The Schistosoma mansoni hepatic egg granuloma provides a favorable microenvironment for sustained growth of Leishmania donovani

American Journal of Pathology

Volumn 169, Issue 3, 2006, Pages 943-953

  Hassan, Mohammed F ^a   Zhang, Yaobi ^a   Engwerda, Christian R ^a   Kaye, Paul M ^a   Sharp, Hannah ^a   Bickle, Quentin D ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EGG; FEMALE; GRANULOMA; LEISHMANIA DONOVANI; LIVER; MICROENVIRONMENT; MOUSE; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SPLEEN;

EID: 33748854303     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.051319     Document Type: Article

References (77)

1. Hoogstraal H, Heyneman D: Leishmaniais in the Sudan Republic. 30. Final epidemiological report. Am J Trop Med Hyg 1969, 18:1091-1210
2. el Gaddal AA: The Blue Nile Health Project: a comprehensive approach to the prevention and control of water-associated diseases in irrigated schemes of the Sudan. J Trop Med Hyg 1985, 88:47-56
3. Zijlstra EE, Ali MS, el-Hassan AM, el-Toum IA, Satti M, Ghalib HW, Sondorp E, Winkler A: Kala-azar in displaced people from southern Sudan: epidemiological, clinical and therapeutic findings. Trans R Soc Trop Med Hyg 1991, 85:365-369
4. Pearce EJ, C MK, Sun J, Taylor JJ, McKee AS, Cervi L: Th2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunol Rev 2004, 201:117-126
5. Murray HW: Tissue granuloma structure-function in experimental visceral leishmaniasis. Int J Exp Pathol 2001, 82:249-267
6. Alvar J, Canavate C, Gutierrez-Solar B, Jimenez M, Laguna F, Lopez-Velez R, Molina R, Moreno J: Leishmania and human immunodeficiency virus coinfection: the first 10 years. Clin Microbiol Rev 1997, 10:298-319
7. Kaye PM, Svensson M, Ato M, Maroof A, Polley R, Stager S, Zubairi S, Engwerda CR: The immunopathology of experimental visceral leishmaniasis. Immunol Rev 2004, 201:239-253
8. Bacellar O, Barral-Netto M, Badaro R, Carvalho EM: Gamma interferon production by lymphocytes from children infected with L. chagasi. Braz J Med Biol Res 1991, 24:791-795
9. Carvalho EM, Barral A, Pedral-Sampaio D, Barral-Netto M, Badaro R, Rocha H, Johnson Jr WD: Immunologic markers of clinical evolution in children recently infected with Leishmania donovani chagasi. J Infect Dis 1992, 165:535-540
10. Ghalib HW, Piuvezam MR, Skeiky YA, Siddig M, Hashim FA, el-Hassan AM, Russo DM, Reed SG: Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J Clin Invest 1993, 92:324-329
11. Carvalho EM, Bacellar O, Brownell C, Regis T, Coffman RL, Reed SG: Restoration of IFN-gamma production and lymphocyte proliferation in visceral leishmaniasis. J Immunol 1994, 152:5949-5956
12. Bacellar O, Brodskyn C, Guerreiro J, Barral-Netto M, Costa CH, Coffman RL, Johnson WD, Carvalho EM: Interleukin-12 restores interferon-gamma production and cytotoxic responses in visceral leishmaniasis. J Infect Dis 1996, 173:1515-1518
13. Ghalib HW, Whittle JA, Kubin M, Hashim FA, el-Hassan AM, Grabstein KH, Trinchieri G, Reed SG: IL-12 enhances Th1-type responses in human Leishmania donovani infections. J Immunol 1995, 154:4623-4629
14. Carvalho EM, Badaro R, Reed SG, Jones TC, Johnson Jr WD: Absence of gamma interferon and interleukin 2 production during active visceral leishmaniasis. J Clin Invest 1985, 76:2066-2069
15. Murray HW, Hariprashad J, Coffman RL: Behavior of visceral Leishmania donovani in an experimentally induced T helper cell 2 (Th2)-associated response model. J Exp Med 1997, 185:867-874
16. Murphy ML, Wille U, Villegas EN, Hunter CA, Farrell JP: IL-10 mediates susceptibility to Leishmania donovani infection. Eur J Immunol 2001, 31:2848-2856
17. Murray HW, Lu CM, Mauze S, Freeman S, Moreira AL, Kaplan G, Coffman RL: Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect Immun 2002, 70:6284-6293
18. Pearce EJ, Caspar P, Grzych JM, Lewis FA, Sher A: Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med 1991, 173:159-166
