Wounding the immune system with its own blade: HIV-induced tryptophan catabolism and pathogenesis

Current Medicinal Chemistry

Volumn 18, Issue 15, 2011, Pages 2247-2256

  Boasso, A ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Human immunodeficiency virus; Immunopathogenesis; Indoleamine 2,3 dioxygenase

Indexed keywords

1 METHYLTRYPTOPHAN; ALPHA INTERFERON; ANTIRETROVIRUS AGENT; B7 ANTIGEN; BETA INTERFERON; CD200 ANTIGEN; CD200 RECEPTOR; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; GAMMA INTERFERON; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; IMMUNOSUPPRESSIVE AGENT; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 6; MESSENGER RNA; NEOPTERIN; TRANSFORMING GROWTH FACTOR BETA; TRYPTOPHAN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; DOWN REGULATION; EFFECTOR CELL; ENCEPHALITIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DYSREGULATION; IMMUNOPATHOGENESIS; IMMUNOREACTIVITY; IMMUNOREGULATION; LYMPHOPROLIFERATIVE DISEASE; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SIMIAN IMMUNODEFICIENCY VIRUS; TH1 CELL; TH1 TH2 BALANCE; TH17 CELL; TH2 CELL; TRYPTOPHAN METABOLISM; UPREGULATION; VIRION;

EID: 79957933574     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986711795656126     Document Type: Article

References (120)

1. Gong, V. Acquired immunodeficiency syndrome (AIDS). Am. J. Emerg. Med., 1984, 2(4), 336-346.
2. Pantaleo, G.; Fauci, A.S. New concepts in the immunopathogenesis of HIV infection. Annu. Rev. Immunol., 1995, 13, 487-512.
3. Picker, L.J. Immunopathogenesis of acute AIDS virus infection. Curr. Opin. Immunol., 2006, 18(4), 399-405. (Pubitemid 43947575)
4. Shearer, G.M. HIV-induced immunopathogenesis. Immunity, 1998, 9(5), 587-593. (Pubitemid 28557587)
5. Vergis, E.N.; Mellors, J.W. Natural history of HIV-1 infection. Infect. Dis. Clin. North Am., 2000, 14(4), 809-825, v-vi. (Pubitemid 32103892)
6. Levy, J.A. HIV pathogenesis: knowledge gained after two decades of research. Adv. Dent. Res., 2006, 19(1), 10-16.
7. Gerstoft, J.; Malchow-Moller, A.; Bygbjerg, I.; Dickmeiss, E.; Enk, C.; Halberg, P.; Haahr, S.; Jacobsen, M.; Jensen, K.; Mejer, J.; Nielsen, J.O.; Thomsen, H.K.; Sondergaard, J.; Lorenzen, I. Severe acquired immunodeficiency in European homosexual men. Br. Med. J. (Clin. Res. Ed)., 1982, 285(6334), 17-19. (Pubitemid 12080389)
8. Mildvan, D.; Mathur, U.; Enlow, R.W.; Romain, P.L.; Winchester, R.J.; Colp, C.; Singman, H.; Adelsberg, B.R.; Spigland, I. Opportunistic infections and immune deficiency in homosexual men. Ann. Intern. Med., 1982, 96(6 Pt 1), 700-704. (Pubitemid 12029335)
9. Grohmann, U.; Fallarino, F.; Puccetti, P. Tolerance, DCs and tryptophan: much ado about IDO. Trends. Immunol., 2003, 24(5), 242-248. (Pubitemid 36555962)
10. Mellor, A.L.; Munn, D.H. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol., 2004, 4(10), 762-774. (Pubitemid 39336293)
11. Boasso, A.; Shearer, G.M. How does indoleamine 2,3-dioxygenase contribute to HIV-mediated immune dysregulation. Curr. Drug Metab., 2007, 8(3), 217-223. (Pubitemid 46628287)
12. Munn, D.H.; Mellor, A.L. IDO and tolerance to tumors. Trends. Mol. Med., 2004, 10(1), 15-18. (Pubitemid 38165324)
13. Douek, D. HIV disease progression: immune activation, microbes, and a leaky gut. Top. HIV Med., 2007, 15(4), 114-117.
14. Moanna, A.; Dunham, R.; Paiardini, M.; Silvestri, G. CD4+ T-cell depletion in HIV infection: killed by friendly fire? Curr. HIV/AIDS Rep., 2005, 2(1), 16-23.
