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Metazoan evolution of the armadillo repeat superfamily

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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.

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References

  1. Riggleman B, Wieschaus E, Schedl P (1989) Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev 3(1):96–113

    Article  CAS  PubMed  Google Scholar 

  2. Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76(5):789–791

    Article  CAS  PubMed  Google Scholar 

  3. Tewari R, Bailes E, Bunting KA, Coates JC (2010) Armadillo-repeat protein functions: questions for little creatures. Trends Cell Biol 20(8):470–481. doi:10.1016/j.tcb.2010.05.003

    Article  CAS  PubMed  Google Scholar 

  4. Huber AH, Nelson WJ, Weis WI (1997) Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell 90(5):871–882

    Article  CAS  PubMed  Google Scholar 

  5. Madhurantakam C, Varadamsetty G, Grutter MG, Pluckthun A, Mittl PR (2012) Structure-based optimization of designed Armadillo-repeat proteins. Protein Sci 21(7):1015–1028. doi:10.1002/pro.2085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Parmeggiani F, Pellarin R, Larsen AP, Varadamsetty G, Stumpp MT, Zerbe O, Caflisch A, Pluckthun A (2008) Designed armadillo repeat proteins as general peptide-binding scaffolds: consensus design and computational optimization of the hydrophobic core. J Mol Biol 376(5):1282–1304. doi:10.1016/j.jmb.2007.12.014

    Article  CAS  PubMed  Google Scholar 

  7. Cingolani G, Petosa C, Weis K, Muller CW (1999) Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 399(6733):221–229. doi:10.1038/20367

    Article  CAS  PubMed  Google Scholar 

  8. Choi HJ, Gross JC, Pokutta S, Weis WI (2009) Interactions of plakoglobin and beta-catenin with desmosomal cadherins: basis of selective exclusion of alpha- and beta-catenin from desmosomes. J Biol Chem 284(46):31776–31788. doi:10.1074/jbc.M109.047928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ishiyama N, Lee SH, Liu S, Li GY, Smith MJ, Reichardt LF, Ikura M (2010) Dynamic and static interactions between p120 catenin and E-cadherin regulate the stability of cell–cell adhesion. Cell 141(1):117–128. doi:10.1016/j.cell.2010.01.017

    Article  CAS  PubMed  Google Scholar 

  10. Andrade MA, Perez-Iratxeta C, Ponting CP (2001) Protein repeats: structures, functions, and evolution. J Struct Biol 134(2–3):117–131. doi:10.1006/jsbi.2001.4392

    Article  CAS  PubMed  Google Scholar 

  11. Kippert F, Gerloff DL (2009) Highly sensitive detection of individual HEAT and ARM repeats with HHpred and COACH. PLoS One 4(9):e7148. doi:10.1371/journal.pone.0007148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Kuhn S, Erdmann C, Kage F, Block J, Schwenkmezger L, Steffen A, Rottner K, Geyer M (2015) The structure of FMNL2-Cdc42 yields insights into the mechanism of lamellipodia and filopodia formation. Nat Commun 6:7088. doi:10.1038/ncomms8088

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Rose R, Weyand M, Lammers M, Ishizaki T, Ahmadian MR, Wittinghofer A (2005) Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 435(7041):513–518. doi:10.1038/nature03604

    Article  CAS  PubMed  Google Scholar 

  14. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38(Database issue):D211–D222. doi:10.1093/nar/gkp985

    Article  CAS  PubMed  Google Scholar 

  15. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. doi:10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43(Database issue):D222–D226. doi:10.1093/nar/gku1221

    Article  PubMed  Google Scholar 

  17. Dalquen DA, Dessimoz C (2013) Bidirectional best hits miss many orthologs in duplication-rich clades such as plants and animals. Genome Biol Evol 5(10):1800–1806. doi:10.1093/gbe/evt132

    Article  PubMed  PubMed Central  Google Scholar 

  18. Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7(Suppl 1):S10 11–12. doi:10.1186/gb-2006-7-s1-s10

  19. Burge CB, Karlin S (1998) Finding the genes in genomic DNA. Curr Opin Struct Biol 8(3):346–354

    Article  CAS  PubMed  Google Scholar 

  20. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36(Web Server issue):W5–W9. doi:10.1093/nar/gkn201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  22. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23(1):127–128. doi:10.1093/bioinformatics/btl529

