A holistic phylogeny of the coronin gene family reveals an ancient origin of the tandem-coronin, defines a new subfamily, and predicts protein function

BMC Evolutionary Biology

Volumn 11, Issue 1, 2011, Pages

  Eckert, Christian ^a   Hammesfahr, Björn ^a   Kollmar, Martin ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTE; EVOLUTIONARY BIOLOGY; GENOME; HOLISTIC APPROACH; MOTILITY; PHYLOGENETICS; PHYLOGENY; PROTEIN; TAXONOMY;

EUKARYOTA; EXCAVATA; FUNGI/METAZOA GROUP; METAZOA;

ACTIN; DRUG DERIVATIVE; GAMMA BUTYROLACTONE; KHELLIN;

ALTERNATIVE RNA SPLICING; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; BIOLOGY; CLASSIFICATION; EUKARYOTE; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

4-BUTYROLACTONE; ACTINS; ALTERNATIVE SPLICING; BASE SEQUENCE; BAYES THEOREM; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; EUKARYOTA; EVOLUTION, MOLECULAR; MODELS, GENETIC; MULTIGENE FAMILY; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

EID: 80053173098     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-11-268     Document Type: Article

References (73)

1. Coronin, an actin binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein beta subunits. de Hostos EL, Bradtke B, Lottspeich F, Guggenheim R, Gerisch G, EMBO J 1991 10 4097 4104 1661669 (Pubitemid 21905440)
2. A Plasmodium falciparum novel gene encoding a coronin-like protein which associates with actin filaments. Tardieux I, Liu X, Poupel O, Parzy D, Dehoux P, Langsley G, FEBS Lett 1998 441 251 256 10.1016/S0014-5793(98)01557-9 9883894 (Pubitemid 29027905)
3. Identification of a coronin-like protein in Babesia species. Figueroa JV, Precigout E, Carcy B, Gorenflot A, Ann N Y Acad Sci 2004 1026 125 138 10.1196/annals.1307.017 15604480 (Pubitemid 39636311)
4. The role of Saccharomyces cerevisiae coronin in the actin and microtubule cytoskeletons. Heil-Chapdelaine RA, Tran NK, Cooper JA, Curr Biol 1998 8 1281 1284 10.1016/S0960-9822(07)00539-8 9822583 (Pubitemid 28540057)
5. Molecular cloning of a novel actin-binding protein, p57, with a WD repeat and a leucine zipper motif. Suzuki K, Nishihata J, Arai Y, Honma N, Yamamoto K, Irimura T, Toyoshima S, FEBS Lett 1995 364 283 288 10.1016/0014-5793(95)00393-N 7758584
6. A brief history of the coronin family. de Hostos EL, Subcell Biochem 2008 48 31 40 10.1007/978-0-387-09595-0-4 18925369
7. The coronin family of proteins. Clemen CS, Rybakin V, Eichinger L, Subcell Biochem 2008 48 1 5 10.1007/978-0-387-09595-0-1 18925366
8. Coronins: the return of the crown. Uetrecht AC, Bear JE, Trends Cell Biol 2006 16 421 426 10.1016/j.tcb.2006.06.002 16806932 (Pubitemid 44118779)
9. Diversity of WD-repeat proteins. Smith TF, Subcell Biochem 2008 48 20 30 10.1007/978-0-387-09595-0-3 18925368
10. The ancient regulatory-protein family of WD-repeat proteins. Neer EJ, Schmidt CJ, Nambudripad R, Smith TF, Nature 1994 371 297 300 10.1038/371297a0 8090199 (Pubitemid 24300613)
11. Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. de Hostos EL, Rehfuess C, Bradtke B, Waddell DR, Albrecht R, Murphy J, Gerisch G, J Cell Biol 1993 120 163 173 10.1083/jcb.120.1.163 8380174 (Pubitemid 23014076)
12. Phosphorylation of coronin 1B by protein kinase C regulates interaction with Arp2/3 and cell motility. Cai L, Holoweckyj N, Schaller MD, Bear JE, J Biol Chem 2005 280 31913 31923 10.1074/jbc.M504146200 16027158 (Pubitemid 41291942)
13. Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Maniak M, Rauchenberger R, Albrecht R, Murphy J, Gerisch G, Cell 1995 83 915 924 10.1016/0092-8674(95)90207-4 8521515 (Pubitemid 26006533)
14. A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Ferrari G, Langen H, Naito M, Pieters J, Cell 1999 97 435 447 10.1016/S0092-8674(00)80754-0 10338208 (Pubitemid 29231167)
