The SOX9-Aldehyde Dehydrogenase Axis Determines Resistance to Chemotherapy in Non-Small-Cell Lung Cancer

REFERENCES

• Jo A, Denduluri S, Zhang B, Wang Z, Yin L, Yan Z, Kang R, Shi LL, Mok J, Lee MJ, Haydon RC. 2014. The versatile functions of Sox9 in development, stem cells, and human diseases. Genes Dis 1:149–161. https://doi.org/10.1016/j.gendis.2014.09.004.
   PubMedGoogle Scholar
• Furuyama K, Kawaguchi Y, Akiyama H, Horiguchi M, Kodama S, Kuhara T, Hosokawa S, Elbahrawy A, Soeda T, Koizumi M, Masui T, Kawaguchi M, Takaori K, Doi R, Nishi E, Kakinoki R, Deng JM, Behringer RR, Nakamura T, Uemoto S. 2011. Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat Genet 43:34–41. https://doi.org/10.1038/ng.722.
   PubMed Web of Science ®Google Scholar
• Scott CE, Wynn SL, Sesay A, Cruz C, Cheung M, Gomez Gaviro MV, Booth S, Gao B, Cheah KS, Lovell-Badge R, Briscoe J. 2010. SOX9 induces and maintains neural stem cells. Nat Neurosci 13:1181–1189. https://doi.org/10.1038/nn.2646.
   PubMed Web of Science ®Google Scholar
• Rockich BE, Hrycaj SM, Shih HP, Nagy MS, Ferguson MA, Kopp JL, Sander M, Wellik DM, Spence JR. 2013. Sox9 plays multiple roles in the lung epithelium during branching morphogenesis. Proc Natl Acad Sci U S A 110:E4456–E4464. https://doi.org/10.1073/pnas.1311847110.
   PubMed Web of Science ®Google Scholar
• Li L, Zhang H, Min D, Zhang R, Wu J, Qu H, Tang Y. 2015. Sox9 activation is essential for the recovery of lung function after acute lung injury. Cell Physiol Biochem 37:1113–1122. https://doi.org/10.1159/000430236.
   PubMedGoogle Scholar
• Matheu A, Collado M, Wise C, Manterola L, Cekaite L, Tye AJ, Canamero M, Bujanda L, Schedl A, Cheah KSE, Skotheim RI, Lothe RA, de Munain AL, Briscoe J, Serrano M, Lovell-Badge R. 2012. Oncogenicity of the developmental transcription factor Sox9. Cancer Res 72:1301–1315. https://doi.org/10.1158/0008-5472.CAN-11-3660.
   PubMed Web of Science ®Google Scholar
• Ruan H, Hu S, Zhang H, Du G, Li X, Li X, Li X. 2017. Upregulated SOX9 expression indicates worse prognosis in solid tumors: a systematic review and meta-analysis. Oncotarget 8:113163–113173. https://doi.org/10.18632/oncotarget.22635.
   PubMedGoogle Scholar
• Lei B, Zhang YX, Liu T, Li YW, Pang D. 2016. Sox9 upregulation in breast cancer is correlated with poor prognosis and the CD44+/CD24−/low phenotype. Int J Clin Exp Pathol 9:7345–7351.
   Web of Science ®Google Scholar
• Jordan CT, Guzman ML, Noble M. 2006. Cancer stem cells. N Engl J Med 355:1253–1261. https://doi.org/10.1056/NEJMra061808.
   PubMed Web of Science ®Google Scholar
• Larsimont JC, Youssef KK, Sanchez-Danes A, Sukumaran V, Defrance M, Delatte B, Liagre M, Baatsen P, Marine JC, Lippens S, Guerin C, Del Marmol V, Vanderwinden JM, Fuks F, Blanpain C. 2015. Sox9 controls self-renewal of oncogene targeted cells and links tumor initiation and invasion. Cell Stem Cell 17:60–73. https://doi.org/10.1016/j.stem.2015.05.008.
