Importin-9 wraps around the H2A-H2B core to act as nuclear importer and histone chaperone.


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
11 03 2019
Historique:
received: 14 11 2018
accepted: 09 03 2019
pubmed: 12 3 2019
medline: 20 3 2020
entrez: 12 3 2019
Statut: epublish

Résumé

We report the crystal structure of nuclear import receptor Importin-9 bound to its cargo, the histones H2A-H2B. Importin-9 wraps around the core, globular region of H2A-H2B to form an extensive interface. The nature of this interface coupled with quantitative analysis of deletion mutants of H2A-H2B suggests that the NLS-like sequences in the H2A-H2B tails play a minor role in import. Importin-9•H2A-H2B is reminiscent of interactions between histones and histone chaperones in that it precludes H2A-H2B interactions with DNA and H3-H4 as seen in the nucleosome. Like many histone chaperones, which prevent inappropriate non-nucleosomal interactions, Importin-9 also sequesters H2A-H2B from DNA. Importin-9 appears to act as a storage chaperone for H2A-H2B while escorting it to the nucleus. Surprisingly, RanGTP does not dissociate Importin-9•H2A-H2B but assembles into a RanGTP•Importin-9•H2A-H2B complex. The presence of Ran in the complex, however, modulates Imp9-H2A-H2B interactions to facilitate its dissociation by DNA and assembly into a nucleosome.

Identifiants

pubmed: 30855230
doi: 10.7554/eLife.43630
pii: 43630
pmc: PMC6453568
doi:
pii:

Substances chimiques

Histones 0
IPO9 protein, human 0
Karyopherins 0
Molecular Chaperones 0
Mutant Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIGMS NIH HHS
ID : R01GM112108
Pays : United States
Organisme : NIH HHS
ID : S10 OD021512
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41GM109824
Pays : United States
Organisme : NIH HHS
ID : S10 OD025018
Pays : United States
Organisme : NIGMS NIH HHS
ID : U01GM98256-01
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM112108
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01GM083960
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01GM069909
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM069909
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM109824
Pays : United States
Organisme : NIH HHS
ID : S10 OD021596
Pays : United States

Informations de copyright

© 2019, Padavannil et al.

