Janus-faced Acrolein prevents allergy but accelerates tumor growth by promoting immunoregulatory Foxp3+ cells: Mouse model for passive respiratory exposure

. 2017 Mar 23 ; 7 () : 45067. [epub] 20170323

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28332605

Acrolein, a highly reactive unsaturated aldehyde, is generated in large amounts during smoking and is best known for its genotoxic capacity. Here, we aimed to assess whether acrolein at concentrations relevant for smokers may also exert immunomodulatory effects that could be relevant in allergy or cancer. In a BALB/c allergy model repeated nasal exposure to acrolein abrogated allergen-specific antibody and cytokine formation, and led to a relative accumulation of regulatory T cells in the lungs. Only the acrolein-treated mice were protected from bronchial hyperreactivity as well as from anaphylactic reactions upon challenge with the specific allergen. Moreover, grafted D2F2 tumor cells grew faster and intratumoral Foxp3+ cell accumulation was observed in these mice compared to sham-treated controls. Results from reporter cell lines suggested that acrolein acts via the aryl-hydrocarbon receptor which could be inhibited by resveratrol and 3'-methoxy-4'-nitroflavone Acrolein- stimulation of human PBMCs increased Foxp3+ expression by T cells which could be antagonized by resveratrol. Our mouse and human data thus revealed that acrolein exerts systemic immunosuppression by promoting Foxp3+ regulatory cells. This provides a novel explanation why smokers have a lower allergy, but higher cancer risk.

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Roy J., Pallepati P., Bettaieb A., Tanel A. & Averill-Bates D. A. Acrolein induces a cellular stress response and triggers mitochondrial apoptosis in A549 cells. Chem Biol Interact 181, 154–167 (2009). PubMed

Alwis K. U., deCastro B. R., Morrow J. C. & Blount B. C. Acrolein Exposure in U.S. Tobacco Smokers and Non-Tobacco Users: NHANES 2005–2006. Environ Health Perspect 123, 1302–1308 (2015). PubMed PMC

Daher N. et al.. Comparison of carcinogen, carbon monoxide, and ultrafine particle emissions from narghile waterpipe and cigarette smoking: Sidestream smoke measurements and assessment of second-hand smoke emission factors. Atmos Environ (1994) 44, 8–14 (2010). PubMed PMC

Herrington J. S. & Myers C. Electronic cigarette solutions and resultant aerosol profiles. J Chromatogr A(2015). PubMed

Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol 2, 372–377 (2002). PubMed

Cassee F. R., Groten J. P. & Feron V. J. Changes in the nasal epithelium of rats exposed by inhalation to mixtures of formaldehyde, acetaldehyde, and acrolein. Fundam Appl Toxicol 29, 208–218 (1996). PubMed

Bein K. & Leikauf G. D. Acrolein - a pulmonary hazard. Molecular nutrition & food research 55, 1342–1360 (2011). PubMed

Toxicological Profile for Acrolein. 227 (U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES, 2007).

Abraham K. et al.. Toxicology and risk assessment of acrolein in food. Molecular nutrition & food research 55, 1277–1290 (2011). PubMed

Stevens J. F. & Maier C. S. Acrolein: sources, metabolism, and biomolecular interactions relevant to human health and disease. Molecular nutrition & food research 52, 7–25 (2008). PubMed PMC

Eckert E. et al.. Mercapturic acids as metabolites of alkylating substances in urine samples of German inhabitants. Int J Hyg Environ Health 214, 196–204 (2011). PubMed

Carmella S. G. et al.. Quantitation of acrolein-derived (3-hydroxypropyl)mercapturic acid in human urine by liquid chromatography-atmospheric pressure chemical ionization tandem mass spectrometry: effects of cigarette smoking. Chem Res Toxicol 20, 986–990 (2007). PubMed PMC

Schettgen T., Musiol A. & Kraus T. Simultaneous determination of mercapturic acids derived from ethylene oxide (HEMA), propylene oxide (2-HPMA), acrolein (3-HPMA), acrylamide (AAMA) and N,N-dimethylformamide (AMCC) in human urine using liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 22, 2629–2638 (2008). PubMed

Shargorodsky J., Garcia-Esquinas E., Navas-Acien A. & Lin S. Y. Allergic sensitization, rhinitis, and tobacco smoke exposure in U.S. children and adolescents. Int Forum Allergy Rhinol 5, 471–476 (2015). PubMed PMC

Havstad S. L. et al.. Tobacco smoke exposure and allergic sensitization in children: a propensity score analysis. Respirology 17, 1068–1072 (2012). PubMed PMC

Vonk J. M. et al.. Perinatal risk factors for bronchial hyperresponsiveness and atopy after a follow-up of 20 years. The Journal of allergy and clinical immunology 114, 270–276 (2004). PubMed

