B cells do not take up bacterial DNA: An essential role for antigen in exposure of DNA to toll-like receptor-9

Immunology and Cell Biology

Volumn 89, Issue 4, 2011, Pages 517-525

  Roberts, Tara L ^a,b   Turner, Marian L ^c   Dunn, Jasmyn A ^a   Lenert, Petar ^d   Ross, Ian L ^a   Sweet, Matthew J ^a   Stacey, Katryn J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

B cell activation; B cell receptor; DNA uptake; macrophages; TLR9

Indexed keywords

ANTIGEN; B LYMPHOCYTE RECEPTOR; BACTERIAL DNA; CD86 ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; DEOXYRIBONUCLEASE I; LYSOZYME; PHOSPHODIESTERASE; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CELL PROLIFERATION; ESCHERICHIA COLI; IMMUNE RESPONSE; MACROPHAGE; MOUSE; NONHUMAN; POLYCLONAL ACTIVATION; PROTEIN FUNCTION; PURIFICATION;

ANIMALS; ANTIGENS; B-LYMPHOCYTES; CELL LINE; DNA, BACTERIAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGODEOXYRIBONUCLEOTIDES; SPLEEN; TOLL-LIKE RECEPTOR 9;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MURINAE;

EID: 79955784664     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2010.112     Document Type: Article

References (51)

