Clinical-pathologic significance of cancer stem cell marker expression in familial breast cancers

Breast Cancer Research and Treatment

Volumn 140, Issue 1, 2013, Pages 195-205

  Bane, Anita ^a   Viloria Petit, Alicia ^b   Pinnaduwage, Dushanthi ^c   Mulligan, Anna Marie ^d   O'Malley, Frances P ^d   Andrulis, Irene L ^c,d  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cancer stem cell markers; Familial breast cancer; Immunohistochemistry

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; BRCA1 PROTEIN; BRCA2 PROTEIN; CD24 ANTIGEN; CELL MARKER; CYTOKERATIN 14; CYTOKERATIN 5; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; HERMES ANTIGEN; PROGESTERONE RECEPTOR; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BREAST CANCER; CANCER GRADING; CANCER REGISTRY; CANCER STEM CELL; CONTROLLED STUDY; FAMILIAL CANCER; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MITOSIS; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE MICROARRAY;

ADULT; ANTIGENS, CD24; ANTIGENS, CD44; BRCA1 PROTEIN; BRCA2 PROTEIN; BREAST NEOPLASMS; FEMALE; HUMANS; ISOENZYMES; KAPLAN-MEIER ESTIMATE; MIDDLE AGED; MUTATION; NEOPLASTIC STEM CELLS; ONTARIO; PROGNOSIS; RETINAL DEHYDROGENASE; TUMOR MARKERS, BIOLOGICAL;

EID: 84880291457     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-013-2591-1     Document Type: Article

References (83)

