The structure, function and evolution of a complete human chromosome 8.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
05 2021
Historique:
received: 04 09 2020
accepted: 04 03 2021
pubmed: 9 4 2021
medline: 28 5 2021
entrez: 8 4 2021
Statut: ppublish

Résumé

The complete assembly of each human chromosome is essential for understanding human biology and evolution

Identifiants

pubmed: 33828295
doi: 10.1038/s41586-021-03420-7
pii: 10.1038/s41586-021-03420-7
pmc: PMC8099727
mid: NIHMS1696366
doi:

Substances chimiques

DNA, Satellite 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

101-107

Subventions

Organisme : NHGRI NIH HHS
ID : K99 HG011041
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG011274
Pays : United States
Organisme : NHGRI NIH HHS
ID : R21 HG010548
Pays : United States
Organisme : NHGRI NIH HHS
ID : U01 HG010971
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG002385
Pays : United States
Organisme : NIAMS NIH HHS
ID : P30 AR074990
Pays : United States
Organisme : NLM NIH HHS
ID : T32 LM012419
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NIGMS NIH HHS
ID : F32 GM134558
Pays : United States
Organisme : NHGRI NIH HHS
ID : T32 HG000035
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG010169
Pays : United States

Références

International Human Genome Project Consortium. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).
doi: 10.1038/35057062
Venter, J. C. et al. The sequence of the human genome. Science 291, 1304–1351 (2001).
pubmed: 11181995 doi: 10.1126/science.1058040
Alkan, C. et al. Genome-wide characterization of centromeric satellites from multiple mammalian genomes. Genome Res. 21, 137–145 (2011).
pubmed: 21081712 pmcid: 3012921 doi: 10.1101/gr.111278.110
International Human Genome Sequencing Consortium. Finishing the euchromatic sequence of the human genome. Nature 431, 931–945 (2004).
doi: 10.1038/nature03001
Nurk, S. et al. HiCanu: accurate assembly of segmental duplications, satellites, and allelic variants from high-fidelity long reads. Genome Res. gr.263566.120 (2020).
Cheng, H., Concepcion, G. T., Feng, X., Zhang, H. & Li, H. Haplotype-resolved de novo assembly with phased assembly graphs. Nat. Methods 18, 170–175 (2021).
pubmed: 33526886 doi: 10.1038/s41592-020-01056-5 pmcid: 7961889
Logsdon, G. A., Vollger, M. R. & Eichler, E. E. Long-read human genome sequencing and its applications. Nat. Rev. Genet. 21, 597–614 (2020).
pubmed: 32504078 pmcid: 7877196 doi: 10.1038/s41576-020-0236-x
McNulty, S. M. & Sullivan, B. A. Alpha satellite DNA biology: finding function in the recesses of the genome. Chromosome Res. 26, 115–138 (2018).
pubmed: 29974361 pmcid: 6121732 doi: 10.1007/s10577-018-9582-3
Ge, Y., Wagner, M. J., Siciliano, M. & Wells, D. E. Sequence, higher order repeat structure, and long-range organization of alpha satellite DNA specific to human chromosome 8. Genomics 13, 585–593 (1992).
pubmed: 1639387 doi: 10.1016/0888-7543(92)90128-F
Hollox, E. J., Armour, J. A. & Barber, J. C. K. Extensive normal copy number variation of a β-defensin antimicrobial-gene cluster. Am. J. Hum. Genet. 73, 591–600 (2003).
pubmed: 12916016 pmcid: 1180683 doi: 10.1086/378157
Hollox, E. J. et al. Psoriasis is associated with increased beta-defensin genomic copy number. Nat. Genet. 40, 23–25 (2008).
pubmed: 18059266 doi: 10.1038/ng.2007.48
Mohajeri, K. et al. Interchromosomal core duplicons drive both evolutionary instability and disease susceptibility of the chromosome 8p23.1 region. Genome Res. 26, 1453–1467 (2016).
pubmed: 27803192 pmcid: 5088589 doi: 10.1101/gr.211284.116
Miga, K. H. et al. Telomere-to-telomere assembly of a complete human X chromosome. Nature 585, 79–84 (2020).
pubmed: 32663838 pmcid: 7484160 doi: 10.1038/s41586-020-2547-7
Sudmant, P. H. et al. Diversity of human copy number variation and multicopy genes. Science 330, 641–646 (2010).
pubmed: 21030649 pmcid: 3020103 doi: 10.1126/science.1197005
Falconer, E. & Lansdorp, P. M. Strand-seq: a unifying tool for studies of chromosome segregation. Semin. Cell Dev. Biol. 24, 643–652 (2013).
