Challenging cytokine redundancy: Inflammatory cell movement and clinical course of experimental autoimmune encephalomyelitis are normal in lymphotoxin-deficient, but not tumor necrosis factor-deficient, mice

Journal of Experimental Medicine

Volumn 187, Issue 9, 1998, Pages 1517-1528

  Riminton, D Sean ^a   Körner, Heinrich ^a   Strickland, Deborah H ^a   Lemckert, Frances A ^a   Pollard, John D ^b   Sedgwick, Jonathon D ^a,c  

^a CENTENARY INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOTOXIN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW TRANSPLANTATION; CHIMERA; CONTROLLED STUDY; DEMYELINATION; FEMALE; INFLAMMATORY CELL; INTRAPERITONEAL DRUG ADMINISTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; AUTOIMMUNE DISEASES; CENTRAL NERVOUS SYSTEM; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS; INFLAMMATION; LEUKOCYTES; LYMPHOTOXIN-ALPHA; MICE; MICE, KNOCKOUT; MYELIN-ASSOCIATED GLYCOPROTEIN; PEPTIDE FRAGMENTS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 2642698865     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.9.1517     Document Type: Article

References (54)

1. Hochman, P.S., G.R. Majeau, F. Mackay, and J.L. Browning. 1995. Proinflammatory responses are efficiently induced by homotrimeric but not heterotrimeric lymphotoxin ligands. J. Inflamm. 46:220-234.
2. Körner, H., and J.D. Sedgwick. 1996. Tumour necrosis factor and lymphotoxin: molecular aspects and role in tissue specific autoimmunity. Immunol. Cell Biol. 74:465-472.
3. Selmaj, K., C.S. Raine, B. Cannella, and C.F. Brosnan. 1991. Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J. Clin. Invest. 87:949-954.
4. Matusevicius, D., V. Navikas, M. Soderstrom, B.G. Xiao, M. Haglund, S. Fredrikson, and H. Link. 1996. Multiple sclerosis: the proinflammatory cytokines lymphotoxin-α and tumour necrosis factor-α are upregulated in cerebrospinal fluid mononuclear cells. J. Neuroimmunol. 66:115-123.
5. Issazadeh, S., A. Ljungdahl, D. Hojeburg, M. Mustafa, and T. Olsson. 1995. Cytokine production in the central nervous system of Lewis rats with experimental autoimmune encephalomyelitis: dynamics of mRNA expression for interleukin-10, interleukin-12, cytolysin, tumor necrosis factor-α and tumor necrosis factor-β. J. Neuroimmunol. 61:205-212.
6. Powell, M.B., D. Mitchell, J. Lederman, J. Buckmeier, S.S. Zamvil, M. Graham, N.H. Ruddle, and L. Steinman. 1990. Lymphotoxin and tumor necrosis factor-alpha production by myelin basic protein-specific T cell clones correlates with encephalitogenicity. Int. Immunol. 2:539-544.
7. Zipp, F., F. Weber, S. Huber, S. Sotgiu, A. Czlonkowska, E. Holler, E. Albert, E.H. Weiss, H. Wekerle, and R. Hohlfeld. 1995. Genetic control of multiple sclerosis: increased production of lymphotoxin and tumor necrosis factor-alpha by HLA-DR2+ T cells. Ann. Neurol. 38:723-730.
8. Voskuhl, R.R., R. Martin, C. Bergman, M. Dalal, N.H. Ruddle, and H.F. McFarland. 1993. T helper 1 (Th1) functional phenotype of human myelin basic protein-specific T lymphocytes. Autoimmunity. 15:137-143.
9. Lafaille, J.J., F. Van de Keere, A.L. Hsu, J.L. Baron, W. Haas, C.S. Raine, and S. Tonegawa. 1997. Myelin basic protein-specific T helper 2 (Th2) cells cause experimental autoimmune encephalomyelitis in immunodeficient hosts rather than protect them from disease. J. Exp. Med. 186:307-312.
