Antagonizing deactivating cytokines to enhance host defense and chemotherapy in experimental visceral leishmaniasis

Infection and Immunity

Volumn 73, Issue 7, 2005, Pages 3903-3911

  Murray, Henry W ^a   Flanders, Kathleen C ^b   Donaldson, Debra D ^c   Sypek, Joseph P ^c   Gotwals, Philip J ^d   Liu, Jianguo ^a   Ma, Xiaojing ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c PFIZER INC   (United States)

^d BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; ANTIMONY DERIVATIVE; CYTOKINE; GAMMA INTERFERON; HYBRID PROTEIN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA2 IMMUNOGLOBULIN FC FRAGMENT; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY INTERLEUKIN 10 RECEPTOR; MONOCLONAL ANTIBODY INTERLEUKIN 4; STIBOGLUCONATE SODIUM; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA II RECEPTOR IMMUNOGLOBULIN FC FRAGMENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE EXACERBATION; DRUG EFFICACY; DRUG TARGETING; FEMALE; GRANULOMA; HEPATITIS; HOST RESISTANCE; IMMUNE RESPONSE; LEISHMANIA DONOVANI; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TH1 CELL; VISCERAL LEISHMANIASIS;

ANIMALS; CYTOKINES; FEMALE; INTERLEUKIN-13; INTERLEUKIN-4; LEISHMANIASIS, VISCERAL; MICE; MICE, INBRED BALB C; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-10; TRANSFORMING GROWTH FACTOR BETA;

EID: 21544455224     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.7.3903-3911.2005     Document Type: Article

References (63)