pubmed: 23665005 doi: 10.1016/j.semcdb.2013.04.005
Sanders, A. D., Falconer, E., Hills, M., Spierings, D. C. J. & Lansdorp, P. M. Single-cell template strand sequencing by Strand-seq enables the characterization of individual homologs. Nat. Protocols 12, 1151–1176 (2017).
pubmed: 28492527 doi: 10.1038/nprot.2017.029
Rhie, A., Walenz, B. P., Koren, S. & Phillippy, A. M. Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol. 21, 245 (2020).
pubmed: 32928274 pmcid: 7488777 doi: 10.1186/s13059-020-02134-9
Simpson, J. T. et al. Detecting DNA cytosine methylation using nanopore sequencing. Nat. Methods 14, 407–410 (2017).
pubmed: 28218898 doi: 10.1038/nmeth.4184
Devriendt, K. et al. Delineation of the critical deletion region for congenital heart defects, on chromosome 8p23.1. Am. J. Hum. Genet. 64, 1119–1126 (1999).
pubmed: 10090897 pmcid: 1377836 doi: 10.1086/302330
Giglio, S. et al. Heterozygous submicroscopic inversions involving olfactory receptor-gene clusters mediate the recurrent t(4;8)(p16;p23) translocation. Am. J. Hum. Genet. 71, 276–285 (2002).
pubmed: 12058347 pmcid: 379160 doi: 10.1086/341610
Cantsilieris, S. & White, S. J. Correlating multiallelic copy number polymorphisms with disease susceptibility. Hum. Mutat. 34, 1–13 (2013).
pubmed: 22837109 doi: 10.1002/humu.22172
Tyson, C. et al. Expansion of a 12-kb VNTR containing the REXO1L1 gene cluster underlies the microscopically visible euchromatic variant of 8q21.2. Eur. J. Hum. Genet. 22, 458–463 (2014).
pubmed: 24045839 doi: 10.1038/ejhg.2013.185
Warburton, P. E. et al. Analysis of the largest tandemly repeated DNA families in the human genome. BMC Genomics 9, 533 (2008).
pubmed: 18992157 pmcid: 2588610 doi: 10.1186/1471-2164-9-533
Hasson, D. et al. Formation of novel CENP-A domains on tandem repetitive DNA and across chromosome breakpoints on human chromosome 8q21 neocentromeres. Chromosoma 120, 621–632 (2011).
pubmed: 21826412 doi: 10.1007/s00412-011-0337-6
Hasson, D. et al. The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat. Struct. Mol. Biol. 20, 687–695 (2013).
pubmed: 23644596 pmcid: 3760417 doi: 10.1038/nsmb.2562
Alkan, C. et al. Organization and evolution of primate centromeric DNA from whole-genome shotgun sequence data. PLOS Comput. Biol. 3, 1807–1818 (2007).
pubmed: 17907796 doi: 10.1371/journal.pcbi.0030181
Cacheux, L., Ponger, L., Gerbault-Seureau, M., Richard, F. A. & Escudé, C. Diversity and distribution of alpha satellite DNA in the genome of an Old World monkey: Cercopithecus solatus. BMC Genomics 17, 916 (2016).
pubmed: 27842493 pmcid: 5109768 doi: 10.1186/s12864-016-3246-5
Jain, M. et al. Linear assembly of a human centromere on the Y chromosome. Nat. Biotechnol. 36, 321–323 (2018).
pubmed: 29553574 pmcid: 5886786 doi: 10.1038/nbt.4109
Warburton, P. E. et al. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr. Biol. 7, 901–904 (1997).
pubmed: 9382805 doi: 10.1016/S0960-9822(06)00382-4
Vafa, O. & Sullivan, K. F. Chromatin containing CENP-A and α-satellite DNA is a major component of the inner kinetochore plate. Curr. Biol. 7, 897–900 (1997).
pubmed: 9382804 doi: 10.1016/S0960-9822(06)00381-2
Smith, G. P. Evolution of repeated DNA sequences by unequal crossover. Science 191, 528–535 (1976).
pubmed: 1251186 doi: 10.1126/science.1251186
Shepelev, V. A., Alexandrov, A. A., Yurov, Y. B. & Alexandrov, I. A. The evolutionary origin of man can be traced in the layers of defunct ancestral alpha satellites flanking the active centromeres of human chromosomes. PLoS Genet. 5, e1000641 (2009).
pubmed: 19749981 pmcid: 2729386 doi: 10.1371/journal.pgen.1000641
Alexandrov, I., Kazakov, A., Tumeneva, I., Shepelev, V. & Yurov, Y. Alpha-satellite DNA of primates: old and new families. Chromosoma 110, 253–266 (2001).
pubmed: 11534817 doi: 10.1007/s004120100146
Koga, A. et al. Evolutionary origin of higher-order repeat structure in alpha-satellite DNA of primate centromeres. DNA Res. 21, 407–415 (2014).
pubmed: 24585002 pmcid: 4131833 doi: 10.1093/dnares/dsu005
Alexandrov, I. A., Mitkevich, S. P. & Yurov, Y. B. The phylogeny of human chromosome specific alpha satellites. Chromosoma 96, 443–453 (1988).
