Muscle wasting and dedifferentiation induced by oxidative stress in a murine model of cachexia is prevented by inhibitors of nitric oxide synthesis and antioxidants

EMBO Journal

Volumn 15, Issue 8, 1996, Pages 1753-1765

  Buck, Martina ^a   Chojkier, Mario ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AIDS; Cancer; Jun D; Myogenin; Myosin creatine phosphokinase

Indexed keywords

3 AMINO 1 (3 TRIFLUOROMETHYLPHENYL) 2 PYRAZOLINE; ALPHA TOCOPHEROL; ANTIOXIDANT; ANTISENSE OLIGONUCLEOTIDE; ARGININE DERIVATIVE; CREATINE KINASE; DITHIOTHREITOL; MYOGENIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NUCLEAR PROTEIN; PHORBOL ESTER; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CACHEXIA; CONTROLLED STUDY; DNA TRANSCRIPTION; ENZYME BINDING; HUMAN; HUMAN CELL; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SKELETAL MUSCLE;

EID: 0029921173     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00524.x     Document Type: Article

References (73)

1. Abate, C., Patel, L., Rauscher, F.J.,III and Curran, T. (1990) Redox regulation of Fos and Jun DNA-binding activity in vitro. Science, 249, 1157-1161
2. Akira, S., Hirano, T., Taga, T. and Kishimoto, T. (1990) Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J., 4, 2860-2867.
3. Bengal, E., Ransone, L., Scharfmann, R., Dwarki, V.J., Tapscott, S.J., Weintraub, H. and Verma, J.M. (1992) Functional antagonism between c-Jun and MyoD proteins: a direct physical association. Cell, 68, 507-19.
4. Beutler, B. (1992) Tumor Necrosis Factors: The Molecules and Their Emerging Role in Medicine. Raven Press, New York.
5. Beutler, B. and Cerami, A. (1986) Cachectin and tumour necrosis factor as two sides of the same biological coin. Nature, 320, 584-588.
6. Brennan, T. and Olson, E.N. (1990) Myogenin resides in the nucleus and acquires high affinity for a conserved enhancer element on heterodimerization. Genes Dev., 4, 582-595.
7. Brenner, D.A. and Chojkier, M. (1987) Acetaldehyde increases collagen gene transcription in cultured human fibroblasts. J. Biol. Chem., 262, 17690-17695.
8. Brenner, D.A., O'Hara, M., Angel, P., Chojkier, M. and Karin, M. (1989) Prolonged activation of jun and collagenase genes by tumour necrosis factor α. Nature, 337, 661-663.
9. Brenner, D.A., Buck, M., Feitelberg, S.P. and Chojkier, M. (1990) Tumor necrosis factor α inhibits albumin gene expression in a murine model of cachexia. J. Clin. Invest., 85, 248-255.
10. Buck, M , Turler, H. and Chojkier, M. (1994) LAP (NF-IL6), a tissue-specific transcriptional activator, is an inhibitor of hepatoma cell proliferation. EMBO J., 13, 851-860.
11. Chaudhary, A.K., Munetaka, N., Reddy, G.R., Yeola, S.N., Morrow, J.D., Blair, I.A. and Marnett, L.J. (1994) Detection of endogenous malondialdehyde-deoxyguanosine adducts in human liver. Science, 265, 1580-1582.
12. Cheng, J., Turksen, K., Yu, Q.C., Schreiber, H., Teng, M. and Fuchs, E. (1992) Cachexia and graft-vs.-host-disease-type skin changes in keratin promoter-driven TNF-α transgenic mice. Genes Dev., 6, 1444-1456.
13. Chojkier, M., Houglum, K., Solis-Herruzo, J.A. and Brenner, D.A. (1989) Stimulation of collagen gene expression by ascorbic acid in cultured human fibroblasts. A role for lipid peroxidation? J. Biol. Chem., 264, 16957-16962.
14. Costelli, P., Carbó, N., Tessitore, L., Bagby, G.J., Lopez-Soriano, F.J., Argilés, J.M. and Baccine, F.M. (1993) Tumor necrosis factor-α mediates changes in tissue protein turnover in a rat cancer cachexia model. J. Clin. Invest., 92, 2783-2789.
15. Descombes, P., Chojkier, M., Lichtsteiner, S., Falvey, E. and Schibler, U. (1990) LAP, a novel member of the C/EBP gene family, encodes a liver-enriched transcriptional activator protein. Genes, Dev., 4, 1541-1551.
