Lipid droplets in activated mast cells – a significant source of triglyceride-derived arachidonic acid for eicosanoid production

European Journal of Pharmacology

Volumn 785, Issue , 2016, Pages 59-69

  Dichlberger, Andrea ^a,c   Schlager, Stefanie ^b,c   Kovanen, Petri T ^a,c   Schneider, Wolfgang J ^a,b,c  

^a WIHURI RESEARCH INSTITUTE   (Finland)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Adipose triglyceride lipase; Arachidonic acid; Eicosanoids; Lipid droplets; Mast cells; Triglycerides

Indexed keywords

ADIPOSE TRIGLYCERIDE LIPASE; ARACHIDONIC ACID; FAT DROPLET; ICOSANOID; LONG CHAIN ACYL COA SYNTHASE; PHOSPHOLIPASE; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID; PROSTAGLANDIN D2; SYNTHETASE; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVATION; CELL FUNCTION; CELL HOMING; CELL MATURATION; CELL STRUCTURE; FATTY ACID SYNTHESIS; HUMAN; IMMUNOMODULATION; LIPID STORAGE; MAST CELL; NONHUMAN; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SECRETORY GRANULE; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; CYTOLOGY; IMMUNOLOGY; METABOLISM;

ANIMALS; ARACHIDONIC ACID; EICOSANOIDS; HUMANS; LIPID DROPLETS; MAST CELLS; TRIGLYCERIDES;

EID: 84979939306     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2015.07.020     Document Type: Article

References (150)

