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Effects of cigarette smoke extract on bronchial epithelial cells stimulated with Cryptococcus neoformans

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Abstract

In the airways, the adhesion of Cryptococcus neoformans with airway epithelial cells is crucial for the establishment of cryptococcosis. Tobacco smoke is considered a risk factor for cryptococcosis. Here, we evaluated the effects of cigarette smoke extract (CSE) on human bronchial epithelial cells (BEAS-2B) stimulated with C. neoformans. Multiplicities of infection (MOIs) of 1–100 of C. neoformans per cell led to increased IL-8 production and no cytotoxic effects when compared to those of controls. C. neoformans (MOI 100) also significantly increased the concentration of IL-6. In cells stimulated with CSE doses (1.0, 2.5 and 5.0%) from one or five cigarettes, increased IL-1β production was observed only in doses from one (1.0%) and five (2.5%) cigarettes when compared to that of controls. However, only 1.0% CSE failed to show cytotoxic effects. In addition, CSE significantly increased the concentration of IL-8. Cells stimulated with both CSE and C. neoformans demonstrated a reduction in IL-6/STAT3 signalling compared to that in cells stimulated by C. neoformans. In addition, a significant increase in IL-10 production was also observed. No alterations in NF-kB or ICAM-1 expression were observed among the groups. The combination of CSE and C. neoformans favoured the increase of fungal numbers and extracellular adhering of C. neoformans on BEAS-2B cells. In addition, the internalization of C. neoformans on BEAS-2B cells was reduced after CSE stimulation. In conclusion, the association of CSE and C. neoformans induced an anti-inflammatory effect in bronchial epithelial cells, which might favour the development of C. neoformans infection in the airways.

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References

  1. Negroni R (2012) Cryptococcosis. Clin Dermatol 30(6):599–609

    Article  Google Scholar 

  2. Blanco JL, Garcia ME (2008) Immune response to fungal infections. Vet Immunol Immunopathol 125(1–2):47–70

    Article  CAS  Google Scholar 

  3. Gullo FP, Rossi SA, Sardi Jde C, Teodoro VL, Mendes-Giannini MJ, Fusco-Almeida AM (2013) Cryptococcosis: epidemiology, fungal resistance, and new alternatives for treatment. Eur J Clin Microbiol Infect Dis 32(11):1377–1391

    Article  CAS  Google Scholar 

  4. Chen K, Kolls JK (2013) T Cell-Mediated Host Immune Defenses in the Lung. Annu Rev Immunol 31:605–633

    Article  CAS  Google Scholar 

  5. Chayakulkeeree M, Perfect JR (2006) Cryptococcosis. Infect Dis Clin North Am 20(3):507–544

    Article  Google Scholar 

  6. Traynor TR, Huffnagle GB (2001) Role of chemokines in fungal infections. Med Mycol 39(1):41–50

    Article  CAS  Google Scholar 

  7. Thorley AJ, Tetley TD (2007) Pulmonary epithelium, cigarette smoke, and chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 2(4):409–428 (PMID: 18268916; PMCID: PMC2699967)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Huston SM, Mody CH (2009) Cryptococcosis: an emerging respiratory mycosis. Clin Chest Med 30(2):253–264

    Article  Google Scholar 

  9. Domej W, Oettl K, Renner W (2014) Oxidative stress and free radicals in COPD – implications and relevance for treatment. Int J Chron Obstruct Pulmon Dis 9:1207–1224

    Article  Google Scholar 

  10. Wang Y, Aisen P, Casadevall A (1995) Cryptococcus neoformans melanin and virulence: mechanism of action. Infect Immun 63(8):3131–3136

    Article  CAS  Google Scholar 

  11. Hiemstra PS, Grootaers G, van der Does AM, Krul CAM, Kooter IM (2018) Human lung epithelial cell cultures for analysis of inhaled toxicants: lessons learned and future directions. Toxicol In Vitro 47:137–146. https://doi.org/10.1016/j.tiv.2017.11.005

    Article  CAS  PubMed  Google Scholar 

  12. Courcot E, Leclerc J, Lafitte JJ et al (2012) Xenobiotic metabolism and disposition in human lung cell models: comparison with in vivo expression profiles. Drug Metab Dispos 40(10):1953–1965. https://doi.org/10.1124/dmd.112.046896

