Comprehensive Analysis of Human Subtelomeres by Whole Genome Mapping
Autoři:
Eleanor Young aff001; Heba Z. Abid aff001; Pui-Yan Kwok aff002; Harold Riethman aff005; Ming Xiao aff001
Působiště autorů:
School of Biomedical Engineering, Drexel University, Philadelphia, PA, United States of America
aff001; Cardiovascular Research Institute, University of California–San Francisco, San Francisco, CA, United States of America
aff002; Department of Dermatology, University of California–San Francisco, San Francisco, CA, United States of America
aff003; Institute for Human Genetics, University of California–San Francisco, San Francisco, CA, United States of America
aff004; Medical Diagnostic & Translational Sciences, Old Dominium University, Norfolk, VA, United States of America
aff005; Institute of Molecular Medicine and Infectious Disease in the School of Medicine, Drexel University, Philadelphia, PA, United States of America
aff006
Vyšlo v časopise:
Comprehensive Analysis of Human Subtelomeres by Whole Genome Mapping. PLoS Genet 16(1): e32767. doi:10.1371/journal.pgen.1008347
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008347
Souhrn
Detailed comprehensive knowledge of the structures of individual long-range telomere-terminal haplotypes are needed to understand their impact on telomere function, and to delineate the population structure and evolution of subtelomere regions. However, the abundance of large evolutionarily recent segmental duplications and high levels of large structural variations have complicated both the mapping and sequence characterization of human subtelomere regions. Here, we use high throughput optical mapping of large single DNA molecules in nanochannel arrays for 154 human genomes from 26 populations to present a comprehensive look at human subtelomere structure and variation. The results catalog many novel long-range subtelomere haplotypes and determine the frequencies and contexts of specific subtelomeric duplicons on each chromosome arm, helping to clarify the currently ambiguous nature of many specific subtelomere structures as represented in the current reference sequence (HG38). The organization and content of some duplicons in subtelomeres appear to show both chromosome arm and population-specific trends. Based upon these trends we estimate a timeline for the spread of these duplication blocks.
Klíčová slova:
Haplotypes – Human genomics – Chromosome mapping – Chromosomes – Repeated sequences – Sequence assembly tools – Sequence motif analysis – Telomeres
Zdroje
1. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science. 2007;318(5851):798–801. Epub 2007/10/06. doi: 10.1126/science.1147182 17916692.
2. Porro A, Feuerhahn S, Delafontaine J, Riethman H, Rougemont J, Lingner J. Functional characterization of the TERRA transcriptome at damaged telomeres. Nature Communications. 2014;5. doi: 10.1038/ncomms6379 WOS:000344063500001. 25359189
3. Porro A, Feuerhahn S, Reichenbach P, Lingner J. Molecular Dissection of Telomeric Repeat-Containing RNA Biogenesis Unveils the Presence of Distinct and Multiple Regulatory Pathways. Molecular and Cellular Biology. 2010;30(20):4808–17. doi: 10.1128/MCB.00460-10 WOS:000282099300005. 20713443
4. Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM. TERRA RNA Binding to TRF2 Facilitates Heterochromatin Formation and ORC Recruitment at Telomeres. Molecular Cell. 2009;35(4):403–13. doi: 10.1016/j.molcel.2009.06.025 WOS:000269432600005. 19716786
5. Chu H-P, Cifuentes-Rojas C, Kesner B, Aeby E, Lee H-G, Wei C, et al. TERRA RNA Antagonizes ATRX and Protects Telomeres. Cell. 2017;170(1):86–101.e16. doi: 10.1016/j.cell.2017.06.017 28666128.
