Tumor necrosis factor-α: A neuromodulator in the CNS

Neuroscience and Biobehavioral Reviews

Volumn 21, Issue 5, 1997, Pages 603-613

  Pan, Weihong ^a,b   Zadina, James E ^a   Harlan, Richard E ^a   Weber, Joseph T ^a   Banks, William A ^a   Kastin, Abba J ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Blood brain barrier; CNS; Demyelination; Development; Regeneration; TNF

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; CELL INTERACTION; CENTRAL NERVOUS SYSTEM; CYTOTOXICITY; DEMYELINATION; DRUG RECEPTOR BINDING; GLIA CELL; IMMUNOCOMPETENT CELL; MACROPHAGE ACTIVATION; MEMBRANE BINDING; NEUROMODULATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; NEUROTRANSMITTER AGENTS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0030711533     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0149-7634(96)00047-4     Document Type: Article

References (118)

1. Abbas, A.K.; Lichtman, A.H.; Pober, J.S. Cellular and molecular immunology. Philadelphia: Saunders; 1994.
2. Aloisi F., Care A., Borsellino G. Production of hemolymphopoietic cytokines (IL-6, IL-8, colony-stimulating factors) by normal human astrocytes in response to IL-1 beta and tumor necrosis factor-alpha. J. Immunol. 149:1992;2358-2366.
3. Baker D., Butler D., Scallon B.J., O'Neill J.K., Truck J.L. 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 proteins. Eur. J. Immunol. 24:1994;2040-2048.
4. 2+ accumulation. Proc. Natl Acad. Sci. USA. 92:1995;9328-9332.
5. Barna B.P., Barnett G.H., Jacobs B.S., Estes M.L. Divergent responses of human astrocytoma and non-neoplastic astrocytes to tumor necrosis factor alpha involve the 55 kDa tumor necrosis factor receptor. J. Neuroimmunol. 43:1993;185-190.
6. Barna B.P., Estes M.L., Jacobs B.S., Hudson S., Ranscohoff R.M. Human astrocytes proliferate in response to tumor necrosis factor alpha. J. Neuroimmunol. 30:1990;239-243.
7. Barnum S.R., Jones J.L., Benveniste E.N. Interleukin-1 and tumor necrosis factor-mediated regulation of C3 gene expression in human astroglioma cells. Glia. 7:1993;225-236.
8. Barrett C.P., Donati E.J., Guth L. Differences between adult and neonatal rats in their response to spinal injury. Exp. Neurol. 84:1984;374-385.
9. Barten D.M., Ruddle N.H. Vascular cell adhesion molecule-1 modulation by tumor necrosis factor in experimental allergic encephalomyelitis. J. Neuroimmunol. 51:1994;123-133.
10. Bebo B.F. Jr., Linthicum D.S. Expression of mRNA for 55-kDa and 75-kDa tumor necrosis factor (TNF) receptors in mouse cerebrovascular endothelium: effects of interleukin-1β, interferon-γ and TNFα on cultured cells. J. Neuroimmunol. 62:1995;161-167.
11. Beyaert R., Fiers W. Molecular mechanisms of tumor necrosis factor-induced cytotoxicity. What we do understand and what we do not. Fedn Eur. Biochem. Socs Lett. 340:1994;9-16.
12. Bisby M.A., Chen S. Delayed Wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons. Brain Res. 530:1990;117-120.
13. Boddeke, H.W.G.M.; Appel, K.; Sauter, A.; Gebicke-Haerter, P.J.; Buttini, M. Expression of TNFα mRNA and protein after focal cerebral ischaemia in the rat. In: Cytokines in the brain. Arcachon, 11-13 September, 1995 (Abstract).
14. Boka G., Anglade P., Wallach D., Javoy-Agid F. Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson's disease. Neurosci. Lett. 172:1994;151-154.
15. Breder C.D., Tsujimoto M., Terano Y. Distribution and characterization of tumor necrosis factor-α-like immunoreactivity in the murine central nervous system. J. Comp. Neurol. 337:1993;543-567.
16. Brenner T., Yamin A., Abramsky O., Gallily R. Stimulation of tumor necrosis factor-alpha production by mycoplasmas and inhibition by dexamethasone in cultured astrocytes. Brain Res. 608:1993;273-279.
