Selectively reducing cytokine/chemokine expressing macrophages in injured nerves impairs the development of neuropathic pain

Experimental Neurology

Volumn 240, Issue 1, 2013, Pages 205-218

  Echeverry, Stefania ^a,c   Wu, Yichen ^a,b   Zhang, Ji ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Inflammation; Macrophages; Nerve injury; Neuropathic pain; Proliferation; T lymphocytes; Transforming growth factor beta

Indexed keywords

AUTACOID; CD11B ANTIGEN; CELL PROTEIN; CHEMOKINE; CYTOKINE; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; PROTEIN ED1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CONTROLLED STUDY; CYTOKINE RELEASE; HISTOPATHOLOGY; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MALE; NERVE DEGENERATION; NERVE INJURY; NERVE LIGATION; NEUROPATHIC PAIN; NEUROPATHOLOGY; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCIATIC NERVE; T LYMPHOCYTE;

ANIMALS; CHEMOKINES; CYTOKINES; DISEASE MODELS, ANIMAL; MACROPHAGES; MALE; NEURALGIA; PERIPHERAL NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84871762730     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.11.013     Document Type: Article

References (76)

1. Andre S., Tough D.F., Lacroix-Desmazes S., Kaveri S.V., Bayry J. Surveillance of antigen-presenting cells by CD4+ CD25+ regulatory T cells in autoimmunity: immunopathogenesis and therapeutic implications. Am. J. Pathol. 2009, 174:1575-1587.
2. Ashcroft G.S., Yang X., Glick A.B., Weinstein M., Letterio J.L., Mizel D.E., Anzano M., Greenwell-Wild T., Wahl S.M., Deng C., Roberts A.B. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1999, 1:260-266.
3. Austin P.J., Moalem-Taylor G. The neuro-immune balance in neuropathic pain: involvement of inflammatory immune cells, immune-like glial cells and cytokines. J. Neuroimmunol. 2010, 229:26-50.
4. Baichwal R.R., Bigbee J.W., DeVries G.H. Macrophage-mediated myelin-related mitogenic factor for cultured Schwann cells. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:1701-1705.
5. Barclay J., Clark A.K., Ganju P., Gentry C., Patel S., Wotherspoon G., Buxton F., Song C., Ullah J., Winter J., Fox A., Bevan S., Malcangio M. Role of the cysteine protease cathepsin S in neuropathic hyperalgesia. Pain 2007, 130:225-234.
6. Barrette B., Hebert M.A., Filali M., Lafortune K., Vallieres N., Gowing G., Julien J.P., Lacroix S. Requirement of myeloid cells for axon regeneration. J. Neurosci. 2008, 28:9363-9376.
7. Bastos L.F., Medeiros D.C., Vieira R.P., Watkins L.R., Coelho M.M., Moraes M.F. Intraneural dexamethasone applied simultaneously to rat sciatic nerve constriction delays the development of hyperalgesia and allodynia. Neurosci. Lett. 2012, 510:20-23.
8. Bogdan C., Paik J., Vodovotz Y., Nathan C. Contrasting mechanisms for suppression of macrophage cytokine release by transforming growth factor-beta and interleukin-10. J. Biol. Chem. 1992, 267:23301-23308.
9. Bottner M., Krieglstein K., Unsicker K. The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions. J. Neurochem. 2000, 75:2227-2240.
10. Calvo M., Bennett D.L. The mechanisms of microgliosis and pain following peripheral nerve injury. Exp. Neurol. 2012, 234:271-282.
11. Campbell J.N., Raja S.N., Meyer R.A., Mackinnon S.E. Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 1988, 32:89-94.
12. Cao L., DeLeo J.A. CNS-infiltrating CD4+ T lymphocytes contribute to murine spinal nerve transection-induced neuropathic pain. Eur. J. Immunol. 2008, 38:448-458.
13. 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.
