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

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Ng, Dorothy H L ^a   Skehel, John J ^a   Kassiotis, George ^a   Langhorne, Jean ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; FCGR2B PROTEIN, MOUSE; VIRUS ANTIBODY;

ANIMAL; BAGG ALBINO MOUSE; HUMORAL IMMUNITY; IMMUNOLOGY; INFLUENZA A VIRUS; MALARIA; MOUSE; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PLASMA CELL; PLASMODIUM CHABAUDI; TIME;

ANIMALS; ANTIBODIES, VIRAL; IMMUNITY, HUMORAL; INFLUENZA A VIRUS; MALARIA; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; PLASMA CELLS; PLASMODIUM CHABAUDI; RECEPTORS, IGG; TIME FACTORS;

EID: 84893722725     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003843     Document Type: Article

References (73)

1. Vieira P, Rajewsky K, (1988) The half-lives of serum immunoglobulins in adult mice. Eur J Immunol 18: 313-316.
2. Yu X, Tsibane T, McGraw PA, House FS, Keefer CJ, et al. (2008) Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455: 532-526.
3. Slifka MK, Antia R, Whitmire JK, Ahmed R, (1998) Humoral immunity due to long-lived plasma cells. Immunity 8: 363-372.
4. Radbruch A, Muehlinghaus G, Luger EO, Inamine A, Smith KGC, et al. (2006) Competence and competition: the challenge of becoming a long-lived plasma cell. Nat Rev Immunol 6: 741-750.
5. Nduati EW, Ng DHL, Ndungu FM, Gardner P, Urban BC, 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. Greenwood BM, (1974) Possible role of a B-cell mitogen in hypergammaglobulinaemia in malaria and trypanosomiasis. Lancet 303: 435-436.
7. Cadman ET, Abdallah AY, Voisine C, Sponaas AM, Corran P, 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. Achtman AH, Stephens R, Cadman ET, Harrison V, Langhorne J, (2007) Malaria-specific antibody responses and parasite persistence after infection of mice with Plasmodium chabaudi chabaudi. Parasite Immunol 29: 435-444.
9. Looareesuwan S, Ho M, Wattanagoon Y, White NJ, Warrell DA, et al. (1987) Dynamic alteration in splenic function during acute falciparum malaria. N Engl J Med 317: 675-679.
10. Wykes MN, Zhou YH, Liu XQ, Good MF, (2005) Plasmodium yoelii can ablate vaccine-induced long-term protection in mice. J Immunol 175: 2510-2516.
11. Strambachová-McBride J, Micklem HS, (1979) Immunosuppression in murine malaria. IV. The secondary response to bovine serum albumin. Parasite Immunol 1: 141-157.
12. Radwanska M, Guirnalda P, De Trez C, Ryffel B, Black S, 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. Xiang Z, Cutler AJ, Brownlie RJ, Fairfax K, Lawlor KE, et al. (2007) FcγRIIb controls bone marrow plasma cell persistence and apoptosis. Nat Immunol 8: 419-429.
14. Goumard P, Vu DN, Maurois P, Camus D, (1982) Influence of malaria on a pre-existing antibody response to heterologous antigens. Ann Immunol (Paris) 133: 313-326.
15. Amanna IJ, Carlson NE, Slifka MK, (2007) Duration of humoral immunity to common viral and vaccine antigens. N Engl J Med 357: 1903-1915.
16. Kassiotis G, Gray D, Kiafard Z, Zwirner J, Stockinger B, (2006) Functional specialization of memory Th cells revealed by expression of integrin CD49b. J Immunol 177: 968-975.
17. Flynn KJ, Belz GT, Altman JD, Ahmed R, Woodland DL, et al. (1998) Virus-Specific CD8+ T Cells in Primary and Secondary Influenza Pneumonia. Immunity 8: 683-691.
18. Odendahl M, Mei H, Hoyer BF, Jacobi AM, Hansen A, 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. Clatworthy MR, Willcocks L, Urban B, Langhorne J, Williams TN, 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. Traggiai E, Puzone R, Lanzavecchia A, (2003) Antigen dependent and independent mechanisms that sustain serum antibody levels. Vaccine 21: S35-S37.
