Chronic stress and peripheral pain: Evidence for distinct, region-specific changes in visceral and somatosensory pain regulatory pathways

Experimental Neurology

Volumn 273, Issue , 2015, Pages 301-311

  Zheng, Gen ^a   Hong, Shuangsong ^a   Hayes, John M ^a   Wiley, John W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

CB1; Chronic stress; Endocannabinoid; Pain; Sodium channel; Somatosensory hyperalgesia; Trpv1; Visceral hyperalgesia

Indexed keywords

CANNABINOID 1 RECEPTOR; CORTICOSTERONE; CYCLOOXYGENASE 2; ENDOCANNABINOID; FATTY ACID AMIDASE; SODIUM CHANNEL NAV1.7; SODIUM CHANNEL NAV1.8; VANILLOID RECEPTOR 1; ACYLGLYCEROL; ARACHIDONIC ACID DERIVATIVE; GLYCERYL 2-ARACHIDONATE; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SUBPOPULATION; CHRONIC STRESS; CONTROLLED STUDY; DISEASE ASSOCIATION; HYPERALGESIA; IN VITRO STUDY; MALE; MYELINATION; NERVE CELL; NONHUMAN; PAIN; PAIN ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SOMATOSENSORY SYSTEM; UPREGULATION; VISCERAL PAIN; ADVERSE EFFECTS; ANIMAL; BLOOD; COMPLICATION; DISEASE MODEL; GENE EXPRESSION REGULATION; INNERVATION; LARGE INTESTINE; MENTAL STRESS; METABOLISM; MOTOR EVOKED POTENTIAL; NEURALGIA; PAIN THRESHOLD; PATHOLOGY; PATHOPHYSIOLOGY; PHYSICAL STIMULATION; PHYSIOLOGY; REACTION TIME; SENSORY NERVE; SPINAL CORD; SPINAL GANGLION; SPRAGUE DAWLEY RAT;

AFFERENT PATHWAYS; ANIMALS; ARACHIDONIC ACIDS; CORTICOSTERONE; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; EVOKED POTENTIALS, MOTOR; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; GLYCERIDES; HYPERALGESIA; INTESTINE, LARGE; MALE; NEURALGIA; PAIN THRESHOLD; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTOR, CANNABINOID, CB1; SPINAL CORD; STRESS, PSYCHOLOGICAL; TRPV CATION CHANNELS; VISCERAL PAIN;

EID: 84942887298     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.09.013     Document Type: Article

References (45)

