Reprogramming NK cells and macrophages via combined antibody and cytokine therapy primes tumors for elimination by checkpoint blockade.


Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
23 11 2021
Historique:
received: 26 05 2021
revised: 29 09 2021
accepted: 27 10 2021
entrez: 24 11 2021
pubmed: 25 11 2021
medline: 15 2 2022
Statut: ppublish

Résumé

Treatments aiming to augment immune checkpoint blockade (ICB) in cancer often focus on T cell immunity, but innate immune cells may have important roles to play. Here, we demonstrate a single-dose combination treatment (termed AIP) using a pan-tumor-targeting antibody surrogate, half-life-extended interleukin-2 (IL-2), and anti-programmed cell death 1 (PD-1), which primes tumors to respond to subsequent ICB and promotes rejection of large established tumors in mice. Natural killer (NK) cells and macrophages activated by AIP treatment underwent transcriptional reprogramming; rapidly killed cancer cells; governed the recruitment of cross-presenting dendritic cells (DCs) and other leukocytes; and induced normalization of the tumor vasculature, facilitating further immune infiltration. Thus, innate cell-activating therapies can initiate critical steps leading to a self-sustaining cycle of T cell priming driven by ICB.

Identifiants

pubmed: 34818534
pii: S2211-1247(21)01503-5
doi: 10.1016/j.celrep.2021.110021
pmc: PMC8653865
mid: NIHMS1759310
pii:
doi:

Substances chimiques

Antibodies 0
Immune Checkpoint Inhibitors 0
Interleukin-2 0
Programmed Cell Death 1 Receptor 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

110021

Subventions

Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA014051
Pays : United States

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests D.J.I. and C.W. are named as inventors on a patent application filed by MIT for 1X AIP therapy.

