The role of TNFα and lymphotoxin in demyelinating disease

Annals of the Rheumatic Diseases

Volumn 58, Issue SUPPL. 1, 1999, Pages

  Lock, Christopher ^a   Oksenberg, Jorge ^b   Steinman, Lawrence ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOCKING AGENT; LYMPHOTOXIN; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC ENCEPHALOMYELITIS; CYTOKINE PRODUCTION; DEMYELINATING DISEASE; GENE TECHNOLOGY; HUMAN; IMMUNOPATHOGENESIS; KNOCKOUT MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSGENIC MOUSE; IMMUNOLOGY;

DEMYELINATING DISEASES; HUMANS; LYMPHOTOXIN-ALPHA; MULTIPLE SCLEROSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0032748352     PISSN: 00034967     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (108)

1. Steinman L. Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system. Cell 1996;85:299-302.
2. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L, Axonal transection in the lesions of multiple sclerosis [see comments]. N Engl J Med 1998;338:278-85.
3. Hartung HP. Pathogenesis of inflammatory demyelination: implications for therapy. Curr Opin Neurol 1995;8:191-9.
4. Warren KG, Catz I, Steinman L. Fine specificity of the antibody response to myelin basic protein in the central nervous system in multiple sclerosis: the minimal B-cell epitope and a model of its features. Proc Natl Acad Sci USA 1995;92:11061-5.
5. Genain CP, Cannella B, Hauser SL, Raine CS. Identification of autoantibodies associated with myelin damage in multiple sclerosis [see comments]. Nat Med 1999,5:170-5.
6. Steinman L. Some misconceptions about understanding autoimmunity through experiments with knockouts. J Exp Med 1997;185:2039-41.
7. Renno T, Krakowski M, Piccirillo C, Lin JY, Owens T. TNF-alpha expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. Regulation by Th1 cytokines. J Immunol 1995;154:944-53.
8. Issazadeh S, Ljungdahl A, Hojeberg B, Mustafa M, Olsson T. 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 alpha and tumor necrosis factor beta. J Neuroimmunol 1995;61:205-12.
9. Begolka WS, Vanderlugt CL, Rabbe SM, Miller SD. Differential expression of inflammatory cytokincs parallels progression of central nervous system pathology in two clinically distinct models of multiple sclerosis. J Immunol 1998;161:4437-46.
10. Kuroda Y, Shimamoto Y. Human tumor necrosis factor-alpha augments experimental allergic encephalomyelitis in rats. J Neuroimmunol 1991;34:159-64.
11. Crisi GM, Santambrogio L, Hochwald GM, Smith SR, Carlino JA, Thorbecke GJ. Staphylococcal enterotoxin B and tumor-necrosis factor-alpha-induced relapses of experimental allergic encephalomyelitis: protection by transforming growth factor-beta and interleukin-10. Eur J Immunol 1995;25:3035-40.
12. Selmaj KW, Raine CS. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol 1988;23:339-46.
13. Selmaj K, Raine CS, Farooq M, Norton WT, Brosnan CF. Cytokine cytotoxicity against oligodendrocytes. Apoptosis induced by lymphotoxin. J Immunol 1991;147:1522-9.
14. Jenkins HG, Ikeda H. Tumour necrosis factor causes an increase in axonal transport of protein and demyelination in the mouse optic nerve. J Neurol Sci 1992;108:99-104.
15. Chung IY, Norris JG, Benveniste EN. Differential tumor necrosis factor alpha expression by astrocytes from experimental allergic encephalomyelitis-susceptible and -resistant rat strains. J Exp Med 1991;173:801-11.
16. Powell MB, Mitchell D, Lederman J, et al. Lymphotoxin and tumor necrosis factor-alpha production by myelin basic protein-specific T cell clones correlates with encephalitogenicity. Int Immunol 1990;2:539-44.
17. Karin N, Mitchell DJ, Brocke S, Ling N, Steinman L. Reversal of experimental autoimmune encephalomyelitis by a soluble peptide variant of a myelin basic protein epitope: T cell receptor antagonism and reduction ofinterferon gamma and tumor necrosis factor alpha production. J Exp Med 1994;180:2227-37.