   PubMed Web of Science ®Google Scholar
• Liu C, Liu L, Chen X, Cheng J, Zhang H, Shen J, Shan J, Xu Y, Yang Z, Lai M, Qian C. 2016. Sox9 regulates self-renewal and tumorigenicity by promoting symmetrical cell division of cancer stem cells in hepatocellular carcinoma. Hepatology 64:117–129. https://doi.org/10.1002/hep.28509.
   PubMed Web of Science ®Google Scholar
• Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, Itzkovitz S, Noske A, Zurrer-Hardi U, Bell G, Tam WL, Mani SA, van Oudenaarden A, Weinberg RA. 2012. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 148:1015–1028. https://doi.org/10.1016/j.cell.2012.02.008.
   PubMed Web of Science ®Google Scholar
• Luanpitpong S, Li J, Manke A, Brundage K, Ellis E, McLaughlin SL, Angsutararux P, Chanthra N, Voronkova M, Chen YC, Wang L, Chanvorachote P, Pei M, Issaragrisil S, Rojanasakul Y. 2016. SLUG is required for SOX9 stabilization and functions to promote cancer stem cells and metastasis in human lung carcinoma. Oncogene 35:2824–2833. https://doi.org/10.1038/onc.2015.351.
   PubMed Web of Science ®Google Scholar
• Santos JC, Carrasco-Garcia E, Garcia-Puga M, Aldaz P, Montes M, Fernandez-Reyes M, de Oliveira CC, Lawrie CH, Araúzo-Bravo MJ, Ribeiro ML, Matheu A. 2016. SOX9 elevation acts with canonical WNT signaling to drive gastric cancer progression. Cancer Res 76:6735–6746. https://doi.org/10.1158/0008-5472.CAN-16-1120.
   PubMed Web of Science ®Google Scholar
• Hong X, Liu W, Song R, Shah JJ, Feng X, Tsang CK, Morgan KM, Bunting SF, Inuzuka H, Zheng XFS, Shen Z, Sabaawy HE, Liu L, Pine SR. 2016. SOX9 is targeted for proteasomal degradation by the E3 ligase FBW7 in response to DNA damage. Nucleic Acids Res 44:8855–8869. https://doi.org/10.1093/nar/gkw748.
   PubMed Web of Science ®Google Scholar
• Suryo Rahmanto A, Savov V, Brunner A, Bolin S, Weishaupt H, Malyukova A, Rosén G, Čančer M, Hutter S, Sundström A, Kawauchi D, Jones DT, Spruck C, Taylor MD, Cho Y-J, Pfister SM, Kool M, Korshunov A, Swartling FJ, Sangfelt O. 2016. FBW7 suppression leads to SOX9 stabilization and increased malignancy in medulloblastoma. EMBO J 35:2192–2212. https://doi.org/10.15252/embj.201693889.
   PubMed Web of Science ®Google Scholar
• Higashihara T, Yoshitomi H, Nakata Y, Kagawa S, Takano S, Shimizu H, Kato A, Furukawa K, Ohtsuka M, Miyazaki M. 2017. Sex determining region Y box 9 induces chemoresistance in pancreatic cancer cells by induction of putative cancer stem cell characteristics and its high expression predicts poor prognosis. Pancreas 46:1296–1304. https://doi.org/10.1097/MPA.0000000000000945.
   PubMed Web of Science ®Google Scholar
• Zhou CH, Ye LP, Ye SX, Li Y, Zhang XY, Xu XY, Gong LY. 2012. Clinical significance of SOX9 in human non-small cell lung cancer progression and overall patient survival. J Exp Clin Cancer Res 31:18. https://doi.org/10.1186/1756-9966-31-18.
