Review: Cytokines and the pathogenesis of multiple sclerosis

Journal of Neuroscience Research

Volumn 45, Issue 4, 1996, Pages 322-333

  Navikas, V ^a   Link, H ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

autoimmunity; cerebrospinal fluid; cytokines; multiple sclerosis; optic neuritis

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 4; INTERLEUKIN 6; LYMPHOTOXIN; PERFORIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; AUTOIMMUNITY; CENTRAL NERVOUS SYSTEM; CYTOLYSIS; IMMUNE RESPONSE; IMMUNOREGULATION; MONONUCLEAR CELL; MULTIPLE SCLEROSIS; NONHUMAN; OPTIC NERVE DISEASE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REMISSION; REVIEW;

CYTOKINES; HUMANS; MULTIPLE SCLEROSIS;

EID: 0029762023     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19960815)45:4<322::AID-JNR1>3.0.CO;2-B     Document Type: Review

References (101)

1. Ando DG, Clayton J, Kono D, Urban JL, Sercarz E (1989): Encephalitogenic T cells in the B10.PL model of experimental allergic encephalomyelitis (EAE) are of Th1 lymphokine subtype. Cell Immunol 124:132-143.
2. Baig S, Olsson T, Jian Y-P, Höjeberg B, Cruz M, Link H (1991): Multiple sclerosis: Cells secreting antibodies against myelin-associated glycoprotein are present in CSF. Scand J Immunol 33:73-79.
3. Barten DM, Ruddle NH (1994): Vascular cell adhesion molecule-1 modulation by tumor necrosis factor in experimental allergic encephalomyelitis. J Neuroimmunol 51:123-133.
4. Beck J, Rondot P, Catinot L, Falcoff E, Kirchner H, Wietzerbin J (1988): Increased production of interferon gamma and tumor necrosis factor precedes clinical manifestations in multiple sclerosis: Do cytokines trigger off exacerbations? Acta Neurol Scand 78:318-323.
5. Beck J, Rondot P, Jullien P, Wietzerbin J, Lawrence DA (1991): TGF-β-like activity produced during regression of exacerbations in multiple sclerosis. Acta Neurol Scand 84:452-455.
6. Bernard CCA, Mandel TE, Mackay IR (1992): Experimental models of human autoimmune diseases: Overview and prototypes. In Rose NR, Mackay IR (eds): "The Autoimmune Diseases II." San Diego: Academic Press, pp 47-106.
7. Brosnan CF, Selmaj K, Raine CS (1988): Hypothesis: A role for tumor necrosis factor in immune-mediated demyelination and its relevance to multiple sclerosis. J Neuroimmunol 18:87-94.
8. Cannella B, Raine CS (1989): Cytokines up-regulate la expression in organotypic cultures of CNS tissue. J Neuroimmunol 24:239-248.
9. Cannella BC, Raine CS (1995): The adhesion molecules and cytokine profile of multiple sclerosis lesion. Ann Neurol 37:424-435.
10. Carson WE, Giri JG, Lindemann MJ, Linett ML, Ahdieh M, Paxton R, Anderson D, Eisenmann J, Grabstein K, Caligiuri MA (1994): Interleukin 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J Exp Med 180:1395-1403.
11. Cash E, Minty A, Ferrara P, Caput D, Fradelizi D, Rott O (1994): Macrophage-inactivating IL-13 suppresses experimental autoimmune encephalomyelitis in rats. J Immunol 153:4258-4267.
12. Cavender DE, Edelbaum D, Ziff M (1989): Endothelial cell activation induced by tumor necrosis factor and lymphotoxin. Am J Pathol 134:551-560.
13. Chen Y, Kuchroo VK, Inobe JI, Hafler DA, Weiner HL (1994): Regulatory T cell clones induced by oral tolerance. Suppression of autoimmune encephalomyelitis. Science 265:1237-1240.