    Article  CAS  PubMed  Google Scholar 

  13. Zhang H, Liu H, Borok Z, Davies KJ, Ursini F, Forman HJ (2012) Cigarette smoke extract stimulates epithelial-mesenchymal transition through Src activation. Free Radic Biol Med 52(8):1437–1442

    Article  CAS  Google Scholar 

  14. Li D, Hu J, Wang T, Zhang X, Liu L, Wang H, Wu Y, Xu D, Wen F (2016) Silymarin attenuates cigarette smoke extract-induced inflammation via simultaneous inhibition of autophagy and ERK/p38 MAPK pathway in human bronchial epithelial cells. Sci Rep 22(6):37751

    Article  Google Scholar 

  15. Liew KL, Jee JM, Yap I, Yong PV (2016) In vitro analysis of metabolites secreted during infection of lung epithelial cells by cryptococcus neoformans. PLoS ONE 11(4):e0153356

    Article  Google Scholar 

  16. Guillot L, Carroll SF, Badawy M, Qureshi ST (2008) Cryptococcus neoformans induces IL-8 secretion and CXCL1 expression by human bronchial epithelial cells. Respir Res 22(9):9

    Article  Google Scholar 

  17. Jang JH, Bruse S, Liu Y, Duffy V, Zhang C, Oyamada N, Randell S, Matsumoto A, Thompson DC, Lin Y, Vasiliou V, Tesfaigzi Y, Nyunoya T (2014) Aldehyde dehydrogenase 3A1 protects airway epithelial cells from cigarette smoke-induced DNA damage and cytotoxicity. Free Radic Biol Med 68:80–86

    Article  CAS  Google Scholar 

  18. de Oliveira JR, Favarin DC, Tanaka SC, Balarin MA, Teixeira DN, Levy BD, Rogério AP (2015) AT-RvD1 modulates CCL-2 and CXCL-8 production and NF-κB, STAT-6, SOCS1, and SOCS3 expression on bronchial epithelial cells stimulated with IL-4. Biomed Res Int 2015:178369. https://doi.org/10.1155/2015/178369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Xie L, Galettis A, Morris J, Jackson C, Twigg SM, Gallery ED (2008) Intercellular adhesion molecule-1 (ICAM-1) expression is necessary for monocyte adhesion to the placental bed endothelium and is increased in type 1 diabetic human pregnancy. Diabetes Metab Res Rev 24(4):294–300

    Article  CAS  Google Scholar 

  20. Chaka W, Scharringa J, Verheul AF, Verhoef J, Van Strijp AG, Hoepelman IM (1995) Quantitative analysis of phagocytosis and killing of Cryptococcus neoformans by human peripheral blood mononuclear cells by flow cytometry. Clin Diagn Lab Immunol 2(6):753–759

    Article  CAS  Google Scholar 

  21. Kamonkhantikul K, Arksornnukit M, Takahashi H (2017) Antifungal, optical, and mechanical properties of polymethylmethacrylate material incorporated with silanized zinc oxide nanoparticles. Int J Nanomed 27(12):2353–2360

    Article  Google Scholar 

  22. Khan ZU (2006) Smoking, melanization, and cryptococcosis: is there a connection? J Clin Microbiol 44(3):1207

    Article  CAS  Google Scholar 

  23. Campbell Reardon C, Kim SJ, Wagner RP, Koziel H, Kornfield H (1996) Phagocytosis and growth inhibition of Cryptococcus neoformans by human alveolar macrophages: effects of HIV-1 infection. AIDS 10:613–618

    Article  Google Scholar 

  24. Tam A, Wadsworth S, Dorscheid D, Man SF, Sin DD (2011) The airway epithelium: more than just a structural barrier. Ther Adv Respir Dis 5(4):255–273. https://doi.org/10.1177/1753465810396539

    Article  PubMed  Google Scholar 

  25. Peeters PM, Wouters EF, Reynaert NL (2015) Immune homeostasis in epithelial cells: evidence and role of inflammasome signaling reviewed. J Immunol Res 2015:828264. https://doi.org/10.1155/2015/828264

