A pain-mediated neural signal induces relapse in murine autoimmune encephalomyelitis, a multiple sclerosis model

eLife

Volumn 4, Issue JULY2015, 2015, Pages

  Arima, Yasunobu ^a,b   Kamimura, Daisuke ^a,b   Atsumi, Toru ^a,b   Harada, Masaya ^a,b   Kawamoto, Tadafumi ^c   Nishikawa, Naoki ^a,b   Stofkova, Andrea ^a,b   Ohki, Takuto ^a,b   Higuchi, Kotaro ^a,b   Morimoto, Yuji ^a   Wieghofer, Peter ^d   Okada, Yuka ^e   Mori, Yuki ^b   Sakoda, Saburo ^f   Saika, Shizuya ^e   Yoshioka, Yoshichika ^b   Komuro, Issei ^g   Yamashita, Toshihide ^b   Hirano, Toshio ^b   Prinz, Marco ^d   Murakami, Masaaki ^a,b   more..

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c TSURUMI UNIVERSITY   (Japan)

^d UNIVERSITY OF FREIBURG   (Germany)

^e WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^f TONEYAMA NATIONAL HOSPITAL   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; ANIMAL; ANTIGEN PRESENTING CELL; CD4+ T LYMPHOCYTE; DISEASE MODEL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IMMUNOLOGY; PAIN; PATHOLOGY; RECURRENT DISEASE; SECRETION (PROCESS); SPINAL CORD;

MURINAE;

CHEMOKINE;

ANIMALS; ANTIGEN-PRESENTING CELLS; CD4-POSITIVE T-LYMPHOCYTES; CHEMOKINES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; MICE; MULTIPLE SCLEROSIS; PAIN; RECURRENCE; SPINAL CORD;

EID: 84938929121     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08733     Document Type: Article

References (54)

