Lymphoadenopathy during lyme borreliosis is caused by spirochete migration-induced specific B cell activation

PLoS Pathogens

Volumn 7, Issue 5, 2011, Pages

  Tunev, Stefan S ^a,b   Hastey, Christine J ^a   Hodzic, Emir ^a   Feng, Sunlian ^a   Barthold, Stephen W ^a   Baumgarth, Nicole ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MEDTRONIC INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN M; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; BACTERIAL ANTIGEN; BACTERIUM ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE ACTIVATION; BORRELIA BURGDORFERI; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; HYBRIDOMA; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LYME DISEASE; LYMPH NODE; LYMPHADENOPATHY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PLASMA CELL; SIGNAL TRANSDUCTION; TICK BORNE DISEASE; ANIMAL; B LYMPHOCYTE; C3H MOUSE; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; ISOLATION AND PURIFICATION; LYMPHATIC SYSTEM DISEASE; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SPIROCHETE; TICK;

BORRELIA; BORRELIA BURGDORFERI; IXODIDA; MUS; SPIROCHAETALES;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; B-LYMPHOCYTES; BORRELIA BURGDORFERI; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; LYME DISEASE; LYMPH NODES; LYMPHATIC DISEASES; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, SCID; MYELOID DIFFERENTIATION FACTOR 88; SPIROCHAETALES; TICKS;

EID: 79958069669     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002066     Document Type: Article

References (62)