    Article  PubMed  PubMed Central  Google Scholar 

  26. Amatngalim GD, Hiemstra PS (2018) Airway epithelial cell function and respiratory host defense in chronic obstructive pulmonary disease. Chin Med J (Engl) 131(9):1099–1107. https://doi.org/10.4103/0366-6999.230743.PMID:29692382;PMCID:PMC5937320

    Article  Google Scholar 

  27. Li Z, Lu G, Meng G (2019) Pathogenic fungal infection in the lung. Front Immunol 10:1524. https://doi.org/10.3389/fimmu.2019.01524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kany S, Vollrath JT, Relja B (2019) Cytokines in inflammatory disease. Int J Mol Sci 20(23):6008. https://doi.org/10.3390/ijms20236008.PMID:31795299;PMCID:PMC6929211

    Article  CAS  PubMed Central  Google Scholar 

  29. Delfino D, Cianci L, Lupis E, Celeste A, Petrelli ML, Curro F et al (1997) Interleukin-6 production by human monocytes stimulated with Cryptococcus neoformans components. Infect Immun 65:2454–2456

    Article  CAS  Google Scholar 

  30. Rizzo J, Oliveira DL, Joffe LS, Hu G, Gazos-Lopes F, Fonseca FL, Almeida IC, Frases S, Kronstad JW, Rodrigues ML (2014) Role of the Apt1 protein in polysaccharide secretion by Cryptococcus neoformans. Eukaryot Cell 13(6):715–726

    Article  Google Scholar 

  31. Li X, Liu G, Ma J, Zhou L, Zhang Q, Gao L (2015) Lack of IL-6 increases blood-brain barrier permeability in fungal meningitis. J Biosci 40(1):7–12. https://doi.org/10.1007/s12038-014-9496-y

    Article  CAS  PubMed  Google Scholar 

  32. Donaldson GC, Seemungal TA, Patel IS et al (2005) Airway and systemic inflammation and decline in lung function in patients with COPD. Chest 128(4):1995–2004. https://doi.org/10.1378/chest.128.4.1995

    Article  PubMed  Google Scholar 

  33. Grubek-Jaworska H, Paplińska M, Hermanowicz-Salamon J et al (2012) IL-6 and IL-13 in induced sputum of COPD and asthma patients: correlation with respiratory tests. Respiration 84(2):101–107. https://doi.org/10.1159/000334900

    Article  CAS  PubMed  Google Scholar 

  34. Celli BR, Locantore N, Yates J et al (2012) Inflammatory biomarkers improve clinical prediction of mortality in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 185(10):1065–1072. https://doi.org/10.1164/rccm.201110-1792OC

    Article  CAS  PubMed  Google Scholar 

  35. Hutchins AP, Diez D, Miranda-Saavedra D (2013) The IL-10/STAT3-mediated anti-inflammatory response: recent developments and future challenges. Brief Funct Genomics 12(6):489–498

    Article  CAS  Google Scholar 

  36. Hillmer EJ, Zhang H, Li HS, Watowich SS (2016) STAT3 signaling in immunity. Cytokine Growth Factor Rev 31:1–15. https://doi.org/10.1016/j.cytogfr.2016.05.001

    Article  PubMed  PubMed Central  Google Scholar 

  37. Geraghty P, Wyman AE, Garcia-Arcos I, Dabo AJ, Gadhvi S, Foronjy R (2013) STAT3 modulates cigarette smoke-induced inflammation and protease expression. Front Physiol 4:267

    Article  Google Scholar 

  38. Liu X (2007) STAT3 activation inhibits human bronchial epithelial cell apoptosis in response to cigarette smoke exposure. Biochem Biophys Res Commun 353(1):121–126. https://doi.org/10.1016/j.bbrc.2006.11.147

    Article  CAS  PubMed  Google Scholar 

  39. Maruvada R, Zhu L, Pearce D, Zheng Y, Perfect J, Kwon-Chung KJ, Kim KS (2012) Cryptococcus neoformans phospholipase B1 activates host cell Rac1 for traversal across the blood-brain barrier. Cell Microbiol 14(10):1544–15453. https://doi.org/10.1111/j.1462-5822.2012.01819.x (Epub 2012 Jun 26. PMID: 22646320; PMCID: PMC344326)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chaudhry H, Zhou J, Zhong Y et al (2013) Role of cytokines as a double-edged sword in sepsis. Vivo 27(6):669–684

