Roles and origins of leukocyte lipid bodies: Proteomic and ultrastructural studies

FASEB Journal

Volumn 21, Issue 1, 2007, Pages 167-178

  Wan, Hsiao Ching ^a   Melo, Rossana C N ^a   Jin, Zhoung ^a   Dvorak, Ann M ^b   Weller, Peter F ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Bodies; Endoplasmic reticulum; Eosinophils; Lipid; Lipid droplets; Neutrophils; U937 cells

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACTIN; ADIPOPHILIN; ALBUMIN; ALPHA TUBULIN; CALGRANULIN; CALNEXIN; CHOLESTEROL; CYCLOPHILIN B; EMERIN; EUKARYOTIC ELONGATION FACTOR 1 ALPHA; EUKARYOTIC ELONGATION FACTOR 1 GAMMA; HEMOGLOBIN A; HEMOGLOBIN BETA CHAIN; HEMOGLOBIN C; HISTONE H2AZ; HISTONE H2BB; LANOSTEROL SYNTHASE; POLYUBIQUITIN; PROTEIN; RAB PROTEIN; RAB10 PROTEIN; RAB11 PROTEIN; RAB14 PROTEIN; RAB18 PROTEIN; RAB1A PROTEIN; RAB1B PROTEIN; RAB7 PROTEIN; SQUALENE MONOOXYGENASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADIPOCYTE; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; EOSINOPHIL; HUMAN; HUMAN CELL; LEUKOCYTE; LIPID METABOLISM; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEOMICS; RIBOSOME; ULTRASTRUCTURE; UNINDEXED SEQUENCE;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HUMANS; LEUKOCYTES; LIPIDS; MICROSCOPY, ELECTRON; MOLECULAR STRUCTURE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; U937 CELLS;

EUKARYOTA; MAMMALIA;

EID: 33846037475     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-6711com     Document Type: Article

References (73)

1. Murphy, D. J. (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog. Lipid Res. 40, 325-438
2. Martin, S., and Parton, R. G. (2006) Lipid droplets: a unified view of a dynamic organelle. Nat. Rev. Mol. Cell. Biol. 7, 373-378
3. Martin, S., and Parton, R. G. (2005) Caveolin, cholesterol, and lipid bodies. Semin. Cell Dev. Biol. 16, 163-174
4. Tauchi-Sato, K., Ozeki, S., Houjou, T., Taguchi, R., and Fujimoto, T. (2002) The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J. Biol. Chem. 277, 44507-44512
5. Blanchette-Mackie, E. J., Dwyer, N. K., Barber, T., Coxey, R. A., Takeda, T., Rondinone, C. M., Theodorakis, J. L., Greenberg, A. S., and Londos, C. (1995) Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J. Lipid Res. 36, 1211-1226
6. Brasaemle, D. L., Barber, T., Wolins, N. E., Serrero, G., Blanchette-Mackie, E. J., and Londos, C. (1997) Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. J. Lipid Res. 38, 2249-2263
7. Miura, S., Gan, J. W., Brzostowski, J., Parisi, M. J., Schultz, C. J., Londos, C., Oliver, B., and Kimmel, A. R. (2002) Functional conservation for lipid storage droplet association among Perilipin, ADRP, and TIP47 (PAT)-related proteins in mammals, Drosophila, and Dictyostelium. J. Biol. Chem. 277, 32253-32257
8. Wolins, N. E., Skinner, J. R., Schoenfish, M. J., Tzekov, A., Bensch, K. G., and Bickel, P. E. (2003) Adipocyte protein S3-12 coats nascent lipid droplets. J. Biol. Chem. 278, 37713-37721
9. Londos, C., Sztalryd, C., Tansey, J. T., and Kimmel, A. R. (2005) Role of PAT proteins in lipid metabolism. Biochimie (Paris) 87, 45-49
10. Liu, P., Ying, Y., Zhao, Y., Mundy, D. I., Zhu, M., and Anderson, R. G. (2004) Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 279, 3787-3792
