A widely employed germ cell marker is an ancient disordered protein with reproductive functions in diverse eukaryotes
Tóm tắt
The advent of sexual reproduction and the evolution of a dedicated germline in multicellular organisms are critical landmarks in eukaryotic evolution. We report an ancient family of GCNA (germ cell nuclear antigen) proteins that arose in the earliest eukaryotes, and feature a rapidly evolving intrinsically disordered region (IDR). Phylogenetic analysis reveals that GCNA proteins emerged before the major eukaryotic lineages diverged; GCNA predates the origin of a dedicated germline by a billion years. Gcna gene expression is enriched in reproductive cells across eukarya – either just prior to or during meiosis in single-celled eukaryotes, and in stem cells and germ cells of diverse multicellular animals. Studies of Gcna-mutant C. elegans and mice indicate that GCNA has functioned in reproduction for at least 600 million years. Homology to IDR-containing proteins implicated in DNA damage repair suggests that GCNA proteins may protect the genomic integrity of cells carrying a heritable genome.
Từ khóa
Tài liệu tham khảo
Abascal, 2005, ProtTest: selection of best-fit models of protein evolution, Bioinformatics, 21, 2104, 10.1093/bioinformatics/bti263
Akbudak, 2011, Improved FLP recombinase, FLPe, efficiently removes marker gene from transgene locus developed by Cre-lox mediated site-specific gene integration in rice, Molecular Biotechnology, 49, 82, 10.1007/s12033-011-9381-y
Balakirev, 2015, Wss1 metalloprotease partners with Cdc48/Doa1 in processing genotoxic SUMO conjugates, eLife, 4, e06763, 10.7554/eLife.06763
Bartholmes, 2012, Evolution of the YABBY gene family with emphasis on the basal eudicot Eschscholzia californica (Papaveraceae), Plant Biology, 14, 11, 10.1111/j.1438-8677.2011.00486.x
Baudat, 2013, Meiotic recombination in mammals: localization and regulation, Nature Reviews. Genetics, 14, 794, 10.1038/nrg3573
Benkert, 2011, Toward the estimation of the absolute quality of individual protein structure models, Bioinformatics, 27, 343, 10.1093/bioinformatics/btq662
Bjellqvist, 1993, The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences, Electrophoresis, 14, 1023, 10.1002/elps.11501401163
Bosch, 2010, The Hydra polyp: nothing but an active stem cell community, Development, Growth & Differentiation, 52, 15, 10.1111/j.1440-169X.2009.01143.x
Bowman, 1999, CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains, Development, 126, 2387, 10.1242/dev.126.11.2387
Brown, 2010, Comparing models of evolution for ordered and disordered proteins, Molecular Biology and Evolution, 27, 609, 10.1093/molbev/msp277
Cartwright, 2007, Fossils and phylogenies: integrating multiple lines of evidence to investigate the origin of early major metazoan lineages, Integrative and Comparative Biology, 47, 744, 10.1093/icb/icm071
Centore, 2012, Spartan/C1orf124, a reader of PCNA ubiquitylation and a regulator of UV-induced DNA damage response, Molecular Cell, 46, 625, 10.1016/j.molcel.2012.05.020
Cerutti, 2006, On the origin and functions of RNA-mediated silencing: from protists to man, Current Genetics, 50, 81, 10.1007/s00294-006-0078-x
Chebaro, 2015, Intrinsically disordered energy landscapes, Scientific Reports, 5, 10386, 10.1038/srep10386
Colaiácovo, 2003, Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination, Developmental Cell, 5, 463, 10.1016/S1534-5807(03)00232-6
Colaiácovo, 2002, A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline, Genetics, 162, 113, 10.1093/genetics/162.1.113
Davey, 2015, Short linear motifs - ex nihilo evolution of protein regulation, Cell Communication and Signaling, 13, 43, 10.1186/s12964-015-0120-z
Davis, 2012, DVC1 (C1orf124) recruits the p97 protein segregase to sites of DNA damage, Nature Structural & Molecular Biology, 19, 1093, 10.1038/nsmb.2394
