The distribution of genomic variations in human iPSCs is related to replication-timing reorganization during reprogramming

Cell Reports

Volumn 7, Issue 1, 2014, Pages 70-78

  Lu, Junjie ^a,b   Li, Hu ^c   Hu, Ming ^d,h   Sasaki, Takayo ^e   Baccei, Anna ^a,b   Gilbert, David M ^e   Liu, Jun S ^d   Collins, James J ^f,g   Lerou, Paul H ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

^d HARVARD UNIVERSITY   (United States)

^e FLORIDA STATE UNIVERSITY   (United States)

^f Boston University   (United States)

^g HARVARD UNIVERSITY   (United States)

^h NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL DIVISION; CELL FATE; CELL STRUCTURE; CONTROLLED STUDY; COPY NUMBER VARIATION; FIBROBLAST CULTURE; GENE LOCATION; GENE LOCUS; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME ANALYSIS; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NUCLEAR REPROGRAMMING; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; CYTOLOGY; DNA REPLICATION; FIBROBLAST; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; METABOLISM; PHYSIOLOGY;

CELLULAR REPROGRAMMING; DNA COPY NUMBER VARIATIONS; DNA REPLICATION; FIBROBLASTS; GENE EXPRESSION PROFILING; GENOMICS; HUMANS; INDUCED PLURIPOTENT STEM CELLS;

EID: 84898041397     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.007     Document Type: Article

References (46)