6. Britt-Compton B, Rowson J, Locke M, Mackenzie I, Kipling D, Baird DM. Structural stability and chromosome-specific telomere length is governed by cis-acting determinants in humans. Human Molecular Genetics. 2006;15(5):725–33. doi: 10.1093/hmg/ddi486 WOS:000235432900006. 16421168
7. Graakjaer J, Bischoff C, Korshohn L, Holstebroe S, Vach W, Bohr VA, et al. The pattern of chromosome-specific variations in telomere length in humans is determined by inherited, telomere-near factors and is maintained throughout life. Mechanisms of Ageing and Development. 2003;124(5):629–40. doi: 10.1016/s0047-6374(03)00081-2 WOS:000183121300007. 12735903
8. Graakjaer J, Der-Sarkissian H, Schmitz A, Bayer J, Thomas G, Kolvraa S, et al. Allele-specific relative telomere lengths are inherited. Human Genetics. 2006;119(3):344–50. doi: 10.1007/s00439-006-0137-x WOS:000237059100012. 16440201
9. Nergadze SG, Farnung BO, Wischnewski H, Khoriauli L, Vitelli V, Chawla R, et al. CpG-island promoters drive transcription of human telomeres. Rna-a Publication of the Rna Society. 2009;15(12):2186–94. doi: 10.1261/rna.1748309 WOS:000272169000010. 19850908
10. Caslini C, Connelly JA, Serna A, Broccoli D, Hess JL. MLL Associates with Telomeres and Regulates Telomeric Repeat-Containing RNA Transcription. Molecular and Cellular Biology. 2009;29(16):4519–26. doi: 10.1128/MCB.00195-09 WOS:000268310000015. 19528237
11. Deng Z, Campbell AE, Lieberman PM. TERRA, CpG methylation and telomere heterochromatin Lessons from ICF syndrome cells. Cell Cycle. 2010;9(1):69–74. doi: 10.4161/cc.9.1.10358 WOS:000273236800024. 20016274
12. Yehezkel S, Segev Y, Viegas-Pequignot E, Skorecki K, Selig S. Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Human Molecular Genetics. 2008;17(18):2776–89. doi: 10.1093/hmg/ddn177 WOS:000258863200003. 18558631
13. Kermouni A, Vanroost E, Arden KC, Vermeesch JR, Weiss S, Godelaine D, et al. THE IL-9 RECEPTOR GENE (IL9R)—GENOMIC STRUCTURE, CHROMOSOMAL LOCALIZATION IN THE PSEUDOAUTOSOMAL REGION OF THE LONG ARM OF THE SEX-CHROMOSOMES, AND IDENTIFICATION OF IL9R PSEUDOGENES AT 9QTER, 10PTER, 16PTER, AND 18PTER. Genomics. 1995;29(2):371–82. WOS:A1995RY05500008. doi: 10.1006/geno.1995.9992 8666384
14. Linardopoulou EV, Parghi SS, Friedman C, Osborn GE, Parkhurst SM, Trask BJ. Human subtelomeric WASH genes encode a new subclass of the WASP family. Plos Genetics. 2007;3(12):2477–85. doi: 10.1371/journal.pgen.0030237 WOS:000253317800013. 18159949
15. Linardopoulou E, Mefford HC, Nguyen O, Friedman C, van den Engh G, Farwell DG, et al. Transcriptional activity of multiple copies of a subtelomerically located olfactory receptor gene that is polymorphic in number and location. Human Molecular Genetics. 2001;10(21):2373–83. doi: 10.1093/hmg/10.21.2373 WOS:000171946100006. 11689484
16. Mah N, Stoehr H, Schulz HL, White K, Weber BHF. Identification of a novel retina-specific gene located in a subtelomeric region with polymorphic distribution among multiple human chromosomes. Biochimica Et Biophysica Acta-Gene Structure and Expression. 2001;1522(3):167–74. doi: 10.1016/s0167-4781(01)00328-1 WOS:000173001600004.
17. Riethman H, Ambrosini A, Castaneda C, Finklestein J, Hu XL, Mudunuri U, et al. Mapping and initial analysis of human subtelomeric sequence assemblies. Genome Research. 2004;14(1):18–28. doi: 10.1101/gr.1245004 WOS:000187889600003. 14707167
18. Cabianca DS, Casa V, Bodega B, Xynos A, Ginelli E, Tanaka Y, et al. A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell. 2012;149(4):819–31. doi: 10.1016/j.cell.2012.03.035 MEDLINE:22541069. 22541069
19. Lou Z, Wei J, Riethman H, Baur JA, Voglauer R, Shay JW, et al. Telomere length regulates ISG15 expression in human cells. Aging-Us. 2009;1(7):608–21. WOS:000276401400003.
