Molecular evolution of Drosophila Cdc6, an essential DNA replication licensing gene, suggests an adaptive choice of replication origins

Fly

Volumn 1, Issue 3, 2007, Pages 155-163

  Wiggins, Benjamin L ^a   Malik, Harmit S ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Drosophila melanogaster; Drosophila pseudoobscura; McDonald Kreitman test; Non coding DNA; Origin 'choice'; Replication origins; Saccharomyces cerevisiae

Indexed keywords

ANIMALIA; DROSOPHILA MELANOGASTER; DROSOPHILA PSEUDOOBSCURA; EUKARYOTA; HEXAPODA; METAZOA; SACCHAROMYCES CEREVISIAE;

CDC6 PROTEIN, DROSOPHILA; CELL CYCLE PROTEIN; DROSOPHILA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; DNA REPLICATION; DNA REPLICATION ORIGIN; DROSOPHILA; DROSOPHILA MELANOGASTER; GENE; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SPECIES DIFFERENCE;

ANIMALS; CELL CYCLE PROTEINS; CONSERVED SEQUENCE; DNA REPLICATION; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; GENES, INSECT; MOLECULAR SEQUENCE DATA; PHYLOGENY; REPLICATION ORIGIN; SELECTION (GENETICS); SPECIES SPECIFICITY;

EID: 34848870447     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: 10.4161/fly.4599     Document Type: Article

References (89)

