Antibody regulation of T-cell immunity: Implications for vaccine strategies against intracellular pathogens

Expert Review of Vaccines

Volumn 3, Issue 1, 2004, Pages 23-34

  Igietseme, Joseph U ^a   Eko, Francis O ^b   He, Qing ^a,b   Black, Carolyn M ^a  

^a NATL CENTER FOR INFECTIOUS DISEASES   (United States)

^b MOREHOUSE SCHOOL OF MEDICINE   (United States)

Author keywords

Antibodies; Antigen processing; Cytokines; Fc receptors; IL 12; Immunity; Immunoregulation; Intracellular microbial pathogens; T cells; T helper type 1; T helper type 2; Vaccines

Indexed keywords

ACID HYDROLASE; ANTIBODY; B7 ANTIGEN; CD40 ANTIGEN; CYTOKINE; FC RECEPTOR; GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G2A ANTIBODY; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; LISTERIOLYSIN; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; NITRIC OXIDE SYNTHASE; STAT2 PROTEIN; STAT4 PROTEIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VACCINE; BACTERIAL VACCINE; FUNGUS VACCINE; PROTOZOAL VACCINE;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY RESPONSE; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CELLULAR IMMUNITY; CHLAMYDIA; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EHRLICHIA CHAFFEENSIS; HELPER CELL; HUMAN; HUMORAL IMMUNITY; IMMUNOBIOLOGY; INFECTION; LISTERIA; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMORY CELL; MYCOBACTERIUM; NONHUMAN; ORIENTIA TSUTSUGAMUSHI; PHAGOSOME; PRIORITY JOURNAL; REVIEW; RICKETTSIA; SALMONELLA; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL; VACCINATION; ANIMAL; ANTIBODY PRODUCTION; IMMUNOLOGY; INNATE IMMUNITY;

ANIMALS; ANTIBODIES; ANTIBODY FORMATION; BACTERIAL VACCINES; FUNGAL VACCINES; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, NATURAL; PROTOZOAN VACCINES; TH1 CELLS;

EID: 1042268186     PISSN: 14760584     EISSN: None     Source Type: Journal    
DOI: 10.1586/14760584.3.1.23     Document Type: Review

References (114)

