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The evolution of human cells in terms of protein innovation

The evolution of human cells in terms of protein innovation
The evolution of human cells in terms of protein innovation

Humans are composed of hundreds of cell types. As the genomic DNA of each somatic cell is identical, cell type is determined by what is expressed and when. Until recently, little has been reported about the determinants of human cell identity, particularly from the joint perspective of gene evolution and expression. Here, we chart the evolutionary past of all documented human cell types via the collective histories of proteins, the principal product of gene expression. FANTOM5 data provide cell-type-specific digital expression of human protein-coding genes and the SUPERFAMILY resource is used to provide protein domain annotation. The evolutionary epoch in which each protein was created is inferred by comparison with domain annotation of all other completely sequenced genomes. Studying the distribution across epochs of genes expressed in each cell type reveals insights into human cellular evolution in terms of protein innovation. For each cell type, its history of protein innovation is charted based on the genes it expresses. Combining the histories of all cell types enables us to create a timeline of cell evolution. This timeline identifies the possibility that our common ancestor Coelomata (cavity-forming animals) provided the innovation required for the innate immune system, whereas cells which now form the brain of human have followed a trajectory of continually accumulating novel proteins since Opisthokonta (boundary of animals and fungi). We conclude that exaptation of existing domain architectures into new contexts is the dominant source of cell-type-specific domain architectures.

Eukaryotic Cells, Evolution, Molecular, Humans, Immunity, Innate, Phylogeny, Protein Structure, Tertiary, Proteins/chemistry, Sequence Analysis, Protein, Transcriptome
1537-1719
1364-74
Sardar, Adam J.
5792acdf-ef01-4d60-9482-ad4948b36683
Oates, Matt E.
c90996e2-2ae0-4784-9633-a1db986b1831
Fang, Hai
58424580-2d92-4db2-934f-4c393989cea9
Forrest, Alistair R.R.
b7b11839-91f7-4543-907d-d0c1c138111a
Kawaji, Hideya
b41d4dc8-fa4b-4f56-b400-9c8f222415a9
Gough, Julian
019ed039-9fd4-45d6-aa7a-12a8fcf7245c
Rackham, Owen J.L.
8122eb1f-6e9f-4da5-90e1-ce108ccbbcbf
FANTOM Consortium
Sardar, Adam J.
5792acdf-ef01-4d60-9482-ad4948b36683
Oates, Matt E.
c90996e2-2ae0-4784-9633-a1db986b1831
Fang, Hai
58424580-2d92-4db2-934f-4c393989cea9
Forrest, Alistair R.R.
b7b11839-91f7-4543-907d-d0c1c138111a
Kawaji, Hideya
b41d4dc8-fa4b-4f56-b400-9c8f222415a9
Gough, Julian
019ed039-9fd4-45d6-aa7a-12a8fcf7245c
Rackham, Owen J.L.
8122eb1f-6e9f-4da5-90e1-ce108ccbbcbf

FANTOM Consortium (2014) The evolution of human cells in terms of protein innovation. Molecular Biology and Evolution, 31 (6), 1364-74. (doi:10.1093/molbev/mst139).

Record type: Article

Abstract

Humans are composed of hundreds of cell types. As the genomic DNA of each somatic cell is identical, cell type is determined by what is expressed and when. Until recently, little has been reported about the determinants of human cell identity, particularly from the joint perspective of gene evolution and expression. Here, we chart the evolutionary past of all documented human cell types via the collective histories of proteins, the principal product of gene expression. FANTOM5 data provide cell-type-specific digital expression of human protein-coding genes and the SUPERFAMILY resource is used to provide protein domain annotation. The evolutionary epoch in which each protein was created is inferred by comparison with domain annotation of all other completely sequenced genomes. Studying the distribution across epochs of genes expressed in each cell type reveals insights into human cellular evolution in terms of protein innovation. For each cell type, its history of protein innovation is charted based on the genes it expresses. Combining the histories of all cell types enables us to create a timeline of cell evolution. This timeline identifies the possibility that our common ancestor Coelomata (cavity-forming animals) provided the innovation required for the innate immune system, whereas cells which now form the brain of human have followed a trajectory of continually accumulating novel proteins since Opisthokonta (boundary of animals and fungi). We conclude that exaptation of existing domain architectures into new contexts is the dominant source of cell-type-specific domain architectures.

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More information

e-pub ahead of print date: 29 March 2014
Published date: June 2014
Additional Information: © The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Keywords: Eukaryotic Cells, Evolution, Molecular, Humans, Immunity, Innate, Phylogeny, Protein Structure, Tertiary, Proteins/chemistry, Sequence Analysis, Protein, Transcriptome

Identifiers

Local EPrints ID: 446819
URI: http://eprints.soton.ac.uk/id/eprint/446819
ISSN: 1537-1719
PURE UUID: 1f0ac656-0373-43d7-bf63-2a1114d31048
ORCID for Owen J.L. Rackham: ORCID iD orcid.org/0000-0002-4390-0872

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Date deposited: 23 Feb 2021 17:32
Last modified: 24 Feb 2021 02:58

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Contributors

Author: Adam J. Sardar
Author: Matt E. Oates
Author: Hai Fang
Author: Alistair R.R. Forrest
Author: Hideya Kawaji
Author: Julian Gough
Corporate Author: FANTOM Consortium

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