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ResearchIn-Press PreviewMetabolismPulmonology Open Access | 10.1172/jci.insight.158100

microRNA-33 deficiency in macrophages enhances autophagy, improves mitochondrial homeostasis, and protects against lung fibrosis

Farida Ahangari,1 Nathan L. Price,2 Shipra Malik,3 Maurizio Chioccioli,1 Thomas Bärnthaler,1 Taylor S. Adams,1 Jooyoung Kim,1 Sai Pallavi Pradeep,3 Shuizi Ding,1 Carlos Cosme Jr,1 Kadi-Ann S. Rose,1 John E. McDonough,4 Nachelle R. Aurelien,1 Gabriel Ibarra,1 Norihito Omote,1 Jonas C. Schupp,1 Giuseppe DeIuliis,1 Julian A. Villalba Nunez,5 Lokesh Sharma,1 Changwan Ryu,1 Charles S. Dela Cruz,1 Xinran Liu,6 Antje Prasse,7 Ivan Rosas,8 Raman Bahal,3 Carlos Fernandez-Hernando,2 and Naftali Kaminski1

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Ahangari, F. in: JCI | PubMed | Google Scholar |

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Price, N. in: JCI | PubMed | Google Scholar |

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Malik, S. in: JCI | PubMed | Google Scholar

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Chioccioli, M. in: JCI | PubMed | Google Scholar |

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Bärnthaler, T. in: JCI | PubMed | Google Scholar

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Kim, J. in: JCI | PubMed | Google Scholar

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Aurelien, N. in: JCI | PubMed | Google Scholar

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

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1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Fernandez-Hernando, C. in: JCI | PubMed | Google Scholar |

1Section of Pulmonary, Critical Care and Sleep Medicine, Yale University School of Medicine, New Haven, United States of America

2Department of Comparative Medicine, Yale University School of Medicine, New Haven, United States of America

3Department of Pharmaceutical Sciences, University of Connecticut, Storrs, United States of America

4Yale University School of Medicine, New Haven, United States of America

5Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, United States of America

6Department of Cell Biology, Yale University School of Medicine, New Haven, United States of America

7Department of Pneumology, Hannover Medical School (MHH), Hannover, Germany

8Department of Medicine, Baylor College of Medicine, Houston, Houston, United States of America

Find articles by Kaminski, N. in: JCI | PubMed | Google Scholar |

Published January 10, 2023 - More info

JCI Insight. https://doi.org/10.1172/jci.insight.158100.
Copyright © 2023, Ahangari et al. This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Published January 10, 2023 - Version history
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Abstract

Idiopathic pulmonary fibrosis (IPF) is a progressive and ultimately fatal disease. Recent findings have shown a marked metabolic reprogramming associated with changes in mitochondrial homeostasis and autophagy during pulmonary fibrosis. The microRNA-33 (miR-33) family of microRNAs (miRNAs) encoded within the introns of SREBP (sterol regulatory element binding protein) genes are master regulators of sterol and fatty acid (FA) metabolism. miR-33 controls macrophage immuno-metabolic response and enhances mitochondrial biogenesis, FA oxidation, and cholesterol efflux. Here, we show that miR-33 levels are increased in Broncho Alveolar Lavage (BAL) cells isolated from IPF patients compared to healthy controls. We demonstrate that specific genetic ablation of miR-33 in macrophages protects against bleomycin-induced pulmonary fibrosis. The absence of miR-33 in macrophages improves mitochondrial homeostasis and increases autophagy while decreasing inflammatory response after bleomycin injury. Notably, pharmacological inhibition of miR-33 in macrophages via administration of anti-miR-33 Peptide Nucleic Acids (PNA-33) attenuates fibrosis in different in vivo and ex vivo mice and human models of pulmonary fibrosis. Together, these studies elucidate a major role of miR-33 in macrophages in the regulation of pulmonary fibrosis and uncover a novel therapeutic approach to treat this disease.

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