Tumor-reprogrammed resident T cells resist radiation to control tumors.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
02 09 2019
Historique:
received: 15 12 2018
accepted: 06 08 2019
entrez: 4 9 2019
pubmed: 4 9 2019
medline: 31 12 2019
Statut: epublish

Résumé

Successful combinations of radiotherapy and immunotherapy depend on the presence of live T cells within the tumor; however, radiotherapy is believed to damage T cells. Here, based on longitudinal in vivo imaging and functional analysis, we report that a large proportion of T cells survive clinically relevant doses of radiation and show increased motility, and higher production of interferon gamma, compared with T cells from unirradiated tumors. Irradiated intratumoral T cells can mediate tumor control without newly-infiltrating T cells. Transcriptomic analysis suggests T cell reprogramming in the tumor microenvironment and similarities with tissue-resident memory T cells, which are more radio-resistant than circulating/lymphoid tissue T cells. TGFβ is a key upstream regulator of T cell reprogramming and contributes to intratumoral Tcell radio-resistance. These findings have implications for the design of radio-immunotherapy trials in that local irradiation is not inherently immunosuppressive, and irradiation of multiple tumors might optimize systemic effects of radiotherapy.

Identifiants

pubmed: 31477729
doi: 10.1038/s41467-019-11906-2
pii: 10.1038/s41467-019-11906-2
pmc: PMC6718618
doi:

Substances chimiques

Interferon-gamma 82115-62-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3959