14. Costigan M., Moss A., Latremoliere A., Johnston C., Verma-Gandhu M., Herbert T.A., Barrett L., Brenner G.J., Vardeh D., Woolf C.J., 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, 29:14415-14422.
15. Cunha T.M., Verri W.A., Silva J.S., Poole S., Cunha F.Q., Ferreira S.H. A cascade of cytokines mediates mechanical inflammatory hypernociception in mice. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1755-1760.
16. Dennler S., Prunier C., Ferrand N., Gauthier J.M., Atfi A. c-Jun inhibits transforming growth factor beta-mediated transcription by repressing Smad3 transcriptional activity. J. Biol. Chem. 2000, 275:28858-28865.
17. Dennler S., Goumans M.J., ten Dijke P. Transforming growth factor beta signal transduction. J. Leukoc. Biol. 2002, 71:731-740.
18. Ding A., Nathan C.F., Graycar J., Derynck R., Stuehr D.J., Srimal S. Macrophage deactivating factor and transforming growth factors-beta 1 -beta 2 and -beta 3 inhibit induction of macrophage nitrogen oxide synthesis by IFN-gamma. J. Immunol. 1990, 145:940-944.
19. Dixon W.J. Efficient analysis of experimental observations. Annu. Rev. Pharmacol. Toxicol. 1980, 20:441-462.
20. Dubovy P. Wallerian degeneration and peripheral nerve conditions for both axonal regeneration and neuropathic pain induction. Ann. Anat. 2011, 193:267-275.
21. Echeverry S., Shi X.Q., Haw A., Liu H., Zhang Z.W., Zhang J. Transforming growth factor-beta1 impairs neuropathic pain through pleiotropic effects. Mol. Pain 2009, 5:16.
22. Echeverry S., Shi X.Q., Rivest S., Zhang J. Peripheral nerve injury alters blood-spinal cord barrier functional and molecular integrity through a selective inflammatory pathway. J. Neurosci. 2011, 31:10819-10828.
23. Fadok V.A., Bratton D.L., Konowal A., Freed P.W., Westcott J.Y., Henson P.M. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Investig. 1998, 101:890-898.
24. Gaudet A.D., Popovich P.G., Ramer M.S. Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. J. Neuroinflammation 2011, 8:110.
25. Grace P.M., Rolan P.E., Hutchinson M.R. Peripheral immune contributions to the maintenance of central glial activation underlying neuropathic pain. Brain Behav. Immun. 2011, 25:1322-1332.
26. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
27. Hirata K., Kawabuchi M. Myelin phagocytosis by macrophages and nonmacrophages during Wallerian degeneration. Microsc. Res. Tech. 2002, 57:541-547.
28. Imai Y., Ibata I., Ito D., Ohsawa K., Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun. 1996, 224:855-862.
29. Imai K., Takeshita A., Hanazawa S. Transforming growth factor-beta inhibits lipopolysaccharide-stimulated expression of inflammatory cytokines in mouse macrophages through downregulation of activation protein 1 and CD14 receptor expression. Infect. Immun. 2000, 68:2418-2423.
30. Jander S., Lausberg F., Stoll G. Differential recruitment of CD8+ macrophages during Wallerian degeneration in the peripheral and central nervous system. Brain Pathol. 2001, 11:27-38.
31. Junger H., Sorkin L.S. Nociceptive and inflammatory effects of subcutaneous TNFalpha. Pain 2000, 85:145-151.
32. Kawasaki Y., Zhang L., Cheng J.K., Ji R.R. Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J. Neurosci. 2008, 28:5189-5194.
33. Kehlet H., Jensen T.S., Woolf C.J. Persistent postsurgical pain: risk factors and prevention. Lancet 2006, 367:1618-1625.
34. Keswani S.C., Polley M., Pardo C.A., Griffin J.W., McArthur J.C., Hoke A. Schwann cell chemokine receptors mediate HIV-1 gp120 toxicity to sensory neurons. Ann. Neurol. 2003, 54:287-296.
35. Kiguchi N., Maeda T., Kobayashi Y., Fukazawa Y., Kishioka S. Macrophage inflammatory protein-1alpha mediates the development of neuropathic pain following peripheral nerve injury through interleukin-1beta up-regulation. Pain 2010, 149:305-315.
