CpG oligonucleotides enhance proliferative and effector responses of B cells in HIV-infected individuals

Journal of Immunology

Volumn 181, Issue 2, 2008, Pages 1199-1206

  Malaspina, Angela ^a   Moir, Susan ^a   DiPoto, Angela C ^a   Ho, Jason ^a   Wang, Wei ^a   Roby, Gregg ^a   O'Shea, Marie A ^a   Faucì, Anthony S ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; B LYMPHOCYTE RECEPTOR; CD27 ANTIGEN; CD40 LIGAND; CPG OLIGODEOXYNUCLEOTIDE; CPG OLIGONUCLEOTIDE TYPE B; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; LYMPHOTOXIN; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CPG OLIGONUCLEOTIDE; CPG-OLIGONUCLEOTIDE; CYTOKINE; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; OLIGODEOXYRIBONUCLEOTIDE; TLR9 PROTEIN, HUMAN;

ANTIBODY RESPONSE; ANTIVIRAL THERAPY; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL PROLIFERATION; CELL STIMULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOMODULATION; MAJOR CLINICAL STUDY; MEMORY CELL; PATIENT COMPLIANCE; PRIORITY JOURNAL; VIREMIA; CELL CULTURE; DRUG POTENTIATION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; VIROLOGY;

ADJUVANTS, IMMUNOLOGIC; B-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; HIV; HIV INFECTIONS; HUMANS; IMMUNOGLOBULIN G; LYMPHOCYTE ACTIVATION; OLIGODEOXYRIBONUCLEOTIDES; TOLL-LIKE RECEPTOR 9;

EID: 49049086136     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.2.1199     Document Type: Article

References (48)

