Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery


Autoři: Alberto Pérez-Posada aff001;  Omaya Dudin aff001;  Eduard Ocaña-Pallarès aff001;  Iñaki Ruiz-Trillo aff001;  Andrej Ondracka aff001
Působiště autorů: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Catalonia, Spain aff001;  Departament de Genètica, Microbiologia i Estadística, Universitat de Barcelona, Barcelona, Catalonia, Spain aff002;  ICREA, Barcelona, Catalonia, Spain aff003
Vyšlo v časopise: Cell cycle transcriptomics of Capsaspora provides insights into the evolution of cyclin-CDK machinery. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008584
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008584

Souhrn

Progression through the cell cycle in eukaryotes is regulated on multiple levels. The main driver of the cell cycle progression is the periodic activity of cyclin-dependent kinase (CDK) complexes. In parallel, transcription during the cell cycle is regulated by a transcriptional program that ensures the just-in-time gene expression. Many core cell cycle regulators are widely conserved in eukaryotes, among them cyclins and CDKs; however, periodic transcriptional programs are divergent between distantly related species. In addition, many otherwise conserved cell cycle regulators have been lost and independently evolved in yeast, a widely used model organism for cell cycle research. For a better understanding of the evolution of the cell cycle regulation in opisthokonts, we investigated the transcriptional program during the cell cycle of the filasterean Capsaspora owczarzaki, a unicellular species closely related to animals. We developed a protocol for cell cycle synchronization in Capsaspora cultures and assessed gene expression over time across the entire cell cycle. We identified a set of 801 periodic genes that grouped into five clusters of expression over time. Comparison with datasets from other eukaryotes revealed that the periodic transcriptional program of Capsaspora is most similar to that of animal cells. We found that orthologues of cyclin A, B and E are expressed at the same cell cycle stages as in human cells and in the same temporal order. However, in contrast to human cells where these cyclins interact with multiple CDKs, Capsaspora cyclins likely interact with a single ancestral CDK1-3. Thus, the Capsaspora cyclin-CDK system could represent an intermediate state in the evolution of animal-like cyclin-CDK regulation. Overall, our results demonstrate that Capsaspora could be a useful unicellular model system for animal cell cycle regulation.

Klíčová slova:

Cell cycle and cell division – Cyclins – DNA transcription – Eukaryota – Gene expression – Gene regulation – Saccharomyces cerevisiae – Transcriptional control


Zdroje

1. Morgan DO. Cell Cycle: Principles of Control. Yale J Biol Med. 2007. doi: 10.1093/icb/icm066

2. Medina EM, Turner JJ, Gordân R, Skotheim JM, Buchler NE. Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi. Elife. 2016;5: 1–23. doi: 10.7554/eLife.09492 27162172

3. Cross FR, Buchler NE, Skotheim JM. Evolution of networks and sequences in eukaryotic cell cycle control. Philos Trans R Soc B Biol Sci. 2011;366: 3532–3544. doi: 10.1098/rstb.2011.0078 22084380

4. Cao L, Chen F, Yang X, Xu W, Xie J, Yu L. Phylogenetic analysis of CDK and cyclin proteins in premetazoan lineages. BMC Evol Biol. 2014. doi: 10.1186/1471-2148-14-10 24433236

5. Li Z. Regulation of the Cell Division Cycle in Trypanosoma brucei. Eukaryot Cell. 2012;11: 1180–1190. doi: 10.1128/EC.00145-12 22865501

6. Gutierrez C. The Arabidopsis Cell Division Cycle. Arab B. 2009. 22303246

7. Nieduszynski CA, Murray J, Carrington M. Whole-genome analysis of animal A- and B-type cyclins. Genome Biol. 2002. doi: 10.1186/gb-2002-3-12-research0070 12537559

8. Satyanarayana A, Kaldis P. Mammalian cell-cycle regulation: Several cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene. 2009. doi: 10.1038/onc.2009.170 19561645

9. Matsushime H, Roussel MF, Ashmun RA, Sherr CJ. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell. 1991;65: 701–713. doi: 10.1016/0092-8674(91)90101-4 1827757

10. Matsushime H, Quelle DE, Shurtleff SA, Shibuya M, Sherr CJ, Kato JY. D-type cyclin-dependent kinase activity in mammalian cells. Mol Cell Biol. 2015;14: 2066–2076. doi: 10.1128/mcb.14.3.2066 8114738

