Chromatin organization in sperm may be the major functional consequence of base composition variation in the human genome

PLoS Genetics

Volumn 7, Issue 4, 2011, Pages

  Vavouri, Tanya ^a,c   Lehner, Ben ^a,b  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c Institute of Predictive and Personalized Medicine of Cancer IMPPC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL ADHESION; CHROMATIN STRUCTURE; DNA BASE COMPOSITION; DNA METHYLATION; EMBRYO; EMBRYO DEVELOPMENT; GC RICH SEQUENCE; GENETIC REGULATION; GENETIC VARIABILITY; HOUSEKEEPING GENE; HUMAN; HUMAN CELL; HUMAN GENOME; MALE; MOLECULAR EVOLUTION; NUCLEOSOME; SPERM; TRANSCRIPTION INITIATION SITE; BIOLOGICAL MODEL; CHROMATIN; GENETICS; METABOLISM; SPERMATOZOON;

MAMMALIA;

TRANSCRIPTION FACTOR;

BASE COMPOSITION; CHROMATIN; DNA METHYLATION; GENETIC VARIATION; GENOME, HUMAN; HUMANS; MALE; MODELS, BIOLOGICAL; NUCLEOSOMES; SPERMATOZOA; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE;

EID: 79955610452     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002036     Document Type: Article

References (68)