pubmed: 3219915 doi: 10.1007/BF00303039
Vollger, M. R. et al. Improved assembly and variant detection of a haploid human genome using single-molecule, high-fidelity long reads. Ann. Hum. Genet. 84, 125–140 (2019).
pubmed: 31711268 pmcid: 7015760 doi: 10.1111/ahg.12364
Huddleston, J. et al. Reconstructing complex regions of genomes using long-read sequencing technology. Genome Res. 24, 688–696 (2014).
pubmed: 24418700 pmcid: 3975067 doi: 10.1101/gr.168450.113
Garg, S. et al. Chromosome-scale, haplotype-resolved assembly of human genomes. Nat. Biotechnol. 39, 309–312 (2021).
Porubsky, D. et al. Fully phased human genome assembly without parental data using single-cell strand sequencing and long reads. Nat. Biotechnol. 39, 302–308 (2021).
Ebert, P. et al. Haplotype-resolved diverse human genomes and integrated analysis of structural variation. Science https://doi.org/10.1126/science.abf7117 (2021).
Logsdon, G. A. HMW gDNA purification and ONT ultra-long-read data generation. protocols.io https://doi.org/10.17504/protocols.io.bchhit36 (2020).
Dvorkina, T., Bzikadze, A. V. & Pevzner, P. A. The string decomposition problem and its applications to centromere analysis and assembly. Bioinformatics 36 (Suppl. 1), i93–i101 (2020).
pubmed: 32657390 pmcid: 7428072 doi: 10.1093/bioinformatics/btaa454
Jain, C. et al. Weighted minimizer sampling improves long read mapping. Bioinformatics 36 (Suppl. 1), i111–i118 (2020).
pubmed: 32657365 doi: 10.1093/bioinformatics/btaa435 pmcid: 7355284
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242 pmcid: 6137996 doi: 10.1093/bioinformatics/bty191
Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589–595 (2010).
pubmed: 20080505 pmcid: 2828108 doi: 10.1093/bioinformatics/btp698
Tarasov, A., Vilella, A. J., Cuppen, E., Nijman, I. J. & Prins, P. Sambamba: fast processing of NGS alignment formats. Bioinformatics 31, 2032–2034 (2015).
pubmed: 25697820 pmcid: 4765878 doi: 10.1093/bioinformatics/btv098
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Porubsky, D. et al. breakpointR: an R/Bioconductor package to localize strand state changes in Strand-seq data. Bioinformatics 36, 1260–1261 (2020).
pubmed: 31504176 doi: 10.1093/bioinformatics/btz681
Chaisson, M. J. P. et al. Multi-platform discovery of haplotype-resolved structural variation in human genomes. Nat. Commun. 10, 1784 (2019).
pubmed: 30992455 pmcid: 6467913 doi: 10.1038/s41467-018-08148-z
Sanders, A. D. et al. Characterizing polymorphic inversions in human genomes by single-cell sequencing. Genome Res. 26, 1575–1587 (2016).
pubmed: 27472961 pmcid: 5088599 doi: 10.1101/gr.201160.115
Ghareghani, M. et al. Strand-seq enables reliable separation of long reads by chromosome via expectation maximization. Bioinformatics 34, i115–i123 (2018).
pubmed: 29949971 pmcid: 6022540 doi: 10.1093/bioinformatics/bty290
Mikheenko, A., Bzikadze, A. V., Gurevich, A., Miga, K. H. & Pevzner, P. A. TandemTools: mapping long reads and assessing/improving assembly quality in extra-long tandem repeats. Bioinformatics 36 (Suppl. 1), i75–i83 (2020).
pubmed: 32657355 pmcid: 7355294 doi: 10.1093/bioinformatics/btaa440
Lee, I. et al. Simultaneous profiling of chromatin accessibility and methylation on human cell lines with nanopore sequencing. Nat. Methods 17, 1191–1199 (2020).
pubmed: 33230324 doi: 10.1038/s41592-020-01000-7 pmcid: 7704922
Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011).
pubmed: 21221095 pmcid: 3346182 doi: 10.1038/nbt.1754
Dougherty, M. L. et al. Transcriptional fates of human-specific segmental duplications in brain. Genome Res. 28, 1566–1576 (2018).
pubmed: 30228200 pmcid: 6169893 doi: 10.1101/gr.237610.118
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677 doi: 10.1093/bioinformatics/btt656
Harrow, J. et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760–1774 (2012).
pubmed: 22955987 pmcid: 3431492 doi: 10.1101/gr.135350.111
Pertea, M. et al. CHESS: a new human gene catalog curated from thousands of large-scale RNA sequencing experiments reveals extensive transcriptional noise. Genome Biol. 19, 208 (2018).
