Mast cell degranulation distinctly activates trigemino-cervical and lumbosacral pain pathways and elicits widespread tactile pain hypersensitivity

Brain, Behavior, and Immunity

Volumn 26, Issue 2, 2012, Pages 311-317

  Levy, Dan ^a   Kainz, Vanessa ^a   Burstein, Rami ^a   Strassman, Andrew M ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Allodynia; Dorsal horn; Dura; Fos; Headache; Mast cell; Pain; Viscera; Visceral pain

Indexed keywords

COMPOUND 48-80; CROMOGLYCATE DISODIUM; PROTEIN C FOS;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAUDA EQUINA SYNDROME; CONTROLLED STUDY; HEADACHE; HYPERSENSITIVITY; LOW BACK PAIN; MALE; MAST CELL DEGRANULATION; NOCICEPTION; NONHUMAN; PAIN; PELVIS PAIN SYNDROME; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SINGLE DRUG DOSE; SPINAL CORD DORSAL HORN; TACTILE PAIN HYPERSENSITIVITY; VISCERAL PAIN;

ANIMALS; LOW BACK PAIN; MALE; MAST CELLS; MASTOCYTOSIS; NECK PAIN; P-METHOXY-N-METHYLPHENETHYLAMINE; PAIN; PAIN MEASUREMENT; POSTERIOR HORN CELLS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; TOUCH;

EID: 84855986247     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2011.09.016     Document Type: Article

References (45)

