Spinal macrophage migration inhibitory factor is a major contributor to rodent neuropathic pain-like hypersensitivity

Anesthesiology

Volumn 114, Issue 3, 2011, Pages 643-659

  Wang, FuZhou ^a,b   Xu, ShiQin ^b   Shen, XiaoFeng ^b   Guo, XiRong ^b   Peng, YuZhu ^b   Yang, Jie ^a  

^a NANJING UNIVERSITY   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD74 ANTIGEN; INTERLEUKIN 8; MACROPHAGE MIGRATION INHIBITION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GENE MUTATION; MALE; MOUSE; NERVE INJURY; NEUROPATHIC PAIN; NEUROPATHIC PAIN LIKE HYPERSENSITIVITY; NONHUMAN; PAIN THRESHOLD; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; UPREGULATION;

EID: 79952038794     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e31820a4bf3     Document Type: Article

References (68)

1. Calmels P, Mick G, Perrouin-Verbe B, Ventura M; SOFMER (French Society for Physical Medicine and Rehabilitation): Neuropathic pain in spinal cord injury: Identification, classification, evaluation. Ann Phys Rehabil Med 2009; 52:83-102
2. Basić-Kes V, Zavoreo I, Bosnar-Puretić M, Ivanković M, Bitunjac M, Govori V, Demarin V: Neuropathic pain. Acta Clin Croat 2009; 48:359-65
3. Vranken JH: Mechanisms and treatment of neuropathic pain. Cent Nerv Syst Agents Med Chem 2009; 9:71-8
4. Namaka M, Leong C, Grossberndt A, Klowak M, Turcotte D, Esfahani F, Gomori A, Intrater H: A treatment algorithm for neuropathic pain: An update. Consult Pharm 2009; 24:885-902
5. Watkins LR, Maier SF: Beyond neurons: Evidence that immune and glial cells contribute to pathological pain states. Physiol Rev 2002; 82:981-1011
6. Marchand F, Perretti M, McMahon SB: Role of the immune system in chronic pain. Nat Rev Neurosci 2005; 6:521-32 (Pubitemid 40942819)
7. Moalem G, Tracey DJ: Immune and inflammatory mechanisms in neuropathic pain. Brain Res Rev 2006; 51:240-64 (Pubitemid 43902971)
8. Costigan M, Moss A, Latremoliere A, Johnston C, Verma-Gandhu M, Herbert TA, Barrett L, Brenner GJ, Vardeh D, Woolf CJ, Fitzgerald M: T-cell infiltration and signaling in the adult dorsal spinal cord is a major contributor to neuropathic pain-like hypersensitivity. J Neurosci 2009; 29:14415-22
9. Li M, Peake PW, Charlesworth JA, Tracey DJ, Moalem-Taylor G: Complement activation contributes to leukocyte recruitment and neuropathic pain following peripheral nerve injury in rats. Eur J Neurosci 2007; 26:3486-500 (Pubitemid 350243542)
10. Inoue K, Tsuda M: Microglia and neuropathic pain. Glia 2009; 57:1469-79
11. Kwon BK, Stammers AM, Belanger LM, Bernardo A, Chan D, Bishop CM, Slobogean GP, Zhang H, Umedaly H, Giffin M, Street J, Boyd MC, Paquette SJ, Fisher CG, Dvorak MF: Cerebrospinal fluid inflammatory cytokines and biomarkers of injury severity in acute human spinal cord injury. J Neurotrauma 2010; 27:669-82
12. Vallejo R, Tilley DM, Vogel L, Benyamin R: The role of glia and the immune system in the development and maintenance of neuropathic pain. Pain Pract 2010; 10:167-84
13. Wieseler-Frank J, Maier SF, Watkins LR: Central proinflammatory cytokines and pain enhancement. Neurosignals 2005; 14:166-74 (Pubitemid 41417105)
14. Crichlow GV, Lubetsky JB, Leng L, Bucala R, Lolis EJ: Structural and kinetic analyses of macrophage migration inhibitory factor active site interactions. Biochemistry 2009; 48:132-9
15. Orita M, Yamamoto S, Katayama N, Fujita S: Macrophage migration inhibitory factor and the discovery of tautomerase inhibitors. Curr Pharm Des 2002; 8:1297-317 (Pubitemid 34594254)
16. Lue H, Dewor M, Leng L, Bucala R, Bernhagen J: Activation of the JNK signalling pathway by macrophage migration inhibitory factor (MIF) and dependence on CXCR4 and CD74. Cell Signal 2011; 23:135-44
