1,516
Views
14
CrossRef citations to date
0
Altmetric
Translational Research Papers

Autophagy initiation correlates with the autophagic flux in 3D models of mesothelioma and with patient outcome

, , , &
Pages 1180-1194 | Received 08 Sep 2015, Accepted 30 Mar 2016, Published online: 10 May 2016

References

  • Dalby KN, Tekedereli I, Lopez-Berestein G, Ozpolat B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy 2010; 6:322-9; PMID:20224296; http://dx.doi.org/10.4161/auto.6.3.11625
  • Janku F, McConkey DJ, Hong DS, Kurzrock R. Autophagy as a target for anticancer therapy. Nat Rev Clin Oncol 2011; 8:528-39; PMID:21587219; http://dx.doi.org/10.1038/nrclinonc.2011.71
  • Rubinsztein DC, Codogno P, Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 2012; 11:709-30; PMID:22935804; http://dx.doi.org/10.1038/nrd3802
  • Sui X, Chen R, Wang Z, Huang Z, Kong N, Zhang M, Han W, Lou F, Yang J, Zhang Q, et al. Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell Death Dis 2013; 4:e838; PMID:24113172; http://dx.doi.org/10.1038/cddis.2013.350
  • Choi AM, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med 2013; 368:1845-6; PMID:23656658; http://dx.doi.org/10.1056/NEJMra1205406
  • Rebecca VW, Amaravadi RK. Emerging strategies to effectively target autophagy in cancer. Oncogene 2016; 35:1–11; PMID:25893285; http://dx.doi.org/10.1038/onc.2015.99
  • Nagelkerke A, Bussink J, Geurts-Moespot A, Sweep FC, Span PN. Therapeutic targeting of autophagy in cancer. Part II: pharmacological modulation of treatment-induced autophagy. Semin Cancer Biol 2015; 31:99-105; PMID:24933034; http://dx.doi.org/10.1016/j.semcancer.2014.06.001
  • Rosenfeldt MT, Nixon C, Liu E, Mah LY, Ryan KM. Analysis of macroautophagy by immunohistochemistry. Autophagy 2012; 8:963-9; PMID:22562096; http://dx.doi.org/10.4161/auto.20186
  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 2016; 12:1-222; PMID:26799652; http://dx.doi.org/10.1080/15548627.2015.1100356
  • Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140:313-26; PMID:20144757; http://dx.doi.org/10.1016/j.cell.2010.01.028
  • Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol 2010; 221:117-24; PMID:20225337; http://dx.doi.org/10.1002/path.2694
  • Zhang XJ, Chen S, Huang KX, Le WD. Why should autophagic flux be assessed? Acta Pharmacol Sin 2013; 34:595-9; PMID:23474710; http://dx.doi.org/10.1038/aps.2012.184
  • Ma XH, Piao S, Wang D, McAfee QW, Nathanson KL, Lum JJ, Li LZ, Amaravadi RK. Measurements of tumor cell autophagy predict invasiveness, resistance to chemotherapy, and survival in melanoma. Clin Cancer Res 2011; 17:3478-89; PMID:21325076; http://dx.doi.org/10.1158/1078-0432.CCR-10-2372
  • do Amaral JB, Rezende-Teixeira P, Freitas VM, Machado-Santelli GM. MCF-7 cells as a three-dimensional model for the study of human breast cancer. Tissue Eng Part C Methods 2011; 17:1097-107; PMID:21882900; http://dx.doi.org/10.1089/ten.tec.2011.0260
