Chromatin Organization in Sperm May Be the Major Functional Consequence of Base Composition Variation in the Human Genome

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Chromatin in sperm is different from that in other cells, with most of the genome packaged by protamines not nucleosomes. Nucleosomes are, however, retained at some genomic sites, where they have the potential to transmit paternal epigenetic information. It is not understood how this retention is specified. Here we show that base composition is the major determinant of nucleosome retention in human sperm, predicting retention very well in both genic and non-genic regions of the genome. The retention of nucleosomes at GC-rich sequences with high intrinsic nucleosome affinity accounts for the previously reported retention at transcription start sites and at genes that regulate development. It also means that nucleosomes are retained at the start sites of most housekeeping genes. We also report a striking link between the retention of nucleosomes in sperm and the establishment of DNA methylation-free regions in the early embryo. Taken together, this suggests that paternal nucleosome transmission may facilitate robust gene regulation in the early embryo. We propose that chromatin organization in the male germline, rather than in somatic cells, is the major functional consequence of fine-scale base composition variation in the human genome. The selective pressure driving base composition evolution in mammals could, therefore, be the need to transmit paternal epigenetic information to the zygote.

Vyšlo v časopise: Chromatin Organization in Sperm May Be the Major Functional Consequence of Base Composition Variation in the Human Genome. PLoS Genet 7(4): e32767. doi:10.1371/journal.pgen.1002036
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002036

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Zdroje

1. PuwaravutipanichTPanyimS 1975 The nuclear basic proteins of human testes and ejaculated spermatozoa. Exp Cell Res 90 153 158

2. WardWSCoffeyDS 1991 DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 44 569 574

3. ArpanahiABrinkworthMIlesDKrawetzSAParadowskaA 2009 Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res 19 1338 1349

4. BrykczynskaUHisanoMErkekSRamosLOakeleyEJ 2010 Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 17 679 687

5. HammoudSSNixDAZhangHPurwarJCarrellDT 2009 Distinctive chromatin in human sperm packages genes for embryo development. Nature 460 473 478

6. PoganyGCCorzettMWestonSBalhornR 1981 DNA and protein content of mouse sperm. Implications regarding sperm chromatin structure. Exp Cell Res 136 127 136

7. de YebraLBallescaJLVanrellJABassasLOlivaR 1993 Complete selective absence of protamine P2 in humans. J Biol Chem 268 10553 10557

8. BrewerLCorzettMLauEYBalhornR 2003 Dynamics of protamine 1 binding to single DNA molecules. J Biol Chem 278 42403 42408

9. WardWS 2009 Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod 16 30 36

10. ChoCWillisWDGouldingEHJung-HaHChoiYC 2001 Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet 28 82 86

11. ChoCJung-HaHWillisWDGouldingEHSteinP 2003 Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice. Biol Reprod 69 211 217

12. HaueterSKawasumiMAsnerIBrykczynskaUCinelliP 2010 Genetic vasectomy-overexpression of Prm1-EGFP fusion protein in elongating spermatids causes dominant male sterility in mice. Genesis 48 151 160

13. Gardiner-GardenMBallesterosMGordonMTamPP 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. WykesSMKrawetzSA 2003 The structural organization of sperm chromatin. J Biol Chem 278 29471 29477

15. GatewoodJMCookGRBalhornRBradburyEMSchmidCW 1987 Sequence-specific packaging of DNA in human sperm chromatin. Science 236 962 964

16. van der HeijdenGWRamosLBaartEBvan den BergIMDerijckAA 2008 Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev Biol 8 34

17. van der HeijdenGWDerijckAARamosLGieleMvan der VlagJ 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. PuschendorfMTerranovaRBoutsmaEMaoXIsonoK 2008 PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat Genet 40 411 420

19. CaroneBRFauquierLHabibNSheaJMHartCE Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143 1084 1096

20. NgSFLinRCLaybuttDRBarresROwensJA 2010 Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467 963 966

21. YoungsonNAWhitelawE 2008 Transgenerational epigenetic effects. Annu Rev Genomics Hum Genet 9 233 257

22. KornbergRDStryerL 1988 Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res 16 6677 6690

23. MavrichTNIoshikhesIPVentersBJJiangCTomshoLP 2008 A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18 1073 1083

24. WeinerAHughesAYassourMRandoOJFriedmanN 2009 High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 20 90 100

25. ZhangYMoqtaderiZRattnerBPEuskirchenGSnyderM 2009 Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol 16 847 852

26. DrewHRTraversAA 1985 DNA bending and its relation to nucleosome positioning. J Mol Biol 186 773 790

27. LowaryPTWidomJ 1998 New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276 19 42

28. SegalEFondufe-MittendorfYChenLThastromAFieldY 2006 A genomic code for nucleosome positioning. Nature 442 772 778

29. FieldYKaplanNFondufe-MittendorfYMooreIKSharonE 2008 Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol 4 e1000216 doi:10.1371/journal.pcbi.1000216

30. KaplanNMooreIKFondufe-MittendorfYGossettAJTilloD 2009 The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458 362 366