15. Silvestri, G.; Paiardini, M.; Pandrea, I.; Lederman, M.M.; Sodora, D.L. Understanding the benign nature of SIV infection in natural hosts. J. Clin. Invest., 2007, 117(11), 3148-3154. (Pubitemid 350096967)
16. Schroecksnadel, K.; Zangerle, R.; Bellmann-Weiler, R.; Garimorth, K.; Weiss, G.; Fuchs, D. Indoleamine-2, 3-dioxygenase and other interferongamma- mediated pathways in patients with human immunodeficiency virus infection. Curr. Drug Metab., 2007, 8(3), 225-236. (Pubitemid 46621672)
17. Fuchs, D.; Moller, A.A.; Reibnegger, G.; Stockle, E.; Werner, E.R.; Wachter, H. Decreased serum tryptophan in patients with HIV-1 infection correlates with increased serum neopterin and with neurologic/psychiatric symptoms. J. Acquir. Immune Defic. Syndr., 1990, 3(9), 873-876. (Pubitemid 20330669)
18. Fuchs, D.; Forsman, A.; Hagberg, L.; Larsson, M.; Norkrans, G.; Reibnegger, G.; Werner, E.R.; Wachter, H. Immune activation and decreased tryptophan in patients with HIV-1 infection. J. Interferon. Res., 1990, 10(6), 599-603.
19. Freese, A.; Swartz, K.J.; During, M.J.; Martin, J.B. Kynurenine metabolites of tryptophan: implications for neurologic diseases. Neurology, 1990, 40(4), 691-695. (Pubitemid 20139104)
20. Ruddick, J.P.; Evans, A.K.; Nutt, D.J.; Lightman, S.L.; Rook, G.A.; Lowry, C.A. Tryptophan metabolism in the central nervous system: medical implications. Expert Rev. Mol. Med., 2006, 8(20), 1-27. (Pubitemid 44322753)
21. Yoshida, R.; Imanishi, J.; Oku, T.; Kishida, T.; Hayaishi, O. Induction of pulmonary indoleamine 2,3-dioxygenase by interferon. Proc. Natl. Acad. Sci. U. S. A., 1981, 78(1), 129-132. (Pubitemid 11131252)
22. Huber, C.; Batchelor, J.R.; Fuchs, D.; Hausen, A.; Lang, A.; Niederwieser, D.; Reibnegger, G.; Swetly, P.; Troppmair, J.; Wachter, H. Immune response-associated production of neopterin. Release from macrophages primarily under control of interferon-gamma. J. Exp. Med., 1984, 160(1), 310-316. (Pubitemid 14089799)
23. Munn, D.H.; Shafizadeh, E.; Attwood, J.T.; Bondarev, I.; Pashine, A.; Mellor, A.L. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med., 1999, 189(9), 1363-1372. (Pubitemid 29227522)
24. Andersson, J.; Boasso, A.; Nilsson, J.; Zhang, R.; Shire, N.J.; Lindback, S.; Shearer, G.M.; Chougnet, C.A. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients. J. Immunol., 2005, 174(6), 3143-3147. (Pubitemid 40354012)
25. Boasso, A.; Herbeuval, J.P.; Hardy, A.W.; Anderson, S.A.; Dolan, M.J.; Fuchs, D.; Shearer, G.M. HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2,3-dioxygenase in plasmacytoid dendritic cells. Blood, 2007, 109(8), 3351-3359. (Pubitemid 46572523)
26. Nilsson, J.; Boasso, A.; Velilla, P.A.; Zhang, R.; Vaccari, M.; Franchini, G.; Shearer, G.M.; Andersson, J.; Chougnet, C. HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood, 2006, 108(12), 3808-3817. (Pubitemid 44864563)
27. Boasso, A.; Vaccari, M.; Hryniewicz, A.; Fuchs, D.; Nacsa, J.; Cecchinato, V.; Andersson, J.; Franchini, G.; Shearer, G.M.; Chougnet, C. Regulatory Tcell markers, indoleamine 2,3-dioxygenase, and virus levels in spleen and gut during progressive simian immunodeficiency virus infection. J. Virol., 2007, 81(21), 11593-11603. (Pubitemid 47623791)
28. Malleret, B.; Maneglier, B.; Karlsson, I.; Lebon, P.; Nascimbeni, M.; Perie, L.; Brochard, P.; Delache, B.; Calvo, J.; Andrieu, T.; Spreux-Varoquaux, O.; Hosmalin, A.; Le Grand, R.; Vaslin, B. Primary infection with simian immunodeficiency virus: plasmacytoid dendritic cell homing to lymph nodes, type I IFN, and immune suppression. Blood, 2008.