1. Akira, S., K. Takeda, and T. Kaisho. 2001. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2: 675-680. (Pubitemid 32747155)
2. Krieg, A. M., A. K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546-549.
3. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745. (Pubitemid 32015992)
4. Hornung, V., S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdorfer, T. Giese, S. Endres, and G. Hartmann. 2002. Quantitative expression of Toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168: 4531-4537. (Pubitemid 34441357)
5. Hartmann, G., J. Battiany, H. Poeck, M. Wagner, M. Kerkmann, N. Lubenow, S. Rothenfusser, and S. Endres. 2003. Rational design of new CpG oligonucleotides that combine B cell activation with high IFN-α induction in plasmacytoid dendritic cells. Eur. J. Immunol. 33: 1633-1641. (Pubitemid 36790424)
6. Krug, A., S. Rothenfusser, V. Hornung, B. Jahrsdorfer, S. Blackwell, Z. K. Ballas, S. Endres, A. M. Krieg, and G. Hartmann. 2001. Identification of CpG oligonucleotide sequences with high induction of IFN-α/βin plasmacytoid dendritic cells. Eur. J. Immunol. 31: 2154-2163. (Pubitemid 32640732)
7. + T-cell responses in vitro. Blood 103: 2162-2169.
8. Krieg, A. M. 2002. CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20: 709-760.
9. Bernasconi, N. L., E. Traggiai, and A. Lanzavecchia. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298: 2199-2202.
10. Ruprecht, C. R., and A. Lanzavecchia. 2006. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur. J. Immunol. 36: 810-816.
11. Huggins, J., T. Pellegrin, R. E. Felgar, C. Wei, M. Brown, B. Zheng, E. C. Milner, S. H. Bernstein, I. Sanz, and M. S. Zand. 2007. CpG DNA activation and plasma-cell differentiation of CD27- naive human B cells. Blood 109: 1611-1619. (Pubitemid 46239595)
12. Jiang, W., M. M. Lederman, C. V. Harding, B. Rodriguez, R. J. Mohner, and S. F. Sieg. 2007. TLR9 stimulation drives naive B cells to proliferate and to attain enhanced antigen presenting function. Eur. J. Immunol. 37: 2205-2213. (Pubitemid 47250213)
13. Freyschmidt, E. J., A. Alonso, G. Hartmann, and L. Gissmann. 2004. Activation of dendritic cells and induction of T cell responses by HPV 16 L1/E7 chimeric virus-like particles are enhanced by CpG ODN or sorbitol. Antiviral Ther. 9: 479-489.
14. Heckelsmiller, K., S. Beck, K. Rall, B. Sipos, A. Schlamp, E. Tuma, S. Rothenfusser, S. Endres, and G. Hartmann. 2002. Combined dendritic cell- and CpG oligonucleotide-based immune therapy cures large murine tumors that resist chemotherapy. Eur. J. Immunol. 32: 3235-3245. (Pubitemid 35414881)
15. Krieg, A. M. 2000. The role of CpG motifs in innate immunity. Curr. Opin. Immunol. 12: 35-43. (Pubitemid 30093448)
16. Krieg, A. M. 2004. Antitumor applications of stimulating Toll-like receptor 9 with CpG oligodeoxynucleotides. Curr. Oncol. Rep. 6: 88-95.
17. + T cell responses to protein antigens in rhesus macaques in vivo. Vaccine 23: 3310-3317.
18. Krieg, A. M. 2006. Therapeutic potential of Toll-like receptor 9 activation. Nat. Rev. Drug Discov. 5: 471-484. (Pubitemid 44136959)
19. Lane, H. C., H. Masur, L. C. Edgar, G. Whalen, A. H. Rook, and A. S. Fauci. 1983. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 309: 453-458.
20. Conge, A. M., K. Tarte, J. Reynes, M. Segondy, J. Gerfaux, M. Zembala, and J. P. Vendrell. 1998. Impairment of B-lymphocyte differentiation induced by dual triggering of the B-cell antigen receptor and CD40 in advanced HIV-1-disease. AIDS 12: 1437-1449.
21. Ballet, J. J., G. Sulcebe, L. J. Couderc, F. Danon, C. Rabian, M. Lathrop, J. P. Clauvel, and M. Seligmann. 1987. Impaired anti-pneumococcal antibody response in patients with AIDS-related persistent generalized lymphadenopathy. Clin. Exp. Immunol. 68: 479-487. (Pubitemid 17077133)
22. Miotti, P. G., K. E. Nelson, G. A. Dallabetta, H. Farzadegan, J. Margolick, and M. L. Clements. 1989. The influence of HIV infection on antibody responses to a two-dose regimen of influenza vaccine. J. Am. Med. Assoc. 262: 779-783.
23. Opravil, M., W. Fierz, L. Matter, J. Blaser, and R. Luthy. 1991. Poor antibody response after tetanus and pneumococcal vaccination in immunocompromised, HIV-infected patients. Clin. Exp. Immunol. 84: 185-189.
24. De Milito, A., C. Morch, A. Sonnerborg, and F. Chiodi. 2001. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS 15: 957-964. (Pubitemid 32476662)
25. Malaspina, A., S. Moir, S. M. Orsega, J. Vasquez, N. J. Miller, E. T. Donoghue, S. Kottilil, M. Gezmu, D. Follmann, G. M. Vodeiko, et al. 2005. Compromised B cell responses to influenza vaccination in HIV-infected individuals. J. Infect. Dis. 191: 1442-1450. (Pubitemid 40563355)
26. Titanji, K., A. De Milito, A. Cagigi, R. Thorstensson, S. Grutzmeier, A. Atlas, B. Hejdeman, F. P. Kroon, L. Lopalco, A. Nilsson, and F. Chiodi. 2006. Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection. Blood 108: 1580-1587. (Pubitemid 44316125)
27. Cooper, C. L., H. L. Davis, J. B. Angel, M. L. Morris, S. M. Elfer, I. Seguin, A. M. Krieg, and D. W. Cameron. 2005. CPG 7909 adjuvant improves hepatitis B virus vaccine seroprotection in antiretroviral-treated HIV-infected adults. AIDS 19: 1473-1479.