14. Clerici M, Shearer GM (1994): The Th1-Th2 hypothesis of HIV infection: New insights. Immunol Today 12:575-581.
15. Czerkinsky C, Andersson G, Ekre HP, Nilsson LA, Klareskog L, Ouchterlony Ö (1988): Reverse ELISPOT assay for clonal analysis of cytokine production. I. Enumeration of gamma interferon secreting cells. J Immunol Methods 25:29-36.
16. Dagerlind Å, Friberg K, Bean AJ, Hökfeld T (1992): Sensitive mRNA detection using unfixed tissue: Combined radioactive and nonradioactive in situ hybridization histochemistry. Histochemistry 98:39-49.
17. Duong TT, St-Louis J, Gilbert JJ, Finkelman FD, Strejan GH (1992): Effect of antiinterferon-gamma and antiinterleukin 2 monoclonal antibody treatment on the development of actively and passively induced experimental allergic encephalomyelitis in the SJL/J mouse. J Neuroimmunol 36:105-115.
18. Durelli L, Bongioanni MR, Cavallo R, Ferrero B, Ferri R, Ferrio MF, Bradac GB, Riva A, Vai S, Geuna M, Bergamini L, Bergamasco B (1994): Chronic systemic high-dose recombinant interferon alpha-2a reduces exacerbation rate, MRI signs of disease activity and lymphocyte interferon gamma production in relapsing-remitting multiple sclerosis. Neurology 44:406-413.
19. Elliott MJ, Maini RN, Feldmann M, Long-Fox A, Charles P, Katsikis P, Brennan FM, Walker J, Bijl H, Ghrayeb J (1993): Treatment of rheumatoid arthritis with chimeric monoclonal antibodies to TNF-α. Arth Rheum 36:1681-1690.
20. Fargeas C, You Wu C, Nakajima T, Cox D, Nutman T, Delespese G (1992): Differential effects of transforming growth factor β on the synthesis of Th1- and Th2-like lymphokines in human T lymphocytes. Bur J Immunol 22:2173-2176.
21. Franciota DM, Grimaldi LM, Martino GV, Piccolo G, Bergamaschi R, Citterio A, Melzi GV (1989): Tumor necrosis factor in serum and cerebrospinal fluid of patients with multiple sclerosis. J Exp Med 26:787-789.
22. Frei K, Malipiero UV, Leist TP, Zinkernagel TP, Schwab ME, Fontana A (1989): On the cellular source and function of interleukin 6 produced in the central nervous system in viral diseases. Eur J Immunol 19:689-694.
23. Frei K, Fredrikson S, Fontana A, Link H (1991): Interleukin-6 is elevated in plasma in multiple sclerosis. J Neuroimmunol 31:147-153.
24. Gallo P, Piccinno MG, Krzalic L, Tavolato B (1989): Tumor necrosis factor alpha (TNF-α) and neurological diseases. Failure in detecting TNF-α in the cerebrospinal fluid from patients with multiple sclerosis, AIDS dementia complex, and brain tumors. J Neuroimmunol 23:41-44.
25. Gallo P, Piccinno MG, Tavolato B, Siden Å (1991): A longitudinal study on IL-2, sIL-2, IL-4 and gamma IFN in multiple sclerosis CSF and serum. J Neurol Sci 101:227-232.
26. Genain CP, Roberts T, Davis RL, Nguyen MH, Uccelli A, Faulds D, Li Y, Hedgpeth J, Hauser S (1995): Prevention of autoimmune demyelination in nonhuman primates by cAMP-specific phosphodiesterase inhibitor. Proc Natl Acad Sci USA 92:3601-3605.
27. Hauser SL, Doolittle TH, Lincoln R, Brown RH, Dinarello CA (1990): Cytokine accumulations in CSF of multiple sclerosis patients: Frequent detection of IL-1 and tumor necrosis factor but not interleukin-6. Neurology 40:1735-1739.
28. Hillert J, Olerup O (1993): Multiple sclerosis is associated with genes within or close to the HLA-DR-DQ subregion on a normal DR15,DQ6,Dw2 haplotype. Neurology 43:163-168.
29. Interferon-β Multiple Sclerosis Group (1993): Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. Neurology 43:662-667.
