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Malaria Research and Treatment
Volume 2016, Article ID 6132734, 9 pages
http://dx.doi.org/10.1155/2016/6132734
Research Article

Nonobese Diabetic (NOD) Mice Lack a Protective B-Cell Response against the “Nonlethal” Plasmodium yoelii 17XNL Malaria Protozoan

1Department of Medicine, Division of Immunology, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, USA
2Benaroya Research Institute at Virginia Mason, 1201 Ninth Avenue, Seattle, WA 98101, USA
3Infectious Diseases Directorate, Division of Malaria, Naval Medical Research Center/Walter Reed Army Institute of Research, Silver Spring, MD 20910, USA

Received 18 August 2016; Revised 6 October 2016; Accepted 6 November 2016

Academic Editor: Kwadwo Koram

Copyright © 2016 Mirian Mendoza 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. C. J. L. Murray, L. C. Rosenfeld, S. S. Lim et al., “Global malaria mortality between 1980 and 2010: a systematic analysis,” The Lancet, vol. 379, no. 9814, pp. 413–431, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Z. Garamszegi, “Global distribution of malaria-resistant MHC-HLA alleles: the number and frequencies of alleles and malaria risk,” Malaria Journal, vol. 13, no. 1, article 349, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. J. May, C. G. Meyer, J. F. J. Kun et al., “HLA class II factors associated with Plasmodium falciparum merozoite surface antigen allele families,” Journal of Infectious Diseases, vol. 179, no. 4, pp. 1042–1045, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. A. D. Osafo-Addo, K. A. Koram, A. R. Oduro, M. Wilson, A. Hodgson, and W. O. Rogers, “HLA-DRB1*04 allele is associated with severe malaria in Northern Ghana,” American Journal of Tropical Medicine and Hygiene, vol. 78, no. 2, pp. 251–255, 2008. View at Google Scholar · View at Scopus
  5. A. V. S. Hill, C. E. M. Allsopp, D. Kwiatkowski et al., “Common West African HLA antigens are associated with protection from severe malaria,” Nature, vol. 352, no. 6336, pp. 595–600, 1991. View at Publisher · View at Google Scholar · View at Scopus
  6. A. V. S. Hill, “The immunogenetics of human infectious diseases,” Annual Review of Immunology, vol. 16, pp. 593–617, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. J. May, B. Lell, A. J. F. Luty, C. G. Meyer, and P. G. Kremsner, “HLA-DQB10501-restricted Th1 type immune responses to Plasmodium falciparum liver stage antigen 1 protect against malaria anemia and reinfections,” Journal of Infectious Diseases, vol. 183, no. 1, pp. 168–172, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Busson, A. Vu Trieu, P. Labelle et al., “HLA-DRB1 and DQB1 allele distribution in the Muong population exposed to malaria in Vietnam,” Tissue Antigens, vol. 59, no. 6, pp. 470–474, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. W. Wijayalath, R. Danner, Y. Kleschenko et al., “HLA class II (DR0401) molecules induce Foxp3+ regulatory T cell suppression of B cells in Plasmodium yoelii strain 17XNL malaria,” Infection and Immunity, vol. 82, no. 1, pp. 286–297, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Arnold, R. Kumar Tyagi, P. Mejia, N. Van Rooijen, J.-L. Pérignon, and P. Druilhe, “Analysis of innate defences against Plasmodium falciparum in immunodeficient mice,” Malaria Journal, vol. 9, pp. 197–209, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Arnold, R. K. Tyagi, P. Meija et al., “Further improvements of the P. falciparum humanized mouse model,” PLOS ONE, vol. 6, no. 3, Article ID e18045, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. W. Wijayalath, S. Majji, Y. Kleschenko et al., “DRAG humanized (DR4.RagKO.IL2RgcKO.NOD) mice sustain the complete vertebrate life cycle of Plasmodium falciparum malaria,” Malaria Journal, vol. 13, pp. 386–400, 2014. View at Google Scholar
  13. T. L. Delovitch and B. Singh, “The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD,” Immunity, vol. 7, no. 6, pp. 727–738, 1997. View at Publisher · View at Google Scholar
  14. M. S. Anderson and J. A. Bluestone, “The NOD mouse: a model of immune dysregulation,” Annual Review of Immunology, vol. 23, pp. 447–485, 2005. View at Publisher · View at Google Scholar
  15. T. L. Van Belle, K. T. Coppieters, and M. G. Von Herrath, “Type 1 diabetes: etiology, immunology, and therapeutic strategies,” Physiological Reviews, vol. 91, no. 1, pp. 79–118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. K. T. Coppieters, A. Wiberg, and M. G. von Herrath, “Viral infections and molecular mimicry in type 1 diabetes,” APMIS, vol. 120, no. 12, pp. 941–949, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. J. A. Pane, N. L. Webster, K. L. Graham, G. Holloway, C. Zufferey, and B. S. Coulson, “Rotavirus acceleration of murine type 1 diabetes is associated with a T helper 1-dependent specific serum antibody response and virus effects in regional lymph nodes,” Diabetologia, vol. 56, no. 3, pp. 573–582, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. Pane and B. S. Coulson, “Lessons from the mouse: potential contribution of bystander lymphocyte activation by viruses to human type 1 diabetes,” Diabetologia, vol. 58, no. 6, pp. 1149–1159, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Knip and O. Simell, “Environmental triggers of type 1 diabetes,” Cold Spring Harbor Perspectives in Medicine, vol. 2, no. 7, Article ID a007690, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. A. S. Lee, D. L. Gibson, Y. Zhang, H. P. Sham, B. A. Vallance, and J. P. Dutz, “Gut barrier disruption by an enteric bacterial pathogen accelerates insulitis in NOD mice,” Diabetologia, vol. 53, no. 4, pp. 741–748, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Wen, R. E. Ley, P. Y. Volchkov et al., “Innate immunity and intestinal microbiota in the development of type 1 diabetes,” Nature, vol. 455, no. 7216, pp. 1109–1113, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Valdés, N. Unanue, M. Hernández et al., “Is there a link between influenza and type I diabetes? Increased incidence of TID during the pandemic H1N1 influenza of 2009 in Chile,” Pediatric Endocrinology Reviews, vol. 11, no. 2, pp. 161–166, 2013. View at Google Scholar · View at Scopus
