Effects of repeated infections with non-typeable Haemophilus influenzae on lung in vitamin D deficient and smoking mice.


Journal

Respiratory research
ISSN: 1465-993X
Titre abrégé: Respir Res
Pays: England
ID NLM: 101090633

Informations de publication

Date de publication:
02 Mar 2022
Historique:
received: 09 02 2021
accepted: 17 02 2022
entrez: 3 3 2022
pubmed: 4 3 2022
medline: 18 3 2022
Statut: epublish

Résumé

In chronic obstructive pulmonary disease (COPD), exacerbations cause acute inflammatory flare-ups and increase the risk for hospitalization and mortality. Exacerbations are common in all disease stages and are often caused by bacterial infections e.g., non-typeable Heamophilus influenzae (NTHi). Accumulating evidence also associates vitamin D deficiency with the severity of COPD and exacerbation frequency. However, it is still unclear whether vitamin D deficiency when combined with cigarette smoking would worsen and prolong exacerbations caused by repeated infections with the same bacterial strain. Vitamin D sufficient (VDS) and deficient (VDD) mice were exposed to nose-only cigarette smoke (CS) for 14 weeks and oropharyngeally instilled with NTHi at week 6, 10 and 14. Three days after the last instillation, mice were assessed for lung function, tissue remodeling, inflammation and immunity. The impact of VDD and CS on inflammatory cells and immunoglobulin (Ig) production was also assessed in non-infected animals while serum Ig production against NTHi and dsDNA was measured in COPD patients before and 1 year after supplementation with Vitamin D3. VDD enhanced NTHi eradication, independently of CS and complete eradication was reflected by decreased anti-NTHi Ig's within the lung. In addition, VDD led to an increase in total lung capacity (TLC), lung compliance (Cchord), MMP12/TIMP1 ratio with a rise in serum Ig titers and anti-dsDNA Ig's. Interestingly, in non-infected animals, VDD exacerbated the CS-induced anti-NTHi Ig's, anti-dsDNA Ig's and inflammatory cells within the lung. In COPD patients, serum Ig production was not affected by vitamin D status but anti-NTHi IgG increased after vitamin D3 supplementation in patients who were Vitamin D insufficient before treatment. During repeated infections, VDD facilitated NTHi eradication and resolution of local lung inflammation through production of anti-NTHi Ig, independently of CS whilst it also promoted autoantibodies. In COPD patients, vitamin D supplementation could be protective against NTHi infections in vitamin D insufficient patients. Future research is needed to decipher the determinants of dual effects of VDD on adaptive immunity. ClinicalTrials, NCT00666367. Registered 23 April 2008, https://www.clinicaltrials.gov/ct2/show/study/NCT00666367 .

Sections du résumé

BACKGROUND BACKGROUND
In chronic obstructive pulmonary disease (COPD), exacerbations cause acute inflammatory flare-ups and increase the risk for hospitalization and mortality. Exacerbations are common in all disease stages and are often caused by bacterial infections e.g., non-typeable Heamophilus influenzae (NTHi). Accumulating evidence also associates vitamin D deficiency with the severity of COPD and exacerbation frequency. However, it is still unclear whether vitamin D deficiency when combined with cigarette smoking would worsen and prolong exacerbations caused by repeated infections with the same bacterial strain.
METHODS METHODS
Vitamin D sufficient (VDS) and deficient (VDD) mice were exposed to nose-only cigarette smoke (CS) for 14 weeks and oropharyngeally instilled with NTHi at week 6, 10 and 14. Three days after the last instillation, mice were assessed for lung function, tissue remodeling, inflammation and immunity. The impact of VDD and CS on inflammatory cells and immunoglobulin (Ig) production was also assessed in non-infected animals while serum Ig production against NTHi and dsDNA was measured in COPD patients before and 1 year after supplementation with Vitamin D3.
RESULTS RESULTS
VDD enhanced NTHi eradication, independently of CS and complete eradication was reflected by decreased anti-NTHi Ig's within the lung. In addition, VDD led to an increase in total lung capacity (TLC), lung compliance (Cchord), MMP12/TIMP1 ratio with a rise in serum Ig titers and anti-dsDNA Ig's. Interestingly, in non-infected animals, VDD exacerbated the CS-induced anti-NTHi Ig's, anti-dsDNA Ig's and inflammatory cells within the lung. In COPD patients, serum Ig production was not affected by vitamin D status but anti-NTHi IgG increased after vitamin D3 supplementation in patients who were Vitamin D insufficient before treatment.
CONCLUSION CONCLUSIONS
During repeated infections, VDD facilitated NTHi eradication and resolution of local lung inflammation through production of anti-NTHi Ig, independently of CS whilst it also promoted autoantibodies. In COPD patients, vitamin D supplementation could be protective against NTHi infections in vitamin D insufficient patients. Future research is needed to decipher the determinants of dual effects of VDD on adaptive immunity.
TRAIL REGISTRATION BACKGROUND
ClinicalTrials, NCT00666367. Registered 23 April 2008, https://www.clinicaltrials.gov/ct2/show/study/NCT00666367 .

