Control of nitric oxide production by transforming growth factor-β1: Mechanistic insights and potential relevance to human disease

Nitric Oxide - Biology and Chemistry

Volumn 1, Issue 1, 1997, Pages 3-17

  Vodovotz, Yoram ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE; TRANSFORMING GROWTH FACTOR BETA1;

ALZHEIMER DISEASE; DEGENERATIVE DISEASE; ENDOTOXEMIA; GENE CONTROL; HUMAN; MACROPHAGE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; TRANSCRIPTION REGULATION;

MAMMALIA;

EID: 0031406928     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1006/niox.1996.0105     Document Type: Article

References (168)

1. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:1992;3051-3064.
2. Nathan C., Xie Q. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269:1994;13725-13728.
3. Stuehr D. J., Griffith O. W. Mammalian nitric oxide synthases. Adv. Enzyme Rel. Areas Mol. Biol. 65:1992;287.
4. Bredt D. S., Snyder S. H. Nitric oxide, a novel neuronal messenger. Neuron. 8:1992;3-11.
5. Knowles R. G. Brain nitric oxide synthesis and neurodegeneration. In. 1994;Int. Acad. Biomed. Drug Research, Basel. p. 112-118.
6. Moncada S., Higgs A. Mechanisms of disease: TheL. N. Engl. J. Med. 329:1993;2002-2012.
7. Sessa W. C. The nitric oxide synthase family of proteins. J. Vasc. Res. 31:1994;131-143.
8. Stamler J. S. Redox signaling: Nitrosylation and related target interactions of nitric oxide. Cell. 78:1994;931-936.
9. Wink D. A., Hanbauer I., Grisham M. B., Laval F., Nims R. W., Laval J., Cook J., Pacelli R., Liebman J., Krishna M. The chemical biology of NO: Insights into regulation, protective and toxic mechanisms of nitric oxide. Curr. Top. Cell Biol. 34:1996;159-187.
10. Lowenstein C. J., Snyder S. H. Nitric oxide, a novel biologic messenger. Cell. 70:1992;705-707.
11. Nathan C. F., Hibbs J. B. Jr. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:1991;65-70.
12. Vallance P., Moncada S. Role of endogenous nitric oxide in septic shock. New Horizons. 1:1993;77-86.
13. Pastor C. M., Billiar T. R. Regulation and functions of nitric oxide in the liver in sepsis and inflammation. New Horizons. 3:1995;65-72.
14. Xie K., Dong Z., Fidler I. J. Activation of nitric oxide synthase gene for inhibition of cancer metastasis. J. Leukocyte Biol. 59:1996;797-803.
15. Ungureanu-Longrois D., Balligand J., Kelly R. A., Smith T. W. Myocardial contractile dysfunction in the systemic inflammatory response syndrome: Role of cytokine-inducible nitric oxide synthase in cardiac myocytes. J. Mol. Cell. Cardiol. 27:1995;155-167.
16. Stefanovic-Racic M., Stadler J., Evans C. H. Nitric oxide and arthritis. Arthritis Rheum. 36:1993;1036-1044.
17. Sparrow J. R. Inducible nitric oxide synthase in the central nervous system. J. Mol. Neurosci. 5:1994;219-229.
18. Sen S., Cheema I. R. Nitric oxide synthase and calmodulin immunoreactivity in plant embryonic tissue. Biochem. Arch. 11:1995;221-227.
19. Ottaviani E., Paemen L. R., Cadet P., Stefano G. B. Evidence for nitric oxide production and utilization as a bacteriocidal agent by invertebrate immunocytes. Eur. J. Pharmacol. 248:1993;319-324.
20. Ribeiro J. M. C., Nussenzveig R. H. Nitric oxide synthase activity from a hematophagous insect salivary gland. FEBS Lett. 330:1993;165-168.
21. Dow J. A. T., Maddrell S. H. P., Davies S., Skaer N. J. V., Kaiser J. A novel role for the nitric oxide-cGMP signaling pathway: The control of epithelial function inDrosophila. Am. J. Physiol. 266:1994;R1716-R1719.
22. 2+Apis melliferaDrosophila melanogaster. Eur. J. Neurosci. 6:1994;1362-1370.
23. 2+. Proc. Natl. Acad. Sci. USA. 92:1995;9072-9076.
24. Porteros A., Arevalo R., Crespo C., Brinon J. G., Weruaga E., Aljon J., Alonso J. R. Nitric-oxide synthase activity in the olfactory-bulb of anuran and urodele amphibians. Brain Res. 724:1996;67-72.
25. Roberts A. B., Sporn M. B. The transforming growth factor-betas. Sporn M. B., Roberts A. B. In. 1990;419-472 Springer-Verlag, Berlin.
