Recovery of an Antiviral Antibody Response following Attrition Caused by Unrelated Infection

English version České info

The homeostatic mechanisms that regulate the maintenance of immunological memory to the multiple pathogen encounters over time are unknown. We found that a single malaria episode caused significant dysregulation of pre-established Influenza A virus-specific long-lived plasma cells (LLPCs) resulting in the loss of Influenza A virus-specific Abs and increased susceptibility to Influenza A virus re-infection. This loss of LLPCs involved an FcγRIIB-dependent mechanism, leading to their apoptosis. However, given enough time following malaria, the LLPC pool and humoral immunity to Influenza A virus were eventually restored. Supporting a role for continuous conversion of Influenza A virus-specific B into LLPCs in the restoration of Influenza A virus immunity, B cell depletion experiments also demonstrated a similar requirement for the long-term maintenance of serum Influenza A virus-specific Abs in an intact LLPC compartment. These findings show that, in addition to their established role in the anamnestic response to reinfection, the B cell pool continues to be a major contributor to the maintenance of long-term humoral immunity following primary Influenza A virus infection, and to the recovery from attrition following heterologous infection. These data have implications for understanding the longevity of protective efficacy of vaccinations in countries where continuous infections are endemic.

Vyšlo v časopise: Recovery of an Antiviral Antibody Response following Attrition Caused by Unrelated Infection. PLoS Pathog 10(1): e32767. doi:10.1371/journal.ppat.1003843
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003843

Souhrn

Zdroje

1. VieiraP, RajewskyK (1988) The half-lives of serum immunoglobulins in adult mice. Eur J Immunol 18: 313–316.

2. YuX, TsibaneT, McGrawPA, HouseFS, KeeferCJ, et al. (2008) Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455: 532–526.

3. SlifkaMK, AntiaR, WhitmireJK, AhmedR (1998) Humoral immunity due to long-lived plasma cells. Immunity 8: 363–372.

4. RadbruchA, MuehlinghausG, LugerEO, InamineA, SmithKGC, et al. (2006) Competence and competition: the challenge of becoming a long-lived plasma cell. Nat Rev Immunol 6: 741–750.

5. NduatiEW, NgDHL, NdunguFM, GardnerP, UrbanBC, et al. (2010) Distinct Kinetics of Memory B-Cell and Plasma-Cell Responses in Peripheral Blood Following a Blood-Stage Plasmodium chabaudi Infection in Mice. PLoS One 5: e15007.

6. GreenwoodBM (1974) Possible role of a B-cell mitogen in hypergammaglobulinaemia in malaria and trypanosomiasis. Lancet 303: 435–436.

7. CadmanET, AbdallahAY, VoisineC, SponaasAM, CorranP, et al. (2008) Alterations of splenic architecture in malaria are induced independently of Toll-like receptors 2, 4, and 9 or MyD88 and may affect antibody affinity. Infect Immun 76: 3924–3931.

8. AchtmanAH, StephensR, CadmanET, HarrisonV, LanghorneJ (2007) Malaria-specific antibody responses and parasite persistence after infection of mice with Plasmodium chabaudi chabaudi. Parasite Immunol 29: 435–444.

9. LooareesuwanS, HoM, WattanagoonY, WhiteNJ, WarrellDA, et al. (1987) Dynamic alteration in splenic function during acute falciparum malaria. N Engl J Med 317: 675–679.

10. WykesMN, ZhouYH, LiuXQ, GoodMF (2005) Plasmodium yoelii can ablate vaccine-induced long-term protection in mice. J Immunol 175: 2510–2516.

11. Strambachová-McBrideJ, MicklemHS (1979) Immunosuppression in murine malaria. IV. The secondary response to bovine serum albumin. Parasite Immunol 1: 141–157.

12. RadwanskaM, GuirnaldaP, De TrezC, RyffelB, BlackS, et al. (2008) Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathog 4: e1000078.

13. XiangZ, CutlerAJ, BrownlieRJ, FairfaxK, LawlorKE, et al. (2007) FcγRIIb controls bone marrow plasma cell persistence and apoptosis. Nat Immunol 8: 419–429.