  • Gomes LR, Vessoni AT, Menck CF. Three-dimensional microenvironment confers enhanced sensitivity to doxorubicin by reducing p53-dependent induction of autophagy. Oncogene 2015; 34:5329–40; PMID: 25619836; http://dx.doi.org/10.1038/onc.2014.461
  • Kim KU, Wilson SM, Abayasiriwardana KS, Collins R, Fjellbirkeland L, Xu Z, Jablons DM, Nishimura SL, Broaddus VC. A novel in vitro model of human mesothelioma for studying tumor biology and apoptotic resistance. Am J Respir Cell Mol Biol 2005; 33:541-8; PMID:16123394; http://dx.doi.org/10.1165/rcmb.2004-0355OC
  • Wilson SM, Barbone D, Yang TM, Jablons DM, Bueno R, Sugarbaker DJ, Nishimura SL, Gordon GJ, Broaddus VC. mTOR mediates survival signals in malignant mesothelioma grown as tumor fragment spheroids. Am J Respir Cell Mol Biol 2008; 39:576-83; PMID:18511708; http://dx.doi.org/10.1165/rcmb.2007-0460OC
  • Bidlingmaier S, He J, Wang Y, An F, Feng J, Barbone D, Gao D, Franc B, Broaddus VC, Liu B. Identification of MCAM/CD146 as the target antigen of a human monoclonal antibody that recognizes both epithelioid and sarcomatoid types of mesothelioma. Cancer Res 2009; 69:1570-7; PMID:19221091; http://dx.doi.org/10.1158/0008-5472.CAN-08-1363
  • Barbone D, Cheung P, Battula S, Busacca S, Gray SG, Longley DB, Bueno R, Sugarbaker DJ, Fennell DA, Broaddus VC. Vorinostat eliminates multicellular resistance of mesothelioma 3D spheroids via restoration of Noxa expression. PLoS One 2012; 7:e52753; PMID:23300762; http://dx.doi.org/10.1371/journal.pone.0052753
  • Lee YJ, Hah YJ, Kang YN, Kang KJ, Hwang JS, Chung WJ, Cho KB, Park KS, Kim ES, Seo HY, et al. The autophagy-related marker LC3 can predict prognosis in human hepatocellular carcinoma. PLoS One 2013; 8:e81540; PMID:24282606; http://dx.doi.org/10.1371/journal.pone.0081540
  • Zhou W, Yue C, Deng J, Hu R, Xu J, Feng L, Lan Q, Zhang W, Ji D, Wu J, et al. Autophagic protein Beclin 1 serves as an independent positive prognostic biomarker for non-small cell lung cancer. PLoS One 2013; 8:e80338; PMID:24260370; http://dx.doi.org/10.1371/journal.pone.0080338
  • Cai M, Hu Z, Liu J, Gao J, Liu C, Liu D, Tan M, Zhang D, Lin B. Beclin 1 expression in ovarian tissues and its effects on ovarian cancer prognosis. Int J Mol Sci 2014; 15:5292-303; PMID:24675697; http://dx.doi.org/10.3390/ijms15045292
  • Choi JH, Cho YS, Ko YH, Hong SU, Park JH, Lee MA. Absence of autophagy-related proteins expression is associated with poor prognosis in patients with colorectal adenocarcinoma. Gastroenterol Res Pract 2014; 2014:179586; PMID:24723943; http://dx.doi.org/10.1155/2014/179586
  • Qiu DM, Wang GL, Chen L, Xu YY, He S, Cao XL, Qin J, Zhou JM, Zhang YX, E Q. The expression of beclin-1, an autophagic gene, in hepatocellular carcinoma associated with clinical pathological and prognostic significance. BMC Cancer 2014; 14:327; PMID:24885292; http://dx.doi.org/10.1186/1471-2407-14-327
  • Winardi D, Tsai HP, Chai CY, Chung CL, Loh JK, Chen YH, Hsieh CL. Correlation of altered expression of the autophagy marker LC3B with poor prognosis in astrocytoma. Biomed Res Int 2014; 2014:723176; PMID:24900981
