- Record: found
- Abstract: found
- Article: found
Neutrophil phenotypes and functions in cancer: A consensus statement
review-article
Author(s):
Daniela F. Quail
1
,
,
Borko Amulic
2 ,
Monowar Aziz
3 ,
Betsy J. Barnes
4
,
5 ,
Evgeniy Eruslanov
6 ,
Zvi G. Fridlender
7 ,
Helen S. Goodridge
8 ,
Zvi Granot
9 ,
Andrés Hidalgo
10
,
11 ,
Anna Huttenlocher
12
,
13 ,
Mariana J. Kaplan
14 ,
Ilaria Malanchi
15 ,
Taha Merghoub
16
,
17
,
18
,
19 ,
Etienne Meylan
20
,
21 ,
Vivek Mittal
22
,
23 ,
Mikael J. Pittet
24
,
25
,
26
,
27 ,
Andrea Rubio-Ponce
11 ,
Irina A. Udalova
28 ,
Timo K. van den Berg
29
,
30 ,
Denisa D. Wagner
31 ,
Ping Wang
3 ,
Arturo Zychlinsky
32 ,
Karin E. de Visser
33
,
34
,
37 ,
Mikala Egeblad
35
,
37 ,
Paul Kubes
36
,
37
,
38
,
39
Publication date (Electronic):
06 May 2022
Journal:
The Journal of Experimental Medicine
Publisher:
Rockefeller University Press
Read this article at
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Abstract
There is a growing appreciation for the vastness of neutrophil functional states in cancer. Quail et al. provide a consensus statement on mechanisms governing neutrophil heterogeneity in the context of malignancy and discuss controversies and solutions in neutrophil research.
Abstract
Neutrophils are the first responders to infection and inflammation and are thus a critical component of innate immune defense. Understanding the behavior of neutrophils as they act within various inflammatory contexts has provided insights into their role in sterile and infectious diseases; however, the field of neutrophils in cancer is comparatively young. Here, we summarize key concepts and current knowledge gaps related to the diverse roles of neutrophils throughout cancer progression. We discuss sources of neutrophil heterogeneity in cancer and provide recommendations on nomenclature for neutrophil states that are distinct in maturation and activation. We address discrepancies in the literature that highlight a need for technical standards that ought to be considered between laboratories. Finally, we review emerging questions in neutrophil biology and innate immunity in cancer. Overall, we emphasize that neutrophils are a more diverse population than previously appreciated and that their role in cancer may present novel unexplored opportunities to treat cancer.
Related collections
Most cited references302
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- Abstract: found
- Article: found
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Carlos López-Otín, Maria Blasco, Linda Partridge … (2014)
Aging is characterized by a progressive loss of physiological integrity, leading to impaired function and increased vulnerability to death. This deterioration is the primary risk factor for major human pathologies, including cancer, diabetes, cardiovascular disorders, and neurodegenerative diseases. Aging research has experienced an unprecedented advance over recent years, particularly with the discovery that the rate of aging is controlled, at least to some extent, by genetic pathways and biochemical processes conserved in evolution. This Review enumerates nine tentative hallmarks that represent common denominators of aging in different organisms, with special emphasis on mammalian aging. These hallmarks are: genomic instability, telomere attrition, epigenetic alterations, loss of proteostasis, deregulated nutrient sensing, mitochondrial dysfunction, cellular senescence, stem cell exhaustion, and altered intercellular communication. A major challenge is to dissect the interconnectedness between the candidate hallmarks and their relative contributions to aging, with the final goal of identifying pharmaceutical targets to improve human health during aging, with minimal side effects. Copyright © 2013 Elsevier Inc. All rights reserved.
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Neutrophils engulf and kill bacteria when their antimicrobial granules fuse with the phagosome. Here, we describe that, upon activation, neutrophils release granule proteins and chromatin that together form extracellular fibers that bind Gram-positive and -negative bacteria. These neutrophil extracellular traps (NETs) degrade virulence factors and kill bacteria. NETs are abundant in vivo in experimental dysentery and spontaneous human appendicitis, two examples of acute inflammation. NETs appear to be a form of innate response that binds microorganisms, prevents them from spreading, and ensures a high local concentration of antimicrobial agents to degrade virulence factors and kill bacteria.
