Host cell lipid bodies triggered by Trypanosoma cruzi infection and enhanced by the uptake of apoptotic cells are associated with prostaglandin E2 generation and increased parasite growth

Journal of Infectious Diseases

Volumn 204, Issue 6, 2011, Pages 951-961

  D'Avila, Heloisa ^a,b   Freire de Lima, Célio G ^c   Roque, Natalia R ^a   Teixeira, Livia ^a,b   Barja Fidalgo, Christina ^d   Silva, Adriana R ^a   Melo, Rossana C N ^b   DosReis, George A ^c   Castro Faria Neto, Hugo C ^a   Bozza, Patrícia T ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ICOSANOID; PROSTAGLANDIN E2; TOLL LIKE RECEPTOR 3; TRANSFORMING GROWTH FACTOR BETA; VITRONECTIN RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; HOST PARASITE INTERACTION; ICOSANOID METABOLISM; LIPID BODY; MACROPHAGE; MICROBIAL GROWTH; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; TRYPANOSOMA CRUZI;

ANIMALS; CHAGAS DISEASE; DINOPROSTONE; FEMALE; HOST-PARASITE INTERACTIONS; LIPID METABOLISM; MACROPHAGES; MICE; MICE, INBRED C57BL; RATS; RATS, SPRAGUE-DAWLEY; TOLL-LIKE RECEPTOR 2; TRYPANOSOMA CRUZI;

EID: 80052249345     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jir432     Document Type: Article

References (50)