15. Coronin 7, the mammalian POD-1 homologue, localizes to the Golgi apparatus. Rybakin V, Stumpf M, Schulze A, Majoul IV, Noegel AA, Hasse A, FEBS Lett 2004 573 161 167 10.1016/j.febslet.2004.07.066 15327992 (Pubitemid 39141052)
16. The coronin family of actin-associated proteins. de Hostos EL, Trends Cell Biol 1999 9 345 350 10.1016/S0962-8924(99)01620-7 10461187 (Pubitemid 29447714)
17. The crystal structure of murine coronin-1: a regulator of actin cytoskeletal dynamics in lymphocytes. Appleton BA, Wu P, Wiesmann C, Structure 2006 14 87 96 10.1016/j.str.2005.09.013 16407068 (Pubitemid 43350076)
18. Oligomerization, F-actin interaction, and membrane association of the ubiquitous mammalian coronin 3 are mediated by its carboxyl terminus. Spoerl Z, Stumpf M, Noegel AA, Hasse A, J Biol Chem 2002 277 48858 48867 10.1074/jbc.M205136200 12377779 (Pubitemid 35470854)
19. Homotypic dimerization of the actin-binding protein p57/coronin-1 mediated by a leucine zipper motif in the C-terminal region. Oku T, Itoh S, Ishii R, Suzuki K, Nauseef WM, Toyoshima S, Tsuji T, Biochem J 2005 387 325 331 10.1042/BJ20041020 15601263 (Pubitemid 40571218)
20. A conserved trimerization motif controls the topology of short coiled coils. Kammerer RA, Kostrewa D, Progias P, Honnappa S, Avila D, Lustig A, Winkler FK, Pieters J, Steinmetz MO, Proc Natl Acad Sci USA 2005 102 13891 13896 10.1073/pnas.0502390102 16172398 (Pubitemid 41377674)
21. Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. Rybakin V, Clemen CS, Bioessays 2005 27 625 632 10.1002/bies.20235 15892111 (Pubitemid 40896093)
22. Molecular phylogeny and evolution of the coronin gene family. Morgan RO, Fernandez MP, Subcell Biochem 2008 48 41 55 10.1007/978-0-387-09595-0-5 18925370
23. diArk - a resource for eukaryotic genome research. Odronitz F, Hellkamp M, Kollmar M, BMC Genomics 2007 8 103 10.1186/1471-2164-8-103 17439643 (Pubitemid 46711331)
24. Organization and expression of eucaryotic split genes coding for proteins. Breathnach R, Chambon P, Annu Rev Biochem 1981 50 349 383 10.1146/annurev.bi.50.070181.002025 6791577
25. WebScipio: an online tool for the determination of gene structures using protein sequences. Odronitz F, Pillmann H, Keller O, Waack S, Kollmar M, BMC Genomics 2008 9 422 10.1186/1471-2164-9-422 18801164
26. Scipio: using protein sequences to determine the precise exon/intron structures of genes and their orthologs in closely related species. Keller O, Odronitz F, Stanke M, Kollmar M, Waack S, BMC Bioinformatics 2008 9 278 10.1186/1471-2105-9-278 18554390 (Pubitemid 351936544)
27. Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. Parfrey LW, Grant J, Tekle YI, Lasek-Nesselquist E, Morrison HG, Sogin ML, Patterson DJ, Katz LA, Syst Biol 2010 59 518 533 10.1093/sysbio/syq037 20656852
28. Interrelationships of chromalveolates within a broadly sampled tree of photosynthetic protists. Reeb VC, Peglar MT, Yoon HS, Bai JR, Wu M, Shiu P, Grafenberg JL, Reyes-Prieto A, Rummele SE, Gross J, Bhattacharya D, Mol Phylogenet Evol 2009 53 202 211 10.1016/j.ympev.2009.04.012 19398025
29. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups". Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, Roger AJ, Proc Natl Acad Sci USA 2009 106 3859 3864 10.1073/pnas.0807880106 19237557
30. Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. Goode BL, Wong JJ, Butty AC, Peter M, McCormack AL, Yates JR, Drubin DG, Barnes G, J Cell Biol 1999 144 83 98 10.1083/jcb.144.1.83 9885246 (Pubitemid 29047013)
31. Mechanism of a Concentration-dependent Switch between Activation and Inhibition of Arp2/3 Complex by Coronin. Liu SL, Needham KM, May JR, Nolen BJ, J Biol Chem 2011 286 17039 17046 10.1074/jbc.M111.219964 21454476
32. WASP family proteins: their evolution and its physiological implications. Veltman DM, Insall RH, Mol Biol Cell 2010 21 2880 2893 10.1091/mbc.E10-04-0372 20573979
