., Hillard C.J., McEwen B.S. Chronic, noninvasive glucocorticoid administration suppresses limbic endocannabinoid signaling in mice. Neuroscience 2012, 204:83-89. 10.1016/j.neuroscience.2011.08.048.
93. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 2003, 11:619-633.
94. Forman M.S., Lee V.M.Y., Trojanowski J.Q. Unfolding pathways in neurodegenerative disease. Trends Neurosci. 2003, 26:407-410.
95. Hübener J., Vauti F., Funke C., Wolburg H., Ye Y., Schmidt T., et al. N-terminal ataxin-3 causes neurological symptoms with inclusions, endoplasmic reticulum stress and ribosomal dislocation. Brain 2011, 134:1925-1942. 10.1093/brain/awr118.
96. Balabanov R., Strand K., Kemper A., Lee J.Y., Popko B. Suppressor of cytokine signaling 1 expression protects oligodendrocytes from the deleterious effects of interferon-gamma. J. Neurosci. 2006, 26:5143-5152. 10.1523/JNEUROSCI.0737-06.2006.
97. Franklin R.J.M., Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 2008, 9:839-855. 10.1038/nrn2480.
98. Wang S.-Z., Dulin J., Wu H., Hurlock E., Lee S.-E., Jansson K., et al. An oligodendrocyte-specific zinc-finger transcription regulator cooperates with Olig2 to promote oligodendrocyte differentiation. Development 2006, 133:3389-3398. 10.1242/dev.02522.