Browse > Article
http://dx.doi.org/10.3839/jabc.2022.050

Association between cancer metabolism and muscle atrophy  

Yeonju Seo (Department of Food Science and Biotechnology, Kyungpook National University)
Ju-Ock Nam (Department of Food Science and Biotechnology, Kyungpook National University)
Publication Information
Journal of Applied Biological Chemistry / v.65, no.4, 2022 , pp. 387-396 More about this Journal
Abstract
Skeletal muscle accounts for about 40-50% of body weight and is an important tissue that performs various functions, such as maintaining posture, supporting soft tissues, maintaining body temperature, and respiration. Cancer, which occurs widely around the world, causes cancer cachexia accompanied by muscular atrophy, which reduces the effectiveness of anticancer drugs and greatly reduces the quality of life and survival rate of cancer patients. Therefore, research to improve cancer cachexia is ongoing. However, there are few studies on the link between cancer and muscle atrophy. Cancer cells exhibit distinct microenvironment and metabolism from tumor cells, including tumor-associated macrophages (TAM), tumor-associated neutrophils (TAN), and insulin resistance due to the Warburg effect. Therefore, we summarize the microenvironment and metabolic characteristics of cancer cells, and the molecular mechanisms of muscle atrophy that can be affected by cytokine and insulin resistance. In addition, this suggests the possibility of improving cancer cachexia of substances affecting TAM, TAN, and Warburg effect. We also summarize the mechanisms identified so far through single agents and the signaling pathways mediated by them that may ameliorate cancer cachexia.
Keywords
Cancer cachexia; Insulin resistance; Muscle atrophy; Tumor-associated macrophages; Tumor-associated neutrophils; Warburg effect;
Citations & Related Records
Times Cited By KSCI : 7  (Citation Analysis)
연도 인용수 순위
1 Fujita J, Tsujinaka T, Yano M, Ebisui C, Saito H, Katsume A, Akamatsu K, Ohsugi Y, Shiozaki H, Monden M (1996) 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. doi: 10.1002/(sici)1097-0215(19961127)68:5<637::Aid-ijc14>3.0.Co;2-z    DOI
2 Abrigo J, Rivera JC, Simon F, Cabrera D, Cabello-Verrugio C (2016) Transforming growth factor type beta (TGF-β) requires reactive oxygen species to induce skeletal muscle atrophy. Cellular Signalling 28: 366-376. doi: 10.1016/j.cellsig.2016.01.010    DOI
3 Abrigo J, Simon F, Cabrera D, Cordova G, Trollet C, Cabello-Verrugio C (2018) Central role of transforming growth factor type beta 1 in skeletal muscle dysfunctions: an update on therapeutic strategies. Curr Protein Pept Sci 19: 1189-1200. doi: 10.2174/1389203718666171117101916    DOI
4 Shen Q, Kuang J-X, Miao C-X, Zhang W-L, Li Y-W, Zhang X-W, Liu X (2022) Alantolactone ameliorates cancer cachexia-associated muscle atrophy mainly by inhibiting the STAT3 signaling pathway. Phytomedicine 95: 153858. doi: 10.1016/j.phymed.2021.153858    DOI
5 Patel HJ, Patel BM (2017) TNF-α and cancer cachexia: Molecular insights and clinical implications. Life Sciences 170: 56-63. doi: 10.1016/j.lfs.2016.11.033    DOI
6 Luo G, Hershko DD, Robb BW, Wray CJ, Hasselgren P-O (2003) IL-1β stimulates IL-6 production in cultured skeletal muscle cells through activation of MAP kinase signaling pathway and NF-κB. Am J Physiol Regul Integr Comp Physiol 284: R1249-R1254. doi: 10.1152/ajpregu.00490.2002    DOI
