A key role for leukemia inhibitory factor in C26 cancer cachexia

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19976-19986

  Seto, Danielle N ^a   Kandarian, Susan C ^a   Jackman, Robert W ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODIES; CHEMICAL ACTIVATION; COMPUTER SOFTWARE MAINTENANCE; DIAGNOSIS; DISEASES; GENES; MAMMALS; PHOSPHORYLATION; TRANSCRIPTION; TUMORS;

CANCER CACHEXIA; CANCER CELLS; COLON CARCINOMA; CONDITIONED MEDIUM; DOMINANT NEGATIVE; LEUKEMIA INHIBITORY FACTORS; OVER-EXPRESSION; REPORTER GENE;

IMMUNOLOGY;

INTERLEUKIN 6; JANUS KINASE 2; LEUKEMIA INHIBITORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOSTATIN; ONCOSTATIN M; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN INHIBITOR OF ACTIVATED STAT1; PROTEIN INHIBITOR OF ACTIVATED STAT3; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CULTURE MEDIUM; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; JAK2 PROTEIN, MOUSE; LIF PROTEIN, MOUSE; LUCIFERASE; NEUTRALIZING ANTIBODY; OSM PROTEIN, MOUSE; PROTEIN KINASE INHIBITOR; STAT3 PROTEIN, MOUSE; TRANSCRIPTION FACTOR AP 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CACHEXIA; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME PHOSPHORYLATION; GENE; GENE OVEREXPRESSION; IN VIVO STUDY; MALE; MOUSE; MUSCLE ATROPHY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; STAT3CBETA EGFP GENE; TRANSCRIPTION INITIATION; UPREGULATION; ADENOCARCINOMA; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SIZE; COLON TUMOR; CULTURE MEDIUM; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHARMACOLOGY; PHOSPHORYLATION; REPORTER GENE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TUMOR CELL LINE;

MUS;

ADENOCARCINOMA; ANIMALS; ANTIBODIES, NEUTRALIZING; CACHEXIA; CELL LINE, TUMOR; CELL SIZE; COLONIC NEOPLASMS; CULTURE MEDIA, CONDITIONED; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; JANUS KINASE 2; LEUKEMIA INHIBITORY FACTOR; LUCIFERASES; MALE; MICE; MUSCLE FIBERS, SKELETAL; ONCOSTATIN M; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP-1;

EID: 84939213063     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.638411     Document Type: Article

References (43)

