Novel H3K4me3 marks are enriched at humanand chimpanzee-specific cytogenetic structures

Genome Research

Volumn 24, Issue 9, 2014, Pages 1455-1468

  Giannuzzi, Giuliana ^a   Migliavacca, Eugenia ^a,b   Reymond, Alexandre ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE;

ARTICLE; CELL LINEAGE; CENTROMERE; CHIMPANZEE; CHROMOSOME 1; CHROMOSOME 18; CHROMOSOME 2; CYTOGENETICS; EPIGENETICS; FUSION GENE; GENE LOCUS; GENE SEQUENCE; GENE STRUCTURE; GENOME ANALYSIS; HETEROCHROMATIN; HISTONE MODIFICATION; HUMAN; LYMPHOBLASTOID CELL LINE; NONHUMAN; PERICENTRIC CHROMOSOME INVERSION; PREFRONTAL CORTEX; REGULATORY SEQUENCE; RNA SEQUENCE; SEGMENTAL DUPLICATION; SPECIES; SPECIES DIFFERENCE; TRANSCRIPTION INITIATION SITE; ANIMAL; ANTIBODY SPECIFICITY; CHROMOSOME ABERRATION; CHROMOSOME BREAKAGE; GENETICS; HUMAN GENOME; METABOLISM; PAN TROGLODYTES; TELOMERE;

ANIMALS; CENTROMERE; CHROMOSOME ABERRATIONS; CHROMOSOME BREAKPOINTS; GENOME, HUMAN; HISTONES; HUMANS; ORGAN SPECIFICITY; PAN TROGLODYTES; PREFRONTAL CORTEX; SPECIES SPECIFICITY; TELOMERE; TRANSCRIPTION INITIATION SITE;

EID: 84907188656     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.167742.113     Document Type: Article

References (90)

1. Anders S, Reyes A, Huber W. 2012. Detecting differential usage of exons from RNA-seq data. Genome Res 22: 2008-2017.
2. Antonacci F, Kidd JM, Marques-Bonet T, Teague B, Ventura M, Girirajan S, Alkan C, Campbell CD, Vives L, Malig M, et al. 2010. A large and complex structural polymorphism at 16p12.1 underlies microdeletion disease risk. Nat Genet 42: 745-750.
3. Bailey JA, Yavor AM, Massa HF, Trask BJ, Eichler EE. 2001. Segmental duplications: organization and impact within the current human genome project assembly. Genome Res 11: 1005-1017.
4. Bailey JA, Gu Z, Clark RA, Reinert K, Samonte RV, Schwartz S, Adams MD, Myers EW, LiPW, Eichler EE. 2002. Recent segmental duplications in the human genome. Science 297: 1003-1007.
5. Baldini A, Ried T, Shridhar V, Ogura K, D'Aiuto L, Rocchi M, Ward DC. 1993. An alphoid DNA sequence conserved in all human and great ape chromosomes: evidence for ancient centromeric sequences at human chromosomal regions 2q21 and 9q13. Hum Genet 90: 577-583.
6. Bardet AF, He Q, Zeitlinger J, Stark A. 2012. A computational pipeline for comparative ChIP-seq analyses. Nat Protoc 7: 45-61.
7. Bekpen C, Tastekin I, Siswara P, Akdis CA, Eichler EE. 2012. Primate segmental duplication creates novel promoters for the LRRC37 gene family within the 17q21.31 inversion polymorphism region. Genome Res 22: 1050-1058.
8. Cain CE, Blekhman R, Marioni JC, Gilad Y. 2011. Gene expression differences among primates are associated with changes in a histone epigenetic modification. Genetics 187: 1225-1234.
9. Chambers EV, Bickmore WA, Semple CA. 2013. Divergence of mammalian higher order chromatin structure is associated with developmental loci. PLoS Comput Biol 9: e1003017.
10. Chiaromonte F, Yap VB, MillerW. 2002. Scoring pairwise genomic sequence alignments. Pac Symp Biocomput 2002: 115-126.