33. Keeping uracil out of DNA: physiological role, structure and catalytic mechanism of dUTPases. Vertessy BG, Toth J, Acc Chem Res 2009 42 97 106 10.1021/ar800114w 18837522
34. Villidin, a novel WD-repeat and villin-related protein from Dictyostelium, is associated with membranes and the cytoskeleton. Gloss A, Rivero F, Khaire N, Muller R, Loomis WF, Schleicher M, Noegel AA, Mol Biol Cell 2003 14 2716 2727 10.1091/mbc.E02-12-0827 12857859 (Pubitemid 36871516)
35. Heterogeneity of mRNA coding for Caenorhabditis elegans coronin-like protein. Yonemura I, Mabuchi I, Gene 2001 271 255 259 10.1016/S0378-1119(01) 00509-1 11418247 (Pubitemid 32545403)
36. Structural and functional diversity of novel coronin 1C (CRN2) isoforms in muscle. Xavier CP, Rastetter RH, Stumpf M, Rosentreter A, Muller R, Reimann J, Cornfine S, Linder S, van Vliet V, Hofmann A, Morgan RO, Fernandez MP, Schroder R, Noegel AA, Clemen CS, J Mol Biol 2009 393 287 299 10.1016/j.jmb.2009.07.079 19651142
37. Coronin forms a stable dimer through its C-terminal coiled coil region: an implicated role in its localization to cell periphery. Asano S, Mishima M, Nishida E, Genes Cells 2001 6 225 235 10.1046/j.1365-2443.2001.00416.x 11260266 (Pubitemid 32273385)
38. A single amino acid can switch the oligomerization state of the alpha-helical coiled-coil domain of cartilage matrix protein. Beck K, Gambee JE, Kamawal A, Bachinger HP, EMBO J 1997 16 3767 3777 10.1093/emboj/16.13.3767 9233786 (Pubitemid 27280992)
39. Two regions responsible for the actin binding of p57, a mammalian coronin family actin-binding protein. Oku T, Itoh S, Okano M, Suzuki A, Suzuki K, Nakajin S, Tsuji T, Nauseef WM, Toyoshima S, Biol Pharm Bull 2003 26 409 416 10.1248/bpb.26.409 12673016 (Pubitemid 39663581)
40. F-actin binding is essential for coronin 1B function in vivo. Cai L, Makhov AM, Bear JE, J Cell Sci 2007 120 1779 1790 10.1242/jcs.007641 17456547 (Pubitemid 46930416)
41. Functional surfaces on the actin-binding protein coronin revealed by systematic mutagenesis. Gandhi M, Jangi M, Goode BL, J Biol Chem 2010 285 34899 34908 10.1074/jbc.M110.171496 20813846
42. 2R or not 2R is not the question anymore. Van de Peer Y, Maere S, Meyer A, Nat Rev Genet 2010 11 166 20084088
43. Three rounds (1R/2R/3R) of genome duplications and the evolution of the glycolytic pathway in vertebrates. Steinke D, Hoegg S, Brinkmann H, Meyer A, BMC Biol 2006 4 16 10.1186/1741-7007-4-16 16756667 (Pubitemid 44070311)
44. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, et al. Nature 2004 431 946 957 10.1038/nature03025 15496914 (Pubitemid 39434410)
45. Unraveling the enigma: progress towards understanding the coronin family of actin regulators. Chan KT, Creed SJ, Bear JE, Trends Cell Biol 2011 21 481 488 10.1016/j.tcb.2011.04.004 21632254
46. Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Odronitz F, Kollmar M, Genome Biol 2007 8 196 10.1186/gb-2007-8-9-r196 17877792 (Pubitemid 351895469)
47. A millennial myosin census. Berg JS, Powell BC, Cheney RE, Mol Biol Cell 2001 12 780 794 11294886 (Pubitemid 33051978)
48. Evolution of the gelsolin family of actin-binding proteins as novel transcriptional coactivators. Archer SK, Claudianos C, Campbell HD, Bioessays 2005 27 388 396 10.1002/bies.20200 15770676 (Pubitemid 40592595)
49. Evolutionary and functional diversity of coronin proteins. Xavier CP, Eichinger L, Fernandez MP, Morgan RO, Clemen CS, Subcell Biochem 2008 48 98 109 10.1007/978-0-387-09595-0-9 18925374
50. Regulation of cell structure and function by actin-binding proteins: villin's perspective. Khurana S, George SP, FEBS Lett 2008 582 2128 2139 10.1016/j.febslet.2008.02.040 18307996
51. Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of "primitive" eukaryotes. Simpson AG, Inagaki Y, Roger AJ, Mol Biol Evol 2006 23 615 625 16308337 (Pubitemid 43278273)