26. Massagué J. The transforming growth factor-β family. Annu. Rev. Cell Biol. 6:1990;597-641.
27. Finch C. E., Laping N. J., Morgan T. E., Nichols N. R., Pasinetti G. M. TGF-β1 is an organizer of responses to neurodegeneration. J. Cell. Biochem. 53:1993;314-322.
28. Shull M. M., Doetschman T. Transforming growth factor-β1 in reproduction and development. Mol. Reprod. Dev. 39:1994;239-246.
29. Flaumenhaft R., Kojima S., Abe M., Rifkin D. B. Activation of latent transforming growth factor β Adv. Pharmacol. 24:1993;51-76.
30. Attisano L., Wrana J. L., Lopez-Casillas F., Massagué J. TGF-β receptors and actions. Biochim. Biophys. Acta. 26:1994;71-80.
31. Derynck R. TGF-β-receptor-mediated signaling. Trends Biochem. Sci. 19:1994;548-553.
32. Miyazono K., Ten Dijke P., Ichijo H., Heldin C. Receptors for transforming growth factor-β Adv. Immunol. 55:1994;181-220.
33. Palladino M. A., Morris R. E., Starnes H. F., Levinson A. D. The transforming growth factor-betas: A new family of immunoregulatory molecules. Ann. NY Acad. Sci. 593:1990;181-187.
34. McCartney-Francis N., Wahl S. M. Transforming growth factor β: A matter of life and death. J. Leukocyte Biol. 55:1994;401-409.
35. Vodovotz Y., Bogdan C. Control of nitric oxide synthase expression by transforming growth factor-β: Implications for homeostasis. Prog. Growth Factor Res. 5:1994;341-351.
36. Ding A., Nathan C. F., Graycar J., Derynck R., Stuehr D. J., Srimal S. Macrophage deactivating factor and transforming growth factors-β1, -β2, and -β3 inhibit induction of macrophage nitrogen oxide synthesis by IFN-γ J. Immunol. 145:1990;940-944.
37. Nelson B. J., Ralph P., Green S. J., Nacy C. A. Differential susceptibility of activated macrophage cytotoxic effector reactions to the suppressive effects of transforming growth factor-β1. J. Immunol. 146:1991;1849-1857.
38. Gazzinelli R. T., Oswald I. P., Hieny S., James S. L., Sher A. The microbicidal activity of interferon-γ-treated macrophages againstTrypanosoma cruziL. Eur. J. Immunol. 22:1992;2501-2506.
39. Oswald I. P., Gazzinelli R. T., Sher A., James S. L. IL-10 synergizes with IL-4 and transforming growth factor-β to inhibit macrophage cytotoxic activity. J. Immunol. 148:1992;3578-3582.
40. Vodovotz Y., Bogdan C., Paik J., Xie Q., Nathan C. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor-β J. Exp. Med. 178:1993;605-613.
41. Gilbert R. S., Herschmann H. R. Transforming growth factor beta differentially modulates the inducible nitric oxide synthase gene in distinct cell types. Biochem. Biophys. Res. Commun. 195:1993;380-384.
42. 2. J. Immunol. 153:1994;1674-1686.
43. Chesrown S. E., Monnier J., Visner G., Nick H. S. Regulation of inducible nitric oxide synthase mRNA levels by LPS, INF-γ, TGF-β, and IL-10 in murine macrophage cell lines and rat peritoneal macrophages. Biochem. Biophys. Res. Commun. 200:1994;126-134.
44. Hausmann E. H. S., Hao S., Pace J., Parmely M. J. Transforming growth factor β1 and gamma interferon provide opposing signals to lipopolysaccharide-activated mouse macrophages. Infect. Immun. 62:1994;3625-3632.
45. Maeda H., Tsuru S., Shiraishi A. Improvement of macrophage dysfunction by administration of anti-transforming growth factor-β antibody in EL4-bearing hosts. Jpn. J. Cancer Res. 85:1994;1137-1143.
46. Adler H., Frech B., Thöny M., Pfister H., Peterhans E., Jungi T. W. Inducible nitric oxide synthase in cattle: Differential cytokine regulation of nitric oxide synthase in bovine and murine macrophages. J. Immunol. 154:1995;4710-4718.
47. Boutard V., Havouis R., Fouqueray B., Philippe C., Moulinoux J., Baud L. Transforming growth factor-β stimulates arginase activity in macrophages: Implications for the regulation of macrophage cytotoxicity. J. Immunol. 155:1995;2077-2084.
48. Jun C., Choi B., Kim S., Lee S. Y., Kim H., Chung H. Down-regulation of transforming growth factor-β gene expression by antisense oligodeoxynucleotides increases recombinant interferon-γ-induced nitric oxide synthesis in murine peritoneal macrophages. Immunology. 85:1995;114-119.