7 Sadeghi M, Keshavarz-Fathi M, Baracos V, Arends J, Mahmoudi M, Rezaei N (2018) Cancer cachexia: Diagnosis, assessment, and treatment. Crit Rev Oncol Hematol 127: 91-104. doi: 10.1016/j.critrevonc.2018.05.006    DOI
8 Aoyagi T, Terracina KP, Raza A, Matsubara H, Takabe K (2015) Cancer cachexia, mechanism and treatment. World J Gastrointest Oncol 7: 17-29. doi: 10.4251/wjgo.v7.i4.17    DOI
9 Hamburger AW, Parnes H, Gordon GB, Shantz LM, O'Donnell KA, Aisner J (1988) Megestrol acetate-induced differentiation of 3T3-L1 adipocytes in vitro. Semin Oncol 15: 76-78 
10 Hu W, Ru Z, Zhou Y, Xiao W, Sun R, Zhang S, Gao Y, Li X, Zhang X, Yang H (2019) Lung cancer-derived extracellular vesicles induced myotube atrophy and adipocyte lipolysis via the extracellular IL-6-mediated STAT3 pathway. Biochimica et Biophysica Acta (BBA) - Mol Cell Biol Lipids 1864: 1091-1102. doi: 10.1016/j.bbalip.2019.04.006    DOI
11 Soda K, Kawakami M, Kashii A, Miyata M (1995) Manifestations of cancer cachexia induced by colon 26 adenocarcinoma are not fully ascribable to interleukin-6. Int J Cancer 62: 332-336. doi: 10.1002/ijc.2910620317    DOI
12 Kurosaka M, Machida S (2013) Interleukin-6-induced satellite cell proliferation is regulated by induction of the JAK2/STAT3 signalling pathway through cyclin D1 targeting. Cell Prolif 46: 365-373. doi: 10.1111/cpr.12045    DOI
13 Lu S, Li Y, Shen Q, Zhang W, Gu X, Ma M, Li Y, Zhang L, Liu X, Zhang X (2021) Carnosol and its analogues attenuate muscle atrophy and fat lipolysis induced by cancer cachexia. Journal of Cachexia, Sarcopenia and Muscle 12: 779-795. doi: 10.1002/jcsm.12710    DOI
14 Dun Y-l, Zhou X-l, Guan H-s, Yu G-l, Li C-x, Hu T, Zhao X, Cheng X-l, He X-x, Hao J-j (2015) Low molecular weight guluronate prevents TNF-α-induced oxidative damage and mitochondrial dysfunction in C2C12 skeletal muscle cells. Food Funct 6: 3056-3064. doi: 10.1039/C5FO00533G    DOI
15 Li W, Moylan JS, Chambers MA, Smith J, Reid MB (2009) Interleukin-1 stimulates catabolism in C2C12 myotubes. Am J Physiol Cell Physiol 297: C706-C714. doi: 10.1152/ajpcell.00626.2008    DOI
16 Cohen TV, Many GM, Fleming BD, Gnocchi VF, Ghimbovschi S, Mosser DM, Hoffman EP, Partridge TA (2015) Upregulated IL-1β in dysferlin-deficient muscle attenuates regeneration by blunting the response to pro-inflammatory macrophages. Skeletal Muscle 5: 24. doi: 10.1186/s13395-015-0048-4    DOI
17 Miao C, Lv Y, Zhang W, Chai X, Feng L, Fang Y, Liu X, Zhang X (2017) Pyrrolidine Dithiocarbamate (PDTC) Attenuates Cancer Cachexia by Affecting Muscle Atrophy and Fat Lipolysis. Front Pharmacol 8: 10.3389/fphar.2017.00915    DOI
18 Castle S, Nguyen C, Joaquin A, Coyne B, Heuston C, Chan A, Percy L, Ohmen J (1995) Megesterol acetate suspension therapy in the treatment of geriatric anorexia/cachexia in nursing home patients. J Am Geriatr Soc 43: 835-836. doi: 10.1111/j.1532-5415.1995.tb07065.x    DOI
19 Park S (2010) Ghrelin. Endocrinol Metab 25: 258-263. doi: 10.3803/EnM.2010.25.4.258    DOI
20 Dixit VD, Schaffer EM, Pyle RS, Collins GD, Sakthivel SK, Palaniappan R, Lillard JW, Jr., Taub DD (2004) Ghrelin inhibits leptin- and activation-induced proinflammatory cytokine expression by human monocytes and T cells. J Clin Investig 114: 57-66. doi: 10.1172/JCI21134    DOI