21. Bernasconi NL, Onai N, Lanzavecchia A, (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. Bernasconi NL, Traggiai E, Lanzavecchia A, (2002) Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298: 2199-2202.
23. Gong Q, Ou Q, Ye S, Lee WP, Cornelius J, et al. (2005) Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J Immunol 174: 817-826.
24. Ahuja A, Shupe J, Dunn R, Kashgarian M, Kehry MR, et al. (2007) Depletion of B cells in murine lupus: efficacy and resistance. J Immunol 179: 3351-3361.
25. Ahuja A, Anderson SM, Khalil A, Shlomchik MJ, (2008) Maintenance of the plasma cell pool is independent of memory B cells. Proc Natl Acad Sci U S A 105: 4802-4807.
26. DiLillo DJ, Hamaguchi Y, Ueda Y, Yang K, Uchida J, 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. Moser K, Tokoyoda K, Radbruch A, MacLennan I, Manz RA, (2006) Stromal niches, plasma cell differentiation and survival. Curr Opin Immunol 18: 265-270.
28. Sze DMY, Toellner KM, de Vinuesa CG, Taylor DR, MacLennan I, (2000) Intrinsic constraint on plasmablast growth and extrinsic limits of plasma cell survival. J Exp Med 192: 813-821.
29. Terstappen LW, Johnsen S, Segers-Nolten IM, Loken MR, (1990) Identification and characterization of plasma cells in normal human bone marrow by high-resolution flow cytometry. Blood 76: 1739-1747.
30. Fairfax KA, Kallies A, Nutt SL, Tarlinton DM, (2008) Plasma cell development: from B-cell subsets to long-term survival niches. Semin Immunol 20: 49-58.
31. Vezys V, Yates A, Casey KA, Lanier G, Ahmed R, et al. (2008) Memory CD8 T-cell compartment grows in size with immunological experience. Nature 457: 196-199.
32. Viki B, Nathalie G, (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. Tokoyoda K, Egawa T, Sugiyama T, Choi BI, Nagasawa T, (2004) Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 20: 707-718.
34. Stephens R, Ndungu FM, Langhorne J, (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. Maruyama M, Lam KP, Rajewsky K, (2000) Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407: 636-642.
36. Tomayko MM, Anderson SM, Brayton CE, Sadanand S, Steinel NC, 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. Crotty S, Felgner P, Davies H, Glidewell J, Villarreal L, et al. (2003) Cutting edge: long-term B cell memory in humans after smallpox vaccination. J Immunol 171: 4969-4973.
38. Benson MJ, Dillon SR, Castigli E, Geha RS, Xu S, 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-Matsuda M, Cosma A, Weller S, Faili A, Staib C, et al. (2008) The human spleen is a major reservoir for long-lived vaccinia virus-specific memory B cells. Blood 111: 4653-4659.
40. Benson MJ, Elgueta R, Schpero W, Molloy M, Zhang W, 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 Porto JM, Haberman AM, Kelsoe G, Shlomchik MJ, (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. Tarlinton DM, Smith KGC, (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-Gibbs DM, Brown DM, Dibble JP, Haynes L, Eaton SM, et al. (2005) Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J Exp Med 202: 697-706.
44. Hebeis BJ, Klenovsek K, Rohwer P, Ritter U, Schneider A, et al. (2004) Activation of virus-specific memory B cells in the absence of T cell help. J Exp Med 199: 593-602.
45. Klenovsek K, Weisel F, Schneider A, Appelt U, Jonjic S, et al. (2007) Protection from CMV infection in immunodeficient hosts by adoptive transfer of memory B cells. Blood 110: 3472-3479.
46. Onodera T, Takahashi Y, Yokoi Y, Ato M, Kodama Y, 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. Greenwood BM, Whittle HC, Bradley AK, Fayet MT, Gilles HM, (1980) The duration of the antibody response to meningococcal vaccination in an African village. Trans R Soc Trop Med Hyg 74: 756-760.
