CpG DNA rescues B cells from apoptosis by activating NFκB and preventing mitochondrial membrane potential disruption via a chloroquine-sensitive pathway

International Immunology

Volumn 11, Issue 12, 1999, Pages 2015-2024

  Yi, Ae Kyung ^a   Peckham, Dave W ^b   Ashman, Robert F ^a,b   Krieg, Arthur M ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c PFIZER INC   (United States)

Author keywords

Apoptosis; B lymphocytes; Cellular activation; Gene regulation; Lupus

Indexed keywords

CD40 ANTIGEN; CHLOROQUINE; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN M ANTIBODY; LIPOPOLYSACCHARIDE; OLIGODEOXYNUCLEOTIDE; ONCOPROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CPG ISLAND; GENE EXPRESSION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTO ONCOGENE; SPLEEN;

EID: 0033406341     PISSN: 09538178     EISSN: None     Source Type: Journal    
DOI: 10.1093/intimm/11.12.2015     Document Type: Article

References (52)

1. Nossal, G. J., Pike, B. L. and Battye, F. L. 1979. Mechanisms of clonal abortion tolerogenesis. II. Clonal behavior of immature B cells following exposure to anti-mu chain antibody. Immunology 37:203.
2. Liu, Y. J., Joshua, D. E., Williams, G. T., Smith, C. A., Gordon, J. and MacLennan, I. C. 1989. Mechanism of antigen-driven selection in germinal centers. Nature 342:929.
3. Liu, Y. J., Mason, Y., Johnson, G. D., Abbot, S., Gregory, C. D., Hardie, D. L., Gordon, J. and MacLennan, I. C. M. 1991. Germinal center cells express bcl-2 protein after activation by signals which prevent their entry into apoptosis. Eur. J. Immunol. 21:1905.
4. Jakway, J. P., Unsinger, W. R., Gold, M. R., Mishell, R. I. and DeFranco, A. L. 1986. Growth regulation of the B lymphoma cell line WEHI-231 by anti-immunoglobulin, lipopolysaccharide, and other bacterial products. J. Immunol. 137:2225.
5. Tsubata, T., Wu, J. and Honjo, T. 1993. B-cell apoptosis induced by antigen receptor crosslinking is blocked by a T-cell signal through CD40. Nature 364:645.
6. Illera, V. A., Perandones, C. E., Stunz, L. L., Mower, D. A., Jr and Ashman, R. F. 1993. Apoptosis in splenic B lymphocytes. Regulation by protein kinase C and IL-4. J. Immunol. 151:2965.
7. Mower, D. A., Jr, Peckham, D. W., Illera, V. A., Fishbaugh, J. K., Stunz, L. L. and Ashman, R. F. 1994. Decreased membrane phospholipid packing and decreased cell size precede DNA cleavage in mature mouse B cell apoptosis. J. Immunol. 152:4832.
8. Ashman, R. F., Peckham, D. W. and Stunz L. L. 1996. Fc receptor off-signal in the B cell involves apoptosis. J. Immunol. 157:5.
9. Yi, A.-K., Chang, M., Peckham, D. W., Krieg, A. M. and Ashman, R. F. 1998. CpG oligodeoxyribonucleotides rescue mature spleen B cells from spontaneous apoptosis and promote cell cycle entry. J. Immunol. 160:5898.
10. Messina, J. P., Gilkeson, G. S. and Pisetsky, D. S. 1991. Stimulation of in vitro murine lymphocyte proliferation by bacterial DNA. J. Immunol. 147:1759.
11. Krieg, A. M., Yi, A.-K., Matson, S., Waldschmidt, T. J., Bishop, G. A., Teasdale, R., Koretzky, G. A. and Klinman, D. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374:546.
12. Yi, A.-K., Klinman, D. M., Martin, T. L., Matson, S. and Krieg A. M. 1996. Rapid immune activation by CpG motifs in bacterial DNA: systemic induction of IL-6 transcription through an antioxidant-sensitive pathway. J. Immunol. 157:5394.
13. Klinman, D. M., Yi, A.-K., Beaucage, S. L., Conover, J. and Krieg, A. M. 1996. CpG motifs present in bacterial DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon γ. Proc. Natl Acad. Sci. USA. 93:2879.