1. Bacon RM, Kugeler KJ, Mead PS, (2008) Surveillance for Lyme disease- United States, 1992-2006. MMWR Surveill Summ 57: 1-9.
2. Randolph SE, (2001) The shifting landscap of tick-borne zoonoses: tick-borne encephalitiis and Lyme borreliosis in Europe. Phil Trans R Soc Lond 356: 1045-1056.
3. Steere AC, Schoen RT, Taylor E, (1987) The clinical evolution of Lyme arthritis. Ann Intern Med 107: 725-731.
4. Steere AC, (1989) Lyme disease. N Engl J Med 321: 586-596.
5. Steere AC, (2001) Lyme disease. N Eng J Med 345: 115-125.
6. Summers BA, Straubinger AF, Jacobson RH, Chang YF, Appel MJG, et al. (2005) Histopathological studies of experimental Lyme disease in dogs. J Comp Path 133: 1-13.
7. Duray PH, Steere AC, (1988) Clinical pathologic correlations of Lyme disease by stage. Ann N Y Acad Sci 539: 65-79.
8. Steere AC, Bartenhagen NH, Craft JE, Hutchinson GJ, Newman JH, et al. (1983) The early clinical manifestations of Lyme disease. Ann Intern Med 99: 76-82.
9. deSouza MS, Fikrig E, Smith AL, Flavell RA, Barthold SW, (1992) Nonspecific proliferative responses of murine lymphocytes to Borrelia burgdorferi antigens. J Infect Dis 165: 471-478.
10. Honarvar N, Schaible UE, Galanos C, Wallich R, Simon MM, (1994) A 14,000 MW lipoprotein and a glycolipid-like structure of Borrelia burgdorferi induce proliferation and immunoglobulin production in mouse B cells at high frequencey. Immunol 82: 389-396.
11. Ma Y, Weis JJ, (1993) Borrelia burgdorferi outer surface lipoproteins OspA and OspB possess B-cell mitogenic and cytokine-stimulatory properties. Infect Immun 61: 3843-3853.
12. Schoenfeld R, Araneo B, Ma Y, Yang L, Weis JJ, (1992) Demonstration of a B-lymphocyte mitogen produced by the Lyme disease pathogen, Borrelia burgdorferi. Infect Immun 60: 455-464.
13. Sigal LH, Steere AC, Dwyer JM, (1988) In vivo and in vitro evidence of B cell hyperactivity during Lyme disease. J Rheumatol 15: 648-654.
14. Tai KF, Ma Y, Weis JJ, (1994) Normal human B lymphocytes and mononuclear cells respond to the mitogenic and cytokine-stimulatory activities of Borrelia burgdorferi and its lipoprotein OspA. Infect Immun 62: 520-528.
15. Whitmire WM, Garon CF, (1993) Specific and nonspecific responses of murine B-cells to membrane blebs of Borrelia burgdorferi. Infect Immun 61: 1460-1467.
16. Yang LM, Ma Y, Schoenfeld R, Griffiths M, Eichwald E, et al. (1992) Evidence for lymphocyte-B mitogen activity in Borrelia burgdorferi-infected mice. Infect Immun 60: 3033-3041.
17. St John AL, Abraham SN, (2009) Salmonella disrupts lymph node architecture by TLR4-mediated suppression of homeostatic chemokines. Nat Med 15: 1259-1265.
18. Jawdat DM, Rowden G, Marshall JS, (2006) Mast cells have a pivotal role in TNF-independent lymph node hypertrophy and the mobilization of Langerhans cells in response to bacterial peptidoglycan. J Immunol 177: 1755-1762.
19. McLachlan JB, Hart JP, Pizzo SV, Shelburne CP, Staats HF, et al. (2003) Mast cell-derived tumor necrosis factor induces hypertrophy of draining lymph nodes during infection. Nat Immunol 4: 1199-1205.
20. Aguero-Rosenfeld ME, Nowakowski J, McKenna DF, Carbonaro CA, Wormser GP, (1993) Serodiagnosis in early Lyme disease. J Clin Microbiol 31: 3090-3095.
21. AgueroRosenfeld ME, Nowakowski J, Bittker S, Cooper D, Nadelman RB, et al. (1996) Evolution of the serologic response to Borrelia burgdorferi in treated patients with culture-confirmed erythema migrans. J Clin Microbiol 34: 1-9.
22. Dressler F, Whalen JA, Reinhardt BN, Steere AC, (1993) Western blotting in the serodiagnosis of early Lyme disease. J Infect Dis 167: 392-400.
23. Kalish RA, McHugh G, Granquist J, Shea B, Ruthazer R, et al. (2001) Persistence of immunoglobulin M or immunoglobulin G antibody responses to Borrelia burgdorferi 10-20 years after active disease. Clin Infect Dis 33: 780-785.
24. Steere AC, Coburn J, Glickstein L, (2004) The emergence of Lyme disease. J Clin Invest 113: 1093-1101.
25. Barthold SW, Levy SA, Fikrig E, Bockenstedt LK, Smith AL, (1995) Serologic response of naturally exposed or vaccinated dogs to Borrelia burgdorferi, the agent of Lyme borreliosis. J Am Vet Med Assoc 207: 1435-1440.
26. Barthold SW, Feng S, Bockenstedt LK, Fikrig E, Feen K, (1997) Protective and arthritis-resolving activity in serum from mice infected with Borrelia burgdorferi. Clin Infect Dis 25: S9-S17.
27. Barthold SW, Fikrig E, Bockenstedt LK, Persing DH, (1995) Circumvention of outer surface protein A immunity by host-adapted Borrelia burgdorferi. Infect Immun 63: 2255-2261.
28. Fikrig E, Bockenstedt LK, Barthold SW, Chen M, Tao H, et al. (1994) Sera from patients with chronic Lyme disease protect mice from Lyme borreliosis. J Infect Dis 169: 568-574.
29. McKisic MD, Barthold SW, (2000) T-cell-independent responses to Borrelia burgdorferi are critical for protective immunity and resolution of Lyme disease. Infect Immun 68: 5190-5197.
30. Barthold SW, Bockenstedt LK, (1993) Passive immunizing activity of sera from mice infected with Borrelia burgdorferi. Infect Immun 61: 4696-4702.
31. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
32. Hodzic E, Tunev S, Feng S, Freet K, Barthold S, (2005) Immunoglobulin-regulated expression of Borrelia burgdorferi outer surface protein A in vivo. Infect Immun 73: 3313-3321.
