Exposure to lipopolysaccharide (LPS) reduces contractile response of small airways from GSTCD-/- mice


Autoři: Bo Liu aff001;  Amanda P. Henry aff001;  Sheyda Azimi aff001;  Suzanne Miller aff001;  Frank K. Lee aff002;  Jane C. Lee aff002;  Kelly Probert aff001;  Michael I. Kotlikoff aff002;  Ian Sayers aff001;  Ian P. Hall aff001
Působiště autorů: Division of Respiratory Medicine, & National Institute for Health Medicine, Nottingham Biomedical Research Centre, University of Nottingham, Nottingham, England, United Kingdom aff001;  Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0221899

Souhrn

Introduction

Genome-Wide Association Studies suggest glutathione S transferase C terminal domain (GSTCD) may play a role in development of Chronic Obstructive Pulmonary Disease. We aimed to define the potential role of GSTCD in airway inflammation and contraction using precision cut lung slice (PCLS) from wild-type (GSTCD+/+) and GSTCD knockout mice (GSTCD-/-).

Methods

PCLS from age and gender matched GSTCD+/+ and GSTCD-/- mice were prepared using a microtome. Contraction was studied after applying either a single dose of Methacholine (Mch) (1 μM) or different doses of Mch (0.001 to 100 μM). Each slice was then treated with lipopolysaccharide (LPS) or vehicle (PBS) for 24 hours. PCLS contraction in the same airway was repeated before and after stimulation. Levels of TNFα production was also measured.

Results

There were no differences in contraction of PCLS from GSTCD+/+ and GSTCD-/- mice in response to Mch (EC50 of GSTCD+/+ vs GSTCD-/- animals: 100.0±20.7 vs 107.7±24.5 nM, p = 0.855, n = 6 animals/group). However, after LPS treatment, there was a 31.6% reduction in contraction in the GSTCD-/- group (p = 0.023, n = 6 animals). There was no significant difference between PBS and LPS treatment groups in GSTCD+/+ animals. We observed a significant increase in TNFα production induced by LPS in GSTCD-/- lung slices compared to the GSTCD+/+ LPS treated slices.

Conclusion

GSTCD knockout mice showed an increased responsiveness to LPS (as determined by TNFα production) that was accompanied by a reduced contraction of small airways in PCLS. These data highlight an unrecognised potential function of GSTCD in mediating inflammatory signals that affect airway responses.

Klíčová slova:

Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Mouse models – Animal models – Imaging techniques – Histochemistry and cytochemistry techniques – Immunohistochemistry techniques – Immunologic techniques – Specimen preparation and treatment – Staining – Cell staining – Medicine and health sciences – Pulmonology – Pulmonary function – Chronic obstructive pulmonary disease – Diagnostic medicine – Diagnostic radiology – Pulmonary imaging – Signs and symptoms – Radiology and imaging – Immunology – Immune response – Inflammation – Pathology and laboratory medicine – Biology and life sciences – Organisms – Eukaryota – Animals – Vertebrates – Amniotes – Mammals – Rodents – Mice


Zdroje

1. Brehm JM, Man Tse S, Croteau-Chonka DC, Forno E, Litonjua AA, Raby BA, et al. A Genome-Wide Association Study of Post-bronchodilator Lung Function in Children with Asthma. Am J Respir Crit Care Med. 2015;192(5):634–7. Epub 2015/09/02. doi: 10.1164/rccm.201501-0047LE 26325155; PubMed Central PMCID: PMC4595689.

2. Castaldi PJ, Cho MH, Litonjua AA, Bakke P, Gulsvik A, Lomas DA, et al. The association of genome-wide significant spirometric loci with chronic obstructive pulmonary disease susceptibility. Am J Respir Cell Mol Biol. 2011;45(6):1147–53. Epub 2011/06/11. doi: 10.1165/rcmb.2011-0055OC 21659657; PubMed Central PMCID: PMC3262664.

