Epigenetically-Inherited Centromere and Neocentromere DNA Replicates Earliest in S-Phase
Eukaryotic centromeres are maintained at specific chromosomal sites over many generations. In the budding yeast Saccharomyces cerevisiae, centromeres are genetic elements defined by a DNA sequence that is both necessary and sufficient for function; whereas, in most other eukaryotes, centromeres are maintained by poorly characterized epigenetic mechanisms in which DNA has a less definitive role. Here we use the pathogenic yeast Candida albicans as a model organism to study the DNA replication properties of centromeric DNA. By determining the genome-wide replication timing program of the C. albicans genome, we discovered that each centromere is associated with a replication origin that is the first to fire on its respective chromosome. Importantly, epigenetic formation of new ectopic centromeres (neocentromeres) was accompanied by shifts in replication timing, such that a neocentromere became the first to replicate and became associated with origin recognition complex (ORC) components. Furthermore, changing the level of the centromere-specific histone H3 isoform led to a concomitant change in levels of ORC association with centromere regions, further supporting the idea that centromere proteins determine origin activity. Finally, analysis of centromere-associated DNA revealed a replication-dependent sequence pattern characteristic of constitutively active replication origins. This strand-biased pattern is conserved, together with centromere position, among related strains and species, in a manner independent of primary DNA sequence. Thus, inheritance of centromere position is correlated with a constitutively active origin of replication that fires at a distinct early time. We suggest a model in which the distinct timing of DNA replication serves as an epigenetic mechanism for the inheritance of centromere position.
Vyšlo v časopise:
Epigenetically-Inherited Centromere and Neocentromere DNA Replicates Earliest in S-Phase. PLoS Genet 6(8): e32767. doi:10.1371/journal.pgen.1001068
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001068
Souhrn
Eukaryotic centromeres are maintained at specific chromosomal sites over many generations. In the budding yeast Saccharomyces cerevisiae, centromeres are genetic elements defined by a DNA sequence that is both necessary and sufficient for function; whereas, in most other eukaryotes, centromeres are maintained by poorly characterized epigenetic mechanisms in which DNA has a less definitive role. Here we use the pathogenic yeast Candida albicans as a model organism to study the DNA replication properties of centromeric DNA. By determining the genome-wide replication timing program of the C. albicans genome, we discovered that each centromere is associated with a replication origin that is the first to fire on its respective chromosome. Importantly, epigenetic formation of new ectopic centromeres (neocentromeres) was accompanied by shifts in replication timing, such that a neocentromere became the first to replicate and became associated with origin recognition complex (ORC) components. Furthermore, changing the level of the centromere-specific histone H3 isoform led to a concomitant change in levels of ORC association with centromere regions, further supporting the idea that centromere proteins determine origin activity. Finally, analysis of centromere-associated DNA revealed a replication-dependent sequence pattern characteristic of constitutively active replication origins. This strand-biased pattern is conserved, together with centromere position, among related strains and species, in a manner independent of primary DNA sequence. Thus, inheritance of centromere position is correlated with a constitutively active origin of replication that fires at a distinct early time. We suggest a model in which the distinct timing of DNA replication serves as an epigenetic mechanism for the inheritance of centromere position.
Zdroje
1. PanchenkoT
BlackBE
2009 The epigenetic basis for centromere identity. Prog Mol Subcell Biol 48 1 32
2. MorrisCA
MoazedD
2007 Centromere Assembly and Propagation. Cell 128 647 650
3. EkwallK
2007 Epigenetic control of centromere behavior. Annu Rev Genet 41 63 81
4. AllshireRC
KarpenGH
2008 Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nature Reviews Genetics 9 923 937
5. MalikHS
HenikoffS
2009 Major evolutionary transitions in centromere complexity. Cell 138 1067 1082
6. SullivanBA
BlowerMD
KarpenGH
2001 Determining centromere identity: cyclical stories and forking paths. Nat Rev Genet 2 584 596
7. KetelC
WangHS
McClellanM
BouchonvilleK
SelmeckiA