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Gut microbiome influences efficacy of PD-1–based immunotherapy against epithelial tumors
Bo Qu, Gladys Ferrere, Céline Clemenson … (2018)
Immune checkpoint inhibitors (ICI) targeting the PD-1/PD-L1 axis induce sustained clinical responses in a sizeable minority of cancer patients. Here, we show that primary resistance to ICI can be due to abnormal gut microbiome composition. Antibiotics (ATB) inhibited the clinical benefit of ICI in patients with advanced cancer. Fecal microbiota transplantation (FMT) from cancer patients who responded to ICI (but not from non-responding patients) into germ-free or ATB-treated mice ameliorated the antitumor effects of PD-1 blockade. Metagenomics of patient stools at diagnosis revealed correlations between clinical responses to ICI and the relative abundance of Akkermansia muciniphila. Oral supplementation with A. muciniphila post-FMT with non-responder feces restored the efficacy of PD-1 blockade in an IL-12-dependent manner, by increasing the recruitment of CCR9+CXCR3+CD4+ T lymphocytes into tumor beds.
Author and article information
Contributors
Daniela F. Quail:
ORCID: https://orcid.org/0000-0002-6969-3250
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Borko Amulic:
ORCID: https://orcid.org/0000-0002-8518-8393
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Monowar Aziz:
ORCID: https://orcid.org/0000-0002-8195-4505
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Betsy J. Barnes:
ORCID: https://orcid.org/0000-0001-6766-4352
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Evgeniy Eruslanov:
ORCID: https://orcid.org/0000-0003-0743-5026
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Zvi G. Fridlender:
ORCID: https://orcid.org/0000-0002-6122-1988
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Helen S. Goodridge:
ORCID: https://orcid.org/0000-0001-8097-2413
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Zvi Granot:
ORCID: https://orcid.org/0000-0001-9692-5785
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Andrés Hidalgo:
ORCID: https://orcid.org/0000-0001-5513-555X
Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: SupervisionRole:
Writing - original draftRole: Writing - review & editing
Anna Huttenlocher:
ORCID: https://orcid.org/0000-0001-7940-6254
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Mariana J. Kaplan:
ORCID: https://orcid.org/0000-0003-2968-0815
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Ilaria Malanchi:
ORCID: https://orcid.org/0000-0003-4867-3311
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Taha Merghoub:
ORCID: https://orcid.org/0000-0002-1518-5111
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Etienne Meylan:
ORCID: https://orcid.org/0000-0002-0899-2230
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Vivek Mittal:
ORCID: https://orcid.org/0000-0002-4764-7413
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Mikael J. Pittet:
ORCID: https://orcid.org/0000-0002-2060-4691
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Andrea Rubio-Ponce:
ORCID: https://orcid.org/0000-0002-4275-8835
Role: Formal analysisRole: Visualization
Irina A. Udalova:
ORCID: https://orcid.org/0000-0002-6716-2528
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Timo K. van den Berg:
ORCID: https://orcid.org/0000-0002-2052-3904
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Denisa D. Wagner:
ORCID: https://orcid.org/0000-0002-4494-413X
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Ping Wang:
ORCID: https://orcid.org/0000-0002-1557-0394
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Arturo Zychlinsky:
ORCID: https://orcid.org/0000-0001-6018-193X
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Karin E. de Visser:
ORCID: https://orcid.org/0000-0002-0293-868X
Role: ConceptualizationRole: Funding acquisitionRole: upervisionRole: Writing - original
draftRole: Writing - review & editing
Mikala Egeblad:
ORCID: https://orcid.org/0000-0002-3371-1445
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Paul Kubes:
ORCID: https://orcid.org/0000-0002-2835-4244
Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing - original
draftRole: Writing - review & editing
Journal
Journal ID (nlm-ta): J Exp Med
Journal ID (iso-abbrev): J Exp Med
Journal ID (publisher-id): jem
Title:
The Journal of Experimental Medicine
Publisher:
Rockefeller University Press
ISSN
(Print):
0022-1007
ISSN
(Electronic):
1540-9538
Publication date Collection: 06
June
2022
Publication date
(Electronic):
06
May
2022
Publication date PMC-release: 06
May
2022
Volume: 219
Issue: 6
Electronic Location Identifier: e20220011
Affiliations
[1
]
Rosalind and Morris Goodman Cancer Institute, Department of Physiology, McGill University,
Montreal, Quebec, Canada
[3
]
Center for Immunology and Inflammation, Feinstein Institutes for Medical Research,