  • Zhao Y, Chen S, Gou WF, Xiao LJ, Takano Y, Zheng HC. Aberrant Beclin 1 expression is closely linked to carcinogenesis, differentiation, progression, and prognosis of ovarian epithelial carcinoma. Tumour Biol 2014; 35:1955-64; PMID:24132590; http://dx.doi.org/10.1007/s13277-013-1261-6
  • Yang M, Zhao H, Guo L, Zhang Q, Zhao L, Bai S, Zhang M, Xu S, Wang F, Wang X, et al. Autophagy-based survival prognosis in human colorectal carcinoma. Oncotarget 2015; 6:7084-103; PMID:25762626; http://dx.doi.org/10.18632/oncotarget.3054
  • Sakakura K, Takahashi H, Kaira K, Toyoda M, Oyama T, Chikamatsu K. Immunological significance of the accumulation of autophagy components in oral squamous cell carcinoma. Cancer Sci 2015; 106:1-8; PMID:25338734; http://dx.doi.org/10.1111/cas.12559
  • Tang H, Sebti S, Titone R, Zhou Y, Isidoro C, Ross TS, Hibshoosh H, Xiao G, Packer M, Xie Y, et al. Decreased mRNA Expression in Human Breast Cancer is Associated with Estrogen Receptor-Negative Subtypes and Poor Prognosis. EBioMedicine 2015; 2:255-63; http://dx.doi.org/10.1016/j.ebiom.2015.01.008
  • Yang Z, Ghoorun RA, Fan X, Wu P, Bai Y, Li J, Chen H, Wang L, Wang J. High expression of Beclin-1 predicts favorable prognosis for patients with colorectal cancer. Clin Res Hepatol Gastroenterol 2015; 39:98-106; PMID:25130795; http://dx.doi.org/10.1016/j.clinre.2014.06.014
  • Alers S, Loffler AS, Paasch F, Dieterle AM, Keppeler H, Lauber K, Campbell DG, Fehrenbacher B, Schaller M, Wesselborg S, et al. Atg13 and FIP200 act independently of Ulk1 and Ulk2 in autophagy induction. Autophagy 2011; 7:1423-33; PMID:22024743; http://dx.doi.org/10.4161/auto.7.12.18027
  • Alers S, Wesselborg S, Stork B. ATG13: just a companion, or an executor of the autophagic program? Autophagy 2014; 10:944-56; PMID:24879146; http://dx.doi.org/10.4161/auto.28987
  • Kaizuka T, Mizushima N. Atg13 is essential for autophagy and cardiac development in mice. Mol Cell Biol 2015; 36(4):585-95; PMID:26644405
  • Karanasios E, Stapleton E, Manifava M, Kaizuka T, Mizushima N, Walker SA, Ktistakis NT. Dynamic association of the ULK1 complex with omegasomes during autophagy induction. J Cell Sci 2013; 126:5224-38; PMID:24013547; http://dx.doi.org/10.1242/jcs.132415
  • Barbone D, Follo C, Echeverry N, Gerbaudo VH, Klabatsa A, Bueno R, Felley-Bosco E, Broaddus VC. Autophagy Correlates with the Therapeutic Responsiveness of Malignant Pleural Mesothelioma in 3D Models. PLoS One 2015; 10:e0134825; PMID:26284517; http://dx.doi.org/10.1371/journal.pone.0134825
  • Altman DG, Lausen B, Sauerbrei W, Schumacher M. Dangers of using “optimal” cutpoints in the evaluation of prognostic factors. J Natl Cancer Inst 1994; 86:829-35; PMID:8182763; http://dx.doi.org/10.1093/jnci/86.11.829
  • Nicotra G, Mercalli F, Peracchio C, Castino R, Follo C, Valente G, Isidoro C. Autophagy-active beclin-1 correlates with favourable clinical outcome in non-Hodgkin lymphomas. Mod Pathol 2010; 23:937-50; PMID:20473282; http://dx.doi.org/10.1038/modpathol.2010.80
