Active immunization with myelin-derived altered peptide ligand reduces mechanical pain hypersensitivity following peripheral nerve injury

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Perera, Chamini J ^a   Duffy, Samuel S ^a   Lees, Justin G ^a   Kim, Cristina F ^a   Cameron, Barbara ^b   Apostolopoulos, Vasso ^c   Moalem Taylor, Gila ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c VICTORIA UNIVERSITY   (Australia)

Author keywords

Altered peptide ligand; Anti inflammatory cytokines; M1 and M2 macrophages; Mechanical allodynia; Myelin basic protein; Neuropathic pain; Pro inflammatory cytokines

Indexed keywords

ALTERED PEPTIDE LIGAND CYCLO (87-99)[ALANINE 91,ALANINE 96]MYELIN BASIC PROTEIN; CYCLO MYELIN BASIC PROTEIN 87-99; ERYTHROPOIETIN; FREUND ADJUVANT; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 7; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; PEPTIDE VACCINE; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN; APL-1 PEPTIDE; CHAPERONIN 60; CYTOKINE; MYELIN BASIC PROTEIN; PEPTIDE FRAGMENT;

ACTIVE IMMUNIZATION; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; CHRONIC CONSTRICTION INJURY; CONTROLLED STUDY; FLOW CYTOMETRY; HYPERSENSITIVITY; IMMUNITY; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; LUMBAR SPINAL CORD; LYMPH NODE; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MALE; MECHANICAL PAIN HYPERSENSITIVITY; MECHANICAL STIMULATION; MICROGLIA; NERVOUS SYSTEM; NERVOUS TISSUE; NONHUMAN; PAIN THRESHOLD; PERIPHERAL NERVE INJURY; PERIPHERAL NEUROPATHY; RAT; REGULATORY T LYMPHOCYTE; SCIATIC NERVE; SPLEEN; UPREGULATION; ANIMAL; BLOOD; COMPLICATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; HEMISPHERIC DOMINANCE; HYPERALGESIA; IMMUNOLOGY; LEWIS RAT; METABOLISM; PROCEDURES; SCIATIC NEUROPATHY; SENSORY NERVE CELL; SPINAL GANGLION; TIME FACTOR; VACCINATION;

ANIMALS; CHAPERONIN 60; CYTOKINES; DISEASE MODELS, ANIMAL; FREUND'S ADJUVANT; FUNCTIONAL LATERALITY; GANGLIA, SPINAL; HYPERALGESIA; MACROPHAGES; MALE; MYELIN BASIC PROTEIN; PAIN THRESHOLD; PEPTIDE FRAGMENTS; RATS; RATS, INBRED LEW; SCIATIC NEUROPATHY; SENSORY RECEPTOR CELLS; TIME FACTORS; VACCINATION;

EID: 84924157762     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0253-4     Document Type: Article

References (74)