36. Kleinschnitz C., Hofstetter H.H., Meuth S.G., Braeuninger S., Sommer C., Stoll G. T cell infiltration after chronic constriction injury of mouse sciatic nerve is associated with interleukin-17 expression. Exp. Neurol. 2006, 200:480-485.
37. Labuz D., Schmidt Y., Schreiter A., Rittner H.L., Mousa S.A., Machelska H. Immune cell-derived opioids protect against neuropathic pain in mice. J. Clin. Investig. 2009, 119:278-286.
38. Labuz D., Schreiter A., Schmidt Y., Brack A., Machelska H. T lymphocytes containing beta-endorphin ameliorate mechanical hypersensitivity following nerve injury. Brain Behav. Immun. 2010, 24:1045-1053.
39. Langermans J.A., Nibbering P.H., Van Vuren-Van Der Hulst M.E., Van Furth R. Transforming growth factor-beta suppresses interferon-gamma-induced toxoplasmastatic activity in murine macrophages by inhibition of tumour necrosis factor-alpha production. Parasite Immunol. 2001, 23:169-175.
40. Lantero A., Tramullas M., Diaz A., Hurle M.A. Transforming growth factor-beta in normal nociceptive processing and pathological pain models. Mol. Neurobiol. 2012, 45:76-86.
41. Lee S.K., Wolfe S.W. Peripheral nerve injury and repair. J. Am. Acad. Orthop. Surg. 2000, 8:243-252.
42. Lee S., Zhang J. Heterogeneity of macrophages in injured trigeminal nerves: Cytokine/chemokine expressing vs. phagocytic macrophages. Brain Behav. Immun. 2012, 26:891-903.
43. Li M.O., Sanjabi S., Flavell R.A. Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 2006, 25:455-471.
44. Li M.O., Wan Y.Y., Sanjabi S., Robertson A.K., Flavell R.A. Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 2006, 24:99-146.
45. Liu T., van Rooijen N., Tracey D.J. Depletion of macrophages reduces axonal degeneration and hyperalgesia following nerve injury. Pain 2000, 86:25-32.
46. Liu Y.L., Zhou L.J., Hu N.W., Xu J.T., Wu C.Y., Zhang T., Li Y.Y., Liu X.G. Tumor necrosis factor-alpha induces long-term potentiation of C-fiber evoked field potentials in spinal dorsal horn in rats with nerve injury: the role of NF-kappa B, JNK and p38 MAPK. Neuropharmacology 2007, 52:708-715.
47. Mahic M., Yaqub S., Bryn T., Henjum K., Eide D.M., Torgersen K.M., Aandahl E.M., Tasken K. Differentiation of naive CD4+ T cells into CD4+CD25+FOXP3+ regulatory T cells by continuous antigen stimulation. J. Leukoc. Biol. 2008, 83:1111-1117.
48. Maloy K.J., Powrie F. Regulatory T cells in the control of immune pathology. Nat. Immunol. 2001, 2:816-822.
49. Marie J.C., Letterio J.J., Gavin M., Rudensky A.Y. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J. Exp. Med. 2005, 201:1061-1067.
50. McDonald P.P., Fadok V.A., Bratton D., Henson P.M. Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-beta in macrophages that have ingested apoptotic cells. J. Immunol. 1999, 163:6164-6172.
51. Mert T., Gunay I., Ocal I., Guzel A.I., Inal T.C., Sencar L., Polat S. Macrophage depletion delays progression of neuropathic pain in diabetic animals. Naunyn Schmiedebergs Arch. Pharmacol. 2009, 379:445-452.
52. Moalem G., Xu K., Yu L. T lymphocytes play a role in neuropathic pain following peripheral nerve injury in rats. Neuroscience 2004, 129:767-777.
53. Myers R.R., Heckman H.M., Rodriguez M. Reduced hyperalgesia in nerve-injured WLD mice: relationship to nerve fiber phagocytosis, axonal degeneration, and regeneration in normal mice. Exp. Neurol. 1996, 141:94-101.
54. Price D.D., Bennett G.J., Rafii A. Psychophysical observations on patients with neuropathic pain relieved by a sympathetic block. Pain 1989, 36:273-288.