11. Klein EA, Assoian RK. Transcriptional regulation of the cyclin D1 gene at a glance. J Cell Sci. 2008;121: 3853–3857. doi: 10.1242/jcs.039131 19020303

12. Cook JG, Park CH, Burke TW, Leone G, DeGregori J, Engel A, et al. Analysis of Cdc6 function in the assembly of mammalian prereplication complexes. Proc Natl Acad Sci U S A. 2002;99: 1347–1352. doi: 10.1073/pnas.032677499 11805305

13. Coverley D, Laman H, Laskey RA. Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Nat Cell Biol. 2002. doi: 10.1038/ncb813 12080347

14. Pomerening JR, Sontag ED, Ferrell JE. Building a cell cycle oscillator: Hysteresis and bistability in the activation of Cdc2. Nat Cell Biol. 2003. doi: 10.1038/ncb954 12629549

15. Pomerening JR, Sun YK, Ferrell JE. Systems-level dissection of the cell-cycle oscillator: Bypassing positive feedback produces damped oscillations. Cell. 2005;122: 565–578. doi: 10.1016/j.cell.2005.06.016 16122424

16. Mendenhall MD, Hodge aE. Regulation of CDC28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1998.

17. Bloom J, Cross FR. Multiple levels of cyclin specificity in cell-cycle control. Nature Reviews Molecular Cell Biology. 2007. doi: 10.1038/nrm2105 17245415

18. Cross FR, Tinkelenberg AH. A potential positive feedback loop controlling CLN1 and CLN2 gene expression at the start of the yeast cell cycle. Cell. 1991;65: 875–883. doi: 10.1016/0092-8674(91)90394-e 2040016

19. Nasmyth K, Dirick L. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell. 1991;66: 995–1013. doi: 10.1016/0092-8674(91)90444-4 1832338

20. Richardson HE, Wittenberg C, Cross F, Reed SI. An essential G1 function for cyclin-like proteins in yeast. Cell. 1989;59: 1127–1133. doi: 10.1016/0092-8674(89)90768-x 2574633

21. Skotheim JM, Di Talia S, Siggia ED, Cross FR. Positive feedback of G1 cyclins ensures coherent cell cycle entry. Nature. 2008;454: 291–296. doi: 10.1038/nature07118 18633409

22. Epstein CB, Cross FR. CLB5: A novel B cyclin from budding yeast with a role in S phase. Genes Dev. 1992;6: 1695–1706. doi: 10.1101/gad.6.9.1695 1387626

23. Schwob E, Nasmyth K. CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev. 1993;7: 1160–1175. doi: 10.1101/gad.7.7a.1160 8319908

24. Surana U, Robitsch H, Price C, Schuster T, Fitch I, Futcher AB, et al. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell. 1991;65: 145–161. doi: 10.1016/0092-8674(91)90416-v 1849457

25. Richardson H, Lew DJ, Henze M, Sugimoto K, Reed SI. Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2. Genes Dev. 1992;6: 2021–2034. doi: 10.1101/gad.6.11.2021 1427070

26. Martin-Castellanos C, Labib K, Moreno S. B-type cyclins regulate G1 progression in fission yeast in opposition to the p25rum1 cdk inhibitor. EMBO J. 1996;15: 839–49. Available: http://www.ncbi.nlm.nih.gov/pubmed/8631305%0Ahttp://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC450282 8631305

27. Mondesert O, McGowan CH, Russell P. Cig2, a B-type cyclin, promotes the onset of S in Schizosaccharomyces pombe. Mol Cell Biol. 2015;16: 1527–1533. doi: 10.1128/mcb.16.4.1527 8657126

28. Booher R, Beach D. Involvement of cdc13+ in mitotic control in Schizosaccharomyces pombe: possible interaction of the gene product with microtubules. EMBO J. 1988. doi: 10.1002/j.1460-2075.1988.tb03075.x

29. Booher RN, Alfa CE, Hyams JS, Beach DH. The fission yeast cdc2/cdc13/suc1 protein kinase: Regulation of catalytic activity and nuclear localization. Cell. 1989. doi: 10.1016/0092-8674(89)90429-7

30. Coudreuse D, Nurse P. Driving the cell cycle with a minimal CDK control network. Nature. 2010. doi: 10.1038/nature09543 21179163

