Stem cell biomarker ALDH1A1 in breast cancer shows an association with prognosis and clinicopathological variables that is highly cut-off dependent

Journal of Clinical Pathology

Volumn 68, Issue 12, 2015, Pages 1012-1019

  Sjostrom, Martin ^a   Hartman, Linda ^a   Honeth, Gabriella ^a   Grabau, Dorthe ^a,b   Malmstrom, Per ^a,b   Hegardt, Cecilia ^a   Ferno, Mårten ^a   Niméus, Emma ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE FAMILY 1 MEMBER A1; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; TAMOXIFEN; TUMOR MARKER; UNCLASSIFIED DRUG; ALDH1A1 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER HORMONE THERAPY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE FREE SURVIVAL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE DISSECTION; MAJOR CLINICAL STUDY; MIDDLE AGED; PARTIAL MASTECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL; TISSUE MICROARRAY; BREAST TUMOR; CANCER STEM CELL; METABOLISM; PATHOLOGY; PROGNOSIS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ALDEHYDE DEHYDROGENASE; BREAST NEOPLASMS; COHORT STUDIES; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; NEOPLASTIC STEM CELLS; PROGNOSIS; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE;

EID: 84958180531     PISSN: 00219746     EISSN: 14724146     Source Type: Journal    
DOI: 10.1136/jclinpath-2015-203092     Document Type: Article

References (46)

1. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
2. Chuthapisith S, Eremin J, El-Sheemey M, et al. Breast cancer chemoresistance: emerging importance of cancer stem cells. Surg Oncol 2010;19:27-32.
3. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat Med 2009;15:1010-12.
4. Sorlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001;98:10869-74.
5. Iqbal J, Chong PY, Tan PH. Breast cancer stem cells: an update. J Clin Pathol 2013;66:485-90.
6. Dontu G. Breast cancer stem cell markers-the rocky road to clinical applications. Breast Cancer Res 2008;10:110.
7. Chute JP, Muramoto GG, Whitesides J, et al. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci USA 2006;103:11707-12.
8. Ginestier C, Hur MH, Charafe-Jauffret E, 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.
9. Marcato P, Dean CA, Pan D, et al. Aldehyde dehydrogenase activity of breast cancer stem cells is primarily due to isoform ALDH1A3 and its expression is predictive of metastasis. Stem Cells 2011;29:32-45.
10. Charafe-Jauffret E, Ginestier C, Bertucci F, et al. ALDH1-positive cancer stem cells predict engraftment of primary breast tumors and are governed by a common stem cell program. Cancer Res 2013;73:7290-300.
11. Dong Y, Bi LR, Xu N, et al. The expression of aldehyde dehydrogenase 1 in invasive primary breast tumors and axillary lymph node metastases is associated with poor clinical prognosis. Pathol Res Pract 2013;209:555-61.
12. Woodward WA, Krishnamurthy S, Lodhi A, et al. Aldehyde dehydrogenase1 immunohistochemical staining in primary breast cancer cells independently predicted overall survival but did not correlate with the presence of circulating or disseminated tumors cells. J Cancer 2014;5:360-7.
13. Liu Y, Lv DL, Duan JJ, et al. ALDH1A1 expression correlates with clinicopathologic features and poor prognosis of breast cancer patients: a systematic review and meta-analysis. BMC Cancer 2014;14:444.
14. Tan EY, Thike AA, Tan PH, Breast Surgical Team at Outram. ALDH1 expression is enriched in breast cancers arising in young women but does not predict outcome. Br J Cancer 2013;109:109-13.
15. Morimoto K, Kim SJ, Tanei T, et al. 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 2009;100:1062-8.
16. Resetkova E, Reis-Filho JS, Jain RK, et al. Prognostic impact of ALDH1 in breast cancer: a story of stem cells and tumor microenvironment. Breast Cancer Res Treat 2010;123:97-108.
17. Ricardo S, Vieira AF, Gerhard R, et al. Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol 2011;64:937-46.
18. Neumeister V, Agarwal S, Bordeaux J, et al. In situ identification of putative cancer stem cells by multiplexing ALDH1, CD44, and cytokeratin identifies breast cancer patients with poor prognosis. Am J Pathol 2010;176:2131-8.
19. Gong Y, Wang J, Huo L, et al. Aldehyde dehydrogenase 1 expression in inflammatory breast cancer as measured by immunohistochemical staining. Clin Breast Cancer 2014;14:e81-8.
20. Lehmann C, Jobs G, Thomas M, et al. Established breast cancer stem cell markers do not correlate with in vivo tumorigenicity of tumor-initiating cells. Int J Oncol 2012;41:1932-42.
21. Neumeister V, Rimm D. Is ALDH1 a good method for definition of breast cancer stem cells? Breast Cancer Res Treat 2010;123:109-11.
22. Isfoss BL, Holmqvist B, Alm P, et al. Distribution of aldehyde dehydrogenase 1-positive stem cells in benign mammary tissue from women with and without breast cancer. Histopathology 2012;60:617-33.
23. De Brot M, Rocha RM, Soares FA, et al. Prognostic impact of the cancer stem cell related markers ALDH1 and EZH2 in triple negative and basal-like breast cancers. Pathology 2012;44:303-12.
24. Ohi Y, Umekita Y, Yoshioka T, et al. Aldehyde dehydrogenase 1 expression predicts poor prognosis in triple-negative breast cancer. Histopathology 2011;59:776-80.
25. Broselid S, Cheng B, Sjostrom M, et al. G protein-coupled estrogen receptor is apoptotic and correlates with increased distant disease-free survival of estrogen receptor-positive breast cancer patients. Clin Cancer Res 2013;19:1681-92.
26. [No authors listed]. Randomized trial of two versus five years of adjuvant tamoxifen for postmenopausal early stage breast cancer. Swedish Breast Cancer Cooperative Group. J Natl Cancer Inst 1996;88:1543-9.
27. Ryden L, Jonsson PE, Chebil G, et al. Two years of adjuvant tamoxifen in premenopausal patients with breast cancer: a randomised, controlled trial with long-term follow-up. Eur J Cancer 2005;41:256-64.
28. Malmstrom P, Bendahl PO, Boiesen P, et al. S-phase fraction and urokinase plasminogen activator are better markers for distant recurrences than Nottingham Prognostic Index and histologic grade in a prospective study of premenopausal lymph node-negative breast cancer. J Clin Oncol 2001;19:2010-19.
29. Strand C, Bak M, Borgquist S, et al. The combination of Ki67, histological grade and estrogen receptor status identifies a low-risk group among 1854 chemo-naive women with N0/N1 primary breast cancer. Springerplus 2013;2:111. http://dx.doi. org/10.1186/2193-1801-2-111
30. Klintman M, Bendahl PO, Grabau D, et al. The prognostic value of Ki67 is dependent on estrogen receptor status and histological grade in premenopausal patients with node-negative breast cancer. Mod Pathol 2010;23:251-9.
31. Sjostrom M, Hartman L, Grabau D, et al. Lack of G protein-coupled estrogen receptor (GPER) in the plasma membrane is associated with excellent long-term prognosis in breast cancer. Breast Cancer Res Treat 2014;145:61-71.
32. Honeth G, Lombardi S, Ginestier C, et al. Aldehyde dehydrogenase and estrogen receptor define a hierarchy of cellular differentiation in the normal human mammary epithelium. Breast Cancer Res 2014;16:R52.
33. Olsson E, Honeth G, Bendahl PO, et al. CD44 isoforms are heterogeneously expressed in breast cancer and correlate with tumor subtypes and cancer stem cell markers. BMC Cancer 2011;11:418.
34. Honeth G, Bendahl PO, Ringner M, et al. The CD44+/CD24-phenotype is enriched in basal-like breast tumors. Breast Cancer Res 2008;10:R53.
35. Ringner M, Fredlund E, Hakkinen J, et al. GOBO: gene expression-based outcome for breast cancer online. PLoS ONE 2011;6:e17911.
36. Schoenfeld D. Partial residuals for the proportional hazards regression model. Biometrika 1982;69:239-41.
37. Chang B, Liu G, Xue F, et al. ALDH1 expression correlates with favorable prognosis in ovarian cancers. Mod Pathol 2009;22:817-23.
38. Nagano M, Yamashita T, Hamada H, et al. Identification of functional endothelial progenitor cells suitable for the treatment of ischemic tissue using human umbilical cord blood. Blood 2007;110:151-60.
39. Estes BT, Wu AW, Storms RW, et al. Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells. J Cell Physiol 2006;209:987-95.
40. Zhong Y, Shen S, Zhou Y, et al. ALDH1 is a better clinical indicator for relapse of invasive ductal breast cancer than the CD44(+)/CD24(-) phenotype. Med Oncol 2014;31:864.
41. Mieog JS, de Kruijf EM, Bastiaannet E, et al. Age determines the prognostic role of the cancer stem cell marker aldehyde dehydrogenase-1 in breast cancer. BMC Cancer 2012;12:42.
42. Schwartz T, Stark A, Pang J, et al. Expression of aldehyde dehydrogenase 1 as a marker of mammary stem cells in benign and malignant breast lesions of Ghanaian women. Cancer 2013;119:488-94.
43. Fridman WH, Galon J, Pages F, et al. Prognostic and predictive impact of intra-and peritumoral immune infiltrates. Cancer Res 2011;71:5601-5.
44. Deng S, Yang X, Lassus H, et al. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS ONE 2010;5:e10277.
45. Okudela K, Woo T, Mitsui H, et al. Downregulation of ALDH1A1 expression in non-small cell lung carcinomas-its clinicopathologic and biological significance. Int J Clin Exp Pathol 2013;6:1-12.
46. Dimou A, Neumeister V, Agarwal S, et al. Measurement of aldehyde dehydrogenase 1 expression defines a group with better prognosis in patients with non-small cell lung cancer. Am J Pathol 2012;181:1436-42.