16. Dinarello, C.A., Cannon, J.G., Wolff, S.M , Bernheim, H.A., Beutler, B., Cerami, A , Figari, I.S., Palladino, M.A.,Jr and O'Connor, J.V. (1986) Tumor necrosis factor (cachectin) is an endogenous pyrogen and induces production of IL-1. J. Exp. Med., 163, 1433-1450.
17. Flores, E.A., Bistran, B.R., Pompselli, J.J., Dinarello, C.A , Blackburn, G.L. and Istfan, N.W (1989) Infusion of tumor necrosis/cachectin promotes muscle catabolism in the rat: a synergistic effect with interleukin 1. J. Clin. Invest., 83, 1614-1622.
18. Fong, Y. et al. (1989) Cachectin/TNF or IL-1 α induces cachexia with redistribution of body proteins. Am. J. Physiol., 256, R659-R665.
19. Goodman, J.C., Robertson, C.S., Grossman, R.G. and Narayan, R.K. (1990) Elevation of tumor necrosis factor in head injury. J. Neuroimmunol , 30, 213-217.
20. Grau, G.E., Taylor, T.E., Molyneaux, M.E., Wirima, M.B., Vassalli, P., Hommel, M. and Lambert, P.H. (1989) Tumor necrosis factor and disease severity in children with falciparum malaria. New Engl. J. Med., 320, 1586-1591.
21. Hasty, P., Bradley, A., Morris, J.H., Edmondson, D.G., Venuti, J.M., Olson, E.N. and Klein, W.H. (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature, 364, 501-506.
22. Henkel, T., Machleidt, T , Alkalay, I , Kronke, M., Ben-Neriah, Y. and Baeuerle, P.A. (1993) Rapid proteolysis of IκB-α is necessary for activation of transcription factor NF-κB. Nature, 365, 182-185.
23. Holvoet, P., Perez, G., Zhao, Z., Brouwers, E., Bernar, H. and Collen, D. (1995) Malondialdehyde-modified low density lipoproteins in patients with atherosclerotic disease. J. Clin. Invest., 95, 2611-2619.
24. Houglum, K., Filip, M., Witztum, J. and Chojkier, M. (1990) Malondialdehyde and 4-hydroxynonenal protein adducts in plasma and liver of rats with iron overload. J. Clin. Invest , 86, 1991-1998.
25. 1(I) gene expression in cultured human fibroblast: modulation of constitutive collagen gene expression by lipid peroxidation. J. Clin. Invest., 87, 2230-2235.
26. Kaushal, S., Schneider, J.W., Nadal-Ginard, B. and Mahdavi, V. (1994) Activation of the myogenic lineage by MEF2A, a factor that induces and cooperates with MyoD. Science, 266, 1236-1240.
27. Kilbourn, R.G., Gross, S.S., Jurban, A., Adams, J., Griffith, O.W., Levi, R. and Lodato, R.F. (1990) N-Methy-L-arginine inhibits tumor necrosis factor-induced hypotension: implications for the involvement of nitric oxide. Proc. Natl Acad. Sci. USA, 87, 3629-3632.
28. Kirchberger, M. (1991) Excitation and contraction of skeletal muscle. In West, J.B. (ed.), Physiological Basis of Medical Practice. Williams & Wilkins, Baltimore, MD, pp. 62-102.
29. Kobzik, L., Reid, M.B., Bredt, D.S. and Stamler, J.S. (1994) Nitric oxide in skeletal muscle. Nature, 372, 546-548.
30. Lassar, A.B., Buskin, D.L., Davis, R.L. and Apone, S. (1989) MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell, 58, 823-831.
31. Li, L., Hu, J S. and Olson, E.N. (1990) Different members of the jun family exhibit distinct patterns of expression in response to type β transforming growth factor. J. Biol. Chem., 265, 1556-1562
32. Li, L., Zhou, J., James, G., Heller-Harrison, R., Czech, M.P. and Olson, E N. (1992a) FGF inactivates myogenic helix-loop-helix proteins through phosphorylation of a conserved protein kinase C site in their DNA-binding domains. Cell, 71, 1181-1194.
33. Li, L., Chambard, J.-C., Karin, M. and Olson, E.N. (1992b) Fos and jun repress transcriptional activation by myogenin and MyoD: the amino terminus of Jun can mediate repression. Genes Dev., 6, 676-689.
