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Unravelling biology and shifting paradigms in cancer with single-cell sequencing. ​

Literature Information ​

DOI10.1038/nrc.2017.58
PMID28835719
JournalNature reviews. Cancer
Impact Factor66.8
JCR QuartileQ1
Publication Year2017
Times Cited224
Keywordssingle-cell sequencing, cancer biology, tumoral heterogeneity, genome evolution, disease relapse
Literature TypeJournal Article, Review, Research Support, Non-U.S. Gov't
ISSN1474-175X
Pages557-569
Issue17(9)
AuthorsTimour Baslan, James Hicks

TL;DR ​

This opinion article highlights the pivotal role of single cells in cancer biology, emphasizing that single-cell sequencing technologies have overcome historical limitations in cancer research. The authors suggest that these advancements will enhance our understanding of genetic heterogeneity, cancer evolution, and the mechanisms behind disease relapse and metastasis, ultimately unraveling the complexities of cancer.

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single-cell sequencing · cancer biology · tumoral heterogeneity · genome evolution · disease relapse

Abstract ​

The fundamental operative unit of a cancer is the genetically and epigenetically innovative single cell. Whether proliferating or quiescent, in the primary tumour mass or disseminated elsewhere, single cells govern the parameters that dictate all facets of the biology of cancer. Thus, single-cell analyses provide the ultimate level of resolution in our quest for a fundamental understanding of this disease. Historically, this quest has been hampered by technological shortcomings. In this Opinion article, we argue that the rapidly evolving field of single-cell sequencing has unshackled the cancer research community of these shortcomings. From furthering an elemental understanding of intra-tumoural genetic heterogeneity and cancer genome evolution to illuminating the governing principles of disease relapse and metastasis, we posit that single-cell sequencing promises to unravel the biology of all facets of this disease.

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Primary Questions Addressed ​

  1. How does single-cell sequencing enhance our understanding of intra-tumoural genetic heterogeneity compared to traditional bulk sequencing methods?
  2. What specific technological advancements in single-cell sequencing have contributed to overcoming previous research limitations in cancer biology?
  3. In what ways can single-cell sequencing inform the development of targeted therapies for different cancer subtypes?
  4. How might the insights gained from single-cell sequencing influence future cancer treatment protocols and patient management strategies?
  5. What are the potential implications of single-cell sequencing findings on our understanding of cancer relapse and metastasis mechanisms?

Key Findings ​

Key Insights ​

1. Research Background and Purpose: Cancer is fundamentally driven by single cells that exhibit genetic and epigenetic variations. These cells, whether actively proliferating or in a quiescent state, play a crucial role in determining the biological characteristics of tumors. Traditional research methods have struggled to provide a comprehensive understanding of cancer due to technological limitations in analyzing single cells. The purpose of this article is to highlight how advancements in single-cell sequencing technologies are transforming cancer research by providing unprecedented resolution in studying the complexities of cancer biology, particularly focusing on intra-tumoral heterogeneity, genome evolution, disease relapse, and metastasis.

2. Main Methods and Findings: The article discusses the advancements in single-cell sequencing techniques that enable researchers to dissect the genetic and epigenetic landscape of individual cancer cells. By utilizing these methods, researchers can gain insights into the diversity present within a tumor, revealing how different cells contribute to tumor behavior, survival, and response to therapy. Key findings include a deeper understanding of genetic heterogeneity within tumors, the mechanisms behind cancer genome evolution, and the factors influencing disease relapse and metastatic spread. This level of detail is crucial for identifying specific cellular populations that may drive aggressive cancer phenotypes or therapeutic resistance.

3. Core Conclusions: The authors conclude that single-cell sequencing is a pivotal technology in cancer research, providing a more refined understanding of the disease's biology. By enabling the investigation of individual cells, this approach allows researchers to identify unique genetic and epigenetic profiles, offering insights into how cancers evolve and adapt over time. This knowledge can lead to the identification of novel therapeutic targets and biomarkers, ultimately improving patient outcomes.

4. Research Significance and Impact: The implications of this research are profound, as it not only enhances our understanding of cancer at a fundamental level but also shifts the paradigm in how we approach cancer diagnosis and treatment. With single-cell sequencing, researchers and clinicians can move towards personalized medicine, tailoring treatments based on the specific cellular makeup of a patient’s tumor. This innovation could lead to more effective interventions and improved management of cancer, addressing challenges such as treatment resistance and disease recurrence. The article emphasizes that the ongoing evolution of single-cell technologies will continue to reshape our strategies in combating cancer, making it a crucial area of focus for future research and clinical applications.

