Increased CD13 expression reduces reactive oxygen species, promoting survival of liver cancer stem cells via an epithelial-mesenchymal transition-like phenomenon

Annals of Surgical Oncology

Volumn 19, Issue SUPPL. 3, 2012, Pages

  Kim, Ho Min ^a   Haraguchi, Naotsugu ^a   Ishii, Hideshi ^a,b   Ohkuma, Masahisa ^a,c   Okano, Miho ^a   Mimori, Koshi ^b   Eguchi, Hidetoshi ^a   Yamamoto, Hirofumi ^a   Nagano, Hiroaki ^a   Sekimoto, Mitsugu ^a   Doki, Yuichiro ^a   Mori, Masaki ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSOMAL AMINOPEPTIDASE; NERVE CELL ADHESION MOLECULE; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER STEM CELL; CELL FUNCTION; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LIVER CANCER; MESENCHYME CELL; PROTEIN EXPRESSION;

ANTIGENS, CD13; APOPTOSIS; CADHERINS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CHI-SQUARE DISTRIBUTION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMANS; LIVER NEOPLASMS; NEOPLASTIC STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 1; REACTIVE OXYGEN SPECIES; RECEPTOR, NOTCH1; RNA, MESSENGER; STATISTICS, NONPARAMETRIC; TRANSFORMING GROWTH FACTOR BETA; TUMOR STEM CELL ASSAY;

EID: 84864987692     PISSN: 10689265     EISSN: 15344681     Source Type: Journal    
DOI: 10.1245/s10434-011-2040-5     Document Type: Article

References (41)

