Rotavirus Activates Lymphocytes from Non-Obese Diabetic Mice by Triggering Toll-Like Receptor 7 Signaling and Interferon Production in Plasmacytoid Dendritic Cells

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Understanding how viruses contribute to type 1 diabetes development is vital for disease prevention. Infection of children at-risk of diabetes with the gastrointestinal pathogen rotavirus is associated with increased immune responses to pancreatic islets, leading to the proposal that rotavirus infection may accelerate progression to diabetes. In a mouse model, we showed previously that rotavirus accelerates diabetes onset, in conjunction with virus spread to the lymph nodes, draining the intestine and pancreas. At these sites, rotavirus associates with antigen-presenting cells of the immune system, including dendritic cells, leading to their maturation, and induces the activation of B and T cells. Here we use this mouse model to define the contribution of rotavirus-exposed antigen-presenting cells to the activation of neighboring B and T cells. We found that rotavirus-exposed dendritic cells induce B and T cell activation through secretion of type I interferon. Activation of these dendritic cells depends on recognition of viral RNA by Toll-like receptor 7. Our studies suggest that this mechanism of B and T cell activation may occur in RRV-infected mice and contribute to their accelerated diabetes development. A similar mechanism may be involved in the enhanced islet autoantibody responses of children following rotavirus infection.

Vyšlo v časopise: Rotavirus Activates Lymphocytes from Non-Obese Diabetic Mice by Triggering Toll-Like Receptor 7 Signaling and Interferon Production in Plasmacytoid Dendritic Cells. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003998
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003998

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Zdroje

1. DanemanD (2006) Type 1 diabetes. Lancet 367: 847–858.

2. RedondoMJ, FainPR, EisenbarthGS (2001) Genetics of type 1A diabetes. Recent Prog Horm Res 56: 69–89.

3. KnipM, VeijolaR, VirtanenSM, HyotyH, VaaralaO, et al. (2005) Environmental triggers and determinants of type 1 diabetes. Diabetes 54 Suppl 2S125–136.

4. VaaralaO (2012) Is the origin of type 1 diabetes in the gut? Immunol Cell Biol 90: 271–276.

5. van der WerfN, KroeseFG, RozingJ, HillebrandsJL (2007) Viral infections as potential triggers of type 1 diabetes. Diabetes Metab Res Rev 23: 169–183.

6. YeungWC, RawlinsonWD, CraigME (2011) Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 342: d35.

7. SaneF, MoumnaI, HoberD (2011) Group B coxsackieviruses and autoimmunity: focus on Type 1 diabetes. Expert Rev Clin Immunol 7: 357–366.

8. HoneymanMC, CoulsonBS, StoneNL, GellertSA, GoldwaterPN, et al. (2000) Association between rotavirus infection and pancreatic islet autoimmunity in children at risk of developing type 1 diabetes. Diabetes 49: 1319–1324.

9. LempainenJ, TauriainenS, VaaralaO, MakelaM, HonkanenH, et al. (2012) Interaction of enterovirus infection and cow's milk-based formula nutrition in type 1 diabetes-associated autoimmunity. Diabetes Metab Res Rev 28: 177–185.

10. CoppietersKT, WibergA, von HerrathMG (2012) Viral infections and molecular mimicry in type 1 diabetes. APMIS 120: 941–949.

11. GrahamKL, SandersN, TanY, AllisonJ, KayTW, et al. (2008) Rotavirus infection accelerates type 1 diabetes in mice with established insulitis. J Virol 82: 6139–6149.

12. PaneJA, WebsterNL, GrahamKL, HollowayG, ZuffereyC, et al. (2013) 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 56: 573–582.

13. GrahamKL, O'DonnellJA, TanY, SandersN, CarringtonEM, et al. (2007) Rotavirus infection of infant and young adult nonobese diabetic mice involves extraintestinal spread and delays diabetes onset. J Virol 81: 6446–6458.

14. PaneJA, WebsterNL, ZuffereyC, CoulsonBS (2014) Rotavirus acceleration of murine type 1 diabetes is associated with increased MHC class I-restricted antigen presentation by B cells and elevated proinflammatory cytokine expression by T cells. Virus Res 179: 73–84.

15. BluttSE, CrawfordSE, WarfieldKL, LewisDE, EstesMK, et al. (2004) The VP7 outer capsid protein of rotavirus induces polyclonal B-cell activation. J Virol 78: 6974–6981.

16. NarvaezCF, FrancoMA, AngelJ, MortonJM, GreenbergHB (2010) Rotavirus differentially infects and polyclonally stimulates human B cells depending on their differentiation state and tissue of origin. J Virol 84: 4543–4555.