10. Selmaj, K., C.S. Raine, M. Farooq, W.T. Norto, and C.F. Brosnan. 1991. Cytokine cytotoxicity against oligodendrocytes. Apoptosis induced by lymphotoxin. J. Immunol. 147:1522-1529.
11. Selmaj, K., W. Papierz, A. Glabinski, and T. Kohno. 1995. Prevention of chronic relapsing experimental autoimmune encephalomyelitis by soluble tumor necrosis factor receptor 1. J. Neuroimmunol. 56:135-141.
12. Körner, H., A.L. Goodsall, F.A. Lemckert, B.J. Scallon, J. Ghrayeb, A.L. Ford, and J.D. Sedgwick. 1995. Unimpaired autoreactive T-cell traffic within the central nervous system during tumor necrosis factor receptor-mediated inhibition of experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 92:11066-11070.
13. Baker, D., D. Butler, B.J. Scallon, J.K. O'Neill, J.L. Turk, and M. Feldmann. 1994. Control of established experimental allergic encephalomyelitis by inhibition of tumor necrosis factor (TNF) activity within the central nervous system using monoclonal antibodies and TNF receptor-immunoglobulin fusion protein. Eur. J. Immunol. 24:2040-2048.
14. Bazzoni, F., and B. Beutler. 1996. The tumor necrosis factor ligand and receptor families. N. Engl. J. Med. 334:1717-1725.
15. Borgstrom, P., G.K. Hughes, P. Hansell, B.A. Wolitsky, and P. Sriramarao. 1997. Leukocyte adhesion in angiogenic blood vessels. Role of P-selectin, P-selectin, and beta2 integrin in lymphotoxin-mediated leukocyte recruitment in tumor microvessels. J. Clin. Invest. 99:2246-2253.
16. Sarin, A., A. Conan, M. Cibotti, and P.A. Henkart. 1995. Cytotoxic effect of TNF and lymphotoxin on T lymphoblasts. J. Immunol. 155:3716-3718.
17. Browning, J.L., A. Ngam-ek, P. Lawton, J. DeMarinis, R. Tizard, E.P. Chow, C. Hession, B. O'Brine-Greco, S.F. Foley, and C.F. Ware. 1993. Lymphotoxin β, a novel member of the TNF family that forms a heteromeric complex with lymphotoxin on the cell surface. Cell. 72:847-856.
18. Pokholok, D.K., I.G. Maroulakou, D.V. Kuprash, M.B. Alimzhanov, S.V. Kozlov, T.I. Novobrantseva, R.L. Turetskaya, J.E. Green, and S.A. Nedospasov. 1995. Cloning and expression analysis of the murine lymphotoxin β gene. Proc. Natl. Acad. Sci. USA. 92:674-678.
19. Crowe, P.D., T.L. VanArsdale, B.N. Walter, C.F. Ware, C. Hession, B. Ehrenfels, J.L. Browning, W.S. Din, R.G. Goodwin, and C.A. Smith. 1994. A lymphotoxin-β-specific receptor. Science. 264:707-709.
20. De Togni, P., J. Goellner, N.H. Ruddle, P.R. Streeter, A. Fick, S. Mariathasan, S.C. Smith, R. Carlson, L.P. Shornick, J. Strauss-Schoenberger, et al. 1994. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science. 264:703-707.
21. Banks, T., B. Rouse, M. Kerley, P. Blair, V. Godfrey, N. Kulkin, D. Bouley, J. Thomas, S. Kanangat, and M. Mucenski. 1995. Lymphotoxin alpha deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness. J. Immunol. 155:1685-1693.
22. Browning, J., K. Miatkowski, I. Sizing, D. Griffiths, M. Zafari, C. Benjamin, W. Meier, and F. Mackay. 1996. Signaling through the lymphotoxin β receptor induces the death of some adenocarcinoma tumor lines. J. Exp. Med. 183:867-878.
23. Körner, H., D.S. Riminton, D.H. Strickland, F.A. Lemckert, J. Pollard, and J.D. Sedgwick. 1997. Critical points of tumor necrosis factor action in central nervous system autoimmune inflammation defined by gene targeting. J. Exp. Med. 186:1585-1590.