  23. K. M. Drescher, K. Kono, S. Bopegamage, S. D. Carson, and S. Tracy, “Coxsackievirus B3 infection and type 1 diabetes development in NOD mice: insulitis determines susceptibility of pancreatic islets to virus infection,” Virology, vol. 329, no. 2, pp. 381–394, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. D. V. Serreze, C. Wasserfall, E. W. Ottendorfer et al., “Diabetes acceleration or prevention by a coxsackievirus B4 infection: critical requirements for both interleukin-4 and gamma interferon,” Journal of Virology, vol. 79, no. 2, pp. 1045–1052, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Jaïdane and D. Hober, “Role of coxsackievirus B4 in the pathogenesis of type 1 diabetes,” Diabetes and Metabolism, vol. 34, no. 6, pp. 537–548, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. C. W. Farnsworth, C. T. Shehatou, R. Maynard et al., “A humoral immune defect distinguishes the response to Staphylococcus aureus infections in mice with obesity and type 2 diabetes from that in mice with type 1 diabetes,” Infection and Immunity, vol. 83, no. 6, pp. 2264–2274, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Petzold, M. Solimena, and K.-P. Knoch, “Mechanisms of beta cell dysfunction associated with viral infection,” Current Diabetes Reports, vol. 15, no. 10, article no. 73, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Jaïdane, P. Sauter, F. Sane, A. Goffard, J. Gharbi, and D. Hober, “Enteroviruses and type 1 diabetes: towards a better understanding of the relationship,” Reviews in Medical Virology, vol. 20, no. 5, pp. 265–280, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Hober and E. K. Alidjinou, “Enteroviral pathogenesis of type 1 diabetes: queries and answers,” Current Opinion in Infectious Diseases, vol. 26, no. 3, pp. 263–269, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. N. G. Morgan and S. J. Richardson, “Enteroviruses as causative agents in type 1 diabetes: loose ends or lost cause?” Trends in Endocrinology and Metabolism, vol. 25, no. 12, pp. 611–619, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Tai, J. Peng, F. Liu et al., “Microbial antigen mimics activate diabetogenic CD8 T cells in NOD mice,” The Journal of Experimental Medicine, vol. 213, no. 10, pp. 2129–2146, 2016. View at Publisher · View at Google Scholar
  32. L. P. Sang, S. Majji, S. Casares, and T. D. Brumeanu, “Long-term silencing of autoimmune diabetes and improved life expectancy by a soluble pHLA-DR4 chimera in a newly-humanized,” Human Vaccines & Immunotherapeutics, vol. 10, no. 3, pp. 693–699, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. F. I. Weinbaum, C. B. Evans, R. E. Tigelaar et al., “Immunity to Phasmodium Berghei Yoelii in mice: I. The course of infection in T cell and B cell deficient mice,” The Journal of Immunology, vol. 117, pp. 1999–2005, 1976. View at Google Scholar
  34. M. G. Morgado, P. Cam, C. Gris-Liebe, P.-A. Cazenava, and E. Jouvin-Marche, “Further evidence that BALB/c and C57BL/6 γ2a genes originate from two distinct isotypes,” EMBO Journal, vol. 8, no. 11, pp. 3245–3251, 1989. View at Google Scholar · View at Scopus
  35. L. Pow Sang, J. Surls, M. Mendoza, S. Casares, and T. Brumeanu, “HLA-DR*0401 expression in the NOD mice prevents the development of autoimmune diabetes by multiple alterations in the T-cell compartment,” Cellular Immunology, vol. 298, no. 1-2, pp. 54–65, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Kreuzer, E. Nikoopour, B. C. Au et al., “Reduced interferon-α production by dendritic cells in type 1 diabetes does not impair immunity to influenza virus,” Clinical & Experimental Immunology, vol. 179, no. 2, pp. 245–255, 2015. View at Publisher · View at Google Scholar
  37. A. Kondrashova, N. Nurminen, M. Patrikainen et al., “Influenza A virus antibodies show no association with pancreatic islet autoantibodies in children genetically predisposed to type 1 diabetes,” Diabetologia, vol. 58, no. 11, pp. 2592–2595, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Casares and T. L. Richie, “Immune evasion by malaria parasites: a challenge for vaccine development,” Current Opinion in Immunology, vol. 21, no. 3, pp. 321–330, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. A. M. D'Alise, V. Auyeung, M. Feuerer et al., “The defect in T-cell regulation in NOD mice is an effect on the T-cell effectors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 50, pp. 19857–19862, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. K. H. Lee, K. W. Wucherpfennig, and D. C. Wiley, “Structure of a human insulin peptide-HLA-DQ8 complex and susceptibility to type I diabetes,” Nature Immunology, vol. 2, no. 6, pp. 501–507, 2001. View at Publisher · View at Google Scholar · View at Scopus