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

doi:10.1084/jem.193.6.713

Published online 19 March 2001.

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© The Rockefeller University Press, 0022-1007/2001/3/713/ $5.00
The Journal of Experimental Medicine, Volume 193, Number 6, March 19, 2001 713-726

Original Article

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

DeRen Huang^a, Jintang Wang^a, Pia Kivisakk^a, Barrett J. Rollins^b, and Richard M. Ransohoff^a
^a Department of Neurosciences, Lerner Research Institute, The Cleveland Clinic Foundation, Cleveland, Ohio 44195
^b Department of Adult Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, Massachusetts 02115

Correspondence to: Richard M. Ransohoff, Department of Neurosciences NC30, Lerner Research Institute, The Cleveland Clinic Foundation, 9500 Euclid Ave., Cleveland, OH 44195. Tel:216-444-8939 Fax:216-444-7927 E-mail:ransohr{at}ccf.org.

Monocyte chemoattractant protein (MCP)-1 plays a critical rolein innate immunity by directing the migration of monocytes intoinflammatory sites. Recent data indicated a function for thischemokine in adaptive immunity as a regulator of T cell commitmentto T helper cell type 2 (Th2) effector function. Studies ina Th1-dependent animal model, experimental autoimmune encephalomyelitis(EAE), showed that MCP-1 was highly expressed in the centralnervous system (CNS) of affected rodents, and MCP-1 antibodiescould block relapses of the disease. Mice deficient for themajor MCP-1 receptor, CC chemokine receptor (CCR)2, did notdevelop EAE after active immunization but generated effectorcells that could transfer the disease to naive wild-type recipients.We analyzed EAE in mice deficient for MCP-1 to define the relevantligand for CCR2, which responds to murine MCP-1, MCP-2, MCP-3,and MCP-5. We found that C57BL/6 MCP-1–null mice weremarkedly resistant to EAE after active immunization, with drasticallyimpaired recruitment of macrophages to the CNS, yet able togenerate effector T cells that transferred severe disease tonaive wild-type recipients. By contrast, adoptive transfer ofprimed T cells from wild-type mice into naive MCP-1–nullrecipients did not mediate clinical EAE. On the SJL background,disruption of the MCP-1 gene produced a milder EAE phenotypewith diminished relapses that mimicked previous findings usinganti–MCP-1 antibodies. There was no compensatory upregulationof MCP-2, MCP-3, or MCP-5 in MCP-1–null mice with EAE.These results indicated that MCP-1 is the major CCR2 ligandin mice with EAE, and provided an opportunity to define therole of MCP-1 in EAE. Compared with wild-type littermates, MCP-1^-/-mice exhibited reduced expression of interferon ${gamma}$ in draininglymph node and CNS and increased antigen-specific immunoglobulinG1 antibody production. Taken together, these data demonstratethat MCP-1 is crucial for Th1 immune responses in EAE inductionand that macrophage recruitment to the inflamed CNS target organis required for primed T cells to execute a Th1 effector programin EAE.

Key Words: autoimmune disease, chemokine, chemokine receptor, macrophage,T helper cell type 1/T helper cell type 2

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deSchoolmeester, M. L., Little, M. C., Rollins, B. J., Else, K. J. (2003). Absence of CC Chemokine Ligand 2 Results in an Altered Th1/Th2 Cytokine Balance and Failure to Expel Trichuris muris Infection. J. Immunol. 170: 4693-4700 [Abstract] [Full Text]
Bleharski, J. R., Kiessler, V., Buonsanti, C., Sieling, P. A., Stenger, S., Colonna, M., Modlin, R. L. (2003). A Role for Triggering Receptor Expressed on Myeloid Cells-1 in Host Defense During the Early-Induced and Adaptive Phases of the Immune Response. J. Immunol. 170: 3812-3818 [Abstract] [Full Text]
Gonnella, P. A., Kodali, D., Weiner, H. L. (2003). Induction of Low Dose Oral Tolerance in Monocyte Chemoattractant Protein-1- and CCR2-Deficient Mice. J. Immunol. 170: 2316-2322 [Abstract] [Full Text]
Subramanian, S., Matejuk, A., Zamora, A., Vandenbark, A. A., Offner, H. (2003). Oral Feeding with Ethinyl Estradiol Suppresses and Treats Experimental Autoimmune Encephalomyelitis in SJL Mice and Inhibits the Recruitment of Inflammatory Cells into the Central Nervous System. J. Immunol. 170: 1548-1555 [Abstract] [Full Text]
Qu, C., Moran, T. M., Randolph, G. J. (2003). Autocrine Type I IFN and Contact with Endothelium Promote the Presentation of Influenza A Virus by Monocyte-Derived APC. J. Immunol. 170: 1010-1018 [Abstract] [Full Text]
Sewell, D., Qing, Z., Reinke, E., Elliot, D., Weinstock, J., Sandor, M., Fabry, Z. (2003). Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol 15: 59-69 [Abstract] [Full Text]
Gaupp, S., Pitt, D., Kuziel, W. A., Cannella, B., Raine, C. S. (2003). Experimental Autoimmune Encephalomyelitis (EAE) in CCR2-/- Mice: Susceptibility in Multiple Strains. Am. J. Pathol. 162: 139-150 [Abstract] [Full Text]
Huang, D., Tani, M., Wang, J., Han, Y., He, T. T., Weaver, J., Charo, I. F., Tuohy, V. K., Rollins, B. J., Ransohoff, R. M. (2002). Pertussis Toxin-Induced Reversible Encephalopathy Dependent on Monocyte Chemoattractant Protein-1 Overexpression in Mice. J. Neurosci. 22: 10633-10642 [Abstract] [Full Text]
Uehara, A., Sugawara, S., Muramoto, K., Takada, H. (2002). Activation of Human Oral Epithelial Cells by Neutrophil Proteinase 3 Through Protease-Activated Receptor-2. J. Immunol. 169: 4594-4603 [Abstract] [Full Text]
Szalai, A. J., Nataf, S., Hu, X.-Z., Barnum, S. R. (2002). Experimental Allergic Encephalomyelitis Is Inhibited in Transgenic Mice Expressing Human C-Reactive Protein. J. Immunol. 168: 5792-5797 [Abstract] [Full Text]
Tuaillon, N., Shen, D. F., Berger, R. B., Lu, B., Rollins, B. J., Chan, C.-C. (2002). MCP-1 Expression in Endotoxin-Induced Uveitis. IOVS 43: 1493-1498 [Abstract] [Full Text]
Traynor, T. R., Herring, A. C., Dorf, M. E., Kuziel, W. A., Toews, G. B., Huffnagle, G. B. (2002). Differential Roles of CC Chemokine Ligand 2/Monocyte Chemotactic Protein-1 and CCR2 in the Development of T1 Immunity. J. Immunol. 168: 4659-4666 [Abstract] [Full Text]
Janatpour, M. J., Hudak, S., Sathe, M., Sedgwick, J. D., McEvoy, L. M. (2001). Tumor Necrosis Factor-dependent Segmental Control of MIG Expression by High Endothelial Venules in Inflamed Lymph Nodes Regulates Monocyte Recruitment. JEM 194: 1375-1384 [Abstract] [Full Text]