Fractalkine/CX3CR1 signalling in chronic pain and inflammation

Current Pharmaceutical Biotechnology

Volumn 12, Issue 10, 2011, Pages 1707-1714

  Clark, Anna K ^a   Staniland, Amelia A ^a   Malcangio, Marzia ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Atherosclerosis; Chronic pain; Fractalkine CX3CR1

Indexed keywords

ACETYLSALICYLIC ACID; ADAM10 ENDOPEPTIDASE; APOLIPOPROTEIN E; CATHEPSIN S; CHEMOKINE RECEPTOR ANTAGONIST; CHEMOKINE RECEPTOR CX3CR1; DISEASE MODIFYING ANTIRHEUMATIC DRUG; FRACTALKINE; FRACTALKINE ANTIBODY; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA INHIBITOR; INTERLEUKIN 6; METHOTREXATE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCLONAL ANTIBODY; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PROTEIN INHIBITOR; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; UNCLASSIFIED DRUG;

ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CHEMOTAXIS; CHRONIC PAIN; DISEASE COURSE; DRUG MEGADOSE; ENDOTHELIUM CELL; HOMEOSTASIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFLAMMATION; LEUKOCYTE; LYMPHOCYTE; MICROGLIA; NERVE CELL; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PATHOGENESIS; PERIPHERAL NERVE; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS;

EID: 80053478471     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920111798357465     Document Type: Review

References (77)

1. Bajetto, A.; Bonavia, R.; Barbero, S.; Schettini, G. Characterization of chemokines and their receptors in the central nervous system, physiopathological implications. J. Neurochem., 2002, 82, 1311-1329.
2. Murphy, P.M.; Baggiolini, M.; Charo, I.F.; Hebert, C.A.; Horuk, R.; Matsushima, K.; Miller, L.H.; Oppenheim, J.J.; Power, C.A. International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol. Rev., 2000, 52,145-176.
3. Bazan, J.F.; Bacon, K.B.; Hardiman, G.; Wang, W.; Soo, K.; Rossi, D.; Greaves, D.R.; Zlotnik, A.; Schall, T.J. A new class of membrane-bound chemokine with a CX3C motif. Nature, 1997, 385, 640-644.
4. Pan, Y.; Lloyd, C.; Zhou, H.; Dolich, S.; Deeds, J.; Gonzalo, J.A.; Vath, J.; Gosselin, M.; Ma, J.; Dussault, B.; Woolf, E.; Alperin, G.; Culpepper, J.; Gutierrez-Ramos, J.C.; Gearing, D. Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature, 1997, 387, 611-617.
5. Hundhausen, C.; Schulte, A.; Schulz, B.; Andrzejewski, M.G.; Schwarz, N.; von Hundelshausen, P.; Winter, U.; Paliga, K.; Reiss, K.; Saftig, P.; Weber, C.; Ludwig, A. Regulated shedding of transmembrane chemokines by the disintegrin and metalloproteinase 10 facilitates detachment of adherent leukocytes. J. Immunol., 2007, 178, 8064-8072.
6. Garton, K. J.; Gough, P. J.; Blobel, C. P.; Murphy, G.; Greaves, D. R.; Dempsey, P. J.; Raines, E.W. Tumor necrosis factor-alphaconverting enzyme (ADAM17) mediates the cleavage and shedding of fractalkine (CX3CL1). J. Biol. Chem., 2001, 276,37993-38001.
7. Clark, A.K.; Yip, P.K.; Grist, J.; Gentry, C.; Staniland, A.A.; Marchand, F.; Dehvari, M.; Wotherspoon, G.; Winter, J.; Ullah, J.; Bevan, S.; Malcangio, M. Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain. Proc. Nat. Acad. Sci. USA, 2007, 104,10655-10660.
8. Clark, A. K.; Yip, P. K.; Malcangio, M. The liberation of fractalkine in the dorsal horn requires microglial cathepsin S. J. Neurosci., 2009, 29, 6945-6954.
9. Schwaeble, W. J.; Stover, C. M.; Schall, T. J.; Dairaghi, D. J.; Trinder, P. K. E.; Linington, C.; Iglesias, A.; Schubart, A.; Lynch, N. J.; Weihe, E.; Schafer, M. K. Neuronal expression of fractalkine in the presence and absence of inflammation. FEBS Lett., 1998, 439,203-207.
