Stage-specific embryonic antigen-3 (SSEA-3) and β3GalT5 are cancer specific and significant markers for breast cancer stem cells

The discovery of cancer stem cells (CSCs), which are responsible for self-renewal and tumor growth in heterogeneous cancer tissues, has stimulated interests in developing new cancer therapies and early diagnosis. However, the markers currently used for isolation of CSCs are often not selective enoug...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 4; pp. 960 - 965
Main Authors Cheung, Sarah K. C., Chuang, Po-Kai, Huang, Han-Wen, Hwang-Verslues, Wendy W., Cho, Candy Hsin-Hua, Yang, Wen-Bin, Shen, Chia-Ning, Hsiao, Michael, Hsu, Tsui-Ling, Chang, Chuan-Fa, Wong, Chi-Huey
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 26.01.2016
National Acad Sciences
Subjects
Animals
Antigens, Tumor-Associated, Carbohydrate - analysis
Apoptosis
Base Sequence
Biological Sciences
Biomarkers, Tumor - analysis
Breast Neoplasms - pathology
Cell Line, Tumor
Female
Galactosyltransferases - analysis
Humans
Mice
Molecular Sequence Data
Neoplastic Stem Cells - chemistry
Stage-Specific Embryonic Antigens - analysis
globo-series
glycolipids
cancer-specific
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Abstract The discovery of cancer stem cells (CSCs), which are responsible for self-renewal and tumor growth in heterogeneous cancer tissues, has stimulated interests in developing new cancer therapies and early diagnosis. However, the markers currently used for isolation of CSCs are often not selective enough to enrich CSCs for the study of this special cell population. Here we show that the breast CSCs isolated with CD44⁺CD24-/loSSEA-3⁺ or ESAhiPROCRhiSSEA-3⁺ markers had higher tumorigenicity than those with conventional markers in vitro and in vivo. As few as 10 cells with CD44⁺CD24-/loSSEA-3⁺ formed tumor in mice, compared with more than 100 cells with CD44⁺CD24-/lo. Suppression of SSEA-3 expression by knockdown of the gene encoding β-1,3-galactosyltransferase 5 (β3GalT5) in the globo-series pathway, led to apoptosis in cancer cells specifically but had no effect on normal cells. This finding is further supported by the analysis of SSEA-3 and the two related globo-series epitopes SSEA4 and globo-H in stem cells (embryonic stem cells and induced pluripotent stem cells) and various normal and cancer cells, and by the antibody approach to target the globo-series glycans and the late-stage clinical trials of a breast cancer vaccine.
AbstractList The discovery of cancer stem cells (CSCs), which are responsible for self-renewal and tumor growth in heterogeneous cancer tissues, has stimulated interests in developing new cancer therapies and early diagnosis. However, the markers currently used for isolation of CSCs are often not selective enough to enrich CSCs for the study of this special cell population. Here we show that the breast CSCs isolated with CD44(+)CD24(-/lo)SSEA-3(+) or ESA(hi)PROCR(hi)SSEA-3(+) markers had higher tumorigenicity than those with conventional markers in vitro and in vivo. As few as 10 cells with CD44(+)CD24(-/lo)SSEA-3(+) formed tumor in mice, compared with more than 100 cells with CD44(+)CD24(-/lo). Suppression of SSEA-3 expression by knockdown of the gene encoding β-1,3-galactosyltransferase 5 (β3GalT5) in the globo-series pathway, led to apoptosis in cancer cells specifically but had no effect on normal cells. This finding is further supported by the analysis of SSEA-3 and the two related globo-series epitopes SSEA4 and globo-H in stem cells (embryonic stem cells and induced pluripotent stem cells) and various normal and cancer cells, and by the antibody approach to target the globo-series glycans and the late-stage clinical trials of a breast cancer vaccine.