3. Hancock DB, Eijgelsheim M, Wilk JB, Gharib SA, Loehr LR, Marciante KD, et al. Meta-analyses of genome-wide association studies identify multiple loci associated with pulmonary function. Nat Genet. 2010;42(1):45–52. Epub 2009/12/17. doi: 10.1038/ng.500 20010835; PubMed Central PMCID: PMC2832852.

4. Repapi E, Sayers I, Wain LV, Burton PR, Johnson T, Obeidat M, et al. Genome-wide association study identifies five loci associated with lung function. Nat Genet. 2010;42(1):36–44. Epub 2009/12/17. doi: 10.1038/ng.501 20010834; PubMed Central PMCID: PMC2862965.

5. Soler Artigas M, Wain LV, Repapi E, Obeidat M, Sayers I, Burton PR, et al. Effect of five genetic variants associated with lung function on the risk of chronic obstructive lung disease, and their joint effects on lung function. Am J Respir Crit Care Med. 2011;184(7):786–95. Epub 2011/10/04. doi: 10.1164/rccm.201102-0192OC 21965014; PubMed Central PMCID: PMC3398416.

6. Yang J, Zhou H, Liang B, Xiao J, Su Z, Chen H, et al. Association of five genetic variants with chronic obstructive pulmonary disease susceptibility and spirometric phenotypes in a Chinese Han population. Respirology. 2014;19(2):262–8. Epub 2013/11/30. doi: 10.1111/resp.12212 24286382.

7. Levinsson A, Olin AC, Modig L, Dahgam S, Bjorck L, Rosengren A, et al. Interaction effects of long-term air pollution exposure and variants in the GSTP1, GSTT1 and GSTCD genes on risk of acute myocardial infarction and hypertension: a case-control study. PLoS One. 2014;9(6):e99043. Epub 2014/06/11. doi: 10.1371/journal.pone.0099043 24915237; PubMed Central PMCID: PMC4051658.

8. Obeidat M, Miller S, Probert K, Billington CK, Henry AP, Hodge E, et al. GSTCD and INTS12 regulation and expression in the human lung. PLoS One. 2013;8(9):e74630. Epub 2013/09/24. doi: 10.1371/journal.pone.0074630 24058608; PubMed Central PMCID: PMC3776747.

9. Hao K, Bossé Y, Nickle DC, Paré PD, Postma DS, Laviolette M, et al. Lung eQTLs to Help Reveal the Molecular Underpinnings of Asthma. PLoS Genetics. 2012;8(11):e1003029. doi: 10.1371/journal.pgen.1003029 PMC3510026. 23209423

10. Bowatte GA, Lodge C, Erbas B, Lowe A, Dennekamp M, Abramson MJ, et al. GSTT1, GSTM1, GSTP1 and GSTCD Polymorphisms and Traffic-Related Air Pollution as Interactive Risk Factors for Childhood and Adolescence Asthma, Wheeze and Eczema. Am J respir Crit Care Mad. 2105;191:A6458.

11. Chaubey N, Ghosh SS. Molecular cloning, purification and functional implications of recombinant GST tagged hGMCSF cytokine. Appl Biochem Biotechnol. 2013;169(5):1713–26. Epub 2013/01/22. doi: 10.1007/s12010-012-0052-7 23334834.

12. Hatton T, Pendleton N, Barraclough R, Green J. Expression of glutathione-s-transferase (gst) subtypes in resected lung-tumors—relationship to histological type and proliferation indexes. Int J Oncol. 1993;3(5):881–6. Epub 1993/11/01. doi: 10.3892/ijo.3.5.881 21573447.

13. Makino T, Ishikawa K, Igarashi I, Yamoto T, Manabe S, Nakayama H. Relationship between GST Yp induction and hepatocyte proliferation in rats treated with phase II drug metabolizing enzyme inducers. Toxicol Pathol. 2008;36(3):420–7. Epub 2008/04/29. doi: 10.1177/0192623308315359 18441256.