pubmed: 30486838 pmcid: 6260756 doi: 10.1186/s13059-018-1590-2
Shumate, A. & Salzberg, S. L. Liftoff: an accurate gene annotation mapping tool. Bioinformatics https://doi.org/10.1093/bioinformatics/btaa1016 (2020).
doi: 10.1093/bioinformatics/btaa1016 pubmed: 33320174
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).
Parsons, J. D. Miropeats: graphical DNA sequence comparisons. Bioinformatics 11, 615–619 (1995).
doi: 10.1093/bioinformatics/11.6.615
Bergström, A. et al. Insights into human genetic variation and population history from 929 diverse genomes. Science 367, eaay5012 (2020).
pubmed: 32193295 pmcid: 7115999 doi: 10.1126/science.aay5012
Mafessoni, F. et al. A high-coverage Neandertal genome from Chagyrskaya Cave. Proc. Natl Acad. Sci. USA 117, 15132–15136 (2020).
pubmed: 32546518 doi: 10.1073/pnas.2004944117 pmcid: 7334501
Mallick, S. et al. The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature 538, 201–206 (2016).
pubmed: 27654912 pmcid: 5161557 doi: 10.1038/nature18964
Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222–226 (2012).
pubmed: 22936568 pmcid: 3617501 doi: 10.1126/science.1224344
Prado-Martinez, J. et al. Great ape genetic diversity and population history. Nature 499, 471–475 (2013).
pubmed: 23823723 pmcid: 3822165 doi: 10.1038/nature12228
Prüfer, K. et al. A high-coverage Neandertal genome from Vindija Cave in Croatia. Science 358, 655–658 (2017).
pubmed: 28982794 pmcid: 6185897 doi: 10.1126/science.aao1887
Hach, F. et al. mrsFAST: a cache-oblivious algorithm for short-read mapping. Nat. Methods 7, 576–577 (2010).
pubmed: 20676076 pmcid: 3115707 doi: 10.1038/nmeth0810-576
Gymrek, M., Golan, D., Rosset, S. & Erlich, Y. lobSTR: A short tandem repeat profiler for personal genomes. Genome Res. 22, 1154–1162 (2012).
pubmed: 22522390 pmcid: 3371701 doi: 10.1101/gr.135780.111
Haaf, T. & Willard, H. F. Chromosome-specific alpha-satellite DNA from the centromere of chimpanzee chromosome 4. Chromosoma 106, 226–232 (1997).
pubmed: 9254724 doi: 10.1007/s004120050243
Iwata-Otsubo, A. et al. Expanded satellite repeats amplify a discrete CENP-A nucleosome assembly site on chromosomes that drive in female meiosis. Curr. Biol. 27, 2365–2373.e8 (2017).
pubmed: 28756949 pmcid: 5567862 doi: 10.1016/j.cub.2017.06.069
Logsdon, G. A. et al. Human artificial chromosomes that bypass centromeric DNA. Cell 178, 624–639.e19 (2019).
pubmed: 31348889 pmcid: 6657561 doi: 10.1016/j.cell.2019.06.006
Ventura, M. et al. Gorilla genome structural variation reveals evolutionary parallelisms with chimpanzee. Genome Res. 21, 1640–1649 (2011).
pubmed: 21685127 pmcid: 3202281 doi: 10.1101/gr.124461.111
Darby, I. A. In Situ Hybridization Protocols (Humana Press, 2000).
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10–12 (2011).
doi: 10.14806/ej.17.1.200
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).
Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187-91 (2014).
pubmed: 24799436 pmcid: 4086134 doi: 10.1093/nar/gku365
Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-4.0 (2013).
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690 pmcid: 3603318 doi: 10.1093/molbev/mst010
Nakamura, T., Yamada, K. D., Tomii, K. & Katoh, K. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 34, 2490–2492 (2018).
pubmed: 29506019 pmcid: 6041967 doi: 10.1093/bioinformatics/bty121
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430 doi: 10.1093/molbev/msu300
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128 (2007).
pubmed: 17050570 doi: 10.1093/bioinformatics/btl529
Tamura, K. & Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526 (1993).
pubmed: 8336541
Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, 1983).
Numanagić, I. et al. Fast characterization of segmental duplications in genome assemblies. Bioinformatics 34, i706–i714 (2018).
pubmed: 30423092 pmcid: 6129265 doi: 10.1093/bioinformatics/bty586
Landry, J. J. M. et al. The genomic and transcriptomic landscape of a HeLa cell line. G3 (Bethesda) 3, 1213–1224 (2013).
doi: 10.1534/g3.113.005777

