Glycolipid GD3 and GD3 synthase are key drivers for glioblastoma stem cells and tumorigenicity

The cancer stem cells (CSCs) of glioblastoma multiforme (GBM), a grade IV astrocytoma, have been enriched by the expressed marker CD133. However, recent studies have shown that CD133⁻ cells also possess tumor-initiating potential. By analysis of gangliosides on various cells, we show that gangliosid...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 20; pp. 5592 - 5597
Main Authors Yeh, Shih-Chi, Wang, Pao-Yuan, Lou, Yi-Wei, Khoo, Kay-Hooi, Hsiao, Michael, Hsu, Tsui-Ling, Wong, Chi-Huey
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 17.05.2016
Subjects
AC133 Antigen - analysis
Animals
Biological Sciences
Brain cancer
Brain Neoplasms - pathology
Cell Line, Tumor
Cytotoxicity
G(M1) Ganglioside - analysis
Gangliosides - analysis
Gangliosides - physiology
Glioblastoma - chemistry
Glioblastoma - etiology
Glioblastoma - pathology
Humans
Mice
Neoplastic Stem Cells - chemistry
Proto-Oncogene Proteins c-met - metabolism
Sialyltransferases - analysis
Sialyltransferases - physiology
Stem cells
Tumors
gangliosides
GBM
cancer stem cells
ST8SIA1
glycosphingolipids
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Abstract The cancer stem cells (CSCs) of glioblastoma multiforme (GBM), a grade IV astrocytoma, have been enriched by the expressed marker CD133. However, recent studies have shown that CD133⁻ cells also possess tumor-initiating potential. By analysis of gangliosides on various cells, we show that ganglioside D3 (GD3) is overexpressed on eight neurospheres and tumor cells; in combination with CD133, the sorted cells exhibit a higher expression of stemness genes and self-renewal potential; and as few as six cells will form neurospheres and 20–30 cells will grow tumor in mice. Furthermore, GD3 synthase (GD3S) is increased in neurospheres and human GBM tissues, but not in normal brain tissues, and suppression of GD3S results in decreased GBM stem cell (GSC)-associated properties. In addition, a GD3 antibody is shown to induce complement-dependent cytotoxicity against cells expressing GD3 and inhibition of GBM tumor growth in vivo. Our results demonstrate that GD3 and GD3S are highly expressed in GSCs, play a key role in glioblastoma tumorigenicity, and are potential therapeutic targets against GBM.
AbstractList The cancer stem cells (CSCs) of glioblastoma multiforme (GBM), a grade IV astrocytoma, have been enriched by the expressed marker CD133. However, recent studies have shown that CD133(-) cells also possess tumor-initiating potential. By analysis of gangliosides on various cells, we show that ganglioside D3 (GD3) is overexpressed on eight neurospheres and tumor cells; in combination with CD133, the sorted cells exhibit a higher expression of stemness genes and self-renewal potential; and as few as six cells will form neurospheres and 20-30 cells will grow tumor in mice. Furthermore, GD3 synthase (GD3S) is increased in neurospheres and human GBM tissues, but not in normal brain tissues, and suppression of GD3S results in decreased GBM stem cell (GSC)-associated properties. In addition, a GD3 antibody is shown to induce complement-dependent cytotoxicity against cells expressing GD3 and inhibition of GBM tumor growth in vivo. Our results demonstrate that GD3 and GD3S are highly expressed in GSCs, play a key role in glioblastoma tumorigenicity, and are potential therapeutic targets against GBM.The cancer stem cells (CSCs) of glioblastoma multiforme (GBM), a grade IV astrocytoma, have been enriched by the expressed marker CD133. However, recent studies have shown that CD133(-) cells also possess tumor-initiating potential. By analysis of gangliosides on various cells, we show that ganglioside D3 (GD3) is overexpressed on eight neurospheres and tumor cells; in combination with CD133, the sorted cells exhibit a higher expression of stemness genes and self-renewal potential; and as few as six cells will form neurospheres and 20-30 cells will grow tumor in mice. Furthermore, GD3 synthase (GD3S) is increased in neurospheres and human GBM tissues, but not in normal brain tissues, and suppression of GD3S results in decreased GBM stem cell (GSC)-associated properties. In addition, a GD3 antibody is shown to induce complement-dependent cytotoxicity against cells expressing GD3 and inhibition of GBM tumor growth in vivo. Our results demonstrate that GD3 and GD3S are highly expressed in GSCs, play a key role in glioblastoma tumorigenicity, and are potential therapeutic targets against GBM.
