Host lipid bodies as platforms for intracellular survival of protozoan parasites

Frontiers in Immunology

Volumn 7, Issue MAY, 2016, Pages

  Toledo, Daniel A M ^a   D'Avila, Heloísa ^a   Melo, Rossana C N ^a  

^a FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

Author keywords

Infectious diseases; Inflammation; Lipid droplets; Lipid mediators; Parasite survival; Parasitophorous vacuole; Phagocytosis

Indexed keywords

PHOSPHATIDYLCHOLINE;

FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; INFLAMMATION; INTRACELLULAR FLUID; LEISHMANIA AMAZONENSIS; MICROSCOPY; NONHUMAN; PHAGOCYTOSIS; PROTOZOAL INFECTION; SHORT SURVEY; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84973533424     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00174     Document Type: Short Survey

References (63)

1. Bar AK, Phukan N, Pinheiro J, Simoes-Barbosa A. The interplay of host microbiota and parasitic protozoans at mucosal interfaces: implications for the outcomes of infections and diseases. PLoS Negl Trop Dis (2015) 9(12):e0004176. doi:10.1371/journal.pntd.0004176
2. Sibley LD. Invasion and intracellular survival by protozoan parasites. Immunol Rev (2011) 240(1):72-91. doi:10.1111/j.1600-065X.2010.00990.x
3. Liévin-Le Moal V, Loiseau PM. Leishmania hijacking of the macrophage intracellular compartments. FEBS J (2015) 282(4):598-607. doi:10.1111/febs.13601
4. Melo RCN, D'Avila H, Wan HC, Bozza PT, Dvorak AM, Weller PF. Lipid bodies in inflammatory cells: structure, function, and current imaging techniques. J Histochem Cytochem (2011) 59(5):540-56. doi:10.1369/0022155411404073
5. Melo RCN, Dvorak AM. Lipid body-phagosome interaction in macrophages during infectious diseases: host defense or pathogen survival strategy? PLoS Pathog (2012) 8(7):e1002729. doi:10.1371/journal.ppat.1002729
6. Saka HA, Valdivia R. Emerging roles for lipid droplets in immunity and host-pathogen interactions. Annu Rev Cell Dev Biol (2012) 28:411-37. doi:10.1146/annurev-cellbio-092910-153958
7. Nicolaou G, Goodall AH, Erridge C. Diverse bacteria promote macrophage foam cell formation via toll-like receptor-dependent lipid body biosynthesis. J Atheroscler Thromb (2012) 19(2):137-48. doi:10.5551/jat.10249
8. Dias FF, Zarantonello VC, Parreira GG, Chiarini-Garcia H, Melo RCN. The intriguing ultrastructure of lipid body organelles within activated macrophages. Microsc Microanal (2014) 20(3):869-78. doi:10.1017/S143192761400066X
9. Pinheiro RO, Nunes MP, Pinheiro CS, D'Avila H, Bozza PT, Takiya CM, 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(2):181-90. doi:10.1016/j.micinf.2008.11.006
10. Lecoeur H, Giraud E, Prevost MC, Milon G, Lang T. Reprogramming neutral lipid metabolism in mouse dendritic leucocytes hosting live Leishmania amazonensis amastigotes. PLoS Negl Trop Dis (2013) 7(6):e2276. doi:10.1371/journal.pntd.0002276
11. Rabhi S, Rabhi I, Trentin B, Piquemal D, Regnault B, Goyard S, et al. Lipid droplet formation, their localization and dynamics during Leishmania major macrophage infection. PLoS One (2016) 11(2):e0148640. doi:10.1371/journal.pone.0148640
12. Rabhi I, Rabhi S, Ben-Othman R, Rasche A, Daskalaki A, Trentin B, et al. Transcriptomic signature of Leishmania infected mice macrophages: a metabolic point of view. PLoS Negl Trop Dis (2012) 6(8):e1763. doi:10.1371/journal.pntd.0001763
