Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2016, Article ID 7053963, 19 pages
http://dx.doi.org/10.1155/2016/7053963
Research Article

Altered Macrophage and Dendritic Cell Response in Mif−/− Mice Reveals a Role of Mif for Inflammatory-Th1 Response in Type 1 Diabetes

1Unidad de Biomedicina, Facultad de Estudios Superiores (FES) Iztacala, Universidad Nacional Autónoma de México (UNAM), 54090 Tlalnepantla, MEX, Mexico
2Carrera de Optometría, FES-Iztacala, UNAM, 54090 Tlalnepantla, MEX, Mexico
3Departamento de Neurodesarrollo y Fisiología, Instituto de Fisiología Celular, UNAM, 04510 Coyoacán, MEX, Mexico

Received 31 May 2016; Accepted 10 July 2016

Academic Editor: Jixin Zhong

Copyright © 2016 Yuriko Itzel Sánchez-Zamora 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. F. S. Malik and C. E. Taplin, “Insulin therapy in children and adolescents with type 1 diabetes,” Pediatric Drugs, vol. 16, no. 2, pp. 141–150, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. American Diabetes Association, “Diagnosis and classification of diabetes mellitus,” Diabetes Care, vol. 37, supplement 1, pp. S81–S90, 2013. View at Publisher · View at Google Scholar
  3. S. Canivell and R. Gomis, “Diagnosis and classification of autoimmune diabetes mellitus,” Autoimmunity Reviews, vol. 13, no. 4-5, pp. 403–407, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Willcox, S. J. Richardson, A. J. Bone, A. K. Foulis, and N. G. Morgan, “Analysis of islet inflammation in human type 1 diabetes,” Clinical & Experimental Immunology, vol. 155, no. 2, pp. 173–181, 2009. View at Publisher · View at Google Scholar
  5. M. E. Craig, S. Nair, H. Stein, and W. D. Rawlinson, “Viruses and type 1 diabetes: a new look at an old story,” Pediatric Diabetes, vol. 14, no. 3, pp. 149–158, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Salvatoni, A. Baj, G. Bianchi, G. Federico, M. Colombo, and A. Toniolo, “Intrafamilial spread of enterovirus infections at the clinical onset of type 1 diabetes,” Pediatric Diabetes, vol. 14, no. 6, pp. 407–416, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Afonso and R. Mallone, “Infectious triggers in type 1 diabetes: is there a case for epitope mimicry?” Diabetes, Obesity and Metabolism, vol. 15, supplement 3, pp. 82–88, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. Å. Lernmark and C.-D. Agardh, “Immunomodulation with human recombinant autoantigens,” Trends in Immunology, vol. 26, no. 11, pp. 608–612, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Pearl-Yafe, A. Kaminitz, E. S. Yolcu, I. Yaniv, J. Stein, and N. Askenasy, “Pancreatic islets under attack: cellular and molecular effectors,” Current Pharmaceutical Design, vol. 13, no. 7, pp. 749–760, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Dogan, S. Akarsu, B. Ustundag, E. Yilmaz, and M. K. Gurgoze, “Serum IL-1β, IL-2, and IL-6 in insulin-dependent diabetic children,” Mediators of Inflammation, vol. 2006, Article ID 59206, 6 pages, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. B. Baumann, H. H. Salem, and B. O. Boehm, “Anti-inflammatory therapy in type 1 diabetes,” Current Diabetes Reports, vol. 12, no. 5, pp. 499–509, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Y. Westwell-Roper, J. A. Ehses, and C. B. Verchere, “Resident macrophages mediate islet amyloid polypeptide-induced islet IL-1β production and β-cell dysfunction,” Diabetes, vol. 63, no. 5, pp. 1698–1711, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Mandrup-Poulsen, L. Pickersgill, and M. Y. Donath, “Blockade of interleukin 1 in type 1 diabetes mellitus,” Nature Reviews Endocrinology, vol. 6, no. 3, pp. 158–166, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Mandrup-Poulsen, “Interleukin-1 antagonists and other cytokine blockade strategies for type 1 diabetes,” Review of Diabetic Studies, vol. 9, no. 4, pp. 338–347, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. X.-L. Zou, Z.-Y. Zhao, Y.-Y. Wan, Z.