A new model of cancer cachexia: Contribution of the ubiquitin-proteasome pathway

American Journal of Physiology - Endocrinology and Metabolism

Volumn 277, Issue 2 40-2, 1999, Pages

  Lazarus, Douglas D ^a   Destree, Antonia T ^a   Mazzola, Laureen M ^a   McCormack, Teresa A ^a   Dick, Lawrence R ^a   Xu, Bi ^a   Huang, Jian Q ^a   Pierce, Jacqueline W ^a   Read, Margaret A ^a   Coggins, Michael B ^a   Solomon, Vered ^b   Goldberg, Alfred L ^b   Brand, Stephen J ^a   Elliott, Peter J ^a  

^a ProScript   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Colon 26; E2(14K); Lactacystin; Muscle weight loss; Protein metabolism; Proteosome inhibitors

Indexed keywords

DEXAMETHASONE; INDOMETACIN; LACTACYSTIN; MUSCLE PROTEIN; PROTEASOME; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CACHEXIA; CANCER; COLON TUMOR; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; MALE; MOUSE; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; WEIGHT REDUCTION;

EID: 0032878934     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.1999.277.2.e332     Document Type: Article

References (62)

1. Andreyev, H. J. N., A. R. Norman, J. Oates, and D. Cunningham. Why do patients with weight loss have a worse outcome when undergoing chemotherapy for gastrointestinal malignancies? Eur. J. Cancer 34: 503-509, 1998.
2. Auclair, D., D. R. Garrel, A. Chaouki Zerouala, and L. H. Ferland. Activation of the ubiquitin pathway in rat skeletal muscle by catabolic doses of glucocorticoids. Am. J. Physiol. 272 (Cell Physiol. 41): C1007-C1016, 1997.
3. Bibby, M. C., J. A. Double, S. A. Ali, K. C. H. Fearon, R. A. Brennan, and M. J. Tisdale. Characterization of a transplantable adenocarcinoma of the mouse producing cachexia in recipient animals. J. Natl. Cancer Inst. 78: 539-546, 1987.
4. Bistrian, B. R., G. L. Blackburn, N. S. Scrimshaw, and J.-P. Flatt. Cellular immunity in semistarved states in hospitalized adults. Am. J. Clin. Nutr. 28: 1148-1153, 1978.
5. Cohen, S. A., and D. P. Michaud. Synthesis of a fluorescent derivatizing reagent, 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate, and its application for the analysis of hydrolysate amino acids via high-performance liquid chromatography. Anal. Biochem. 211: 279-287, 1993.
6. Corbett, T. H., D. P. Griswold, Jr., B. J. Roberts, J. C. Peckman, and F. M. Schabel, Jr. Tumor induction relationships in development of transplantable cancers of the colon in mice for chemotherapy assays, with a note on carcinogen structure. Cancer Res. 35: 2434-2439, 1975.
7. Costelli, P., N. Carbo, L. Tessitore, G. J. Bagby, F. J. Lopez-Soriano, J. P. Argiles, and F. M. Baccino. Tumor necrosis factor-α mediates changes in tissue protein turnover in a rat cancer cachexia model. J. Clin. Invest. 92: 2783-2789, 1993.
8. Dagnelie, P. C., J. D. Bell, S. C. Williams, T. E. Bates, P. D. Abel, and C. S. Foster. Effect of fish oil on cancer cachexia and host liver metabolism in rats with prostate tumors. Lipids 29: 195-203, 1994.
9. DeWys, W. D., C. Begg, P. T. Lavin, P. R. Band, J. M. Bennett, J. R. Bertino, M. H. Cohen, H. O. Douglass, Jr., P. F. Engstrom, E. Z. Ezdinli, J. Horton, G. J. Johnson, C. G. Moertel, M. M. Oken, C. Perlia, C. Rosenbaum, M. N. Silverstein, R. T. Skeel, R. W. Sponzo, and D. C. Tormey. Prognostic effect of weight loss prior to chemotherapy in cancer patients. Am. J. Med. 69: 491-497, 1980.