    Article  CAS  PubMed  Google Scholar 

  23. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. doi:10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Pruitt KD, Brown GR, Hiatt SM, Thibaud-Nissen F, Astashyn A, Ermolaeva O, Farrell CM, Hart J, Landrum MJ, McGarvey KM, Murphy MR, O’Leary NA, Pujar S, Rajput B, Rangwala SH, Riddick LD, Shkeda A, Sun H, Tamez P, Tully RE, Wallin C, Webb D, Weber J, Wu W, DiCuccio M, Kitts P, Maglott DR, Murphy TD, Ostell JM (2014) RefSeq: an update on mammalian reference sequences. Nucleic Acids Res 42(Database issue):D756–D763. doi:10.1093/nar/gkt1114

    Article  CAS  PubMed  Google Scholar 

  25. Imasaki T, Shimizu T, Hashimoto H, Hidaka Y, Kose S, Imamoto N, Yamada M, Sato M (2007) Structural basis for substrate recognition and dissociation by human transportin 1. Mol Cell 28(1):57–67. doi:10.1016/j.molcel.2007.08.006

    Article  CAS  PubMed  Google Scholar 

  26. Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, McAnulla C, McMenamin C, Nuka G, Pesseat S, Sangrador-Vegas A, Scheremetjew M, Rato C, Yong SY, Bateman A, Punta M, Attwood TK, Sigrist CJ, Redaschi N, Rivoire C, Xenarios I, Kahn D, Guyot D, Bork P, Letunic I, Gough J, Oates M, Haft D, Huang H, Natale DA, Wu CH, Orengo C, Sillitoe I, Mi H, Thomas PD, Finn RD (2015) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43(Database issue):D213–D221. doi:10.1093/nar/gku1243

    Article  PubMed  Google Scholar 

  27. Suga H, Chen Z, de Mendoza A, Sebe-Pedros A, Brown MW, Kramer E, Carr M, Kerner P, Vervoort M, Sanchez-Pons N, Torruella G, Derelle R, Manning G, Lang BF, Russ C, Haas BJ, Roger AJ, Nusbaum C, Ruiz-Trillo I (2013) The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun 4:2325. doi:10.1038/ncomms3325

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Goldfarb DS, Corbett AH, Mason DA, Harreman MT, Adam SA (2004) Importin alpha: a multipurpose nuclear-transport receptor. Trends Cell Biol 14(9):505–514. doi:10.1016/j.tcb.2004.07.016

    Article  CAS  PubMed  Google Scholar 

  29. Chalkia D, Nikolaidis N, Makalowski W, Klein J, Nei M (2008) Origins and evolution of the formin multigene family that is involved in the formation of actin filaments. Mol Biol Evol 25(12):2717–2733. doi:10.1093/molbev/msn215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lopez-Domenech G, Serrat R, Mirra S, D’Aniello S, Somorjai I, Abad A, Vitureira N, Garcia-Arumi E, Alonso MT, Rodriguez-Prados M, Burgaya F, Andreu AL, Garcia-Sancho J, Trullas R, Garcia-Fernandez J, Soriano E (2012) The Eutherian Armcx genes regulate mitochondrial trafficking in neurons and interact with Miro and Trak2. Nat Commun 3:814. doi:10.1038/ncomms1829

    Article  PubMed  CAS  Google Scholar 

  31. Zhao ZM, Reynolds AB, Gaucher EA (2011) The evolutionary history of the catenin gene family during metazoan evolution. BMC Evol Biol 11:198. doi:10.1186/1471-2148-11-198

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hall BG (2005) Comparison of the accuracies of several phylogenetic methods using protein and DNA sequences. Mol Biol Evol 22(3):792–802. doi:10.1093/molbev/msi066

    Article  CAS  PubMed  Google Scholar 

  33. Gaucher EA, Kratzer JT, Randall RN (2010) Deep phylogeny—how a tree can help characterize early life on Earth. Cold Spring Harb Perspect Biol 2(1):a002238. doi:10.1101/cshperspect.a002238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Wang LS, Leebens-Mack J, Kerr Wall P, Beckmann K, dePamphilis CW, Warnow T (2011) The impact of multiple protein sequence alignment on phylogenetic estimation. IEEE/ACM Trans Comput Biol Bioinform 8(4):1108–1119. doi:10.1109/TCBB.2009.68