13. Rodríguez-Acosta A, Finol HJ, Pulido-Méndez M, Márquez A, Andrade G, González N, et al. Liver ultrastructural pathology in mice infected with Plasmodium berghei. J Submicrosc Cytol Pathol (1998) 30(2):299-307
14. Pulido-Méndez M, Finol HJ, Girón ME, Aguilar I. Ultrastructural pathological changes in mice kidney caused by Plasmodium berghei infection. J Submicrosc Cytol Pathol (2006) 38(2-3):143-8
15. Dumont ME, Dei-Cas E, Maurois P, Slomianny C, Prensier G, Houcke-Lecomte M, et al. [Histopathology of the liver and kidney during malaria: relation to malaria-induced dyslipoproteinemia]. Ann Parasitol Hum Comp (1988) 63(3):171-83
16. Charron AJ, Sibley LD. Host cells: mobilizable lipid resources for the intracellular parasite Toxoplasma gondii. J Cell Sci (2002) 115(Pt 15):3049-59
17. Gomes AF, Magalhaes KG, Rodrigues RM, de Carvalho L, Molinaro R, Bozza PT, et al. Toxoplasma gondii-skeletal muscle cells interaction increases lipid droplet biogenesis and positively modulates the production of IL-12, IFN-g and PGE2. Parasit Vectors (2014) 7:47. doi:10.1186/1756-3305-7-47
18. 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(1):59-67. doi:10.1016/S0040-8166(02)00105-2
19. Melo RCN, Fabrino DL, Dias FF, Parreira GG. Lipid bodies: structural markers of inflammatory macrophages in innate immunity. Inflamm Res (2006) 55(8):342-8. doi:10.1007/s00011-006-5205-0
20. D'Avila H, Freire-de-Lima CG, Roque NR, Teixeira L, Barja-Fidalgo C, Silva AR, et al. Host cell lipid bodies triggered by Trypanosoma cruzi infection and enhanced by the uptake of apoptotic cells are associated with prostaglandin E generation and increased parasite growth. J Infect Dis (2011) 204(6):951-61. doi:10.1093/infdis/jir432
21. Fabro AE, Calzolari G. [Increase of lipids in human chagasic placentas: cytochemical and biochemical study]. Rev Fac Cien Med Univ Nac Cordoba (1990) 48(1-2):25-32
22. Helms JB, Kaloyanova DV, Strating JR, van Hellemond JJ, van der Schaar HM, Tielens AG, et al. Targeting of the hydrophobic metabolome by pathogens. Traffic (2015) 16(5):439-60. doi:10.1111/tra.12280
23. Coppens I. Contribution of host lipids to Toxoplasma pathogenesis. Cell Microbiol (2006) 8(1):1-9. doi:10.1111/j.1462-5822.2005.00647.x
24. Welte MA. Proteins under new management: lipid droplets deliver. Trends Cell Biol (2007) 17(8):363-9. doi:10.1016/j.tcb.2007.06.004
25. Wan HC, Melo RCN, Jin Z, Dvorak AM, Weller PF. Roles and origins of leukocyte lipid bodies: proteomic and ultrastructural studies. FASEB J (2007) 21(1):167-78. doi:10.1096/fj.06-6711com
26. Melo RCN, Weller PF. Unraveling the complexity of lipid body organelles in human eosinophils. J Leukoc Biol (2014) 96(5):703-12. doi:10.1189/jlb.3RU0214-110R
27. Melo RCN, Machado CRS. Trypanosoma cruzi: peripheral blood monocytes and heart macrophages in the resistance to acute experimental infection in rats. Exp Parasitol (2001) 97(1):15-23. doi:10.1006/expr.2000.4576
28. Melo RCN. Acute heart inflammation: ultrastructural and functional aspects of macrophages elicited by Trypanosoma cruzi infection. J Cell Mol Med (2009) 13(2):279-94. doi:10.1111/j.1582-4934.2008.00388.x
29. 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(5):3087-97. doi:10.4049/jimmunol.176.5.3087
30. Mattos KA, D'Avila H, Rodrigues LS, Oliveira VG, Sarno EN, Atella GC, 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(3):371-84. doi:10.1189/jlb.0609433