20. Robin JD, Ludlow AT, Batten K, Magdinier F, Stadler G, Wagner KR, et al. Telomere position effect: regulation of gene expression with progressive telomere shortening over long distances. Genes & Development. 2014;28(22):2464–76. doi: 10.1101/gad.251041.114 WOS:000345269300004. 25403178
21. Church DM, Schneider VA, Graves T, Auger K, Cunningham F, Bouk N, et al. Modernizing Reference Genome Assemblies. PLOS Biology. 2011;9(7):e1001091. doi: 10.1371/journal.pbio.1001091 21750661
22. Young E, Pastor S, Rajagopalan R, McCaffrey J, Sibert J, Mak AC, et al. High-throughput single-molecule mapping links subtelomeric variants and long-range haplotypes with specific telomeres. Nucleic acids research. 2017. Epub 2017/02/10. doi: 10.1093/nar/gkx017 28180280.
23. Riethman H. Human subtelomeric copy number variations. Cytogenet Genome Res. 2008;123(1–4):244–52. Epub 03/11. doi: 10.1159/000184714 19287161.
24. Stong N, Deng Z, Gupta R, Hu S, Paul S, Weiner AK, et al. Subtelomeric CTCF and cohesin binding site organization using improved subtelomere assemblies and a novel annotation pipeline. Genome Research. 2014;24(6):1039–50. doi: 10.1101/gr.166983.113 WOS:000336662200015. 24676094
25. Kidd JM, Cooper GM, Donahue WF, Hayden HS, Sampas N, Graves T, et al. Mapping and sequencing of structural variation from eight human genomes. Nature. 2008;453(7191):56–64. Epub 2008/05/03. doi: 10.1038/nature06862 18451855; PubMed Central PMCID: PMC2424287.
26. Linardopoulou EV, Williams EM, Fan Y, Friedman C, Young JM, Trask BJ. Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature. 2005;437. doi: 10.1038/nature04029 16136133
27. Lam ET, Hastie A, Lin C, Ehrlich D, Das SK, Austin MD, et al. Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly. Nature Biotechnology. 2012;30(8):771–6. doi: 10.1038/nbt.2303 WOS:000307416900020. 22797562
28. Mak ACY, Lai YYY, Lam ET, Kwok T-P, Leung AKY, Poon A, et al. Genome-Wide Structural Variation Detection by Genome Mapping on Nanochannel Arrays. Genetics. 2015. doi: 10.1534/genetics.115.183483 26510793
29. Alkan C, Sajjadian S, Eichler EE. Limitations of next-generation genome sequence assembly. Nat Methods. 2011;8(1):61–5. doi: 10.1038/nmeth.1527 WOS:000285712000023. 21102452
30. Riethman HC, Xiang Z, Paul S, Morse E, Hu XL, Flint J, et al. Integration of telomere sequences with the draft human genome sequence. Nature. 2001;409(6822):948–51. doi: 10.1038/35057180 11237019
31. Levy-Sakin M, Pastor S, Mostovoy Y, Li L, Leung AKY, McCaffrey J, et al. Genome maps across 26 human populations reveal population-specific patterns of structural variation. Nature Communications. 2019;10(1):1025. doi: 10.1038/s41467-019-08992-7 30833565
32. McCaffrey J, Young E, Lassahn K, Sibert J, Pastor S, Riethman H, et al. High-throughput single-molecule telomere characterization. Genome research. 2017;27(11):1904–15. doi: 10.1101/gr.222422.117 29025896.