    Article  PubMed  Google Scholar 

  35. Garces RG, Gillon W, Pai EF (2007) Atomic model of human Rcd-1 reveals an armadillo-like-repeat protein with in vitro nucleic acid binding properties. Protein Sci 16(2):176–188. doi:10.1110/ps.062600507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Schonichen A (1803) Geyer M (2010) Fifteen formins for an actin filament: a molecular view on the regulation of human formins. Biochim Biophys Acta 2:152–163. doi:10.1016/j.bbamcr.2010.01.014

    Google Scholar 

  37. Hulpiau P, Gul IS, van Roy F (2013) New insights into the evolution of metazoan cadherins and catenins. Prog Mol Biol Transl Sci 116:71–94. doi:10.1016/B978-0-12-394311-8.00004-2

    Article  CAS  PubMed  Google Scholar 

  38. Hulpiau P, van Roy F (2011) New insights into the evolution of metazoan cadherins. Mol Biol Evol 28(1):647–657. doi:10.1093/molbev/msq233

    Article  CAS  PubMed  Google Scholar 

  39. Yamamoto Y, Izumi Y, Matsuzaki F (2008) The GC kinase Fray and Mo25 regulate Drosophila asymmetric divisions. Biochem Biophys Res Commun 366(1):212–218. doi:10.1016/j.bbrc.2007.11.128

    Article  CAS  PubMed  Google Scholar 

  40. Filippi BM, de los Heros P, Mehellou Y, Navratilova I, Gourlay R, Deak M, Plater L, Toth R, Zeqiraj E, Alessi DR (2011) MO25 is a master regulator of SPAK/OSR1 and MST3/MST4/YSK1 protein kinases. EMBO J 30(9):1730–1741. doi:10.1038/emboj.2011.78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Mendoza M, Redemann S, Brunner D (2005) The fission yeast MO25 protein functions in polar growth and cell separation. Eur J Cell Biol 84(12):915–926. doi:10.1016/j.ejcb.2005.09.013

    Article  CAS  PubMed  Google Scholar 

  42. Suzuki T, Ueda A, Kobayashi N, Yang J, Tomaru K, Yamamoto M, Takeno M, Ishigatsubo Y (2008) Proteasome-dependent degradation of alpha-catenin is regulated by interaction with ARMc8alpha. Biochem J 411(3):581–591. doi:10.1042/BJ20071312

    Article  CAS  PubMed  Google Scholar 

  43. Menssen R, Schweiggert J, Schreiner J, Kusevic D, Reuther J, Braun B, Wolf DH (2012) Exploring the topology of the Gid complex, the E3 ubiquitin ligase involved in catabolite-induced degradation of gluconeogenic enzymes. J Biol Chem 287(30):25602–25614. doi:10.1074/jbc.M112.363762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Francis O, Han F, Adams JC (2013) Molecular phylogeny of a RING E3 ubiquitin ligase, conserved in eukaryotic cells and dominated by homologous components, the muskelin/RanBPM/CTLH complex. PLoS One 8(10):e75217. doi:10.1371/journal.pone.0075217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Nakajima H, Hirata A, Ogawa Y, Yonehara T, Yoda K, Yamasaki M (1991) A cytoskeleton-related gene, uso1, is required for intracellular protein transport in Saccharomyces cerevisiae. J Cell Biol 113(2):245–260

    Article  CAS  PubMed  Google Scholar 

  46. Striegl H, Roske Y, Kummel D, Heinemann U (2009) Unusual armadillo fold in the human general vesicular transport factor p115. PLoS One 4(2):e4656. doi:10.1371/journal.pone.0004656

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Geles KG, Adam SA (2001) Germline and developmental roles of the nuclear transport factor importin alpha3 in C. elegans. Development 128(10):1817–1830

    CAS  PubMed  Google Scholar 

  48. Phadnis N, Hsieh E, Malik HS (2012) Birth, death, and replacement of karyopherins in Drosophila. Mol Biol Evol 29(5):1429–1440. doi:10.1093/molbev/msr306

    Article  CAS  PubMed  Google Scholar 

  49. Grimson MJ, Coates JC, Reynolds JP, Shipman M, Blanton RL, Harwood AJ (2000) Adherens junctions and beta-catenin-mediated cell signalling in a non-metazoan organism. Nature 408(6813):727–731. doi:10.1038/35047099

    Article  CAS  PubMed  Google Scholar 

  50. Coates JC, Grimson MJ, Williams RS, Bergman W, Blanton RL, Harwood AJ (2002) Loss of the beta-catenin homologue aardvark causes ectopic stalk formation in Dictyostelium. Mech Dev 116(1–2):117–127

