Eukaryotic protein domains as functional units of cellular evolution

Jing Jin*, Xueying Xie, Chen Chen, Jin Gyoon Park, Chris Stark, D. Andrew James, Marina Olhovsky, Rune Linding, Yongyi Mao, Tony Pawson

*Corresponding author for this work

Research output: Contribution to journalArticle

88 Citations (Scopus)

Abstract

Modular protein domains are functional units that can be modified through the acquisition of new intrinsic activities or by the formation of novel domain combinations, thereby contributing to the evolution of proteins with new biological properties. Here, we assign proteins to groups with related domain compositions and functional properties, termed "domain clubs," which we use to compare multiple eukaryotic proteomes. This analysis shows that different domain types can take distinct evolutionary trajectories, which correlate with the conservation, gain, expansion, or decay of particular biological processes. Evolutionary jumps are associated with a domain that coordinately acquires a new intrinsic function and enters new domain clubs, thereby providing the modified domain with access to a new cellular microenvironment. We also coordinately analyzed the covalent and noncovalent interactions of different domain types to assess the molecular compartment occupied by each domain. This reveals that specific subsets of domains demarcate particular cellular processes, such as growth factor signaling, chromatin remodeling, apoptotic and inflammatory responses, or vesicular trafficking. We suggest that domains, and the proteins in which they reside, are selected during evolution through reciprocal interactions with protein domains in their local microenvironment. Based on this scheme, we propose a mechanism by which Tudor domains may have evolved to support different modes of epigenetic regulation and suggest a role for the germline group of mammalian Tudor domains in Piwiregulated RNA biology.

Original languageEnglish (US)
JournalScience Signaling
Volume2
Issue number98
DOIs
StatePublished - Nov 24 2009

Fingerprint

Protein Interaction Domains and Motifs
Biological Phenomena
Cellular Microenvironment
Chromatin Assembly and Disassembly
Proteome
Epigenomics
Intercellular Signaling Peptides and Proteins
Proteins
RNA
Chromatin
Conservation
Trajectories
Tudor Domain
Protein Domains
Chemical analysis

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Jin, J., Xie, X., Chen, C., Park, J. G., Stark, C., James, D. A., ... Pawson, T. (2009). Eukaryotic protein domains as functional units of cellular evolution. Science Signaling, 2(98). https://doi.org/10.1126/scisignal.2000546
Jin, Jing ; Xie, Xueying ; Chen, Chen ; Park, Jin Gyoon ; Stark, Chris ; James, D. Andrew ; Olhovsky, Marina ; Linding, Rune ; Mao, Yongyi ; Pawson, Tony. / Eukaryotic protein domains as functional units of cellular evolution. In: Science Signaling. 2009 ; Vol. 2, No. 98.
@article{0cf3ce701b6b4eb9acf59042df4b406c,
title = "Eukaryotic protein domains as functional units of cellular evolution",
abstract = "Modular protein domains are functional units that can be modified through the acquisition of new intrinsic activities or by the formation of novel domain combinations, thereby contributing to the evolution of proteins with new biological properties. Here, we assign proteins to groups with related domain compositions and functional properties, termed {"}domain clubs,{"} which we use to compare multiple eukaryotic proteomes. This analysis shows that different domain types can take distinct evolutionary trajectories, which correlate with the conservation, gain, expansion, or decay of particular biological processes. Evolutionary jumps are associated with a domain that coordinately acquires a new intrinsic function and enters new domain clubs, thereby providing the modified domain with access to a new cellular microenvironment. We also coordinately analyzed the covalent and noncovalent interactions of different domain types to assess the molecular compartment occupied by each domain. This reveals that specific subsets of domains demarcate particular cellular processes, such as growth factor signaling, chromatin remodeling, apoptotic and inflammatory responses, or vesicular trafficking. We suggest that domains, and the proteins in which they reside, are selected during evolution through reciprocal interactions with protein domains in their local microenvironment. Based on this scheme, we propose a mechanism by which Tudor domains may have evolved to support different modes of epigenetic regulation and suggest a role for the germline group of mammalian Tudor domains in Piwiregulated RNA biology.",
author = "Jing Jin and Xueying Xie and Chen Chen and Park, {Jin Gyoon} and Chris Stark and James, {D. Andrew} and Marina Olhovsky and Rune Linding and Yongyi Mao and Tony Pawson",
year = "2009",
month = "11",
day = "24",
doi = "10.1126/scisignal.2000546",
language = "English (US)",
volume = "2",
journal = "Science Signaling",
issn = "1937-9145",
publisher = "American Association for the Advancement of Science",
number = "98",