17. Brodie C. Platelet activating factor induces nerve growth factor production by rat astrocytes. Neurosci. Lett. 186:1995;5-8.
18. Burns T.M., Clough J.A., Klein R.M., Wood G.W., Berman N.E. Developmental regulation of cytokine expression in the mouse brain. Growth Factors. 9:1993;253-258.
19. Camussi G., Turello E., Bussolino F., Baglioni C. Tumor necrosis factor alters cytoskeletal organization and barrier function of endothelial cells. Int. Arch. Allergy Appl. Immunol. 96:1991;84-91.
20. Carswell E.A., Old L.J., Dassel R.L. An endotoxin-induced serum factor that causes necrosis of tumors. Proc. Natl Acad. Sci. USA. 72:1975;3666-3670.
21. Cavender D., Saegusa Y., Ziff M. Stimulation of endothelial cell binding of lymphocytes by tumor necrosis factor. J. Immunol. 139:1987;1855-1860.
22. Chao C.C., Hu S. Tumor necrosis factor-alpha potentiates glutamate neurotoxicity in human fetal brain cell cultures. Devl. Neurosci. 16:1994;172-179.
23. Chao C.C., Hu S., Sheng W.S., Peterson P.K. Tumor necrosis factor-alpha production by human fetal microglial cells: regulation by other cytokines. Devl. Neurosci. 17:1995;97-105.
24. Cheng B., Christakos S., Mattson M.P. Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron. 12:1994;139-153.
25. Chiang C.S., McBride W.H. Radiation enhances tumor necrosis factor alpha production by murine brain cells. Brain Res. 566:1991;265-269.
26. Chung I.Y., Norris J.G., Benveniste E.N. Differential tumor necrosis factor α expression from experimental allergic encephalomyelitis-susceptible and resistant rat strains. J. Exp. Med. 173:1991;801-811.
27. Curfs J.H., Hermsen C.C., Kremsner P. Tumour necrosis factor-alpha and macrophages in Plasmodium berghei-induced cerebral malaria. Parasitology. 107:1993;125-134.
28. Dore-Duffy P., Washington R.A., Balabanov R. Cytokine-mediated activation of cultured CNS microvessels: a system for examining antigenic modulation of CNS endothelial cells, and evidence for long-term expression of the adhesion protein E-selectin. J. Cereb. Blood Flow Metab. 14:1994;837-844.
29. Estrada C., Gomez C., Martin C. Effects of TNFα on the production of vasoactive substances by cerebral endothelial and smooth muscle cells in culture. Soc. Neurosci. Abstr. 21:1995;1086.
30. Fan L., Perlman K.P., Young P.R. Experimental brain injury induces expression of tumor necrosis factor-α mRNA. J. Neurotrauma. 11:1994;108.
31. Ganter S., Northoff H., Mannel D., Gebicke-Harter P.J. Growth control of cultured microglia. J. Neurosci. Res. 33:1992;218-230.
32. Gelbard H.A., Dzenko K.A., DiLoreto D., del Cerro C., del Cerro M., Epstein L.G. Neurotoxic effects of tumor necrosis factor alpha in primary human neuronal cultures are mediated by activation of the glutamate AMPA receptor subtype: implications for AIDS neuropathogensis. Devl. Neurosci. 15:1993;417-422.
33. Gendron R.L., Nestel F.P., Lapp W.S., Baines M.G. Expression of tumor necrosis factor alpha in the developing nervous system. Int. J. Neurosci. 60:1991;129-136.
34. Genestier L., Bonnefoy-Berard N., Rouault J.P., Flacher M., Revillard J.P. Tumor necrosis factor-alpha up-regulates Bcl-2 expression and decreases calcium-dependent apoptosis in human B cell lines. Int. Immunol. 7:1995;533-540.
35. Gighi M., Mori L., De Libero G. Monokine production by microglial cell clones. Eur. J. Immunol. 19:1989;1443-1448.
36. Giulian D., Ingeman J.E. Colony-stimulating factors as promoters of ameboid microglia. J. Neurosci. 8:1988;4707-4717.
37. Grassi F., Mileo A.M., Monaco L., Punturieri A., Santoni A., Eusebi F. TNF-alpha increases the frequency of spontaneous miniature synaptic currents in cultured rat hippocampal neurons. Brain Res. 659:1994;226-230.