1. J Sagar B Chaib K Sales M Winslet A Seifalian 2007 Role of stem cells in cancer therapy and cancer stem cells: a review Cancer Cell Int. 4 7 9
2. T Reya SJ Morrison MF Clarke IL Weissman 2001 Stem cells, cancer, and cancer stem cells Nature 414 6859 105 111 11689955 10.1038/35102167 1:CAS:528:DC%2BD3MXot1ahs7c%3D
3. BT Tan CY Park LE Ailles IL Weissman 2006 The cancer stem cell hypothesis: a work in progress Lab Invest. 86 12 1203 1207 17075578 10.1038/labinvest.3700488 1:CAS:528:DC%2BD28Xht1akur3O
4. GG Wulf RY Wang I Kuehnle, et al. 2001 A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia Blood. 98 4 1166 1173 11493466 10.1182/blood.V98.4.1166 1:CAS:528:DC%2BD3MXmtFeitrw%3D
5. T Lapidot C Sirard J Vormoor, et al. 1994 A cell initiating human acute myeloid leukaemia after transplantation into SCID mice Nature. 367 6464 645 648 7509044 10.1038/367645a0 1:STN:280:DyaK2c7ltVKrsg%3D%3D
6. D Bonnet JE Dick 1997 Human acute leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nat Med. 3 7 730 737 9212098 10.1038/nm0797-730 1:CAS:528:DyaK2sXkt1GrtLY%3D
7. SG Piccirillo BA Reynolds N Zanetti, et al. 2006 Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells Nature. 444 7120 761 765 17151667 10.1038/nature05349 1:CAS:528: DC%2BD28Xht1Ontb3J
8. S Bao Q Wu RE McLendon, et al. 2006 Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature. 444 7120 756 760 17051156 10.1038/nature05236 1:CAS:528:DC%2BD28Xht1OntbzP
9. ME Prince R Sivanandan A Kaczorowski, et al. 2007 Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma Proc Natl Acad Sci USA. 104 3 973 978 17210912 10.1073/pnas.0610117104 1:CAS:528:DC%2BD2sXhtVSitLk%3D
10. M Al-Hajj MS Wicha A Benito-Hernandez SJ Morrison MF Clarke 2003 Prospective identification of tumorigenic breast cancer cells Proc Natl Acad Sci USA. 100 7 3983 3988 12629218 10.1073/pnas.0530291100 1:CAS:528: DC%2BD3sXivFSqtbs%3D
11. L Ricci-Vitiani DG Lombardi E Pilozzi, et al. 2007 Identification and expansion of human colon-cancer-initiating cells Nature. 445 7123 111 115 17122771 10.1038/nature05384 1:CAS:528:DC%2BD2sXhsFOmug%3D%3D
12. CA O'Brien A Pollett S Gallinger JE Dick 2007 A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature. 445 7123 106 110 17122772 10.1038/nature05372
13. N Haraguchi T Utsunomiya H Inoue, et al. 2006 Characterization of a side population of cancer cells from human gastrointestinal system Stem Cells. 24 3 506 513 16239320 10.1634/stemcells.2005-0282 1:CAS:528:DC%2BD28XhtFKitbvL
14. T Chiba K Kita YW Zheng, et al. 2006 Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties Hepatology. 44 1 240 251 16799977 10.1002/hep.21227 1:CAS:528: DC%2BD28XnsFWjur0%3D
15. W Ding M Mouzaki H You, et al. 2009 CD133 + liver cancer stem cells from methionine adenosyl transferase 1A-deficient mice demonstrate resistance to transforming growth factor (TGF)-beta-induced apoptosis Hepatology. 49 4 1277 1286 19115422 10.1002/hep.22743 1:CAS:528:DC%2BD1MXkslWjsrY%3D
16. S Ma KW Chan L Hu, et al. 2007 Identification and characterization of tumorigenic liver cancer stem/progenitor cells Gastroenterology. 132 7 2542 2556 17570225 10.1053/j.gastro.2007.04.025 1:CAS:528:DC%2BD2sXnvFOgsr4%3D
17. Z Zhu X Hao M Yan, et al. 2010 Cancer stem/progenitor cells are highly enriched in CD133(+)CD44(+) population in hepatocellular carcinoma Int J Cancer. 126 9 2067 2078 19711346 1:CAS:528:DC%2BC3cXisFemtLk%3D
18. ZF Yang P Ngai DW Ho, et al. 2008 Identification of local and circulating cancer stem cells in human liver cancer Hepatology. 47 3 919 928 18275073 10.1002/hep.22082 1:CAS:528:DC%2BD1cXktVOhs7w%3D
19. ZF Yang DW Ho MN Ng, et al. 2008 Significance of CD90 + cancer stem cells in human liver cancer Cancer Cell. 13 2 153 166 18242515 10.1016/j.ccr.2008.01. 013 1:CAS:528:DC%2BD1cXitFWrs7c%3D
20. T Yamashita J Ji A Budhu, et al. 2009 EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features Gastroenterology. 136 3 1012 1024 19150350 10.1053/j.gastro.2008.12.004 1:CAS:528:DC%2BD1MXjslSju78%3D
21. N Haraguchi H Ishii K Mimori, et al. 2010 CD13 is a therapeutic target in human liver cancer stem cells J Clin Invest. 120 9 3326 3339 20697159 10.1172/JCI42550 1:CAS:528:DC%2BC3cXhtFertbvI
22. A Menrad D Speicher J Wacker M Herlyn 1993 Biochemical and functional characterization of aminopeptidase N expressed by human melanoma cells Cancer Res. 53 6 1450 1455 8095183 1:CAS:528:DyaK3sXitFSnt7w%3D
23. R Pasqualini E Koivunen R Kain, et al. 2000 Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis Cancer Res. 60 3 722 727 10676659 1:CAS:528:DC%2BD3cXht1Gmtbc%3D
24. Y Mishima Y Matsumoto-Mishima Y Terui, et al. 2002 Leukemic cell-surface CD13/aminopeptidase N and resistance to apoptosis mediated by endothelial cells J Natl Cancer Inst. 94 13 1020 1028 12096087 10.1093/jnci/94.13.1020 1:CAS:528:DC%2BD38Xlsl2hsbs%3D
25. JP Thiery H Acloque RY Huang MA Nieto 2009 Epithelial-mesenchymal transitions in development and disease Cell. 139 5 871 890 19945376 10.1016/j.cell.2009.11.007 1:CAS:528:DC%2BC3cXksFWltA%3D%3D
26. J Yang RA Weinberg 2008 Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis Dev Cell. 14 6 818 829 18539112 10.1016/j.devcel.2008.05.009 1:CAS:528:DC%2BD1cXnsVCrs7g%3D
27. SA Mani W Guo MJ Liao, et al. 2008 The epithelial-mesenchymal transition generates cells with properties of stem cells Cell. 133 4 704 715 18485877 10.1016/j.cell.2008.03.027 1:CAS:528:DC%2BD1cXmsVOru7w%3D
28. WS Wu 2006 The signaling mechanism of ROS in tumor progression Cancer Metastasis Rev. 25 4 695 705 17160708 10.1007/s10555-006-9037-8 1:CAS:528:DC%2BD2sXisVyrsg%3D%3D
29. DC Radisky DD Levy LE Littlepage, et al. 2005 Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability Nature. 436 7047 123 127 16001073 10.1038/nature03688 1:CAS:528:DC%2BD2MXlvVGiurk%3D
30. JR Rees BA Onwuegbusi VE Save D Alderson RC Fitzgerald 2006 In vivo and in vitro evidence for transforming growth factor-beta1-mediated epithelial to mesenchymal transition in esophageal adenocarcinoma Cancer Res. 66 19 9583 9590 17018615 10.1158/0008-5472.CAN-06-1842 1:CAS:528:DC%2BD28XhtVams77E
31. K Ito A Hirao F Arai, et al. 2004 Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells Nature. 431 7011 997 1002 15496926 10.1038/nature02989 1:CAS:528:DC%2BD2cXoslSlt78%3D
32. K Ito A Hirao F Arai, et al. 2006 Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells Nat Med. 12 4 446 451 16565722 10.1038/nm1388 1:CAS:528:DC%2BD28XjtFKjtbw%3D
33. M Diehn RW Cho NA Lobo, et al. 2009 Association of reactive oxygen species levels and radioresistance in cancer stem cells Nature. 458 7239 780 783 19194462 10.1038/nature07733 1:CAS:528:DC%2BD1MXhsVCrtbc%3D
34. JL Dembinski S Krauss 2009 Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma Clin Exp Metastasis. 26 7 611 623 19421880 10.1007/s10585-009-9260-0 1:CAS:528: DC%2BD1MXhsVWls7%2FM
35. GJ Klarmann EM Hurt LA Mathews, et al. 2009 Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature Clin Exp Metastasis. 26 5 433 446 19221883 10.1007/s10585-009-9242-2 1:CAS:528:DC%2BD1MXmtVKgsLY%3D
36. Z Wang Y Li FH Sarkar 2010 Signaling mechanism(s) of reactive oxygen species in epithelial-mesenchymal transition reminiscent of cancer stem cells in tumor progression Curr Stem Cell Res Ther. 5 1 74 80 19951255 10.2174/157488810790442813
37. KM Mahoney N Petrovic W Schacke LH Shapiro 2007 CD13/APN transcription is regulated by the proto-oncogene c-Maf via an atypical response element Gene. 403 1-2 178 187 17897790 10.1016/j.gene.2007.08.010 1:CAS:528:DC%2BD2sXhtFalsbbJ
38. CL Nilsson R Dillon A Devakumar, et al. 2010 Quantitative phosphoproteomic analysis of the STAT3/IL-6/HIF1alpha signaling network: an initial study in GSC11 glioblastoma stem cells J Proteome Res. 9 1 430 443 19899826 10.1021/pr9007927 1:CAS:528:DC%2BD1MXhsVyjt7fM
39. K Kataoka 2007 Multiple mechanisms and functions of Maf transcription factors in the regulation of tissue-specific genes J Biochem. 141 6 775 781 17569705 10.1093/jb/mvm105 1:CAS:528:DC%2BD2sXhtV2ntrvL
40. A Cvekl Y Yang BK Chauhan K Cveklova 2004 Regulation of gene expression by Pax6 in ocular cells: a case of tissue-preferred expression of crystalines in lens Int J Dev Biol. 48 8-9 829 844 15558475 10.1387/ijdb.041866ac 1:CAS:528:DC%2BD2MXivFegsb4%3D
41. Y Hiramatsu A Suto D Kashiwakuma, et al. 2010 c-Maf activates the promoter and enhancer of the IL-21 gene, and TGF-b inhibits c-Maf-induced IL-21 production in CD4+T cells J Leukoc Biol. 87 4 703 712 20042469 10.1189/jlb.0909639 1:CAS:528:DC%2BC3cXmvVChtr8%3D