Calpain-2 contributes to neuropathic pain following motor nerve injury via up-regulating interleukin-6 in DRG neurons

Brain, Behavior, and Immunity

Volumn 44, Issue , 2015, Pages 37-47

  Zang, Ying ^a   Chen, Shao Xia ^a   Liao, Guang Jie ^a,b   Zhu, He Quan ^a   Wei, Xu hong ^a   Cui, Yu ^a   Na, Xiao Dong ^a   Pang, Rui Ping ^a   Xin, Wen jun ^a   Zhou, Li jun ^a   Liu, Xian Guo ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b Department of Pathology The Red Cross Hospital of Yulin   (China)

Author keywords

Calpain; Dorsal root ganglia; Interleukin 6; L5 ventral root transection; Neuropathic pain

Indexed keywords

CALPAIN 1; CALPAIN 2; INTERLEUKIN 6; SPECTRIN; [1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER; CALPAIN;

ALLODYNIA; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DORSAL ROOT; DRUG HALF LIFE; ENZYME ACTIVATION; ENZYME INHIBITION; IMMUNOFLUORESCENCE; IN VITRO STUDY; MALE; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; SURFACE PROPERTY; UPREGULATION; WESTERN BLOTTING; ANIMAL; ENZYMOLOGY; HYPERALGESIA; INJURIES; METABOLISM; NERVE CELL; NEURALGIA; SPINAL GANGLION; SPINAL ROOT; SPRAGUE DAWLEY RAT;

ANIMALS; CALPAIN; GANGLIA, SPINAL; HYPERALGESIA; INTERLEUKIN-6; MALE; NEURALGIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SPECTRIN; SPINAL NERVE ROOTS; UP-REGULATION;

EID: 84918566779     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.08.003     Document Type: Article

References (75)