Références

N Engl J Med. 2010 Aug 19;363(8):711-23
pubmed: 20525992
N Engl J Med. 2015 Jun 25;372(26):2509-20
pubmed: 26028255
Nature. 2017 May 4;545(7652):98-102
pubmed: 28445461
Cell. 2017 Sep 7;170(6):1109-1119.e10
pubmed: 28886381
Cancer Cell. 2017 May 8;31(5):711-723.e4
pubmed: 28486109
Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):E50-9
pubmed: 23248310
Cell Rep. 2015 May 19;11(7):1018-30
pubmed: 25959818
Cancer Immunol Res. 2017 Jan;5(1):17-28
pubmed: 28003187
N Engl J Med. 2018 Jun 14;378(24):2288-2301
pubmed: 29863955
Br J Cancer. 2006 Jan 30;94(2):259-67
pubmed: 16404427
N Engl J Med. 2017 Nov 16;377(20):1919-1929
pubmed: 28885881
N Engl J Med. 2014 Dec 4;371(23):2189-2199
pubmed: 25409260
Cell Rep. 2017 Jul 5;20(1):236-250
pubmed: 28683317
Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17561-6
pubmed: 23045683
J Immunol. 2015 Dec 1;195(11):5495-502
pubmed: 26525286
Cell. 2018 Nov 1;175(4):998-1013.e20
pubmed: 30388456
J Immunol. 2009 Apr 1;182(7):4339-48
pubmed: 19299734
Proc Natl Acad Sci U S A. 2013 Sep 3;110(36):14598-603
pubmed: 23950221
Proc Natl Acad Sci U S A. 2012 May 15;109(20):7841-6
pubmed: 22547817
J Exp Med. 2021 Jan 4;218(1):
pubmed: 33045061
Nat Med. 2018 Aug;24(8):1178-1191
pubmed: 29942093
Nat Commun. 2017 Oct 26;8(1):1136
pubmed: 29070816
Oncoimmunology. 2017 Nov 20;7(3):e1393598
pubmed: 29399390
Science. 2006 Sep 29;313(5795):1960-4
pubmed: 17008531
EMBO J. 2001 Oct 15;20(20):5568-77
pubmed: 11598000
Nat Biomed Eng. 2017;1:
pubmed: 28868207
Int J Cancer. 2009 Jul 15;125(2):367-73
pubmed: 19378341
Nat Med. 2020 May;26(5):693-698
pubmed: 32405063
J Immunother Cancer. 2020 Mar;8(1):
pubmed: 32169869
Proteins. 2009 Nov 1;77(2):359-69
pubmed: 19452550
Cancer Res. 2016 Jul 1;76(13):3767-72
pubmed: 27197178
Eur J Immunol. 2003 Oct;33(10):2736-43
pubmed: 14515257
PLoS One. 2015 Dec 23;10(12):e0145342
pubmed: 26699615
MAbs. 2015;7(3):494-504
pubmed: 25933349
Genome Biol. 2014;15(12):550
pubmed: 25516281
Int J Cancer. 2011 Jan 15;128(2):371-8
pubmed: 20333679
N Engl J Med. 2012 Jun 28;366(26):2443-54
pubmed: 22658127
Bioinformatics. 2019 Jun 1;35(12):2084-2092
pubmed: 30395178
Cancer Discov. 2016 Apr;6(4):414-29
pubmed: 26873347
Cancer Res. 2017 Oct 1;77(19):5215-5221
pubmed: 28928130
Front Immunol. 2011 Sep 12;2:35
pubmed: 22566825
J Immunol. 2009 Nov 15;183(10):6413-21
pubmed: 19841170
J Exp Med. 2017 Jun 5;214(6):1679-1690
pubmed: 28473400
Front Immunol. 2018 Jul 10;9:1593
pubmed: 30042766
N Engl J Med. 2016 Nov 10;375(19):1823-1833
pubmed: 27718847
Cancer Discov. 2016 Aug;6(8):827-37
pubmed: 27301722
Sci Transl Med. 2017 Sep 13;9(407):
pubmed: 28904226
Nat Immunol. 2012 Nov;13(11):1118-28
pubmed: 23023392
Nature. 2014 Nov 27;515(7528):568-71
pubmed: 25428505
Cell Metab. 2006 Jul;4(1):13-24
pubmed: 16814729
Nature. 2014 Mar 27;507(7493):519-22
pubmed: 24531764
J Med Chem. 2014 Aug 14;57(15):6301-15
pubmed: 24568695
Nature. 2017 Apr 13;544(7649):250-254
pubmed: 28371798
Am J Pathol. 2002 Nov;161(5):1749-59
pubmed: 12414522
Cell. 2015 May 21;161(5):1035-1045
pubmed: 25976835
J Control Release. 2015 Jul 28;210:134-46
pubmed: 26003042
Front Immunol. 2019 Feb 08;10:147
pubmed: 30800123
J Biol Chem. 2017 Aug 25;292(34):14003-14015
pubmed: 28687632
Cancer Cell. 2015 Apr 13;27(4):489-501
pubmed: 25873172
Proc Natl Acad Sci U S A. 1999 May 11;96(10):5640-4
pubmed: 10318937
F1000Res. 2015 Dec 30;4:1521
pubmed: 26925227
Cell Syst. 2015 Dec 23;1(6):417-425
pubmed: 26771021
J Biol Chem. 2017 Mar 3;292(9):3900-3908
pubmed: 28077575
Genome Biol. 2010;11(10):R106
pubmed: 20979621
Nat Commun. 2016 Oct 31;7:12849
pubmed: 27796300
N Engl J Med. 2018 May 31;378(22):2093-2104
pubmed: 29658845
J Immunol. 2015 Mar 1;194(5):2358-68
pubmed: 25637019
Nat Immunol. 2012 Oct;13(10):1000-9
pubmed: 22902830
Front Immunol. 2017 Mar 06;8:218
pubmed: 28321218
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
pubmed: 16199517
Pigment Cell Melanoma Res. 2016 Sep;29(5):590-7
pubmed: 27287723
Structure. 2019 Sep 3;27(9):1443-1451.e6
pubmed: 31353240
J Immunol. 2008 Nov 1;181(9):6664-9
pubmed: 18941257
Cancer Cell. 2010 Aug 9;18(2):160-70
pubmed: 20708157
J Immunol. 2004 Jun 15;172(12):7661-8
pubmed: 15187148
J Transl Med. 2016 Jun 24;14(1):187
pubmed: 27342639
Br J Cancer. 2006 Jan 30;94(2):218-26
pubmed: 16434984
J Exp Med. 2020 May 4;217(5):
pubmed: 32097462
Semin Oncol. 2015 Aug;42(4):663-71
pubmed: 26320069
Immunity. 2017 Feb 21;46(2):197-204
pubmed: 28228279
Cancer Discov. 2020 Aug;10(8):1158-1173
pubmed: 32439653
Blood. 2009 Jul 16;114(3):589-95
pubmed: 19349616
J Immunother Cancer. 2019 Sep 11;7(1):244
pubmed: 31511088
Nature. 2009 Jan 29;457(7229):557-61
pubmed: 19136945
Proc Natl Acad Sci U S A. 2019 May 14;116(20):9999-10008
pubmed: 31028147
Nature. 2015 May 7;521(7550):99-104
pubmed: 25924063
Sci Transl Med. 2010 Dec 22;2(63):63ra94
pubmed: 21178137
Trends Immunol. 2009 Dec;30(12):592-602
pubmed: 19879803
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
Nat Biotechnol. 1999 Oct;17(10):969-73
pubmed: 10504696
Nature. 2015 Jul 9;523(7559):231-5
pubmed: 25970248
Cell. 2016 Oct 6;167(2):397-404.e9
pubmed: 27667683
Nat Med. 2013 Jun;19(6):730-8
pubmed: 23685841
N Engl J Med. 2016 Sep 1;375(9):819-29
pubmed: 27433843
J Exp Med. 2008 Jun 9;205(6):1261-8
pubmed: 18490490
J Immunol. 2012 Mar 15;188(6):2687-94
pubmed: 22323546
Future Oncol. 2021 Feb;17(5):491-501
pubmed: 33167735
Nat Med. 2016 Dec;22(12):1402-1410
pubmed: 27775706
Front Immunol. 2019 May 24;10:1084
pubmed: 31178859
Cell. 2018 Feb 22;172(5):1022-1037.e14
pubmed: 29429633
Sci Immunol. 2017 Jan 6;2(7):
pubmed: 28783667
J Immunol. 2014 Nov 1;193(9):4477-84
pubmed: 25261477
Cancer Res. 1996 Jan 1;56(1):21-6
pubmed: 8548765

Auteurs

Chensu Wang (C)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Ang Cui (A)

Broad Institute of MIT and Harvard, Cambridge, MA, USA; Harvard-MIT Division of Health Sciences and Technology, MIT, Cambridge, MA, USA.

Maurice Bukenya (M)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Aereas Aung (A)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Dikshant Pradhan (D)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Charles A Whittaker (CA)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Yash Agarwal (Y)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA.

Ayush Thomas (A)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Simon Liang (S)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Parastoo Amlashi (P)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Heikyung Suh (H)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA.

Stefani Spranger (S)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Nir Hacohen (N)

Broad Institute of MIT and Harvard, Cambridge, MA, USA; Center for Cancer Research, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.

Darrell J Irvine (DJ)

Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard, Cambridge, MA, USA; Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Howard Hughes Medical Institute, Chevy Chase, MD, USA. Electronic address: djirvine@mit.edu.

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