Repeated forced swim stress differentially affects formalin-evoked nociceptive behaviour and the endocannabinoid system in stress normo-responsive and stress hyper-responsive rat strains

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 64, Issue , 2016, Pages 181-189

  Jennings, Elaine M ^a   Okine, Bright N ^a   Olango, Weredeselam M ^a   Roche, Michelle ^a   Finn, David P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Endocannabinoid; Pain; Sprague Dawley; Stress induced hyperalgesia; Wistar Kyoto

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLGLYCEROL LIPASE; ANANDAMIDE; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; FATTY ACID AMIDASE; FORMALDEHYDE; MESSENGER RNA;

ADULT; AFFECT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DORSAL ROOT; FORCED SWIM TEST; HYPERALGESIA; LATERAL AMYGDALA; MALE; NEGATIVE AFFECT; NOCICEPTION; NONHUMAN; RAT; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; SPRAGUE DAWLEY RAT; STRESS; WISTAR KYOTO RAT; AMYGDALA; ANIMAL; COMPARATIVE STUDY; COPING BEHAVIOR; DISEASE MODEL; GENETIC PREDISPOSITION; HEAT; HEMISPHERIC DOMINANCE; MENTAL STRESS; METABOLISM; MOTOR ACTIVITY; NOCICEPTIVE PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; POSTERIOR HORN CELL; PSYCHOLOGY; RANDOMIZATION; SPECIES DIFFERENCE; SWIMMING;

AMYGDALA; ANIMALS; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; FORMALDEHYDE; FUNCTIONAL LATERALITY; GENETIC PREDISPOSITION TO DISEASE; HOT TEMPERATURE; MALE; MOTOR ACTIVITY; NOCICEPTIVE PAIN; POSTERIOR HORN CELLS; RANDOM ALLOCATION; RATS, INBRED WKY; RATS, SPRAGUE-DAWLEY; RESILIENCE, PSYCHOLOGICAL; RNA, MESSENGER; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 84941177291     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2015.05.008     Document Type: Article

References (71)