1. Ali Z., Ringkamp M., Hartke T.V., Chien H.F., Flavahan N.A., Campbell J.N., Meyer R.A. Uninjured C-fiber nociceptors develop spontaneous activity and alpha-adrenergic sensitivity following L6 spinal nerve ligation in monkey. J. Neurophysiol. 1999, 81:455-466.
2. Banik N.L., Matzelle D.C., Gantt-Wilford G., Osborne A., Hogan E.L. Increased calpain content and progressive degradation of neurofilament protein in spinal cord injury. Brain Res. 1997, 752:301-306.
3. Baudry M., Chou M.M., Bi X. Targeting calpain in synaptic plasticity. Expert Opin. Ther. Targets 2013, 17:579-592.
4. Bi X., Chang V., Siman R., Tocco G., Baudry M. Regional distribution and time-course of calpain activation following kainate-induced seizure activity in adult rat brain. Brain Res. 1996, 726:98-108.
5. Brana C., Benham C.D., Sundstrom L.E. Calpain activation and inhibition in organotypic rat hippocampal slice cultures deprived of oxygen and glucose. Eur. J. Neurosci. 1999, 11:2375-2384.
6. Castejon M.S., Culver D.G., Glass J.D. Generation of spectrin breakdown products in peripheral nerves by addition of M-calpain. Muscle Nerve 1999, 22:905-909.
7. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 1994, 53:55-63.
8. Chen F., Lu Y., Kuhn D.C., Maki M., Shi X., Sun S.C., Demers L.M. Calpain contributes to silica-induced I kappa B-alpha degradation and nuclear factor-kappa B activation. Arch. Biochem. Biophys. 1997, 342:383-388.
9. Chen X., Pang R.P., Shen K.F., Zimmermann M., Xin W.J., Li Y.Y., Liu X.G. TNF-alpha enhances the currents of voltage gated sodium channels in uninjured dorsal root ganglion neurons following motor nerve injury. Exp. Neurol. 2011, 227:279-286.
10. Cheng C.F., Cheng J.K., Chen C.Y., Lien C.C., Chu D., Wang S.Y., Tsaur M.L. Mirror-image pain is mediated by nerve growth factor produced from tumor necrosis factor alpha-activated satellite glia after peripheral nerve injury. Pain 2014, 155:906-920.
11. Croall D.E., Ersfeld K. The calpains: modular designs and functional diversity. Genome Biol. 2007, 8:218.
12. DeLeo J.A., Colburn R.W., Nichols M., Malhotra A. Interleukin-6-mediated hyperalgesia/allodynia and increased spinal IL-6 expression in a rat mononeuropathy model. J. Interferon Cytokine Res. 1996, 16:695-700.
13. Dieb W., Ouachikh O., Durif F., Hafidi A. Lesion of the dopaminergic nigrostriatal pathway induces trigeminal dynamic mechanical allodynia. Brain Behav. 2014, 4:368-380.
14. Dubovy P., Brazda V., Klusakova I., Hradilova-Svizenska I. Bilateral elevation of interleukin-6 protein and mRNA in both lumbar and cervical dorsal root ganglia following unilateral chronic compression injury of the sciatic nerve. J. Neuroinflammation 2013, 10:55.
15. Fenouille N., Grosso S., Yunchao S., Mary D., Pontier-Bres R., Imbert V., Czerucka D., Caroli-Bosc F.X., Peyron J.F., Lagadec P. Calpain 2-dependent IkappaBalpha degradation mediates CPT-11 secondary resistance in colorectal cancer xenografts. J. Pathol. 2012, 227:118-129.
16. Gao Y.J., Xu Z.Z., Liu Y.C., Wen Y.R., Decosterd I., Ji R.R. The c-Jun N-terminal kinase 1 (JNK1) in spinal astrocytes is required for the maintenance of bilateral mechanical allodynia under a persistent inflammatory pain condition. Pain 2010, 148:309-319.
17. Glass J.D., Culver D.G., Levey A.I., Nash N.R. Very early activation of m-calpain in peripheral nerve during Wallerian degeneration. J. Neurol. Sci. 2002, 196:9-20.
18. Gold M.S. Spinal nerve ligation: what to blame for the pain and why. Pain 2000, 84:117-120.
19. Guroff G. A neutral, calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 1964, 239:149-155.
20. Hamakubo T., Kannagi R., Murachi T., Matus A. Distribution of calpains I and II in rat brain. J. Neurosci. 1986, 6:3103-3111.
21. Hatashita S., Sekiguchi M., Kobayashi H., Konno S., Kikuchi S. Contralateral neuropathic pain and neuropathology in dorsal root ganglion and spinal cord following hemilateral nerve injury in rats. Spine (Phila Pa 1976) 2008, 33:1344-1351.
22. He X.H., Zang Y., Chen X., Pang R.P., Xu J.T., Zhou X., Wei X.H., Li Y.Y., Xin W.J., Qin Z.H., Liu X.G. TNF-alpha contributes to up-regulation of Nav1.3 and Nav1.8 in DRG neurons following motor fiber injury. Pain 2010, 151:266-279.
23. Huang D., Yu B. The mirror-image pain: an unclered phenomenon and its possible mechanism. Neurosci. Biobehav. Rev. 2010, 34:528-532.
24. Iguchi-Hashimoto M., Usui T., Yoshifuji H., Shimizu M., Kobayashi S., Ito Y., Murakami K., Shiomi A., Yukawa N., Kawabata D., Nojima T., Ohmura K., Fujii T., Mimori T. Overexpression of a minimal domain of calpastatin suppresses IL-6 production and Th17 development via reduced NF-kappaB and increased STAT5 signals. PLoS ONE 2011, 6:e27020.
25. Koltzenburg M., Wall P.D., McMahon S.B. Does the right side know what the left is doing?. Trends Neurosci. 1999, 22:122-127.