10. Sunnemark, D.; Eltayeb, S.; Nilsson, M.; Wallstrom, E.; Lassmann, H.; Olsson, T.; Berg, A.L.; Ericsson-Dahlstrand, A. CX3CL1 (fractalkine) and CX3CR1 expression in myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis, kinetics and cellular origin. J. Neuroinflam., 2005, 17, 17.
11. Hughes, P.M.; Botham, M.S.; Frentzel, S.; Mir, A.; Perry, V.H. Expression of fractalkine (CX3CL1) and its receptor, CX3CR1, during acute and chronic inflammation in the rodent CNS. Glia, 2002, 37,314-327.
12. Verge, G.M.; Milligan, E.D.; Maier, S.F.; Watkins, L.R.; Naeve, G.S.; Foster, A.C. Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur. J. Neurosci., 2004, 20,1150-1160.
13. Lindia, J.A.; McGowan, E.; Jochnowitz, N.; Abbadie, C. Induction of CX3CL1 expression in astrocytes and CX3CR1 in microglia in the spinal cord of a rat model of neuropathic pain. J. Pain, 2005, 6,434-438.
14. Imai, T.; Hieshima, K.; Haskell, C.; Baba, M.; Nagira, M.; Nishimura, M.; Kakizaki, M.; Takagi, S.; Nomiyama, H.; Schall, T.J.; Yoshie, O. Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell, 1997, 91,521-530.
15. Combadiere, C.; Salzwedel, K.; Smith, E.D.; Tiffany, H.L.; Berger, E.A.; Murphy, P.M. Identification of CX3CR1. a chemotactic receptor for the human CX3C chemokine fractalkine and a fusion coreceptor for HIV-1. J. Biol. Chem., 1998, 273,23799-23804.
16. Harrison, J.K.; Jiang, Y.; Chen S.,; Xia, Y.; Maciejewski, D.; McNamara, R.K.; Streit, W.J.; Salafranca, M.N.; Adhikari, S.; Thompson, D.A.; Botti, P.; Bacon, K.B.; Feng, L. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natal. Acad. Ssi. USA, 1998, 95,10896-10901.
17. Geissmann, F.; Jung, S.; Littman, D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity, 2003, 19, 71-82.
18. Abbadie, C.; Bhangoo, S.; De, K.Y.; Malcangio, M.; Melik-Parsadaniantz, S.; White, F.A. Chemokines and pain mechanisms. Brain Res. Rev., 2009, 60,125-134.
19. Milligan, E.D.; Sloane, E.M.; Watkins, L.R. Glia in pathological pain, A role for fractalkine. J. Neuroimmunol, 2008, 198,113-120.
20. Nishiyori, A.; Minami, M.; Ohtani, Y.; Takami, S.; Yamamoto, J.; Kawaguchi, N.; Kume, T.; Akaike, A.; Satoh, M. Localization of fractalkine and CX3CR1 mRNAs in rat brain, does fractalkine play a role in signaling from neuron to microglia? FEBS Lett., 1998, 429,167-172.
21. Zhuang, Z.Y.; Kawasaki, Y.; Tan, P.H.; Wen, Y.R.; Huang, J.; Ji, R.R. Role of the CX3CR1/p38 MAPK pathway in spinal microglia for the development of neuropathic pain following nerve injuryinduced cleavage of fractalkine. Brain, Behavior, Immunity, 2007, 21,642-651.
22. Holmes, F.E.; Arnott, N.; Vanderplank, P.; Kerr, N.C.; Longbrake, E.E.; Popovich, P.G.; Imai, T.; Combadiere, C.; Murphy, P.M.; Wynick, D. Intra-neural administration of fractalkine attenuates neuropathic pain-related behaviour. J. Neurochem., 2008, 106,640-649.
23. Staniland, A.A.; Clark, A.K.; Wodarski, R.; Sasso, O.; Maione, F.; D'Acquisto, F.; Malcangio, M. Reduced inflammatory and neuropathic pain and decreased spinal microglial response in fractalkine receptor (CX3CR1) knockout mice. J. Neurochem., 2010, 114, 1143-1157.