1. Bell SP, Dutta A. DNA replication in eukaryotic cells. Annu Rev Biochem 2002; 71:333-74.
2. Blumenthal AB, Kriegstein HJ, Hogness DS. The units of DNA replication in Drosophila melanogaster chromosomes. Cold Spring Harb Symp Quant Biol 1974; 38:205-23.
3. Spradling AC. ORC binding, gene amplification, and the nature of metazoan replication origins. Genes Dev 1999; 13:2619-23.
4. Blow JJ, Gillespie PJ, Francis D, Jackson DA. Replication origins in Xenopus egg extract Are 5-15 kilobases apart and are activated in clusters that fire at different times. J Cell Biol 2001; 152:15-25.
5. Fangman WL, Hice RH, Chlebowicz-Sledziewska E. ARS replication during the yeast S phase. Cell 1983; 32:831-8.
6. Brewer BJ, Fangman WL. The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 1987; 51:463-71.
7. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, Conway A, Lockhart DJ, Davis RW, Brewer BJ, Fangman WL. Replication dynamics of the yeast genome. Science 2001; 294:115-21.
8. Dubey DD, Kim SM, Todorov IT, Huberman JA. Large, complex modular structure of a fission yeast DNA replication origin. Curr Biol 1996; 6:467-73.
9. Dai J, Chuang RY, Kelly TJ. DNA replication origins in the Schizosaccharomyces pombe genome. Proc Natl Acad Sci USA 2005; 102:337-42.
10. MacAlpine DM, Rodriguez HK, Bell SP. Coordination of replication and transcription along a Drosophila chromosome. Genes Dev 2004; 18:3094-105.
11. MacAlpine DM, Bell SP. A genomic view of eukaryotic DNA replication. Chromosome Res 2005; 13:309-26.
12. Takeda DY, Dutta A. DNA replication and progression through S phase. Oncogene 2005; 24:2827-43.
13. Mello CC, Kramer JM, Stinchcomb D, Ambros V. Efficient gene transfer in C.elegans: Extrachromosomal maintenance and integration of transforming sequences. Embo J 1991; 10:3959-70.
14. Kim CS, Preer Jr JR, Polisky B. Bacteriophage lambda DNA fragments replicate in the Paramecium macronucleus: Absence of active copy number control. Dev Genet 1992; 13:97-102.
15. Smith JG, Calos MP. Autonomous replication in Drosophila melanogaster tissue culture cells. Chromosoma 1995; 103:597-605.
16. Coverley D, Laskey RA. Regulation of eukaryotic DNA replication. Annu Rev Biochem 1994; 63:745-76.
17. Cvetic C, Walter JC. Eukaryotic origins of DNA replication: Could you please be more specific? Semin Cell Dev Biol 2005; 16:343-53.
18. Austin RJ, Orr-Weaver TL, Bell SP. Drosophila ORC specifically binds to ACE3, an origin of DNA replication control element. Genes Dev 1999; 13:2639-49.
19. Beall EL, Manak JR, Zhou S, Bell M, Lipsick JS, Botchan MR. Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 2002; 420:833-7.
20. Mendez J, Zou-Yang XH, Kim SY, Hidaka M, Tansey WP, Stillman B. Human origin recognition complex large subunit is degraded by ubiquitin-mediated proteolysis after initiation of DNA replication. Mol Cell 2002; 9:481-91.
21. Tye BK. MCM proteins in DNA replication. Annu Rev Biochem 1999; 68:649-86.
22. Diffley JF. Regulation of early events in chromosome replication. Curr Biol 2004; 14: R778-86.
23. Harvey KJ, Newport J. Metazoan origin selection: Origin recognition complex chromatin binding is regulated by CDC6 recruitment and ATP hydrolysis. J Biol Chem 2003; 278:48524-8.
24. Nishitani H, Lygerou Z, Nishimoto T, Nurse P. The Cdt1 protein is required to license DNA for replication in fission yeast. Nature 2000; 404:625-8.
25. Lemaitre JM, Bocquet S, Mechali M. Competence to replicate in the unfertilized egg is conferred by Cdc6 during meiotic maturation. Nature 2002; 419:718-22.
26. Lemaitre JM, Bocquet S, Terret ME, Namdar M, Ait-Ahmed O, Kearsey S, Verlhac MH, Mechali M. The regulation of competence to replicate in meiosis by Cdc6 is conserved during evolution. Mol Reprod Dev 2004; 69:94-100.
27. Takeda DY, Shibata Y, Parvin JD, Dutta A. Recruitment of ORC or CDC6 to DNA is sufficient to create an artificial origin of replication in mammalian cells. Genes Dev 2005; 19:2827-36.
28. Speck C, Stillman B. Cdc6 ATPase activity regulates ORC x Cdc6 stability and the selection of specific DNA sequences as origins of DNA replication. J Biol Chem 2007; 282:11705-14.
29. Endo T, Ikeo K, Gojobori T. Large-scale search for genes on which positive selection may operate. Mol Biol Evol 1996; 13:685-90.
30. Malik HS, Henikoff S. Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 2001; 157:1293-8.
31. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997; 25:4876-82.