29. Grant, R.S.; Naif, H.; Thuruthyil, S.J.; Nasr, N.; Littlejohn, T.; Takikawa, O.; Kapoor, V. Induction of indolamine 2,3-dioxygenase in primary human macrophages by human immunodeficiency virus type 1 is strain dependent. J. Virol., 2000, 74(9), 4110-4115. (Pubitemid 30214416)
30. Grant, R.S.; Naif, H.; Thuruthyil, S.J.; Nasr, N.; Littlejohn, T.; Takikawa, O.; Kapoor, V. Induction of indoleamine 2,3-dioxygenase in primary human macrophages by HIV-1. Redox Rep., 2000, 5(2-3), 105-107. (Pubitemid 30487978)
31. Smith, D.G.; Guillemin, G.J.; Pemberton, L.; Kerr, S.; Nath, A.; Smythe, G.A.; Brew, B.J. Quinolinic acid is produced by macrophages stimulated by platelet activating factor, Nef and Tat. J. Neurovirol., 2001, 7(1), 56-60. (Pubitemid 32904359)
32. Grohmann, U.; Fioretti, M.C.; Bianchi, R.; Belladonna, M.L.; Ayroldi, E.; Surace, D.; Silla, S.; Puccetti, P. Dendritic cells, interleukin 12, and CD4+ lymphocytes in the initiation of class I-restricted reactivity to a tumor/self peptide. Crit. Rev. Immunol., 1998, 18(1-2), 87-98. (Pubitemid 128670060)
33. Hwu, P.; Du, M.X.; Lapointe, R.; Do, M.; Taylor, M.W.; Young, H.A. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J. Immunol., 2000, 164(7), 3596-3599. (Pubitemid 30169812)
34. Baban, B.; Hansen, A.M.; Chandler, P.R.; Manlapat, A.; Bingaman, A.; Kahler, D.J.; Munn, D.H.; Mellor, A.L. A minor population of splenic dendritic cells expressing CD19 mediates IDO-dependent T cell suppression via type I IFN signaling following B7 ligation. Int. Immunol., 2005, 17(7), 909-919. (Pubitemid 41417958)
35. Mellor, A.L.; Baban, B.; Chandler, P.R.; Manlapat, A.; Kahler, D.J.; Munn, D.H. Cutting edge: CpG oligonucleotides induce splenic CD19+ dendritic cells to acquire potent indoleamine 2,3-dioxygenase-dependent T cell regulatory functions via IFN Type 1 signaling. J. Immunol., 2005, 175(9), 5601-5605. (Pubitemid 41508038)
36. Munn, D.H.; Sharma, M.D.; Lee, J.R.; Jhaver, K.G.; Johnson, T.S.; Keskin, D.B.; Marshall, B.; Chandler, P.; Antonia, S.J.; Burgess, R.; Slingluff, C.L. Jr.; Mellor, A.L. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science, 2002, 297(5588), 1867-1870. (Pubitemid 35024345)
37. Puccetti, P. On watching the watchers: IDO and type I/II IFN. Eur. J. Immunol., 2007, 37(4), 876-879. (Pubitemid 46925324)
38. Konan, K.V.; Taylor, M.W. Importance of the two interferon-stimulated response element (ISRE) sequences in the regulation of the human indoleamine 2,3-dioxygenase gene. J. Biol. Chem., 1996, 271(32), 19140-19145. (Pubitemid 26271576)
39. Dai, W.; Gupta, S.L. Regulation of indoleamine 2,3-dioxygenase gene expression in human fibroblasts by interferon-gamma. Upstream control region discriminates between interferon-gamma and interferon-alpha. J. Biol. Chem., 1990, 265(32), 19871-19877. (Pubitemid 120013943)
40. Cano, O.D.; Neurauter, G.; Fuchs, D.; Shearer, G.M.; Boasso, A. Differential effect of type I and type II interferons on neopterin production and amino acid metabolism in human astrocyte-derived cells. Neurosci. Lett., 2008, 438(1), 22-25.
41. Taylor, M.W.; Feng, G.S. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J., 1991, 5(11), 2516-2522. (Pubitemid 21905800)
42. Pulendran, B. Modulating TH1/TH2 responses with microbes, dendritic cells, and pathogen recognition receptors. Immunol. Res., 2004, 29(1-3), 187-196. (Pubitemid 38822408)
43. Watford, W.T.; Moriguchi, M.; Morinobu, A.; O'Shea, J.J. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev., 2003, 14(5), 361-368. (Pubitemid 37099449)
44. Brenchley, J.M.; Price, D.A.; Schacker, T.W.; Asher, T.E.; Silvestri, G.; Rao, S.; Kazzaz, Z.; Bornstein, E.; Lambotte, O.; Altmann, D.; Blazar, B.R.; Rodriguez, B.; Teixeira-Johnson, L.; Landay, A.; Martin, J.N.; Hecht, F.M.; Picker, L.J.; Lederman, M.M.; Deeks, S.G.; Douek, D.C. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med., 2006, 12(12), 1365-1371. (Pubitemid 44924494)
45. Curreli, S.; Romerio, F.; Mirandola, P.; Barion, P.; Bemis, K.; Zella, D. Human primary CD4 + T cells activated in the presence of IFN-alpha 2b express functional indoleamine 2,3-dioxygenase. J. Interferon. Cytokine Res., 2001, 21(6), 431-437. (Pubitemid 32692465)
46. Abb, J.; Zachoval, R.; Zachoval, V.; Deinhardt, F. HIV antigen, HIV antibody and serum interferon in a patient with encephalopathy. Infection, 1987, 15(6), 425-426. (Pubitemid 18082257)
47. Minagawa, T.; Mizuno, K.; Hirano, S.; Asano, M.; Numata, A.; Kohanawa, M.; Nakane, A.; Hachimori, K.; Tamagawa, S.; Negishi, M.; et al. Detection of high levels of immunoreactive human beta-1 interferon in sera from HIVinfected patients. Life Sci., 1989, 45(11), iii-vii. (Pubitemid 19251920)
48. von Sydow, M.; Sonnerborg, A.; Gaines, H.; Strannegard, O. Interferonalpha and tumor necrosis factor-alpha in serum of patients in various stages of HIV-1 infection. AIDS Res. Hum. Retroviruses, 1991, 7(4), 375-380.
