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Application of high-throughput single-nucleus DNA sequencing in pancreatic cancer

Author

Listed:
  • Haochen Zhang

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center)

  • Elias-Ramzey Karnoub

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center)

  • Shigeaki Umeda

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center)

  • Ronan Chaligné

    (Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center)

  • Ignas Masilionis

    (Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center)

  • Caitlin A. McIntyre

    (Memorial Sloan Kettering)

  • Palash Sashittal

    (Princeton University)

  • Akimasa Hayashi

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center
    Kyorin University School of Medicine)

  • Amanda Zucker

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center
    Oregon Health and Science University)

  • Katelyn Mullen

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center)

  • Jungeui Hong

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center)

  • Alvin Makohon-Moore

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center
    Hackensack Meridian Health)

  • Christine A. Iacobuzio-Donahue

    (Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center
    Memorial Sloan Kettering Cancer Center)

Abstract

Despite insights gained by bulk DNA sequencing of cancer it remains challenging to resolve the admixture of normal and tumor cells, and/or of distinct tumor subclones; high-throughput single-cell DNA sequencing circumvents these and brings cancer genomic studies to higher resolution. However, its application has been limited to liquid tumors or a small batch of solid tumors, mainly because of the lack of a scalable workflow to process solid tumor samples. Here we optimize a highly automated nuclei extraction workflow that achieves fast and reliable targeted single-nucleus DNA library preparation of 38 samples from 16 pancreatic ductal adenocarcinoma patients, with an average library yield per sample of 2867 single nuclei. We demonstrate that this workflow not only performs well using low cellularity or low tumor purity samples but reveals genomic evolution patterns of pancreatic ductal adenocarcinoma as well.

Suggested Citation

  • Haochen Zhang & Elias-Ramzey Karnoub & Shigeaki Umeda & Ronan Chaligné & Ignas Masilionis & Caitlin A. McIntyre & Palash Sashittal & Akimasa Hayashi & Amanda Zucker & Katelyn Mullen & Jungeui Hong & A, 2023. "Application of high-throughput single-nucleus DNA sequencing in pancreatic cancer," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36344-z
    DOI: 10.1038/s41467-023-36344-z
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    References listed on IDEAS

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    1. Johannes G. Reiter & Alvin P. Makohon-Moore & Jeffrey M. Gerold & Ivana Bozic & Krishnendu Chatterjee & Christine A. Iacobuzio-Donahue & Bert Vogelstein & Martin A. Nowak, 2017. "Reconstructing metastatic seeding patterns of human cancers," Nature Communications, Nature, vol. 8(1), pages 1-10, April.
    2. Andrew V. Biankin & Nicola Waddell & Karin S. Kassahn & Marie-Claude Gingras & Lakshmi B. Muthuswamy & Amber L. Johns & David K. Miller & Peter J. Wilson & Ann-Marie Patch & Jianmin Wu & David K. Chan, 2012. "Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes," Nature, Nature, vol. 491(7424), pages 399-405, November.
    3. Faiyaz Notta & Michelle Chan-Seng-Yue & Mathieu Lemire & Yilong Li & Gavin W. Wilson & Ashton A. Connor & Robert E. Denroche & Sheng-Ben Liang & Andrew M. K. Brown & Jaeseung C. Kim & Tao Wang & Jared, 2016. "A renewed model of pancreatic cancer evolution based on genomic rearrangement patterns," Nature, Nature, vol. 538(7625), pages 378-382, October.
    4. Kiyomi Morita & Feng Wang & Katharina Jahn & Tianyuan Hu & Tomoyuki Tanaka & Yuya Sasaki & Jack Kuipers & Sanam Loghavi & Sa A. Wang & Yuanqing Yan & Ken Furudate & Jairo Matthews & Latasha Little & C, 2020. "Clonal evolution of acute myeloid leukemia revealed by high-throughput single-cell genomics," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    5. Kiyomi Morita & Feng Wang & Katharina Jahn & Tianyuan Hu & Tomoyuki Tanaka & Yuya Sasaki & Jack Kuipers & Sanam Loghavi & Sa A. Wang & Yuanqing Yan & Ken Furudate & Jairo Matthews & Latasha Little & C, 2020. "Publisher Correction: Clonal evolution of acute myeloid leukemia revealed by high-throughput single-cell genomics," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    6. Darlan C. Minussi & Michael D. Nicholson & Hanghui Ye & Alexander Davis & Kaile Wang & Toby Baker & Maxime Tarabichi & Emi Sei & Haowei Du & Mashiat Rabbani & Cheng Peng & Min Hu & Shanshan Bai & Yu-w, 2021. "Breast tumours maintain a reservoir of subclonal diversity during expansion," Nature, Nature, vol. 592(7853), pages 302-308, April.
    7. Salem Malikic & Katharina Jahn & Jack Kuipers & S. Cenk Sahinalp & Niko Beerenwinkel, 2019. "Integrative inference of subclonal tumour evolution from single-cell and bulk sequencing data," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    8. Jochen Singer & Jack Kuipers & Katharina Jahn & Niko Beerenwinkel, 2018. "Single-cell mutation identification via phylogenetic inference," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    9. Yulei Zhao & Yonina R. Murciano-Goroff & Jenny Y. Xue & Agnes Ang & Jessica Lucas & Trang T. Mai & Arnaud F. Cruz Paula & Anne Y. Saiki & Deanna Mohn & Pragathi Achanta & Ann E. Sisk & Kanika S. Arora, 2021. "Diverse alterations associated with resistance to KRAS(G12C) inhibition," Nature, Nature, vol. 599(7886), pages 679-683, November.
    10. Linde A. Miles & Robert L. Bowman & Tiffany R. Merlinsky & Isabelle S. Csete & Aik T. Ooi & Robert Durruthy-Durruthy & Michael Bowman & Christopher Famulare & Minal A. Patel & Pedro Mendez & Chrysanth, 2020. "Single-cell mutation analysis of clonal evolution in myeloid malignancies," Nature, Nature, vol. 587(7834), pages 477-482, November.
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