Obesity alters the lung myeloid cell landscape to enhance breast cancer metastasis through IL5 and GM-CSF

Obesity is associated with chronic, low-grade inflammation, which can disrupt homeostasis within tissue microenvironments. Given the correlation between obesity and relative risk of death from cancer, we investigated whether obesity-associated inflammation promotes metastatic progression. We demonst...

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Published inNature cell biology Vol. 19; no. 8; pp. 974 - 987
Main Authors Quail, Daniela F., Olson, Oakley C., Bhardwaj, Priya, Walsh, Logan A., Akkari, Leila, Quick, Marsha L., Chen, I-Chun, Wendel, Nils, Ben-Chetrit, Nir, Walker, Jeanne, Holt, Peter R., Dannenberg, Andrew J., Joyce, Johanna A.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.08.2017
Nature Publishing Group
Subjects
13/1
13/106
13/31
13/51
14/1
14/5
14/63
38/77
59/5
631/443/319/1642/393
631/67
631/67/322
631/67/327
64/60
82
82/79
Adiposity
Adoptive Transfer
Animal models
Animals
Body weight loss
Breast cancer
Breast Neoplasms - genetics
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Cancer
Cancer Research
Cell Biology
Cell Line, Tumor
Coculture Techniques
Complications and side effects
Development and progression
Developmental Biology
Diet, Fat-Restricted
Disease Models, Animal
Disease Progression
Female
Gene Expression Regulation, Neoplastic
Granulocyte colony-stimulating factor
Granulocyte-macrophage colony-stimulating factor
Granulocyte-Macrophage Colony-Stimulating Factor - blood
Granulocyte-Macrophage Colony-Stimulating Factor - metabolism
Health aspects
Homeostasis
Interleukin 5
Interleukin-5 - blood
Interleukin-5 - metabolism
Leukocytes (neutrophilic)
Life Sciences
Lung - metabolism
Lung - pathology
Lung Neoplasms - genetics
Lung Neoplasms - metabolism
Lung Neoplasms - prevention & control
Lung Neoplasms - secondary
Lungs
Metastases
Metastasis
Mice, Inbred BALB C
Mice, Inbred C57BL
Mice, Inbred NOD
Mice, SCID
Mice, Transgenic
Microenvironments
Neutrophil Infiltration
Neutrophilia
Neutrophils - metabolism
Neutrophils - pathology
Neutrophils - transplantation
Obesity
Obesity - complications
Obesity - diet therapy
Obesity - metabolism
Obesity - pathology
Physiological aspects
Pneumonia - etiology
Pneumonia - metabolism
Pneumonia - pathology
Pneumonia - prevention & control
Serum levels
Signal Transduction
Stem Cells
Time Factors
Tumor Microenvironment
Tumors
Weight control
Weight Loss
Weight reduction
United States
Online AccessGet full text

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Abstract Obesity is associated with chronic, low-grade inflammation, which can disrupt homeostasis within tissue microenvironments. Given the correlation between obesity and relative risk of death from cancer, we investigated whether obesity-associated inflammation promotes metastatic progression. We demonstrate that obesity causes lung neutrophilia in otherwise normal mice, which is further exacerbated by the presence of a primary tumour. The increase in lung neutrophils translates to increased breast cancer metastasis to this site, in a GM-CSF- and IL5-dependent manner. Importantly, weight loss is sufficient to reverse this effect, and reduce serum levels of GM-CSF and IL5 in both mouse models and humans. Our data indicate that special consideration of the obese patient population is critical for effective management of cancer progression. Joyce and colleagues report that obesity promotes lung neutrophilia in mice, which in the presence of a primary breast tumour fosters metastasis to the lung in a manner dependent on GM-CSF and IL5.
AbstractList Obesity is associated with chronic, low-grade inflammation, which can disrupt homeostasis within tissue microenvironments. Given the correlation between obesity and relative risk of death from cancer, we investigated whether obesity-associated inflammation promotes metastatic progression. We demonstrate that obesity causes lung neutrophilia in otherwise normal mice, which is further exacerbated by the presence of a primary tumour. The increase in lung neutrophils translates to increased breast cancer metastasis to this site, in a GM-CSF- and IL5-dependent manner. Importantly, weight loss is sufficient to reverse this effect, and reduce serum levels of GM-CSF and IL5 in both mouse models and humans. Our data indicate that special consideration of the obese patient population is critical for effective management of cancer progression.