    CAS  Google Scholar 

  41. Sahoo M, Ceballos-Olvera I, del Barrio L, Re F (2011) Role of the inflammasome, IL-1β, and IL-18 in bacterial infections. Scient World J 11:2037–2050. https://doi.org/10.1100/2011/212680

    Article  CAS  Google Scholar 

  42. Dinarello CA (1992) The role of interleukin-1 in host responses to infectious diseases. Infect Agents Dis 1(5):227–236

    CAS  PubMed  Google Scholar 

  43. Shin NR, Ryu HW, Ko JW, Park JW, Kwon OK, Oh SR, Kim JC, Shin IS, Ahn KS (2016) A standardized bark extract of Pinus pinaster Aiton (Pycnogenol®) attenuated chronic obstructive pulmonary disease via Erk-sp1 signaling pathway. J Ethnopharmacol 24(194):412–420

    Article  Google Scholar 

  44. Boulware DR, von Hohenberg M, Rolfes MA, Bahr NC, Rhein J, Akampurira A, Williams DA, Taseera K, Schutz C, McDonald T, Muzoora C, Meintjes G, Meya DB, Nielsen K, Huppler HK (2015) Human immune response varies by the degree of relative cryptococcal antigen shedding. Open Forum Infect Dis 3(1):194

    Article  Google Scholar 

  45. Vecchiarelli A, Retini C, Pietrella D et al (1995) Downregulation by cryptococcal polysaccharide of tumor necrosis factor alpha and interleukin-1 beta secretion from human monocytes. Infect Immun 63(8):2919–2923

    Article  CAS  Google Scholar 

  46. Chen M, Xing Y, Lu A et al (2015) Internalized Cryptococcus neoformans activates the canonical Caspase-1 and the noncanonical Caspase-8 inflammasomes. J Immunol 195(10):4962–4972. https://doi.org/10.4049/jimmunol.1500865

    Article  CAS  PubMed  Google Scholar 

  47. Upadhya R, Lam WC, Maybruck B, Specht CA, Levitz SM, Lodge JK (2016) Induction of protective immunity to cryptococcal infection in mice by a heat-killed chitosan-deficient strain of cryptococcus neoformans. MBio 7(3):e00547-e1516. https://doi.org/10.1128/mBio.00547-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Manabu H, Hiroo W, Tetsuo Y, Shinichiro M, Kojiro H, Masuo N, Mamoru N, Fumie K, Shigeru K, Hajime G (2011) IL-10 resolves the neutrophilic inflammation in mice exposed to cigarette smoke. Eur Res J 38:419

    Google Scholar 

  49. Hussain T, Shah SZA, Zhao D, Sreevatsan S, Zhou X (2016) The role of IL-10 in Mycobacterium avium subsp Paratuberculosis infection. Cell Commun Signal 14:29

    Article  Google Scholar 

  50. Jafari-Nedooshan J, Moghimi M, Zare M, Heiranizadeh N, Morovati-Sharifabad M, Akbarian-Bafghi MJ, Jarahzadeh MH, Neamatzadeh H (2019) Association of promoter region polymorphisms of IL-10 gene with susceptibility to lung cancer: systematic review and meta-analysis. Asian Pac J Cancer Prev 20(7):1951–1957. https://doi.org/10.31557/APJCP.2019.20.7.1951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Retini C, Kozel TR, Pietrella D, Monari C, Bistoni F, Vecchiarelli A (2001) Interdependency of interleukin-10 and interleukin-12 in regulation of T-cell differentiation and effector function of monocytes in response to stimulation with Cryptococcus neoformans. Infect Immun 69(10):6064–6073. https://doi.org/10.1128/IAI.69.10.6064-6073.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lortholary O, Improvisi L, Rayhane N et al (1999) Cytokine profiles of AIDS patients are similar to those of mice with disseminated Cryptococcus neoformans infection. Infect Immun 67(12):6314–6320