1. Ismail N, Olano JP, HM Feng, DH Walker. Current status of immune mechanisn is of killing of intracellular microorganisms. FEMS Microbiol. Lett. 207(2), 111-120 (2002).
2. Plotkin SA. Immunologic correlates of protection induced by vaccination. Pediatr. Infect. Dis. J. 20(1), 63-75 (2001).
3. Moore T, Ekworomadu C, Eko F et al. Fc receptor-mediated antibody regulation of T-cell immunity against intracellular pathogens. J. Infect. Dis. 188(4), 617-624 (2003). Confirms that antibodies of specific isotypes enhance Th1 activation against intracellular pathogens.
4. Arulanandam B, Raeder R, Nedrud JG et al. IgA Immunodeficiency leads to Inadequate Th cell priming and increased susceptibility to influenza virus infection. J. Immunol. 166, 226-231 (2001). Report revealed that antibodies of the IgA isotype enhance Th1 activation against viruses.
5. Guyre PM, Graziano RF, Goldstein J et al. Increased potency of Fc-receptor-targeted antigens. Cancer Immunol. Immunother. 45, 146-148 (1997). One of the first reports revealing that antibodies are capable of enhancing T cell response via FcR mechanisms.
6. Mackaness GB. Resistance to intracellular infection. J. Infect. Dis. 123, 439-445 (1971).
7. Collins FM. Cellular antimicrobial immunity. Crit. Rev. Microbiol. 7, 27-91 (1978).
8. Dorman SE, Holland SM. Interferon-γ and interleukin-12 pathway defects and human disease. Cytokine Growth Factor Rev. 11(4), 321-333 (2000). Recent finding of heightened susceptibility of humans to mycobacterial and intracellular pathogens due to mutations in certain Th1 cytokines, especially IL-12 and IFN-γ.
9. Igietseme JU, Eko FO, Black CM. Contemporary approaches to designing and evaluating vaccines against Chlamydia. Expert Rev. Vaccines 2(1), 129-146 (2003).
10. Morrison RP, Caldwell HD. Immunity to murine chlamydial genital infection. Infect. Immun. 70(6), 2741-2751 (2002).
11. Loomis PW, Starnbach MN. T cell responses to Chlamydia trachomatis. Curr. Opin. Microbiol. 5, 87-91 (2002).
12. Cooper A, Dalton D, Stewart T et al. Disseminated tuberculosis in interferon-γ gene-disrupted mice. J. Exp. Med. 178(6), 2243-2247 (1993). The requirement for T-cell-derived IFN-γ for host control of mycobacterial infection.
13. Unanue, E, Inter-relationship among macrophages, natural killer cells and neutrophils in early stages of Listeria resistance. Curr. Opin. Immunol. 9(1), 35-43 (1997).
14. + TCR-α,β cells and IFN-γ in bacterial clearance independent of intracellular location. J. Immunol. 156(9), 3321-3326 (1996). The requirement for T-cell-derived IFN-γ for host control of salmonella infection.
15. Walker D, Olano J, Feng H. Critical role of cytotoxic T lymphocytes in immune clearance of rickettsial infection. Infect. Immun. 69(3), 1841-1846 (2001). The demonstration of a critical role of CTLs in host control of rickettsial infection.
16. Rank RG. Models of immunity. In Chlamydia: Intracellular Biology, Pathogenesis and Immunity. Stephens RS (Ed.), ASM Press, DC, USA 239-295 (1999).
17. Rank RG. Animal models of urogenital infections. Methods Enzymol. 235, 83-93 (1994).
18. Feng H, Popov V, Yuoh G, Walker D. Role of T lymphocyte subsets in immunity to spotted fever group Rickettsiae. J. Immunol. 158(11), 5314-5320 (1997).
19. +) T cells. Infect. Immun. 68(12), 6979-6987 (2000).
20. Rottenberg ME, Gigliotti-Rothfuchs A, Wigzell H. The role of IFN-γ in the outcome of chlamydial infection. Curr. Opin. Immunol. 14(4), 444-451 (2002).
21. Byrne GI, Lehmann LK, Landry GJ. Induction of tryptophan catabolism is the mechanism for γ interferon-mediated inhibition of intracellular Chlamydia psittaci replication in T24 cells. Infect. Immun. 53, 347-351 (1986).
22. Holtmann H, Shemer-Avni Y, Wessel K, Sarov I, Wallach D. Inhibition of growth of Chlamydia trachomatis by tumor necrosis factor is accompanied by increased prostaglandin synthesis. Infect. Immun. 58, 3168-3172 (1990).
23. Kaufmann SHE. Immunity to intracellular bacteria. Annu. Rev. Immunol. 11, 29-163 (1993).
24. Zhong G, de la Maza LM. Activation of mouse peritoneal macrophages in vitro or in vivo by recombinant murine γ-interferon inhibits the growth of Chlamydia trachomatis serovar L1. Infect. Immun. 56, 3322-3325 (1988).