49. Herbeuval, J.P.; Hardy, A.W.; Boasso, A.; Anderson, S.A.; Dolan, M.J.; Dy, M.; Shearer, G.M. Regulation of TNF-related apoptosis-inducing ligand on primary CD4+ T cells by HIV-1: role of type I IFN-producing plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. U. S. A., 2005, 102(39), 13974-13979. (Pubitemid 41377688)
50. Herbeuval, J.P.; Nilsson, J.; Boasso, A.; Hardy, A.W.; Kruhlak, M.J.; Anderson, S.A.; Dolan, M.J.; Dy, M.; Andersson, J.; Shearer, G.M. Differential expression of IFN-alpha and TRAIL/DR5 in lymphoid tissue of progressor versus nonprogressor HIV-1-infected patients. Proc. Natl. Acad. Sci. U. S. A., 2006, 103(18), 7000-7005.
51. Colonna, M.; Trinchieri, G.; Liu, Y.J. Plasmacytoid dendritic cells in immunity. Nat. Immunol., 2004, 5(12), 1219-1226. (Pubitemid 41057736)
52. Beignon, A.S.; McKenna, K.; Skoberne, M.; Manches, O.; DaSilva, I.; Kavanagh, D.G.; Larsson, M.; Gorelick, R.J.; Lifson, J.D.; Bhardwaj, N. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J. Clin. Invest., 2005, 115(11), 3265-3275. (Pubitemid 41567591)
53. Potula, R.; Poluektova, L.; Knipe, B.; Chrastil, J.; Heilman, D.; Dou, H.; Takikawa, O.; Munn, D.H.; Gendelman, H.E.; Persidsky, Y. Inhibition of indoleamine 2,3-dioxygenase (IDO) enhances elimination of virus-infected macrophages in an animal model of HIV-1 encephalitis. Blood, 2005, 106(7), 2382-2390. (Pubitemid 41510811)
54. Grohmann, U.; Orabona, C.; Fallarino, F.; Vacca, C.; Calcinaro, F.; Falorni, A.; Candeloro, P.; Belladonna, M.L.; Bianchi, R.; Fioretti, M.C.; Puccetti, P. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol., 2002, 3(11), 1097-1101. (Pubitemid 35363664)
55. Boasso, A.; Herbeuval, J.P.; Hardy, A.W.; Winkler, C.; Shearer, G.M. Regulation of indoleamine 2,3-dioxygenase and tryptophanyl-tRNAsynthetase by CTLA-4-Fc in human CD4+ T cells. Blood, 2005, 105(4), 1574-1581. (Pubitemid 40223677)
56. Munn, D.H.; Sharma, M.D.; Mellor, A.L. Ligation of B7-1/B7-2 by human CD4+ T cells triggers indoleamine 2,3-dioxygenase activity in dendritic cells. J. Immunol., 2004, 172(7), 4100-4110. (Pubitemid 38375222)
57. Leng, Q.; Bentwich, Z.; Magen, E.; Kalinkovich, A.; Borkow, G. CTLA-4 upregulation during HIV infection: association with anergy and possible target for therapeutic intervention. Aids, 2002, 16(4), 519-529. (Pubitemid 34218846)
58. Kaufmann, D.E.; Kavanagh, D.G.; Pereyra, F.; Zaunders, J.J.; Mackey, E.W.; Miura, T.; Palmer, S.; Brockman, M.; Rathod, A.; Piechocka-Trocha, A.; Baker, B.; Zhu, B.; Le Gall, S.; Waring, M.T.; Ahern, R.; Moss, K.; Kelleher, A.D.; Coffin, J.M.; Freeman, G.J.; Rosenberg, E.S.; Walker, B.D. Upregulation of CTLA-4 by HIV-specific CD4+ T cells correlates with disease progression and defines a reversible immune dysfunction. Nat. Immunol., 2007, 8(11), 1246-1254. (Pubitemid 350011764)
59. Fontenot, J.D.; Gavin, M.A.; Rudensky, A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol., 2003, 4(4), 330-336. (Pubitemid 36432314)
60. Fallarino, F.; Grohmann, U.; Hwang, K.W.; Orabona, C.; Vacca, C.; Bianchi, R.; Belladonna, M.L.; Fioretti, M.C.; Alegre, M.L.; Puccetti, P. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol., 2003, 4(12), 1206-1212. (Pubitemid 37547898)
61. Chase, A.J.; Sedaghat, A.R.; German, J.R.; Gama, L.; Zink, M.C.; Clements, J.E.; Siliciano, R.F. Severe depletion of CD4+ CD25+ regulatory T cells from the intestinal lamina propria but not peripheral blood or lymph nodes during acute simian immunodeficiency virus infection. J. Virol., 2007, 81(23), 12748-12757. (Pubitemid 350156912)
62. Moreno-Fernandez, M.E.; Zapata, W.; Blackard, J.T.; Franchini, G.; Chougnet, C.A. Human regulatory T cells are targets for HIV infection and their susceptibility differs depending on the HIV-1 strain. J. Virol., 2009.
