Tumour-infiltrating neutrophils counteract anti-VEGF therapy in metastatic colorectal cancer.


Journal

British journal of cancer
ISSN: 1532-1827
Titre abrégé: Br J Cancer
Pays: England
ID NLM: 0370635

Informations de publication

Date de publication:
01 2019
Historique:
received: 27 03 2018
accepted: 04 07 2018
revised: 25 06 2018
pubmed: 1 11 2018
medline: 19 9 2019
entrez: 1 11 2018
Statut: ppublish

Résumé

Immune infiltration is implicated in the development of acquired resistance to anti-angiogenic cancer therapy. We therefore investigated the correlation between neutrophil infiltration in metastasis of colorectal cancer (CRC) patients and survival after treatment with bevacizumab. Our study identifies CD177+ tumour neutrophil infiltration as an adverse prognostic factor for bevacizumab treatment. We further demonstrate that a novel anti-VEGF/anti-Ang2 compound (BI-880) can overcome resistance to VEGF inhibition in experimental tumour models. A total of 85 metastatic CRC patients were stratified into cohorts that had either received chemotherapy alone (n = 39) or combined with bevacizumab (n = 46). Tumour CD177+ neutrophil infiltration was correlated to clinical outcome. The impact of neutrophil infiltration on anti-VEGF or anti-VEGF/anti-Ang2 therapy was studied in both xenograft and syngeneic tumour models by immunohistochemistry. The survival of bevacizumab-treated CRC patients in the presence of CD177+ infiltrates was significantly reduced compared to patients harbouring CD177- metastases. BI-880 treatment reduced the development of hypoxia associated with bevacizumab treatment and improved vascular normalisation in xenografts. Furthermore, neutrophil depletion or BI-880 treatment restored treatment sensitivity in a syngeneic tumour model of anti-VEGF resistance. Our findings implicate CD177 as a biomarker for bevacizumab and suggest VEGF/Ang2 inhibition as a strategy to overcome neutrophil associated resistance to anti-angiogenic treatment.

Sections du résumé

BACKGROUND
Immune infiltration is implicated in the development of acquired resistance to anti-angiogenic cancer therapy. We therefore investigated the correlation between neutrophil infiltration in metastasis of colorectal cancer (CRC) patients and survival after treatment with bevacizumab. Our study identifies CD177+ tumour neutrophil infiltration as an adverse prognostic factor for bevacizumab treatment. We further demonstrate that a novel anti-VEGF/anti-Ang2 compound (BI-880) can overcome resistance to VEGF inhibition in experimental tumour models.
METHODS
A total of 85 metastatic CRC patients were stratified into cohorts that had either received chemotherapy alone (n = 39) or combined with bevacizumab (n = 46). Tumour CD177+ neutrophil infiltration was correlated to clinical outcome. The impact of neutrophil infiltration on anti-VEGF or anti-VEGF/anti-Ang2 therapy was studied in both xenograft and syngeneic tumour models by immunohistochemistry.
RESULTS
The survival of bevacizumab-treated CRC patients in the presence of CD177+ infiltrates was significantly reduced compared to patients harbouring CD177- metastases. BI-880 treatment reduced the development of hypoxia associated with bevacizumab treatment and improved vascular normalisation in xenografts. Furthermore, neutrophil depletion or BI-880 treatment restored treatment sensitivity in a syngeneic tumour model of anti-VEGF resistance.
CONCLUSIONS
Our findings implicate CD177 as a biomarker for bevacizumab and suggest VEGF/Ang2 inhibition as a strategy to overcome neutrophil associated resistance to anti-angiogenic treatment.

Identifiants

pubmed: 30377339
doi: 10.1038/s41416-018-0198-3
pii: 10.1038/s41416-018-0198-3
pmc: PMC6325148
doi:

Substances chimiques

Angiogenesis Inhibitors 0
Antibodies, Monoclonal, Humanized 0
Biomarkers, Tumor 0
CD177 protein, human 0
GPI-Linked Proteins 0
Isoantigens 0
Receptors, Cell Surface 0
VEGFA protein, human 0
VPS51 protein, human 0
Vascular Endothelial Growth Factor A 0
Vesicular Transport Proteins 0
Bevacizumab 2S9ZZM9Q9V