14. GoumardP, VuDN, MauroisP, CamusD (1982) Influence of malaria on a pre-existing antibody response to heterologous antigens. Ann Immunol (Paris) 133: 313–326.

15. AmannaIJ, CarlsonNE, SlifkaMK (2007) Duration of humoral immunity to common viral and vaccine antigens. N Engl J Med 357: 1903–1915.

16. KassiotisG, GrayD, KiafardZ, ZwirnerJ, StockingerB (2006) Functional specialization of memory Th cells revealed by expression of integrin CD49b. J Immunol 177: 968–975.

17. FlynnKJ, BelzGT, AltmanJD, AhmedR, WoodlandDL, et al. (1998) Virus-Specific CD8+ T Cells in Primary and Secondary Influenza Pneumonia. Immunity 8: 683–691.

18. OdendahlM, MeiH, HoyerBF, JacobiAM, HansenA, et al. (2005) Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood 105: 1614–1621.

19. ClatworthyMR, WillcocksL, UrbanB, LanghorneJ, WilliamsTN, et al. (2007) Systemic lupus erythematosus-associated defects in the inhibitory receptor FcγRIIb reduce susceptibility to malaria. Proc Natl Acad Sci U S A 104: 7169–7174.

20. TraggiaiE, PuzoneR, LanzavecchiaA (2003) Antigen dependent and independent mechanisms that sustain serum antibody levels. Vaccine 21: S35–S37.

21. BernasconiNL, OnaiN, LanzavecchiaA (2003) A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101: 4500–4504.

22. BernasconiNL, TraggiaiE, LanzavecchiaA (2002) Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298: 2199–2202.

23. GongQ, OuQ, YeS, LeeWP, CorneliusJ, et al. (2005) Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J Immunol 174: 817–826.

24. AhujaA, ShupeJ, DunnR, KashgarianM, KehryMR, et al. (2007) Depletion of B cells in murine lupus: efficacy and resistance. J Immunol 179: 3351–3361.

25. AhujaA, AndersonSM, KhalilA, ShlomchikMJ (2008) Maintenance of the plasma cell pool is independent of memory B cells. Proc Natl Acad Sci U S A 105: 4802–4807.

26. DiLilloDJ, HamaguchiY, UedaY, YangK, UchidaJ, et al. (2008) Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol 180: 361–371.

27. MoserK, TokoyodaK, RadbruchA, MacLennanI, ManzRA (2006) Stromal niches, plasma cell differentiation and survival. Curr Opin Immunol 18: 265–270.

28. SzeDMY, ToellnerKM, de VinuesaCG, TaylorDR, MacLennanI (2000) Intrinsic constraint on plasmablast growth and extrinsic limits of plasma cell survival. J Exp Med 192: 813–821.

29. TerstappenLW, JohnsenS, Segers-NoltenIM, LokenMR (1990) Identification and characterization of plasma cells in normal human bone marrow by high-resolution flow cytometry. Blood 76: 1739–1747.

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

31. VezysV, YatesA, CaseyKA, LanierG, AhmedR, et al. (2008) Memory CD8 T-cell compartment grows in size with immunological experience. Nature 457: 196–199.

32. VikiB, NathalieG (2011) Acute Disruption of Bone Marrow B Lymphopoiesis and Apoptosis of Transitional and Marginal Zone B Cells in the Spleen following a Blood-Stage Plasmodium chabaudi Infection in Mice. J Parasitol Res 2011: 534697.

33. TokoyodaK, EgawaT, SugiyamaT, ChoiBI, NagasawaT (2004) Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 20: 707–718.

34. StephensR, NdunguFM, LanghorneJ (2009) Germinal centre and marginal zone B cells expand quickly in a second Plasmodium chabaudi malaria infection producing mature plasma cells. Parasite Immunol 31: 20–31.

35. MaruyamaM, LamKP, RajewskyK (2000) Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407: 636–642.

36. TomaykoMM, AndersonSM, BraytonCE, SadanandS, SteinelNC, et al. (2008) Systematic comparison of gene expression between murine memory and naive B cells demonstrates that memory B cells have unique signaling capabilities. J Immunol 181: 27–38.

