title: Dissecting the roles of the histone chaperones reveals the evolutionary conserved mechanism of transcription-coupled deposition of H3.3.
abstract: The mammalian genome encodes multiple variants of histone H3 including H3.1/H3.2 and H3.3. In contrast to H3.1/H3.2, H3.3 is enriched in the actively transcribed euchromatin and the telomeric heterochromatins. However, the mechanism for H3.3 to incorporate into the different domains of chromatin is not known. Here, taking the advantage of well-defined transcription analysis system of yeast, we attempted to understand the molecular mechanism of selective deposition of human H3.3 into actively transcribed genes. We show that there are systemic H3 substrate-selection mechanisms operating even in yeasts, which encode a single type of H3. Yeast HIR complex mediated H3-specific recognition specificity for deposition of H3.3 in the transcribed genes. A critical component of this process was the H3 A-IG code composed of amino acids 87, 89 and 90. The preference toward H3.3 was completely lost when HIR subunits were absent and partially suppressed by human HIRA. Asf1 allows the influx of H3, regardless of H3 type. We propose that H3.3 is introduced into the active euchromatin by targeting the recycling pathway that is mediated by HIRA (or HIR), and this H3-selection mechanism is highly conserved through the evolution. These results also uncover an unexpected role of RI chaperones in evolution of variant H3s.
authors.affiliation: School of Pharmacy, Sungkyunkwan University, Suwon, Gyeonggi-do 440-746, Republic of Korea.
authors.forename: Yunkyoung
authors.initials: Y
authors.lastname: Song
authors.forename: Ja-Hwan
authors.initials: JH
authors.lastname: Seol
authors.forename: Jae-Hyun
authors.initials: JH
authors.lastname: Yang
authors.forename: Hye-Jin
authors.initials: HJ
authors.lastname: Kim
authors.forename: Jeung-Whan
authors.initials: JW
authors.lastname: Han
authors.forename: Hong-Duk
authors.initials: HD
authors.lastname: Youn
authors.forename: Eun-Jung
authors.initials: EJ
authors.lastname: Cho
mesh_terms: D000595:Amino Acid Sequence; D005075:Biological Evolution; D018797:Cell Cycle Proteins / Q000235:genetics; D017124:Conserved Sequence; D005656:Fungal Proteins / Q000737:chemistry / Q000378:metabolism / Q000502:physiology; D056488:Histone Chaperones / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D006657:Histones / Q000737:chemistry / Q000378:metabolism*; D006801:Humans; D009154:Mutation; D017434:Protein Structure, Tertiary; D014157:Transcription Factors / Q000235:genetics; D014158:Transcription, Genetic; D015003:Yeasts / Q000235:genetics / Q000378:metabolism
chemical_list: D018797:Cell Cycle Proteins; D005656:Fungal Proteins; C086057:HIRA protein, human; D056488:Histone Chaperones; D006657:Histones; D014157:Transcription Factors
references.citation: Nat Struct Mol Biol. 2006 Oct;13(10):921-9
references.pmid: 16980972
references.citation: BMB Rep. 2009 Apr 30;42(4):227-31
references.pmid: 19403047
references.citation: Mol Cell Biol. 2009 Feb;29(3):758-70
references.pmid: 19029251
references.citation: Mol Biosyst. 2009 Mar;5(3):269-75
references.pmid: 19225618
references.citation: Curr Biol. 2005 Nov 22;15(22):2044-9
references.pmid: 16303565
references.citation: Nat Struct Mol Biol. 2012 Sep;19(9):884-92
references.pmid: 22922743
references.citation: J Virol. 2009 Feb;83(3):1416-21
references.pmid: 19004946
references.citation: Biochim Biophys Acta. 2013 Mar-Apr;1819(3-4):230-237
references.pmid: 24459725
references.citation: Cell. 2006 Nov 3;127(3):495-508
references.pmid: 17081973
references.citation: J Biol Chem. 2006 Mar 3;281(9):5539-45
references.pmid: 16407267
references.citation: EMBO J. 2007 Oct 31;26(21):4467-74
references.pmid: 17914459
references.citation: Cell. 2004 Jan 9;116(1):51-61
references.pmid: 14718166
references.citation: Proc Natl Acad Sci U S A. 2005 Apr 26;102(17):5975-80
references.pmid: 15840725
references.citation: Nature. 2012 Sep 20;489(7416):452-5
references.pmid: 22914091
references.citation: Exp Mol Med. 2007 Jun 30;39(3):247-54
references.pmid: 17603278
references.citation: Yeast. 1998 Jul;14(10):953-61
references.pmid: 9717241
references.citation: Curr Opin Genet Dev. 2010 Apr;20(2):110-7
references.pmid: 20153629
references.citation: Genetics. 2002 Dec;162(4):1557-71
references.pmid: 12524332
references.citation: Nat Struct Mol Biol. 2012 Dec;19(12):1287-92
references.pmid: 23142979
references.citation: Nature. 2012 Nov 22;491(7425):560-5
references.pmid: 23075851
references.citation: EMBO J. 2003 Apr 15;22(8):1846-56
references.pmid: 12682017
references.citation: Glycobiology. 2003 Feb;13(2):87-95
references.pmid: 12626410
references.citation: Science. 2007 Aug 24;317(5841):1087-90
references.pmid: 17717186
references.citation: Proc Natl Acad Sci U S A. 2010 Aug 10;107(32):14075-80
references.pmid: 20651253
references.citation: Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1525-30
references.pmid: 14732680
references.citation: Mol Cell Biol. 2011 Oct;31(19):4107-18
references.pmid: 21807893
references.citation: Genetics. 1989 May;122(1):19-27
references.pmid: 2659436
references.citation: Mol Cell. 2011 Dec 23;44(6):928-41
references.pmid: 22195966
references.citation: Genes Dev. 2000 Oct 1;14(19):2452-60
references.pmid: 11018013
references.citation: Biochim Biophys Acta. 2011 Oct;1809(10):557-66
references.pmid: 21782987
references.citation: Genes Dev. 2010 Jul 1;24(13):1334-8
references.pmid: 20595228
references.citation: Nature. 1997 Sep 18;389(6648):251-60
references.pmid: 9305837
references.citation: Cell. 2010 Mar 5;140(5):678-91
references.pmid: 20211137
references.citation: Mol Cell. 2002 Jun;9(6):1191-200
references.pmid: 12086617
references.citation: Mol Cell Biol. 2010 Mar;30(5):1116-29
references.pmid: 20048053
references.citation: Nat Struct Biol. 2003 Nov;10(11):882-91
references.pmid: 14583738
references.citation: J Biol Chem. 2008 Oct 10;283(41):27350-27354
references.pmid: 18708354
references.citation: Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6428-35
references.pmid: 16571659
references.citation: Mol Cell Biol. 2004 Dec;24(23):10111-7
references.pmid: 15542822
references.citation: J Biol Chem. 2010 Dec 31;285(53):41567-77
references.pmid: 21041298
references.citation: Curr Opin Genet Dev. 2007 Apr;17(2):88-93
references.pmid: 17307351
references.citation: J Biol Chem. 2011 Dec 2;286(48):41883-41892
references.pmid: 21969370
references.citation: Proc Natl Acad Sci U S A. 2011 Jan 4;108(1):85-90
references.pmid: 21173268
references.citation: Eukaryot Cell. 2006 Oct;5(10):1780-7
references.pmid: 16936140
references.citation: J Biol Chem. 2012 Mar 30;287(14):10753-60
references.pmid: 22337870
references.citation: Genes Dev. 2001 Dec 15;15(24):3319-29
references.pmid: 11751637