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

69-78

Références

Int J Cancer. 2016 Jul 15;139(2):446-56
pubmed: 26939802
J Clin Oncol. 2012 Nov 10;30(32):4026-34
pubmed: 23008289
Br J Cancer. 2017 Feb 28;116(5):600-608
pubmed: 28141797
Front Pharmacol. 2017 Jan 06;7:519
pubmed: 28111549
Science. 2005 Jan 7;307(5706):58-62
pubmed: 15637262
Cancer Res. 2007 Aug 1;67(15):7358-67
pubmed: 17671206
Br J Cancer. 2010 Oct 26;103(9):1407-14
pubmed: 20924372
Cancer. 2018 Apr 1;124(7):1438-1448
pubmed: 29266174
PLoS One. 2012;7(1):e30806
pubmed: 22295111
EMBO Mol Med. 2014 May 01;6(5):624-39
pubmed: 24648500
Oncotarget. 2016 Apr 19;7(16):21763-74
pubmed: 26943575
Br J Cancer. 2017 Apr 25;116(9):1119-1125
pubmed: 28301873
Br J Cancer. 2011 Apr 12;104(8):1288-95
pubmed: 21448173
Cancer Res. 2013 Mar 15;73(6):1649-57
pubmed: 23467610
Proc Natl Acad Sci U S A. 2016 Apr 19;113(16):4470-5
pubmed: 27044097
Nat Med. 2013 Sep;19(9):1114-23
pubmed: 23913124
Nat Rev Cancer. 2016 Jul;16(7):431-46
pubmed: 27282249
Clin Cancer Res. 2011 Mar 1;17(5):1001-11
pubmed: 21233403
Cancer Cell. 2011 Apr 12;19(4):512-26
pubmed: 21481792
J Clin Invest. 2017 Aug 1;127(8):3039-3051
pubmed: 28691930
Blood. 2017 Nov 9;130(19):2092-2100
pubmed: 28807980
Cold Spring Harb Perspect Med. 2012 Sep 01;2(9):a006550
pubmed: 22951441
J Transl Med. 2004 Mar 29;2(1):8
pubmed: 15050027
Nat Biotechnol. 2007 Aug;25(8):911-20
pubmed: 17664940
PLoS One. 2013 May 29;8(5):e64814
pubmed: 23734221
Br J Cancer. 2015 Feb 3;112(3):495-503
pubmed: 25562438
Trends Immunol. 2016 Jan;37(1):41-52
pubmed: 26700397
Cancer Cell. 2013 Mar 18;23(3):277-86
pubmed: 23518347
Cancer Res. 2012 Aug 15;72(16):3906-11
pubmed: 22751463
Cancer Res. 2010 Mar 15;70(6):2213-23
pubmed: 20197469
Oncotarget. 2016 May 31;7(22):33210-9
pubmed: 27120807
Nature. 2015 Jun 18;522(7556):345-348
pubmed: 25822788
BMC Cancer. 2011 Jun 02;11:216
pubmed: 21635742
J Natl Cancer Inst. 2017 Nov 1;109(11):
pubmed: 29059426

Auteurs

Lars Mortimer Schiffmann (LM)

Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne (CMMC) and Institute for Medical Microbiology, Immunology and Hygiene, University of Cologne, CECAD Research Center, Joseph-Stelzmann-Str. 26, 50931, Cologne, Germany. lars.schiffmann@uk-koeln.de.
Department of General, Visceral and Cancer Surgery, University of Cologne, Kerpener Str. 62, 50937, Cologne, Germany. lars.schiffmann@uk-koeln.de.
Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany. lars.schiffmann@uk-koeln.de.

Melanie Fritsch (M)

Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne (CMMC) and Institute for Medical Microbiology, Immunology and Hygiene, University of Cologne, CECAD Research Center, Joseph-Stelzmann-Str. 26, 50931, Cologne, Germany.

Florian Gebauer (F)

Department of General, Visceral and Cancer Surgery, University of Cologne, Kerpener Str. 62, 50937, Cologne, Germany.
Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.

Saskia Diana Günther (SD)

Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne (CMMC) and Institute for Medical Microbiology, Immunology and Hygiene, University of Cologne, CECAD Research Center, Joseph-Stelzmann-Str. 26, 50931, Cologne, Germany.

Neil Richard Stair (NR)

Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne (CMMC) and Institute for Medical Microbiology, Immunology and Hygiene, University of Cologne, CECAD Research Center, Joseph-Stelzmann-Str. 26, 50931, Cologne, Germany.

Jens Michael Seeger (JM)

Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne (CMMC) and Institute for Medical Microbiology, Immunology and Hygiene, University of Cologne, CECAD Research Center, Joseph-Stelzmann-Str. 26, 50931, Cologne, Germany.

Fabinshy Thangarajah (F)

Department of Gynaecology and Obstetrics, University of Cologne, Kerpener Str. 34, 50931, Cologne, Germany.

Georg Dieplinger (G)

Department of General, Visceral and Cancer Surgery, University of Cologne, Kerpener Str. 62, 50937, Cologne, Germany.
Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.

Marc Bludau (M)

Department of General, Visceral and Cancer Surgery, University of Cologne, Kerpener Str. 62, 50937, Cologne, Germany.
Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.

Hakan Alakus (H)

Department of General, Visceral and Cancer Surgery, University of Cologne, Kerpener Str. 62, 50937, Cologne, Germany.
Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.

Heike Göbel (H)

Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.
Institute for Pathology, University of Cologne, Kerpener Str. 62, 50937, Cologne, Germany.

Alexander Quaas (A)

Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.
Institute for Pathology, University of Cologne, Kerpener Str. 62, 50937, Cologne, Germany.

Thomas Zander (T)

Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.
Department I of Internal Medicine, University of Cologne, Kerpener Str. 62, 50924, Cologne, Germany.

Frank Hilberg (F)

Boehringer Ingelheim RCV, Doktor-Boehringer-Gasse 5-11, 1120, Vienna, Austria.

Christiane Josephine Bruns (CJ)

Department of General, Visceral and Cancer Surgery, University of Cologne, Kerpener Str. 62, 50937, Cologne, Germany.
Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.

Hamid Kashkar (H)

Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne (CMMC) and Institute for Medical Microbiology, Immunology and Hygiene, University of Cologne, CECAD Research Center, Joseph-Stelzmann-Str. 26, 50931, Cologne, Germany.
Center for Integrated Oncology (CIO) Cologne Bonn, Gastrointestinal Cancer Group Cologne (GCGC), Kerpener Str. 62, 50924, Cologne, Germany.

Oliver Coutelle (O)

Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne (CMMC) and Institute for Medical Microbiology, Immunology and Hygiene, University of Cologne, CECAD Research Center, Joseph-Stelzmann-Str. 26, 50931, Cologne, Germany.

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