21 Shukla SK, Dasgupta A, Mehla K, Gunda V, Vernucci E, Souchek J, Goode G, King R, Mishra A, Rai I, Nagarajan S, Chaika NV, Yu F, Singh PK (2015) Silibinin-mediated metabolic reprogramming attenuates pancreatic cancer-induced cachexia and tumor growth. Oncotarget Vol 6, No 38: 41146-41161. doi: 10.18632/oncotarget.5843    DOI
22 Sun R, Zhang S, Hu W, Lu X, Lou N, Yang Z, Chen S, Zhang X, Yang H (2016) Valproic acid attenuates skeletal muscle wasting by inhibiting C/EBPβ-regulated atrogin1 expression in cancer cachexia. Am J Physiol Cell Physiol 311: C101-C115. doi: 10.1152/ajpcell.00344.2015    DOI
23 Wang H, Lai Y-J, Chan Y-L, Li T-L, Wu C-J (2011) Epigallocatechin-3-gallate effectively attenuates skeletal muscle atrophy caused by cancer cachexia. Cancer Letters 305: 40-49. doi: 10.1016/j.canlet.2011.02.023    DOI
24 Jung YY, Ko J-H, Um J-Y, Sethi G, Ahn KS (2021) A Novel Role of Bergamottin in Attenuating Cancer Associated Cachexia by Diverse Molecular Mechanisms. Cancers 13. doi: 10.3390/cancers13061347    DOI
25 Wang X, Hu Z, Hu J, Du J, Mitch WE (2006) Insulin Resistance Accelerates Muscle Protein Degradation: Activation of the Ubiquitin-Proteasome Pathway by Defects in Muscle Cell Signaling. Endocrinology 147: 4160-4168. doi: 10.1210/en.2006-0251    DOI
26 Stewart GD, Skipworth RJ, Fearon KC (2006) Cancer cachexia and fatigue. Clin Med (Lond) 6: 140-143. doi: 10.7861/clinmedicine.6-2-140    DOI
27 Petruzzelli M, Wagner EF (2016) Mechanisms of metabolic dysfunction in cancer-associated cachexia. Genes Dev 30: 489-501. doi: 10.1101/gad.276733.115    DOI
28 Vuorinen-Markkola H, Koivisto VA, Yki-Jarvinen H (1992) Mechanisms of Hyperglycemia-Induced Insulin Resistance in Whole Body and Skeletal Muscle of Type I Diabetic Patients. Diabetes 41: 571-580. doi: 10.2337/diab.41.5.571    DOI
29 Coleman ME, DeMayo F, Yin KC, Lee HM, Geske R, Montgomery C, Schwartz RJ (1995) Myogenic Vector Expression of Insulin-like Growth Factor I Stimulates Muscle Cell Differentiation and Myofiber Hypertrophy in Transgenic Mice. J Biol Chem 270: 12109-12116. doi: 10.1074/jbc.270.20.12109    DOI
30 Behring JB, van der Post S, Mooradian AD, Egan MJ, Zimmerman MI, Clements JL, Bowman GR, Held JM (2020) Spatial and temporal alterations in protein structure by EGF regulate cryptic cysteine oxidation. Science Signaling 13: eaay7315. doi: 10.1126/scisignal.aay7315    DOI
31 Kvandova M, Dovinova I (2017) Functioning of the PPAR Gamma and its Effect on Cardiovascular and Metabolic Diseases. Metabolic Syndrome: 1-41 
32 Huot JR, Marino JS, Turner MJ, Arthur ST (2020) Notch Inhibition via GSI Treatment Elevates Protein Synthesis in C2C12 Myotubes. Biology 9. doi: 10.3390/biology9060115    DOI
33 Deng B, Wehling-Henricks M, Villalta SA, Wang Y, Tidball JG (2012) IL-10 Triggers Changes in Macrophage Phenotype That Promote Muscle Growth and Regeneration. J Immunol 189: 3669. doi: 10.4049/jimmunol.1103180    DOI
34 Li H, Mittal A, Makonchuk DY, Bhatnagar S, Kumar A (2009) Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum Mol Genet 18: 2584-2598. doi: 10.1093/hmg/ddp191    DOI