24. Milligan, E.D.; Zapata, V.; Chacur, M.; Schoeniger, D.; Biedenkapp, J.; O'Connor, K.A.; Verge, G.M.; Chapman, G.; Green, P.; Foster, A.C.; Naeve, G.S.; Maier, S.F.; Watkins, L.R. Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats. Eur. J. Neuroscience, 2004, 20, 2294-2302.
25. Milligan, E.; Zapata, V.; Schoeniger, D.; Chacur, M.; Green, P.; Poole, S.; Martin, D.; Maier, S.F.; Watkins, L.R. An initial investigation of spinal mechanisms underlying pain enhancement induced by fractalkine, a neuronally released chemokine. Eur. J. Neuroscience, 2005, 22, 2775-2782.
26. Cardona, A.E.; Pioro, E.P.; Sasse, M.E.; Kostenko, V.; Cardona, S.M.; Dijkstra, I.M.; Huang, D.; Kidd, G.; Dombrowski, S.; Dutta, R.; Lee, J.C.; Cook, D.N.; Jung, S.; Lira, S.A.; Littman, D.R.; Ransohoff, R.M. Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci., 2006, 9,917-924.
27. Owolabi, S.A.; Saab, C.Y. Fractalkine and minocycline alter neuronal activity in the spinal cord dorsal horn. FEBS Lett., 2006, 580,4306-4310.
28. Mogil, J.S.; Wilson, S.G.; Bon, K.; Lee, S.E.; Chung, K.; Raber, P.; Pieper, J.O.; Hain, H.S.; Belknap, J.K.; Hubert, L.; Elmer, G.I.; Chung, J.M.; Devor, M. Heritability of nociception I, responses of 11 inbred mouse strains on 12 measures of nociception. Pain, 1999, 80, 67-82.
29. Kigerl, K.A.; McGaughy, V.M.; Popovich, P.G. Comparative analysis of lesion development and intraspinal inflammation in four strains of mice following spinal contusion injury. J. Compu. Neurol., 2006, 494,578-594.
30. Yasuda, Y.; Shimoda, T.; Uno, K.; Tateishi, N.; Furuya, S.; Yagi, K.; Suzuki, K.; Fujita, S. The effects of MPTP on the activation of microglia/astrocytes and cytokine/chemokine levels in different mice strains. J. Neuroimmunol., 2008, 204,43-51.
31. Hurst, L.A.; Bunning, R.A.D.; Couraud, P.O.; Romero, I.A.; Weksler, B.B.; Sharrack, B.; Woodroofe, M.N. Expression of ADAM-17, TIMP-3 and fractalkine in the human adult brain endothelial cell line, hCMEC/D3, following pro-inflammatory cytokine treatment. J. Neuroimmunol., 2009, 210,108-112.
32. Springer, T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration. The multistep paradigm. Cell, 1994, 76,301-314.
33. Fong, A.M.; Robinson, L.A.; Steeber, D.A.; Tedder, T.F.; Yoshie, O.; Imai, T.; Patel, D.D. fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, and activation under physiologic flow. J.Exp.Med., 1998, 188,1413-1419.
34. Yoneda, O.; Imai, T.; Goda, S.; Inoue, H.; Yamauchi, A.; Okazaki, T.; Imai, H.; Yoshie, O.; Bloom, E.T.; Domae, N.; Umehara, H. Fractalkine-mediated endothelial cell injury by NK cells. J. Immunol., 2000, 164, 4055-4062.
35. Fong, A.M.; Erickson, H.P.; Zachariah, J.P.; Poon, S.; Schamberg, N.J.; Imai, T.; Patel, D.D. Ultrastructure and function of the fractalkine mucin domain in CX3C chemokine domain presentation. J. Biol. Chem., 2000, 275,3781-3786.
36. Papadopoulos, E.J.; Fitzhugh, D.J.; Tkaczyk, C.; Gilfillan, A.M.; Sassetti, C.; Metcalfe, D.D.; Hwang, S.T. Mast cells migrate, but do not degranulate, in response to fractalkine, a membrane-bound chemokine expressed constitutively in diverse cells of the skin. Eur.J. Immunol., 2000, 30, 2355-2361.