33. Macina RA, Negorev DG, Spais C, Ruthig LA, Hu XL, Riethman HC. SEQUENCE ORGANIZATION OF THE HUMAN-CHROMOSOME 2Q TELOMERE. Human Molecular Genetics. 1994;3(10):1847–53. doi: 10.1093/hmg/3.10.1847 WOS:A1994PN13800022. 7545974
34. Inglehearn CF, Cooke HJ. A VNTR immediately adjacent to the human pseudoautosomal telomere. Nucleic acids research. 1990;18(3):471–6. doi: 10.1093/nar/18.3.471 2155401.
35. Brown WR. A physical map of the human pseudoautosomal region. EMBO J. 1988;7(8):2377–85. 2847916.
36. Genomics B. Bionano Prep Direct Label and Stain (DLS) Protocol 2018 [cited 2019 4/11/19]. Available from: https://bionanogenomics.com/wp-content/uploads/2018/04/30206-Bionano-Prep-Direct-Label-and-Stain-DLS-Protocol.pdf.
37. Wilkie AOM, Higgs DR, Rack KA, Buckle VJ, Spurr NK, Fischel-Ghodsian N, et al. Stable length polymorphism of up to 260 kb at the tip of the short arm of human chromosome 16. Cell. 1991;64(3):595–606. doi: 10.1016/0092-8674(91)90243-r 1991321
38. Xiang Z, Hu XL, Flint J, Riethman HC. A Sequence-Ready Map of the Human Chromosome 17p Telomere. Genomics. 1999;58(2):207–10. doi: 10.1006/geno.1999.5826 10366453
39. Zeng W, Chen Y-Y, Newkirk DA, Wu B, Balog J, Kong X, et al. Genetic and Epigenetic Characteristics of FSHD-Associated 4q and 10q D4Z4 that are Distinct from Non-4q/10q D4Z4 Homologs. Human Mutation. 2014;35(8):998–1010. doi: 10.1002/humu.22593 WOS:000339431600014. 24838473
40. Trask BJ, Friedman C, Martin-Gallardo A, Rowen L, Akinbami C, Blankenship J, et al. Members of the olfactory receptor gene family are contained in large blocks of DNA duplicated polymorphically near the ends of human chromosomes. Human Molecular Genetics. 1998;7(1):13–26. doi: 10.1093/hmg/7.1.13 9384599
41. Der-Sarkissian H, Vergnaud G, Borde Y-M, Thomas G, Londoño-Vallejo J-A. Segmental Polymorphisms in the Proterminal Regions of a Subset of Human Chromosomes. Genome Research. 2002;12(11):1673–8. doi: 10.1101/gr.322802 12421753
42. Hastie AR, Dong L, Smith A, Finklestein J, Lam ET, Huo N, et al. Rapid Genome Mapping in Nanochannel Arrays for Highly Complete and Accurate De Novo Sequence Assembly of the Complex Aegilops tauschii Genome. Plos One. 2013;8(2). doi: 10.1371/journal.pone.0055864 WOS:000315153400168. 23405223
43. Mefford HC, Trask BJ. The complex structure and dynamic evolution of human subtelomeres. Nature Reviews Genetics. 2002;3:91+. doi: 10.1038/nrg727 11836503
44. Brown CA, Murray AW, Verstrepen KJ. Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Current biology: CB. 2010;20(10):895–903. Epub 2010/05/18. doi: 10.1016/j.cub.2010.04.027 20471265; PubMed Central PMCID: PMC2877759.
45. Chen NWG, Thareau V, Ribeiro T, Magdelenat G, Ashfield T, Innes RW, et al. Common Bean Subtelomeres Are Hot Spots of Recombination and Favor Resistance Gene Evolution. Frontiers in plant science. 2018;9:1185. Epub 2018/08/30. doi: 10.3389/fpls.2018.01185 30154814; PubMed Central PMCID: PMC6102362.
46. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, et al. The Genome of the African Trypanosome Trypanosoma brucei. Science. 2005;309(5733):416–22. doi: 10.1126/science.1112642 16020726
47. Xiao M, Phong A, Ha C, Chan T-F, Cai D, Leung L, et al. Rapid DNA mapping by fluorescent single molecule detection. Nucleic acids research. 2007;35(3). doi: 10.1093/nar/gkl987 WOS:000244429800003.
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