-Q. Su, and M. Xiang, “Diabetogenic T cells induce autoimmune diabetes in BALB/c mice,” Chinese Medical Sciences Journal, vol. 23, no. 2, pp. 88–94, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Myśliwska, M. Smardzewski, N. Marek-Trzonkowska, M. Myśliwiec, and K. Raczyńska, “Expansion of CD14+CD16+ monocytes producing TNF-α in complication-free diabetes type 1 juvenile onset patients,” Cytokine, vol. 60, no. 1, pp. 309–317, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Rachmiel, O. Bloch, A. A. Shaul et al., “Young patients with both type 1 diabetes mellitus and asthma have a unique IL-12 and IL-18 secretory pattern,” Pediatric Diabetes, vol. 12, no. 7, pp. 596–603, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. A. E. Altinova, D. Engin, E. Akbay et al., “Association of polymorphisms in the IL-18 and IL-12 genes with susceptibility to type 1 diabetes in Turkish patients,” Journal of Endocrinological Investigation, vol. 33, no. 7, pp. 451–454, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Hanifi-Moghaddam, N. C. Schloot, S. Kappler, J. Seißler, and H. Kolb, “An association of autoantibody status and serum cytokine levels in type 1 diabetes,” Diabetes, vol. 52, no. 5, pp. 1137–1142, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Bojunga, K. Kusterer, M. Bacher, R. Kurek, K.-H. Usadel, and H. Renneberg, “Macrophage migration inhibitory factor and development of type-1 diabetes in non-obese diabetic mice,” Cytokine, vol. 21, no. 4, pp. 179–186, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. I. Cvetkovic, Y. Al-Abed, D. Miljkovic et al., “Critical role of macrophage migration inhibitory factor activity in experimental autoimmune diabetes,” Endocrinology, vol. 146, no. 7, pp. 2942–2951, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Stosic-Grujicic, I. Stojanovic, D. Maksimovic-Ivanic et al., “Macrophage migration inhibitory factor (MIF) is necessary for progression of autoimmune diabetes mellitus,” Journal of Cellular Physiology, vol. 215, no. 3, pp. 665–675, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. I. Sánchez-Zamora and M. Rodriguez-Sosa, “The role of MIF in type 1 and type 2 diabetes mellitus,” Journal of Diabetes Research, vol. 2014, Article ID 804519, 6 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Stojanovic, T. Saksida, I. Nikolic, F. Nicoletti, and S. Stosic-Grujicic, “Macrophage migration inhibitory factor deficiency protects pancreatic islets from cytokine-induced apoptosis in vitro,” Clinical and Experimental Immunology, vol. 169, no. 2, pp. 156–163, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Roger, M. P. Glauser, and T. Calandra, “Macrophage migration inhibitory factor (MIF) modulates innate immune responses induced by endotoxin and Gram-negative bacteria,” Journal of Endotoxin Research, vol. 7, no. 6, pp. 456–460, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. S. N. Babu, G. Chetal, and S. Kumar, “Macrophage migration inhibitory factor: a potential marker for cancer diagnosis and therapy,” Asian Pacific Journal of Cancer Prevention, vol. 13, no. 5, pp. 1737–1744, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Nishihira, “Molecular function of macrophage migration inhibitory factor and a novel therapy for inflammatory bowel disease,” Annals of the New York Academy of Sciences, vol. 1271, no. 1, pp. 53–57, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Nishihira and K. Mitsuyama, “Overview of the role of macrophage migration inhibitory factor (MIF) in inflammatory bowel disease,” Current Pharmaceutical Design, vol. 15, no. 18, pp. 2104–2109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. L. L. Santos and E. F. Morand, “Macrophage migration inhibitory factor: a key cytokine in RA, SLE and atherosclerosis,” Clinica Chimica Acta, vol. 399, no. 1-2, pp. 1–7, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. Z. Szekanecz, T. Besenyei, Á. Szentpétery, and A. E. Koch, “Angiogenesis and vasculogenesis in rheumatoid arthritis,” Current Opinion in Rheumatology, vol. 22, no. 3, pp. 299–306, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. O. M. Finucane, C. M. Reynolds, F. C. McGillicuddy, and H. M. Roche, “Insights into the role of macrophage migration inhibitory factor in obesity and insulin resistance,” Proceedings of the Nutrition Society, vol. 71, no. 4, pp. 622–633, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Kleemann and R. Bucala, “Macrophage migration inhibitory factor: critical role in obesity, insulin resistance, and associated comorbidities,” Mediators of Inflammation, vol. 2010, Article ID 610479, 7 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Toso, J. A. Emamaullee, S. Merani, and A. M. J. Shapiro, “The role of macrophage migration inhibitory factor on glucose metabolism and diabetes,” Diabetologia, vol. 51, no. 11, pp. 1937–1946, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Nishihira, “Novel pathophysiological aspects of macrophage migration inhibitory factor (review),” International Journal of Molecular Medicine, vol. 2, no. 1, pp. 17–28, 1998. View at Google Scholar · View at Scopus