38. Grell M., Douni E., Wajant H. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell. 83:1995;793-802.
39. Gutierrez E.G., Banks W.A., Kastin A.J. Murine tumor necrosis factor alpha is transported from blood to brain in the mouse. J. Neuroimmunol. 47:1993;169-176.
40. Hattori A., Iwasaki S., Murase K., Tsujimoto M. Tumor necrosis factor is markedly synergistic with interleukin 1 and interferon-gamma in stimulating the production of nerve growth factor in fibroblasts. Fedn Eur. Biochem. Socs Lett. 340:1994;177-180.
41. Hattori A., Tanaka E., Murase K. Tumor necrosis factor stimulates the synthesis and secretion of biologically active nerve growth factor in non-neuronal cell. J. Biol. Chem. 268:1993;2577-2582.
42. Heller R.A., Song K., Fan N., Chang D.J. The p70 tumor necrosis factor receptor mediates cytotoxicity. Cell. 70:1992;47-56.
43. Heuschling P., Faber C., Morga E. Astrocytes express regional heterogeneity after lipopolysaccharide induction of the immune-reactive phenotype. Soc. Neurosci. Abstr. 21:1995;885.
44. Hirschberg D.L., Yoles E., Belkin M., Schwartz M. Inflammation after axonal injury has conflicting consequences for recovery of function: rescue of spared axons is impaired but regeneration is supported. J. Neuroimmunol. 50:1994;9-16.
45. Hsu K.C., Chao M.V. Differential expression and ligand binding properties of tumor necrosis factor receptor chimeric mutants. J. Biol. Chem. 268:1993;16430-16436.
46. Ignatowski T.A., Spengler R.N. Tumor necrosis factor-α: presynaptic sensitivity is modified after antidepressant drug administration. Brain Res. 665:1994;293-299.
47. 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. 61:1995;205-212.
48. Kiernan J.A. Hypothesis concerned with axonal regeneration in the mammalian nervous system. Biol. Rev. 54:1979;155-197.
49. Kinouchi K., Brown G., Pasternak G., Donner D.B. Identification and characterization of receptors for tumor necrosis factor-α in the brain. Biochem. Biophys. Res. Commun. 181:1991;1532-1538.
50. Klefstrom J., Vastrik I., Saksela E., Valle J., Eilers M., Alitalo K. c-Myc induces cellular susceptibility to the cytotoxic action of TNF-alpha. Eur. Molec. Biol. Org. J. 13:1994;5442-5450.
51. Korner H., Goodsall A.L., Lemckert F.A. Unimpaired autoreactive T-cell traffic within the central nervous system during tumor necrosis factor receptor-mediated inhibition of experimental auto-immune encephalomyelitis. Proc. Natl Acad. Sci. USA. 92:1995;11066-11070.
52. Krönke M., Schütze S., Scheurich P. Tumor necrosis factor signal transduction. Cell. Signal. 2:1990;1-8.
53. Kuroda Y., Shimamoto Y. Human tumor necrosis factor-α augments experimental allergic encephalomyelitis in rats. J. Neuroimmunol. 34:1991;159-164.
54. Lachman L.B., Brown D.C., Dinarello C.A. Growth promoting effect of recombinant interleukin-1 and tumor necrosis factor for a human astrocytoma cell line. J. Immunol. 138:1987;2913-2916.
55. Lapierre L.A., Fiers W., Pober J.S. Three distinct classes of regulatory cytokines control endothelial cell MHC antigen expression. Interactions with immune (gamma) interferon differentiate the effects of tumor necrosis factor and lymphotoxin from those of leukocyte (α) and fibroblast (β) interferons. J. Exp. Med. 167:1988;794-804.
56. Lee S.C., Liu W., Dickson D.W., Brosnan C.F., Berman J.W. Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J. Immunol. 150:1993;2659-2667.
57. Liberski P.P., Yanagihara R., Nerurkar V., Gajdusek D.C. Further ultrastructural studies of lesions produced in the optic nerve by tumor necrosis factor alpha (TNF-alpha): a comparison with experimental Creutzfeldt-Jakob disease. Acta Neurobiol. Exp. (Warsz). 54:1994;209-218.
58. Lieberman A.P., Pitha P.M., Shin H.S. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc. Natl Acad. Sci. USA. 86:1989;6348-6352.