1. Perou CM, Sorlie T, Eisen MB, et al. (2000) Molecular portraits of human breast tumours. Nature 406:747-752
2. Sorlie T, Perou CM, Tibshirani R, et al. (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 98:10869-10874 (Pubitemid 32878711)
3. Sorlie T, Tibshirani R, Parker J, et al. (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 100:8418-8423 (Pubitemid 36842560)
4. Herschkowitz JI, Simin K, Weigman VJ, et al. (2007) Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 8:R76 (Pubitemid 351902765)
5. Prat A, Parker JS, Karginova O, et al. (2010) Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 12:R68
6. Farmer P, Bonnefoi H, Becette V, et al. (2005) Identification of molecular apocrine breast tumours by microarray analysis. Oncogene 24:4660-4671 (Pubitemid 41032603)
7. Mulligan AM, Pinnaduwage D, Bane AL, et al. (2010) CK8/18 expression, the basal phenotype, and family history in identifying BRCA1-associated breast cancer in the Ontario site of the Breast Cancer Family Registry. Cancer 117(7):1350-1359
8. Bane AL, Beck JC, Bleiweiss I, et al. (2007) BRCA2 mutation-associated breast cancers exhibit a distinguishing phenotype based on morphology and molecular profiles from tissue microarrays. Am J Surg Pathol 31:121-128 (Pubitemid 46036911)
9. Lakhani SR, Reis-Filho JS, Fulford L, et al. (2005) Prediction of BRCA1 status in patients with breast cancer using estrogen receptor and basal phenotype. Clin Cancer Res 11:5175-5180 (Pubitemid 41003703)
10. Palacios J, Honrado E, Osorio A, et al. (2005) Phenotypic characterization of BRCA1 and BRCA2 tumors based in a tissue microarray study with 37 immunohistochemical markers. Breast Cancer Res Treat 90:5-14 (Pubitemid 40486996)
11. Palacios J, Honrado E, Osorio A, et al. (2003) Immunohistochemical characteristics defined by tissue microarray of hereditary breast cancer not attributable to BRCA1 or BRCA2 mutations: differences from breast carcinomas arising in BRCA1 and BRCA2 mutation carriers. Clin Cancer Res 9:3606-3614 (Pubitemid 37169224)
12. Booth BW, Smith GH (2006) Estrogen receptor-alpha and progesterone receptor are expressed in label-retaining mammary epithelial cells that divide asymmetrically and retain their template DNA strands. Breast Cancer Res 8:R49 (Pubitemid 44314777)
13. Sleeman KE, Kendrick H, Robertson D, et al. (2007) Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J Cell Biol 176:19-26 (Pubitemid 46041676)
14. Dontu G, Al-Hajj M, Abdallah WM, et al. (2003) Stem cells in normal breast development and breast cancer. Cell Prolif 36(Suppl 1):59-72 (Pubitemid 37521844)
15. Theodoropoulos PA, Polioudaki H, Agelaki S, et al. (2009) Circulating tumor cells with a putative stem cell phenotype in peripheral blood of patients with breast cancer. Cancer Lett 288(1):99-106
16. Aktas B, Tewes M, Fehm T, et al. (2009) Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 11:R46
17. Lu J, Fan T, Zhao Q, et al. (2009) Isolation of circulating epithelial and tumor progenitor cells with an invasive phenotype from breast cancer patients. Int J Cancer 126(3):669-683
18. Balic M, Lin H, Young L, et al. (2006) Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin Cancer Res 12:5615-5621 (Pubitemid 44629587)
19. Phillips TM, McBride WH, Pajonk F (2006) The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 98:1777-1785 (Pubitemid 46017929)
20. Diehn M, Cho RW, Lobo NA, et al. (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458:780-783
21. Li X, Lewis MT, Huang J, et al. (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100:672-679
22. Tanei T, Morimoto K, Shimazu K, 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
23. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100:3983-3988 (Pubitemid 36418143)
24. Ponti D, Costa A, Zaffaroni N, et al. (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65:5506-5511 (Pubitemid 40911148)
25. Ginestier C, Hur MH, Charafe-Jauffret E, 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 (Pubitemid 350056407)
26. Aruffo A, Stamenkovic I, Melnick M, et al. (1990) CD44 is the principal cell surface receptor for hyaluronate. Cell 61:1303-1313 (Pubitemid 20208834)
27. Gunthert U, Hofmann M, Rudy W, et al. (1991) A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell 65:13-24 (Pubitemid 121001209)
28. Herrlich P, Morrison H, Sleeman J, et al. (2000) CD44 acts both as a growth- and invasiveness-promoting molecule and as a tumor-suppressing cofactor. Ann N Y Acad Sci 910:106-118 discussion 118-20