31. Mota LA, Roberto Neto J, Monteiro VG, Lobato CS, Oliveira MA, Cunha M, et al. Culture of mouse peritoneal macrophages with mouse serum induces lipid bodies that associate with the parasitophorous vacuole and decrease their microbicidal capacity against Toxoplasma gondii. Mem Inst Oswaldo Cruz (2014) 109(6):767-74
32. Combs TP, Nagajyothi, Mukherjee S, de Almeida CJ, Jelicks LA, Schubert W, et al. The adipocyte as an important target cell for Trypanosoma cruzi infection. J Biol Chem (2005) 280(25):24085-94. doi:10.1074/jbc.M412802200
33. Cocchiaro JL, Kumar Y, Fischer ER, Hackstadt T, Valdivia RH. Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci U S A (2008) 105(27):9379-84. doi:10.1073/pnas.0712241105
34. Dumoux M, Hayward RD. Membrane contact sites between pathogen-containing compartments and host organelles. Biochim Biophys Acta (2016). doi:10.1016/j.bbalip.2016.01.018
35. Simoes AP, Roelofsen B, Op den Kamp JA. Incorporation of free fatty acids can explain alterations in the molecular species composition of phosphatidylcholine and phosphatidylethanolamine in human erythrocytes as induced by Plasmodium falciparum. Cell Biol Int Rep (1992) 16(6):533-45. doi:10.1016/S0309-1651(05)80052-9
36. Itoe MA, Sampaio JL, Cabal GG, Real E, Zuzarte-Luis V, March S, et al. Host cell phosphatidylcholine is a key mediator of malaria parasite survival during liver stage infection. Cell Host Microbe (2014) 16(6):778-86. doi:10.1016/j.chom.2014.11.006
37. Hamid PH, Hirzmann J, Kerner K, Gimpl G, Lochnit G, Hermosilla CR, et al. Eimeria bovis infection modulates endothelial host cell cholesterol metabolism for successful replication. Vet Res (2015) 46:100. doi:10.1186/s13567-015-0230-z
38. Nishikawa Y, Quittnat F, Stedman TT, Voelker DR, Choi JY, Zahn M, et al. Host cell lipids control cholesteryl ester synthesis and storage in intracellular Toxoplasma. Cell Microbiol (2005) 7(6):849-67. doi:10.1111/j.1462-5822.2005.00518.x
39. Labaied M, Jayabalasingham B, Bano N, Cha SJ, Sandoval J, Guan G, et al. Plasmodium salvages cholesterol internalized by LDL and synthesized de novo in the liver. Cell Microbiol (2011) 13(4):569-86. doi:10.1111/j.1462-5822.2010.01555.x
40. Ehrenman K, Wanyiri JW, Bhat N, Ward HD, Coppens I. Cryptosporidium parvum scavenges LDL-derived cholesterol and micellar cholesterol internalized into enterocytes. Cell Microbiol (2013) 15(7):1182-97. doi:10.1111/cmi.12107
41. 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(1):109-22. doi:10.1111/j.1365-2958.2004.04284
42. Caffaro CE, Boothroyd JC. Evidence for host cells as the major contributor of lipids in the intravacuolar network of Toxoplasma-infected cells. Eukaryot Cell (2011) 10(8):1095-9. doi:10.1128/EC.00002-11
43. Hamid PH, Hirzmann J, Hermosilla C, Taubert A. Differential inhibition of host cell cholesterol de novo biosynthesis and processing abrogates Eimeria bovis intracellular development. Parasitol Res (2014) 113(11):4165-76. doi:10.1007/s00436-014-4092-5
44. Sibley LD, Niesman IR, Parmley SF, Cesbron-Delauw MF. Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J Cell Sci (1995) 108(Pt 4):1669-77
45. Farese RV Jr, Walther TC. Lipid droplets finally get a little R-E-S-P-E-C-T. Cell (2009) 139(5):855-60. doi:10.1016/j.cell.2009.11.005
46. Wenk MR. Lipidomics of host-pathogen interactions. FEBS Lett (2006) 580(23):5541-51. doi:10.1016/j.febslet.2006.07.007
47. Penno A, Hackenbroich G, Thiele C. Phospholipids and lipid droplets. Biochim Biophys Acta (2013) 1831(3):589-94. doi:10.1016/j.bbalip.2012.12.001