26. Konopka K.H., Harbers M., Houghton A., Kortekaas R., van Vliet A., Timmerman W., den Boer J.A., Struys M.M., van Wijhe M. Bilateral sensory abnormalities in patients with unilateral neuropathic pain; a quantitative sensory testing (QST) study. PLoS ONE 2012, 7:e37524.
27. Kunz S., Niederberger E., Ehnert C., Coste O., Pfenninger A., Kruip J., Wendrich T.M., Schmidtko A., Tegeder I., Geisslinger G. The calpain inhibitor MDL 28170 prevents inflammation-induced neurofilament light chain breakdown in the spinal cord and reduces thermal hyperalgesia. Pain 2004, 110:409-418.
28. Lee F.Y., Kim D.W., Karmin J.A., Hong D., Chang S.S., Fujisawa M., Takayanagi H., Bigliani L.U., Blaine T.A., Lee H.J. Mu-Calpain regulates receptor activator of NF-kappaB ligand (RANKL)-supported osteoclastogenesis via NF-kappaB activation in RAW 264.7 cells. J. Biol. Chem. 2005, 280:29929-29936.
29. Li Z., Banik N.L. The localization of mcalpain in myelin: immunocytochemical evidence in different areas of rat brain and nerves. Brain Res. 1995, 697:112-121.
30. Li Y., Dorsi M.J., Meyer R.A., Belzberg A.J. Mechanical hyperalgesia after an L5 spinal nerve lesion in the rat is not dependent on input from injured nerve fibers. Pain 2000, 85:493-502.
31. Li L., Xian C.J., Zhong J.H., 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. 2002, 175:23-34.
32. Li C., Chen S., Yue P., Deng X., Lonial S., Khuri F.R., Sun S.Y. Proteasome inhibitor PS-341 (bortezomib) induces calpain-dependent IkappaB(alpha) degradation. J. Biol. Chem. 2010, 285:16096-16104.
33. Lindia J.A., Kohler M.G., Martin W.J., Abbadie C. Relationship between sodium channel NaV1.3 expression and neuropathic pain behavior in rats. Pain 2005, 117:145-153.
34. Liu J., Liu M.C., Wang K.K. Physiological and pathological actions of calpains in glutamatergic neurons. Sci. Signal 2008, 1:tr3.
35. Ma M. Role of calpains in the injury-induced dysfunction and degeneration of the mammalian axon. Neurobiol. Dis. 2013, 60:61-79.
36. Ma M., Ferguson T.A., Schoch K.M., Li J., Qian Y., Shofer F.S., Saatman K.E., Neumar R.W. Calpains mediate axonal cytoskeleton disintegration during Wallerian degeneration. Neurobiol. Dis. 2013, 56:34-46.
37. Markgraf C.G., Velayo N.L., Johnson M.P., McCarty D.R., Medhi S., Koehl J.R., Chmielewski P.A., Linnik M.D. Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. Stroke 1998, 29:152-158.
38. Michaelis M., Liu X., 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. 2000, 20:2742-2748.
39. Murachi T., Murakami T., Ueda M., Fukui I., Hamakubo T., Adachi Y., Hatanaka M. The calpain-calpastatin system in hematopoietic cells. Adv. Exp. Med. Biol. 1989, 255:445-454.
40. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., Fukuoka T., Tokunaga A., 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 2006, 137:961-970.
41. Obata H., Sakurazawa S., Kimura M., Saito S. Activation of astrocytes in the spinal cord contributes to the development of bilateral allodynia after peripheral nerve injury in rats. Brain Res. 2010, 1363:72-80.
42. Pahl H.L. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 1999, 18:6853-6866.
43. Pellaprat J., Ory-Magne F., Canivet C., Simonetta-Moreau M., Lotterie J.A., Radji F., Arbus C., Gerdelat A., Chaynes P., Brefel-Courbon C. Deep brain stimulation of the subthalamic nucleus improves pain in Parkinson's disease. Parkinsonism Relat. Disord. 2014, 20:662-664.
44. Rawlings N.D., Barrett A.J., Bateman A. MEROPS: the peptidase database. Nucleic Acids Res. 2010, 38:D227-D233.
45. 2+ influx upregulate calpain and induce apoptosis in PC12 cells. Brain Res. 2000, 852:326-334.
46. Rekand T., Gramstad A., Vedeler C.A. Fatigue, pain and muscle weakness are frequent after Guillain-Barre syndrome and poliomyelitis. J. Neurol. 2009, 256:349-354.
47. Schaecher K., Goust J.M., Banik N.L. The effects of calpain inhibition on IkB alpha degradation after activation of PBMCs: identification of the calpain cleavage sites. Neurochem. Res. 2004, 29:1443-1451.
48. Schreiber K.L., Beitz A.J., Wilcox G.L. Activation of spinal microglia in a murine model of peripheral inflammation-induced, long-lasting contralateral allodynia. Neurosci. Lett. 2008, 440:63-67.
49. Shumway S.D., Maki M., Miyamoto S. The PEST domain of IkappaBalpha is necessary and sufficient for in vitro degradation by mu-calpain. J. Biol. Chem. 1999, 274:30874-30881.
50. Sorimachi H., Suzuki K. The structure of calpain. J. Biochem. 2001, 129:653-664.
51. Springer J.E., Azbill R.D., Kennedy S.E., George J., Geddes J.W. Rapid calpain I activation and cytoskeletal protein degradation following traumatic spinal cord injury: attenuation with riluzole pretreatment. J. Neurochem. 1997, 69:1592-1600.
