Literature DB >> 33482715

Conserved paradoxical relationships among the evolutionary, structural and expressional features of KRAB zinc-finger proteins reveal their special functional characteristics.

Pan Shen1, Aishi Xu1,2, Yushan Hou1, Huqiang Wang1, Chao Gao1, Fuchu He3, Dong Yang4.   

Abstract

BACKGROUND: One striking feature of the large KRAB domain-containing zinc finger protein (KZFP) family is its rapid evolution, leading to hundreds of member genes with various origination time in a certain mammalian genome. However, a comprehensive genome-wide and across-taxa analysis of the structural and expressional features of KZFPs with different origination time is lacking. This type of analysis will provide valuable clues about the functional characteristics of this special family.
RESULTS: In this study, we found several conserved paradoxical phenomena about this issue. 1) Ordinary young domains/proteins tend to be disordered, but most of KRAB domains are completely structured in 64 representative species across the superclass of Sarcopterygii and most of KZFPs are also highly structured, indicating their rigid and unique structural and functional characteristics; as exceptions, old-zinc-finger-containing KZFPs have relatively disordered KRAB domains and linker regions, contributing to diverse interacting partners and functions. 2) In general, young or highly structured proteins tend to be spatiotemporal specific and have low abundance. However, by integrated analysis of 29 RNA-seq datasets, including 725 samples across early embryonic development, embryonic stem cell differentiation, embryonic and adult organs, tissues in 7 mammals, we found that KZFPs tend to express ubiquitously with medium abundance regardless of evolutionary age and structural disorder degree, indicating the wide functional requirements of KZFPs in various states. 3) Clustering and correlation analysis reveal that there are differential expression patterns across different spatiotemporal states, suggesting the specific-high-expression KZFPs may play important roles in the corresponding states. In particular, part of young-zinc-finger-containing KZFPs are highly expressed in early embryonic development and ESCs differentiation into endoderm or mesoderm. Co-expression analysis revealed that young-zinc-finger-containing KZFPs are significantly enriched in five co-expression modules. Among them, one module, including 13 young-zinc-finger-containing KZFPs, showed an 'early-high and late-low' expression pattern. Further functional analysis revealed that they may function in early embryonic development and ESC differentiation via participating in cell cycle related processes.
CONCLUSIONS: This study shows the conserved and special structural, expressional features of KZFPs, providing new clues about their functional characteristics and potential causes of their rapid evolution.

Entities:  

Keywords:  Evolutionary age; Expression; Function; KZFP; Structure

Year:  2021        PMID: 33482715     DOI: 10.1186/s12860-021-00346-w

Source DB:  PubMed          Journal:  BMC Mol Cell Biol        ISSN: 2661-8850


  70 in total

1.  KRAB zinc finger proteins: an analysis of the molecular mechanisms governing their increase in numbers and complexity during evolution.

Authors:  Camilla Looman; Magnus Abrink; Charlotta Mark; Lars Hellman
Journal:  Mol Biol Evol       Date:  2002-12       Impact factor: 16.240

2.  Coevolution of retroelements and tandem zinc finger genes.

Authors:  James H Thomas; Sean Schneider
Journal:  Genome Res       Date:  2011-07-22       Impact factor: 9.043

3.  KRAB zinc-finger proteins contribute to the evolution of gene regulatory networks.

Authors:  Michaël Imbeault; Pierre-Yves Helleboid; Didier Trono
Journal:  Nature       Date:  2017-03-08       Impact factor: 49.962

Review 4.  Introducing protein intrinsic disorder.

Authors:  Johnny Habchi; Peter Tompa; Sonia Longhi; Vladimir N Uversky
Journal:  Chem Rev       Date:  2014-04-17       Impact factor: 60.622

5.  Evolutionary expansion and divergence in the ZNF91 subfamily of primate-specific zinc finger genes.

Authors:  Aaron T Hamilton; Stuart Huntley; Mary Tran-Gyamfi; Daniel M Baggott; Laurie Gordon; Lisa Stubbs
Journal:  Genome Res       Date:  2006-04-10       Impact factor: 9.043

Review 6.  KRAB zinc finger proteins.

Authors:  Gabriela Ecco; Michael Imbeault; Didier Trono
Journal:  Development       Date:  2017-08-01       Impact factor: 6.868

7.  Meisetz and the birth of the KRAB motif.

Authors:  Zoë Birtle; Chris P Ponting
Journal:  Bioinformatics       Date:  2006-10-10       Impact factor: 6.937

8.  Gain, loss and divergence in primate zinc-finger genes: a rich resource for evolution of gene regulatory differences between species.

Authors:  Katja Nowick; Christopher Fields; Tim Gernat; Derek Caetano-Anolles; Nadezda Kholina; Lisa Stubbs
Journal:  PLoS One       Date:  2011-06-29       Impact factor: 3.240

9.  An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons.

Authors:  Frank M J Jacobs; David Greenberg; Ngan Nguyen; Maximilian Haeussler; Adam D Ewing; Sol Katzman; Benedict Paten; Sofie R Salama; David Haussler
Journal:  Nature       Date:  2014-09-28       Impact factor: 49.962

10.  Adaptive evolution in zinc finger transcription factors.

Authors:  Ryan O Emerson; James H Thomas
Journal:  PLoS Genet       Date:  2009-01-02       Impact factor: 5.917

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