11. The Chimpanzee Sequencing and Analysis Consortium. 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437: 69-87.
12. Davison AC, Hinkley DV. 1997. Bootstrap methods and their application. Cambridge University Press, Cambridge, UK.
13. Dennehey BK, Gutches DG, McConkey EH, Krauter KS. 2004. Inversion, duplication, and changes in gene context are associated with human chromosome 18 evolution. Genomics 83: 493-501.
14. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
15. Fan Y, Linardopoulou E, Friedman C, Williams E, Trask BJ. 2002. Genomic structure and evolution of the ancestral chromosome fusion site in 2q13-2q14.1 and paralogous regions on other human chromosomes. Genome Res 12: 1651-1662.
16. Farré M, Micheletti D, Ruiz-Herrera A. 2013. Recombination rates and genomic shuffling in human and chimpanzee-a new twist in the chromosomal speciation theory. Mol Biol Evol 30: 853-864.
17. Fernandez T, Morgan T, Davis N, Klin A, Morris A, Farhi A, Lifton RP, State MW. 2004. Disruption of contactin 4 (CNTN4) results in developmental delay and other features of 3p deletion syndrome. Am J Hum Genet 74: 1286-1293.
18. Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9: 397-405.
19. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, et al. 2014. Ensembl 2014. Nucleic Acids Res 42: D749-D755.
20. Giannuzzi G, Siswara P, Malig M, Marques-Bonet T, Mullikin JC, Ventura M, Eichler EE. 2013. Evolutionary dynamism of the primate LRRC37 gene family. Genome Res 23: 46-59.
21. Girirajan S, Rosenfeld JA, Cooper GM, Antonacci F, Siswara P, Itsara A, Vives L, Walsh T, McCarthy SE, Baker C, et al. 2010. A recurrent 16p12.1 microdeletion supports a two-hit model for severe developmental delay. Nat Genet 42: 203-209.
22. Glessner JT, Wang K, Cai G, Korvatska O, Kim CE, Wood S, Zhang H, Estes A, Brune CW, Bradfield JP, et al. 2009. Autism genome-wide copy number variation reveals ubiquitin and neuronal genes. Nature 459: 569-573.
23. Goidts V, Szamalek JM, de Jong PJ, Cooper DN, Chuzhanova N, Hameister H, Kehrer-Sawatzki H. 2005. Independent intrachromosomal recombination events underlie the pericentric inversions of chimpanzee and gorilla chromosomes homologous to human chromosome 16. Genome Res 15: 1232-1242.
24. Grimwood J, Gordon LA, Olsen A, Terry A, Schmutz J, Lamerdin J, Hellsten U, Goodstein D, Couronne O, Tran-Gyamfi M, et al. 2004. The DNA sequence and biology of human chromosome 19. Nature 428: 529-535.
25. Hastings PJ, Lupski JR, Rosenberg SM, Ira G. 2009. Mechanisms of change in gene copy number. Nat Rev Genet 10: 551-564.
26. Henrichsen CN, Chaignat E, Reymond A. 2009a. Copy number variants, diseases and gene expression. Hum Mol Genet 18: R1-R8.
27. Henrichsen CN, Vinckenbosch N, Zollner S, Chaignat E, Pradervand S, Schutz F, RuediM, Kaessmann H, Reymond A. 2009b. Segmental copy number variation shapes tissue transcriptomes. Nat Genet 41: 424-429.
28. Horvath JE, Schwartz S, Eichler EE. 2000. The mosaic structure of human pericentromeric DNA: a strategy for characterizing complex regions of the human genome. Genome Res 10: 839-852.
29. Horvath JE, Bailey JA, Locke DP, Eichler EE. 2001. Lessons from the human genome: transitions between euchromatin and heterochromatin. Hum Mol Genet 10: 2215-2223.
30. Horvath JE, Gulden CL, Bailey JA, Yohn C, McPherson JD, Prescott A, Roe BA, de Jong PJ, VenturaM, Misceo D, et al. 2003. Using a pericentromeric interspersed repeat to recapitulate the phylogeny and expansion of humancentromeric segmental duplications.Mol Biol Evol 20: 1463-1479.
