Evolution of RNA-binding proteins in animals: Insights from genome-wide analysis in the sponge amphimedon queenslandica

Molecular Biology and Evolution

Volumn 28, Issue 8, 2011, Pages 2289-2303

  Kerner, Pierre ^a,d   Degnan, Sandie M ^b   Marchand, Lauriane ^a   Degnan, Bernard M ^b   Vervoort, Michel ^a,c  

^a INSTITUT JACQUES MONOD   (France)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c INSTITUT UNIVERSITAIRE DE FRANCE   (France)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

development; evolution; miRNA; ncRNA; RNA binding proteins; stem cells

Indexed keywords

DEAD BOX PROTEIN; DSRM PROTEIN; KH PROTEIN; RNA BINDING PROTEIN; RNA INDUCED SILENCING COMPLEX; RRM PROTEIN; UNCLASSIFIED DRUG;

AMPHIMEDON QUEENSLANDICA; ANIMAL CELL; ARTICLE; CELL MATURATION; CHOANOFLAGELLATE; CONTROLLED STUDY; DNA BINDING MOTIF; GENETIC ASSOCIATION; GERM CELL; MONOSIGA BREVICOLIS; MOUSE; NEMATOSTELLA VECTENSIS; NONHUMAN; PROTEIN DOMAIN; RNA BINDING; SPONGE (PORIFERA); TRICHOPLAX ADHAERENS;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; EVOLUTION, MOLECULAR; GENOMICS; HUMANS; PHYLOGENY; PORIFERA; PROTEOMICS; RNA-BINDING PROTEINS;

AMPHIMEDON; ANIMALIA; BILATERIA; FUNGI; METAZOA; PLACOZOA;

EID: 79961091137     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr046     Document Type: Article

References (101)