1. Akopian A.N., Souslova V., England S., Okuse K., Ogata N., Ure J., Smith A., Kerr B.J., McMahon S.B., Boyce S., Hill R., Stanfa L.C., Dickenson A.H., Wood J.N. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat. Neurosci. 1999, 2:541-548.
2. Aldrich B.T., Frakes E.P., Kasuya J., Hammond D.L., Kitamoto T. Changes in expression of sensory organ-specific microRNAs in rat dorsal root ganglia in association with mechanical hypersensitivity induced by spinal nerve ligation. Neuroscience 2009, 164:711-723.
3. Bagal S.K., Chapman M.L., Marron B.E., Prime R., Storer R.I., Swain N.A. Recent progress in sodium channel modulators for pain. Bioorg. Med. Chem. Lett. 2014, 24:3690-3699.
4. Bisogno T., Howell F., Williams G., Minassi A., Cascio M.G., Ligresti A., Matias I., Schiano-Moriello A., Paul P., Williams E.J., Gangadharan U., Hobbs C., Di M.V., Doherty P. Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 2003, 163:463-468.
5. Bradesi S., Schwetz I., Ennes H.S., Lamy C.M., Ohning G., Fanselow M., Pothoulakis C., McRoberts J.A., Mayer E.A. Repeated exposure to water avoidance stress in rats: a new model for sustained visceral hyperalgesia. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289:G42-G53.
6. Carrier E.J., Patel S., Hillard C.J. Endocannabinoids in neuroimmunology and stress. Curr. Drug Targets CNS Neurol. Disord. 2005, 4:657-665.
7. Catterall W.A. Cellular and molecular biology of voltage-gated sodium channels. Physiol. Rev. 1992, 72:S15-S48.
8. Chappell P.B., Smith M.A., Kilts C.D., Bissette G., Ritchie J., Anderson C., Nemeroff C.B. Alterations in corticotropin-releasing factor-like immunoreactivity in discrete rat brain regions after acute and chronic stress. J. Neurosci. 1986, 6:2908-2914.
9. Cheng H.T., Dauch J.R., Hayes J.M., Hong Y., Feldman E.L. Nerve growth factor mediates mechanical allodynia in a mouse model of type 2 diabetes. J. Neuropathol. Exp. Neurol. 2009, 68:1229-1243.
10. Christianson J.A., Liang R., Ustinova E.E., Davis B.M., Fraser M.O., Pezzone M.A. Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain 2007, 128:235-243.
11. Cummins T.R., Sheets P.L., Waxman S.G. The roles of sodium channels in nociception: implications for mechanisms of pain. Pain 2007, 131:243-257.
12. de Carvalho Rocha H.A., Dantas B.P., Rolim T.L., Costa B.A., de Medeiros A.C. Main ion channels and receptors associated with visceral hypersensitivity in irritable bowel syndrome. Ann. Gastroenterol. 2014, 27:200-206.
13. Gray J.D., Milner T.A., McEwen B.S. Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience 2013, 239:214-227.
14. Grove G.L. Physiologic changes in older skin. Clin. Geriatr. Med. 1989, 5:115-125.
15. Hannibal K.E., Bishop M.D. Chronic stress, cortisol dysfunction, and pain: a psychoneuroendocrine rationale for stress management in pain rehabilitation. Phys. Ther. 2014, 94:1816-1825.
16. Herrity A.N., Rau K.K., Petruska J.C., Stirling D.P., Hubscher C.H. Identification of bladder and colon afferents in the nodose ganglia of male rats. J. Comp. Neurol. 2014, 522:3667-3682.
17. Hong S., Wiley J.W. Early painful diabetic neuropathy is associated with differential changes in the expression and function of vanilloid receptor 1. J. Biol. Chem. 2005, 280:618-627.
18. Hong S., Morrow T.J., Paulson P.E., Isom L.L., Wiley J.W. Early painful diabetic neuropathy is associated with differential changes in tetrodotoxin-sensitive and -resistant sodium channels in dorsal root ganglion neurons in the rat. J. Biol. Chem. 2004, 279:29341-29350.
19. Hong S., Agresta L., Guo C., Wiley J.W. The TRPV1 receptor is associated with preferential stress in large dorsal root ganglion neurons in early diabetic sensory neuropathy. J. Neurochem. 2008, 105:1212-1222.
20. 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.
21. 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.
22. Hu S., Xiao Y., Zhu L., Li L., Hu C.Y., Jiang X., Xu G.Y. Neonatal maternal deprivation sensitizes voltage-gated sodium channel currents in colon-specific dorsal root ganglion neurons in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 304:G311-G321.
23. Jeske N.A., Patwardhan A.M., Gamper N., Price T.J., Akopian A.N., Hargreaves K.M. Cannabinoid WIN 55,212-2 regulates TRPV1 phosphorylation in sensory neurons. J. Biol. Chem. 2006, 281:32879-32890.