59. Lindvall L., Lantz M., Gullberg U., Olsson I. Modulation of the constitutive gene expression of the 55 kd tumor necrosis factor receptor in hematopoietic cells. Biochem. Biophys. Res. Commun. 172:1990;557-563.
60. Liu T., Clark R.K., McDonnell P.C. Tumor necrosis factor-alpha expression in ischemic neurons. Stroke. 25:1994;1481-1488.
61. Lotan M., Solomon A., Ben-Bassat S., Schwartz M. Cytokines modulate the inflammatory response and change permissiveness to neuronal adhesion in injured mammalian central nervous system. Exp. Neurol. 126:1994;284-290.
62. Low K.G., Allen R.G., Melner M.H. Differential regulation of proenkephalin expression in astrocytes by cytokines. Endocrinology. 131:1992;1908-1914.
63. Müller U., Jongeneel C.V., Nedospasov S.A., Lindahl K.F., Steinmetz M. Tumour necrosis factor and lymphotoxin genes map close to H-2D in the mouse major histocompatibility complex. Nature. 325:1987;265-267.
64. Male D., Rahman J., Pryce G., Tamatani T., Miyasaka M. Lymphocyte migration into the CNS modelled in vitro: roles of LFA-1, ICAM-1 and VLA-4. Immunology. 81:1994;366-372.
65. Malipiero U.V., Frei K., Fontana A. Production of hemopoietic colony-stimulating factors by astrocytes. J. Immunol. 144:1990;3816-3821.
66. Maness L.M., Kastin A.J., Banks W.A., Gutierrez E.G. Saturable transport of TNFα across the neonatal BBB. Soc. Neurosci. Abstr. 18:1992;1128.
67. Martin R., McFarland H.F., McFarlin D.E. Immunological aspects of demyelinating diseases. A. Rev. Immunol. 10:1992;153-187.
68. McCarron R.M., Wang L., Racke M.K., McFarlin D.E., Spatz M. Cytokine-regulated adhesion between encephalitogenic T lymphocytes and cerebrovascular endothelial cells. J. neuroimmunol. 43:1993;23-30.
69. McLaurin J., D'Souza S., Stewart J. Effect of tumor necrosis factor alpha and beta on human oligodendrocytes and neurons in culture. Int. J. Devl. Neurosci. 13:1995;369-381.
70. Megyeri P., Abraham C.S., Temesvari P., Kovacs J., Vas T., Speer C.P. Recombinant human tumor necrosis factor α constricts pial arterioles and increases blood-brain barrier permeability in newborn piglets. Neurosci. Lett. 148:1992;137-140.
71. Merrill J.E. Effects of interleukin 1 and tumor necrosis factor alpha on astrocytes, microglia, oligodendrocytes and glial precursors in vitro. Devl. Neurosci. 13:1991;130-137.
72. Merrill J.E. Tumor necrosis factor alpha, interleukin 1 and related cytokines in brain development: normal and pathological. Devl. Neurosci. 14:1992;1-10.
73. Mitrovic B., Martin F.C., Charles A.C. Neurotransmitters and cytokines in CNS pathology. Progr. Brain Res. 103:1994;319-330.
74. Mizuno T., Sawada M., Suzumura A., Marunouchi T. Expression of cytokines during glial differentiation. Brain Res. 656:1994;141-146.
75. Mogi M., Harada M., Riederer P., Narabayashi H. Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from Parkinsonian patients. Neurosci. Lett. 165:1994;208-210.
76. Monastra G., Cross A.H., Bruni A., Raine C.S. Phosphatidylserine, a putative inhibitor of tumor necrosis factor, prevents auto-immune demyelination. Neurology. 43:1993;153-163.
77. Moretto G., Yoo A., Kim S.U. Human astrocytes and cytokines: tumor necrosis factor alpha and interferon gamma do not promote astrocytic proliferation. Neurosci. Lett. 151:1993;17-20.
78. Munoz-Fernández M.A., Armas-Portela R., Diaz-Nido J. Differential effects of tumor necrosis factor on the growth and differentiation of neuroblastoma and glioma cells. Exp. Cell Res. 194:1991;161-164.