25. Feng H, Walker D. Mechanisms of intracellular killing of Rickettsia conorii in infected human endothelial cells, hepatocytes, and macrophages. Infect. Immun. 68(12), 6729-6736 (2000).
26. MacKenzie C, Gonzalez R, Kniep E, Roch S, Daubener W. Cytokine mediated regulation of interferon-γ-induced IDO activation. Adv. Exp. Med. Biol. 467, 533-539 (1999).
27. Daubener W, MacKenzie C. IFN-γ activated indoleamine 2,3-dioxygenase activity in human cells is an antiparasitic and an antibacterial effector mechanism. Adv. Exp. Med. Biol. 467, 517-524 (1999).
28. Chen B, Stout R, Campbell WF. Nitric oxide production: a mechanism of Chlamydia trachomatis inhibition in interferon-γ-treated RAW264.7 cells. FEMS Immunol. Med. Microbiol. 14(2-3), 109-120 (1996).
29. Bogdan C. Nitric oxide and the immune response. Nat. Immunol. 2(10), 907-916 (2001).
30. Bogdan C, Rollinghoff M, Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr. Opin. Immunol. 12(1), 64-76 (2000).
31. Barnewall R, Rikihisa Y. Abrogation of γ interferon-induced inhibition of Ehrlichia chaffeensis infection in human monocytes with iron-transferrin. Infect. Immun. 62(11), 4804-4810 (1994).
32. Byrd TF, MA Horwitz. Regulation of transferrin receptor expression and ferritin content in human mononuclear phagocytes. Coordinate upregulation by iron transferrin and downregulation by interferon-γ. J. Clin. Invest. 91, 969-976 (1993).
33. Edelson B, Cossart P, Unanue E. Paradigm revisited: antibody provides resistance to Listeria infection. J. Immunol. 163(8), 4087-4090 (1999).
34. Caldwell HD, Perry LJ. Neutralization of Chlamydia trachomatis infectivity with antibodies to the major outer membrane protein. Infect. Immun. 38, 745-754 (1982).
35. Zhang Y-X, Stewart SJ, Caldwell HD. Protective monoclonal antibodies to Chlamydia trachomatis serovar- and serogroup-specific major outer membrane protein determinants. Infect. Immun. 57, 636-638 (1989).
36. Edelson B, Unanue E. Intracellular antibody neutralizes Listeria growth. Immunity 14(5), 503-512 (2001).
37. Cotter TW, Meng Q, Shen Z-L, et al. Protective efficacy of outer membrane protein-specific immunoglobulin (Ig)A and IgG monoclonal antibodies in a murine model of Chlamydia trachomatis genital tract infection. Infect. Immun. 63, 4704-4714 (1995).
38. Mazanec MB, Nedrud JG, Kaetzel CS, Lamm ME. A three-tiered view of the role of IgA in mucosal defense. Immunol. Today 14, 430-435 (1993).
39. Corthesy B, Spertini F. Secretory immunoglobulin A: from mucosal protection to vaccine development. Biol. Chem. 380(11), 1251-1262 (1999).
40. Brandtzaeg P. Mucosal immunity-integration between mother and the breast-fed infant. Vaccine 21(24), 3382-3388 (2003).
41. Li J, Yager E, Reilly M et al. Outer membrane protein-specific monoclonal antibodies protect SCID mice from fatal infection by the obligate intracellular bacterial pathogen Ehrlichia chaffeensis. J. Immunol. 166(3), 1855-1862 (2001).
42. Casadevall A, Pirofski L. Antibody-mediated regulation of cellular immunity and the inflammatory response. Trends Immunol. 24(9), 474-478 (2003).
43. Casadevall A. Antibody-mediated immunity against intracellular pathogens: two-dimensional thinking comes full circle. Infect. Immun. 71(8), 4225-4228 (2003). A review of the role of antibodies in controlling intracellular pathogens that involves targeting the extracellular phase of certain microbes.
44. Burton DR, Parren PWHI. Vaccines and the induction of functional antibodies: time to look beyond the molecules of natural infection? Nat. Med. 6(2), 123-125 (2000).
45. Moore T, Ananaba GA, Bolier J et al. Fc Receptors regulation of protective immunity against Chlamydia trachomatis. Immunology 105(2), 213-221 (2002). The first report suggesting that the requirement for antibodies for optimal memory T-cell response is related to FcR-mediated functions of antibodies.
46. Brunham RC, Cohen CR, Kimani J, Bwayo J, Plummer F. Type1/Type2 immunity and Chlamydia trachomatis: insights from the influence of HIV, In: Chlamydial Infections. Schachter J, Saikku P, Stephens R, Rank RG (Eds.), University press, Antayla, Turkey, 202 (2002).
