Autophagy is involved in TGF-β1-induced protective mechanisms and formation of cancer-associated fibroblasts phenotype in tumor microenvironment

Oncotarget

Volumn 7, Issue 4, 2016, Pages 4122-4141

  Liu, Fang Lan ^a   Mo, En Pan ^a   Yang, Liu ^a   Du, Jun ^b   Wang, Hong Sheng ^b   Zhang, Huan ^a   Kurihara, Hiroshi ^a   Xu, Jun ^a   Cai, Shao Hui ^a  

^a JINAN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Autophagy; Cancer associated fibroblasts; Mitochondria; TGF 1; Tumor microenvironment

Indexed keywords

3 METHYLADENINE; AUTOPHAGY PROTEIN 5; GALUNISERTIB; RAPAMYCIN; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; MESSENGER RNA; PROTECTIVE AGENT;

3T3 CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATG5 GENE; AUTOPHAGY; BREAST CANCER; CANCER ASSOCIATED FIBROBLAST; CANCER GROWTH; CELL DAMAGE; CONTROLLED STUDY; FEMALE; FIBROBLAST; GENE SILENCING; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; BREAST NEOPLASMS; CELL PROLIFERATION; CELL TRANSFORMATION; CYTOLOGY; DRUG EFFECTS; DRUG SCREENING; ENZYME IMMUNOASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; NIH 3T3 CELL LINE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RETROSPECTIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED BALB C; NIH 3T3 CELLS; PHENOTYPE; PROTECTIVE AGENTS; REAL-TIME POLYMERASE CHAIN REACTION; RETROSPECTIVE STUDIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84958012934     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6702     Document Type: Article

References (46)