1. Krieg AM, Yi AK, Matson S, Waldschmidt TJ, Bishop GA, Teasdale R et al. CpG motifs in bacterial-DNA trigger direct B-cell activation. Nature 1995; 374: 546-549.
2. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H et al. A toll-like receptor recognizes bacterial DNA. Nature 2000; 408: 740-745. (Pubitemid 32015992)
3. Stacey KJ, Sweet MJ, Hume DA. Macrophages ingest and are activated by bacterial DNA. J Immunol 1996; 157: 2116-2122. (Pubitemid 126449689)
4. Sparwasser T, Koch ES, Vabulas RM, Heeg K, Lipford GB, Ellwart JW et al. Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur J Immunol 1998; 28: 2045-2054. (Pubitemid 28271721)
5. Latz E, Schoenemeyer A, Visintin A, Fitzgerald KA, Monks BG, Knetter CF et al. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat Immunol 2004; 5: 190-198. (Pubitemid 38208361)
6. Leifer CA, Brooks JC, Hoelzer K, Lopez J, Kennedy MN, Mazzoni A et al. Cytoplasmic targeting motifs control localization of toll-like receptor 9. J Biol Chem 2006; 281: 35585-35592. (Pubitemid 46036592)
7. Brinkmann MM, Spooner E, Hoebe K, Beutler B, Ploegh HL, Kim YM. The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling. J Cell Biol 2007; 177: 265-275. (Pubitemid 46658638)
8. Ivanov S, Dragoi AM, Wang X, Dallacosta C, Louten J, Musco G et al. A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 2007; 110: 1970-1981. (Pubitemid 47443911)
9. Chaturvedi A, Dorward D, Pierce SK. The B cell receptor governs the subcellular location of toll-like receptor 9 leading to hyperresponses to DNA-containing antigens. Immunity 2008; 28: 799-809.
10. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002; 416: 603-607. (Pubitemid 34406754)
11. Uccellini MB, Busconi L, Green NM, Busto P, Christensen SR, Shlomchik MJ et al. Autoreactive B cells discriminate CpG-rich and CpG-poor DNA and this response is modulated by IFN-alpha. J Immunol 2008; 181: 5875-5884.
12. Viglianti GA, Lau CM, Hanley TM, Miko BA, Shlomchik MJ, Marshak-Rothstein A. Activation of autoreactive B cells by CpG dsDNA. Immunity 2003; 19: 837-847. (Pubitemid 37542304)
13. Stacey KJ, Blackwell JM. Immunostimulatory DNA as an adjuvant in vaccination against Leishmania major. Infect Immun 1999; 67: 3719-3726. (Pubitemid 29356983)
14. Sester DP, Naik S, Beasley SJ, Hume DA, Stacey KJ. Phosphorothioate backbone modification modulates macrophage activation by CpG DNA. J Immunol 2000; 165: 4165-4173.
15. Roberts TL, Sweet MJ, Hume DA, Stacey KJ. Cutting edge: species-specific TLR9- mediated recognition of CpG and non-CpG phosphorothioate-modified oligonucleotides. J Immunol 2005; 174: 605-608. (Pubitemid 40094250)
16. Monteith DK, Henry SP, Howard RB, Flournoy S, Levin AA, Bennett CF et al. Immune stimulation-a class effect of phosphorothioate oligodeoxynucleotides in rodents. Anticancer Drug Des 1997; 12: 421-432. (Pubitemid 27292377)
17. Liang H, Nishioka Y, Reich CF, Pisetsky DS, Lipsky PE. Activation of human B cells by phosphorothioate oligodeoxynucleotides. J Clin Invest 1996; 98: 1119-1129. (Pubitemid 26299924)
18. Roberts TL, Dunn JA, Terry TD, Jennings MP, Hume DA, Sweet MJ et al. Differences in macrophage activation by bacterial DNA and CpG-containing oligonucleotides. J Immunol 2005; 175: 3569-3576. (Pubitemid 41292015)
19. Stacey KJ, Young GR, Clark F, Sester DP, Roberts TL, Naik S et al. The molecular basis for the lack of immunostimulatory activity of vertebrate DNA. J Immunol 2003; 170: 3614-3620. (Pubitemid 36359230)
20. Lanzavecchia A, Sallusto F. Toll-like receptors and innate immunity in B-cell activation and antibody responses. Curr Opin Immunol 2007; 19: 268-274. (Pubitemid 46687008)
21. Bourke E, Bosisio D, Golay J, Polentarutti N, Mantovani A. The toll-like receptor repertoire of human B lymphocytes: inducible and selective expression of TLR9 and TLR10 in normal and transformed cells. Blood 2003; 102: 956-963. (Pubitemid 36917790)
22. Bernasconi NL, Onai N, Lanzavecchia A. 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 2003; 101: 4500-4504. (Pubitemid 36857820)
23. Busconi L, Bauer JW, Tumang JR, Laws A, Perkins-Mesires K, Tabor AS et al. Functional outcome of B cell activation by chromatin immune complex engagement of the B cell receptor and TLR9. J Immunol 2007; 179: 7397-7405.
24. Hartmann G, Krieg AM. Mechanism and function of a newly identified CpG DNA motif in human primary B cells. J Immunol 2000; 164: 944-952. (Pubitemid 30043721)
25. Goeckeritz BE, Flora M, Witherspoon K, Vos Q, Lees A, Dennis GJ et al. Multivalent cross-linking of membrane Ig sensitizes murine B cells to a broader spectrum of CpGcontaining oligodeoxynucleotide motifs, including their methylated counterparts, for stimulation of proliferation and Ig secretion. Int Immunol 1999; 11: 1693-1700. (Pubitemid 29481736)
26. Brummel R, Lenert P. Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J Immunol 2005; 174: 2429-2434. (Pubitemid 40223993)