   PubMed Web of Science ®Google Scholar
• Jiang SS, Fang WT, Hou YH, Huang SF, Yen BL, Chang JL, Li SM, Liu HP, Liu YL, Huang CT, Li YW, Jang TH, Chan SH, Yang SJ, Hsiung CA, Wu CW, Wang LH, Chang IS. 2010. Upregulation of SOX9 in lung adenocarcinoma and its involvement in the regulation of cell growth and tumorigenicity. Clin Cancer Res 16:4363–4373. https://doi.org/10.1158/1078-0432.CCR-10-0138.
   PubMed Web of Science ®Google Scholar
• Barr MP, Gray SG, Hoffmann AC, Hilger RA, Thomale J, O'Flaherty JD, Fennell DA, Richard D, O'Leary JJ, O'Byrne KJ. 2013. Generation and characterisation of cisplatin-resistant non-small cell lung cancer cell lines displaying a stem-like signature. PLoS One 8:e54193. https://doi.org/10.1371/journal.pone.0054193.
   PubMed Web of Science ®Google Scholar
• Dallas NA, Xia L, Fan F, Gray MJ, Gaur P, van Buren G, II, Samuel S, Kim MP, Lim SJ, Ellis LM. 2009. Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition. Cancer Res 69:1951–1957. https://doi.org/10.1158/0008-5472.CAN-08-2023.
   PubMed Web of Science ®Google Scholar
• Levina V, Marrangoni AM, DeMarco R, Gorelik E, Lokshin AE. 2008. Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS One 3:e3077. https://doi.org/10.1371/journal.pone.0003077.
   PubMed Web of Science ®Google Scholar
• Dean M, Fojo T, Bates S. 2005. Tumour stem cells and drug resistance. Nat Rev Cancer 5:275–284. https://doi.org/10.1038/nrc1590.
   PubMed Web of Science ®Google Scholar
• Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. 2003. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17:1253–1270. https://doi.org/10.1101/gad.1061803.
   PubMed Web of Science ®Google Scholar
• Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, De Maria R. 2008. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15:504–514. https://doi.org/10.1038/sj.cdd.4402283.
   PubMed Web of Science ®Google Scholar
• Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R. 2007. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448:318–324. https://doi.org/10.1038/nature05944.
   PubMed Web of Science ®Google Scholar
• Marchitti SA, Brocker C, Stagos D, Vasiliou V. 2008. Non-P450 aldehyde oxidizing enzymes: the aldehyde dehydrogenase superfamily. Expert Opin Drug Metab Toxicol 4:697–720. https://doi.org/10.1517/17425255.4.6.697.
   PubMed Web of Science ®Google Scholar
• Pors K, Moreb JS. 2014. Aldehyde dehydrogenases in cancer: an opportunity for biomarker and drug development? Drug Discov Today 19:1953–1963. https://doi.org/10.1016/j.drudis.2014.09.009.
   PubMed Web of Science ®Google Scholar
• Wei Y, Wu S, Xu W, Liang Y, Li Y, Zhao W, Wu J. 2017. Depleted aldehyde dehydrogenase 1A1 (ALDH1A1) reverses cisplatin resistance of human lung adenocarcinoma cell A549/DDP. Thorac Cancer 8:26–32. https://doi.org/10.1111/1759-7714.12400.
   PubMed Web of Science ®Google Scholar
• Januchowski R, Wojtowicz K, Sterzyska K, Sosiska P, Andrzejewska M, Zawierucha P, Nowicki M, Zabel M. 2016. Inhibition of ALDH1A1 activity decreases expression of drug transporters and reduces chemotherapy resistance in ovarian cancer cell lines. Int J Biochem Cell Biol 78:248–259. https://doi.org/10.1016/j.biocel.2016.07.017.
   PubMed Web of Science ®Google Scholar
• Tomita H, Tanaka K, Tanaka T, Hara A. 2016. Aldehyde dehydrogenase 1A1 in stem cells and cancer. Oncotarget 7:11018–11032. https://doi.org/10.18632/oncotarget.6920.
