Novel Program of Macrophage Gene Expression Induced by Phagocytosis of Leishmania chagasi

Infection and Immunity

Volumn 72, Issue 4, 2004, Pages 2111-2122

  Rodriguez, Nilda E ^a   Chang, Haeok K ^b   Wilson, Mary E ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; BACTERIUM LIPOPOLYSACCHARIDE; BIOLOGICAL MARKER; CYTOKINE; GAMMA INTERFERON; GENE PRODUCT; INTERLEUKIN 10; RECEPTOR; RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOASSAY; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; ENVIRONMENT; GENE EXPRESSION; GENE INDUCTION; GENE REPRESSION; IMMUNE RESPONSE; IMMUNOBLOTTING; IMMUNOREGULATION; LEISHMANIA CHAGASI; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PARASITE IMMUNITY; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTOZOAL INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBONUCLEASE PROTECTION ASSAY; SURVIVAL; TH1 CELL; TH2 CELL;

ANIMALS; CRICETINAE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; LEISHMANIA; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MESOCRICETUS; MICE; MICE, INBRED BALB C; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHAGOCYTOSIS; PROTEINS; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 1842588609     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.4.2111-2122.2004     Document Type: Article

References (71)

1. Ahmed, A. A., A. H. Wahbi, and K. Nordlind. 2001. Neuropeptides modulate a murine monocyte/macrophage cell line capacity for phagocytosis and killing Leishmania major parasites. Immunopharmacol. Immunotoxicol. 23:397-409.
2. Anderson, C. F., and D. M. Mosser. 2002. A novel phenotype for an activated macrophage: the type 2 activated macrophage. J. Leukoc. Biol. 72:101-106.
3. Barral, A., M. Barral-Netto, E. C. Yong, C. E. Brownell, D. R. Twardzik, and S. G. Reed. 1993. Transforming growth factor β as a virulence mechanism for Leishmania braziliensis. Proc. Natl. Acad. Sci. 90:3442-3446.
4. 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.
5. Bebo, B. F., J. C. Schuster, A. A. Vandenbark, and H. Offner. 1999. Androgens alter the cytokine profile and reduce encephalitogenicity of myelin-reactive T cells. J. Immunol. 162:35-40.
6. Blackwell, J. M. 1985. Role of macrophage complement and lectin-like receptors in binding Leishmania parasites to host macrophages. Immunol. Lett. 11:227-232.
7. Bogdan, C., A. Gessner, W. Solbach, and M. Rollinghoff. 1996. Invasion, control and persistence of Leishmania parasites. Curr. Opin. Immunol. 8:517-525.
8. Boldrick, J. C., A. A. Alizadeh, M. Diehn, S. Dudoit, C. L. Liu, C. E. Belcher, D. Botstein, L. M. Staudt, L. O. Brown, and D. A. Relman. 2002. Stereotyped and specific gene expression programs in human innate immune responses to bacteria. Proc. Natl. Acad. Sci. 99:972-977.
9. Boutard, V., R. Havouis, B. Fouqueray, C. Philippe, J.-P. Moulinoux, and L. Baud. 1995. Transforming growth factor-β stimulates arginase activity in macrophages. J. Immunol. 155:2077-2084.
10. Chaussabel, D., R. T. Semnani, M. A. McDowell, D. Sacks, A. Sher, and T. B. Nutman. 2003. Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood 102:672-681.
11. Cohen, P., M. Bouaboula, M. Bellis, V. Baron, O. Jbilo, C. Poinot-Chazel, S. Galiegue, E. H. Hadibi, and P. Casselas. 2000. Monitoring cellular responses to Listeria monocytogenes with oligonucleotide arrays. J. Biol. Chem. 275:11181-11190.
12. Coligan, J. E., A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober. 1991. Current protocols in immunology. John Wiley and Sons, New York, N.Y.
13. Constantinescu, C. S., B. D. Hondowicz, M. M. Elloso, M. Wysocka, G. Trinchieri, and P. Scott. 1998. The role of IL-12 in the maintenance of an established Th1 immune response in experimental leishmaniasis. Eur. J. Immunol. 28:2227-2233.