79. Nathan C.F. Secretory products of macrophages. J. Clin. Invest. 79:1987;319-326.
80. Nitta T., Ebato M., Sato K., Okumura K. Expression of tumour necrosis factor-alpha, -beta and interferon-gamma genes within human neuroglial tumour cells and brain specimens. Cytokine. 6:1994;171-180.
81. Oh Y.J., Markelonis G.J., Oh T.H. Effects of interleukin-1 beta and tumor necrosis factor-alpha on the expression of glial-fibrillary acidic protein and transferrin in cultured astrocytes. Glia. 8:1993;77-86.
82. Paya C.V., Leibson P.J., Patick A.K., Rodriguez M. Inhibition of Theiler's virus-induced demyelination in vivo by tumor necrosis factor alpha. Int. Immunol. 2:1990;909-913.
83. Perez C., Albert I., DeFay K., Zachariades N., Gooding L., Kriegler M. A nonsecretable cell surface mutant of tumor necrosis factor (TNF) kills by cell-to-cell contact. Cell. 63:1996;251-258.
84. Perry V.H., Andersson P.B., Gordon S. Macrophages and inflammation in the central nervous system. Trends Neurosci. 16:1993;268-273.
85. Perry V.H., Brown M.C., Gordon S. The macrophage response to central and peripheral nerve injury: a possible role for macrophages in regeneration. J. Exp. Med. 165:1987;1218-1223.
86. Pober J.S., Cotran R.S. Cytokines and endothelial cell biology. Physiol. Rev. 70:1990;427-451.
87. Powers J.M., Liu Y., Moser A.B., Moser H.W. The inflammatory myelinopathy of adreno-leukodystrophy: cells, effector molecules, and pathogenetic implications. J. Neuropathol. Exp. Neurol. 51:1992;630-643.
88. Powrie F., Coffman R.L. Cytokine regulation of T-cell function: potential for therapeutic intervention. Immunol. Today. 14:1993;270-274.
89. Renno T., Krakowski M., Piccirillo C., Lin J.Y., 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. 154:1995;944-953.
90. Rieckmann P., Albrecht M., Kitze B. Tumor necrosis factor-α messenger RNA expression in patients with relapsing-remitting multiple sclerosis is associated with disease activity. Ann. Neurol. 37:1995;82-88.
91. Rothe J., Gehr G., Loetscher H., Lesslauer W. Tumor necrosis factor receptors - structure and function. Immunol. Res. 11:1992;81-90.
92. Rovelli G., Heller R.A., Canossa M., Shooter E.M. Chimeric tumor necrosis factor-TrkA receptors reveal that ligand-dependent activation of the TrkA tyrosine kinase is sufficient for differentiation and survival of PC12 cells. Proc. Natl Acad. Sci. USA. 90:1993;8717-8721.
93. Saija A., Princi P., Lanza M., Scalese M., Aramnejad E., De Sarro A. Systemic cytokine administration can affect blood-brain barrier permeability in the rat. Life Sci. 56:1995;775-784.
94. Sato N., Goto T., Haranaka K., Satomi N., Hirano Y., Sawasaki Y. Actions of tumor necrosis factor on cultured vascular endothelial cells: morphologic modulation, growth inhibition and cytotoxicity. J. Natl Cancer Inst. 76:1986;1113-1121.
95. Sawada M., Suzumura A., Marunouchi T. TNF alpha induces IL-6 production by astrocytes but not by microglia. Brain Res. 583:1992;296-299.
96. Schwartz M., Solomon A., Lavie V., Ben-Bassat S., Belkin M., Cohen A. Tumor necrosis factor facilitates regeneration of injured central nervous system axons. Brain Res. 545:1991;334-338.
97. Selmaj K., Raine C.S., Cross A.H. Anti-tumor necrosis factor therapy abrogates autoimmune demyelination. Ann. Neurol. 30:1991;694-700.
98. Selmaj K.W., Farooq M., Norton W.T., Raine C.S., Brosnan C.F. Proliferation of astrocytes in vitro in response to cytokines. A primary role for tumor necrosis factor. J. Immunol. 144:1990;129-135.
99. Selmaj K.W., Raine C.S. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23:1988;339-346.
100. Shafit-Zagardo B., Sharma N., Berman J.W., Borstein M.B., Brosnan C.F. CSF-1 expression is upregulated in astrocyte cultures by IL-1 and TNF and affects microglial proliferation and morphology in organic cultures. Int. J. Devl. Neurosci. 11:1993;189-198.