1. Allen, S., Dashwood, M., Morrison, K., Yacoub, M., Differential leukotriene constrictor responses in human atherosclerotic coronary arteries. Circulation 97 (1998), 2406–2413.
2. Andersen, H.B., Holm, M., Hetland, T.E., Dahl, C., Junker, S., Schiøtz, P.O., Hoffmann, H.J., Comparison of short term in vitro cultured human mast cells from different progenitors – peripheral blood-derived progenitors generate highly mature and functional mast cells. J. Immunol. Methods 336 (2008), 166–174, 10.1016/j.jim.2008.04.016.
3. Aoki, N., Jin-no, S., Nakagawa, Y., Asai, N., Arakawa, E., Tamura, N., Tamura, T., Matsuda, T., Identification and characterization of microvesicles secreted by 3T3-L1 adipocytes: redox- and hormone-dependent induction of milk fat globule-epidermal growth factor 8-associated microvesicles. Endocrinology 148 (2007), 3850–3862.
4. Araújo-Santos, T., Prates, D.B., Andrade, B.B., Nascimento, D.O., Clarêncio, J., Entringer, P.F., Carneiro, A.B., Silva-Neto, M.A.C., Miranda, J.C., Brodskyn, C.I., Barral, A., Bozza, P.T., Borges, V.M., Lutzomyia longipalpis saliva triggers lipid body formation and prostaglandin E2 production in murine macrophages. PLoS Negl. Trop. Dis., 4, 2010, e873, 10.1371/journal.pntd.0000873.
5. Azouz, N.P., Matsui, T., Fukuda, M., Sagi-Eisenberg, R., Decoding the regulation of mast cell exocytosis by networks of Rab GTPases. J. Immunol. 189 (2012), 2169–2180.
6. Barber, E., Sinclair, A.J., Cameron-Smith, D., Comparative actions of omega-3 fatty acids on in-vitro lipid droplet formation. Prostaglandins Leukot. Essent. Fatty Acids 89 (2013), 359–366, 10.1016/j.plefa.2013.07.006.
7. Bartz, R., Li, W.-H., Venables, B., Zehmer, J.K., Roth, M.R., Welti, R., Anderson, R.G.W., Liu, P., Chapman, K.D., Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic. J. Lipid Res. 48 (2007), 837–847, 10.1194/jlr.M600413-JLR200.
8. Basiouni, S., Fuhrmann, H., Schumann, J., The influence of polyunsaturated fatty acids on the phospholipase d isoforms trafficking and activity in mast cells. Int. J. Mol. Sci. 14 (2013), 9005–9017, 10.3390/ijms14059005.
9. Basiouni, S., Stöckel, K., Fuhrmann, H., Schumann, J., Polyunsaturated fatty acid supplements modulate mast cell membrane microdomain composition. Cell. Immunol. 275 (2012), 42–46, 10.1016/j.cellimm.2012.03.004.
10. Beasley, R., Hovel, C., Mani, R., Robinson, C., Varley, J., Holgate, S.T., Comparative vascular effects of histamine, prostaglandin (PG) D2 and its metabolite 9 alpha,11 beta-PGF2 in human skin. Clin. Allergy 18 (1988), 619–627.
11. Beil, W.J., Weller, P.F., Peppercorn, M.A., Galli, S.J., Dvorak, A.M., Ultrastructural immunogold localization of subcellular sites of TNF-alpha in colonic Crohn's disease. J. Leukoc. Biol. 58 (1995), 284–298.
12. Beller, M., Thiel, K., Thul, P.J., Jäckle, H., Lipid droplets: a dynamic organelle moves into focus. FEBS Lett. 584 (2010), 2176–2182, 10.1016/j.febslet.2010.03.022.
13. Benditt, E.P., Arase, M., An enzyme in mast cells with properties like chymotrypsin. J. Exp. Med. 110 (1959), 451–460.
14. Blaner, W.S., O'Byrne, S.M., Wongsiriroj, N., Kluwe, J., D'Ambrosio, D.M., Jiang, H., Schwabe, R.F., Hillman, E.M., Piantedosi, R., Libien, J., Hepatic stellate cell lipid droplets: a specialized lipid droplet for retinoid storage. Biochim. Biophys. Acta 1791 (2009), 467–473.
15. Blank, U., Madera-Salcedo, I.K., Danelli, L., Claver, J., Tiwari, N., Sánchez-Miranda, E., Vázquez-Victorio, G., Ramírez-Valadez, K.A., Macias-Silva, M., González-Espinosa, C., Vesicular trafficking and signaling for cytokine and chemokine secretion in mast cells. Front. Immunol., 5, 2014, 453, 10.3389/fimmu.2014.00453.
16. Bot, I., Shi, G.-P., Kovanen, P.T., Mast cells as effectors in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 35 (2015), 265–271, 10.1161/ATVBAHA.114.303570.
17. Boyce, J.A., Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunol. Rev. 217 (2007), 168–185, 10.1111/j.1600-065X.2007.00512.x.
18. Bozza, P.T., Bakker-Abreu, I., Navarro-Xavier, R.A., Bandeira-Melo, C., Lipid body function in eicosanoid synthesis: an update. Prostaglandins Leukot. Essent. Fat. Acids 85 (2011), 205–213.
