Sensitization of dural afferents underlies migraine-related behavior following meningeal application of interleukin-6 (IL-6)

Molecular Pain

Volumn 8, Issue , 2012, Pages

  Yan, Jin ^a   Melemedjian, Ohannes K ^a   Price, Theodore J ^a,b   Dussor, Gregory ^a,b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Dural afferents; Headache; Interleukin 6; Meninges; Migraine; Nav1.7; Pain

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; SODIUM CHANNEL NAV1.7; 1,3 BUTADIENE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NITRILE; SCN9A PROTEIN, RAT; SODIUM CHANNEL;

ACTION POTENTIAL; ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CENTRAL NERVOUS SYSTEM SENSITIZATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FACE PAIN; IN VIVO STUDY; MALE; MENINX; MIGRAINE; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SENSORY NERVE CONDUCTION; TRIGEMINAL NERVE; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECT; DURA MATER; ELECTROSTIMULATION; ENZYMOLOGY; HYPERALGESIA; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN BINDING; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; BUTADIENES; DURA MATER; ELECTRIC STIMULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HYPERALGESIA; INTERLEUKIN-6; MALE; MAP KINASE SIGNALING SYSTEM; MENINGES; MIGRAINE DISORDERS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEURONS, AFFERENT; NITRILES; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNELS;

EID: 84856070350     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-8-6     Document Type: Article

References (41)