35 Arsic N, Zacchigna S, Zentilin L, Ramirez-Correa G, Pattarini L, Salvi A, Sinagra G, Giacca M (2004) Vascular endothelial growth factor stimulates skeletal muscle regeneration in Vivo. Mol Ther 10: 844-854. doi: 10.1016/j.ymthe.2004.08.007    DOI
36 Karvinen H, Pasanen E, Rissanen TT, Korpisalo P, Vahakangas E, Jazwa A, Giacca M, Yla-Herttuala S (2011) Long-term VEGF-A expression promotes aberrant angiogenesis and fibrosis in skeletal muscle. Gene Ther 18: 1166-1172. doi: 10.1038/gt.2011.66    DOI
37 Callaway CS, Delitto AE, D'Lugos AC, Patel R, Nosacka RL, Delitto D, Deyhle MR, Trevino JG, Judge SM, Judge AR (2019) IL-8 Released from Human Pancreatic Cancer and Tumor-Associated Stromal Cells Signals through a CXCR2-ERK1/2 Axis to Induce Muscle Atrophy. Cancers 11. doi: 10.3390/cancers11121863    DOI
38 Santiloni Cury S, de Moraes D, Paccielli Freire P, de Oliveira G, Venancio Pereira Marques D, Javier Fernandez G, Dal-Pai-Silva M, Nishida Hasimoto E, Pintor dos Reis P, Regina Rogatto S, Francisco Carvalho R (2019) Tumor Transcriptome Reveals High Expression of IL-8 in Non-Small Cell Lung Cancer Patients with Low Pectoralis Muscle Area and Reduced Survival. Cancers 11. doi: 10.3390/cancers11091251    DOI
39 Cheng H, Huang H, Guo Z, Chang Y, Li Z (2021) Role of prostaglandin E2 in tissue repair and regeneration. Theranostics 11: 8836-8854. doi: 10.7150/thno.63396    DOI
40 Chun J, Li R-J, Cheng M-S, Kim YS (2015) Alantolactone selectively suppresses STAT3 activation and exhibits potent anticancer activity in MDA-MB-231 cells. Cancer Lett 357: 393-403. doi: 10.1016/j.canlet.2014.11.049    DOI
41 Zheng H, Yang L, Kang Y, Chen M, Lin S, Xiang Y, Li C, Dai X, Huang X, Liang G, Zhao C (2019) Alantolactone sensitizes human pancreatic cancer cells to EGFR inhibitors through the inhibition of STAT3 signaling. Mol Carcinog 58: 565-576. doi: 10.1002/mc.22951    DOI
42 Ahmad B, Gamallat Y, Su P, Husain A, Rehman AU, Zaky MY, Bakheet AMH, Tahir N, Xin Y, Liang W (2021) Alantolactone induces apoptosis in THP-1 cells through STAT3, survivin inhibition, and intrinsic apoptosis pathway. Chem Biol Drug Des 97: 266-272. doi: 10.1111/cbdd.13778    DOI
43 Chen L, Yang Q, Zhang H, Wan L, Xin B, Cao Y, Zhang J, Guo C (2020) Cryptotanshinone prevents muscle wasting in CT26-induced cancer cachexia through inhibiting STAT3 signaling pathway. J Ethnopharmacol 260: 113066. doi: 10.1016/j.jep.2020.113066    DOI
44 Lu S, Zhang Y, Li H, Zhang J, Ci Y, Han M (2020) Ginsenoside Rb1 can ameliorate the key inflammatory cytokines TNF-α and IL-6 in a cancer cachexia mouse model. BMC Complementary Medicine and Therapies 20: 11. doi: 10.1186/s12906-019-2797-9   DOI
45 Argiles JM, Campos N, Lopez-Pedrosa JM, Rueda R, Rodriguez-Manas L (2016) Skeletal muscle regulates metabolism via interorgan crosstalk: roles in health and disease. J Am Med Dir Assoc 17: 789-796    DOI
46 Schutz Y (2011) Protein Turnover, Ureagenesis and Gluconeogenesis. Int J Vitam Nutr Res 81: 101-107. doi: 10.1024/0300-9831/a000064    DOI
47 Conte E, Bresciani E, Rizzi L, Cappellari O, De Luca A, Torsello A, Liantonio A (2020) Cisplatin-Induced Skeletal Muscle Dysfunction: Mechanisms and Counteracting Therapeutic Strategies. Int J Mol Sci 21: 10.3390/ijms21041242    DOI
48 Pallafacchina G, Calabria E, Serrano AL, Kalhovde JM, Schiaffino S (2002) A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc Natl Acad Sci 99: 9213-9218. doi: 10.1073/pnas.142166599    DOI