24. Jeske N.A., Patwardhan A.M., Ruparel N.B., Akopian A.N., Shapiro M.S., Henry M.A. A-kinase anchoring protein 150 controls protein kinase C-mediated phosphorylation and sensitization of TRPV1. Pain 2009.
25. Joels M., Karst H., Krugers H.J., Lucassen P.J. Chronic stress: implications for neuronal morphology, function and neurogenesis. Front. Neuroendocrinol. 2007, 28:72-96.
26. Johnson A.C., Greenwood-Van M.B. Stress-induced pain: a target for the development of novel therapeutics. J. Pharmacol. Exp. Ther. 2014, 351:327-335.
27. La J.H., Schwartz E.S., Gebhart G.F. Differences in the expression of transient receptor potential channel V1, transient receptor potential channel A1 and mechanosensitive two pore-domain K+ channels between the lumbar splanchnic and pelvic nerve innervations of mouse urinary bladder and colon. Neuroscience 2011, 186:179-187.
28. Larauche M., Mulak A., Tache Y. Stress and visceral pain: from animal models to clinical therapies. Exp. Neurol. 2012, 233:49-67.
29. Lightman S.L. The neuroendocrinology of stress: a never ending story. J. Neuroendocrinol. 2008, 20:880-884.
30. Liu M., Wood J.N. The roles of sodium channels in nociception: implications for mechanisms of neuropathic pain. Pain Med. 2011, 12(Suppl. 3):S93-S99.
31. Liu J., Gao Z., Li J. Femoral artery occlusion increases expression of ASIC3 in dorsal root ganglion neurons. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H1357-H1364.
32. Lowin T., Zhu W., Dettmer-Wilde K., Straub R.H. Cortisol-mediated adhesion of synovial fibroblasts is dependent on the degradation of anandamide and activation of the endocannabinoid system. Arthritis Rheum. 2012, 64:3867-3876.
33. Mitrirattanakul S., Ramakul N., Guerrero A.V., Matsuka Y., Ono T., Iwase H., Mackie K., Faull K.F., Spigelman I. Site-specific increases in peripheral cannabinoid receptors and their endogenous ligands in a model of neuropathic pain. Pain 2006, 126:102-114.
34. Okamoto Y., Morishita J., Tsuboi K., Tonai T., Ueda N. Molecular characterization of a phospholipase D generating anandamide and its congeners. J. Biol. Chem. 2004, 279:5298-5305.
35. 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.
36. Pernia-Andrade A.J., Kato A., Witschi R., Nyilas R., Katona I., Freund T.F., Watanabe M., Filitz J., Koppert W., Schuttler J., Ji G., Neugebauer V., Marsicano G., Lutz B., Vanegas H., Zeilhofer H.U. Spinal endocannabinoids and CB1 receptors mediate C-fiber-induced heterosynaptic pain sensitization. Science 2009, 325:760-764.
37. Starowicz K., Makuch W., Osikowicz M., Piscitelli F., Petrosino S., Di M.V., Przewlocka B. Spinal anandamide produces analgesia in neuropathic rats: possible CB(1)- and TRPV1-mediated mechanisms. Neuropharmacology 2012, 62:1746-1755.
38. Sullivan K.A., Hayes J.M., Wiggin T.D., Backus C., Su O.S., Lentz S.I., Brosius F., Feldman E.L. Mouse models of diabetic neuropathy. Neurobiol. Dis. 2007, 28:276-285.
39. Suri D., Vaidya V.A. Glucocorticoid regulation of brain-derived neurotrophic factor: relevance to hippocampal structural and functional plasticity. Neuroscience 2013, 239:196-213.
40. Swett J.E., Torigoe Y., Elie V.R., Bourassa C.M., Miller P.G. Sensory neurons of the rat sciatic nerve. Exp. Neurol. 1991, 114:82-103.
41. Tran L., Schulkin J., Greenwood-Van M.B. Importance of CRF receptor-mediated mechanisms of the bed nucleus of the stria terminalis in the processing of anxiety and pain. Neuropsychopharmacology 2014, 39:2633-2645.
42. Waleh N.S., Cravatt B.F., Apte-Deshpande A., Terao A., Kilduff T.S. Transcriptional regulation of the mouse fatty acid amide hydrolase gene. Gene 2002, 291:203-210.
43. Wood J.N. Recent advances in understanding molecular mechanisms of primary afferent activation. Gut 2004, 53(Suppl. 2):ii9-i12.
44. Yang Y., Wang Y., Li S., Xu Z., Li H., Ma L., Fan J., Bu D., Liu B., Fan Z., Wu G., Jin J., Ding B., Zhu X., Shen Y. Mutations in SCN9A, encoding a sodium channel alpha subunit, in patients with primary erythermalgia. J. Med. Genet. 2004, 41:171-174.
45. Yiangou Y., Facer P., Chessell I.P., Bountra C., Chan C., Fertleman C., Smith V., Anand P. Voltage-gated ion channel Nav1.7 innervation in patients with idiopathic rectal hypersensitivity and paroxysmal extreme pain disorder (familial rectal pain). Neurosci. Lett. 2007, 427:77-82.