  35. Y. Sanchez-Zamora, L. I. Terrazas, A. Vilches-Flores et al., “Macrophage migration inhibitory factor is a therapeutic target in treatment of non-insulin-dependent diabetes mellitus,” The FASEB Journal, vol. 24, no. 7, pp. 2583–2590, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Grieb, M. Merk, J. Bernhagen, and R. Bucala, “Macrophage Migration Inhibitory Factor (MIF): a promising biomarker,” Drug News and Perspectives, vol. 23, no. 4, pp. 257–264, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Leech, C. Metz, P. Hall et al., “Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids,” Arthritis and Rheumatism, vol. 42, no. 8, pp. 1601–1608, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Onodera, H. Tanji, K. Suzuki et al., “High expression of macrophage migration inhibitory factor in the synovial tissues of rheumatoid joints,” Cytokine, vol. 11, no. 2, pp. 163–167, 1999. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Yun, C.-T. Xu, and B.-R. Pan, “Epidemiology and gene markers of ulcerative colitis in the Chinese,” World Journal of Gastroenterology, vol. 15, no. 7, pp. 788–803, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. P. W. Laird, A. Zijderveld, K. Linders, M. A. Rudnicki, R. Jaenisch, and A. Berns, “Simplified mammalian DNA isolation procedure,” Nucleic Acids Research, vol. 19, no. 15, article 4293, 1991. View at Publisher · View at Google Scholar · View at Scopus
  41. M. L. Lukic, S. Stošic-Grujicic, and A. Shahin, “Effector mechanisms in low-dose streptozotocin-induced diabetes,” Developmental Immunology, vol. 6, no. 1-2, pp. 119–128, 1998. View at Publisher · View at Google Scholar
  42. M. A. K. Markwell, S. M. Haas, L. L. Bieber, and N. E. Tolbert, “A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples,” Analytical Biochemistry, vol. 87, no. 1, pp. 206–210, 1978. View at Publisher · View at Google Scholar · View at Scopus
  43. E. E. Hillhouse, R. Collin, G. Chabot-Roy et al., “Nearby construction impedes the progression to overt autoimmune diabetes in NOD mice,” Journal of Diabetes Research, vol. 2013, Article ID 620313, 7 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. D. S. Li, Y. Yuan, H. Tu, Q. Liang, and L. Dai, “A protocol for islet isolation from mouse pancreas,” Nature Protocols, vol. 4, no. 11, pp. 1649–1652, 2009. View at Publisher · View at Google Scholar
  45. A. M. Ortiz-Flores, Y. Ledesma-Soto, E. A. Calleja, M. Rodríguez-Sosa, I. Juárez, and L. I. Terrazas, “Taenia crassiceps infection does not influence the development of experimental rheumatoid arthritis,” BioMed Research International, vol. 2013, Article ID 316980, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Yu, D. T. Robles, N. Abiru et al., “Early expression of antiinsulin autoantibodies of humans and the NOD mouse: evidence for early determination of subsequent diabetes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 4, pp. 1701–1706, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. A. K. Steck, K. Johnson, K. J. Barriga et al., “Age of islet autoantibody appearance and mean levels of insulin, but not GAD or IA-2 autoantibodies, predict age of diagnosis of type 1 diabetes: diabetes autoimmunity study in the young,” Diabetes Care, vol. 34, no. 6, pp. 1397–1399, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Rex, S. Kraemer, G. Grieb et al., “The role of macrophage migration inhibitory factor in critical illness,” Mini-Reviews in Medicinal Chemistry, vol. 14, no. 14, pp. 1116–1124, 2014. View at Google Scholar · View at Scopus
  49. J. D. D. Rosado and M. Rodriguez-Sosa, “Macrophage migration inhibitory factor (MIF): a key player in protozoan infections,” International Journal of Biological Sciences, vol. 7, no. 9, pp. 1239–1256, 2011. View at Google Scholar · View at Scopus
  50. K. Kim and H. Kim, “Macrophage migration inhibitory factor: a potential therapeutic target for rheumatoid arthritis,” The Korean Journal of Internal Medicine, vol. 31, no. 4, pp. 634–642, 2016. View at Publisher · View at Google Scholar
  51. C. Pfleger, N. C. Schloot, M. D. Brendel et al., “Circulating cytokines are associated with human islet graft function in type 1 diabetes,” Clinical Immunology, vol. 138, no. 2, pp. 154–161, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Kolb, “Mouse models of insulin dependent diabetes: low-dose streptozocin-induced diabetes and nonobese diabetic (NOD) mice,” Diabetes/Metabolism Reviews, vol. 3, no. 3, pp. 751–778, 1987. View at Publisher · View at Google Scholar · View at Scopus