    Article  CAS  PubMed  Google Scholar 

  51. Dickinson DJ, Nelson WJ, Weis WI (2011) A polarized epithelium organized by beta- and alpha-catenin predates cadherin and metazoan origins. Science 331(6022):1336–1339. doi:10.1126/science.1199633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ha NC, Tonozuka T, Stamos JL, Choi HJ, Weis WI (2004) Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Mol Cell 15(4):511–521. doi:10.1016/j.molcel.2004.08.010

    Article  CAS  PubMed  Google Scholar 

  53. Yang J, Zhang W, Evans PM, Chen X, He X, Liu C (2006) Adenomatous polyposis coli (APC) differentially regulates beta-catenin phosphorylation and ubiquitination in colon cancer cells. J Biol Chem 281(26):17751–17757. doi:10.1074/jbc.M600831200

    Article  CAS  PubMed  Google Scholar 

  54. Cai X, Zhang Y (2006) Molecular evolution of the ankyrin gene family. Mol Biol Evol 23(3):550–558. doi:10.1093/molbev/msj056

    Article  CAS  PubMed  Google Scholar 

  55. Abu-Helo A, Simonin F (2010) Identification and biological significance of G protein-coupled receptor associated sorting proteins (GASPs). Pharmacol Ther 126(3):244–250. doi:10.1016/j.pharmthera.2010.03.004

    Article  CAS  PubMed  Google Scholar 

  56. Simonin F, Karcher P, Boeuf JJ, Matifas A, Kieffer BL (2004) Identification of a novel family of G protein-coupled receptor associated sorting proteins. J Neurochem 89(3):766–775. doi:10.1111/j.1471-4159.2004.02411.x

    Article  CAS  PubMed  Google Scholar 

  57. Kemphues KJ, Wolf N, Wood WB, Hirsh D (1986) Two loci required for cytoplasmic organization in early embryos of Caenorhabditis elegans. Dev Biol 113(2):449–460

    Article  CAS  PubMed  Google Scholar 

  58. Reichen C, Hansen S, Pluckthun A (2014) Modular peptide binding: from a comparison of natural binders to designed armadillo repeat proteins. J Struct Biol 185(2):147–162. doi:10.1016/j.jsb.2013.07.012

    Article  CAS  PubMed  Google Scholar 

  59. Stamos JL, Weis WI (2013) The beta-catenin destruction complex. Cold Spring Harb Perspect Biol 5(1). doi:10.1101/cshperspect.a007898

  60. Hatzfeld M (2007) Plakophilins: multifunctional proteins or just regulators of desmosomal adhesion? Biochim Biophys Acta 1773(1):69–77. doi:10.1016/j.bbamcr.2006.04.009

    Article  CAS  PubMed  Google Scholar 

  61. Carramusa L, Ballestrem C, Zilberman Y, Bershadsky AD (2007) Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell–cell junctions. J Cell Sci 120(Pt 21):3870–3882. doi:10.1242/jcs.014365

    Article  CAS  PubMed  Google Scholar 

  62. Ireton RC, Davis MA, van Hengel J, Mariner DJ, Barnes K, Thoreson MA, Anastasiadis PZ, Matrisian L, Bundy LM, Sealy L, Gilbert B, van Roy F, Reynolds AB (2002) A novel role for p120 catenin in E-cadherin function. J Cell Biol 159(3):465–476. doi:10.1083/jcb.200205115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Kourtidis A, Ngok SP, Anastasiadis PZ (2013) p120 catenin: an essential regulator of cadherin stability, adhesion-induced signaling, and cancer progression. Prog Mol Biol Transl Sci 116:409–432. doi:10.1016/B978-0-12-394311-8.00018-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Young KG (1803) Copeland JW (2010) Formins in cell signaling. Biochim Biophys Acta 2:183–190. doi:10.1016/j.bbamcr.2008.09.017

    Google Scholar 

  65. Buckley CD, Tan J, Anderson KL, Hanein D, Volkmann N, Weis WI, Nelson WJ, Dunn AR (2014) Cell adhesion. The minimal cadherin-catenin complex binds to actin filaments under force. Science 346(6209):1254211. doi:10.1126/science.1254211

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Valenta T, Hausmann G, Basler K (2012) The many faces and functions of beta-catenin. EMBO J 31(12):2714–2736. doi:10.1038/emboj.2012.150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Haraguchi K, Hayashi T, Jimbo T, Yamamoto T, Akiyama T (2006) Role of the kinesin-2 family protein, KIF3, during mitosis. J Biol Chem 281(7):4094–4099. doi:10.1074/jbc.M507028200