  • Lazova R, Camp RL, Klump V, Siddiqui SF, Amaravadi RK, Pawelek JM. Punctate LC3B expression is a common feature of solid tumors and associated with proliferation, metastasis, and poor outcome. Clin Cancer Res 2012; 18:370-9; PMID:22080440; http://dx.doi.org/10.1158/1078-0432.CCR-11-1282
  • Chen S, Jiang YZ, Huang L, Zhou RJ, Yu KD, Liu Y, Shao ZM. The residual tumor autophagy marker LC3B serves as a prognostic marker in local advanced breast cancer after neoadjuvant chemotherapy. Clin Cancer Res 2013; 19:6853-62; PMID:24141623; http://dx.doi.org/10.1158/1078-0432.CCR-13-1617
  • Sakurai T, Okumura H, Matsumoto M, Uchikado Y, Setoyama T, Omoto I, Owaki T, Maemura K, Ishigami S, Natsugoe S. The expression of LC-3 is related to tumor suppression through angiogenesis in esophageal cancer. Med Oncol 2013; 30:701; PMID:24122254; http://dx.doi.org/10.1007/s12032-013-0701-x
  • Tang JY, Hsi E, Huang YC, Hsu NC, Chen YK, Chu PY, Chai CY. ATG9A overexpression is associated with disease recurrence and poor survival in patients with oral squamous cell carcinoma. Virchows Arch 2013; 463:737-42; PMID:24085552; http://dx.doi.org/10.1007/s00428-013-1482-5
  • Tang JY, Hsi E, Huang YC, Hsu NC, Chu PY, Chai CY. High LC3 expression correlates with poor survival in patients with oral squamous cell carcinoma. Hum Pathol 2013; 44:2558-62; PMID:24055091; http://dx.doi.org/10.1016/j.humpath.2013.06.017
  • Lefort S, Joffre C, Kieffer Y, Givel AM, Bourachot B, Zago G, Bieche I, Dubois T, Meseure D, Vincent-Salomon A, et al. Inhibition of autophagy as a new means of improving chemotherapy efficiency in high-LC3B triple-negative breast cancers. Autophagy 2014; 10:2122-42; PMID:25427136; http://dx.doi.org/10.4161/15548627.2014.981788
  • Liu JL, Chen FF, Lung J, Lo CH, Lee FH, Lu YC, Hung CH. Prognostic significance of p62/SQSTM1 subcellular localization and LC3B in oral squamous cell carcinoma. Br J Cancer 2014; 111:944-54; PMID:24983366; http://dx.doi.org/10.1038/bjc.2014.355
  • Wu DH, Jia CC, Chen J, Lin ZX, Ruan DY, Li X, Lin Q, Min D, Ma XK, Wan XB, et al. Autophagic LC3B overexpression correlates with malignant progression and predicts a poor prognosis in hepatocellular carcinoma. Tumour Biol 2014; 35:12225-33; PMID:25256671; http://dx.doi.org/10.1007/s13277-014-2531-7
  • Yun M, Bai HY, Zhang JX, Rong J, Weng HW, Zheng ZS, Xu Y, Tong ZT, Huang XX, Liao YJ, et al. ULK1: a promising biomarker in predicting poor prognosis and therapeutic response in human nasopharygeal carcinoma. PLoS One 2015; 10:e0117375; PMID:25714809; http://dx.doi.org/10.1371/journal.pone.0117375
  • Gu Y, Li P, Peng F, Zhang M, Zhang Y, Liang H, Zhao W, Qi L, Wang H, Wang C, et al. Autophagy-related prognostic signature for breast cancer. Mol Carcinog 2016; 55:292–9; PMID: 25620657; http://dx.doi.org/10.1002/mc.22278
  • Jao CC, Ragusa MJ, Stanley RE, Hurley JH. A HORMA domain in Atg13 mediates PI 3-kinase recruitment in autophagy. Proc Natl Acad Sci U S A 2013; 110:5486-91; PMID:23509291; http://dx.doi.org/10.1073/pnas.1220306110
