Spinal cathepsin S and fractalkine contribute to chronic pain in the collagen-induced arthritis model

Arthritis and Rheumatism

Volumn 64, Issue 6, 2012, Pages 2038-2047

  Clark, Anna K ^a,c   Grist, John ^a   Al Kashi, Adam ^b   Perretti, Mauro ^b   Malcangio, Marzia ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN S; CATHEPSIN S INHIBITOR; COLLAGEN TYPE 2; FRACTALKINE; MORPHOLINUREA LEUCINEHOMOPHENYLALANINE VINYL SULFONE PHENYL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; ASTROCYTE; CHRONIC PAIN; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; IMMUNIZATION; LYMPHOCYTIC INFILTRATION; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD;

ANIMALS; ANTIBODIES, NEUTRALIZING; ARTHRITIS, EXPERIMENTAL; CATHEPSINS; CHEMOKINE CX3CL1; CHRONIC PAIN; DIPEPTIDES; FEMALE; HYPERALGESIA; MICROGLIA; NEURONS; RATS; RATS, INBRED LEW; SPINAL CORD; SULFONES;

EID: 84861804692     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.34351     Document Type: Article

References (47)

1. Trentham DE,. Collagen arthritis as a relevant model for rheumatoid arthritis: evidence pro and con. Arthritis Rheum 1982; 25: 911-6.
2. Williams RO,. Collagen-induced arthritis as a model for rheumatoid arthritis. Methods Mol Med 2004; 98: 207-16.
3. Inglis JJ, Notley CA, Essex D, Wilson AW, Feldmann M, Anand P, et al. Collagen-induced arthritis as a model of hyperalgesia: functional and cellular analysis of the analgesic actions of tumor necrosis factor blockade. Arthritis Rheum 2007; 56: 4015-23.
4. Christianson CA, Corr M, Firestein GS, Mobargha A, Yaksh TL, Svensson CI,. Characterization of the acute and persistent pain state present in K/BxN serum transfer arthritis. Pain 2010; 151: 394-403.
5. Schaible HG, Richter F, Ebersberger A, Boettger MK, Vanegas H, Natura G, et al. Joint pain. Exp Brain Res 2009; 196: 153-62.
6. McMahon SB, Malcangio M,. Current challenges in glia-pain biology. Neuron 2009; 64: 46-54.
7. Sweitzer SM, Hickey WF, Rutkowski MD, Pahl JL, DeLeo JA,. Focal peripheral nerve injury induces leukocyte trafficking into the central nervous system: potential relationship to neuropathic pain. Pain 2002; 100: 163-70.
8. + T lymphocytes contribute to murine spinal nerve transection-induced neuropathic pain. Eur J Immunol 2008; 38: 448-58.
9. Leger T, Grist J, D'Acquisto F, Clark AK, Malcangio M,. Glatiramer acetate attenuates neuropathic allodynia through modulation of adaptive immune cells. J Neuroimmunol 2011; 234: 19-26.
10. Clark AK, Yip PK, Grist J, Gentry C, Staniland AA, Marchand F, et al. Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain. Proc Natl Acad Sci U S A 2007; 104: 10655-60.
11. Clark AK, Marchand F, D'Auria M, Davies M, Grist J, Malcangio M, et al. Cathepsin S inhibiton attenuates neuropathic pain and microglial response associated with spinal cord injury. The Open Pain Journal 2010; 3: 117-22.
12. Clark AK, Yip PK, Malcangio M,. The liberation of fractalkine in the dorsal horn requires microglial cathepsin S. J Neurosci 2009; 29: 6945-54.
13. Ruth JH, Volin MV, Haines GK III, Woodruff DC, Katschke KJ Jr, Woods JM, et al. Fractalkine, a novel chemokine in rheumatoid arthritis and in rat adjuvant-induced arthritis. Arthritis Rheum 2001; 44: 1568-81.
14. Nanki T, Imai T, Nagasaka K, Urasaki Y, Nonomura Y, Taniguchi K, et al. Migration of CX3CR1-positive T cells producing type 1 cytokines and cytotoxic molecules into the synovium of patients with rheumatoid arthritis. Arthritis Rheum 2002; 46: 2878-83.
15. Nakagawa TY, Brissette WH, Lira PD, Griffiths RJ, Petrushova N, Stock J, et al. Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 1999; 10: 207-17.
16. Biroc SL, Gay S, Hummel K, Magill C, Palmer JT, Spencer DR, et al. Cysteine protease activity is up-regulated in inflamed ankle joints of rats with adjuvant-induced arthritis and decreases with in vivo administration of a vinyl sulfone cysteine protease inhibitor. Arthritis Rheum 2001; 44: 703-11.
17. Pozgan U, Caglic D, Rozman B, Nagase H, Turk V, Turk B,. Expression and activity profiling of selected cysteine cathepsins and matrix metalloproteinases in synovial fluids from patients with rheumatoid arthritis and osteoarthritis. Biol Chem 2010; 391: 571-9.
18. Nanki T, Urasaki Y, Imai T, Nishimura M, Muramoto K, Kubota T, et al. Inhibition of fractalkine ameliorates murine collagen-induced arthritis. J Immunol 2004; 173: 7010-6.
19. Paul-Clark MJ, Mancini L, Del Soldato P, Flower RJ, Perretti M,. Potent antiarthritic properties of a glucocorticoid derivative, NCX-1015, in an experimental model of arthritis. Proc Natl Acad Sci U S A 2002; 99: 1677-82.
