Mitochondrial SOD2 regulates epithelial–mesenchymal transition and cell populations defined by differential CD44 expression (original) (raw)

• Nieto MA . The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 2011; 27: 347–376.
  Article CAS Google Scholar
• Kalluri R, Weinberg RA . The basics of epithelial-mesenchymal transition. J Clin Invest 2009; 119: 1420–1428.
  Article CAS Google Scholar
• Thiery JP . Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002; 2: 442–454.
  Article CAS Google Scholar
• De Craene B, Berx G . Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013; 13: 97–110.
  Article CAS Google Scholar
• Giannoni E, Parri M, Chiarugi P . EMT and oxidative stress: a bidirectional interplay affecting tumor malignancy. Antioxid Redox Signal 2012; 16: 1248–1263.
  Article CAS Google Scholar
• Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER et al. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 1997; 275: 1649–1652.
  Article CAS Google Scholar
• Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008; 14: 79–89.
  Article CAS Google Scholar
• Zoller M . CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer 2011; 11: 254–267.
  Article Google Scholar
• Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF . Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983–3988.
  Article CAS Google Scholar
• Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007; 104: 973–978.
  Article CAS Google Scholar
• Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704–715.
  Article CAS Google Scholar
• Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A . Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008; 3: e2888.
  Article Google Scholar
• Sena LA, Chandel NS . Physiological roles of mitochondrial reactive oxygen species. Mol Cell 2012; 48: 158–167.
  Article CAS Google Scholar
• Thannickal VJ, Fanburg BL . Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 2000; 279: L1005–L1028.
  Article CAS Google Scholar
• Lambert AJ, Brand MD . Reactive oxygen species production by mitochondria. Methods Mol Biol 2009; 554: 165–181.
  Article CAS Google Scholar
• Radisky DC, Levy DD, Littlepage LE, Liu H, Nelson CM, Fata JE et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 2005; 436: 123–127.
  Article CAS Google Scholar
• Zhou G, Dada LA, Wu M, Kelly A, Trejo H, Zhou Q et al. Hypoxia-induced alveolar epithelial-mesenchymal transition requires mitochondrial ROS and hypoxia-inducible factor 1. Am J Physiol Lung Cell Mol Physiol 2009; 297: L1120–L1130.
  Article CAS Google Scholar
• Kagawa S, Natsuizaka M, Whelan KA, Facompre N, Naganuma S, Ohashi S et al. Cellular senescence checkpoint function determines differential Notch1-dependent oncogenic and tumor-suppressor activities. Oncogene 2014, e-pub ahead of print 16 June 2014; doi:10.1038/onc.2014.169.
  Article Google Scholar
• Yoon YS, Lee JH, Hwang SC, Choi KS, Yoon G . TGF beta1 induces prolonged mitochondrial ROS generation through decreased complex IV activity with senescent arrest in Mv1Lu cells. Oncogene 2005; 24: 1895–1903.
  Article CAS Google Scholar
• Ohashi S, Natsuizaka M, Wong GS, Michaylira CZ, Grugan KD, Stairs DB et al. Epidermal growth factor receptor and mutant p53 expand an esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors. Cancer Res 2010; 70: 4174–4184.
  Article CAS Google Scholar
• Trachootham D, Lu W, Ogasawara MA, Nilsa RD, Huang P . Redox regulation of cell survival. Antioxid Redox Signal 2008; 10: 1343–1374.
  Article CAS Google Scholar
• Zelko IN, Mariani TJ, Folz RJ . Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 2002; 33: 337–349.
  Article CAS Google Scholar
• Dhar SK St, Clair DK . Manganese superoxide dismutase regulation and cancer. Free Radic Biol Med 2012; 52: 2209–2222.
  Article CAS Google Scholar
• Connor KM, Hempel N, Nelson KK, Dabiri G, Gamarra A, Belarmino J et al. Manganese superoxide dismutase enhances the invasive and migratory activity of tumor cells. Cancer Res 2007; 67: 10260–10267.
  Article CAS Google Scholar
• Huber MA, Azoitei N, Baumann B, Grunert S, Sommer A, Pehamberger H et al. NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest 2004; 114: 569–581.
  Article CAS Google Scholar
• Thiery JP, Acloque H, Huang RY, Nieto MA . Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871–890.
  Article CAS Google Scholar
• Lamouille S, Xu J, Derynck R . Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 2014; 15: 178–196.
  Article CAS Google Scholar
• Chaudhuri L, Nicholson AM, Kalen AL, Goswami PC . Preferential selection of MnSOD transcripts in proliferating normal and cancer cells. Oncogene 2012; 31: 1207–1216.
  Article CAS Google Scholar
• Xu Y, Kiningham KK, Devalaraja MN, Yeh CC, Majima H, Kasarskis EJ et al. An intronic NF-kappaB element is essential for induction of the human manganese superoxide dismutase gene by tumor necrosis factor-alpha and interleukin-1beta. DNA Cell Biol 1999; 18: 709–722.
  Article CAS Google Scholar
• Kim HP, Roe JH, Chock PB, Yim MB . Transcriptional activation of the human manganese superoxide dismutase gene mediated by tetradecanoylphorbol acetate. J Biol Chem 1999; 274: 37455–37460.
  Article CAS Google Scholar
• Yeh CC, Wan XS, St Clair DK . Transcriptional regulation of the 5' proximal promoter of the human manganese superoxide dismutase gene. DNA Cell Biol 1998; 17: 921–930.