34. Lipton, S.A , Choi, Y.-B., Pan, Z.-H., Lei, S.Z., Chen, H.-S.V., Sucher, N.J., Loscalzo, J., Singel, D.J. and Stamler, J.S. (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature, 364, 626-632
35. McWhirter, R.B. and Hille, R. (1991) The reductive half-reaction of xanthine oxidase J. Biol. Chem., 35, 23724-23731.
36. Meier, B., Radeke, H.H , Selle, S. Younes, M., Sies, H., Resch, K and Habermehl, G.G. (1989) Human fibroblasts release reactive oxygen species in response to interleukin-1 or tumor necrosis factor-α. Biochem J., 263, 539-545.
37. Moldawer, L.L., Svaninger, G., Gelin, J. and Lundholm, K.G. (1987) Interleukin 1 and tumor necrosis factor do not regulate protein balance in skeletal muscle. Am. J Physiol., 253, C766-C773.
38. Murre, C., McCaw, PS and Baltimore, D. (1989) A new DNA binding motif in immunoglobulin enhancer binding, daughterless, myoD and myc proteins. Cell, 56, 777-783.
39. Nabeshima, Y., Hanaoka, K , Hayasaka, M , Esumi, E., Shaowei, L., Nonaka, I. and Nabeshima, Y.-I. (1993) Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature, 364, 532-535.
40. Nakabeppu, Y., Ryder, K. and Nathans, D. (1988) DNA binding activities of three murine Jun proteins, stimulation by fos Cell, 55, 907-915.
41. Oliff, A., Defeo-Jones, D , Boyer, M., Martinez, D., Kiefer, D., Vuocolo, G., Wolfe, A. and Socher, S H. (1987) Tumors secreting human TNFα/ cachectin induce cachexia in mice Cell, 50, 555-563.
42. Palombella, V.J., Rando, O.J., Goldberg, A.L. and Maniatis, T. (1994) The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell, 78, 773-785
43. Pfarr, C., Mechta, F., Spyrou, G., Lallemand, D., Carillo, S. and Yaniv, M. (1994) Mouse Jun-D negatively regulates fibroblast growth and antagonizes transformation by ras. Cell, 76, 747-760.
44. Roubenoff, R., Roubenoff, R.A., Cannon, J.G., Kehayias, J.J., Zhuang, H., Dawson-Hughes, B., Dinarello, C.A. and Rosenberg, IH. (1994) Rheumatoid cachexia: cytokine-driven hypermetabolism accompanying reduced body cell mass in chronic inflammation. J. Clin. Invest., 93, 2379-2386.
45. Ryseck, R.-P. and Bravo, R. (1991) c-Jun, Jun B and Jun D differ in their binding affinities to AP-1 and CRE consensus sequences: effect of FOS proteins. Oncogene, 6, 533-542.
46. Sassoon, D., Lyons, G., Wright, W.E., Lin, V., Lassar, A., Weintraub, H and Buckingham, M. (1989) Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature, 341, 303-307.
47. Schauenstein, E., Estebauer, H and Zollner, H. (1977) In Schauenstein, E , Estebaur, H. and Zollner, H. (eds). Aldehydes in Biological Systems. Pion, London, pp. 1-102.
48. Schreck, R., Rieber, P. and Baeuerle, P. (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J., 10, 2247-2258.
49. Schulze-Osthoff, K., Beyaert, R., Vandevoorde, V., Haegeman, G. and Fiers, W. (1993) Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene-inductive effects of TNF. EMBO J., 12, 3095-3104
50. Scuderi, P., Lam, K.S., Ryan, K.J., Petersen, E., Sterling, K.E., Finley, P.R . Ray, C.G and Sylmen, D.J. (1986) Raised serum levels of tumour necrosis factor in parasitic infections. Lancet, ii, 1364-1365.
51. Sherry, B.A., Gelin, J., Fong, Y., Marano, M., Wei, H., Cerami, A , Lowry, S.F., Lundholm, K.G. and Moldawer, L.L (1989) Anticachectin/ tumor necrosis factor-alpha antibodies attenuate development of cachexia in tumor models. FASEB J., 3, 1956-1962.
52. Skapek, S.X., Rhee, J., Spicer, D.B. and Lassar, A.B. (1995) Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science, 267, 1022-1024.
53. Spiegelman, B.M. and Hotamisligil, G.S. (1993) Through thick and thin: wasting, obesity and TNFα Cell, 73, 625-627.
54. Stalmer, J.S. (1994) Redox signaling: nitrosylation and related interactions of nitric oxide. Cell, 78, 931-936