33. Barbour AG, (1984) Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57: 521-525.
34. Hodzic E, Feng S, Freet KJ, Borjesson DL, Barthold SW, (2002) Borrelia burgdorferi population kinetics and selected gene expression at the host-vector interface. Infect Immun 70: 3382-3388.
35. Rothaeusler K, Baumgarth N, (2006) Evaluation of intranuclear BrdU detection procedures for use in multicolor flow cytometry. Cytometry A 69: 249-259.
36. Feng S, Hodzic E, Stevenson B, Barthold SW, (1998) Humoral immunity to Borrelia burgdorferi N40 decorin binding proteins during infection of laboratory mice. Infect Immun 66: 2827-2835.
37. Rau FC, Dieter J, Luo Z, Priest SO, Baumgarth N, (2009) B7-1/2 (CD80/CD86) direct signaling to B cells enhances IgG secretion. J Immunol 183: 7661-7671.
38. Barthold SW, Beck DS, Hansen GM, Terwilliger GA, Moody KD, (1990) Lyme borreliosis in selected strains and ages of laboratory mice. J Infect Dis 162: 133-138.
39. deSilva AM, Fikrig E, (1997) Arthropod- and host-specific gene expression by Borrelia burgdorferi. J Clin Invest 99: 377-379.
40. Fikrig E, Barthold SW, Chen M, Grewal IS, Craft J, et al. (1996) Protective antibodies in murine Lyme disease arise independently of CD40 ligand. J Immunol 157: 1-3.
41. Barthold SW, Hodzic E, Tunev S, Feng S, (2006) Antibody-mediated disease remission in the mouse model of Lyme borreliosis. Infect Immun 74: 4817-4825.
42. Liu N, Montgomery RR, Barthold SW, Bockenstedt LK, (2004) Myeloid differentiation antigen 88 deficiency impairs pathogen clearance but does not alter inflammation in Borrelia burgdorferi-infected mice. Infect Immun 72: 3195-3203.
43. MacLennan IC, Toellner KM, Cunningham AF, Serre K, Sze DM, et al. (2003) Extrafollicular antibody responses. Immunol Rev 194: 8-18.
44. Goodnow CC, Vinuesa CG, Randall KL, Mackay F, Brink R, (2010) Control systems and decision making for antibody production. Nat Immunol 11: 681-688.
45. Bockenstedt LK, Kang I, Shanafelt M-C, Kumar H, Campbell M, et al. (1997) Lyme borreliosis in B cell- and ab T cell-deficient mice: distinct roles for specific immunity in disease regression. Clin Infect Dis 25.
46. Crother TR, Champion CI, Wu XY, Blanco DR, Miller JN, et al. (2003) Antigenic composition of Borrelia burgdorferi during infection of SCID mice. Infect Immun 71: 3419-3428.
47. Feng S, Hodzic E, Freet K, Barthold SW, (2003) Immunogenicity of Borrelia burgdorferi arthritis-related protein. Infect Immun 71: 7211-7214.
48. Liang FT, Yan J, Mbow ML, Sviat SL, Gilmore RD, et al. (2004) Borrelia burgdorferi changes its surface antigenic expression in response to host immune responses. Infect Immun 72: 5759-5767.
49. Schwan TG, Piesman J, (2000) Temporal changes in outer surface proteins A and C of the Lyme disease-associated spirochete, Borrelia burgdorferi, during the chain of infection in ticks and mice. J Clin Microbiol 38: 382-388.
50. Suk K, Das S, Sun W, Jwang B, Barthold SW, et al. (1995) Borrelia burgdorferi genes selectively expressed in the infected host. Proc Natl Acad Sci USA 92: 4269-4273.
51. Cassatt DR, Patel NK, Ulbrandt ND, Hanson MS, (1998) DbpA, but not OspA, is expressed by Borrelia burgdorferi during spirochemia and is a target for protective antibodies. Infect Immun 66: 5379-5387.
52. Liang FT, Jacobs MB, Bowers LC, Philipp MT, (2002) An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J Exp Med 195: 415-422.
53. Simpson WJ, Cieplak W, Schrumpf ME, Barbour AG, Schwan TG, (1994) Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen. F E M S Microbiol Lett 119: 381-388.
54. Feng S, Hodzic E, Barthold SW, (2000) Lyme arthritis resolution with antiserum to a 37-kilodalton Borrelia burgdorferi protein. Infect Immun 68: 4169-4173.
55. Hanson MS, Cassatt DR, Guo BP, Patel NK, McCarthy MP, et al. (1998) Active and passive immunity against Borrelia burgdorferi decorin binding protein A (DbpA) protects against infection. Infect Immun 66: 2143-2153.
56. Pal U, Wang P, Bao F, Yang X, Samanta S, et al. (2008) Borrelia burgdorferi basic membrane proteins A and B participate in the genesis of Lyme arthritis. J Exp Med 205: 133-141.
57. Probert WS, LeFebvre RB, (1994) Protection of C3H/HeN mice from challenge with Borrelia burgdorferi through active immunization with OspA, OspB, or OspC, but not with OspD or the 83-kilodalton antigen. Infect Immun 62: 1920-1926.
58. Barthold SW, deSouza M, Feng S, (1996) Serum-mediated resolution of Lyme arthritis in mice. Lab Invest 74: 57-67.
59. Cabello FC, Godfrey HP, Newman SA, (2007) Hidden in plain sight: Borrelia burgdorferi and the extracellular matrix. Trends Microbiol 15: 350-354.
60. Belperron AA, Dailey CM, Booth CJ, Bockenstedt LK, (2007) Marginal zone B-cell depletion impairs murine host defense against Borrelia burgdorferi infection. Infect Immun 75: 3354-3360.
61. de Souza MS, Smith AL, Beck DS, Kim LJ, Hansen GM Jr, et al. (1993) Variant responses of mice to Borrelia burgdorferi depending on the site of intradermal inoculation. Infect Immun 61: 4493-4497.
62. Pachner AR, Delaney E, Ricalton NS, (1993) Murine Lyme borreliosis: route of inoculation determines immune response and infectivity. Regional Immunol 4: 345-351.