1. Arima Y, Harada M, Kamimura D, Park JH, Kawano F, Yull FE, Kawamoto T, Iwakura Y, Betz UA, Ma´ rquez G, Blackwell TS, Ohira Y, Hirano T, Murakami M.2012.Regional neural activation defines a gateway for autoreactive T cells to cross the blood-brain barrier.Cell 148:447-457.doi: 10.1016/j.cell.2012.01.022.
2. Atsumi T, Singh R, Sabharwal L, Bando H, Meng J, Arima Y, Yamada M, Harada M, Jiang JJ, Kamimura D, Ogura H, Hirano T, Murakami M.2014.Inflammation amplifier, a new paradigm in cancer biology.Cancer Research 74: 8-14.doi: 10.1158/0008-5472.CAN-13-2322.
3. Beiske AG, Pedersen ED, Czujko B, Myhr KM.2004.Pain and sensory complaints in multiple sclerosis.European Journal of Neurology 11:479-482.doi: 10.1111/j.1468-1331.2004.00815.x.
4. Chwastiak L, Ehde DM, Gibbons LE, Sullivan M, Bowen JD, Kraft GH.2002.Depressive symptoms and severity of illness in multiple sclerosis: epidemiologic study of a large community sample.The American Journal of Psychiatry 159:1862-1868.doi: 10.1176/appi.ajp.159.11.1862.
5. Crawford MP, Yan SX, Ortega SB, Mehta RS, Hewitt RE, Price DA, Stastny P, Douek DC, Koup RA, Racke MK, Karandikar NJ.2004.High prevalence of autoreactive, neuroantigen-specific CD8+ T cells in multiple sclerosis revealed by novel flow cytometric assay.Blood 103:4222-4231.doi: 10.1182/blood-2003-11-4025.
6. Critchley HD.2005.Neural mechanisms of autonomic, affective, and cognitive integration.The Journal of Comparative Neurology 493:154-166.doi: 10.1002/cne.20749.
7. Delmas P, Hao J, Rodat-Despoix L.2011.Molecular mechanisms of mechanotransduction in mammalian sensory neurons.Nature Reviews.Neuroscience 12:139-153.doi: 10.1038/nrn2993.
8. Dressel A, Chin JL, Sette A, Gausling R, Ho¨ llsberg P, Hafler DA.1997.Autoantigen recognition by human CD8 T cell clones: enhanced agonist response induced by altered peptide ligands.The Journal of Immunology 159: 4943-4951.
9. Duyverman AM, Kohno M, Duda DG, Jain RK, Fukumura D.2012.A transient parabiosis skin transplantation model in mice.Nature Protocols 7:763-770.doi: 10.1038/nprot.2012.032.
10. Ehde DM, Gibbons LE, Chwastiak L, Bombardier CH, Sullivan MD, Kraft GH.2003.Chronic pain in a large community sample of persons with multiple sclerosis.Multiple Sclerosis 9:605-611.doi: 10.1191/1352458503ms939oa.
11. Ehde DM, Osborne TL, Hanley MA, Jensen MP, Kraft GH.2006.The scope and nature of pain in persons with multiple sclerosis.Multiple Sclerosis 12:629-638.doi: 10.1177/1352458506071346.
12. Guinjoan SM, Bernabo´ JL, Cardinali DP.1995.Cardiovascular tests of autonomic function and sympathetic skin responses in patients with major depression.Journal of Neurology, Neurosurgery, and Psychiatry 59:299-302.doi: 10.1136/jnnp.59.3.299.
13. Hirano T.2010.Interleukin 6 in autoimmune and inflammatory diseases: a personal memoir.Proceedings of the Japan Academy.Series B, Physical and Biological Sciences 86:717-730.doi: 10.2183/pjab.86.717.
14. Huber SJ, Paulson GW, Chakeres D, Pakalnis A, Brogan M, Phillips BL, Myers MA, Rammohan KW.1988.Magnetic resonance imaging and clinical correlations in multiple sclerosis.Journal of the Neurological Sciences 86:1-12.doi: 10.1016/0022-510X(88)90002-0.
15. Ikemoto K, Kitahama K, Nishimura A, Jouvet A, Nishi K, Arai R, Jouvet M, Nagatsu I.1999.Tyrosine hydroxylase and aromatic L-amino acid decarboxylase do not coexist in neurons in the human anterior cingulate cortex.Neuroscience Letters 269:37-40.doi: 10.1016/S0304-3940(99)00409-7.
16. International Multiple Sclerosis Genetics Consortium, Wellcome Trust Case Control Consortium 2.2011.Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis.Nature 476:214-219.doi: 10.1038/nature10251.
17. Kalia LV, O'Connor PW.2005.Severity of chronic pain and its relationship to quality of life in multiple sclerosis.Multiple Sclerosis 11:322-327.doi: 10.1191/1352458505ms1168oa.
18. Kawamoto T.2003.Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants.Archives of Histology and Cytology 66:123-143.doi: 10.1679/aohc.66.123.
19. Kim SS, Wang H, Li XY, Chen T, Mercaldo V, Descalzi G, Wu LJ, Zhuo M.2011.Neurabin in the anterior cingulate cortex regulates anxiety-like behavior in adult mice.Molecular Brain 19:4-6.doi: 10.1186/1756-6606-4-6.