Déclaration de conflit d'intérêts

AP, PS, SK, TC, JJ, CB, DT, AS, SD, YC No competing interests declared

Références

Methods Enzymol. 1997;276:523-30
pubmed: 9048379
EMBO J. 1997 Nov 3;16(21):6535-47
pubmed: 9351834
Mol Cell. 2010 Jan 29;37(2):211-22
pubmed: 20122403
J Biol Chem. 2007 Jul 13;282(28):20142-50
pubmed: 17507373
Cell. 2018 Apr 19;173(3):693-705.e22
pubmed: 29677513
J Mol Biol. 2013 Jun 12;425(11):1852-1868
pubmed: 23541588
Biochim Biophys Acta. 2013 Mar-Apr;1819(3-4):196-210
pubmed: 24459722
Methods Enzymol. 2015;562:109-33
pubmed: 26412649
Mol Cell. 2015 Oct 15;60(2):294-306
pubmed: 26455391
Biochim Biophys Acta. 2011 Sep;1813(9):1593-606
pubmed: 21029754
Biochem J. 2015 Jun 15;468(3):353-62
pubmed: 26173234
FEBS Lett. 2000 Feb 11;467(2-3):169-74
pubmed: 10675532
EMBO J. 2002 Dec 2;21(23):6527-38
pubmed: 12456659
Curr Opin Genet Dev. 1999 Apr;9(2):185-90
pubmed: 10322140
Biophys J. 2000 Mar;78(3):1606-19
pubmed: 10692345
Eur J Cell Biol. 2001 Nov;80(11):669-77
pubmed: 11824786
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):426-36
pubmed: 20382996
FEBS Lett. 2015 Sep 14;589(19 Pt A):2570-7
pubmed: 26320411
EMBO J. 1999 May 4;18(9):2411-23
pubmed: 10228156
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
J Cell Biol. 2002 Oct 28;159(2):267-78
pubmed: 12403813
Nature. 2009 Sep 3;461(7260):60-5
pubmed: 19680239
J Cell Sci. 2000 Mar;113 ( Pt 5):899-906
pubmed: 10671379
J Biol Chem. 2016 Sep 30;291(40):21171-21183
pubmed: 27528606
Nature. 2013 Jul 4;499(7456):111-4
pubmed: 23698368
Genes Dev. 2001 Aug 15;15(16):2048-53
pubmed: 11511536
Biophys J. 1999 Jun;76(6):2879-86
pubmed: 10354416
Biochim Biophys Acta. 2013 Mar-Apr;1819(3-4):211-221
pubmed: 24459723
Acta Crystallogr F Struct Biol Commun. 2014 Jun;70(Pt 6):723-9
pubmed: 24915079
Cell. 1999 May 28;97(5):635-46
pubmed: 10367892
Science. 2016 Apr 15;352(6283):363-5
pubmed: 27081072
J Synchrotron Radiat. 2002 Nov 1;9(Pt 6):401-6
pubmed: 12409628
Nature. 2004 Dec 16;432(7019):872-7
pubmed: 15602554
Science. 2017 May 26;356(6340):
pubmed: 28495876
Elife. 2015 Sep 08;4:
pubmed: 26349033
Methods. 2015 Apr;76:137-148
pubmed: 25477226
Methods Enzymol. 2004;375:23-44
pubmed: 14870657
EMBO J. 2011 Jan 19;30(2):427-38
pubmed: 21139563
EMBO J. 2011 Jul 08;30(16):3309-21
pubmed: 21743438
Science. 2016 Apr 15;352(6283):aaf1015
pubmed: 27081075
Annu Rev Cell Dev Biol. 1999;15:607-60
pubmed: 10611974
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Acta Crystallogr D Biol Crystallogr. 2003 Nov;59(Pt 11):2031-8
pubmed: 14573959
Mol Biol Cell. 2011 Jan 15;22(2):245-55
pubmed: 21118997
Science. 2017 Aug 18;357(6352):
pubmed: 28818916
Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41
pubmed: 11517324
Nat Struct Mol Biol. 2008 Aug;15(8):868-9
pubmed: 18641662
EMBO J. 2002 Feb 1;21(3):377-86
pubmed: 11823430
Nature. 2005 Jun 2;435(7042):693-6
pubmed: 15864302
Acta Crystallogr A. 2003 May;59(Pt 3):228-34
pubmed: 12714773
Acta Crystallogr D Biol Crystallogr. 2006 Aug;62(Pt 8):859-66
pubmed: 16855301
EMBO Rep. 2015 Nov;16(11):1454-66
pubmed: 26459557
Science. 2009 Nov 27;326(5957):1275-9
pubmed: 19965479
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
EMBO J. 2013 Mar 20;32(6):899-913
pubmed: 23435562
Anal Chem. 2012 Jun 5;84(11):5066-73
pubmed: 22530732
J Synchrotron Radiat. 2012 May;19(Pt 3):431-4
pubmed: 22514181
Nature. 2014 Jan 30;505(7485):648-53
pubmed: 24463511
Nature. 1999 May 20;399(6733):230-7
pubmed: 10353245
Proc Natl Acad Sci U S A. 2014 Feb 18;111(7):2728-33
pubmed: 24449914
Elife. 2017 Jan 24;6:
pubmed: 28117667
J Cell Biol. 2001 Apr 16;153(2):251-62
pubmed: 11309407
Nature. 1997 Sep 18;389(6648):251-60
pubmed: 9305837
EMBO Rep. 2001 Aug;2(8):690-6
pubmed: 11493596
Eur J Cell Biol. 2004 Oct;83(10):511-20
pubmed: 15679097
Mol Cell. 2010 Mar 26;37(6):834-42
pubmed: 20347425
Nature. 1978 Oct 5;275(5679):416-20
pubmed: 692721
J Biol Chem. 2008 Nov 21;283(47):32412-8
pubmed: 18728017
J Synchrotron Radiat. 2013 Jan;20(Pt 1):37-48
pubmed: 23254654
Biochemistry. 2002 Jun 4;41(22):6955-66
pubmed: 12033928
Mol Cell Biol. 1987 Nov;7(11):4048-57
pubmed: 3123916
J Synchrotron Radiat. 2004 Nov 1;11(Pt 6):462-8
pubmed: 15496733
Mol Cell. 2014 Feb 6;53(3):498-505
pubmed: 24507717
Annu Rev Biochem. 2007;76:647-71
pubmed: 17506639
J Appl Crystallogr. 2009 Apr 1;42(Pt 2):342-346
pubmed: 27630371
Nature. 2018 Mar 22;555(7697):475-482
pubmed: 29539637
Nat Rev Mol Cell Biol. 2017 Mar;18(3):141-158
pubmed: 28053344
Genes Dev. 2000 Jun 15;14(12):1430-8
pubmed: 10859162
Nat Commun. 2016 Jun 16;7:11952
pubmed: 27306458
J Biol Chem. 2002 Jan 4;277(1):862-8
pubmed: 11694505
Protein Sci. 2007 Jan;16(1):30-42
pubmed: 17192587
J Appl Crystallogr. 2012 Mar 15;45(Pt 2):342-350
pubmed: 25484842

Auteurs

Abhilash Padavannil (A)

Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, United States.

Prithwijit Sarkar (P)

Department of Biological Sciences, University of Texas at Dallas, Richardson, United States.

Seung Joong Kim (SJ)

Department of Physics, Korea Advanced Institute of Science and Technology (KAIST), Daejeon, Korea.

Tolga Cagatay (T)

Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, United States.

Jenny Jiou (J)

Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, United States.

Chad A Brautigam (CA)

Department of Biophysics, University of Texas Southwestern Medical Center, Dallas, United States.

Diana R Tomchick (DR)

Department of Biophysics, University of Texas Southwestern Medical Center, Dallas, United States.

Andrej Sali (A)

Department of Bioengineering and Therapeutic Sciences, California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, United States.
Department of Pharmaceutical Chemistry, California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, United states.

Sheena D'Arcy (S)

Department of Chemistry and Biochemistry, University of Texas at Dallas, Richardson, United States.

Yuh Min Chook (YM)

Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, United States.

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