Enrichment of CD44 in basal-type breast cancer correlates with EMT, cancer stem cell gene profile, and prognosis

OncoTargets and Therapy

Volumn 9, Issue , 2016, Pages 431-444

  Xu, Hanxiao ^a   Tian, Yijun ^a   Yuan, Xun ^a   Liu, Yu ^b   Wu, Hua ^a   Liu, Qian ^a   Wu, Gen Sheng ^c   Wu, Kongming ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biomarker; Breast cancer; CD44; Meta analysis; Survival prediction

Indexed keywords

ALDEHYDE DEHYDROGENASE ISOENZYME 1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; HERMES ANTIGEN; KRUPPEL LIKE FACTOR 4; MESSENGER RNA; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROGESTERONE RECEPTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR ZEB1; VIMENTIN;

ARTICLE; BASAL TYPE BREAST CANCER; BREAST CANCER; CANCER PROGNOSIS; CANCER STAGING; CANCER STEM CELL; CANCER SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENETIC DATABASE; HISTOPATHOLOGY; HUMAN; META ANALYSIS; METASTASIS FREE SURVIVAL; MOLECULAR DYNAMICS; OVERALL SURVIVAL; PROTEIN EXPRESSION; PUBLISHING; RECURRENCE FREE SURVIVAL; SURVIVAL RATE; SURVIVAL TIME;

EID: 84955493784     PISSN: None     EISSN: 11786930     Source Type: Journal    
DOI: 10.2147/OTT.S97192     Document Type: Article