18. Brocke S, Gijbels K, Allegretta M, et al. Treatment of experimental encephalomyelitis with a peptide analogue of myelin basic protein [published erratum appears in Nature 19989;392:630]. Nature 1996;379:343-6.
19. Brocke S, Gaur A, Piercy C, et al. Induction of relapsing paralysis in experimental autoimmune encephalomyelitis by bacterial superantigen. Nature 1993;365:642-4.
20. Dal Canto RA, Shaw MK, Nolan GP, Steinman L, Fathman CG. Local delivery of TNF by retrovirus-transduced T lymphocytes exacerbates experimental autoimmune encephalomyelitis. Clin Immunol 1999;90:10-14.
21. Selmaj K, Raine CS, Cross AH. Anti-tumor necrosis factor therapy abrogates autoimmune demyelination. Ann Neurol 1991;30:694-700.
22. Ruddle NH, Bergman CM, McGrath KM, et al. An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J Exp Med 1990;172:1193-200.
23. Klinkert WE, Kojima K, Lesslauer W, Rinner W, Lassmann H, Wekerle H. TNF-alpha receptor fusion protein prevents experimental auto-immune encephalomyelitis and demyelination in Lewis rats: an overview. J Neuroimmunol 1997;72:163-8.
24. Selmaj K, Papierz W, Glabinski A, Kohno T. Prevention of chronic relapsing experimental autoimmune encephalomyelitis by soluble tumor necrosis factor receptor I. J Neuroimmunol 1995;56:135-41.
25. Baker D, Butler D, Scallon BJ, O'Neill JK, Turk JL, Feldmann M. Control of established experimental allergic encephalomyelitis by inhibition of tumor necrosis factor (TNF) activity within the central nervous system using monoclonal antibodies and TNF receptorimmunoglobulin fusion proteins. Eur J Immunol 1994;24:2040-8.
26. Genain CP, Roberts T, Davis RL, et al. Prevention of autoimmune demyelination in non-human primates by a cAMP- specific phosphodiesterase inhibitor. Proc Natl Acad Sci USA 1995;92:3601-5.
27. Sommer N, Loschmann PA, Northoff GH, et al. The antidepressant rolipram suppresses cytokine production and prevents autoimmune encephalomyelitis [see comments]. Nat Med 1995;1:244-8.
28. Sommer N, Martin R, McFarland HF, et al. Therapeutic potential of phosphodiesterase type 4 inhibition in chronic autoimmune demyelinating disease. J Neuroimmunol 1997;79:54-61.
29. Probert L, Akassoglou K, Pasparakis M, Kontogeorgos G, Kollias G. Spontaneous inflammatory demyelinating disease in transgenic mice showing central nervous system-specific expression of tumor necrosis factor alpha. Proc Natl Acad Sci USA 1995;92:11294-8.
30. Taupin V, Renno T, Bourbonniere L, Peterson AC, Rodriguez M, Owens T. Increased severity of experimental autoimmune encephalomyelitis, chronic macrophage/ microglial reactivity, and demyelination in transgenic mice producing tumor necrosis factor-alpha in the central nervous system. Eur J Immunol 1997;27:905-13.
31. Akassoglou K, Probert L, Kontogeorgos G, Kollias G. Astrocyte-specific but not neuronspecific transmembrane TNF triggers inflammation and degeneration in the central nervous system of transgenic mice. J Immunol 1997;158: 438-45.
32. Akassoglou K, Bauer J, Kassiotis G, et al. Oligodendrocyte apoptosis and primary demyelination induced by local TNF/p55TNF receptor signaling in the central nervous system of transgenic mice: models for multiple sclerosis with primary oligodendrogliopathy. Am J Pathol 1998;153: 801-13
33. Kassiotis G, Bauer J, Akassoglou K, Lassmann H, Kollias G, Probert L. A tumor necrosis, factor-induced model of human primary demyelinating diseases develops in immunodeficient mice. Eur J Immunol 1999;29:912-17.
34. Frei K, Eugster HP, Bopst M, Constantinescu CS, Lavi E, Fontana A. Tumor necrosis factor alpha and lymphotoxin alpha are not required, for induction of acute experimental autoimmune encephalomyelitis. J Exp Med 1997;185: 2177-82.