Subventions

Organisme : NCI NIH HHS
ID : R01 CA134563
Pays : United States

Références

Cancer Res. 2002 Oct 15;62(20):5627-31
pubmed: 12384514
Mutat Res. 2002 Jan 15;513(1-2):27-36
pubmed: 11719087
Cancer Res. 2006 Nov 15;66(22):10861-9
pubmed: 17090522
Nature. 2017 May 4;545(7652):98-102
pubmed: 28445461
Proc R Soc Lond B Biol Sci. 1966 Oct 11;165(1001):413-23
pubmed: 4380568
Oncotarget. 2016 May 3;7(18):26496-515
pubmed: 27034163
Proc Natl Acad Sci U S A. 2016 Jul 5;113(27):7551-6
pubmed: 27317748
Nat Immunol. 2017 Aug;18(8):940-950
pubmed: 28628092
Nat Immunol. 2018 Jun;19(6):538-546
pubmed: 29777219
Mol Ther. 2012 May;20(5):1046-55
pubmed: 22334019
Nat Immunol. 2009 May;10(5):524-30
pubmed: 19305395
Bioinformatics. 2012 Mar 15;28(6):882-3
pubmed: 22257669
Am J Pathol. 1948 Sep;24(5):1055-65
pubmed: 18883953
J Cell Sci. 2003 Mar 15;116(Pt 6):1013-22
pubmed: 12584245
Oncotarget. 2016 Jul 12;7(28):43039-43051
pubmed: 27343548
Immunol Today. 1987;8(3):88-92
pubmed: 25289473
J Immunol. 2011 Dec 1;187(11):5510-4
pubmed: 22058417
Immunity. 2013 Oct 17;39(4):687-96
pubmed: 24076049
Oncotarget. 2018 May 4;9(34):23519-23531
pubmed: 29805752
Biostatistics. 2007 Jan;8(1):118-27
pubmed: 16632515
Cell Rep. 2017 Sep 19;20(12):2921-2934
pubmed: 28930685
Oncoimmunology. 2013 Nov 1;2(11):e26677
pubmed: 24482750
Immunity. 2014 Nov 20;41(5):843-52
pubmed: 25517616
Biostatistics. 2003 Apr;4(2):249-64
pubmed: 12925520
J Clin Oncol. 2018 Nov 10;36(32):3240-3250
pubmed: 30260759
Int J Cancer. 2004 Mar 20;109(2):214-9
pubmed: 14750172
Nat Commun. 2017 Jul 17;8:16073
pubmed: 28714465
J Immunol. 2002 Oct 1;169(7):3760-70
pubmed: 12244170
Oncotarget. 2016 Nov 15;7(46):75130-75144
pubmed: 27650547
Sci Immunol. 2016 Sep;1(3):
pubmed: 28018989
Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):12092-12093
pubmed: 29138347
Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1714-9
pubmed: 14755057
Clin Cancer Res. 2017 Sep 15;23(18):5514-5526
pubmed: 28533222
Bioinformatics. 2010 Oct 1;26(19):2363-7
pubmed: 20688976
JAMA Oncol. 2015 Dec;1(9):1325-32
pubmed: 26270858
Cancer Res. 2011 Apr 1;71(7):2488-96
pubmed: 21300764
Proc Natl Acad Sci U S A. 2014 Apr 8;111(14):5307-12
pubmed: 24706879
J Exp Med. 1986 May 1;163(5):1037-50
pubmed: 2871125
Hum Gene Ther. 2003 Aug 10;14(12):1155-68
pubmed: 12908967
Cell. 2015 May 7;161(4):737-49
pubmed: 25957682
J Immunol. 2015 Apr 1;194(7):3475-86
pubmed: 25725111
J Leukoc Biol. 1991 Apr;49(4):388-96
pubmed: 1900523
Radiat Res. 2010 Apr;173(4):469-78
pubmed: 20334519
J Clin Oncol. 2018 Jun 1;36(16):1611-1618
pubmed: 29437535
Nat Protoc. 2014 Jan;9(1):209-22
pubmed: 24385150
Curr Protoc Immunol. 2014 Aug 01;106:3.25.1-3.25.13
pubmed: 25081911
Radiat Res. 1997 Jan;147(1):55-60
pubmed: 8989370
Sci Rep. 2018 May 3;8(1):7012
pubmed: 29725089
J Pathol Bacteriol. 1952 Oct;64(4):687-704
pubmed: 13000583
Clin Cancer Res. 2011 Nov 1;17(21):6754-65
pubmed: 22028490
J Cell Comp Physiol. 1947 Dec;30(3):203-24
pubmed: 18896922
J Am Assoc Lab Anim Sci. 2009 Jan;48(1):11-22
pubmed: 19245745
Nature. 2017 May 4;545(7652):60-65
pubmed: 28397821
Radiat Res. 2010 Feb;173(2):148-57
pubmed: 20095846
Nature. 2017 Dec 14;552(7684):253-257
pubmed: 29211713
Nat Immunol. 2013 Dec;14(12):1294-301
pubmed: 24162776
Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5116-21
pubmed: 11309499
Adv Immunol. 1976;24:215-335
pubmed: 14486
J Clin Invest. 2012 Oct;122(10):3718-30
pubmed: 22945631
Cancer Res. 2005 Apr 15;65(8):3146-54
pubmed: 15833844
Semin Immunol. 2016 Feb;28(1):54-63
pubmed: 26872631
Clin Cancer Res. 2016 Dec 15;22(24):6290-6297
pubmed: 27267849
Nature. 2004 Jan 22;427(6972):355-60
pubmed: 14737169
Cancer Res. 2002 Mar 1;62(5):1462-70
pubmed: 11888921
Eur J Immunol. 1994 Nov;24(11):2914-7
pubmed: 7957582
Nature. 2012 Feb 29;483(7388):227-31
pubmed: 22388819
PLoS One. 2014 Jan 09;9(1):e85398
pubmed: 24416401
J Immunol. 2008 Sep 1;181(5):3099-107
pubmed: 18713980
J Immunol. 2012 Oct 15;189(8):3936-46
pubmed: 22984076
J Immunol. 2005 Jun 15;174(12):7516-23
pubmed: 15944250
Nat Rev Immunol. 2016 Mar;16(3):193-201
pubmed: 26852928

Auteurs

Ainhoa Arina (A)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA. aarina@bsd.uchicago.edu.

Michael Beckett (M)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Christian Fernandez (C)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Wenxin Zheng (W)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Sean Pitroda (S)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Steven J Chmura (SJ)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Jason J Luke (JJ)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.

Martin Forde (M)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Yuzhu Hou (Y)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Byron Burnette (B)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Helena Mauceri (H)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Israel Lowy (I)

Regeneron Pharmaceuticals, Tarrytown, NY, USA.

Tasha Sims (T)

Regeneron Pharmaceuticals, Tarrytown, NY, USA.

Nikolai Khodarev (N)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA.

Yang-Xin Fu (YX)

Department of Pathology, University of Texas Southwestern, Dallas, TX, 75390, USA.

Ralph R Weichselbaum (RR)

Department of Radiation and Cellular Oncology and Ludwig Center for Metastasis Research, The University of Chicago, Chicago, IL, 60637, USA. rrw@radonc.uchicago.edu.

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