1. Akhurst, R. J. 2002. TGF-β antagonists: why suppress a tumor suppressor? J. Clin. Investig. 109:1533-1536.
2. Alexander, J., K. C. Carter, N. Al-Fasi, A. Satoskar, and F. Brombacher. 2000. Endogenous IL-4 is necessary for effective drug therapy against visceral leishmaniasis. Eur. J. Immunol. 30:2935-2943.
3. Alexander, J. F. Brombacher, H. A. McGachy, A. N. McKenzie, W. Walker, and K. C. Carter. 2002. An essential role for IL-13 in maintaining a nonhealing response following Leishmania mexicana infection. Eur. J. Immunol. 32:2923-2933.
4. Babaloo, Z., P. M. Kaye, and M. B. Eslami. 2001. Interleukin-13 in Iranian patients with visceral leishmaniaisis: relationship to other Th2 and Th1 cytokines. Trans. R. Soc. Trop. Med. Hyg. 95:85-88.
5. Barral-Netto, M., A. Barral, C. E. Brownell, Y. A. W. Skeiky, L. R. Ellingsworth, D. R. Twardzik, and S. G. Reed. 1992. Transforming growth factor-β in leishmanial infection: a parasite escape mechanism. Science 257:545-548.
6. Bourreau, E., G. Prevot, R. Pradinaud, and P. Lainois. 2001. Interleukin (IL)-13 is the predominant Th2 cytokine in localized cutaneous leishmaniasis lesions and renders specific CD4+ T cells unresponsive to IL-12. J. Infect. Dis. 183:953-959.
7. Cenci, E., A. Mencacci, G. Del Sero, F. Bistoni, and L. Romani. 1997. Induction of protective Th1 responses to Candida albicans by antifungal therapy alone or in combination with an interleukin-4 antagonist. J. Infect. Dis. 176:217-226.
8. Chiaramonte, M. G., D. D. Donaldson, A. W. Cheever, and T. A. Wynn. 1999. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J. Clin. Investig. 104: 777-785.
9. deVries, J. E. 1998. The role of IL-13 and its receptor in allergy and inflammatory responses. J. Allergy Clin. Immunol. 102:165-169.
10. Ding, A., C. F. Nathan, J. Graycar, R. Derynck, D. J. Stuehr, and S. Srimal. 1990. Macrophage deactivating factor and transforming growth factors-β1, -β2 and -β3 inhibit induction of macrophage nitrogen oxide synthesis by IFN-γ. J. Immunol. 145:940-944.
11. Engwerda, C. R., M. L. Murphy, S. E. Cotterell, S. C. Smelt, and P. M. Kaye. 1998. Neutralization of IL-12 demonstrates the existence of discrete organ-specific phases in the control of Leishmania donovani. Eur. J. Immunol. 28:669-680.
12. Escobar, P., V. Yardley, and S. L. Croft. 2001. Activities of hexadecylphosphocholine (miltefosine), AmBisome, and sodium stibogluconate (Pentostam) against Leishmania donovani in immunodeficient scid mice. Antimicrob. Agents Chemother. 45:1872-1875.
13. Flanders, K. C., C. D. Sullivan, M. Fujii, A. Sowers, M. A. Anzano, A. Arabshabi, C. Major, J. B. Mitchell, and A. B. Roberts. 2002. Mice lacking Smad3 are protected against cutaneous injury induced by ionizing radiation. Am. J. Pathol. 160:1057-1068.
14. Gantt, K. R., S. Schulz-Cherry, N. Rodriguez, S. M. B. Jeronimo, E. T. Nascimento, T. L. Goldman, T. J. Recker, M. A. Miller, and M. E. Wilson. 2003. Activation of TGF-β by Leishmania chagasi: importance for parasite survival in macrophages. J. Immunol. 170:2613-2620.
15. Gassim, S., A. M. El-Hassan, E. A. G. Khalil, A. Ismail, A. M. Y. Kadarn, A. Kharazmi, and T. G. Theander. 1998. High levels of plasma IL-10 and expression of IL-10 by keratinocytes during visceral leishmaniasis predict subsequent development of post-kala-azar dermal leishmaniasis. Clin. Exp. Immunol. 111:64-69.
16. Ghosh, M., C. Pal, M. Ray, S. Maitra, L. Mandal, and S. Bandyopadhyay. 2003. Dendritic cell-based immunotherapy combined with antimony-based chemotherapy cures established murine visceral leishmaniasis. J. Immunol. 170:5625-5629.
17. Gomes-Pereira, S., O. R. Rodrigues, N. Rolao, P. D. Almeida, and G. M. Santos-Gomes. 2004. Hepatic cellular immune responses in mice with "cure" and "non-cure" phenotype to Leishmania infantum infection: importance of CD8+ T cells and TGF-β production. FEMS Immun. Med. Microbiol. 41:59-68.
18. Gorelik, L., and R. A. Flavell. 2002. Transforming growth factor-β in T cell biology. Nat. Rev. Immunol. 2:46-53.
19. Jones, D. E., L. V. Buxbaum, and P. Scott. 2000. IL-4-independent inhibition of IL-12 responsiveness during Leishmania amazonensis infection. J. Immunol. 165:364-372.
20. Karp, C. L., S. H. El-Safi, T. A. Wynn, M. M. H. Satti, A. N. Kordofani, F. A. Hashim, M. Hag-Ali, F. A. Neva, T. B. Nutman, and D. L. Sacks. 1993. In vivo cytokine profiles in patients with kala-azar. Marked elevation of both interleukin-10 and interferon-gamma. J. Clin. Investig. 91:1644-1648.