1. Dworkin RH, Backonja M, Rowbotham MC, Allen RR, Argoff CR, Bennett GJ, et al. Advances in neuropathic pain: diagnosis, mechanisms, and treatment recommendations. Arch Neurol. 2003;60:1524-34.
2. Myers RR, Campana WM, Shubayev VI. The role of neuroinflammation in neuropathic pain: mechanisms and therapeutic targets. Drug Discov Today. 2006;11:8-20.
3. Gao YJ, Ji RR. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther. 2010;126:56-68.
4. Austin PJ, 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.
5. Costigan M, Moss A, Latremoliere A, Johnston C, Verma-Gandhu M, Herbert TA, et al. 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.
6. Moalem G, Xu K, Yu L. T lymphocytes play a role in neuropathic pain following peripheral nerve injury in rats. Neuroscience. 2004;129:767-77.
7. Cui JG, Holmin S, Mathiesen T, Meyerson BA, Linderoth B. Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy. Pain. 2000;88:239-48.
8. Hu P, Bembrick AL, Keay KA, McLachlan EM. Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve. Brain Behav Immun. 2007;21:599-616.
9. Hu P, McLachlan EM. Macrophage and lymphocyte invasion of dorsal root ganglia after peripheral nerve lesions in the rat. Neuroscience. 2002;112:23-38.
10. Cao L, DeLeo JA. CNS-infiltrating CD4+ T lymphocytes contribute to murine spinal nerve transection-induced neuropathic pain. Eur J Immunol. 2008;38:448-58.
11. Draleau K, Maddula S, Slaiby A, Nutile-McMenemy N, De Leo J, Cao L. Phenotypic Identification of Spinal Cord-Infiltrating CD4 T Lymphocytes in a Murine Model of Neuropathic Pain. J Pain Relief Suppl. 2014;3:003.
12. Kim CF, Moalem-Taylor G. Detailed characterization of neuro-immune responses following neuropathic injury in mice. Brain Res. 2011;1405:95-108.
13. Austin PJ, Kim CF, Perera CJ, Moalem-Taylor G. Regulatory T cells attenuate neuropathic pain following peripheral nerve injury and experimental autoimmune neuritis. Pain. 2012;153:1916-31.
14. Kalergis AM, Nathenson SG. Altered peptide ligand-mediated TCR antagonism can be modulated by a change in a single amino acid residue within the CDR3 beta of an MHC class I-restricted TCR. J Immunol. 2000;165:280-5.
15. Katsara M, Minigo G, Plebanski M, Apostolopoulos V. The good, the bad and the ugly: how altered peptide ligands modulate immunity. Expert Opin Biol Ther. 2008;8:1873-84.
16. Gaur A, Boehme SA, Chalmers D, Crowe PD, Pahuja A, Ling N, et al. Amelioration of relapsing experimental autoimmune encephalomyelitis with altered myelin basic protein peptides involves different cellular mechanisms. J Neuroimmunol. 1997;74:149-58.
17. Katsara M, Yuriev E, Ramsland PA, Deraos G, Tselios T, Matsoukas J, et al. Mannosylation of mutated MBP83-99 peptides diverts immune responses from Th1 to Th2. Mol Immunol. 2008;45:3661-70.
18. Karin N, Mitchell DJ, Brocke S, Ling N, Steinman L. Reversal of experimental autoimmune encephalomyelitis by a soluble peptide variant of a myelin basic protein epitope: T cell receptor antagonism and reduction of interferon gamma and tumor necrosis factor alpha production. J Exp Med. 1994;180:2227-37.
19. Young DA, Lowe LD, Booth SS, Whitters MJ, Nicholson L, Kuchroo VK, et al. IL-4, IL-10, IL-13, and TGF-beta from an altered peptide ligand-specific Th2 cell clone down-regulate adoptive transfer of experimental autoimmune encephalomyelitis. J Immunol. 2000;164:3563-72.
20. Nicholson LB, Murtaza A, Hafler BP, Sette A, Kuchroo VK. A T cell receptor antagonist peptide induces T cells that mediate bystander suppression and prevent autoimmune encephalomyelitis induced with multiple myelin antigens. Proc Natl Acad Sci U S A. 1997;94:9279-84.
21. Nicholson LB, Greer JM, Sobel RA, Lees MB, Kuchroo VK. An altered peptide ligand mediates immune deviation and prevents autoimmune encephalomyelitis. Immunity. 1995;3:397-405.
22. Mantzourani ED, Tselios TV, Grdadolnik SG, Platts JA, Brancale A, Deraos GN, et al. Comparison of Proposed Putative Active Conformations of Myelin Basic Protein Epitope 87-99 Linear Altered Peptide Ligands by Spectroscopic and Modelling Studies: The Role of Positions 91 and 96 in T-Cell Receptor Activation. J Med Chem. 2006;49:6683-91.
23. Matsoukas J, Apostolopoulos V, Kalbacher H, Papini A-M, Tselios T, Chatzantoni K, et al. Design And Synthesis of a Novel Potent Myelin Basic Protein Epitope 87-99 Cyclic Analogue: Enhanced Stability and Biological Properties of Mimics Render Them a Potentially New Class of Immunomodulators†. J Med Chem. 2005;48:1470-80.