  53. A. K. Steck, K. Vehik, E. Bonifacio et al., “Predictors of progression from the appearance of islet autoantibodies to early childhood diabetes: the Environmental Determinants of Diabetes in the Young (TEDDY),” Diabetes Care, vol. 38, no. 5, pp. 808–813, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Waeber, T. Calandra, R. Roduit et al., “Insulin secretion is regulated by the glucose-dependent production of islet β cell macrophage migration inhibitory factor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 9, pp. 4782–4787, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. G. Waeber, T. Calandra, C. Bonny, and R. Bucala, “A role for the endocrine and pro-inflammatory mediator MIF in the control of insulin secretion during stress,” Diabetes/Metabolism Research and Reviews, vol. 15, no. 1, pp. 47–54, 1999. View at Publisher · View at Google Scholar · View at Scopus
  56. N. G. Morgan, P. Leete, A. K. Foulis, and S. J. Richardson, “Islet inflammation in human type 1 diabetes mellitus,” IUBMB Life, vol. 66, no. 11, pp. 723–734, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. E. P. C. van der Vorst, Y. Döring, and C. Weber, “Chemokines and their receptors in Atherosclerosis,” Journal of Molecular Medicine, vol. 93, no. 9, pp. 963–971, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. D. L. Eizirik, M. L. Colli, and F. Ortis, “The role of inflammation in insulitis and β-cell loss in type 1 diabetes,” Nature Reviews Endocrinology, vol. 5, no. 4, pp. 219–226, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. A. B. Stavitsky and J. Xianli, “In vitro and in vivo regulation by macrophage migration inhibitory factor (MIF) of expression of MHC-II, costimulatory, adhesion, receptor, and cytokine molecules,” Cellular Immunology, vol. 217, no. 1-2, pp. 95–104, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. C. A. Terrazas, E. Huitron, A. Vazquez et al., “MIF synergizes with Trypanosoma cruzi antigens to promote efficient dendritic cell maturation and IL-12 production via p38 MAPK,” International Journal of Biological Sciences, vol. 7, no. 9, pp. 1298–1310, 2011. View at Google Scholar · View at Scopus
  61. J. de Dios Ruiz-Rosado, J. E. Olguín, I. Juárez-Avelar et al., “MIF promotes classical activation and conversion of inflammatory Ly6Chigh monocytes into tipdcs during murine toxoplasmosis,” Mediators of Inflammation, vol. 2016, Article ID 9101762, 18 pages, 2016. View at Publisher · View at Google Scholar
  62. B. Salomon and J. A. Bluestone, “Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation,” Annual Review of Immunology, vol. 19, pp. 225–252, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. D. J. Lenschow, S. C. Ho, H. Sattar et al., “Differential effects of anti-B7-1 and anti-B7-2 monoclonal antibody treatment on the development of diabetes in the nonobese diabetic mouse,” Journal of Experimental Medicine, vol. 181, no. 3, pp. 1145–1155, 1995. View at Publisher · View at Google Scholar · View at Scopus
  64. J. J. Racine, M. Zhang, M. Wang, W. Morales, C. Shen, and D. Zeng, “MHC-mismatched mixed chimerism mediates thymic deletion of cross-reactive autoreactive T cells and prevents insulitis in nonobese diabetic mice,” The Journal of Immunology, vol. 194, no. 1, pp. 407–417, 2015. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Espinoza-Jiménez, A. N. Peón, and L. I. Terrazas, “Alternatively activated macrophages in types 1 and 2 diabetes,” Mediators of Inflammation, vol. 2012, Article ID 815953, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. B.-S. Kim, N. Pallua, J. Bernhagen, and R. Bucala, “The macrophage migration inhibitory factor protein superfamily in obesity and wound repair,” Experimental and Molecular Medicine, vol. 47, article e161, 2015. View at Publisher · View at Google Scholar · View at Scopus
  67. D. Heinrichs, M.-L. Berres, M. Coeuru et al., “Protective role of macrophage migration inhibitory factor in nonalcoholic steatohepatitis,” The FASEB Journal, vol. 28, no. 12, pp. 5136–5147, 2014. View at Publisher · View at Google Scholar · View at Scopus
  68. K. Yaddanapudi, K. Putty, B. E. Rendon et al., “Control of tumor-associated macrophage alternative activation by macrophage migration inhibitory factor,” The Journal of Immunology, vol. 190, no. 6, pp. 2984–2993, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. L. Prieto-Lafuente, W. F. Gregory, J. E. Allen, and R. M. Maizels, “MIF homologues from a filarial nematode parasite synergize with IL-4 to induce alternative activation of host macrophages,” Journal of Leukocyte Biology, vol. 85, no. 5, pp. 844–854, 2009. View at Publisher · View at Google Scholar · View at Scopus