63. Oswald-Richter, K.; Grill, S.M.; Shariat, N.; Leelawong, M.; Sundrud, M.S.; Haas, D.W.; Unutmaz, D. HIV infection of naturally occurring and genetically reprogrammed human regulatory T-cells. PLoS Biol., 2004, 2(7), E198.
64. Cecchinato, V.; Tryniszewska, E.; Ma, Z.M.; Vaccari, M.; Boasso, A.; Tsai, W.P.; Petrovas, C.; Fuchs, D.; Heraud, J.M.; Venzon, D.; Shearer, G.M.; Koup, R.A.; Lowy, I.; Miller, C.J.; Franchini, G. Immune activation driven by ctla-4 blockade augments viral replication at mucosal sites in simian immunodeficiency virus infection. J. Immunol., 2008, 180(8), 5439-5447.
65. Hryniewicz, A.; Boasso, A.; Edghill-Smith, Y.; Vaccari, M.; Fuchs, D.; Venzon, D.; Nacsa, J.; Betts, M.R.; Tsai, W.P.; Heraud, J.M.; Beer, B.; Blanset, D.; Chougnet, C.; Lowy, I.; Shearer, G.M.; Franchini, G. CTLA-4 blockade decreases TGF-beta, IDO, and viral RNA expression in tissues of SIVmac251-infected macaques. Blood, 2006, 108(12), 3834-3842. (Pubitemid 44864566)
66. Shevach, E.M.; Stephens, G.L. The GITR-GITRL interaction: co-stimulation or contrasuppression of regulatory activity? Nat. Rev. Immunol., 2006, 6(8), 613-618. (Pubitemid 44134094)
67. Grohmann, U.; Volpi, C.; Fallarino, F.; Bozza, S.; Bianchi, R.; Vacca, C.; Orabona, C.; Belladonna, M.L.; Ayroldi, E.; Nocentini, G.; Boon, L.; Bistoni, F.; Fioretti, M.C.; Romani, L.; Riccardi, C.; Puccetti, P. Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat. Med., 2007, 13(5), 579-586. (Pubitemid 46828479)
68. Epple, H.J.; Loddenkemper, C.; Kunkel, D.; Troger, H.; Maul, J.; Moos, V.; Berg, E.; Ullrich, R.; Schulzke, J.D.; Stein, H.; Duchmann, R.; Zeitz, M.; Schneider, T. Mucosal but not peripheral FOXP3+ regulatory T cells are highly increased in untreated HIV infection and normalize after suppressive HAART. Blood, 2006, 108(9), 3072-3078.
69. Lahey, T.P.; Loisel, S.D.; Wieland-Alter, W. Glucocorticoid-induced tumor necrosis factor receptor family-related protein triggering enhances HIVspecific CD4+ T cell cytokine secretion and protects HIV-specific CD4+ T cells from apoptosis. J. Infect. Dis., 2007, 196(1), 43-49. (Pubitemid 46982736)
70. Wright, G.J.; Cherwinski, H.; Foster-Cuevas, M.; Brooke, G.; Puklavec, M.J.; Bigler, M.; Song, Y.; Jenmalm, M.; Gorman, D.; McClanahan, T.; Liu, M.R.; Brown, M.H.; Sedgwick, J.D.; Phillips, J.H.; Barclay, A.N. Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J. Immunol., 2003, 171(6), 3034-3046. (Pubitemid 37093527)
71. Wright, G.J.; Puklavec, M.J.; Willis, A.C.; Hoek, R.M.; Sedgwick, J.D.; Brown, M.H.; Barclay, A.N. Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity, 2000, 13(2), 233-242.
72. Hoek, R.M.; Ruuls, S.R.; Murphy, C.A.; Wright, G.J.; Goddard, R.; Zurawski, S.M.; Blom, B.; Homola, M.E.; Streit, W.J.; Brown, M.H.; Barclay, A.N.; Sedgwick, J.D. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science, 2000, 290(5497), 1768-1771. (Pubitemid 32004808)
73. Rosenblum, M.D.; Olasz, E.; Woodliff, J.E.; Johnson, B.D.; Konkol, M.C.; Gerber, K.A.; Orentas, R.J.; Sandford, G.; Truitt, R.L. CD200 is a novel p53- target gene involved in apoptosis-associated immune tolerance. Blood, 2004, 103(7), 2691-2698. (Pubitemid 38393026)
74. Fallarino, F.; Asselin-Paturel, C.; Vacca, C.; Bianchi, R.; Gizzi, S.; Fioretti, M.C.; Trinchieri, G.; Grohmann, U.; Puccetti, P. Murine plasmacytoid dendritic cells initiate the immunosuppressive pathway of tryptophan catabolism in response to CD200 receptor engagement. J. Immunol., 2004, 173(6), 3748-3754. (Pubitemid 39280736)
75. Chen, Z.; Marsden, P.A.; Gorczynski, R.M. Role of a distal enhancer in the transcriptional responsiveness of the human CD200 gene to interferongamma and tumor necrosis factor-alpha. Mol. Immunol., 2009, 46(10), 1951-1963.