30. Issazadeh S, Mustafa M, Ljungdahl Å, Höjeberg B, Dagerlind Å, Elde R, Olsson T (1995): Interferon-γ, interleukin-4 and transforming growth factor-β in experimental allergic encephalomyelitis in Lewis rats: Dynamics of cellular mRNA expression in the central nervous system and lymphoid cells. J Neurosci Res 40:579-590.
31. Janeway CA, Travers P (eds; 1994): "Immunobiology. The Immune Cytokines in Multiple Sclerosis 331 System in Health and Disease." Oxford: Blackwell Scientific Publications.
32. Kägi D, Ledermann B, Burki K, Seiler P, Odermatt B, Olsen KJ, Podack ER, Zinkernagel RM, Hengartner H (1994): Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369:31-37.
33. + suppressor cells of autoimmune encephalomyelitis respond to T cell receptor-associated determinants on effector cells by interleukin-4 secretion. Eur J Neurosci 22:1757-1763.
34. Khoury SJ, Hancock WW, Weiner HL (1992): Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of transforming growth factor β, interleukin 4 and prostaglandin E in the brain. J Exp Med 176:1355-1364.
35. Kuchroo VK, Das MP, Brown AM, Ranger AM, Zamvil SS, Sobel RA, Weiner HL, Nabovi N, Glimcher LH (1995): B7-1 and B7-2 costimulatory molecules activate differentially the Th1/ Th2 developmental pathways: Application to autoimmune disease therapy. Cell 80:707-718.
36. + T cells: Their activation and effector functions. Curr Opin Immunol 6:453-457.
37. Leonard JP, Waldburger KE, Goldman SJ (1995): Prevention of experimental autoimmune encephalomyelitis by antibodies against interleukin 12. J Exp Med 181:381-386.
38. Lieberman AP, Pitha PM, Shin HS, Shin ML (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.
39. Link H, Sun JB, Wang ZY, Xu Z, Löve A, Fredrikson S, Olsson T (1992): Virus-reactive and autoreactive T cells are accumulated in cerebrospinal fluid in multiple sclerosis. J Neuroimmunol 78:63-73.
40. Link J, Söderström M, Olsson T, Höjeberg B, Ljungdahl Å, Link H (1994a): Increased transforming growth factor-β, interleukin-4 and interferon-γ in multiple sclerosis. Ann Neurol 36:379-386.
41. Link J, Söderström M, Ljungdahl Å, Höjeberg B, Olsson T, Xu Z, Fredrikson S, Wang Z-Y (1994b): Organ-specific autoantigens induce interferon-γ and interleukin-4 mRNA expression in mononuclear cells in multiple sclerosis and myasthenia gravis. Neurology 44:728-734.
42. Link J, Fredrikson S, Söderström M, Olsson T, Höjeberg B, Ljungdahl Å, Link H (1994c): Organ-specific autoantigens induce transforming growth factor-β mRNA expression in mononuclear cells in multiple sclerosis and myasthenia gravis. Ann Neurol 35:197-203.
43. Link J, Söderström M, Kostulas V, Olsson T, Höjeberg B, Ljungdahl Å, Link H (1994d): Optic neuritis is associated with myelin basic protein and proteolipid protein reactive cells producing IFN-γ, IL-4 and TGF-β. J Neuroimmunol 49:9-18.
44. Link J, He B, Navikas V, Palasik W, Fredrikson S, Söderström M, Link H (1995): TGF-β suppresses autoantigen-induced expression of proinflammatory cytokines but not of IL-10 in multiple sclerosis and myasthenia gravis. J Neuroimmunol 58:21-35.
45. Lu CZ, Jensen MA, Arnason BGW (1993): Interferon γ- and interleukin-4-secreting cells in multiple sclerosis. J Neuroimmunol 46:123-128.
46. Maimone D, Gregory S, Arnason BG, Reder AT (1991): Cytokine levels in the cerebrospinal fluid and serum of patients with multiple sclerosis. J Neuroimmunol 32:67-74.
47. Maimone D, Reder AT, Gregory S (1993): T-cell lymphokine-induced secretion of cytokines from patients with multiple sclerosis. Cell Immunol 146:96-106.