47. Szabo S, Dighe A, Gubler U, Murphy K. Regulation of the interleukin (IL)-12R β-2 subunit expression in developing T helper (Th)1 and Th2 cells. J. Exp. Med. 185(5), 817-824 (1997).
48. Jefferies C, O'Niell LAJ. Signal transduction pathway activated by Toll-like receptors. Mod. Asp. Immunobiol. 2(4), 169-175 (2002).
49. Dabbagh K, Lewis D. Toll-like receptors and T-helper-1/T-helper-2 responses. Curr. Opin. Infect. Dis. 16(3), 199-204 (2003).
50. Underhill D. Toll-like receptors: networking for success. Eur. J. Immunol. 33(7), 1767-1775 (2003).
51. Kaisho T, Akira S. Regulation of dendrit cell function through Toll-like receptors. Curr. Mol. Med. 3(4), 373-385 (2003).
52. Park A, Scott P. IL-12: keeping cell-mediated immunity alive. Scand. J. Immunol. 53(6), 529-532 (2001).
53. Lezzi G, Scotet E, Scheidegger D, Lanzaveochia A. The interplay between the duration of TCR and cytokine signaling determines T-cell polarization. Eur. J. Immunol. 29, 4029-4101 (1999).
54. Lu H, Zhong G. Interleukin-12 production is required for chlamydial antigen-pulsed dendritic cells to induce protection against live Chlamydia trachomatis infection. Infect. Immun. 67(4), 1763-1769 (1999). The first experimental evidence for the requirement of IL-12 in chlamydial immunity.
55. Igietseme JU, Ananaba GA, Bolier J et al. Suppression of endogenous IL-10 gene expression in dendritic cells enhances antigen presentation for enhanced specific Th1 induction: potential for cellular vaccine development. J. Immunol. 164 (4) 4212-4219 (2000). A demonstration of the impact of a deficiency of endogenous IL-10 on Th1 activation and the application of this process in vaccine design against pathogens (and possibly tumors) that require elevated Th1 activation.
56. Gherardi M, Ramirez J, Esteban M. Towards a new generation of vaccines: the cytokine IL-12 as an adjuvant to enhance cellular immune responses to pathogens during prime-booster vaccination regimens. Histol. Histopathol. 16(2), 655-667 (2001).
57. Villinger F. Cyrokines as clinical adjuvant how far are we? Expert. Rev. Vaccines 2(2), 317-326 (2003).
58. Fieschi C, Casanova J. The role of interleukin-12 in human infectious diseases: only a faint signature. Eur. J. Immunol. 33(6), 1461-1464 (2003).
59. Heinzel FP, Schoenhaut DS, Rerko RM, Rosser LE, Gately MK. Recombinant interleukin 12 cures mice infected with Leishmania major. J. Exp. Med 177(5), 1505-1509 (1993).
60. Sypek JP, Chung CL, Mayor SE et al. Resolution of cutaneous leishmaniasis: interleukin 12 initiates a protective T helper type 1 immune response. J. Exp. Med. 177(6), 1797-1802 (1993).
61. Neighbors M, Xu X, Barrat F et al. A critical role for interleukin 18 in primary and memory effector responses to Listeria monocytogenes that extends beyond its effects on interferon γ production. J. Exp. Med 194(3), 343-354 (2001).
62. Su H, Parnell M, Caldwell HD. Protective efficacy of a parenterally administered MOMP-derived synthetic oligopeptide vaccine in a murine model of Chlamydia trachomatis genital tract infection: serum neutralizing IgG antibodies do not protect against genital tract infection. Vaccine 13(11), 1023-1032 (1995).
63. Bailey RL, Kajbaf M, Whittle HC, Ward ME, Mabey DC. The influence of local antichlamydial antibody on the acquisition and persistence of human ocular chlamydial infection: IgG antibodies are not protective. Epidemiol. Infect. 111(2), 315-324 (1993).
64. Johansson M, Schon K, Ward M, Lycke N. Studies in knockout mice reveal that antichlamydial protection requires Th1 cells producing IFN-γ: is this true for human? Scand. J. Immunol. 46(6), 546-552 (1997).
65. Cohen CR, Nguti R, Bukusi EA et al. Human immunodeficiency virus type 1-infected women exhibit reduced interferon-γ after Chlamydia trachomatis stimulation of peripheral lymphocytes. J. Infect. Dis. 182(6), 1672-1677 (2000).
66. Johansson M, Schon K, Ward M, Lycke N. Genital tract infection with Chlamydia trachomatis fails to induce protective immunity in γ-interferon receptor-deficient mice despite a strong local immunoglobulin A response. Infect. Immun. 65(3), 1032-1044 (1997).