49. Tomioka H., Sato K., Maw W. W., Saito H. The role of tumor necrosis factor, interferon-g, transforming growth factor-β, and nitric oxide in the expression of immunosuppressive functions of splenic macrophages induced byMycobacterium avium. J. Leukocyte Biol. 58:1995;704-712.
50. 2. Biochem. Biophys. Res. Commun. 175:1991;372-379.
51. Junquero D. C., Scott-Burden T., Schini V. B., Vanhoutte P. M. Inhibition of cytokine-induced nitric oxide production by transforming growth factor-β1 in human smooth muscle cells. J. Physiol. (London). 454:1992;451-465.
52. ABBB. Eur. J. Pharmacol. 216:1992;379-383.
53. Perrella M. A., Yoshizumi M., Fen Z., Tsai J., Hsieh C., Kourembanas S., Lee M. Transforming growth factor-β1, but not dexamethasone, down-regulates nitric-oxide synthase mRNA after its induction by interleukin-1β in rat smooth muscle cells. J. Biol. Chem. 269:1994;14595-14600.
54. Scott-Burden T., Elizondo E., Ge T. Growth factor regulation of interleukin-1β-induced nitric oxide synthase and GTP:cyclohydrolase expression in cultured smooth muscle cells. Biochem. Biophys. Res. Commun. 196:1993;1261-1266.
55. Finder J., Stark W. W., Nakayama D. K., Geller D., Wasserloos K., Pitt B. R., Davies P. TGF-β regulates production of NO in pulmonary-artery smooth-muscle cells by inhibiting expression of NOS. Am. J. Physiol. 12:1995.
56. Perrella M. A., Patterson C., Tan L., Yet S. F., Hsieh C. M., Yoshizumi M., Lee M. E. Suppression of interleukin-1β-induced nitric oxide synthase promoter/enhancer activity by transforming growth factor-β1 in vascular smooth muscle cells: Evidence for mechanisms other than NF-κB. J. Biol. Chem. 271:1996;13776-13780.
57. Merrill J. E., Ignarro L. J., Sherman M. P., Melinek J., Lane T. E. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151:1993;2132-2141.
58. Haregewoin A., Alexander E. III, Black P. M., Loeffler J. S. Autocrine regulation of the production of the gaseous messenger nitric oxide in a glioblastoma cell line. Exp. Cell Res. 210:1994;137-139.
59. Park S. K., Grzybicki D., Lin H. L., Murphy S. Modulation of inducible nitric oxide synthase expression in astroglial cells. Neuropharmacology. 33:1994;1419-1423.
60. Goureau O., Hicks D., Courtois Y., De Kozak Y. Induction and regulation of nitric oxide synthase in retinal Müller glial cells. J. Neurochem. 63:1994;310-317.
61. Young M. R. I., Farietta T., Crayton J. W. Production of nitric oxide and transforming growth factor-β in developing and adult rat brain. Mech. Ageing Dev. 79:1995;115-126.
62. Roberts A. B., Vodovotz Y., Roche N. S., Sporn M. B., Nathan C. F. Role of nitric oxide in antagonistic effects of transforming growth factor-β and interleukin-1β on the beating rate of cultured cardiac myocytes. Mol. Endocrinol. 6:1992;1921-1930.
63. Pinsky D. J., Cai B., Yang X., Rodriguez C., Sciacca R. R., Cannon P. J. The lethal effects of cytokine-induced nitric oxide on cardiac myocytes are blocked by nitric oxide synthase antagonism or transforming growth factor β J. Clin. Invest. 95:1995;677-685.
64. Shindo T., Ikeda U., Ohkawa F., Kawahara Y., Yokoyama M., Shimada K. Nitric oxide synthesis in cardiac myocytes and fibroblasts by inflammatory cytokines. Cardiovasc. Res. 29:1995;813-819.
65. Sparrow J., Nathan C., Vodovotz Y. Cytokine regulation of nitric oxide synthase in mouse retinal pigment epithelial cells in culture. Exp. Eye Res. 59:1994;129-139.
66. Goureau O., Hicks D., Courtois Y. Human retinal pigmented epithelial cells produce nitric oxide in response to cytokines. Biochem. Biophys. Res. Commun. 198:1994;120-126.
67. Kutty R. K., Kutty G., Hooks J. J., Wigert B., Nagineni C. N. Transforming growth factor-β inhibits the cytokine-mediated expression of the inducible nitric oxide synthase mRNA in human retinal pigment epithelial cells. Biochem. Biophys. Res. Commun. 215:1995;386-393.
68. Vodovotz Y., Letterio J. J., Geiser A. G., Chesler L., Roberts A. B., Sparrow J. Control of nitric oxide production by endogenous transforming growth factor-β1 and systemic nitric oxide in retinal pigment epithelial cells and peritoneal macrophages. J. Leukocyte Biol. 60:1996;261-270.