  Article CAS Google Scholar
• Ohashi S, Natsuizaka M, Naganuma S, Kagawa S, Kimura S, Itoh H et al. A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors. Cancer Res 2011; 71: 6836–6847.
  Article CAS Google Scholar
• Ovcharenko I, Nobrega MA, Loots GG, Stubbs L . ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res 2004; 32: W280–W286.
  Article CAS Google Scholar
• Rhyu DY, Yang Y, Ha H, Lee GT, Song JS, Uh ST et al. Role of reactive oxygen species in TGF-beta1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J Am Soc Nephrol 2005; 16: 667–675.
  Article CAS Google Scholar
• Lin CH, Hung PH, Chen YJ . CD44 is associated with the aggressive phenotype of nasopharyngeal carcinoma through redox regulation. Int J Mol Sci 2013; 14: 13266–13281.
  Article Google Scholar
• Gammon L, Biddle A, Heywood HK, Johannessen AC, Mackenzie IC . Sub-sets of cancer stem cells differ intrinsically in their patterns of oxygen metabolism. PLoS One 2013; 8: e62493.
  Article CAS Google Scholar
• Natsuizaka M, Kinugasa H, Kagawa S, Whelan KA, Naganuma S, Subramanian H et al. IGFBP3 promotes esophageal cancer growth by suppressing oxidative stress in hypoxic tumor microenvironment. Am J Cancer Res 2014; 4: 29–41.
  PubMed PubMed Central Google Scholar
• Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 2011; 19: 387–400.
  Article CAS Google Scholar
• Dhar SK, Tangpong J, Chaiswing L, Oberley TD, St Clair DK . Manganese superoxide dismutase is a p53-regulated gene that switches cancers between early and advanced stages. Cancer Res 2011; 71: 6684–6695.
  Article CAS Google Scholar
• Guha M, Srinivasan S, Ruthel G, Kashina AK, Carstens RP, Mendoza A et al. Mitochondrial retrograde signaling induces epithelial-mesenchymal transition and generates breast cancer stem cells. Oncogene 2013; 33: 5238–5250.
  Article Google Scholar
• Chua HL, Bhat-Nakshatri P, Clare SE, Morimiya A, Badve S, Nakshatri H . NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 2007; 26: 711–724.
  Article CAS Google Scholar
• Nam EH, Lee Y, Zhao XF, Park YK, Lee JW, Kim S . ZEB2-Sp1 cooperation induces invasion by upregulating cadherin-11 and integrin alpha5 expression. Carcinogenesis 2014; 35: 302–314.
  Article CAS Google Scholar
• Nam EH, Lee Y, Park YK, Lee JW, Kim S . ZEB2 upregulates integrin alpha5 expression through cooperation with Sp1 to induce invasion during epithelial-mesenchymal transition of human cancer cells. Carcinogenesis 2012; 33: 563–571.
  Article CAS Google Scholar
• Chen PM, Wu TC, Wang YC, Cheng YW, Sheu GT, Chen CY et al. Activation of NF-kappaB by SOD2 promotes the aggressiveness of lung adenocarcinoma by modulating NKX2-1-mediated IKKbeta expression. Carcinogenesis 2013; 34: 2655–2663.
  Article CAS Google Scholar
• Meng X, Wu J, Pan C, Wang H, Ying X, Zhou Y et al. Genetic and epigenetic down-regulation of microRNA-212 promotes colorectal tumor metastasis via dysregulation of MnSOD. Gastroenterology 2013; 145: 426–436.e421–426.
  Article CAS Google Scholar
• Ji G, Lv K, Chen H, Wang T, Wang Y, Zhao D et al. MiR-146a regulates SOD2 expression in H2O2 stimulated PC12 cells. PLoS One 2013; 8: e69351.
  Article CAS Google Scholar
• Bai XY, Ma Y, Ding R, Fu B, Shi S, Chen XM . miR-335 and miR-34a Promote renal senescence by suppressing mitochondrial antioxidative enzymes. J Am Soc Nephrol 2011; 22: 1252–1261.
  Article CAS Google Scholar
• Kriegel AJ, Fang Y, Liu Y, Tian Z, Mladinov D, Matus IR et al. MicroRNA-target pairs in human renal epithelial cells treated with transforming growth factor beta 1: a novel role of miR-382. Nucleic Acids Res 2010; 38: 8338–8347.
  Article CAS Google Scholar
• Liu X, Yu J, Jiang L, Wang A, Shi F, Ye H et al. MicroRNA-222 regulates cell invasion by targeting matrix metalloproteinase 1 (MMP1) and manganese superoxide dismutase 2 (SOD2) in tongue squamous cell carcinoma cell lines. Cancer Genomics Proteomics 2009; 6: 131–139.
  CAS PubMed PubMed Central Google Scholar
• Wang Q, Wang Y, Minto AW, Wang J, Shi Q, Li X et al. MicroRNA-377 is up-regulated and can lead to increased fibronectin production in diabetic nephropathy. FASEB J 2008; 22: 4126–4135.
  Article CAS Google Scholar
• Ju X, Casimiro MC, Gormley M, Meng H, Jiao X, Katiyar S et al. Identification of a cyclin D1 network in prostate cancer that antagonizes epithelial-mesenchymal restraint. Cancer Res 2014; 74: 508–519.
  Article CAS Google Scholar
• Dickson MA, Hahn WC, Ino Y, Ronfard V, Wu JY, Weinberg RA et al. Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 2000; 20: 1436–1447.
  Article CAS Google Scholar