67. Cotter TW, Ramsey KH, Miranpuri GS, Poulsen CE, Byrne GI. Dissemination of Chlamydia trachomatis chronic genital tract infection in γ interferon gene knockout mice. Infect. Immun. 65(6), 2145-2152 (1997).
68. Igietseme JU, Black CM, Caldwell HD. Chlamydia vaccine: strategies and status. Bio. Drugs 16(1), 19-35 (2002).
69. Igietseme JU, Ananaba GA, Candal DH, Lyn D, Black CM. Immune control of chlamydial growth in the human epithelial cell line RT4 involves multiple mechanisms that include nitric oxide induction, tryptophan catabolism and iron deprivation. Microbiol. Immunol. 42(9), 617-625 (1998).
70. Igietseme JU, Rank RG. Susceptibility to reinfection after a primary chlamydial genital infection is associated with a decrease of antigen-specific T cells in the genital tract. Infect. Immun. 59, 1346-1351 (1991).
71. Su H, Feilzer K, Caldwell HD, Morrison RP. Chlamydia trachomatis genital tract Infection of antibody-deficient gene knockout mice. Infect. Immun. 65(6), 1993-1999 (1997). One of the initial evidence that memory T-cell response is diminished during reinfections in the absence of specific antichlamydial antibodies.
72. Yang X, Brunham RC. Gene knockout B cell-deficient mice demonstrate that B cells play an important role in the initiation of T cell responses to Chlamydia trachomatis (mouse pneumonitis) lung infection. J. Immunol. 161(3), 1439-1446 (1998). One of the initial evidence that memory T-cell response is diminished during reinfections in the absence of specific antichlamydial antibodies.
73. Caron E, Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282(5394), 1717-1721 (1998).
74. Huber VC, Lynch JM, Bucher DJ, Le J, Metzger DW. Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J. Immunol. 166, 7381-7388 (2001).
75. Geissmann F, Lauunay P, Pasquier B et al. A subset of human dendritic cells expresses IgA Fc receptor (CD89), which mediates intemalization and activation upon cross-linking by IgA complexes. J. Immunol. 166, 346-352 (2001).
76. Lanzavecchia A. Mechanisms of antigen uptake for presentation. Curr. Opin. Immunol. 8(3), 348-354 (1996).
77. Regnault A, Lankar D, Lacabanne V et al. Fcγ receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J. Exp. Med. 189(2), 371-380 (1999).
78. Gosselin EJ, Wardwell K, Gosselin DR, et al. Enhanced antigen presentation using human Fcy receptor (monocyte/macrophage)-specific immunogens. J. Immunol. 149, 3477-3481 (1992).
79. Fanger NA, Vogitlaender D, Liu C et al. Characterization of expression, cytokine regulation, and effector function of the high affinity IgG receptor (CD64) expressed on human blood dendritic cells. J. Immunol. 158, 3090-3098 (1997).
80. Bell D, Young JW, Banchereau J. Dendritic cells. Adv. Immunol. 72, 255-324 (1999).
81. Guermonprez P, Valladeau J, Zitvogel L, Thery C, Amigorena C. Antigen presentation and T cell stimulation by dendritic cells. Ann. Rev. Immunol. 20, 621-667 (2002).
82. Ojcius DM, Bravo de Alba Y, Kanellopoulos JM et al. Internalization of Chlamydia by dendritic cells and stimulation of Chlamydia-specific T cells. J. Immunol. 160(3), 12970-1303 (1998).
83. Su H, Messer R, Whitmire W, et al. Vaccination against chlamydial genital tract infection after immunization with dendritic cells pulsed ex vivo with nonviable chlamydiae. J. Exp. Med. 188(5), 809-818 (1998).
84. Stagg AJ, Stackpoole A, Elsley WJ, Knight SC. Acquisition of chlamydial antigen by dendritic cells and monocytes. Adv. Exp. Med. Biol. 329, 581-586 (1993).
85. Stagg AJ, Tuffrey M, Woods C, Wunderink E, Knight SC. Protection against ascending infection of the genital tract by Chlamydia trachomatis is associated with recruitment of major histocompatibility complex class II antigen-presenting cells into uterine tissue. Infect. Immun. 66(8), 3535-3544 (1998).
86. Wen YM, Qu D, Zhou SH. Antigen-antibody complex as therapeutic vaccine for viral hepatitis B. Intern. Rev. Immunol. 18, 251-258 (1999).
87. Heyman B. Feedback regulation by IgG antibodies. Immunol. Lett. 88(2), 157-161 (2003).
