Malondialdehyde-Acetaldehyde Adduct Formation Decreases Immunoglobulin A Transport Across Airway Epithelium in Smokers Who Abuse Alcohol

Overview

Journal Am J Pathol

Publisher Elsevier

Specialty Pathology

Date 2021 Jun 29

PMID 34186073

Citations 3

Authors

Todd A Wyatt

Kristi J Warren

Tanner J Wetzel

Troy Suwondo

Gage P Rensch

Jane M DeVasure

Deanna D Mosley

Kusum K Kharbanda

Geoffrey M Thiele

Ellen L Burnham

Kristina L Bailey

Samantha M Yeligar

Affiliations

Soon will be listed here.

Abstract

Alcohol misuse and smoking are risk factors for pneumonia, yet the impact of combined cigarette smoke and alcohol on pneumonia remains understudied. Smokers who misuse alcohol form lung malondialdehyde-acetaldehyde (MAA) protein adducts and have decreased levels of anti-MAA secretory IgA (sIgA). Transforming growth factor-β (TGF-β) down-regulates polymeric Ig receptor (pIgR) on mucosal epithelium, resulting in decreased sIgA transcytosis to the mucosa. It is hypothesized that MAA-adducted lung protein increases TGF-β, preventing expression of epithelial cell pIgR and decreasing sIgA. Cigarette smoke and alcohol co-exposure on sIgA and TGF-β in human bronchoalveolar lavage fluid and in mice instilled with MAA-adducted surfactant protein D (SPD-MAA) were studied herein. Human bronchial epithelial cells (HBECs) and mouse tracheal epithelial cells were treated with SPD-MAA and sIgA and TGF-β was measured. Decreased sIgA and increased TGF-β were observed in bronchoalveolar lavage from combined alcohol and smoking groups in humans and mice. CD204 (MAA receptor) knockout mice showed no changes in sIgA. SPD-MAA decreased pIgR in HBECs. Conversely, SPD-MAA stimulated TGF-β release in both HBECs and mouse tracheal epithelial cells, but not in CD204 knockout mice. SPD-MAA stimulated TGF-β in alveolar macrophage cells. These data show that MAA-adducted surfactant protein stimulates lung epithelial cell TGF-β, down-regulates pIgR, and decreases sIgA transcytosis. These data provide a mechanism for the decreased levels of sIgA observed in smokers who misuse alcohol.

Citing Articles

Hepatic pIgR-mediated secretion of IgA limits bacterial translocation and prevents ethanol-induced liver disease in mice.

Hendrikx T, Lang S, Rajcic D, Wang Y, McArdle S, Kim K Gut. 2023; 72(10):1959-1970.

PMID: 36690432 PMC: 10841342. DOI: 10.1136/gutjnl-2022-328265.

Pharmacological reversal of post-transcriptional alterations implicated in alcohol-induced alveolar macrophage dysfunction.

Yeligar S, Harris F, Brown L, Hart C Alcohol. 2022; 106:30-43.

PMID: 36328183 PMC: 10080543. DOI: 10.1016/j.alcohol.2022.10.003.

Malondialdehyde Acetaldehyde-Adduction Changes Surfactant Protein D Structure and Function.

Nissen C, Mosley D, Kharbanda K, Katafiasz D, Bailey K, Wyatt T Front Immunol. 2022; 13():866795.

PMID: 35669781 PMC: 9164268. DOI: 10.3389/fimmu.2022.866795.

References

Overgaard C, Schlingmann B, Dorsainvil White S, Ward C, Fan X, Swarnakar S . The relative balance of GM-CSF and TGF-β1 regulates lung epithelial barrier function. Am J Physiol Lung Cell Mol Physiol. 2015; 308(12):L1212-23. PMC: 4499033. DOI: 10.1152/ajplung.00042.2014. View

Omidvari K, Casey R, Nelson S, Olariu R, Shellito J . Alveolar macrophage release of tumor necrosis factor-alpha in chronic alcoholics without liver disease. Alcohol Clin Exp Res. 1998; 22(3):567-72. DOI: 10.1111/j.1530-0277.1998.tb04294.x. View

Bailey K, Kharbanda K, Katafiasz D, Sisson J, Wyatt T . Oxidative stress associated with aging activates protein kinase Cε, leading to cilia slowing. Am J Physiol Lung Cell Mol Physiol. 2018; 315(5):L882-L890. PMC: 6295504. DOI: 10.1152/ajplung.00033.2018. View

Burnham E, Kovacs E, Davis C . Pulmonary cytokine composition differs in the setting of alcohol use disorders and cigarette smoking. Am J Physiol Lung Cell Mol Physiol. 2013; 304(12):L873-82. PMC: 3680749. DOI: 10.1152/ajplung.00385.2012. View