17. DealEM, LahlK, NarvaezCF, ButcherEC, GreenbergHB (2013) Plasmacytoid dendritic cells promote rotavirus-induced human and murine B cell responses. J Clin Invest 123: 2464–2474.

18. DealEM, JaimesMC, CrawfordSE, EstesMK, GreenbergHB (2010) Rotavirus structural proteins and dsRNA are required for the human primary plasmacytoid dendritic cell IFN alpha response. PLoS Pathog 6: e1000931 doi:1000910.1001371/journal.ppat.1000931

19. MesaMC, RodriguezLS, FrancoMA, AngelJ (2007) Interaction of rotavirus with human peripheral blood mononuclear cells: plasmacytoid dendritic cells play a role in stimulating memory rotavirus specific T cells in vitro. Virology 366: 174–184.

20. LiQ, XuB, MichieSA, RubinsKH, SchreriberRD, et al. (2008) Interferon-alpha initiates type 1 diabetes in nonobese diabetic mice. Proc Natl Acad Sci U S A 105: 12439–12444.

21. LiQ, McDevittHO (2011) The role of interferon alpha in initiation of type I diabetes in the NOD mouse. Clin Immunol 140: 3–7.

22. DianaJ, SimoniY, FurioL, BeaudoinL, AgerberthB, et al. (2013) Crosstalk between neutrophils, B-1a cells and plasmacytoid dendritic cells initiates autoimmune diabetes. Nat Med 19: 65–73.

23. ChehadehW, WeillJ, VantyghemMC, AlmG, LefebvreJ, et al. (2000) Increased level of interferon-alpha in blood of patients with insulin-dependent diabetes mellitus: relationship with coxsackievirus B infection. J Infect Dis 181: 1929–1939.

24. FinkelmanFD, SveticA, GresserI, SnapperC, HolmesJ, et al. (1991) Regulation by interferon alpha of immunoglobulin isotype selection and lymphokine production in mice. J Exp Med 174: 1179–1188.

25. FairfaxKA, KalliesA, NuttSL, TarlintonDM (2008) Plasma cell development: from B-cell subsets to long-term survival niches. Semin Immunol 20: 49–58.

26. LudertJE, RuizMC, HidalgoC, LiprandiF (2002) Antibodies to rotavirus outer capsid glycoprotein VP7 neutralize infectivity by inhibiting virion decapsidation. J Virol 76: 6643–6651.

27. NarvaezCF, AngelJ, FrancoMA (2005) Interaction of rotavirus with human myeloid dendritic cells. J Virol 79: 14526–14535.

28. LosekeS, Grage-GriebenowE, HeineH, WagnerA, AkiraS, et al. (2006) In vitro-generated viral double-stranded RNA in contrast to polyinosinic:polycytidylic acid induces interferon-alpha in human plasmacytoid dendritic cells. Scand J Immunol 63: 264–274.

29. HornungV, Guenthner-BillerM, BourquinC, AblasserA, SchleeM, et al. (2005) Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat Med 11: 263–270.

30. Silva-AyalaD, LopezT, GutierrezM, PerrimonN, LopezS, et al. (2013) Genome-wide RNAi screen reveals a role for the ESCRT complex in rotavirus cell entry. Proc Natl Acad Sci U S A 110: 10270–10275.

31. AokiST, TraskSD, CoulsonBS, GreenbergHB, DormitzerPR, et al. (2011) Cross-linking of rotavirus outer capsid protein VP7 by antibodies or disulfides inhibits viral entry. J Virol 85: 10509–10517.

32. GroeneWS, ShawRD (1992) Psoralen preparation of antigenically intact noninfectious rotavirus particles. J Virol Methods 38: 93–102.

33. ShawRD, HempsonSJ, MackowER (1995) Rotavirus diarrhea is caused by nonreplicating viral particles. J Virol 69: 5946–5950.

34. RuscanuS, PascaleF, BourgeM, HematiB, Elhmouzi-YounesJ, et al. (2012) The double-stranded RNA bluetongue virus induces type I interferon in plasmacytoid dendritic cells via a MYD88-dependent TLR7/8-independent signaling pathway. J Virol 86: 5817–5828.

35. ColonnaM, TrinchieriG, LiuYJ (2004) Plasmacytoid dendritic cells in immunity. Nat Immunol 5: 1219–1226.

36. KieferK, OropalloMA, CancroMP, Marshak-RothsteinA (2012) Role of type I interferons in the activation of autoreactive B cells. Immunol Cell Biol 90: 498–504.

37. MarinoE, TanB, BingeL, MackayCR, GreyST (2012) B-cell cross-presentation of autologous antigen precipitates diabetes. Diabetes 61: 2893–2905.

