Ribosomal Proteins Regulate MHC Class I Peptide Generation for Immunosurveillance.


Journal

Molecular cell
ISSN: 1097-4164
Titre abrégé: Mol Cell
Pays: United States
ID NLM: 9802571

Informations de publication

Date de publication:
21 03 2019
Historique:
received: 13 07 2018
revised: 29 10 2018
accepted: 21 12 2018
pubmed: 5 2 2019
medline: 15 9 2020
entrez: 5 2 2019
Statut: ppublish

Résumé

The MHC class I antigen presentation system enables T cell immunosurveillance of cancers and viruses. A substantial fraction of the immunopeptidome derives from rapidly degraded nascent polypeptides (DRiPs). By knocking down each of the 80 ribosomal proteins, we identified proteins that modulate peptide generation without altering source protein expression. We show that 60S ribosomal proteins L6 (RPL6) and RPL28, which are adjacent on the ribosome, play opposite roles in generating an influenza A virus-encoded peptide. Depleting RPL6 decreases ubiquitin-dependent peptide presentation, whereas depleting RPL28 increases ubiquitin-dependent and -independent peptide presentation. 40S ribosomal protein S28 (RPS28) knockdown increases total peptide supply in uninfected cells by increasing DRiP synthesis from non-canonical translation of "untranslated" regions and non-AUG start codons and sensitizes tumor cells for T cell targeting. Our findings raise the possibility of modulating immunosurveillance by pharmaceutical targeting ribosomes.

Identifiants

pubmed: 30712990
pii: S1097-2765(18)31096-7
doi: 10.1016/j.molcel.2018.12.020
pmc: PMC6697054
mid: NIHMS1519606
pii:
doi:

Substances chimiques

Histocompatibility Antigens Class I 0
RPL28 protein, human 0
RPS28 protein, human 0
Ribosomal Proteins 0
ribosomal protein L6 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

Pagination

1162-1173.e5

Subventions

Organisme : NIA NIH HHS
ID : R01 AG042400
Pays : United States
Organisme : Intramural NIH HHS
ID : Z01 AI000542-20
Pays : United States
Organisme : Intramural NIH HHS
ID : Z01 AI000542-21
Pays : United States

Informations de copyright

Published by Elsevier Inc.

Références

Nature. 2000 Apr 13;404(6779):770-4
pubmed: 10783891
J Immunol. 2001 Aug 1;167(3):1212-21
pubmed: 11466336
J Exp Med. 1992 Jan 1;175(1):163-8
pubmed: 1309852
Science. 1992 Mar 6;255(5049):1264-6
pubmed: 1546329
J Exp Med. 2005 Jan 3;201(1):95-104
pubmed: 15623576
J Virol. 2005 Jul;79(13):8431-9
pubmed: 15956587
Trends Immunol. 2006 Aug;27(8):368-73
pubmed: 16815756
J Virol. 2007 Jul;81(13):7220-9
pubmed: 17459927
Nat Biotechnol. 2008 Dec;26(12):1367-72
pubmed: 19029910
Nat Protoc. 2009;4(1):44-57
pubmed: 19131956
Genome Biol. 2009;10(3):R25
pubmed: 19261174
Bioinformatics. 2009 May 1;25(9):1105-11
pubmed: 19289445
Nat Genet. 2009 Jun;41(6):753-61
pubmed: 19412179
J Immunol. 2010 Feb 1;184(3):1419-24
pubmed: 20038640
J Immunol. 2010 Dec 1;185(11):6728-33
pubmed: 21048111
Curr Protoc Cell Biol. 2010 Dec;Chapter 3:Unit 3.40
pubmed: 21154551
Nature. 2011 May 19;473(7347):337-42
pubmed: 21593866
Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11572-7
pubmed: 21709220
Mol Cell. 2011 Oct 21;44(2):325-40
pubmed: 21906983
Cell. 2011 Nov 11;147(4):789-802
pubmed: 22056041
Nat Rev Mol Cell Biol. 2012 May 23;13(6):355-69
pubmed: 22617470
Science. 2012 Jun 29;336(6089):1719-23
pubmed: 22745432
Nat Protoc. 2012 Jul 26;7(8):1534-50
pubmed: 22836135
J Virol. 2013 Mar;87(6):3155-62
pubmed: 23283949
PLoS Pathog. 2013 Jan;9(1):e1003129
pubmed: 23382674
Mol Cell. 2013 May 9;50(3):368-78
pubmed: 23583076
Proc Natl Acad Sci U S A. 2013 Oct 29;110(44):17951-6
pubmed: 24082107
Nature. 2013 Oct 17;502(7471):333-339
pubmed: 24132290
J Leukoc Biol. 2014 Apr;95(4):551-62
pubmed: 24532645
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Genome Biol. 2014;15(12):550
pubmed: 25516281
Biotechnol J. 2015 Apr;10(4):647-53
pubmed: 25650551
J Biol Chem. 2015 Jun 26;290(26):16431-9
pubmed: 25971973
Mol Cell. 2015 Jul 2;59(1):35-49
pubmed: 26051182
Annu Rev Cell Dev Biol. 2015;31:31-54
pubmed: 26443190
Mol Cell. 2015 Dec 3;60(5):816-827
pubmed: 26638175
J Mol Biol. 2016 May 22;428(10 Pt B):2186-94
pubmed: 26764228
J Immunol. 2016 May 1;196(9):3608-17
pubmed: 27016602
Nucleic Acids Res. 2016 Sep 19;44(16):e135
pubmed: 27302133
Immunol Rev. 2016 Jul;272(1):8-16
pubmed: 27319338
Bioinformatics. 2017 Jan 1;33(1):135-136
pubmed: 27605098
J Immunol. 2016 Oct 15;197(8):2981-2991
pubmed: 27647836
BMC Genomics. 2016 Nov 22;17(1):958
pubmed: 27875984
EMBO Mol Med. 2017 Apr;9(4):498-507
pubmed: 28264936
J Immunol. 2017 May 15;198(10):3835-3845
pubmed: 28363906
Methods. 2017 Aug 15;126:112-129
pubmed: 28579404
Mol Cell. 2017 Jul 6;67(1):71-83.e7
pubmed: 28625553
Mol Cell. 2017 Jul 6;67(1):3-4
pubmed: 28686875
Nature. 2017 Aug 31;548(7669):537-542
pubmed: 28783722
Methods Mol Biol. 2018;1649:29-48
pubmed: 29130188
Proc Natl Acad Sci U S A. 2017 Dec 5;114(49):12934-12939
pubmed: 29158377
Hematology Am Soc Hematol Educ Program. 2017 Dec 8;2017(1):716-719
pubmed: 29222326
Eur J Haematol. 2018 Mar 30;:null
pubmed: 29603798
Genetics. 1995 Aug;140(4):1247-58
pubmed: 7498767
Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7976-80
pubmed: 7644523
Nature. 1995 Jun 1;375(6530):411-5
pubmed: 7760935
Proc Natl Acad Sci U S A. 1994 May 10;91(10):4145-9
pubmed: 8183884
Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9538-41
pubmed: 8415737
J Immunol. 1996 May 15;156(10):3755-64
pubmed: 8621911
J Immunol. 1996 Sep 1;157(5):1823-6
pubmed: 8757297
J Exp Med. 1996 Oct 1;184(4):1319-29
pubmed: 8879204
Immunity. 1997 Jun;6(6):715-26
pubmed: 9208844
J Immunol. 1997 Jul 15;159(2):554-64
pubmed: 9218569
J Immunol. 1998 Jul 1;161(1):83-9
pubmed: 9647210