11. Umlauf, E., Csaszar, E., Moertelmaier, M., Schuetz, G. J., Parton, R. G., and Prohaska, R. (2004) Association of stomatin with lipid bodies. J. Biol. Chem. 279, 23699-23709
12. Fujimoto, Y., Itabe, H., Sakai, J., Makita, M., Noda, J., Mori, M., Higashi, Y., Kojima, S., and Takano, T. (2004) Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. Biochim. Biophys. Acta 1644, 47-59
13. Sato, S., Fukasawa, M., Yamakawa, Y., Natsume, T., Suzuki, T., Shoji, I., Aizaki, H., Miyamura, T., and Nishijima, M. (2006) Proteomic profiling of lipid droplet proteins in hepatoma cell lines expressing hepatitis C virus core protein. J. Biochem. (Tokyo) 139, 921-930
14. Brasaemle, D. L., Dolios, G., Shapiro, L., and Wang, R. (2004) Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 279, 46835-46842
15. Martin, S., Driessen, K., Nixon, S. J., Zerial, M., and Parton, R. G. (2005) Regulated localization of Rab18 to lipid droplets: Effects of lipolytic stimulation and inhibition of lipid droplet catabolism. J. Biol. Chem. 280, 42405-42419
16. Robenek, H., Lorkowski, S., Schnoor, M., and Troyer, D. (2005) Spatial integration of TIP47 and adipophilin in macrophage lipid bodies. J. Biol. Chem. 280, 5789-5794
17. Robenek, M. J., Severs, N. J., Schlattmann, K., Plenz, G., Zimmer, K. P., Troyer, D., and Robenek, H. (2004) Lipids partition caveolin-1 from ER membranes into lipid droplets: updating the model of lipid droplet biogenesis. FASEB J. 18, 866-868
18. Robenek, H., Robenek, M. J., and Troyer, D. (2005) PAT family proteins pervade lipid droplet cores. J. Lipid Res. 46, 1331-1338
19. Pacheco, P., Bozza, F. A., Gomes, R. N., Bozza, M., Weller, P. F., Castro-Faria-Neto, H. C., and Bozza, P. T. (2002) Lipopolysaccharide-induced leukocyte lipid body formation in vivo: innate immunity elicited intracellular loci involved in eicosanoid metabolism. J. Immunol. 169, 6498-6506
20. D'Avila, 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-Guerin induces TLR2-mediated formation of lipid bodies: Intracellular domains for eicosanoid synthesis in vivo. J. Immunol. 176, 3087-3097
21. Bozza, P. T., Payne, J. L., Goulet, J. L., and Weller, P. F. (1996) Mechanisms of platelet-activating factor-induced lipid body formation: requisite roles for 5-lipoxygenase and de novo protein synthesis in the compartmentalization of neutrophil lipids. J. Exp. Med. 183, 1515-1525
22. Bozza, P. T., Yu, W., Penrose, J. F., Morgan, E. S., Dvorak, A. M., and Weller, P. F. (1997) Eosinophil lipid bodies: specific, inducible intracellular sites for enhanced eicosanoid formation. J. Exp. Med. 186, 909-920
23. Bandeira-Melo, C., Phoofolo, M., and Weller, P. F. (2001) 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. 276, 22779-22787
24. Weller, P. F., Monahan-Earley, R. A., Dvorak, H. F., and Dvorak, A. M. (1991) Cytoplasmic lipid bodies of human eosinophils. Subcellular isolation and analysis of arachidonate incorporation. Am. J. Pathol. 138, 141-148
25. Triggiani, M., Oriente, A., Seeds, M. C., Bass, D. A., Marone, G., and Chilton, F. H. (1995) Migration of human inflammatory cells into the lung results in the remodeling of arachidonic acid into a triglyceride pool. J. Exp. Med. 182, 1181-1190
26. Yu, W., Bozza, P. T., Tzizik, D. M., Gray, J. P., Cassara, J., Dvorak, A. M., and Weller, P. F. (1998) Co-compartmentalization of MAP kinases and cytosolic phospholipase A2 at cytoplasmic arachidonate-rich lipid bodies. Am.. J. Pathol. 152, 759-769