37. Maciejewski, D.; Chen, S.; Feng, L.; Maki, R.; Bacon, K.B. Characterization of fractalkine in rat brain cells, migratory and activation signals for CX3CR-1-expressing microglia. J. Immunol., 1999, 163,1628-1635.
38. Ransohoff, R.M. Chemokines in neurological disease models, correlation between chemokine expression patterns and inflammatory pathology. J. Leukoc. Biol., 1997, 62,645-652.
39. Koziolek, M.J.; Vasko, R.; Bramlage, C.; Muller, G.A.; Strutz, F. The CX(3)C-chemokine fractalkine in kidney diseases. Mini. Rev. Med. Chem., 2009, 9,1215-1228.
40. Nishimura, M.; Kuboi, Y.; Muramoto, K.; Kawano, T.; Imai, T. Chemokines as novel therapeutic targets for inflammatory bowel disease. Ann. N.Y. Acad. Sci., 2009, 1173, 350-356.
41. Kasama, T.; Wakabayashi, K.; Sato, M.; Takahashi, R.; Isozaki, T. Relevance of the CX3CL1/fractalkine-CX3CR1 pathway in vasculitis and vasculopathy. Transl. Res., 2010, 155,20-26.
42. Glass, C.K.; Witztum, J. L. Atherosclerosis. the road ahead. Cell, 2001, 104,503-516.
43. Harrison, J.K.; Jiang, Y.; Wees, E.A.; Salafranca, M.N.; Liang, H.X.; Feng, L.; Belardinelli, L. Inflammatory agents regulate in vivo expression of fractalkine in endothelial cells of the rat heart. J. Leukoc. Biol., 1999, 66,937-944.
44. Lucas, A.D.; Bursill, C.; Guzik, T.J.; Sadowski, J.; Channon, K.M.; Greaves, D.R. Smooth muscle cells in human atherosclerotic plaques express the fractalkine receptor CX3CR1 and undergo chemotaxis to the CX3C chemokine fractalkine (CX3CL1). Circulation, 2003, 108,2498-2504.
45. Faure, S.; Meyer, L.; Costagliola, D.; Vaneensberghe, C.; Genin, E.; Autran, B.; Delfraissy, J.F.; McDermott, D.H.; Murphy, P.M.; Debre, P.; Theodorou, I.; Combadiere, C. Rapid progression to AIDS in HIV+ individuals with a structural variant of the chemokine receptor CX3CR1. Science, 2000, 287,2274-2277.
46. Moatti, D.; Faure, S.; Fumeron, F.; Amara, M.E.W.; Seknadji, P.; McDermott, D.H.; Debre, P.; Aumont, M.C.; Murphy, P.M.; de Prost, D.; Combadiere, C. Polymorphism in the fractalkine receptor CX3CR1 as a genetic risk factor for coronary artery disease. Blood, 2001, 97,1925-1928.
47. McDermott, D.H.; Halcox, J.P.J.; Schenke, W.H.; Waclawiw, M.A.; Merrell, M.N.; Epstein, N.; Quyyumi, A.A.; Murphy, P.M. Association between polymorphism in the chemokine receptor CX3CR1 and coronary vascular endothelial dysfunction and atherosclerosis. Circ. Res., 2001, 89,401-407.
48. McDermott, D.H.; Fong, A.M.; Yang, Q.; Sechler, J.M.; Cupples, L.A.; Merrell, M.N.; Wilson, P.W.; D'Agostino, R.B.; O'Donnell, C.J.; Patel, D.D.; Murphy, P.M. Chemokine receptor mutant CX3CR1-M280 has impaired adhesive function and correlates with protection from cardiovascular disease in humans. J. Clin. Invest., 2003, 111,1241-1250.
49. Wong, B.W.; Wong, D.; McManus, B.M. Characterization of fractalkine (CX3CL1) and CX3CR1 in human coronary arteries with native atherosclerosis, diabetes mellitus, and transplant vascular disease. Cardiovasc. Pathol., 2002, 11,332-338.