14. 2) in murine bone marrow-derived macrophages. Biochem. Biophys. Res. Commun. 206:667-673.
15. D'Agostino, P., S. Milano, C. Barbera, G. Di Bella, M. La Rosa, V. Ferlazzo, R. Farruggio, D. M. Miceli, M. Miele, L. Castagnetta, and E. Cillari. 1999. Sex hormones modulate inflammatory mediators produced by macrophages. Ann. N. Y. Acad. Sci. 876:426-429.
16. Duncan, M. J., J.-S. Shin, and S. N. Abraham. 2002. Microbial entry through caveolae: variations on a theme. Cell. Microbiol. 4:783-791.
17. Ehrt, S., D. Schnappinger, S. Bekiranov, J. Drenkow, S. Shi, T. R. Gingeras, T. Gassterland, G. Schoolnik, and C. Nathan. 2001. Reprogramming of the macrophage transcriptome in response to interferon-γ and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J. Exp. Med. 194:1123-1139.
18. Eskra, L., A. Mathison, and G. Splitter. 2003. Microarray analysis of mRNA levels from RAW264.7 macrophages infected with Brucella abortus. Infect. Immun. 71:1125-1133.
19. Fedyk, E. R., D. Jones, H. O. D. Critchley, R. P. Phipps, T. M. Blieden, and T. A. Sprinter. 2001. Expression of stromal-derived factor-1 is decreased by IL-1 and TNF and in dermal wound healing. J. Immunol. 166:5749-5755.
20. Forget, G., K. A. Siminovitch, S. Brochu, S. Rivest, D. Radzioch, and M. Olivier. 2001. Role of host phosphotyrosine phosphatase SHP-1 in the development of murine leishmaniasis. J. Immunol. 31:3185-3196.
21. Fukaura, H., S. C. Kent, M. J. Pietrusewicz, S. J. Khoury, H. L. Weiner, and D. A. Hafler. 1996. Induction of circulating myelin basic protein and proteolipid protein-specific transforming growth factor-β1-secreting Th3 T cells by oral administration of myelin in multiple sclerosis patients. J. Clin. Investig. 98:70-77.
22. Gantt, K. R., T. L. Goldman, M. A. Miller, M. L. McCormick, S. M. B. Jeronimo, E. T. Nascimento, B. E. Britigan, and M. E. Wilson. 2001. Oxidative responses of human and murine macrophages during phagocytosis of Leishmania chagasi. J. Immunol. 167:893-901.
23. Gantt, K. R., S. Schultz-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.
24. Gao, J. J., V. Diesl, T. Wittmann, D. C. Morrison, J. L. Ryan, S. N. Vogel, and M. T. Follettie. 2002. Regulation of gene expression in mouse macrophages stimulated with bacterial CpG-DNA and lipopolysaccharide. J. Leukoc. Biol. 72:1234-1245.
25. Goerdt, S., and C. E. Orfanos. 1999. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10:137-142.
26. Gomes, N. A., C. R. Gattass, V. Barreto-de-Souza, M. E. Wilson, and G. A. DosReis. 2000. Transforming growth factor beta regulates CTLA-4 suppression of cellular immunity in murine Kala-Azar. J. Immunol. 164:2001-2008.
27. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3:23-35.
28. Gorelik, L., P. E. Fields, and R. A. Flavell. 2000. TGF-β inhibits Th type 2 development through inhibition of GATA-3 expression. J. Immunol. 165:4773-4777.
29. Gorham, J. D., M. L. Guler, D. Fenoglio, U. Gubler, and K. M. Murphy. 1998. Low dose TGF-β attenuates IL-12 responsiveness in murine Th cells. J. Immunol. 161:1664-1670.
30. Gougerot-Pocidalo, M. A., J. el Benna, C. Elbim, S. Chollet-Martin, and M. C. Dang. 2002. Regulation of human neutrophil oxidative burst by pro- and anti-inflammatory cytokines. J. Soc. Biol. 196:37-46.
31. Gratchev, A., K. Schledzewski, P. Guillot, and S. Goerdt. 2001. Alternatively activated antigen-presenting cells: molecular repertoire, immune regulation, and healing. Skin Pharmacol. Appl. Skin Physiol. 15:272-279.