1. Tisdale, M. J. (2009) Mechanisms of cancer cachexia. Physiol. Rev. 89, 381-410
2. Argilés, J. M., Busquets, S., and López-Soriano, F. J. (2005) The pivotal role of cytokines in muscle wasting during cancer. Int. J. Biochem. Cell Biol. 37, 1609-1619
3. Di Marco, S., Cammas, A., Lian, X. J., Kovacs, E. N., Ma, J. F, Hall, D. T., Mazroui, R., Richardson, J., Pelletier, J., and Gallouzi, I. E. (2012) The translation inhibitor pateamine A prevents cachexia-induced muscle wasting in mice. Nat. Commun. 3, 1-12
4. Fearon, K. C., Glass, D. J., Guttridge, D. C. (2012) Cancer cachexia: mediators, signaling, and metabolic pathways. Cell Metab. 16, 153-166
5. Tanaka, Y., Eda, H., Tanaka, T., Udagawa, T., Ishikawa, T., Horii, I., Ishitsuka, H., Kataoka, T., and Taguchi, T. (1990) Experimental cancer cachexia induced by transplantable colon 26 adenocarcinoma in mice. Cancer Res. 50, 2290-2295
6. Yasumoto, K., Mukaida, N., Harada, A., Kuno, K., Akiyama, M., Nakashima, E., Fujioka, N., Mai, M., Kasahara, T., and Fujimoto-Ouchi, K. (1995) Molecular analysis of the cytokine network involved in cachexia in colon 26 adenocarcinoma-bearing mice. Cancer Res. 55, 921-927
7. Aulino, P., Berardi, E., Cardillo, V. M., Rizzuto, E., Perniconi, B., Ramina, C., Padula, F., Spugnini, E. P., Baldi, A., Faiola, F., Adamo, S., Coletti, D. (2010) Molecular, cellular and physiological characterization of the cancer cachexia-inducing C26 colon carcinoma in mouse. BMC Cancer 10, 363-378
8. Bonetto, A., Aydogdu, T., Kunzevitzky, N., Guttridge, D. C., Khuri, S., Koniaris, L. G., and Zimmers, T. A. (2011) STAT3 activation in skeletal muscle links muscle wasting and the acute phase response in cancer cachexia. PLoS ONE 6, e22538
9. Zhou, X., Wang, J. L., Lu, J., Song, Y., Kwak, K. S., Jiao, Q., Rosenfeld, R., Chen, Q., Boone, T., Simonet, W. S., Lacey, D. L., Goldberg, A. L., and Han, H. Q. (2010) Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 142, 531-543
10. Lokireddy, S., Wijesoma, I. W., Bonala, S., Wei, M., Sze, S. K., McFarlane, C., Kambadur, R., and Sharma, M. (2012) Myostatin is a novel tumoral factor that induces cancer cachexia. Biochem. J. 446, 23-36
11. Penna, F., Costamagna, D., Fanzani, A., Bonelli, G., Baccino, F. M., and Costelli, P. (2010) Muscle wasting and impaired myogenesis in tumor bearing mice are prevented by ERK inhibition. PLoS ONE 5, e13604
12. Bonetto, A., Aydogdu, T., Jin, X., Zhang, Z., Zhan, R., Puzis, L., Koniaris, L. G., and Zimmers, T. A. (2012) JAK/STAT3 pathway inhibition blocks skeletal muscle wasting downstream of IL-6 and in experimental cancer cachexia. Am. J. Physiol. Endocrinol. Metab. 303, E410-E421
13. Judge, S. M., Wu, C. L., Beharry, A. W., Roberts, B. M., Ferreira, L. F., Kandarian, S. C., and Judge, A. R. (2014) Genome-wide identification of FoxO-dependent gene networks in skeletal muscle during C26 cancer cachexia. BMC Cancer 14, 997
14. 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
15. Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676
16. Caldenhoven, E., van Dijk, T. B., Solari, R., Armstrong, J., Raaijmakers, J. A., Lammers, J. W., Koenderman, L., and de Groot, R. P. (1996) STAT3β, a splice variant of transcription factor STAT3, is a dominant negative regulator of transcription. J. Biol. Chem. 271, 13221-13227
17. Chung, C. D., Liao, J., Liu, B., Rao, X., Jay, P., Berta, P., and Shuai, K. (1997) Specific inhibition of Stat3 signal transduction by PIAS3. Science 278, 1803-1805
18. Hunter, R. B., Stevenson, E., Koncarevic, A., Mitchell-Felton, H., Essig, D. A., and Kandarian, S. C. (2002) Activation of an alternative NF-κB pathway in skeletal muscle during disuse atrophy. FASEB J. 16, 529-538
19. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, M. J., Arden, K. C., Blenis, J., and Greenberg, M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868
20. Yamaki, T., Wu, C. L., Gustin, M., Lim, J., Jackman, R. W., and Kandarian, S. C. (2012) Rel A/p65 is required for cytokine-induced myotube atrophy. Am. J. Physiol. Cell Physiol. 303, C135-C142
21. Cornwell, E. W., Mirbod, A., Wu, C. L., Kandarian, S. C., and Jackman, R. W. (2014) C26 cancer-induced muscle wasting is IKKβ-dependent and NF-κB-independent. PLoS ONE 9, e87776
22. Zhang, G., Jin, B., and Li, Y. P. (2011) C/EBPβ mediates tumour-induced ubiquitin ligase atrogin1/MAFbx upregulation and muscle wasting. EMBO J. 30, 4323-4335
23. Acharyya, S., Butchbach, M. E., Sahenk, Z., Wang, H., Saji, M., Carathers, M., Ringel, M. D., Skipworth, R. J., Fearon, K. C., Hollingsworth, M. A., Muscarella, P., Burghes, A. H., Rafael-Fortney, J. A., and Guttridge, D. C. (2005) Dystrophin glycoprotein complex dysfunction: a regulatory link between muscular dystrophy and cancer cachexia. Cancer Cell 8, 421-432
