Modulation of lipid droplets by Mycobacterium leprae in Schwann cells: A putative mechanism for host lipid acquisition and bacterial survival in phagosomes

Cellular Microbiology

Volumn 13, Issue 2, 2011, Pages 259-273

  Mattos, Katherine A ^a   Lara, Flavio A ^a   Oliveira, Viviane G C ^a   Rodrigues, Luciana S ^a   D'Avila, Heloisa ^b   Melo, Rossana C N ^b   Manso, Pedro P A ^a   Sarno, Euzenir N ^a   Bozza, Patricia T ^a   Pessolani, Maria Cristina V ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOPHILIN; LIPID; PHOSPHATIDYLINOSITOL 3 KINASE; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; BIOGENESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; HOMEOSTASIS; HOST CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LEPROMATOUS LEPROSY; MOUSE; MYCOBACTERIUM LEPRAE; NONHUMAN; PATHOGENESIS; PERIPHERAL NEUROPATHY; PHAGOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SCHWANN CELL; SIGNAL TRANSDUCTION; SURVIVAL;

CELLS, CULTURED; CYTOPLASM; CYTOSKELETON; HUMANS; IMMUNOHISTOCHEMISTRY; LIPID METABOLISM; MEMBRANE PROTEINS; MICROBIAL VIABILITY; MICROSCOPY; MYCOBACTERIUM LEPRAE; PHAGOSOMES; PHOSPHATIDYLINOSITOL 3-KINASES; SCHWANN CELLS; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM LEPRAE;

EID: 78651466240     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01533.x     Document Type: Article

References (60)