35. Suen WE, Bergman CM, Hjelmstrom P, Ruddle NH. A critical role for lymphotoxin in experimental allergic encephalomyelitis. J Exp Med 1997;186:1233-40.
36. Sean Riminton D, Korner H, Strickland DH, Lemckert FA, Pollard JD, Sedgwick JD. Challenging cytokinc redundancy: inflammatory cell movement and clinical course of experimental autoimmune encephalomyelitis are normal in lymphotoxin-deficient, but not tumor necrosis factor-deficient, mice. J Exp Med 1998;187:1517-28.
37. Korner H, Riminton DS, Strickland DH, Lemckert FA, Pollard JD, Sedgwick JD. Critical points of tumor necrosis factor action in central nervous system autoimmune inflammation defined by gene targeting. J Exp Med 1997;186:1585-90.
38. Willenborg DO, Fordham SA, Cowden WB, Ramshaw IA, Cytokines and murine autoimmune encephalomyelitis: inhibition or enhancement of disease with antibodies to select cytokines, or by delivery of exogenous cytokines using a recombinant vaccinia virus system. Scand J Immunol 1995;41:31-41.
39. Liu J, Marino MW, Wong G, et al. TNF is a potent antiinflammatory cytokine in autoimmune-mediated demyelination. Nat Med 1998;4:78-83.
40. Baron JL, Madri JA, Ruddle NH, Hashim G, Janeway CA, Jr. Surface expression of alpha 4 integrin by CD4 T cells is required for their entry into brain parenchyma. J Exp Med 1993;177:57-68.
41. Lafaille JJ, Keere FV, Hsu AL, et al. Myelin basic proteinspecific T helper 2 (Th2) cells cause experimental autoimmune encephalomyelitis in immunodeficient hosts rather than protect them from the disease. J Exp Med 1997;186:307-12.
42. Raine CS, Bonetti B, Cannella B. Multiple sclerosis: expression of molecule of the tumor necrosis factor ligand and receptor families in relationship to the demyelinated plaque. Rev Neurol (Paris) 1998;154:577-85.
43. Woodroofe MN, Cuzner ML. Cytokine mRNA expression in inflammatory multiple sclerosis lesions: detection by non-radioactive in situ hybridization. Cytokine 1993;5: 583-8.
44. Selmaj K, Raine CS, Cannella B, Brosnan CF. Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J Clin Invest 1991;87:949-54.
45. Hofman FM, Hinton DR, Johnson K, Merrill JE. Tumor necrosis factor identified in multiple sclerosis brain. J Exp Med 1989;170:607-12.
46. Maimone D, Gregory S, Arnason BG, Reder AT. Cytokine levels in the cerebrospinal fluid and serum of patients with multiple sclerosis. J Neuroimmunol 1991;32;67-74.
47. Hauser SL, Doolittle TH, Lincoln R, Brown RH, Dinarello CA. Cytokine accumulations in CSF of multiple sclerosis patients: frequent detection of interleukin-1 and tumor necrosis factor but not interleukin-6. Neurology 1990;40: 1735-9.
48. Drulovic J, Mostarica-Stojkovic M, Levic Z, Stojsavljevic N, Pravica V, Mesaros S. Interletikin-12 and tumor necrosis factor-alpha levels in cerebrospinal fluid of multiple sclerosis patients. J Neurol Sci 1997;147:145-50.
49. Sharief MK, Hentges R. Association between tumor necrosis factor-alpha and disease progression in patients with multiple sclerosis [see comments]. N Engl J Med 1991;325:467-72.
50. Duchini A, Govindarajan S, Samucci M, Zampi G, Hofman FM. Effects of tumor necrosis factor-alpha and interleukin-6 on fluid-phase permeability and ammonia diffusion in CNS-derived endothelial cells. J Investig Med 1996;44:474-82.
51. Sharief MK, Thompson EJ. In vivo relationship of tumor necrosis factor-alpha to bloodbrain barrier damage in patients with active multiple sclerosis. J Neuroimmunol 1992;38:27-33.
52. Monteyne P, Sindic CJ. Data on cytokine mRNA expression in CSF and peripheral blood mononuclear cells from MS patients as detected by PCR. Multiple Sclerosis 1998;4: 143-6.