14. Nakajima S, Ohsawa I, Ohta S, Ohno M, Mikami T. Regular voluntary exercise cures stress-induced impairment of cognitive function and cell proliferation accompanied by increases in cerebral IGF-1 and GST activity in mice. Behav Brain Res. 2010;211(2):178–84. Epub 2010/03/24. doi: 10.1016/j.bbr.2010.03.028 20307585.

15. Me Obeidat, Miller S, Probert K, Billington CK, Henry AP, Hodge E, et al. GSTCD and INTS12 Regulation and Expression in the Human Lung. PLOS ONE. 2013;8(9):e74630. doi: 10.1371/journal.pone.0074630 24058608

16. Bigliani MC, Rossetti V, Grondona E, Lo Presti S, Paglini PM, Rivero V, et al. Chemical compositions and properties of Schinus areira L. essential oil on airway inflammation and cardiovascular system of mice and rabbits. Food Chem Toxicol. 2012;50(7):2282–8. Epub 2012/05/02. doi: 10.1016/j.fct.2012.04.025 22546367.

17. Brandolini L, Asti C, Ruggieri V, Intilangelo A, Pellegrini L, Chiusaroli R, et al. Lipopolysaccharide-induced lung injury in mice. II. Evaluation of functional damage in isolated parenchyma strips. Pulm Pharmacol Ther. 2000;13(2):71–8. Epub 2000/05/09. doi: 10.1006/pupt.2000.0232 10799284.

18. Donovan C, Royce SG, Vlahos R, Bourke JE. Lipopolysaccharide does not alter small airway reactivity in mouse lung slices. PloS one. 2015;10(3):e0122069–e. doi: 10.1371/journal.pone.0122069 25822969.

19. Royce SG, Nold MF, Bui C, Donovan C, Lam M, Lamanna E, et al. Airway Remodeling and Hyperreactivity in a Model of Bronchopulmonary Dysplasia and Their Modulation by IL-1 Receptor Antagonist. Am J Respir Cell Mol Biol. 2016;55(6):858–68. Epub 2016/08/03. doi: 10.1165/rcmb.2016-0031OC 27482635.

20. Hiorns JE, Bidan CM, Jensen OE, Gosens R, Kistemaker LE, Fredberg JJ, et al. Airway and Parenchymal Strains during Bronchoconstriction in the Precision Cut Lung Slice. Front Physiol. 2016;7:309. Epub 2016/08/26. doi: 10.3389/fphys.2016.00309 27559314; PubMed Central PMCID: PMC4989902.

21. Kim HJ, Kim Y, Park SJ, Bae B, Kang HR, Cho SH, et al. Airway Smooth Muscle Sensitivity to Methacholine in Precision-Cut Lung Slices (PCLS) from Ovalbumin-induced Asthmatic Mice. Korean J Physiol Pharmacol. 2015;19(1):65–71. Epub 2015/01/22. doi: 10.4196/kjpp.2015.19.1.65 25605999; PubMed Central PMCID: PMC4297764.

22. Rosner SR, Ram-Mohan S, Paez-Cortez JR, Lavoie TL, Dowell ML, Yuan L, et al. Airway contractility in the precision-cut lung slice after cryopreservation. Am J Respir Cell Mol Biol. 2014;50(5):876–81. Epub 2013/12/10. doi: 10.1165/rcmb.2013-0166MA 24313705; PubMed Central PMCID: PMC4068941.

23. Hecker D, Kappler J, Glassmann A, Schilling K, Alt W. Image analysis of time-lapse movies—a precision control guided approach to correct motion artefacts. J Neurosci Methods. 2008;172(1):67–73. Epub 2008/05/27. doi: 10.1016/j.jneumeth.2008.04.010 18502517.