101. Sharif S.F., Hariri R.J., Chang V.A., Barie P.S., Wang R.S., Ghajar J.B. Human astrocyte production of tumour necrosis factor-alpha, interleukin-1 beta, and interleukin-6 following exposure to lipopolysaccharide endotoxin. Neurol. Res. 15:1993;109-112.
102. Shohami E., Novikov M., Bass R., Yamin A., Gallily R. Closed head injury triggers early production of TNF alpha and IL-6 by brain tissue. J. Cereb. Blood Flow Metab. 14:1994;615-619.
103. Sierra A., Rubio N. Theiler's murine encephalomyelitis virus induces tumour necrosis factor-alpha in murine astrocyte cell cultures. Immunology. 78:1993;399-404.
104. Skaper S.D., Facci L., Leon A. Inflammatory mediator stimulation of astrocytes and meningeal fibroblasts induces neuronal degeneration via the nitridergic pathway. J. Neurochem. 64:1995;266-276.
105. Smith R.A., Baglioni C. The active form of tumor necrosis factor is a trimer. J. Biol. Chem. 262:1987;6951-6954.
106. Sparacio S.M., Zhang Y., Vilcek J., Benveniste E.N. Cytokine regulation of interleukin-6 gene expression in astrocytes involves activation of an NF-kappa B-like nuclear protein. J. Neuroimmunol. 39:1992;231-242.
107. Sriram S., Topham D.J., Carroll L., Shenoy M., Adesina A., Craighead J.E. In vivo administration of TNF-alpha prevents EMC-M virus induced viral encephalitis. Int. Immunol. 3:1991;641-645.
108. Stolphen A.H., Guinan E.C., Fiers W., Pober J.S. Recombinant tumor necrosis factor and immune interferon act singly and in combination to reorganize human vascular endothelial cell monolayers. Am. J. Pathol. 123:1986;16-24.
109. Talley A.K., Dewhurst S., Perry S.W. Tumor necrosis factor alpha-induced apoptosis in human neuronal cells: protection by the antioxidant N-acetylcysteine and the genes bcl-2 and crmA. Molec. Cell. Biol. 15:1995;2359-2366.
110. Tancredi V., D'Arcangelo G., Grassi F. Tumor necrosis factor alters synaptic transmission in rat hippocampal slices. Neurosci. Lett. 146:1992;176-178.
111. Tartaglia L.A., Ayres T.M., Wong G.H., Goeddel D.V. A novel domain within the 55 kd TNF receptor signals cell death. Cell. 74:1993;845-853.
112. Tartaglia L.A., Pennica D., Goeddel D.V. Ligand passing: the 75-kDa tumor necrosis factor (TNF) receptor recruits TNF for signaling by the 55-kDa TNF receptor. J. Biol. Chem. 268:1993;18542-18548.
113. Tartaglia L.A., Weber R.F., Figari I.S., Reynolds C., Palladino M.A., Goeddel D.V. The two different receptor for tumor necrosis factor mediate distinct cellular responses. Proc. Natl Acad. Sci. USA. 88:1991;9292-9296.
114. Teuscher C., Hickey W.F., Korngold R. An analysis of the role of tumor necrosis factor in the phenotypic expression of actively induced experimental allergic orchitis and experimental allergic encephalomyelitis. Clin. Immunol. Immunopathol. 54:1990;442-453.
115. Vandenabeele P., Declercq W., Vanhaesebroeck B., Grooten J., Fiers W. Both TNF receptors are required for TNF-mediated induction of apoptosis in PC60 cells. J. Immunol. 154:1995;2904-2913.
116. Wilt S.G., Milward E., Zhou J.M. In vitro evidence for a dual role of tumor necrosis factor-alpha in human immunodeficiency virus type 1 encephalopathy. Ann. Neurol. 37:1995;381-394.
117. Wingfield P., Pain R.H., Craig S. Tumor necrosis factor is a compact trimer. Fedn Eur. Biochem. Socs Lett. 211:1987;179-184.
118. Pan W., Banks W.A., Kennedy M.K., Guttierez E.G., Kastin A.J. Differential permeability of the BBB in acute EAE: enhanced transport of TNF-α Am. J. Physiol. 271:1996;E636-E642.