52. The endosymbiotic origin, diversification and fate of plastids. Keeling PJ, Philos Trans R Soc Lond B Biol Sci 2010 365 729 748 10.1098/rstb.2009.0103 20124341
53. Phylogenomics reveals a new 'megagroup' including most photosynthetic eukaryotes. Burki F, Shalchian-Tabrizi K, Pawlowski J, Biol Lett 2008 4 366 369 10.1098/rsbl.2008.0224 18522922 (Pubitemid 351961461)
54. Phylogenomics reshuffles the eukaryotic supergroups. Burki F, Shalchian-Tabrizi K, Minge M, Skjaeveland A, Nikolaev SI, Jakobsen KS, Pawlowski J, PLoS One 2007 2 790 10.1371/journal.pone.0000790 17726520 (Pubitemid 351377326)
55. Phylogenetic positions of Glaucophyta, green plants (Archaeplastida) and Haptophyta (Chromalveolata) as deduced from slowly evolving nuclear genes. Nozaki H, Maruyama S, Matsuzaki M, Nakada T, Kato S, Misawa K, Mol Phylogenet Evol 2009 53 872 880 10.1016/j.ympev.2009.08.015 19698794
56. Chromalveolates and the evolution of plastids by secondary endosymbiosis. Keeling PJ, J Eukaryot Microbiol 2009 56 1 8 10.1111/j.1550-7408.2008.00371.x 19335769
57. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Hackett JD, Yoon HS, Li S, Reyes-Prieto A, Rummele SE, Bhattacharya D, Mol Biol Evol 2007 24 1702 1713 10.1093/molbev/msm089 17488740 (Pubitemid 47236689)
58. diArk-a resource for eukaryotic genome research. http://www.diark.org
59. NCBI BLAST: a better web interface. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL, Nucleic Acids Res 2008 36 5 9 10.1093/nar/gkn201 18440982
60. Pfarao: a web application for protein family analysis customized for cytoskeletal and motor proteins (CyMoBase). Odronitz F, Kollmar M, BMC genomics 2006 7 300 10.1186/1471-2164-7-300 17134497 (Pubitemid 44941453)
61. CyMoBase-a database for cytoskeletal and motor proteins. http://www.cymobase.org
62. Multiple sequence alignment using ClustalW and ClustalX. Thompson JD, Gibson TJ, Higgins DG, Curr Protoc Bioinformatics 2002 Chapter 2 nit 2 3 18792934
63. A rapid bootstrap algorithm for the RAxML Web servers. Stamatakis A, Hoover P, Rougemont J, Syst Biol 2008 57 758 771 10.1080/10635150802429642 18853362
64. MrBayes 3: Bayesian phylogenetic inference under mixed models. Ronquist F, Huelsenbeck JP, Bioinformatics 2003 19 1572 1574 10.1093/bioinformatics/ btg180 12912839 (Pubitemid 37038874)
65. Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F, Bioinformatics 2004 20 407 415 10.1093/bioinformatics/btg427 14960467 (Pubitemid 38262773)
66. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Whelan S, Goldman N, Mol Biol Evol 2001 18 691 699 11319253 (Pubitemid 32372940)
67. ProtTest: selection of best-fit models of protein evolution. Abascal F, Zardoya R, Posada D, Bioinformatics 2005 21 2104 2105 10.1093/bioinformatics/ bti263 15647292 (Pubitemid 40668057)
68. An improved general amino acid replacement matrix. Le SQ, Gascuel O, Mol Biol Evol 2008 25 1307 1320 10.1093/molbev/msn067 18367465 (Pubitemid 351882003)
69. SMART 6: recent updates and new developments. Letunic I, Doerks T, Bork P, Nucleic Acids Res 2009 37 229 232 10.1093/nar/gkn808 18978020
70. The Pfam protein families database. 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, Nucleic Acids Res 2010 38 211 222 10.1093/nar/gkp985 19920124
71. PROSITE, a protein domain database for functional characterization and annotation. Sigrist CJ, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N, Nucleic Acids Res 2010 38 161 166 10.1093/nar/gkp885 19858104
72. WebLogo: a sequence logo generator. Crooks GE, Hon G, Chandonia JM, Brenner SE, Genome Res 2004 14 1188 1190 10.1101/gr.849004 15173120 (Pubitemid 38811555)
73. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Letunic I, Bork P, Bioinformatics 2007 23 127 128 10.1093/bioinformatics/btl529 17050570 (Pubitemid 46017867)