    Article  CAS  PubMed  Google Scholar 

  68. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS (2001) A role for the adenomatous polyposis coli protein in chromosome segregation. Nat Cell Biol 3(4):429–432. doi:10.1038/35070123

    Article  CAS  PubMed  Google Scholar 

  69. Stolz A, Neufeld K, Ertych N, Bastians H (2015) Wnt-mediated protein stabilization ensures proper mitotic microtubule assembly and chromosome segregation. EMBO Rep 16(4):490–499. doi:10.15252/embr.201439410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Jimbo T, Kawasaki Y, Koyama R, Sato R, Takada S, Haraguchi K, Akiyama T (2002) Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat Cell Biol 4(4):323–327. doi:10.1038/ncb779

    Article  CAS  PubMed  Google Scholar 

  71. Onoufriadis A, Shoemark A, Munye MM, James CT, Schmidts M, Patel M, Rosser EM, Bacchelli C, Beales PL, Scambler PJ, Hart SL, Danke-Roelse JE, Sloper JJ, Hull S, Hogg C, Emes RD, Pals G, Moore AT, Chung EM, UK10 K, Mitchison HM (2014) Combined exome and whole-genome sequencing identifies mutations in ARMC4 as a cause of primary ciliary dyskinesia with defects in the outer dynein arm. J Med Genet 51(1):61–67. doi:10.1136/jmedgenet-2013-101938

    Article  CAS  PubMed  Google Scholar 

  72. Cheng W, Ip YT, Xu Z (2013) Gudu, an Armadillo repeat-containing protein, is required for spermatogenesis in Drosophila. Gene 531(2):294–300. doi:10.1016/j.gene.2013.08.080

    Article  CAS  PubMed  Google Scholar 

  73. Pausch H, Venhoranta H, Wurmser C, Hakala K, Iso-Touru T, Sironen A, Vingborg RK, Lohi H, Soderquist L, Fries R, Andersson M (2016) A frameshift mutation in ARMC3 is associated with a tail stump sperm defect in Swedish Red (Bos taurus) cattle. BMC Genet 17(1):49. doi:10.1186/s12863-016-0356-7

    Article  PubMed  PubMed Central  Google Scholar 

  74. Iida H, Urasoko A, Doiguchi M, Mori T, Toshimori K, Shibata Y (2003) Complementary DNA cloning and characterization of rat spergen-2, a spermatogenic cell-specific gene 2 encoding a 56-kilodalton nuclear protein bearing ankyrin repeat motifs. Biol Reprod 69(2):421–429. doi:10.1095/biolreprod.102.013987

    Article  CAS  PubMed  Google Scholar 

  75. Wang HL, Fan SS, Pang M, Liu YH, Guo M, Liang JB, Zhang JL, Yu BF, Guo R, Xie J, Zheng GP (2015) The Ankyrin repeat domain 49 (ANKRD49) augments autophagy of serum-starved GC-1 cells through the NF-kappaB pathway. PLoS One 10(6):e0128551. doi:10.1371/journal.pone.0128551

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Straschil U, Talman AM, Ferguson DJ, Bunting KA, Xu Z, Bailes E, Sinden RE, Holder AA, Smith EF, Coates JC, Rita T (2010) The Armadillo repeat protein PF16 is essential for flagellar structure and function in Plasmodium male gametes. PLoS One 5(9):e12901. doi:10.1371/journal.pone.0012901

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Holt JE, Ly-Huynh JD, Efthymiadis A, Hime GR, Loveland KL, Jans DA (2007) Regulation of nuclear import during differentiation; the IMP alpha gene family and spermatogenesis. Curr Genomics 8(5):323–334. doi:10.2174/138920207782446151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Mudgil Y, Shiu SH, Stone SL, Salt JN, Goring DR (2004) A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family. Plant Physiol 134(1):59–66. doi:10.1104/pp.103.029553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Sharma M, Singh A, Shankar A, Pandey A, Baranwal V, Kapoor S, Tyagi AK, Pandey GK (2014) Comprehensive expression analysis of rice Armadillo gene family during abiotic stress and development. DNA Res 21(3):267–283. doi:10.1093/dnares/dst056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Teotia S, Lamb RS (2011) RCD1 and SRO1 are necessary to maintain meristematic fate in Arabidopsis thaliana. J Exp Bot 62(3):1271–1284. doi:10.1093/jxb/erq363