Cancer stem cells are cancer cells with self-renewal and tumor-growth properties and are important targets for development of anticancer therapy. We have found breast cancer stem cells can be enriched by stage-specific embryonic antigen 3 (SSEA-3) and known protein markers (CD24 and CD44), and as few as 10 such enriched cells can develop tumor in mice. Also, the enzyme galactosyltransferase (β3GalT5) for the biosynthesis of SSEA-3 is expressed in breast cancer stem cells and cancer cells but not in normal cells, and both SSEA-3 and β3GalT5 are shown to be essential for cancer cell survival. These findings have led to the development of a new anticancer strategy with a proof of principle shown in this and previous studies. The discovery of cancer stem cells (CSCs), which are responsible for self-renewal and tumor growth in heterogeneous cancer tissues, has stimulated interests in developing new cancer therapies and early diagnosis. However, the markers currently used for isolation of CSCs are often not selective enough to enrich CSCs for the study of this special cell population. Here we show that the breast CSCs isolated with CD44 + CD24 -/lo SSEA-3 + or ESA hi PROCR hi SSEA-3 + markers had higher tumorigenicity than those with conventional markers in vitro and in vivo. As few as 10 cells with CD44 + CD24 -/lo SSEA-3 + formed tumor in mice, compared with more than 100 cells with CD44 + CD24 -/lo . Suppression of SSEA-3 expression by knockdown of the gene encoding β-1,3-galactosyltransferase 5 (β3GalT5) in the globo-series pathway, led to apoptosis in cancer cells specifically but had no effect on normal cells. This finding is further supported by the analysis of SSEA-3 and the two related globo-series epitopes SSEA4 and globo-H in stem cells (embryonic stem cells and induced pluripotent stem cells) and various normal and cancer cells, and by the antibody approach to target the globo-series glycans and the late-stage clinical trials of a breast cancer vaccine.
The discovery of cancer stem cells (CSCs), which are responsible for self-renewal and tumor growth in heterogeneous cancer tissues, has stimulated interests in developing new cancer therapies and early diagnosis. However, the markers currently used for isolation of CSCs are often not selective enough to enrich CSCs for the study of this special cell population. Here we show that the breast CSCs isolated with CD44(+)CD24(-/lo)SSEA-3(+) or ESA(hi)PROCR(hi)SSEA-3(+) markers had higher tumorigenicity than those with conventional markers in vitro and in vivo. As few as 10 cells with CD44(+)CD24(-/lo)SSEA-3(+) formed tumor in mice, compared with more than 100 cells with CD44(+)CD24(-/lo). Suppression of SSEA-3 expression by knockdown of the gene encoding β-1,3-galactosyltransferase 5 (β3GalT5) in the globo-series pathway, led to apoptosis in cancer cells specifically but had no effect on normal cells. This finding is further supported by the analysis of SSEA-3 and the two related globo-series epitopes SSEA4 and globo-H in stem cells (embryonic stem cells and induced pluripotent stem cells) and various normal and cancer cells, and by the antibody approach to target the globo-series glycans and the late-stage clinical trials of a breast cancer vaccine.The discovery of cancer stem cells (CSCs), which are responsible for self-renewal and tumor growth in heterogeneous cancer tissues, has stimulated interests in developing new cancer therapies and early diagnosis. However, the markers currently used for isolation of CSCs are often not selective enough to enrich CSCs for the study of this special cell population. Here we show that the breast CSCs isolated with CD44(+)CD24(-/lo)SSEA-3(+) or ESA(hi)PROCR(hi)SSEA-3(+) markers had higher tumorigenicity than those with conventional markers in vitro and in vivo. As few as 10 cells with CD44(+)CD24(-/lo)SSEA-3(+) formed tumor in mice, compared with more than 100 cells with CD44(+)CD24(-/lo). Suppression of SSEA-3 expression by knockdown of the gene encoding β-1,3-galactosyltransferase 5 (β3GalT5) in the globo-series pathway, led to apoptosis in cancer cells specifically but had no effect on normal cells. This finding is further supported by the analysis of SSEA-3 and the two related globo-series epitopes SSEA4 and globo-H in stem cells (embryonic stem cells and induced pluripotent stem cells) and various normal and cancer cells, and by the antibody approach to target the globo-series glycans and the late-stage clinical trials of a breast cancer vaccine.