53. Matusevicius D, Navikas V, Soderstrom M, et al. Multiple sclerosis: the proinflammatory cytokines lymphotoxin-alpha and tumour necrosis factor-alpha are upregulated in cerebrospinal fluid mononuclear cells. J Neuroimmunol 1996;66:115-23.
54. Mokhtarian F, Shi Y, Shirazian D, Morgante L, Miller A, Grob D. Defective production of anti-inflammatory cytokine, TGF-beta by T cell lines of patients with active multiple sclerosis. J Immunol 1994;152:6003-10.
55. Navikas V, He B, Link J, et al. Augmented expression of tumour necrosis factor-alpha and lymphotoxin in mononuclear cells in multiple sclerosis and optic neuritis. Brain 1996;119:213-23.
56. Correale J, Gilmore W, McMillan M, et al. Patterns of cytokine secretion by autoreactive proteolipid protein- specific T cell clones during ihc course of multiple sclerosis. J Immunol 1995;154:2959-68.
57. Rieckmann P, Albrecht M, Kitze B, et al. Tumor necrosis factor-alpha messenger RNA expression in patients with relapsing-remitting multiple sclerosis is associated with disease activity. Ann Neurol 1995;37:82-8.
58. Martino G, Consiglio A, Franciotia DM, et al. Tumor necrosis factor alpha and its receptors in relapsing-remitting multiple sclerosis. J Neurol Sci 1997;152:51-61.
59. Beck J, Rondot P, Catinot L, Falcoff E, Kirchner H, Wietzerbin J. Increased production of interferon gamma and tumor necrosis factor precedes clinical manifestation in multiple sclerosis: do cytokines trigger off exacerbations? Acta Neurol Scand 1988;78:318-23.
60. Selmaj KW, Farooq M, Norton WT, Raine CS, Brosnan CF. Proliferation of astrocytes in vitro in response to cytokines. A primary role for tumor necrosis factor. J Immunol 1990; 144:129-35.
61. Selmaj K, Shafit-Zagardo B, Aquino DA, et al. Tumor necrosis factor-induced proliferation of astrocytes from mature brain is associated with downregulation of glial fibrillary acidic protein mRNA. J Neurochem 1991;57: 823-30.
62. Oksenberg JR, Seboun E, Hauser SL. Genetics of demyelinating diseases. Brain Pathol 1996;6:289-302.
63. Andersson PB, Goodkin DE. Glucocorticosteroid therapy for multiple sclerosis: a critical review. J Neurol Sci 1998;160:16-25.
64. Rosenberg GA, Dencoff JE, Correa N Jr, Reiners M, Ford CC. Effect of steroids on CSF matrix metalloproteinases in multiple sclerosis: relation to blood-brain barrier injury. Neurology 1996;46:1626-32.
65. Yong VW, Chabot S, Stuve O, Williams G. Interferon beta in the treatmeni of multiple sclerosis: mechanisms of action. Neurology 1998;51:682-9.
66. Chabot S, Williams G, Yong VW, Microglial production of TNF-alpha is induced by acrivated T lymphocytes. Involvement of VLA-4 and inhibition by interferonbeta-lb. J Clin Invest 1997;100:604-12.
67. Noronha A, Tuscas A, Jensen MA. Interferon beta decreases T cell activation and interferon gamma production in multiple sclerosis. J Neuroimmunol 1993;46:145-53.
68. Revel M, Chebath J, Mangelus M, Harroch S, Moviglia GA. Antagonism of interferon beta on interferon gamma: inhibition of signal transduction in vitro and reduction of serum levels in multiple sclerosis patients. Multiple Sclerosis 1995;1 (suppl 1):S5-11.
69. Rudick RA, Ransohoff RM, Peppler R, VanderBrug Medendorp S, Lehmann P, Alam J. Interferon beta induces interleukin-10 expression: relevance to multiple sclerosis. Ann Neurol 1996;40:618-27.
70. McRae BL, Picker LJ, van Seventer GA. Human recombinant interferon-beta influences T helper subset differentiation by regulating cytokine secretion pattern and expression of homing receptors. Eur J Immunol 1997;27:2650-6.