76. Suh, H.S.; Zhao, M.L.; Rivieccio, M.; Choi, S.; Connolly, E.; Zhao, Y.; Takikawa, O.; Brosnan, C.F.; Lee, S.C. Astrocyte indoleamine 2,3- dioxygenase is induced by the TLR3 ligand poly(I:C): mechanism of induction and role in antiviral response. J. Virol., 2007, 81(18), 9838-9850. (Pubitemid 350067687)
77. Gottlieb, M.S.; Schroff, R.; Schanker, H.M.; Weisman, J.D.; Fan, P.T.; Wolf, R.A.; Saxon, A. Pneumocystis carinii pneumonia and mucosal candidiasis in previously healthy homosexual men: evidence of a new acquired cellular immunodeficiency. N. Engl. J. Med., 1981, 305(24), 1425-1431. (Pubitemid 12240076)
78. Clerici, M.; Stocks, N.I.; Zajac, R.A.; Boswell, R.N.; Lucey, D.R.; Via, C.S.; Shearer, G.M. Detection of three distinct patterns of T helper cell dysfunction in asymptomatic, human immunodeficiency virus-seropositive patients. Independence of CD4+ cell numbers and clinical staging. J. Clin. Invest., 1989, 84(6), 1892-1899. (Pubitemid 20016195)
79. Boasso, A.; Hardy, A.W.; Anderson, S.A.; Dolan, M.J.; Shearer, G.M. HIVinduced type I interferon and tryptophan catabolism drive T cell dysfunction despite phenotypic activation. PLoS ONE, 2008, 3(8), e2961.
80. Fallarino, F.; Grohmann, U.; You, S.; McGrath, B.C.; Cavener, D.R.; Vacca, C.; Orabona, C.; Bianchi, R.; Belladonna, M.L.; Volpi, C.; Santamaria, P.; Fioretti, M.C.; Puccetti, P. The Combined Effects of Tryptophan Starvation and Tryptophan Catabolites Down-Regulate T Cell Receptor {zeta}-Chain and Induce a Regulatory Phenotype in Naive T Cells. J. Immunol., 2006, 176(11), 6752-6761. (Pubitemid 43787857)
81. Trimble, L.A.; Shankar, P.; Patterson, M.; Daily, J.P.; Lieberman, J. Human immunodeficiency virus-specific circulating CD8 T lymphocytes have downmodulated CD3zeta and CD28, key signaling molecules for T-cell activation. J. Virol., 2000, 74(16), 7320-7330. (Pubitemid 30613077)
82. Boasso, A.; Vaccari, M.; Fuchs, D.; Hardy, A.W.; Tsai, W.P.; Tryniszewska, E.; Shearer, G.M.; Franchini, G. Combined effect of antiretroviral therapy and blockade of IDO in SIV-infected rhesus macaques. J.. Immunol.., 2009, 182(7), 4313-4320.
83. Xu, H.; Zhang, G.X.; Ciric, B.; Rostami, A. IDO: a double-edged sword for T(H)1/T(H)2 regulation. Immunol. Lett., 2008, 121(1), 1-6.
84. Gurtner, G.J.; Newberry, R.D.; Schloemann, S.R.; McDonald, K.G.; Stenson, W.F. Inhibition of indoleamine 2,3-dioxygenase augments trinitrobenzene sulfonic acid colitis in mice. Gastroenterology, 2003, 125(6), 1762-1773. (Pubitemid 37500441)
85. Kong, Q.F.; Sun, B.; Wang, G.Y.; Zhai, D.X.; Mu, L.L.; Wang, D.D.; Wang, J.H.; Li, R.; Li, H.L. BM stromal cells ameliorate experimental autoimmune myasthenia gravis by altering the balance of Th cells through the secretion of IDO. Eur. J. Immunol., 2009, 39(3), 800-809.