The discovery of cancer stem cells (CSCs), which are responsible for self-renewal and tumor growth in heterogeneous cancer tissues, has stimulated interests in developing new cancer therapies and early diagnosis. However, the markers currently used for isolation of CSCs are often not selective enough to enrich CSCs for the study of this special cell population. Here we show that the breast CSCs isolated with CD44⁺CD24-/loSSEA-3⁺ or ESAhiPROCRhiSSEA-3⁺ markers had higher tumorigenicity than those with conventional markers in vitro and in vivo. As few as 10 cells with CD44⁺CD24-/loSSEA-3⁺ formed tumor in mice, compared with more than 100 cells with CD44⁺CD24-/lo. Suppression of SSEA-3 expression by knockdown of the gene encoding β-1,3-galactosyltransferase 5 (β3GalT5) in the globo-series pathway, led to apoptosis in cancer cells specifically but had no effect on normal cells. This finding is further supported by the analysis of SSEA-3 and the two related globo-series epitopes SSEA4 and globo-H in stem cells (embryonic stem cells and induced pluripotent stem cells) and various normal and cancer cells, and by the antibody approach to target the globo-series glycans and the late-stage clinical trials of a breast cancer vaccine.
Author Huang, Han-Wen
Hwang-Verslues, Wendy W.
Cho, Candy Hsin-Hua
Chuang, Po-Kai
Shen, Chia-Ning
Hsiao, Michael
Cheung, Sarah K. C.
Yang, Wen-Bin
Wong, Chi-Huey
Hsu, Tsui-Ling
Chang, Chuan-Fa
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Keywords globo-series
glycolipids
cancer-specific
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1S.K.C.C. and P.-K.C. contributed equally to this work.
Contributed by Chi-Huey Wong, November 22, 2015 (sent for review October 5, 2015; reviewed by Sabine Flitsch and Peng George Wang)
Author contributions: S.K.C.C., P.-K.C., M.H., T.-L.H., and C.-H.W. designed research; S.K.C.C., P.-K.C., H.-W.H., W.W.H.-V., and W.-B.Y. performed research; C.H.-H.C. and C.-N.S. contributed new reagents/analytic tools; S.K.C.C., P.-K.C., T.-L.H., C.-F.C., and C.-H.W. analyzed data; and S.K.C.C., T.-L.H., and C.-H.W. wrote the paper.
Reviewers: S.F., The University of Manchester; and P.G.W., Georgia State University.
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Snippet The discovery of cancer stem cells (CSCs), which are responsible for self-renewal and tumor growth in heterogeneous cancer tissues, has stimulated interests in...
Cancer stem cells are cancer cells with self-renewal and tumor-growth properties and are important targets for development of anticancer therapy. We have found...
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SubjectTerms Animals
Antigens, Tumor-Associated, Carbohydrate - analysis
Apoptosis
Base Sequence
Biological Sciences
Biomarkers, Tumor - analysis
Breast Neoplasms - pathology
Cell Line, Tumor
Female
Galactosyltransferases - analysis
Humans
Mice
Molecular Sequence Data
Neoplastic Stem Cells - chemistry
Stage-Specific Embryonic Antigens - analysis
Title Stage-specific embryonic antigen-3 (SSEA-3) and β3GalT5 are cancer specific and significant markers for breast cancer stem cells
URI https://www.jstor.org/stable/26467517
http://www.pnas.org/content/113/4/960.abstract
https://www.ncbi.nlm.nih.gov/pubmed/26677875
https://www.proquest.com/docview/1761077773
https://pubmed.ncbi.nlm.nih.gov/PMC4743801
Volume 113
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