69. Murata J., Corradin S. B., Felley-Bosco E., Juillerat-Jeanneret L. Involvement of a transforming-growth-factor-β-like molecule in tumor-cell-derived inhibition of nitric-oxide synthesis in cerebral endothelial cells. Int. J. Cancer. 62:1995;743-748.
70. Schoedon G., Schneemann M., Blau N. Modulation of human endothelial cell tetrahydrobiopterin synthesis by activating and deactivating cytokines: New perspectives on endothelium-derived relaxing factor. Biochem. Biophys. Res. Commun. 196:1993;1343-1348.
71. Ungureanu-Longrois D., Balligand J., Odada I., Simmons W. W., Kobzik L., Lowenstein C. J., Kunkel S. L., Michel T., Kelly R. A., Smith T. W. Contractile responsiveness of ventricular myocytes isoproterenol is regulated by induction of nitric oxide synthase activity in cardiac microvascular endothelial cells in heterotypic primary culture. Circ. Res. 77:1995;486-493.
72. Löwik C. G. M., Nibbering P. H., van de Ruit M., Papapoulos S. E. Inducible production of nitric oxide in osteoblast-like cells and in fetal mouse bone explants is associated with suppression of osteoclastic bone resorption. J. Clin. Invest. 93:1994;1465-1472.
73. Roland C. R., Goss J. A., Mangino M. J., Hafenrichter D., Flye M. W. Autoregulation by eicosanoids of human kupffer cell secretory products: A study of interleukin-1, interleukin-6, tumor necrosis factor-α, transforming growth factor-β, and nitric oxide. Ann. Surg. 219:1994;389-399.
74. Nussler A. K., Di Silvio M., Liu Z., Geller D. A., Freeswick P., Dorko K., Bartoli F., Billiar T. R. Further characterization and comparison of inducible nitric oxide synthase in mouse, rat, and human hepatocytes. Hepatology. 21:1995;1552-1560.
75. Laskin D. L., Rodriguez del Valle M., Heck D. E., Hwang S., Ohnishi S. T., Durham S. K., Goller N. L., Laskin J. D. Hepatic nitric oxide production following acute endotoxemia in rats is mediated by increased inducible nitric oxide synthase gene expression. Hepatology. 22:1995;223-234.
76. Blanco F. J., Geng Y., Lotz M. Differentiation-dependent effects of IL-1 and TGF-β on human articular chondrocyte proliferation are related to inducible nitric oxide synthase expression. J. Immunol. 154:1995;4018-4026.
77. Arany I., Brysk M. M., Brysk H., Tyring S. K. Regulation of inducible nitric oxide synthase mRNA levels by differentiation and cytokines in human keratinocytes. Biochem. Biophys. Res. Commun. 220:1996;618-622.
78. Bogdan C., Vodovotz Y., Xie Q., Nathan C., Röllinghoff M. Regulation of inducible nitric oxide synthase in macrophages by cytokines and microbial products. Masihi N. In. 1994;37-54 Dekker, New York.
79. Geller D. A., de Vera M. E., Russell D. A., Shapiro R. A., Nussler A. K., Simmons R. L., Billiar T. R. A central role for IL-1 beta in the in vitro and in vivo regulation of hepatic inducible nitric oxide synthase: IL-1 beta induces hepatic nitric oxide synthesis. J. Immunol. 155:1995;4890-4898.
80. de Vera M. E., Shapiro R. A., Nussler A. K., Mudgett J. S., Simmons R. L., Morris S. M. Jr., Billiar T. R., Geller D. A. Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: Initial analysis of the human NOS2 promoter. Proc. Natl. Acad. Sci. USA. 93:1996;1054-1059.
81. Xie Q., Kashiwabara Y., Nathan C. Role of transcription factor NF-kappaB/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269:1994;4705-4708.
82. Kamijo R., Harada H., Matsuyama T., Bosland M., Gerecitano J., Shapiro D., Le J., Koh S. I., Kimura T., Green S. J. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science. 263:1994;1612-1615.
83. Fujihara C. K., De Nucci G., Zatz R. Chronic nitric oxide synthase inhibition aggravates glomerular injury in rats with subtotal nephrectomy. J. Am. Soc. Nephrol. 5:1995;1498-1507.
84. Arsura M., Wu M., Sonenshein G. E. TGFβ1 inhibits NF-κB/Rel activity inducing apoptosis of B cells: Transcriptional activation of IκBα Immunity. 5:1996;31-40.
85. Tran-Thi T. A., Decker K., Baeuerle P. A. Differential activation of transcription factors NF-kappa B and AP-1 in rat liver macrophages. Hepatology. 22:1995;613-619.
86. Chung K. Y., Agarwal A., Uitto J., Mauviel A. An AP-1 binding sequence is essential for regulation of the human α2(I) collagen promoter activity by transforming growth factor-β J. Biol. Chem. 271:1996;3272-3278.