}

Jin, J, Xie, X, Chen, C, Park, JG, Stark, C, James, DA, Olhovsky, M, Linding, R, Mao, Y & Pawson, T 2009, 'Eukaryotic protein domains as functional units of cellular evolution', Science Signaling, vol. 2, no. 98. https://doi.org/10.1126/scisignal.2000546

Eukaryotic protein domains as functional units of cellular evolution. / Jin, Jing; Xie, Xueying; Chen, Chen; Park, Jin Gyoon; Stark, Chris; James, D. Andrew; Olhovsky, Marina; Linding, Rune; Mao, Yongyi; Pawson, Tony.

In: Science Signaling, Vol. 2, No. 98, 24.11.2009.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Eukaryotic protein domains as functional units of cellular evolution

AU - Jin, Jing

AU - Xie, Xueying

AU - Chen, Chen

AU - Park, Jin Gyoon

AU - Stark, Chris

AU - James, D. Andrew

AU - Olhovsky, Marina

AU - Linding, Rune

AU - Mao, Yongyi

AU - Pawson, Tony

PY - 2009/11/24

Y1 - 2009/11/24

N2 - Modular protein domains are functional units that can be modified through the acquisition of new intrinsic activities or by the formation of novel domain combinations, thereby contributing to the evolution of proteins with new biological properties. Here, we assign proteins to groups with related domain compositions and functional properties, termed "domain clubs," which we use to compare multiple eukaryotic proteomes. This analysis shows that different domain types can take distinct evolutionary trajectories, which correlate with the conservation, gain, expansion, or decay of particular biological processes. Evolutionary jumps are associated with a domain that coordinately acquires a new intrinsic function and enters new domain clubs, thereby providing the modified domain with access to a new cellular microenvironment. We also coordinately analyzed the covalent and noncovalent interactions of different domain types to assess the molecular compartment occupied by each domain. This reveals that specific subsets of domains demarcate particular cellular processes, such as growth factor signaling, chromatin remodeling, apoptotic and inflammatory responses, or vesicular trafficking. We suggest that domains, and the proteins in which they reside, are selected during evolution through reciprocal interactions with protein domains in their local microenvironment. Based on this scheme, we propose a mechanism by which Tudor domains may have evolved to support different modes of epigenetic regulation and suggest a role for the germline group of mammalian Tudor domains in Piwiregulated RNA biology.

AB - Modular protein domains are functional units that can be modified through the acquisition of new intrinsic activities or by the formation of novel domain combinations, thereby contributing to the evolution of proteins with new biological properties. Here, we assign proteins to groups with related domain compositions and functional properties, termed "domain clubs," which we use to compare multiple eukaryotic proteomes. This analysis shows that different domain types can take distinct evolutionary trajectories, which correlate with the conservation, gain, expansion, or decay of particular biological processes. Evolutionary jumps are associated with a domain that coordinately acquires a new intrinsic function and enters new domain clubs, thereby providing the modified domain with access to a new cellular microenvironment. We also coordinately analyzed the covalent and noncovalent interactions of different domain types to assess the molecular compartment occupied by each domain. This reveals that specific subsets of domains demarcate particular cellular processes, such as growth factor signaling, chromatin remodeling, apoptotic and inflammatory responses, or vesicular trafficking. We suggest that domains, and the proteins in which they reside, are selected during evolution through reciprocal interactions with protein domains in their local microenvironment. Based on this scheme, we propose a mechanism by which Tudor domains may have evolved to support different modes of epigenetic regulation and suggest a role for the germline group of mammalian Tudor domains in Piwiregulated RNA biology.

UR - http://www.scopus.com/inward/record.url?scp=75549086174&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=75549086174&partnerID=8YFLogxK

U2 - 10.1126/scisignal.2000546

DO - 10.1126/scisignal.2000546

M3 - Article

VL - 2

JO - Science Signaling

JF - Science Signaling

SN - 1937-9145

IS - 98

ER -