1. Castells M, Thibault B, Delord JP and Couderc B. Implication of tumor microenvironment in chemoresistance: tumor-associated stromal cells protect tumor cells from cell death. International journal of molecular sciences. 2012; 13:9545-9571.
2. Hanahan D and Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
3. Franco OE, Shaw AK, Strand DW and Hayward SW. Cancer associated fibroblasts in cancer pathogenesis. Seminars in cell & developmental biology. 2010; 21:33-39.
4. Li T, Yang Y, Hua X, Wang G, Liu W, Jia C, Tai Y, Zhang Q and Chen G. Hepatocellular carcinoma-associated fibroblasts trigger NK cell dysfunction via PGE2 and IDO. Cancer letters. 2012; 318:154-161.
5. Chen H, Yang WW, Wen QT, Xu L and Chen M. TGFbeta induces fibroblast activation protein expression; fibroblast activation protein expression increases the proliferation, adhesion, and migration of HO-8910PM [corrected]. Experimental and molecular pathology. 2009; 87:189-194.
6. Kakarla S, Song XT and Gottschalk S. Cancer-associated fibroblasts as targets for immunotherapy. Immunotherapy. 2012; 4:1129-1138.
7. Trimis G, Chatzistamou I, Politi K, Kiaris H and Papavassiliou AG. Expression of p21waf1/Cip1 in stromal fibroblasts of primary breast tumors. Human molecular genetics. 2008; 17:3596-3600.
8. Hu M, Peluffo G, Chen H, Gelman R, Schnitt S and Polyak K. Role of COX-2 in epithelial-stromal cell interactions and progression of ductal carcinoma in situ of the breast. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106:3372-3377.
9. Hua X, Yu L, Huang X, Liao Z and Xian Q. Expression and role of fibroblast activation protein-alpha in microinvasive breast carcinoma. Diagnostic pathology. 2011; 6:111.
10. Wakefield LM and Roberts AB. TGF-beta signaling: positive and negative effects on tumorigenesis. Current opinion in genetics & development. 2002; 12:22-29.
11. Weber CE, Kothari AN, Wai PY, Li NY, Driver J, Zapf MA, Franzen CA, Gupta GN, Osipo C, Zlobin A, Syn WK, Zhang J, Kuo PC and Mi Z. Osteopontin mediates an MZF1-TGF-beta1-dependent transformation of mesenchymal stem cells into cancer-associated fibroblasts in breast cancer. Oncogene. 2015; 34:4821-4833.
12. Fuyuhiro Y, Yashiro M, Noda S, Kashiwagi S, Matsuoka J, Doi Y, Kato Y, Hasegawa T, Sawada T and Hirakawa K. Upregulation of cancer-associated myofibroblasts by TGFbeta from scirrhous gastric carcinoma cells. British journal of cancer. 2011; 105:996-1001.
13. Brenmoehl J, Miller SN, Hofmann C, Vogl D, Falk W, Scholmerich J and Rogler G. Transforming growth factor beta 1 induces intestinal myofibroblast differentiation and modulates their migration. World journal of gastroenterology. 2009; 15:1431-1442.
14. Mizushima N, Levine B, Cuervo AM and Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature. 2008; 451:1069-1075.
15. Rosenfeldt MT and Ryan KM. The role of autophagy in tumour development and cancer therapy. Expert reviews in molecular medicine. 2009; 11:e36.
16. Kang R, Zeh HJ, Lotze MT and Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011; 18:571-580.
17. He C and Levine B. The Beclin 1 interactome. Current opinion in cell biology. 2010; 22:140-149.
18. Mathew R, Karantza-Wadsworth V and White E. Role of autophagy in cancer. Nature reviews Cancer. 2007; 7:961-967.
19. Kroemer G and Jaattela M. Lysosomes and autophagy in cell death control. Nature reviews Cancer. 2005; 5:886-897.
20. Honscheid P, Datta K and Muders MH. Autophagy: detection, regulation and its role in cancer and therapy response. International journal of radiation biology. 2014; 90:628-635.
21. Maiuri MC, Zalckvar E, Kimchi A and Kroemer G. Selfeating and self-killing: crosstalk between autophagy and apoptosis. Nature reviews Molecular cell biology. 2007; 8:741-752.
22. Yang W, Han W, Ye S, Liu D, Wu J, Liu H, Li C and Chen H. Fibroblast activation protein-alpha promotes ovarian cancer cell proliferation and invasion via extracellular and intracellular signaling mechanisms. Experimental and molecular pathology. 2013; 95:105-110.
23. Martinez-Outschoorn UE, Whitaker-Menezes D, Lin Z, Flomenberg N, Howell A, Pestell RG, Lisanti MP and Sotgia F. Cytokine production and inflammation drive autophagy in the tumor microenvironment: role of stromal caveolin-1 as a key regulator. Cell cycle. 2011; 10:1784-1793.
24. Sotgia F, Martinez-Outschoorn UE, Howell A, Pestell RG, Pavlides S and Lisanti MP. Caveolin-1 and cancer metabolism in the tumor microenvironment: markers, models, and mechanisms. Annual review of pathology. 2012; 7:423-467.
25. Martinez-Outschoorn UE, Whitaker-Menezes D, Pavlides S, Chiavarina B, Bonuccelli G, Casey T, Tsirigos A, Migneco G, Witkiewicz A, Balliet R, Mercier I, Wang C, Flomenberg N, Howell A, Lin Z, Caro J, et al. The autophagic tumor stroma model of cancer or "batteryoperated tumor growth": A simple solution to the autophagy paradox. Cell cycle. 2010; 9:4297-4306.