87. Kim S. J., Jeang K. T., Glick A. B., Sporn M. B., Roberts A. B. Promoter sequences of the human transforming growth factor-β1 gene responsive to transforming growth factor-β1 autoinduction. J. Biol. Chem. 264:1989;7041.
88. Miller C. L., Feldhaus A. L., Rooney J. W., Rhodes L. D., Sibley C. H., Singh H. Regulation and a possible stage-specific function of Oct-2 during pre-B-cell differentiation. Mol. Cell. Biol. 11:1991;4885-1894.
89. Xie Q., Whisnant R., Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon τ and bacterial lipopolysaccharide. J. Exp. Med. 177:1993;1779-1784.
90. Lowenstein C. J., Alley E. W., Raval P., Snowman A. M., Snyder S. H., Russell S. W., Murphy W. J. Macrophage nitric oxide synthase gene: Two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. USA. 90:1993;9730-9734.
91. Salkowski C. A., Barber S. A., Detore G. R., Vogel S. N. Differential dysregulation of nitric oxide production in macrophages with targeted disruptions in IFN regulatory factor-1 and -2 genes. J. Immunol. 156:1996;3107-3110.
92. Chartrain N. A., Geller D. A., Koty P. P., Sitrin N. F., Nussler A. K., Hoffman E. P., Billiar T. R., Hutchinson N. I., Mudgett J. S. Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J. Biol. Chem. 269:1994;6765-6772.
93. Werner-Lelmayer G., Gross S. S. Analysis of tetrahydrobiopterin and its role in nitric oxide synthesis. Feelisch M., Stamler J. S. In. 1996;271-299 Wiley, New York.
94. Griscavage J. M., Rogers N. E., Sherman M. P., Ignarro L. J. Inducible nitric oxide synthase from a rat alveolar macrophage cell line in inhibited by nitric oxide. J. Immunol. 151:1993;6329-6337.
95. Vodovotz Y., Kwon N., Popischil M., Manning J., Paik J., Nathan C. Inactivation of nitric oxide synthase following prolonged incubation of mouse macrophages with interferon-gamma and bacterial lipopolysaccharide. J. Immunol. 152:1994;4110-4118.
96. Griscavage J. M., Hobbs A. J., Ignarro L. J. Negative modulation of nitric oxide synthase by nitric oxide and nitroso compounds. Adv. Pharmacol. 34:1995;215-234.
97. Goureau O., Lepoivre M., Becquet F., Courtois Y. Differential regulation of inducible nitric oxide synthase by fibroblast growth factors and transforming growth factor β in bovine retinal epithelial cells: Inverse correlation with cellular proliferation. Proc. Natl. Acad. Sci. USA. 90:1993;4276-4280.
98. Weinberg J. B., Misukonis M. A., Shami P. J., Mason S. N., Sauls D. L., Ditman W. A., Wood E. R., Smith G. K., McDonald B., Bachus K. E. Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): Analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages. Blood. 86:1995;1184-1195.
99. Albina J. E. On the expression of nitric oxide synthase by human macrophages: Why no NO? J. Leukocyte Biol. 58:1995;643-649.
100. Di Rosa M., Radomski M., Carnuccio R., Moncada S. Glucocorticoids inhibit the induction of nitric oxide synthase in macrophages. Biochem. Biophys. Res. Commun. 172:1990;1246-1252.
101. Szabó C., Thiemermann C., Wu C., Perretti M., Vane J. R. Attenuation of the induction of nitric oxide synthase by endogenous glucocorticoids accounts for endotoxin tolerancein vivo. Proc. Natl. Acad. Sci. USA. 91:1994;271-275.
102. Vallance P., Leone A., Calver A., Collier J., Moncada S. Endogenous dimethylarginine as an inhibitor of nitric oxide synthesis. J. Cardiovasc. Pharmacol. 20:1992.
103. Schini V. B., Catovsky S., Scott-Burden T., Vanhoutte P. M. The inducible nitric oxide synthase is impaired by thrombin in vascular smooth muscle cells. J. Cardiovasc. Pharmacol. 20:1992.
104. Nakayama I., Kawahara Y., Tsuda T., Okuda M., Yokoyama M. Angiotensin II inhibits cytokine-stimulated inducible nitric oxide synthase expression in vascular smooth muscle cells. J. Biol. Chem. 269:1994;11628-11633.
105. Hwang S., Lopez C. A., Heck D. E., Gardner C. R., Laskin D. L., Laskin J. D., Denhardt D. T. Osteopontin inhibits induction of nitric oxide synthase gene expression by inflammatory mediators in mouse kidney epithelial cells. J. Biol. Chem. 269:1994;711-715.