   PubMed Web of Science ®Google Scholar
• Morgan CA, Parajuli B, Buchman CD, Dria K, Hurley TD. 2015. N,N-Diethylaminobenzaldehyde (DEAB) as a substrate and mechanism-based inhibitor for human ALDH isoenzymes. Chem Biol Interact 234:18–28. https://doi.org/10.1016/j.cbi.2014.12.008.
   PubMed Web of Science ®Google Scholar
• Marcato P, Dean CA, Pan D, Araslanova R, Gillis M, Joshi M, Helyer L, Pan L, Leidal A, Gujar S, Giacomantonio CA, Lee P. 2011. Aldehyde dehydrogenase activity of breast cancer stem cells is primarily due to isoform ALDH1A3 and its expression is predictive of metastasis. Stem Cells 29:32–45. https://doi.org/10.1002/stem.563.
   PubMed Web of Science ®Google Scholar
• Ma F, Ye H, He HH, Gerrin SJ, Chen S, Tanenbaum BA, Cai C, Sowalsky AG, He L, Wang H, Balk SP, Yuan X. 2016. SOX9 drives WNT pathway activation in prostate cancer. J Clin Invest 126:1745–1758. https://doi.org/10.1172/JCI78815.
   PubMed Web of Science ®Google Scholar
• Cronin KA, Lake AJ, Scott S, Sherman RL, Noone AM, Howlader N, Henley SJ, Anderson RN, Firth AU, Ma J, Kohler BA, Jemal A. 2018. Annual report to the nation on the status of cancer, part I: national cancer statistics. Cancer 124:2785–2800. https://doi.org/10.1002/cncr.31551.
   PubMed Web of Science ®Google Scholar
• Zhao W, Zang C, Zhang T, Li J, Liu R, Feng F, Lv Q, Zheng L, Tian J, Sun C. 2018. Clinicopathological characteristics and prognostic value of the cancer stem cell marker ALDH1 in ovarian cancer: a meta-analysis. Onco Targets Ther 11:1821–1831. https://doi.org/10.2147/OTT.S160207.
   PubMed Web of Science ®Google Scholar
• Li J, Zhang B, Yang YF, Jin J, Liu YH. 2018. Aldehyde dehydrogenase 1 as a predictor of the neoadjuvant chemotherapy response in breast cancer: a meta-analysis. Medicine (Baltimore) 97:e12056. https://doi.org/10.1097/MD.0000000000012056.
   Google Scholar
• Ajani JA, Wang X, Song S, Suzuki A, Taketa T, Sudo K, Wadhwa R, Hofstetter WL, Komaki R, Maru DM, Lee JH, Bhutani MS, Weston B, Baladandayuthapani V, Yao Y, Honjo S, Scott AW, Skinner HD, Johnson RL, Berry D. 2014. ALDH-1 expression levels predict response or resistance to preoperative chemoradiation in resectable esophageal cancer patients. Mol Oncol 8:142–149. https://doi.org/10.1016/j.molonc.2013.10.007.
   PubMed Web of Science ®Google Scholar
• Huo W, Du M, Pan X, Zhu X, Li Z. 2015. Prognostic value of ALDH1 expression in lung cancer: a meta-analysis. Int J Clin Exp Med 8:2045–2051.
   PubMedGoogle Scholar
• Wei D, Peng J-J, Gao H, Zhang T, Tan Y, Hu Y-H. 2015. ALDH1 expression and the prognosis of lung cancer: a systematic review and meta-analysis. Heart Lung Circ 24:780–788. https://doi.org/10.1016/j.hlc.2015.03.021.
   PubMed Web of Science ®Google Scholar
• Chen J, Xia Q, Jiang B, Chang W, Yuan W, Ma Z, Liu Z, Shu X. 2015. Prognostic value of cancer stem cell marker ALDH1 expression in colorectal cancer: a systematic review and meta-analysis. PLoS One 10:e0145164. https://doi.org/10.1371/journal.pone.0145164.