86. Sakurai, K.; Zou, J.P.; Tschetter, J.R.; Ward, J.M.; Shearer, G.M. Effect of indoleamine 2,3-dioxygenase on induction of experimental autoimmune encephalomyelitis. J. Neuroimmunol., 2002, 129(1-2), 186-196. (Pubitemid 34874924)
87. Xu, H.; Oriss, T.B.; Fei, M.; Henry, A.C.; Melgert, B.N.; Chen, L.; Mellor, A.L.; Munn, D.H.; Irvin, C.G.; Ray, P.; Ray, A. Indoleamine 2,3- dioxygenase in lung dendritic cells promotes Th2 responses and allergic inflammation. Proc. Natl. Acad. Sci. U. S. A., 2008, 105(18), 6690-6695. (Pubitemid 351754568)
88. Clark, D.A.; Blois, S.; Kandil, J.; Handjiski, B.; Manuel, J.; Arck, P.C. Reduced uterine indoleamine 2,3-dioxygenase versus increased Th1/Th2 cytokine ratios as a basis for occult and clinical pregnancy failure in mice and humans. Am. J. Reprod. Immunol., 2005, 54(4), 203-216. (Pubitemid 41309278)
89. Odemuyiwa, S.O.; Ghahary, A.; Li, Y.; Puttagunta, L.; Lee, J.E.; Musat- Marcu, S.; Ghahary, A.; Moqbel, R. Cutting edge: human eosinophils regulate T cell subset selection through indoleamine 2,3-dioxygenase. J. Immunol., 2004, 173(10), 5909-5913. (Pubitemid 39487742)
90. Clerici, M.; Shearer, G.M. A TH1->TH2 switch is a critical step in the etiology of HIV infection. Immunol. Today, 1993, 14(3), 107-111. (Pubitemid 23068292)
91. Clerici, M.; Shearer, G.M. The Th1-Th2 hypothesis of HIV infection: new insights. Immunol. Today, 1994, 15(12), 575-581. (Pubitemid 24353909)
92. Fallarino, F.; Grohmann, U.; Vacca, C.; Orabona, C.; Spreca, A.; Fioretti, M.C.; Puccetti, P. T cell apoptosis by kynurenines. Adv. Exp. Med. Biol., 2003, 527, 183-190. (Pubitemid 38197643)
93. Lee, G.K.; Park, H.J.; Macleod, M.; Chandler, P.; Munn, D.H.; Mellor, A.L. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology, 2002, 107(4), 452-460. (Pubitemid 36693650)
94. Fallarino, F.; Grohmann, U.; Vacca, C.; Bianchi, R.; Orabona, C.; Spreca, A.; Fioretti, M.C.; Puccetti, P. T cell apoptosis by tryptophan catabolism. Cell Death Differ., 2002, 9(10), 1069-1077.
95. Curti, A.; Pandolfi, S.; Valzasina, B.; Aluigi, M.; Isidori, A.; Ferri, E.; Salvestrini, V.; Bonanno, G.; Rutella, S.; Durelli, I.; Horenstein, A.L.; Fiore, F.; Massaia, M.; Colombo, M.P.; Baccarani, M.; Lemoli, R.M. Modulationof tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ T regulatory cells. Blood, 2007, 109(7), 2871-2877. (Pubitemid 46482083)
96. Manches, O.; Munn, D.; Fallahi, A.; Lifson, J.; Chaperot, L.; Plumas, J.; Bhardwaj, N. HIV-activated human plasmacytoid DCs induce Tregs through an indoleamine 2,3-dioxygenase-dependent mechanism. J. Clin. Invest., 2008, 118(10), 3431-3439.
97. Estes, J.D.; Li, Q.; Reynolds, M.R.; Wietgrefe, S.; Duan, L.; Schacker, T.; Picker, L.J.; Watkins, D.I.; Lifson, J.D.; Reilly, C.; Carlis, J.; Haase, A.T. Premature induction of an immunosuppressive regulatory T cell response during acute simian immunodeficiency virus infection. J. Infect. Dis., 2006, 193(5), 703-712. (Pubitemid 43271504)
98. Sallusto, F.; Lanzavecchia, A. Human Th17 cells in infection and autoimmunity. Microbes. Infect., 2009, 11(5), 620-624.
99. Iwakura, Y.; Nakae, S.; Saijo, S.; Ishigame, H. The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol. Rev., 2008, 226, 57-79.
100. Romani, L. Cell mediated immunity to fungi: a reassessment. Med. Mycol., 2008, 46(6), 515-529.
101. Zhou, L.; Littman, D.R. Transcriptional regulatory networks in Th17 cell differentiation. Curr. Opin. Immunol., 2009, 21(2), 146-152.
102. Baban, B.; Chandler, P.R.; Sharma, M.D.; Pihkala, J.; Koni, P.A.; Munn, D.H.; Mellor, A.L. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J. Immunol., 2009, 183(4), 2475-2483.
103. Sharma, M.D.; Hou, D.Y.; Liu, Y.; Koni, P.A.; Metz, R.; Chandler, P.; Mellor, A.L.; He, Y.; Munn, D.H. Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes. Blood, 2009, 113(24), 6102-6111.
104. Criado, G.; Simelyte, E.; Inglis, J.J.; Essex, D.; Williams, R.O. Indoleamine 2,3 dioxygenase-mediated tryptophan catabolism regulates accumulation of Th1/Th17 cells in the joint in collagen-induced arthritis. Arthritis Rheum, 2009, 60(5), 1342-1351.
