IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36344-z.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36344-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-36344-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Etienne Sollier & Jack Kuipers & Koichi Takahashi & Niko Beerenwinkel & Katharina Jahn, 2023. "COMPASS: joint copy number and mutation phylogeny reconstruction from amplicon single-cell sequencing data," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Ayşegül Erdem & Silvia Marin & Diego A. Pereira-Martins & Marjan Geugien & Alan Cunningham & Maurien G. Pruis & Isabel Weinhäuser & Albert Gerding & Barbara M. Bakker & Albertus T. J. Wierenga & Eduar, 2022. "Inhibition of the succinyl dehydrogenase complex in acute myeloid leukemia leads to a lactate-fuelled respiratory metabolic vulnerability," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Aleksandr Ianevski & Kristen Nader & Kyriaki Driva & Wojciech Senkowski & Daria Bulanova & Lidia Moyano-Galceran & Tanja Ruokoranta & Heikki Kuusanmäki & Nemo Ikonen & Philipp Sergeev & Markus Vähä-Ko, 2024. "Single-cell transcriptomes identify patient-tailored therapies for selective co-inhibition of cancer clones," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Peng Dai & Lucia Ruojia Wu & Sherry Xi Chen & Michael Xiangjiang Wang & Lauren Yuxuan Cheng & Jinny Xuemeng Zhang & Pengying Hao & Weijie Yao & Jabra Zarka & Ghayas C. Issa & Lawrence Kwong & David Yu, 2021. "Calibration-free NGS quantitation of mutations below 0.01% VAF," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    5. Xiang Ge Luo & Jack Kuipers & Niko Beerenwinkel, 2023. "Joint inference of exclusivity patterns and recurrent trajectories from tumor mutation trees," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    6. Sebastien Martinez & Shifei Wu & Michael Geuenich & Ahmad Malik & Ramona Weber & Tristan Woo & Amy Zhang & Gun Ho Jang & Dzana Dervovic & Khalid N. Al-Zahrani & Ricky Tsai & Nassima Fodil & Philippe G, 2024. "In vivo CRISPR screens reveal SCAF1 and USP15 as drivers of pancreatic cancer," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Chunyang Bao & Richard W. Tourdot & Gregory J. Brunette & Chip Stewart & Lili Sun & Hideo Baba & Masayuki Watanabe & Agoston T. Agoston & Kunal Jajoo & Jon M. Davison & Katie S. Nason & Gad Getz & Ken, 2023. "Genomic signatures of past and present chromosomal instability in Barrett’s esophagus and early esophageal adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    8. David Lähnemann & Johannes Köster & Ute Fischer & Arndt Borkhardt & Alice C. McHardy & Alexander Schönhuth, 2021. "Accurate and scalable variant calling from single cell DNA sequencing data with ProSolo," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    9. Cheryl A. C. Peretz & Vanessa E. Kennedy & Anushka Walia & Cyrille L. Delley & Andrew Koh & Elaine Tran & Iain C. Clark & Corey E. Hayford & Chris D’Amato & Yi Xue & Kristina M. Fontanez & Aaron A. Ma, 2024. "Multiomic single cell sequencing identifies stemlike nature of mixed phenotype acute leukemia," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. Zicheng Wang & Yunong Xia & Lauren Mills & Athanasios N. Nikolakopoulos & Nicole Maeser & Scott M. Dehm & Jason M. Sheltzer & Ruping Sun, 2024. "Evolving copy number gains promote tumor expansion and bolster mutational diversification," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Brooks A. Benard & Logan B. Leak & Armon Azizi & Daniel Thomas & Andrew J. Gentles & Ravindra Majeti, 2021. "Clonal architecture predicts clinical outcomes and drug sensitivity in acute myeloid leukemia," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    12. Seong-Hwan Jun & Hosein Toosi & Jeff Mold & Camilla Engblom & Xinsong Chen & Ciara O’Flanagan & Michael Hagemann-Jensen & Rickard Sandberg & Samuel Aparicio & Johan Hartman & Andrew Roth & Jens Lagerg, 2023. "Reconstructing clonal tree for phylo-phenotypic characterization of cancer using single-cell transcriptomics," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Humberto Contreras-Trujillo & Jiya Eerdeng & Samir Akre & Du Jiang & Jorge Contreras & Basia Gala & Mary C. Vergel-Rodriguez & Yeachan Lee & Aparna Jorapur & Areen Andreasian & Lisa Harton & Charles S, 2021. "Deciphering intratumoral heterogeneity using integrated clonal tracking and single-cell transcriptome analyses," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    14. Chi Zhou & Wenxin Li & Zhenxing Liang & Xianrui Wu & Sijing Cheng & Jianhong Peng & Kaixuan Zeng & Weihao Li & Ping Lan & Xin Yang & Li Xiong & Ziwei Zeng & Xiaobin Zheng & Liang Huang & Wenhua Fan & , 2024. "Mutant KRAS-activated circATXN7 fosters tumor immunoescape by sensitizing tumor-specific T cells to activation-induced cell death," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    15. Maria E. Monberg & Heather Geiger & Jaewon J. Lee & Roshan Sharma & Alexander Semaan & Vincent Bernard & Justin Wong & Fang Wang & Shaoheng Liang & Daniel B. Swartzlander & Bret M. Stephens & Matthew , 2022. "Occult polyclonality of preclinical pancreatic cancer models drives in vitro evolution," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    16. Adam C. Weiner & Marc J. Williams & Hongyu Shi & Ignacio Vázquez-García & Sohrab Salehi & Nicole Rusk & Samuel Aparicio & Sohrab P. Shah & Andrew McPherson, 2024. "Inferring replication timing and proliferation dynamics from single-cell DNA sequencing data," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    17. Jinhyun Kim & Sungsik Kim & Huiran Yeom & Seo Woo Song & Kyoungseob Shin & Sangwook Bae & Han Suk Ryu & Ji Young Kim & Ahyoun Choi & Sumin Lee & Taehoon Ryu & Yeongjae Choi & Hamin Kim & Okju Kim & Yu, 2023. "Barcoded multiple displacement amplification for high coverage sequencing in spatial genomics," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    18. Dan Lu & Yuan Chen & Min Jiang & Jie Wang & Yiting Li & Keke Ma & Wenqiao Sun & Xing Zheng & Jianxun Qi & Wenjing Jin & Yu Chen & Yan Chai & Catherine W. H. Zhang & Hao Liang & Shuguang Tan & George F, 2023. "KRAS G12V neoantigen specific T cell receptor for adoptive T cell therapy against tumors," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    19. Diletta Fontana & Ilaria Crespiatico & Valentina Crippa & Federica Malighetti & Matteo Villa & Fabrizio Angaroni & Luca De Sano & Andrea Aroldi & Marco Antoniotti & Giulio Caravagna & Rocco Piazza & A, 2023. "Evolutionary signatures of human cancers revealed via genomic analysis of over 35,000 patients," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    20. Hidenori Kitai & Philip H. Choi & Yu C. Yang & Jacob A. Boyer & Adele Whaley & Priya Pancholi & Claire Thant & Jason Reiter & Kevin Chen & Vladimir Markov & Hirokazu Taniguchi & Rui Yamaguchi & Hiromi, 2024. "Combined inhibition of KRASG12C and mTORC1 kinase is synergistic in non-small cell lung cancer," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36344-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.