1. Coura JR, Dias JC. Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery. Mem Inst Oswaldo Cruz 2009; 104(Suppl 1):31-40.
2. Chagas C. Nova tripanozomiase humana. Estudos sobre a morfolojía e o ciclo evolutivo de Schizotrypanum cruzi n.gen., n.sp., ajente etiolójico de nova entidade morbida do homen. Mem Inst Oswaldo Cruz 1909; 1:159-218.
3. Andrews NW, Schenkman S, Ley V, Whitlow MB, Robbins ES, Nussenzweig V. Trypanosoma cruzi: mechanisms of cell-invasion and intracellular survival. Mem Inst Oswaldo Cruz 1988; 83(Suppl 1):452-5.
4. Nagajyothi F, Desruisseaux MS, Weiss LM, et al. Chagas disease, adipose tissue and the metabolic syndrome. Mem Inst Oswaldo Cruz 2009; 104(Suppl 1):219-25.
5. Bozza PT, D'Avila H, Almeida PE, et al. Lipid droplets in host-pathogen interactions. Clin Lipidol 2009; 4:791-807.
6. Farese RV Jr, Walther TC. Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 2009; 139:855-60.
7. D'Avila H, Maya-Monteiro CM, Bozza PT. Lipid bodies in innate immune response to bacterial and parasite infections. Int Immunopharmacol 2008; 8:1308-15.
8. D'Avila H, Melo RCN, Parreira GG, Werneck-Barroso E, Castro-Faria-Neto HC, Bozza PT. Mycobacterium bovis bacillus Calmette-Guerin induces TLR2-mediated formation of lipid bodies: intracellular domains for eicosanoid synthesis in vivo. J Immunol 2006; 176:3087-97.
9. D'Avila H, Almeida PE, Roque NR, Castro-Faria-Neto HC, Bozza PT. Toll-like receptor-2-mediated C-C chemokine receptor 3 and eotaxin-driven eosinophil influx induced by Mycobacterium bovis BCG pleurisy. Infect Immun 2007; 75:1507-11.
10. Almeida PE, Silva AR, Maya-Monteiro CM, et al. Mycobacterium bovis bacillus Calmette-Guerin infection induces TLR2-dependent peroxisome proliferator-activated receptor {gamma} expression and activation: functions in inflammation, lipid metabolism, and pathogenesis. J Immunol 2009; 183:1337-45.
11. Mattos KA, D'Avila H, Rodrigues LS, et al. 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.
12. Pacheco P, Bozza FA, Gomes RN, et al. Lipopolysaccharide-induced leukocyte lipid body formation in vivo: innate immunity elicited intracellular loci involved in eicosanoid metabolism. J Immunol 2002; 169:6498-506.
13. Pacheco P, Vieira-de-Abreu A, Gomes RN, et al. Monocyte chemoattractant protein-1/CC chemokine ligand 2 controls microtubule-driven biogenesis and leukotriene B4-synthesizing function of macrophage lipid bodies elicited by innate immune response. J Immunol 2007; 179: 8500-8.
14. Sorgi CA, Secatto A, Fontanari C, et al. Histoplasma capsulatum cell wall β-glucan induces lipid body formation through CD18, TLR2, and dectin-1 receptors: correlation with leukotriene B4 generation and role in HIV-1 infection. J Immunol 2009; 182:4025-35.
15. Melo RCN, D'Avila H, Fabrino DL, Almeida PE, Bozza PT. Macrophage lipid body induction by Chagas disease in vivo: putative intracellular domains for eicosanoid formation during infection. Tissue Cell 2003; 35:59-67.
16. Melo RCN, Fabrino DL, Dias FF, Parreira GG. Lipid bodies: structural markers of inflammatory macrophages in innate immunity. Inflamm Res 2006; 55:342-8.
17. Pinheiro RO, Nunes MP, Pinheiro CS, et al. Induction of autophagy correlates with increased parasite load of Leishmania amazonensis in BALB/c but not C57BL/6 macrophages. Microbes Infect 2009; 11:181-90.
18. Charron AJ, Sibley LD. Host cells: mobilizable lipid resources for the intracellular parasite Toxoplasma gondii. J Cell Sci 2002; 115:3049-59.
19. Nishikawa Y, Quittnat F, Stedman TT, et al. Host cell lipids control cholesteryl ester synthesis and storage in intracellular Toxoplasma. Cell Microbiol 2005; 7:849-67.
20. Jackson KE, Klonis N, Ferguson DJ, Adisa A, Dogovski C, Tilley L. Food vacuole-associated lipid bodies and heterogeneous lipid environments in the malaria parasite, Plasmodium falciparum. Mol Microbiol 2004; 54:109-22.
21. Rodriguez-Acosta A, Finol HJ, Pulido-Mendez M, et al. Liver ultra-structural pathology in mice infected with Plasmodium berghei. J Submicrosc Cytol Pathol 1998; 30:299-307.
22. Combs TP, Nagajyothi, Mukherjee S, et al. The adipocyte as an important target cell for Trypanosoma cruzi infection. J Biol Chem 2005; 280:24085-94.
23. Takeuchi O, Hoshino K, Kawai T, et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999; 11:443-51.