    Article  CAS  PubMed  Google Scholar 

  81. Latijnhouwers M, Gillespie T, Boevink P, Kriechbaumer V, Hawes C, Carvalho CM (2007) Localization and domain characterization of Arabidopsis golgin candidates. J Exp Bot 58(15–16):4373–4386. doi:10.1093/jxb/erm304

    Article  CAS  PubMed  Google Scholar 

  82. Baumgartner W (2013) Possible roles of LI-Cadherin in the formation and maintenance of the intestinal epithelial barrier. Tissue Barriers 1(1):e23815. doi:10.4161/tisb.23815

    Article  PubMed  PubMed Central  Google Scholar 

  83. Oda H, Takeichi M (2011) Evolution: structural and functional diversity of cadherin at the adherens junction. J Cell Biol 193(7):1137–1146. doi:10.1083/jcb.201008173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Sotomayor M, Gaudet R, Corey DP (2014) Sorting out a promiscuous superfamily: towards cadherin connectomics. Trends Cell Biol 24(9):524–536. doi:10.1016/j.tcb.2014.03.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Xing Y, Takemaru K, Liu J, Berndt JD, Zheng JJ, Moon RT, Xu W (2008) Crystal structure of a full-length beta-catenin. Structure 16(3):478–487. doi:10.1016/j.str.2007.12.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Schuld NJ, Hauser AD, Gastonguay AJ, Wilson JM, Lorimer EL, Williams CL (2014) SmgGDS-558 regulates the cell cycle in pancreatic, non-small cell lung, and breast cancers. Cell Cycle 13(6):941–952. doi:10.4161/cc.27804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Hauser AD, Bergom C, Schuld NJ, Chen X, Lorimer EL, Huang J, Mackinnon AC, Williams CL (2014) The SmgGDS splice variant SmgGDS-558 is a key promoter of tumor growth and RhoA signaling in breast cancer. Mol Cancer Res 12(1):130–142. doi:10.1158/1541-7786.MCR-13-0362

    Article  CAS  PubMed  Google Scholar 

  88. Tew GW, Lorimer EL, Berg TJ, Zhi H, Li R, Williams CL (2008) SmgGDS regulates cell proliferation, migration, and NF-kappaB transcriptional activity in non-small cell lung carcinoma. J Biol Chem 283(2):963–976. doi:10.1074/jbc.M707526200

    Article  CAS  PubMed  Google Scholar 

  89. de Bruyn KM, Zwartkruis FJ, de Rooij J, Akkerman JW, Bos JL (2003) The small GTPase Rap1 is activated by turbulence and is involved in integrin [alpha]IIb[beta]3-mediated cell adhesion in human megakaryocytes. J Biol Chem 278(25):22412–22417. doi:10.1074/jbc.M212036200

    Article  PubMed  CAS  Google Scholar 

  90. Chung KT, Shen Y, Hendershot LM (2002) BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J Biol Chem 277(49):47557–47563. doi:10.1074/jbc.M208377200

    Article  CAS  PubMed  Google Scholar 

  91. Inaguma Y, Hamada N, Tabata H, Iwamoto I, Mizuno M, Nishimura YV, Ito H, Morishita R, Suzuki M, Ohno K, Kumagai T, Nagata K (2014) SIL1, a causative cochaperone gene of Marinesco–Sojgren syndrome, plays an essential role in establishing the architecture of the developing cerebral cortex. EMBO Mol Med 6(3):414–429. doi:10.1002/emmm.201303069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Lee CF, Hauenstein AV, Fleming JK, Gasper WC, Engelke V, Sankaran B, Bernstein SI, Huxford T (2011) X-ray crystal structure of the UCS domain-containing UNC-45 myosin chaperone from Drosophila melanogaster. Structure 19(3):397–408. doi:10.1016/j.str.2011.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Price MG, Landsverk ML, Barral JM, Epstein HF (2002) Two mammalian UNC-45 isoforms are related to distinct cytoskeletal and muscle-specific functions. J Cell Sci 115(Pt 21):4013–4023

    Article  CAS  PubMed  Google Scholar 

  94. Jilani Y, Lu S, Lei H, Karnitz LM, Chadli A (2015) UNC45A localizes to centrosomes and regulates cancer cell proliferation through ChK1 activation. Cancer Lett 357(1):114–120. doi:10.1016/j.canlet.2014.11.009