31. Goodrich DW, Wang NP, Qian YW, Lee EYHP, Lee WH. The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle. Cell. 1991. doi: 10.1016/0092-8674(91)90181-W

32. Grant GD, Brooks L, Zhang X, Mahoney JM, Martyanov V, Wood TA, et al. Identification of cell cycle-regulated genes periodically expressed in U2OS cells and their regulation by FOXM1 and E2F transcription factors. Mol Biol Cell. 2013;24: 3634–3650. doi: 10.1091/mbc.E13-05-0264 24109597

33. Ishida S, Huang E, Zuzan H, Spang R, Leone G, West M, et al. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cell Biol. 2001;21: 4684–4699. doi: 10.1128/MCB.21.14.4684-4699.2001 11416145

34. Iyer VR, Horak CE, Scafe CS, Botstein D, Snyder M, Brown PO. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature. 2001;409: 533–538. doi: 10.1038/35054095 11206552

35. Gefeng Z, Spellman PT, Volpe T, Brown PO, Botstein D, Davis TN, et al. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature. 2000;406: 90–94. doi: 10.1038/35017581 10894548

36. Reynolds D, Shi BJ, McLean C, Katsis F, Kemp B, Dalton S. Recruitment of Thr 319-phosphorylated Ndd1p to the FHA domain of Fkh2p requires C1b kinase activity: A mechanism for CLB cluster gene activation. Genes Dev. 2003;17: 1789–1802. doi: 10.1101/gad.1074103 12865300

37. Pramila T, Wu W, Miles S, Noble WS, Breeden LL. The Forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes Dev. 2006. doi: 10.1101/gad.1450606 16912276

38. Laoukili J, Kooistra MRH, Brás A, Kauw J, Kerkhoven RM, Morrison A, et al. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol. 2005. doi: 10.1038/ncb1217 15654331

39. Iyer VR, Eisen MB, Ross DT, Schuler G, Moore T, Lee JCF, et al. The transcriptional program in the response of human fibroblasts to serum. Science (80-). 1999;283: 83–87. doi: 10.1126/science.283.5398.83 9872747

40. Kelliher CM, Leman AR, Sierra CS, Haase SB. Investigating Conservation of the Cell-Cycle-Regulated Transcriptional Program in the Fungal Pathogen, Cryptococcus neoformans. PLoS Genet. 2016;12: 1–23. doi: 10.1371/journal.pgen.1006453 27918582

41. Zones JM, Blaby IK, Merchant SS, Umen JG. High-Resolution Profiling of a Synchronized Diurnal Transcriptome from Chlamydomonas reinhardtii Reveals Continuous Cell and Metabolic Differentiation. Plant Cell. 2015;27: 2743–2769. 26432862

42. Peña-Diaz J, Hegre SA, Anderssen E, Aas PA, Mjelle R, Gilfillan GD, et al. Transcription profiling during the cell cycle shows that a subset of Polycomb-targeted genes is upregulated during DNA replication. Nucleic Acids Res. 2013;41: 2846–2856. doi: 10.1093/nar/gks1336 23325852

43. Dominguez D, Tsai YH, Gomez N, Jha DK, Davis I, Wang Z. A high-resolution transcriptome map of cell cycle reveals novel connections between periodic genes and cancer. Cell Res. 2016;26: 946–962. doi: 10.1038/cr.2016.84 27364684

44. Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, Alexander KE, et al. Identification of Genes Periodically Expressed in the Human Cell Cycle and Their Expression in Tumors. Mol Biol Cell. 2002;13: 1977–2000. doi: 10.1091/mbc.02-02-0030 12058064

45. Cho RJ, Huang M, Campbell MJ, Dong H, Steinmetz L, Sapinoso L, et al. Transcriptional regulation and function during the human cell cycle. Nat Genet. 2001. doi: 10.1038/83751 11137997

46. Bar-Joseph Z, Siegfried Z, Brandeis M, Brors B, Lu Y, Eils R, et al. Genome-wide transcriptional analysis of the human cell cycle identifies genes differentially regulated in normal and cancer cells. Proc Natl Acad Sci. 2008. doi: 10.1073/pnas.0704723105 18195366

47. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, et al. Comprehensive Identification of Cell Cycle-regulated Genes of the Yeast Saccharomyces cerevisiae by Microarray Hybridization. Mol Biol Cell. 1998. doi: 10.1091/mbc.9.12.3273 9843569