32. Iniesta, V., L. C. Gomez-Nieto, and I. Corraliza. 2001. The inhibition of arginase by N-hydroxy-L-arginine controls the growth of Leishmania inside macrophages. J. Exp. Med. 193:777-783.
33. Kaye, P. M., A. J. Curry, and J. M. Blackwell. 1991. 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. 146:2763-2770.
34. Kwan, W. C., W. R. McMaster, N. Wong, and N. E. Reiner. 1992. Inhibition of expression of major histocompatibility complex class II molecules in macrophages infected with Leishmania donovani occurs at the level of gene transcription via a cyclic AMP-independent mechanism. Infect. Immun. 60:2115-2120.
35. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
36. Lang, R., D. Patel, J. J. Morris, R. L. Rutschman, and P. J. Murray. 2002. Shaping gene expression in activated and resting primary macrophages by IL-10. J. Immunol. 169:2253-2263.
37. Mantovani, A., P. A. Gray, J. Van Damme, and S. Sozzani. 2000. Macrophage-derived chemokine (MDC). J. Leukoc. Biol. 68:400-404.
38. Matlashewski, G., and S. Buates. 2001. General suppression of macrophage gene expression during Leishmania donovani infection. J. Immunol. 166:3416-3422.
39. Moll, H. 1997. The role of chemokines and accessory cells in the immunoregulation of cutaneous leishmaniasis. Behring Inst. Mitt. 99:73-78.
40. Mosser, D. M. 2003. The many faces of macrophage activation. J. Leukoc. Biol. 73:209-212.
41. Mosser, D. M., and P. J. Edelson. 1985. The mouse macrophage receptor for C3bi (CR3) is a major mechanism in the phagocytosis of Leishmania promastigotes. J. Immunol. 135:2785-2789.
42. Murray, H. W., G. L. Spitalny, and C. F. Nathan. 1985. Activation of mouse peritoneal macrophages in vitro and in vivo by interferon-γ. J. Immunol. 134:1619-1622.
43. Nakachi, N., K. Matsunaga, T. W. Kleih, H. Friedman, and Y. Yamamoto. 2000. Differential effects of virulent versus avirulent Legionella pneumophila on chemokine gene expression in murine alveolar macropahges determined by cDNA expression array technique. Infect. Immun. 68:6069-6072.
44. Nandan, D., and N. E. Reiner. 1995. Attenuation of gamma interferon-induced tyrosine phosphorylation in mononuclear phagocytes infected with Leishmania donovani: selective inhibition of signaling through Janus kinases and Stat1. Infect. Immun. 63:4495-4500.
45. Nandan, D., and N. E. Reiner. 1999. Activation of phosphotyrosine phosphatase activity attenuates mitogen-activated protein kinase signaling and inhibits c-FOS and nitric oxide synthase expression in macrophages infected with Leishmania donovani. Infect. Immun. 67:4055-4063.
46. Nandan, D., T. Yi, M. Lopez, C. Lai, and N. E. Reiner. 2002. Leishmania EF-1α activates the Src homology 2 domain containing tyrosine phosphatase SHP-1 leading to macrophage deactivation. J. Biol. Chem. 277:50190-50197.
47. Nathan, C. F., H. W. Murray, M. E. Wiebe, and B. Y. Rubin. 1983. Identification of interferon-γ as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158:670-689.
48. Nau, G. J., J. F. L. Richmond, A. Schlesinger, E. G. Jennings, E. S. Lander, and R. A. Young. 2002. Human macrophage activation programs induced by bacterial pathogens. Proc. Natl. Acad. Sci. 99:1503-1508.
49. Olivier, M., R. W. Brownsey, and N. E. Reiner. 1992. Defective stimulus-response coupling in human monocytes infected with Leishmania donovani is associated with altered activation and translocation of protein kinase C. Proc. Natl. Acad. Sci. 89:7481-7485.
50. Pearson, R. D., and A. D. Q. Sousa. 1996. Clinical spectrum of leishmaniasis. Clin. Infect. Dis. 22:1-13.
51. Pelkmans, L., J. Kartenbeck, and A. Helenius. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:473-483.
52. Prive, C., and A. Descoteaux. 2000. Leishmania donovani promastigotes evade the activation of mitogen-activated protein kinases p38, c-Jun N-terminal kinase, and extracellular signal-regulated kinase-1/2 during infection of naive macrophages. Eur. J. Immunol. 30:2235-2244.