10. Earnest, D. L. NSAID-induced gastric injury: its pathogenesis and management. Semin. Arthritis Rheum. 19: 6-10, 1990.
11. Fenteany, G., R. F. Standaert, W. S. Lane, S. Choi, E. J. Corey, and S. L. Schreiber. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268: 726-731, 1995.
12. Fujimoto-Ouchi, K., S. Tamura, K. Mori, Y. Tanaka, and H. Ishitsuka. Establishment and characterization of cachexia-inducing and -non-inducing clones of murine colon 26 carcinoma. Int. J. Cancer 61: 522-528, 1995.
13. Fujita, J., T. Tsujinaka, M. Yano, C. Ebisui, H. Saito, A. Katsume, K. Akamatsu, Y. Ohsugi, H. Shiozaki, and M. Monden. Anti-interleukin-6 receptor antibody prevents muscle atrophy in colon-26 adenocarcinoma-bearing mice with modulation of lysosomal and ATP-ubiquitin-dependent proteolytic pathways. Int. J. Cancer 68: 637-643, 1996.
14. Garattini, S., A. Bizzi, M. G. Donelli, A. Guaitani, R. Samandi, and F. Spreafici. Anorexia and cancer in animals and man. Cancer Treat. Rev. 7: 115-139, 1980.
15. Garcia-Martinez, C., N. Agell, M. Llovera, F. J. Lopez-Soriano, and J. M. Argiles. Tumor necrosis factor-α increases the ubiquitinization of rat skeletal muscle proteins. FEBS Lett. 323: 631-637, 1993.
16. Garcia-Martinez, C., M. Llovera, N. Agell, F. J. Lopez-Soriano, and J. M. Argiles. Ubiquitin gene expression in skeletal muscle is increased by tumor necrosis factor-α. Biochem. Biophys. Res. Commun. 201: 682-686, 1994.
17. Gelin, J., C. Andersson, and K. Lundholm. Effects of indomethacin, cytokines, and cyclosporin A on tumor growth and the subsequent development of cancer cachexia. Cancer Res. 51: 880-885, 1991.
18. Godil, A., D. Berriman, S. Knapik, M. Norman, F. Godil, and A. F. Firek. Diabetic neuropathic cachexia. West. J. Med. 165: 382-385, 1996.
19. Heber, D., L. O. Byerley, and N. S. Tchekmedyian. Hormonal and metabolic abnormalities in the malnourished cancer patient: effects on host-tumor interaction. J. Paren. Enter. Nutr., Suppl. 6, 16: 60S-64S, 1992.
20. Kambayashi, T, H. R. Alexander, M. Fong, and G. Strassmann. Potential involvement of IL-10 in suppressing tumor-associated macrophages. J. Immunol. 154: 3383-3390, 1995.
21. Kotler, D. P., and C. Grunfeld. Pathophysiology and treatment of the AIDS wasting syndrome. AIDS Clinical Review, edited by P. A. Volberding and M. A. Jacobson. Monticello, NY: Marcel Dekker, 1996, p. 229-275.
22. Kreis, T., and R. Vale (Editors). Guidebook to the Cytoskeletal and Motor Proteins. New York: Oxford Univ. Press, 1994, p. 193.
23. Larsson, J., I. Akerlund, J. Permerth, and J. O. Hornquist. Impact of nutritional state on quality of life in surgical patients. Nutrition 11: 217-220, 1995.
24. Llovera, M., C. Garcia-Martinez, N. Agell, M. Marzabal, F. J. Lopez-Soriano, and J. M. Argiles. Ubiquitin gene expression is increased in skeletal muscle of tumour-bearing rats. FEBS Lett. 338: 311-318, 1994.
25. Llovera, M., C. Garcia-Martinez, J. Lopez-Soriano, N. Carbo, N. Agell, F. J. Lopez-Soriano, and J. M. Argiles. Role for TNF receptor 1 in protein turnover during cancer cachexia using gene knockout mice. Mol. Cell. Endocrinol. 142: 183-189, 1998.
26. Loprinzi, C. L., R. M. Goldberg, and N. L. Burnham. Cancer-associated anorexia and cachexia. Implications for drug therapy. Drugs 43: 499-506, 1992.
27. Lorite, M. J., M. G. Thompson, J. L. Drake, G. Carling, and M. J. Tisdale. Mechanism of muscle protein degradation induced by a cancer cachectic factor. Br. J. Cancer 78: 850-856, 1998.