24. Contreras VT, Salles JM, Thomas N, Morel CM, Goldenberg S. In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol Biochem Parasitol 1985; 16:315-27.
25. Liu LX, Buhlmann JE, Weller PF. Release of prostaglandin E2 by microfilariae of Wuchereria bancrofti and Brugia malayi. Am J Trop Med Hyg 1992; 46:520-3.
26. 4 production in eosinophils and basophils. J Biol Chem 2001; 276:22779-87.
27. Melo RCN. Acute heart inflammation: ultrastructural and functional aspects of macrophages elicited by Trypanosoma cruzi infection. J Cell Mol Med 2009; 13:279-94.
28. D'Avila H, Roque NR, Cardoso RM, Castro-Faria-Neto HC, Melo RCN, Bozza PT. Neutrophils recruited to the site of Mycobacterium bovis BCG infection undergo apoptosis and modulate lipid body biogenesis and prostaglandin E production by macrophages. Cell Microbiol 2008; 10:2589-604.
29. DosReis GA, Freire-de-Lima CG, Nunes MP, Lopes MF. The importance of aberrant T-cell responses in Chagas disease. Trends Parasitol 2005; 21:237-43.
30. Zhang J, Andrade ZA, Yu ZX, et al. Apoptosis in a canine model of acute Chagasic myocarditis. J Mol Cell Cardiol 1999; 31:581-96.
31. Freire-de-Lima CG, Nascimento DO, Soares MB, et al. Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 2000; 403:199-203.
32. Erwig LP, Henson PM. Clearance of apoptotic cells by phagocytes. Cell Death Differ 2008; 15:243-50.
33. Pfaff M, Tangemann K, Muller B, et al. Selective recognition of cyclic RGD peptides of NMR defined conformation by alpha IIb beta 3, alpha V beta 3, and alpha 5 beta 1 integrins. J Biol Chem 1994; 269:20233-8.
34. Lu X, Lu D, Scully MF, Kakkar VV. Snake venom metalloproteinase containing a disintegrin-like domain, its structure-activity relationships at interacting with integrins. Curr Med Chem Cardiovasc Hematol Agents 2005; 3:249-60.
35. Bandeira Melo C, Weller PF, Bozza PT. EicosaCell - an immunofluorescent-based assay to localize newly synthesized eicosanoid lipid mediators at intracellular sites. Methods Mol Biol 2011; 689:163-81.
36. van der Meer-Janssen YP, van Galen J, Batenburg JJ, Helms JB. Lipids in host-pathogen interactions: pathogens exploit the complexity of the host cell lipidome. Prog Lipid Res 2010; 49:1-26.
37. Bozza PT, Magalhaes KG, Weller PF. Leukocyte lipid bodies: biogenesis and functions in inflammation. Biochim Biophys Acta 2009; 1791:540-51.
38. Gazzinelli RT, Denkers EY. Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nat Rev Immunol 2006; 6:895-906.
39. DosReis GA, Lopes MF. The importance of apoptosis for immune regulation in Chagas disease. Mem Inst Oswaldo Cruz 2009; 104(Suppl 1):259-62.
40. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 1998; 101:890-8.
41. D'Mello V, Birge RB. Apoptosis: conserved roles for integrins in clearance. Curr Biol 2010; 20:R324-7.
42. Silva JS, Twardzik DR, Reed SG. Regulation of Trypanosoma cruzi infections in vitro and in vivo by transforming growth factor beta (TGF-beta). J Exp Med 1991; 174:539-45.
43. Ming M, Ewen ME, Pereira ME. Trypanosome invasion of mammalian cells requires activation of the TGF beta signaling pathway. Cell 1995; 82:287-96.
44. Freire-de-Lima CG, Xiao YQ, Gardai SJ, Bratton DL, Schiemann WP, Henson PM. Apoptotic cells, through transforming growth factor-beta, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J Biol Chem 2006; 281:38376-84.
45. Bozza PT, Pacheco P, Yu W, Weller PF. NS-398: cyclooxygenase-2 independent inhibition of leukocyte priming for lipid body formation and enhanced leukotriene generation. Prostaglandins Leukot Essent Fatty Acids 2002; 67:237-44.
46. Bozza PT, Payne JL, Morham SG, Langenbach R, Smithies O, Weller PF. Leukocyte lipid body formation and eicosanoid generation: cyclooxygenase- independent inhibition by aspirin. Proc Natl Acad Sci U S A 1996; 93:11091-6.
47. 2 synthesis in colon cancer cells. Cancer Res 2008; 68:1732-40.
48. Schmid B, Rippmann JF, Tadayyon M, Hamilton BS. Inhibition of fatty acid synthase prevents preadipocyte differentiation. Biochem Biophys Res Commun 2005; 328:1073-82.
49. Samsa MM, Mondotte JA, Iglesias NG, et al. Dengue virus capsid protein usurps lipid droplets for viral particle formation. PLoS Pathog 2009; 5:e1000632.
50. Boulant S, Targett-Adams P, McLauchlan J. Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. J Gen Virol 2007; 88:2204-13.