Regenerative Metaplastic Clones in COPD Lung Drive Inflammation and Fibrosis.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
14 05 2020
Historique:
received: 26 07 2019
revised: 26 11 2019
accepted: 20 03 2020
pubmed: 17 4 2020
medline: 5 1 2021
entrez: 17 4 2020
Statut: ppublish

Résumé

Chronic obstructive pulmonary disease (COPD) is a progressive condition of chronic bronchitis, small airway obstruction, and emphysema that represents a leading cause of death worldwide. While inflammation, fibrosis, mucus hypersecretion, and metaplastic epithelial lesions are hallmarks of this disease, their origins and dependent relationships remain unclear. Here we apply single-cell cloning technologies to lung tissue of patients with and without COPD. Unlike control lungs, which were dominated by normal distal airway progenitor cells, COPD lungs were inundated by three variant progenitors epigenetically committed to distinct metaplastic lesions. When transplanted to immunodeficient mice, these variant clones induced pathology akin to the mucous and squamous metaplasia, neutrophilic inflammation, and fibrosis seen in COPD. Remarkably, similar variants pre-exist as minor constituents of control and fetal lung and conceivably act in normal processes of immune surveillance. However, these same variants likely catalyze the pathologic and progressive features of COPD when expanded to high numbers.

Identifiants

pubmed: 32298651
pii: S0092-8674(20)30340-8
doi: 10.1016/j.cell.2020.03.047
pmc: PMC7294989
mid: NIHMS1580700
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

848-864.e18

Subventions

Organisme : NCI NIH HHS
ID : U24 CA228550
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK054759
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK047967
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL129795
Pays : United States
Organisme : NHLBI NIH HHS
ID : P01 HL108808
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA241600
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA016672
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL136961
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK115445
Pays : United States
Organisme : NIEHS NIH HHS
ID : P30 ES005605
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL136370
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL138510
Pays : United States

Informations de copyright

Copyright © 2020 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests W.X., F.D.M., W.R., S.W., J.X., M.D., and M.V. have filed patents related to technologies used in the present work. M.V., F.D.M., and W.X. have financial interests in Nüwa Medical Systems, Houston, TX, USA and Tract pharmaceuticals, Houston, TX, USA. Nuwa Medical Systems is a trade name of Tract Pharmaceuticals.