24. Strandberg S, Wretling ML, Wredmark T, Shalabi A. Reliability of computed tomography measurements in assessment of thigh muscle cross-sectional area and attenuation. BMC Med Imaging. 2010;10:18. Epub 2010/08/13. doi: 10.1186/1471-2342-10-18 20701775; PubMed Central PMCID: PMC2928755.

25. Oyoshi MK, Bryce P, Goya S, Pichavant M, Umetsu DT, Oettgen HC, et al. TNF receptor-associated factor 1 expressed in resident lung cells is required for the development of allergic lung inflammation. J Immunol. 2008;180(3):1878–85. Epub 2008/01/23. doi: 10.4049/jimmunol.180.3.1878 18209085.

26. Trifilieff A, Walker C, Keller T, Kottirsch G, Neumann U. Pharmacological profile of PKF242-484 and PKF241-466, novel dual inhibitors of TNF-alpha converting enzyme and matrix metalloproteinases, in models of airway inflammation. Br J Pharmacol. 2002;135(7):1655–64. Epub 2002/04/06. doi: 10.1038/sj.bjp.0704616 11934805; PubMed Central PMCID: PMC1573282.

27. Verheggen MM, van Hal PT, Adriaansen-Soeting PW, Goense BJ, Hoogsteden HC, Brinkmann AO, et al. Modulation of glucocorticoid receptor expression in human bronchial epithelial cell lines by IL-1 beta, TNF-alpha and LPS. Eur Respir J. 1996;9(10):2036–43. Epub 1996/10/01. doi: 10.1183/09031936.96.09102036 8902464.

28. Zerfaoui M, Naura AS, Errami Y, Hans CP, Rezk BM, Park J, et al. Effects of PARP-1 deficiency on airway inflammatory cell recruitment in response to LPS or TNF: differential effects on CXCR2 ligands and Duffy Antigen Receptor for Chemokines. J Leukoc Biol. 2009;86(6):1385–92. Epub 2009/09/11. doi: 10.1189/jlb.0309183 19741160; PubMed Central PMCID: PMC2780916.

29. Kheirallah AK, de Moor CH, Faiz A, Sayers I, Hall IP. Lung function associated gene Integrator Complex subunit 12 regulates protein synthesis pathways. BMC Genomics. 2017;18(1):248. Epub 2017/03/25. doi: 10.1186/s12864-017-3628-3 28335732; PubMed Central PMCID: PMC5364626.

30. Littler DR, Assaad NN, Harrop SJ, Brown LJ, Pankhurst GJ, Luciani P, et al. Crystal structure of the soluble form of the redox-regulated chloride ion channel protein CLIC4. FEBS J. 2005;272(19):4996–5007. Epub 2005/09/24. doi: 10.1111/j.1742-4658.2005.04909.x 16176272.

31. Littler DR, Harrop SJ, Brown LJ, Pankhurst GJ, Mynott AV, Luciani P, et al. Comparison of vertebrate and invertebrate CLIC proteins: the crystal structures of Caenorhabditis elegans EXC-4 and Drosophila melanogaster DmCLIC. Proteins. 2008;71(1):364–78. Epub 2007/11/07. doi: 10.1002/prot.21704 17985355.

32. Mapp CE, Fryer AA, De Marzo N, Pozzato V, Padoan M, Boschetto P, et al. Glutathione S-transferase GSTP1 is a susceptibility gene for occupational asthma induced by isocyanates. J Allergy Clin Immunol. 2002;109(5):867–72. Epub 2002/05/08. doi: 10.1067/mai.2002.123234 11994713.

33. Spiteri MA, Bianco A, Strange RC, Fryer AA. Polymorphisms at the glutathione S-transferase, GSTP1 locus: a novel mechanism for susceptibility and development of atopic airway inflammation. Allergy. 2000;55 Suppl 61:15–20. Epub 2000/08/05. doi: 10.1034/j.1398-9995.2000.00502.x 10919500.

