Elevated expression of fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) in the dorsal root ganglia and spinal cord in experimental autoimmune encephalomyelitis: Implications in multiple sclerosis-induced neuropathic pain

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Zhu, Wenjun ^a   Acosta, Crystal ^a   Macneil, Brian ^b   Cortes, Claudia ^a   Intrater, Howard ^b   Gong, Yuewen ^a   Namaka, Mike ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; CHEMOKINE RECEPTOR; CX3CL1 PROTEIN, RAT; CX3CR1 PROTEIN, RAT;

ALLERGIC ENCEPHALOMYELITIS; ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CHRONIC PAIN; CONTROLLED STUDY; DISABILITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GLIA CELL; GRAY MATTER; HYPOALGESIA; MACROPHAGE; MICROGLIA; MULTIPLE SCLEROSIS; NEUROLOGIC DISEASE; NEUROPATHIC PAIN; NONHUMAN; PROTEIN EXPRESSION; RAT; SPINAL CORD; SPINAL GANGLION; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEURALGIA; PATHOLOGY;

ANIMALS; CHEMOKINE CX3CL1; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; HUMANS; MICROGLIA; MULTIPLE SCLEROSIS; NEURALGIA; RATS; RECEPTORS, CHEMOKINE; RNA, MESSENGER;

EID: 84885659367     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/480702     Document Type: Article

References (54)

1. Namaka M. P., Ethans K., Jensen B., Esfahani F., Frost E. E., Multiple sclerosis. Therapeutic Choices/e-Therapeutic 2011 Ottawa, Canada Canadian Pharmacists Association 309 319
2. Acosta C. M. R., Cortes C., Macphee H., Namaka M. P., Exploring the role of nerve growth factor in multiple sclerosis: implications in myelin repair. CNS & Neurological Disorders. In press
3. Zhu W., Le Dorze J. A., Prout M., Frost E. E., Namaka M. P., An overview of Relapsing Remitting Multiple Sclerosis (RRMS) and current treatment options. Pharmacy Practice 2010 9
4. Tullman M. J., Overview of the epidemiology, diagnosis, and disease progression associated with multiple sclerosis. American Journal of Managed Care 2013 19 supplement 2 s15 s20
5. Begum F., Zhu W., Cortes C., Macneil B., Namaka M., Elevation of tumor necrosis factor alpha in dorsal root ganglia and spinal cord is associated with neuroimmune modulation of pain in an animal model of multiple sclerosis. Journal of NeuroImmune Pharmacology 2013 8 3 677 690
6. Ransohoff R. M., Chemokines and chemokine receptors: standing at the crossroads of immunobiology and neurobiology. Immunity 2009 31 5 711 721 2-s2.0-70449525704 10.1016/j.immuni.2009.09.010
7. Karpus W. J., Chemokines and central nervous system disorders. Journal of NeuroVirology 2001 7 6 493 500 2-s2.0-0035669481 10.1080/135502801753248079 (Pubitemid 34041050)
8. Abbadie C., Bhangoo S., De Koninck Y., Malcangio M., Melik-Parsadaniantz S., White F. A., Chemokines and pain mechanisms. Brain Research Reviews 2009 60 1 125 134 2-s2.0-63649140837 10.1016/j.brainresrev.2008.12.002
9. Pan Y., Lloyd C., Zhou H., Dolich S., Deeds J., Gonzalo J., 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 6633 611 617 2-s2.0-0030949298 10.1038/42491 (Pubitemid 27248766)
10. 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 6617 640 642 2-s2.0-0031036347 10.1038/385640a0 (Pubitemid 27087578)
11. Chapman G. A., Moores K., Harrison D., Campbell C. A., Stewart B. R., Strijbos P. J., Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. The Journal of Neuroscience 2000 20 15 RC87 2-s2.0-0345381021
12. 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. Proceedings of the National Academy of Sciences of the United States of America 1998 95 18 10896 10901 2-s2.0-13144279282 10.1073/pnas.95.18.10896 (Pubitemid 28413165)