48. Abdurrahman MB, Greenwood BM, Olafimihan O, Whitle HC, (1982) Measles antibody levels from birth to 9 months of age in Nigerian infants. Afr J Med Med Sci 11: 113-115.
49. Hanlon P, Hanlon L, Marsh V, Byass P, Sillah H, et al. (1987) Serological comparisons of approaches to polio vaccination in the Gambia. Lancet 1: 800-801.
50. Schellenberg A, (2000) Humoral immune responses during a malaria vaccine trial in Tanzanian infants. Parasite Immunol 22: 437-443.
51. Williamson WA, Greenwood BM, (1978) Impairment of the immune response to vaccination after acute malaria. Lancet 311: 1328-1329.
52. Temple K, Greenwood B, Inskip H, Hall A, Koskela M, et al. (1991) Antibody response to pneumococcal capsular polysaccharide vaccine in African children. Pediatr Infect Dis J 10: 386-390.
53. MacLennan J, Obaro S, Deeks J, Lake D, Elie C, et al. (2001) Immunologic memory 5 years after meningococcal A/C conjugate vaccination in infancy. J Infect Dis 183: 97-104.
54. Campbell H, Byass P, Ahonkhai VI, Vella PP, Greenwood BM, (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. Cutts FT, Zaman SMA, Enwere G, Jaffar S, Levine OS, 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. Holland WG, Do TT, Huong NT, Dung NT, Thanh NG, et al. (2003) The effect of Trypanosoma evansi infection on pig performance and vaccination against classical swine fever. Vet Parasitol 111: 115-123.
57. Rurangirwa FR, Musoke AJ, Nantulya VM, Tabel H, (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. Sharpe RT, Langley AM, Mowat GN, Macaskill JA, Holmes PH, (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. Whitelaw DD, Scott JM, Reid HW, Holmes PH, Jennings FW, et al. (1979) Immunosuppression in bovine trypanosomiasis: studies with louping-ill vaccine. Res Vet Sci 26: 102-107.
60. Mwangi DM, Munyua WK, Nyaga PN, (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. Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, et al. (1992) RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V (D) J rearrangement. Cell 68: 855-867.
62. Boross P, Arandhara VL, Martin-Ramirez J, Santiago-Raber ML, Carlucci F, et al. (2011) The inhibiting Fc receptor for IgG, FcγRIIB, is a modifier of autoimmune susceptibility. J Immunol 187: 1304-1313.
63. Ioan-Facsinay A, De Kimpe SJ, Hellwig SMM, Van Lent PL, Hofhuis FMA, et al. (2002) FcγRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 16: 391-402.
64. Slade SJ, Langhorne J, (1989) Production of Interferon-Gamma during Infection of Mice with Plasmodium chabaudi chabaudi. Immunobiology 179: 353-365.
65. Langhorne J, Gillard S, Simon B, Slade S, Eichmann K, (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. Ha Y, Stevens DJ, Skehel JJ, Wiley DC, (2002) H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes. EMBO J 21: 865-875.
67. Blackman MJ, Scott-Finnigan TJ, Shai S, Holder AA, (1994) Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. J Exp Med 180: 389-393.
68. Kaviratne M, Khan SM, Jarra W, Preiser PR, (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. Antunes I, Kassiotis G, (2010) Suppression of innate immune pathology by regulatory T cells during influenza A virus infection of immunodeficient mice. J Virol 84: 12564-12575.
70. Ward CL, Dempsey MH, Ring CJA, Kempson RE, Zhang L, 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. Quin SJ, Langhorne J, (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. Crotty S, Aubert RD, Glidewell J, Ahmed R, (2004) Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J Immunol Methods 286: 111-122.
73. Ndungu FM, Cadman ET, Coulcher J, Nduati E, Couper E, 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.