38. FeldmanAG, TuckerRM, FennerEK, PelandaR, MackCL (2013) B cell deficient mice are protected from biliary obstruction in the rotavirus-induced mouse model of biliary atresia. PLoS One 8: e73644 doi:73610.71371/journal.pone.0073644

39. BraunD, CaramalhoI, DemengeotJ (2002) IFN-alpha/beta enhances BCR-dependent B cell responses. Int Immunol 14: 411–419.

40. Bekeredjian-DingIB, WagnerM, HornungV, GieseT, SchnurrM, et al. (2005) Plasmacytoid dendritic cells control TLR7 sensitivity of naive B cells via type I IFN. J Immunol 174: 4043–4050.

41. CoroES, ChangWL, BaumgarthN (2006) Type I IFN receptor signals directly stimulate local B cells early following influenza virus infection. J Immunol 176: 4343–4351.

42. FenauxM, CuadrasMA, FengN, JaimesM, GreenbergHB (2006) Extraintestinal spread and replication of a homologous EC rotavirus strain and a heterologous rhesus rotavirus in BALB/c mice. J Virol 80: 5219–5232.

43. TurleySJ, LeeJW, Dutton-SwainN, MathisD, BenoistC (2005) Endocrine self and gut non-self intersect in the pancreatic lymph nodes. Proc Natl Acad Sci U S A 102: 17729–17733.

44. JaakkolaI, JalkanenS, HanninenA (2003) Diabetogenic T cells are primed both in pancreatic and gut-associated lymph nodes in NOD mice. Eur J Immunol 33: 3255–3264.

45. ChenX, MakalaLH, JinY, HopkinsD, MuirA, et al. (2008) Type 1 diabetes patients have significantly lower frequency of plasmacytoid dendritic cells in the peripheral blood. Clin Immunol 129: 413–418.

46. HuangX, YuangJ, GoddardA, FoulisA, JamesRF, et al. (1995) Interferon expression in the pancreases of patients with type I diabetes. Diabetes 44: 658–664.

47. AllenJS, PangK, SkoweraA, EllisR, RackhamC, et al. (2009) Plasmacytoid dendritic cells are proportionally expanded at diagnosis of type 1 diabetes and enhance islet autoantigen presentation to T-cells through immune complex capture. Diabetes 58: 138–145.

48. BrodSA, MaloneM, DarcanS, PapollaM, NelsonL (1998) Ingested interferon alpha suppresses type I diabetes in non-obese diabetic mice. Diabetologia 41: 1227–1232.

49. SobelDO, AhvaziB (1998) Alpha-interferon inhibits the development of diabetes in NOD mice. Diabetes 47: 1867–1872.

50. De BoissieuD, LebonP, BadoualJ, BompardY, DupontC (1993) Rotavirus induces alpha-interferon release in children with gastroenteritis. J Pediatr Gastroenterol Nutr 16: 29–32.

51. VerdaguerJ, SchmidtD, AmraniA, AndersonB, AverillN, et al. (1997) Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice. J Exp Med 186: 1663–1676.

52. HewishMJ, TakadaY, CoulsonBS (2000) Integrins alpha2beta1 and alpha4beta1 can mediate SA11 rotavirus attachment and entry into cells. J Virol 74: 228–236.

53. HollowayG, CoulsonBS (2006) Rotavirus activates JNK and p38 signaling pathways in intestinal cells, leading to AP-1-driven transcriptional responses and enhanced virus replication. J Virol 80: 10624–10633.

54. HalaszP, HollowayG, TurnerSJ, CoulsonBS (2008) Rotavirus replication in intestinal cells differentially regulates integrin expression by a phosphatidylinositol 3-kinase-dependent pathway, resulting in increased cell adhesion and virus yield. J Virol 82: 148–160.

55. KolumamGA, ThomasS, ThompsonLJ, SprentJ, Murali-KrishnaK (2005) Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 202: 637–650.

56. WeiJ, WaithmanJ, LataR, MifsudNA, CebonJ, et al. (2010) Influenza A infection enhances cross-priming of CD8+ T cells to cell-associated antigens in a TLR7- and type I IFN-dependent fashion. J Immunol 185: 6013–6022.

57. CoulsonBS, UnicombLE, PitsonGA, BishopRF (1987) Simple and specific enzyme immunoassay using monoclonal antibodies for serotyping human rotaviruses. J Clin Microbiol 25: 509–515.

58. CoulsonBS, FowlerKJ, BishopRF, CottonRG (1985) Neutralizing monoclonal antibodies to human rotavirus and indications of antigenic drift among strains from neonates. J Virol 54: 14–20.

59. BarratFJ, MeekerT, GregorioJ, ChanJH, UematsuS, et al. (2005) Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J Exp Med 202: 1131–1139.

60. CnopM, WelshN, JonasJC, JornsA, LenzenS, et al. (2005) Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 54 Suppl 2S97–107.