27. Spies B, Hochrein H, Vabulas M, Huster K, Busch DH, Schmitz F et al. Vaccination with plasmid DNA activates dendritic cells via toll-like receptor 9 (TLR9) but functions in TLR9-deficient mice. J Immunol 2003; 171: 5908-5912. (Pubitemid 37467208)
28. Wagner M, Poeck H, Jahrsdoerfer B, Rothenfusser S, Prell D, Bohle B et al. IL-12p70- dependent Th1 induction by human B cells requires combined activation with CD40 ligand and CpG DNA. J Immunol 2004; 172: 954-963. (Pubitemid 38113754)
29. Macfarlane DE, Manzel L, Krieg AM. Unmethylated CpG-containing oligodeoxynucleotides inhibit apoptosis in WEHI-231 B lymphocytes induced by several agents: evidence for blockade of apoptosis at a distal signalling step. Immunology 1997; 91: 586-593. (Pubitemid 27312342)
30. Yi AK, Krieg AM. CpG DNA rescue from anti-IgM-induced WEHI-231 B lymphoma apoptosis via modulation of I kappa B alpha and I kappa B beta and sustained activation of nuclear factor-kappa B/c-Rel. J Immunol 1998; 160: 1240-1245. (Pubitemid 28093421)
31. Gantner F, Hermann P, Nakashima K, Matsukawa S, Sakai K, Bacon KB. CD40- dependent and -independent activation of human tonsil B cells by CpG oligodeoxynucleotides. Eur J Immunol 2003; 33: 1576-1585. (Pubitemid 36790418)
32. Eckl-Dorna J, Batista FD. BCR-mediated uptake of antigen linked to TLR9 ligand stimulates B-cell proliferation and antigen-specific plasma cell formation. Blood 2009; 113: 3969-3977.
33. Messina JP, Gilkeson GS, Pisetsky DS. Stimulation of in vitro murine lymphocyte proliferation by bacterial DNA. J Immunol 1991; 147: 1759-1764.
34. Messina JP, Gilkeson GS, Pisetsky DS. The influence of DNA structure on the in vitro stimulation of murine lymphocytes by natural and synthetic polynucleotide antigens. Cell Immunol 1993; 147: 148-157. (Pubitemid 23100973)
35. Yi AK, Chace JH, Cowdery JS, Krieg AM. IFN-gamma promotes IL-6 and IgM secretion in response to CpG motifs in bacterial DNA and oligodeoxynucleotides. J Immunol 1996; 156: 558-564.
36. Brummel R, Roberts TL, Stacey KJ, Lenert P. Higher-order CpG-DNA stimulation reveals distinct activation requirements for marginal zone and follicular B cells in lupus mice. Eur J Immunol 2006; 36: 1951-1962. (Pubitemid 44089060)
37. Hurtado P, Peh CA. LL-37 promotes rapid sensing of CpG oligodeoxynucleotides by B lymphocytes and plasmacytoid dendritic cells. J Immunol 2010; 184: 1425-1435.
38. Lin KC, Wey MT, Kan LS, Shiuan D. Characterization of the interactions of lysozyme with DNA by surface plasmon resonance and circular dichroism spectroscopy. Appl Biochem Biotechnol 2009; 158: 631-641.
39. McGovern EM, Moquin AE, Caballero A, Drake JR. The effect of B cell receptor signaling on antigen endocytosis and processing. Immunol Invest 2004; 33: 143-156. (Pubitemid 38685928)
40. Avalos AM, Latz E, Mousseau B, Christensen SR, Shlomchik MJ, Lund F et al. Differential cytokine production and bystander activation of autoreactive B cells in response to CpG-A and CpG-B oligonucleotides. J Immunol 2009; 183: 6262-6268.
41. Turner ML, Hawkins ED, Hodgkin PD. Quantitative regulation of B cell division destiny by signal strength. J Immunol 2008; 181: 374-382.
42. Ruprecht CR, Lanzavecchia A. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur J Immunol 2006; 36: 810-816.
43. Herlands RA, Christensen SR, Sweet RA, Hershberg U, Shlomchik MJ. T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity 2008; 29: 249-260.
44. Carrasco YR, Batista FD. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 2007; 27: 160-171. (Pubitemid 47089026)
45. Junt T, Moseman EA, Iannacone M, Massberg S, Lang PA, Boes M et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007; 450: 110-114. (Pubitemid 350070574)
46. Costelloe EO, Stacey KJ, Antalis TM, Hume DA. Regulation of the plasminogen activator inhibitor-2 (PAI-2) gene in murine macrophages. Demonstration of a novel pattern of responsiveness to bacterial endotoxin. J Leukocyte Biolo 1999; 66: 172-182. (Pubitemid 29321386)
47. Phan TG, Amesbury M, Gardam S, Crosbie J, Hasbold J, Hodgkin PD et al. B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J Exp Med 2003; 197: 845-860. (Pubitemid 36437862)
48. Wells SM, Kantor AB, Stall AM. CD43 (S7) expression identifies peripheral B cell subsets. J Immunol 1994; 153: 5503-5515. (Pubitemid 24377686)
49. Driver DJ, McHeyzer-Williams LJ, Cool M, Stetson DB, McHeyzer-Williams MG. Development and maintenance of a B220- memory B cell compartment. J Immunol 2001; 167: 1393-1405. (Pubitemid 32703137)
50. Yi AK, Hornbeck P, Lafrenz DE, Krieg AM. CpG DNA rescue of murine B lymphoma cells from anti-IgM-induced growth arrest and programmed cell death is associated with increased expression of c-myc and bcl-xL. J Immunol 1996; 157: 4918-4925. (Pubitemid 126449568)
51. Sweet MJ, Leung BP, Kang D, Sogaard M, Schulz K, Trajkovic V et al. A novel pathway regulating lipopolysaccharide-induced shock by ST2/T1 via inhibition of Toll-like receptor 4 expression. J Immunol 2001; 166: 6633-6639. (Pubitemid 32467204)