49 Yu M, Wang H, Xu Y, Yu D, Li D, Liu X, Du W (2015) Insulin-like growth factor-1 (IGF-1) promotes myoblast proliferation and skeletal muscle growth of embryonic chickens via the PI3K/Akt signalling pathway. Cell Biol Int 39: 910-922. doi: 10.1002/cbin.10466    DOI
50 Fruman D, Limon J (2012) Akt and mTOR in B Cell Activation and Differentiation. Front Immunol 3: 10.3389/fimmu.2012.00228    DOI
51 Shu L, Zhang X, Houghton PJ (2002) Myogenic Differentiation Is Dependent on Both the Kinase Function and the N-terminal Sequence of Mammalian Target of Rapamycin. J Biol Chem 277: 16726-16732. doi: 10.1074/jbc.M112285200    DOI
52 Busby S, Ebright RH (1999) Transcription activation by catabolite activator protein (CAP). J Mol Biol 293: 199-213. doi: 10.1006/jmbi.1999.3161    DOI
53 Feldman ME, Apsel B, Uotila A, Loewith R, Knight ZA, Ruggero D, Shokat KM (2009) Active-Site Inhibitors of mTOR Target RapamycinResistant Outputs of mTORC1 and mTORC2. PLOS Biology 7: e1000038. doi: 10.1371/journal.pbio.1000038    DOI
54 Lai Y-C, Liu Y, Jacobs R, Rider Mark H (2012) A novel PKB/Akt inhibitor, MK-2206, effectively inhibits insulin-stimulated glucose metabolism and protein synthesis in isolated rat skeletal muscle. Biochem J 447: 137-147. doi: 10.1042/BJ20120772    DOI
55 Bauer DE, Hatzivassiliou G, Zhao F, Andreadis C, Thompson CB (2005) ATP citrate lyase is an important component of cell growth and transformation. Oncogene 24: 6314-6322. doi: 10.1038/sj.onc.1208773    DOI
56 Kwak A-W, Lee M-J, Lee M-H, Yoon G, Cho S-S, Chae J-I, Shim J-H (2021) The 3-deoxysappanchalcone induces ROS-mediated apoptosis and cell cycle arrest via JNK/p38 MAPKs signaling pathway in human esophageal cancer cells. Phytomedicine 86: 153564. doi: 10.1016/j.phymed.2021.153564    DOI
57 Kayagaki N, Yamaguchi N, Nakayama M, Takeda K, Akiba H, Tsutsui H, Okamura H, Nakanishi K, Okumura K, Yagita H (1999) Expression and function of TNF-related apoptosis-inducing ligand on murine activated NK cells. J Immunol 163: 1906-1913    DOI
58 Szulc-Kielbik I, Klink M (2022) Polymorphonuclear Neutrophils and Tumors: Friend or Foe? Exp Suppl 113: 141-167. doi: 10.1007/978-3-7091-1300-4_7    DOI
59 Chetram MA, Bethea DA, Odero-Marah VA, Don-Salu-Hewage AS, Jones KJ, Hinton CV (2013) ROS-mediated activation of AKT induces apoptosis via pVHL in prostate cancer cells. Mol Cell Biochem 376: 63-71. doi: 10.1007/s11010-012-1549-7    DOI
60 Tazzyman S, Lewis CE, Murdoch C (2009) Neutrophils: key mediators of tumour angiogenesis. Int J Exp Pathol 90: 222-231. doi: 10.1111/j.1365-2613.2009.00641.x    DOI
61 McCourt M, Wang JH, Sookhai S, Redmond HP (1999) Proinflammatory Mediators Stimulate Neutrophil-Directed Angiogenesis. Arch Surg 134: 1325-1331. doi: 10.1001/archsurg.134.12.1325    DOI
62 Huang S, Van Arsdall M, Tedjarati S, McCarty M, Wu W, Langley R, Fidler IJ (2002) Contributions of Stromal Metalloproteinase-9 to Angiogenesis and Growth of Human Ovarian Carcinoma in Mice. JNCI: J Natl Cancer Inst 94: 1134-1142. doi: 10.1093/jnci/94.15.1134    DOI
63 Coussens LM, Tinkle CL, Hanahan D, Werb Z (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103: 481-490    DOI