27. Dvorak, A. M., Morgan, E., Schleimer, R. P., Ryeom, S. W., Lichtenstein, L. M., and Weller, P. F. (1992) 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. 40, 759-769
28. Dvorak, A. M., Morgan, E. S., Tzizik, D. M., and Weller, P. F. (1994) Prostaglandin endoperoxide synthase (cyclooxygenase): ultrastructural localization to nonmembrane-bound cytoplasmic lipid bodies in human eosinophils and 3T3 fibroblasts. Int. Arch. Allergy Immunol. 105, 245-250
29. Bozza, P. T., Payne, J. L., Morham, S. G., Langenbach, R., Smithies, O., and Weller, P. F. (1996) Leukocyte lipid body formation and eicosanoid generation: cyclooxygenase-independent inhibition by aspirin. Proc. Natl. Acad. Sci. U. S. A. 93, 11091-11096
30. Meadows, J. W., Pitzer, B., Brockman, D. E., and Myatt, L. (2005) Expression and localizatio of adipophilin and perilipin in human fetal membranes: association with lipid bodies and enzymes involved in prostaglandin synthesis. J. Clin. Endocrinol. Metab. 90, 2344-2350
31. Arend, A., Masso, R., Masso, M., and Selstam, G. (2004) Electron microscope immunocytochemical localization of cyclooxygenase-1 and -2 in pseudopregnant rat corpus luteum during luteolysis. Prostaglandins Other Lipid Mediat. 74, 1-10
32. Van Manen, H. J., Kraan, Y. M., Roos, D., and Otto, C. (2005) Single-cell Raman and fluorescence microscopy reveal the association of lipid bodies with phagosomes in leukocytes. Proc. Natl. Acad. Sci. U. S. A. 102, 10159-10164
33. Beil, W. J., Weller, P. F., Peppercorn, M. A., Galli, S. J., and Dvorak, A. M. (1995) Ultrastructural immunogold localization of subcellular sites of TNF-alpha in colonic Crohn's disease. J. Leukoc. Biol. 58, 284-298
34. Dvorak, A. M., Morgan, E. S., and Weller, P. F. (2001) Ultrastructural immunolocalization of basic fibroblast growth factor to lipid bodies and secretory granules in human mast cells. Histochem. J. 33, 397-402
35. Yu, W., Cassara, J., and Weller, P. F. (2000) Phosphatidylinositide 3-kinase localizes to cytoplasmic lipid bodies in human polymorphonuclear leukocytes and other myeloid-derived cells. Blood 95, 1078-1085
36. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
37. Peng, J., and Gygi, S. P. (2001) Proteomics: the move to mixtures. J. Mass Spectrom. 36, 1083-1091
38. Persson, B., and Argos, P. (1994) Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J. Mol. Biol. 237, 182-192
39. Melo, R. C. N., Perez, S. A. C., Spencer, L. A., Dvorak, A. M., and Weller, P. F. (2005) Intragranular vesiculotubular compartments are involved in piecemeal degranulation by activated human eosinophils. Traffic 6, 866-879
40. Weller, P. F., Ackerman, S. J., Nicholson-Weller, A., and Dvorak, A. M. (1989) Cytoplasmic lipid bodies of human neutrophilic leukocytes. Am.. J. Pathol. 135, 947-959
41. 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
42. Bandeira-Melo, C., Bozza, P. T., and Weller, P. F. (2002) The cellular biology of eosinophil eicosanoid formation and function. J. Allergy Clin. Immunol. 109, 393-400
43. Lefevre, C., Jobard, F., Caux, F., Bouadjar, B., Karaduman, A., Heilig, R., Lakhdar, H., Wollenberg, A., Verret, J. L., Weissenbach, J., et al. (2001) Mutations in CGI-58, the gene encoding a new protein of the esterase/lipase/ thioesterase subfamily, in Chanarin-Dorfman syndrome. Am.. J. Hum. Genet. 69, 1002-1012
