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Cell, Tumor, and Stem Cell Biology

Identification and Characterization of Ovarian Cancer-Initiating Cells from Primary Human Tumors

Shu Zhang, Curt Balch, Michael W. Chan, Hung-Cheng Lai, Daniela Matei, Jeanne M. Schilder, Pearlly S. Yan, Tim H-M. Huang and Kenneth P. Nephew
Shu Zhang
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Curt Balch
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Michael W. Chan
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Hung-Cheng Lai
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Daniela Matei
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Jeanne M. Schilder
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Pearlly S. Yan
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Tim H-M. Huang
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Kenneth P. Nephew
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DOI: 10.1158/0008-5472.CAN-08-0364 Published June 2008
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Abstract

The objective of this study was to identify and characterize a self-renewing subpopulation of human ovarian tumor cells (ovarian cancer-initiating cells, OCICs) fully capable of serial propagation of their original tumor phenotype in animals. Ovarian serous adenocarcinomas were disaggregated and subjected to growth conditions selective for self-renewing, nonadherent spheroids previously shown to derive from tissue stem cells. To affirm the existence of OCICs, xenoengraftment of as few as 100 dissociated spheroid cells allowed full recapitulation of the original tumor (grade 2/grade 3 serous adenocarcinoma), whereas >105 unselected cells remained nontumorigenic. Stemness properties of OCICs (under stem cell–selective conditions) were further established by cell proliferation assays and reverse transcription–PCR, demonstrating enhanced chemoresistance to the ovarian cancer chemotherapeutics cisplatin or paclitaxel and up-regulation of stem cell markers (Bmi-1, stem cell factor, Notch-1, Nanog, nestin, ABCG2, and Oct-4) compared with parental tumor cells or OCICs under differentiating conditions. To identify an OCIC cell surface phenotype, spheroid immunostaining showed significant up-regulation of the hyaluronate receptor CD44 and stem cell factor receptor CD117 (c-kit), a tyrosine kinase oncoprotein. Similar to sphere-forming OCICs, injection of only 100 CD44+CD117+ cells could also serially propagate their original tumors, whereas 105 CD44−CD117− cells remained nontumorigenic. Based on these findings, we assert that epithelial ovarian cancers derive from a subpopulation of CD44+CD117+ cells, thus representing a possible therapeutic target for this devastating disease. [Cancer Res 2008;68(11):4311–20]

  • ovarian cancer
  • cancer stem cells
  • drug resistance

Footnotes

  • Note: Supplementary data for this article are available at Cancer Research Online (http://cancerres.aacrjournals.org/).

  • Received January 30, 2008.
  • Revision received March 31, 2008.
  • Accepted April 1, 2008.
  • ©2008 American Association for Cancer Research.
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Cancer Research: 68 (11)
June 2008
Volume 68, Issue 11
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Identification and Characterization of Ovarian Cancer-Initiating Cells from Primary Human Tumors
Shu Zhang, Curt Balch, Michael W. Chan, Hung-Cheng Lai, Daniela Matei, Jeanne M. Schilder, Pearlly S. Yan, Tim H-M. Huang and Kenneth P. Nephew
Cancer Res June 1 2008 (68) (11) 4311-4320; DOI: 10.1158/0008-5472.CAN-08-0364

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Identification and Characterization of Ovarian Cancer-Initiating Cells from Primary Human Tumors
Shu Zhang, Curt Balch, Michael W. Chan, Hung-Cheng Lai, Daniela Matei, Jeanne M. Schilder, Pearlly S. Yan, Tim H-M. Huang and Kenneth P. Nephew
Cancer Res June 1 2008 (68) (11) 4311-4320; DOI: 10.1158/0008-5472.CAN-08-0364
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