Références

Methods Mol Biol. 2020;2111:47-57
pubmed: 31933197
Nat Med. 2019 Jul;25(7):1153-1163
pubmed: 31209336
Bioinformatics. 2014 Feb 15;30(4):523-30
pubmed: 24336805
Respir Res. 2016 Jul 16;17(1):83
pubmed: 27423691
N Engl J Med. 2016 Sep 1;375(9):871-8
pubmed: 27579637
Dev Cell. 2018 Mar 26;44(6):752-761.e4
pubmed: 29587145
Eur J Radiol. 2016 Nov;85(11):2144-2151
pubmed: 27776670
Am J Respir Cell Mol Biol. 2017 Jul;57(1):35-46
pubmed: 28170284
Nature. 2018 Aug;560(7720):649-654
pubmed: 30135581
Thorax. 2011 Aug;66(8):651-7
pubmed: 21422041
Am J Respir Crit Care Med. 2007 May 15;175(10):998-1005
pubmed: 17332482
N Engl J Med. 2017 Sep 7;377(10):986-987
pubmed: 28877010
J Immunol. 2012 Nov 1;189(9):4313-20
pubmed: 23018460
Am J Respir Crit Care Med. 2018 Jun 15;197(12):1540-1551
pubmed: 29406779
Kidney Int Suppl. 2010 Dec;(119):S22-6
pubmed: 21116313
Int J Chron Obstruct Pulmon Dis. 2010 Oct 05;5:327-34
pubmed: 21037956
Annu Rev Pathol. 2009;4:435-59
pubmed: 18954287
Nature. 2015 Oct 1;526(7571):75-81
pubmed: 26432246
BMC Bioinformatics. 2013 Apr 15;14:128
pubmed: 23586463
Bioinformatics. 2010 Mar 1;26(5):589-95
pubmed: 20080505
N Engl J Med. 2010 Dec 2;363(23):2233-47
pubmed: 21121836
Matrix Biol. 2018 Aug;68-69:28-43
pubmed: 29288716
Nat Rev Dis Primers. 2015 Dec 03;1:15076
pubmed: 27189863
Nat Protoc. 2015 Oct;10(10):1556-66
pubmed: 26379229
JCO Precis Oncol. 2017 Jul;2017:
pubmed: 28890946
Genome Res. 2010 Sep;20(9):1297-303
pubmed: 20644199
Sci Rep. 2015 Feb 02;5:8163
pubmed: 25641363
Science. 1998 Dec 18;282(5397):2258-61
pubmed: 9856949
Respir Res. 2007 Nov 26;8:85
pubmed: 18039368
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Genome Biol. 2014;15(12):550
pubmed: 25516281
Cell Tissue Res. 2017 Mar;367(3):427-444
pubmed: 28144783
Cell. 2011 Oct 28;147(3):525-38
pubmed: 22036562
J Allergy Clin Immunol. 2016 Jul;138(1):16-27
pubmed: 27373322
JCI Insight. 2018 Aug 23;3(16):
pubmed: 30135312
N Engl J Med. 2016 May 12;374(19):1842-1852
pubmed: 27168434
Nature. 2015 Jan 29;517(7536):616-20
pubmed: 25383540
J Immunol. 2005 May 15;174(10):6477-89
pubmed: 15879151
N Engl J Med. 2011 Oct 27;365(17):1567-75
pubmed: 22029978
Am J Respir Crit Care Med. 2000 Feb;161(2 Pt 1):381-90
pubmed: 10673175
Lancet. 2012 Apr 7;379(9823):1341-51
pubmed: 22314182
Nature. 2015 Jan 29;517(7536):621-5
pubmed: 25533958
Eur Respir J. 2019 May 18;53(5):
pubmed: 30846476
Cancer Treat Rev. 2018 Feb;63:40-47
pubmed: 29207310
Eur Rev Med Pharmacol Sci. 2018 Jun;22(11):3553-3569
pubmed: 29917210
Thorax. 2002 Jul;57(7):590-5
pubmed: 12096201
Eur Respir J. 2007 Sep;30(3):467-71
pubmed: 17504799
Bioinformatics. 2016 Apr 15;32(8):1220-2
pubmed: 26647377
Nat Genet. 2011 May;43(5):491-8
pubmed: 21478889
Chest. 2011 Jun;139(6):1380-1387
pubmed: 20966041
N Engl J Med. 2004 Jun 24;350(26):2645-53
pubmed: 15215480
Annu Rev Pathol. 2010;5:77-98
pubmed: 20078216
Immunol Rev. 2016 Sep;273(1):94-111
pubmed: 27558330
J Histochem Cytochem. 2019 Sep;67(9):663-681
pubmed: 31116067
N Engl J Med. 2017 Sep 7;377(10):911-922
pubmed: 28877023
COPD. 2018 Jun-Aug;15(4):392-404
pubmed: 30064276
Sci Rep. 2017 Aug 25;7(1):9562
pubmed: 28842670
J Allergy Clin Immunol. 2007 May;119(5):1065-71
pubmed: 17270263
Nature. 2018 Sep;561(7724):473-478
pubmed: 30185910
JCI Insight. 2016 Sep 22;1(15):e87536
pubmed: 27699245
J Immunol. 1995 Jan 1;154(1):180-91
pubmed: 7995938
Br Med J. 1977 Jun 25;1(6077):1645-8
pubmed: 871704
Int J Chron Obstruct Pulmon Dis. 2017 Jun 22;12:1857-1865
pubmed: 28694696
Nat Methods. 2018 Aug;15(8):591-594
pubmed: 30013048
J Clin Invest. 2007 Nov;117(11):3551-62
pubmed: 17965775
J Clin Invest. 2013 Sep;123(9):3967-82
pubmed: 23945235
PLoS One. 2013;8(3):e58658
pubmed: 23527003
Stem Cell Reports. 2016 Nov 8;7(5):817-825
pubmed: 27773701
Curr Protoc Bioinformatics. 2013;43:11.10.1-11.10.33
pubmed: 25431634
Ann Am Thorac Soc. 2014 Dec;11 Suppl 5:S287-91
pubmed: 25525734
Lab Invest. 2002 Oct;82(10):1335-45
pubmed: 12379768
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
Exp Cell Res. 2018 Nov 15;372(2):141-149
pubmed: 30268759
J Biol Chem. 2005 Apr 29;280(17):16891-900
pubmed: 15734732
Adv Immunol. 2016;129:25-53
pubmed: 26791857
Nat Biotechnol. 2014 Sep;32(9):896-902
pubmed: 25150836
Cell Tissue Res. 2017 Mar;367(3):537-550
pubmed: 28108847
Bioinformatics. 2012 Jun 15;28(12):i172-8
pubmed: 22689758
Pain. 2019 Dec;160(12):2691-2698
pubmed: 31433352
Am J Respir Crit Care Med. 2019 Mar 15;199(6):715-727
pubmed: 30352166
Int J Mol Sci. 2018 Aug 05;19(8):
pubmed: 30081609
Blood. 2016 Aug 25;128(8):e20-31
pubmed: 27365425
Annu Rev Immunol. 2014;32:513-45
pubmed: 24555472
Am J Respir Cell Mol Biol. 2016 May;54(5):647-55
pubmed: 26796672
JCI Insight. 2016 Dec 8;1(20):e90558
pubmed: 27942595
Glob Health Epidemiol Genom. 2018 Apr 6;3:e4
pubmed: 29868229
Nat Biotechnol. 2015 May;33(5):495-502
pubmed: 25867923

Auteurs

Wei Rao (W)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Shan Wang (S)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Marcin Duleba (M)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Suchan Niroula (S)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Kristina Goller (K)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Jingzhong Xie (J)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Rajasekaran Mahalingam (R)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Rahul Neupane (R)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Audrey-Ann Liew (AA)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA.

Matthew Vincent (M)

Nüwa Medical Systems, Houston, TX 77479, USA.

Kenichi Okuda (K)

Marsico Lung Center, University of North Carolina, Chapel Hill, NC 27599, USA.

Wanda K O'Neal (WK)

Marsico Lung Center, University of North Carolina, Chapel Hill, NC 27599, USA.

Richard C Boucher (RC)

Marsico Lung Center, University of North Carolina, Chapel Hill, NC 27599, USA.

Burton F Dickey (BF)

Department of Pulmonary Medicine, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.

Michael E Wechsler (ME)

Department of Medicine, National Jewish Health, Denver, CO 80206, USA.

Omar Ibrahim (O)

Department of Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, University of Connecticut School of Medicine, Farmington, CT 06032, USA.

John F Engelhardt (JF)

Department of Anatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA 52242, USA.

Tinne C J Mertens (TCJ)

Department of Biochemistry and Molecular Biology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX 77030, USA.

Wei Wang (W)

Department of Biochemistry and Molecular Biology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX 77030, USA.

Soma S K Jyothula (SSK)

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

Christopher P Crum (CP)

Department of Pathology, Harvard Medical School and Brigham and Women's Hospital, Boston, MA 02215, USA.

Harry Karmouty-Quintana (H)

Department of Biochemistry and Molecular Biology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX 77030, USA.

Kalpaj R Parekh (KR)

Department of Anatomy and Cell Biology, University of Iowa Carver College of Medicine, Iowa City, IA 52242, USA; Department of Surgery, Division of Cardiothoracic Surgery, University of Iowa Carver College of Medicine, Iowa City, IA 52242, USA.

Mark L Metersky (ML)

Department of Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, University of Connecticut School of Medicine, Farmington, CT 06032, USA.

Frank D McKeon (FD)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA. Electronic address: fdmckeon@uh.edu.

Wa Xian (W)

Stem Cell Center, Department of Biology and Biochemistry, University of Houston, Houston, TX 77003, USA. Electronic address: wxian@uh.edu.

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Classifications MeSH