Chronic exposure to carbon black ultrafine particles reprograms macrophage metabolism and accelerates lung cancer

Chronic exposure to airborne carbon black ultrafine (nCB) particles generated from incomplete combustion of organic matter drives IL-17A–dependent emphysema. However, whether and how they alter the immune responses to lung cancer remains unknown. Here, we show that exposure to nCB particles increased PD-L1
+
PD-L2
+
CD206
+
antigen-presenting cells (APCs), exhausted T cells, and T
reg
cells. Lung macrophages that harbored nCB particles showed selective mitochondrial structure damage and decreased oxidative respiration. Lung macrophages sustained the HIF1α axis that increased glycolysis and lactate production, culminating in an immunosuppressive microenvironment in multiple mouse models of non–small cell lung cancers. Adoptive transfer of lung APCs from nCB-exposed wild type to susceptible mice increased tumor incidence and caused early metastasis. Our findings show that nCB exposure metabolically rewires lung macrophages to promote immunosuppression and accelerates the development of lung cancer.

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Details

Published: Nov 16, 2022
Vol/Issue: 8(46)

Authors

C

Cheng-Yen Chang

Translational Biology and Molecular Medicine Program, Baylor College of Medicine, Houston, TX 77030, USA.; Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.

R

Ran You

Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.; Immunology and Microbiology Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA.

D

Dominique Armstrong

Translational Biology and Molecular Medicine Program, Baylor College of Medicine, Houston, TX 77030, USA.; Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.

A

Ashwini Bandi

Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.

Y

Yi-Ting Cheng

Developmental Biology Program, Baylor College of Medicine, Houston, TX 77030, USA.; Center for Cell and Gene Therapy, Baylor College of Medicine, Houston, TX 77030, USA.

P

Philip M. Burkhardt

Immunology and Microbiology Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA.

L

Luis Becerra-Dominguez

Immunology and Microbiology Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA.

M

Matthew C. Madison

Translational Biology and Molecular Medicine Program, Baylor College of Medicine, Houston, TX 77030, USA.; Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.

H

Hui-Ying Tung

Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.; Immunology and Microbiology Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA.

Z

Zhimin Zeng

Departments of Pathology and Immunology, Baylor College of Medicine, Houston, TX 77030, USA.

L

Lizhen Song

Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.

P

Patricia E. Phillips

Cytometry and Cell Sorting Core, Baylor College of Medicine, Houston TX 77030, USA.

P

Paul Porter

Cytometry and Cell Sorting Core, Baylor College of Medicine, Houston TX 77030, USA.

J

John M. Knight

Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.

N

Nagireddy Putluri

Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA.; Dan L. Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA.

X

Xiaoyi Yuan

Department of Anesthesiology, University of Texas Health Science Center at Houston, McGovern Medical School, Houston, TX 77030, USA.

D

Daniela C. Marcano

Department of Chemistry and Smalley-Curl Institute, NanoCarbon Center, The Welch Institute for Advanced Materials, and Department of Materials Science and NanoEngineering, Rice University, Houston, TX 77005 USA.

E

Emily A. McHugh

Department of Chemistry and Smalley-Curl Institute, NanoCarbon Center, The Welch Institute for Advanced Materials, and Department of Materials Science and NanoEngineering, Rice University, Houston, TX 77005 USA.

J

James M. Tour

Department of Chemistry and Smalley-Curl Institute, NanoCarbon Center, The Welch Institute for Advanced Materials, and Department of Materials Science and NanoEngineering, Rice University, Houston, TX 77005 USA.

A

Andre Catic

Translational Biology and Molecular Medicine Program, Baylor College of Medicine, Houston, TX 77030, USA.; Immunology and Microbiology Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA.; Developmental Biology Program, Baylor College of Medicine, Houston, TX 77030, USA.; Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA.; Dan L. Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA.

L

Laure Maneix

Center for Cell and Gene Therapy, Baylor College of Medicine, Houston, TX 77030, USA.; Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA.; Dan L. Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA.; Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA.

B

Bryan M. Burt

Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.; Dan L. Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA.; Division of Thoracic Surgery, Baylor College of Medicine, Houston, TX 77030, USA.

H

Hyun-Sung Lee

Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.; Dan L. Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA.; Division of Thoracic Surgery, Baylor College of Medicine, Houston, TX 77030, USA.

D

David B. Corry

Translational Biology and Molecular Medicine Program, Baylor College of Medicine, Houston, TX 77030, USA.; Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.; Immunology and Microbiology Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA.; Departments of Pathology and Immunology, Baylor College of Medicine, Houston, TX 77030, USA.; Biology of Inflammation Center, Baylor College of Medicine, Houston, TX 77030, USA.

F

Farrah Kheradmand

Translational Biology and Molecular Medicine Program, Baylor College of Medicine, Houston, TX 77030, USA.; Department of Medicine, Baylor College of Medicine, Houston, TX 77030, USA.; Immunology and Microbiology Graduate Program, Baylor College of Medicine, Houston, TX 77030, USA.; Departments of Pathology and Immunology, Baylor College of Medicine, Houston, TX 77030, USA.; Biology of Inflammation Center, Baylor College of Medicine, Houston, TX 77030, USA.

Cite This Article

Cheng-Yen Chang, Ran You, Dominique Armstrong, et al. (2022). Chronic exposure to carbon black ultrafine particles reprograms macrophage metabolism and accelerates lung cancer. Science Advances, 8(46). https://doi.org/10.1126/sciadv.abq0615

Chronic exposure to carbon black ultrafine particles reprograms macrophage metabolism and accelerates lung cancer

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