50. Chandrasekar, B.; Mummidi, S.; Perla, R.P.; Bysani, S.; Dulin, N.O.; Liu, F.; Melby, P.C. Fractalkine (CX3CL1) stimulated by nuclear factor kappaB (NF-kappaB)-dependent inflammatory signals induces aortic smooth muscle cell proliferation through an autocrine pathway. Biochem.J., 2003, 373,547-558.
51. White, G.E.; Tan, T.C.C.; John, A.E.; Whatling, C.; McPheat, W.L.; Greaves, D.R. Fractalkine has anti-apoptotic and proliferative effects on human vascular smooth muscle cells via epidermal growth factor receptor signalling. Cardiovasc. Res., 2010, 85, 825-835.
52. Huo, Y.; Schober, A.; Forlow, S.B.; Smith, D.F.; Hyman, M.C.; Jung, S.; Littman, D.R.; Weber, C.; Ley, K. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat. Med., 2003, 9,61-67.
53. Schafer, A.; Schulz, C.; Eigenthaler, M.; Fraccarollo, D.; Kobsar, A.; Gawaz, M.; Ertl, G.; Walter, U.; Bauersachs, J. Novel role of the membrane-bound chemokine fractalkine in platelet activation and adhesion. Blood, 2004, 103,407-412.
54. Lesnik, P.; Haskell, C.A.; Charo, I.F. Decreased atherosclerosis in CX3CR1-/-mice reveals a role for fractalkine in atherogenesis. J. Clin. Invest., 2003, 111,333-340.
55. Combadiere, C.; Potteaux, S.; Gao, J.L.; Esposito, B.; Casanova, S.; Lee, E.J.; Debre, P.; Tedgui, A.; Murphy, P.M.; Mallat, Z. Decreased atherosclerotic lesion formation in CX3CR1/apolipoprotein E double knockout mice. Circulation, 2003, 107,1009-1016.
56. Liu, H.; Jiang, D.; Zhang, S.; Ou, B. Aspirin inhibits fractalkine expression in atherosclerotic plaques and reduces atherosclerosis in ApoE gene knockout mice. cardiovasc Drugs Ther., 2009, 24,17-24
57. Landsman, L.; Bar-On, L.; Zernecke, A.; Kim, K.W.; Krauthgamer, R.; Shagdarsuren, E.; Lira, S.A.; Weissman, I.L.; Weber, C.; Jung, S. CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood, 2009, 113, 963-972.
58. Majithia, V.; Geraci, S.A. Rheumatoid arthritis, diagnosis and management. The Am. J. Med., 2007, 120, 936-939.
59. Iwamoto, T.; Okamoto, H.; Toyama, Y.; Momohara, S. Molecular aspects of rheumatoid arthritis, chemokines in the joints of patients. FEBS J., 2008, 275, 4448-4455.
60. Kinne, R.W.; Brauer, R.; Stuhlmuller, B.; Palombo-Kinne, E.; Burmester, G.R. Macrophages in rheumatoid arthritis. Arthritis Res., 2000, 2,189-202.
61. Murphy, G.; Caplice, N.; Molloy, M. Fractalkine in rheumatoid arthritis, a review to date. Rheumatology, 2008, 47,1446-1451.
62. Ruth, J.H.; Volin, M.V.; Haines, G.K. III.; Woodruff, D.C.; Katschke, K.J. Jr.; Woods, J.M.; Park, C.C.; Morel, J.C.; Koch, A.E. Fractalkine, a novel chemokine in rheumatoid arthritis and in rat adjuvant-induced arthritis. Arthritis Rheum., 2001, 44,1568-1581.
63. Blaschke, S.; Koziolek, M.; Schwarz, A.; Benohr, P.; Middel, P.; Schwarz, G.; Hummel, K.M.; Muller, G.A. Proinflammatory role of fractalkine (CX3CL1) in rheumatoid arthritis. J. Rheumatol., 2003, 30,1918-1927.
64. Konttinen, Y.T.; Ainola, M.; Valleala, H.; Ma, J.; Ida, H.; Mandelin, J.; Kinne, R.W.; Santavirta, S.; Sorsa, T.; Lopez-Otin, C.; Takagi, M. Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane, different profiles in trauma and rheumatoid arthritis. Ann. Rheum. Dis., 1999, 58,691-697.