20. Krzyzanowska A, Pittolo S, Cabrerizo M, Sa´ nchez-Lo´ pez J, Krishnasamy S, Venero C, Avendan˜ o C.2011.Assessing nociceptive sensitivity in mouse models of inflammatory and neuropathic trigeminal pain.Journal of Neuroscience Methods 201:46-54.doi: 10.1016/j.jneumeth.2011.07.006.
21. LaMotte RH, Dong X, Ringkamp M.2014.Sensory neurons and circuits mediating itch.Nature Reviews.Neuroscience 15:19-31.doi: 10.1038/nrn3641.
22. Lee J, Nakagiri T, Kamimura D, Harada M, Oto T, Susaki Y, Shintani Y, Inoue M, Miyoshi S, Morii E, Hirano T, Murakami M, Okumura M.2013.IL-6 amplifier activation in epithelial regions of bronchi after allogeneic lung transplantation.International Immunology 25:319-332.doi: 10.1093/intimm/dxs158.
23. Lee J, Nakagiri T, Oto T, Harada M, Morii E, Shintani Y, Inoue M, Iwakura Y, Miyoshi S, Okumura M, Hirano T, Murakami M.2012.NFκB-triggered positive-feedback for IL-6 signaling in grafts plays a role for allogeneic rejection responses.The Journal of Immunology 189:1928-1936.doi: 10.4049/jimmunol.1103613.
24. Li XY, Ko HG, Chen T, Descalzi G, Koga K, Wang H, Kim SS, Shang Y, Kwak C, Park SW, Shim J, Lee K, Collingridge GL, Kaang BK, Zhuo M.2010.Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex.Science 330:1400-1404.doi: 10.1126/science.1191792.
25. Martin BY, Avendano C.2009.Effects of removal of dietary polyunsaturated fatty acids on plasma extravasation and mechanical allodynia in a trigeminal neuropathic pain model.Mol Pain.5:8.doi: 10.1186/1744-8069-5-8.
26. Michalski D, Liebig S, Thomae E, Hinz A, Bergh FT.2011.Pain in patients with multiple sclerosis: a complex assessment including quantitative and qualitative measurements provides for a disease-related biopsychosocial pain model.Journal of Pain Research 4:219-225.doi: 10.2147/JPR.S20309.
27. Miller SD, Vanderlugt CL, Lenschow DJ, Pope JG, Karandikar NJ, Dal Canto MC, Bluestone JA.1995.Blockade of CD28/B7-1 interaction prevents epitope spreading and clinical relapses of murine EAE.Immunity 3:739-745.doi: 10.1016/1074-7613(95)90063-2.
28. Mori Y, Murakami M, Arima Y, Zhu D, Terayama Y, Komai Y, Nakatsuji Y, Kamimura D, Yoshioka Y.2014.Early pathological alterations of lower lumber cords detected by ultra-high field MRI in a mouse multiple sclerosis model.International Immunology 26:93-101.doi: 10.1093/intimm/dxt044.
29. Moriya M, Nakatsuji Y, Miyamoto K, Okuno T, Kinoshita M, Kumanogoh A, Kusunoki S, Sakoda S.2008.Edaravone, a free radical scavenger, ameliorates experimental autoimmune encephalomyelitis.Neuroscience Letters 440:323-326.doi: 10.1016/j.neulet.2008.05.110.
30. Murakami M, Harada M, Kamimura D, Ogura H, Okuyama Y, Kumai N, Okuyama A, Singh R, Jiang JJ, Atsumi T, Shiraya S, Nakatsuji Y, Kinoshita M, Kohsaka H, Nishida M, Sakoda S, Miyasaka N, Yamauchi-Takihara K, Hirano T.2013.Disease-association analysis of an inflammation-related feedback loop.Cell Reports 3:946-959.doi: 10.1016/j.celrep.2013.01.028.
31. Murakami M, Hirano T.2011.A four step model for the IL-6 amplifier, a critical regulator of chromic inflammations in tissue specific MHC class II-associated autoimmune diseases.Fromtiers Immunology 2:22.doi: 10.3389/fimmu.2011.00022.
32. Murakami M, Okuyama Y, Ogura H, Asano S, Arima Y, Tsuruoka M, Harada M, Kanamoto M, Sawa Y, Iwakura Y, Takatsu K, Kamimura D, Hirano T.2011.Local microbleeding facilitates IL-6- and IL-17-dependent arthritis in the absence of tissue antigen recognition by activated T cells.The Journal of Experimental Medicine 208:103-114.doi: 10.1084/jem.20100900.
33. Ogura H, Arima Y, Kamimura D, Murakami M.2013.The gate theory: how regional neural activation creates a gateway for immune cells via an inflammation amplifier.Biomedical Journal 36:269-273.doi: 10.4103/2319- 4170.113187.
34. Ogura H, Murakami M, Okuyama Y, Tsuruoka M, Kitabayashi C, Kanamoto M, Nishihara M, Iwakura Y, Hirano T.2008.Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction.Immunity 29:628-636.doi: 10.1016/j.immuni.2008.07.018.