24. Tian DH, Perera CJ, Apostolopoulos V, Moalem-Taylor G. Effects of vaccination with altered peptide ligand on chronic pain in experimental autoimmune encephalomyelitis, an animal model of multiple sclerosis. Front Neurol. 2013;4:168.
25. Hauben E, Agranov E, Gothilf A, Nevo U, Cohen A, Smirnov I, et al. Posttraumatic therapeutic vaccination with modified myelin self-antigen prevents complete paralysis while avoiding autoimmune disease. J Clin Invest. 2001;108:591-9.
26. Lewitus GM, Wilf-Yarkoni A, Ziv Y, Shabat-Simon M, Gersner R, Zangen A, et al. Vaccination as a novel approach for treating depressive behavior. Biol Psychiatry. 2009;65:283-8.
27. Kobayashi H, Chattopadhyay S, Kato K, Dolkas J, Kikuchi S-i, Myers RR, et al. MMPs initiate Schwann cell-mediated MBP degradation and mechanical nociception after nerve damage. MolCell Neurosci. 2008;39:619-27.
28. Liu H, Shiryaev SA, Chernov AV, Kim Y, Shubayev I, Remacle AG, et al. Immunodominant fragments of myelin basic protein initiate T cell-dependent pain. J Neuroinflammation. 2012;9:119.
29. 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.
30. Raghavendra V, Tanga FY, DeLeo JA. Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur J Neurosci. 2004;20:467-73.
31. Gould KE, Swanborg RH. T and B cell responses to myelin basic protein and encephalitogenic epitopes. J Neuroimmunol. 1993;46:193-8.
32. Katsara M, Yuriev E, Ramsland PA, Tselios T, Deraos G, Lourbopoulos A, et al. Altered peptide ligands of myelin basic protein (MBP87-99) conjugated to reduced mannan modulate immune responses in mice. Immunology. 2009;128:521-33.
33. Moalem-Taylor G, Allbutt HN, Iordanova MD, Tracey DJ. Pain hypersensitivity in rats with experimental autoimmune neuritis, an animal model of human inflammatory demyelinating neuropathy. Brain Behav Immun. 2007;21:699-710.
34. Liu T, van Rooijen N, Tracey DJ. Depletion of macrophages reduces axonal degeneration and hyperalgesia following nerve injury. Pain. 2000;86:25-32.
35. Barclay J, Clark AK, Ganju P, Gentry C, Patel S, Wotherspoon G, et al. Role of the cysteine protease cathepsin S in neuropathic hyperalgesia. Pain. 2007;130:225-34.
36. Mert T, Gunay I, Ocal I, Guzel AI, Inal TC, Sencar L, et al. Macrophage depletion delays progression of neuropathic pain in diabetic animals. Naunyn Schmiedebergs Arch Pharmacol. 2009;379:445-52.
37. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci. 2009;29:13435-44.
38. Ibarra A, Sosa M, García E, Flores A, Cruz Y, Mestre H, et al. Prophylactic neuroprotection with A91 improves the outcome of spinal cord injured rats. Neurosci Lett. 2013;554:59-63.
39. Martiñon S, García E, Flores N, Gonzalez I, Ortega T, Buenrostro M, et al. Vaccination with a neural-derived peptide plus administration of glutathione improves the performance of paraplegic rats. Eur J Neurosci. 2007;26:403-12.
40. Sloan-Lancaster J, Shaw AS, Rothbard JB, Allen PM. Partial T cell signaling: altered phospho-zeta and lack of zap70 recruitment in APL-induced T cell anergy. Cell. 1994;79:913-22.
41. von Herrath MG, Harrison LC. Antigen-induced regulatory T cells in autoimmunity. Nat Rev Immunol. 2003;3:223-32.
42. McGuirk P, Mills KH. Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends Immunol. 2002;23:450-5.
43. Zhang X, Wu Z, Hayashi Y, Okada R, Nakanishi H. Peripheral role of cathepsin S in Th1 cell-dependent transition of nerve injury-induced acute pain to a chronic pain state. J Neurosci. 2014;34:3013-22.
44. Cao X, Cai SF, Fehniger TA, Song J, Collins LI, Piwnica-Worms DR, et al. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity. 2007;27:635-46.
45. Ydens E, Cauwels A, Asselbergh B, Goethals S, Peeraer L, Lornet G, et al. Acute injury in the peripheral nervous system triggers an alternative macrophage response. J Neuroinflammation. 2012;9:176.
46. Turtzo LC, Lescher J, Janes L, Dean DD, Budde MD, Frank JA. Macrophagic and microglial responses after focal traumatic brain injury in the female rat. J Neuroinflammation. 2014;11:82.
47. Hsieh CL, Kim CC, Ryba BE, Niemi EC, Bando JK, Locksley RM, et al. Traumatic brain injury induces macrophage subsets in the brain. Eur J Immunol. 2013;43:2010-22.
48. Wang G, Zhang J, Hu X, Zhang L, Mao L, Jiang X, et al. Microglia/macrophage polarization dynamics in white matter after traumatic brain injury. J Cereb Blood Flow Metab. 2013;33:1864-74.
49. Shechter R, London A, Varol C, Raposo C, Cusimano M, Yovel G, et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med. 2009;6:e1000113.
50. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol. 2009;27:451-83.
51. Weber MS, Prod'homme T, Youssef S, Dunn SE, Rundle CD, Lee L, et al. Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat Med. 2007;13:935-43.