21. Kaye, P. M., M. Svensson, M. Ato, A. Maroof, R. Polley, S. Stager, S. Zubairi, and C. R. Engwerda. 2004. The immunopathology of experimental visceral leishmaniasis. Immunol. Rev. 201:239-253.
22. Kropf P., L. R. Schopf, C. L. Chung, D. Xu, F. Y. Liew, J. P. Sypek, and I. Muller. 1999. Expression of Th2 cytokines and the stable Th2 marker ST2L in the absence of IL-4 during Leishmania major infection. Eur. J. Immunol. 29:3621-3628.
23. Lehmann, J., K-H. Ensle, I. Lehmann, A. Emmendorfer, and M-L. Lohmann-Mattes. 2000. The capacity to produce IFN-γ rather than the presence of interleukin 4 determines the resistance and the degree of susceptibility to Leishmania donovani infection in mice. J. Interferon Cytokine Res. 20:63-77.
24. Li, J., C. A. Hunter, and J. P. Farrell. 1999. Anti-TGF-β treatment promotes rapid healing of Leishmania major infection in mice by enhancing in vivo nitric oxide production. J. Immunol. 162:974-979.
25. Matthews, D. J., C. L. Emson, G. J. McKenzie, H. E. Jolin, J. M. Blackwell, and A. N. J. McKenzie. 2000. IL-13 is a susceptibility factor for Leishmania major infection. J. Immunol. 164:1458-1462.
26. McKenzie, A. N. J., and P. G. Fallon. 2003. Decoy receptors in the regulation of T helper cell type 2 responses. J. Exp. Med. 197:675-679.
27. McMahon-Pratt, D., and J. Alexander. 2004. Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniases or the visceral disease? Immunol. Rev. 201:206-224.
28. Melby, P. C., A. Tabares, B. I. Restrepo, A. E. Cardona, H. S. McGruff, and J. M. Teale. 2001. Leishmania donovani: evolution and architecture of the splenic cellular immune response related to control of infection. Exp. Parasitol. 99:17-25.
29. Melby, P. C., B. Chandrasekar, W. Zhao, and J. E. Coe. 2001. The hamster as a model of human visceral leishmaniasis: progressive disease and impaired generation of nitric oxide in the face of a prominent Th1-like cytokine response. J. Immunol. 166:1912-1920.
30. Miralles, G. D., M. Y. Stoeckle, D. F. McDermott, F. D. Finkelman, and H. W. Murray. 1994. Induction of Th1 and Th2 cell-associated cytokines in experimental visceral leishmaniasis. Infect. Immun. 62:1058-1063.
31. Mohrs, M., B. Ledermann, G. Kohler, A. Dorfmuller, A. Gessner, and F. Brombacher. 1999. Differences between IL-4- and IL-4-receptor α-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J. Immunol. 162:7302-7308.
32. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
33. Mukherjee, P., A. K. Ghosh, and A. C. Ghose. 2003. Infection pattern and immune response in the spleen and liver of BALB/c mice intracardially infected with Leishmania donovani amastigotes. Immunol. Lett. 86:131-138.
34. Muraoka, R. S., N. Dumont, C. A. Ritter, T. C. Dugger, D. M. Brantley, J. Chen, E. Easterly, L. R. Roebuck, S. Ryan, P. J. Gotwals, V. Koteliansky, and C. L. Arteaga. 2002. Blockade of TGF-β inhibits mammary tumor cell viablity, migration, and metastases. J. Clin. Investig. 109:1551-1559.
35. Murphy, M. L., U. Wille, E. N. Villegas, C. A. Hunter, and J. P. Farrell. 2001. IL-10 mediates susceptibility to Leishmania donovani infection. Eur. J. Immunol. 31:2848-2856.
36. Murray, H. W., H. Masur, and J. S. Keithly. 1982. Cell-mediated immune response in experimental visceral leishmaniasis. I. Correlation between resistance to Leishmania donovani and lymphokine-generating capacity. J. Immunol. 129:344-350.
37. Murray, H. W., J. D. Berman, and S. D. Wright. 1988. Immunochemotherapy for intracellular Leishmania donovani infection: interferon-gamma plus pentavalent antimony. J. Infect. Dis. 157:973-978.
38. Murray, H. W., M. J. Oca, A. M. Granger, and R. D. Schreiber. 1989. Successful response to chemotherapy in experimental visceral leishmaniasis: requirement for T cells and effect of lymphokines. J. Clin. Investig. 83:1254-1259.
39. Murray, H. W., J. Hariprashad, and R. L. Coffman. 1997. Behavior of visceral Leishmania donovani in an experimentally-induced Th2 cell-associated response model. J. Exp. Med. 185:867-874.
40. Murray, H. W., and S. Delph-Etienne. 2000. Role of endogenous gamma interferon and macrophage microbicidal mechanisms in host response to chemotherapy in experimental visceral leishmaniasis. Infect. Immun. 68:288-293.