24. Frei, K., H.-P. Eugster, M. Bopst, C. Constantinescu, E. Lavi, and A. Fontana. 1997. Tumor necrosis factor α and lymphotoxin α are not required for induction of acute experimental autoimmune encephalomyelitis. J. Exp. Med. 185:2177-2182.
25. Suen, W.E., C.M. Bergman, P. Hjelmström, and N.H. Ruddle. 1997. A critical role for lymphotoxin in experimental allergic encephalomyelitis. J. Exp. Med. 186:1233-1240.
26. Koni, P.A., R. Sacca, P. Lawton, J.L. Browning, N.H. Ruddle, and R.A. Flavell. 1997. Distinct roles in lymphoid organogenesis for lymphotoxins α and β revealed in lymphotoxin β-deficient mice. Immunity. 6:491-500.
27. Müller, U., C.V. Jongeneel, S.A. Nedospasov, K.F. Lindahl, and M. Steinmetz. 1987. Tumor necrosis factor and lymphotoxin genes map close to H-2D in the mouse major histocompatibility complex. Nature. 325:265-267.
28. Theofilopoulos, A.N. 1995. The genetic basis of autoimmunity: part II genetic predisposition. Immunol. Today. 16:150-159.
29. Körner, H., M. Cook, D.S. Riminton, F.A. Lemckert, R.M. Hoek, B. Ledermann, F. Köntgen, B. Fazekas de St. Groth, and J.D. Sedgwick. 1997. Distinct roles for lymphotoxin-α and tumor necrosis factor in organogenesis and spatial organisation of lymphoid tissue. Eur. J. Immunol. 27:2600-2609.
30. Mosmann, T.R., and S. Sad. 1996. The expanding universe of T-cell subsets: Th1, Th2, and more. Immunol. Today. 17:138-146.
31. Mariathasan, S., M. Matsumoto, F. Baranyay, M.H. Nahm, O. Kanagawa, and D.D. Chaplin. 1995. Absence of lymph nodes in lymphotoxin-alpha (LT α)-deficient mice is due to abnormal organ development, not defective lymphocyte migration. J. Inflamm. 45:72-78.
32. Spanopoulou, E., C.A. Roman, L.M. Corcoran, M.S. Schlissel, D.P. Silver, D. Nemazee, M.C. Nussenzweig, S.A. Shinton, R.R. Hardy, and D. Baltimore. 1994. Functional immunoglobulin transgenes guide ordered B-cell differentiation in Rag-1-deficient mice. Genes Dev. 8:1030-1042.
33. Nedospasov, S.A., B. Hirt, A.N. Shakhov, V.N. Dobrynin, E. Kawashima, R.S. Accolla, and C.V. Jongeneel. 1986. The genes for tumor necrosis factor (TNF-alpha) and lymphotoxin (TNF-beta) are tandemly arranged on chromosome 17 of the mouse. Nucleic Acids Res. 14:7713-7725.
34. Köntgen, F., G. Süss, C. Stewart, M. Steinmetz, and H. Blüthmann. 1993. Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int. Immunol. 5:957-964.
35. Stewart, C.L., M. Vanek, and E.F. Wagner. 1985. Expression of foreign genes from retroviral vectors in mouse teratocarcinoma chimaeras. EMBO (Eur. Mol. Biol. Organ.) J. 4:3701-3709.
36. Galli-Taliadoros, L.A., S.A. Wood, J.D. Sedgwick, and H. Körner. 1995. Gene knockout technology: a methodological overview for the interested novice. J. Immunol. Methods. 181:1-15.
37. Lemckert, F.A., J.D. Sedgwick, and H. Körner. 1997. Gene targeting in C57BL/6 ES cells. Successful germ line transmission using recipient BALB/c blastocysts developmentally matured in vitro. Nucleic Acids Res. 25:917-918.
38. Laird, P., A. Zilderveld, K. Linders, M. Rudnicki, R. Jaenisch, and A. Berns. 1991. Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19:4293.