Glioblastoma multiforme (GBM) is the most malignant brain tumor. The recurrence or chemoresistance of GBM is attributed to the presence of cancer stem cells (CSCs). Although many studies indicate that CD133 protein is a biomarker for GBM CSC (GSC) enrichment, CD133 is not specific for GSCs and is also present on cancer cells. In this study, we report that ganglioside D3 (GD3) is not only an alternative marker but also an additional marker to CD133 for the identification and enrichment of GSCs. We further prove that the properties of CSCs in GBM are suppressed when GD3 synthase is inhibited, supporting GD3 as a GBM stem cell marker and a promising therapeutic target for GBM treatment. The cancer stem cells (CSCs) of glioblastoma multiforme (GBM), a grade IV astrocytoma, have been enriched by the expressed marker CD133. However, recent studies have shown that CD133 − cells also possess tumor-initiating potential. By analysis of gangliosides on various cells, we show that ganglioside D3 (GD3) is overexpressed on eight neurospheres and tumor cells; in combination with CD133, the sorted cells exhibit a higher expression of stemness genes and self-renewal potential; and as few as six cells will form neurospheres and 20–30 cells will grow tumor in mice. Furthermore, GD3 synthase (GD3S) is increased in neurospheres and human GBM tissues, but not in normal brain tissues, and suppression of GD3S results in decreased GBM stem cell (GSC)-associated properties. In addition, a GD3 antibody is shown to induce complement-dependent cytotoxicity against cells expressing GD3 and inhibition of GBM tumor growth in vivo. Our results demonstrate that GD3 and GD3S are highly expressed in GSCs, play a key role in glioblastoma tumorigenicity, and are potential therapeutic targets against GBM.
The cancer stem cells (CSCs) of glioblastoma multiforme (GBM), a grade IV astrocytoma, have been enriched by the expressed marker CD133. However, recent studies have shown that CD133(-) cells also possess tumor-initiating potential. By analysis of gangliosides on various cells, we show that ganglioside D3 (GD3) is overexpressed on eight neurospheres and tumor cells; in combination with CD133, the sorted cells exhibit a higher expression of stemness genes and self-renewal potential; and as few as six cells will form neurospheres and 20-30 cells will grow tumor in mice. Furthermore, GD3 synthase (GD3S) is increased in neurospheres and human GBM tissues, but not in normal brain tissues, and suppression of GD3S results in decreased GBM stem cell (GSC)-associated properties. In addition, a GD3 antibody is shown to induce complement-dependent cytotoxicity against cells expressing GD3 and inhibition of GBM tumor growth in vivo. Our results demonstrate that GD3 and GD3S are highly expressed in GSCs, play a key role in glioblastoma tumorigenicity, and are potential therapeutic targets against GBM.
The cancer stem cells (CSCs) of glioblastoma multiforme (GBM), a grade IV astrocytoma, have been enriched by the expressed marker CD133. However, recent studies have shown that CD133⁻ cells also possess tumor-initiating potential. By analysis of gangliosides on various cells, we show that ganglioside D3 (GD3) is overexpressed on eight neurospheres and tumor cells; in combination with CD133, the sorted cells exhibit a higher expression of stemness genes and self-renewal potential; and as few as six cells will form neurospheres and 20–30 cells will grow tumor in mice. Furthermore, GD3 synthase (GD3S) is increased in neurospheres and human GBM tissues, but not in normal brain tissues, and suppression of GD3S results in decreased GBM stem cell (GSC)-associated properties. In addition, a GD3 antibody is shown to induce complement-dependent cytotoxicity against cells expressing GD3 and inhibition of GBM tumor growth in vivo. Our results demonstrate that GD3 and GD3S are highly expressed in GSCs, play a key role in glioblastoma tumorigenicity, and are potential therapeutic targets against GBM.