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. Journal of Pain 2005 6 7 434 438 2-s2.0-21544469729 10.1016/j.jpain.2005.02.001 (Pubitemid 40922694)
14. Haskell C. A., Hancock W. W., Salant D. J., Gao W., Csizmadia V., Peters W., Faia K., Fituri O., Rottman J. B., Charo I. F., Targeted deletion of CX3CR1 reveals a role for fractalkine in cardiac allograft rejection. Journal of Clinical Investigation 2001 108 5 679 688 2-s2.0-0034800041 10.1172/JCI200112976 (Pubitemid 32906196)
15. Ceyhan G. O., Deucker S., Demir I. E., Erkan M., Schmelz M., Bergmann F., Müller M. W., Giese T., Büchler M. W., Giese N. A., Friess H., Neural fractalkine expression is closely linked to pain and pancreatic neuritis in human chronic pancreatitis. Laboratory Investigation 2009 89 3 347 361 2-s2.0-61349173880 10.1038/labinvest.2008.170
16. Zhuang Z., Kawasaki Y., Tan P., Wen Y., Huang J., Ji R., Role of the CX3CR1/p38 MAPK pathway in spinal microglia for the development of neuropathic pain following nerve injury-induced cleavage of fractalkine. Brain, Behavior, and Immunity 2007 21 5 642 651 2-s2.0-34249717859 10.1016/j.bbi.2006.11.003 (Pubitemid 46830963)
17. Yasuda M., Ito T., Oono T., Kawabe K., Kaku T., Igarashi H., Nakamura T., Takayanagi R., Fractalkine and TGF- β 1 levels reflect the severity of chronic pancreatitis in humans. World Journal of Gastroenterology 2008 14 42 6488 6495 2-s2.0-63449139617 10.3748/wjg.14.6488
18. Lamb B., The roles of fractalkine signaling in neurodegenerative disease. Molecular Neurodegeneration 2012 7 supplement 1 L21
19. 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 Letters 1998 429 2 167 172 2-s2.0-0032510831 10.1016/S0014-5793(98)00583-3 (Pubitemid 28288203)
20. Milligan E. D., Sloane E. M., Watkins L. R., Glia in pathological pain: a role for fractalkine. Journal of Neuroimmunology 2008 198 1-2 113 120 2-s2.0-47249157141 10.1016/j.jneuroim.2008.04.011
21. 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. European Journal of Neuroscience 2004 20 5 1150 1160 2-s2.0-4544252839 10.1111/j.1460-9568.2004.03593.x (Pubitemid 39233569)
22. Holmes F. E., Arnott N., Vanderplank P., Kerr N. C. H., Longbrake E. E., Popovich P. G., Imai T., Combadière C., Murphy P. M., Wynick D., Intra-neural administration of fractalkine attenuates neuropathic pain-related behaviour. Journal of Neurochemistry 2008 106 2 640 649 2-s2.0-51649107644 10.1111/j.1471-4159.2008.05419.x
23. Hu P., Bembrick A. L., Keay K. A., McLachlan E. M., Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve. Brain, Behavior, and Immunity 2007 21 5 599 616 2-s2.0-34249661663 10.1016/j.bbi.2006.10.013 (Pubitemid 46830961)
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. European Journal of Neuroscience 2004 20 9 2294 2302 2-s2.0-8144221210 10.1111/j.1460-9568.2004. 03709.x (Pubitemid 39472392)
25. Johnston I. N., Milligan E. D., Wieseler-Frank J., Frank M. G., Zapata V., Campisi J., Langer S., Martin D., Green P., Fleshner M., Leinwand L., Maier S. F., Watkins L. R., A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. The Journal of Neuroscience 2004 24 33 7353 7365 2-s2.0-7244226284 10.1523/JNEUROSCI.1850-04.2004 (Pubitemid 39100704)
26. Zhu W., Frost E. E., Begum F., Vora P., Au K., Gong Y., Macneil B., Pillai P., Namaka M., The role of dorsal root ganglia activation and brain-derived neurotrophic factor in multiple sclerosis. Journal of Cellular and Molecular Medicine 2012 16 8 1856 1865