37. CrottyS, FelgnerP, DaviesH, GlidewellJ, VillarrealL, et al. (2003) Cutting edge: long-term B cell memory in humans after smallpox vaccination. J Immunol 171: 4969–4973.

38. BensonMJ, DillonSR, CastigliE, GehaRS, XuS, et al. (2008) Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J Immunol 180: 3655–3659.

39. Mamani-MatsudaM, CosmaA, WellerS, FailiA, StaibC, et al. (2008) The human spleen is a major reservoir for long-lived vaccinia virus-specific memory B cells. Blood 111: 4653–4659.

40. BensonMJ, ElguetaR, SchperoW, MolloyM, ZhangW, et al. (2009) Distinction of the memory B cell response to cognate antigen versus bystander inflammatory signals. J Exp Med 206: 2013–2025.

41. Dal PortoJM, HabermanAM, KelsoeG, ShlomchikMJ (2002) Very low affinity B cells form germinal centers, become memory B cells, and participate in secondary immune responses when higher affinity competition is reduced. J Exp Med 195: 1215–1221.

42. TarlintonDM, SmithKGC (2000) Dissecting affinity maturation: a model explaining selection of antibody-forming cells and memory B cells in the germinal centre. Immunol Today 21: 436–441.

43. Jelley-GibbsDM, BrownDM, DibbleJP, HaynesL, EatonSM, et al. (2005) Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J Exp Med 202: 697–706.

44. HebeisBJ, KlenovsekK, RohwerP, RitterU, SchneiderA, et al. (2004) Activation of virus-specific memory B cells in the absence of T cell help. J Exp Med 199: 593–602.

45. KlenovsekK, WeiselF, SchneiderA, AppeltU, JonjicS, et al. (2007) Protection from CMV infection in immunodeficient hosts by adoptive transfer of memory B cells. Blood 110: 3472–3479.

46. OnoderaT, TakahashiY, YokoiY, AtoM, KodamaY, et al. (2012) Memory B cells in the lung participate in protective humoral immune responses to pulmonary influenza virus reinfection. Proc Natl Acad Sci U S A 109: 2485–2490.

47. GreenwoodBM, WhittleHC, BradleyAK, FayetMT, GillesHM (1980) The duration of the antibody response to meningococcal vaccination in an African village. Trans R Soc Trop Med Hyg 74: 756–760.

48. AbdurrahmanMB, GreenwoodBM, OlafimihanO, WhitleHC (1982) Measles antibody levels from birth to 9 months of age in Nigerian infants. Afr J Med Med Sci 11: 113–115.

49. HanlonP, HanlonL, MarshV, ByassP, SillahH, et al. (1987) Serological comparisons of approaches to polio vaccination in the Gambia. Lancet 1: 800–801.

50. SchellenbergA (2000) Humoral immune responses during a malaria vaccine trial in Tanzanian infants. Parasite Immunol 22: 437–443.

51. WilliamsonWA, GreenwoodBM (1978) Impairment of the immune response to vaccination after acute malaria. Lancet 311: 1328–1329.

52. TempleK, GreenwoodB, InskipH, HallA, KoskelaM, et al. (1991) Antibody response to pneumococcal capsular polysaccharide vaccine in African children. Pediatr Infect Dis J 10: 386–390.

53. MacLennanJ, ObaroS, DeeksJ, LakeD, ElieC, et al. (2001) Immunologic memory 5 years after meningococcal A/C conjugate vaccination in infancy. J Infect Dis 183: 97–104.

54. CampbellH, ByassP, AhonkhaiVI, VellaPP, GreenwoodBM (1990) Serologic responses to an Haemophilus influenzae type b polysaccharide-Neisseria meningitidis outer membrane protein conjugate vaccine in very young Gambian infants. Pediatrics 86: 102–107.