106. Stenger S., Thüring H., Röllinghoff M., Bogdan C. Tissue expression of inducible nitric oxide synthase is closely associated with resistance toLeishmania major. J. Exp. Med. 180:1994;783-793.
107. Shull M. M., Ormsby I., Kier A. B., Pawlowski S., Diebold R. J., Yin M., Allen R., Sidman C., Proetzel G., Calvin D. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature. 359:1992;693-699.
108. Kulkarni A. B., Huh C., Becker D., Geiser A., Lyght M., Flanders K. C., Roberts A. B., Sporn M. B., Ward J. M., Karlsson S. Transforming growth factor β1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA. 90:1993;770-774.
109. Letterio J. J., Roberts A. B. Transforming growth factor-β1-deficient mice: Identification of isoform-specific activities in vivo. J. Leukocyte Biol. 59:1996;769-774.
110. Sanderson N., Factor V., Nagy P., Kopp J., Kondaiah P., Wakefield L., Roberts A. B., Sporn M. B., Thorgeirsson S. S. Hepatic expression of mature transforming growth factor β1 in transgenic mice results in multiple tissue lesions. Proc. Natl. Acad. Sci. USA. 92:1995;2572-2576.
111. Vodovotz Y., Geiser A. G., Chesler L., Letterio J. J., Campbell A., Lucia M. S., Sporn M. B., Roberts A. B. Spontaneously increased production of nitric oxide and aberrant expression of the inducible nitric oxide synthasein vivo. J. Exp. Med. 183:1996;2337-2342.
112. Thomson A. W., Starzl T. E. New immunosuppressive drugs: Mechanistic insights and potential therapeutic advances. Immunol. Rev. 136:1993;98.
113. Burkart V., Imai Y., Kallmann B., Kolb H. Cyclosporin A protects pancreatic islet cells from nitric oxide-dependent macrophage cytotoxicity. FEBS Lett. 313:1992;56-58.
114. Mühl H., Kunz D., Rob P., Pfeilschifter J. Cyclosporin derivatives inhibit interleukin 1β induction of nitric oxide synthase in renal mesangial cells. Eur. J. Pharmacol. 249:1993;95-100.
115. Akita K., Dusting G. J., Hickey H. Suppression of nitric oxide production by cyclosporin A and FK506A in rat vascular smooth muscle cells. Clin. Exp. Pharmacol. Physiol. 21:1994;231-233.
116. Amore A., Giangoglio B., Ghigo D., Peruzzi L., Porcellini M. G., Bussolino F., Costamagna C., Cacace G., Picciotto G., Mazzucco G. A possible role for nitric oxide in modulating the functional cyclosporine toxicity by arginine. Kidney Int. 47:1995;1507-1514.
117. Bloom I. T. M., Bentley F. R., Spain D. A., Garrison R. N. An experimental study of altered nitric oxide metabolism as a mechanism of cyclosporin-induced renal vasoconstriction. Br. J. Surg. 82:1995;195-198.
118. Gaston R. S., Schlessinger S. D., Sanders P. W., Barker C. V., Curtis J. J., Warnock D. G. Cyclosporine inhibits the renal response toL. J. Am. Soc. Nephrol. 5:1995;1426-1433.
119. Hattori Y., Nakanishi N. Effects of cyclosporin A and FK506 on nitric oxide and tetrahydrobiopterin synthesis in bacterial lipopolysaccharide-treated J774 macrophages. Cell. Immunol. 165:1995;7-11.
120. Levy M. M., Ketchum R. J., Perloff J. R., Park D. H., Brayman K. L. Cyclosporin A inhibits nitric oxide production in an in vitro xenogeneic islet/splenocyte co-culture system. Transplant. Proc. 26:1995;2886-2887.
121. Khanna A., Li B., Stenzel K. H., Suthanthiran M. Regulation of new DNA synthesis in mammalian cells by cyclosporine: Demonstration of a transforming growth factor β-dependent mechanism of inhibition of cell growth. Transplantation. 57:1994;577-582.
122. Wang T., Donahoe P. K., Zervos A. S. Specific interaction of type I receptors of the TGF-β family with the immunophilin FKBP-12. Science. 265:1994;674-676.
123. Wang T., Li B., Danielson P. D., Shah P. C., Rockwell S., Lechleider R. J., Martin J., Manganaro T., Donahoe P. K. The immunophilin FKB12 functions as a common inhibitor of the TGFβ family type I receptors. Cell. 86:1996;435-444.
124. Perrella M. A., Hsieh C. M., Lee W. S., Shieh S., Tsai J. C., Patterson C., Lowenstein C. J., Long N. C., Haber E., Shore S. Arrest of endotoxin-induced hypotension by transforming growth factor-β1. Proc. Natl. Acad. Sci. USA. 93:1996;2054-2059.