    Article  CAS  Google Scholar 

  53. Scriven JE, Graham LM, Schutz C et al (2016) A glucuronoxylomannan-associated immune signature, characterized by monocyte deactivation and an increased interleukin 10 level, Is a predictor of death in cryptococcal meningitis. J Infect Dis 213(11):1725–1734. https://doi.org/10.1093/infdis/jiw007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Silva BSA, Lira FS, Ramos D et al (2018) Severity of COPD and its relationship with IL-10. Cytokine 106:95–100. https://doi.org/10.1016/j.cyto.2017.10.018

    Article  CAS  PubMed  Google Scholar 

  55. Takanashi S, Hasegawa Y, Kanehira Y et al (1999) Interleukin-10 level in sputum is reduced in bronchial asthma, COPD and in smokers. Eur Respir J 14(2):309–314. https://doi.org/10.1034/j.1399-3003.1999.14b12.x

    Article  CAS  PubMed  Google Scholar 

  56. Mednick AJ, Nosanchuk JD, Casadevall A (2005) Melanization of Cryptococcus neoformans affects lung inflammatory responses during cryptococcal infection. Infect Immun 73(4):2012–2019. https://doi.org/10.1128/IAI.73.4.2012-2019.2005.PMID:15784542;PMCID:PMC1087470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Mohagheghpour N, Waleh N, Garger SJ, Dousman L, Grill LK, Tusé D (2000) Synthetic melanin suppresses production of proinflammatory cytokines. Cell Immunol 199(1):25–36. https://doi.org/10.1006/cimm.1999.1599 (PMID: 10675272)

    Article  CAS  PubMed  Google Scholar 

  58. Rohatgi S, Pirofski LA (2015) Host immunity to cryptococcus neoformans. Future Microbiol 10(4):565–581. https://doi.org/10.2217/fmb.14.132.PMID:25865194;PMCID:PMC4523559

    Article  CAS  PubMed  Google Scholar 

  59. Feldman C, Anderson R (2013) Cigarette smoking and mechanisms of susceptibility to infections of the respiratory tract and other organ systems. J Infect 67(3):169–184. https://doi.org/10.1016/j.jinf.2013.05.004 (Epub 2013 May 21 PMID: 23707875)

    Article  PubMed  Google Scholar 

  60. Garmendia J, Morey P, Bengoechea JA (2012) Impact of cigarette smoke exposure on host-bacterial pathogen interactions. Eur Respir J 39(2):467–477. https://doi.org/10.1183/09031936.00061911 (Epub 2011 Jul 7 PMID: 21737564)

    Article  CAS  PubMed  Google Scholar 

  61. Taylor-Smith LM (2017) Cryptococcus-epithelial adhesions. J Fungi (Basel) 3(4):53. https://doi.org/10.3390/jof3040053

    Article  CAS  Google Scholar 

  62. Taylor-Smith LM, May RC (2016) New weapons in the Cryptococcus infection toolkit. Curr Opin Microbiol 34:67–74

    Article  CAS  Google Scholar 

  63. Yoneshige A, Hagiyama M, Fujita M, Ito A (2015) Pathogenic actions of cell adhesion molecule 1 in pulmonary emphysema and atopic dermatitis. Front Cell Dev Biol 20(3):75

    Google Scholar 

  64. Hubbard AK, Rothlein R (2000) Intercellular adhesion molecule- 1 (ICAM-1) expression and cell signaling cascades. Free Radic Biol Med 28:1379–1386

    Article  CAS  Google Scholar 

  65. Zandvoort A, van der Geld YM, Jonker MR, Noordhoek JA, Vos JT, Wesseling J, Kauffman HF, Timens W, Postma DS (2006) High ICAM-1 gene expression in pulmonary fibroblasts of COPD patients: a reflection of an enhanced immunological function. Eur Respir J 28(1):113–122

    Article  CAS  Google Scholar 

  66. Buchanan KL, Murphy JW (1998) What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis 4(1):71–83

    Article  CAS  Google Scholar 

  67. Hayden MS, Ghosh S (2011) NF-κB in immunobiology. Cell Res 21(2):223–244. https://doi.org/10.1038/cr.2011.13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Rastrick JM, Stevenson CS, Eltom S, Grace M, Davies M, Kilty I, Evans SM, Pasparakis M, Catley MC, Lawrence T, Adcock IM, Belvisi MG, Birrell MA (2013) Cigarette smoke induced airway inflammation is independent of NF-κB signalling. PLoS ONE 8(1):54128

