Activation of p38 mitogen-activated protein kinase in spinal microglia contributes to incision-induced mechanical allodynia

Anesthesiology

Volumn 110, Issue 1, 2009, Pages 155-165

  Wen, Yeong Ray ^a,b,c   Suter, Marc R ^d   Ji, Ru Rong ^d   Yeh, Geng Chang ^e   Wu, Yen Sheng ^c   Wang, Kuo Ching ^f   Kohno, Tatsuro ^g   Sun, Wei Zen ^h   Wang, Chia Chuan ^h  

^a Graduate Institute of Basic Medical Science   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c SHIN KONG WU HO SU MEMORIAL HOSPITAL   (Taiwan)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^f NIIGATA UNIVERSITY   (Japan)

^g NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^h FU JEN CATHOLIC UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

1 [7 (4 FLUOROPHENYL) 1,2,3,4 TETRAHYDRO 8 (4 PYRIDYL)PYRAZOLO[5,1 C][1,2,4]TRIAZIN 2 YL] 2 PHENYLETHANEDIONE; MITOGEN ACTIVATED PROTEIN KINASE P38; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HYPERALGESIA; INCISION; INFLAMMATION; MALE; MICROGLIA; NEUROPATHIC PAIN; NONHUMAN; POSTOPERATIVE PAIN; PRIORITY JOURNAL; RAT; SPINAL CORD DORSAL HORN; ANIMAL; COMPARATIVE STUDY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; INSTRUMENTATION; METABOLISM; METHODOLOGY; PAIN; PAIN ASSESSMENT; PHYSIOLOGY; SPINAL CORD; SPRAGUE DAWLEY RAT; STIMULATION;

ANIMALS; ENZYME ACTIVATION; MALE; MICROGLIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PAIN; PAIN MEASUREMENT; PHYSICAL STIMULATION; PYRAZOLES; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 58749098812     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e318190bc16     Document Type: Article

References (57)

