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PMID: 27229144 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Whole-organism lineage tracing by combinatorial and cumulative genome editing.

Science (New York, N.Y.) ·Vol. 353 ·No. 6298 ·2016-07-29 ·Pages aaf7907

McKenna A, Findlay GM, Gagnon JA, Horwitz MS, Schier AF, Shendure J

Abstract

Multicellular systems develop from single cells through distinct lineages. However, current lineage-tracing approaches scale poorly to whole, complex organisms. Here, we use genome editing to progressively introduce and accumulate diverse mutations in a DNA barcode over multiple rounds of cell division. The barcode, an array of clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9 target sites, marks cells and enables the elucidation of lineage relationships via the patterns of mutations shared between cells. In cell culture and zebrafish, we show that rates and patterns of editing are tunable and that thousands of lineage-informative barcode alleles can be generated. By sampling hundreds of thousands of cells from individual zebrafish, we find that most cells in adult organs derive from relatively few embryonic progenitors. In future analyses, genome editing of synthetic target arrays for lineage tracing (GESTALT) can be used to generate large-scale maps of cell lineage in multicellular systems for normal development and disease.

MeSH Terms
Animals Bacterial Proteins CRISPR-Associated Protein 9 CRISPR-Cas Systems Cell Division/genetics Cell Lineage Cell Tracking/methods DNA Barcoding, Taxonomic Endonucleases Genetic Engineering/methods Mutation Single-Cell Analysis Stem Cells/cytology,metabolism Zebrafish Zygote
Chemicals
Bacterial Proteins CRISPR-Associated Protein 9 Cas9 protein, Francisella novicida Endonucleases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
McKenna Aaron
Department of Genome Sciences, University of Washington, Seattle, WA, USA.
Findlay Gregory M
Department of Genome Sciences, University of Washington, Seattle, WA, USA.
Gagnon James A
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, USA.
Horwitz Marshall S
Department of Genome Sciences, University of Washington, Seattle, WA, USA. Department of Pathology, University of Washington, Seattle, WA, USA.
Schier Alexander F
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, USA. Center for Brain Science, Harvard University, Cambridge, MA, USA. The Broad Institute of Harvard and MIT, Cambridge, MA, USA. FAS Center for Systems Biology, Harvard University, Cambridge, MA, USA. shendure@uw.edu schier@fas.harvard.edu.
Shendure Jay
Department of Genome Sciences, University of Washington, Seattle, WA, USA. Howard Hughes Medical Institute, Seattle, WA, USA. shendure@uw.edu schier@fas.harvard.edu.
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Article Info
Journal
Science (New York, N.Y.)
Abbr.
Science
ISSN
1095-9203
Published
2016-07-29
Epub
2016-00-26
Pages
aaf7907
Language
English
Region
United States
NLM ID
0404511
PMCID
PMC4967023
Subset
IM
Grants
NIMH NIH HHS · MH105960 · United States
NHLBI NIH HHS · T32HL007312 · United States
NIGMS NIH HHS · GM056211 · United States
NHLBI NIH HHS · T32 HL007312 · United States
NIGMS NIH HHS · R37 GM056211 · United States
NCCDPHP CDC HHS · DP1HG007811 · United States
NIMH NIH HHS · U01 MH105960 · United States
NICHD NIH HHS · R01 HD085905 · United States
NIGMS NIH HHS · R01 GM056211 · United States
Howard Hughes Medical Institute · United States
NICHD NIH HHS · HD085905 · United States
NIGMS NIH HHS · T32 GM007266 · United States
NHGRI NIH HHS · DP1 HG007811 · United States
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