71. McRae BL, Semnani RT, Hayes MP, van Seventer GA. Type I IFNs inhibit human dendritic cell IL-12 production and Thl cell development. J Immunol 1998;160:4298-304.
72. Gayo A, Mozo L, Suarez A, Tunon A, Lahoz C, Gutierrez C. Interferon beta-lb treatment modulates TNFalpha and IFNgamma spontaneous gene expression in MS [see comments]. Neurology 1999;52:1764-70.
73. Rep MH, Hintzen RQ, Polman CH, van Lier RA. Recombinant interferon-beta blocks proliferation but enhances interleukin-10 secretion by activated human T-cells. J Neuroimmunol 1996;67:111-18.
74. Bongioanni P, Mosti S, Moscato G, Lombardo F, Manildo C, Meucci G. Decreases in Tcell tumor necrosis factor alpha binding with interferon beta treatment in patients with multiple sclerosis. Arch Neurol 1999;56:71-8.
75. Stuve O, Dooley NP, Uhm JH, Antel JP, Francis GS, Williams G, et al. Interferon betalb decreases the migration of T lymphocytes in vitro: effects on matrix metalloproteinase-9. Ann Neurol 1996;40:853-63.
76. Leppert D, Waubant E, Burk MR, Oksenberg JR, Hauser SL. Interferon beta-lb inhibits gelatinase secretion and in vitro migration of human T cells: a possible mechanism for treatment efficacy in multiple sclerosis. Ann Neurol 1996; 40:846-52.
77. Miller A, Shapiro S, Gershtein R, et al. Treatment of multiple sclerosis with copolymer-1 (Copaxone): implicating mechanisms of Th1 to Th2/Th3 immune-deviation [In Process Citation]. J Neuroimmunol 1998;92:113-21.
78. van Oosten BW, Barkhof F, Truyen L, et al. Increased MRI activity and immune activation in two multiple sclerosis patients treated with the monoclonal anti-tumor necrosis factor antibody cA2. Neurology 1996;47:1531-4.
79. The Lenercept Multiple Sclerosis Study Group and the University of British Columbia MS/MRI Analysis Group. TNF neutralization in MS: results of a randomized, placebo-controlled multicenter study. Neurology 1999;53: 457-65.
80. Rott O, Cash E, Fleischer B. Phosphodiesterase inhibitor pentoxifylline, a selective suppressor of T helper type 1- but not type 2-associated lymphokine production, prevents induction of experimental autoimmune encephalomyelitis in Lewis rats. Eur J Immunol 1993;23:1745-51.
81. Nataf S, Louboutin JP, Chabannes D, Feve JR, Muller JY. Pentoxifylline inhibits experimental allergic encephalomyelitis. Acta Neurol Scand 1993;88:97-9.
82. Rieckmann P, Weber F, Gunther A, et al. Pentoxifylline, a phosphodiesterase inhibitor, induces immune deviation in patients with multiple sclerosis. J Neuroimmunol 1996;64: 193-200.
83. Myers LW, Ellison GW, Merrill JE, et al. Pentoxifylline is not a promising treatment for multiple sclerosis in progression phase. Neurology 1998;51:1483-6.
84. van Oosten BW, Rep MH, van Lier RA, et al. A pilot study investigating the effects of orally administered pentoxifylline on selected immune variables in patients with multiple sclerosis. J Neuroimmunol 1996;66:49-55.
85. Yong VW, Krekoski CA, Forsyth PA, Bell R, Edwards DR. Matrix metalloproteinases and diseases of the CNS. Trends Neurosci 1998;21:75-80.
86. Goetzl EJ, Banda MJ, Leppert D. Matrix metalloproteinases in immunity. J Immunol 1996;156:1-4.
87. Gottschall PE, Deb S. Regulation of matrix metalloproteinase expressions in astrocytes, microglia and neurons. Neuroimmunomodulation 1996;3:69-75.
88. Apodaca G, Rutka JT, Bouhana K, et al. Expression of metalloproteinases and metalloprotoinase inhibitors by fetal astrocytes and glioma cells. Cancer Res 1990;50:2322-9.