29. Bourguignon LY, Wong G, Earle C, et al. (2010) Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, microRNA-10b expression, and RhoA/RhoC up-regulation, leading to Rho-kinase-associated cytoskeleton activation and breast tumor cell invasion. J Biol Chem 285:36721-36735
30. Brown RL, Reinke LM, Damerow MS, et al. (2011) CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J Clin Invest 121:1064-1074
31. Louderbough JM, Schroeder JA (2011) Understanding the dual nature of CD44 in breast cancer progression. Mol Cancer Res 9:1573-1586
32. Fogel M, Friederichs J, Zeller Y, et al. (1999) CD24 is a marker for human breast carcinoma. Cancer Lett 143:87-94 (Pubitemid 29327194)
33. Baumann P, Cremers N, Kroese F, et al. (2005) CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res 65:10783-10793 (Pubitemid 41715227)
34. Athanassiadou P, Grapsa D, Gonidi M, et al. (2009) CD24 expression has a prognostic impact in breast carcinoma. Pathol Res Pract 205:524-533
35. Sophos NA, Vasiliou V (2003) Aldehyde dehydrogenase gene superfamily: the 2002 update. Chem Biol Interact 143-144:5-22 (Pubitemid 36253575)
36. Chute JP, Muramoto GG, Whitesides J, et al. (2006) Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci U S A 103:11707-11712 (Pubitemid 44182515)
37. Ginestier C, Wicinski J, Cervera N, et al. (2009) Retinoid signaling regulates breast cancer stem cell differentiation. Cell Cycle 8:3297-3302
38. Andrulis IL, Anton-Culver H, Beck J, et al. (2002) Comparison of DNA- and RNA-based methods for detection of truncating BRCA1 mutations. Hum Mutat 20:65-73 (Pubitemid 34747718)
39. Youil R, Kemper BW, Cotton RG (1995) Screening for mutations by enzyme mismatch cleavage with T4 endonuclease VII. Proc Natl Acad Sci U S A 92:87-91
40. Tavassoli T, Devilee P (2003) Pathology and genetics. Tumours of the breast and female genital organs. IARC Press, Lyon
41. Elston CW, Ellis IO (1991) Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 19:403-410
42. Allred DC, Harvey JM, Berardo M, et al. (1998) Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 11:155-168 (Pubitemid 28144151)
43. Harvey JM, Clark GM, Osborne CK, et al. (1999) Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol 17:1474-1481 (Pubitemid 29220854)
44. Mohsin SK, Weiss H, Havighurst T, et al. (2004) Progesterone receptor by immunohistochemistry and clinical outcome in breast cancer: a validation study. Mod Pathol 17:1545-1554 (Pubitemid 39627082)
45. Wolff AC, Hammond ME, Schwartz JN, et al. (2007) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. Arch Pathol Lab Med 131:18-43 (Pubitemid 46174133)
46. Liu CL, Montgomery KD, Natkunam Y, et al. (2005) TMA-Combiner, a simple software tool to permit analysis of replicate cores on tissue microarrays. Mod Pathol 18:1641-1648 (Pubitemid 41670665)
47. Nielsen TO, Hsu FD, Jensen K, et al. (2004) Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 10:5367-5374 (Pubitemid 39100473)
48. Wicha MS, Liu S, Dontu G (2006) Cancer stem cells: an old idea - a paradigm shift. Cancer Res 66:1883-1890 discussion 1895-6
49. Guler G, Balci S, Costinean S, et al. (2012) Stem cell-related markers in primary breast cancers and associated metastatic lesions. Mod Pathol 25:949-955
50. Honeth G, Bendahl PO, Ringner M, et al. (2008) The CD44+/CD24- phenotype is enriched in basal-like breast tumors. Breast Cancer Res 10:R53
51. Abraham BK, Fritz P, McClellan M, et al. (2005) Prevalence of CD44+/CD24-/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin Cancer Res 11:1154-1159 (Pubitemid 40175765)
52. Park SY, Lee HE, Li H, et al. (2010) Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res 16:876-887
53. Giatromanolaki A, Sivridis E, Fiska A, et al. (2011) The CD44+/CD24- phenotype relates to 'triple-negative' state and unfavorable prognosis in breast cancer patients. Med Oncol 28:745-752
54. Ricardo S, Vieira AF, Gerhard R, et al. (2011) Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol 64:937-946
55. Mylona E, Giannopoulou I, Fasomytakis E, et al. (2008) The clinicopathologic and prognostic significance of CD44+/CD24(-/low) and CD44-/CD24+ tumor cells in invasive breast carcinomas. Hum Pathol 39:1096-1102
56. Heerma van Voss MR, van der Groep P, Bart J, et al. (2011) Expression of the stem cell marker ALDH1 in BRCA1 related breast cancer. Cell Oncol (Dordr) 34:3-10
57. Charafe-Jauffret E, Ginestier C, Iovino F, 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
58. Morimoto K, Kim SJ, Tanei T, 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
59. Nalwoga H, Arnes JB, Wabinga H, et al. (2010) Expression of aldehyde dehydrogenase 1 (ALDH1) is associated with basal-like markers and features of aggressive tumours in African breast cancer. Br J Cancer 102:369-375
