Active autophagy in the tumor microenvironment: A novel mechanism for cancer metastasis (Review)
- Authors:
- Yinghua Xu
- Xiaoping Xia
- Hongming Pan
-
Affiliations: Department of Oncology, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310016, P.R. China, Department of Clinical Laboratory, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310016, P.R. China - Published online on: November 7, 2012 https://doi.org/10.3892/ol.2012.1015
- Pages: 411-416
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Abstract
Klionsky DJ: Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 8:931–937. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hippert MM, O’Toole PS and Thorburn A: Autophagy in cancer: good, bad, or both? Cancer Res. 66:9349–9351. 2006. View Article : Google Scholar : PubMed/NCBI | |
Høyer-Hansen M and Jäättelä M: Autophagy: an emerging target for cancer therapy. Autophagy. 4:574–580. 2008. | |
Chen N and Debnath J: Autophagy and tumorigenesis. FEBS Lett. 584:1427–1435. 2010. View Article : Google Scholar | |
Tsuchihara K, Fujii S and Esumi H: Autophagy and cancer: dynamism of the metabolism of tumor cells and tissues. Cancer Lett. 278:130–138. 2009. View Article : Google Scholar : PubMed/NCBI | |
Bao XH, Naomoto Y, Hao HF, Watanabe N, Sakurama K, Noma K, et al: Autophagy: Can it become a potential therapeutic target? Int J Mol Med. 25:493–503. 2010.PubMed/NCBI | |
Kondo Y, Kanzawa T, Sawaya R and Kondo S: The role of autophagy in cancer development and response to therapy. Nat Rev Cancer. 5:726–734. 2005. View Article : Google Scholar : PubMed/NCBI | |
Yang Z and Klionsky DJ: An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol. 335:1–32. 2009.PubMed/NCBI | |
Vousden KH and Ryan KM: p53 and metabolism. Nat Rev Cancer. 9:691–700. 2009. View Article : Google Scholar | |
Kenific CM, Thorburn A and Debnath J: Autophagy and metastasis: another double-edged sword. Curr Opin Cell Biol. 22:241–245. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lum JJ, DeBerardinis RJ and Thompson CB: Autophagy in metazoans: cell survival in the land of plenty. Nat Rev Mol Cell Biol. 6:439–448. 2005. View Article : Google Scholar : PubMed/NCBI | |
Apel A, Zentgraf H, Büchler MW and Herr I: Autophagy-A double-edged sword in oncology. Int J Cancer. 125:991–995. 2009. View Article : Google Scholar : PubMed/NCBI | |
Roy S and Debnath J: Autophagy and tumorigenesis. Semin Immunopathol. 32:383–396. 2010. View Article : Google Scholar | |
Brech A, Ahlquist T, Lothe RA and Stenmark H: Autophagy in tumour suppression and promotion. Mol Oncol. 3:366–375. 2009. View Article : Google Scholar : PubMed/NCBI | |
Wang RC and Levine B: Autophagy in cellular growth control. FEBS Lett. 584:1417–1426. 2010. View Article : Google Scholar : PubMed/NCBI | |
Altman BJ and Rathmell JC: Autophagy: not good OR bad, but good AND bad. Autophagy. 5:569–570. 2009. View Article : Google Scholar : PubMed/NCBI | |
Rosenfeldt MT and Ryan KM: The role of autophagy in tumour development and cancer therapy. Expert Rev Mol Med. 11:e362009. View Article : Google Scholar : PubMed/NCBI | |
Kroemer G, Mariño G and Levine B: Autophagy and the integrated stress response. Mol Cell. 40:280–293. 2010. View Article : Google Scholar | |
Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, et al: Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell. 10:51–64. 2006. View Article : Google Scholar : PubMed/NCBI | |
Bertout JA, Patel SA and Simon MC: The impact of O2 availability on human cancer. Nat Rev Cancer. 8:967–975. 2008. | |
Mazure NM and Pouysségur J: Hypoxia-induced autophagy: cell death or cell survival. Curr Opin Cell Biol. 22:177–180. 2010. View Article : Google Scholar : PubMed/NCBI | |
Mazure NM and Pouysségur J: Atypical BH3-domains of BNIP3 and BNIP3L lead to autophagy in hypoxia. Autophagy. 5:868–869. 2009. View Article : Google Scholar : PubMed/NCBI | |
Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M and Wang J: Essential role for Nix in autophagic maturation of erythroid cells. Nature. 454:232–235. 2008. View Article : Google Scholar : PubMed/NCBI | |
