Thiamine deficiency promotes T cell infiltration in experimental autoimmune encephalomyelitis: The involvement of CCL2

Journal of Immunology

Volumn 193, Issue 5, 2014, Pages 2157-2167

  Ji, Zhe ^a   Fan, Zhiqin ^a   Zhang, Ying ^a   Yu, Ronghuan ^a   Yang, Haihua ^a   Zhou, Chenghua ^a   Luo, Jia ^b   Ke, Zun Ji ^a,c  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF KENTUCKY   (United States)

^c SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; CCL2 PROTEIN, MOUSE; MYELIN OLIGODENDROCYTE GLYCOPROTEIN (35-55); PEPTIDE FRAGMENT;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CELL INFILTRATION; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE SEVERITY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IN VITRO STUDY; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; MICROGLIA; MOUSE; NONHUMAN; SPINAL CORD; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; THIAMINE DEFICIENCY; UPREGULATION; ANIMAL; CELL MOTION; CELL PROLIFERATION; COMPLICATION; DRUG EFFECTS; IMMUNOLOGY; LYMPH NODE; PATHOLOGY; RAT; SPLEEN; TOXICITY;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CCL2; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; LYMPH NODES; MICE; MICROGLIA; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; RATS; SPINAL CORD; SPLEEN; TH1 CELLS; TH17 CELLS; THIAMINE DEFICIENCY;

EID: 84907033451     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302702     Document Type: Article

References (72)