20. Mancini L, Paul-Clark MJ, Rosignoli G, Hannon R, Martin JE, Macintyre I, et al. Calcitonin and prednisolone display antagonistic actions on bone and have synergistic effects in experimental arthritis. Am J Pathol 2007; 170: 1018-27.
21. Clark AK, D'Aquisto F, Gentry C, Marchand F, McMahon SB, Malcangio M,. Rapid co-release of interleukin 1β and caspase 1 in spinal cord inflammation. J Neurochem 2006; 99: 868-80.
22. Clark AK, Staniland AA, Marchand F, Kaan TK, McMahon SB, Malcangio M,. P2X7-dependent release of interleukin-1β and nociception in the spinal cord following lipopolysaccharide. J Neurosci 2010; 30: 573-82.
23. 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.
24. Zimmermann M,. Pathobiology of neuropathic pain. Eur J Pharmacol 2001; 429: 23-37.
25. Costigan M, Scholz J, Woolf CJ,. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu Rev Neurosci 2009; 32: 1-32.
26. Svensson CI, Marsala M, Westerlund A, Calcutt NA, Campana WM, Freshwater JD, et al. Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J Neurochem 2003; 86: 1534-44.
27. 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.
28. Staniland AA, Clark AK, Wodarski R, Sasso O, Maione F, D'Acquisto F, et al. Reduced inflammatory and neuropathic pain and decreased spinal microglial response in fractalkine receptor (CX3CR1) knockout mice. J Neurochem 2010; 114: 1143-57.
29. Sokka T, Kautiainen H, Toloza S, Makinen H, Verstappen SM, Lund Hetland M, et al. QUEST-RA: quantitative clinical assessment of patients with rheumatoid arthritis seen in standard rheumatology care in 15 countries. Ann Rheum Dis 2007; 66: 1491-6.
30. Kidd BL, Langford RM, Wodehouse T,. Arthritis and pain: current approaches in the treatment of arthritic pain. Arthritis Res Ther 2007; 9: 214.
31. Dray A,. New horizons in pharmacologic treatment for rheumatic disease pain. Rheum Dis Clin North Am 2008; 34: 481-505.
32. Olechowski CJ, Truong JJ, Kerr BJ,. Neuropathic pain behaviours in a chronic-relapsing model of experimental autoimmune encephalomyelitis (EAE). Pain 2009; 141: 156-64.
33. Clark AK, Malcangio M,. Microglial signalling mechanisms: cathepsin S and fractalkine. Exp Neurol 2012; 234: 283-92.
34. 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.
35. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, Miki K, et al. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol Cell Neurosci 2000; 15: 170-82.
36. Andersson AK, Li C, Brennan FM,. Recent developments in the immunobiology of rheumatoid arthritis. Arthritis Res Ther 2008; 10: 204.
37. Notley CA, McCann FE, Inglis JJ, Williams RO,. Anti-CD3 therapy expands the numbers of CD4+ and CD8+ Treg cells and induces sustained amelioration of collagen-induced arthritis. Arthritis Rheum 2010; 62: 171-8.
38. 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.
39. Boyle DL, Jones TL, Hammaker D, Svensson CI, Rosengren S, Albani S, et al. Regulation of peripheral inflammation by spinal p38 MAP kinase in rats. PLoS Med 2006; 3: e338.
40. Hess A, Axmann R, Rech J, Finzel S, Heindl C, Kreitz S, et al. Blockade of TNF-α rapidly inhibits pain responses in the central nervous system. Proc Natl Acad Sci U S A 2011; 108: 3731-6.
41. Williams RO, Feldmann M, Maini RN,. Anti-tumor necrosis factor ameliorates joint disease in murine collagen-induced arthritis. Proc Natl Acad Sci U S A 1992; 89: 9784-8.
42. Feldmann M, Maini RN,. TNF defined as a therapeutic target for rheumatoid arthritis and other autoimmune diseases. Nat Med 2003; 9: 1245-50.
43. Riese RJ, Mitchell RN, Villadangos JA, Shi GP, Palmer JT, Karp ER, et al. Cathepsin S activity regulates antigen presentation and immunity. J Clin Invest 1998; 101: 2351-63.
44. Podolin PL, Bolognese BJ, Carpenter DC, Davis TG, Johanson RA, Fox JH, et al. Inhibition of invariant chain processing, antigen-induced proliferative responses, and the development of collagen-induced arthritis and experimental autoimmune encephalomyelitis by a small molecule cysteine protease inhibitor. J Immunol 2008; 180: 7989-8003.
45. Baugh M, Black D, Westwood P, Kinghorn E, McGregor K, Bruin J, et al. Therapeutic dosing of an orally active, selective cathepsin S inhibitor suppresses disease in models of autoimmunity. J Autoimmun 2011; 36: 201-9.
46. Murphy G, Caplice N, Molloy M,. Fractalkine in rheumatoid arthritis: a review to date. Rheumatology (Oxford) 2008; 47: 1446-51.
47. Clark AK, Staniland AA, Malcangio M,. Fractalkine/CX3CR1 signalling in chronic pain and inflammation. Curr Pharm Biotechnol 2011; 12: 1707-14.