1. Alié A, Leclère L, Jager M, Dayraud C, Chang P, Le Guyader H, Quéinnec E, Manuel M. 2010. Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of "germline genes" with stemness. Dev Biol. 350:183-197.
2. Alsford S, Kemp LE, Kawahara T, Horn D. 2010. RNA interference, growth and differentiation appear normal in African trypanosomes lacking Tudor staphylococcal nuclease. Mol Biochem Parasitol. 174:70-73.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
4. Amaral PP, Dinger ME, Mercer TR, Mattick JS. 2008. The eukaryotic genome as an RNA machine. Science 319:1787-1788.
5. Anantharaman V, Koonin EV, Aravind L. 2002. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res. 30:1427-1464. (Pubitemid 34679722)
6. Anisimova M, Gascuel O. 2006. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol. 55:539-552. (Pubitemid 43922340)
7. Aviv T, Lin Z, Lau S, Rendl LM, Sicheri F, Smibert CA. 2003. The RNA-binding SAM domain of Smaug defines a new family of post-transcriptional regulators. Nat Struct Biol. 10:614-621. (Pubitemid 36944714)
8. Baez MV, Boccaccio GL. 2005. Mammalian Smaug is a translational repressor that forms cytoplasmic foci similar to stress granules. J Biol Chem. 280:43131-43140. (Pubitemid 43049279)
9. Baines RA. 2005. Neuronal homeostasis through translational control. Mol Neurobiol. 32:113-121. (Pubitemid 41397180)
10. Barreau C, Paillard L, Méreau A, Osborne HB. 2006. Mammalian CELF/Bruno-like RNA-binding proteins: molecular characteristics and biological functions. Biochimie 88:515-525. (Pubitemid 43867902)
11. Begemann G, Paricio N, Artero R, Kiss I, Pérez-Alonso M, Mlodzik M. 1997. muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zincfinger-containing proteins. Development. 124:4321-4331. (Pubitemid 27496867)
12. Bork P, Dandekar T, Diaz-Lazcoz Y, Eisenhaber F, Huynen M, Yuan Y. 1998. Predicting function: from genes to genomes and back. J Mol Biol. 283:707-725. (Pubitemid 28495340)
13. Burd CG, Dreyfuss G. 1994. Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615-621. (Pubitemid 24268271)
14. Carmell MA, Xuan Z, Zhang MQ, Hannon GJ. 2002. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16:2733-2742. (Pubitemid 35253139)
15. Caudy AA, Ketting RF, Hammond SM, Denli AM, Bathoorn AM, Tops BB, Silva JM, Myers MM, Hannon GJ, Plasterk RH. 2003. A micrococcal nuclease homologue in RNAi effector complexes. Nature 425:411-414. (Pubitemid 37187271)
16. Caudy AA, Myers M, Hannon GJ, Hammond SM. 2002. Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16:2491-2496.
17. Chang JL, Lin HV, Blauwkamp TA, Cadigan KM. 2008. Spenito and Split ends act redundantly to promote Wingless signaling. Dev Biol. 314:100-111.
18. Chekulaeva M, Hentze MW, Ephrussi A. 2006. Bruno acts as a dual repressor of oskar translation, promoting mRNA oligomerization and formation of silencing particles. Cell 124:521-533. (Pubitemid 43199438)
19. Chen Y, Varani G. 2005. Protein families and RNA recognition. FEBS J. 272:2088-2097. (Pubitemid 40646780)
20. Chendrimada TP, Finn KJ, Ji X, Baillat D, Gregory RI, Liebhaber SA, Pasquinelli AE, Shiekhattar R. 2007. MicroRNA silencing through RISC recruitment of eIF6. Nature 447:823-828. (Pubitemid 46920131)
21. Chevenet F, Brun C, Bañuls AL, Jacq B, Christen R. 2006. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics. 7:439.
22. Chicoine J, Benoit P, Gamberi C, Paliouras M, Simonelig M, Lasko P. 2007. Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev Cell. 13:691-704. (Pubitemid 350011988)
23. Ciosk R, DePalma M, Priess JR. 2006. Translational regulators maintain totipotency in the Caenorhabditis elegans germline. Science 311:851-853. (Pubitemid 43228849)
24. Couvillion MT, Sachidanandam R, Collins K. 2010. A growthessential Tetrahymena Piwi protein carries tRNA fragment cargo. Genes Dev. 24:2742-2747.
25. Degnan BM, Vervoort M, Larroux C, Richards GS. 2009. Early evolution of metazoan transcription factors. Curr Opin Genet Dev. 19:591-599.
26. de Jong D, Eitel M, Jakob W, Osigus HJ, Hadrys H, Desalle R, Schierwater B. 2009. Multiple dicer genes in the early-diverging metazoa. Mol Biol Evol. 26:1333-1340.
27. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. 2004. Processing of primary microRNAs by the Microprocessor complex. Nature 432:231-235. (Pubitemid 39545854)
28. Dereeper A, Guignon V, Blanc G, et al. (12 co-authors). 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465-W469.
29. Deschênes-Furry J, Perrone-Bizzozero N, Jasmin BJ. 2006. The RNA-binding protein HuD: a regulator of neuronal differentiation, maintenance and plasticity. Bioessays 28:822-833. (Pubitemid 44433744)
30. Dill KK, Seaver EC. 2008. Vasa and nanos are coexpressed in somatic and germ line tissue from early embryonic cleavage stages through adulthood in the polychaete Capitella sp. I. Dev Genes Evol. 218:453-463.
31. dit Frey NF, Muller P, Jammes F, Kizis D, Leung J, Perrot-Rechenmann C, Bianchi MW. 2010. The RNA binding protein Tudor-SN is essential for stress tolerance and stabilizes levels of stress-responsive mRNAs encoding secreted proteins in Arabidopsis. Plant Cell. 22:1575-1591.
32. Draper BW, Mello CC, Bowerman B, Hardin J, Priess JR. 1996. MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 87:205-216. (Pubitemid 26358999)