32. Comeron JM. K-Estimator: Calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 1999; 15:763-4.
33. Rozas J, Rozas R. DnaSP version 2.0: A novel software package for extensive molecular population genetics analysis. Comput Appl Biosci 1997; 13:307-11.
34. Henikoff JG, Pietrokovski S, McCallum CM, Henikoff S. Blocks-based methods for detecting protein homology. Electrophoresis 2000; 21:1700-6.
35. Schneider TD, Stephens RM. Sequence logos: A new way to display consensus sequences Nucleic Acids Res 1990; 18:6097-6100.
36. Bailey TL, Gribskov M. Concerning the accuracy of MAST E-values. Bioinformatics 2000:16:488-9.
37. Bailey TL, Gribskov M. Methods and statistics for combining motif match scores. J CompuBiol 1998; 5:211-221.
38. Malik HS, Vermaak D, Henikoff S. Recurrent evolution of DNA-binding motifs in thDrosophila centromeric histone. Proc Natl Acad Sci USA 2002; 99:1449-54.
39. Wong WS, Yang Z, Goldman N, Nielsen R. Accuracy and power of statistical methodfor detecting adaptive evolution in protein coding sequences and for identifying positivelselected sites. Genetics 2004; 168:1041-51.
40. Pond SL, Frost SD. Datamonkey: Rapid detection of selective pressure on individual siteof codon alignments. Bioinformatics 2005; 21:2531-3.
41. Li YJ, Satta Y, Takahata N. Paleo-demography of the Drosophila melanogaster subgroupApplication of the maximum likelihood method. Genes Genet Syst 1999; 74:117-27.
42. McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila Nature1991; 351:652-4.
43. Nachman MW, Brown WM, Stoneking M, Aquadro CF. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 1996; 142:953-63.
44. Rooney AP, Zhang J., Rapid evolution of a primate sperm protein: Relaxation of functionaconstraint or positive Darwinian selection? Mol Biol Evol 1999; 16:706-10.
45. Wyckoff GJ, Wang W, Wu CI. Rapid evolution of male reproductive genes in the descenof man. Nature 2000; 403:304-9.
46. Akashi H. Inferring weak selection from patterns of polymorphism and divergence a"silent" sites in Drosophila DNA. Genetics 1995; 139:1067-76.
47. Wright F. The 'effective number of codons' used in a gene. Gene 1990; 87:23-9.
48. Morton BR. Chloroplast DNA codon use: Evidence for selection at the psb A locus baseon tRNA availability. J Mol Evol 1993; 37:273-80.
49. Schlenke TA, Begun DJ. Natural selection drives Drosophila immune system evolution Genetics 2003; 164:1471-80.
50. Zhang J, Rosenberg HF, Nei M. Positive Darwinian selection after gene duplication iprimate ribonuclease genes. Proc Natl Acad Sci USA 1998; 95:3708-13.
51. Eyre-Walker A. Changing effective population size and the McDonald-Kreitman test Genetics 2002; 162:2017-24.
52. Smith NG, Eyre-Walker A. Adaptive protein evolution in Drosophila. Nature 2002:415:1022-4.
53. Wang RL, Hey J. The speciation history of Drosophila pseudoobscura and close relatives: Inferences from DNA sequence variation at the period locus. Genetics 1996:144:1113-26.
54. Goto SG, Kimura MT. Phylogenetic utility of mitochondrial COI and nuclear Gpdh genein Drosophila. Mol Phylogenet Evol 2001; 18:404-22.
55. Malik HS, Henikoff S. Positive selection of Iris, a retroviral envelope-derived host gene iDrosophila melanogaster. PLoS Genet 2005; 1:e44.
56. Kopp A. Basal relationships in the Drosophila melanogaster species group. Mol PhylogeneEvol 2006; 39:787-98.
57. Sawyer SL, Wu LI, Emerman M, Malik HS. Positive selection of primate TRIM5alphidentifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 2005; 102:2832-7.
58. Yang Z. The power of phylogenetic comparison in revealing protein function. Proc NatAcad Sci USA 2005; 102:3179-80.
59. Kosakovsky Pond SL, Frost SD. Not so different after all: A comparison of methods fodetecting amino acid sites under selection. Mol Biol Evol 2005; 22:1208-1222.
60. Cook JG, Chasse DA, Nevins JR. The regulated association of Cdt1 with minichromosommaintenance proteins and Cdc6 in mammalian cells. J Biol Chem 2004; 279:9625-33.
61. Sanchez M, Calzada A, Bueno A. The Cdc6 protein is ubiquitinated in vivo for proteolysiin Saccharomyces cerevisiae. J Biol Chem 1999; 274:9092-7.
62. Drury LS, Perkins G, Diffley JF. The Cdc4/34/53 pathway targets Cdc6p for proteolysis ibudding yeast. Embo J 1997; 16:5966-76.
63. Furstenthal L, Kaiser BK, Swanson C, Jackson PK. Cyclin E uses Cdc6 as a chromatin-associated receptor required for DNA replication. J Cell Biol 2001; 152:1267-78.