28. Lundholm, K., J. Gelin, A. Hyltander, C. Lonnroth, R. Sandstrom, and G. Svaninger. Anti-inflammatory treatment may prolong survival in undernourished patients with metastatic solid tumors. Cancer Res. 54: 5602-5606, 1994.
29. McDevitt, T. M., and M. J. Tisdale. Tumor-associated hypoglycemia in a murine cachexia model. Br. J. Cancer 66: 815-820, 1992.
30. Millward, D. J., and P. C. Bates. Protein degradation in skeletal muscle: implications of a first order reaction for the degradative process. Acta Biol. Med. Ger. 40: 1309-1315, 1981.
31. Mori, K., K. Fujimoto-Ouchi, T. Ishikawa, F. Sekiguchi, H. Ishitsuka, and Y. Tanaka. Murine interleukin-12 prevents the development of cancer cachexia in a murine model. Int. J. Cancer 67: 849-855, 1996.
32. Medina, R., S. Wing, and A. L. Goldberg. Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy. Biochem. J. 307: 631-637, 1995.
33. Mulligan, H. D., S. M. Mahoney, J. A. Ross, and M. J. Tisdale. Weight loss in a murine cachexia model is not associated with the cyokines tumor necrosis factor-α or interleukin-6. Cancer Lett. 65: 239-243, 1992.
34. Ohira, T., K. Nishio, Y. Ohe, H. Arioka, M. Nishio, Y. Funayama, H. Ogasawara, M. Fukuda, K. Yazawa, H. Kato, and N. Saijo. Improvement by eicosanoids in cancer cachexia induced by LLC-IL6 transplantation. J. Cancer Res. Clin. Oncol. 122: 711-715, 1996.
35. Ottery, F. D. Supportive nutrition to prevent cachexia and improve quality of life. Semin. Oncol. 22: 98-111, 1995.
36. Pisters, P. W., and D. B. Pearlstone. Protein and amino acid metabolism in cancer cachexia: investigative techniques and therapeutic interventions. Crit. Rev. Clin. Lab. Sci. 30: 223-272, 1993.
37. Puccio, M., and L. Nathanson. The cancer cachexia syndrome. Semin. Oncol. 24: 277-287, 1997.
38. Rannels, R., and L. S. Jefferson. Effects of glucocorticoids on muscle protein turnover in perfused rat hemicorpus. Am. J. Physiol. 238 (Endocrinol. Metab. 1): E564-E572, 1980.
39. Santidrian, S., P. Marchon, X. H. Zhao, H. N. Munro, and V. R. Young. Effect of corticosterone on rate of myofibrillar protein breakdown in adult male rats. Growth 45: 342-350, 1981.
40. Shaw, J. H., D. A. Humberstone, R. G. Douglas, and J. Koea. Leucine kinetics in patients with benign disease, non-weight-losing cancer, and cancer cachexia: studies at the whole-body and tissue level and the response to nutritional support. Surgery 109: 37-50, 1991.
41. Shoji, S., and R. J. Pennington. The effect of cortisone on protein breakdown and synthesis in rat skeletal muscle. Mol. Cell. Endocrinol. 6: 159-169, 1977.
42. Soda, K., M. Kawakami, A. Kashii, and M. Miyata. Manifestations of cancer cachexia induced by colon 26 adenocarcinoma are not fully ascribable to interleukin-6. Int. J. Cancer 62: 332-336, 1995.
43. Solomon, V., V. Baracos, P. Sarraf, and A. L. Goldberg. Rates of ubiquitin conjugation increase when muscles atrophy, largely through activation of the N-end rule pathway. Proc. Natl. Acad. Sci. USA 95:12602-12607, 1998.
44. Solomon, V., and A. L. Goldberg. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J. Biol. Chem. 27: 26690-26697, 1996.
45. Solomon, V., S. H. Lecker, and A. L. Goldberg. The N-end rule pathway catalyzes a major fraction of the protein degradation in skeletal muscle. J. Biol. Chem. 273: 25216-25222, 1998.