27. Melanson M., Miao P., Eisenstat D., Gong Y., Gu X., Au K., Zhu W., Begum F., Frost E. E., Namaka M., Experimental autoimmune encephalomyelitis-induced upregulation of tumor necrosis factor-alpha in the dorsal root ganglia. Multiple Sclerosis 2009 15 10 1135 1145 2-s2.0-72449136385 10.1177/1352458509106856
28. Begum F., Zhu W., Namaka M. P., Frost E. E., A novel decalcification method for adult rodent bone for histological analysis of peripheral-central nervous system connections. The Journal of Neuroscience Methods 2010 187 1 59 66 2-s2.0-77249135520 10.1016/j.jneumeth.2009.12.013
29. 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 1 77 88 2-s2.0-0023924046
30. Moller K. A., Johansson B., Berge O., Assessing mechanical allodynia in the rat paw with a new electronic algometer. The Journal of Neuroscience Methods 1998 84 1-2 41 47 2-s2.0-16744365823 10.1016/S0165-0270(98)00083-1 (Pubitemid 28485045)
31. Sporkel O., Uschkureit T., Bussow H., Stoffel W., Oligodendrocytes expressing exclusively the DM20 isoform of the proteolipid protein gene: myelination and development. Glia 2002 37 1 19 30 2-s2.0-0036006720 10.1002/glia.10014 (Pubitemid 34103091)
32. Wang E., Huang Z., Hobson G. M., Dimova N., Sperle K., McCullough A., Cambi F., PLP1 alternative splicing in differentiating oligodendrocytes: characterization of an exonic splicing enhancer. Journal of Cellular Biochemistry 2006 97 5 999 1016 2-s2.0-33645239497 10.1002/jcb.20692
33. Bradford M. M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 1976 72 1-2 248 254 2-s2.0-0017184389
34. Mix E., Meyer-Rienecker H., Zettl U. K., Animal models of multiple sclerosis for the development and validation of novel therapies-potential and limitations. Journal of Neurology 2008 255 supplement 6 7 14 2-s2.0-64149114563 10.1007/s00415-008-6003-0
35. Namaka M., Turcotte D., Leong C., Grossberndt A., Klassen D., Multiple sclerosis: etiology and treatment strategies. Consultant Pharmacist 2008 23 11 886 896 2-s2.0-58249093589 10.4140/TCP.n.2008.886
36. Aicher S. A., Silverman M. B., Winkler C. W., Bebo B. F. Jr., Hyperalgesia in an animal model of multiple sclerosis. Pain 2004 110 3 560 570 2-s2.0-3843060543 10.1016/j.pain.2004.03.025 (Pubitemid 39036787)
37. Miao P., Madec K., Gong Y., Shen H., Eisenstat D., Melanson M., Gu X., Leong C., Klowak M., Namaka M., Axotomy-induced up-regulation of tumor necrosis factor-alpha in the dorsal root ganglia. Neurological Research 2008 30 6 623 631 2-s2.0-47749119150 10.1179/174313208X289606 (Pubitemid 352032561)
38. Solaro C., Trabucco E., Uccelli M. M., Pain and multiple sclerosis: pathophysiology and treatment. Current Neurology and Neuroscience Reports 2013 13 1 320
39. Foley P. L., Vesterinen H. M., Laird B. J., Sena E. S., Colvin L. A., Chandran S., Macleod M. R., Fallon M. T., Prevalence and natural history of pain in adults with multiple sclerosis: systematic review and meta-analysis. Pain 2013 154 5 632 642
40. D'Haese J. G., Demir I. E., Friess H., Ceyhan G. O., Fractalkine/CX3CR1: why a single chemokine-receptor duo bears a major and unique therapeutic potential. Expert Opinion on Therapeutic Targets 2010 14 2 207 219 2-s2.0-74949104597 10.1517/14728220903540265
41. Ludwig A., Hundhausen C., Lambert M. H., Broadway N., Andrews R. C., Bickett D. M., Leesnitzer M. A., Becherer J. D., Metalloproteinase inhibitors for the disintegrin-like metalloproteinases ADAM10 and ADAM17 that differentially block constitutive and phorbol ester-inducible shedding of cell surface molecules. Combinatorial Chemistry and High Throughput Screening 2005 8 2 161 171 2-s2.0-15244349837 10.2174/1386207053258488 (Pubitemid 40388743)