14. Yi, A.-K., Chace, J. H., Cowdery, J. S. and Krieg, A. M. 1996. IFN-γ promotes IL-6 and IgM secretion in response to CpG motifs in bacterial DNA and oligodeoxynucleotides. J. Immunol. 156:558.
15. Cowdery, J. S., Chace, J. H., Yi, A.-K. and Krieg, A. M. 1996. Bacterial DNA induces NK cells to produce IFN-γ in vivo and increases the toxicity of lipopolysaccharides. J. Immunol. 156:4570.
16. Ballas, Z. K., Rasmussen, W. L. and Krieg, A. M. 1996. Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleotides and bacterial DNA. J. Immunol. 157:1840.
17. Anitescu, M., Chace, J. H., Tuetken, R., Yi, A.-K., Berg, D. J., Krieg, A. M. and Cowdery, J. S. 1997. Interleukin-10 functions in vitro and in vivo to inhibit bacterial DNA-induced secretion of interleukin-12. J. Interferon Cytokine Res. 17:781.
18. Wooldridge, J. E., Ballas, Z., Krieg, A. M. and Weiner, G. J. 1997. Immunostimulatory oligodeoxynucleotides containing CpG motifs enhance the efficacy of monoclonal antibody therapy of lymphoma. Blood 89:2994.
19. Kline, J. N., Waldschmidt, T. J., Businga, T. R., Lemish, J. E., Weinstock, J. V., Thorne, P. S. and Krieg, A. M. 1998. Modulation of airway inflammation by CpG oligodeoxynucleotides in a murine model of asthma. J. Immunol. 160:255.
20. Weiner, G. J., Liu H.-M., Wooldridge, J. E., Dahle, C. E. and Krieg, A. M. 1997. Immunostimulatory oligodeoxynucleotides containing the CpG motifs are effective as immune adjuvants in tumor antigen immunization. Proc. Natl Acad. Sci. USA 94:10833.
21. Chu, R. S., Targoni, O. S., Krieg, A. M., Lehmann, P. V. and Harding, C. V. 1997. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J. Exp. Med. 186:1623.
22. Davis, H. L., Weeratna, R., Waldschmidt, T. J., Tygrett, L., Schorr, J. and Krieg, A. M. 1998. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J. Immunol. 160:870.
23. Lipford, G. B., Bauer, M., Blank, C., Reiter, R., Wagner, H. and Heeg, K. 1997. CpG-containing synthetic oligonucleotides promote B and cytotoxic T cell responses to protein antigen: a new class of vaccine adjuvants. Eur. J. Immunol. 27:2340.
24. Roman, M., Martin-Orozco, E., Goodman, J. S., Nguyen, M. D., Sato, Y., Ronaghy, A., Kornbluth, R. S., Richman, D. D., Carson, D. A. and Raz, E. 1997. Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nat. Med. 3:849.
25. Sparwasser, T., Miethke, T., Lipford, G., Borschert, K., Hacker, H., Heeg, K. and Wagner, H. 1997. Bacterial DNA causes septic shock. Nature 386:336.
26. L. J. Immunol. 157:4918.
27. Yi, A.-K. and Krieg, A. M. 1998. CpG DNA rescue from anti-IgM induced WEHI-231 B lymphoma apoptosis via modulation of IκBα and IκBβ and sustained activation of nuclear factor-κB/c-Rel. J. Immunol. 160:1240.
28. Yi, A.-K., Tuetken, R., Redford, T., Waldschmidt, M., Kirsch, J. and Krieg, A. M.. 1998. CpG motifs in bacterial DNA activate leukocytes through the pH-dependent generation of reactive oxygen species. J. Immunol. 160:4755.
29. Macfarlane, D. E. and Manzel, L. 1998. Antagonism of immunostimulatory CpG- oligodeoxynucleotides by quinacrine, chloroquine, and structurally related compounds. J. Immunol. 160:1122.
30. Darzynkiewicz, Z. 1979. Acridine orange as a molecular probe in studies of nucleic acids in site. In Melamed, M.K., Mullaney, P. P. and Mendelson, M. L., eds, Flow Cytometry and Sorting., p. 285. Wiley, New York.
31. + T cells from young and old mice. J. Immunol. 150:3602.
32. Rajchel, A., Chan, Y. L. and Wool, I. G. 1987. The primary structure of rat ribosomal protein L32. Nucleic Acids Res. 16:2347.
33. Briskin, M., Damore, M., Law, R., Lee, G., Kincade, P. W., Sibley, C. H., Kuehl, M. and Wall, R. 1990. Lipopolysaccharide-unresponsive mutant pre-B-cell lines blocked in NF-kappa B activation. Mol. Cell. Biol. 10:422.