55. Starnes, H.F.,Jr. Warren, R.S., Jeevanandam, M., Gabrilove, J.L , Larchian, W., Oettgen, H.F and Brennan, M F. (1988) Tumor necrosis factor and the acute metabolic response to tissue injury in man. J. Clin. Invest., 82, 1321-1325.
56. Strassmann, G., Fong, M., Kenney, J.S. and Jacob, C.O. (1992) Evidence for the involvement of interleukin 6 in experimental cancer cachexia. J. Clin. Invest., 89, 1681-1684.
57. Tapscott, S.J., Thayer, M.J. and Weintraub, H. (1993) Deficiency in rhabdomyosarcomas of a factor required for myoD activity and myogenesis. Science, 259, 1450-1453.
58. Tracey, K.J. (1992) The acute and chronic pathophysiologic effects of TNF: mediation of septic shock and wasting (cachexia). In Butler, B. (ed), Turner Necrosis Factors: The Molecules and Their Emerging Role in Medicine. Raven Press, New York, pp. 255-273.
59. Tracey, K.J. and Cerami, A (1993) Tumor necrosis factor, other cytokines and disease. Annu. Rev. Cell Biol., 9, 317-343.
60. Tracey, K.J. et al (1988) Cachectin/tumor necrosis factor induces cachexia, anemia and inflammation J. Exp. Med., 167, 1211-1227.
61. Tracey, K.J., Morgello, S., Koplin, B., Fahey, T.J.,III, Fox, J., Aledo, A , Manogue, K.R. and Cerami, A. (1990) Metabolic effects of cachectin/ tumor necrosis factor are modified by site of production. J. Clin. Invest., 86, 2014-2024.
62. Traenckner, E.B.-M., Wilk, S. and Baeuerle, P.A. (1994) A proteasome inhibitor prevents activation of NF-κB and stabilizes a newly phosphorylated form of IκB-α that is still bound to NF-κB. EMBO J., 13, 5433-5441.
63. Trautwein, C., Caelles, C., van der Geer, P., Hunter, T., Karin, M. and Chojkier, M. (1993) Transactivation by NF-IL6/LAP is enhanced by phosphorylation of its activation domain. Nature, 364, 544-547.
64. Trautwein, C., van der Geer, P., Karin, M., Hunter, T. and Chojkier, M. (1994) Protein kinase A and C site-specific phosphorylations of LAP (NF-IL6) modulate its binding affinity to DNA-recognition elements. J. Clin. Invest , 93, 2554-2561
65. Vale, R.D. (1994) Getting a grip on myosin. Cell, 78, 733-737.
66. Voth, R., Rossol, S., Klein, K., Hess, G., Schutt, K H., Schroder, H.C., Buschenfelde, K.-H.M.Z. and Müller, W.E.G. (1990) Differential gene expression of IFN-α and tumor necrosis factor-α in peripheral blood mononuclear cells from patients with AIDS related complex and AIDS. J. Immunol , 144, 970-975.
67. Waage, A., Halstensen, A. and Espevik, T. (1987) Association between tumour necrosis factor in serum and fatal outcome in patients with meningococcal disease Lancet, i, 355-357.
68. Weintraub, H., Davis, R., Lockshon, D. and Lassar, A. (1990) MyoD binds cooperatively to two sites in a target enhancer sequence: occupancy of two sites is required for activation. Proc. Natl Acad. Sci. USA, 87, 5623-5627.
69. Wing, S.S. and Goldberg, A L. (1993) Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am. J. Physiol., 264, E668-E676.
70. Wong, GH.W , Elwell, J.H., Oberley, L.W. and Goeddel, D.V. (1989) Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell, 58, 923-931
71. Xanthoudakis, S. and Curran, T. (1992) Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity EMBO J., 11, 653-665
72. Xanthoudakis, S., Miao, G., Wang, F., Pan, Y.C.E. and Curran, T. (1992) Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme EMBO J., 11, 3323-3335.
73. Yoneda, T., Alsina, M.A., Chavez, J.B., Bonewald, L., Nishimura, R. and Mundy, G.R. (1991) Evidence that tumor necrosis factor plays a pathogenetic role in the paraneoplastic syndromes of cachexia, hypercalcemia and leukocytosis in a human tumor in nude mice. J. Clin. Invest., 87, 977-985