60. Madjd Z, Ramezani B, Molanae S, et al. (2012) High expression of stem cell marker ALDH1 is associated with reduced BRCA1 in invasive breast carcinomas. Asian Pac J Cancer Prev 13:2973-2978
61. Resetkova E, Reis-Filho JS, Jain RK, et al. (2010) Prognostic impact of ALDH1 in breast cancer: a story of stem cells and tumor microenvironment. Breast Cancer Res Treat 123:97-108
62. Wright MH, Calcagno AM, Salcido CD, et al. (2008) Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res 10:R10
63. Boecker W, Buerger H (2003) Evidence of progenitor cells of glandular and myoepithelial cell lineages in the human adult female breast epithelium: a new progenitor (adult stem) cell concept. Cell Prolif 36(Suppl 1):73-84 (Pubitemid 37521845)
64. Lim E, Vaillant F, Wu D, et al. (2009) Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 15:907-913
65. Slamon DJ, Godolphin W, Jones LA, et al. (1989) Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244:707-712 (Pubitemid 19147683)
66. Goldhirsch A, Wood WC, Gelber RD, et al. (2007) Progress and promise: highlights of the international expert consensus on the primary therapy of early breast cancer 2007. Ann Oncol 18:1133-1144 (Pubitemid 47244357)
67. Neumeister V, Agarwal S, Bordeaux J, et al. (2010) In situ identification of putative cancer stem cells by multiplexing ALDH1, CD44, and cytokeratin identifies breast cancer patients with poor prognosis. Am J Pathol 176:2131-2138
68. Ridolfi RL, Rosen PP, Port A, et al. (1977) Medullary carcinoma of the breast: a clinicopathologic study with 10 year follow-up. Cancer 40:1365-1385 (Pubitemid 8221704)
69. Marginean F, Rakha EA, Ho BC, et al. (2010) Histological features of medullary carcinoma and prognosis in triple-negative basal-like carcinomas of the breast. Mod Pathol 23:1357-1363
70. Quenneville LA, Phillips KA, Ozcelik H, et al. (2002) HER-2/neu status and tumor morphology of invasive breast carcinomas in Ashkenazi women with known BRCA1 mutation status in the Ontario Familial Breast Cancer Registry. Cancer 95:2068-2075 (Pubitemid 35253367)
71. Lakhani SR, Van De Vijver MJ, Jacquemier J, et al. (2002) The pathology of familial breast cancer: predictive value of immunohistochemical markers estrogen receptor, progesterone receptor, HER-2, and p53 in patients with mutations in BRCA1 and BRCA2. J Clin Oncol 20:2310-2318 (Pubitemid 34441658)
72. Liu S, Lachapelle J, Leung S, et al. (2012) CD8+ lymphocyte infiltration is an independent favorable prognostic indicator in basal-like breast cancer. Breast Cancer Res 14:R48
73. West NR, Milne K, Truong PT, et al. (2011) Tumor-infiltrating lymphocytes predict response to anthracycline-based chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res 13:R126
74. Rody A, Holtrich U, Pusztai L, et al. (2009) T-cell metagene predicts a favorable prognosis in estrogen receptor-negative and HER2-positive breast cancers. Breast Cancer Res 11:R15
75. van de Rijn M, Perou CM, Tibshirani R, et al. (2002) Expression of cytokeratins 17 and 5 identifies a group of breast carcinomas with poor clinical outcome. Am J Pathol 161:1991-1996 (Pubitemid 35434844)
76. Mulligan AM, Pinnaduwage D, Bull SB, et al. (2008) Prognostic effect of basal-like breast cancers is time dependent: evidence from tissue microarray studies on a lymph node-negative cohort. Clin Cancer Res 14:4168-4174
77. Dent R, Hanna WM, Trudeau M, et al. (2009) Time to disease recurrence in basal-type breast cancers: effects of tumor size and lymph node status. Cancer 115:4917-4923
78. Blows FM, Driver KE, Schmidt MK, et al. (2010) Subtyping of breast cancer by immunohistochemistry to investigate a relationship between subtype and short and long term survival: a collaborative analysis of data for 10,159 cases from 12 studies. PLoS Med 7:e1000279
79. Kubista M, Rosner M, Kubista E, et al. (2002) Brca1 regulates in vitro differentiation of mammary epithelial cells. Oncogene 21:4747-4756 (Pubitemid 34879450)
80. Furuta S, Jiang X, Gu B, et al. (2005) Depletion of BRCA1 impairs differentiation but enhances proliferation of mammary epithelial cells. Proc Natl Acad Sci U S A 102:9176-9181 (Pubitemid 40923537)
81. Liu S, Ginestier C, Charafe-Jauffret E, et al. (2008) BRCA1 regulates human mammary stem/progenitor cell fate. Proc Natl Acad Sci U S A 105:1680-1685 (Pubitemid 351346574)
82. Molyneux G, Geyer FC, Magnay FA, et al. (2010) BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 7:403-417
83. Turner NC, Reis-Filho JS, Russell AM, et al. (2007) BRCA1 dysfunction in sporadic basal-like breast cancer. Oncogene 26:2126-2132 (Pubitemid 46514749)