Dinkel, 2016, ELM 2016--data update and new functionality of the eukaryotic linear motif resource, Nucleic Acids Research, 44, D294, 10.1093/nar/gkv1291
Dosztányi, 2005, IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content, Bioinformatics, 21, 3433, 10.1093/bioinformatics/bti541
Dunker, 2015, Intrinsically disordered proteins and multicellular organisms, Seminars in Cell & Developmental Biology, 37, 44, 10.1016/j.semcdb.2014.09.025
Dunker, 2000, Intrinsic protein disorder in complete genomes, Genome Informatics. Workshop on Genome Informatics, 11, 161
Eddy, 2009, A new generation of homology search tools based on probabilistic inference, Genome Informatics. International Conference on Genome Informatics, 23, 205, 10.1142/9781848165632_0019
Edgar, 2004, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Research, 32, 1792, 10.1093/nar/gkh340
Eirín-López, 2011, Boule and the Evolutionary Origin of Metazoan Gametogenesis: A Grandpa's Tale, International Journal of Evolutionary Biology, 2011, 972457, 10.4061/2011/972457
Enders, 1994, Developmentally regulated expression of a mouse germ cell nuclear antigen examined from embryonic day 11 to adult in male and female mice, Developmental Biology, 163, 331, 10.1006/dbio.1994.1152
Ewen-Campen, 2010, The molecular machinery of germ line specification, Molecular Reproduction and Development, 77, 3, 10.1002/mrd.21091
Extavour, 2003, Mechanisms of germ cell specification across the metazoans: epigenesis and preformation, Development, 130, 5869, 10.1242/dev.00804
Graveley, 2011, The developmental transcriptome of Drosophila melanogaster, Nature, 471, 473, 10.1038/nature09715
Guindon, 2010, New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0, Systematic Biology, 59, 307, 10.1093/sysbio/syq010
He, 2009, Predicting intrinsic disorder in proteins: an overview, Cell Research, 19, 929, 10.1038/cr.2009.87
He, 2014, An alternative root for the eukaryote tree of life, Current Biology , 24, 465, 10.1016/j.cub.2014.01.036
Hedges, 2006, TimeTree: a public knowledge-base of divergence times among organisms, Bioinformatics, 22, 2971, 10.1093/bioinformatics/btl505
Hedglin, 2015, Regulation of Rad6/Rad18 activity during DNA damage tolerance, Annual Review of Biophysics, 44, 207, 10.1146/annurev-biophys-060414-033841
Hegyi, 2012, Increased structural disorder of proteins encoded on human sex chromosomes, Molecular BioSystems, 8, 229, 10.1039/c1mb05285c
Hemmrich, 2012, Molecular signatures of the three stem cell lineages in hydra and the emergence of stem cell function at the base of multicellularity, Molecular Biology and Evolution, 29, 3267, 10.1093/molbev/mss134
Hopman, 1998, Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochrome-labeled tyramides and their application for In situ hybridization using CARD amplification, Journal of Histochemistry & Cytochemistry, 46, 771, 10.1177/002215549804600611
Hu, 2015, Licensing of Primordial Germ Cells for Gametogenesis Depends on Genital Ridge Signaling, PLOS Genetics, 11, e1005019, 10.1371/journal.pgen.1005019
Hu, 2013, Gata4 is required for formation of the genital ridge in mice, PLoS Genetics, 9, e1003629, 10.1371/journal.pgen.1003629
Huntley, 2000, Evolution of simple sequence in proteins, Journal of Molecular Evolution, 51, 131, 10.1007/s002390010073
Inoue, 2011, Expression of a Testis-Specific Nuclear Protein, TRA98, in Mouse Testis during Spermatogenesis. A Quantitative and Qualitative Immunoelectron Microscopy (IEM) Analysis, Open Journal of Cell Biology, 01, 11, 10.4236/ojcb.2011.11002
Juhasz, 2012, Characterization of human Spartan/C1orf124, an ubiquitin-PCNA interacting regulator of DNA damage tolerance, Nucleic Acids Research, 40, 10795, 10.1093/nar/gks850
Juliano, 2010, A conserved germline multipotency program, Development, 137, 4113, 10.1242/dev.047969