48. Mchugh SM, Rifkin IR, Deighton J, Wilson AB, Lachmann PJ, Lockwood CM, Ewan PW (1995): The immunosuppressive drug thalidomide induces T helper type 2 (Th2) and concomitantly inhibits Th1 cytokine production in mitogen- and antigen-stimulated human peripheral blood mononuclear cell cultures. Clin Exp Immunol 99:160-167.
49. Mokhtarian F, Shi Y, Shirazian D, Morgante L, Miller A, Grob D (1994): Defective production of antiinflammatory cytokine, TGF-β by T cell lines of patients with active multiple sclerosis. J Immunol 152:6003-6010.
50. Mosmann TR, Sad S (1996): The expanding universe of T cell subsets: Th1, Th2 and more. Immunol Today 17:138-146.
51. Mustafa M, Vingsbo C, Olsson T, Ljungdahl Å, Höjeberg B, Holmdahl R (1993): The major histocompatibility complex influences myelin basic protein 63-88 induced EAE in rats. Bur J Immunol 23:3089-3095.
52. Navikas V, Link J, Wahren B, Persson C, Link H (1994): Increased levels of IFN-γ, IL-4 and TGF-β mRNA expressing blood mononuclear cells in human HIV infection. Clin Exp Immunol 96:59-63.
53. Navikas V, Link J, Persson C, Olsson T, Höjeberg B, Ljungdahl Å, Link H, Wahren B (1995a): Increased mRNA expression of IL-6, IL-10, TNF-α and perforin in blood mononuclear cells in human HIV infection. J AIDS Hum Retrovirology 5:484-489.
54. Navikas V, Link J, Palasik W, Söderström M, Fredrikson S, Olsson T, Link H (1995b): Increased mRNA expression of IL-10 in mononuclear cells in multiple sclerosis and optic neuritis. Scand J Immunol 41:171-178.
55. Navikas V, He B, Link J, Haglund M, Söderström M, Fredrikson S, Höjeberg B, Qiao J, Olsson T, Link H (1996a): Augmented expression of tumor necrosis factor-α and lymphotoxin mRNA in mononuclear cells in multiple sclerosis and optic neuritis. Brain 119:213-223.
56. Navikas V, Matusevicius D, Söderström M, Fredrikson S, KivisäkkP, Ljungdahl Å, Höjeberg B, Link H (1996b): Increased IL-6 mRNA expression in blood and cerebrospinal fluid mononuclear cells in multiple sclerosis. J Neuroimmunol 64:63-69.
57. Noronha A, Toscas A, Jensen MA (1993): Interferon beta decreases T cell activation and interferon gamma production in multiple sclerosis. J Neuroimmunol 46:145-153.
58. Noseworthy JH, Rodriguez M, Jiang NS, Sneve DM, Carter JL, Shuster EA, Rubino FA (1993): TNF-α in multiple sclerosis. Neurology (Abstr) 43:A355.
59. Olsson T, Baig S, Höjeberg B, Link H (1990a): Antimyelin basic protein and antimyelin antibody-producing cells in multiple sclerosis. Ann Neurol 27:132-136.
60. Olsson T, Wang WZ, Höjeberg B, Kostulas V, Yiang YP, Andersson G, Ekre HP, Link H (1990b): Autoreactive T lymphocytes in multiple sclerosis determined by antigen induced secretion of interferon-gamma. J Clin Invest 86:981-985.
61. Oswald IP, Wynn TA, Sher A, James SJ (1992): Interleukin-10 inhibits macrophage microbial activity by blocking the endogenous production of tumor necrosis factor α required as a costimulatory factor for interferon γ-induced activation. Proc Natl Acad Sci USA 89:8676-8680.
62. Panitch HS, Hirsch L, Schindler J, Johnson KP (1987): Treatment of multiple sclerosis with gamma interferon: Exacerbations associated with activation of the immune system. Neurology 37:1097-1102.