References (92)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65(1):5-29.
2. Radenkovic S, Milosevic Z, Konjevic G, et al. Lactate dehydrogenase, catalase, and superoxide dismutase in tumor tissue of breast cancer patients in respect to mammographic findings. Cell Biochem Biophys. 2013;66(2):287-295.
3. Radenkovic S, Konjevic G, Jurisic V, et al. Values of MMP-2 and MMP-9 in tumor tissue of basal-like breast cancer patients. Cell Biochem Biophys. 2014;68(1):143-152.
4. Stankovic S, Konjevic G, Gopcevic K, et al. Activity of MMP-2 and MMP-9 in sera of breast cancer patients. Pathol Res Pract. 2010;206(4): 241-247.
5. Screaton GR, Caceres JF, Mayeda A, et al. Identification and characterization of three members of the human SR family of pre-mRNA splicing factors. EMBO J. 1995;14(17):4336-4349.
6. van der Windt GJ, Schouten M, Zeerleder S, et al. CD44 is protective during hyperoxia-induced lung injury. Am J Respir Cell Mol Biol. 2011; 44(3):377-383.
7. Xu H, Tian Y, Yuan X, et al. The role of CD44 in epithelial-mesenchymal transition and cancer development. Onco Targets Ther. 2015;8: 3783-3792.
8. Erb U, Megaptche AP, Gu X, et al. CD44 standard and CD44v10 isoform expression on leukemia cells distinctly influences niche embedding of hematopoietic stem cells. J Hematol Oncol. 2014;7:29.
9. Naor D, Sionov RV, Ish-Shalom D. CD44: structure, function, and association with the malignant process. Adv Cancer Res. 1997;71: 241-319.
10. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol. 2003;4(1):33-45.
11. Zoller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer. 2011;11(4):254-267.
12. Basakran NS. CD44 as a potential diagnostic tumor marker. Saudi Med J. 2015;36(3):273-279.
13. Dalerba P, Dylla SJ, Park IK, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A. 2007; 104(24):10158-10163.
14. Du L, Wang H, He L, et al. CD44 is of functional importance for colorectal cancer stem cells. Clin Cancer Res. 2008;14(21):6751-6760.
15. Santoyo-Ramos P, Likhatcheva M, Garcia-Zepeda EA, et al. Hypoxia-inducible factors modulate the stemness and malignancy of colon cancer cells by playing opposite roles in canonical Wnt signaling. PLoS One. 2014;9(11):e112580.
16. Wu K, Ning Z, Zeng J, et al. Silibinin inhibits beta-catenin/ZEB1 signaling and suppresses bladder cancer metastasis via dual-blocking epithelial-mesenchymal transition and stemness. Cell Signal. 2013; 25(12):2625-2633.
17. Yu D, Shin HS, Lee YS, et al. miR-106b modulates cancer stem cell characteristics through TGF-beta/Smad signaling in CD44-positive gastric cancer cells. Lab Invest. 2014;94(12):1370-1381.
18. Xie G, Yao Q, Liu Y, et al. IL-6-induced epithelial-mesenchymal transition promotes the generation of breast cancer stem-like cells analogous to mammosphere cultures. Int J Oncol. 2012;40(4): 1171-1179.
19. Uchino M, Kojima H, Wada K, et al. Nuclear beta-catenin and CD44 upregulation characterize invasive cell populations in non-aggressive MCF-7 breast cancer cells. BMC Cancer. 2010;10:414.
20. Cho Y, Lee HW, Kang HG, et al. Cleaved CD44 intracellular domain supports activation of stemness factors and promotes tumorigenesis of breast cancer. Oncotarget. 2015;6(11):8709-8721.
21. Desmedt C, Piette F, Loi S, et al. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res. 2007;13(11):3207-3214.
22. Dan T, Hewitt SM, Ohri N, et al. CD44 is prognostic for overall survival in the NCI randomized trial on breast conservation with 25 year follow-up. Breast Cancer Res Treat. 2014;143(1):11-18.
23. Tomao F, Papa A, Zaccarelli E, et al. Triple-negative breast cancer: new perspectives for targeted therapies. Onco Targets Ther. 2015;8: 177-193.
24. Jang MH, Kim HJ, Kim EJ, et al. Expression of epithelial-mesenchymal transition-related markers in triple-negative breast cancer: ZEB1 as a potential biomarker for poor clinical outcome. Hum Pathol. 2015; 46(9):1267-1274.
25. Ma F, Li H, Wang H, et al. Enriched CD44(+)/CD24(-) population drives the aggressive phenotypes presented in triple-negative breast cancer (TNBC). Cancer Lett. 2014;353(2):153-159.
26. Tierney JF, Stewart LA, Ghersi D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.
27. Heikkinen T, Greco D, Pelttari LM, et al. Variants on the promoter region of PTEN affect breast cancer progression and patient survival. Breast Cancer Res. 2011;13(6):R130.
28. Terunuma A, Putluri N, Mishra P, et al. MYC-driven accumulation of 2-hydroxyglutarate is associated with breast cancer prognosis. J Clin Invest. 2014;124(1):398-412.
29. Sircoulomb F, Bekhouche I, Finetti P, et al. Genome profiling of ERBB2-amplified breast cancers. BMC Cancer. 2010;10:539.
30. Clarke C, Madden SF, Doolan P, et al. Correlating transcriptional networks to breast cancer survival: a large-scale coexpression analysis. Carcinogenesis. 2013;34(10):2300-2308.
31. Ma XJ, Dahiya S, Richardson E, et al. Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res. 2009;11(1):R7.
32. Hatzis C, Pusztai L, Valero V, et al. A genomic predictor of response and survival following taxane-anthracycline chemotherapy for invasive breast cancer. JAMA. 2011;305(18):1873-1881.