Keeney, 2008, Spo11 and the formation of DNA double-strand breaks in Meiosis, Genome Dynamics and Stability, 2, 81, 10.1007/7050_2007_026
Kerner, 2011, Evolution of RNA-binding proteins in animals: insights from genome-wide analysis in the sponge Amphimedon queenslandica, Molecular Biology and Evolution, 28, 2289, 10.1093/molbev/msr046
Kim, 2014, A co-CRISPR strategy for efficient genome editing in Caenorhabditis elegans, Genetics, 197, 1069, 10.1534/genetics.114.166389
Kim, 2013, Regulation of error-prone translesion synthesis by Spartan/C1orf124, Nucleic Acids Research, 41, 1661, 10.1093/nar/gks1267
King, 2013, In situ hybridization protocol for enhanced detection of gene expression in the planarian Schmidtea mediterranea, BMC Developmental Biology, 13, 8, 10.1186/1471-213X-13-8
Kohara, 1998, NEXTDB: The expression pattern map database for C. elegans, Genome Inform, 1998, 222
Kumar, 2010, Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice, Genes & Development, 24, 1266, 10.1101/gad.571710
Littlefield, 1985, Germ cells in Hydra oligactis males. I. Isolation of a subpopulation of interstitial cells that is developmentally restricted to sperm production, Developmental Biology, 112, 185, 10.1016/0012-1606(85)90132-0
Lécuyer, 2007, Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function, Cell, 131, 174, 10.1016/j.cell.2007.08.003
López-Pelegrín, 2013, A novel family of soluble minimal scaffolds provides structural insight into the catalytic domains of integral membrane metallopeptidases, The Journal of Biological Chemistry, 288, 21279, 10.1074/jbc.M113.476580
Maatouk, 2006, DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages, Development, 133, 3411, 10.1242/dev.02500
Machida, 2012, Spartan/C1orf124 is important to prevent UV-induced mutagenesis, Cell Cycle, 11, 3395, 10.4161/cc.21694
Mata, 2002, The transcriptional program of meiosis and sporulation in fission yeast, Nature Genetics, 32, 143, 10.1038/ng951
Matzuk, 2002, Genetic dissection of mammalian fertility pathways, Nature Cell Biology, 4, S33, 10.1038/ncb-nm-fertilityS41
Melo, 2002, Statistical potentials for fold assessment, Protein Science: A Publication of the Protein Society, 11, 430, 10.1002/pro.110430
Moore, 2013, Quantification and functional analysis of modular protein evolution in a dense phylogenetic tree, Biochimica Et Biophysica Acta, 1834, 898, 10.1016/j.bbapap.2013.01.007
Morelli, 2005, Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis, Reproduction, 130, 761, 10.1530/rep.1.00865
Mosbech, 2012, DVC1 (C1orf124) is a DNA damage-targeting p97 adaptor that promotes ubiquitin-dependent responses to replication blocks, Nature Structural & Molecular Biology, 19, 1084, 10.1038/nsmb.2395
Mueller, 2013, Independent specialization of the human and mouse X chromosomes for the male germ line, Nature Genetics, 45, 1083, 10.1038/ng.2705
Ning, 2013, Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates, Genes & Development, 27, 1198, 10.1101/gad.212746.112
Nolte, 2001, ACRC codes for a novel nuclear protein with unusual acidic repeat tract and maps to DYT3 (dystonia parkinsonism) critical interval in xq13.1, Neurogenetics, 3, 207, 10.1007/s100480100120
Parfrey, 2011, Estimating the timing of early eukaryotic diversification with multigene molecular clocks, PNAS, 108, 13624, 10.1073/pnas.1110633108
Peterson, 2008, The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records, Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 1435, 10.1098/rstb.2007.2233
Ramesh, 2005, A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis, Current Biology , 15, 185, 10.1016/j.cub.2005.01.003
Ramsköld, 2009, An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data, PLoS Computational Biology, 5, e1000598, 10.1371/journal.pcbi.1000598