34. Liu B, Billington CK, Henry AP, Bhaker SK, Kheirallah AK, Swan C, et al. Chloride intracellular channel 1 (CLIC1) contributes to modulation of cyclic AMP-activated whole-cell chloride currents in human bronchial epithelial cells. Physiol Rep. 2018;6(2). Epub 2018/01/26. doi: 10.14814/phy2.13508 29368798; PubMed Central PMCID: PMC5789713.

35. Dulhunty A, Gage P, Curtis S, Chelvanayagam G, Board P. The glutathione transferase structural family includes a nuclear chloride channel and a ryanodine receptor calcium release channel modulator. J Biol Chem. 2001;276(5):3319–23. Epub 2000/10/18. doi: 10.1074/jbc.M007874200 11035031.

36. Freitag A, Reimann A, Wessler I, Racke K. Effects of bacterial lipopolysaccharides (LPS) and tumour necrosis factor-alpha (TNF alpha) on rat tracheal epithelial cells in culture: morphology, proliferation and induction of nitric oxide (NO) synthase. Pulm Pharmacol. 1996;9(3):149–56. Epub 1996/06/01. 8948511.

37. Honda K, Wada H, Nakamura M, Nakamoto K, Inui T, Sada M, et al. IL-17A synergistically stimulates TNF-alpha-induced IL-8 production in human airway epithelial cells: A potential role in amplifying airway inflammation. Exp Lung Res. 2016;42(4):205–16. Epub 2016/06/09. doi: 10.1080/01902148.2016.1190796 27269887.

38. Moreland JG, Fuhrman RM, Wohlford-Lenane CL, Quinn TJ, Benda E, Pruessner JA, et al. TNF-alpha and IL-1 beta are not essential to the inflammatory response in LPS-induced airway disease. Am J Physiol Lung Cell Mol Physiol. 2001;280(1):L173–80. Epub 2001/01/03. doi: 10.1152/ajplung.2001.280.1.L173 11133507.

39. Morello S, Ito K, Yamamura S, Lee KY, Jazrawi E, Desouza P, et al. IL-1 beta and TNF-alpha regulation of the adenosine receptor (A2A) expression: differential requirement for NF-kappa B binding to the proximal promoter. J Immunol. 2006;177(10):7173–83. Epub 2006/11/04. doi: 10.4049/jimmunol.177.10.7173 17082635.

40. Anaparti V, Pascoe CD, Jha A, Mahood TH, Ilarraza R, Unruh H, et al. Tumor necrosis factor regulates NMDA receptor-mediated airway smooth muscle contractile function and airway responsiveness. Am J Physiol Lung Cell Mol Physiol. 2016;311(2):L467–80. Epub 2016/07/03. doi: 10.1152/ajplung.00382.2015 27371735.

41. Alcorn JF, Ckless K, Brown AL, Guala AS, Kolls JK, Poynter ME, et al. Strain-dependent activation of NF-kappaB in the airway epithelium and its role in allergic airway inflammation. Am J Physiol Lung Cell Mol Physiol. 2010;298(1):L57–66. Epub 2009/11/10. doi: 10.1152/ajplung.00037.2009 19897746; PubMed Central PMCID: PMC2806198.


Článek vyšel v časopise

PLOS One


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Výhody léčby pacientů s DM 2. typu GLP-1 agonisty
nový kurz
Autoři: prof. MUDr. Martin Haluzík, DrSc.

Syndrom suchého oka – diagnostika, komplikace a léčba
Autoři: MUDr. Petr Výborný, CSc., FEBO

Systémová léčba psoriázy
Autoři: MUDr. Jiří Horažďovský, Ph.D

Klinická farmakokinetika betablokátorů
Autoři:

Současné možnosti terapie osteoartrózy
Autoři: MUDr. Jakub Holešovský

Všechny kurzy
Kurzy Doporučená témata