Manhasset, NY
[4
]
Center for Autoimmune, Musculoskeletal and Hematopoietic Diseases, Feinstein Institutes
for Medical Research, Manhasset, NY
[5
]Departments of Molecular Medicine and Pediatrics, Donald and Barbara Zucker School
of Medicine at Hofstra/Northwell, Hempstead, NY
[6
]
Division of Thoracic Surgery, Department of Surgery, Perelman School of Medicine at
the University of Pennsylvania, Philadelphia, PA
[7
]
Hadassah Medical Center, Institute of Pulmonary Medicine, Faculty of Medicine, Hebrew
University of Jerusalem, Jerusalem, Israel
[8
]
Board of Governors Regenerative Medicine Institute and Research Division of Immunology,
Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, CA
[9
]
Department of Developmental Biology and Cancer Research, Hebrew University of Jerusalem,
Jerusalem, Israel
[10
]
Vascular Biology and Therapeutics Program and Department of Immunobiology, Yale University
School of Medicine, New Haven, CT
[11
]
Area of Cell and Developmental Biology, Centro Nacional de Investigaciones Cardiovasculares
Carlos III, Madrid, Spain
[12
]
Department of Medical Microbiology and Immunology, University of Wisconsin-Madison,
Madison, WI
[14
]
Systemic Autoimmunity Branch, Intramural Research Program, National Institute of Arthritis
and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD
[16
]
Ludwig Collaborative and Swim Across America Laboratory, Memorial Sloan Kettering
Cancer Center, New York, NY
[17
]
Parker Institute for Cancer Immunotherapy, Memorial Sloan Kettering Cancer Center,
New York, NY
[20
]
Lung Cancer and Immuno-Oncology Laboratory, Bordet Cancer Research Laboratories, Institut
Jules Bordet, Université Libre de Bruxelles, Anderlecht, Belgium
[22
]
Department of Cardiothoracic Surgery, Neuberger Berman Foundation Lung Cancer Research
Center, Weill Cornell Medicine, New York, NY
[30
]
Department of Molecular Cell Biology and Immunology, Amsterdam University Medical
Center, Amsterdam, Netherlands
[31
]
Program in Cellular and Molecular Medicine, Division of Hematology/Oncology, Boston
Children’s Hospital and Harvard Medical School, Boston, MA
[32
]
Department of Cellular Microbiology, Max Planck Institute for Infection Biology, Berlin,
Germany
[33
]
Division of Tumour Biology and Immunology, Oncode Institute, Netherlands Cancer Institute,
Amsterdam, Netherlands
[34
]
Department of Immunohematology and Blood Transfusion, Leiden University Medical Centre,
Leiden, Netherlands
[36
]
Department of Pharmacology and Physiology, Cumming School of Medicine, University
of Calgary, Calgary, Alberta, Canada
[37
]Banbury Center meeting organizers, Diverse Functions of Neutrophils in Cancer, Cold
Spring Harbor Laboratory, New York, NY
Author notes
Correspondence to Daniela F. Quail:
daniela.quail@
123456mcgill.ca
Disclosures: E. Eruslanov reported a patent to the use of HLA-DR+CD32hiCD64hi hybrid neutrophils with characteristics of antigen-presenting cells to augment therapy for cancer or infectious diseases pending. Z.G. Fridlender reported “other” from Immunyx outside the submitted work; in addition, Z.G. Fridlender had a patent to ID - 6494-1 licensed "Immunyx." Z. Granot reported personal fees from Immunyx Pharma outside the submitted work. A. Hidalgo is a paid consultant for Flagship Pioneering, which is not related to this work. M.J. Pittet reported personal fees from AstraZeneca, Debiopharm, Elstar Therapeutics, ImmuneOncia, KSQ Therapeutics, MaxiVax, Merck, Molecular Partners, Third Rock Ventures, and Tidal outside the submitted work; in addition, M.J. Pittet has been a consultant for Aileron Therapeutics, Cygnal Therapeutics, and Siamab Therapeutics. T.K van den Berg is an inventor on patent application WO2009/131453 A1, owned by Sanquin Blood Supply Organization, licensed to Byondis BV, related to the targeting of CD47-SIRPα in cancer. D.D. Wagner reported personal fees from Takeda Pharmaceutical and “other” from Neutrolis, SAB during the conduct of the study. K.E. de Visser reported grants from Roche/Genentech and personal fees from Macomics outside the submitted work. M. Egeblad is a member of the research advisory board for brensocatib for Insmed, Inc, a member of the scientific advisory board for Vividion Therapeutics, Inc., and a consultant for Protalix, Inc outside the submitted work. T. Merghoub is a co-founder and holds equity in IMVAQ Therapeutics. He is a consultant of Immunos Therapeutics, ImmunoGenesis, and Pfizer. In addition, T Merghoub has research support from Bristol-Myers Squibb, Surface Oncology, Kyn Therapeutics, Infinity Pharmaceuticals Inc., Peregrine Pharmaceuticals Inc., Adaptive Biotechnologies, Leap Therapeutics Inc., and Aprea. He has patents on applications related to work on oncolytic viral therapy, α-virus-based vaccine, neo antigen modeling, CD40, GITR, OX40, PD-1, and CTLA-4. No other disclosures were reported.