   Google Scholar
• Zhou C, Sun B. 2014. The prognostic role of the cancer stem cell marker aldehyde dehydrogenase 1 in head and neck squamous cell carcinomas: a meta-analysis. Oral Oncol 50:1144–1148. https://doi.org/10.1016/j.oraloncology.2014.08.018.
   PubMed Web of Science ®Google Scholar
• Duong HQ, Hwang JS, Kim HJ, Kang HJ, Seong YS, Bae I. 2012. Aldehyde dehydrogenase 1A1 confers intrinsic and acquired resistance to gemcitabine in human pancreatic adenocarcinoma MIA PaCa-2 cells. Int J Oncol 41:855–861. https://doi.org/10.3892/ijo.2012.1516.
   PubMed Web of Science ®Google Scholar
• von Eitzen U, Meier-Tackmann D, Agarwal DP, Goedde HW. 1994. Detoxification of cyclophosphamide by human aldehyde dehydrogenase isozymes. Cancer Lett 76:45–49. https://doi.org/10.1016/0304-3835(94)90132-5.
   PubMed Web of Science ®Google Scholar
• Moreb J, Zucali JR, Zhang Y, Colvin MO, Gross MA. 1992. Role of aldehyde dehydrogenase in the protection of hematopoietic progenitor cells from 4-hydroperoxycyclophosphamide by interleukin 1 beta and tumor necrosis factor. Cancer Res 52:1770–1774.
   PubMed Web of Science ®Google Scholar
• Mizuno T, Suzuki N, Makino H, Furui T, Morii E, Aoki H, Kunisada T, Yano M, Kuji S, Hirashima Y, Arakawa A, Nishio S, Ushijima K, Ito K, Itani Y, Morishige K. 2015. Cancer stem-like cells of ovarian clear cell carcinoma are enriched in the ALDH-high population associated with an accelerated scavenging system in reactive oxygen species. Gynecol Oncol 137:299–305. https://doi.org/10.1016/j.ygyno.2014.12.005.
   PubMed Web of Science ®Google Scholar
• Shi Z, Chiang CI, Labhart P, Zhao Y, Yang J, Mistretta TA, Henning SJ, Maity SN, Mori-Akiyama Y. 2015. Context-specific role of SOX9 in NF-Y mediated gene regulation in colorectal cancer cells. Nucleic Acids Res 43:6257–6269. https://doi.org/10.1093/nar/gkv568.
   PubMed Web of Science ®Google Scholar
• Patel M, Lu L, Zander DS, Sreerama L, Coco D, Moreb JS. 2008. ALDH1A1 and ALDH3A1 expression in lung cancers: correlation with histologic type and potential precursors. Lung Cancer 59:340–349. https://doi.org/10.1016/j.lungcan.2007.08.033.
   PubMed Web of Science ®Google Scholar
• Shao C, Sullivan JP, Girard L, Augustyn A, Yenerall P, Rodriguez-Canales J, Liu H, Behrens C, Shay JW, Wistuba II, Minna JD. 2014. Essential role of aldehyde dehydrogenase 1A3 for the maintenance of non-small cell lung cancer stem cells is associated with the STAT3 pathway. Clin Cancer Res 20:4154–4166. https://doi.org/10.1158/1078-0432.CCR-13-3292.
   PubMed Web of Science ®Google Scholar
• Piao CQ, Liu L, Zhao YL, Balajee AS, Suzuki M, Hei TK. 2005. Immortalization of human small airway epithelial cells by ectopic expression of telomerase. Carcinogenesis 26:725–731. https://doi.org/10.1093/carcin/bgi016.
   PubMed Web of Science ®Google Scholar
• Voronkova MA, Luanpitpong S, Rojanasakul LW, Castranova V, Dinu CZ, Riedel H, Rojanasakul Y. 2017. SOX9 regulates cancer stem-like properties and metastatic potential of single-walled carbon nanotube-exposed cells. Sci Rep 7:11653. https://doi.org/10.1038/s41598-017-12037-8.
   PubMed Web of Science ®Google Scholar