Previous maternal infection protects offspring from enterovirus infection and prevents experimental diabetes development in mice

Diabetologia

Volumn 56, Issue 4, 2013, Pages 867-874

  Larsson, P G ^a   Lakshmikanth, T ^a,b   Svedin, E ^a   King, C ^c   Flodstrom Tullberg M ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Coxsackievirus; Enterovirus; Maternal antibodies; NOD mouse; Poliovirus hypothesis; Socs1 tg mouse; Type 1 diabetes

Indexed keywords

MATERNAL ANTIBODY; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; COXSACKIE VIRUS B3; COXSACKIE VIRUS INFECTION; DIABETES MELLITUS; FEMALE; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTECTION; VERTICAL TRANSMISSION; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, VIRAL; DIABETES MELLITUS, EXPERIMENTAL; ENTEROVIRUS INFECTIONS; FEMALE; IMMUNOGLOBULIN G; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; PREGNANCY; PREGNANCY, ANIMAL;

EID: 84876483384     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-013-2834-z     Document Type: Article

References (40)

1. Richer MJ, Horwitz MS (2009) Coxsackievirus infection as an environmental factor in the etiology of type 1 diabetes. Autoimmun Rev 8:611-615
2. Hober D, Sauter P (2010) Pathogenesis of type 1 diabetes mellitus: interplay between enterovirus and host. Nat Rev Endocrinol 6:279-289
3. Stene LC, Oikarinen S, Hyoty H et al (2010) Enterovirus infection and progression from islet autoimmunity to type 1 diabetes: the Diabetes and Autoimmunity Study in the Young (DAISY). Diabetes 59:3174-3180
4. Yeung WC, Rawlinson WD, Craig ME (2011) Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 342:d35
5. Ghazarian L, Diana J, Simoni Y, Beaudoin L, Lehuen A (2013) Prevention or acceleration of type 1 diabetes by viruses. Cell Mol Life Sci 70:239-255
6. Ylipaasto P, Klingel K, Lindberg AM et al (2004) Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet beta cells. Diabetologia 47:225-239
7. Dotta F, Censini S, van Halteren AG et al (2007) Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci U S A 104:5115-5120
8. Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG (2009) The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 52:1143-1151
9. Oikarinen M, Tauriainen S, Honkanen T et al (2008) Detection of enteroviruses in the intestine of type 1 diabetic patients. Clin Exp Immunol 151:71-75
10. Oikarinen M, Tauriainen S, Oikarinen S et al (2012) Type 1 diabetes is associated with enterovirus infection in gut mucosa. Diabetes 61:687-691
11. Mercalli A, Lampasona V, Klingel K et al (2012) No evidence of enteroviruses in the intestine of patients with type 1 diabetes. Diabetologia 55:2479-2488
12. Hultcrantz M, Huhn MH, Wolf M et al (2007) Interferons induce an antiviral state in human pancreatic islet cells. Virology 367:92-101
13. Flodstrom M, Maday A, Balakrishna D, Cleary MM, Yoshimura A, Sarvetnick N (2002) Target cell defense prevents the development of diabetes after viral infection. Nat Immunol 3:373-382
14. Flodstrom M, Tsai D, Fine C, Maday A, Sarvetnick N (2003) Diabetogenic potential of human pathogens uncovered in experimentally permissive beta-cells. Diabetes 52:2025-2034
15. Serreze DV, Ottendorfer EW, Ellis TM, Gauntt CJ, Atkinson MA (2000) Acceleration of type 1 diabetes by a coxsackievirus infection requires a preexisting critical mass of autoreactive T cells in pancreatic islets. Diabetes 49:708-711
16. Tracy S, Drescher KM, Chapman NM et al (2002) Toward testing the hypothesis that group B coxsackieviruses (CVB) trigger insulin-dependent diabetes: inoculating nonobese diabetic mice with CVB markedly lowers diabetes incidence. J Virol 76:12097-12111
17. Serreze DV, Wasserfall C, Ottendorfer EW et al (2005) Diabetes acceleration or prevention by a coxsackievirus B4 infection: critical requirements for both interleukin-4 and gamma interferon. J Virol 79:1045-1052