1. Brennan TJ, Vandermeulen EP, Gebhart GF: Characterization of a rat model of incisional pain. Pain 1996; 64:493-501
2. Kawamata M, Takahashi T, Kozuka Y, Nawa Y, Nishikawa K, Narimatsu E, Watanabe H, Namiki A: Experimental incision-induced pain in human skin: effects of systemic lidocaine on flare formation and hyperalgesia. Pain 2002; 100:77-89
3. Honore P, Wade CL, Zhong C, Harris RR, Wu C, Ghayur T, Iwakura Y, Decker MW, Faltynek C, Sullivan J, Jarvis MF: Interleukin-1alphabeta gene-deficient mice show reduced nociceptive sensitivity in models of inflammatory and neuropathic pain but not post-operative pain. Behav Brain Res 2006; 167:355-64
4. Zahn PK, Umali E, Brennan TJ: Intrathecal non-NMDA excitatory amino acid receptor antagonists inhibit pain behaviors in a rat model of postoperative pain. Pain 1998; 74:213-23
5. Zahn PK, Brennan TJ: Lack of effect of intrathecally administered N-methyl- D-aspartate receptor antagonists in a rat model for postoperative pain. ANESTHESIOLOGY 1998; 88:143-56
6. Yamamoto T, Sakashita Y: The role of the spinal opioid receptor like1 receptor, the NK-1 receptor, and cyclooxygenase-2 in maintaining postoperative pain in the rat. Anesth Analg 1999; 89:1203-8
7. Zhu CZ, Hsieh G, Ei-Kouhen O, Wilson SG, Mikusa JP, Hollingsworth PR, Chang R, Moreland RB, Brioni J, Decker MW, Honore P: Role of central and peripheral mGluR5 receptors in post-operative pain in rats. Pain 2005; 114:195- 202
8. Zahn PK, Pogatzki-Zahn EM, Brennan TJ: Spinal administration of MK-801 and NBQX demonstrates NMDA-independent dorsal horn sensitization in incisional pain. Pain 2005; 114:499-510
9. Yamamoto T, Shimoyama N, Mizuguchi T: The effects of morphine, MK- 801, an NMDA antagonist, and CP-96,345, an NK1 antagonist, on the hyperesthesia evoked by carageenan injection in the rat paw. ANESTHESIOLOGY 1993; 78:124-33
10. Widmann C, Gibson S, Jarpe MB, Johnson GL: Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 1999; 79:143-80
11. Ji RR, Strichartz G: Cell signaling and the genesis of neuropathic pain. Sci STKE 2004; 2004:reE14
12. Ji RR, Kawasaki Y, Zhuang ZY, Wen YR, Zhang YQ: Protein kinases as potential targets for the treatment of pathological pain. Handb Exp Pharmacol 2007:359-89
13. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ: p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 2002; 36:57-68
14. Kim SY, Bae JC, Kim JY, Lee HL, Lee KM, Kim DS, Cho HJ: Activation of p38 MAP kinase in the rat dorsal root ganglia and spinal cord following peripheral inflammation and nerve injury. Neuroreport 2002; 13:2483-6
15. Svensson CI, Marsala M, Westerlund A, Calcutt NA, Campana WM, Freshwater JD, Catalano R, Feng Y, Protter AA, Scott B, Yaksh TL: Activation of p38 mitogenactivated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J Neurochem 2003; 86:1534-44
16. Hua XY, Svensson CI, Matsui T, Fitzsimmons B, Yaksh TL, Webb M: Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur J Neurosci 2005; 22:2431-40
17. Jin SX, Zhuang ZY, Woolf CJ, Ji RR: p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci 2003; 23:4017-22
18. Obata K, Yamanaka H, Kobayashi K, Dai Y, Mizushima T, Katsura H, Fukuoka T, Tokunaga A, Noguchi K: Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation. J Neurosci 2004; 24:10211-22
19. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K: Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 2004; 45:89-95
20. Tsuda M, Inoue K, Salter MW: Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci 2005; 28:101-7
21. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL: Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Meth 1994; 53:55-63
22. Dixon WJ: Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 1980; 20:441-62
23. Gorog P, Kovacs IB: Effect of dimethyl sulfoxide (DMSO) on various experimental inflammations. Curr Ther Res Clin Exp 1968; 10:486-92
24. Evans MS, Reid KH, Sharp JB: Dimethylsulfoxide (DMSO) blocks conduction in peripheral nerve C fibers: a possible mechanism of analgesia. Neurosci Lett 1993;150: 145-8
25. Lin CS, Tsaur ML, Chen CC, Wang TY, Lin CF, Lai YL, Hsu TC, Pan YY, Yang CH, Cheng JK: Chronic intrathecal infusion of minocycline prevents the development of spinal-nerve ligation-induced pain in rats. Reg Anesth Pain Med 2007; 32:209-16
26. Boyle DL, Jones TL, Hammaker D, Svensson CI, Rosengren S, Albani S, Sorkin L, Firestein GS: Regulation of peripheral inflammation by spinal p38 MAP kinase in rats. PLoS Med 2006; 3:e338
27. Kobayashi M, Takeyoshi I, Yoshinari D, Matsumoto K, Morishita Y: P38 mitogen-activated protein kinase inhibition attenuates ischemia-reperfusion injury of the rat liver. Surgery 2002; 131:344-9
28. Furuichi K, Wada T, Iwata Y, Sakai N, Yoshimoto K, Kobayashi KK, Mukaida N, Matsushima K, Yokoyama H: Administration of FR167653, a new anti-inflammatory compound, prevents renal ischaemia/reperfusion injury in mice. Nephrol Dial Transplant 2002; 17:399-407
29. Kawashima Y, Takeyoshi I, Otani Y, Koibuchi Y, Yoshinari D, Koyama T, Kobayashi M, Matsumoto K, Morishita Y: FR167653 attenuates ischemia and reperfusion injury of the rat lung with suppressing p38 mitogen-activated protein kinase. J Heart Lung Transplant 2001; 20:568-74