1. Goadsby PJ, Lipton RB, Ferrari MD. Migraine-current understanding and treatment. N Engl J Med 2002, 346:257-270. 10.1056/NEJMra010917, 11807151.
2. Waeber C, Moskowitz MA. Migraine as an inflammatory disorder. Neurology 2005, 64:S9-S15.
3. Sarchielli P, Alberti A, Baldi A, Coppola F, Rossi C, Pierguidi L, Floridi A, Calabresi P. Proinflammatory cytokines, adhesion molecules, and lymphocyte integrin expression in the internal jugular blood of migraine patients without aura assessed ictally. Headache 2006, 46:200-207. 10.1111/j.1526-4610.2006.00337.x, 16492228.
4. Fidan I, Yuksel S, Ymir T, Irkec C, Aksakal FN. The importance of cytokines, chemokines and nitric oxide in pathophysiology of migraine. J Neuroimmunol 2006, 171:184-188. 10.1016/j.jneuroim.2005.10.005, 16325275.
5. Clark JD, Shi X, Li X, Qiao Y, Liang D, Angst MS, Yeomans DC. Morphine reduces local cytokine expression and neutrophil infiltration after incision. Mol Pain 2007, 3:28. 10.1186/1744-8069-3-28, 2096620, 17908329.
6. De Jongh RF, Vissers KC, Meert TF, Booij LH, De Deyne CS, Heylen RJ. The role of interleukin-6 in nociception and pain. Anesth Analg 2003, 96:1096-1103. table of contents.
7. Vardanyan M, Melemedjian OK, Price TJ, Ossipov MH, Lai J, Roberts E, Boos TL, Deschamps JR, Jacobson AE, Rice KC, Porreca F. Reversal of pancreatitis-induced pain by an orally available, small molecule interleukin-6 receptor antagonist. Pain 2010, 151:257-265. 10.1016/j.pain.2010.05.022, 20599324.
8. Xu XJ, Hao JX, Andell-Jonsson S, Poli V, Bartfai T, Wiesenfeld-Hallin Z. Nociceptive responses in interleukin-6-deficient mice to peripheral inflammation and peripheral nerve section. Cytokine 1997, 9:1028-1033. 10.1006/cyto.1997.0243, 9417815.
9. Summer GJ, Romero-Sandoval EA, Bogen O, Dina OA, Khasar SG, Levine JD. Proinflammatory cytokines mediating burn-injury pain. Pain 2008, 135:98-107. 10.1016/j.pain.2007.05.012, 17590515.
10. Kurek JB, Austin L, Cheema SS, Bartlett PF, Murphy M. Up-regulation of leukaemia inhibitory factor and interleukin-6 in transected sciatic nerve and muscle following denervation. Neuromuscul Disord 1996, 6:105-114. 10.1016/0960-8966(95)00029-1, 8664561.
11. Bao L, Zhu Y, Elhassan AM, Wu Q, Xiao B, Zhu J, Lindgren JU. Adjuvant-induced arthritis: IL-1 beta, IL-6 and TNF-alpha are up-regulated in the spinal cord. Neuroreport 2001, 12:3905-3908. 10.1097/00001756-200112210-00010, 11742208.
12. Arruda JL, Colburn RW, Rickman AJ, Rutkowski MD, DeLeo JA. Increase of interleukin-6 mRNA in the spinal cord following peripheral nerve injury in the rat: potential role of IL-6 in neuropathic pain. Brain Res Mol Brain Res 1998, 62:228-235.
13. Andratsch M, Mair N, Constantin CE, Scherbakov N, Benetti C, Quarta S, Vogl C, Sailer CA, Uceyler N, Brockhaus J, et al. A key role for gp130 expressed on peripheral sensory nerves in pathological pain. J Neurosci 2009, 29:13473-13483. 10.1523/JNEUROSCI.1822-09.2009, 19864560.
14. Nishimoto N, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T, Azuma J. Long-term safety and efficacy of tocilizumab, an anti-IL-6 receptor monoclonal antibody, in monotherapy, in patients with rheumatoid arthritis (the STREAM study): evidence of safety and efficacy in a 5-year extension study. Ann Rheum Dis 2009, 68:1580-1584. 10.1136/ard.2008.092866, 2732899, 19019888.
15. Melemedjian OK, Asiedu MN, Tillu DV, Peebles KA, Yan J, Ertz N, Dussor GO, Price TJ. IL-6- and NGF-induced rapid control of protein synthesis and nociceptive plasticity via convergent signaling to the eIF4F complex. J Neurosci 2010, 30:15113-15123. 10.1523/JNEUROSCI.3947-10.2010, 3056511, 21068317.
16. Ji RR, Gereau R, Malcangio M, Strichartz GR. MAP kinase and pain. Brain Res Rev 2009, 60:135-148. 10.1016/j.brainresrev.2008.12.011, 2666786, 19150373.
17. Karim F, Wang CC, Gereau R. Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 2001, 21:3771-3779.
18. Rush AM, Cummins TR, Waxman SG. Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J Physiol 2007, 579:1-14. 10.1113/jphysiol.2006.121483, 2075388, 17158175.
19. Stamboulian S, Choi JS, Ahn HS, Chang YW, Tyrrell L, Black JA, Waxman SG, Dib-Hajj SD. ERK1/2 mitogen-activated protein kinase phosphorylates sodium channel Na(v)1.7 and alters its gating properties. J Neurosci 2010, 30:1637-1647. 10.1523/JNEUROSCI.4872-09.2010, 20130174.
20. Wei X, Edelmayer RM, Yan J, Dussor G. Activation of TRPV4 on dural afferents produces headache-related behavior in a preclinical rat model. Cephalalgia 2011, 31:1595-1600. 10.1177/0333102411427600, 22049072.