    Article  CAS  PubMed  Google Scholar 

  95. Nozaki M, Onishi Y, Togashi S, Miyamoto H (1996) Molecular characterization of the Drosophila Mo25 gene, which is conserved among Drosophila, mouse, and yeast. DNA Cell Biol 15(6):505–509

    Article  CAS  PubMed  Google Scholar 

  96. Zeqiraj E, Filippi BM, Deak M, Alessi DR, van Aalten DM (2009) Structure of the LKB1-STRAD-MO25 complex reveals an allosteric mechanism of kinase activation. Science 326(5960):1707–1711. doi:10.1126/science.1178377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Dettmann A, Illgen J, Marz S, Schurg T, Fleissner A, Seiler S (2012) The NDR kinase scaffold HYM1/MO25 is essential for MAK2 map kinase signaling in Neurospora crassa. PLoS Genet 8(9):e1002950. doi:10.1371/journal.pgen.1002950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Alberti S, Bohse K, Arndt V, Schmitz A, Hohfeld J (2004) The cochaperone HspBP1 inhibits the CHIP ubiquitin ligase and stimulates the maturation of the cystic fibrosis transmembrane conductance regulator. Mol Biol Cell 15(9):4003–4010. doi:10.1091/mbc.E04-04-0293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Rogon C, Ulbricht A, Hesse M, Alberti S, Vijayaraj P, Best D, Adams IR, Magin TM, Fleischmann BK, Hohfeld J (2014) HSP70-binding protein HSPBP1 regulates chaperone expression at a posttranslational level and is essential for spermatogenesis. Mol Biol Cell 25(15):2260–2271. doi:10.1091/mbc.E14-02-0742

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Feral C, Wu YQ, Pawlak A, Guellaen G (2001) Meiotic human sperm cells express a leucine-rich homologue of Caenorhabditis elegans early embryogenesis gene, Zyg-11. Mol Hum Reprod 7(12):1115–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Vasudevan S, Starostina NG, Kipreos ET (2007) The Caenorhabditis elegans cell-cycle regulator ZYG-11 defines a conserved family of CUL-2 complex components. EMBO Rep 8(3):279–286. doi:10.1038/sj.embor.7400895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Hjeij R, Lindstrand A, Francis R, Zariwala MA, Liu X, Li Y, Damerla R, Dougherty GW, Abouhamed M, Olbrich H, Loges NT, Pennekamp P, Davis EE, Carvalho CM, Pehlivan D, Werner C, Raidt J, Kohler G, Haffner K, Reyes-Mugica M, Lupski JR, Leigh MW, Rosenfeld M, Morgan LC, Knowles MR, Lo CW, Katsanis N, Omran H (2013) ARMC4 mutations cause primary ciliary dyskinesia with randomization of left/right body asymmetry. Am J Hum Genet 93(2):357–367. doi:10.1016/j.ajhg.2013.06.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Lonergan KM, Chari R, Deleeuw RJ, Shadeo A, Chi B, Tsao MS, Jones S, Marra M, Ling V, Ng R, Macaulay C, Lam S, Lam WL (2006) Identification of novel lung genes in bronchial epithelium by serial analysis of gene expression. Am J Respir Cell Mol Biol 35(6):651–661. doi:10.1165/rcmb.2006-0056OC

    Article  CAS  PubMed  Google Scholar 

  104. Sapiro R, Kostetskii I, Olds-Clarke P, Gerton GL, Radice GL, Strauss IJ (2002) Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6. Mol Cell Biol 22(17):6298–6305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Teves ME, Sears PR, Li W, Zhang Z, Tang W, van Reesema L, Costanzo RM, Davis CW, Knowles MR, Strauss JF 3rd, Zhang Z (2014) Sperm-associated antigen 6 (SPAG6) deficiency and defects in ciliogenesis and cilia function: polarity, density, and beat. PLoS One 9(10):e107271. doi:10.1371/journal.pone.0107271

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Li W, Mukherjee A, Wu J, Zhang L, Teves ME, Li H, Nambiar S, Henderson SC, Horwitz AR, Strauss Iii JF, Fang X, Zhang Z (2015) Sperm Associated Antigen 6 (SPAG6) regulates fibroblast cell growth, morphology, migration and ciliogenesis. Sci Rep 5:16506. doi:10.1038/srep16506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Manning BD, Snyder M (2000) Drivers and passengers wanted! the role of kinesin-associated proteins. Trends Cell Biol 10(7):281–289