39. Chomczynski, C., and N. Sacchi. 1987. Single step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal. Biochem. 162:156-159.
40. Bhattacharya, A., M.E. Dorf, and T.A. Springer. 1981. A shared alloantigenic determinant on Ia antigens encoded by the I-A and I-E subregions: evidence for I region gene duplication. J. Immunol. 127:2488-2495.
41. Shen, F.W., J.S. Tung, and E.A. Boyse. 1986. Further definition of the Ly-5 system. Immunogenetics. 24:146-149.
42. Ford, A., A. Goodsall, W. Mickey, and J.D. Sedgwick. 1995. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex-vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J. Immunol. 154:43119-1321.
43. MacKay, F., P.R. Bourdon, D.A. Griffiths, P. Lawton, M. Zafari, I.R. Sizing, K. Miatkowski, A. Ngamek, C.D. Benjamin, C. Hession, et al. 1997. Cytotoxic activities of recombinant soluble murine lymphotoxin-α and lymphotoxin-α/β complexes. J. Immunol. 159:3299-3310.
44. Scallon, B.J., H. Trinh, M. Nedelmann, F.M. Brennan, M. Feldmann, and J. Ghrayeb. 1995. Functional comparisons of different tumour necrosis factor receptor/IgG fusion proteins. Cytokine. 7:759-770.
45. Eugster, H.-P., M. Muller, U. Karer, B. Car, B. Schnyder, V. Eng, G. Woerly, M. Le Hir, F. di Padova, M. Aguet, et al. 1996. Multiple immune abnormalities in tumor necrosis factor and lymphotoxin-α double deficient mice. Int. Immunol. 8:23-36.
46. Linington, C., M. Bradl, H. Lassmann, C. Brunner, and K. Vass. 1988. Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am. J. Pathol. 130:443-454.
47. Lieberman, A.P., P.M. Pitha, H.S. Shin, and M.L. Shin. 1989. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc. Natl. Acad. Sci. USA. 86:6348-6352.
48. Pasparakis, M., L. Alexopoulou, V. Episkopou, and G. Kollias. 1996. Immune and inflammatory responses in TNFα-deficient mice: a critical requirement for TNF-α in the formation of primary B cell follicles, follicular dendritic cell networks, and germinal centers, and in the maturation of the humoral immune response. J. Exp. Med. 184:1397-1411.
49. Rennert, P.D., J.L. Browning, R. Mebius, F. Mackay, and P.S. Hochman. 1996. Surface lymphotoxin α/β complex is required for the development of peripheral lymphoid organs. J. Exp. Med. 184:1999-2006.
50. Karpus, W.J., N.W. Lukacs, B.L. McRae, R.M. Stricter, S.L. Kunkel, and S.D. Miller. 1995. An important role for the chemokine macrophage inflammatory protein-1 alpha in the pathogenesis of the T cell-mediated autoimmune disease, experimental autoimmune encephalomyelitis. J. Immunol. 155:5003-5010.
51. Gijbels, K., R.E. Galardy, and L. Steinman. 1994. Reversal of experimental autoimmune encephalomyelitis with a hydroxamate inhibitor of matrix metalloproteases. J. Clin. Invest. 94:2177-2182.
52. Chandler, S., K.M. Miller, J.M. Clements, J. Lury, D. Corkill, D.C.C. Anthony, S.E. Adams, and A.J.H. Gearing. 1997. Matrix metalloproteinases, tumor necrosis factor and multiple sclerosis: an overview. J. Neuroimmunol. 72:155-161.
53. Klinkert, W.E.F., K. Kojima, W. Lesslauer, W. Rinner, H. Lassmann, and H. Wekerle. 1997. TNF-α receptor fusion protein prevents experimental autoimmune encephalomyelitis and demyelination in Lewis rats: an overview. J. Neuroimminol. 72:163-168.
54. Kratz, A., A. Campos-Neto, M.S. Hanson, and N.H. Ruddle. 1996. Chronic inflammation caused by lymphotoxin is lymphoid neogenesis. J. Exp. Med. 183:1461-1462.