52. Qin H, Yeh W-I, De Sarno P, Holdbrooks AT, Liu Y, Muldowney MT, et al. Signal transducer and activator of transcription-3/suppressor of cytokine signaling-3 (STAT3/SOCS3) axis in myeloid cells regulates neuroinflammation. Proc Natl Acad Sci. 2012;109:5004-9.
53. Clark AK, Gentry C, Bradbury EJ, McMahon SB, Malcangio M. Role of spinal microglia in rat models of peripheral nerve injury and inflammation. Eur J Pain. 2007;11:223-30.
54. Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maier SF, et al. Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain. 2005;115:71-83.
55. 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.
56. Zheng FY, Xiao WH, Bennett GJ. The response of spinal microglia to chemotherapy-evoked painful peripheral neuropathies is distinct from that evoked by traumatic nerve injuries. Neuroscience. 2011;176:447-54.
57. Gritsch S, Lu J, Thilemann S, Wortge S, Mobius W, Bruttger J, et al. Oligodendrocyte ablation triggers central pain independently of innate or adaptive immune responses in mice. Nat Commun. 2014;5:5472.
58. Ledeboer A, Jekich BM, Sloane EM, Mahoney JH, Langer SJ, Milligan ED, et al. Intrathecal interleukin-10 gene therapy attenuates paclitaxel-induced mechanical allodynia and proinflammatory cytokine expression in dorsal root ganglia in rats. Brain Behav Immun. 2007;21:686-98.
59. Mika J, Osikowicz M, Rojewska E, Korostynski M, Wawrzczak-Bargiela A, Przewlocki R, et al. Differential activation of spinal microglial and astroglial cells in a mouse model of peripheral neuropathic pain. Eur J Pharmacol. 2009;623:65-72.
60. Moalem-Taylor G, Li M, Allbutt H, Wu A, Tracey D. A preconditioning nerve lesion inhibits mechanical pain hypersensitivity following subsequent neuropathic injury. Molecular Pain. 2011;7:1.
61. Bileviciute-Ljungar I, Biella G, Bellomi P, Sotgiu ML. Contralateral treatment with lidocaine reduces spinal neuronal activity in mononeuropathic rats. Neurosci Lett. 2001;311:157-60.
62. Koltzenburg M, Wall PD, McMahon SB. Does the right side know what the left is doing? Trends Neurosci. 1999;22:122-7.
63. Kleinschnitz C, Brinkhoff J, Sommer C, Stoll G. Contralateral cytokine gene induction after peripheral nerve lesions: dependence on the mode of injury and NMDA receptor signaling. Brain Res Mol Brain Res. 2005;136:23-8.
64. Parkitny L, McAuley JH, Kelly PJ, Di Pietro F, Cameron B, Moseley GL. Multiplex cytokine concentration measurement: how much do the medium and handling matter? Mediators Inflamm. 2013;2013:890706.
65. Mika J, Korostynski M, Kaminska D, Wawrzczak-Bargiela A, Osikowicz M, Makuch W, et al. Interleukin-1alpha has antiallodynic and antihyperalgesic activities in a rat neuropathic pain model. Pain. 2008;138:587-97.
66. Hopkins SJ, Rothwell NJ. Cytokines and the nervous system. I: expression and recognition. Trends Neurosci. 1995;18:83-8.
67. Giulian D, Baker TJ, Shih LC, Lachman LB. Interleukin 1 of the central nervous system is produced by ameboid microglia. J Exp Med. 1986;164:594-604.
68. Okamoto K, Martin DP, Schmelzer JD, Mitsui Y, Low PA. Pro- and anti-inflammatory cytokine gene expression in rat sciatic nerve chronic constriction injury model of neuropathic pain. Exp Neurol. 2001;169:386-91.
69. Gillen C, Jander S, Stoll G. Sequential expression of mRNA for proinflammatory cytokines and interleukin-10 in the rat peripheral nervous system: comparison between immune-mediated demyelination and Wallerian degeneration. J Neurosci Res. 1998;51:489-96.
70. Liu L, Yang TM, Liedtke W, Simon SA. Chronic IL-1beta signaling potentiates voltage-dependent sodium currents in trigeminal nociceptive neurons. J Neurophysiol. 2006;95:1478-90.
71. Reeve AJ, Patel S, Fox A, Walker K, Urban L. Intrathecally administered endotoxin or cytokines produce allodynia, hyperalgesia and changes in spinal cord neuronal responses to nociceptive stimuli in the rat. Eur J Pain. 2000;4:247-57.
72. Sung CS, Wen ZH, Chang WK, Ho ST, Tsai SK, Chang YC, et al. Intrathecal interleukin-1beta administration induces thermal hyperalgesia by activating inducible nitric oxide synthase expression in the rat spinal cord. Brain Res. 2004;1015:145-53.
73. Zhang RX, Li A, Liu B, Wang L, Ren K, Zhang H, et al. IL-1ra alleviates inflammatory hyperalgesia through preventing phosphorylation of NMDA receptor NR-1 subunit in rats. Pain. 2008;135:232-9.
74. Wolf G, Gabay E, Tal M, Yirmiya R, Shavit Y. Genetic impairment of interleukin-1 signaling attenuates neuropathic pain, autotomy, and spontaneous ectopic neuronal activity, following nerve injury in mice. Pain. 2006;120:315-24.