55. Ramer M.S., French G.D., Bisby M.A. Wallerian degeneration is required for both neuropathic pain and sympathetic sprouting into the DRG. Pain 1997, 72:71-78.
56. Rutkowski M.D., Pahl J.L., Sweitzer S., van Rooijen N., DeLeo J.A. Limited role of macrophages in generation of nerve injury-induced mechanical allodynia. Physiol. Behav. 2000, 71:225-235.
57. Scholz J., Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 2007, 10:1361-1368.
58. Scholzen T., Gerdes J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 2000, 182:311-322.
59. Seltzer Z., Dubner R., Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 1990, 43:205-218.
60. Smith P.D., Smythies L.E., Shen R., Greenwell-Wild T., Gliozzi M., Wahl S.M. Intestinal macrophages and response to microbial encroachment. Mucosal Immunol. 2011, 4:31-42.
61. Smythies L.E., Shen R., Bimczok D., Novak L., Clements R.H., Eckhoff D.E., Bouchard P., George M.D., Hu W.K., Dandekar S., Smith P.D. Inflammation anergy in human intestinal macrophages is due to Smad-induced IkappaBalpha expression and NF-kappaB inactivation. J. Biol. Chem. 2010, 285:19593-19604.
62. Sommer C., Kress M. Recent findings on how proinflammatory cytokines cause pain: peripheral mechanisms in inflammatory and neuropathic hyperalgesia. Neurosci. Lett. 2004, 361:184-187.
63. Sommer C., Schafers M. Painful mononeuropathy in C57BL/Wld mice with delayed wallerian degeneration: differential effects of cytokine production and nerve regeneration on thermal and mechanical hypersensitivity. Brain Res. 1998, 784:154-162.
64. Sorkin L.S., Xiao W.H., Wagner R., Myers R.R. Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience 1997, 81:255-262.
65. Takaki H., Minoda Y., Koga K., Takaesu G., Yoshimura A., Kobayashi T. TGF-beta1 suppresses IFN-gamma-induced NO production in macrophages by suppressing STAT1 activation and accelerating iNOS protein degradation. Genes Cells 2006, 11:871-882.
66. Tramullas M., Lantero A., Diaz A., Morchon N., Merino D., Villar A., Buscher D., Merino R., Hurle J.M., Izpisua-Belmonte J.C., Hurle M.A. BAMBI (bone morphogenetic protein and activin membrane-bound inhibitor) reveals the involvement of the transforming growth factor-beta family in pain modulation. J. Neurosci. 2010, 30:1502-1511.
67. Tsai Y.C., Won S.J. Effects of tramadol on T lymphocyte proliferation and natural killer cell activity in rats with sciatic constriction injury. Pain 2001, 92:63-69.
68. Tsunawaki S., Sporn M., Ding A., Nathan C. Deactivation of macrophages by transforming growth factor-beta. Nature 1988, 334:260-262.
69. 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.
70. Uceyler N., Kafke W., Riediger N., He L., Necula G., Toyka K.V., Sommer C. Elevated proinflammatory cytokine expression in affected skin in small fiber neuropathy. Neurology 2010, 74:1806-1813.
71. Vargas M.E., Barres B.A. Why is Wallerian degeneration in the CNS so slow?. Annu. Rev. Neurosci. 2007, 30:153-179.
72. Vodovotz Y., Bogdan C., Paik J., Xie Q.W., Nathan C. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor beta. J. Exp. Med. 1993, 178:605-613.
73. Wagner R., Myers R.R. Endoneurial injection of TNF-alpha produces neuropathic pain behaviors. Neuroreport 1996, 7:2897-2901.
74. Woolf C.J. Central sensitization: implications for the diagnosis and treatment of pain. Pain 2011, 152:S2-S15.
75. Zelenka M., Schafers M., 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 2005, 116:257-263.
76. Zhang J., Shi X.Q., Echeverry S., Mogil J.S., De Koninck Y., Rivest S. Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J. Neurosci. 2007, 27:12396-12406.