The role of indoleamine 2, 3-dioxygenase in lepromatous leprosy immunosuppression

Clinical and Experimental Immunology

Volumn 165, Issue 2, 2011, Pages 251-263

  de Souza Sales, J ^a   Lara, F A ^a   Amadeu, T P ^a   de Oliveira Fulco, T ^a   da Costa Nery, J A ^a   Sampaio, E P ^a,b   Pinheiro, R O ^a   Sarno, E N ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

IDO; IFN ; Lepromatous leprosy; Monocytes; Mycobacterium leprae

Indexed keywords

CD14 ANTIGEN; CD68 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; N METHYLTRYPTOPHAN;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME ACTIVITY; ENZYME SYNTHESIS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOSUPPRESSIVE TREATMENT; LEPROMATOUS LEPROSY; MACROPHAGE; MAJOR CLINICAL STUDY; MONOCYTE; MYCOBACTERIUM LEPRAE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; SKIN BIOPSY; WESTERN BLOTTING;

ANTIGENS, CD; ANTIGENS, CD14; ANTIGENS, CD86; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BLOTTING, WESTERN; CELLS, CULTURED; DENDRITIC CELLS; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNE TOLERANCE; IMMUNOBLOTTING; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-GAMMA; LEPROSY, LEPROMATOUS; LEPROSY, TUBERCULOID; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; MONOCYTES; MYCOBACTERIUM LEPRAE; POLYMERASE CHAIN REACTION; SKIN; TRYPTOPHAN;

EID: 79960043535     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2011.04412.x     Document Type: Article

References (59)