References ​

  1. Analyzing tumor heterogeneity and driver genes in single myeloid leukemia cells with SBCapSeq. - Karen M Mann;Justin Y Newberg;Michael A Black;Devin J Jones;Felipe Amaya-Manzanares;Liliana Guzman-Rojas;Takahiro Kodama;Jerrold M Ward;Alistair G Rust;Louise van der Weyden;Christopher Chin Kuan Yew;Jill L Waters;Marco L Leung;Keith Rogers;Susan M Rogers;Leslie A McNoe;Luxmanan Selvanesan;Nicholas Navin;Nancy A Jenkins;Neal G Copeland;Michael B Mann - Nature biotechnology (2016)
  2. Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution. - Peter Eirew;Adi Steif;Jaswinder Khattra;Gavin Ha;Damian Yap;Hossein Farahani;Karen Gelmon;Stephen Chia;Colin Mar;Adrian Wan;Emma Laks;Justina Biele;Karey Shumansky;Jamie Rosner;Andrew McPherson;Cydney Nielsen;Andrew J L Roth;Calvin Lefebvre;Ali Bashashati;Camila de Souza;Celia Siu;Radhouane Aniba;Jazmine Brimhall;Arusha Oloumi;Tomo Osako;Alejandra Bruna;Jose L Sandoval;Teresa Algara;Wendy Greenwood;Kaston Leung;Hongwei Cheng;Hui Xue;Yuzhuo Wang;Dong Lin;Andrew J Mungall;Richard Moore;Yongjun Zhao;Julie Lorette;Long Nguyen;David Huntsman;Connie J Eaves;Carl Hansen;Marco A Marra;Carlos Caldas;Sohrab P Shah;Samuel Aparicio - Nature (2015)
  3. Single-cell epigenomics: techniques and emerging applications. - Omer Schwartzman;Amos Tanay - Nature reviews. Genetics (2015)
  4. A Multiplexed Single-Cell CRISPR Screening Platform Enables Systematic Dissection of the Unfolded Protein Response. - Britt Adamson;Thomas M Norman;Marco Jost;Min Y Cho;James K Nuñez;Yuwen Chen;Jacqueline E Villalta;Luke A Gilbert;Max A Horlbeck;Marco Y Hein;Ryan A Pak;Andrew N Gray;Carol A Gross;Atray Dixit;Oren Parnas;Aviv Regev;Jonathan S Weissman - Cell (2016)
  5. EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing. - Joshua M Francis;Cheng-Zhong Zhang;Cecile L Maire;Joonil Jung;Veronica E Manzo;Viktor A Adalsteinsson;Heather Homer;Sam Haidar;Brendan Blumenstiel;Chandra Sekhar Pedamallu;Azra H Ligon;J Christopher Love;Matthew Meyerson;Keith L Ligon - Cancer discovery (2014)
  6. Rapid phenotypic and genomic change in response to therapeutic pressure in prostate cancer inferred by high content analysis of single circulating tumor cells. - Angel E Dago;Asya Stepansky;Anders Carlsson;Madelyn Luttgen;Jude Kendall;Timour Baslan;Anand Kolatkar;Michael Wigler;Kelly Bethel;Mitchell E Gross;James Hicks;Peter Kuhn - PloS one (2014)
  7. Mutations in regulators of the epigenome and their connections to global chromatin patterns in cancer. - Christoph Plass;Stefan M Pfister;Anders M Lindroth;Olga Bogatyrova;Rainer Claus;Peter Lichter - Nature reviews. Genetics (2013)
  8. The future is now: single-cell genomics of bacteria and archaea. - Paul C Blainey - FEMS microbiology reviews (2013)
  9. Computational and analytical challenges in single-cell transcriptomics. - Oliver Stegle;Sarah A Teichmann;John C Marioni - Nature reviews. Genetics (2015)
  10. The cancer genome. - Michael R Stratton;Peter J Campbell;P Andrew Futreal - Nature (2009)

Literatures Citing This Work ​

  1. Closing the Genotype-Phenotype Loop for Precision Medicine. - Calum A MacRae;Christine E Seidman - Circulation (2017)
  2. Nothing in cancer makes sense except…. - Mel Greaves - BMC biology (2018)
  3. Isoform-level gene expression patterns in single-cell RNA-sequencing data. - Trung Nghia Vu;Quin F Wills;Krishna R Kalari;Nifang Niu;Liewei Wang;Yudi Pawitan;Mattias Rantalainen - Bioinformatics (Oxford, England) (2018)
  4. Defining Cell Identity with Single-Cell Omics. - Laura Mincarelli;Ashleigh Lister;James Lipscombe;Iain C Macaulay - Proteomics (2018)
  5. Taking Systems Medicine to Heart. - Kalliopi Trachana;Rhishikesh Bargaje;Gustavo Glusman;Nathan D Price;Sui Huang;Leroy E Hood - Circulation research (2018)
  6. Power in Numbers: Single-Cell RNA-Seq Strategies to Dissect Complex Tissues. - Kenneth D Birnbaum - Annual review of genetics (2018)
  7. [Advances on Recognizing and Managing Tumor Heterogeneity]. - Rui Zhong;Hui Li;Shuang Zhang;Jingjing Liu;Ying Cheng - Zhongguo fei ai za zhi = Chinese journal of lung cancer (2018)
  8. Quantification of somatic mutation flow across individual cell division events by lineage sequencing. - Yehuda Brody;Robert J Kimmerling;Yosef E Maruvka;David Benjamin;Juniper J Elacqua;Nicholas J Haradhvala;Jaegil Kim;Kent W Mouw;Kristjana Frangaj;Amnon Koren;Gad Getz;Scott R Manalis;Paul C Blainey - Genome research (2018)
  9. Translocation-Related Sarcomas. - Kenji Nakano;Shunji Takahashi - International journal of molecular sciences (2018)
  10. Single-Cell Applications of Next-Generation Sequencing. - Naishitha Anaparthy;Yu-Jui Ho;Luciano Martelotto;Molly Hammell;James Hicks - Cold Spring Harbor perspectives in medicine (2019)

... (214 more literatures)

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