64. Araki M, Wharton RP, Tang Z, Yu H, Asano M. Degradation of origin recognitiocomplex large subunit by the anaphase-promoting complex in Drosophila. Embo J 2003:22:6115-26.
65. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. Sequencing and comparison oyeast species to identify genes and regulatory elements. Nature 2003; 423:241-54.
66. Yang Z, Bielawski JP. Statistical methods for detecting molecular adaptation. Trends iEcology and Evolution 2000; 15:496-503.
67. Crevel G, Mathe E, Cotterill S. The Drosophila Cdc6/18 protein has functions in both earland late S phase in S2 cells. J Cell Sci 2005; 118:2451-9.
68. Gonzalez S, Klatt P, Delgado S, Conde E, Lopez-Rios F, Sanchez-Cespedes M, Mendez JAntequera F, Serrano M. Oncogenic activity of Cdc6 through repression of the INK4/ARlocus. Nature 2006; 440:702-6.
69. Tian J, Thomsen GH, Gong H, Lennarz WJ. Xenopus Cdc6 confers sperm binding competence to oocytes without inducing their maturation. Proc Natl Acad Sci USA 1997:94:10729-34.
70. Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci USA 2001; 98:7375-9.
71. Swanson WJ, Wong A, Wolfner MF, Aquadro CF. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics 2004; 168:1457-65.
72. Rabinowitz M. Studies on the cytology and early embryology of the egg of Drosophila melanogaster. J Morphol 1941; 69:1.
73. Edgar BA, Lehner CF. Developmental control of cell cycle regulators: A fly's perspective. Science 1996; 274:1646-52.
74. Lee LA, Orr-Weaver TL. Regulation of cell cycles in Drosophila development: Intrinsic and extrinsiccues. Annu Rev Genet 2003; 37:545-78.
75. Calvi BR Spradling AC., Chorion gene amplification in Drosophila: A model for metazoan origins of DNA replication and S-phase control. Methods 1999; 18:407-17.
76. Engels WR, Johnson-Schlitz DM, Eggleston WB, Sved J. High-frequency P element loss in Drosophila is homolog dependent. Cell 1990; 62:515-25.
77. Green MM. Genetic instability in Drosophila melanogaster: De novo induction of putative insertion mutations. Proc Natl Acad Sci USA 1977; 74:3490-3.
78. Berg CA, Spradling AC. Studies on the rate and site-specificity of P element transposition. Genetics 1991; 127:515-24.
79. Schubeler D, Scalzo D, Kooperberg C, van Steensel B, Delrow J, Groudine M. Genome-wide DNA replication profile for Drosophila melanogaster: A link between transcription and replication timing. Nat Genet 2002; 32:438-42.
80. Barigozzi C, Dolfini S, Fraccaro M, Raimondi GR, Tiepolo L. In vitro study of the DNA replication patterns of somatic chromosomes of Drosophila melanogaster. Exp Cell Res 1966; 43:231-4.
81. Dolfini S. Karyotype polymorphism in a cell population of Drosophila melanogaster cultured in vitro. Chromosoma 1971; 33:196-208.
82. Ahmad K, Henikoff S. Centromeres are specialized replication domains in heterochromatin. J Cell Biol 2001; 153:101-1110.
83. Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, Li Y, Hao YL, Ooi CE, Godwin B, Vitols E, Vijayadamodar G, Pochart P, Machineni H, Welsh M, Kong Y, Zerhusen B, Malcolm R, Varrone Z, Collis A, Minto M, Burgess S, McDaniel L, Stimpson E, Spriggs F, Williams J, Neurath K, Ioime N, Agee M, Voss E, Furtak K, Renzulli R, Aanensen N, Carrolla S, Bickelhaupt E, Lazovatsky Y, DaSilva A, Zhong J, Stanyon CA, Finley Jr RL, White KP, Braverman M, Jarvie T, Gold S, Leach M, Knight J, Shimkets RA, McKenna MP, Chant J, Rothberg JM. A protein interaction map of Drosophila melanogaster. Science 2003; 302:1727-36.
84. Vermaak D, Henikoff S, Malik HS. Positive selection drives the evolution of rhino, a member of the heterochromatin protein 1 family in Drosophila. PLoS Genet 2005; 1:96-108.
85. Auth T, Kunkel E, Grummt F. Interaction between HP1alpha and replication proteins in mammalian cells. Exp Cell Res 2006; 312:3349-59.
86. Pak DT, Pflumm M, Chesnokov I, Huang DW, Kellum R, Marr J, Romanowski P, Botchan MR. Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 1997; 91:311-23.
87. Nieduszynski CA, Knox Y, Donaldson AD. Genome-wide identification of replication origins in yeast by comparative genomics. Genes Dev 2006; 20:1874-9.
88. Touchon M, Nicolay S, Audit B, Brodie of Brodie EB,d'Aubenton-Carafa Y,Arneodo A,Thermes C. Replication-associated strand asymmetries in mammalian genomes: Toward detection of replication origins. Proc Natl Acad Sci USA 2005; 102:9836-41.
89. Malik HS, Henikoff S. Phylogenomics of the nucleosome. Nat Struct Biol 2003; 10:882-91.