1. Almeida, P.E., Silva, A.R., Maya-Monteiro, C.M., Töröcsik, D., D'Avila, H., Dezsö, B., et al. (2009) Mycobacterium bovis bacillus Calmette-Guérin infection induces TLR2-dependent peroxisome proliferator-activated receptor gamma expression and activation: functions in inflammation, lipid metabolism, and pathogenesis. J Immunol 183: 1337-1345.
2. Barba, G., Harper, F., Harada, T., Kohara, M., Goulinet, S., Matsuura, Y., et al. (1997) Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci USA 94: 1200-1205.
3. Bentrup, K.H., and Russell, D.G. (2001) Mycobacterial persistence: adaptation to a changing environment. Trends Microbiol 9: 597-605.
4. Betz, M., and Fox, B.S. (1991) Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J Immunol 146: 108-113.
5. Bligh, E.G., and Dyer, W.J. (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
6. Boström, P., Rutberg, M., Ericsson, J., Holmdahl, P., Andersson, L., Frohman, M.A., et al. (2005) Cytosolic lipid droplets increase in size by microtubule-dependent complex formation. Arterioscler Thromb Vasc Biol 25: 1945-1951.
7. Boström, P., Andersson, L., Rutberg, M., Perman, J., Lidberg, U., Johansson, B.R., et al. (2007) SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nat Cell Biol 9: 1286-1293.
8. Boulant, S., Douglas, M.W., Moody, L., Budkowska, A., Targett-Adams, P., and McLauchlan, J. (2008) Hepatitis C virus core protein induces lipid droplet redistribution in a microtubule- and dynein-dependent manner. Traffic 9: 1268-1282.
9. Bozza, P.T., and Viola, J.P. (2010) Lipid droplets in inflammation and cancer. Prostaglandins Leukot Essent Fatty Acids 82: 243-250.
10. Bozza, P.T., Magalhães, K.G., and Weller, P.F. (2009) Leukocyte lipid bodies - biogenesis and functions in inflammation. Biochim Biophys Acta 1791: 540-551.
11. Brennan, P. (1984) Mycobacterium leprae - the outer lipoidal surface. J Biosci 6: 685-689.
12. Cáceres, N., Tapia, G., Ojanguren, I., Altare, F., Gil, O., Pinto, S., et al. (2009) Evolution of foamy macrophages in the pulmonary granulomas of experimental tuberculosis models. Tuberculosis 89: 175-182.
13. Cámara-Lemarroy, C.R., Guzmán-de la Garza, F.J., and Fernández-Garza, N.E. (2010) Molecular inflammatory mediators in peripheral nerve degeneration and regeneration. Neuroimmunomodulation 17: 314-324.
14. Chatterjee, K.R., Das Gupta, N.N., and De, M.L. (1959) Electron microscopic observations on the morphology of Mycobacterium leprae. Exp Cell Res 18: 521-527.
15. Cocchiaro, J.L., Kumar, Y., Fischer, E.R., Hackstadt, T., and Valdivia, R.H. (2008) Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci USA 105: 9379-9384.
16. Cole, S.T., Eiglmeier, K., Parkhill, J., James, K.D., Thomson, N.R., Wheeler, P.R., et al. (2001) Massive gene decay in the leprosy bacillus. Nature 409: 1007-1011.
17. Cruz, D., Watson, A.D., Miller, C.S., Montoya, D., Ochoa, M.T., Sieling, P.A., et al. (2008) Host-derived oxidized phospholipids and HDL regulate innate immunity in human leprosy. J Clin Invest 118: 2917-2928.
18. D'Ávila, H., Melo, R.C.N., Parreira, G.G., Werneck-Barroso, E., Castro-Faria-Neto, H.C., and Bozza, P.T. (2006) Mycobacterium bovis bacillus calmette-guérin induces TLR2-mediated formation of lipid bodies: intracellular domains for eicosanoid synthesis in vivo. J Immunol 176: 3087-3097.
19. D'Ávila, H., Maya-Monteiro, C.M., and Bozza, P.T. (2008) Lipid bodies in innate immune response to bacterial and parasite infections. Int J Immunopharmacol 8: 1308-1315.
20. Folch, J., Lees, M., and Stanley, G.H.S. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
21. Franzblau, S.G. (1988) Oxidation of palmitic acid by Mycobacterium leprae in an axenic medium. J Clin Microbiol 26: 18-21.
22. Gao, J., Ye, H., and Serrero, G. (2000) Stimulation of adipose differentiation related protein (ADRP) expression in adipocyte precursors by long-chain fatty acids. J Cell Physiol 182: 297-302.
23. Grigoriev, I.S., Chernobelskaya, A.A., and Vorobjev, I.A. (1999) Nocodazole, vinblastine and taxol at low concentrations affect fibroblast locomotion and saltatory movements of organelles. Membr Cell Biol 13: 23-48.
24. Hagge, D.A., Oby Robinson, S., Scollard, D., McCormick, G., and Williams, D.L. (2002) A new model for studying the effects of Mycobacterium leprae on Schwann cell and neuron interactions. J Infect Dis 186: 1283-1296.
25. Job, C.K. (1970) Mycobacterium leprae in nerve lesions in lepromatous leprosy: an electron microscopic study. Arch Pathol 89: 195-207.
26. Kaplan, G., Van Voorhis, W.C., Sarno, E.N., Nogueira, N., and Cohn, Z.A. (1983) The cutaneous infiltrates of leprosy. A transmission electron microscopy study. J Exp Med 158: 1145-1159.
27. Lasunskaia, E.B., Campos, M.N.N., de Andrade, M.R.M., DaMatta, R.A., Kipnis, T.L., Einicker-Lamas, M., and Da Silva, W.D. (2006) Mycobacteria directly induce cytoskeletal rearrangements for macrophage spreading and polarization through TLR2- dependent PI3K signaling. J Leukoc Biol 80: 1480-1490.
28. Lisak, R.P., Skundric, D., Bealmear, B., and Ragheb, S. (1997) The role of cytokines in Schwann cell damage, protection, and repair. J Infect Dis 176: 173-179.
29. Mahlberg, F.H., Glick, J.M., Jerome, W.G., and Rothblat, G.H. (1990) Metabolism of cholesteryl ester lipid droplets in a J774 macrophage foam cell model. Biochim Biophys Acta 1045: 291-298.