1. Abyzov A., Mariani J., Palejev D., Zhang Y., Haney M.S., Tomasini L., Ferrandino A.F., Rosenberg Belmaker L.A., Szekely A., Wilson M., et al. Somatic copy number mosaicism in human skin revealed by induced pluripotent stem cells. Nature 2012, 492:438-442.
2. Amps K., Andrews P.W., Anyfantis G., Armstrong L., Avery S., Baharvand H., Baker J., Baker D., Munoz M.B., Beil S., et al. Screening ethnically diverse human embryonic stem cells identifies a chromosome 20minimal amplicon conferring growth advantage. Nat. Biotechnol. 2011, 29:1132-1144. International Stem Cell Initiative.
3. Apostolou E., Ferrari F., Walsh R.M., Bar-Nur O., Stadtfeld M., Cheloufi S., Stuart H.T., Polo J.M., Ohsumi T.K., Borowsky M.L., et al. Genome-wide chromatin interactions of the Nanog locus in pluripotency, differentiation, and reprogramming. Cell Stem Cell 2013, 12:699-712.
4. Cavalli G., Misteli T. Functional implications of genome topology. Nat. Struct. Mol. Biol. 2013, 20:290-299.
5. Chang D.J., Cimprich K.A. DNA damage tolerance: when it's OK to make mistakes. Nat. Chem. Biol. 2009, 5:82-90.
6. Cheng L., Hansen N.F., Zhao L., Du Y., Zou C., Donovan F.X., Chou B.K., Zhou G., Li S., Dowey S.N., et al. Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem Cell 2012, 10:337-344. NISC Comparative Sequencing Program.
7. De S., Michor F. DNA replication timing and long-range DNA interactions predict mutational landscapes of cancer genomes. Nat. Biotechnol. 2011, 29:1103-1108.
8. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
9. Fudenberg G., Getz G., Meyerson M., Mirny L.A. High order chromatin architecture shapes the landscape of chromosomal alterations in cancer. Nat. Biotechnol. 2011, 29:1109-1113.
10. Gilbert D.M., Takebayashi S.I., Ryba T., Lu J., Pope B.D., Wilson K.A., Hiratani I. Space and time in the nucleus: developmental control of replication timing and chromosome architecture. Cold Spring Harb. Symp. Quant. Biol. 2010, 75:143-153.
11. Goodarzi A.A., Noon A.T., Deckbar D., Ziv Y., Shiloh Y., Löbrich M., Jeggo P.A. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 2008, 31:167-177.
12. Gore A., Li Z., Fung H.L., Young J.E., Agarwal S., Antosiewicz-Bourget J., Canto I., Giorgetti A., Israel M.A., Kiskinis E., et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011, 471:63-67.
13. Hansen R.S., Thomas S., Sandstrom R., Canfield T.K., Thurman R.E., Weaver M., Dorschner M.O., Gartler S.M., Stamatoyannopoulos J.A. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc. Natl. Acad. Sci. USA 2010, 107:139-144.
14. Helmrich A., Ballarino M., Nudler E., Tora L. Transcription-replication encounters, consequences and genomic instability. Nat. Struct. Mol. Biol. 2013, 20:412-418.
15. Hiratani I., Ryba T., Itoh M., Yokochi T., Schwaiger M., Chang C.W., Lyou Y., Townes T.M., Schübeler D., Gilbert D.M. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 2008, 6:e245.
16. Hiratani I., Ryba T., Itoh M., Rathjen J., Kulik M., Papp B., Fussner E., Bazett-Jones D.P., Plath K., Dalton S., et al. Genome-wide dynamics of replication timing revealed by invitro models of mouse embryogenesis. Genome Res. 2010, 20:155-169.
17. Hu M., Deng K., Qin Z., Dixon J., Selvaraj S., Fang J., Ren B., Liu J.S. Bayesian inference of spatial organizations of chromosomes. PLoS Comput. Biol. 2013, 9:e1002893.
18. Hussein S.M., Batada N.N., Vuoristo S., Ching R.W., Autio R., Närvä E., Ng S., Sourour M., Hämäläinen R., Olsson C., et al. Copy number variation and selection during reprogramming to pluripotency. Nature 2011, 471:58-62.
19. Koren A., Polak P., Nemesh J., Michaelson J.J., Sebat J., Sunyaev S.R., McCarroll S.A. Differential relationship of DNA replication timing to different forms of human mutation and variation. Am. J. Hum. Genet. 2012, 91:1033-1040.
20. Labib K., Hodgson B. Replication fork barriers: pausing for a break or stalling for time?. EMBO Rep. 2007, 8:346-353.
21. Laurent L.C., Ulitsky I., Slavin I., Tran H., Schork A., Morey R., Lynch C., Harness J.V., Lee S., Barrero M.J., et al. Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCsand iPSCs during reprogramming and time in culture. Cell Stem Cell 2011, 8:106-118.
22. Leonhardt H., Rahn H.P., Weinzierl P., Sporbert A., Cremer T., Zink D., Cardoso M.C. Dynamics of DNA replication factories in living cells. J.Cell Biol. 2000, 149:271-280.