1. Puwaravutipanich T, Panyim S, (1975) The nuclear basic proteins of human testes and ejaculated spermatozoa. Exp Cell Res 90: 153-158.
2. Ward WS, Coffey DS, (1991) DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 44: 569-574.
3. Arpanahi A, Brinkworth M, Iles D, Krawetz SA, Paradowska A, et al. (2009) Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res 19: 1338-1349.
4. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, et al. (2010) Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 17: 679-687.
5. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, et al. (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460: 473-478.
6. Pogany GC, Corzett M, Weston S, Balhorn R, (1981) DNA and protein content of mouse sperm. Implications regarding sperm chromatin structure. Exp Cell Res 136: 127-136.
7. de Yebra L, Ballesca JL, Vanrell JA, Bassas L, Oliva R, (1993) Complete selective absence of protamine P2 in humans. J Biol Chem 268: 10553-10557.
8. Brewer L, Corzett M, Lau EY, Balhorn R, (2003) Dynamics of protamine 1 binding to single DNA molecules. J Biol Chem 278: 42403-42408.
9. Ward WS, (2009) Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod 16: 30-36.
10. Cho C, Willis WD, Goulding EH, Jung-Ha H, Choi YC, et al. (2001) Haploinsufficiency of protamine-1 or-2 causes infertility in mice. Nat Genet 28: 82-86.
11. Cho C, Jung-Ha H, Willis WD, Goulding EH, Stein P, et al. (2003) Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice. Biol Reprod 69: 211-217.
12. Haueter S, Kawasumi M, Asner I, Brykczynska U, Cinelli P, et al. (2010) Genetic vasectomy-overexpression of Prm1-EGFP fusion protein in elongating spermatids causes dominant male sterility in mice. Genesis 48: 151-160.
13. Gardiner-Garden M, Ballesteros M, Gordon M, Tam PP, (1998) Histone- and protamine-DNA association: conservation of different patterns within the beta-globin domain in human sperm. Mol Cell Biol 18: 3350-3356.
14. Wykes SM, Krawetz SA, (2003) The structural organization of sperm chromatin. J Biol Chem 278: 29471-29477.
15. Gatewood JM, Cook GR, Balhorn R, Bradbury EM, Schmid CW, (1987) Sequence-specific packaging of DNA in human sperm chromatin. Science 236: 962-964.
16. van der Heijden GW, Ramos L, Baart EB, van den Berg IM, Derijck AA, et al. (2008) Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev Biol 8: 34.
17. van der Heijden GW, Derijck AA, Ramos L, Giele M, van der Vlag J, et al. (2006) Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev Biol 298: 458-469.
18. Puschendorf M, Terranova R, Boutsma E, Mao X, Isono K, et al. (2008) PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat Genet 40: 411-420.
19. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143: 1084-1096.
20. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, et al. (2010) Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467: 963-966.
21. Youngson NA, Whitelaw E, (2008) Transgenerational epigenetic effects. Annu Rev Genomics Hum Genet 9: 233-257.
22. Kornberg RD, Stryer L, (1988) Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res 16: 6677-6690.
23. Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, et al. (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18: 1073-1083.
24. Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N, (2009) High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 20: 90-100.
25. Zhang Y, Moqtaderi Z, Rattner BP, Euskirchen G, Snyder M, et al. (2009) Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol 16: 847-852.
26. Drew HR, Travers AA, (1985) DNA bending and its relation to nucleosome positioning. J Mol Biol 186: 773-790.
27. Lowary PT, Widom J, (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276: 19-42.
28. Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, et al. (2006) A genomic code for nucleosome positioning. Nature 442: 772-778.
29. Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, et al. (2008) Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol 4: e1000216 doi:10.1371/journal.pcbi.1000216.
30. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362-366.
31. Tillo D, Hughes TR, (2009) G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 10: 442.
32. Chung HR, Vingron M, (2009) Sequence-dependent nucleosome positioning. J Mol Biol 386: 1411-1422.
33. Vinogradov AE, (2005) Noncoding DNA, isochores and gene expression: nucleosome formation potential. Nucleic Acids Res 33: 559-563.
34. Tillo D, Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, et al. (2010) High nucleosome occupancy is encoded at human regulatory sequences. PLoS ONE 5: e9129 doi:10.1371/journal.pone.0009129.
35. Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C, et al. (2009) A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 138: 114-128.
36. Gardiner-Garden M, Frommer M, (1987) CpG islands in vertebrate genomes. J Mol Biol 196: 261-282.
37. Schug J, Schuller WP, Kappen C, Salbaum JM, Bucan M, et al. (2005) Promoter features related to tissue specificity as measured by Shannon entropy. Genome Biol 6: R33.
38. Tanay A, O'Donnell AH, Damelin M, Bestor TH, (2007) Hyperconserved CpG domains underlie Polycomb-binding sites. Proc Natl Acad Sci U S A 104: 5521-5526.
39. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, et al. (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30: 755-766.
40. Bird A, Taggart M, Frommer M, Miller OJ, Macleod D, (1985) A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell 40: 91-99.
41. Straussman R, Nejman D, Roberts D, Steinfeld I, Blum B, et al. (2009) Developmental programming of CpG island methylation profiles in the human genome. Nat Struct Mol Biol 16: 564-571.
42. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, et al. (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39: 457-466.
43. Frank D, Keshet I, Shani M, Levine A, Razin A, et al. (1991) Demethylation of CpG islands in embryonic cells. Nature 351: 239-241.
44. Chodavarapu RK, Feng S, Bernatavichute YV, Chen PY, Stroud H, et al. (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466: 388-392.
45. Kafri T, Ariel M, Brandeis M, Shemer R, Urven L, et al. (1992) Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev 6: 705-714.
46. Brandeis M, Frank D, Keshet I, Siegfried Z, Mendelsohn M, et al. (1994) Sp1 elements protect a CpG island from de novo methylation. Nature 371: 435-438.
47. Macleod D, Charlton J, Mullins J, Bird AP, (1994) Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev 8: 2282-2292.
48. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448: 714-717.
49. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
50. Dohm JC, Lottaz C, Borodina T, Himmelbauer H, (2008) Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Res 36: e105.
51. Schones DE, Cui K, Cuddapah S, Roh TY, Barski A, et al. (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell 132: 887-898.
52. Monesi V, (1965) Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse. Chromosoma 17: 11-21.
53. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.
54. Lidor Nili E, Field Y, Lubling Y, Widom J, Oren M, et al. (2010) p53 binds preferentially to genomic regions with high DNA-encoded nucleosome occupancy. Genome Res 20: 1361-1368.
55. Hajkova P, (2010) Epigenetic reprogramming-taking a lesson from the embryo. Curr Opin Cell Biol 22: 342-350.
56. Thomson JP, Skene PJ, Selfridge J, Clouaire T, Guy J, et al. (2010) CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464: 1082-1086.
57. Hajkova P, Ancelin K, Waldmann T, Lacoste N, Lange UC, et al. (2008) Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452: 877-881.
58. Tirosh I, Barkai N, (2008) Two strategies for gene regulation by promoter nucleosomes. Genome Res 18: 1084-1091.
59. Nix DA, Courdy SJ, Boucher KM, (2008) Empirical methods for controlling false positives and estimating confidence in ChIP-Seq peaks. BMC Bioinformatics 9: 523.
60. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, et al. (2009) NCBI GEO: archive for high-throughput functional genomic data. Nucleic Acids Res 37: D885-890.
61. Rhead B, Karolchik D, Kuhn RM, Hinrichs AS, Zweig AS, et al. (2010) The UCSC Genome Browser database: update 2010. Nucleic Acids Res 38: D613-619.
62. Song JS, Johnson WE, Zhu X, Zhang X, Li W, et al. (2007) Model-based analysis of two-color arrays (MA2C). Genome Biol 8: R178.
63. Hubbard TJ, Aken BL, Ayling S, Ballester B, Beal K, et al. (2009) Ensembl 2009. Nucleic Acids Res 37: D690-697.
64. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
65. Ramskold D, Wang ET, Burge CB, Sandberg R, (2009) An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput Biol 5: e1000598 doi:10.1371/journal.pcbi.1000598.
66. Platts AE, Dix DJ, Chemes HE, Thompson KE, Goodrich R, et al. (2007) Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum Mol Genet 16: 763-773.
67. Sing T, Sander O, Beerenwinkel N, Lengauer T, (2005) ROCR: visualizing classifier performance in R. Bioinformatics 21: 3940-3941.
68. Sabo PJ, Kuehn MS, Thurman R, Johnson BE, Johnson EM, et al. (2006) Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat Methods 3: 511-518.