48. Tzipori S, Ward H. Cryptosporidiosis: biology, pathogenesis and disease. Microbes Infect (2002) 4(10):1047-58. doi:10.1016/S1286-4579(02)01629-5
49. Melo RCN, Weller PF. Lipid droplets in leukocytes: organelles linked to inflammatory responses. Exp Cell Res (2016) 340(2):193-7. doi:10.1016/j.yexcr.2015.10.028
50. Weller PF, Dvorak AM. Arachidonic acid incorporation by cytoplasmic lipid bodies of human eosinophils. Blood (1985) 65(5):1269-74
51. Weller PF, Monahan-Earley RA, Dvorak HF, Dvorak AM. Cytoplasmic lipid bodies of human eosinophils. Subcellular isolation and analysis of arachidonate incorporation. Am J Pathol (1991) 138(1):141-8
52. Dvorak AM, Morgan E, Schleimer RP, Ryeom SW, Lichtenstein LM, Weller PF. Ultrastructural immunogold localization of prostaglandin endoperoxide synthase (cyclooxygenase) to non-membrane-bound cytoplasmic lipid bodies in human lung mast cells, alveolar macrophages, type II pneumocytes, and neutrophils. J Histochem Cytochem (1992) 40(6):759-69. doi:10.1177/40.6.1316915
53. Dvorak AM, Morgan ES, Tzizik DM, Weller PF. Prostaglandin endoperoxide synthase (cyclooxygenase): ultrastructural localization to nonmembrane-bound cytoplasmic lipid bodies in human eosinophils and 3T3 fibroblasts. Int Arch Allergy Immunol (1994) 105(3):245-50. doi:10.1159/000236764
54. Bozza PT, Yu W, Penrose JF, Morgan ES, Dvorak AM, Weller PF. Eosinophil lipid bodies: specific, inducible intracellular sites for enhanced eicosanoid formation. J Exp Med (1997) 186(6):909-20. doi:10.1084/jem.186.6.909
55. Bozza PT, Yu W, Cassara J, Weller PF. Pathways for eosinophil lipid body induction: differing signal transduction in cells from normal and hypereosinophilic subjects. J Leukoc Biol (1998) 64(4):563-9
56. Bandeira-Melo C, Phoofolo M, Weller PF. Extranuclear lipid bodies, elicited by CCR3-mediated signaling pathways, are the sites of chemokine-enhanced leukotriene C4 production in eosinophils and basophils. J Biol Chem (2001) 276(25):22779-87. doi:10.1074/jbc.M101436200
57. Vieira-de-Abreu A, Assis EF, Gomes GS, Castro-Faria-Neto HC, Weller PF, Bandeira-Melo C, et al. Allergic challenge-elicited lipid bodies compartmentalize in vivo leukotriene C4 synthesis within eosinophils. Am J Respir Cell Mol Biol (2005) 33(3):254-61. doi:10.1165/rcmb.2005-0145OC
58. Pacheco P, Vieira-de-Abreu A, Gomes RN, Barbosa-Lima G, Wermelinger LB, Maya-Monteiro CM, 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(12):8500-8. doi:10.4049/jimmunol.179.12.8500
59. 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(20):11091-6. doi:10.1073/pnas.93.20.11091
60. Renz H, Gong J-H, Schmidt A, Nain M, Gemsa D. Release of tumor necrosis factor-alpha from macrophages. Enhancement and suppression are dose-dependently regulated by prostaglandin E2 and cyclic nucleotides. J Immunol (1988) 141(7):2388-93
61. Betz M, Fox BS. Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J Immunol (1991) 146(1):108-13
62. Kalinski P. Regulation of immune responses by prostaglandin E2. J Immunol (2012) 188(1):21-8. doi:10.4049/jimmunol.1101029
63. Mattos KA, Oliveira VC, Berredo-Pinho M, Amaral JJ, Antunes LC, Melo RCN, et al. Mycobacterium leprae intracellular survival relies on cholesterol accumulation in infected macrophages: a potential target for new drugs for leprosy treatment. Cell Microbiol (2014) 16(6):797-815. doi:10.1111/cmi.12279