34. Zamzami, N., Marchetti, P., Castedo, M., Zanin, C., Vayssiere, J.-L., Petit, P. X. and Kroemer, G. 1995. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1661.
35. Schauer, S. L., Wang, Z., Sonenshein, G. E. and Rothstein, T. L. 1996. Maintenance of nuclear factor-κB/Rel and c-myc expression during CD40 ligand rescue of WEHI-231 early B cells from receptor-mediated apoptosis through modulation of IκB proteins. J. Immunol. 157:81.
36. Lernbecher, T., Muller, U. and Wirth, T. 1993. Distinct NF-κB/ Rel transcription factors are responsible for tissue-specific and inducible gene activation. Nature 365:767.
37. Lernbecher, T., Kistler, B. and Wirth, T. 1994. Two distinct mechanisms contribute to the constitutive activation of RelB in lymphoid cells. EMBO J. 13:4060.
38. Weih, F., Carrasco, D. and Bravo, R. 1994. Constitutive and inducible Rel/ NF-κB activities in mouse and spleen. Oncogene 9:3289.
39. Krieg, A. M. 1995. CpG DNA: a pathogenic factor in SLE? J. Clin. Immunol. 15:284.
40. Stacey, K. J., Sweet, M. J. and Hume, D. A. 1996. Macrophages ingest and are activated by bacterial DNA. J. Immunol. 157:2116.
41. Sparwasser, T., Miethe, T., Lipford, G., Erdmann, A., Hacker, H., Heeg, K. and Wagner, H. 1997. Macrophages sense pathogens via DNA motifs: induction of tumor necrosis factor-α-mediated shock. Eur. J. Immunol. 27:1671.
42. Lee, H., Arsura, M., Wu, M., Duyao, M., Buckler, A. J. and Sonenshein, G. E. 1995. Role of Rel-related factors in control of c-myc gene transcription in receptor-mediated apoptosis of the murine B cell WEHI-231 line. J. Exp. Med. 181:1169.
43. Van Antwerp, Martin, D. J., S. J., Kafri, T., Green, D. R. and Verma, I. M. 1996. Suppression of TNF-α-induced apoptosis by NF-kappaB. Science 274:787.
44. Yi, A.-K. and Krieg, A. M. 1998. Rapid induction of mitogen-activated protein kinases by immune stimulatory CpG DNA. J. Immunol. 161:4493.
45. Fox, R. I. 1993. Mechanism of action of hydroxychloroquine as an antirheumatic drug. Semin. Arthritis Rheum. 23:82.
46. Hahn, F. E. 1974. Chloroquine (Resochin). In Corcoran, J. and Hahn, F. E., eds, Antibiotics III: Mechanism of Action of Antimicroal and Antitumor Agents, p. 58. Springer, Berlin.
47. Matsuzawa, Y. and Hosteller, K. Y. 1980. Studies on drug-induced lipidosis: subcellular localization of phospholipid and cholesterol in the liver of rats treated with chloroquine or 4,4′-(diethyl-aminoethoxy)alpha, beta-diethyldiphenylethane. J. Lipid. Res. 21:202.
48. Hostetler, K. Y., Reasor, M. and Yazaki, P. J. 1985. Chloroquine-induced phospholipid fatty liver. Measurement of drug and lipid concentrations in rat liver lysosomes. J. Biol. Chem. 260:215.
49. Kubo, M. and Hostetler, K. Y. 1987. Metabolic basis of diethyl-aminoethoxyhextrol-induced phospholipid fatty liver. Am. J. Physiol. 252:E375.
50. Hurst, N. P., French, J. K., Bell, A. L., Nuki, G., O'Donnell, M. L., Betts, W. H. and Cleland, L. G. 1986. Differential effects of mepacrine, chloroquine and hydroxychloroquine on superoxide anion generation, phospholipid methylation and arachidnic acid release by human blood monocytes. Biochem. Pharmacol. 35:3083.
51. Jeong, J.-Y. and Jue, D.-M. 1997. Chloroquine inhibits processing of tumor necrosis factor in lipopolysaccharide-stimulated RAW 264.7 macrophages. J. Immunol. 158:4901.
52. Krieg, A. M. 1995. Uptake and localization of phosphodiester and chimeric oligodeoxynucleotides in normal and leukemic primary cells. In Akhtar, S., ed., Delivery Strategies for Antisense Oligonucleotide Therapeutics, p. 177. CRC Press, Boca Raton, FL.