48. Orlando DA, Lin CY, Bernard A, Wang JY, Socolar JES, Iversen ES, et al. Global control of cell-cycle transcription by coupled CDK and network oscillators. Nature. 2008;453: 944–947. doi: 10.1038/nature06955 18463633

49. Menges M, Hennig L, Gruissem W, Murray JAH. Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol. 2003;53: 423–442. doi: 10.1023/B:PLAN.0000019059.56489.ca 15010610

50. Breyne P, Dreesen R, Vandepoele K, De Veylder L, Van Breusegem F, Callewaert L, et al. Transcriptome analysis during cell division in plants. Proc Natl Acad Sci. 2002;99: 14825–14830. doi: 10.1073/pnas.222561199 12393816

51. Jensen LJ, Jensen TS, De Lichtenberg U, Brunak S, Bork P. Co-evolution of transcriptional and post-translational cell-cycle regulation. Nature. 2006;443: 594–597. doi: 10.1038/nature05186 17006448

52. Giotti B, Joshi A, Freeman TC. Meta-analysis reveals conserved cell cycle transcriptional network across multiple human cell types. BMC Genomics. 2017. doi: 10.1186/s12864-016-3435-2 28056781

53. Rhind N, Russell P. Chk1 and Cds1: linchpins of the DNA damage and replication checkpoint pathways. J Cell Sci. 2000;113 (Pt 2: 3889–96. Available: http://www.ncbi.nlm.nih.gov/pubmed/11058076%0Ahttp://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC2863124

54. Cooper K. Rb, whi it’s not just for metazoans anymore. Oncogene. 2006;25: 5228–5232. doi: 10.1038/sj.onc.1209630 16936741

55. Kearsey SE, Cotterill S. Enigmatic variations: Divergent modes of regulating eukaryotic DNA replication. Molecular Cell. 2003. pp. 1067–1075. doi: 10.1016/S1097-2765(03)00441-6

56. Ferrer-Bonet M, Ruiz-Trillo I. Capsaspora owczarzaki. Current Biology. 2017. doi: 10.1016/j.cub.2017.05.074 28898640

57. Hertel LA, Bayne CJ, Loker ES. The symbiont Capsaspora owczarzaki, nov. gen. nov. sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea. Int J Parasitol. 2002;32: 1183–1191. doi: 10.1016/s0020-7519(02)00066-8 12117501

58. Ruiz-Trillo I, Inagaki Y, Davis LA, Sperstad S, Landfald B, Roger AJ. Capsaspora owczarzaki is an independent opisthokont lineage. Curr Biol. 2004;14: R946–R947. doi: 10.1016/j.cub.2004.10.037 15556849

59. Suga H, Chen Z, de Mendoza A, Sebé-Pedrós A, Brown MW, Kramer E, et al. The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun. 2013;4: 1–9. doi: 10.1038/ncomms3325 23942320

60. Sebé-Pedrós A, Ballaré C, Parra-Acero H, Chiva C, Tena JJ, Sabidó E, et al. The Dynamic Regulatory Genome of Capsaspora and the Origin of Animal Multicellularity. Cell. 2016;165: 1224–1237. doi: 10.1016/j.cell.2016.03.034 27114036

61. Sebé-Pedrós A, Peña MI, Capella-Gutiérrez S, Antó M, Gabaldón T, Ruiz-Trillo II, et al. High-Throughput Proteomics Reveals the Unicellular Roots of Animal Phosphosignaling and Cell Differentiation. Dev Cell. 2016;39: 186–197. doi: 10.1016/j.devcel.2016.09.019 27746046

62. Sebé-Pedrós A, Irimia M, del Campo J, Parra-Acero H, Russ C, Nusbaum C, et al. Regulated aggregative multicellularity in a close unicellular relative of metazoa. Elife. 2013;2: 1–20. doi: 10.7554/eLife.01287 24368732

63. Parra-Acero H, Ros-Rocher N, Perez-Posada A, Kożyczkowska A, Sánchez-Pons N, Nakata A, et al. Transfection of Capsaspora owczarzaki, a close unicellular relative of animals. Dev. 2018;145. doi: 10.1242/dev.162107 29752387

64. Banfalvi G. Cell Cycle Synchronization Methods and Protocols. Methods in molecular biology (Clifton, N.J.). 2011.

65. Blajeski AL, Phan VA, Kottke TJ, Kaufmann SH. G1 and G2 cell-cycle arrest following microtubule depolymerization in human breast cancer cells. J Clin Invest. 2002. doi: 10.1172/JCI13275 12093892

66. Jackman J, O’Connor PM. Methods for Synchronizing Cells at Specific Stages of the Cell Cycle. Current Protocols in Cell Biology. 2001.