    Article  Google Scholar 

  69. Shoham S et al (2001) "Toll-like receptor 4 mediates intracellular signaling without TNF-α release in response to Cryptococcus neoformans polysaccharide capsule. J Immunol 166(7):4620–4626

    Article  CAS  Google Scholar 

  70. Eblen ST (2018) Extracellular-Regulated Kinases: Signaling From Ras to ERK Substrates to Control Biological Outcomes. Adv Cancer Res 138:99–142. https://doi.org/10.1016/bs.acr.2018.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Mercer BA, D’Armiento JM (2006) Emerging role of MAP kinase pathways as therapeutic targets in COPD. Int J Chron Obstruct Pulmon Dis 1(2):137–150. https://doi.org/10.2147/copd.2006.1.2.137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Pericolini E, Gabrielli E, Bistoni G et al (2010) Role of CD45 signaling pathway in galactoxylomannan-induced T cell damage. PLoS ONE 5(9):12720. https://doi.org/10.1371/journal.pone.0012720

    Article  CAS  Google Scholar 

  73. Merkel GJ, Scofield BA (2000) The effects of Cryptococcus neoformans-secreted antigens on tumor necrosis factor-α-induced intercellular adhesion molecule-1 expression on human lung epithelial cells. FEMS Immunol Med Microbiol 29:329–332. https://doi.org/10.1016/S0928-8244(00)00222-4

    Article  CAS  PubMed  Google Scholar 

  74. Jones CP, Pitchford SC, Lloyd CM, Rankin SM (2009) CXCR2 mediates the recruitment of endothelial progenitor cells during allergic airways remodeling. Stem Cells 27(12):3074–3081. https://doi.org/10.1002/stem.222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kroeze KL, Boink MA, Sampat-Sardjoepersad SC, Waaijman T, Scheper RJ, Gibbs S (2012) Autocrine regulation of re-epithelialization after wounding by chemokine receptors CCR1, CCR10, CXCR1, CXCR2, and CXCR3. J Invest Dermatol 132(1):216–225. https://doi.org/10.1038/jid.2011.245

    Article  CAS  PubMed  Google Scholar 

  76. Matsukawa A, Lukacs NW, Standiford TJ, Chensue SW, Kunkel SL (2000) Adenoviral-mediated overexpression of monocyte chemoattractant protein-1 differentially alters the development of Th1 and Th2 type responses in vivo. J Immunol 164(4):1699–1704. https://doi.org/10.4049/jimmunol.164.4.1699

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by Grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (no. 475349/2010-5), Fundação de Apoio a Pesquisa do Estado de Minas Gerais (FAPEMIG; APQ 01631/11 e APQ-01873-14), Rede de Pesquisa em Doenças Infecciosas Humanas e Animais do Estado de Minas Gerais and Universidade Federal do Triângulo Mineiro (UFTM), Brazil. This study was financed in part by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) –Finance Code 001.

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  1. Laboratory of Experimental Immunopharmacology, Department of Clinical Medicine, Institute of Health Sciences, Federal University of Triangulo Mineiro, Street Vigário Carlos 162, Uberaba, MG, 38025-380, Brazil

    Aline Beatriz Mahler Pereira, Jhony Robison Oliveira, Ana Leticia Julio Souza, Paulo Roberto Silva & Alexandre Paula Rogerio

  2. Laboratory of Mycology, Department of Clinical Medicine, Institute of Health Sciences, Federal University of Triangulo Mineiro, Uberaba, MG, Brazil

    Leonardo Andrade-Silva & Mario Leon Silva-Vergara

  3. Laboratory of Immunology, Institute Department of Clinical Medicine, of Health Sciences, Federal University of Triangulo Mineiro, Uberaba, MG, Brazil

    Marcos Vinicius Silva

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  1. Aline Beatriz Mahler Pereira
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Pereira, A., Oliveira, J., Souza, A. et al. Effects of cigarette smoke extract on bronchial epithelial cells stimulated with Cryptococcus neoformans. Med Microbiol Immunol 210, 221–233 (2021). https://doi.org/10.1007/s00430-021-00715-4

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