1. Alvarez P., Green P.G., Levine J.D. Stress in the adult rat exacerbates muscle pain induced by early-life stress. Biol Psychiatry 2013, 74:688-695.
2. Bardin L., Malfetes N., Newman-Tancredi A., DepoortãrRe R. Chronic restraint stress induces mechanical and cold allodynia, and enhances inflammatory pain in rat: relevance to human stress-associated painful pathologies. Behav Brain Res 2009, 205:360-366.
3. Burke N.N., Hayes E., Calpin P., Kerr D.M., Moriarty O., Finn D.P., et al. Enhanced nociceptive responding in two rat models of depression is associated with alterations in monoamine levels in discrete brain regions. Neuroscience 2010, 171:1300-1313.
4. Burke N.N., Kerr D.M., Moriarty O., Finn D.P., Roche M. Minocycline modulates neuropathic pain behaviour and cortical M1-M2 microglial gene expression in a rat model of depression. Brain Behav Immun 2014, 42:147-156.
5. Butler R.K., Finn D.P. Stress-induced analgesia. Prog Neurbiol 2009, 88:184-202.
6. Butler R.K., Ford G.K., Hogan M., Roche M., Doyle K.M., Kelly J.P., et al. Fear-induced suppression of nociceptive behaviour and activation of Akt signalling in the rat periaqueductal grey: role of fatty acid amide hydrolase. J Psychopharmacol 2012, 26:83-91.
7. Connell K., Bolton N., Olsen D., Piomelli D., Hohmann A.G. Role of the basolateral nucleus of the amygdala in endocannabinoid-mediated stress-induced analgesia. Neurosci Lett 2006, 397:180-184.
8. Connor T.J., Kelly J.P., Leonard B.E. Forced swim test-induced neurochemical endocrine, and immune changes in the rat. Pharmacol Biochem Behav 1997, 58:961-967.
9. Cravatt B.F., Giang D.K., Mayfield S.P., Boger D.L., Lerner R.A., Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 1996, 384:83-87.
10. 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.
11. Dina O.A., Levine J.D., Green P.G. Enhanced cytokine-induced mechanical hyperalgesia in skeletal muscle produced by a novel mechanism in rats exposed to unpredictable sound stress. Eur J Pain 2011, 15:796-800.
12. Dinh T.P., Carpenter D., Leslie F.M., Freund T.F., Katona I., Sensi S.L., et al. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci U S A 2002, 99:10819-10824.
13. Dubuisson D., Dennis S.G. The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 1977, 4:161-174.
14. Fichna J., Wood J.T., Papanastasiou M., Vadivel S.K., Oprocha P., Salaga M., et al. Endocannabinoid and cannabinoid-like fatty acid amide levels correlate with pain-related symptoms in patients with IBS-D and IBS-C: a pilot study. PLoS ONE 2013, 8:e85073.
15. Finn D.P. Endocannabinoid-mediated modulation of stress responses: physiological and pathophysiological significance. Immunobiology 2010, 215:629-646.
16. Finn D.P., Jhaveri M.D., Beckett S.R., Roe C.H., Kendall D.A., Marsden C.A., et al. Effects of direct periaqueductal grey administration of a cannabinoid receptor agonist on nociceptive and aversive responses in rats. Neuropharmacology 2003, 45:594-604.
17. Finn D.P., Viveros M.P., Marco E.M. The endocannabinoid system and emotional processing: pathophysiology and therapeutic potential. J Psychopharmacol 2012, 26:3-6.
18. Ford G.K., Kieran S., Dolan K., Harhen B., Finn D.P. A role for the ventral hippocampal endocannabinoid system in fear-conditioned analgesia and fear responding in the presence of nociceptive tone in rats. Pain 2011, 152:2495-2504.
19. Gibbons C.H., Adler G.K., Bonyhay I., Freeman R. Experimental hypoglycemia is a human model of stress-induced hyperalgesia. Pain 2012, 153:2204-2209.
20. Green P.G., Chen X.J., Alvarez P., Ferrari L.F., Levine J.D. Early-life stress produces muscle hyperalgesia and nociceptor sensitization in the adult rat. Pain 2011, 152:2549-2556.
21. Hasanein P., Parviz M., Keshavarz M., Javanmardi K. CB1 receptor activation in the basolateral amygdala produces antinociception in animal models of acute and tonic nociception. Clin Exp Pharmacol Physiol 2007, 34:439-449.
22. Hauer D., Schelling G., Gola H., Campolongo P., Morath J., Roozendaal B., et al. Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder. PLoS ONE 2013, 8:e62741.
23. Hill M.N., McLaughlin R.J., Morrish A.C., Viau V., Floresco S.B., Hillard C.J., et al. Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology 2009, 34:2733-2745.