41. Murray, H. W., C. Montelibano, R. Peterson, J. P. Sypek. 2000. Interleukin 12 regulates the response to chemotherapy in experimental visceral leishmaniasis J. Infect. Dis. 182:1497-1503.
42. Murray, H. W., A. Jungbluth, E. Ritter, C. Montelibano, and M. W. Marino. 2000. Visceral leishmaniasis in mice devoid of tumor necrosis factor and response to treatment. Infect. Immun. 68:6289-6293.
43. Murray, H. W. 2001. Clinical and experimental advances in treatment in visceral leishmaniasis. Antimicrob. Agents Chemother. 45:2185-2197.
44. Murray, H. W. 2001. Tissue granuloma structure-function in experimental visceral leishmaniasis. Int. J. Exp. Pathol. 82:249-267.
45. Murray, H. W., C. M. Lu, S. Mauze, S. Freeman, A. L. Moreira, G. Kaplan, and R. L. Coffman. 2002. Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect. Immun. 70:6284-6293.
46. Murray, H. W., C. M. Lu, E. B. Brooks, R. E. Fichtl, J. L. DeVecchio, and F. P. Heinzel. 2003. Modulation of T-cell costimulation as immuno- or immunochemotherapy in experimental visceral leishmaniasis. Infect. Immun. 71:6453-6462.
47. Murray, H. W., A. L. Moreira, C. M. Lu, J. L. DeVecchio, M. Matsuhashi, X. Ma, and F. P. Heinzel. 2003. Determinants of response to interleukin 10 receptor blockade immunotherapy in experimental visceral leishmaniasis. J. Infect. Dis. 188:458-464.
48. Murray, H. W., E. B. Brooks, J. L. DeVecchio, and F. P. Heinzel. 2003. Immunoenhancement combined with amphotericin B as treatment in experimental visceral leishmaniasis. Antimicrob. Agents Chemother. 47:2513-2517.
49. Nabors, G. S. 1997. Modulating ongoing Th2-cell responses in experimental leishmaniasis. Parasitol. Today 13:76-79.
50. Noben-Trauth, N., R. Lira, H. Nagase, W. E. Paul, and D. L. Sacks. 2003. The relative contribution of IL-4 receptor signaling and IL-10 to susceptibility to Leishmania major. J. Immunol. 170:5152-5158.
51. Powrie, F., S. Menon, and R. L. Coffman. 1993. IL-4 and IL-10 synergize to inhibit cell-mediated immunity in vivo. Eur. J. Immunol. 23:2223-2229.
52. Reed, S. G. 1999. TGF-β in infections and infectious diseases. Microbes Infect. 1:1313-1325.
53. Reiner, S. L., and R. M. Locksley. 1995. The regulation of immunity to Leishmania major. Annu. Rev. Immunol. 13:151-177.
54. Satoskar, A. R., S. Rodig, S. R. Telford, A. A. Satoskar, S. K. Ghosh, F. von Lichtenberg, and J. R. David. 2000. IL-12 gene-deficient C57BL/6 mice are susceptible to Leishmania donovani but have diminshed hepatic pathology. Eur. J. Immunol. 30:834-839.
55. Schmidt-Weber, C. B., and K. Blaser. 2004. Regulation and role of transforming growth factor-β in immune tolerance induction and inflammation. Curr. Opin. Immunol. 16:709-716.
56. Sosa, M. R., L. E. Rosas, A. N. J. McKenzie, and A. R. Satoskar. 2001. IL-13 gene-deficient mice are susceptible to cutaneous Leishmania mexicana infection. Eur. J. Immunol. 31:3255-3260.
57. Stager, S., J. Alexander, K. C. Carter, F. Brombacher, and P. M. Kaye. 2003. Both interleukin-4 (IL-4) and IL-4 receptor α signaling contribute to the development of hepatic granulomas with optimal antileishmanial activity. Infect. Immun. 71:4804-4807.
58. Sundar, S., S. G. Reed, S. Sharma, A. Mehrota, and H. W. Murray. 1997. Circulating Th1 cell- and Th2 cell-associated cytokines in Indian patients with visceral leishmaniasis. Am. J. Trop. Med. Hyg. 56:522-525.
59. Tumang, M. C. T., C. Keogh, L. L. Moldawer, D. C. Helfgott, R. Teitelbaum, J. Hariprashad, and H. W. Murray. 1994. Role and effect of TNF-α in experimental visceral leishmaniasis. J. Immunol. 153:768-775.
60. Wilson, M. E., B. M. Young, B. L. Davidson, K. A. Mente, and S. E. McGowan. 1998. The importance of TGF-β in murine visceral leishmaniasis. J. Immunol. 161:6148-6155.
61. Wilson, M. E., T. J. Recker, N. E. Rodriguez, B. M. Young, K. K. Burnell, J. A. Streit, and J. N. Kline. 2002. The TGF-β response to Leishmania chagasi in the absence of IL-12. Eur. J. Immunol. 32:3556-3565.
62. Wood, N., M. J. Whitters, B. A. Jacobson, J. Witek, J. P. Sypek, M. Kasaian, M. J. Eppihimer, M. Unger, T. Tanaka, S. J. Goldman, M. Collins, D. D. Donaldson, and M. J. Grusby. 2003. Enhanced interleukin (IL)-13 responses in mice lacking IL-13 receptor α2. J. Exp. Med. 197:703-709.
63. Zubairi, S., S. L. Sanos, S. Hill, and P. M. Kaye. 2004. Immunotherapy with OX40L-Fc or anti-CTLA-4 enhances local tissue responses and killing of Leishmania donovani. Eur. J. Immunol. 34:1-8.