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The MAPKinase Signaling and the Stimulatory Protein-1 (Sp1) Transcription Factor Are Involved in the Phototherapy Effect on Cytokines Secretion from Human Bronchial Epithelial Cells Stimulated with Cigarette Smoke Extract

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Abstract

The present study was aimed to investigate the phototherapy effect with low-level laser on human bronchial epithelial cells activated by cigarette smoke extract (CSE). Phototherapy has been reported to actuate positively for controlling the generation/release of anti-inflammatory and pro-inflammatory mediators from different cellular type activated by distinct stimuli. It is not known whether the IL-8 and IL-10 release from CSE-stimulated human bronchial epithelium (BEAS) cells can be influenced by phototherapy. Human bronchial epithelial cell (BEAS) line was cultured in a medium with CSE and irradiated (660 nm) at 9 J. Apoptosis index was standardized with Annexin V and the cellular viability was evaluated by MTT. IL-8, IL-10, cAMP, and NF-κB were measured by ELISA as well as the Sp1, JNK, ERK1/2, and p38MAPK. Phototherapy effect was studied in the presence of mithramycin or the inhibitors of JNK or ERK. The IL-8, cAMP, NF-κB, JNK, p38, and ERK1/2 were downregulated by phototherapy. Both the JNK and the ERK inhibitors potentiated the phototherapy effect on IL-8 as well as on cAMP secretion from BEAS. On the contrary, IL-10 and Sp1 were upregulated by phototherapy. The mithramycin blocked the phototherapy effect on IL-10. The results suggest that phototherapy has a dual effect on BEAS cells because it downregulates the IL-8 secretion by interfering with CSE-mediated signaling pathways, and oppositely upregulates the IL-10 secretion through of Sp1 transcription factor.

Graphical Abstract

The manuscript provides evidence that the phototherapy can interfere with MAPK signaling via cAMP in order to attenuate the IL-8 secretion from CSE-stimulated BEAS. In addition, the present study showed that phototherapy effect is driven to downregulation of the both the IL-8 and the ROS secretion and at the same time the upregulation of IL-10 secretion. Besides it, the increase of Sp-1 transcription factor was crucial for laser effect in upregulating the IL-10 secretion. The dexamethasone corticoid produces a significant inhibitory effect on IL-8 as well as ROS secretion, but on the other hand, the corticoid blocked the IL-10 secretion. Taking it into consideration, it is reasonable to suggest that the beneficial effect of laser therapy on lung diseases involves its action on unbalance between pro-inflammatory and anti-inflammatory mediators secreted by human bronchial epithelial cells through different signaling pathway.

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References

  1. Chung, K.F., and I.M. Adcock. 2008. Multifaceted mechanisms in COPD: inflammation, immunity, and tissue repair and destruction. European Respiratory Journal 31: 1334–1356. https://doi.org/10.1183/09031936.00018908.

    Article  CAS  PubMed  Google Scholar 

  2. Thorley, A.J., and T.D. Tetley. 2007. Pulmonary epithelium, cigarette smoke, and chronic obstructive pulmonary disease. International Journal of Chronic Obstructive Pulmonary Disease 2: 409–428.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. de Vries, M., I.H. Heijink, R. Gras, L.E. den Boef, M. Reinders-Luinge, S.D. Pouwels, M.N. Hylkema, M. van der Toorn, U. Brouwer, A.J. van Oosterhout, and M.C. Nawijn. 2014. Pim1 kinase protects airway epithelial cells from cigarette smoke-induced damage and airway inflammation. American Journal of Physiology. Lung Cellular and Molecular Physiology 307: 240–251.

    Article  CAS  Google Scholar 

  4. Abboud, R.T., and S. Vimalanathan. 2008. Pathogenesis of COPD. Part I. The role of protease-antiprotease imbalance in emphysema. The International Journal of Tuberculosis and Lung Disease 12: 361–367.

    CAS  PubMed  Google Scholar 

  5. Mak, J.C. 2008. Pathogenesis of COPD. Part II. Oxidative-antioxidative imbalance. The International Journal of Tuberculosis and Lung Disease 12: 368–374.

    CAS  PubMed  Google Scholar 

  6. Roth, M. 2008. Pathogenesis of COPD. Part III. Inflammation in COPD. The International Journal of Tuberculosis and Lung Disease 12: 375–380.

    CAS  PubMed  Google Scholar 

  7. Fischer, B.M., E. Pavlisko, and J.A. Voynow. 2011. Pathogenic triad in COPD: oxidative stress, protease-antiprotease imbalance, and inflammation. International Journal of Chronic Obstructive Pulmonary Disease 6: 413–421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Plataki, M., E. Tzortzaki, P. Rytila, M. Demosthenes, A. Koutsopoulos, and N.M. Siafakas. 2006. Apoptotic mechanisms in the pathogenesis of COPD. International Journal of Chronic Obstructive Pulmonary Disease 1: 161–171.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Ito, K., and P.J. Barnes. 2009. COPD as a disease of accelerated lung aging. Chest. 135: 173–180.

    Article  PubMed  Google Scholar 

  10. Lee, K.H., C.H. Lee, J. Jeong, A.H. Jang, and C.G. Yoo. 2015. Neutrophil elastase differentially regulates interleukin 8 (IL-8) and vascular endothelial growth factor (VEGF) Production by cigarette smoke extract. The Journal of Biological Chemistry 290: 28438–28445.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. O’Donnell, R., D. Breen, S. Wilson, and R. Djukanovic. 2006. Inflammatory cells in the airways in COPD. Thorax. 61: 448–454.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Deslee, G., T.L. Adair-Kirk, T. Betsuyaku, J.C. Woods, C.H. Moore, D.S. Gierada, S.H. Conradi, J.J. Atkinson, H.M. Toennies, J.T. Battaile, D.K. Kobayashi, G.A. Patterson, M.J. Holtzman, and R.A. Pierce. 2010. Cigarette smoke induces nucleic-acid oxidation in lung fibroblasts. American Journal of Respiratory Cell and Molecular Biology 43: 576–584.

    Article  CAS  PubMed  Google Scholar 

  13. Rahman, I., and I.M. Adcock. 2006. Oxidative stress and redox regulation of lung inflammation in COPD. The European Respiratory Journal 28: 219–242.

    Article  CAS  PubMed  Google Scholar 

  14. Milara, J., G. Juan, T. Peiró, A. Serrano, and J. Cortijo. 2012. Neutrophil activation in severe, early-onset COPD patients versus healthy non-smoker subjects in vitro: effects of antioxidant therapy. Respiration. 83 (2): 147–158.

    Article  CAS  PubMed  Google Scholar 

  15. Bjordal, J.M., M. Johnson, V. Iversen, F. Aimbire, and R. Lopes-Martins. 2006. Photoradiation in acute pain: a systemic review of possible mechanisms of action and clinical effects in randomized placebo-controlled trials. Photomedicine and Laser Surgery 12: 158–168.

    Article  Google Scholar 

  16. Shimizu, N., M. Yamagushi, T. Goseki, Y. Shibata, H. Takiguchi, and T. Iwasawa. 1995. Inhibition of prostaglandin E2 and interleukin-1β production by low power laser irradiation in stretched human periodontal ligament cells. Journal of Dental Research 21: 1382–1388.

    Article  Google Scholar 

  17. Sakurai, Y., M. Yamagushi, and Y. Abiko. 2000. Inhibitory effect of low-level laser irradiation on LPS-stimulated prostaglandin E2 and cyclooxygenase-2 in human gingival fibroblast. European Journal of Oral Sciences 10: 29–34.

    Article  Google Scholar 

  18. Milojevic, M., and V. Kuruc. 2000. Laser biostimulation in the treatment of pleurisy. Medicinski Pregled 18: 516–520.

    Google Scholar 

  19. Landyshev, Iu, N. Avdeeva, N. Goborov, N. Krasavina, G. Tikhonova, and S. Tkacheva. 2002. Efficacy of low intensity laser irradiation and sodium nedocromil in the complex treatment of patients with bronchial asthma. Terapevticheskiĭ Arkhiv 12: 25–28.

    Google Scholar 

  20. Ostronosova, N. 2006. Outpatient use of laser therapy in bronchial asthma. Terapevticheskiĭ Arkhiv 21: 41–44.

    Google Scholar 

  21. Lin, F., S.F. Josephs, D.T. Alexandrescu, F. Ramos, V. Bogin, V. Gammill, C.A. Dasanu, R. De Necochea-Campion, A.N. Patel, E. Carrier, and D.R. Koos. 2010. Lasers, stem cells, and COPD. Journal of Translational Medicine 16: 8–16.

    Google Scholar 

  22. Nikitin, A.V., and S.I. Marks. 2014. The application of chromo- and laserotherapy for the treatment of the patients presenting with chronic obstructive pulmonary disease and concomitant arterial hypertension. Voprosy Kurortologii, Fizioterapii, i Lechebnoĭ Fizicheskoĭ Kultury 4: 3–6.

    Google Scholar 

  23. Aimbire, F., R. Albertine, and R. de Magalhães. 2005. Effect of LLLT Ga-As-Al (685 nm) on LPS-induced inflammation of the airway and lung in rat. Lasers in Medical Science 4: 11–20.

    Article  Google Scholar 

  24. Aimbire, F., R. Albertini, M. Pacheco, F. Aimbire, R. Albertini, M.T. Pacheco, and J.M. Bjordal. 2006. Low-level laser therapy induces dose-dependent reduction of TNF-alpha levels in acute inflammation. Photomedicine and Laser Surgery 10: 33–37.

    Article  Google Scholar 

  25. Mafra de Lima, F., M. Costa, R. Albertini, J. Silva Jr., and F. Aimbire. 2009. Low level laser therapy (LLLT): attenuation of cholinergic hyperreactivity, β2-adrenergic hyporesponsiveness and TNF-α mRNA expression in rat bronchi segments in E. coli lipopolysaccharide-induced airway inflammation by a NF-κB dependent mechanism. Lasers in Surgery and Medicine 3: 68–74.

    Article  Google Scholar 

  26. Aimbire, F., A.P. Ligeiro de Oliveira, R. Albertini, J.C. Corrêa, C.B. Ladeira de Campos, J.P. Lyon, J.A. Silva Jr., and M.S. Costa. 2008. Low-level laser therapy (LLLT) decreases pulmonary microvascular leakage, neutrophil influx and IL-1beta levels in airway and lung from rat subjected to LPS-induced inflammation. Inflammation. 31: 189–197.

    Article  CAS  PubMed  Google Scholar 

  27. Hallstrand, T.S., T.L. Hackett, W.A. Altemeier, G. Matute-Bello, P.M. Hansbro, and D.A. Knight. 2014. Airway epithelial regulation of pulmonary immune homeostasis and inflammation. Clinical Immunology 151: 1–15.

    Article  CAS  PubMed  Google Scholar 

  28. de Lima, F., A. Villaverde, R. Albertini, A.P. de Oliveira, H. Faria-Neto, and F. Aimbire. 2010. Low-level laser therapy associated to N-acetylcysteine lowers macrophage inflammatory protein-2 (MIP-2) expression and generation of intracellular reactive oxygen species in alveolar macrophage. Photomedicine and Laser Surgery 28: 763–771.

    Article  PubMed  CAS  Google Scholar 

  29. de Lima, F.M., R. Albertini, Y. Dantas, A.L. Maia-Filho, L. Santana Cde, H.C. Castro-Faria-Neto, C. França, A.B. Villaverde, and F. Aimbire. 2013. Low-level laser therapy restores the oxidative stress balance in acute lung injury induced by gut ischemia and reperfusion. Photochemistry and Photobiology 89: 179–188.

    Article  PubMed  CAS  Google Scholar 

  30. de Lima, F., L. Vitoretti, F. Coelho, R. Albertini, A.C. Breithaupt-Faloppa, W. de Lima, and F. Aimbire. 2012. Suppressive effect of low-level laser therapy on tracheal hyperresponsiveness and lung inflammation in rat subjected to intestinal ischemia and reperfusion. Lasers in Medical Science 28: 179–188.

    Google Scholar 

  31. Souza, N.H., P.T. Marcondes, R. Albertini, R.A. Mesquita-Ferrari, K.P. Fernandes, and F. Aimbire. 2014. Low-level laser therapy suppresses the oxidative stress-induced glucocorticoids resistance in U937 cells: relevance to cytokine secretion and histone deacetylase in alveolar macrophages. Journal of Photochemistry and Photobiology 130: 327–336.

    Article  CAS  Google Scholar 

  32. Peron, J.P., A.A. de Brito, M. Pelatti, W.N. Brandão, L.B. Vitoretti, F.R. Greiffo, E.C. da Silveira, M.C. Oliveira-Junior, M. Maluf, L. Evangelista, S. Halpern, M.G. Nisenbaum, P. Perin, C.E. Czeresnia, N.O. Câmara, F. Aimbire, P. Vieira Rde, M. Zatz, and A.P. Ligeiro de Oliveira. 2015. Human tubal-derived mesenchymal stromal cells associated with low-level laser therapy significantly reduces cigarette smoke-induced COPD in C57BL/6 mice. PLoS One 10: 532–537.

    Google Scholar 

  33. Ostronosova, N. 2006. Outpatient use of laser therapy in bronchial asthma. Terapevticheskiĭ Arkhiv 78: 41–44.

    CAS  PubMed  Google Scholar 

  34. Kashanskaia, E.P., and A.A. Fedorov. 2009. Low-intensity laser radiation in the combined treatment of patients with chronic obstructive bronchitis. Voprosy Kurortologii, Fizioterapii, i Lechebnoĭ Fizicheskoĭ Kultury 2: 19–22.

    Google Scholar 

  35. Farkhutdinov, U.R., and ShU Farkhutdinov. 2007. Effect of laser radiation on production of reactive oxygen species in the blood of patients with chronic obstructive pulmonary disease. Bulletin of Experimental Biology and Medicine 144: 238–240.

    Article  CAS  PubMed  Google Scholar 

  36. Baker, R., J.R. Pereira da Silva, and J.R. Smith. 2004. The effect of tobacco ingredients on smoke chemistry. part 1: flavorings and additives. Food and Chemical Toxicology 42: 33–37.

    Google Scholar 

  37. Zhao, J., R. Harper, A. Barchowsky, and Y.P. Di. 2007. Identification of multiple MAPK-mediated transcription factors regulated by tobacco smoke in airway epithelial cells. American Journal of Physiology. Lung Cellular and Molecular Physiology 293: 480–490.

    Article  CAS  Google Scholar 

  38. Henkel, K.M., K. Frondorf, M.E. Gonzalez-Mejia, A.L. Doseff, and J.G. Cambronero. 2011. IL-8-induced neutrophil chemotaxis is mediated by Janus kinase 3 (JAK3). FEBS Letters 585: 159–166.

    Article  CAS  Google Scholar 

  39. Groneberg, D.A., and K.F. Chung. 2004. Models of chronic obstructive pulmonary disease. Respiratory Research 5: 18–21.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Qiu, Y., V. Bandi, R.L. Atmar, K. Hattotuwa, K.K. Guntupalli, and P.K. Jeffery. 2003. Biopsy neutrophilia, neutrophil chemokine and receptor gene expression in severe exacerbations of chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine 168: 968–975.

    Article  PubMed  Google Scholar 

  41. Aimbire, F., F. Santos, R. Albertini, H. Castro-Faria-Neto, J. Mittmann, and C. Pacheco-Soares. 2008. Low-level laser therapy decreases levels of lung neutrophils anti-apoptotic factors by a NF-kB dependent mechanism. International Immunopharmacology 8: 603–605.

    Article  CAS  PubMed  Google Scholar 

  42. Wang, S., S. Kotamraju, E. Konorev, S. Kalivendi, J. Joseph, and B. Kalyanaraman. 2002. Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: the role of hydrogen peroxide. The Biochemical Journal 367: 729–740.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lim, W., J. Kim, S. Kim, S. Karna, J. Won, S. Jeon, S. Kim, Y. Choi, H. Choi, and O. Kim. 2013. Modulation of lipopolysaccharide-induced NF-κB signaling pathway by 635 nm irradiation via heat shock protein 27 in human gingival fibroblast cells. Photochemistry and Photobiology 89: 199–207.

    Article  CAS  PubMed  Google Scholar 

  44. Junttila, M.R., S.P. Li, and J. Westermarck. 2008. Phosphatase mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. The FASEB Journal 22: 954–965.

    Article  CAS  PubMed  Google Scholar 

  45. Cossa, G.L., G. Gatti, C. Cassinelli, N. Lanzi, and P. Perego. 2013. Modulation of sensitivity to antitumor agents by targeting the MAPK survival pathway. Current Pharmaceutical Design 19: 883–894.

    Article  CAS  PubMed  Google Scholar 

  46. Renda, T., S. Baraldo, G. Pelaia, E. Bazzan, G. Turato, A. Papi, P. Maestrelli, R. Maselli, A. Vatrella, L.M. Fabbri, R. Zuin, S.A. Marsico, and M. Saetta. 2008. Increased activation of p38 MAPK in COPD. The European Respiratory Journal 31: 62–69.

    Article  CAS  PubMed  Google Scholar 

  47. Rahman, I., and W. MacNee. 1998. Role of transcription factors in inflammatory lung diseases. Thorax. 53: 601–612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Chung, K.F. 2011. p38 mitogen-activated protein kinase pathways in asthma and COPD. Chest. 139: 1470–1479.

    Article  CAS  PubMed  Google Scholar 

  49. Gaffey, K., S. Reynolds, J. Plumb, M. Kaur, and D. Singh. 2013. Increased phosphorylated p38 mitogen-activated protein kinase in COPD lungs. The European Respiratory Journal 42: 28–41.

    Article  CAS  PubMed  Google Scholar 

  50. Mehra, D., P.M. Geraghty, A.A. Hardigan, and R.A. Foronjy. 2012. Comparison of the inflammatory and proteolytic effects of dung biomass and cigarette smoke exposure in the lung. PLoS One 7: 52889–52933.

    Article  CAS  Google Scholar 

  51. Hoffman, E., O. Dittrich-Breiholz, H. Holtmann, and M. Kracht. 2002. Multiple control of interleukin-8 gene expression. Journal of Leukocyte Biology 72: 847–855.

    Article  Google Scholar 

  52. Arndt, P.G., S.K. Young, J.G. Lieber, M.B. Fessler, J.A. Nick, and G.S. Worthen. 2005. Inhibition of c-Jun N-terminal kinase limits lipopolysaccharide-induced pulmonary neutrophil influx. American Journal of Respiratory and Critical Care Medicine 171: 978–986.

    Article  PubMed  Google Scholar 

  53. Pantano, C., V. Anathy, P. Ranjan, N.H. Heintz, and Y.M. Janssen-Heininger. 2007. Nonphagocytic oxidase 1 causes death in lung epithelial cells via a TNF-RI-JNK signaling axis. American Journal of Respiratory Cell and Molecular Biology 36: 473–479.

    Article  CAS  PubMed  Google Scholar 

  54. Stork, P.J., and J.M. Schmitt. 2002. Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends in Cell Biology 12: 258–266.

    Article  CAS  PubMed  Google Scholar 

  55. Holden, N.S., C.F. Rider, M.J. Bell, J. Velayudhan, E.M. King, M. Kaur, M. Salmon, M.A. Giembycz, and R. Newton. 2010. Enhancement of inflammatory mediator release by beta(2)-drenoceptor agonists in airway epithelial cells is reversed by glucocorticoid action. British Journal of Pharmacology 160: 410–420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kasama, T., R. Strieter, N. Lukacs, M. Burdick, and S. Kunkel. 1994. Regulation of neutrophil-derived chemokine expression by IL-10. Journal of Immunology 152: 3559–3569.

    Article  CAS  Google Scholar 

  57. Pajkrt, D., L. Camoglio, M. Tiel-van Buul, K. de Bruin, D. Cutler, and M. Affrime. 1997. Attenuation of proinflammatory response by recombinant human IL-10 in human endotoxemia: effect of timing of recombinant human IL-10 administration. Journal of Immunology 158: 3971–3977.

    Article  CAS  Google Scholar 

  58. Dokka, S., X. Shi, S. Leonard, L. Wang, V. Castranova, and Y. Rojanasakul. 2001. Interleukin-10-mediated inhibition of free radical generation in macrophages. American Journal of Physiology. Lung Cellular and Molecular Physiology 280: 1196–1202.

    Article  Google Scholar 

  59. Deng, J., X. Wang, F. Qian, S. Vogel, L. Xiao, R. Ranjan, H. Park, M. Karpurapu, R. Ye, G. Park, and J. Christman. 2012. Protective role of reactive oxygen species in endotoxin-induced lung inflammation through modulation of IL-10 expression. Journal of Immunology 188: 5734–5740.

    Article  CAS  Google Scholar 

  60. Brightbill, H., S. Plevy, R. Modlin, and S. Smale. 2000. A prominent role for Sp1 during lipopolysaccharide-mediated induction of the IL-10 promoter in macrophages. Journal of Immunology 164: 1940–1951.

    Article  CAS  Google Scholar 

  61. Tone, M., M. Powell, Y. Tone, S. Thompson, and H. Waldmann. 2000. IL-10 gene expression is controlled by the transcription factors Sp1 and Sp3. Journal of Immunology 165: 286–291.

    Article  CAS  Google Scholar 

  62. Ma, W., W. Lim, K. Gee, S. Aucoin, D. Nandan, M. Kozlowski, F. Diaz-Mitoma, and A. Kumar. 2001. The p38 mitogen-activated kinase pathway regulates the human interleukin-10 promoter via the activation of Sp1 transcription factor in lipopolysaccharide-stimulated human macrophages. The Journal of Biological Chemistry 276: 13664–13674.

    Article  CAS  PubMed  Google Scholar 

  63. Zaman, K., L. Palmer, A. Doctor, J. Hunt, and B. Gaston. 2004. Concentration-dependent effects of endogenous S-nitrosoglutathione on gene regulation by specificity proteins Sp3 and Sp1. The Biochemical Journal 380: 67–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Chanteux, H., A. Guisset, C. Pilette, and Y. Sibille. 2007. LPS induces IL-10 production by human alveolar macrophages via MAPKinases- and Sp1-dependent mechanisms. Respiratory Research 8: 71–75.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Henson, P.M., R.W. Vandivier, and I.S. Douglas. 2006. Cell death, remodeling, and repair in chronic obstructive pulmonary disease? Proceedings of the American Thoracic Society 3: 713–717.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was sponsored by the Foundation for Research Support of the State of São Paulo (FAPESP) 2012/16498-5.

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Authors and Affiliations

  1. Pos-graduation in Biophotonic, University Nove de Julho – Uninove, São Paulo, São Paulo, Brazil

    A. Brito, T. Santos, K. Herculano, M. Miranda & A. P. Ligeiro-de-Oliveira

  2. Department of Science and Technology, Institute of Science and Technology, Federal University of São Paulo – UNIFESP, Rua Talim, no. 330 – Vila Nair, CEP: 12231-280, São José dos Campos, São Paulo, Brazil

    A. K. Sá, J. L. Carvalho, R. Albertini & Flávio Aimbire

  3. Laboratory of Immunopharmacology, Oswaldo Cruz Foundation – FioCruz, Rio de Janeiro, Rio de Janeiro, Brazil

    H. Castro-Faria-Neto

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Contributions

Conceived and designed the experiments: FA and APLO. Performed the experiments: AB, TS, KH, MM, AKS, and JLC. Analyzed the data: JLC, APLO, and FA. Contributed reagents/materials/analysis tools: FA, HCFN, RA, and APLO. Wrote the paper: FA and APLO.

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Correspondence to Flávio Aimbire.

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Brito, A., Santos, T., Herculano, K. et al. The MAPKinase Signaling and the Stimulatory Protein-1 (Sp1) Transcription Factor Are Involved in the Phototherapy Effect on Cytokines Secretion from Human Bronchial Epithelial Cells Stimulated with Cigarette Smoke Extract. Inflammation 44, 1643–1661 (2021). https://doi.org/10.1007/s10753-021-01448-5

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