19. Grzych JM, Pearce E, Cheever A, Caulada ZA, Caspar P, Heiny S, Lewis F, Sher A: Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. J Immunol 1991, 146:1322-1327
20. Wynn TA, Eltoum I, Cheever AW, Lewis FA, Gause WC, Sher A: Analysis of cytokine mRNA expression during primary granuloma formation induced by eggs of Schistosoma mansoni. J Immunol 1993, 151:1430-1440
21. Araujo MI, de Jesus AR, Bacellar O, Sabin E, Pearce E, Carvalho EM: Evidence of a T helper type 2 activation in human schistosomiasis. Eur J Immunol 1996, 26:1399-1403
22. de Jesus AR, Magalhaes A, Miranda DG, Miranda RG, Araujo MI, de Jesus AA, Silva A, Santana LB, Pearce E, Carvalho EM: Association of type 2 cytokines with hepatic fibrosis in human Schistosoma mansoni infection. Infect Immun 2004, 72:3391-3397
23. Okano M, Satoskar AR, Nishizaki K, Abe M, Harn Jr DA: Induction of Th2 responses and IgE is largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens. J Immunol 1999, 163:6712-6717
24. MacDonald AS, Straw AD, Bauman B, Pearce EJ: CD8-dendritic cell activation status plays an integral role in influencing Th2 response development. J Immunol 2001, 167:1982-1988
25. Chiaramonte MG, Schopf LR, Neben TY, Cheever AW, Donaldson DD, Wynn TA: IL-13 is a key regulatory cytokine for Th2 cell-mediated pulmonary granuloma formation and IgE responses induced by Schistosoma mansoni eggs. J Immunol 1999, 162:920-930
26. Dessein AJ, Hillaire D, Elwali NE, Marquet S, Mohamed-Ali Q, Mirghani A, Henri S, Abdelhameed AA, Saeed OK, Magzoub MM, Abel L: Severe hepatic fibrosis in Schistosoma mansoni infection is controlled by a major locus that is closely linked to the interferon-gamma receptor gene. Am J Hum Genet 1999, 65:709-721
27. Wynn TA, Eltoum I, Oswald IP, Cheever AW, Sher A: Endogenous interleukin 12 (IL-12) regulates granuloma formation induced by eggs of Schistosoma mansoni and exogenous IL-12 both inhibits and prophylactically immunizes against egg pathology. J Exp Med 1994, 179:1551-1561
28. Henri S, Chevillard C, Mergani A, Paris P, Gaudart J, Camilla C, Dessein H, Montera F, Elwali NE, Saeed OK, Magzoub M, Dessein AJ: Cytokine regulation of periportal fibrosis in humans infected with Schistosoma mansoni: IFN-gamma is associated with protection against fibrosis and TNF-alpha with aggravation of disease. J Immunol 2002, 169:929-936
29. Brunet LR, Finkelman FD, Cheever AW, Kopf MA, Pearce EJ: IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. J Immunol 1997, 159:777-785
30. Herbert DR, Holscher C, Mohrs M, Arendse B, Schwegmann A, Radwanska M, Leeto M, Kirsch R, Hall P, Mossmann H, Claussen B, Forster I, Brombacher F: Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 2004, 20:623-635
31. Hoffmann KF, Cheever AW, Wynn TA: IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J Immunol 2000, 164:6406-6416
32. Sher A, Fiorentino D, Caspar P, Pearce E, Mosmann T: Production of IL-10 by CD4+ T lymphocytes correlates with down-regulation of Th1 cytokine synthesis in helminth infection. J Immunol 1991, 147:2713-2716
33. King CL, Medhat A, Malhotra I, Nafeh M, Helmy A, Khaudary J, Ibrahim S, El-Sherbiny M, Zaky S, Stupi RJ, Brustoski K, Shehata M, Shata MT: Cytokine control of parasite-specific anergy in human urinary schistosomiasis. IL-10 modulates lymphocyte reactivity. J Immunol 1996, 156:4715-4721
34. Wynn TA, Cheever AW, Williams ME, Hieny S, Caspar P, Kuhn R, Muller W, Sher A: IL-10 regulates liver pathology in acute murine Schistosomiasis mansoni but is not required for immune down-modulation of chronic disease. J Immunol 1998, 160:4473-4480
35. Sadler CH, Rutitzky LI, Stadecker MJ, Wilson RA: IL-10 is crucial for the transition from acute to chronic disease state during infection of mice with Schistosoma mansoni. Eur J Immunol 2003, 33:880-888
36. Flores-Villanueva PO, Zheng XX, Strom TB, Stadecker MJ: Recombinant IL-10 and IL-10/Fc treatment down-regulate egg antigen-specific delayed hypersensitivity reactions and egg granuloma formation in schistosomiasis. J Immunol 1996, 156:3315-3320