125. Espevik T., Figari I. S., Shalaby M. R., Lackides G. A., Lewis G. D., Shepard H. M., Palladino M. A. Inhibition of cytokine production by cyclosporin A and transforming growth factor β J. Exp. Med. 166:1987;571-576.
126. Bogdan C., Paik J., Vodovotz Y., Nathan C. Contrasting mechanisms for suppression of macrophage cytokine release by transforming growth factor-β and interleukin-10. J. Biol. Chem. 267:1992;23301-23308.
127. Florquin S., Amraoui Z., Dubois C., Decuyper J., Goldman M. The protective role of endogenously synthesized nitric oxide in staphylococcal enterotoxin B-induced shock in mice. J. Exp. Med. 180:1994;1153-1158.
128. Fukatsu K., Saito H., Fukushima R., Inoue T., Lin M., Inaba T., Muto T. Detrimental effects of a nitric oxide synthase inhibitor (NL. Arch. Surg. 130:1995;410-414.
129. Pheng L. H., Francoeur C., Denis M. The involvement of nitric oxide in a mouse model of adult respiratory distress syndrome. Inflammation. 19:1995;599-610.
130. Vouldoukis I., Riveros-Moreno V., Dugas B., Ouaaz F., Becherel P., Debre P., Moncada S., Mossalayi M. D. The killing ofLeishmania major. Proc. Natl. Acad. Sci. USA. 92:1995;7804-7808.
131. Melby P. C., Andrade-Narvaez F. J., Darnell B. J., Valencia-Pacheco G., Tryon W., Palomo-Cetina A. Increased expression of proinflammatory cytokines in chronic lesions of human cutaneous leishmaniasis. Infect. Immun. 62:1994;837-842.
132. Barral A., Teixeira M., Reis P., Vinhas V., Costa J., Lessa H., Bittencourt A. L., Reed S., Carvalho E. M., Barral-Netto M. Transforming growth factor-β in human cutaneous leishmaniasis. Am. J. Pathol. 147:1995;947-954.
133. de Belder A., Radomski M., Hancock V., Brown A., Moncada S., Martin J. Megakaryocytes from patients with coronary atherosclerosis express the inducible nitric oxide synthase. Arterioscler. Thromb. 15:1995;637-641.
134. Grainger D. J., Kemp P. R., Metcalfe J. C., Liu A. C., Lawn R. M., Williams N. R., Grace A. A., Schofield P. M., Chauhan A. The serum concentration of active transforming growth factor-β is severely depressed in advanced atherosclerosis. Nat. Med. 1:1995;74-79.
135. 1. Proc. Natl. Acad. Sci. USA. 90:1993;1018-1022.
136. 1. Arterioscler. Thromb. Vasc. Biol. 15:1995;1255-1261.
137. Freeman B. A., White C. R., Gutierrez H., Paler-Martinez A., Tarpey M. M., Rubbo H. Oxygen radical-nitric oxide reactions in vascular diseases. Adv. Pharmacol. 34:1995;45-69.
138. Rachmilewitz D., Stamler J. S., Bachwich D., Karmeli F., Ackerman Z., Podolsky D. K. Enhanced colonic nitric oxide generation and nitric oxide synthase activity in ulcerative colitis and Crohn's disease. Gut. 36:1995;718-723.
139. Babyatsky M. W., Rossiter G., Podolsky D. K. Expression of transforming growth factors alpha and beta in colonic mucose in inflammatory bowel disease. Gastroenterology. 110:1996;975-984.
140. Ohtani H., Kagaya H., Nagura H. Immunohistochemical localization of transforming growth factor-beta receptors I and II in inflammatory bowel disease. J. Gastroenterol. 30:1995.
141. Giladi E., Raz E., Karmeli F., Okon E., Rachmilewitz D. Transforming growth factor-beta gene therapy ameliorates experimental colitis in rats. Eur. J. Gastroenterol. Hepatol. 7:1995;341-347.
142. Ketteler M., Border W. A., Noble N. A. Cytokines andL. Am. J. Physiol. 36:1994.
143. Lipton S. A., Gendelman H. E. Dementia associated with the acquired immunodeficiency syndrome. N. Engl. J. Med. 332:1995;934-940.
144. Wink D. A., Hanbauer I., Krishna M. C., DeGraff W., Gamson J., Mitchell J. B. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc. Natl. Acad. Sci. USA. 90:1993;9813-9817.
145. Dinerman J. L., Dawson T. M., Schell M. J., Snowman A., Snyder S. H. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: Implications for synaptic plasticity. Proc. Natl. Acad. Sci. USA. 91:1994;4214-4218.
146. Mokhtarian F., Shi Y., Shirazian D., Morgante L., Miller A., Grob D. Defective production of anti-inflammatory cytokine, TGF-β by T cell lines of patients with active multiple sclerosis. J. Immunol. 152:1994;6003-6010.