28. Moir, S., A. Malaspina, O. K. Pickeral, E. T. Donoghue, J. Vasquez, N. J. Miller, S. R. Krishnan, M. A. Planta, J. F. Turney, J. S. Justement, et al. 2004. Decreased survival of B cells of HIV-viremic patients mediated by altered expression of receptors of the TNF superfamily. J. Exp. Med. 200: 587-599. (Pubitemid 39258308)
29. Malaspina, A., S. Moir, J. Ho, W. Wang, M. L. Howell, M. A. O'Shea, G. A. Roby, C. A. Rehm, J. M. Mican, T. W. Chun, and A. S. Fauci. 2006. Appearance of immature/transitional B cells in HIV-infected individuals with advanced disease: correlation with increased IL-7. Proc. Natl. Acad. Sci. USA 103: 2262-2267. (Pubitemid 43271658)
30. Moir, S., A. Malaspina, K. M. Ogwaro, E. T. Donoghue, C. W. Hallahan, L. A. Ehler, S. Liu, J. Adelsberger, R. Lapointe, P. Hwu, et al. 2001. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc. Natl. Acad. Sci. USA 98: 10362-10367. (Pubitemid 32803025)
31. Moir, S., A. Malaspina, J. Ho, W. Wang, A. C. DiPoto, M. A. O'Shea, G. Roby, J. M. Mican, S. Kottilil, T. W. Chun, et al. 2008. Normalization of B cell counts and subpopulations following antiretroviral therapy in chronic HIV disease. J. Infect. Dis. 197: 572-579. (Pubitemid 351321535)
32. Ehrhardt, G. R., J. T. Hsu, L. Gartland, C. M. Leu, S. Zhang, R. S. Davis, and M. D. Cooper. 2005. Expression of the immunoregulatory molecule FcRH4 de- fines a distinctive tissue-based population of memory B cells. J. Exp. Med. 202: 783-791.
33. Bernasconi, N. L., N. Onai, and A. Lanzavecchia. 2003. A role for Toll-like receptors in acquired immunity: upregulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101: 4500-4504.
34. Randall, T. D., A. W. Heath, L. Santos-Argumedo, M. C. Howard, I. L. Weissman, and F. E. Lund. 1998. Arrest of B lymphocyte terminal differentiation by CD40 signaling: mechanism for lack of antibody-secreting cells in germinal centers. Immunity 8: 733-742.34.
35. Halperin, S. A., G. Van Nest, B. Smith, S. Abtahi, H. Whiley, and J. J. Eiden. 2003. A phase I study of the safety and immunogenicity of recombinant hepatitis B surface antigen co-administered with an immunostimulatory phosphorothioate oligonucleotide adjuvant. Vaccine 21: 2461-2467.
36. Halperin, S. A., S. Dobson, S. McNeil, J. M. Langley, B. Smith, R. McCall-Sani, D. Levitt, G. V. Nest, D. Gennevois, and J. J. Eiden. 2006. Comparison of the safety and immunogenicity of hepatitis B virus surface antigen co-administered with an immunostimulatory phosphorothioate oligonucleotide and a licensed hepatitis B vaccine in healthy young adults. Vaccine 24: 20-26.
37. Cooper, C. L., H. L. Davis, M. L. Morris, S. M. Efler, A. M. Krieg, Y. Li, C. Laframboise, M. J. Al Adhami, Y. Khaliq, I. Seguin, and D. W. Cameron. 2004. Safety and immunogenicity of CPG 7909 injection as an adjuvant to Fluarix influenza vaccine. Vaccine 22: 3136-3143.
38. Cooper, C. L., H. L. Davis, M. L. Morris, S. M. Efler, M. A. Adhami, A. M. Krieg, D. W. Cameron, and J. Heathcote. 2004. CPG 7909, an immunostimulatory TLR9 agonist oligodeoxynucleotide, as adjuvant to Engerix-B HBV vaccine in healthy adults: a double-blind phase I/II study. J. Clin. Immunol. 24: 693-701.
39. Fu, Y. X., and D. D. Chaplin. 1999. Development and maturation of secondary lymphoid tissues. Annu. Rev. Immunol. 17: 399-433. (Pubitemid 29241130)
40. Feikin, D. R., C. Feldman, A. Schuchat, and E. N. Janoff. 2004. Global strategies to prevent bacterial pneumonia in adults with HIV disease. Lancet Infect. Dis. 4: 445-455. (Pubitemid 38844129)
41. Kroon, F. P., G. F. Rimmelzwaan, M. T. Roos, A. D. Osterhaus, D. Hamann, F. Miedema, and J. T. van Dissel. Restored humoral immune response to influenza vaccination in HIV-infected adults treated with highly active antiretroviral therapy. AIDS 12: F217-223, 1998.
42. Overton, E. T., S. Sungkanuparph, W. G. Powderly, W. Seyfried, R. K. Groger, and J. A. Aberg. 2005. Undetectable plasma HIV RNA load predicts success after hepatitis B vaccination in HIV-infected persons. Clin. Infect. Dis. 41: 1045-1048.
43. Anderson, S. M., M. M. Tomayko, and M. J. Shlomchik. 2006. Intrinsic properties of human and murine memory B cells. Immunol. Rev. 211: 280-294. (Pubitemid 43882979)
44. + peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J. Exp. Med. 188: 1679-1689.
45. Chong, Y., H. Ikematsu, K. Kikuchi, M. Yamamoto, M. Murata, M. Nishimura, S. Nabeshima, S. Kashiwagi, and J. Hayashi. 2004. Selective CD27+ (memory) B cell reduction and characteristic B cell alteration in drugnaive and HAART-treated HIV type 1-infected patients. AIDS Res. Hum. Retroviruses 20: 219-226. (Pubitemid 38280933)
46. De Milito, A. 2004. B lymphocyte dysfunctions in HIV infection. Curr. HIV Res. 2: 11-21.
47. De Milito, A., A. Nilsson, K. Titanji, R. Thorstensson, E. Reizenstein, M. Narita, S. Grutzmeier, A. Sonnerborg, and F. Chiodi. 2004. Mechanisms of hypergammaglobulinemia and impaired antigen-specific humoral immunity in HIV-1 infection. Blood 103: 2180-2186. (Pubitemid 38326236)
48. Moir, S., J. Ho, A. Malaspina, W. Wang, A. C. DiPoto, M. A. O'Shea, G. Roby, S. Kottilil, J. Arthos, M. A. Proschan, et al. 2008. Evidence for HIV-associated B-cell exhaustion in a dysfunctional memory B-cell compartment in HIV-infected viremic individuals. J. Exp. Med. In press.