1. Kaplan G, Weinstein DE, Steinman RM etal. An analysis of in vitro T cell responsiveness in lepromatous leprosy. J Exp Med 1985; 162:917-29.
2. Sieling PA, Abrams JS, Yamamura M etal. Immunosuppressive roles for IL-10 and IL-4 in human infection. In vitro modulation of T cell responses in leprosy. J Immunol 1993; 150:5501-10.
3. Barnes PF, Abrams JS, Lu S, Sieling PA, Rea TH, Modlin RL. Patterns of cytokine production by mycobacterium-reactive human T-cell clones. Infect Immun 1993; 61:197-203.
4. Modlin RL, Mehra V, Wong L etal. Suppressor T lymphocytes from lepromatous leprosy skin lesions. J Immunol 1986; 137:2831-4.
5. Yamamura M, Uyemura K, Deans RJ etal. Defining protective responses to pathogens: cytokine profiles in leprosy lesions. Science 1991; 254:277-9.
6. Laal S, Bhutani LK, Nath I. Natural emergence of antigen-reactive T cells in lepromatous leprosy patients during erythema nodosum leprosum. Infect Immun 1985; 50:887-92.
7. Moraes MO, Sarno EN, Almeida AS etal. Cytokine mRNA expression in leprosy: a possible role for interferon-gamma and interleukin-12 in reactions (RR and ENL). Scand J Immunol 1999; 50:541-9.
8. Moura DF, Teles RM, Ribeiro-Carvalho MM etal. Long-Term culture of multibacillary leprosy macrophages isolated from skin lesions: a new model to study Mycobacterium leprae-human cell interation. Br J Dermatol 2007; 157:273-83.
9. Nath I, Vemuri N, Reddi AL etal. The effect of antigen presenting cells on the cytokine profiles of stable and reactional lepromatous leprosy patients. Immunol Lett 2000; 75:69-76.
10. Hume DA. Differentiation and heterogeneity in the mononuclear phagocyte system. Mucosal Immunol 2008; 1:432-41.
11. Hume DA. Macrophages as APC and the dendritic cell myth. J Immunol 2008; 181:5829-35.
12. Sampaio EP, Moreira AL, Sarno EN, Malta AM, Kaplan G. Prolonged treatment with recombinant interferon gamma induces erythema nodosum leprosum in lepromatous leprosy patients. J Exp Med 1992; 175:1729-37.
13. Kaplan G, Nusrat A, Sarno EN etal. Cellular responses to the intradermal injection of recombinant human gamma-interferon in lepromatous leprosy patients. Am J Pathol 1987; 128:345-53.
14. Alcaïs A, Sanchez FO, Thuc NV etal. Granulomatous reaction to intradermal injection of lepromin (Mitsuda reaction) is linked to the human NRAMP1 gene in Vietnamese leprosy sibships. J Infect Dis 2000; 181:302-8.
15. Moraes MO, Duppre NC, Suffys PN etal. Tumor necrosis factor-alpha promoter polymorphism TNF2 is associated with a stronger delayed-type hypersensitivity reaction in the skin of borderline tuberculoid leprosy patients. Immunogenetics 2001; 53:45-7.
16. Salgame PR, Birdi TJ, Mahadevan PR, Antia NH. Role of macrophages in defective cell mediated immunity in lepromatous leprosy. I. Factor(s) from macrophages affecting protein synthesis and lymphocyte transformation. Int J Lepr Other Mycobact Dis 1980; 48:172-7.
17. Mattos KA, D'Avila H, Rodrigues LS etal. Lipid droplet formation in leprosy: toll-like receptor-regulated organelles involved in eicosanoid formation and Mycobacterium leprae pathogenesis. J Leukoc Biol 2010; 87:371-84.
18. Kiszewski AE, Becerril E, Baquera J, Ruiz-Maldonado R, Hernández Pando R. Expression of cyclooxygenase type 2 in lepromatous and tuberculoid leprosy lesions. Br J Dermatol 2003; 148:795-8.
19. Katz JB, Muller AJ, Prendergast GC. Indoleamine 2, 3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol Rev 2008; 222:206-21.
20. Munn DH, Mellor AL. Macrophages and the regulation of self-reactive T cells. Curr Pharm Des 2003; 9:257-64.
21. Fallarino F, Grohmann U, Vacca C etal. T cell apoptosis by kynurenines. Adv Exp Med Biol 2003; 527:183-90.
22. Fallarino F, Grohmann U, Vacca C etal. T cell apoptosis by tryptophan catabolism. Cell Death Differ 2002; 9:1069-77.
23. Savage ND, de Boer T, Walburg KV etal. Human anti-inflammatory macrophages induce Foxp3+ GITR+ CD25+ regulatory T cells, which suppress via membrane-bound TGFbeta-1. J Immunol 2008; 181:2220-6.
24. Ribas A, Comin-Anduix B, Economou JS etal. Intratumoral immune cell infiltrates, FoxP3, and indoleamine 2, 3-dioxygenase in patients with melanoma undergoing CTLA4 blockade. Clin Cancer Res 2009; 15:390-9.
25. Däubener W, Spors B, Hucke C etal. Restriction of Toxoplasma gondii growth in human brain microvascular endothelial cells by activation of indoleamine 2, 3-dioxygenase. Infect Immun 2001; 69:6527-31.
26. Popov A, Abdullah Z, Wickenhauser C etal. Indoleamine 2, 3-dioxygenase-expressing dendritic cells form suppurative granulomas following Listeria monocytogenes. J Clin Invest 2006; 116:3160-70.
27. Munn DH, Zhou M, Attwood JT etal. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998; 281:1191-3.
28. Munn DH, Mellor AL. Indoleamine 2, 3-dioxygenase and tumor-induced tolerance. J Clin Invest 2007; 117:1147-54.
29. Cole ST, Eiglmeier K, Parkhill J etal. Massive gene decay in the leprosy bacillus. Nature 2001; 409:1007-11.