Shargorodsky J., Garcia-Esquinas E., Galan I., Navas-Acien A. & Lin S. Y. Allergic Sensitization, Rhinitis and Tobacco Smoke Exposure in US Adults. PloS one 10, e0131957 (2015). PubMed PMC

Wulaningsih W. et al.. Investigating the association between allergen-specific immunoglobulin E, cancer risk and survival. Oncoimmunology 5, e1154250 (2016). PubMed PMC

Jensen-Jarolim E. et al.. AllergoOncology - The impact of Allergy in Oncology. EAACI Position Paper. AllergyDec 29. doi: 10.1111/all.13119. [Epub ahead of print] (2016). PubMed PMC

Egle J. L. Jr. Retention of inhaled formaldehyde, propionaldehyde, and acrolein in the dog. Arch Environ Health 25, 119–124 (1972). PubMed

Kasahara D. I., Poynter M. E., Othman Z., Hemenway D. & van der Vliet A. Acrolein inhalation suppresses lipopolysaccharide-induced inflammatory cytokine production but does not affect acute airways neutrophilia. J Immunol 181, 736–745 (2008). PubMed PMC

O’Brien E. et al.. Inhalation of the reactive aldehyde acrolein promotes antigen sensitization to ovalbumin and enhances neutrophilic inflammation. J Immunotoxicol 13, 191–197 (2016). PubMed PMC

Spiess P. C. et al.. Acrolein exposure suppresses antigen-induced pulmonary inflammation. Respir Res 14, 107 (2013). PubMed PMC

Struve M. F. et al.. Nasal uptake of inhaled acrolein in rats. Inhal Toxicol 20, 217–225 (2008). PubMed

Babjuk M. et al.. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2013. Eur Urol 64, 639–653 (2013). PubMed

Hodi F. S. et al.. Improved Survival with Ipilimumab in Patients with Metastatic Melanoma. New Engl J Med 363, 711–723 (2010). PubMed PMC

Melero I., Hervas-Stubbs S., Glennie M., Pardoll D. M. & Chen L. Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer 7, 95–106 (2007). PubMed

Gerondakis S. et al.. Unravelling the complexities of the NF-kappaB signalling pathway using mouse knockout and transgenic models. Oncogene 25, 6781–6799 (2006). PubMed

Roth-Walter F. et al.. Immune suppressive effect of cinnamaldehyde due to inhibition of proliferation and induction of apoptosis in immune cells: implications in cancer. PloS one 9, e108402 (2014). PubMed PMC

Novotna A., Pavek P. & Dvorak Z. Novel stably transfected gene reporter human hepatoma cell line for assessment of aryl hydrocarbon receptor transcriptional activity: construction and characterization. Environ Sci Technol 45, 10133–10139 (2011). PubMed

Du L., Neis M. M., Ladd P. A. & Keeney D. S. Differentiation-specific factors modulate epidermal CYP1-4 gene expression in human skin in response to retinoic acid and classic aryl hydrocarbon receptor ligands. The Journal of pharmacology and experimental therapeutics 319, 1162–1171 (2006). PubMed

Revel A. et al.. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects lung from DNA damage and apoptosis caused by benzo[a]pyrene. J Appl Toxicol 23, 255–261 (2003). PubMed

Singh S. U. et al.. Inhibition of dioxin effects on bone formation in vitro by a newly described aryl hydrocarbon receptor antagonist, resveratrol. J Endocrinol 167, 183–195 (2000). PubMed

Hancox R. J. et al.. Cigarette smoking and allergic sensitization: a 32-year population-based cohort study. The Journal of allergy and clinical immunology 121, 38–42 e33 (2008). PubMed

Yamazaki S. et al.. Patterns of Sensitization to Inhalant Allergens in Japanese Lower-Grade Schoolchildren and Related Factors. Int Arch Allergy Immunol 167, 253–263 (2015). PubMed

Luo X. et al.. Effect modification by gender and smoking status on the association between obesity and atopic sensitization in Chinese adults: a hospital-based case-control study. BMC Public Health 14, 1105 (2014). PubMed PMC

Eriksson J. et al.. Cigarette smoking is associated with high prevalence of chronic rhinitis and low prevalence of allergic rhinitis in men. Allergy 68, 347–354 (2013). PubMed

Ronmark E., Bjerg A., Perzanowski M., Platts-Mills T. & Lundback B. Major increase in allergic sensitization in schoolchildren from 1996 to 2006 in northern Sweden. The Journal of allergy and clinical immunology 124, 357–363, 363 e351–315 (2009). PubMed PMC

Moore P. A. et al.. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science 285, 260–263 (1999). PubMed

Brandsma C. A. et al.. Heme oxygenase-1 prevents smoke induced B-cell infiltrates: a role for regulatory T cells? Respir Res 9, 17 (2008). PubMed PMC