42. 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. Journal of Neurochemistry 2010 114 4 1143 1157 2-s2.0-77954707933 10.1111/j.1471-4159.2010.06837.x
43. Clark A. K., Yip P. K., Malcangio M., The liberation of fractalkine in the dorsal horn requires microglial cathepsin S. The Journal of Neuroscience 2009 29 21 6945 6954 2-s2.0-66149186748 10.1523/JNEUROSCI.0828-09.2009
44. Coddou C., Stojilkovic S. S., Huidobro-Toro J. P., Allosteric modulation of ATP-gated P2X receptor channels. Reviews in the Neurosciences 2011 22 3 335 354 2-s2.0-80051925231 10.1515/RNS.2011.014
45. Clark A. K., Staniland A. A., Marchand F., Kaan T. K. Y., McMahon S. B., Malcangio M., P2X7-dependent release of interleukin-1 β and nociception in the spinal cord following lipopolysaccharide. The Journal of Neuroscience 2010 30 2 573 582 2-s2.0-74949123761 10.1523/JNEUROSCI.3295-09.2010
46. Matsumiya T., Ota K., Imaizumi T., Yoshida H., Kimura H., Satoh K., Characterization of synergistic induction of CX3CL1/fractalkine by TNF- α and IFN- γ in vascular endothelial cells: an essential role for TNF- α in post-transcriptional regulation of CX3CL1. Journal of Immunology 2010 184 8 4205 4214 2-s2.0-77952753340 10.4049/jimmunol.0903212
47. Sung M. J., Kim D., Davaatseren M., Hur H. J., Kim W., Jung Y. J., Park S. K., Kwon D. Y., Genistein suppression of TNF- α -induced fractalkine expression in endothelial cells. Cellular Physiology and Biochemistry 2010 26 3 431 440 2-s2.0-78650019202 10.1159/000320566
48. Huang D., Shi F., Jung S., Pien G. C., Wang J., Salazar-Mather T. P., He T. T., Weaver J. T., Ljunggren H., Biron C. A., Littman D. R., Ransohoff R. M., The neuronal chemokine CX3CL1/fractalkine selectively recruits NK cells that modify experimental autoimmune encephalomyelitis within the central nervous system. The FASEB Journal 2006 20 7 896 905 2-s2.0-33744465815 10.1096/fj.05-5465com (Pubitemid 44943947)
49. Mills J. H., Alabanza L. M., Mahamed D. A., Bynoe M. S., Extracellular adenosine signaling induces CX3CL1 expression in the brain to promote experimental autoimmune encephalomyelitis. Journal of Neuroinflammation 2012 9 193
50. Watkins L. R., Maier S. F., Glia: a novel drug discovery target for clinical pain. Nature Reviews Drug Discovery 2003 2 12 973 985 2-s2.0-0347169249 (Pubitemid 37540579)
51. Sweitzer S., Martin D., DeLeo J. A., Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain. Neuroscience 2001 103 2 529 539 2-s2.0-0035857748 10.1016/S0306-4522(00)00574-1 (Pubitemid 32201938)
52. Sweitzer S. M., Schubert P., DeLeo J. A., Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. Journal of Pharmacology and Experimental Therapeutics 2001 297 3 1210 1217 2-s2.0-0035018058 (Pubitemid 32472523)
53. Kastenbauer S., Koedel U., Wick M., Kieseier B. C., Hartung H., Pfister H., CSF and serum levels of soluble fractalkine (CX3CL1) in inflammatory diseases of the nervous system. Journal of Neuroimmunology 2003 137 1-2 210 217 2-s2.0-0037379079 10.1016/S0165-5728(03)00085-7 (Pubitemid 36355942)
54. Gomes C., Ferreira R., George J., Sanches R., Rodrigues D. I., Goncalves N., Cunha R. A., Activation of microglial cells triggers a release of brain-derived neurotrophic factor (BDNF) inducing their proliferation in an adenosine A2A receptor-dependent manner: A2A receptor blockade prevents BDNF release and proliferation of microglia. Journal of Neuroinflammation 2013 10 16