31. IJdo JW, Baldini A, Ward DC, Reeders ST, Wells RA. 1991. Origin of human chromosome 2: an ancestral telomere-telomere fusion. Proc Natl Acad Sci 88: 9051-9055.
32. The International HapMap Consortium. 2005. A haplotype map of the human genome. Nature 437: 1299-1320.
33. Jacquemont S, Reymond A, Zufferey F, Harewood L, Walters RG, Kutalik Z, Martinet D, Shen Y, Valsesia A, Beckmann ND, et al. 2011. Mirror extreme BMI phenotypes associated with gene dosage at the chromosome 16p11.2 locus. Nature 478: 97-102.
34. Johnson ME, Viggiano L, Bailey JA, Abdul-Rauf M, Goodwin G, Rocchi M, Eichler EE. 2001. Positive selection of a gene family during the emergence of humans and African apes. Nature 413: 514-519.
35. Kehrer-Sawatzki H, Cooper DN. 2007. Understanding the recent evolution of the human genome: insights from human-chimpanzee genome comparisons. Hum Mutat 28: 99-130.
36. Kehrer-Sawatzki H, Schreiner B, Tanzer S, Platzer M, Muller S, Hameister H. 2002. Molecular characterization of the pericentric inversion that causes differences between chimpanzee chromosome 19 and human chromosome 17. Am J Hum Genet 71: 375-388.
37. Kehrer-Sawatzki H, Sandig C, Chuzhanova N, Goidts V, Szamalek JM, Tanzer S, Muller S, Platzer M, Cooper DN, Hameister H. 2005a. Breakpoint analysis of the pericentric inversion distinguishing human chromosome 4 from the homologous chromosome in the chimpanzee (Pan troglodytes). Hum Mutat 25: 45-55.
38. Kehrer-Sawatzki H, Sandig CA, Goidts V, Hameister H. 2005b. Breakpoint analysis of the pericentric inversion between chimpanzee chromosome 10 and the homologous chromosome 12 in humans. Cytogenet Genome Res 108: 91-97.
39. Kehrer-Sawatzki H, Szamalek JM, Tanzer S, Platzer M, Hameister H. 2005c. Molecular characterization of the pericentric inversion of chimpanzee chromosome 11 homologous to human chromosome 9. Genomics 85: 542-550.
40. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12: 996-1006.
41. Kent WJ, Baertsch R, Hinrichs A, Miller W, Haussler D. 2003. Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc Natl Acad Sci 100: 11484-11489.
42. Kilpinen H, Waszak SM, Gschwind AR, Raghav SK, Witwicki RM, Orioli A, Migliavacca E, Wiederkehr M, Gutierrez-Arcelus M, Panousis N, et al. 2013. Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342: 744-747.
43. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36.
44. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
45. Law CW, Chen Y, Shi W, Smyth GK. 2014. Voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol 15: R29.
46. Linardopoulou EV, Williams EM, Fan Y, Friedman C, Young JM, Trask BJ. 2005. Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437: 94-100.
47. Locke DP, Archidiacono N, Misceo D, Cardone MF, Deschamps S, Roe B, Rocchi M, Eichler EE. 2003. Refinement of a chimpanzee pericentric inversion breakpoint to a segmental duplication cluster. Genome Biol 4: R50.
48. Locke DP, Jiang Z, Pertz LM, Misceo D, Archidiacono N, Eichler EE. 2005. Molecular evolution of the human chromosome 15 pericentromeric region. Cytogenet Genome Res 108: 73-82.
49. Lu J, Li WH, Wu CI. 2003. Comment on ''Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes''. Science 302: 988.
50. Marques-Bonet T, Caceres M, Bertranpetit J, Preuss TM, Thomas JW, Navarro A. 2004. Chromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees. Trends Genet 20: 524-529.
51. Marques-Bonet T, Sanchez-Ruiz J, Armengol L, Khaja R, Bertranpetit J, Lopez-Bigas N, RocchiM, Gazave E, Navarro A. 2007. On the association between chromosomal rearrangements and genic evolution in humans and chimpanzees. Genome Biol 8: R230.