17. Flaster H, Bernhagen J, Calandra T, Bucala R: The macrophage migration inhibitory factor-glucocorticoid dyad: Regulation of inflammation and immunity. Mol Endocrinol 2007; 21:1267-80 (Pubitemid 46984737)
18. Grieb G, Merk M, Bernhagen J, Bucala R: Macrophage migration inhibitory factor (MIF): A promising biomarker. Drug News Perspect 2010; 23:257-64
19. Tierney T, Patel R, Stead CA, Leng L, Bucala R, Buckingham JC: Macrophage migration inhibitory factor is released from pituitary folliculo-stellate-like cells by endotoxin and dexamethasone and attenuates the steroid-induced inhibition of interleukin 6 release. Endocrinology 2005; 146:35-43 (Pubitemid 40051720)
20. Dios A, Mitchell RA, Aljabari B, Lubetsky J, O'Connor K, Liao H, Senter PD, Manogue KR, Lolis E, Metz C, Bucala R, Callaway DJ, Al-Abed Y: Inhibition of MIF bioactivity by rational design of pharmacological inhibitors of MIF tautomerase activity. J Med Chem 2002; 45:2410-6 (Pubitemid 34595211)
21. Gibbings DJ, Ghetu AF, Dery R, Befus AD: Macrophage migration inhibitory factor has a MHC class I-like motif and function. Scand J Immunol 2008; 67:121-32
22. Ogata A, Nishihira J, Suzuki T, Nagashima K, Tashiro K: Identification of macrophage migration inhibitory factor mRNA expression in neural cells of the rat brain by in situ hybridization. Neurosci Lett 1998; 246:173-7 (Pubitemid 28231237)
23. Bacher M, Meinhardt A, Lan HY, Dhabhar FS, Mu W, Metz CN, Chesney JA, Gemsa D, Donnelly T, Atkins RC, Bucala R: MIF expression in the rat brain: Implications for neuronal function. Mol Med 1998; 4:217-30 (Pubitemid 28331239)
24. Nishio Y, Minami A, Kato H, Kaneda K, Nishihira J: Identification of macrophage migration inhibitory factor (MIF) in rat peripheral nerves: Its possible involvement in nerve regeneration. Biochim Biophys Acta 1999; 1453:74-82 (Pubitemid 29065459)
25. Nishio Y, Nishihira J, Ishibashi T, Kato H, Minami A: Role of macrophage migration inhibitory factor (MIF) in peripheral nerve regeneration: Anti-MIF antibody induces delay of nerve regeneration and the apoptosis of Schwann cells. Mol Med 2002; 8:509-20 (Pubitemid 36332362)
26. Yang Y, Xie Y, Chai H, Fan M, Liu S, Liu H, Bruce I, Wu W: Microarray analysis of gene expression patterns in adult spinal motoneurons after different types of axonal injuries. Brain Res 2006; 1075:1-12
27. Chalimoniuk M, King-Pospisil K, Metz CN, Toborek M: Macrophage migration inhibitory factor induces cell death and decreases neuronal nitric oxide expression in spinal cord neurons. Neuroscience 2006; 139:1117-28
28. Nishio Y, Koda M, Hashimoto M, Kamada T, Koshizuka S, Yoshinaga K, Onodera S, Nishihira J, Okawa A, Yamazaki M: Deletion of macrophage migration inhibitory factor attenuates neuronal death and promotes functional recovery after compression-induced spinal cord injury in mice. Acta Neuropathol 2009; 117:321-8
29. Melzack R, Coderre TJ, Katz J, Vaccarino AL: Central neuroplasticity and pathological pain. Ann N Y Acad Sci 2001; 933:157-74 (Pubitemid 32386032)
30. Hathway GJ, Vega-Avelaira D, Moss A, Ingram R, Fitzgerald M: Brief, low frequency stimulation of rat peripheral C-fibres evokes prolonged microglial-induced central sensitization in adults but not in neonates. Pain 2009; 144:110-8
31. Wang F, Shen X, Guo X, Peng Y, Liu Y, Xu S, Yang J: Spinal macrophage migration inhibitory factor contributes to the pathogenesis of inflammatory hyperalgesia in rats. Pain 2010; 148:275-83
32. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R: MIF signal transduction initiated by binding to CD74. J Exp Med 2003; 197:1467-76 (Pubitemid 36686708)
33. Balachandran S, Rodge A, Gadekar PK, Yadav VN, Kamath D, Chetrapal-Kunwar A, Bhatt P, Srinivasan S, Sharma S, Vishwakarma RA, Dagia NM: Novel derivatives of ISO-1 as potent inhibitors of MIF biological function. Bioorg Med Chem Lett 2009; 19:4773-6
34. Pogatzki EM, Zahn PK, Brennan TJ: Lumbar catheterization of the subarachnoid space with a 32-gauge polyurethane catheter in the rat. Eur J Pain 2000; 4:111-3 (Pubitemid 30230801)
35. Wu WP, Xu XJ, Hao JX: Chronic lumbar catheterization of the spinal subarachnoid space in mice. J Neurosci Meth 2004; 133:65-9
36. Poon YY, Chang AY, Ko SF, Chan SH: An improved procedure for catheterization of the thoracic spinal subarachnoid space in the rat. Anesth Analg 2005; 101:155-60 (Pubitemid 40853368)
37. Bennett GJ, Xie YK: A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988; 33:87-107
38. Lambert GA, Mallos G, Zagami AS: Von Frey's hairs - a review of their technology and use - a novel automated von Frey device for improved testing for hyperalgesia. J Neurosci Meth 2009; 177:420-6
39. Hantman AW, van den Pol AN, Perl ER: Morphological and physiological features of a set of spinal substantia gelatinosa neurons defined by green fluorescent protein expression. J Neurosci 2004; 24:836-42 (Pubitemid 38146594)
40. Bird GC, Han JS, Fu Y, Adwanikar H, Willis WD, Neugebauer V: Pain-related synaptic plasticity in spinal dorsal horn neurons: Role of CGRP. Mol Pain 2006; 2:31
41. Li H, Gang Z, Yuling H, Luokun X, Jie X, Hao L, Li W, Chunsong H, Junyan L, Mingshen J, Youxin J, Feili G, Boquan J, Jinquan T: Different neurotropic pathogens elicit neurotoxic CCR9- or neurosupportive CXCR3-expressing microglia. J Immunol 2006; 177:3644-56 (Pubitemid 44359896)
42. Ekmark-Lewén S, Lewén A, Israelsson C, Li GL, Farooque M, Olsson Y, Ebendal T, Hillered L: Vimentin and GFAP responses in astrocytes after contusion trauma to the murine brain. Restor Neurol Neurosci 2010; 28:311-21
43. Dent MA, Segura-Anaya E, Alva-Medina J, Aranda-Anzaldo A: NeuN/Fox-3 is an intrinsic component of the neuronal nuclear matrix. FEBS Lett 2010; 584:2767-71
44. Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, Bucala R: Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: Regulatory role in the innate immune response. Proc Natl Acad Sci U S A 2002; 99:345-50 (Pubitemid 34060365)
45. Bendrat K, Al-Abed Y, Callaway DJ, Peng T, Calandra T, Metz CN, Bucala R: Biochemical and mutational investigations of the enzymatic activity of macrophage migration inhibitory factor. Biochemistry 1997; 36:15356-62 (Pubitemid 27528002)
46. Lolis E, Bucala R: Macrophage migration inhibitory factor. Exp Opin Ther Targets 2003; 7:153-64 (Pubitemid 36512017)
47. Vega-Avelaira D, Géranton SM, Fitzgerald M: Differential regulation of immune responses and macrophage/neuron interactions in the dorsal root ganglion in young and adult rats following nerve injury. Mol Pain 2009; 5:70
48. Leiphart JW, Vasudevan PP, Rajjoub SR, Dominguez LW, Chang J: The effect of acute postoperative pain and chronic neuropathic pain on subsequent weight gain in the rat. J Neurosurg 2010; 112:780-3
49. Bölcskei K, Helyes Z, Szabó A, Sándor K, Elekes K, Németh J, Almási R, Pintér E, Petho G, Szolcsányi J: Investigation of the role of TRPV1 receptors in acute and chronic nociceptive processes using gene-deficient mice. Pain 2005; 117:368-76