33. Dreyfuss G, Kim VN, Kataoka N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol. 3:195-205.
34. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. (Pubitemid 38832724)
35. Extavour CG, Pang K, Matus DQ, Martindale MQ. 2005. vasa and nanos expression patterns in a sea anemone and the evolution of bilaterian germ cell specification mechanisms. Evol Dev. 7:201-215. (Pubitemid 40697767)
36. Feng Y, Bommer GT, Zhai Y, Akyol A, Hinoi T, Winer I, Lin HV, Cadigan KM, Cho KR, Fearon ER. 2007. Drosophila split ends homologue SHARP functions as a positive regulator of Wnt/β-Catenin/T-cell factor signaling in neoplastic transformation. Cancer Res. 6:485-491.
37. Gamberi C, Johnstone O, Lasko P. 2006. Drosophila RNA binding proteins. Int Rev Cytol. 248:43-139. (Pubitemid 43238170)
38. Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: an expanding universe. Nat Rev Genet. 10:94-108.
39. Glisovic T, Bachorik JL, Yong J, Dreyfuss G. 2008. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 582:1977-1986.
40. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 27:221-224.
41. Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP. 2008. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455:1193-1197.
42. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704. (Pubitemid 37365050)
43. Guindon S, Lethiec F, Duroux P, Gascuel O. 2005. PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33:W557-W559. (Pubitemid 44529983)
44. Guo T, Peters AH, Newmark PA. 2006. A Bruno-like gene is required for stem cell maintenance in planarians. Dev Cell. 11:159-169. (Pubitemid 44138497)
45. Gustafson EA, Wessel GM. 2010. Vasa genes: emerging roles in the germ line and in multipotent cells. Bioessays 32:626-637.
46. Hammond SM. 2005. Dicing and slicing: the core machinery of RNA interference pathway. FEBS Lett. 579:5822-5829. (Pubitemid 41484128)
47. He L, Hannon GJ. 2004. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 5:522-531. (Pubitemid 38868508)
48. Heinrichs V, Ryner LC, Baker BS. 1998. Regulation of sex-specific selection of fruitless 5' splice sites by transformer and transformer-2. Mol Cell Biol. 18:450-458. (Pubitemid 28021056)
49. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755. (Pubitemid 32851390)
50. Jaubert-Possamai S, Rispe C, Tanguy S, Gordon K, Walsh T, Edwards O, Tagu D. 2010. Expansion of the miRNA pathway in the hemipteran insect Acyrthosiphon pisum. Mol Biol Evol. 27:979-987.
51. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 8:275-282.
52. Kanadia RN, Johnstone KA, Mankodi A, Lungu C, Thornton CA, Esson D, Timmers AM, Hauswirth WW, Swanson MS. 2003. A muscleblind knockout model for myotonic dystrophy. Science 302:1978-1980. (Pubitemid 37523508)
53. Keene JD. 2001. Ribonucleoprotein infrastructure regulating the flow of genetic information between the genome and the proteome. Proc Natl Acad Sci U S A. 98:7018-7024. (Pubitemid 32567896)
54. Kim VN, Han J, Siomi MC. 2009. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol. 10:126-139.
55. King N, Westbrook MJ, Young SL, et al. (36 co-authors). 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783-788. (Pubitemid 351253174)
56. Kranz AM, Tollenaere A, Norris BJ, Degnan BM, Degnan SM. 2010. Identifying the germ-line in an equally cleaving mollusc: Vasa and Nanos expression during embryonic and larval development of the vetigastropod Haliotis asinina. J Exp Zool B (Mol Dev Evol). 314 B: 267-279.
57. Kuo MW, Wang SH, Chang JC, Chang CH, Huang LJ, Lin HH, Yu AL, Li WH, Yu J. 2009. A novel puf-A gene predicted from evolutionary analysis is involved in the development of eyes and primordial germ-cells. PLoS One. 4:e4980.
58. Larroux C, Luke GN, Koopman P, Rokhsar DS, Shimeld SM, Degnan BM. 2008. Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol. 25:980-996.
59. Lasko P. 2000. The Drosophila melanogaster genome: translation factors and RNA binding proteins. J Cell Biol. 150:F51-F56. (Pubitemid 30491346)
60. Lasko P. 2003. Gene regulation at the RNA layer: RNA binding proteins in intercellular signaling networks. Sci STKE. 2003: RE6.
61. Le SQ, Gascuel O. 2008. An improved general amino acid replacement matrix. Mol Biol Evol. 25:1307-1320. (Pubitemid 351882003)
62. Lee MH, Schedl T. 2006. RNA-binding proteins. WormBook. 1-13.
63. Li Y, Lin L, Jin P. 2008. The microRNA pathway and fragile X mental retardation protein. Biochim Biophys Acta. 1779:702-705.
64. Lukong KE, Chang KW, Khandjian EW, Richard S. 2008. RNA-binding proteins in human genetic disease. Trends Genet. 24:416-425.
65. Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U. 2004. Nuclear export of microRNA precursors. Science 303:95-98. (Pubitemid 38055779)
66. Lunde BM, Moore C, Varani G. 2007. RNA-binding proteins: modular design for efficient function. Nat Rev Mol Cell Biol. 8:479-490. (Pubitemid 46809150)
67. Maisonneuve C, Guilleret I, Vick P, Weber T, Andre P, Beyer T, Blum M, Constam DB. 2009. Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development 136:3019-3030.
68. Marlow HQ, Srivastava M, Matus DQ, Rokhsar D, Martindale MQ. 2009. Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev Neurobiol. 69:235-254.