19. Bozza, P.T., Magalhaes, K.G., Weller, P.F., Leukocyte lipid bodies – biogenesis and functions in inflammation. Biochim. Biophys. Acta 1791 (2009), 540–551 S1388-1981(09)00008-0 [pii] 10.1016/j.bbalip.2009.01.005.
20. Brasaemle, D.L., Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J. Lipid Res. 48 (2007), 2547–2559 doi:R700014-JLR200 [pii] 10.1194/jlr.R700014-JLR200.
21. Brasaemle, D.L., Dolios, G., Shapiro, L., Wang, R., Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 279 (2004), 46835–46842, 10.1074/jbc.M409340200.
22. Campagna, F., Nanni, L., Quagliarini, F., Pennisi, E., Michailidis, C., Pierelli, F., Bruno, C., Casali, C., DiMauro, S., Arca, M., Novel mutations in the adipose triglyceride lipase gene causing neutral lipid storage disease with myopathy. Biochem. Biophys. Res. Commun. 377 (2008), 843–846, 10.1016/j.bbrc.2008.10.081.
23. Chilton, F.H., Connell, T.R., 1-ether-linked phosphoglycerides. Major endogenous sources of arachidonate in the human neutrophil. J. Biol. Chem. 263 (1988), 5260–5265.
24. Chock, S.P., Rhee, S.G., Tang, L.C., Schmauder-Chock, E.A., Linking phospholipase A2 to phospholipid turnover and prostaglandin synthesis in mast cell granules. Eur. J. Biochem. 195 (1991), 707–713.
25. Choi, H.W., Abraham, S.N., Mast cell mediator responses and their suppression by pathogenic and commensal microorganisms. Mol. Immunol. 63 (2015), 74–79, 10.1016/j.molimm.2014.02.006.
26. Christie, P.E., Schmitz-Schumann, M., Spur, B.W., Lee, T.H., Airway responsiveness to leukotriene C4 (LTC4), leukotriene E4 (LTE4) and histamine in aspirin-sensitive asthmatic subjects. Eur. Respir. J. 6 (1993), 1468–1473.
27. Dahlén, S.E., Björk, J., Hedqvist, P., Arfors, K.E., Hammarström, S., Lindgren, J.A., Samuelsson, B., Leukotrienes promote plasma leakage and leukocyte adhesion in postcapillary venules: in vivo effects with relevance to the acute inflammatory response. Proc. Natl. Acad. Sci. USA 78 (1981), 3887–3891.
28. Dahlin, J.S., Hallgren, J., Mast cell progenitors: origin, development and migration to tissues. Mol. Immunol. 63 (2015), 9–17, 10.1016/j.molimm.2014.01.018.
29. Davey, A.M., Krise, K.M., Sheets, E.D., Heikal, A.A., Molecular perspective of antigen-mediated mast cell signaling. J. Biol. Chem. 283 (2008), 7117–7127, 10.1074/jbc.M708879200.
30. De Paulis, A., Marinò, I., Ciccarelli, A., de Crescenzo, G., Concardi, M., Verga, L., Arbustini, E., Marone, G., Human synovial mast cells. I. Ultrastructural in situ and in vitro immunologic characterization. Arthritis Rheumatol. 39 (1996), 1222–1233.
31. Dichlberger, A., Kovanen, P.T., Schneider, W.J., Mast cells: from lipid droplets to lipid mediators. Clin. Sci. 1979:125 (2013), 121–130, 10.1042/CS20120602.
32. Dichlberger, A., Schlager, S., Lappalainen, J., Kakela, R., Hattula, K., Butcher, S.J., Schneider, W.J., Kovanen, P.T., Lipid body formation during maturation of human mast cells. J. Lipid Res. 52 (2011), 2198–2208.
33. Dichlberger, A., Schlager, S., Maaninka, K., Schneider, W.J., Kovanen, P.T., Adipose triglyceride lipase regulates eicosanoid production in activated human mast cells. J. Lipid Res. 55 (2014), 2471–2478, 10.1194/jlr.M048553.
34. Ducharme, N.A., Bickel, P.E., Lipid droplets in lipogenesis and lipolysis. Endocrinology 149 (2008), 942–949 doi:en.2007-1713 [pii] 10.1210/en.2007-1713.
35. Dvorak, A.M., Mast cell secretory granules and lipid bodies contain the necessary machinery important for the in situ synthesis of proteins. Chem. Immunol. Allergy 85 (2005), 252–315 doi:86520 [pii] 10.1159/000086520.
36. Dvorak, A.M., Ultrastructural studies of human basophils and mast cells. J. Histochem. Cytochem. 53 (2005), 1043–1070 doi:jhc.5R6647.2005 [pii] 10.1369/jhc.5R6647.2005.
37. Dvorak, A.M., Ultrastructure of human mast cells. Int. Arch. Allergy Immunol. 127 (2002), 100–105 doi:iaa27100 [pii].
38. Dvorak, A.M., Ultrastructural analysis of human mast cells and basophils. Marone, G., (eds.) Human Basophils and Mast Cells: Biological Aspects, 1995.
39. Dvorak, A.M., 1992. Human mast cells. Ultrastructural observations of in situ, ex vivo and in vitro sites, sources and systems. In: Lainer, M., Metcalfe, D.D. (Eds.), The Mast Cell in Health and Disease. Marcel Dekker Inc., New York, pp. 1–90.