Lambert C. et al.. Acrolein in cigarette smoke inhibits T-cell responses. J Allergy Clin Immunol 116, 916–922 (2005). PubMed

Hampras S. S. et al.. Predictors of immunosuppressive regulatory T lymphocytes in healthy women. J Cancer Epidemiol 2012, 191090 (2012). PubMed PMC

Dutta A., Bhattacharya P., Lahiri T. & Ray M. R. Immune cells and cardiovascular health in premenopausal women of rural India chronically exposed to biomass smoke during daily household cooking. Sci Total Environ 438, 293–298 (2012). PubMed

Barcelo B. et al.. Phenotypic characterisation of T-lymphocytes in COPD: abnormal CD4+CD25+ regulatory T-lymphocyte response to tobacco smoking. Eur Respir J 31, 555–562 (2008). PubMed

Roos-Engstrand E., Pourazar J., Behndig A. F., Bucht A. & Blomberg A. Expansion of CD4+CD25+ helper T cells without regulatory function in smoking and COPD. Respir Res 12, 74 (2011). PubMed PMC

Wang H. et al.. Imbalance of peripheral blood Th17 and Treg responses in patients with chronic obstructive pulmonary disease. Clin Respir J 9, 330–341 (2015). PubMed

Kalathil S. G. et al.. T-regulatory cells and programmed death 1+ T cells contribute to effector T-cell dysfunction in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 190, 40–50 (2014). PubMed PMC

Plumb J. et al.. Increased T-regulatory cells within lymphocyte follicles in moderate COPD. Eur Respir J 34, 89–94 (2009). PubMed

Isajevs S. et al.. Decreased FOXP3 expression in small airways of smokers with COPD. Eur Respir J 33, 61–67 (2009). PubMed

Peto R. et al.. Smoking, smoking cessation, and lung cancer in the UK since 1950: combination of national statistics with two case-control studies. BMJ 321, 323–329 (2000). PubMed PMC

Guan H. et al.. PD-L1 is a critical mediator of regulatory B cells and T cells in invasive breast cancer. Sci Rep 6, 35651 (2016). PubMed PMC

Tu J. F. et al.. Regulatory T cells, especially ICOS+ FOXP3+ regulatory T cells, are increased in the hepatocellular carcinoma microenvironment and predict reduced survival. Sci Rep 6, 35056 (2016). PubMed PMC

Zhang N. N. et al.. Accumulation Mechanisms of CD4(+)CD25(+)FOXP3(+) Regulatory T Cells in EBV-associated Gastric Carcinoma. Sci Rep 5, 18057 (2015). PubMed PMC

Ortiz-Martinez F. et al.. Association of Notch pathway down-regulation with Triple Negative/Basal-like breast carcinomas and high tumor-infiltrating FOXP3+ Tregs. Exp Mol Pathol 100, 460–468 (2016). PubMed

Geng Y. et al.. Prognostic Role of Tumor-Infiltrating Lymphocytes in Lung Cancer: a Meta-Analysis. Cell Physiol Biochem 37, 1560–1571 (2015). PubMed

Schetter A. J. et al.. Association of inflammation-related and microRNA gene expression with cancer-specific mortality of colon adenocarcinoma. Clin Cancer Res 15, 5878–5887 (2009). PubMed PMC

Fricker M., Deane A. & Hansbro P. M. Animal models of chronic obstructive pulmonary disease. Expert Opin Drug Discov 9, 629–645 (2014). PubMed

Jones B. et al.. Animal models of COPD: What do they tell us? Respirology 22, 21–32 (2017). PubMed

Youn H. S. et al.. Cinnamaldehyde suppresses toll-like receptor 4 activation mediated through the inhibition of receptor oligomerization. Biochem Pharmacol 75, 494–502 (2008). PubMed

Negishi T. et al.. Effects of aryl hydrocarbon receptor signaling on the modulation of TH1/TH2 balance. J Immunol 175, 7348–7356 (2005). PubMed

Schulz V. J. et al.. Non-dioxin-like AhR ligands in a mouse peanut allergy model. Toxicol Sci 128, 92–102 (2012). PubMed

Esser C., Rannug A. & Stockinger B. The aryl hydrocarbon receptor in immunity. Trends Immunol 30, 447–454 (2009). PubMed

Kotecha R., Takami A. & Espinoza J. L. Dietary phytochemicals and cancer chemoprevention: a review of the clinical evidence. Oncotarget(2016). PubMed PMC

Mahoney K. H., Miller B. E. & Heppner G. H. FACS quantitation of leucine aminopeptidase and acid phosphatase on tumor-associated macrophages from metastatic and nonmetastatic mouse mammary tumors. J Leukoc Biol 38, 573–585 (1985). PubMed

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