Author information
Daniela F. Quail
https://orcid.org/0000-0002-6969-3250
Borko Amulic
https://orcid.org/0000-0002-8518-8393
Monowar Aziz
https://orcid.org/0000-0002-8195-4505
Betsy J. Barnes
https://orcid.org/0000-0001-6766-4352
Evgeniy Eruslanov
https://orcid.org/0000-0003-0743-5026
Zvi G. Fridlender
https://orcid.org/0000-0002-6122-1988
Helen S. Goodridge
https://orcid.org/0000-0001-8097-2413
Zvi Granot
https://orcid.org/0000-0001-9692-5785
Andrés Hidalgo
https://orcid.org/0000-0001-5513-555X
Anna Huttenlocher
https://orcid.org/0000-0001-7940-6254
Mariana J. Kaplan
https://orcid.org/0000-0003-2968-0815
Ilaria Malanchi
https://orcid.org/0000-0003-4867-3311
Taha Merghoub
https://orcid.org/0000-0002-1518-5111
Etienne Meylan
https://orcid.org/0000-0002-0899-2230
Vivek Mittal
https://orcid.org/0000-0002-4764-7413
Mikael J. Pittet
https://orcid.org/0000-0002-2060-4691
Andrea Rubio-Ponce
https://orcid.org/0000-0002-4275-8835
Irina A. Udalova
https://orcid.org/0000-0002-6716-2528
Timo K. van den Berg
https://orcid.org/0000-0002-2052-3904
Denisa D. Wagner
https://orcid.org/0000-0002-4494-413X
Ping Wang
https://orcid.org/0000-0002-1557-0394
Arturo Zychlinsky
https://orcid.org/0000-0001-6018-193X
Karin E. de Visser
https://orcid.org/0000-0002-0293-868X
Mikala Egeblad
https://orcid.org/0000-0002-3371-1445
Paul Kubes
https://orcid.org/0000-0002-2835-4244
Article
Publisher ID: jem.20220011DOI: 10.1084/jem.20220011
PMC ID: 9086501
PubMed ID: 35522219
SO-VID: f9843c13-0c06-4c6b-a2c5-8b3e151a715f
Copyright © © 2022 Quail et al.
License:
This article is available under a Creative Commons License (Attribution 4.0 International, as described at https://creativecommons.org/licenses/by/4.0/).