33. Tofigh A, Suderman M, Paquet ER, et al. The prognostic ease and difficulty of invasive breast carcinoma. Cell Rep. 2014;9(1): 129-142.
34. Kao KJ, Chang KM, Hsu HC, et al. Correlation of microarray-based breast cancer molecular subtypes and clinical outcomes: implications for treatment optimization. BMC Cancer. 2011;11:143.
35. Minn AJ, Gupta GP, Siegel PM, et al. Genes that mediate breast cancer metastasis to lung. Nature. 2005;436(7050):518-524.
36. Desmedt C, Di Leo A, de Azambuja E, et al. Multifactorial approach to predicting resistance to anthracyclines. J Clin Oncol. 2011;29(12): 1578-1586.
37. Schmidt M, Bohm D, von Torne C, et al. The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res. 2008;68(13):5405-5413.
38. Nagalla S, Chou JW, Willingham MC, et al. Interactions between immunity, proliferation and molecular subtype in breast cancer prognosis. Genome Biol. 2013;14(4):R34.
39. Loi S, Haibe-Kains B, Desmedt C, et al. Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J Clin Oncol. 2007;25(10):1239-1246.
40. Dedeurwaerder S, Desmedt C, Calonne E, et al. DNA methylation profiling reveals a predominant immune component in breast cancers. EMBO Mol Med. 2011;3(12):726-741.
41. Miller LD, Smeds J, George J, et al. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc Natl Acad Sci U S A. 2005; 102(38):13550-13555.
42. Symmans WF, Hatzis C, Sotiriou C, et al. Genomic index of sensitivity to endocrine therapy for breast cancer. J Clin Oncol. 2010;28(27): 4111-4119.
43. Pawitan Y, Bjohle J, Amler L, et al. Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res. 2005; 7(6):R953-R964.
44. Wang Y, Klijn JG, Zhang Y, et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet. 2005;365(9460):671-679.
45. Hu Z, Fan C, Livasy C, et al. A compact VEGF signature associated with distant metastases and poor outcomes. BMC Med. 2009;7:9.
46. Hennessy BT, Gonzalez-Angulo AM, Stemke-Hale K, et al. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res. 2009;69(10):4116-4124.
47. Bild AH, Yao G, Chang JT, et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature. 2006; 439(7074):353-357.
48. Minn AJ, Gupta GP, Padua D, et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc Natl Acad Sci U S A. 2007;104(16):6740-6745.
49. Adamczyk A, Niemiec JA, Ambicka A, et al. CD44/CD24 as potential prognostic markers in node-positive invasive ductal breast cancer patients treated with adjuvant chemotherapy. J Mol Histol. 2014;45(1): 35-45.
50. Wu Y, Sarkissyan M, Elshimali Y, et al. Triple negative breast tumors in African-American and Hispanic/Latina women are high in CD44+, low in CD24+, and have loss of PTEN. PLoS One. 2013;8(10): e78259.
51. Bernardi MA, Logullo AF, Pasini FS, et al. Prognostic significance of CD24 and claudin-7 immunoexpression in ductal invasive breast cancer. Oncol Rep. 2012;27(1):28-38.
52. Uchoa Dde M, Graudenz MS, Callegari-Jacques SM, et al. Expression of cancer stem cell markers in basal and penta-negative breast carcinomas -a study of a series of triple-negative tumors. Pathol Res Pract. 2014; 210(7):432-439.
53. Ahmed MA, Aleskandarany MA, Rakha EA, et al. A CD44(-)/CD24(+) phenotype is a poor prognostic marker in early invasive breast cancer. Breast Cancer Res Treat. 2012;133(3):979-995.
54. Wang Z, Shi Q, Wang Z, et al. Clinicopathologic correlation of cancer stem cell markers CD44, CD24, VEGF and HIF-1alpha in ductal carcinoma in situ and invasive ductal carcinoma of breast: an immunohistochemistry-based pilot study. Pathol Res Pract. 2011; 207(8):505-513.
55. 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(11):937-946.
56. Kim HJ, Kim MJ, Ahn SH, et al. Different prognostic significance of CD24 and CD44 expression in breast cancer according to hormone receptor status. Breast. 2011;20(1):78-85.
57. Giatromanolaki A, Sivridis E, Fiska A, et al. The CD44+/CD24- phenotype relates to ‘triple-negative’ state and unfavorable prognosis in breast cancer patients. Med Oncol. 2011;28(3):745-752.
58. Looi LM, Cheah PL, Zhao W, et al. CD44 expression and axillary lymph node metastasis in infiltrating ductal carcinoma of the breast. Malays J Pathol. 2006;28(2):83-86.
59. Han Z, Chen Z, Zheng R, et al. Clinicopathological significance of CD133 and CD44 expression in infiltrating ductal carcinoma and their relationship to angiogenesis. World J Surg Oncol. 2015;13:56.
60. Smith AD, Roda D, Yap TA. Strategies for modern biomarker and drug development in oncology. J Hematol Oncol. 2014;7:70.
61. Montgomery N, Hill A, McFarlane S, et al. CD44 enhances invasion of basal-like breast cancer cells by upregulating serine protease and collagen-degrading enzymatic expression and activity. Breast Cancer Res. 2012;14(3):R84.
62. Park J, Schlederer M, Schreiber M, et al. AF1q is a novel TCF7 co-factor which activates CD44 and promotes breast cancer metastasis. Oncotarget. 2015;6(24):20697-20710.