69. McKee AE, Minet E, Stern C, Riahi S, Stiles CD, Silver PA. 2005. A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain. BMC Dev Biol. 5:14.
70. Miki T, Takano K, Yoneda Y. 2005. The role of mammalian Staufen on mRNA traffic: a view from its nucleocytoplasmic shuttling function. Cell Struct Funct. 30:51-56.
71. Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA. 2002. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 110:689-699. (Pubitemid 35283959)
72. Murphy D, Dancis B, Brown JR. 2008. The evolution of core proteins involved in microRNA biogenesis. BMC Evol Biol. 8:92.
73. Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T. 2005. Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res. 306:349-356. (Pubitemid 40732760)
74. Orphanides G, Reinberg D. 2002. A unified theory of gene expression. Cell 108:439-451. (Pubitemid 34260870)
75. Panopoulou G, Poustka AJ. 2005. Timing and mechanism of ancient vertebrate genome duplications-the adventure of a hypothesis. Trends Genet. 21:559-567. (Pubitemid 41278461)
76. Parisi M, Lin H. 2000. Translational repression: a duet of Nanos and Pumilio. Curr Biol. 10:R81-R83. (Pubitemid 30079188)
77. Pascale A, Amadio M, Quattrone A. 2008. Defining a neuron: neuronal ELAV proteins. Cell Mol Life Sci. 65:128-140. (Pubitemid 351152226)
78. Pascual M, Vicente M, Monferrer L, Artero R. 2006. The Muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing. Differentiation 74:65-80. (Pubitemid 43376167)
79. Philippe H, Derelle R, Lopez P, et al. (20 co-authors). 2009. Phylogenomics revives traditional views on deep animal relationships. Curr Biol. 19:706-712.
80. Pick KS, Philippe H, Schreiber F, et al. (11 co-authors). 2010. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol. 27:1983-1987.
81. Putnam NH, Srivastava M, Hellsten U, et al. (19 co-authors). 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86-94. (Pubitemid 47056460)
82. Rebscher N, Zelada-González F, Banisch TU, Raible F, Arendt D. 2007. Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. Dev Biol. 306:599-611. (Pubitemid 46873538)
83. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. (Pubitemid 37038874)
84. Rossi JJ. 2005. Mammalian Dicer finds a partner. EMBO Rep. 6:927-929. (Pubitemid 41521946)
85. Schoppmeier M, Fischer S, Schmitt-Engel C, Löhr U, Klingler M. 2009. An ancient anterior patterning system promotes caudal repression and head formation in ecdysozoa. Curr Biol. 19:1811-1815.
86. Shukla S, Fisher SA. 2008. Tra2beta as a novel mediator of vascular smooth muscle diversification. Circ Res. 103:485-492.
87. Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, Degnan BM, Vervoort M. 2007. Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol. 7:33.
88. Spassov DS, Jurecic R. 2003. The PUF family of RNA-binding proteins: does evolutionarily conserved structure equal conserved function? IUBMB Life. 55:359-66. (Pubitemid 37271093)
89. Srivastava M, Begovic E, Chapman J, et al. (21 co-authors). 2008. The Trichoplax genome and the nature of placozoans. Nature 454:955-960.
90. Srivastava M, Simakov O, Chapman J, et al. (33 co-authors). 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720-726.
91. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, Hughes TR, Westwood JT, Smibert CA, Lipshitz HD. 2007. SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell. 12:143-155. (Pubitemid 46002594)
92. Tam PP, Barrette-Ng IH, Simon DM, Tam MW, Ang AL, Muench DG. 2010. The Puf family of RNA-binding proteins in plants: phylogeny, structural modeling, activity and subcellular localization. BMC Plant Biol. 10:44.
93. Tatusov RL, Koonin EV, Lipman DJ. 1997. A genomic perspective on protein families. Science 278:631-637. (Pubitemid 27464953)
94. Thomson T, Lin H. 2009. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol. 25:355-376.
95. Tomari Y, Du T, Haley B, Schwarz DS, Bennett R, Cook HA, Koppetsch BS, Theurkauf WE, Zamore PD. 2004. RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 116:831-841. (Pubitemid 38410728)
96. Tran U, Pickney LM, Ozpolat BD, Wessely O. 2007. Xenopus Bicaudal-C is required for the differentiation of the amphibian pronephros. Dev Biol. 307:152-164. (Pubitemid 46900819)
97. Tsui S, Dai T, Roettger S, Schempp W, Salido EC, Yen PH. 2000. Identification of two novel proteins that interact with germcell-specific RNA-binding proteins DAZ and DAZL1. Genomics 65:266-273. (Pubitemid 30332030)
98. Wakabayashi-Ito N, Belvin MP, Bluestein DA, Anderson KV. 2001. fusilli, an essential gene with a maternal role in Drosophila embryonic dorsal-ventral patterning. Dev Biol. 229:44-54. (Pubitemid 32061713)
99. Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP. 2009. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol Cell. 33:591-601.
100. Warzecha CC, Shen S, Xing Y, Carstens RP. 2009. The epithelial splicing factors ESRP1 and ESRP2 positively and negatively regulate diverse types of alternative splicing events. RNA Biol. 6:546-562.
101. Wiellette EL, Harding KW, Mace KA, Ronshaugen MR, Wang FY, McGinnis W. 1999. spen encodes an RNP motif protein that interacts with Hox pathways to repress the development of head-like sclerites in the Drosophila trunk. Development 126:5373-5385. (Pubitemid 30015930)