Methylomic correlates of autophagy activity in cystic fibrosis.

Animals Autophagy Catechin / analogs & derivatives Cells, Cultured Cystic Fibrosis / physiopathology Macrophages / physiology Mice Mice, Inbred C57BL

Journal

Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society
ISSN: 1873-5010
Titre abrégé: J Cyst Fibros
Pays: Netherlands
ID NLM: 101128966

Informations de publication

Date de publication:
07 2019
Historique:
received: 25 09 2018
revised: 21 01 2019
accepted: 22 01 2019
pubmed: 10 2 2019
medline: 18 9 2020
entrez: 10 2 2019
Statut: ppublish

Résumé

Autophagy is a highly regulated, biological process that provides energy during periods of stress and starvation. This conserved process also acts as a defense mechanism and clears microbes from the host cell. Autophagy is impaired in Cystic Fibrosis (CF) patients and CF mice, as their cells exhibit low expression levels of essential autophagy molecules. The genetic disorder in CF is due to mutations in the cystic fibrosis transmembrane conductance regulator (cftr) gene that encodes for a chloride channel. CF patients are particularly prone to infection by pathogens that are otherwise cleared by autophagy in healthy immune cells including Burkholderia cenocepacia (B. cenocepacia). The objective of this study is to determine the mechanism underlying weak autophagic activity in CF macrophages and find therapeutic targets to correct it. Using reduced representation bisulfite sequencing (RRBS) to determine DNA methylation profile, we found that the promoter regions of Atg12 in CF macrophages are significantly more methylated than in the wild-type (WT) immune cells, accompanied by low protein expression. The natural product epigallocatechin-3-gallate (EGCG) significantly reduced the methylation of Atg12 promoter improving its expression. Accordingly, EGCG restricted B. cenocepacia replication within CF mice and their derived macrophages by improving autophagy and preventing dissemination. In addition, EGCG improved the function of CFTR protein. Altogether, utilizing RRBS for the first time in the CF field revealed a previously unrecognized mechanism for reduced autophagic activity in CF. Our data also offers a mechanism by which EGCG exerts its positive effects in CF.

Identifiants

DOI: 10.1016/j.jcf.2019.01.011 PMID: 30737168 PMC: PMC6591064
pubmed: 30737168
pii: S1569-1993(18)30824-5
doi: 10.1016/j.jcf.2019.01.011
pmc: PMC6591064
mid: NIHMS1521632
pii:
doi:

Substances chimiques

Catechin 8R1V1STN48
epigallocatechin gallate BQM438CTEL

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

491-500

Subventions

Organisme : NCATS NIH HHS
ID : UL1 TR001070
Pays : United States
Organisme : NCI NIH HHS
ID : R50 CA211524
Pays : United States
Organisme : NIGMS NIH HHS
ID : U54 GM104942
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA016058
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI113477
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL127651
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI124121
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2019. Published by Elsevier B.V.