Obesity is associated with chronic, low-grade inflammation, which can disrupt homeostasis within tissue microenvironments. Given the correlation between obesity and relative risk of death from cancer, we investigated whether obesity-associated inflammation promotes metastatic progression. We demonstrate that obesity causes lung neutrophilia in otherwise normal mice, which is further exacerbated by the presence of a primary tumour. The increase in lung neutrophils translates to increased breast cancer metastasis to this site, in a GM-CSF- and IL5-dependent manner. Importantly, weight loss is sufficient to reverse this effect, and reduce serum levels of GM-CSF and IL5 in both mouse models and humans. Our data indicate that special consideration of the obese patient population is critical for effective management of cancer progression. Joyce and colleagues report that obesity promotes lung neutrophilia in mice, which in the presence of a primary breast tumour fosters metastasis to the lung in a manner dependent on GM-CSF and IL5.
Obesity is associated with chronic, low-grade inflammation, which can disrupt homeostasis within tissue microenvironments. Given the correlation between obesity and relative risk of death from cancer, we investigated whether obesity-associated inflammation promotes metastatic progression. We demonstrate that obesity causes lung neutrophilia in otherwise normal mice, which is further exacerbated by the presence of a primary tumour. The increase in lung neutrophils translates to increased breast cancer metastasis to this site, in a GM-CSF- and IL5-dependent manner. Importantly, weight loss is sufficient to reverse this effect, and reduce serum levels of GM-CSF and IL5 in both mouse models and humans. Our data indicate that special consideration of the obese patient population is critical for effective management of cancer progression.Obesity is associated with chronic, low-grade inflammation, which can disrupt homeostasis within tissue microenvironments. Given the correlation between obesity and relative risk of death from cancer, we investigated whether obesity-associated inflammation promotes metastatic progression. We demonstrate that obesity causes lung neutrophilia in otherwise normal mice, which is further exacerbated by the presence of a primary tumour. The increase in lung neutrophils translates to increased breast cancer metastasis to this site, in a GM-CSF- and IL5-dependent manner. Importantly, weight loss is sufficient to reverse this effect, and reduce serum levels of GM-CSF and IL5 in both mouse models and humans. Our data indicate that special consideration of the obese patient population is critical for effective management of cancer progression.
Obesity is associated with chronic, low-grade inflammation, which can disrupt homeostasis within tissue microenvironments. Given the correlation between obesity and relative risk of death from cancer, we investigated whether obesity-associated inflammation promotes metastatic progression. We demonstrate that obesity causes lung neutrophilia in otherwise normal mice, which is further exacerbated by the presence of a primary tumour. The increase in lung neutrophils translates to increased breast cancer metastasis to this site, in a GM-CSF- and IL5-dependent manner. Importantly, weight loss is sufficient to reverse this effect, and reduce serum levels of GM-CSF and IL5 in both mouse models and humans. Our data indicate that special consideration of the obese patient population is critical for effective management of cancer progression. Joyce and colleagues report that obesity promotes lung neutrophilia in mice, which in the presence of a primary breast tumour fosters metastasis to the lung in a manner dependent on GM-CSF and IL5.
Audience Academic
Author Joyce, Johanna A.
Holt, Peter R.
Chen, I-Chun
Olson, Oakley C.
Bhardwaj, Priya
Dannenberg, Andrew J.
Quick, Marsha L.
Akkari, Leila
Walker, Jeanne
Walsh, Logan A.
Wendel, Nils
Ben-Chetrit, Nir
Quail, Daniela F.