1. Gold, R., C. Linington, and H. Lassmann. 2006. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 129: 1953-1971.
2. Albelda, S. M., C. W. Smith, and P. A. Ward. 1994. Adhesion molecules and inflammatory injury. FASEB J. 8: 504-512.
3. McFarland, H. F., and R. Martin. 2007. Multiple sclerosis: a complicated picture of autoimmunity. Nat. Immunol. 8: 913-919.
4. International Multiple Sclerosis Genetics Consortium, Wellcome Trust Case Control Consortium 2, S. Sawcer, G. Hellenthal, M. Pirinen, C. C. Spencer, N. A. Patsopoulos, L. Moutsianas, A. Dilthey, Z. Su, et al. 2011. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476: 214-219.
5. Marrie, R. A. 2004. Environmental risk factors in multiple sclerosis aetiology. Lancet Neurol. 3: 709-718.
6. Ascherio, A., K. L. Munger, and J. D. Lünemann. 2012. The initiation and prevention of multiple sclerosis. Nat. Rev. Neurol. 8: 602-612.
7. Agranoff, B. W., and D. Goldberg. 1974. Diet and the geographical distribution of multiple sclerosis. Lancet 2: 1061-1066.
8. Simpson, S., Jr., L. Blizzard, P. Otahal, I. Van der Mei, and B. Taylor. 2011. Latitude is significantly associated with the prevalence of multiple sclerosis: a meta-analysis. J. Neurol. Neurosurg. Psychiatry 82: 1132-1141.
9. Niino, M. 2010. Vitamin D and its immunoregulatory role in multiple sclerosis. Drugs Today (Barc). 46: 279-290.
10. Kriegel, M.A., J. E. Manson, and K. H. Costenbader. 2011. Does vitamin D affect risk of developing autoimmune disease? A systematic review. Semin. Arthritis Rheum. 40: 512-531.e518.
11. Zhu, Y., Z. Y. He, and H. N. Liu. 2011. Meta-analysis of the relationship between homocysteine, vitamin B12, folate, and multiple sclerosis. J. Clin. Neurosci. 18: 933-938.
12. Najafi, M. R., V. Shaygannajad, M. Mirpourian, and A. Gholamrezaei. 2012. Vitamin B(12) deficiency and multiple sclerosis; is there any association? Int. J. Prev. Med. 3: 286-289.
13. Verma, R., and H. N. Praharaj. 2012. Unusual association of Arnold-Chiari malformation and vitamin B12 deficiency. BMJ Case Rep. pii: bcr0320126138.
14. Moghaddasi, M., M. Mamarabadi, N. Mohebi, H. Razjouyan, and M. Aghaei. 2013. Homocysteine, vitamin B12 and folate levels in Iranian patients with Multiple Sclerosis: a case control study. Clin. Neurol. Neurosurg. 115: 1802-1805.
15. Simmons, S. B., E. R. Pierson, S. Y. Lee, and J. M. Goverman. 2013. Modeling the heterogeneity of multiple sclerosis in animals. Trends Immunol. 34: 410-422.
16. Bramow, S., J. M. Frischer, H. Lassmann, N. Koch-Henriksen, C. F. Lucchinetti, P. S. Sørensen, and H. Laursen. 2010. Demyelination versus remyelination in progressive multiple sclerosis. Brain 133: 2983-2998.
17. Sospedra, M., and R. Martin. 2005. Immunology of multiple sclerosis. Annu. Rev. Immunol. 23: 683-747.
18. Lassmann, H., and H. M. Wisniewski. 1979. Chronic relapsing experimental allergic encephalomyelitis: clinicopathological comparison with multiple sclerosis. Arch. Neurol. 36: 490-497.
19. Bernard, C. C., J. Leydon, and I. R. Mackay. 1976. T cell necessity in the pathogenesis of experimental autoimmune encephalomyelitis in mice. Eur. J. Immunol. 6: 655-660.
20. Yasuda, T., T. Tsumita, Y. Nagai, E. Mitsuzawa, and S. Ohtani. 1975. Experimental allergic encephalomyelitis (EAE) in mice. I. Induction of EAE with mouse spinal cord homogenate and myelin basic protein. Jpn. J. Exp. Med. 45: 423-427.
21. Mendel, I., N. Kerlero de Rosbo, and A. Ben-Nun. 1995. A myelin oligodendrocyte glycoprotein peptide induces typical chronic experimental autoimmune encephalomyelitis in H-2b mice: fine specificity and T cell receptor V beta expression of encephalitogenic T cells. Eur. J. Immunol. 25: 1951-1959.
22. Homey, B., A. Müller, and A. Zlotnik. 2002. Chemokines: agents for the immunotherapy of cancer? Nat. Rev. Immunol. 2: 175-184.
23. Rossi, D., and A. Zlotnik. 2000. The biology of chemokines and their receptors. Annu. Rev. Immunol. 18: 217-242.
24. Rollins, B. J. 1997. Chemokines. Blood 90: 909-928.
25. Matsushima, K., C. G. Larsen, G. C. DuBois, and J. J. Oppenheim. 1989. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line. J. Exp. Med. 169: 1485-1490.
26. Carr, M. W., S. J. Roth, E. Luther, S. S. Rose, and T. A. Springer. 1994. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc. Natl. Acad. Sci. USA 91: 3652-3656.
27. Allavena, P., G. Bianchi, D. Zhou, J. van Damme, P. Jílek, S. Sozzani, and A. Mantovani. 1994. Induction of natural killer cell migration by monocyte chemotactic protein-1, -2 and -3. Eur. J. Immunol. 24: 3233-3236.
28. Kuna, P., S. R. Reddigari, D. Rucinski, J. J. Oppenheim, and A. P. Kaplan. 1992. Monocyte chemotactic and activating factor is a potent histamine-releasing factor for human basophils. J. Exp. Med. 175: 489-493.