44. Ozeki, S., Cheng, J., Tauchi-Sato, K., Hatano, N., Taniguchi, H., and Fujimoto, T. (2005) Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J. Cell Sci. 118, 2601-2611
45. Hayess, K., Kraft, R., Sachsinger, J., Janke, J., Beckmann, G., Rohde, K., Jandrig, B., and Benndorf, R. (1998) Mammalian protein homologous to VAT-1 of Torpedo californica: isolation from Ehrlich ascites tumor cells, biochemical characterization, and organization of its gene. J. Cell. Biochem. 69, 304-315
46. 2+-binding protein, p22, is required for constitutive membrane traffic. J. Biol. Chem. 271, 10183-10187
47. 2+-binding requirements. Mol. Biol. Cell. 15, 481-496
48. Andrade, J., Pearce, S. T., Zhao, H., and Barroso, M. (2004) Interactions among p22, glyceraldehyde-3-phosphate dehydrogenase and microtubules. Biochem. J. 384, 327-336
49. Marshall, K. R., Gong, M., Wodke, L., Lamb, J. H., Jones, D. J., Farmer, P. B., Scrutton, N. S., and Munro, A. W. (2005) The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity. J. Biol. Chem. 280, 30735-30740
50. Blum, R., Feick, P., Puype, M., Vandekerckhove, J., Klengel, R., Nastainczyk, W., and Schulz, I. (1996) Tmp21 and p24A, two type I proteins enriched in pancreatic microsomal membranes, are members of a protein family involved in vesicular trafficking. J. Biol. Chem. 271, 17183-17189
51. Yamaguchi, T., Omatsu, N., Omukae, A., and Osumi, T. (2006) Analysis of interaction partners for perilipin and ADRP on lipid droplets. Mol. Cell Biochem. 284, 167-173
52. Zhang, Q., Ye, M., Wu, X., Ren, S., Zhao, M., Zhao, C., Fu, G., Shen, Y., Fan, H., Lu, G., et al. (2000) Cloning and functional analysis of cDNAs with open reading frames for 300 previously undefined genes expressed in CD34+ haematopoietic stem/progenitor cells. Genome Res. 10, 1546-1560
53. Roulin, K., Hagens, G., Hotz, R., Saurat, J. H., Veerkamp, J. H., and Siegenthaler, G. (1999) The fatty acid-binding heterocomplex FA-p34 formed by S100A8 and S100A9 is the major fatty acid carrier in neutrophils and translocates from the cytosol to the membrane upon stimulation. Exp. Cell Res. 247, 410-421
54. Kerkhoff, C., Klempt, M., Kaever, V., and Sorg, C. (1999) The two calcium-binding proteins, S100A8 and S100A9, are involved in the metabolism of arachidonic acid in human neutrophils. J. Biol. Chem. 274, 32672-32679
55. Berthier, S., Paclet, M. H., Lerouge, S., Roux, F., Vergnaud, S., Coleman, A. W., and Morel, F. (2003) Changing the conformation state of cytochrome b558 initiates NADPH oxidase activation: MRP8/MRP14 regulation. J. Biol. Chem. 278, 25499-25508
56. Chilton, F. H., and Murphy, R. C. (1986) Remodeling of arachidonate-containing phosphoglycerides within the human neutrophil. J. Biol. Chem. 261, 7771-7777
57. Beller, M., Riedel, D., Jansch, L., Dieterich, G., Wehland, J., Jackle, H., and Kuhnlein, R. P. (2006) Characterization of the Drosophila lipid droplet subproteome. Mol. Cell. Proteomics 5, 1082-1094
58. Binns, D., Januszewski, T., Chen, Y., Hill, J., Markin, V. S., Zhao, Y., Gilpin, C., Chapman, K. D., Anderson, R. G., and Goodman, J. M. (2006) An intimate collaboration between peroxisomes and lipid bodies. J. Cell Biol. 173, 719-731