2009 Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5 e1000400 doi:10.1371/journal.pgen.1000400
8. MarshallOJ
ChuehAC
WongLH
ChooKH
2008 Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82 261 282
9. ShelbyRD
MonierK
SullivanKF
2000 Chromatin Assembly at Kinetochores Is Uncoupled from DNA Replication. J Cell Biol 151 1113 1118
10. HenikoffS
AhmadK
PlateroJS
van SteenselB
2000 Heterochromatic deposition of centromeric histone H3-like proteins. Proceedings of the National Academy of Sciences USA 97 716 721
11. TakahashiK
ChenES
YanagidaM
2000 Requirement of Mis6 Centromere Connector for Localizing a CENP-A-Like Protein in Fission Yeast. Science 288 2215 2219
12. TakayamaY
SatoH
SaitohS
OgiyamaY
MasudaF
2008 Biphasic Incorporation of Centromeric Histone CENP-A in Fission Yeast. Mol Biol Cell 19 682 690
13. DuPrawEJ
1968 Cell and Molecular Biology. Academic Press
14. CsinkAK
HenikoffS
1998 Something from nothing: the evolution and utility of satellite repeats. Trends in Genetics 14 200 204
15. AhmadK
HenikoffS
2001 Centromeres Are Specialized Replication Domains in Heterochromatin. J Cell Biol 153 101 110
16. SullivanB
KarpenG
2001 Centromere identity in Drosophila is not determined in vivo by replication timing. J Cell Biol 154 683 690
17. Weidtkamp-PetersS
RahnHP
CardosoMC
HemmerichP
2006 Replication of centromeric heterochromatin in mouse fibroblasts takes place in early, middle, and late S phase. Histochem Cell Biol 125 91 102
18. SanyalK
BaumM
CarbonJ
2004 Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proceedings of the National Academy of Sciences USA 101 11374 11379
19. BaumM
SanyalK
MishraPK
ThalerN
CarbonJ
2006 Formation of functional centromeric chromatin is specified epigenetically in Candida albicans. Proceedings of the National Academy of Sciences USA 103 14877 14882
20. MishraPK
BaumM
CarbonJ
2007 Centromere size and position in Candida albicans are evolutionarily conserved independent of DNA sequence heterogeneity. Mol Genet Genomics 278 455 465
21. PadmanabhanS
ThakurJ
SiddharthanR
SanyalK
2008 Rapid evolution of Cse4p-rich centromeric DNA sequences in closely related pathogenic yeasts, Candida albicans and Candida dubliniensis. Proceedings of the National Academy of Sciences USA 105 19797 19802
22. KorenA
SoiferI
BarkaiN
2010 MRC1-dependent scaling of the budding yeast DNA replication timing program. Genome Res 20 781 790
23. RaghuramanMK
WinzelerEA
CollingwoodD
HuntS
WodickaL
2001 Replication Dynamics of the Yeast Genome. Science 294 115 121
24. SernovaNV
GelfandMS
2008 Identification of replication origins in prokaryotic genomes. Brief Bioinform 9 376 391
25. PavlovYI
NewlonCS
KunkelTA
2002 Yeast origins establish a strand bias for replicational mutagenesis. Mol Cell 10 207 213
26. VernisL
PoljakL
ChaslesM
UchidaK
CasaregolaS
2001 Only centromeres can supply the partition system required for ARS function in the yeast Yarrowia lipolytica. J Mol Biol 305 203 217
27. FournierP
AbbasA
ChaslesM
KudlaB
OgrydziakDM
1993 Colocalization of centromeric and replicative functions on autonomously replicating sequences isolated from the yeast Yarrowia lipolytica. Proceedings of the National Academy of Sciences USA 90 4912 4916
28. KimS-M
DubeyDD
HubermanJA
2003 Early-replicating heterochromatin. Genes & Development 17 330 335
29. MeraldiP
McAinshA
RheinbayE
SorgerP
2006 Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biology 7 R23
30. HenikoffS
AhmadK
MalikHS
2001 The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293 1098 1102
31. SanyalK
CarbonJ
2002 The CENP-A homolog CaCse4p in the pathogenic yeast Candida albicans is a centromere protein essential for chromosome transmission. Proc Natl Acad Sci U S A 99 12969 12974
32. BrewerBJ
FangmanWL
1987 The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51 463 471
33. WyrickJJ
AparicioJG
ChenT
BarnettJD
JenningsEG
2001 Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science 294 2357 2360
34. HeichingerC
PenkettCJ
BahlerJ
NurseP
2006 Genome-wide characterization of fission yeast DNA replication origins. EMBO J 25 5171 5179
35. FengW
CollingwoodD
BoeckME
FoxLA
AlvinoGM
2006 Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nature Cell Biology 8 148 155
36. MickleK
RamanathanS
RosebrockA
OlivaA
ChaudariA
2007 Checkpoint independence of most DNA replication origins in fission yeast. BMC Molecular Biology 8 112
37. DujonB
ShermanD
FischerG
DurrensP
CasaregolaS
2004 Genome evolution in yeasts. Nature 430 35 44
38. HayashiM
KatouY
ItohT
TazumiM
YamadaY
2007 Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast. EMBO J 26 1327 1339
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 8
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