29. Izikson, L., R. S. Klein, I. F. Charo, H. L. Weiner, and A. D. Luster. 2000. Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J. Exp. Med. 192: 1075-1080.
30. Huang, D. R., J. Wang, P. Kivisakk, B. J. Rollins, and R. M. Ransohoff. 2001. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J. Exp. Med. 193: 713-726.
31. Ransohoff, R. M., T. A. Hamilton, M. Tani, M. H. Stoler, H. E. Shick, J. A. Major, M. L. Estes, D. M. Thomas, and V. K. Tuohy. 1993. Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J. 7: 592-600.
32. Glabinski, A. R., M. Tani, R. M. Strieter, V. K. Tuohy, and R. M. Ransohoff. 1997. Synchronous synthesis of alpha- and beta-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of chronic experimental autoimmune encephalomyelitis. Am. J. Pathol. 150: 617-630.
33. Juedes, A. E., P. Hjelmström, C. M. Bergman, A. L. Neild, and N. H. Ruddle. 2000. Kinetics and cellular origin of cytokines in the central nervous system: insight into mechanisms of myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis. J. Immunol. 164: 419-426.
34. Sun, D., M. Tani, T. A. Newman, K. Krivacic, M. Phillips, A. Chernosky, P. Gill, T. Wei, K. J. Griswold, R. M. Ransohoff, and R. O. Weller. 2000. Role of chemokines, neuronal projections, and the blood-brain barrier in the enhancement of cerebral EAE following focal brain damage. J. Neuropathol. Exp. Neurol. 59: 1031-1043.
35. Sagar, D., A. Lamontagne, C. A. Foss, Z. K. Khan, M. G. Pomper, and P. Jain. 2012. Dendritic cell CNS recruitment correlates with disease severity in EAE via CCL2 chemotaxis at the blood-brain barrier through paracellular transmigration and ERK activation. J. Neuroinflammation 9: 245.
36. Poliani, P. L., H. Brok, R. Furlan, F. Ruffini, A. Bergami, G. Desina, P. C. Marconi, M. Rovaris, A. Uccelli, J. C. Glorioso, et al. 2001. Delivery to the central nervous system of a nonreplicative herpes simplex type 1 vector engineered with the interleukin 4 gene protects rhesus monkeys from hyperacute autoimmune encephalomyelitis. Hum. Gene Ther. 12: 905-920.
37. Karpus, W. J., and K. J. Kennedy. 1997. MIP-1alpha and MCP-1 differentially regulate acute and relapsing autoimmune encephalomyelitis as well as Th1/Th2 lymphocyte differentiation. J. Leukoc. Biol. 62: 681-687.
38. Fife, B. T., G. B. Huffnagle, W. A. Kuziel, and W. J. Karpus. 2000. CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J. Exp. Med. 192: 899-905.
39. Hakim, A. M., and H. M. Pappius. 1981. The effect of thiamine deficiency on local cerebral glucose utilization. Ann. Neurol. 9: 334-339.
40. Ke, Z. J., L. A. DeGiorgio, B. T. Volpe, and G. E. Gibson. 2003. Reversal of thiamine deficiency-induced neurodegeneration. J. Neuropathol. Exp. Neurol. 62: 195-207.
41. Ke, Z. J., and G. E. Gibson. 2004. Selective response of various brain cell types during neurodegeneration induced by mild impairment of oxidative metabolism. Neurochem. Int. 45: 361-369.
42. Zhang, G., H. Ding, H. Chen, X. Ye, H. Li, X. Lin, and Z. Ke. 2013. Thiamine nutritional status and depressive symptoms are inversely associated among older Chinese adults. J. Nutr. 143: 53-58.
43. Liu, L., D. Huang, M. Matsui, T. T. He, T. Hu, J. Demartino, B. Lu, C. Gerard, and R. M. Ransohoff. 2006. Severe disease, unaltered leukocyte migration, and reduced IFN-gamma production in CXCR3-/- mice with experimental autoimmune encephalomyelitis. J. Immunol. 176: 4399-4409.
44. Marusic, S., M. W. Leach, J. W. Pelker, M. L. Azoitei, N. Uozumi, J. Cui, M.W. Shen, C. M. DeClercq, J. S. Miyashiro, B. A. Carito, et al. 2005. Cytosolic phospholipase A2 alpha-deficient mice are resistant to experimental autoimmune encephalomyelitis. J. Exp. Med. 202: 841-851.
45. Wang, X., B. Wang, Z. Fan, X. Shi, Z. J. Ke, and J. Luo. 2007. Thiamine deficiency induces endoplasmic reticulum stress in neurons. Neuroscience 144: 1045-1056.
46. Zhang, Q., G. Yang, W. Li, Z. Fan, A. Sun, J. Luo, and Z. J. Ke. 2011. Thiamine deficiency increases b-secretase activity and accumulation of b-amyloid peptides. Neurobiol. Aging 32: 42-53.
47. Cioli, V., M. G. Ciarniello, A. Guglielmotti, M. R. Luparini, L. Durando, B. Martinelli, B. Catanese, L. Fava, and B. Silvestrini. 1992. A new protein antidenaturant agent, bindarit, reduces secondary phase of adjuvant arthritis in rats. J. Rheumatol. 19: 1735-1742.
48. Ge, S., B. Shrestha, D. Paul, C. Keating, R. Cone, A. Guglielmotti, andJ. S. Pachter. 2012. The CCL2 synthesis inhibitor bindarit targets cells of the neurovascular unit, and suppresses experimental autoimmune encephalomyelitis. J. Neuroinflammation 9: 171.
49. Xia, Y. F., L. P. Liu, C. P. Zhong, and J. G. Geng. 2001. NF-kappaB activation for constitutive expression of VCAM-1 and ICAM-1 on B lymphocytes and plasma cells. Biochem. Biophys. Res. Commun. 289: 851-856.