40. Dvorak, A.M., Dvorak, H.F., Peters, S.P., Shulman, E.S., W. Jr, M.D., Pyne, K., Harvey, V.S., Galli, S.J., Lichtenstein, L.M., Lipid bodies: cytoplasmic organelles important to arachidonate metabolism in macrophages and mast cells. J. Immunol. 131 (1983), 2965–2976.
41. Dvorak, A.M., Hammel, I., Schulman, E.S., Peters, S.P., W. Jr, M.D., Schleimer, R.P., Newball, H.H., Pyne, K., Dvorak, H.F., Lichtenstein, L.M., Differences in the behavior of cytoplasmic granules and lipid bodies during human lung mast cell degranulation. J. Cell Biol. 99 (1984), 1678–1687.
42. Dvorak, A.M., Kissell, S., Granule changes of human skin mast cells characteristic of piecemeal degranulation and associated with recovery during wound healing in situ. J. Leukoc. Biol. 49 (1991), 197–210.
43. Dvorak, A.M., Massey, W., Warner, J., Kissell, S., Kagey-Sobotka, A., Lichtenstein, L.M., IgE-mediated anaphylactic degranulation of isolated human skin mast cells. Blood 77 (1991), 569–578.
44. Dvorak, A.M., Morgan, E.S., Weller, P.F., RNA is closely associated with human mast cell lipid bodies. Histol. Histopathol. 18 (2003), 943–968.
45. Eichmann, T.O., Kumari, M., Haas, J.T., V. Jr, F.R., Zimmermann, R., Lass, A., Zechner, R., Studies on the substrate and stereo/regioselectivity of adipose triglyceride lipase, hormone-sensitive lipase, and diacylglycerol-O-acyltransferases. J. Biol. Chem. 287 (2012), 41446–41457 doi:M112.400416 [pii] 10.1074/jbc.M112.400416.
46. Enerbäck, L., Pipkorn, U., Olofsson, A., Intraepithelial migration of mucosal mast cells in hay fever: ultrastructural observations. Int. Arch. Allergy Appl. Immunol. 81 (1986), 289–297.
47. Enomoto, A., Murakami, M., Valentin, E., Lambeau, G., Gelb, M.H., Kudo, I., Redundant and segregated functions of granule-associated heparin-binding group II subfamily of secretory phospholipases A2 in the regulation of degranulation and prostaglandin D2 synthesis in mast cells. J. Immunol. 165 (2000), 4007–4014.
48. Fonteh, A.N., Bass, D.A., Marshall, L.A., Seeds, M., Samet, J.M., Chilton, F.H., Evidence that secretory phospholipase A2 plays a role in arachidonic acid release and eicosanoid biosynthesis by mast cells. J. Immunol. 152 (1994), 5438–5446.
49. Fujimoto, T., Kogo, H., Ishiguro, K., Tauchi, K., Nomura, R., Caveolin-2 is targeted to lipid droplets, a new “membrane domain” in the cell. J. Cell. Biol. 152 (2001), 1079–1085.
50. Fujishima, H., Sanchez Mejia, R.O., Bingham, C.O. 3rd, Lam, B.K., Sapirstein, A., Bonventre, J.V., Austen, K.F., Arm, J.P., Cytosolic phospholipase A2 is essential for both the immediate and the delayed phases of eicosanoid generation in mouse bone marrow-derived mast cells. Proc. Natl. Acad. Sci. USA 96 (1999), 4803–4807.
51. Funk, C.D., Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294 (2001), 1871–1875 doi:10.1126/science.294.5548.1871 294/5548/1871 [pii].
52. Galli, S.J., Borregaard, N., Wynn, T.A., Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat. Immunol. 12 (2011), 1035–1044, 10.1038/ni.2109.
53. Galli, S.J., Nakae, S., Tsai, M., Mast cells in the development of adaptive immune responses. Nat. Immunol. 6 (2005), 135–142, 10.1038/ni1158.
54. Galli, S.J., Tsai, M., IgE and mast cells in allergic disease. Nat. Med. 18 (2012), 693–704 doi:nm.2755 [pii] 10.1038/nm.2755.
55. Galli, S.J., Tsai, M., Wershil, B.K., Tam, S.Y., Costa, J.J., Regulation of mouse and human mast cell development, survival and function by stem cell factor, the ligand for the c-kit receptor. Int. Arch. Allergy Immunol. 107 (1995), 51–53.
56. Garcia-Gil, M., Siraganian, R.P., Source of the arachidonic acid released on stimulation of rat basophilic leukemia cells. J. Immunol. 136 (1986), 3825–3828.
57. Ghosh, M., Tucker, D.E., Burchett, S.A., Leslie, C.C., Properties of the Group IV phospholipase A2 family. Prog. Lipid Res. 45 (2006), 487–510, 10.1016/j.plipres.2006.05.003.
58. Glenner, G.G., Cohen, L.A., Histochemical demonstration of a species-specific trypsin-like enzyme in mast cells. Nature 185 (1960), 846–847.
59. Goetzl, E.J., An, S., Diversity of cellular receptors and functions for the lysophospholipid growth factors lysophosphatidic acid and sphingosine 1-phosphate. FASEB J. 12 (1998), 1589–1598.