88. Kane MM, Mosser DM. The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 166(2), 1141-1147 (2001).
89. Ravetch JV, Bolland S. IgG Fc Receptors. Ann. Rev. Immunol. 19, 275-290 (2001).
90. Hamano Y, Arase H, Saisho H, Saito T. Immune complex and Fc receptor-mediated augmentation of antigen presentation for in vivo Th cell responses. J. Immunol. 164, 6113-6119 (2000).
91. Amigorena S, Bonnerot C. Fc receptor signaling and trafficking: a connection for antigen processing. Immunol. Rev. 172, 279-284 (1999).
92. Amigorena S, Bonnerot C. Fc receptors for IgG and antigen presentation on MHC class I and class II molecules. Semin. Immunol. 11, 385-390 (1999).
93. Rao A, Avni O. Molecular aspects of T-cell differentiation. Br. Med. Bull. 56(4), 969-984 (2000).
94. Wurster AL, Tanaka T, Grusby MJ. The Biology of Stat4 and Stat6. Oncogene 19(21), 577-2584 (2000).
95. Murphy KM, Ouyang J, Farrar D et al. Signaling and transcription in T helper development. Ann. Rev. Immunol. 18, 451-494 (2000).
96. Cohen BE, Rosenthal AS, Paul WE. Antigen-macrophage interaction. II. Relative roles of cytophilic antibody and other membrane sites. J. Immunol. 111, 820-828 (1973).
97. Chang TW. Regulation of immune response by antibodies: the importance of antibody and monocyte Fc receptor interaction in T cell activation. Immunol. Today 6, 245 (1985).
98. Manca F, Fenoglio D, Kunkl A. Differential activation of T cell dones stimulated by macrophages exposed to antigen complexed with monoclonal antibodies. J. Immunol. 140, 2893-2898 (1988). One of the first in vitro observations that antigen delivery via antibodies could lead to an enhanced T-cell activation.
99. Pieters J. MHC class II-restricted antigen processing and presentation. Adv. Immunol. 75, 159-208 (2000).
100. Moser M, Murphy KM. Dendritic cell regulation of TH1-TH2 development. Nature Immunol. 1(3), 199-205 (2000).
101. Heijnen IA, van Vugt MJ, Fanger NA et al. Antigen targeting to myeloid-specific human FcγRI/CD64 triggers enhanced antibody responses in transgenic mice. J. Clin. Invest. 97(2), 331-338 (1996).
102. Igietseme JU, Eko FO, Ananaba GA, et al. Immunologic basis for the protective efficacy of chlamydia vaccines and the mechanism of T and B cell co-operaton in chlamydia immunity. In: Chlamydia Infections. Schachter J, Saikku P, Stephens R (Eds.), University press, Antalya, Turkey 400-415 (2002).
103. Chu RS, Targoni OS, Krieg AM, Lehmann PV, Harding CV. CpG Oligodeoxynudeotides acts as adjuvants that switch on T-helper (Th)1 immunity. J. Exp. Med. 186, 1623-1631 (1997).
104. Klinman DM, Barnhart KM, Conover J. CpG motifs as immune adjuvants. Vaccine 17(1), 19-25 (1999).
105. Carson DA, Raz E. Oligonucleotide adjuvants for T helper (Th)1-specific vaccination. J. Exp. Med. 186, 1621-1622 (1997).
106. Huang L-Y, Sousa CR, Itoh Y, Inman J, Scott DE. IL-12 induction by a Th1-inducing adjuvant in vivo: dendritic cell subsets and regulation by IL-10. J. Immunol. 167, 1423-1430 (2001).
107. Schijns VE. Antigen delivery systems and immunostimulation. Vet. Immunol. Immunopathol. 87, 195-198 (2002).
108. Kersten GFA, Crommelin DJA. Liposomes and ISCOMS as vaccine formulations. Biochim. Biophys. Acta 1241, 117-138 (1995).
109. Singh M, O'Hagan D. Advances in vaccine adjuvants. Nat. Biotechnol. 17(11), 1075-1081 (1999).
110. de la Maza LM, Peterson EM. Vaccines for Chamydia trachomatis infections. Curr. Opin. Investig. Drugs 3(7), 980-986 (2002).
111. Flynn, JL and Chan, J. Immunology of tuberculosis. Ann. Rev. Immunol. 19, 93-129 (2001).
112. Mazurek GH, LoBue PA, Daley CL et al. Comparison of a whole-blood interferon gamma assay with tuberculin skin testing for detecting latent Mycobacterium tuberculosis infection. JAMA 14, 1740-1747 (2003).
113. Casanova JL, Abel L. Genetic dissection of immunity to mycobacteria: the human model. Ann. Rev. Immunol. 20, 581-620 (2002). Genetic evidence for a crucial of Th1-related cytokines in protective immunity against mycobacterial infections.
114. MacMicking JD, Taylor GA, McKinney JD. Immune Control of tuberculosis by IFN-γ-inducible LRG-47. Science 302, 654-659 (2003).