50. Liu, L. P., Y. F. Xia, L. Yang, J. A. DiDonato, P. E. DiCorleto, C. P. Zhong, and J. G. Geng. 2001. B lymphocytes and plasma cells express functional E-selectin by constitutive activation of NF-kappaB. Biochem. Biophys. Res. Commun. 286: 281-291.
51. Bruce, B., G. Khanna, L. Ren, G. Landberg, K. Jirström, C. Powell, A. Borczuk, E. T. Keller, K. J. Wojno, P. Meltzer, et al. 2007. Expression of the cytoskeleton linker protein ezrin in human cancers. Clin. Exp. Metastasis 24: 69-78.
52. Yang, G., Y. Meng, W. Li, Y. Yong, Z. Fan, H. Ding, Y. Wei, J. Luo, and Z. J. Ke. 2011. Neuronal MCP-1 mediates microglia recruitment and neurodegeneration induced by the mild impairment of oxidative metabolism. Brain Pathol. 21: 279-297.
53. Methner, A., and F. Zipp. 2013. Multiple sclerosis in 2012: novel therapeutic options and drug targets in MS. Nat. Rev. Neurol. 9: 72-73.
54. Scalfari, A., V. Knappertz, G. Cutter, D. S. Goodin, R. Ashton, and G. C. Ebers. 2013. Mortality in patients with multiple sclerosis. Neurology 81: 184-192.
55. Miller, A., M. Korem, R. Almog, and Y. Galboiz. 2005. Vitamin B12, demyelination, remyelination and repair in multiple sclerosis. J. Neurol. Sci. 233: 93-97.
56. Reynolds, E. 2006. Vitamin B12, folic acid, and the nervous system. Lancet Neurol. 5: 949-960.
57. Cordiglieri, C., F. Odoardi, B. Zhang, M. Nebel, N. Kawakami, W. E. Klinkert, D. Lodygin, F. Lühder, E. Breunig, D. Schild, et al. 2010. Nicotinic acid adenine dinucleotide phosphate-mediated calcium signalling in effector T cells regulates autoimmunity of the central nervous system. Brain 133: 1930-1943.
58. Limmroth, V. 2013. Multiple sclerosis: oral BG12 for treatment of relapsingremitting MS. Nat. Rev. Neurol. 9: 8-10.
59. Oh, J., and P. W. O'Connor. 2013. Safety, tolerability, and efficacy of oral therapies for relapsing-remitting multiple sclerosis. CNS Drugs 27: 591-609.
60. Gold, R., L. Kappos, D. L. Arnold, A. Bar-Or, G. Giovannoni, K. Selmaj, C. Tornatore, M. T. Sweetser, M. Yang, S. I. Sheikh, and K. T. Dawson, DEFINE Study Investigators. 2012. Placebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosis. N. Engl. J. Med. 367: 1098-1107.
61. Shehadah, A., J. Chen, A. Zacharek, Y. Cui, M. Ion, C. Roberts, A. Kapke, and M. Chopp. 2010. Niaspan treatment induces neuroprotection after stroke. Neurobiol. Dis. 40: 277-283.
62. Calingasan, N. Y., W. J. Chun, L. C. Park, K. Uchida, and G. E. Gibson. 1999. Oxidative stress is associated with region-specific neuronal death during thiamine deficiency. J. Neuropathol. Exp. Neurol. 58: 946-958.
63. Ji, Z., Z. J. Ke, and J. G. Geng. 2012. SAP suppresses the development of experimental autoimmune encephalomyelitis in C57BL/6 mice. Immunol. Cell Biol. 90: 388-395.
64. Reiseter, B. S., G. T. Miller, M. P. Happ, and M. T. Kasaian. 1998. Treatment of murine experimental autoimmune encephalomyelitis with a myelin basic protein peptide analog alters the cellular composition of leukocytes infiltrating the cerebrospinal fluid. J. Neuroimmunol. 91: 156-170.
65. Domingues, H. S., M. Mues, H. Lassmann, H. Wekerle, and G. Krishnamoorthy. 2010. Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLoS ONE 5: e15531.
66. Schulze-Topphoff, U., S. Casazza, M. Varrin-Doyer, K. Pekarek, R. A. Sobel, S. L. Hauser, J. R. Oksenberg, S. S. Zamvil, and S. E. Baranzini. 2013. Tob1 plays a critical role in the activation of encephalitogenic T cells in CNS autoimmunity. J. Exp. Med. 210: 1301-1309.
67. Huber, M., S. Heink, A. Pagenstecher, K. Reinhard, J. Ritter, A. Visekruna, A. Guralnik, N. Bollig, K. Jeltsch, C. Heinemann, et al. 2013. IL-17A secretion by CD8+ T cells supports Th17-mediated autoimmune encephalomyelitis. J. Clin. Invest. 123: 247-260.
68. Ji, Q., L. Castelli, and J. M. Goverman. 2013. MHC class I-restricted myelin epitopes are cross-presented by Tip-DCs that promote determinant spreading to CD8+ T cells. Nat. Immunol. 14: 254-261.
69. Ortega, S. B., V. P. Kashi, A. F. Tyler, K. Cunnusamy, J. P. Mendoza, and N. J. Karandikar. 2013. The disease-ameliorating function of autoregulatory CD8 T cells is mediated by targeting of encephalitogenic CD4 T cells in experimental autoimmune encephalomyelitis. J. Immunol. 191: 117-126.
70. Rot, A., and U. H. von Andrian. 2004. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22: 891-928.
71. Mahad, D. J., and R. M. Ransohoff. 2003. The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin. Immunol. 15: 23-32.
72. Kivisäkk, P., C. Trebst, Z. Liu, B. H. Tucky, T. L. Sørensen, R. A. Rudick, M. Mack, and R. M. Ransohoff. 2002. T-cells in the cerebrospinal fluid express a similar repertoire of inflammatory chemokine receptors in the absence or presence of CNS inflammation: implications for CNS trafficking. Clin. Exp. Immunol. 129: 510-518.