64 Yuan L, Han J, Meng Q, Xi Q, Zhuang Q, Jiang Y, Han Y, Zhang B, Fang J, Wu G (2015) Muscle-specific E3 ubiquitin ligases are involved in muscle atrophy of cancer cachexia: An in vitro and in vivo study. Oncol Rep 33: 2261-2268. doi: 10.3892/or.2015.3845    DOI
65 Guigni BA, Callahan DM, Tourville TW, Miller MS, Fiske B, Voigt T, Korwin-Mihavics B, Anathy V, Dittus K, Toth MJ (2018) Skeletal muscle atrophy and dysfunction in breast cancer patients: role for chemotherapy-derived oxidant stress. Am J Physio-Cell Physiol 315: C744-C756. doi: 10.1152/ajpcell.00002.2018    DOI
66 Hiensch AE, Bolam KA, Mijwel S, Jeneson JAL, Huitema ADR, Kranenburg O, van der Wall E, Rundqvist H, Wengstrom Y, May AM (2020) Doxorubicin-induced skeletal muscle atrophy: Elucidating the underlying molecular pathways. Acta Physiol (Oxf) 229: e13400. doi: 10.1111/apha.13400    DOI
67 Costamagna D, Duelen R, Penna F, Neumann D, Costelli P, Sampaolesi M (2020) Interleukin-4 administration improves muscle function, adult myogenesis, and lifespan of colon carcinoma-bearing mice. J Cachexia Sarcopenia Muscle 11: 783-801. doi: 10.1002/jcsm.12539    DOI
68 Fernandez GJ, Ferreira JH, Vechetti Jr IJ, De Moraes LN, Cury SS, Freire PP, Gutierrez J, Ferretti R, Dal-Pai-Silva M, Rogatto SR (2020) MicroRNA-mRNA co-sequencing identifies transcriptional and post-transcriptional regulatory networks underlying muscle wasting in cancer cachexia. Front Genet 11: 541. doi: 10.3389/fgene.2020.00541    DOI
69 Zhang W, Sun W, Gu X, Miao C, Feng L, Shen Q, Liu X, Zhang X (2022) GDF-15 in tumor-derived exosomes promotes muscle atrophy via Bcl-2/caspase-3 pathway. Cell Death Discovery 8: 162. doi: 10.1038/s41420-022-00972-z    DOI
70 Wang F, Liu H, Hu L, Liu Y, Duan Y, Cui R, Tian W (2018) The Warburg effect in human pancreatic cancer cells triggers cachexia in athymic mice carrying the cancer cells. BMC Cancer 18: 360. doi: 10.1186/s12885-018-4271-3    DOI
71 Erreni M, Mantovani A, Allavena P (2011) Tumor-associated Macrophages (TAM) and Inflammation in Colorectal Cancer. Cancer Microenviron 4: 141-154. doi: 10.1007/s12307-010-0052-5    DOI
72 Paradies G, Paradies V, Ruggiero FM, Petrosillo G (2019) Role of Cardiolipin in Mitochondrial Function and Dynamics in Health and Disease: Molecular and Pharmacological Aspects. Cells 8. doi: 10.3390/cells8070728    DOI
73 Das S, Morvan F, Morozzi G, Jourde B, Minetti GC, Kahle P, Rivet H, Brebbia P, Toussaint G, Glass DJ, Fornaro M (2017) ATP Citrate Lyase Regulates Myofiber Differentiation and Increases Regeneration by Altering Histone Acetylation. Cell Reports 21: 3003-3011. doi: 10.1016/j.celrep.2017.11.038    DOI
74 Chen Y, Song Y, Du W, Gong L, Chang H, Zou Z (2019) Tumor-associated macrophages: an accomplice in solid tumor progression. J Biomed Sci 26: 78. doi: 10.1186/s12929-019-0568-z    DOI
75 Ruffell B, Coussens Lisa M (2015) Macrophages and Therapeutic Resistance in Cancer. Cancer Cell 27: 462-472. doi: 10.1016/j.ccell.2015.02.015    DOI
76 Lin L, Chen Y-S, Yao Y-D, Chen J-Q, Chen J-N, Huang S-Y, Zeng Y-J, Yao H-R, Zeng S-H, Fu Y-S, Song E-W (2015) CCL18 from tumor-associated macrophages promotes angiogenesis in breast cancer. Oncotarget Vol 6, No 33: 34758-34773. doi: 10.18632/oncotarget.5325    DOI