Références

Am J Respir Crit Care Med. 2001 Jun;163(7):1683-92
pubmed: 11401894
Arch Dis Child. 2002 Oct;87(4):306-11
pubmed: 12244003
Nutr Rev. 2004 May;62(5):204-11
pubmed: 15212320
Expert Opin Ther Targets. 2004 Dec;8(6):551-64
pubmed: 15584862
Nucleic Acids Res. 2005 Oct 13;33(18):5868-77
pubmed: 16224102
J Biol Chem. 2006 Feb 10;281(6):3329-34
pubmed: 16339147
Cell. 1991 Sep 6;66(5):1027-36
pubmed: 1716180
J Biol Chem. 2007 Dec 28;282(52):37298-302
pubmed: 17986448
PLoS Pathog. 2009 Apr;5(4):e1000361
pubmed: 19343209
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Pharm Res. 2010 Jun;27(6):1103-14
pubmed: 20232120
J Thorac Cardiovasc Surg. 2011 Feb;141(2):511-7
pubmed: 20546800
Free Radic Biol Med. 2010 Nov 15;49(9):1444-52
pubmed: 20708679
Nat Cell Biol. 2010 Sep;12(9):863-75
pubmed: 20711182
Chem Biol Interact. 2010 Dec 5;188(3):659-67
pubmed: 20816778
J Biol Chem. 2011 Feb 4;286(5):3203-8
pubmed: 21097506
Nature. 2011 Jan 20;469(7330):323-35
pubmed: 21248839
Nat Protoc. 2011 Apr;6(4):468-81
pubmed: 21412275
Bioinformatics. 2011 Jun 1;27(11):1571-2
pubmed: 21493656
Autophagy. 2011 Nov;7(11):1359-70
pubmed: 21997369
Immunity. 2012 Jul 27;37(1):35-47
pubmed: 22658523
Autophagy. 2012 Nov;8(11):1657-72
pubmed: 22874563
Genome Biol. 2012 Oct 03;13(10):R87
pubmed: 23034086
Br J Pharmacol. 2013 Mar;168(5):1059-73
pubmed: 23072320
J Biol Chem. 2013 Jan 18;288(3):2049-58
pubmed: 23148214
Nutrients. 2012 Nov 08;4(11):1679-91
pubmed: 23201840
Autophagy. 2013 Mar;9(3):424-5
pubmed: 23321721
Mol Cell Biol. 2013 Oct;33(20):3974-5
pubmed: 23979595
Hum Mutat. 2013 Dec;34(12):1606-10
pubmed: 24106010
Autophagy. 2014;10(11):2053-74
pubmed: 25350163
Methods Mol Biol. 2015;1238:273-87
pubmed: 25421665
BMC Evol Biol. 2015 Mar 18;15:48
pubmed: 25887897
Epigenetics. 2016 May 3;11(5):381-8
pubmed: 26909551
Cell Death Differ. 2016 Aug;23(8):1380-93
pubmed: 27035618
Autophagy. 2016 Nov;12(11):2248-2249
pubmed: 27487449
Autophagy. 2016 Nov;12(11):2026-2037
pubmed: 27541364
Oncotarget. 2017 Jan 17;8(3):5629-5637
pubmed: 27895318
Cell Cycle. 2017 Feb;16(3):271-279
pubmed: 28059601
Cell Death Dis. 2017 Jan 12;8(1):e2544
pubmed: 28079883
J Zhejiang Univ Sci B. 2017 Feb.;18(2):89-98
pubmed: 28124838
Mol Cell. 2017 Mar 2;65(5):781-785
pubmed: 28257699
Clin Epigenetics. 2017 Feb 14;9:19
pubmed: 28289476
Biochem Biophys Res Commun. 2017 Sep 23;491(3):595-602
pubmed: 28760340
Am J Respir Crit Care Med. 2018 Jan 15;197(2):214-224
pubmed: 28930490
J Autoimmun. 2018 Mar;88:11-20
pubmed: 29108670
J Mol Biol. 2018 Jan 19;430(2):174-192
pubmed: 29162504
J Cyst Fibros. 2018 Jul;17(4):454-461
pubmed: 29241629
Immunol Rev. 2018 Jan;281(1):62-73
pubmed: 29248000
Org Biomol Chem. 2018 Feb 28;16(9):1419-1435
pubmed: 29265160
Biol Lett. 2018 Jan;14(1):
pubmed: 29321247
Cell Death Dis. 2018 Feb 7;9(2):191
pubmed: 29415993
Front Immunol. 2018 Apr 10;9:766
pubmed: 29692785
J Zhejiang Univ Sci B. 2018 May;19(5):333-341
pubmed: 29732743
Front Neurosci. 2018 May 22;12:255
pubmed: 29872373
Epigenomics. 2018 Aug;10(8):1131-1145
pubmed: 30052057
Transplant Proc. 2018 Jul - Aug;50(6):1904-1909
pubmed: 30056926
Autophagy. 2018;14(11):1928-1942
pubmed: 30165781
J Cell Sci Suppl. 1993;17:235-9
pubmed: 7511616
BMJ. 1995 Jun 17;310(6994):1571-2
pubmed: 7787647
Cancer Res. 1998 Jan 1;58(1):95-101
pubmed: 9426064
Physiol Rev. 1999 Jan;79(1 Suppl):S175-91
pubmed: 9922381

Auteurs

Kyle Caution (K)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Alexander Pan (A)

Genomics Shared Resource, Comprehensive Cancer Center, USA; The Ohio State University, Columbus, OH 43210, USA.

Kathrin Krause (K)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Asmaa Badr (A)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Kaitlin Hamilton (K)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Anup Vaidya (A)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Hawin Gosu (H)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Kylene Daily (K)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Shady Estfanous (S)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Mikhail A Gavrilin (MA)

Department of Internal Medicine, The Ohio State University, USA; The Ohio State University, Columbus, OH 43210, USA.

Mark E Drew (ME)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA.

Estelle Cormet-Boyaka (E)

Department of Veterinary Biosciences, The Ohio State University, USA; The Ohio State University, Columbus, OH 43210, USA.

Xi Chen (X)

Department of Veterinary Biosciences, The Ohio State University, USA; The Ohio State University, Columbus, OH 43210, USA.

David E Frankhouser (DE)

Genomics Shared Resource, Comprehensive Cancer Center, USA; The Ohio State University, Columbus, OH 43210, USA.

Ralf Bundschuh (R)

Genomics Shared Resource, Comprehensive Cancer Center, USA; Department of Internal Medicine, The Ohio State University, USA; The Ohio State University, Columbus, OH 43210, USA.

Pearlly Yan (P)

Genomics Shared Resource, Comprehensive Cancer Center, USA; Department of Internal Medicine, The Ohio State University, USA; The Ohio State University, Columbus, OH 43210, USA.

Duaa Dakhlallah (D)

West Virginia University, Department of Microbiology, Immunology and Cell Biology, The Ohio State University, USA.

Amal O Amer (AO)

Department of Microbial Infection and Immunity, Infectious Diseases Institute, USA; The Ohio State University, Columbus, OH 43210, USA. Electronic address: amal.amer@osumc.edu.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Methylomic correlates of autophagy activity in...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Autophagie › Methylomic correlates of autophagy activity in...
questionsmedicales.fr › Composés hétérocycliques › Composés hétérocycliques à cycles fusionnés › Composés hétérobicycliques › Benzopyranes › 4H-1-Benzopyran-4-ones › Flavonoïdes › Catéchine › Methylomic correlates of autophagy activity in...
questionsmedicales.fr › Cellules › Cellules cultivées › Methylomic correlates of autophagy activity in...
questionsmedicales.fr › Malformations et maladies congénitales, héréditaires et néonatales › Maladies néonatales › Mucoviscidose › Methylomic correlates of autophagy activity in...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Phagocytes › Macrophages › Methylomic correlates of autophagy activity in...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Methylomic correlates of autophagy activity in...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Lignées consanguines de souris › Souris de lignée C57BL › Methylomic correlates of autophagy activity in...