35. Osterberg A, Boivie J, Thuomas KA.2005.Central pain in multiple sclerosis-prevalence and clinical characteristics.European Journal of Pain 9:531-542.doi: 10.1016/j.ejpain.2004.11.005.
36. Palazzo E, Luongo L, de Novellis V, Rossi F, Marabese I, Maione S.2012.Transient receptor potential vanilloid type 1 and pain development.Current Opinion in Pharmacology 12:9-17.doi: 10.1016/j.coph.2011.10.022.
37. Rumsfeld JS, Ho PM.2005.Depression and cardiovascular disease: a call for recognition.Circulation 111:250-253.doi: 10.1161/01.CIR.0000154573.62822.89.
38. Sabharwal L, Kamimura D, Meng J, Bando H, Ogura H, Nakayama C, Jiang JJ, Kumai N, Suzuki H, Atsumi T, Arima Y, Murakami M.2014.The Gateway Reflex, which is mediated by the inflammation amplifier, directs pathogenic immune cells into the CNS.Journal of Biochemistry 156:299-304.doi: 10.1093/jb/mvu057.
39. Seeley EJ, Barry SS, Narala S, Matthay MA, Wolters PJ.2013.Noradrenergic neurons regulate monocyte trafficking and mortality during gram-negative peritonitis in mice.The Journal of Immunology 190:4717-4724.doi: 10.4049/jimmunol.1300027.
40. Siegert RJ, Abernethy DA.2005.Depression in multiple sclerosis: a review.Journal of Neurology, Neurosurgery, and Psychiatry 76:469-475.doi: 10.1136/jnnp.2004.054635.
41. Solaro C, Brichetto G, Amato MP, Cocco E, Colombo B, D'Aleo G, Gasperini C, Ghezzi A, Martinelli V, Milanese C, Patti F, Trojano M, Verdun E, Mancardi GL, PaIMS Study Group.2004.The prevalence of pain in multiple sclerosis: a multicenter cross-sectional study.Neurology 63:919-921.
42. Steinman L.2009.A molecular trio in relapse and remission in multiple sclerosis.Nature Reviews.Immunology 9: 440-447.doi: 10.1038/nri2548.
43. Steinman L.2014.Immunology of relapse and remission in multiple sclerosis.Annual Review of Immunology 32: 257-281.doi: 10.1146/annurev-immunol-032713-120227.
44. Stone EA, Lin Y.2011.Open-space forced swim model of depression for mice.Current Protocols in Neuroscience.Chapter 9, Unit9.36.doi: 10.1002/0471142301.ns0936s54.
45. Thompson AJ, Toosy AT, Ciccarelli O.2010.Pharmacological management of symptoms in multiple sclerosis: current approaches and future directions.Lancet Neurology 9:1182-1199.doi: 10.1016/S1474-4422(10)70249-0.
46. Thygesen TH, Baad-Hansen L, Svensson P.2009.Sensory action potentials of the maxillary nerve: a methodologic study with clinical implications.Journal of Oral and Maxillofacial Surgery 67:537-542.doi: 10.1016/j.joms.2008.02.015.
47. Tracey KJ.2012.Immune cells exploit a neural circuit to enter the CNS.Cell 148:392-394.doi: 10.1016/j.cell.2012.01.025.
48. Tsuchida T, Parker KC, Turner RV, McFarland HF, Coligan JE, Biddison WE.1994.Autoreactive CD8+ T-cell responses to human myelin protein-derived peptides.Proceedings of the National Academy of Sciences of USA 91:10859-10863.doi: 10.1073/pnas.91.23.10859.
49. Ueda N, Kuki H, Kamimura D, Sawa S, Seino K, Tashiro T, Fushuku K, Taniguchi M, Hirano T, Murakami M.2006.CD1d-restricted NKT cell activation enhanced homeostatic proliferation of CD8+ T cells in a manner dependent on IL-4.International Immunology 18:1397-1404.doi: 10.1093/intimm/dxl073.
50. Vos BP, Strassman AM, Maciewicz RJ.1994.Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve.J Neurosci 14:2708-2723.
51. Watson CP, Deck JH, Morshead C, Van der Kooy D, Evans RJ.1991.Post-herpetic neuralgia: further post-mortem studies of cases with and without pain.Pain 44:105-117.doi: 10.1016/0304-3959(91)90124-G.
52. Xie L, Kang H, Xu Q, Chen JM, Liao Y, Thiyagarajan M, O'Donnell J, Christensen JD, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M.2013.Sleep drives metabolite clearance from the adult brain.Science 342:1373-377.doi: 10.1126/science.1241224.
53. Yoshihara T, Yawaka Y.2013.Differential effects of repeated immobilization stress in early vs.late postnatal period on stress-induced corticosterone response in adult rats.Neuroscience Letters 8:30-34.doi: 10.1016/j.neulet.2012.12.011.
54. Zimmermann M.1983.Ethical guidelines for investigations of experimental pain in conscious animals.Pain 16: 109-110.doi: 10.1016/0304-3959(83)90201-4.