Auteurs

Jiajie Wei (J)

Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA. Electronic address: weijiajie@gmail.com.

Rigel J Kishton (RJ)

National Cancer Institute, NIH, Bethesda, MD 20892, USA.

Matthew Angel (M)

Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA.

Crystal S Conn (CS)

Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853, USA.

Nicole Dalla-Venezia (N)

University of Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Center Léon Bérard, Center de Recherche en Cancérologie de Lyon, Lyon, 69373 Cedex 08, France.

Virginie Marcel (V)

University of Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Center Léon Bérard, Center de Recherche en Cancérologie de Lyon, Lyon, 69373 Cedex 08, France.

Anne Vincent (A)

University of Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Center Léon Bérard, Center de Recherche en Cancérologie de Lyon, Lyon, 69373 Cedex 08, France.

Frédéric Catez (F)

University of Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Center Léon Bérard, Center de Recherche en Cancérologie de Lyon, Lyon, 69373 Cedex 08, France.

Sabrina Ferré (S)

University of Grenoble Alpes, CEA, INSERM, BIG-BGE, 38000 Grenoble, France.

Lilia Ayadi (L)

Next-Generation Sequencing Core Facility, UMS2008 IBSLor CNRS-INSERM-University of Lorraine, 54505 Vandoeuvre-les-Nancy, France; Laboratory IMoPA, UMR7365 CNRS-University of Lorraine, 54505 Vandoeuvre-les-Nancy, France.

Virginie Marchand (V)

Next-Generation Sequencing Core Facility, UMS2008 IBSLor CNRS-INSERM-University of Lorraine, 54505 Vandoeuvre-les-Nancy, France; Laboratory IMoPA, UMR7365 CNRS-University of Lorraine, 54505 Vandoeuvre-les-Nancy, France.

Devin Dersh (D)

Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA.

James S Gibbs (JS)

Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA.

Ivaylo P Ivanov (IP)

Laboratory of Gene Regulation and Development, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD 20892, USA.

Nathan Fridlyand (N)

Laboratory of Translational Biology, School of Biosciences and Biotechnology, University of Camerino, Camerino MC 62032, Italy.

Yohann Couté (Y)

University of Grenoble Alpes, CEA, INSERM, BIG-BGE, 38000 Grenoble, France.

Jean-Jacques Diaz (JJ)

University of Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Center Léon Bérard, Center de Recherche en Cancérologie de Lyon, Lyon, 69373 Cedex 08, France.

Shu-Bing Qian (SB)

Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853, USA.

Louis M Staudt (LM)

Lymphoid Malignancies Branch, National Cancer Institute, NIH, Bethesda, MD 20892, USA.

Nicholas P Restifo (NP)

National Cancer Institute, NIH, Bethesda, MD 20892, USA; Center for Cell-Based Therapy, Center for Cancer Research, NIH, Bethesda, MD 20892, USA.

Jonathan W Yewdell (JW)

Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA. Electronic address: jyewdell@niaid.nih.gov.

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