Polosukhin V, Cates J, Lawson W, Zaynagetdinov R, Milstone A, Massion P . Bronchial secretory immunoglobulin a deficiency correlates with airway inflammation and progression of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2011; 184(3):317-27. PMC: 3265275. DOI: 10.1164/rccm.201010-1629OC. View

Song K, Coleman R, Zhu X, Alber C, Ballas Z, Waldschmidt T . Chronic ethanol consumption by mice results in activated splenic T cells. J Leukoc Biol. 2002; 72(6):1109-16. View

Gupta N, Lindenauer P, Yu P, Imrey P, Haessler S, Deshpande A . Association Between Alcohol Use Disorders and Outcomes of Patients Hospitalized With Community-Acquired Pneumonia. JAMA Netw Open. 2019; 2(6):e195172. PMC: 6563577. DOI: 10.1001/jamanetworkopen.2019.5172. View

Garmendia J, Morey P, Bengoechea J . Impact of cigarette smoke exposure on host-bacterial pathogen interactions. Eur Respir J. 2011; 39(2):467-77. DOI: 10.1183/09031936.00061911. View

Berger J, Simet S, DeVasure J, Boten J, Sweeter J, Kharbanda K . Malondialdehyde-acetaldehyde (MAA) adducted proteins bind to scavenger receptor A in airway epithelial cells. Alcohol. 2014; 48(5):493-500. PMC: 4128016. DOI: 10.1016/j.alcohol.2014.02.005. View

10.

Gotoh T, Ueda S, Nakayama T, TAKISHITA Y, Yasuoka S, Tsubura E . Protein components of bronchoalveolar lavage fluids from non-smokers and smokers. Eur J Respir Dis. 1983; 64(5):369-77. View

11.

Hemann E, McGill J, Legge K . Chronic ethanol exposure selectively inhibits the influenza-specific CD8 T cell response during influenza a virus infection. Alcohol Clin Exp Res. 2014; 38(9):2403-13. PMC: 4461571. DOI: 10.1111/acer.12522. View

12.

Bechara R, Brown L, Roman J, Joshi P, Guidot D . Transforming growth factor beta1 expression and activation is increased in the alcoholic rat lung. Am J Respir Crit Care Med. 2004; 170(2):188-94. DOI: 10.1164/rccm.200304-478OC. View

13.

Sapkota M, Burnham E, DeVasure J, Sweeter J, Hunter C, Duryee M . Malondialdehyde-Acetaldehyde (MAA) Protein Adducts Are Found Exclusively in the Lungs of Smokers with Alcohol Use Disorders and Are Associated with Systemic Anti-MAA Antibodies. Alcohol Clin Exp Res. 2017; 41(12):2093-2099. PMC: 5711572. DOI: 10.1111/acer.13509. View

14.

Sollid L, Kvale D, Brandtzaeg P, Markussen G, Thorsby E . Interferon-gamma enhances expression of secretory component, the epithelial receptor for polymeric immunoglobulins. J Immunol. 1987; 138(12):4303-6. View

15.

McCaskill M, Kharbanda K, Tuma D, Reynolds J, DeVasure J, Sisson J . Hybrid malondialdehyde and acetaldehyde protein adducts form in the lungs of mice exposed to alcohol and cigarette smoke. Alcohol Clin Exp Res. 2011; 35(6):1106-13. PMC: 3097262. DOI: 10.1111/j.1530-0277.2011.01443.x. View

16.

Wyatt T, Bailey K, Simet S, Warren K, Sweeter J, DeVasure J . Alcohol potentiates RSV-mediated injury to ciliated airway epithelium. Alcohol. 2019; 80:17-24. PMC: 7100607. DOI: 10.1016/j.alcohol.2018.07.010. View

17.

Bailey K, Smith H, Mathai S, Huber J, Yacoub M, Yang I . Alcohol Use Disorders Are Associated With a Unique Impact on Airway Epithelial Cell Gene Expression. Alcohol Clin Exp Res. 2020; 44(8):1571-1584. PMC: 7484391. DOI: 10.1111/acer.14395. View

18.

Croft J, Wheaton A, Liu Y, Xu F, Lu H, Matthews K . Urban-Rural County and State Differences in Chronic Obstructive Pulmonary Disease - United States, 2015. MMWR Morb Mortal Wkly Rep. 2018; 67(7):205-211. PMC: 5858043. DOI: 10.15585/mmwr.mm6707a1. View

19.

You Y, Richer E, Huang T, Brody S . Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am J Physiol Lung Cell Mol Physiol. 2002; 283(6):L1315-21. DOI: 10.1152/ajplung.00169.2002. View

20.

Yeligar S, Chen M, Kovacs E, Sisson J, Burnham E, Brown L . Alcohol and lung injury and immunity. Alcohol. 2016; 55:51-59. PMC: 5319482. DOI: 10.1016/j.alcohol.2016.08.005. View