Identifiants

pubmed: 35236342
doi: 10.1186/s12931-022-01962-6
pii: 10.1186/s12931-022-01962-6
pmc: PMC8889723
doi:

Banques de données

ClinicalTrials.gov
['NCT00666367']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

40

Subventions

Organisme : Onderzoeksraad, KU Leuven
ID : C24/15/30

Informations de copyright

© 2022. The Author(s).

Références

Am J Pathol. 2019 Sep;189(9):1711-1720
pubmed: 31220453
Horm Metab Res. 2019 May;51(5):296-301
pubmed: 31071734
Z Rheumatol. 2018 Nov;77(9):833-840
pubmed: 29460148
Ann Am Thorac Soc. 2015 Nov;12 Suppl 2:S169-75
pubmed: 26595735
Sci Rep. 2019 Jul 25;9(1):10798
pubmed: 31346202
J Infect Dis. 2011 May 1;203(9):1240-8
pubmed: 21357942
Lupus. 2009 Nov;18(13):1176-80
pubmed: 19880564
Thorax. 2019 Apr;74(4):337-345
pubmed: 30630893
Respir Res. 2015 Mar 20;16:41
pubmed: 25890119
Eur Respir J. 2017 Sep 11;50(3):
pubmed: 28893867
Eur Respir J. 2010 Jun;35(6):1209-15
pubmed: 20513910
N Engl J Med. 2010 Sep 16;363(12):1128-38
pubmed: 20843247
Mucosal Immunol. 2016 Jul;9(4):873-83
pubmed: 26577570
Lupus. 2018 Nov;27(13):2003-2011
pubmed: 30157716
PLoS One. 2016 Aug 11;11(8):e0160482
pubmed: 27513734
Mol Med Rep. 2016 Feb;13(2):1186-94
pubmed: 26675943
Trop Doct. 2017 Jan;47(1):77-84
pubmed: 27178217
Front Immunol. 2018 Nov 05;9:2530
pubmed: 30455693
J Steroid Biochem Mol Biol. 2014 Oct;144 Pt A:138-45
pubmed: 24239505
Infect Immun. 2016 Oct 17;84(11):3097-3104
pubmed: 27400722
Arch Intern Med. 2009 Feb 23;169(4):384-90
pubmed: 19237723
Ann Intern Med. 2012 Jan 17;156(2):105-14
pubmed: 22250141
Proc Am Thorac Soc. 2004;1(2):109-14
pubmed: 16113422
Front Immunol. 2019 Jul 17;10:1667
pubmed: 31379858
J Steroid Biochem Mol Biol. 2019 Apr;188:103-110
pubmed: 30605776
Respir Res. 2014 Dec 13;15:131
pubmed: 25496239
Chron Respir Dis. 2019 Jan-Dec;16:1479973119867954
pubmed: 31409129
Immunol Lett. 2019 Oct;214:8-15
pubmed: 31472176
Chest. 2000 May;117(5 Suppl 1):286S-91S
pubmed: 10843957
Cell Immunol. 2018 Sep;331:121-129
pubmed: 29935764
PLoS One. 2013 Nov 15;8(11):e81120
pubmed: 24260547
J Steroid Biochem Mol Biol. 2019 Mar;187:42-51
pubmed: 30399417
PLoS One. 2014 Jun 13;9(6):e99805
pubmed: 24926881
Biochem Biophys Res Commun. 2011 Mar 4;406(1):127-33
pubmed: 21300024
Tissue Barriers. 2018;6(4):1-13
pubmed: 30409076
Infect Immun. 2008 Aug;76(8):3481-90
pubmed: 18490462
Photochem Photobiol Sci. 2017 Mar 16;16(3):339-346
pubmed: 27849096
Mymensingh Med J. 2019 Apr;28(2):441-448
pubmed: 31086164
J Nutr. 2014 Dec;144(12):2073-82
pubmed: 25320188
J Steroid Biochem Mol Biol. 2019 Mar;187:134-145
pubmed: 30481575
Am J Respir Cell Mol Biol. 2010 Jan;42(1):96-104
pubmed: 19346316
Eur Respir J. 2008 Jun;31(6):1334-56
pubmed: 18515558
Exp Toxicol Pathol. 2015 Mar;67(3):261-9
pubmed: 25601416
Clin Exp Immunol. 2009 Oct;158(1):20-5
pubmed: 19737226
Diabetes. 2002 May;51(5):1367-74
pubmed: 11978632
Respir Res. 2015 Sep 16;16:110
pubmed: 26376849
Drug Des Devel Ther. 2016 Dec 28;11:91-102
pubmed: 28096657
Clin Endocrinol (Oxf). 2011 Nov;75(5):608-13
pubmed: 21595731
Am J Respir Crit Care Med. 2015 Aug 15;192(4):438-45
pubmed: 25945594
Chest. 1999 Mar;115(3):829-35
pubmed: 10084499
Respir Res. 2014 Feb 04;15:11
pubmed: 24495712
Can Respir J. 2009 May-Jun;16(3):75-80
pubmed: 19557213
Thorax. 2010 Mar;65(3):215-20
pubmed: 19996341

