Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling

Cancer Research

Volumn 70, Issue 23, 2010, Pages 9937-9948

  Sullivan, James P ^a,b   Spinola, Monica ^a,b   Dodge, Michael ^a   Raso, Maria G ^c   Behrens, Carmen ^d   Gao, Boning ^a,b,d   Schuster, Katja ^b,d   Shao, Chunli ^a,b   Larsen, Jill E ^a,b   Sullivan, Laura A ^a,b   Honorio, Sofia ^a,b   Xie, Yang ^a,b   Scaglioni, Pier P ^b,d   DiMaio, J Michael ^b,d   Gazdar, Adi F ^a,b,d   Shay, Jerry W ^a,b   Wistuba, Ignacio I ^c   Minna, John D ^a,b,d  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE1A1; ALDEHYDE DEHYDROGENASE3A1; CD133 ANTIGEN; GAMMA SECRETASE INHIBITOR; NOTCH RECEPTOR; NOTCH3 RECEPTOR; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER STAGING; CANCER STEM CELL; CARCINOGENESIS; CELL PROLIFERATION; CELL RENEWAL; CELL SUBPOPULATION; CLONOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STABLE EXPRESSION; STEM CELL; TUMOR CELL;

ADENOCARCINOMA; ALDEHYDE DEHYDROGENASE; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; NEOPLASTIC STEM CELLS; PROGNOSIS; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE ARRAY ANALYSIS; TRANSPLANTATION, HETEROLOGOUS;

EID: 78649960144     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0881     Document Type: Article

References (50)

1. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
2. Clarke MF, Fuller M. Stem cells and cancer: two faces of eve. Cell 2006;124:1111-5.
3. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8:755-68.
4. Wicha MS, Liu SL, Dontu G. Cancer stem cells: an old idea - a paradigm shift. Cancer Res 2006;66:1883-90. (Pubitemid 43294892)
5. Sullivan JP, Minna JD, Shay JW. Evidence for self-renewing lung cancer stem cells and their implications in tumor initiation, progression, and targeted therapy. Cancer Metastasis Rev 2010;29:61-72.
6. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005;121:823-35.
7. Giangreco A, Groot KR, Janes SM. Lung cancer and lung stem cells - strange bedfellows? Am J Resp and Criti Care Med 2007;175:547-53.
8. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature 2004;432:396-401. (Pubitemid 39551674)
9. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007;445:111-5. (Pubitemid 46067311)
10. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008;15:504-14.
11. Wang J, Sakariassen PO, Tsinkalovsky O, Immervoll H, Boe SO, Svendsen A, et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Cancer 2008;122:761-8.
12. Salnikov AV, Gladkich J, Moldenhauer G, Volm M, Mattern J, Herr I. CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer 2010;126:950-8.
13. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, et al. CD133 expression is not restricted to stem cells, and both CD133+ and CD133-metastatic colon cancer cells initiate tumors. J Clin Invest 2008;118:2111-20.
14. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555-67.
15. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009;69:3382-9.
16. Moreb J, Schweder M, Suresh A, Zucali JR. Overexpression of the human aldehyde dehydrogenase class I results in increased resistance to 4-hydroperoxycyclophosphamide. Cancer Gene Ther 1996;3:24-30. (Pubitemid 126732422)
17. Chute JP, Muramoto GG, Whitesides J, Colvin M, Safi R, Chao NJ, et al. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci U S A 2006;103:11707-12. (Pubitemid 44182515)
18. Cheung AM, Wan TS, Leung JC, Chan LY, Huang H, Kwong YL, et al. Aldehyde dehydrogenase activity in leukemic blasts defines a subgroup of acute myeloid leukemia with adverse prognosis and superior NOD/SCID engrafting potential. Leukemia 2007;21:1423-30.
19. Pearce DJ, Taussig D, Simpson C, Allen K, Rohatiner AZ, Lister TA, et al. Characterization of cells with a high aldehyde dehydrogenase activity from cord blood and acute myeloid leukemia samples. Stem Cells 2005;23:752-60.
20. Patel M, Lu L, Zander DS, Sreerama L, Coco D, Moreb JS. ALDH1A1 and ALDH3A1 expression in lung cancers: correlation with histologic type and potential precursors. Lung Cancer 2008;59:340-9.
21. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 2009;7:330-8.
22. Curtis SJ, Sinkevicius KW, Li D, Lau AN, Roach RR, Zamponi R, et al. Primary tumor genotype is an important determinant in identification of lung cancer propagating cells. Cell Stem Cell 2010;7:127-33.
23. Phelps RM, Johnson BE, Ihde DC, Gazdar AF, Carbone DP, McClintock PR, et al. NCI-Navy Medical Oncology Branch cell line data base. J Cell Biochem Suppl. 1996;24:32-91. (Pubitemid 26277220)
24. Gazdar AF, Girard L, Lockwood WW, Lam LL, Minna JD. Lung cancer cell lines as tools for biomedical discovery and research. J Natl Cancer Inst 2010;102:1-12.
25. Fisher GH, Wellen SL, Klimstra D, Lenczowski JM, Tichelaar JW, Lizak MJ, et al. Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes. Genes Dev 2001;15:3249-62.
26. Tsao AS, Tang XM, Sabloff B, Xiao L, Shigematsu H, Roth J, et al. Clinicopathologic characteristics of the EGFR gene mutation in nonsmall cell lung cancer. J Thorac Oncol 2006;1:231-9.
27. Cai D, Shames DS, Raso MG, Xie Y, Kim YH, Pollack JR, et al. Steroid receptor coactivator-3 expression in lung cancer and its role in the regulation of cancer cell survival and proliferation. Cancer Res 2010;70:6477-85.
28. Ho MM, Ng AV, Lam S, Hung JY. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007;67:4827-33. (Pubitemid 46910191)
29. Paroo Z, Bollinger RA, Braasch DA, Richer E, Corey DR, Antich PP, et al. Validating bioluminescence imaging as a high-throughput, quantitative modality for assessing tumor burden. Mol Imaging 2004;3:117-24.
30. Moreb JS, Zucali JR, Ostmark B, BenSon NA. Heterogeneity of aldehyde dehydrogenase expression in lung cancer cell lines is revealed by aldefluor flow cytometry-based assay. Cytometry B Clin Cytom 2007;72B:281-9.
31. Moreb JS, Baker HV, Chang LJ, Amaya M, Lopez MC, Ostmark B, et al. ALDH isozymes downregulation affects cell growth, cell motility and gene expression in lung cancer cells. Mol Cancer 2008;7:87.
32. Li H, Chen X, Calhoun-Davis T, Claypool K, Tang DG. PC3 human prostate carcinoma cell holoclones contain self-renewing tumor-initiating cells. Cancer Res 2008;68:1820-5.
33. Sansone P, Storci G, Giovannini C, Pandolfi S, Pianetti S, Taffurelli M, et al. p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres. Stem Cells 2007;25:807-15.
34. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM, et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 2006;66:7445-52. (Pubitemid 44289197)
35. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, et al. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 2006;442:823-6. (Pubitemid 44258913)
36. Rasul S, Balasubramanian R, Filipovic A, Slade MJ, Yague E, Coombes RC. Inhibition of gamma-secretase induces G2/M arrest and triggers apoptosis in breast cancer cells. Br J Cancer 2009;100:1879-88.
37. Grabher C, von Boehmer H, Look AT. Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat Rev Cancer 2006;6:347-59.
38. Konishi J, Kawaguchi KS, Vo H, Haruki N, Gonzalez A, Carbone DP, et al. Gamma-secretase inhibitor prevents Notch3 activation and reduces proliferation in human lung cancers. Cancer Res 2007;67:8051-7. (Pubitemid 47395139)
39. Haruki N, Kawaguchi KS, Eichenberger S, Massion PP, Olson S, Gonzalez A, et al. Dominant-negative Notch3 receptor inhibits mitogen-activated protein kinase pathway and the growth of human lung cancers. Cancer Res 2005;65:3555-61.
40. Dang TP, Eichenberger S, Gonzalez A, Olson S, Carbone DP. Constitutive activation of Notch3 inhibits terminal epithelial differentiation in lungs of transgenic mice. Oncogene 2003;22:1988-97.
41. Jiang TY, Collins BJ, Jin N, Watkins DN, Brock MV, Matsui W, et al. Achaete-Scute complex homologue 1 regulates tumor-initiating capacity in human small cell lung cancer. Cancer Res 2009;69:845-54.
42. Welm BE, Tepera SB, Venezia T, Graubert TA, Rosen JM, Goodell MA. Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol 2002;245:42-56.
43. Lawson DA, Xin L, Lukacs RU, Cheng D, Witte ON. Isolation and functional characterization of murine prostate stem cells. Proc Natl Acad Sci U S A 2007;104:181-6.
44. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science 1999;284:770-6.
45. Westhoff B, Colaluca IN, D'Ario G, Donzelli M, Tosoni D, Volorio S, et al. Alterations of the Notch pathway in lung cancer. Proc Natl Acad Sci U S A 2009;106:22293-8.
46. Chen Y, De Marco MA, Graziani I, Gazdar AF, Strack PR, Miele L, et al. Oxygen concentration determines the biological effects of NOTCH-1 signaling in adenocarcinoma of the lung. Cancer Res 2007;67:7954-9. (Pubitemid 47395124)
47. Collins BJ, Kleeberger W, Ball DW. Notch in lung development and lung cancer. Semin Cancer Biol 2004;14:357-64.
48. Lin L, Mernaugh R, Yi F, Blum D, Carbone DP, Dang TP. Targeting specific regions of the Notch3 ligand-binding domain induces apoptosis and inhibits tumor growth in lung cancer. Cancer Res 2010;70:632-8.
49. Sikandar SS, Pate KT, Anderson S, Dizon D, Edwards RA, Waterman ML, et al. NOTCH signaling is required for formation and self-renewal of tumor-initiating cells and for repression of secretory cell differentiation in colon cancer. Cancer Res 2010;70:1469-78.
50. Harrison H, Farnie G, Howell SJ, Rock RE, Stylianou S, Brennan KR, et al. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res 2010;70:709-18.