67. Slater ML. Effect of reversible inhibition of deoxyribonucleic acid synthesis on the yeast cell cycle. J Bacteriol. 1973.

68. Fox MH, Read RA, Bedford JS. Comparison of synchronized Chinese hamster ovary cells obtained by mitotic shake-off, hydroxyurea, aphidicolin, or methotrexate. Cytometry. 1987. doi: 10.1002/cyto.990080312 3109858

69. Singh A, Agarwal A, Xu Y jie. Novel Cell-killing mechanisms of hydroxyurea and the implication toward combination therapy for the treatment of fungal infections. Antimicrob Agents Chemother. 2017. doi: 10.1128/AAC.00734-17 28893786

70. Aubin JE, Weber K, Osborn M. Analysis of actin and microfilament-associated proteins in the mitotic spindle and cleavage furrow of PtK2 cells by immunofluorescence microscopy. A critical note. Exp Cell Res. 1979. doi: 10.1016/0014-4827(79)90260-X

71. Cadart C, Zlotek-Zlotkiewicz E, Le Berre M, Piel M, Matthews HK. Exploring the function of cell shape and size during mitosis. Dev Cell. 2014;29: 159–169. doi: 10.1016/j.devcel.2014.04.009 24780736

72. Cramer LP, Mitchison TJ. Investigation of the mechanism of retraction of the cell margin and rearward flow of nodules during mitotic cell rounding. Mol Biol Cell. 1997. doi: 10.1091/mbc.8.1.109 9017599

73. Harris A. Location of cellular adhesions to solid substrata. Dev Biol. 1973. doi: 10.1016/0012-1606(73)90009-2

74. Kunda P, Pelling AE, Liu T, Baum B. Moesin Controls Cortical Rigidity, Cell Rounding, and Spindle Morphogenesis during Mitosis. Curr Biol. 2008. doi: 10.1016/j.cub.2007.12.051 18207738

75. Luxenburg C, Amalia Pasolli H, Williams SE, Fuchs E. Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat Cell Biol. 2011. doi: 10.1038/ncb2163 21336301

76. Mcconnell CH. The mitosis found in hydra. Science (80-). 1930. doi: 10.1126/science.72.1859.170-b 17811676

77. Zang JH, Cavet G, Sabry JH, Wagner P, Moores SL, Spudich JA. On the role of myosin-II in cytokinesis: division of Dictyostelium cells under adhesive and nonadhesive conditions. Mol Biol Cell. 1997. doi: 10.1091/mbc.8.12.2617 9398680

78. Fukui Y, Inoue S. Cell division in Dictyostelium with special emphasis on actomyosin organization in cytokinesis. Cell Motil Cytoskeleton. 1991;18: 41–54. doi: 10.1002/cm.970180105 2004432

79. Azimzadeh J. Exploring the evolutionary history of centrosomes. Philosophical Transactions of the Royal Society B: Biological Sciences. 2014.

80. Mahoney NM, Goshima G, Douglass AD, Vale RD. Making microtubules and mitotic spindles in cells without functional centrosomes. Curr Biol. 2006;16: 564–569. doi: 10.1016/j.cub.2006.01.053 16546079

81. Jaspersen SL, Winey M. THE BUDDING YEAST SPINDLE POLE BODY: Structure, Duplication, and Function. Annu Rev Cell Dev Biol. 2004. doi: 10.1146/annurev.cellbio.20.022003.114106 15473833

82. Bray NL, Pimentel H, Melsted P, Pachter L. Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol. 2016. doi: 10.1038/nbt.3519 27043002

83. Hughes ME, Hogenesch JB, Kornacker K. JTK-CYCLE: An efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms. 2010;25: 372–380. doi: 10.1177/0748730410379711 20876817

84. Thaben PF, Westermark PO. Detecting rhythms in time series with rain. J Biol Rhythms. 2014;29: 391–400. doi: 10.1177/0748730414553029 25326247

85. Rustici G, Mata J, Kivinen K, Lió P, Penkett CJ, Burns G, et al. Periodic gene expression program of the fission yeast cell cycle. Nat Genet. 2004;36: 809–817. doi: 10.1038/ng1377 15195092