77 Steitz AM, Steffes A, Finkernagel F, Unger A, Sommerfeld L, Jansen JM, Wagner U, Graumann J, Muller R, Reinartz S (2020) Tumor-associated macrophages promote ovarian cancer cell migration by secreting transforming growth factor beta induced (TGFBI) and tenascin C. Cell Death Dis 11: 249. doi: 10.1038/s41419-020-2438-8    DOI
78 Li Y, Foster W, Deasy BM, Chan Y, Prisk V, Tang Y, Cummins J, Huard J (2004) Transforming Growth Factor-β1 Induces the Differentiation of Myogenic Cells into Fibrotic Cells in Injured Skeletal Muscle: A Key Event in Muscle Fibrogenesis. Am J Pathol 164: 1007-1019. doi: 10.1016/S0002-9440(10)63188-4    DOI
79 Zugmaier G, Paik S, Wilding G, Knabbe C, Bano M, Lupu R, Deschauer B, Simpson S, Dickson RB, Lippman M (1991) Transforming growth factor beta 1 induces cachexia and systemic fibrosis without an antitumor effect in nude mice. Cancer Res 51: 3590-3594 
80 Allen RE, Boxhorn LK (1987) Inhibition of skeletal muscle satellite cell differentiation by transforming growth factor-beta. J Cell Physiol 133: 567-572. doi: 10.1002/jcp.1041330319    DOI
81 Abrigo J, Campos F, Simon F, Riedel C, Cabrera D, Vilos C, Cabello-Verrugio C (2018) TGF-β requires the activation of canonical and non-canonical signalling pathways to induce skeletal muscle atrophy. Biol Chem 399: 253-264. doi: doi: 10.1515/hsz-2017-0217    DOI
82 Janssen SPM, Gayan-Ramirez G, Van Den Bergh A, Herijgers P, Maes K, Verbeken E, Decramer M (2005) Interleukin-6 Causes Myocardial Failure and Skeletal Muscle Atrophy in Rats. Circulation 111: 996-1005. doi: 10.1161/01.CIR.0000156469.96135.0D    DOI
83 Masucci MT, Minopoli M, Carriero MV (2019) Tumor Associated Neutrophils. Their Role in Tumorigenesis, Metastasis, Prognosis and Therapy. Front Oncol 9: 10.3389/fonc.2019.01146    DOI
84 Zeng X-Y, Xie H, Yuan J, Jiang X-Y, Yong J-H, Zeng D, Dou Y-Y, Xiao S-S (2019) M2-like tumor-associated macrophages-secreted EGF promotes epithelial ovarian cancer metastasis via activating EGFR-ERK signaling and suppressing lncRNA LIMT expression. Cancer Biol Ther 20: 956-966. doi: 10.1080/15384047.2018.1564567    DOI
85 Liu L, Wang X, Li X, Wu X, Tang M, Wang X (2018) Upregulation of IGF1 by tumor-associated macrophages promotes the proliferation and migration of epithelial ovarian cancer cells. Oncol Rep 39: 818-826. doi: 10.3892/or.2017.6148    DOI
86 Chen Y, Zhang S, Wang Q, Zhang X (2017) Tumor-recruited M2 macrophages promote gastric and breast cancer metastasis via M2 macrophage-secreted CHI3L1 protein. JHematol Oncol 10: 36. doi: 10.1186/s13045-017-0408-0    DOI
87 Hajizadeh F, Aghebati Maleki L, Alexander M, Mikhailova MV, Masjedi A, Ahmadpour M, Hashemi V, Jadidi-Niaragh F (2021) Tumor-associated neutrophils as new players in immunosuppressive process of the tumor microenvironment in breast cancer. Life Sci 264: 118699. doi: 10.1016/j.lfs.2020.118699    DOI
88 Koga Y, Matsuzaki A, Suminoe A, Hattori H, Hara T (2004) Neutrophil-Derived TNF-Related Apoptosis-Inducing Ligand (TRAIL): A Novel Mechanism of Antitumor Effect by Neutrophils. Cancer Res 64: 1037-1043. doi: 10.1158/0008-5472.CAN-03-1808    DOI
89 Ludwig AT, Moore JM, Luo Y, Chen X, Saltsgaver NA, O'Donnell MA, Griffith TS (2004) Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand: A Novel Mechanism for Bacillus Calmette-Guerin-Induced Antitumor Activity. Cancer Res 64: 3386-3390. doi: 10.1158/0008-5472.Can-04-0374    DOI