History
Date
received
: 23
December
2021
Date
revision received
: 11
March
2022
Date
accepted
: 23
March
2022
Funding
Funded by:
Cold Spring Harbor Laboratory, DOI http://dx.doi.org/10.13039/100013356;
Funded by:
Canadian Institutes of Health Research, DOI http://dx.doi.org/10.13039/501100000024;
Award ID: PJT-159742
Award ID: PJT-178306
Funded by:
Terry Fox Research Institute, DOI http://dx.doi.org/10.13039/501100004376;
Funded by:
Canada Research Chair, DOI http://dx.doi.org/10.13039/501100001804;
Funded by:
Medical Research Council, DOI http://dx.doi.org/10.13039/501100000265;
Award ID: MR/R02149x/1
Funded by:
National Institutes of Health, DOI http://dx.doi.org/10.13039/100000002;
Award ID: R01GM129633
Award ID: P01CA240239
Award ID: R01CA218579
Award ID: P30 CA008748
Funded by:
National Institute of Arthritis and Musculoskeletal and Skin Diseases, DOI http://dx.doi.org/10.13039/100000069;
Award ID: AR065959-01
Award ID: ZIAAR041199
Funded by:
Department of Defense, DOI http://dx.doi.org/10.13039/100000005;
Award ID: W81XWH-18-1-0674
Award ID: W81XWH-15-1-0717
Award ID: W81XWH2010753
Funded by:
National Cancer Institute, DOI http://dx.doi.org/10.13039/100000054;
Award ID: R01CA187392
Award ID: R01 CA056821
Funded by:
Israel Science Foundation, DOI http://dx.doi.org/10.13039/501100003977;
Award ID: 1708/20
Award ID: 405/18
Funded by:
Sasson and Luisa Naor Fund;
Funded by:
National Institute of Allergy and Infectious Diseases, DOI http://dx.doi.org/10.13039/100000060;
Award ID: R01AI134987
Funded by:
Israel Cancer Research Fund, DOI http://dx.doi.org/10.13039/100001698;
Funded by:
Deutsche Forschungsgemeinschaft, DOI http://dx.doi.org/10.13039/501100001659;
Funded by:
Rosetrees Trust, DOI http://dx.doi.org/10.13039/501100000833;
Funded by:
European Commission, DOI http://dx.doi.org/10.13039/501100000780;
Award ID: 861878
Funded by:
Centro Nacional de Investigaciones Cardiovasculares, DOI http://dx.doi.org/10.13039/501100005884;
Funded by:
Pro-CNIC Foundation;
Funded by:
European Research Council, DOI http://dx.doi.org/10.13039/100010663;
Award ID: ERC CoG-H2020-725492
Funded by:
Francis Crick Institute, DOI http://dx.doi.org/10.13039/100010438;
Funded by:
Cancer Research UK, DOI http://dx.doi.org/10.13039/501100000289;
Award ID: FC001112
Funded by:
UK Medical Research Council, DOI http://dx.doi.org/10.13039/501100000265;
Award ID: FC001112
Funded by:
Wellcome Trust, DOI http://dx.doi.org/10.13039/100010269;
Award ID: FC001112
Award ID: 209422/Z/17/Z
Funded by:
Swim Across America, DOI http://dx.doi.org/10.13039/100016947;
Funded by:
Ludwig Institute for Cancer Research, DOI http://dx.doi.org/10.13039/100009729;
Award ID: P01CA240239
Award ID: R01CA218579
Funded by:
Ludwig Institute for Cancer Immunotherapy;
Funded by:
Memorial Sloan Kettering Cancer Research Institute;
Funded by:
Parker Institute for Cancer Immunotherapy, DOI http://dx.doi.org/10.13039/100014547;
Funded by:
Swiss National Science Foundation;
Award ID: 310030_179324
Funded by:
Fonds de la Recherche Scientifique, DOI http://dx.doi.org/10.13039/501100002661;
Award ID: MISU F.6003.22
Funded by:
Ludwig Cancer Research, DOI http://dx.doi.org/10.13039/501100017035;
Funded by:
Byondis BV;
Funded by:
Dutch Ministry of Health;
Funded by:
The Dutch Cancer Society, DOI http://dx.doi.org/10.13039/501100004622;
Award ID: 10300
Award ID: KWF10623
Award ID: KWF10083
Award ID: KWF13191
Funded by:
National Health, Lung and Blood Institute, DOI http://dx.doi.org/10.13039/100000050;
Award ID: R35HL135765
Funded by:
National Institute of General Medical Sciences, DOI http://dx.doi.org/10.13039/100000057;
Award ID: R35GM118337
Funded by:
Max Planck Society, DOI http://dx.doi.org/10.13039/501100004189;
Funded by:
Oncode Institute, DOI http://dx.doi.org/10.13039/501100021821;
Funded by:
Ministerio de Ciencia e Innovación, DOI http://dx.doi.org/10.13039/501100004837;
Funded by:
Institut Suisse de Recherche Expérimentale sur le Cancer;
Funded by:
Netherlands Organization for Scientific Research;
Award ID: NWO-VICI 91819616
Categories
Subject:
Review
Subject:
Innate immunity and inflammation
Subject:
Tumor immunology
Subject:
Cancer Focus
Series title:
Cancer Focus
ScienceOpen disciplines: Medicine
Data availability:
ScienceOpen disciplines: Medicine