31. TilloDHughesTR 2009 G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 10 442

32. ChungHRVingronM 2009 Sequence-dependent nucleosome positioning. J Mol Biol 386 1411 1422

33. VinogradovAE 2005 Noncoding DNA, isochores and gene expression: nucleosome formation potential. Nucleic Acids Res 33 559 563

34. TilloDKaplanNMooreIKFondufe-MittendorfYGossettAJ 2010 High nucleosome occupancy is encoded at human regulatory sequences. PLoS ONE 5 e9129 doi:10.1371/journal.pone.0009129

35. Ramirez-CarrozziVRBraasDBhattDMChengCSHongC 2009 A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 138 114 128

36. Gardiner-GardenMFrommerM 1987 CpG islands in vertebrate genomes. J Mol Biol 196 261 282

37. SchugJSchullerWPKappenCSalbaumJMBucanM 2005 Promoter features related to tissue specificity as measured by Shannon entropy. Genome Biol 6 R33

38. TanayAO'DonnellAHDamelinMBestorTH 2007 Hyperconserved CpG domains underlie Polycomb-binding sites. Proc Natl Acad Sci U S A 104 5521 5526

39. MohnFWeberMRebhanMRoloffTCRichterJ 2008 Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30 755 766

40. BirdATaggartMFrommerMMillerOJMacleodD 1985 A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell 40 91 99

41. StraussmanRNejmanDRobertsDSteinfeldIBlumB 2009 Developmental programming of CpG island methylation profiles in the human genome. Nat Struct Mol Biol 16 564 571

42. WeberMHellmannIStadlerMBRamosLPaaboS 2007 Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39 457 466

43. FrankDKeshetIShaniMLevineARazinA 1991 Demethylation of CpG islands in embryonic cells. Nature 351 239 241

44. ChodavarapuRKFengSBernatavichuteYVChenPYStroudH 2010 Relationship between nucleosome positioning and DNA methylation. Nature 466 388 392

45. KafriTArielMBrandeisMShemerRUrvenL 1992 Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev 6 705 714

46. BrandeisMFrankDKeshetISiegfriedZMendelsohnM 1994 Sp1 elements protect a CpG island from de novo methylation. Nature 371 435 438

47. MacleodDCharltonJMullinsJBirdAP 1994 Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev 8 2282 2292

48. OoiSKQiuCBernsteinELiKJiaD 2007 DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448 714 717

49. LanderESLintonLMBirrenBNusbaumCZodyMC 2001 Initial sequencing and analysis of the human genome. Nature 409 860 921

50. DohmJCLottazCBorodinaTHimmelbauerH 2008 Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Res 36 e105

51. SchonesDECuiKCuddapahSRohTYBarskiA 2008 Dynamic regulation of nucleosome positioning in the human genome. Cell 132 887 898

52. MonesiV 1965 Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse. Chromosoma 17 11 21

53. WangETSandbergRLuoSKhrebtukovaIZhangL 2008 Alternative isoform regulation in human tissue transcriptomes. Nature 456 470 476

54. Lidor NiliEFieldYLublingYWidomJOrenM 2010 p53 binds preferentially to genomic regions with high DNA-encoded nucleosome occupancy. Genome Res 20 1361 1368

55. HajkovaP 2010 Epigenetic reprogramming–taking a lesson from the embryo. Curr Opin Cell Biol 22 342 350

56. ThomsonJPSkenePJSelfridgeJClouaireTGuyJ 2010 CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464 1082 1086

57. HajkovaPAncelinKWaldmannTLacosteNLangeUC 2008 Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452 877 881

58. TiroshIBarkaiN 2008 Two strategies for gene regulation by promoter nucleosomes. Genome Res 18 1084 1091

59. NixDACourdySJBoucherKM 2008 Empirical methods for controlling false positives and estimating confidence in ChIP-Seq peaks. BMC Bioinformatics 9 523

60. BarrettTTroupDBWilhiteSELedouxPRudnevD 2009 NCBI GEO: archive for high-throughput functional genomic data. Nucleic Acids Res 37 D885 890

61. RheadBKarolchikDKuhnRMHinrichsASZweigAS 2010 The UCSC Genome Browser database: update 2010. Nucleic Acids Res 38 D613 619

62. SongJSJohnsonWEZhuXZhangXLiW 2007 Model-based analysis of two-color arrays (MA2C). Genome Biol 8 R178

63. HubbardTJAkenBLAylingSBallesterBBealK 2009 Ensembl 2009. Nucleic Acids Res 37 D690 697

64. MortazaviAWilliamsBAMcCueKSchaefferLWoldB 2008 Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5 621 628

65. RamskoldDWangETBurgeCBSandbergR 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. PlattsAEDixDJChemesHEThompsonKEGoodrichR 2007 Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum Mol Genet 16 763 773

67. SingTSanderOBeerenwinkelNLengauerT 2005 ROCR: visualizing classifier performance in R. Bioinformatics 21 3940 3941

68. SaboPJKuehnMSThurmanRJohnsonBEJohnsonEM 2006 Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat Methods 3 511 518