63. Peter JB, Boctor FN, Tourtellotte WW (1991): Serum and CSF levels of IL-2, sIL-2R, TNF-α, and IL-1β in chronic progressive multiple sclerosis: Expected lack of clinical utility. Neurology 41:121-123.
64. Prineas JW, Wright RG (1978): Macrophages, lymphocytes, and plasma cells in the perivascular compartment in chronic multiple sclerosis. Lab Invest 38:409-421.
65. Racke M, Dhib-Jalbut S, McFarland H, McFarlin D (1990): Modification of murine experimental allergic encephalomyelitis with cytokines. Ann Neurol (Abstr) 28:24.
66. Racke MK, Bonomo A, Scott DE, Cannella B, Levine A, Raine CS, Shevach M, Röcken M (1994): Cytokine-induced immune deviation as a therapy for inflammatory autoimmune disease. J Exp Med 180:1961-1966.
67. Raine C (1994): The Dale E. McFarlin memorial lecture: The immunology of the multiple sclerosis lesion. Ann Neurol 36:S61-S72.
68. Reiner SL, Locksley RM (1995): The regulation of immunity to Leishmania major. Annu Rev Immunol 13:151-177.
69. Rieckmann P, Albrecht M, Kitze B, Weber T, Tumani H, Broocks A, Luer W, Poser S (1994): Cytokine mRNA levels in mononuclear blood cells from patients with multiple sclerosis. Neurology 44:1523-1526.
70. Rieckmann P, Albrecht M, Kitze B, Weber T, Tumani H, Broocks A, Luer W, Helwig A, Poser S (1995): Tumor necrosis factor-α messenger RNA expression in patients with relapsing-remitting multiple sclerosis is associated with disease activity. Ann Neurol 37:82-88.
71. Rodriguez M, Pavelko KD, McKinney CW, Leibowitz JL (1994): Recombinant human IL-6 suppresses demyelination in a viral model of multiple sclerosis. I Immunol 153:3811-3821.
72. Romagnani S (1994): Lymphokine production by human T cells in disease states. Annu Rev Immunol 12:227-257.
73. Rott O, Fleischer B, Cash E (1994): Interleukin-10 prevents experimental allergic encephalomyelitis in rats. Eur J Immunol 24:1434-1440.
74. Santambrogio L, Crisi GM, Leu J, Hochwald GM, Ryan T, Thorbecke GJ (1995): Tolerogenic forms of auto-antigens and cytokines in the induction of resistance to experimental allergic encephalomyelitis. J Neuroimmunol 58:211-222.
75. Schindler R, Mancilla J, Endres S, Ghorbani R, Clark, SC, Dinarello CA (1990): Correlations and interactions in the production of IL-6, IL-1 and tumor necrosis factor in human blood mononuclear cells. Blood 75:40-47.
76. Schluesener HJ (1990): Transforming growth factors type β1 and β2 suppress rat astrocyte autoantigen presentation and antagonize hyperinduction of class II major histocompatibility complex antigen expression by interferon-γ and tumor necrosis factor-α. J Neuroimmunol 27:41-47.
77. Scolding NJ, Jones J, Compston DA, Morgan BP (1990): Oligodendrocyte susceptibility to injury by T cell perform. Immunology 70:6-10.
78. Selmaj K, Raine CS (1988): Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol 21:339-346.
79. Selmaj K, Raine CS, Cannella B, Brosnan CF (1991a): Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J Clin Invest 87:949-954.
80. Selmaj K, Raine CS, Farooq M, Norton WT, Brosnan CF (1991b): Cytokine cytoloxicity against oligodendrocytes: Apoptosis induced by lymphotoxin. J Immunol 147:1522-1529.
81. Selmaj K, Raine CS, Cross AH (1991c): Antitumor necrosis factor therapy abrogates autoimmune demyelination. Ann Neurol 30:694-700.
82. Sharief MK, Hentges R (1991): Association between tumor necrosis factor-α and disease progression in patients with multiple sclerosis. N Engl J Med 325:467-472.
83. Shull MM, Ormsby I, Kier A, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, Annunzziata N, Doetschman T (1992): Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359:693-699.
