Reconstructing Progenitor State Hierarchy and Dynamics Using Lineage Barcoding Data

Overview

Journal Methods Mol Biol

Specialty Molecular Biology

Date 2025 Jan 2

PMID 39745641

Authors

Weixiang Fang

Yi Yang

Hongkai Ji

Reza Kalhor

Affiliations

Soon will be listed here.

Abstract

Measurements of cell phylogeny based on natural or induced mutations, known as lineage barcodes, in conjunction with molecular phenotype have become increasingly feasible for a large number of single cells. In this chapter, we delve into Quantitative Fate Mapping (QFM) and its computational pipeline, which enables the interrogation of the dynamics of progenitor cells and their fate restriction during development. The methods described here include inferring cell phylogeny with the Phylotime model, and reconstructing progenitor state hierarchy, commitment time, population size, and commitment bias with the ICE-FASE algorithm. Evaluation of adequate sampling based on progenitor state coverage statistics is emphasized for interpreting the QFM results. Overall, this chapter describes a general framework for characterizing the dynamics of cell fate changes using lineage barcoding data.

References

Garcia-Marques J, Espinosa-Medina I, Lee T . The art of lineage tracing: From worm to human. Prog Neurobiol. 2020; 199:101966. DOI: 10.1016/j.pneurobio.2020.101966. View

Wagner D, Weinreb C, Collins Z, Briggs J, Megason S, Klein A . Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo. Science. 2018; 360(6392):981-987. PMC: 6083445. DOI: 10.1126/science.aar4362. View

Biddy B, Kong W, Kamimoto K, Guo C, Waye S, Sun T . Single-cell mapping of lineage and identity in direct reprogramming. Nature. 2018; 564(7735):219-224. PMC: 6635140. DOI: 10.1038/s41586-018-0744-4. View

McKenna A, Findlay G, Gagnon J, Horwitz M, Schier A, Shendure J . Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science. 2016; 353(6298):aaf7907. PMC: 4967023. DOI: 10.1126/science.aaf7907. View

Spanjaard B, Hu B, Mitic N, Olivares-Chauvet P, Janjuha S, Ninov N . Simultaneous lineage tracing and cell-type identification using CRISPR-Cas9-induced genetic scars. Nat Biotechnol. 2018; 36(5):469-473. PMC: 5942543. DOI: 10.1038/nbt.4124. View

Liu X, Weng W, He L, Zhou B . Genetic recording of in vivo cell proliferation by ProTracer. Nat Protoc. 2023; 18(7):2349-2373. DOI: 10.1038/s41596-023-00833-8. View

Bowling S, Sritharan D, Osorio F, Nguyen M, Cheung P, Rodriguez-Fraticelli A . An Engineered CRISPR-Cas9 Mouse Line for Simultaneous Readout of Lineage Histories and Gene Expression Profiles in Single Cells. Cell. 2020; 181(7):1693-1694. PMC: 7530571. DOI: 10.1016/j.cell.2020.06.018. View

Kalhor R, Mali P, Church G . Rapidly evolving homing CRISPR barcodes. Nat Methods. 2016; 14(2):195-200. PMC: 5322472. DOI: 10.1038/nmeth.4108. View

Alemany A, Florescu M, Baron C, Peterson-Maduro J, van Oudenaarden A . Whole-organism clone tracing using single-cell sequencing. Nature. 2018; 556(7699):108-112. DOI: 10.1038/nature25969. View

10.

Espinosa-Medina I, Feliciano D, Belmonte-Mateos C, Linda Miyares R, Garcia-Marques J, Foster B . TEMPO enables sequential genetic labeling and manipulation of vertebrate cell lineages. Neuron. 2022; 111(3):345-361.e10. DOI: 10.1016/j.neuron.2022.10.035. View

11.

Bizzotto S, Dou Y, Ganz J, Doan R, Kwon M, Bohrson C . Landmarks of human embryonic development inscribed in somatic mutations. Science. 2021; 371(6535):1249-1253. PMC: 8170505. DOI: 10.1126/science.abe1544. View

12.

Spencer Chapman M, Ranzoni A, Myers B, Williams N, Coorens T, Mitchell E . Lineage tracing of human development through somatic mutations. Nature. 2021; 595(7865):85-90. DOI: 10.1038/s41586-021-03548-6. View

13.

Coorens T, Moore L, Robinson P, Sanghvi R, Christopher J, Hewinson J . Extensive phylogenies of human development inferred from somatic mutations. Nature. 2021; 597(7876):387-392. DOI: 10.1038/s41586-021-03790-y. View

14.

Salipante S, Horwitz M . Phylogenetic fate mapping. Proc Natl Acad Sci U S A. 2006; 103(14):5448-53. PMC: 1414797. DOI: 10.1073/pnas.0601265103. View

15.

Baron C, van Oudenaarden A . Unravelling cellular relationships during development and regeneration using genetic lineage tracing. Nat Rev Mol Cell Biol. 2019; 20(12):753-765. DOI: 10.1038/s41580-019-0186-3. View

16.

Wagner D, Klein A . Lineage tracing meets single-cell omics: opportunities and challenges. Nat Rev Genet. 2020; 21(7):410-427. PMC: 7307462. DOI: 10.1038/s41576-020-0223-2. View

17.

Fang W, Bell C, Sapirstein A, Asami S, Leeper K, Zack D . Quantitative fate mapping: A general framework for analyzing progenitor state dynamics via retrospective lineage barcoding. Cell. 2022; 185(24):4604-4620.e32. PMC: 9708097. DOI: 10.1016/j.cell.2022.10.028. View

18.

FITCH W, MARGOLIASH E . Construction of phylogenetic trees. Science. 1967; 155(3760):279-84. DOI: 10.1126/science.155.3760.279. View

19.

Felsenstein J . Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981; 17(6):368-76. DOI: 10.1007/BF01734359. View

20.

Leeper K, Kalhor K, Vernet A, Graveline A, Church G, Mali P . Lineage barcoding in mice with homing CRISPR. Nat Protoc. 2021; 16(4):2088-2108. PMC: 8049957. DOI: 10.1038/s41596-020-00485-y. View