Author Khoo, Kay-Hooi
Yeh, Shih-Chi
Hsiao, Michael
Wong, Chi-Huey
Wang, Pao-Yuan
Hsu, Tsui-Ling
Lou, Yi-Wei
Author_xml – sequence: 1
  givenname: Shih-Chi
  surname: Yeh
  fullname: Yeh, Shih-Chi
  organization: Institute of Biochemistry and Molecular Biology, National Yang-Ming University, Taipei 112, Taiwan
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  givenname: Pao-Yuan
  surname: Wang
  fullname: Wang, Pao-Yuan
  organization: Institute of Biochemical Sciences, National Taiwan University, Taipei 106, Taiwan
– sequence: 3
  givenname: Yi-Wei
  surname: Lou
  fullname: Lou, Yi-Wei
  organization: Genomics Research Center, Academia Sinica, Taipei 115, Taiwan
– sequence: 4
  givenname: Kay-Hooi
  surname: Khoo
  fullname: Khoo, Kay-Hooi
  organization: Institute of Biological Chemistry, Academia Sinica, Taipei 115, Taiwan
– sequence: 5
  givenname: Michael
  surname: Hsiao
  fullname: Hsiao, Michael
  organization: Genomics Research Center, Academia Sinica, Taipei 115, Taiwan
– sequence: 6
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  surname: Hsu
  fullname: Hsu, Tsui-Ling
  organization: Genomics Research Center, Academia Sinica, Taipei 115, Taiwan
– sequence: 7
  givenname: Chi-Huey
  surname: Wong
  fullname: Wong, Chi-Huey
  organization: Genomics Research Center, Academia Sinica, Taipei 115, Taiwan
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27143722$$D View this record in MEDLINE/PubMed
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Keywords gangliosides
GBM
cancer stem cells
ST8SIA1
glycosphingolipids
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Reviewers: X.H., Michigan State University; and V.W., University of Konstanz.
Author contributions: S.-C.Y., Y.-W.L., M.H., T.-L.H., and C.-H.W. designed research; S.-C.Y., P.-Y.W., and Y.-W.L. performed research; S.-C.Y., P.-Y.W., Y.-W.L., K.-H.K., and T.-L.H. analyzed data; S.-C.Y., T.-L.H., and C.-H.W. wrote the paper.
Contributed by Chi-Huey Wong, March 30, 2016 (sent for review January 30, 2016; reviewed by Xuefei Huang and Valentin Wittmann)
1S.-C.Y. and P.-Y.W. contributed equally to this work.
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Snippet The cancer stem cells (CSCs) of glioblastoma multiforme (GBM), a grade IV astrocytoma, have been enriched by the expressed marker CD133. However, recent...
Glioblastoma multiforme (GBM) is the most malignant brain tumor. The recurrence or chemoresistance of GBM is attributed to the presence of cancer stem cells...
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SubjectTerms AC133 Antigen - analysis
Animals
Biological Sciences
Brain cancer
Brain Neoplasms - pathology
Cell Line, Tumor
Cytotoxicity
G(M1) Ganglioside - analysis
Gangliosides - analysis
Gangliosides - physiology
Glioblastoma - chemistry
Glioblastoma - etiology
Glioblastoma - pathology
Humans
Mice
Neoplastic Stem Cells - chemistry
Proto-Oncogene Proteins c-met - metabolism
Sialyltransferases - analysis
Sialyltransferases - physiology
Stem cells
Tumors
Title Glycolipid GD3 and GD3 synthase are key drivers for glioblastoma stem cells and tumorigenicity
URI https://www.jstor.org/stable/26469896
https://www.ncbi.nlm.nih.gov/pubmed/27143722
https://www.proquest.com/docview/1793611198
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https://pubmed.ncbi.nlm.nih.gov/PMC4878508
Volume 113
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