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Identification of Distinct Tumor Subpopulations in Lung Adenocarcinoma via Single-Cell RNA-seq

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Listed:
  • Jae-Woong Min
  • Woo Jin Kim
  • Jeong A Han
  • Yu-Jin Jung
  • Kyu-Tae Kim
  • Woong-Yang Park
  • Hae-Ock Lee
  • Sun Shim Choi

Abstract

Single-cell sequencing, which is used to detect clinically important tumor subpopulations, is necessary for understanding tumor heterogeneity. Here, we analyzed transcriptomic data obtained from 34 single cells from human lung adenocarcinoma (LADC) patient-derived xenografts (PDXs). To focus on the intrinsic transcriptomic signatures of these tumors, we filtered out genes that displayed extensive expression changes following xenografting and cell culture. Then, we performed clustering analysis using co-regulated gene modules rather than individual genes to minimize read drop-out errors associated with single-cell sequencing. This combined approach revealed two distinct intra-tumoral subgroups that were primarily distinguished by the gene module G64. The G64 module was predominantly composed of cell-cycle genes. E2F1 was found to be the transcription factor that most likely mediates the expression of the G64 module in single LADC cells. Interestingly, the G64 module also indicated inter-tumoral heterogeneity based on its association with patient survival and other clinical variables such as smoking status and tumor stage. Taken together, these results demonstrate the feasibility of single-cell RNA sequencing and the strength of our analytical pipeline for the identification of tumor subpopulations.

Suggested Citation

  • Jae-Woong Min & Woo Jin Kim & Jeong A Han & Yu-Jin Jung & Kyu-Tae Kim & Woong-Yang Park & Hae-Ock Lee & Sun Shim Choi, 2015. "Identification of Distinct Tumor Subpopulations in Lung Adenocarcinoma via Single-Cell RNA-seq," PLOS ONE, Public Library of Science, vol. 10(8), pages 1-17, August.
  • Handle: RePEc:plo:pone00:0135817
    DOI: 10.1371/journal.pone.0135817
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    References listed on IDEAS

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    1. Gerard I. Evan & Karen H. Vousden, 2001. "Proliferation, cell cycle and apoptosis in cancer," Nature, Nature, vol. 411(6835), pages 342-348, May.
    2. Yong Wang & Jill Waters & Marco L. Leung & Anna Unruh & Whijae Roh & Xiuqing Shi & Ken Chen & Paul Scheet & Selina Vattathil & Han Liang & Asha Multani & Hong Zhang & Rui Zhao & Franziska Michor & Fun, 2014. "Clonal evolution in breast cancer revealed by single nucleus genome sequencing," Nature, Nature, vol. 512(7513), pages 155-160, August.
    3. Philippe L. Bedard & Aaron R. Hansen & Mark J. Ratain & Lillian L. Siu, 2013. "Tumour heterogeneity in the clinic," Nature, Nature, vol. 501(7467), pages 355-364, September.
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