21. Yan J, Edelmayer RM, Wei X, De Felice M, Porreca F, Dussor G. Dural afferents express acid-sensing ion channels: a role for decreased meningeal pH in migraine headache. Pain 2011, 152:106-113. 10.1016/j.pain.2010.09.036, 3005011, 20971560.
22. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63. 10.1016/0165-0270(94)90144-9, 7990513.
23. Edelmayer RM, Vanderah TW, Majuta L, Zhang ET, Fioravanti B, De Felice M, Chichorro JG, Ossipov MH, King T, Lai J, et al. Medullary pain facilitating neurons mediate allodynia in headache-related pain. Ann Neurol 2009, 65:184-193. 10.1002/ana.21537, 2772103, 19259966.
24. Burstein R, Cutrer MF, Yarnitsky D. The development of cutaneous allodynia during a migraine attack clinical evidence for the sequential recruitment of spinal and supraspinal nociceptive neurons in migraine. Brain 2000, 123(Pt 8):1703-1709.
25. Bigal ME, Ashina S, Burstein R, Reed ML, Buse D, Serrano D, Lipton RB. Prevalence and characteristics of allodynia in headache sufferers: a population study. Neurology 2008, 70:1525-1533. 10.1212/01.wnl.0000310645.31020.b1, 2664547, 18427069.
26. Cummins TR, Howe JR, Waxman SG. Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/PN1 sodium channel. J Neurosci 1998, 18:9607-9619.
27. Rush AM, Dib-Hajj SD, Liu S, Cummins TR, Black JA, Waxman SG. A single sodium channel mutation produces hyper- or hypoexcitability in different types of neurons. Proc Natl Acad Sci USA 2006, 103:8245-8250. 10.1073/pnas.0602813103, 1472458, 16702558.
28. Choi JS, Waxman SG. Physiological interactions between Nav1.7 and Nav1.8 sodium channels: a computer simulation study. J Neurophysiol 2011, 106:3173-3184. 10.1152/jn.00100.2011, 21940606.
29. Levy D. Migraine pain, meningeal inflammation, and mast cells. Curr Pain Headache Rep 2009, 13:237-240. 10.1007/s11916-009-0040-y, 19457286.
30. Reuter U, Bolay H, Jansen-Olesen I, Chiarugi A, Sanchez del Rio M, Letourneau R, Theoharides TC, Waeber C, Moskowitz MA. Delayed inflammation in rat meninges: implications for migraine pathophysiology. Brain 2001, 124:2490-2502. 10.1093/brain/124.12.2490, 11701602.
31. Dimlich RV, Keller JT, Strauss TA, Fritts MJ. Linear arrays of homogeneous mast cells in the dura mater of the rat. J Neurocytol 1991, 20:485-503. 10.1007/BF01252276, 1869885.
32. Rozniecki JJ, Dimitriadou V, Lambracht-Hall M, Pang X, Theoharides TC. Morphological and functional demonstration of rat dura mater mast cell-neuron interactions in vitro and in vivo. Brain Res 1999, 849:1-15. 10.1016/S0006-8993(99)01855-7, 10592282.
33. Strassman AM, Weissner W, Williams M, Ali S, Levy D. Axon diameters and intradural trajectories of the dural innervation in the rat. J Comp Neurol 2004, 473:364-376. 10.1002/cne.20106, 15116396.
34. Kruger-Krasagakes S, Moller A, Kolde G, Lippert U, Weber M, Henz BM. Production of interleukin-6 by human mast cells and basophilic cells. J Invest Dermatol 1996, 106:75-79. 10.1111/1523-1747.ep12327815, 8592085.
35. Grabbe J, Welker P, Moller A, Dippel E, Ashman LK, Czarnetzki BM. Comparative cytokine release from human monocytes, monocyte-derived immature mast cells, and a human mast cell line (HMC-1). J Invest Dermatol 1994, 103:504-508. 10.1111/1523-1747.ep12395649, 7523530.
36. Obreja O, Biasio W, Andratsch M, Lips KS, Rathee PK, Ludwig A, Rose-John S, Kress M. Fast modulation of heat-activated ionic current by proinflammatory interleukin 6 in rat sensory neurons. Brain 2005, 128:1634-1641. 10.1093/brain/awh490, 15817518.
37. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG. From genes to pain: Na v 1.7 and human pain disorders. Trends Neurosci 2007, 30:555-563. 10.1016/j.tins.2007.08.004, 17950472.
38. Schmalhofer WA, Calhoun J, Burrows R, Bailey T, Kohler MG, Weinglass AB, Kaczorowski GJ, Garcia ML, Koltzenburg M, Priest BT. ProTx-II, a selective inhibitor of NaV1.7 sodium channels, blocks action potential propagation in nociceptors. Mol Pharmacol 2008, 74:1476-1484. 10.1124/mol.108.047670, 18728100.
39. Estacion M, Waxman SG, Dib-Hajj SD. Effects of ranolazine on wild-type and mutant hNav1.7 channels and on DRG neuron excitability. Mol Pain 2010, 6:35. 10.1186/1744-8069-6-35, 2898769, 20529343.
40. Nassar MA, Stirling LC, Forlani G, Baker MD, Matthews EA, Dickenson AH, Wood JN. Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci USA 2004, 101:12706-12711. 10.1073/pnas.0404915101, 515119, 15314237.
41. Black JA, Liu S, Tanaka M, Cummins TR, Waxman SG. Changes in the expression of tetrodotoxin-sensitive sodium channels within dorsal root ganglia neurons in inflammatory pain. Pain 2004, 108:237-247. 10.1016/j.pain.2003.12.035, 15030943.