AuthorAffiliation 4 Ludwig Institute for Cancer Research, Lausanne 1066, Switzerland
1 Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, USA
7 These authors contributed equally to this work
6 Laboratory of Biochemical Genetics and Metabolism, The Rockefeller University, New York, New York 10065, USA
5 Department of Oncology, University of Lausanne, Lausanne 1066, Switzerland
2 Department of Medicine, Weill Cornell Medical College, New York, New York 10065, USA
3 Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, USA
AuthorAffiliation_xml – name: 2 Department of Medicine, Weill Cornell Medical College, New York, New York 10065, USA
– name: 3 Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, USA
– name: 4 Ludwig Institute for Cancer Research, Lausanne 1066, Switzerland
– name: 5 Department of Oncology, University of Lausanne, Lausanne 1066, Switzerland
– name: 1 Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, USA
– name: 6 Laboratory of Biochemical Genetics and Metabolism, The Rockefeller University, New York, New York 10065, USA
– name: 7 These authors contributed equally to this work
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  givenname: Daniela F.
  surname: Quail
  fullname: Quail, Daniela F.
  organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center
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  surname: Quick
  fullname: Quick, Marsha L.
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  surname: Wendel
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  organization: Department of Medicine, Weill Cornell Medical College
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  surname: Ben-Chetrit
  fullname: Ben-Chetrit, Nir
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– sequence: 10
  givenname: Jeanne
  surname: Walker
  fullname: Walker, Jeanne
  organization: Laboratory of Biochemical Genetics and Metabolism, The Rockefeller University
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  surname: Holt
  fullname: Holt, Peter R.
  organization: Laboratory of Biochemical Genetics and Metabolism, The Rockefeller University
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  orcidid: 0000-0002-6332-2598
  surname: Joyce
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  email: johanna@joycelab.org
  organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, Ludwig Institute for Cancer Research, Department of Oncology, University of Lausanne
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28737771$$D View this record in MEDLINE/PubMed
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AUTHOR CONTRIBUTIONS
D.F.Q., O.C.O. and J.A.J. conceived the study, designed and interpreted experiments, and wrote the manuscript. D.F.Q., O.C.O., P.B., L.A.W., L.A., M.L.Q., I.-C.C., N.W. and N.B.-C. performed experiments and analysed results. J.W., P.R.H. and A.J.D. provided human sera and blood, and A.J.D. helped design and interpret experiments. J.A.J. supervised the study. All authors commented on the manuscript.
ORCID 0000-0002-6332-2598
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Snippet Obesity is associated with chronic, low-grade inflammation, which can disrupt homeostasis within tissue microenvironments. Given the correlation between...
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Adiposity
Adoptive Transfer
Animal models
Animals
Body weight loss
Breast cancer
Breast Neoplasms - genetics
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Cancer
Cancer Research
Cell Biology
Cell Line, Tumor
Coculture Techniques
Complications and side effects
Development and progression
Developmental Biology
Diet, Fat-Restricted
Disease Models, Animal
Disease Progression
Female
Gene Expression Regulation, Neoplastic
Granulocyte colony-stimulating factor
Granulocyte-macrophage colony-stimulating factor
Granulocyte-Macrophage Colony-Stimulating Factor - blood
Granulocyte-Macrophage Colony-Stimulating Factor - metabolism
Health aspects
Homeostasis
Interleukin 5
Interleukin-5 - blood
Interleukin-5 - metabolism
Leukocytes (neutrophilic)
Life Sciences
Lung - metabolism
Lung - pathology
Lung Neoplasms - genetics
Lung Neoplasms - metabolism
Lung Neoplasms - prevention & control
Lung Neoplasms - secondary
Lungs
Metastases
Metastasis
Mice, Inbred BALB C
Mice, Inbred C57BL
Mice, Inbred NOD
Mice, SCID
Mice, Transgenic
Microenvironments
Neutrophil Infiltration
Neutrophilia
Neutrophils - metabolism
Neutrophils - pathology
Neutrophils - transplantation
Obesity
Obesity - complications
Obesity - diet therapy
Obesity - metabolism
Obesity - pathology
Physiological aspects
Pneumonia - etiology
Pneumonia - metabolism
Pneumonia - pathology
Pneumonia - prevention & control
Serum levels
Signal Transduction
Stem Cells
Time Factors
Tumor Microenvironment
Tumors
Weight control
Weight Loss
Weight reduction
Title Obesity alters the lung myeloid cell landscape to enhance breast cancer metastasis through IL5 and GM-CSF
URI https://link.springer.com/article/10.1038/ncb3578
https://www.ncbi.nlm.nih.gov/pubmed/28737771
https://www.proquest.com/docview/1946517269
https://www.proquest.com/docview/1923107262
https://pubmed.ncbi.nlm.nih.gov/PMC6759922
Volume 19
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