65. Volin, M.V.; Woods, J.M.; Amin, M.A.; Connors, M.A.; Harlow, L.A.; Koch, A.E. Fractalkine, A novel angiogenic chemokine in rheumatoid arthritis. Am. J. Pathol., 2001, 159,1521-1530.
66. Szekanecz, Z.; Pakozdi, A.; Szentpetery, A.; Besenyei, T.; Koch, A.E. Chemokines and angiogenesis in rheumatoid arthritis. Front Biosci.,(Elite.Ed), 2009, 1,44-51.
67. Nanki, T.; Imai, T.; Nagasaka, K.; Urasaki, Y.; Nonomura, Y.; Taniguchi, K.; Hayashida, K.; Hasegawa, J.; Yoshie, O.; Miyasaka, N. 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, 2878-2883.
68. Sawai, H.; Park, Y.W.; He, X.; Goronzy, J.J.; Weyand, C.M. Fractalkine mediates T cell-dependent proliferation of synovial fibroblasts in rheumatoid arthritis. Arthritis Rheum. 2007, 56, 3215-3225.
69. Sawai, H.; Park, Y.W.; Roberson, J.; Imai, T.; Goronzy, J.J.; Weyand, C.M. T cell costimulation by fractalkine-expressing synoviocytes in rheumatoid arthritis. Arthritis Rheum., 2005, 52,1392-1401.
70. Ruth, J.H.; Rottman, J.B.; Katschke, K.J. Jr.; Qin, S.; Wu, L.; LaRosa, G.; Ponath, P.; Pope, R.M.; Koch, A.E. Selective lymphocyte chemokine receptor expression in the rheumatoid joint. Arthritis Rheum., 2001, 44,2750-2760.
71. Yano, R.; Yamamura, M.; Sunahori, K.; Takasugi, K.; Yamana, J.; Kawashima, M.; Makino, H. Recruitment of CD16+ monocytes into synovial tissues is mediated by fractalkine and CX3CR1 in rheumatoid arthritis patients. Acta Med. Okayama, 2007, 61,89-98.
72. Koizumi, K.; Saitoh, Y.; Minami, T.; Takeno, N.; Tsuneyama, K.; Miyahara, T.; Nakayama, T.; Sakurai, H.; Takano, Y.; Nishimura, M.; Imai, T., Yoshie, O.; Saiki, I. Role of CX3CL1/fractalkine in osteoclast differentiation and bone resorption. J. Immunol., 2009, 183,7825-7831.
73. Nanki, T.; Urasaki, Y.; Imai, T.; Nishimura, M.; Muramoto, K.; Kubota, T.; Miyasaka, N. Inhibition of fractalkine ameliorates murine collagen-induced arthritis. J. Immunol., 2004, 173,7010-7016.
74. Odai, T.; Matsunawa, M.; Takahashi, R.; Wakabayashi, K.; Isozaki, T.; Yajima, N.; Miwa, Y.; Kasama, T. Correlation of CX3CL1 and CX3CR1 levels with response to infliximab therapy in patients with rheumatoid arthritis. J. Rheumatol., 2009, 36,1158-1165.
75. Pingiotti, E.; Cipriani, P.; Marrelli, A.; Liakouli, V.; Fratini, S.; Penco, M.; Giacomelli, R. Surface expression of fractalkine receptor (CX3CR1) on CD4+/CD28 T cells in RA patients and correlation with atherosclerotic damage. Ann. N.Y. Acad. Sci., 2007, 1107, 32-41.
76. Inglis, J.J.; Notley, C.A.; Essex, D.; Wilson, A.W.; Feldmann, M.; Anand, P.; Williams, R. Collagen-induced arthritis as a model of hyperalgesia, functional and cellular analysis of the analgesic actions of tumor necrosis factor blockade. Arthritis Rheum., 2007, 56,4015-4023.
77. Dorgham, K.; Ghadiri, A.; Hermand, P.; Rodero, M.; Poupel, L.; Iga, M.; Hartley, O.; Gorochov, G.; Combadiere, C.; Deterre, P. An engineered CX3CR1 antagonist endowed with anti-inflammatory activity. J. Leukoc. Biol., 2009, 86, 903-911.