46. Stein, R. L., F. Melandri, and L. Dick. Kinetic characteristics of the chymotryptic activity of the 20S proteasome. Biochemistry 35: 3899-3908, 1996.
47. Strassmann, G., M. Fong, J. S. Kenney, and C. O. Jacob. Evidence for the involvement of interleukin 6 in experimental cancer cachexia. J. Clin. Invest. 89: 1681-1684, 1992.
48. Strassmann, G. Experimental cancer cachexia: role for IL-6. In: Clinical Applications of Cytokines, edited by J. J. Oppenheim. New York: Oxford Univ. Press, 1993, p. 181-185.
49. Strassmann, G., Y. Masui, R. Chizzonite, and M. Fong. Mechanisms of experimental cancer cachexia. J. Immunol. 150: 2341-2345, 1993.
50. Tanaka, Y., T. Tanaka, and H. Ishitsuka. Antitumor activity of indomethacin in mice bearing advanced colon 26 carcinoma compared with those with early transplants. Cancer Res. 49: 5935-5939, 1989.
51. Tawa, N. E., Jr., R. Odessey, and A. L. Goldberg. Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J. Clin. Invest. 100: 197-203, 1997.
52. Temparis, S., M. Asensi, D. Taillandier, E. Aurousseau, D. Larband, A. Obled, D. Bechet, M. Ferrara, J. M. Estrela, and D. Attaix. Increased ATP-ubiqui tin-dependent proteolysis in skeletal muscles of tumor-bearing rats. Cancer Res. 54: 5568-5573, 1994.
53. Tessitore, L., G. Bonelli, and F. M. Baccino. Early development of protein metabolic perturbations in the liver and skeletal muscle of tumour-bearing rats. A model system for cancer cachexia. Biochem. J. 241: 153-159, 1987.
54. Tessitore, L., P. Costelli, and F. M. Baccino. Pharmacological interference with tissue hypercatabolism in tumour-bearing rats. Biochem. J. 299: 71-78, 1994.
55. Tiao, G., J. Fagan, V. Roegner, M. Lieberman, J. J. Wang, J. E. Fischer, and P. O. Hasselgren. Energy-ubiquitin-dependent muscle proteolysis during sepsis in rats is regulated by glucocorticoids. J. Clin. Invest. 97: 339-348, 1996.
56. Tisdale, M. J., and S. A. Beck. Inhibition of tumour-induced lipolysis in vitro and cachexia and tumour growth in vivo by eicosapentaenoic acid. Biochem. Pharmacol. 41: 103-107, 1991.
57. Todorov, P., P. Cariuk, T. McDevitt, B. Coles, K. Fearon, and M. Tisdale. Characterization of a cancer cachectic factor. Nature 379: 739-742, 1996.
58. Tsujinaka, T., J. Fujita, C. Ebisui, M. Yano, E. Kominami, K. Suzuki, K. Tanaka, A. Katsume, Y. Ohsugi, H. Shiozaki, arid M. Monden. Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice. J. Clin. Invest. 97: 244-249, 1996.
59. Wing, S. S., and D. Banville. 14-kDa ubiquitin-conjugating enzyme: structure of the rat gene and regulation upon fasting and by insulin. Am. J. Physiol. 267 (Endocrinol. Metab. 30): E39-E48, 1994.
60. Wing, S. S., F. Dumas, and D. Banville. A rabbit reticulocyte ubiquitin carrier protein that supports ubiquitin-dependent proteolysis (E2-14k) is homologous to the yeast DNA repair gene RAD6. J. Biol. Chem. 267: 6495-6501, 1992.
61. Wing, S. S., A. L. Haas, and A. L. Goldberg. Increase in ubiquitin-protein conjugates concomitant with the increase in proteolysis in rat skeletal muscle during starvation and atrophy denervation. Biochem. J. 307: 639-645, 1995.
62. Yasumoto, K., N. Mukaida, A. Harada, K. Kuno, M. Akiyama, E. Nakashima, N. Fujioka, M. Mai, T. Kasahara, K. Fujimoto-Ouchi, K. Mori, Y. Tanaka, and K. Matsushima. Molecular analysis of the cytokine network involved in cachexia in colon 26 adenocarcinoma-bearing mice. Cancer Res. 55: 921-927, 1995.