24. Hill M.N., McLaughlin R.J., Bingham B., Shrestha L., Lee T.T., Gray J.M., et al. Endogenous cannabinoid signaling is essential for stress adaptation. Proc Natl Acad Sci U S A 2010, 107:9406-9411.
25. Hill M.N., Kumar S.A., Filipski S.B., Iverson M., Stuhr K.L., Keith J.M., et al. Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdalar microstructure. Mol Psychiatry 2013, 18:1125-1135.
26. Hohmann A.G., Suplita R.L. Endocannabinoid mechanisms of pain modulation. AAPS J 2006, 8:E693-E708.
27. Hohmann A.G., Suplita R.L., Bolton N.M., Neely M.H., Fegley D., Mangieri R., et al. An endocannabinoid mechanism for stress-induced analgesia. Nature 2005, 435:1108-1112.
28. Hong S., Fan J., Kemmerer E.S., Evans S., Li Y., Wiley J.W. Reciprocal changes in vanilloid (TRPV1) and endocannabinoid (CB1) receptors contribute to visceral hyperalgesia in the water avoidance stressed rat. Gut 2009, 58:202-210.
29. 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 e4-637 e4.
30. Honndorf S., Lindemann C., Tollner K., Gernert M. Female Wistar rats obtained from different breeders vary in anxiety-like behavior and epileptogenesis. Epilepsy Res 2011, 94:26-38.
31. Hu W., Zhang M., Czeh B., Zhang W., Flugge 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.
32. Jennings E.M., Okine B.N., Roche M., Finn D.P. Stress-induced hyperalgesia. Prog Neurobiol 2014, 121:1-18.
33. Ji G., Neugebauer V. Hemispheric lateralization of pain processing by amygdala neurons. J Neurophysiol 2009, 102:2253-2264.
34. Kaufmann I., Schelling G., Eisner C., Richter H.P., Krauseneck T., Vogeser M., et al. Anandamide and neutrophil function in patients with fibromyalgia. Psychoneuroendocrinology 2008, 33:676-685.
35. Kelliher P., Connor T.J., Harkin A., Sanchez C., Kelly J.P., Leonard B.E. Varying responses to the rat forced-swim test under diurnal and nocturnal conditions. Physiol Behav 2000, 69:531-539.
36. Kerr D.M., Burke N.N., Ford G.K., Connor T.J., Harhen B., Egan L.J., et al. Pharmacological inhibition of endocannabinoid degradation modulates the expression of inflammatory mediators in the hypothalamus following an immunological stressor. Neuroscience 2012, 204:53-63.
37. Knaster P., Karlsson H., Estlander A.M., Kalso E. Psychiatric disorders as assessed with SCID in chronic pain patients: the anxiety disorders precede the onset of pain. Gen Hosp Psychiatry 2012, 34:46-52.
38. Kolber B.J., Montana M.C., Carrasquillo Y., Xu J., Heinemann S.F., Muglia L.J., et al. Activation of metabotropic glutamate receptor 5 in the amygdala modulates pain-like behavior. J Neurosci 2010, 30:8203-8213.
39. Kuehl L.K., Michaux G.P., Richter S., SchãChinger H., Anton F. Increased basal mechanical pain sensitivity but decreased perceptual wind-up in a human model of relative hypocortisolism. Pain 2010, 149:539-546.
40. Le Roy C., Laboureyras E., Gavello-Baudy S.P., Chateauraynaud J.R.M., Laulin J.-P., Simonnet G. Endogenous opioids released during non-nociceptive environmental stress induce latent pain sensitization via a NMDA-dependent process. J Pain 2011, 12:1069-1079.
41. Lutz B. Endocannabinoid signals in the control of emotion. Curr Opin Pharmacol 2009, 9:46-52.
42. 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.
43. Martin W.J., Coffin P.O., Attias E., Balinsky M., Tsou K., Walker J.M. Anatomical basis for cannabinoid-induced antinociception as revealed by intracerebral microinjections. Brain Res 1999, 822:237-242.
44. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346:561-564.
45. Mechoulam R., Ben-Shabat S., Hanus L., Ligumsky M., Kaminski N.E., Schatz A.R., et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 1995, 50:83-90.
46. Meng I.D., Manning B.H., Martin W.J., Fields H.L. An analgesia circuit activated by cannabinoids. Nature 1998, 395:381-383.
47. Munro S., Thomas K.L., Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365:61-65.
48. Naderi N., Shafaghi B., Khodayar M.J., Zarindast M.R. Interaction between gamma-aminobutyric acid GABAB and cannabinoid CB1 receptors in spinal pain pathways in rat. Eur J Pharmacol 2005, 514:159-164.
49. Olango W.M., Finn D.P. Neurobiology of stress-induced hyperalgesia. Curr Top Behav Neurosci 2014, 20:251-280.
50. Olango W.M., Roche M., Ford G.K., Harhen B., Finn D.P. The endocannabinoid system in the rat dorsolateral periaqueductal grey mediates fear-conditioned analgesia and controls fear expression in the presence of nociceptive tone. Br J Pharmacol 2011, 165:2549-2560.