23. Liang G., Zhang Y. Genetic and epigenetic variations in iPSCs: potential causes and implications for application. Cell Stem Cell 2013, 13:149-159.
24. Liu L., De S., Michor F. DNA replication timing and higher-order nuclear organization determine single-nucleotide substitution patterns in cancer genomes. Nat. Commun. 2013, 4:1502.
25. MacDonald J.R., Ziman R., Yuen R.K., Feuk L., Scherer S.W. The database of genomic variants: a curated collection of structural variation in the human genome. Nucleic Acids Res. 2014, 42:D986-D992.
26. Martins-Taylor K., Nisler B.S., Taapken S.M., Compton T., Crandall L., Montgomery K.D., Lalande M., Xu R.H. Recurrent copy number variations in human induced pluripotent stem cells. Nat. Biotechnol. 2011, 29:488-491.
27. Mayshar Y., Ben-David U., Lavon N., Biancotti J.C., Yakir B., Clark A.T., Plath K., Lowry W.E., Benvenisty N. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010, 7:521-531.
28. Misteli T. Parallel genome universes. Nat. Biotechnol. 2012, 30:55-56.
29. Murga M., Jaco I., Fan Y., Soria R., Martinez-Pastor B., Cuadrado M., Yang S.M., Blasco M.A., Skoultchi A.I., Fernandez-Capetillo O. Global chromatin compaction limits the strength of the DNA damage response. J.Cell Biol. 2007, 178:1101-1108.
30. Orkin S.H., Hochedlinger K. Chromatin connections to pluripotency and cellular reprogramming. Cell 2011, 145:835-850.
31. Park I.H., Lerou P.H., Zhao R., Huo H., Daley G.Q. Generation of human-induced pluripotent stem cells. Nat. Protoc. 2008, 3:1180-1186.
32. Phillips-Cremins J.E., Sauria M.E., Sanyal A., Gerasimova T.I., Lajoie B.R., Bell J.S., Ong C.T., Hookway T.A., Guo C., Sun Y., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 2013, 153:1281-1295.
33. Quinlan A.R., Boland M.J., Leibowitz M.L., Shumilina S., Pehrson S.M., Baldwin K.K., Hall I.M. Genome sequencing of mouse induced pluripotent stem cells reveals retroelement stability and infrequent DNA rearrangement during reprogramming. Cell Stem Cell 2011, 9:366-373.
34. Rübe C.E., Lorat Y., Schuler N., Schanz S., Wennemuth G., Rübe C. DNA repair in the context of chromatin: new molecular insights by the nanoscale detection of DNA repair complexes using transmission electron microscopy. DNA Repair (Amst.) 2011, 10:427-437.
35. Ryba T., Hiratani I., Lu J., Itoh M., Kulik M., Zhang J., Schulz T.C., Robins A.J., Dalton S., Gilbert D.M. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 2010, 20:761-770.
36. Ryba T., Battaglia D., Pope B.D., Hiratani I., Gilbert D.M. Genome-scale analysis of replication timing: from bench to bioinformatics. Nat. Protoc. 2011, 6:870-895.
37. Ryba T., Battaglia D., Chang B.H., Shirley J.W., Buckley Q., Pope B.D., Devidas M., Druker B.J., Gilbert D.M. Abnormal developmental control of replication-timing domains in pediatric acute lymphoblastic leukemia. Genome Res. 2012, 22:1833-1844.
38. Schuster-Böckler B., Lehner B. Chromatin organization is a major influence on regional mutation rates in human cancer cells. Nature 2012, 488:504-507.
39. Schwaiger M., Stadler M.B., Bell O., Kohler H., Oakeley E.J., Schübeler D. Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev. 2009, 23:589-601.
40. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
41. Wang P., Zhang W., Yang J., Qu J., Liu G.H. Higher-order genomic organization in pluripotent stem cells. Protein Cell 2012, 3:483-486.
42. Watanabe Y., Fujiyama A., Ichiba Y., Hattori M., Yada T., Sakaki Y., Ikemura T. Chromosome-wide assessment of replication timing for human chromosomes 11q and 21q: disease-related genes in timing-switch regions. Hum. Mol. Genet. 2002, 11:13-21.
43. Watanabe Y., Ikemura T., Sugimura H. Amplicons on human chromosome 11q are located in the early/late-switch regions of replication timing. Genomics 2004, 84:796-805.
44. Watanabe A., Yamada Y., Yamanaka S. Epigenetic regulation in pluripotent stem cells: a key to breaking the epigenetic barrier. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:20120292.
45. Wei Z., Gao F., Kim S., Yang H., Lyu J., An W., Wang K., Lu W. Klf4 organizes long-range chromosomal interactions with the oct4 locus in reprogramming and pluripotency. Cell Stem Cell 2013, 13:36-47.
46. Zhang H., Jiao W., Sun L., Fan J., Chen M., Wang H., Xu X., Shen A., Li T., Niu B., et al. Intrachromosomal looping is required for activation of endogenous pluripotency genes during reprogramming. Cell Stem Cell 2013, 13:30-35.