    Article  CAS  PubMed  Google Scholar 

  108. Bansal SK, Gupta N, Sankhwar SN, Rajender S (2015) Differential genes expression between fertile and infertile spermatozoa revealed by transcriptome analysis. PLoS One 10(5):e0127007. doi:10.1371/journal.pone.0127007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Ratan R, Mason DA, Sinnot B, Goldfarb DS, Fleming RJ (2008) Drosophila importin alpha1 performs paralog-specific functions essential for gametogenesis. Genetics 178(2):839–850. doi:10.1534/genetics.107.081778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Jabbour L, Welter JF, Kollar J, Hering TM (2003) Sequence, gene structure, and expression pattern of CTNNBL1, a minor-class intron-containing gene—evidence for a role in apoptosis. Genomics 81(3):292–303

    Article  CAS  PubMed  Google Scholar 

  111. Ganesh K, Adam S, Taylor B, Simpson P, Rada C, Neuberger M (2011) CTNNBL1 is a novel nuclear localization sequence-binding protein that recognizes RNA-splicing factors CDC5L and Prp31. J Biol Chem 286(19):17091–17102. doi:10.1074/jbc.M110.208769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Huang X, Wang G, Wu Y, Du Z (2013) The structure of full-length human CTNNBL1 reveals a distinct member of the armadillo-repeat protein family. Acta Crystallogr D Biol Crystallogr 69(Pt 8):1598–1608. doi:10.1107/S0907444913011360

    Article  CAS  PubMed  Google Scholar 

  113. Hiroi N, Ito T, Yamamoto H, Ochiya T, Jinno S, Okayama H (2002) Mammalian Rcd1 is a novel transcriptional cofactor that mediates retinoic acid-induced cell differentiation. EMBO J 21(19):5235–5244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Ryu JR, Echarri A, Li R, Pendergast AM (2009) Regulation of cell–cell adhesion by Abi/Diaphanous complexes. Mol Cell Biol 29(7):1735–1748. doi:10.1128/MCB.01483-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Schulze N, Graessl M, Blancke Soares A, Geyer M, Dehmelt L, Nalbant P (2014) FHOD1 regulates stress fiber organization by controlling the dynamics of transverse arcs and dorsal fibers. J Cell Sci 127(Pt 7):1379–1393. doi:10.1242/jcs.134627

    Article  CAS  PubMed  Google Scholar 

  116. Kim HC, Jo YJ, Kim NH, Namgoong S (2015) Small molecule inhibitor of formin homology 2 domains (SMIFH2) reveals the roles of the formin family of proteins in spindle assembly and asymmetric division in mouse oocytes. PLoS One 10(4):e0123438. doi:10.1371/journal.pone.0123438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Xie C, Jiang G, Fan C, Zhang X, Zhang Y, Miao Y, Lin X, Wu J, Wang L, Liu Y, Yu J, Yang L, Zhang D, Xu K, Wang E (2014) ARMC8alpha promotes proliferation and invasion of non-small cell lung cancer cells by activating the canonical Wnt signaling pathway. Tumour Biol 35(9):8903–8911. doi:10.1007/s13277-014-2162-z

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Amin Bredan for critical reading and careful editing of the manuscript and our colleagues for helpful discussions. This work was supported by the Research Foundation—Flanders (FWO-Vlaanderen, Award G.0320.11N), the Belgian Science Policy (Interuniversity Attraction Poles—Award IAP7/07), and the Special Research Fund of Ghent University (Award BOF 01J14211).

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Authors and Affiliations

  1. Inflammation Research Center (IRC), VIB, Ghent, Belgium

    Ismail Sahin Gul, Paco Hulpiau, Yvan Saeys & Frans van Roy

  2. Department of Biomedical Molecular Biology, Ghent University, FSVM Building, Technologiepark 927, 9052, Ghent, Belgium

    Ismail Sahin Gul, Paco Hulpiau & Frans van Roy

  3. Department of Respiratory Medicine, Ghent University, Ghent, Belgium

    Yvan Saeys

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  1. Ismail Sahin Gul
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Correspondence to Frans van Roy.

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Gul, I.S., Hulpiau, P., Saeys, Y. et al. Metazoan evolution of the armadillo repeat superfamily. Cell. Mol. Life Sci. 74, 525–541 (2017). https://doi.org/10.1007/s00018-016-2319-6

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