37. Sabin EA, Araujo MI, Carvalho EM, Pearce EJ: Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J Infect Dis 1996, 173:269-272
38. Cooke A, Tonks P, Jones FM, O'Shea H, Hutchings P, Fulford AJ, Dunne DW: Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol 1999, 21:169-176
39. Sewell D, Qing Z, Reinke E, Elliot D, Weinstock J, Sandor M, Fabry Z: Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol 2003, 15:59-69
40. Cox FE: Concomitant infections, parasites and immune responses. Parasitology 2001, 122:323-338
41. La Flamme AC, Scott P, Pearce EJ: Schistosomiasis delays lesion resolution during Leishmania major infection by impairing parasite killing by macrophages. Parasite Immunol 2002, 24:339-345
42. Madwar MA, el Tahawy M, Strickland GT: The relationship between uncomplicated schistosomiasis and hepatitis B infection. Trans R Soc Trop Med Hyg 1989, 83:233-236
43. Kamal S, Madwar M, Bianchi L, Tawil AE, Fawzy R, Peters T, Rasenack JW: Clinical, virological and histopathologioal features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver 2000, 20:281-289
44. Kamal SM, Rasenack JW, Bianchi L, Al Tawil A, El Sayed Khalifa K, Peter T, Mansour H, Ezzat W, Koziel M: Acute hepatitis C without and with schistosomiasis: correlation with hepatitis C-specific CD4(+) T-cell and cytokine response. Gastroenterology 2001, 121:646-656
45. Kamal SM, Graham CS, He Q, Bianchi L, Tawil AA, Rasenack JW, Khalifa KA, Massoud MM, Koziel MJ: Kinetics of intrahepatic hepatitis C virus (HCV)-specific CD4+ T cell responses in HCV and Schistosoma mansoni coinfection: relation to progression of liver fibrosis. J Infect Dis 2004, 189:1140-1150
46. Actor JK, Shirai M, Kullberg MC, Buller RM, Sher A, Berzofsky JA: Helminth infection results in decreased virus-specific CD8+ cytotoxic T-cell and Th1 cytokine responses as well as delayed virus clearance. Proc Natl Acad Sci USA 1993, 90:948-952
47. Edwards MJ, Buchatska O, Ashton M, Montoya M, Bickle QD, Borrow P: Reciprocal immunomodulation in a schistosome and hepatotropic virus coinfection model. J Immunol 2005, 175:6275-6285
48. Actor JK, Marshall MA, Eltoum IA, Buller RM, Berzofsky JA, Sher A: Increased susceptibility of mice infected with Schistosoma mansoni to recombinant vaccinia virus: association of viral persistence with egg granuloma formation. Eur J Immunol 1994, 24:3050-3056
49. Smithers SR, Terry RJ: The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 1965, 55:695-700
50. Kaye PM, Curry AJ, Blackwell JM: Differential production of Th1- and Th2-derived cytokines does not determine the genetically controlled or vaccine-induced rate of cure in murine visceral leishmaniasis. J Immunol 1991, 146:2763-2770
51. Doenhoff M, Bickle Q, Long E, Bain J, McGregor A: Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. I. Demonstration of resistance to reinfection using a model system that involves perfusion of mice within three weeks of challenge. J Helminthol 1978, 52:173-186
52. Engwerda CR, Murphy ML, Cotterell SE, Smelt SC, Kaye PM: Neutralization of IL-12 demonstrates the existence of discrete organ-specific phases in the control of Leishmania donovani. Eur J Immunol 1998, 28:669-680
53. Stauber L: Host resistance to the genus Leishmania. Rice Inst Pamph 1958, 45:80-96
54. McElrath MJ, Murray HW, Cohn ZA: The dynamics of granuloma formation in experimental visceral leishmaniasis. J Exp Med 1988, 167:1927-1937
55. Murphy ML, Cotterell SE, Gorak PM, Engwerda CR, Kaye PM: Blockade of CTLA-4 enhances host resistance to the intracellular pathogen, Leishmania donovani. J Immunol 1998, 161:4153-4160
56. Taylor AP, Murray HW: Intracellular antimicrobial activity in the absence of interferon-gamma: effect of interleukin-12 in experimental visceral leishmaniasis in interferon-gamma gene-disrupted mice. J Exp Med 1997, 185:1231-1239
57. Engwerda CR, Ato M, Stager S, Alexander CE, Stanley AC, Kaye PM: Distinct roles for lymphotoxin-alpha and tumor necrosis factor in the control of Leishmania donovani infection. Am J Pathol 2004, 165:2123-2133