Auteurs

Jef Serré (J)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium.

Ajime Tom Tanjeko (AT)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium.

Carolien Mathyssen (C)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium.

Tobias Heigl (T)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium.

Annelore Sacreas (A)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium.

Dana Paulina Cook (DP)

Clinical and Experimental Endocrinology (CEE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Leuven, Belgium.

Erik Verbeken (E)

Translational Cell & Tissue Research, Department of Imaging & Pathology, KU Leuven, Leuven, Belgium.

Karen Maes (K)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium.

Jan Verhaegen (J)

Laboratory of Clinical Bacteriology and Mycology, Department of Microbiology, Immunology and Transplantation, KU Leuven, Leuven, Belgium.

Charles Pilette (C)

Institute of Experimental & Clinical Research, Pole of Pneumology, ENT and Dermatology, and Cliniques Universitaires Saint-Luc, Department of Pulmonology, Université Catholique de Louvain (UCL), Brussels, Belgium.

Jeroen Vanoirbeek (J)

Centre of Environment and Health, Department of Public Health and Primary Care, KU Leuven, Leuven, Belgium.

Conny Gysemans (C)

Clinical and Experimental Endocrinology (CEE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Leuven, Belgium.

Chantal Mathieu (C)

Clinical and Experimental Endocrinology (CEE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Leuven, Belgium.

Bart Vanaudenaerde (B)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium.

Wim Janssens (W)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium.

Ghislaine Gayan-Ramirez (G)

Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), Department of Chronic Diseases and Metabolism (CHROMETA), KU Leuven, Herestraat 49, O&NI bis, box 706, 3000, Leuven, Belgium. ghislaine.gayan-ramirez@kuleuven.be.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH