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Mediators of Inflammation
Volume 2018 (2018), Article ID 6150843, 11 pages
https://doi.org/10.1155/2018/6150843
Research Article

Diabetes Downregulates Allergen-Induced Airway Inflammation in Mice

1Laboratory of Inflammation, Oswaldo Cruz Institute, FIOCRUZ, Av. Brasil No. 4365, 21045-900 Manguinhos, RJ, Brazil
2Federal University of Alagoas, 57072-970 Maceió, AL, Brazil
3Cedars-Sinai Medical Center, 8700 Beverly Blvd, Los Angeles, CA 90048, USA

Correspondence should be addressed to Patrícia M. R. Silva; moc.liamg@0191avlistap

Received 24 November 2017; Accepted 20 February 2018; Published 15 April 2018

Academic Editor: Sonya Marshall-Gradisnik

Copyright © 2018 Vinicius F. Carvalho et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. S. Coutinho, E. A. Anjos-Valotta, C. do Nascimento et al., “15-Deoxy-delta-12,14-prostaglandin J2 inhibits lung inflammation and remodeling in distinct murine models of asthma,” Frontiers in Immunology, vol. 8, p. 740, 2017. View at Publisher · View at Google Scholar · View at Scopus
  2. J. A. Walker and A. N. J. McKenzie, “TH2 cell development and function,” Nature Reviews Immunology, vol. 18, no. 2, pp. 121–133, 2017. View at Publisher · View at Google Scholar
  3. Pavord, Green, and Haldar, Clinical Respiratory Medicine, S. Spiro, G. Silvestri, and A. Agustí, Eds., Elsevier, Philadelphia, PA, USA, Fourth edition, 2012.
  4. E. H. Meyer, R. H. DeKruyff, and D. T. Umetsu, “T cells and NKT cells in the pathogenesis of asthma,” Annual Review of Medicine, vol. 59, no. 1, pp. 281–292, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. T. P. Ferreira, A. C. de Arantes, C. V. do Nascimento et al., “IL-13 immunotoxin accelerates resolution of lung pathological changes triggered by silica particles in mice,” The Journal of Immunology, vol. 191, no. 10, pp. 5220–5229, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. G. d'Annunzio, M. A. Tosca, A. Pistorio et al., “Type 1 diabetes mellitus and asthma: a follow-up study,” Allergologia et Immunopathologia, vol. 43, no. 2, pp. 225–227, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. M. A. Tosca, M. Silovestri, G. D'Annunzio, R. Lorini, G. A. Rossi, and G. Ciprandi, “May T1 diabetes mellitus protect from asthma?” Allergologia et Immunopathologia, vol. 41, no. 5, pp. 288–291, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. Y. T. Hsiao, W. C. Cheng, W. C. Liao et al., “Type 1 diabetes and increased risk of subsequent asthma: a nationwide population-based cohort study,” Medicine, vol. 94, no. 36, article e1466, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. C. H. Lin, C. C. Wei, C. L. Lin, W. C. Lin, and C. H. Kao, “Childhood type 1 diabetes may increase the risk of atopic dermatitis,” The British Journal of Dermatology, vol. 174, no. 1, pp. 88–94, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Kubo, “Innate and adaptive type 2 immunity in lung allergic inflammation,” Immunological Reviews, vol. 278, no. 1, pp. 162–172, 2017. View at Publisher · View at Google Scholar · View at Scopus
  11. L. T. Hellman, S. Akula, M. Thorpe, and Z. Fu, “Tracing the origins of IgE, mast cells, and allergies by studies of wild animals,” Frontiers in Immunology, vol. 8, p. 1749, 2017. View at Publisher · View at Google Scholar · View at Scopus
  12. C. N. McBrien and A. Menzies-Gow, “The biology of eosinophils and their role in asthma,” Frontiers in Medicine, vol. 4, p. 93, 2017. View at Publisher · View at Google Scholar
  13. D. Bagnasco, M. Ferrando, G. Varricchi, F. Puggioni, G. Passalacqua, and G. W. Canonica, “Anti-interleukin 5 (IL-5) and IL-5Ra biological drugs: efficacy, safety, and future perspectives in severe eosinophilic asthma,” Frontiers in Medicine, vol. 4, p. 135, 2017. View at Publisher · View at Google Scholar
  14. M. Kato, Y. Yamada, K. Maruyama, and Y. Hayashi, “Serum eosinophil cationic protein and 27 cytokines/chemokines in acute exacerbation of childhood asthma,” International Archives of Allergy and Immunology, vol. 152, no. 1, pp. 62–66, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Thunberg, G. Gafvelin, M. Nord et al., “Allergen provocation increases TH2-cytokines and FOXP3 expression in the asthmatic lung,” Allergy, vol. 65, no. 3, pp. 311–318, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. B. L. Diaz, M. F. Serra, E. O. Barreto, R. S. B. Cordeiro, M. A. Martins, and P. M. R. . Silva, “Antigen-induced pleural eosinophilia is suppressed in diabetic rats: role of corticosteroid hormones,” Memórias do Instituto Oswaldo Cruz, vol. 92, Supplement 2, pp. 219–222, 1997. View at Publisher · View at Google Scholar
  17. E. O. Vianna and J. Garcia-Leme, “Allergen-induced airway inflammation in rats. Role of insulin,” American Journal of Respiratory and Critical Care Medicine, vol. 151, 3, Part 1, pp. 809–814, 1995. View at Publisher · View at Google Scholar
  18. S. C. Cavalher-Machado, W. T. de Lima, A. S. Damazo et al., “Down-regulation of mast cell activation and airway reactivity in diabetic rats: role of insulin,” European Respiratory Journal, vol. 24, no. 4, pp. 552–558, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. V. F. Carvalho, L. T. Florim, E. de O Barreto et al., “Inhibition of advanced glycation end products by aminoguanidine restores mast cell numbers and reactivity in alloxan-diabetic rats,” European Journal of Pharmacology, vol. 669, no. 1–3, pp. 143–148, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. E. de Oliveira Barreto, V. de Frias Carvalho, B. L. Diaz et al., “Adoptive transfer of mast cells abolishes the inflammatory refractoriness to allergen in diabetic rats,” International Archives of Allergy and Immunology, vol. 131, no. 3, pp. 212–220, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. R. C. Torres, N. S. Magalhaes, P. M. E Silva, M. A. Martins, and V. F. Carvalho, “Activation of PPAR-γ reduces HPA axis activity in diabetic rats by up-regulating PI3K expression,” Experimental and Molecular Pathology, vol. 101, no. 2, pp. 290–301, 2016. View at Publisher · View at Google Scholar · View at Scopus
  22. V. F. Carvalho, E. O. Barreto, M. F. Serra et al., “Aldose reductase inhibitor zopolrestat restores allergic hyporesponsiveness in alloxan-diabetic rats,” European Journal of Pharmacology, vol. 549, no. 1–3, pp. 173–178, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. V. de F Carvalho, L. V. Campos, F. A. Farias-Filho et al., “Suppression of allergic inflammatory response in the skin of alloxan-diabetic rats: relationship with reduced local mast cell numbers,” International Archives of Allergy and Immunology, vol. 147, no. 3, pp. 246–254, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. B. L. Diaz, M. F. Serra, A. C. Alves et al., “Alloxan diabetes reduces pleural mast cell numbers and the subsequent eosinophil influx induced by allergen in sensitized rats,” International Archives of Allergy and Immunology, vol. 111, no. 1, pp. 36–43, 1996. View at Publisher · View at Google Scholar · View at Scopus
  25. B. P. Tian, H. B. Zhou, L. X. Xia, H. H. Shen, and S. Ying, “Balance of apoptotic cell death and survival in allergic diseases,” Microbes and Infection, vol. 16, no. 10, pp. 811–821, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. J. S. Park, A. S. Jang, S. W. Park et al., “Protection of leukotriene receptor antagonist against aspirin-induced bronchospasm in asthmatics,” Allergy Asthma & Immunology Research, vol. 2, no. 1, pp. 48–54, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Pazdrak, C. Straub, R. Maroto et al., “Cytokine-induced glucocorticoid resistance from eosinophil activation: protein phosphatase 5 modulation of glucocorticoid receptor phosphorylation and signaling,” The Journal of Immunology, vol. 197, no. 10, pp. 3782–3791, 2016. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Hirsch, A. Lavoie-Lamoureux, G. Beauchamp, and J. P. Lavoie, “Neutrophils are not less sensitive than other blood leukocytes to the genomic effects of glucocorticoids,” PLoS One, vol. 7, no. 9, article e44606, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Y. Gaisano, P. E. Macdonald, and M. Vranic, “Glucagon secretion and signaling in the development of diabetes,” Frontiers in Physiology, vol. 3, p. 349, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. D. B. Insuela, J. B. Daleprane, L. P. Coelho et al., “Glucagon induces airway smooth muscle relaxation by nitric oxide and prostaglandin E2,” The Journal of Endocrinology, vol. 225, no. 3, pp. 205–217, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Banuelos, S. Shin, Y. Cao et al., “BCL-2 protects human and mouse Th17 cells from glucocorticoid-induced apoptosis,” Allergy, vol. 71, no. 5, pp. 640–650, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Cosmi, F. Liotta, E. Maggi, S. Romagnani, and F. Annunziato, “Th17 cells: new players in asthma pathogenesis,” Allergy, vol. 66, no. 8, pp. 989–998, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. E. O. Barreto, I. Riederer, A. C. Arantes et al., “Thymus involution in alloxan diabetes: analysis of mast cells,” Memórias do Instituto Oswaldo Cruz, vol. 100, Supplement 1, pp. 127–130, 2005. View at Publisher · View at Google Scholar
  34. M. E. Elder and N. K. Maclaren, “Identification of profound peripheral T lymphocyte immunodeficiencies in the spontaneously diabetic BB rat,” The Journal of Immunology, vol. 130, no. 4, pp. 1723–1731, 1983. View at Google Scholar
  35. R. Otton, F. G. Soriano, R. Verlengia, and R. Curi, “Diabetes induces apoptosis in lymphocytes,” The Journal of Endocrinology, vol. 182, no. 1, pp. 145–156, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Satoh and R. Iwasaki, “Experimental diabetes attenuates calcium mobilization and proliferative response in splenic lymphocytes from mice,” The Journal of Physiological Sciences, vol. 61, no. 1, pp. 23–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Mantle, E. Thakore, E. Atkins, R. Mathison, and J. S. Davison, “Effects of streptozotocin-diabetes on rat intestinal mucin and goblet cells,” Gastroenterology, vol. 97, no. 1, pp. 68–75, 1989. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Bachert and J. Maspero, “Efficacy of second-generation antihistamines in patients with allergic rhinitis and comorbid asthma,” Journal of Asthma, vol. 48, no. 9, pp. 965–973, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. Q. Hamid and M. Tulic, “Immunobiology of asthma,” Annual Review of Physiology, vol. 71, no. 1, pp. 489–507, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Takatsu and H. Nakajima, “IL-5 and eosinophilia,” Current Opinion in Immunology, vol. 20, no. 3, pp. 288–294, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Radinger, A. Bossios, M. Sjostrand et al., “Local proliferation and mobilization of CCR3+ CD34+ eosinophil-lineage-committed cells in the lung,” Immunology, vol. 132, no. 1, pp. 144–154, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Rot, M. Krieger, T. Brunner, S. C. Bischoff, T. J. Schall, and C. A. Dahinden, “RANTES and macrophage inflammatory protein 1 alpha induce the migration and activation of normal human eosinophil granulocytes,” Journal of Experimental Medicine, vol. 176, no. 6, pp. 1489–1495, 1992. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Viardot, S. T. Grey, F. Mackay, and D. Chisholm, “Potential antiinflammatory role of insulin via the preferential polarization of effector T cells toward a T helper 2 phenotype,” Endocrinology, vol. 148, no. 1, pp. 346–353, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. J. V. Fahy, “Type 2 inflammation in asthma--present in most, absent in many,” Nature Reviews Immunology, vol. 15, no. 1, pp. 57–65, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. S. M. Tarlo and G. M. Liss, “Occupational asthma: an approach to diagnosis and management,” CMAJ, vol. 168, no. 7, pp. 867–871, 2003. View at Google Scholar
  46. Z. L. Lummus, A. V. Wisnewski, and D. I. Bernstein, “Pathogenesis and disease mechanisms of occupational asthma,” Immunology and Allergy Clinics of North America, vol. 31, no. 4, pp. 699–716, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. V. F. Carvalho, E. O. Barreto, B. L. Diaz et al., “Systemic anaphylaxis is prevented in alloxan-diabetic rats by a mechanism dependent on glucocorticoids,” European Journal of Pharmacology, vol. 472, no. 3, pp. 221–227, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. W. Ptak, M. Rewicka, J. Strzyzewska, and M. Kollat, “Alleviation of IgE-mediated immune reactions in hypoinsulinaemic and hyperglycaemic mice,” Clinical and Experimental Immunology, vol. 52, no. 1, pp. 54–60, 1983. View at Google Scholar
  49. M. Kashiwada, D. M. Levy, L. McKeag et al., “IL-4-induced transcription factor NFIL3/E4BP4 controls IgE class switching,” Proceedings of the National Academy of Sciences of the Unites States of America, vol. 107, no. 2, pp. 821–826, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. M. J. Rapoport, A. H. Lazarus, A. Jaramillo, E. Speck, and T. L. Delovitch, “Thymic T cell anergy in autoimmune nonobese diabetic mice is mediated by deficient T cell receptor regulation of the pathway of p21ras activation,” Journal of Experimental Medicine, vol. 177, no. 4, pp. 1221–1226, 1993. View at Publisher · View at Google Scholar · View at Scopus
  51. P. S. Foster, S. P. Hogan, A. J. Ramsay, K. I. Matthaei, and I. G. Young, “Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model,” Journal of Experimental Medicine, vol. 183, no. 1, pp. 195–201, 1996. View at Publisher · View at Google Scholar · View at Scopus
  52. D. B. Corry, H. G. Folkesson, M. L. Warnock et al., “Interleukin 4, but not interleukin 5 or eosinophils, is required in a murine model of acute airway hyperreactivity,” The Journal of Experimental Medicine, vol. 183, no. 1, pp. 109–117, 1996. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Kobayashi, T. Miura, T. Haba et al., “An essential role of mast cells in the development of airway hyperresponsiveness in a murine asthma model,” Journal of Immunology, vol. 164, no. 7, pp. 3855–3861, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Nagai, S. Yamaguchi, Y. Maeda, and H. Tanaka, “Role of mast cells, eosinophils and IL-5 in the development of airway hyperresponsiveness in sensitized mice,” Clinical and Experimental Allergy, vol. 26, no. 6, pp. 642–647, 1996. View at Publisher · View at Google Scholar · View at Scopus
  55. S. I. Mayr, R. I. Zuberi, M. Zhang et al., “IgE-dependent mast cell activation potentiates airway responses in murine asthma models,” Journal of Immunology, vol. 169, no. 4, pp. 2061–2068, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. T. D. Green, A. L. Crews, J. Park, S. Fang, and K. B. Adler, “Regulation of mucin secretion and inflammation in asthma: a role for MARCKS protein?” Biochimica et Biophysica Acta (BBA) - General Subjects, vol. 1810, no. 11, pp. 1110–1113, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Roy, B. Collier, and A. Roy, “Hypothalamic-pituitary-adrenal axis dysregulation among diabetic outpatients,” Psychiatry Research, vol. 31, no. 1, pp. 31–37, 1990. View at Publisher · View at Google Scholar · View at Scopus
  58. M. S. Roy, A. Roy, and S. Brown, “Increased urinary-free cortisol outputs in diabetic patients,” Journal of Diabetes and its Complications, vol. 12, no. 1, pp. 24–27, 1998. View at Publisher · View at Google Scholar · View at Scopus
  59. O. Chan, K. Inouye, M. C. Riddell, M. Vranic, and S. G. Matthews, “Diabetes and the hypothalamo-pituitary-adrenal (HPA) axis,” Minerva Endocrinologica, vol. 28, no. 2, pp. 87–102, 2003. View at Google Scholar