Auteurs

Glennis A Logsdon (GA)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Mitchell R Vollger (MR)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

PingHsun Hsieh (P)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Yafei Mao (Y)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Mikhail A Liskovykh (MA)

Developmental Therapeutics Branch, National Cancer Institute, Bethesda, MD, USA.

Sergey Koren (S)

Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.

Sergey Nurk (S)

Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.

Ludovica Mercuri (L)

Department of Biology, University of Bari, Aldo Moro, Bari, Italy.

Philip C Dishuck (PC)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Arang Rhie (A)

Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.

Leonardo G de Lima (LG)

Stowers Institute for Medical Research, Kansas City, MO, USA.

Tatiana Dvorkina (T)

Center for Algorithmic Biotechnology, Institute of Translational Biomedicine, Saint Petersburg State University, Saint Petersburg, Russia.

David Porubsky (D)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

William T Harvey (WT)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Alla Mikheenko (A)

Center for Algorithmic Biotechnology, Institute of Translational Biomedicine, Saint Petersburg State University, Saint Petersburg, Russia.

Andrey V Bzikadze (AV)

Graduate Program in Bioinformatics and Systems Biology, University of California, San Diego, San Diego, CA, USA.

Milinn Kremitzki (M)

McDonnell Genome Institute, Department of Genetics, Washington University School of Medicine, St Louis, MO, USA.

Tina A Graves-Lindsay (TA)

McDonnell Genome Institute, Department of Genetics, Washington University School of Medicine, St Louis, MO, USA.

Chirag Jain (C)

Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.

Kendra Hoekzema (K)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Shwetha C Murali (SC)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.
Howard Hughes Medical Institute, University of Washington, Seattle, WA, USA.

Katherine M Munson (KM)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Carl Baker (C)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Melanie Sorensen (M)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Alexandra M Lewis (AM)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA.

Urvashi Surti (U)

Department of Pathology, University of Pittsburgh, Pittsburgh, PA, USA.

Jennifer L Gerton (JL)

Stowers Institute for Medical Research, Kansas City, MO, USA.

Vladimir Larionov (V)

Developmental Therapeutics Branch, National Cancer Institute, Bethesda, MD, USA.

Mario Ventura (M)

Department of Biology, University of Bari, Aldo Moro, Bari, Italy.

Karen H Miga (KH)

Center for Biomolecular Science and Engineering, University of California, Santa Cruz, Santa Cruz, CA, USA.

Adam M Phillippy (AM)

Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.

Evan E Eichler (EE)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA. eee@gs.washington.edu.
Howard Hughes Medical Institute, University of Washington, Seattle, WA, USA. eee@gs.washington.edu.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C

Classifications MeSH