Martinez-Outschoorn UE, Trimmer C, Lin Z, Whitaker-Menezes D, Chiavarina B, Zhou J, et al: Autophagy in cancer associated fibroblasts promotes tumor cell survival: Role of hypoxia, HIF1 induction and NFκB activation in the tumor stromal microenvironment. Cell Cycle. 9:3515–3533. 2010.PubMed/NCBI | |
Srinivas V, Bohensky J, Zahm AM and Shapiro IM: Autophagy in mineralizing tissues: microenvironmental perspectives. Cell Cycle. 8:391–393. 2009. View Article : Google Scholar : PubMed/NCBI | |
Li X and Fan Z: The epidermal growth factor receptor antibody cetuximab induces autophagy in cancer cells by downregulating HIF-1alpha and Bcl-2 and activating the beclin 1/hVps34 complex. Cancer Res. 70:5942–5952. 2010. View Article : Google Scholar : PubMed/NCBI | |
Rouschop KM and Wouters BG: Regulation of autophagy through multiple independent hypoxic signaling pathways. Curr Mol Med. 9:417–424. 2009. View Article : Google Scholar : PubMed/NCBI | |
Pouysségur J, Dayan F and Mazure NM: Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature. 441:437–443. 2006.PubMed/NCBI | |
Sato K, Tsuchihara K, Fujii S, Sugiyama M, Goya T, Atomi Y, et al: Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res. 67:9677–9684. 2007. View Article : Google Scholar : PubMed/NCBI | |
Moreau K, Luo S and Rubinsztein DC: Cytoprotective roles for autophagy. Curr Opin Cell Biol. 22:206–211. 2010. View Article : Google Scholar : PubMed/NCBI | |
Jin S and White E: Role of autophagy in cancer: management of metabolic stress. Autophagy. 3:28–31. 2007. View Article : Google Scholar : PubMed/NCBI | |
Eng CH and Abraham RT: Glutaminolysis yields a metabolic by-product that stimulates autophagy. Autophagy. 6:968–970. 2010. View Article : Google Scholar : PubMed/NCBI | |
Marambio P, Toro B, Sanhueza C, Troncoso R, Parra V, Verdejo H, et al: Glucose deprivation causes oxidative stress and stimulates aggresome formation and autophagy in cultured cardiac myocytes. Biochim Biophys Acta. 1802:509–518. 2010. View Article : Google Scholar : PubMed/NCBI | |
Neufeld TP: TOR-dependent control of autophagy: biting the hand that feeds. Curr Opin Cell Biol. 22:157–168. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lum JJ, DeBerardinis RJ and Thompson CB: Autophagy in metazoans: cell survival in the land of plenty. Nat Rev Mol Cell Biol. 6:439–448. 2005. View Article : Google Scholar : PubMed/NCBI | |
N’Diaye EN, Debnath J and Brown EJ: Ubiquilins accelerate autophagosome maturation and promote cell survival during nutrient starvation. Autophagy. 5:573–575. 2009.PubMed/NCBI | |
Liao XH, Majithia A, Huang X and Kimmel AR: Growth control via TOR kinase signaling, an intracellular sensor of amino acid and energy availability, with crosstalk potential to proline metabolism. Amino Acids. 35:761–770. 2008. View Article : Google Scholar | |
Kumar SH and Rangarajan A: Simian virus 40 small T antigen activates AMPK and triggers autophagy to protect cancer cells from nutrient deprivation. J Virol. 83:8565–8574. 2009. View Article : Google Scholar : PubMed/NCBI | |
Hardie DG: AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol. 8:774–785. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kang R, Tang D, Schapiro NE, Livesey KM, Farkas A, Loughran P, et al: The receptor for advanced glycation end products (RAGE) sustains autophagy and limits apoptosis, promoting pancreatic tumor cell survival. Cell Death Differ. 17:666–676. 2010. View Article : Google Scholar : PubMed/NCBI | |
Miranti CK and Brugge JS: Sensing the environment: a historical perspective on integrin signal transduction. Nat Cell Biol. 4:E83–E90. 2002. View Article : Google Scholar : PubMed/NCBI | |
Gilmore AP: Anoikis. Cell Death Differ. 12(Suppl 2): 1473–1477. 2005. View Article : Google Scholar | |
Debnath J: Detachment-induced autophagy during anoikis and lumen formation in epithelial acini. Autophagy. 4:351–353. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lock R and Debnath J: Extracellular matrix regulation of autophagy. Curr Opin Cell Biol. 20:583–588. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tuloup-Minguez V, Greffard A, Codogno P and Botti J: Regulation of autophagy by extracellular matrix glycoproteins in HeLa cells. Autophagy. 77:27–39. 2011. View Article : Google Scholar | |
Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK and Brugge JS: The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell. 111:29–40. 2002. View Article : Google Scholar : PubMed/NCBI | |
Inagi R: Endoplasmic reticulum stress as a progression factor for kidney injury. Curr Opin Pharmacol. 10:156–165. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kaushik S, Singh R and Cuervo AM: Autophagic pathways and metabolic stress. Diabetes Obes Metab. 12:4–14. 2010. View Article : Google Scholar | |
Verfaillie T, Salazar M, Velasco G and Agostinis P: Linking ER Stress to Autophagy: Potential Implications for Cancer Therapy. Int J Cell Biol. 17:9305–9309. 2010.PubMed/NCBI | |
Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, et al: Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol. 26:9220–9231. 2006. View Article : Google Scholar : PubMed/NCBI | |
Rzymski T, Milani M, Pike L, Buffa F, Mellor HR, Winchester L, et al: Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene. 29:4424–4435. 2010. View Article : Google Scholar : PubMed/NCBI | |
Yang PM, Liu YL, Lin YC, Shun CT, Wu MS and Chen CC: Inhibition of autophagy enhances anticancer effects of atorvastatin in digestive malignancies. Cancer Res. 70:7699–7709. 2010. View Article : Google Scholar : PubMed/NCBI | |
Ishida Y and Nagata K: Autophagy eliminates a specific species of misfolded procollagen and plays a protective role in cell survival against ER stress. Autophagy. 5:1217–1219. 2009. View Article : Google Scholar : PubMed/NCBI | |
Salazar M, Carracedo A, Salanueva IJ, Hernández-Tiedra S, Lorente M, Egia A, et al: Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Invest. 119:1359–1372. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kim KW, Moretti L, Mitchell LR, Jung DK and Lu B: Endoplasmic reticulum stress mediates radiation-induced autophagy by perk-eIF2alpha in caspase-3/7-deficient cells. Oncogene. 29:3241–3251. 2010. View Article : Google Scholar : PubMed/NCBI | |
Qin L, Wang Z, Tao L and Wang Y: ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy. 6:239–247. 2010. View Article : Google Scholar : PubMed/NCBI | |
Fujii S, Mitsunaga S, Yamazaki M, Hasebe T, Ishii G, Kojima M, et al: Autophagy is activated in pancreatic cancer cells and correlates with poor patient outcome. Cancer Sci. 99:1813–1819. 2008.PubMed/NCBI | |
Wan XB, Fan XJ, Chen MY, Xiang J, Huang PY, Guo L, et al: Elevated Beclin 1 expression is correlated with HIF-1alpha in predicting poor prognosis of nasopharyngeal carcinoma. Autophagy. 6:395–404. 2010. View Article : Google Scholar : PubMed/NCBI | |
Giatromanolaki A, Koukourakis MI, Harris AL, Polychronidis A, Gatter KC and Sivridis E: Prognostic relevance of light chain 3 (LC3A) autophagy patterns in colorectal adenocarcinomas. J Clin Pathol. 63:867–872. 2010. View Article : Google Scholar : PubMed/NCBI | |
Bartholomeusz C, Rosen D, Wei C, Kazansky A, Yamasaki F, Takahashi T, et al: PEA-15 induces autophagy in human ovarian cancer cells and is associated with prolonged overall survival. Cancer Res. 68:9302–9310. 2008. View Article : Google Scholar : PubMed/NCBI | |
Miao Y, Zhang Y, Chen Y, Chen L and Wang F: GABARAP is overexpressed in colorectal carcinoma and correlates with shortened patient survival. Hepatogastroenterology. 57:257–261. 2010.PubMed/NCBI | |
Li BX, Li CY, Peng RQ, Wu XJ, Wang HY, Wan DS, et al: The expression of beclin 1 is associated with favorable prognosis in stage IIIB colon cancers. Autophagy. 5:303–306. 2009. View Article : Google Scholar : PubMed/NCBI | |
Nicotra G, Mercalli F, Peracchio C, Castino R, Follo C, Valente G and Isidoro C: Autophagy-active beclin-1 correlates with favourable clinical outcome in non-Hodgkin lymphomas. Mod Pathol. 23:937–950. 2010. View Article : Google Scholar : PubMed/NCBI | |
Miracco C, Cevenini G, Franchi A, Luzi P, Cosci E, Mourmouras V, et al: Beclin 1 and LC3 autophagic gene expression in cutaneous melanocytic lesions. Hum Pathol. 41:503–512. 2010. View Article : Google Scholar : PubMed/NCBI | |
Won KY, Kim GY, Kim YW, Song JY and Lim SJ: Clinicopathologic correlation of beclin-1 and bcl-2 expression in human breast cancer. Hum Pathol. 41:107–112. 2010. View Article : Google Scholar : PubMed/NCBI | |
