Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Deng, Shan ^a,c   Yang, Xiaojun ^a,d   Lassus, Heini ^e   Liang, Shun ^a   Kaur, Sippy ^e   Ye, Qunrui ^a   Li, Chunsheng ^a   Wang, Li Ping ^a   Roby, Katherine F ^f   Orsulic, Sandra ^g   Connolly, Denise C ^h   Zhang, Youcheng ^d   Montone, Kathleen ^a   Bützow, Ralf ^e   Coukos, George ^a,b   Zhang, Lin ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c PEKING UNION MEDICAL COLLEGE   (China)

^d Lanzhou University Second Hospital   (Taiwan)

^e HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^f UNIVERSITY OF KANSAS   (United States)

^g CEDARS SINAI MEDICAL CENTER   (United States)

^h FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOFORM 1; UNCLASSIFIED DRUG; ALDEHYDE DEHYDROGENASE ISOENZYME 1; BIOLOGICAL MARKER; ISOENZYME; RETINAL DEHYDROGENASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL; CANCER STEM CELL; CARCINOGENICITY; CELL POPULATION; CELL RENEWAL; CELL STRUCTURE; COLON CANCER; CONTROLLED STUDY; DISEASE FREE SURVIVAL; ENZYME ACTIVITY; EPITHELIUM TUMOR; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OVARY CANCER; OVERALL SURVIVAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; TISSUE MICROARRAY; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; CARCINOMA; ENZYMOLOGY; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; OVARY TUMOR; PATHOLOGY; PROGNOSIS; TUMOR CELL LINE;

MURINAE; MUS MUSCULUS;

ANIMALS; BIOLOGICAL MARKERS; CARCINOMA; CELL LINE, TUMOR; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MICE; MICE, TRANSGENIC; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; PROGNOSIS; RETINAL DEHYDROGENASE;

EID: 77956302698     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010277     Document Type: Article

References (53)

1. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, et al. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645-648.
2. Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737.
3. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988.
4. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, et al. (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401.
5. Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, et al. (2005) A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 65: 9328-9337.
6. Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, et al. (2006) Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci USA 103: 11154-11159.
7. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, et al. (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104: 10158-10163.
8. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110.
9. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, et al. (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115.
10. Szotek PP, Chang HL, Brennand K, Fujino A, Pieretti-Vanmarcke R, et al. (2008) Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. Proc Natl Acad Sci USA 105: 12469-12473.
11. Smalley M, Ashworth A (2003) Stem cells and breast cancer: A field in transit. Nat Rev Cancer 3: 832-844.
12. Jordan CT, Guzman ML, Noble M (2006) Cancer stem cells. N Engl J Med 355: 1253-1261.
13. Lobo NA, Shimono Y, Qian D, Clarke MF (2007) The biology of cancer stem cells. Annu Rev Cell Dev Biol 23: 675-699.
14. Stingl J, Caldas C (2007) Molecular heterogeneity of breast carcinomas and the cancer stem cell hypothesis. Nat Rev Cancer 7: 791-799.
15. Ward RJ, Dirks PB (2007) Cancer stem cells: at the headwaters of tumor development. Annu Rev Pathol 2: 175-189.
16. Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8: 755-768.
17. Lee JT, Herlyn M (2007) Old disease, new culprit: tumor stem cells in cancer. J Cell Physiol 213: 603-609.
18. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760.
19. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, et al. (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100: 672-679.
20. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, et al. (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783.
21. Dontu G (2008) Breast cancer stem cell markers - the rocky road to clinical applications. Breast Cancer Res 10: 110.
22. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, et al. (2008) Identification of cells initiating human melanomas. Nature 451: 345-349.
23. Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, et al. (2008) Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13: 153-166.
24. Vaillant F, Asselin-Labat ML, Shackleton M, Forrest NC, Lindeman GJ, et al. (2008) The mammary progenitor marker CD61/beta3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res 68: 7711-7717.
25. Vlashi E, Kim K, Lagadec C, Donna LD, McDonald JT, et al. (2009) In vivo imaging, tracking, and targeting of cancer stem cells. J Natl Cancer Inst 101: 350-359.
26. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183: 1797-1806.
27. Hadnagy A, Gaboury L, Beaulieu R, Balicki D (2006) SP analysis may be used to identify cancer stem cell populations. Exp Cell Res 312: 3701-3710.
28. Yoshida A, Rzhetsky A, Hsu LC, Chang C (1998) Human aldehyde dehydrogenase gene family. Eur J Biochem 251: 549-557.
29. Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, et al. (1999) Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci USA 96: 9118-9123.
30. Hess DA, Meyerrose TE, Wirthlin L, Craft TP, Herrbrich PE, et al. (2004) Functional characterization of highly purified human hematopoietic repopulating cells isolated according to aldehyde dehydrogenase activity. Blood 104: 1648-1655.
31. Armstrong L, Stojkovic M, Dimmick I, Ahmad S, Stojkovic P, et al. (2004) Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells 22: 1142-1151.
32. Gentry T, Foster S, Winstead L, Deibert E, Fiordalisi M, et al. (2007) Simultaneous isolation of human BM hematopoietic, endothelial and mesenchymal progenitor cells by flow sorting based on aldehyde dehydrogenase activity: implications for cell therapy. Cytotherapy 9: 259-274.
33. Corti S, Locatelli F, Papadimitriou D, Donadoni C, Salani S, et al. (2006) Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. Stem Cells 24: 975-985.
34. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 Is a Marker of Normal and Malignant Human Mammary Stem Cells and a Predictor of Poor Clinical Outcome. Cell Stem Cell 1: 555-567.
35. Ibarra I, Erlich Y, Muthuswamy SK, Sachidanandam R, Hannon GJ (2007) A role for microRNAs in maintenance of mouse mammary epithelial progenitor cells. Genes Dev 21: 3238-3243.
36. Burger PE, Gupta R, Xiong X, Ontiveros CS, Salm SN, et al. (2009) High ALDH Activity: A Novel Functional Marker of Murine Prostate Stem/Progenitor Cells. Stem Cells.
37. Morimoto K, Kim SJ, Tanei T, Shimazu K, Tanji Y, et al. (2009) Stem cell marker aldehyde dehydrogenase 1-positive breast cancers are characterized by negative estrogen receptor, positive human epidermal growth factor receptor type 2, and high Ki67 expression. Cancer Sci 100: 1062-1068.
38. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, et al. (2009) Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 7: 330-338.
39. Chang B, Liu G, Xue F, Rosen DG, Xiao L, et al. (2009) ALDH1 expression correlates with favorable prognosis in ovarian cancers. Mod Pathol 22: 817-823.
40. Rasheed ZA, Yang J, Wang Q, Kowalski J, Freed I, et al. (2010) Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst 102: 340-351.
41. Su Y, Qiu Q, Zhang X, Jiang Z, Leng Q, et al. (2010) Aldehyde dehydrogenase 1 A1-positive cell population is enriched in tumor-initiating cells and associated with progression of bladder cancer. Cancer Epidemiol Biomarkers Prev 19: 327-337.
42. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, et al. (2010) Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 16: 45-55.
43. Li T, Su Y, Mei Y, Leng Q, Leng B, et al. (2010) ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients' outcome. Lab Invest 90: 234-244.
44. Roby KF, Taylor CC, Sweetwood JP, Cheng Y, Pace JL, et al. (2000) Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 21: 585-591.
45. Connolly DC, Bao R, Nikitin AY, Stephens KC, Poole TW, et al. (2003) Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res 63: 1389-1397.
46. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, et al. (2009) Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 69: 3382-3389.
47. Zhang L, Yang N, Garcia JR, Mohamed A, Benencia F, et al. (2002) Generation of a syngeneic mouse model to study the effects of vascular endothelial growth factor in ovarian carcinoma. Am J Pathol 161: 2295-2309.
48. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, et al. (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17: 1253-1270.
49. Carpentino JE, Hynes MJ, Appelman HD, Zheng T, Steindler DA, et al. (2009) Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res 69: 8208-8215.
50. Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, et al. (2008) Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS ONE 3: e2428.
51. Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, et al. (2009) Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 15: 4234-4241.
52. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, et al. (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69: 1302-1313.
53. Wang L, Park P, Zhang H, La Marca F, Lin CY (2010) Prospective identification of tumorigenic osteosarcoma cancer stem cells in OS99-1 cells based on high aldehyde dehydrogenase activity. Int J Cancer, Epub ahead of print.