86. Bauer S, Grossmann S, Vingron M, Robinson PN. Ontologizer 2.0—A multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics. 2008. doi: 10.1093/bioinformatics/btn250 18511468

87. Popow J, Jurkin J, Schleiffer A, Martinez J. Analysis of orthologous groups reveals archease and DDX1 as tRNA splicing factors. Nature. 2014. doi: 10.1038/nature13284 24870230

88. Chen M, Gartenberg MR. Coordination of tRNA transcription with export at nuclear pore complexes in budding yeast. Genes Dev. 2014. doi: 10.1101/gad.236729.113 24788517

89. Herrera MC, Chymkowitch P, Robertson JM, Eriksson J, Bøe SO, Alseth I, et al. Cdk1 gates cell cycle-dependent tRNA synthesis by regulating RNA polymerase III activity. Nucleic Acids Res. 2018. doi: 10.1093/nar/gky846 30247619

90. White RJ, Gottlieb TM, Downes CS, Jackson SP. Cell Cycle Regulation of RNA Polymerase III Transcription. Mol Cell Biol. 1995. doi: 10.1128/MCB.15.12.6653 8524230

91. Schieke SM, McCoy JP, Finkel T. Coordination of mitochondrial bioenergetics with G1phase cell cycle progression. Cell Cycle. 2008. doi: 10.4161/cc.7.12.6067 18583942

92. Obaya AJ, Sedivy JM. Regulation of cyclin-Cdk activity in mammalian cells. Cell Mol Life Sci. 2002;59: 126–142. doi: 10.1007/s00018-002-8410-1 11846025

93. Santos A, Wernersson R, Jensen LJ. Cyclebase 3.0: A multi-organism database on cell-cycle regulation and phenotypes. Nucleic Acids Res. 2015. doi: 10.1093/nar/gku1092 25378319

94. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16: 157. doi: 10.1186/s13059-015-0721-2 26243257

95. Burkhart DL, Sage J. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer. 2008;8: 671–682. doi: 10.1038/nrc2399 18650841

96. Aksoy O, Chicas A, Zeng T, Zhao Z, McCurrach M, Wang X, et al. The atypical E2F family member E2F7 couples the p53 and RB pathways during cellular senescence. Genes Dev. 2012;26: 1546–1557. doi: 10.1101/gad.196238.112 22802529

97. Di Stefano L, Jensen MR, Helin K. E2F7, a novel E2F featuring DP-independent repression of a subset of E2F-regulated genes. EMBO J. 2003;22: 6289–6298. doi: 10.1093/emboj/cdg613 14633988

98. Fu J, Bian M, Jiang Q, Zhang C. Roles of Aurora Kinases in Mitosis and Tumorigenesis. Mol Cancer Res. 2007. doi: 10.1158/1541-7786.MCR-06-0208 17259342

99. Li J, Dallmayer M, Kirchner T, Musa J, Grünewald TGP. PRC1: Linking Cytokinesis, Chromosomal Instability, and Cancer Evolution. Trends in Cancer. 2018. doi: 10.1016/j.trecan.2017.11.002 29413422

100. Li M, Zhang P. The function of APC/CCdh1 in cell cycle and beyond. Cell Div. 2009. doi: 10.1186/1747-1028-4-2 19152694

101. Wang R, Burton JL, Solomon MJ. Transcriptional and post-transcriptional regulation of Cdc20 during the spindle assembly checkpoint in S. cerevisiae. Cell Signal. 2017. doi: 10.1016/j.cellsig.2017.02.003 28189585

102. Csurös M. Count: Evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics. 2010. doi: 10.1093/bioinformatics/btq315 20551134

103. Forth S, Kapoor TM. The mechanics of microtubule networks in cell division. Journal of Cell Biology. 2017. doi: 10.1083/jcb.201612064 28490474

104. Wu J, Akhmanova A. Microtubule-Organizing Centers. Annu Rev Cell Dev Biol. 2017. doi: 10.1146/annurev-cellbio-100616-060615 28645217

105. Santamaría D, Barrière C, Cerqueira A, Hunt S, Tardy C, Newton K, et al. Cdk1 is sufficient to drive the mammalian cell cycle. Nature. 2007;448: 811–815. doi: 10.1038/nature06046 17700700

106. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012. doi: 10.1038/nmeth.2019 22743772

107. The R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. 2018.

108. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, et al. Package “gplots”: Various R programming tools for plotting data. R Packag version 2170. 2016.