Reinke, 2004, Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans, Development, 131, 311, 10.1242/dev.00914
Rice, 2000, EMBOSS: the European molecular biology open software suite, Trends in Genetics, 16, 276, 10.1016/S0168-9525(00)02024-2
Robinson, 2013, FlyAtlas: database of gene expression in the tissues of Drosophila melanogaster, Nucleic Acids Research, 41, D744, 10.1093/nar/gks1141
Roest, 1996, Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification, Cell, 86, 799, 10.1016/S0092-8674(00)80154-3
Shabalina, 2008, Origins and evolution of eukaryotic RNA interference, Trends in Ecology & Evolution, 23, 578, 10.1016/j.tree.2008.06.005
Simpson, 2004, The real 'kingdoms' of eukaryotes, Current Biology , 14, R693, 10.1016/j.cub.2004.08.038
Skarnes, 2011, A conditional knockout resource for the genome-wide study of mouse gene function, Nature, 474, 337, 10.1038/nature10163
Srivastava, 2014, Whole-body acoel regeneration is controlled by Wnt and Bmp-Admp signaling, Current Biology, 24, 1107, 10.1016/j.cub.2014.03.042
Stingele, 2015, DNA-protein crosslink repair: proteases as DNA repair enzymes, Trends in Biochemical Sciences, 40, 67, 10.1016/j.tibs.2014.10.012
Stingele, 2014, A DNA-dependent protease involved in DNA-protein crosslink repair, Cell, 158, 327, 10.1016/j.cell.2014.04.053
Swarts, 2014, The evolutionary journey of Argonaute proteins, Nature Structural & Molecular Biology, 21, 743, 10.1038/nsmb.2879
Söding, 2005, The HHpred interactive server for protein homology detection and structure prediction, Nucleic Acids Research, 33, W244, 10.1093/nar/gki408
Tanaka, 2000, The mouse homolog of Drosophila Vasa is required for the development of male germ cells, Genes & Development, 14, 841, 10.1101/gad.14.7.841
Tantos, 2012, Intrinsic disorder in cell signaling and gene transcription, Molecular and Cellular Endocrinology, 348, 457, 10.1016/j.mce.2011.07.015
Tomancak, 2002, Systematic determination of patterns of gene expression during Drosophila embryogenesis, Genome Biology, 3, RESEARCH0088, 10.1186/gb-2002-3-12-research0088
Tompa, 2003, Intrinsically unstructured proteins evolve by repeat expansion, BioEssays, 25, 847, 10.1002/bies.10324
Uanschou, 2007, A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene, The EMBO Journal, 26, 5061, 10.1038/sj.emboj.7601913
Uversky, 2000, Why are "natively unfolded" proteins unstructured under physiologic conditions?, Proteins: Structure, Function, and Genetics, 41, 415, 10.1002/1097-0134(20001115)41:3<415::AID-PROT130>3.0.CO;2-7
Vacic, 2007, Composition Profiler: a tool for discovery and visualization of amino acid composition differences, BMC Bioinformatics, 8, 211, 10.1186/1471-2105-8-211
van der Lee, 2014, Classification of intrinsically disordered regions and proteins, Chemical Reviews, 114, 6589, 10.1021/cr400525m
van Wolfswinkel, 2014, Single-cell analysis reveals functionally distinct classes within the planarian stem cell compartment, Cell Stem Cell, 15, 326, 10.1016/j.stem.2014.06.007
Waterhouse, 2009, Jalview Version 2--a multiple sequence alignment editor and analysis workbench, Bioinformatics, 25, 1189, 10.1093/bioinformatics/btp033
Wheeler, 2014, Skylign: a tool for creating informative, interactive logos representing sequence alignments and profile hidden Markov models, BMC Bioinformatics, 15, 7, 10.1186/1471-2105-15-7
Wright, 1999, Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm, Journal of Molecular Biology, 293, 321, 10.1006/jmbi.1999.3110
Xie, 2007, Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions, Journal of Proteome Research, 6, 1882, 10.1021/pr060392u
Yang, 2015, The I-TASSER Suite: protein structure and function prediction, Nature Methods, 12, 7, 10.1038/nmeth.3213
Ye, 2004, FATCAT: a web server for flexible structure comparison and structure similarity searching, Nucleic Acids Research, 32, W582, 10.1093/nar/gkh430