51. O'Mahony, Clarke G., Mckernan D.P., Bravo J.A., Dinan T.G., Cryan J.F. Differential visceral nociceptive, behavioural and neurochemical responses to an immune challenge in the stress-sensitive Wistar Kyoto rat strain. Behav Brain Res 2013, 253:310-317.
52. Perez J., Ware M.A., Chevalier S., Gougeon R., Bennett G.J., Shir Y. Dietary fat and protein interact in suppressing neuropathic pain-related disorders following a partial sciatic ligation injury in rats. Pain 2004, 111:297-305.
53. Phelps E.A., O'Connor K.J., Gatenby J.C., Gore J.C., Grillon C., Davis M. Activation of the left amygdala to a cognitive representation of fear. Nat Neurosci 2001, 4:437-441.
54. Quintero L., Moreno M., Avila C., Arcaya J., Maixner W., Suarez-Roca H. Long-lasting delayed hyperalgesia after subchronic swim stress. Pharmacol Biochem Behav 2000, 67:449-458.
55. Quintero L., Cuesta M.C., Silva J.A., Arcaya J.L., Pinerua-Suhaibar L., Maixner W., et al. Repeated swim stress increases pain-induced expression of c-Fos in the rat lumbar cord. Brain Res 2003, 965:259-268.
56. Quintero L., Cardenas R., Suarez-Roca H. Stress-induced hyperalgesia is associated with a reduced and delayed GABA inhibitory control that enhances post-synaptic NMDA receptor activation in the spinal cord. Pain 2011, 152:1909-1922.
57. Rea K., Olango W.M., Harhen B., Kerr D.M., Galligan R., Fitzgerald S., et al. Evidence for a role of GABAergic and glutamatergic signalling in the basolateral amygdala in endocannabinoid-mediated fear-conditioned analgesia in rats. Pain 2013, 154:576-585.
58. Rea K., Olango W.M., Okine B.N., Madasu M.K., Mcguire I.C., Coyle K., et al. Impaired endocannabinoid signalling in the rostral ventromedial medulla underpins genotype-dependent hyper-responsivity to noxious stimuli. Pain 2014, 155:69-79.
59. Robbins M., Deberry J., Ness T. Chronic psychological stress enhances nociceptive processing in the urinary bladder in high-anxiety rats. Physiol Behav 2007, 91:544-550.
60. Roche M., O'Connor E., Diskin C., Finn D.P. The effect of CB(1) receptor antagonism in the right basolateral amygdala on conditioned fear and associated analgesia in rats. Eur J Neurosci 2007, 26:2643-2653.
61. Shen L., Yang X.J., Qian W., Hou X.H. The role of peripheral cannabinoid receptors type 1 in rats with visceral hypersensitivity induced by chronic restraint stress. J Neurogastroenterol Motil 2010, 16:281-290.
62. Simpson J., Kelly J.P. The impact of environmental enrichment in laboratory rats-behavioural and neurochemical aspects. Behav Brain Res 2011, 222:246-264.
63. Suarez-Roca H., Quintero L., Arcaya J.L., Maixner W., Rao S.G. Stress-induced muscle and cutaneous hyperalgesia: differential effect of milnacipran. Physiol Behav 2006, 88:82-87.
64. Suarez-Roca H., Leal L., Silva J.A., Pinerua-Shuhaibar L., Quintero L. Reduced GABA neurotransmission underlies hyperalgesia induced by repeated forced swimming stress. Behav Brain Res 2008, 189:159-169.
65. Suarez-Roca H., Quintero L., Avila R., Medina S., De Freitas M., Cardenas R. Central immune overactivation in the presence of reduced plasma corticosterone contributes to swim stress-induced hyperalgesia. Brain Res Bull 2014, 100:61-69.
66. Sugiura T., Kondo S., Sukagawa A., Nakane S., Shinoda A., Itoh K., et al. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 1995, 215:89-97.
67. Vinod K.Y., Xie S., Psychoyos D., Hungund B.L., Cooer T.B., Tejani-Butt S.M. Dysfunction in fatty acid amide hydrolase is associated with depressive-like behavior in Wistar Kyoto rats. PLoS One 2012, 7:e36743. 10.1371/journal.pone.0036743.
68. Viveros M.P., Marco E.M., File S.E. Endocannabinoid system and stress and anxiety responses. Pharmacol Biochem Behav 2005, 81:331-342.
69. Walker J.M., Huang S.M., Strangman N.M., Tsou K., Sanudo-Pena M.C. Pain modulation by release of the endogenous cannabinoid anandamide. Proc Natl Acad Sci U S A 1999, 96:12198-12203.
70. 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.
71. Zhang R.X., Zhang M., Li A., Pan L., Berman B.M., Ren K., et al. DAMGO in the central amygdala alleviates the affective dimension of pain in a rat model of inflammatory hyperalgesia. Neuroscience 2013, 252:359-366.