26. Ghavami S, Cunnington RH, Gupta S, Yeganeh B, Filomeno KL, Freed DH, Chen S, Klonisch T, Halayko AJ, Ambrose E, Singal R and Dixon IM. Autophagy is a regulator of TGF-beta1-induced fibrogenesis in primary human atrial myofibroblasts. Cell death & disease. 2015; 6:e1696.
27. Xu Y, Yang S, Huang J, Ruan S, Zheng Z and Lin J. Tgfbeta1 induces autophagy and promotes apoptosis in renal tubular epithelial cells. International journal of molecular medicine. 2012; 29:781-790.
28. Gajewska M, Gajkowska B and Motyl T. Apoptosis and autophagy induced by TGF-B1 in bovine mammary epithelial BME-UV1 cells. Journal of physiology and pharmacology: an official journal of the Polish Physiological Society. 2005; 56:143-157.
29. Ding Y, Kim JK, Kim SI, Na HJ, Jun SY, Lee SJ and Choi ME. TGF-{beta}1 protects against mesangial cell apoptosis via induction of autophagy. The Journal of biological chemistry. 2010; 285:37909-37919.
30. Kiyono K, Suzuki HI, Matsuyama H, Morishita Y, Komuro A, Kano MR, Sugimoto K and Miyazono K. Autophagy is activated by TGF-beta and potentiates TGF-beta-mediated growth inhibition in human hepatocellular carcinoma cells. Cancer research. 2009; 69:8844-8852.
31. Duan W, Jin X, Li Q, Tashiro S, Onodera S and Ikejima T. Silibinin induced autophagic and apoptotic cell death in HT1080 cells through a reactive oxygen species pathway. Journal of pharmacological sciences. 2010; 113:48-56.
32. Xing F, Saidou J and Watabe K. Cancer associated fibroblasts (CAFs) in tumor microenvironment. Frontiers in bioscience (Landmark edition). 2010; 15:166-179.
33. Shimoda M, Mellody KT and Orimo A. Carcinoma-associated fibroblasts are a rate-limiting determinant for tumour progression. Seminars in cell & developmental biology. 2010; 21:19-25.
34. Hursting SD, Lashinger LM, Colbert LH, Rogers CJ, Wheatley KW, Nunez NP, Mahabir S, Barrett JC, Forman MR and Perkins SN. Energy balance and carcinogenesis: underlying pathways and targets for intervention. Current cancer drug targets. 2007; 7:484-491.
35. Sanchez CG, Penfornis P, Oskowitz AZ, Boonjindasup AG, Cai DZ, Dhule SS, Rowan BG, Kelekar A, Krause DS and Pochampally RR. Activation of autophagy in mesenchymal stem cells provides tumor stromal support. Carcinogenesis. 2011; 32:964-972.
36. Guido C, Whitaker-Menezes D, Lin Z, Pestell RG, Howell A, Zimmers TA, Casimiro MC, Aquila S, Ando S, Martinez-Outschoorn UE, Sotgia F and Lisanti MP. Mitochondrial fission induces glycolytic reprogramming in cancer-associated myofibroblasts, driving stromal lactate production, and early tumor growth. Oncotarget. 2012; 3:798-810. doi: 10.18632/oncotarget.574.
37. Yang X, Yu DD, Yan F, Jing YY, Han ZP, Sun K, Liang L, Hou J and Wei LX. The role of autophagy induced by tumor microenvironment in different cells and stages of cancer. Cell & bioscience. 2015; 5:14.
38. Xu Y, Xia X and Pan H. Active autophagy in the tumor microenvironment: A novel mechanism for cancer metastasis. Oncology letters. 2013; 5:411-416.
39. Kim SE, Park HJ, Jeong HK, Kim MJ, Kim M, Bae ON and Baek SH. Autophagy sustains the survival of human pancreatic cancer PANC-1 cells under extreme nutrient deprivation conditions. Biochem Biophys Res Commun. 2015; 463:205-210.
40. Sato K, Tsuchihara K, Fujii S, Sugiyama M, Goya T, Atomi Y, Ueno T, Ochiai A and Esumi H. Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer research. 2007; 67:9677-9684.
41. Fu MY, He YJ, Lv X, Liu ZH, Shen Y, Ye GR, Deng YM and Shu JC. Transforming growth factorbeta1 reduces apoptosis via autophagy activation in hepatic stellate cells. Molecular medicine reports. 2014; 10:1282-1288.
42. Gurney MA, Huang C, Ramil JM, Ravindran N, Andres AM, Sin J, Linton PJ and Gottlieb RA. Measuring cardiac autophagic flux in vitro and in vivo. Methods Mol Biol. 2015; 1219:187-197.
43. Shintani T and Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science. 2004; 306:990-995.
44. Capparelli C, Guido C, Whitaker-Menezes D, Bonuccelli G, Balliet R, Pestell TG, Goldberg AF, Pestell RG, Howell A, Sneddon S, Birbe R, Tsirigos A, Martinez-Outschoorn U, Sotgia F and Lisanti MP. Autophagy and senescence in cancer-associated fibroblasts metabolically supports tumor growth and metastasis via glycolysis and ketone production. Cell cycle. 2012; 11:2285-2302.
45. Motyl T, Gajkowska B, Zarzynska J, Gajewska M and Lamparska-Przybysz M. Apoptosis and autophagy in mammary gland remodeling and breast cancer chemotherapy. Journal of physiology and pharmacology: an official journal of the Polish Physiological Society. 2006; 57:17-32.
46. Martinez-Outschoorn UE, Lisanti MP and Sotgia F. Catabolic cancer-associated fibroblasts transfer energy and biomass to anabolic cancer cells, fueling tumor growth. Seminars in cancer biology. 2014; 25:47-60.