S Phase Progression in Human Cells Is Dictated by the Genetic Continuity of DNA Foci
DNA synthesis must be performed with extreme precision to maintain genomic integrity. In mammalian cells, different genomic regions are replicated at defined times, perhaps to preserve epigenetic information and cell differentiation status. However, the molecular principles that define this S phase program are unknown. By analyzing replication foci within discrete chromosome territories during interphase, we show that foci which are active during consecutive intervals of S phase are maintained as spatially adjacent neighbors throughout the cell cycle. Using extended DNA fibers, we demonstrate that this spatial continuity of replication foci correlates with the genetic continuity of adjacent replicon clusters along chromosomes. Finally, we used bioinformatic tools to compare the structure of DNA foci with DNA domains that are seen to replicate during discrete time intervals of S phase using genome-wide strategies. Data presented show that a major mechanism of S phase progression involves the sequential synthesis of regions of the genome because of their genetic continuity along the chromosomal fiber.
Vyšlo v časopise:
S Phase Progression in Human Cells Is Dictated by the Genetic Continuity of DNA Foci. PLoS Genet 6(4): e32767. doi:10.1371/journal.pgen.1000900
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000900
Souhrn
DNA synthesis must be performed with extreme precision to maintain genomic integrity. In mammalian cells, different genomic regions are replicated at defined times, perhaps to preserve epigenetic information and cell differentiation status. However, the molecular principles that define this S phase program are unknown. By analyzing replication foci within discrete chromosome territories during interphase, we show that foci which are active during consecutive intervals of S phase are maintained as spatially adjacent neighbors throughout the cell cycle. Using extended DNA fibers, we demonstrate that this spatial continuity of replication foci correlates with the genetic continuity of adjacent replicon clusters along chromosomes. Finally, we used bioinformatic tools to compare the structure of DNA foci with DNA domains that are seen to replicate during discrete time intervals of S phase using genome-wide strategies. Data presented show that a major mechanism of S phase progression involves the sequential synthesis of regions of the genome because of their genetic continuity along the chromosomal fiber.
Zdroje
1. BlowJJ
DuttaA
2005 Preventing re-replication of chromosomal DNA. Nat Rev Mol Cell Biol 6 476 486
2. DePamphilisML
BlowJJ
GhoshS
SahaT
NoguchiK
2006 Regulating the licensing of DNA replication origins in metazoa. Curr Opin Cell Biol 18 231 239
3. SclafaniRA
HolzenTM
2007 Cell cycle regulation of DNA replication. Annu Rev Genet 41 237 280
4. MachidaYJ
HamlinJL
DuttaA
2005 Right place, right time, and only once: replication initiation in metazoans. Cell 123 13 24
5. NorioP
KosiyatrakulS
YangQ
GuanZ
BrownNM
2005 Progressive activation of DNA replication initiation in large domains of the immunoglobulin heavy chain locus during B cell development. Mol Cell 20 575 87
6. MesnerLD
CrawfordEL
HamlinJL
2006 Isolating apparently pure libraries of replication origins from complex genomes. Mol Cell 21 719 726
7. GrothA
RochaW
VerreaultA
AlmouzniG
2007 Chromatin challenges during DNA replication and repair. Cell 128 721 733
8. DrouinR
LemieuxN
RicherCL
1990 Analysis of DNA replication during S-phase by means of dynamic chromosome banding at high resolution. Chromosoma 99 273 280
9. WoodfineK
FieglerH
BeareDM
CollinsJE
McCannOT
2004 Replication timing of the human genome. Hum Mol Genet 13 191 202
10. DespratR
Thierry-MiegD
LaillerN
LajugieJ
SchildkrautC
2009 Predictable dynamic program of timing of DNA replication in human cells. Genome Res 19 2288 2299
11. Farkash-AmarS
LipsonD
PoltenA
GorenA
HelmstetterC
2008 Global organization of replication time zones of the mouse genome. Genome Res 18 1562 1570
12. HirataniI
RybaT
ItohM
YokochiT
SchwaigerM
2008 Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6 e245 doi:10.1371/journal.pbio.0060245
13. CadoretJ-C
MeischF
Hassan-ZadehV
LuytenI
GuilletC
2008 Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci USA 105 15837 15842
14. Sequeira-MendesJ
Diaz-UriarteR
ApedaileA
HuntleyD
BrockdorffN
2009 Transcription initiation activity sets replication origin efficiency in mammalian cells. PLoS Genet 5 e1000446 doi:10.1371/journal.pgen.1000446
15. HansenRS
ThomasS
SandstromR
CanfieldTK
ThurmanRE
2010 Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc Natl Acad Sci USA 107 139 144