Duan ZL, Peng ZL and Wang ZH: Expression and involved signal transduction pathway of autophagy gene Beclin 1 in epithelial ovarian cancer. Sichuan Da Xue Xue Bao Yi Xue Ban. 38:239–242. 2007.(In Chinese). | |
Pirtoli L, Cevenini G, Tini P, Vannini M, Oliveri G, Marsili S, et al: The prognostic role of Beclin 1 protein expression in high-grade gliomas. Autophagy. 5:930–936. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ding ZB, Shi YH, Zhou J, Qiu SJ, Xu Y, Dai Z, et al: Association of autophagy defect with a malignant phenotype and poor prognosis of hepatocellular carcinoma. Cancer Res. 68:9167–9175. 2008. View Article : Google Scholar : PubMed/NCBI | |
Huang JJ, Li HR, Huang Y, Jiang WQ, Xu RH, Huang HQ, et al: Beclin 1 expression: a predictor of prognosis in patients with extranodal natural killer T-cell lymphoma, nasal type. Autophagy. 6:777–783. 2010. View Article : Google Scholar : PubMed/NCBI | |
Mizushima N, Yoshimori T and Levine B: Methods in mammalian autophagy research. Cell. 140:313–326. 2010. View Article : Google Scholar : PubMed/NCBI | |
Smith EL and Schuchman EH: Acid sphingomyelinase over-expression enhances the antineoplastic effects of irradiation in vitro and in vivo. Mol Ther. 16:1565–1571. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wei S, Kulp SK and Chen CS: Energy restriction as an antitumor target of thiazolidinediones. J Biol Chem. 285:9780–9791. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zismanov V, Lishner M, Tartakover-Matalon S, Radnay J, Shapiro H and Drucker L: Tetraspanin-induced death of myeloma cell lines is autophagic and involves increased UPR signaling. Br J Cancer. 101:1402–1409. 2009. View Article : Google Scholar : PubMed/NCBI | |
Fels DR, Ye J, Segan AT, Kridel SJ, Spiotto M, Olson M, et al: Preferential cytotoxicity of bortezomib toward hypoxic tumor cells via overactivation of endoplasmic reticulum stress pathways. Cancer Res. 68:9323–9330. 2008. View Article : Google Scholar : PubMed/NCBI | |
Buzzai M, Jones RG, Amaravadi RK, Lum JJ, DeBerardinis RJ, Zhao F, et al: Systemic treatment with the antidiabetic drug metformin selectively impairs p53-deficient tumor cell growth. Cancer Res. 67:6745–6752. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ben Sahra I, Laurent K, Giuliano S, Larbret F, Ponzio G, Gounon P, et al: Targeting cancer cell metabolism: the combination of metformin and 2-deoxyglucose induces p53-dependent apoptosis in prostate cancer cells. Cancer Res. 70:2465–2475. 2010. | |
Kim RH, Coates JM, Bowles TL, McNerney GP, Sutcliffe J, Jung JU, et al: Arginine deiminase as a novel therapy for prostate cancer induces autophagy and caspase-independent apoptosis. Cancer Res. 69:700–708. 2009. View Article : Google Scholar : PubMed/NCBI | |
Mathew R, Karantza-Wadsworth V and White E: Role of autophagy in cancer. Nat Rev Cancer. 7:961–967. 2007. View Article : Google Scholar | |
Zhu K, Dunner K Jr and McConkey DJ: Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells. Oncogene. 29:451–462. 2010. View Article : Google Scholar : PubMed/NCBI | |
Dalby KN, Tekedereli I, Lopez-Berestein G and Ozpolat B: Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy. 6:322–329. 2010. View Article : Google Scholar : PubMed/NCBI | |
White E and DiPaola RS: The double-edged sword of autophagy modulation in cancer. Clin Cancer Res. 15:5308–5316. 2009. View Article : Google Scholar : PubMed/NCBI | |
Scherz-Shouval R, Weidberg H, Gonen C, Wilder S, Elazar Z and Oren M: p53-dependent regulation of autophagy protein LC3 supports cancer cell survival under prolonged starvation. Proc Natl Acad Sci USA. 107:18511–18516. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chouaib S, Kieda C, Benlalam H, Noman MZ, Mami-Chouaib F and Rüegg C: Endothelial cells as key determinants of the tumor microenvironment: interaction with tumor cells, extracellular matrix and immune killer cells. Crit Rev Immunol. 30:529–545. 2010. View Article : Google Scholar : PubMed/NCBI | |
McPhee CK, Logan MA, Freeman MR and Baehrecke EH: Activation of autophagy during cell death requires the engulfment receptor Draper. Nature. 465:1093–1096. 2010. View Article : Google Scholar : PubMed/NCBI |