89. Colton CA, Keri JE, Chen WT, Monsky WL. Protease production by cultured microglia: substrate gel analysis and immobilized matrix degradation. J Neurosci Res 1993;35: 297-304.
90. Uhm JH, Dooley NP, Oh LY, Yong VW. Oligodendrocytes utilize a matrix metalloproteinase, MMP-9, to extend processes along an astrocyte extracellular matrix. Glia 1998;22:53-63.
91. Cossins JA, Clements JM, Ford J, et al. Enhanced expression of MMP-7 and MMP-9 in demyelinating multiple sclerosis lesions. Acta Neuropathol (Berl) 1997;94:590-8.
92. Cuzner ML, Davison AN, Rudge P. Proteolytic enzyme activity of blood leukocytes and cerebrospinal fluid in multiple sclerosis. Ann Neurol 1978;4:337-44.
93. Richards PT, Cuzner ML. Proteolytic activity in CSF. Adv Exp Med Biol 1978;100:521-7.
94. Maeda A, Sobel RA. Matrix metalloproteinases in the normal human central nervous system, microglial nodules, and multiple sclerosis lesions. J Neuropathol Exp Neurol 1996; 55:300-9.
95. Cuzner ML, Gveric D, Strand C, et al. The expression of tissue-type plasminogen activator, matrix metalloproteases and endogenous inhibitors in the central nervous system in multiple sclerosis: comparison of stages in lesion evolution. J Neuropathol Exp Neurol 1990;55:1194-204.
96. Leppert D, Ford J, Stabler G, et al. Matrix metalloproteinase-9 (gelatinase B) is selectively elevated in CSF during relapses and stable phases of multiple sclerosis [In Process Citation]. Brain 1998;121:2327-31.
97. Gijbels K, Masure S, Carton H, Opdenakker G. Gelatinase in the cerebrospinal fluid of patients with multiple sclerosis and other inflammatory neurological disorders. J Neuroimmunol 1992;41:29-34.
98. Gijbels K, Proost P, Masure S, Carton H, Billiau A, Opdenakker G. Gelatinase B is present in the cerebrospinal fluid during experimental autoimmune encephalomyelitis and cleaves myelin basic protein. J Neurosci Res 1991;36:412-40.
99. Gijbels K, Galardy RE, Steinman L. Reversal of experimental autoimmune encephalomyelitis with a hydroxamate inhibitor of matrix metalloproteases. J Clin Invest 1994;94: 2177-82.
100. Clements JM, Cossins JA, Wells GM, et al. Matrix metalloproteinase expression during experimental autoimmune encephalomyelitis and effects of a combined matrix metalloproteinase and tumour necrosis factor-alpha inhibitor. J Neuroimmunol 1997;74:85-91.
101. Hewson AK, Smith T, Leonard JP, Cuzner ML. Suppression of experimental allergic encephalomyelitis in the Lewis rat by the matrix metalloproteinase inhibitor Ro31-9790. Inflamm Res 1995;44:345-9.
102. Matyszak MK, Perry VH. Delayed-type hypersensitivity lesions in the central nervous system are prevented by inhibitors of matrix metalloproteinases. J Neuroimmunol 1996;69:441-9.
103. Liedtke W, Cannella B, Mazzaccaro RJ, et al. Effective treatment of models of multiple sclerosis by matrix metalloproteinase inhibitors. Ann Neurol 1998;44:35-46.
104. Dubois B, DiHooghe MB, De Lepcleire K, Ketelaer P, Opdenakker G, Carton H. Toxicity in a double-blind, placebo-controlled pilot trial with D-penicillamine and metacycline in secondary progressive multiple sclerosis. Multiple Sclerosis 1998;4:74-8.
105. Wodicka L, Dong H, Mittmann M, Ho MH, Lockhart DJ. Genome-wide expression monitoring in Saccharomyces cerevisiae. Nat Biotechnol 1997;15:1359-67.
106. Lockhart DJ, Dong H, Byrne MC, et al. Expression monitoring by hybridization to high-density oligonucleotide arrays [see comments]. Nat Biotechnol 1996;14:1675-80.
107. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genomewide expression patterns. Proc Natl Acad Sci USA 1998;95:14863-8.
108. Lander ES. Array of hope. Nat Genet 1999;21(suppl 1):3-4.