63. Nam K, Oh S, Lee KM, et al. CD44 regulates cell proliferation, migration, and invasion via modulation of c-Src transcription in human breast cancer cells. Cell Signal. 2015;27(9):1882-1894.
64. So JY, Smolarek AK, Salerno DM, et al. Targeting CD44-STAT3 signaling by Gemini vitamin D analog leads to inhibition of invasion in basal-like breast cancer. PLoS One. 2013;8(1):e54020.
65. Boulbes DR, Chauhan GB, Jin Q, et al. CD44 expression contributes to trastuzumab resistance in HER2-positive breast cancer cells. Breast Cancer Res Treat. 2015;151(3):501-513.
66. Wei X, Xu M, Wei Y, et al. The addition of rituximab to CHOP therapy alters the prognostic significance of CD44 expression. J Hematol Oncol. 2014;7:34.
67. Cheng Y, Tao L, Xu J, et al. CD44/cellular prion protein interact in multidrug resistant breast cancer cells and correlate with responses to neoadjuvant chemotherapy in breast cancer patients. Mol Carcinog. 2014;53(9):686-697.
68. Ma L, Jiang T. Clinical implications of Ezrin and CD44 coexpression in breast cancer. Oncol Rep. 2013;30(4):1899-1905.
69. Yang C, He Y, Zhang H, et al. Selective killing of breast cancer cells expressing activated CD44 using CD44 ligand-coated nanoparticles in vitro and in vivo. Oncotarget. 2015;6(17):15283-15296.
70. Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000;406(6797):747-752.
71. Sorlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001;98(19):10869-10874.
72. Camerini A, Donati S, Viacava P, et al. Evaluation of HER2 and p53 expression in predicting response to docetaxel-based first-line chemotherapy in advanced breast cancer. J Exp Clin Canc Res. 2011;30:38.
73. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490(7418):61-70.
74. McFarlane S, Coulter JA, Tibbits P, et al. CD44 increases the efficiency of distant metastasis of breast cancer. Oncotarget. 2015;6(13): 11465-11476.
75. Bolodeoku J, Yoshida K, Sugino T, et al. CD44 expression in human breast cancer cell lines is related to oestrogen receptor (ER) status and confluency in vitro. Biochem Soc Trans. 1997;25(2):356S.
76. Sorlie T, Tibshirani R, Parker J, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A. 2003;100(14):8418-8423.
77. Heldin P, Basu K, Kozlova I, et al. HAS2 and CD44 in breast tumorigenesis. Adv Cancer Res. 2014;123:211-229.
78. Cho SH, Park YS, Kim HJ, et al. CD44 enhances the epithelial-mesenchymal transition in association with colon cancer invasion. Int J Oncol. 2012;41(1):211-218.
79. Fernando J, Malfettone A, Cepeda EB, et al. A mesenchymal-like phenotype and expression of CD44 predict lack of apoptotic response to sorafenib in liver tumor cells. Int J Cancer. 2015;136(4):E161-E172.
80. Schulenburg A, Blatt K, Cerny-Reiterer S, et al. Cancer stem cells in basic science and in translational oncology: can we translate into clinical application? J Hematol Oncol. 2015;8(1):16.
81. Yin X, Zhang BH, Zheng SS, et al. Coexpression of gene Oct4 and Nanog initiates stem cell characteristics in hepatocellular carcinoma and promotes epithelial-mesenchymal transition through activation of Stat3/Snail signaling. J Hematol Oncol. 2015;8:23.
82. Witzel I, Milde-Langosch K, Schmidt M, et al. Role of urokinase plasminogen activator and plasminogen activator inhibitor mRNA expression as prognostic factors in molecular subtypes of breast cancer. Onco Targets Ther. 2014;7:2205-2213.
83. Wu K, Chen K, Wang C, et al. Cell fate factor DACH1 represses YB-1-mediated oncogenic transcription and translation. Cancer Res. 2014; 74(3):829-839.
84. Wu K, Li Z, Cai S, et al. EYA1 phosphatase function is essential to drive breast cancer cell proliferation through cyclin D1. Cancer Res. 2013; 73(14):4488-4499.
85. Liu Y, Han N, Zhou S, et al. The DACH/EYA/SIX gene network and its role in tumor initiation and progression. Int J Cancer. Epub 2015 Apr 9.
86. Yan S, Jiao X, Li K, et al. The impact of IGF-1R expression on the outcomes of patients with breast cancer: a meta-analysis. Onco Targets Ther. 2015;8:279-287.
87. Han T, Liu Z, Li H, et al. High expression of UBD correlates with epirubicin resistance and indicates poor prognosis in triple-negative breast cancer. Onco Targets Ther. 2015;8:1643-1649.
88. Dong MJ, Wang LB, Jiang ZN, et al. The transcription factor KLF4 as an independent predictive marker for pathologic complete remission in breast cancer neoadjuvant chemotherapy: a case-control study. Onco Targets Ther. 2014;7:1963-1969.
89. Chekhun SV, Zadvorny TV, Tymovska YO, et al. CyrillicD44+/CD24- markers of cancer stem cells in patients with breast cancer of different molecular subtypes. Exp Oncol. 2015;37(1):58-63.
90. Loh TJ, Moon H, Cho S, et al. CD44 alternative splicing and hnRNP A1 expression are associated with the metastasis of breast cancer. Oncol Rep. 2015;34(3):1231-1238.
91. Martin TA, Jiang WG. Evaluation of the expression of stem cell markers in human breast cancer reveals a correlation with clinical progression and metastatic disease in ductal carcinoma. Oncol Rep. 2014;31(1): 262-272.
92. De Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer. 2013;13(2):97-110.