109. Carvalho-Santos Z, Azimzadeh J, Pereira-Leal JB, Bettencourt-Dias M. Tracing the origins of centrioles, cilia, and flagella. J Cell Biol. 2011;194: 165–175. doi: 10.1083/jcb.201011152 21788366

110. Hodges ME, Scheumann N, Wickstead B, Langdale JA, Gull K. Reconstructing the evolutionary history of the centriole from protein components. J Cell Sci. 2010;123: 1407–1413. doi: 10.1242/jcs.064873 20388734

111. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990. doi: 10.1016/S0022-2836(05)80360-2

112. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: Architecture and applications. BMC Bioinformatics. 2009. doi: 10.1186/1471-2105-10-421 20003500

113. Bateman A, Martin MJ, O’Donovan C, Magrane M, Alpi E, Antunes R, et al. UniProt: The universal protein knowledgebase. Nucleic Acids Res. 2017. doi: 10.1093/nar/gkw1099 27899622

114. Vandepoele K. Genome-Wide Analysis of Core Cell Cycle Genes in Arabidopsis. PLANT CELL ONLINE. 2002. doi: 10.1105/tpc.010445 11971144

115. Wang G. Genome-Wide Analysis of the Cyclin Family in Arabidopsis and Comparative Phylogenetic Analysis of Plant Cyclin-Like Proteins. PLANT Physiol. 2004. doi: 10.1104/pp.104.040436 15208425

116. Katoh K. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002. doi: 10.1093/nar/gkf436 12136088

117. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009. doi: 10.1093/bioinformatics/btp348 19505945

118. Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015. doi: 10.1093/molbev/msu300 25371430

119. Minh BQ, Nguyen MAT, Von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013. doi: 10.1093/molbev/mst024 23418397

120. Denbo S, Aono K, Kai T, Yagasaki R, Ruiz-Trillo I, Suga H. Revision of the Capsaspora genome using read mating information adjusts the view on premetazoan genome. Dev Growth Differ. 2019;61: 34–42. doi: 10.1111/dgd.12587 30585312

121. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013. doi: 10.1186/gb-2013-14-4-r36 23618408

122. Milne I, Stephen G, Bayer M, Cock PJA, Pritchard L, Cardle L, et al. Using tablet for visual exploration of second-generation sequencing data. Brief Bioinform. 2013. doi: 10.1093/bib/bbs012 22445902

123. Bhattacharya D, Price DC, Xin Chan C, Qiu H, Rose N, Ball S, et al. Genome of the red alga Porphyridium purpureum. Nat Commun. 2013. doi: 10.1038/ncomms2931 23770768

124. Nordberg H, Cantor M, Dusheyko S, Hua S, Poliakov A, Shabalov I, et al. The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res. 2014. doi: 10.1093/nar/gkt1069 24225321

125. Zerbino DR, Achuthan P, Akanni W, Amode MR, Barrell D, Bhai J, et al. Ensembl 2018. Nucleic Acids Res. 2018. doi: 10.1093/nar/gkx1098 29155950

126. Huerta-Cepas J, Capella-Gutiérrez S, Pryszcz LP, Marcet-Houben M, Gabaldón T. PhylomeDB v4: Zooming into the plurality of evolutionary histories of a genome. Nucleic Acids Res. 2014. doi: 10.1093/nar/gkt1177 24275491

127. Smedley D, Haider S, Durinck S, Pandini L, Provero P, Allen J, et al. The BioMart community portal: An innovative alternative to large, centralized data repositories. Nucleic Acids Res. 2015. doi: 10.1093/nar/gkv350 25897122

128. Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 2016;44: D286–D293. doi: 10.1093/nar/gkv1248 26582926


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 3

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Imunitní trombocytopenie (ITP) u dospělých pacientů
nový kurz
Autoři: prof. MUDr. Tomáš Kozák, Ph.D., MBA

Pěnová skleroterapie
Autoři: MUDr. Marek Šlais

White paper - jak vidíme optimální péči o zubní náhrady
Autoři: MUDr. Jindřich Charvát, CSc.

Hemofilie - série kurzů

Faktory ovlivňující léčbu levotyroxinem
Autoři:

Všechny kurzy
Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×