52. Marshall CR, Noor A, Vincent JB, Lionel AC, Feuk L, Skaug J, Shago M, Moessner R, Pinto D, Ren Y, et al. 2008. Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet 82: 477-488.
53. Marzella R, Viggiano L, Miolla V, Storlazzi CT, Ricco A, Gentile E, Roberto R, Surace C, Fratello A, Mancini M, et al. 2000. Molecular cytogenetic resources for chromosome 4 and comparative analysis of phylogenetic chromosome IV in great apes. Genomics 63: 307-313.
54. McConkey EH. 1997. The origin of human chromosome 18 from a human/ ape ancestor. Cytogenet Cell Genet 76: 189-191.
55. McVean GA, Myers SR, Hunt S, Deloukas P, Bentley DR, Donnelly P. 2004. The fine-scale structure of recombination rate variation in the human genome. Science 304: 581-584.
56. Mefford HC, Trask BJ. 2002. The complex structure and dynamic evolution of human subtelomeres. Nat Rev Genet 3: 91-102.
57. Merla G, Howald C, Henrichsen CN, Lyle R, Wyss C, Zabot MT, Antonarakis SE, Reymond A. 2006. Submicroscopic deletion in patients with Williams-Beuren syndrome influences expression levels of the nonhemizygous flanking genes. Am J Hum Genet 79: 332-341.
58. Munoz A, Sankoff D. 2012. Detection of gene expression changes at chromosomal rearrangement breakpoints in evolution. BMC Bioinformatics (Suppl 3) 13: S6.
59. Navarro A, Barton NH. 2003. Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes. Science 300: 321-324.
60. Newman TL, Tuzun E, Morrison VA, Hayden KE, Ventura M, McGrath SD, Rocchi M, Eichler EE. 2005. A genome-wide survey of structural variation between human and chimpanzee. Genome Res 15: 1344-1356.
61. Nickerson E, Nelson DL. 1998. Molecular definition of pericentric inversion breakpoints occurring during the evolution of humans and chimpanzees. Genomics 50: 368-372.
62. Pickrell JK, Gaffney DJ, Gilad Y, Pritchard JK. 2011. False positive peaks in ChIP-seq and other sequencing-based functional assays caused by unannotated high copy number regions. Bioinformatics 27: 2144-2146.
63. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
64. R Development Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
65. Reymond A, Henrichsen CN, Harewood L, Merla G. 2007. Side effects of genome structural changes. Curr Opin Genet Dev 17: 381-386.
66. Rhesus Macaque Genome Sequencing and Analysis Consortium. 2007. Evolutionary and biomedical insights from the rhesus macaque genome. Science 316: 222-234.
67. Ricard G, Molina J, Chrast J, GuW, Gheldof N, Pradervand S, Schutz F, Young JI, Lupski JR, Reymond A, et al. 2010. Phenotypic consequences of copy number variation: insights from Smith-Magenis and Potocki-Lupski syndrome mouse models. PLoS Biol 8: e1000543.
68. Roohi J, Montagna C, Tegay DH, Palmer LE, DeVincent C, Pomeroy JC, Christian SL, Nowak N, Hatchwell E. 2009. Disruption of contactin 4 in three subjects with autism spectrum disorder. J Med Genet 46: 176-182.
69. Sakurai K, Migita O, Toru M, Arinami T. 2002. An association between a missense polymorphism in the close homologue of L1 (CHL1, CALL) gene and schizophrenia. Mol Psychiatry 7: 412-415.
70. Salyakina D, Cukier HN, Lee JM, Sacharow S, Nations LD, Ma D, Jaworski JM, Konidari I, Whitehead PL, Wright HH, et al. 2011. Copy number variants in extended autism spectrum disorder families reveal candidates potentially involved in autism risk. PLoS ONE 6: e26049.
71. Schwartz S, Kent WJ, Smit A, Zhang Z, Baertsch R, Hardison RC, Haussler D, Miller W. 2003. Human-mouse alignments with BLASTZ. Genome Res 13: 103-107.