50. Chu KL, Faltynek CR, Jarvis MF, McGaraughty S: Increased WDR spontaneous activity and receptive field size in rats following a neuropathic or inflammatory injury: Implications for mechanical sensitivity. Neurosci Lett 2004; 372:123-6 (Pubitemid 39505241)
51. Chernova T, Steinert JR, Guerin CJ, Nicotera P, Forsythe ID, Smith AG: Neurite degeneration induced by heme deficiency mediated via inhibition of NMDA receptor-dependent extracellular signal-regulated kinase 1/2 activation. J Neurosci 2007; 27:8475-85
52. Peng HY, Chen GD, Tung KC, Chien YW, Lai CY, Hsieh MC, Chiu CH, Lai CH, Lee SD, Lin TB: Estrogen-dependent facilitation on spinal reflex potentiation involves the Cdk5/ERK1/2/NR2B cascade in anesthetized rats. Am J Physiol Endocrinol Metab 2009; 297:E416-26
53. Oprée A, Kress M: Involvement of the proinflammatory cytokines tumor necrosis factor-alpha, IL-1 beta, and IL-6 but not IL-8 in the development of heat hyperalgesia: Effects on heat-evoked calcitonin gene-related peptide release from rat skin. J Neurosci 2000; 20:6289-93 (Pubitemid 30658424)
54. Uçeyler N, Kafke W, Riediger N, He L, Necula G, Toyka KV, Sommer C: Elevated proinflammatory cytokine expression in affected skin in small fiber neuropathy. Neurology 2010; 74:1806-13
55. Wang XM, Hamza M, Wu TX, Dionne RA: Upregulation of IL-6, IL-8, and CCL2 gene expression after acute inflammation: Correlation to clinical pain. Pain 2009; 142:275-83
56. Ma W, Chabot JG, Vercauteren F, Quirion R: Injured nerve-derived COX2/PGE2 contributes to the maintenance of neuropathic pain in aged rats. Neurobiol Aging 2010; 31:1227-37
57. Carli C, Metz CN, Al-Abed Y, Naccache PH, Akoum A: Up-regulation of cyclooxygenase-2 expression and prostaglandin E2 production in human endometriotic cells by macrophage migration inhibitory factor: Involvement of novel kinase signaling pathways. Endocrinology 2009; 150:3128-37
58. O'Callaghan JP, Miller DB: Spinal glia and chronic pain. Metabolism 2010; 59:S21-6
59. Smith HS: Activated microglia in nociception. Pain Phys 2010; 13:295-304
60. DeLeo JA, Yezierski RP: The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 2001; 90:1-6 (Pubitemid 32146552)
61. Wu LJ, Zhuo M: Targeting the NMDA receptor subunit NR2B for the treatment of neuropathic pain. Neurotherapeutics 2009; 6:693-702
62. Myers RR, Campana WM, Shubayev VI: The role of neuroinflammation in neuropathic pain: Mechanisms and therapeutic targets. Drug Discov Today 2006; 11:8-20 (Pubitemid 43227847)
63. 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
64. Xu Q, Garraway SM, Weyerbacher AR, Shin SJ, Inturrisi CE: Activation of the neuronal extracellular signal-regulated kinase 2 in the spinal cord dorsal horn is required for complete Freund's adjuvant-induced pain hypersensitivity. J Neurosci 2008; 28:14087-96
65. Klinger MB, Sacks S, Cervero F: A role for extracellular signal-regulated kinases 1 and 2 (ERK 1/2) in the maintenance of persistent mechanical hyperalgesia in ovariectomized mice. Neuroscience 2011; 172:483-93
66. Alter BJ, Zhao C, Karim F, Landreth GE, Gereau RW IV: Genetic targeting of ERK1 suggests a predominant role for ERK2 in murine pain models. J Neurosci 2010; 30:11537-47
67. Campillo A, González-Cuello A, Cabañero D, Garcia-Nogales P, Romero A, Milanés MV, Laorden ML, Puig MM: Increased spinal dynorphin levels and phospho-extracellular signal-regulated kinases 1 and 2 and c-Fos immunoreactivity after surgery under remifentanil anesthesia in mice. Mol Pharmacol 2010; 77:185-94
68. Yu YQ, Zhao F, Chen J: Activation of ERK1/2 in the primary injury site is required to maintain melittin-enhanced wind-up of rat spinal wide-dynamic-range neurons. Neurosci Lett 2009; 459:137-41