53. Proudfoot, L., A. V. Nikolaev, G.-J. Feng, X.-Q. Wei, M. A. Ferguson, J. S. Brimacombe, and F. Y. Liew. 1996. Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc. Natl. Acad. Sci. 93:10984-10989.
54. Ravasi, T., C. Wells, A. Forrest, D. M. Underhill, B. J. Wainwright, A. Aderem, S. Grimmond, and D. A. Hume. 2002. Generation of diversity in the innate immune system: macrophage heterogeneity arises from gene-autonomous transcriptional probability of individual inducible genes. J. Immunol. 168:44-50.
55. Ray, M., A. A. Gam, and R. A. Boykins. 2000. Inhibition of interferon-γ signaling by Leishmania donovani. J. Infect. Dis. 181:1121-1128.
56. Reiner, N. E. 1994. Altered cell signaling and mononuclear phagocyte deactivation during intracellular infection. Immunol. Today 15:374-381.
57. Ritter, U., and H. Korner. 2002. Divergent expression of inflammatory dermal chemokines in cutaneous leishmaniasis. Parasite Immunol. 24:295-301.
58. Romagnani, S. 2002. Cytokines and chemoattractants in allergic inflammation. Mol. Immunol. 38:881-885.
59. Rosenberger, C. M., A. J. Pollard, and B. B. Finlay. 2001. Gene array technology to determine host responses to Salmonella. Microbes Infect. 3:1353-1360.
60. Rosenberger, C. M., M. G. Scott, M. R. Gold, R. E. W. Hancock, and B. B. Finlay. 2000. Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J. Immunol. 164:5894-5904.
61. Rueesll, A. S., and U. T. Ruegg. 1980. Arginase production by peritoneal macrophages: a new assay. J. Immunol. Methods 32:375-382.
62. Sauvonet, N., B. Pradet-Balade, J. A. Garcia-Sanz, and G. R. Cornelis. 2002. Regulation of mRNA expression in macrophages after Yersinia enterocolitica infection. J. Biol. Chem. 277:25133-25142.
63. Shin, J.-S., and S. N. Abraham. 2001. Co-option of endocytic functions of cellular caveolae by pathogens. Immunology 102:2-7.
64. Shin, J.-S., Z. Gao, and S. N. Abraham. 2000. Involvement of cellular caveolae in bacterial entry into mast cells. Science 289:785-788.
65. + Th2 response in BALB/c mice infected with Leishmania major. J. Immunol. 165:2628-2636.
66. Wang, Z.-M., C. Liu, and R. Dziarski. 2000. Chemokines are the main proinflammatory mediators in human monocytes activated by Staphylococcus aureus, peptidoglycan, and endotoxin. J. Biol. Chem. 275:20260-20267.
67. Welch, J. S., L. Escoubet-Lozach, D. B. Sykes, K. Liddiard, D. R. Greaves, and C. K. Glass. 2002. TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J. Biol. Chem. 277:42821-42829.
68. Wilson, M. E., and R. D. Pearson. 1986. Evidence that Leishmania donovani utilizes a mannose receptor on human mononuclear phagocytes to establish intracellular parasitism. J. Immunol. 136:4681-4688.
69. Wilson, M. E., M. Sandor, A. M. Blum, B. M. Young, A. Metwali, D. Elliott, R. G. Lynch, and J. V. Weinstock. 1996. Local suppression of IFN-γ in hepatic granulomas correlates with tissue-specific replication of Leishmania chagasi. J. Immunol. 156:2231-2239.
70. Wilson, M. E., B. M. Young, B. L. Davidson, K. A. Mente, and S. E. McGowan. 1998. The importance of transforming growth factor-β in murine visceral leishmaniasis. J. Immunol. 161:6148-6155.
71. Xanthou, G., C. E. Duchesnes, T. J. Williams, and J. E. Pease. 2003. CCR3 functional responses are regulated by both CXCR3 and its ligands CXCL9, CXCL10 and CXC11. Eur. J. Immunol. 33:2241-2250.