147. Brosnan C. F., Cannella B., Battistini L., Raine C. S. Cytokine localization in multiple sclerosis lesions: Correlation with adhesion molecule expression and reactive nitrogen species. Neurology. 45:1995.
148. Bö L., Dawson T. M., Wesselingh S., Mörk S., Choi S., Kong P. A., Hanley D., Trapp B. D. Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann. Neurol. 36:1994;778-786.
149. Johnson A. W., Land J. M., Thompson E. J., Bolanos J. P., Clark J. B., Heales S. J. R. Evidence for increased nitric oxide production in multiple sclerosis. J. Neurol. Neurosurg. Psychiatr. 58:1995;107.
150. Bagasra O., Michaels F. H., Zheng Y. M., Bobroski L. E., Spitsin S. V., Fu Z. F., Tawadros R., Koprowski H. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc. Natl. Acad. Sci. USA. 92:1995;12041-12045.
151. Dorheim M., Tracey W. R., Pollock J. S., Grammas P. Nitric oxide synthase activity is elevated in brain microvessels in Alzheimer's disease. Biochem. Biophys. Res. Commun. 205:1994;659-665.
152. Vodovotz Y., Lucia M. S., Flanders K. C., Chesler L., Xie Q., Smith T. W., Weidner J., Mumford R., Webber R., Nathan C. Inducible nitric oxide synthase in tangle-bearing neurons of patients with Alzheimers disease. J. Exp. Med. 184:1996;1425-1434.
153. Flanders K. C., Lippa C. F., Smith T. W., Pollen D. A., Sporn M. B. Altered expression of transforming growth factor-β in Alzheimer's disease. Neurology. 45:1995;1561-1569.
154. Peress N. S., Perillo E. Differential expression of TGF-β1, 2 and 3 isotypes in Alzheimer's disease: A comparative immunohistochemical study with cerebral infarction, aged human and mouse control brains. J. Neuropathol. Exp. Neurol. 54:1995;802-811.
155. Schorderet M. Alzheimer's disease: Fundamental and therapeutic aspects. Experientia. 51:1995;99-105.
156. Hu J., el-Fakahany E. E. β-Amyloid 25-35 activates nitric oxide synthase in a neuronal clone. NeuroReport. 4:1993;760-762.
157. Klegeris A., Walker D. G., McGeer P. L. Activation of macrophages by Alzheimer β-amyloid peptide. Biochem. Biophys. Res. Commun. 199:1994;984-991.
158. Meda L., Cassatella M. A., Szendrei G. I., Otvos Jr., Baron P., Villalba M., Ferrari D., Rossi F. Activation of microglial cells by β-amyloid protein and interferon-γ Nature. 374:1995;647-650.
159. Chao C. C., Hug C., Kravitz F. H., Tsang M., Anderson W. R., Peterson P. K. Transforming growth factor β protects human neurons against β-amyloid induced injury. Mol. Chem. Neuropathol. 23:1994;159-169.
160. Ren R. F., Flanders K. C. Transforming growth factors-β protect primary rat hippocampal neuronal cultures from degeneration induced by β-amyloid peptide. Brain Res. 1996.
161. Prehn J. H. M., Bindokas V. P., Jordan J., Galindo M. F., Ghadge G. D., Roos R. P., Boise L. H., Thompson C. B., Krajewski S., Reed J. C. Protective effect of transforming growth factor-β1 on β-amyloid neurotoxicity in rat hippocampal neurons. Mol. Pharmacol. 49:1996;319-328.
162. Behl C., Davis J. B., Lesley R., Schubert D. Hydrogen peroxide mediates amyloid β protein toxicity. Cell. 77:1994;817-827.
163. Colton C. A., Snell J., Chernyshev O., Gilbert D. L. Induction of superoxide anion and nitric oxide production in cultured microglia. Ann. N.Y. Acad. Sci. 738:1994;54-63.
164. Kowall N. W., Beal M. F. Cortical somatostatin, neuropeptide Y, and NADPH diaphorase neurons: Normal anatomy and alterations in Alzheimer's disease. Ann. Neurol. 23:1988;105-114.
165. Hyman B. T., Marzloff K., Wenninger J. J., Dawson T. M., Bredt D. S., Snyder S. H. Relative sparing of nitric oxide synthase-containing neurons in the hippocampal formation in Alzheimer's disease. Ann. Neurol. 32:1992;818-820.
166. Tsunawaki S., Sporn M., Ding A., Nathan C. Deactivation of macrophages by transforming growth factor-β Nature. 334:1988;260-262.
167. 22. J. Biol. Chem. 270:1995;30334-30338.
168. Vodovotz Y. A modified assay for serum nitrite and nitrate. BioTechniques. 20:1996;390-394.