84. Sommer N, Löschmann PA, Northoff GH, Weller M, Steinbrecher A, Steinbach JP, Lichtenfels R, Meyermann R, Riethmuller A, Fontana A, Dichgans J, Martin R (1995): The antidepressant rolipram suppresses cytokine production and prevents autoimmune encephalomyelitis. Nature Med 1:244-248.
85. Sun JB, Olsson T, Wang WZ, Xiao B-G, Kostulas V, Fredrikson S, Ekre H-P, Link H (1991a): Autoreactive T and B cells responding to myelin proteolipid protein in multiple sclerosis and controls. Eur J Immunol 21:1461-1468.
86. Sun JB, Link H, Xiao BG, Diener P, Andersson G, Ekre HP, Linington C, Olsson T (1991b): T and B cell responses to myelinoligodendrocyte glycoprotein in multiple sclerosis. J Immunol 146:1490-1495.
87. Thomson A (ed; 1994): "The Cytokine Handbook, 2nd Ed." London: Academic Press.
88. Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW (1994): Interleukin-6 as an anti inflammatory cytokine: Induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 83:113-118.
89. Traugott U, Lebon P (1988): Multiple sclerosis: Involvement of interferons in lesion pathogenesis. Ann Neural 24:243-251.
90. Trinchieri G (1995): Interleukin-12: A proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu Rev Immunol 13:251-276.
91. Tsukada N, Miagi K, Matsuda M, Yanagisawa N, Yone K (1991): Tumor necrosis factor and interleukin-1 in CSF and sera of patients with multiple sclerosis. J Neuroimmunol 102:230-234.
92. Van der Ween R, Stohlman SA (1993): Encephalitogenic Th1 cells are inhibited by Th2 cells with related peptide specificity: Relative roles of interleukin (IL)-4 and IL-10. J Neuroimmunol 48:213-220.
93. Vartanian T, Li Y, Zhao M, Stefansson K (1995): Interferon-γ-induced oligodendrocyte cell death: Implications for the pathogenesis of multiple sclerosis. Mol Med 1:732-742.
94. Vassalli P (1992): The pathophysiology of tumor necrosis factors. Annu Rev Immunol 10:411-452.
95. Voorthuis JAC, Uitdehaag BMJ, De Groot CJA, Goede PH, Van der Meide P (1990): Suppression of experimental allergic encephalomyelitis by intravenous administration of interferon-gamma in Lewis rats. Clin Exp Immunol 81:183-188.
96. Wang WZ, Olsson T, Kostulas V, Höjeberg B, Ekre HP, Link H (1992): Myelin antigen reactive T cells in cerebrovascular diseases. Clin Exp Immunol 88:157-162.
97. Willenborg DO, Fordham SA, Cowden WB, Ramshaw IA (1995): Cytokines and murine autoimmune encephalomyelitis: Inhibition or enhancement of disease with antibodies to select cytokines, or by delivery of exogenous cytokines using recombinant Vaccinia virus system. Scand J Immunol 1:31-42.
98. Windhagen A, Newcombe J, Dangond F, Strand C, Woodroofe MN, Cuzner ML, Hafler D (1995): Expression of costimulatory molecules B7-1 (CD80), B7-2 (CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J Exp Med 182:1985-1996.
99. Wogensen L, Lee MS, Servetnick N (1994): Production of interleukin 10 by islets cells accelerates immune-mediated destruction of beta cells in non-obese diabetic mice. J Exp Med 179:1379-1384.
100. Woodroofe MN, Cuzner ML (1993): Cytokine mRNA expression in inflammatory multiple sclerosis lesions: Detection by nonradioactive in situ hybridization. Cytokine 5:583-588.
101. Zoja C, Wang JM, Bettoni S, Sironi M, Renzi D, Chiaffarino F, Abboud HE, Van Damme J, Antovani A, Remuzzi G, Rambaldi A (1991): Interleukin-1β and tumor necrosis factor-α induce gene expression and production of leucocyte chemotactic factors, colony-stimulating factors, and interleukin-6 in human mesangial cells. Am J Pathol 138:991-1003.