p38 activation in uninjured primary afferent neurons and in spinal microglia contributes to the development of neuropathic pain induced by selective motor fiber injury

Experimental Neurology

Volumn 204, Issue 1, 2007, Pages 355-365

  Xu, Ji Tian ^a,b   Xin, Wen Jun ^a   Wei, Xu Hong ^a   Wu, Chang You ^a   Ge, Yu Xing ^a   Liu, Yan Ling ^a   Zang, Ying ^a   Zhang, Tong ^a   Li, Yong Yong ^a   Liu, Xian Guo ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b ZHENGZHOU UNIVERSITY   (China)

Author keywords

Dorsal root ganglion; Immunohistochemistry; Neuropathic pain; p38 MAPK; Spinal cord; Ventral root transection

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ISOLECTIN B4; LECTIN; MITOGEN ACTIVATED PROTEIN KINASE P38; THALIDOMIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; BRAIN NERVE CELL; ENZYME ACTIVATION; IMMUNOREACTIVITY; LUMBAR SPINE; MALE; MICROGLIA; MOTOR NERVE; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE; SENSORY NERVE CELL; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD TRANSSECTION; SPINAL GANGLION; VENTRAL ROOT;

ANIMALS; DENERVATION; ENZYME ACTIVATION; ENZYME INHIBITORS; GANGLIA, SPINAL; HYPERALGESIA; HYPESTHESIA; IMIDAZOLES; IMMUNOHISTOCHEMISTRY; LUMBOSACRAL REGION; MALE; MICROGLIA; MOTOR NEURONS; NERVE FIBERS; NEURALGIA; NEURONS, AFFERENT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL NERVE ROOTS; THALIDOMIDE; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33847325194     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2006.11.016     Document Type: Article

References (48)