16. JacksonDA
1995 Nuclear organization: uniting replication foci, chromatin domains and chromosome structure. BioEssays 17 587 591
17. ZinkD
2006 The temporal program of DNA replication: new insights into old questions. Chromosoma 115 273 287
18. HozakP
HassanAB
JacksonDA
CookPR
1993 Visualization of replication factories attached to a nucleoskeleton. Cell 73 361 373
19. JacksonDA
PomboA
1998 Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140 1285 1295
20. LebofskyR
HeiligR
SonnleitnerM
WeissenbachJ
BensimonA
2006 DNA replication origin interference increases the spacing between initiation events in human cells. Mol Biol Cell 17 5337 5345
21. MaH
SamarabanduJ
DevdharRS
AcharyaR
ChengPC
1998 Spatial and temporal dynamics of DNA replication sites in mammalian cells. J Cell Biol 143 1415 1425
22. BerezneyR
DubeyDD
HubermanJA
2000 Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108 471 484
23. CremerT
CremerC
2001 Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2 292 301
24. ShoplandLS
LynchCR
PetersonKA
ThorntonK
KepperN
2006 Folding and organization of a contiguous chromosome region according to the gene distribution pattern in primary genomic sequence. J Cell Biol 174 27 38
25. GoetzeS
Mateos-LangerakJ
GiermanHJ
de LeeuwW
GiromusO
2007 The three-dimensional structure of human interphase chromosomes in related to the transcriptome map. Mol Cell Biol 27 4475 4487
26. GoenA
CedarH
2003 Replicating by the clock. Nat Rev Mol Cell Biol 4 25 32
27. AladjemMI
2007 Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat Rev Genet 8 588 600
28. MandersEMM
StapJ
BrakenhoffGJ
van DrielR
AtenJA
1992 Dynamics of three-dimensional replication patterns during the S-phase, analyzed by double labeling of DNA and confocal microscopy. J Cell Sci 103 857 862
29. SporbertA
GahlA
AnkerholdR
LeonhardtH
CardosoMC
2002 DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters. Mol Cell 10 1355 1365
30. TakebayashiS
SugimuraK
SaitoT
SatoC
FukushimaY
2004 Regulation of replication at the R/G chromosomal band boundary and pericentromeric heterochromatin of mammalian cells. Exp Cell Res 304 162 174
31. BornflethH
EdelmannP
ZinkD
CremerT
CremerC
1999 Quantitative motion analysis of subchromosomal foci in living cells using four-dimensional microscopy. Biophys J 77 2871 2886
32. BlowJJ
GillespiePJ
FrancisD
JacksonDA
2001 Replication origins in Xenopus egg extracts are 5–15 kb apart and are activated in clusters that fire at different times. J Cell Biol 152 15 26
33. HyrienO
MarheinekeK
GoldarA
2003 Paradoxes of eukaryotic DNA replication: MCM proteins and the random completion problem. BioEssays 25 116 125
34. HassanAB
ErringtonRJ
WhiteNS
JacksonDA
CookPR
1994 Replication and transcription sites are colocalized in human cells. J Cell Sci 107 425 434
35. KatsunoY
SuzukiA
SugimuraK
OkumuraK
ZineldeenDH
2009 Cyclin A-CDK1 regulates the origin firing program in mammalian cells. Proc Natl Acad Sci USA 106 3184 3189
36. ZhangJM
XuF
HashimshonyT
KeshetN
CedarH
2002 Establishment of transcriptional competence in early and late S phase. Nature 420 198 202
37. Lande-DinerL
ZhangJM
CedarH
2009 Shifts in replication timing actively affect histone acetylation during nucleosome reassembly. Mol Cell 34 767 774
38. AlbiezH
CremerM
TiberiC
VecchioL
SchermellehL
2006 Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks. Chromosome Res 14 707 733
39. Mateos-LangerakJ
BohnM
de LeeuwW
GiromusO
MandersEMM
2009 Spatially confined folding of chromatin in the interphase nucleus. Proc Natl Acad Sci USA 106 3812 3817
40. FetniR
DrouinR
RicherCL
LemieuxN
1996 Complementary replication R- and G-band patterns induced by cell blocking at the R-band/G-band transition, a possible regulatory checkpoint within the S phase of the cell cycle. Cytogenet Cell Genet 75 172 179
41. HirataniI
RybaT
ItohM
RathjenJ
KulikM
2010 Genome-wide dynamics of replication timing revealed by in vitro models of mouse embryogenesis. Genome Res 20 155 169
42. Maya-MendozaA
TangCW
PomboA
JacksonDA
2009 Mechanisms regulating S phase progression in mammalian cells. Front Biosci 14 4199 4213
43. CourbetS
GayS
ArnoultN
WronkaG
AnglanaM
2008 Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455 557 560
44. Maya-MendozaA
PetermannE
GillespieDA
CaldecottKW
JacksonDA
2007 Chk1 regulates the density of active replication origins during the vertebrate S phase. EMBO J 26 2719 2731
45. ShawA
Olivares-ChauvetP
Maya-MendozaA
JacksonDA
2010 S phase progression in mammalian cells: modelling the influence of nuclear organization. Chromosome Res 18 163 178
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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