30. Zganiacz A, Santosuosso M, Wang J etal. TNF-alpha is a critical negative regulator of type 1 immune activation during intracellular bacterial infection. J Clin Invest 2004; 113:401-13.
31. Muller AJ, Sharma MD, Chandler PR etal. Chronic inflammation that facilitates tumor progression creates local immune suppression by inducing indoleamine 2, 3 dioxygenase. Proc Natl Acad Sci USA 2008; 105:17073-8.
32. Prendergast GC, Metz R, Muller AJ. Towards a genetic definition of cancer-associated inflammation: role of the IDO pathway. Am J Pathol 2010; 176:2082-7.
33. Ridley DS, Jopling WH. Classification of leprosy according to immunity. A five-group system. Int J Lepr Other Mycobact Dis 1966; 34:255-73.
34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 2001; 25:402-8.
35. Widner B, Werner ER, Schennach H, Wachter H, Fuchs D. Simultaneous measurement of serum tryptophan and kynurenine by HPLC. Clin Chem 1997; 43:2424-6.
36. Scheinman RI, Cogswell PC, Lofquist AK, Baldwin AS. Role of transcriptional activation of I kappa B alpha in mediation of immunosuppression by glucocorticoids. Science 1995; 270:283-6.
37. O'Connor JC, André C, Wang Y etal. Interferon-gamma and tumor necrosis factor-alpha mediate the upregulation of indoleamine 2, 3-dioxygenase and the induction of depressive-like behavior in mice in response to bacillus Calmette-Guerin. J Neurosci 2009; 29:4200-9.
38. Hernandez MO, Neves I, Sales JS, Carvalho DS, Sarno EN, Sampaio EP. Induction of apoptosis in monocytes by Mycobacterium leprae in vitro: a possible role for tumour necrosis factor-alpha. Immunology 2003; 109:156-64.
39. Fulco TO, Lopes UG, Sarno EN, Sampaio EP, Saliba AM. The proteasome function is required for Mycobacterium leprae-induced apoptosis and cytokine secretion. Immunol Lett 2007; 110:82-5.
40. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008; 8:958-69.
41. Zhang FR, Huang W, Chen SM etal. Genomewide association study of leprosy. N Engl J Med 2009; 361:2609-18.
42. Krutzik SR, Tan B, Li H etal. TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat Med 2005; 11:653-60.
43. Scheler M, Wenzel J, Tüting T, Takikawa O, Bieber T, von Bubnoff D. Indoleamine 2, 3 dioxygenase (IDO): the antagonist of type I interferon-driven skin inflammation? Am J Pathol 2007; 171:1936-43.
44. Popov A, Schultze JL. IDO-expressing regulatory dendritic cells in cancer and chronic infection. J Mol Med 2008; 86:145-60.
45. Zelante T, Fallarino F, Bistoni F, Puccetti P, Romani L. Indoleamine 2, 3-dioxygenase in infection: the paradox of an evasive strategy that benefits the host. Microbes Infect 2009; 11:133-41.
46. Walker SL, Lockwood DN. Leprosy type 1 (reversal) reactions and their management. Lepr Rev 2008; 79:372-86.
47. Becerra A, Warke RV, Xhaja K etal. Increased activity of indoleamine 2, 3-dioxygenase in serum from acutely infected dengue patients linked to gamma interferon antiviral function. J Gen Virol 2009; 90:810-17.
48. Löb S, Königsrainer A, Zieker D etal. IDO1 and IDO2 are expressed in human tumors: levo-but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol Immunother 2009; 58:153-7.
49. Sun Y. Indoleamine 2, 3-dioxygenase - a new antioxidant enzyme. Mater Med Pol 1989; 21:244-50.
50. Hayaishi O. Utilization of superoxide anion by indoleamine oxygenase-catalyzed tryptophan and indoleamine oxidation. Adv Exp Med Biol 1996; 398:285-9.
51. Tattevin P, Monnier D, Tribut O etal. Enhanced indoleamine 2, 3-dioxygenase activity in patients with severe sepsis and septic shock. J Infect Dis 2010; 201:956-66.
52. Lee SS, Gao W, Mazzola S etal. Heme oxygenase-1, carbon monoxide, and bilirubin induce tolerance in recipients toward islet allografts by modulating T regulatory cells. FASEB J 2007; 21:3450-7.
53. Xu H, Zhang G, Ciric B, Rostami A. IDO: a double-edged sword for T(H)1/T(H)2 regulation. Immunol Lett 2008; 121:1-6.
54. Thomas SR, Terentis AC, Cai H etal. Post-translational regulation of human indoleamine 2, 3-dioxygenase activity by nitric oxide. J Biol Chem 2007; 282:23778-87.
55. Anderson P. Post-transcriptional control of cytokine production. Nat Immunol 2008; 9:353-9.
56. Knubel CP, Martínez FF, Fretes RE etal. Indoleamine 2, 3-dioxigenase (IDO) is critical for host resistance against Trypanosoma cruzi. FASEB J 2010; 24:2689-701.
57. Manéglier B, Malleret B, Guillemin GJ etal. Modulation of indoleamine-2, 3-dioxygenase expression and activity by HIV-1 in human macrophages. Fundam Clin Pharmacol 2009; 23:573-81.
58. Romani L, Zelante T, De Luca A, Fallarino F, Puccetti P. IL-17 and therapeutic kynurenines in pathogenic inflammation to fungi. J Immunol 2008; 180:5157-62.
59. Soliman HH, Antonia S, Sullivan D, Vahanian N, Link C. Overcoming tumor antigen anergy in human malignancies using the novel indeolamine 2, 3 dioxygenase (IDO) enzyme inhibitor, 1-methyl-D-tryptophan (1MT). J Clin Oncol 2009; 27:15s.