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Metazoan evolution of the armadillo repeat superfamily

Ismail Sahin Gül (UGent) , Paco Hulpiau (UGent) , Yvan Saeys (UGent) and Frans Van Roy (UGent)
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Abstract
The superfamily of armadillo repeat proteins is a fascinating archetype of modular-binding proteins involved in various fundamental cellular processes, including cell-cell adhesion, cytoskeletal organization, nuclear import, and molecular signaling. Despite their diverse functions, they all share tandem armadillo (ARM) repeats, which stack together to form a conserved three-dimensional structure. This superhelical armadillo structure enables them to interact with distinct partners by wrapping around them. Despite the important functional roles of this superfamily, a comprehensive analysis of the composition, classification, and phylogeny of this protein superfamily has not been reported. Furthermore, relatively little is known about a subset of ARM proteins, and some of the current annotations of armadillo repeats are incomplete or incorrect, often due to high similarity with HEAT repeats. We identified the entire armadillo repeat superfamily repertoire in the human genome, annotated each armadillo repeat, and performed an extensive evolutionary analysis of the armadillo repeat proteins in both metazoan and premetazoan species. Phylogenetic analyses of the superfamily classified them into several discrete branches with members showing significant sequence homology, and often also related functions. Interestingly, the phylogenetic structure of the superfamily revealed that about 30 % of the members predate metazoans and represent an ancient subset, which is gradually evolving to acquire complex and highly diverse functions.
Keywords
NONSMALL CELL LUNG, PRIMARY CILIARY DYSKINESIA, PROTEIN FAMILIES, DATABASE, BETA-CATENIN, GENE FAMILY, CAENORHABDITIS-ELEGANS, UBIQUITIN, LIGASE, P120 CATENIN, CHROMOSOME SEGREGATION, SEQUENCE ALIGNMENT, Phylogeny, ARM repeat, HEAT repeat, Metazoa, Premetazoan, Molecular, evolution, Protein domains, Catenins, Importins

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Citation

Please use this url to cite or link to this publication:

Chicago
Gül, Ismail Sahin, Paco Hulpiau, Yvan Saeys, and Frans Van Roy. 2017. “Metazoan Evolution of the Armadillo Repeat Superfamily.” Cellular and Molecular Life Sciences 74 (3): 525–541.
APA
Gül, I. S., Hulpiau, P., Saeys, Y., & Van Roy, F. (2017). Metazoan evolution of the armadillo repeat superfamily. CELLULAR AND MOLECULAR LIFE SCIENCES, 74(3), 525–541.
Vancouver
1.
Gül IS, Hulpiau P, Saeys Y, Van Roy F. Metazoan evolution of the armadillo repeat superfamily. CELLULAR AND MOLECULAR LIFE SCIENCES. 2017;74(3):525–41.
MLA
Gül, Ismail Sahin, Paco Hulpiau, Yvan Saeys, et al. “Metazoan Evolution of the Armadillo Repeat Superfamily.” CELLULAR AND MOLECULAR LIFE SCIENCES 74.3 (2017): 525–541. Print.
@article{8513969,
  abstract     = {The superfamily of armadillo repeat proteins is a fascinating archetype of modular-binding proteins involved in various fundamental cellular processes, including cell-cell adhesion, cytoskeletal organization, nuclear import, and molecular signaling. Despite their diverse functions, they all share tandem armadillo (ARM) repeats, which stack together to form a conserved three-dimensional structure. This superhelical armadillo structure enables them to interact with distinct partners by wrapping around them. Despite the important functional roles of this superfamily, a comprehensive analysis of the composition, classification, and phylogeny of this protein superfamily has not been reported. Furthermore, relatively little is known about a subset of ARM proteins, and some of the current annotations of armadillo repeats are incomplete or incorrect, often due to high similarity with HEAT repeats. We identified the entire armadillo repeat superfamily repertoire in the human genome, annotated each armadillo repeat, and performed an extensive evolutionary analysis of the armadillo repeat proteins in both metazoan and premetazoan species. Phylogenetic analyses of the superfamily classified them into several discrete branches with members showing significant sequence homology, and often also related functions. Interestingly, the phylogenetic structure of the superfamily revealed that about 30 \% of the members predate metazoans and represent an ancient subset, which is gradually evolving to acquire complex and highly diverse functions.},
  author       = {G{\"u}l, Ismail Sahin and Hulpiau, Paco and Saeys, Yvan and Van Roy, Frans},
  issn         = {1420-682X},
  journal      = {CELLULAR AND MOLECULAR LIFE SCIENCES},
  keyword      = {NONSMALL CELL LUNG,PRIMARY CILIARY DYSKINESIA,PROTEIN FAMILIES,DATABASE,BETA-CATENIN,GENE FAMILY,CAENORHABDITIS-ELEGANS,UBIQUITIN,LIGASE,P120 CATENIN,CHROMOSOME SEGREGATION,SEQUENCE ALIGNMENT,Phylogeny,ARM repeat,HEAT repeat,Metazoa,Premetazoan,Molecular,evolution,Protein domains,Catenins,Importins},
  language     = {eng},
  number       = {3},
  pages        = {525--541},
  title        = {Metazoan evolution of the armadillo repeat superfamily},
  url          = {http://dx.doi.org/10.1007/s00018-016-2319-6},
  volume       = {74},
  year         = {2017},
}

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