1. Blumberg H., and Janig W. Discharge pattern of afferent fibers from a neuroma. Pain 20 (1984) 335-353
2. Boucher T.J., Okuse K., Bennett D.L., Munson J.B., Wood J.N., and McMahon S.B. Potent analgesic effects of GDNF in neuropathic pain states. Science 290 (2000) 124-127
3. Chacur M., Milligan E.D., Gazda L.S., Armstrong C., Wang H., Tracey K.J., Maier S.F., and Watkins LR. A new model of sciatic inflammatory neuritis (SIN): induction of unilateral and bilateral mechanical allodynia following acute unilateral peri-sciatic immune activation in rats. Pain 94 (2001) 231-244
4. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53 (1994) 55-63
5. Coggeshall R.E., Emery D.G., Ito H., and Maynard C.W. Unmyelinated and small myelinated axons in rat ventral roots. J. Comp. Neurol. 173 (1977) 175-184
6. Cunha F.Q., Poole S., Lorenzetti B.B., and Ferreira S.H. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br. J. Pharmacol. 107 (1992) 660-664
7. Cunha T.M., Verri Jr. W.A., Silva J.S., Poole S., Cunha F.Q., and Ferreira S.H. A cascade of cytokines mediates mechanical inflammatory hypernociception in mice. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 1755-1760
8. Djouhri L., Koutsikou S., Fang X., McMullan S., and Lawson S.N. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J. Neurosci. 26 (2006) 1281-1292
9. George A., Marziniak M., Schafers M., Toyka K.V., and Sommer C. Thalidomide treatment in chronic constrictive neuropathy decreases endoneurial tumor necrosis factor-alpha, increases interleukin-10 and has long-term effects on spinal cord dorsal horn met-enkephalin. Pain 88 (2000) 267-275
10. George A., Buehl A., and Sommer C. Wallerian degeneration after crush injury of rat sciatic nerve increases endo- and epineurial tumor necrosis factor-alpha protein. Neurosci. Lett. 372 (2004) 215-219
11. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
12. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
13. Jin S.X., Zhuang Z.Y., Woolf C.J., and 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. 23 (2003) 4017-4022
14. Koistinaho M., and Koistinaho J. Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 40 (2002) 175-183
15. Koschorke G.M., Meyer R.A., Tillman D.B., and Campbell J.N. Ectopic excitability of injured nerves in monkey: entrained responses to vibratory stimuli. J. Neurophysiol. 65 (1991) 693-701
16. Li Y., Dorsi M.J., Meyer R.A., and Belzberg A.J. Mechanical hyperalgesia after an L5 spinal nerve lesion in the rat is not dependent on input from injured nerve fibers. Pain 85 (2000) 493-502
17. Li L., Xian C.J., Zhong J.H., and Zhou X.F. Effect of lumbar 5 ventral root transection on pain behaviors: a novel rat model for neuropathic pain without axotomy of primary sensory neurons. Exp. Neurol. 175 (2002) 23-34
18. Liefner M., Siebert H., Sachse T., Michel U., Kollias G., and Bruck W. The role of TNF-alpha during Wallerian degeneration. J. Neuroimmunol. 108 (2000) 147-152
19. Liu T., van Rooijen N., and Tracey D.J. Depletion of macrophages reduces axonal degeneration and hyperalgesia following nerve injury. Pain 86 (2000) 25-32
20. Meyer R.A., Raja S.N., Campbell J.N., Mackinnon S.E., and Dellon A.L. Neural activity originating from a neuroma in the baboon. Brain Res. 325 (1985) 255-260
21. Michaelis M., Liu X., and Janig W. Axotomized and intact muscle afferents but no skin afferents develop ongoing discharges of dorsal root ganglion origin after peripheral nerve lesion. J. Neurosci. 20 (2000) 2742-2748
22. Milligan E.D., Twining C., Chacur M., Biedenkapp J., O'Connor K., Poole S., Tracey K., Martin D., Maier S.F., and Watkins L.R. Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J. Neurosci. 23 (2003) 1026-1040
23. Mizushima T., Obata K., Yamanaka H., Dai Y., Fukuoka T., Tokunaga A., Mashimo T., and Noguchi K. Activation of p38 MAPK in primary afferent neurons by noxious stimulation and its involvement in the development of thermal hyperalgesia. Pain 113 (2005) 51-60
24. Myers R.R., Campana W.M., and Shubayev V.I. The role of neuroinflammation in neuropathic pain: mechanisms and therapeutic targets. Drug Discov. Today 11 (2006) 8-20
25. Nam S.C., Kim K.J., Leem J.W., Chung K.S., and Chung J.M. Fiber counts at multiple sites along the rat ventral root after neonatal peripheral neurectomy or dorsal rhizotomy. J. Comp. Neurol. 290 (1989) 336-342
26. Obata K., Yamanaka H., Dai Y., Mizushima T., Fukuoka T., Tokunaga A., Yoshikawa H., and Noguchi K. Contribution of degeneration of motor and sensory fibers to pain behavior and the changes in neurotrophic factors in rat dorsal root ganglion. Exp. Neurol. 188 (2004) 149-160
27. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., Fukuoka T., Tokunaga A., and 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. 24 (2004) 10211-10222
28. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., Fukuoka T., Tokunaga A., and Noguchi K. The effect of site and type of nerve injury on the expression of brain-derived neurotrophic factor in the dorsal root ganglion and on neuropathic pain behavior. Neuroscience 137 (2006) 961-970
29. Pollock J., McFarlane S.M., Connell M.C., Zehavi U., Vandenabeele P., MacEwan D.J., and Scott R.H. TNF-alpha receptors simultaneously activate Ca2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology 42 (2002) 93-106
30. Proske U., Iggo A., and Luff A.R. Mechanical sensitivity of regenerating myelinated skin and muscle afferents in the cat. Exp. Brain Res. 104 (1995) 89-98
31. Schafers M., Geis C., Svensson C.I., Luo Z.D., and Sommer C. Selective increase of tumor necrosis factor-alpha in injured and spared myelinated primary afferents after chronic constrictive injury of rat sciatic nerve. Eur. J. Neurosci. 17 (2003) 791-804
32. Schafers M., Svensson C.I., Sommer C., and Sorkin L.S. Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J. Neurosci. 23 (2003) 2517-2521
33. Shamash S., Reichert F., and Rotshenker S. The cytokine network of Wallerian degeneration: tumor necrosis factor-alpha, interleukin-1alpha, and interleukin-1beta. J. Neurosci. 22 (2002) 3052-3060
34. Sheth RN., Dorsi M.J., Li Y., Murinson B.B., Belzberg A.J., Griffin J.W., and Meyer R.A. Mechanical hyperalgesia after an L5 ventral rhizotomy or an L5 ganglionectomy in the rat. Pain 96 (2002) 63-72
35. Spataro L.E., Sloane E.M., Milligan E.D., Wieseler-Frank J., Schoeniger D., Jekich B.M., Barrientos R.M., Maier S.F., and Watkins L.R. Spinal gap junctions: potential involvement in pain facilitation. J. Pain 5 (2004) 392-405
36. Tsuda M., Mizokoshi A., Shigemoto-Mogami Y., Koizumi S., and Inoue K. Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 45 (2004) 89-95
37. Twining C.M., Sloane E.M., Milligan E.D., Chacur M., Martin D., Poole S., Marsh H., Maier S.F., and Watkins L.R. Peri-sciatic proinflammatory cytokines, reactive oxygen species, and complement induce mirror-image neuropathic pain in rats. Pain 110 (2004) 299-309
38. Wall P.D., Waxman S., and Basbaum A.I. Ongoing activity in peripheral nerve: injury discharge. Exp. Neurol. 45 (1974) 576-589
39. Watkins L.R., and Maier SF. Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiol. Rev. 82 (2002) 981-1011
40. Woolf C.J., Shortland P., and Coggeshall R.E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355 (1992) 75-78
41. Woolf C.J., Allchorne A., Safieh-Garabedian B., and Poole S. Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor alpha. Br. J. Pharmacol. 121 (1997) 417-424
42. Wu G., Ringkamp M., Hartke T.V., Murinson B.B., Campbell J.N., Griffin J.W., and Meyer R.A. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J. Neurosci. 21 (2001) RC140
43. Wu G., Ringkamp M., Murinson B.B., Pogatzki E.M., Hartke T.V., Weerahandi H.M., Campbell J.N., Griffin J.W., and Meyer R.A. Degeneration of myelinated efferent fibers induces spontaneous activity in uninjured C-fiber afferents. J. Neurosci. 22 (2002) 7746-7753
44. Xu J.T., Xin W.J., Zang Y., Wu C.Y., and Liu X.G. The role of tumor necrosis factor-alpha in the neuropathic pain induced by Lumbar 5 ventral root transection in rat. Pain 123 (2006) 306-321
45. Zelenka M., Schafers M., and Sommer C. Intraneural injection of interleukin-1beta and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 116 (2005) 257-263
46. Zenker W., Stelzig M., Sulzgruber S.C., and Neumann A. Fiber analysis of human ventral and dorsal roots on the basis of different acetylcholinesterase activity. Acta Anat. (Basel) 103 (1979) 319-326
47. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110
48. Zimmermann M. Pathobiology of neuropathic pain. Eur. J. Pharmacol. 429 (2001) 23-37