30. Marques, M.A., Neves-Ferreira, A.G., da Silveira, E.K., Valente, R.H., Chapeaurouge, A., Perales, J., et al. (2008) Deciphering the proteomic profile of Mycobacterium leprae cell envelope. Proteomics 8: 2477-2491.
31. Marri, P.R., Bannantine, J.P., and Golding, G.B. (2006) Comparative genomics of metabolic pathways in Mycobacterium species: gene duplication, gene decay and lateral gene transfer. FEMS Microbiol Rev 30: 6906-6925.
32. Mattos, K.A., D'Avila, H., Rodrigues, L.S., Oliveira, V.G.C., Sarno, E.N., Atella, G.C., et al. (2010) Lipid droplet formation in Leprosy: Toll-like Receptor-regulated organelles involved in eicosanoid formation and Mycobacterium leprae pathogenesis. J Leukoc Biol 87: 371-384.
33. van der Meer-Janssen, Y.P., van Galen, J., Batenburg, J.J., and Helms, J.B. (2010) Lipids in host-pathogen interactions: pathogens exploit the complexity of the host cell lipidome. Prog Lipid Res 1: 1-26.
34. Melo, R.C.N., D'Avila, H., Fabrino, D.L., Almeida, P.E., and Bozza, P.T. (2003) Macrophage lipid body induction by Chagas disease in vivo: putative intracellular domains for eicosanoid formation during infection. Tissue Cell 35: 59-67.
35. Mosmann, T. (1983) Rapid colorimetrie assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 55: 55-63.
36. Oliveira, R.B., Ochoa, M.T., Sieling, P.A., Rea, T.H., Rambukkana, A., Sarno, E.N., and Modlin, R.L. (2003) Expression of toll-like receptor 2 on human schwann cells: a mechanism of nerve damage in leprosy. Infect Immun 71: 1427-1433.
37. Pacheco, P., Vieira-de-Abreu, A., Gomes, R.N., Barbosa-Lima, G., Wermelinger, L.B., Maya-Monteiro, C.M., et al. (2007) 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 179: 8500-8508.
38. Pelc, S., Gompel, C., and Simonet, M.L. (1986) S-100 protein expression in satellite and schwann cells in neuroblastoma. An immunohistochemical and ultrastructural study. Virchows Arch B Cell Pathol Incl Mol Pathol 51: 487-495.
39. Persson, J., Nilsson, J., and Lindholm, M.W. (2008) Interleukin-1β and tumor necrosis factor-α impede neutral lipid turnover in macrophage-derived foam cells. BMC Immunol 25: 70.
40. Peyron, P., Vaubourgeix, J., Poquet, Y., Levillain, F., Botanch, C., Bardou, F., et al. (2008) Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 4: 1000204.
41. Pol, A., Lu, A., Pons, M., Peiró, S., and Enrich, C. (2000) Epidermal growth factor-mediated caveolin recruitment to early endosomes and MAPK activation. Role of cholesterol and actin cytoskeleton. J Biol Chem 275: 30566-30572.
42. Quesniaux, V., Fremond, C., Jacobs, M., Parida, S., Nicolle, D., Yeremeev, V., et al. (2004) Toll-like receptor pathways in the immune responses to mycobacteria. Microbes Infect 6: 946-959.
43. Ridley, D.S., and Jopling, W.H. (1966) Classification of leprosy according to immunity: a five-group system. Int J Lepr 34: 255-273.
44. Robenek, H., and Severs, N.J. (2009) Lipid droplet growth by fusion: insights from freeze-fracture imaging. J Cell Mol Med 13: 4657-4661.
45. Russell, D.G., Cardona, P.J., Kim, M.J., Allain, S., and Altare, F. (2009) Foamy macrophages and the progression of the human tuberculosis granuloma. Nat Immunol 10: 943-948.
46. Rutkowski, J.L., Tuite, G.F., Lincoln, P.M., Boyer, P.J., Tennekoon, G.I., and Kunkel, S.L. (1999) Signals for proinflammatory cytokine secretion by human Schwann cells. J Neuroimmunol 101: 47-60.
47. Sakurai, I.S., and Skinsnes, O.K. (1970) Lipids in leprosy 2. Histochemistry of lipids in human leprosy. Int J Lepr Other Mycobact Dis 38: 389-403.
48. Samsa, M.M., Mondotte, J.A., Iglesias, N.G., Assunção-Miranda, I., Barbosa-Lima, G., Da Poian, A.T., et al. (2009) Dengue virus capsid protein usurps lipid droplets for viral particle formation. PLoS Pathog 5: e1000632.
49. Scollard, D.M., Adams, L.B., Gillis, T.P., Krahenbuhl, J.L., Truman, R.W., and Williams, D.L. (2006) The continuing challenges of leprosy. Clin Microbiol Rev 19: 338-381.
50. Singh, A.K., Shirasawa, N., Kyoshima, K., Kobayashi, S., and Shimizu, Y. (1996) Schwann cell culture from the adult animal sciatic nerve: technique and review. J Clin Neurosci 3: 69-74.
51. Tanigawa, K., Suzuki, K., Nakamura, K., Akama, T., Kawashima, A., Wu, H., et al. (2008) Expression of adipose differentiation-related protein (ADRP) and perilipin in macrophages infected with Mycobacterium leprae. FEMS Microbiol Lett 289: 72-79.
52. Teles, R.M., Antunes, S.L., Jardim, M.R., Oliveira, A.L., Nery, J.A., Sales, A.M., et al. (2007) Expression of metalloproteinases (MMP-2, MMP-9, and TACE) and TNF-alpha in the nerves of leprosy patients. J Peripher Nerv Syst 12: 195-204.
53. Van Meer, G. (2001) Caveolin, cholesterol, and lipid droplets? J Cell Biol 152: F29-F34.
54. Virchow, R. (1863) Die krankhaften Geschwülste. Berlin: Hirschwald. 3: 325-327.
55. Wade, H.W. (1962) Zenker vs formalin fixation for the histopathology of leprosy tissues and other desirable features of technique. Int J Lepr 30: 477-488.
56. Wenk, M.R. (2006) Lipidomics of host-pathogen interactions. FEBS Lett 580: 5541-5551.
57. Wheeler, P.R. (1989) Biosynthetic pathways in Mycobacterium leprae. Acta Leprol 7: 21-24.
58. Wheeler, P.R. (2003) Leprosy - clues about the biochemistry of Mycobacterium leprae and its host-dependency from the genome. World J Microbiol Biotechnol 19: 1-16.
59. WHO (2010) WHO Leprosy Today, WHO Report 2010. [WWW document]. URL
60. Zehmer, J.K., Huang, Y., Peng, G., Pu, J., Anderson, R.G.W., and Liu, P. (2009) A role for lipid droplets in inter-membrane lipid traffic. Proteomics 9: 914-921.