55. CuttsFT, ZamanSMA, EnwereG, JaffarS, LevineOS, et al. (2005) Efficacy of nine-valent pneumococcal conjugate vaccine against pneumonia and invasive pneumococcal disease in The Gambia: randomised, double-blind, placebo-controlled trial. Lancet 365: 1139–1146.

56. HollandWG, DoTT, HuongNT, DungNT, ThanhNG, et al. (2003) The effect of Trypanosoma evansi infection on pig performance and vaccination against classical swine fever. Vet Parasitol 111: 115–123.

57. RurangirwaFR, MusokeAJ, NantulyaVM, TabelH (1983) Immune depression in bovine trypanosomiasis: effects of acute and chronic Trypanosoma congolense and chronic Trypanosoma vivax infections on antibody response to Brucella abortus vaccine. Parasite Immunol 5: 267–276.

58. SharpeRT, LangleyAM, MowatGN, MacaskillJA, HolmesPH (1982) Immunosuppression in bovine trypanosomiasis: response of cattle infected with Trypanosoma congolense to foot-and-mouth disease vaccination and subsequent live virus challenge. Res Vet Sci 32: 289–293.

59. WhitelawDD, ScottJM, ReidHW, HolmesPH, JenningsFW, et al. (1979) Immunosuppression in bovine trypanosomiasis: studies with louping-ill vaccine. Res Vet Sci 26: 102–107.

60. MwangiDM, MunyuaWK, NyagaPN (1990) Immunosuppression in caprine trypanosomiasis: effects of acute Trypanosoma congolense infection on antibody response to anthrax spore vaccine. Trop Anim Health Prod 22: 95–100.

61. ShinkaiY, RathbunG, LamKP, OltzEM, StewartV, et al. (1992) RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V (D) J rearrangement. Cell 68: 855–867.

62. BorossP, ArandharaVL, Martin-RamirezJ, Santiago-RaberML, CarlucciF, et al. (2011) The inhibiting Fc receptor for IgG, FcγRIIB, is a modifier of autoimmune susceptibility. J Immunol 187: 1304–1313.

63. Ioan-FacsinayA, De KimpeSJ, HellwigSMM, Van LentPL, HofhuisFMA, et al. (2002) FcγRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 16: 391–402.

64. SladeSJ, LanghorneJ (1989) Production of Interferon-Gamma during Infection of Mice with Plasmodium chabaudi chabaudi. Immunobiology 179: 353–365.

65. LanghorneJ, GillardS, SimonB, SladeS, EichmannK (1989) Frequencies of CD4+ T cells reactive with Plasmodium chabaudi chabaudi: distinct response kinetics for cells with Th1 and Th2 characteristics during infection. Int Immunol 1: 416–424.

66. HaY, StevensDJ, SkehelJJ, WileyDC (2002) H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes. EMBO J 21: 865–875.

67. BlackmanMJ, Scott-FinniganTJ, ShaiS, HolderAA (1994) Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. J Exp Med 180: 389–393.

68. KaviratneM, KhanSM, JarraW, PreiserPR (2002) Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells. Eukaryot Cell 1: 926–935.

69. AntunesI, KassiotisG (2010) Suppression of innate immune pathology by regulatory T cells during influenza A virus infection of immunodeficient mice. J Virol 84: 12564–12575.

70. WardCL, DempseyMH, RingCJA, KempsonRE, ZhangL, et al. (2004) Design and performance testing of quantitative real time PCR assays for influenza A and B viral load measurement. J Clin Virol 29: 179–188.

71. QuinSJ, LanghorneJ (2001) Different regions of the malaria merozoite surface protein 1 of Plasmodium chabaudi elicit distinct T-cell and antibody isotype responses. Infect Immun 69: 2245–2251.

72. CrottyS, AubertRD, GlidewellJ, AhmedR (2004) Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J Immunol Methods 286: 111–122.

73. NdunguFM, CadmanET, CoulcherJ, NduatiE, CouperE, et al. (2009) Functional Memory B Cells and Long-Lived Plasma Cells Are Generated after a Single Plasmodium chabaudi Infection in Mice. PLoS Pathog 5: e1000690.