1. Ahluwalia A., Giuliani S., Scotland R., Maggi C.A. Ovalbumin-induced neurogenic inflammation in the bladder of sensitized rats. Br. J. Pharmacol. 1998, 124:190-196.
2. Anton F., Herdegen T., Peppel P., Leah J.D. C-FOS-like immunoreactivity in rat brainstem neurons following noxious chemical stimulation of the nasal mucosa. Neuroscience 1991, 41:629-641.
3. Anton P.M., Theodorou V., Fioramonti J., Bueno L. Chronic low-level administration of diquat increases the nociceptive response to gastric distension in rats: role of mast cells and tachykinin receptor activation. Pain 2001, 92:219-227.
4. Ashina S., Ashina M. Headache in systemic mastocytosis: a case report with pathophysiological considerations. Cephalalgia 2005, 25:314-316.
5. Barbara G., Wang B., Stanghellini V., de Giorgio R., Cremon C., Di Nardo G., Trevisani M., Campi B., Geppetti P., Tonini M., Bunnett N.W., Grundy D., Corinaldesi R. Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 2007, 132:26-37.
6. Birder L.A., de Groat W.C. Increased c-fos expression in spinal neurons after irritation of the lower urinary tract in the rat. J. Neurosci. 1992, 12:4878-4889.
7. Bon K., Lanteri-Minet M., de Pommery J., Michiels J.F., Menetrey D. Cyclophosphamide cystitis as a model of visceral pain in rats. A survey of hindbrain structures involved in visceroception and nociception using the expression of c-Fos and Krox-24 proteins. Exp. Brain. Res. Experimentelle Hirnforschung 1996, 108:404-416.
8. Bon K., Lichtensteiger C.A., Wilson S.G., Mogil J.S. Characterization of cyclophosphamide cystitis, a model of visceral and referred pain, in the mouse: species and strain differences. J. Urol. 2003, 170:1008-1012.
9. Burstein R., Jakubowski M., Garcia-Nicas E., Kainz V., Bajwa Z., Hargreaves R., Becerra L., Borsook D. Thalamic sensitization transforms localized pain into widespread allodynia. Ann. Neurol. 2010, 68:81-91.
10. Burstein R., Yamamura H., Malick A., Strassman A.M. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J. Neurophysiol. 1998, 79:964-982.
11. Burstein R., Yarnitsky D., Goor-Aryeh I., Ransil B.J., Bajwa Z.H. An association between migraine and cutaneous allodynia. Ann. Neurol. 2000, 47:614-624.
12. Cameron D.M., Brennan T.J., Gebhart G.F. Hind paw incision in the rat produces long-lasting colon hypersensitivity. J. Pain 2008, 9:246-253.
13. Cervero F., Laird J.M. Visceral pain. Lancet 1999, 353:2145-2148.
14. Coelho A.M., Fioramonti J., Bueno L. Mast cell degranulation induces delayed rectal allodynia in rats: role of histamine and 5-HT. Dig. Dis. Sci. 1998, 43:727-737.
15. Davis K.D., Meyer R.A., Campbell J.N. Chemosensitivity and sensitization of nociceptive afferents that innervate the hairy skin of monkey. J. Neurophysiol. 1993, 69:1071-1081.
16. Drummond P.D. The effect of cutaneous mast cell degranulation on sensitivity to heat. Inflamm. Res. 2004, 53:309-315.
17. Edelmayer R.M., Vanderah T.W., Majuta L., Zhang E.T., Fioravanti B., De Felice M., Chichorro J.G., Ossipov M.H., King T., Lai J., Kori S.H., Nelsen A.C., Cannon K.E., Heinricher M.M., Porreca F. Medullary pain facilitating neurons mediate allodynia in headache-related pain. Ann. Neurol. 2009, 65:184-193.
18. Esposito P., Gheorghe D., Kandere K., Pang X., Connolly R., Jacobson S., Theoharides T.C. Acute stress increases permeability of the blood-brain-barrier through activation of brain mast cells. Brain Res. 2001, 888:117-127.
19. Greene R., Fowler J., MacGlashan D., Weinreich D. IgE-challenged human lung mast cells excite vagal sensory neurons in vitro. J. Appl. Physiol. 1988, 64:2249-2253.
20. Hamilton, M.J., Hornick, J.L., Akin, C., Castells, M.C., Greenberger, N.J., 2011. Mast cell activation syndrome: A newly recognized disorder with systemic clinical manifestations. J. Allergy Clin. Immunol.
21. Hermine O., Lortholary O., Leventhal P.S., Catteau A., Soppelsa F., Baude C., Cohen-Akenine A., Palmerini F., Hanssens K., Yang Y., Sobol H., Fraytag S., Ghez D., Suarez F., Barete S., Casassus P., Sans B., Arock M., Kinet J.P., Dubreuil P., Moussy A. Case-control cohort study of patients' perceptions of disability in mastocytosis. PloS one 2008, 3:e2266.
22. Horan R.F., Austen K.F. Systemic mastocytosis: retrospective review of a decade's clinical experience at the Brigham and Women's Hospital. J. Invest. Dermatol. 1991, 96:5S-13S. discussion 13S-14S, 60S-65S.
23. Jaggar S.I., Scott H.C., Rice A.S. Inflammation of the rat urinary bladder is associated with a referred thermal hyperalgesia which is nerve growth factor dependent. Br. J. Anaesth. 1999, 83:442-448.
24. Klooker T.K., Braak B., Koopman K.E., Welting O., Wouters M.M., van der Heide S., Schemann M., Bischoff S.C., van den Wijngaard R.M., Boeckxstaens G.E. The mast cell stabiliser ketotifen decreases visceral hypersensitivity and improves intestinal symptoms in patients with irritable bowel syndrome. Gut 2010, 59:1213-1221.
25. Lanteri-Minet M., Isnardon P., de Pommery J., Menetrey D. Spinal and hindbrain structures involved in visceroception and visceronociception as revealed by the expression of Fos, Jun and Krox-24 proteins. Neuroscience 1993, 55:737-753.
26. Levy D. Migraine pain, meningeal inflammation, and mast cells. Curr. Pain Headache Reports 2009, 13:237-240.
27. Levy D., Burstein R., Kainz V., Jakubowski M., Strassman A.M. Mast cell degranulation activates a pain pathway underlying migraine headache. Pain 2007, 130:166-176.
28. Martin H.A., Basbaum A.I., Goetzl E.J., Levine J.D. Leukotriene B4 decreases the mechanical and thermal thresholds of C- fiber nociceptors in the hairy skin of the rat. J. Neurophysiol. 1988, 60:438-445.
29. Martinez V., Wang L., Mayer E., Tache Y. Proximal colon distention increases Fos expression in the lumbosacral spinal cord and activates sacral parasympathetic NADPHd-positive neurons in rats. J. Comp. Neurol. 1998, 390:311-321.
30. McCulloch P.F., Panneton W.M. Fos immunohistochemical determination of brainstem neuronal activation in the muskrat after nasal stimulation. Neuroscience 1997, 78:913-925.
31. Ohashi K., Sato Y., Kawai M., Kurebayashi Y. Abolishment of TNBS-induced visceral hypersensitivity in mast cell deficient rats. Life Sci. 2008, 82:419-423.
32. Oshinsky M.L., Gomonchareonsiri S. Episodic dural stimulation in awake rats: a model for recurrent headache. Headache 2007, 47:1026-1036.
33. Rao K.N., Brown M.A. Mast cells: multifaceted immune cells with diverse roles in health and disease. Ann. N.Y. Acad. Sci. 2008, 1143:83-104.
34. Sorkin L.S., Xiao W.H., Wagner R., Myers R.R. Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience 1997, 81:255-262.
35. Strassman A.M., Mineta Y., Vos B.P. Distribution of fos-like immunoreactivity in the medullary and upper cervical dorsal horn produced by stimulation of dural blood vessels in the rat. J. Neurosci. 1994, 14:3725-3735.
36. Strassman A.M., Vos B.P. Somatotopic and laminar organization of fos-like immunoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation in the rat. J. Comp. Neurol. 1993, 331:495-516.
37. Taiwo Y.O., Levine J.D. Serotonin is a directly-acting hyperalgesic agent in the rat. Neuroscience 1992, 48:485-490.
38. Theoharides T.C., Sant G.R., el-Mansoury M., Letourneau R., Ucci A.A., Meares E.M. Activation of bladder mast cells in interstitial cystitis: a light and electron microscopic study. J. Urol. 1995, 153:629-636.
39. Verne G.N., Robinson M.E., Price D.D. Hypersensitivity to visceral and cutaneous pain in the irritable bowel syndrome. Pain 2001, 93:7-14.
40. Vos B.P., Strassman A.M., Maciewicz R.J. Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J. Neurosci. 1994, 14:2708-2723.
41. Wood J.D. Visceral Pain: Spinal Afferents, Enteric Mast Cells, Enteric Nervous System and Stress. Curr. Pharm. Des. 2011, 17:1573-1575.
42. Zhang X., Strassman A.M., Burstein R., Levy D. Sensitization and activation of intracranial meningeal nociceptors by mast cell mediators. J. Pharmacol. Exp. Ther. 2007, 322:806-812.
43. Zhang X.C., Kainz V., Burstein R., Levy D. Tumor necrosis factor-alpha induces sensitization of meningeal nociceptors mediated via local COX and p38 MAP kinase actions. Pain 2010, 152:140-149.
44. Zhang X.C., Levy D. Modulation of meningeal nociceptors mechanosensitivity by peripheral proteinase-activated receptor-2: the role of mast cells. Cephalalgia 2008, 28:276-284.
45. Zhou Q., Price D.D., Caudle R.M., Verne G.N. Visceral and somatic hypersensitivity in a subset of rats following TNBS-induced colitis. Pain 2008, 134:9-15.