  • Cuzick J. Controversies in design and interpretation of adjuvant clinical trials. Cancer Invest 2010; 28 Suppl 1:28-34; PMID:20653405; http://dx.doi.org/10.3109/07357907.2010.501633
  • Hamai A, Codogno P, Mehrpour M. Cancer stem cells and autophagy: Facts and Perspectives. J Cancer Stem Cell Res 2014; 2:e1005; http://dx.doi.org/10.14343/JCSCR.2014.2e1005
  • Cortes-Dericks L, Froment L, Boesch R, Schmid RA, Karoubi G. Cisplatin-resistant cells in malignant pleural mesothelioma cell lines show ALDH(high)CD44(+) phenotype and sphere-forming capacity. BMC Cancer 2014; 14:304; PMID:24884875; http://dx.doi.org/10.1186/1471-2407-14-304
  • Pasdar EA, Smits M, Stapelberg M, Bajzikova M, Stantic M, Goodwin J, Yan B, Stursa J, Kovarova J, Sachaphibulkij K, et al. Characterisation of mesothelioma-initiating cells and their susceptibility to anti-cancer agents. PLoS One 2015; 10:e0119549; PMID:25932953; http://dx.doi.org/10.1371/journal.pone.0119549
  • Eskelinen EL. The dual role of autophagy in cancer. Curr Opin Pharmacol 2011; 11:294-300; PMID:21498118; http://dx.doi.org/10.1016/j.coph.2011.03.009
  • Liu B, Wen X, Cheng Y. Survival or death: disequilibrating the oncogenic and tumor suppressive autophagy in cancer. Cell Death Dis 2013; 4:e892; PMID:24176850; http://dx.doi.org/10.1038/cddis.2013.422
  • Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F, Codogno P, Debnath J, Gewirtz DA, Karantza V, et al. Autophagy in malignant transformation and cancer progression. EMBO J 2015; 34:856-80; PMID:25712477; http://dx.doi.org/10.15252/embj.201490784
  • Denton D, Xu T, Kumar S. Autophagy as a pro-death pathway. Immunol Cell Biol 2015; 93:35-42; PMID:25331550; http://dx.doi.org/10.1038/icb.2014.85
  • White E. The role for autophagy in cancer. J Clin Invest 2015; 125:42-6; PMID:25654549; http://dx.doi.org/10.1172/JCI73941
  • Sharma K, Le N, Alotaibi M, Gewirtz DA. Cytotoxic autophagy in cancer therapy. Int J Mol Sci 2014; 15:10034-51; PMID:24905404; http://dx.doi.org/10.3390/ijms150610034
  • Liu Y, Levine B. Autosis and autophagic cell death: the dark side of autophagy. Cell Death Differ 2015; 22:367-76; PMID:25257169; http://dx.doi.org/10.1038/cdd.2014.143
  • Echeverry N, Ziltener G, Barbone D, Weder W, Stahel RA, Broaddus VC, Felley-Bosco E. Inhibition of autophagy sensitizes malignant pleural mesothelioma cells to dual PI3K/mTOR inhibitors. Cell Death Dis 2015; 6:e1757; PMID:25950487; http://dx.doi.org/10.1038/cddis.2015.124
  • Harasawa R, Mizusawa H, Nozawa K, Nakagawa T, Asada K, Kato I. Detection and tentative identification of dominant mycoplasma species in cell cultures by restriction analysis of the 16S-23S rRNA intergenic spacer regions. Res Microbiol 1993; 144:489-93; PMID:7910696; http://dx.doi.org/10.1016/0923-2508(93)90057-9
  • Barbone D, Yang TM, Morgan JR, Gaudino G, Broaddus VC. Mammalian target of rapamycin contributes to the acquired apoptotic resistance of human mesothelioma multicellular spheroids. J Biol Chem 2008; 283:13021-30; PMID:18339627; http://dx.doi.org/10.1074/jbc.M709698200