52. Stoelb B.L., Carter G.T., Abresch R.T., Purekal S., McDonald C.M., Jensen M.P. Pain in persons with postpolio syndrome: frequency, intensity, and impact. Arch. Phys. Med. Rehabil. 2008, 89:1933-1940.
53. Tyagarajan S.K., Ghosh H., Yevenes G.E., Imanishi S.Y., Zeilhofer H.U., Gerrits B., Fritschy J.M. Extracellular signal-regulated kinase and glycogen synthase kinase 3beta regulate gephyrin postsynaptic aggregation and GABAergic synaptic function in a calpain-dependent mechanism. J. Biol. Chem. 2013, 288:9634-9647.
54. Uceyler N., Tscharke A., Sommer C. Early cytokine expression in mouse sciatic nerve after chronic constriction nerve injury depends on calpain. Brain Behav. Immun. 2007, 21:553-560.
55. Uceyler N., Biko L., Sommer C. MDL-28170 has no analgesic effect on CCI induced neuropathic pain in mice. Molecules 2010, 15:3038-3047.
56. Vissers K.C., De Jongh R.F., Hoffmann V.L., Meert T.F. Exogenous interleukin-6 increases cold allodynia in rats with a mononeuropathy. Cytokine 2005, 30:154-159.
57. Wang J.J., Chen G.J., Chen W., Du J., Luo A.L., Huang Y.G. Analgesic effect of calpain inhibitor ALLN on the zymosan-induced paw inflammatory pain and its effect on the expression of cyclooxygenase-2 in the spinal dorsal horn. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 2012, 34:25-31.
58. Wang Y., Briz V., Chishti A., Bi X., Baudry M. Distinct roles for mu-calpain and m-calpain in synaptic NMDAR-mediated neuroprotection and extrasynaptic NMDAR-mediated neurodegeneration. J. Neurosci. 2013, 33:18880-18892.
59. Wei X.H., Na X.D., Liao G.J., Chen Q.Y., Cui Y., Chen F.Y., Li Y.Y., Zang Y., Liu X.G. The up-regulation of IL-6 in DRG and spinal dorsal horn contributes to neuropathic pain following L5 ventral root transection. Exp. Neurol. 2013, 241:159-168.
60. Wei X.H., Wei X., Chen F.Y., Zang Y., Xin W.J., Pang R.P., Chen Y., Wang J., Li Y.Y., Shen K.F., Zhou L.J., Liu X.G. The upregulation of translocator protein (18 kDa) promotes recovery from neuropathic pain in rats. J. Neurosci. 2013, 33:1540-1551.
61. Wu H.Y., Lynch D.R. Calpain and synaptic function. Mol. Neurobiol. 2006, 33:215-236.
62. Wu G., Ringkamp M., Murinson B.B., Pogatzki E.M., Hartke T.V., Weerahandi H.M., Campbell J.N., Griffin J.W., Meyer R.A. Degeneration of myelinated efferent fibers induces spontaneous activity in uninjured C-fiber afferents. J. Neurosci. 2002, 22:7746-7753.
63. Xie W.R., Deng H., Li H., Bowen T.L., Strong J.A., Zhang J.M. Robust increase of cutaneous sensitivity, cytokine production and sympathetic sprouting in rats with localized inflammatory irritation of the spinal ganglia. Neuroscience 2006, 142:809-822.
64. Xie W., Uchida H., Nagai J., Ueda M., Chun J., Ueda H. Calpain-mediated down-regulation of myelin-associated glycoprotein in lysophosphatidic acid-induced neuropathic pain. J. Neurochem. 2010, 113:1002-1011.
65. Xu J.T., Xin W.J., Zang Y., Wu C.Y., Liu X.G. The role of tumor necrosis factor-alpha in the neuropathic pain induced by Lumbar 5 ventral root transection in rat. Pain 2006, 123:306-321.
66. Yang J., Weimer R.M., Kallop D., Olsen O., Wu Z., Renier N., Uryu K., Tessier-Lavigne M. Regulation of axon degeneration after injury and in development by the endogenous calpain inhibitor calpastatin. Neuron 2013, 80:1175-1189.
67. Yoshifuji H., Umehara H., Maruyama H., Itoh M., Tanaka M., Kawabata D., Fujii T., Mimori T. Amelioration of experimental arthritis by a calpain-inhibitory compound: regulation of cytokine production by E-64-d in vivo and in vitro. Int. Immunol. 2005, 17:1327-1336.
68. Zadran S., Bi X., Baudry M. Regulation of calpain-2 in neurons: implications for synaptic plasticity. Mol. Neurobiol. 2010, 42:143-150.
69. Zang Y., He X.H., Xin W.J., Pang R.P., Wei X.H., Zhou L.J., Li Y.Y., Liu X.G. Inhibition of NF-kappaB prevents mechanical allodynia induced by spinal ventral root transection and suppresses the re-expression of Nav1.3 in DRG neurons in vivo and in vitro. Brain Res. 2010, 1363:151-158.
70. Zanjani T.M., Sabetkasaei M., Mosaffa N., Manaheji H., Labibi F., Farokhi B. Suppression of interleukin-6 by minocycline in a rat model of neuropathic pain. Eur. J. Pharmacol. 2006, 538:66-72.
71. Zhang S.X., Bondada V., Geddes J.W. Evaluation of conditions for calpain inhibition in the rat spinal cord: effective postinjury inhibition with intraspinal MDL28170 microinjection. J. Neurotrauma 2003, 20:59-67.
72. Zhou X.F., Rush R.A., McLachlan E.M. Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection. J. Neurosci. 1996, 16:2901-2911.
73. - cotransporter-2 impairs spinal chloride homeostasis in neuropathic pain. J. Biol. Chem. 2012, 287:33853-33864.
74. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
75. Ziv N.E., Spira M.E. Axotomy induces a transient and localized elevation of the free intracellular calcium concentration to the millimolar range. J. Neurophysiol. 1995, 74:2625-2637.