105. Bonifazi, P.; Zelante, T.; D'Angelo, C.; De Luca, A.; Moretti, S.; Bozza, S.; Perruccio, K.; Iannitti, R.G.; Giovannini, G.; Volpi, C.; Fallarino, F.; Puccetti, P.; Romani, L. Balancing inflammation and tolerance in vivo through dendritic cells by the commensal Candida albicans. Mucosal. Immunol., 2009, 2(4), 362-374.
106. Romani, L.; Fallarino, F.; De Luca, A.; Montagnoli, C.; D'Angelo, C.; Zelante, T.; Vacca, C.; Bistoni, F.; Fioretti, M.C.; Grohmann, U.; Segal, B.H.; Puccetti, P. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature, 2008, 451(7175), 211-215.
107. Brenchley, J.M.; Paiardini, M.; Knox, K.S.; Asher, A.I.; Cervasi, B.; Asher, T.E.; Scheinberg, P.; Price, D.A.; Hage, C.A.; Kholi, L.M.; Khoruts, A.; Frank, I.; Else, J.; Schacker, T.; Silvestri, G.; Douek, D.C. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood, 2008, 112(7), 2826-2835.
108. Cecchinato, V.; Trindade, C.J.; Laurence, A.; Heraud, J.M.; Brenchley, J.M.; Ferrari, M.G.; Zaffiri, L.; Tryniszewska, E.; Tsai, W.P.; Vaccari, M.; Parks, R.W.; Venzon, D.; Douek, D.C.; O'Shea, J.J.; Franchini, G. Altered balance between Th17 and Th1 cells at mucosal sites predicts AIDS progression in simian immunodeficiency virus-infected macaques. Mucosal. Immunol., 2008, 1(4), 279-288. (Pubitemid 351850534)
109. Brenchley, J.M.; Price, D.A.; Douek, D.C. HIV disease: fallout from a mucosal catastrophe? Nat. Immunol., 2006, 7(3), 235-239.
110. Cecchinato, V.; Trindade, C.J.; Laurence, A.; Heraud, J.M.; Brenchley, J.M.; Ferrari, M.G.; Zaffiri, L.; Tryniszewska, E.; Tsai, W.P.; Vaccari, M.; Washington Parks, R.; Venzon, D.; Douek, D.C.; O'Shea, J.J.; Franchini, G. Altered balance between Th17 and Th1 cells at mucosal sites predicts AIDS progression in simian immunodeficiency virus-infected macaques. Mucosal. Immunol., 2008, 1, 279-288. (Pubitemid 351850534)
111. Li, Q.; Estes, J.D.; Schlievert, P.M.; Duan, L.; Brosnahan, A.J.; Southern, P.J.; Reilly, C.S.; Peterson, M.L.; Schultz-Darken, N.; Brunner, K.G.; Nephew, K.R.; Pambuccian, S.; Lifson, J.D.; Carlis, J.V.; Haase, A.T. Glycerol monolaurate prevents mucosal SIV transmission. Nature, 2009, 458(7241), 1034-1038.
112. Fauci, A.S.; Mavilio, D.; Kottilil, S. NK cells in HIV infection: paradigm for protection or targets for ambush. Nat. Rev. Immunol., 2005, 5(11), 835-843. (Pubitemid 41581665)
113. Frumento, G.; Rotondo, R.; Tonetti, M.; Damonte, G.; Benatti, U.; Ferrara, G.B. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J. Exp. Med., 2002, 196(4), 459-468.
114. Chiesa, M.D.; Carlomagno, S.; Frumento, G.; Balsamo, M.; Cantoni, C.; Conte, R.; Moretta, L.; Moretta, A.; Vitale, M. The tryptophan catabolite Lkynurenine inhibits the surface expression of NKp46- and NKG2Dactivating receptors and regulates NK-cell function. Blood, 2006, 108(13), 4118-4125. (Pubitemid 44913283)
115. Terness, P.; Bauer, T.M.; Rose, L.; Dufter, C.; Watzlik, A.; Simon, H.; Opelz, G. Inhibition of allogeneic T cell proliferation by indoleamine 2,3- dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J. Exp. Med., 2002, 196(4), 447-457.
116. De Milito, A. B lymphocyte dysfunctions in HIV infection. Curr. HIV Res., 2004, 2(1), 11-21. (Pubitemid 38854921)
117. Zandman-Goddard, G.; Shoenfeld, Y. HIV and autoimmunity. Autoimmun Rev., 2002, 1(6), 329-337. (Pubitemid 38340245)
118. Scott, G.N.; DuHadaway, J.; Pigott, E.; Ridge, N.; Prendergast, G.C.; Muller, A.J.; Mandik-Nayak, L. The immunoregulatory enzyme IDO paradoxically drives B cell-mediated autoimmunity. J. Immunol., 2009, 182(12), 7509-7517.
119. Nguyen, B.Y.; Reveille, J.D. Rheumatic manifestations associated with HIV in the highly active antiretroviral therapy era. Curr. Opin. Rheumatol., 2009, 21(4), 404-410.
120. Zack, J.A. The role of the cell cycle in HIV-1 infection. Adv. Exp. Med. Biol., 1995, 374, 27-31.