18. The DIAMOND Project Group (2006) Incidence and trends of childhood type 1 diabetes worldwide 1990-1999. Diabet Med 23:857-866
19. Viskari H, Ludvigsson J, Uibo R et al (2004) Relationship between the incidence of type 1 diabetes and enterovirus infections in different European populations: results from the EPIVIR project. J Med Virol 72:610-617
20. Viskari H, Ludvigsson J, Uibo R et al (2005) Relationship between the incidence of type 1 diabetes and maternal enterovirus antibodies: time trends and geographical variation. Diabetologia 48:1280-1287
21. Nathanson N, Martin JR (1979) The epidemiology of poliomyelitis: enigmas surrounding its appearance, epidemicity, and disappearance. Am J Epidemiol 110:672-692
22. Viskari HR, Koskela P, Lonnrot M et al (2000) Can enterovirus infections explain the increasing incidence of type 1 diabetes? Diabetes Care 23:414-416
23. Zinkernagel RM (2001) Maternal antibodies, childhood infections, and autoimmune diseases. N Engl J Med 345:1331-1335
24. Zinkernagel RM (2003) On natural and artificial vaccinations. Annu Rev Immunol 21:515-546
25. Gamble DR (1980) The epidemiology of insulin dependent diabetes with particular reference to the relationship of virus infection to its etiology. Epidemiol Rev 2:49-70
26. Sadeharju K, Knip M, Virtanen SM et al (2007) Maternal antibodies in breast milk protect the child from enterovirus infections. Pediatrics 119:941-946
27. Tirabassi RS, Guberski DL, Blankenhorn EP et al (2010) Infection with viruses from several families triggers autoimmune diabetes in LEW1WR1 rats: prevention of diabetes by maternal immunization. Diabetes 59:110-118
28. Flodstrom-Tullberg M, Yadav D, Hagerkvist R et al (2003) Target cell expression of suppressor of cytokine signaling-1 prevents diabetes in the NOD mouse. Diabetes 52:2696-2700
29. Hultcrantz M, Jacobson S, Hill NJ, Santamaria P, Flodstrom-Tullberg M (2009) The target cell response to cytokines governs the autoreactive T cell repertoire in the pancreas of NOD mice. Diabetologia 52:299-305
30. Flodstrom-Tullberg M, Hultcrantz M, Stotland A et al (2005) RNase L and double-stranded RNA-dependent protein kinase exert complementary roles in islet cell defense during coxsackievirus infection. J Immunol 174:1171-1177
31. Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N (1998) Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med 4:781-785
32. Appleby P, Catty D (1983) Transmission of immunoglobulin to foetal and neonatal mice. J Reprod Immunol 5:203-213
33. Ziegler AG, Hummel M, Schenker M, Bonifacio E (1999) Autoantibody appearance and risk for development of childhood diabetes in offspring of parents with type 1 diabetes: the 2-year analysis of the German BABYDIAB Study. Diabetes 48:460-468
34. Kimpimaki T, Kupila A, Hamalainen AM et al (2001) The first signs of beta-cell autoimmunity appear in infancy in genetically susceptible children from the general population: the Finnish Type 1 Diabetes Prediction and Prevention Study. J Clin Endocrinol Metab 86:4782-4788
35. Ohashi PS, Oehen S, Buerki K et al (1991) Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 65:305-317
36. Oldstone MB, Nerenberg M, Southern P, Price J, Lewicki H (1991) Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 65:319-331
37. Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299:1259-1260
38. Bach JF (2001) Protective role of infections and vaccinations on autoimmune diseases. J Autoimmun 16:347-353
39. PrabhuDas M, Adkins B, Gans H et al (2011) Challenges in infant immunity: implications for responses to infection and vaccines. Nat Immunol 12:189-194
40. Salur L, Oikarinen S, Tauriainen S, Mandel M, Hyoty H, Uibo R (2011) Enterovirus infections in young infants: are children still protected by maternal antibodies? Hum Vaccines 7:966-971