58. Stein M, Keshav S, Harris N, Gordon S: Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 1992, 176:287-292
59. Linehan SA, Coulson PS, Wilson RA, Mountford AP, Brombacher F, Martinez-Pomares L, Gordon S: IL-4 receptor signaling is required for mannose receptor expression by macrophages recruited to granulomata but not resident cells in mice infected with Schistosoma mansoni. Lab Invest 2003, 83:1223-1231
60. Murray HW, Nathan CF: Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. J Exp Med 1999, 189:741-746
61. Hirata M, Hirata K, Kage M, Zhang M, Hara T, Fukuma T: Effect of nitric oxide synthase inhibition on Schistosoma japonicum egg-induced granuloma formation in the mouse liver. Parasite Immunol 2001, 23:281-289
62. Abbas AK, Murphy KM, Sher A: Functional diversity of helper T lymphocytes. Nature 1996, 383:787-793
63. Engwerda CR, Kaye PM: Organ-specific immune responses associated with infectious disease. Immunol Today 2000, 21:73-78
64. Squires KE, Schreiber RD, McElrath MJ, Rubin BY, Anderson SL, Murray HW: Experimental visceral leishmaniasis: role of endogenous IFN-gamma in host defense and tissue granulomatous response. J Immunol 1989, 143:4244-4249
65. Murray HW, Squires KE, Miralles CD, Stoeckle MY, Granger AM, Granelli-Piperno A, Bogdan C: Acquired resistance and granuloma formation in experimental visceral leishmaniasis. Differential T cell and lymphokine roles in initial versus established immunity. J Immunol 1992, 148:1858-1863
66. Tumang MC, Keogh C, Moldawer LL, Helfgott DC, Teitelbaum R, Hariprashad J, Murray HW: Role and effect of TNF-alpha in experimental visceral leishmaniasis. J Immunol 1994, 153:768-775
67. Bogdan C: Nitric oxide and the immune response. Nat Immunol 2001, 2:907-916
68. Weinstock JV, Boros DL: Organ-dependent differences in composition and function observed in hepatic and intestinal granulomas isolated from mice with Schistosomiasis mansoni. J Immunol 1983, 130:418-422
69. King CL, Xianli J, Stavitsky AB: Murine schistosomiasis mansoni: coordinate cytokine regulation and differences in cellular immune responses of granuloma cells and splenocytes to endogenous and exogenous schistosome egg antigens. Parasite Immunol 2001, 23:607-615
70. Hesse M, Piccirillo CA, Belkaid Y, Prufer J, Mentink-Kane M, Leusink M, Cheever AW, Shevach EM, Wynn TA: The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J Immunol 2004, 172:3157-3166
71. Stadecker MJ, Kamisato JK, Chikunguwo SM: Induction of T helper cell unresponsiveness to antigen by macrophages from schistosomal egg granulomas. A basis for immunomodulation in schistosomiasis? J Immunol 1990, 145:2697-2700
72. Flores Villanueva PO, Harris TS, Ricklan DE, Stadecker MJ: Macrophages from schistosomal egg granulomas induce unresponsiveness in specific cloned Th-1 lymphocytes in vitro and down-regulate schistosomal granulomatous disease in vivo. J Immunol 1994, 152:1847-1855
73. Hesse M, Modolell M, La Flamme AC, Schito M, Fuentes JM, Cheever AW, Pearce EJ, Wynn TA: Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J Immunol 2001, 167:6533-6544
74. La Flamme AC, Patton EA, Bauman B, Pearce EJ: IL-4 plays a crucial role in regulating oxidative damage in the liver during schistosomiasis. J Immunol 2001, 166:1903-1911
75. Iniesta V, Gomez-Nieto LC, Corraliza I: The inhibition of arginase by N(omega)-hydroxy-1-arginine controls the growth of Leishmania inside macrophages. J Exp Med 2001, 193:777-784
76. Iniesta V, Gomez-Nieto LC, Molano I, Mohedano A, Carcelen J, Miron C, Alonso C, Corraliza I: Arginase I induction in macrophages, triggered by Th2-type cytokines, supports the growth of intracellular Leishmania parasites. Parasite Immunol 2002, 24:113-118
77. Mukhopadhyay R, Madhubala R: Leishmania donovani: cellular control of ornithine decarboxylase in promastigotes. Int J Biochem Cell Biol 1995, 27:947-952