24. Schindler, C., Levy, D. E., and Decker, T. (2007) JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282, 20059-20063
25. McFarlane, C., Plummer, E., Thomas, M., Hennebry, A., Ashby, M., Ling, N., Smith, H., Sharma, M., and Kambadur, R. (2006) Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-κB-independent, FoxO1-dependent mechanism. J. Cell Physiol. 209, 501-514
26. Bromberg, J. F., Wrzeszczynska, M. H., Devgan, G., Zhao, Y., Pestell, R. G., Albanese, C., and Darnell, J. E., Jr. (1999) Stat3 as an oncogene. Cell 98, 295-303
27. Li, J., Favata, M., Kelley, J. A., Caulder, E., Thomas, B., Wen, X., Sparks, R. B., Arvanitis, A., Rogers, J. D., Combs, A. P., Vaddi, K., Solomon, K. A., Scherle, P. A., Newton, R., and Fridman, J. S. (2010) INCB16562, a JAK1/2 selective inhibitor, is efficacious against multiple myeloma cells and reverses the protective effects of cytokine and stromal cell support. Neoplasia 12, 28-38
28. Park, J. I., Strock, C. J., Ball, D. W., and Nelkin, B. D. (2003) The Ras/Raf/MEK/extracellular signal-regulated kinase pathway induces autocrine-paracrine growth inhibition via the leukemia inhibitory factor/JAK/STAT pathway. Mol. Cell Biol. 23, 543-554
29. Zimmers, T. A., Davies, M. V., Koniaris, L. G., Haynes, P., Esquela, A. F., Tomkinson, K. N., McPherron, A. C., Wolfman, N. M., and Lee, S. J. (2002) Induction of cachexia in mice by systemically administered myostatin. Science 296, 1486-1488
30. Silva, K. A., Dong, J., Dong, Y., Schor, N., Tweardy, D. J., Zhang, L., and Mitch, W. E. (2015) Inhibition of stat3 activation suppresses caspase-3 and the ubiquitin-proteasome system, leading to preservation of muscle mass in cancer cachexia. J. Biol. Chem. 290, 11177-11187
31. Mori, M., Yamaguchi, K., Honda, S., Nagasaki, K., Ueda, M., Abe, O., and Abe, K. (1991) Cancer cachexia syndrome developed in nude mice bearing melanoma cells producing leukemia-inhibitory factor. Cancer Res. 51, 6656-6659
32. Berg, M., Fraker, D. L., and Alexander, H. R. (1994) Characterization of differentiation factor/leukaemia inhibitory factor effect on lipoprotein lipase activity and mRNA in 3T3-L1 adipocytes. Cytokine 6, 425-432
33. Metcalf, D., Nicola, N. A., and Gearing, D. P. (1990) Effects of injected leukemia inhibitory factor on hematopoietic and other tissues in mice. Blood 76, 50-56
34. Gascan, H., Anegón, I., Praloran, V., Naulet, J., Godard, A., Soulillou, J. P., and Jacques, Y. (1990) Constitutive production of human interleukin for DA cells/leukemia inhibitory factor by human tumor cell lines derived from various tissues. J. Immunol. 144, 2592-2598
35. Duluc, D., Delneste, Y., Tan, F., Moles, M. P., Grimaud, L., Lenoir, J., Preisser, L., Anegon, I., Catala, L., Ifrah, N., Descamps, P., Gamelin, E., Gascan, H., Hebbar, M., and Jeannin, P. (2007) Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood 110, 4319-4330
36. Tomida, M., Yamamoto-Yamaguchi, Y., and Hozumi, M. (1984) Characterization of a factor inducing differentiation of mouse myeloid leukemic cells purified from conditioned medium of mouse Ehrlich ascites tumor cells. FEBS Lett. 178, 291-296
37. Dauer, D. J., Ferraro, B., Song, L., Yu, B., Mora, L., Buettner, R., Enkemann, S., Jove, R., and Haura, E. B. (2005) Stat3 regulates genes common to both wound healing and cancer. Oncogene 24, 3397-3408
38. Fujiki, F., Mukaida, N., Hirose, K., Ishida, H., Harada, A., Ohno, S., Bluethmann, H., Kawakami, M., Akiyama, M., Sone, S., and Matsushima, K. (1997) Prevention of adenocarcinoma colon 26-induced cachexia by interleukin 10 gene transfer. Cancer Res. 57, 94-99
39. Soda, K., Kawakami, M., Kashii, A., and Miyata, M. (1994) Characterization of mice bearing subclones of colon 26 adenocarcinoma disqualifies interleukin-6 as the sole inducer of cachexia. Jpn. J. Cancer Res. 85, 1124-1130
40. Lazarus, D. D., Destree, A. T., Mazzola, L. M., McCormack, T. A., Dick, L. R., Xu, B., Huang, J. Q., Pierce, J. W., Read, M. A., Coggins, M. B., Solomon, V., Goldberg, A. L., Brand, S. J., and Elliott, P. J. (1999) A new model of cancer cachexia: contribution of the ubiquitin-proteasome pathway. Am. J. Physiol. Endocrinol. Metab. 277, E332-E341
41. Baltgalvis, K. A., Berger, F. G., Pena, M. M., Davis, J. M., Muga, S. J., and Carson, J. A. (2008) Interleukin-6 and cachexia in ApcMin/+ mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R393-R401
42. Janssen, S. P., Gayan-Ramirez, G., Van den Bergh, A., Herijgers, P., Maes, K., Verbeken, E., and Decramer, M. (2005) Interleukin-6 causes myocardial failure and skeletal muscle atrophy in rats. Circulation 111, 996-1005
43. Villiger, P. M., Geng, Y., and Lotz, M. (1993) Induction of cytokine expression by leukemia inhibitory factor. J. Clin. Invest. 91, 1575-1581