59. Dvorak, A. M., Morgan, E. S., and Weller, P. F. (2003) RNA is closely associated with human mast cell lipid bodies. Histol. Histopathol. 18, 943-968
60. Dvorak, A. M. (2005) Mast cell secretory granules and lipid bodies contain the necessary machinery important for the in situ synthesis of proteins. Chem. Immunol. Allergy 85, 252-315
61. Smith, W. L., DeWitt, D. L., and Garavito, R. M. (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 69, 145-182
62. Paciga, M., McCudden, C. R., Londos, C., DiMattia, G. E., and Wagner, G. F. (2003) Targeting of big stanniocalcin and its receptor to lipid storage droplets of ovarian steroidogenic cells. J. Biol. Chem. 278, 49549-49554
63. Wolins, N. E., Rubin, B., and Brasaemle, D. L. (2001) TIP47 associates with lipid droplets. J. Biol. Chem. 276, 5101-5108
64. Than, N. G., Sumegi, B., Bellyei, S., Berki, T., Szekeres, G., Janaky, T., Szigeti, A., Bohn, H., and Than, G. N. (2003) Lipid droplet and milk lipid globule membrane associated placental protein 17b (PP17b) is involved in apoptotic and differentiation processes of human epithelial cervical carcinoma cells. Eur. J. Biochem. 270, 1176-1188
65. Yamaguchi, T., Omatsu, N., Matsushita, S., and Osumi, T. (2004) CGI-58 interacts with perilipin and is localized to lipid droplets. Possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome. J. Biol. Chem. 279, 30490-30497
66. Subramanian, V., Rothenberg, A., Gomez, C., Cohen, A. W., Garcia, A., Bhattacharyya, S., Shapiro, L., Dolios, G., Wang, R., Lisanti, M. P., and Brasaemle, D. L. (2004) Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes. J. Biol. Chem. 279, 42062-42071
67. Zimmermann, R., Strauss, J. G., Haemmerle, G., Schoiswohl, G., Birner-Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., and Zechner, R. (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306, 1383-1386
68. Smirnova, E., Goldberg, E. B., Makarova, K. S., Lin, L., Brown, W. J., and Jackson, C. L. (2006) ATGL has a key role in lipid droplet/adiposome degradation in mammalian cells. EMBO Rep. 7, 106-113
69. Ohashi, M., Mizushima, N., Kabeya, Y., and Yoshimori, T. (2003) Localization of mammalian NAD(P)H steroid dehydrogenase-like protein on lipid droplets. J. Biol. Chem. 278, 36819-36829
70. Caldas, H., and Herman, G. E. (2003) NSDHL, an enzyme involved in cholesterol biosynthesis, traffics through the Golgi and accumulates on ER membranes and on the surface of lipid droplets. Hum. Mol Genet. 12, 2981-2991
71. Fong, T. H., Wu, C. H., Liao, E. W., Chang, C. Y., Pai, M. H., Chiou, R. J., and Lee, A. W. (2001) Association of globular beta-actin with intracellular lipid droplets in rat adrenocortical cells and adipocytes. Biochem. Biophys. Res. Commun. 289, 1168-1174
72. Wu, C. C., Howell, K. E., Neville, M. C., Yates III, J. R., and McManaman, J. L. (2000) Proteomics reveal a link between the endoplasmic reticulum and lipid secretory mechanisms in mammary epithelial cells. Electrophoresis 21, 3470-3482
73. Prattes, S., Horl, G., Hammer, A., Blaschitz, A., Graier, W. F., Sattler, W., Zechner, R., and Steyrer, E. (2000) Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: triglyceride droplets are surrounded by cholesterolrich ER-like surface layer structures. J. Cell Sci. 113, 2977-2989