30. Daulhac L, Mallet C, Courteix C, Etienne M, Duroux E, Privat AM, Eschalier A, Fialip J: Diabetes-induced mechanical hyperalgesia involves spinal mitogenactivated protein kinase activation in neurons and microglia via N-methyl-Daspartate- dependent mechanisms. Mol Pharmacol 2006; 70:1246-54
31. Sweitzer SM, Peters MC, Ma JY, Kerr I, Mangadu R, Chakravarty S, Dugar S, Medicherla S, Protter AA, Yeomans DC: Peripheral and central p38 MAPK mediates capsaicin-induced hyperalgesia. Pain 2004; 111:278-85
32. Cui XY, Dai Y, Wang SL, Yamanaka H, Kobayashi K, Obata K, Chen J, Noguchi K: Differential activation of p38 and extracellular signal-regulated kinase in spinal cord in a model of bee venom-induced inflammation and hyperalgesia. Mol Pain 2008; 4:17
33. Xu M, Bruchas MR, Ippolito DL, Gendron L, Chavkin C: Sciatic nerve ligation-induced proliferation of spinal cord astrocytes is mediated by kappa opioid activation of p38 mitogen-activated protein kinase. J Neurosci 2007; 27:2570-81
34. Zhuang ZY, Gerner P, Woolf CJ, Ji RR: ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 2005; 114:149-59
35. Ma W, Quirion R: Partial sciatic nerve ligation induces increase in the phosphorylation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) in astrocytes in the lumbar spinal dorsal horn and the gracile nucleus. Pain 2002; 99:175-84
36. Mogensen T, Eliasen K, Ejlersen E, Vegger P, Nielsen IK, Kehlet H: Epidural clonidine enhances postoperative analgesia from a combined low-dose epidural bupivacaine and morphine regimen. Anesth Analg 1992; 75:607-10
37. Wen YR, Suter MR, Kawasaki Y, Huang J, Pertin M, Kohno T, Berde CB, Decosterd I, Ji RR: Nerve conduction blockade in the sciatic nerve prevents but does not reverse the activation of p38 mitogen-activated protein kinase in spinal microglia in the rat spared nerve injury model. ANESTHESIOLOGY 2007; 107:312-21
38. Milligan ED, Twining C, Chacur M, Biedenkapp J, O'Connor K, Poole S, Tracey K, Martin D, Maier SF, Watkins LR: Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J Neurosci 2003; 23: 1026-40
39. Yamamoto N, Sakai F, Yamazaki H, Nakahara K, Okuhara M: Effect of FR167653, a cytokine suppressive agent, on endotoxin-induced disseminated intravascular coagulation. Eur J Pharmacol 1996; 314:137-42
40. Yamamoto N, Sakai F, Yamazaki H, Sato N, Nakahara K, Okuhara M: FR167653, a dual inhibitor of interleukin-1 and tumor necrosis factor-alpha, ameliorates endotoxin-induced shock. Eur J Pharmacol 1997; 327:169-74
41. Scholz J, Woolf CJ: The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 2007; 10:1361-8
42. Koistinaho M, Koistinaho J: Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 2002; 40:175-83
43. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D: The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997; 389:816-24
44. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D: Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000; 288:306-13
45. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA: Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 2000; 405:183-7
46. Pogatzki-Zahn EM, Shimizu I, Caterina M, Raja SN: Heat hyperalgesia after incision requires TRPV1 and is distinct from pure inflammatory pain. Pain 2005; 115:296-307
47. Mizushima T, Obata K, Yamanaka H, Dai Y, Fukuoka T, Tokunaga A, Mashimo T, Noguchi K: Activation of p38 MAPK in primary afferent neurons by noxious stimulation and its involvement in the development of thermal hyperalgesia. Pain 2005; 113:51-60
48. Michael GJ, Averill S, Nitkunan A, Rattray M, Bennett DL, Yan Q, Priestley JV: Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J Neurosci 1997; 17:8476-90
49. Porreca F, Lai J, Bian D, Wegert S, Ossipov MH, Eglen RM, Kassotakis L, Novakovic S, Rabert DK, Sangameswaran L, Hunter JC: A comparison of the potential role of the tetrodotoxin-insensitive sodium channels, PN3/SNS and NaN/SNS2, in rat models of chronic pain. Proc Natl Acad Sci U S A 1999; 96:7640-4
50. Obata H, Eisenach JC, Hussain H, Bynum T, Vincler M: Spinal glial activation contributes to postoperative mechanical hypersensitivity in the rat. J Pain 2006; 7:816-22
51. Colburn RW, DeLeo JA, Rickman AJ, Yeager MP, Kwon P, Hickey WF: Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat. J Neuroimmunol 1997; 79:163-75
52. Suter MR, Wen YR, Decosterd I, Ji RR: Do glial cells control pain? Neuron Glia Biol 2007; 3:255-68
53. Echeverry S, Shi XQ, Zhang J: Characterization of cell proliferation in rat spinal cord following peripheral nerve injury and the relationship with neuropathic pain. Pain 2008; 135:37-47
54. Svensson CI, Fitzsimmons B, Azizi S, Powell HC, Hua XY, Yaksh TL: Spinal p38beta isoform mediates tissue injury-induced hyperalgesia and spinal sensitization. J Neurochem 2005; 92:1508-20
55. Crown ED, Ye Z, Johnson KM, Xu GY, McAdoo DJ, Hulsebosch CE: Increases in the activated forms of ERK 1/2, p38 MAPK, and CREB are correlated with the expression of at-level mechanical allodynia following spinal cord injury. Exp Neurol 2006; 199:397-407
56. Winkelstein BA, DeLeo JA: Nerve root injury severity differentially modulates spinal glial activation in a rat lumbar radiculopathy model: considerations for persistent pain. Brain Res 2002; 956:294-301
57. Romero-Sandoval A, Eisenach JC: Spinal cannabinoid receptor type 2 activation reduces hypersensitivity and spinal cord glial activation after paw incision. ANESTHESIOLOGY 2007; 106:787-94