72. Sharp AJ, Locke DP, McGrath SD, Cheng Z, Bailey JA, Vallente RU, Pertz LM, Clark RA, Schwartz S, Segraves R, et al. 2005. Segmental duplications and copy-number variation in the human genome. Am J Hum Genet 77: 78-88.
73. She X, Horvath JE, Jiang Z, Liu G, Furey TS, Christ L, Clark R, Graves T, Gulden CL, Alkan C, et al. 2004. The structure and evolution of centromeric transition regions within the human genome. Nature 430: 857-864.
74. Shimada MK, Kim CG, Kitano T, Ferrell RE, Kohara Y, Saitou N. 2005. Nucleotide sequence comparison of a chromosome rearrangement on human chromosome 12 and the corresponding ape chromosomes. Cytogenet Genome Res 108: 83-90.
75. Shulha HP, Crisci JL, Reshetov D, Tushir JS, Cheung I, Bharadwaj R, Chou HJ, Houston IB, Peter CJ, Mitchell AC, et al. 2012. Human-specific histone methylation signatures at transcription start sites in prefrontal neurons. PLoS Biol 10: e1001427.
76. Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV. 2011. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472: 375-378.
77. Sudmant PH, Huddleston J, Catacchio CR, Malig M, Hillier LW, Baker C, Mohajeri K, Kondova I, Bontrop RE, Persengiev S, et al. 2013. Evolution and diversity of copy number variation in the great ape lineage. Genome Res 23: 1373-1382.
78. Szamalek JM, Goidts V, Chuzhanova N, Hameister H, Cooper DN, Kehrer- Sawatzki H. 2005. Molecular characterisation of the pericentric inversion that distinguishes human chromosome 5 from the homologous chimpanzee chromosome. Hum Genet 117: 168-176.
79. Szamalek JM, Goidts V, Cooper DN, Hameister H, Kehrer-Sawatzki H. 2006. Characterization of the human lineage-specific pericentric inversion that distinguishes human chromosome 1 from the homologous chromosomes of the great apes. Hum Genet 120: 126-138.
80. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
81. Vallender EJ, Lahn BT. 2004. Effects of chromosomal rearrangements on human-chimpanzee molecular evolution. Genomics 84: 757-761.
82. Walters RG, Jacquemont S, Valsesia A, de Smith AJ, Martinet D, Andersson J, Falchi M, Chen F, Andrieux J, Lobbens S, et al. 2010. A new highly penetrant form of obesity due to deletions on chromosome 16p11.2. Nature 463: 671-675.
83. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, et al. 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903.
84. Wang T, Wu H, Li Y, Szulwach KE, Lin L, Li X, Chen IP, Goldlust IS, Chamberlain SJ, Dodd A, et al. 2013. Subtelomeric hotspots of aberrant 5-hydroxymethylcytosine-mediated epigenetic modifications during reprogramming to pluripotency. Nat Cell Biol 15: 700-711.
85. Weise A, Starke H, Mrasek K, Claussen U, Liehr T. 2005. New insights into the evolution of chromosome 1. Cytogenet Genome Res 108: 217-222.
86. Winckler W, Myers SR, Richter DJ, Onofrio RC, McDonald GJ, Bontrop RE, McVean GA, Gabriel SB, Reich D, Donnelly P, et al. 2005. Comparison of fine-scale recombination rates in humans and chimpanzees. Science 308: 107-111.
87. Yunis JJ, Prakash O. 1982. The origin of man: a chromosomal pictorial legacy. Science 215: 1525-1530.
88. Yunis JJ, Sawyer JR, Dunham K. 1980. The striking resemblance of highresolution G-banded chromosomes of man and chimpanzee. Science 208: 1145-1148.
89. Zhang J, Wang X, Podlaha O. 2004. Testing the chromosomal speciation hypothesis for humans and chimpanzees. Genome Res 14: 845-851.
90. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, LiW, et al. 2008. Model-based analysis of ChIPSeq (MACS). Genome Biol 9: R137.