60. Golej, D.L., Askari, B., Kramer, F., Barnhart, S., Vivekanandan-Giri, A., Pennathur, S., Bornfeldt, K.E., Long-chain acyl-CoA synthetase 4 modulates prostaglandin E2 release from human arterial smooth muscle cells. J. Lipid Res. 52 (2011), 782–793, 10.1194/jlr.M013292.
61. Goodman, J.M., The gregarious lipid droplet. J. Biol. Chem. 283 (2008), 28005–28009.
62. Granata, F., Nardicchi, V., Loffredo, S., Frattini, A., Ilaria Staiano, R., Agostini, C., Triggiani, M., Secreted phospholipases A(2): a proinflammatory connection between macrophages and mast cells in the human lung. Immunobiology 214 (2009), 811–821 doi:S0171-2985(09)00109-0 [pii] 10.1016/j.imbio.2009.06.006.
63. Greineisen, W.E., Shimoda, L.M., Maaetoft-Udsen, K., Turner, H., Insulin-containing lipogenic stimuli suppress mast cell degranulation potential and up-regulate lipid body biogenesis and eicosanoid secretion in a PPARgamma-independent manner. J. Leukoc. Biol. 92 (2012), 653–665.
64. Gueck, T., Seidel, A., Fuhrmann, H., Effects of essential fatty acids on mediators of mast cells in culture. Prostaglandins Leukot. Essent. Fat. Acids 68 (2003), 317–322.
65. Haas, R., Heinrich, P.C., Sasse, D., Proteolytic enzymes of rat liver mitochondria. Evidence for a mast cell origin. FEBS Lett. 103 (1979), 168–171.
66. Hagenlocher, Y., Lorentz, A., Immunomodulation of mast cells by nutrients. Mol. Immunol. 63 (2015), 25–31, 10.1016/j.molimm.2013.12.005.
67. Hammel, I., Dvorak, A.M., Peters, S.P., Schulman, E.S., Dvorak, H.F., Lichtenstein, L.M., Galli, S.J., Differences in the volume distributions of human lung mast cell granules and lipid bodies: evidence that the size of these organelles is regulated by distinct mechanisms. J. Cell Biol. 100 (1985), 1488–1492.
68. Henderson, W.R., Chi, E.Y., Degranulation of cystic fibrosis nasal polyp mast cells. J. Pathol. 166 (1992), 395–404, 10.1002/path.1711660412.
69. Hevonoja, T., Pentikäinen, M.O., Hyvönen, M.T., Kovanen, P.T., Ala-Korpela, M., Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim. Biophys. Acta 1488 (2000), 189–210.
70. Ibarguren, M., López, D.J., Escribá, P.V., The effect of natural and synthetic fatty acids on membrane structure, microdomain organization, cellular functions and human health. Biochim. Biophys. Acta 1838 (2014), 1518–1528, 10.1016/j.bbamem.2013.12.021.
71. Igal, R.A., Wang, P., Coleman, R.A., Triacsin C blocks de novo synthesis of glycerolipids and cholesterol esters but not recycling of fatty acid into phospholipid: evidence for functionally separate pools of acyl-CoA. Biochem. J. 324:Pt 2 (1997), 529–534.
72. Irani, A.A., Schechter, N.M., Craig, S.S., DeBlois, G., Schwartz, L.B., Two types of human mast cells that have distinct neutral protease compositions. Proc. Natl. Acad. Sci. USA 83 (1986), 4464–4468.
73. Irani, A.M., Bradford, T.R., Kepley, C.L., Schechter, N.M., Schwartz, L.B., Detection of MCT and MCTC types of human mast cells by immunohistochemistry using new monoclonal anti-tryptase and anti-chymase antibodies. J. Histochem. Cytochem. 37 (1989), 1509–1515.
74. Juremalm, M., Nilsson, G., Chemokine receptor expression by mast cells. Chem. Immunol. Allergy 87 (2005), 130–144, 10.1159/000087640.
75. Kennerly, D.A., Phosphatidylcholine is a quantitatively more important source of increased 1,2-diacylglycerol than is phosphatidylinositol in mast cells. J. Immunol. 144 (1990), 3912–3919.
76. Kennerly, D.A., Diacylglycerol metabolism in mast cells. Analysis of lipid metabolic pathways using molecular species analysis of intermediates. J. Biol. Chem. 262 (1987), 16305–16313.
77. Kimmel, A.R., Brasaemle, D.L., McAndrews-Hill, M., Sztalryd, C., Londos, C., Adoption of PERILIPIN as a unifying nomenclature for the mammalian PAT-family of intracellular lipid storage droplet proteins. J. Lipid Res. 51 (2010), 468–471, 10.1194/jlr.R000034.
78. Kitamura, Y., Go, S., Hatanaka, K., Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood 52 (1978), 447–452.
79. Kitatani, K., Akiba, S., Sato, T., Role of phospholipase d-derived phosphatidic acid as a substrate for phospholipase A2 in RBL-2H3 cells. Biol. Pharm. Bull. 23 (2000), 1430–1433.
80. Kobayashi, K., Inoguchi, T., Maeda, Y., Nakashima, N., Kuwano, A., Eto, E., Ueno, N., Sasaki, S., Sawada, F., Fujii, M., Matoba, Y., Sumiyoshi, S., Kawate, H., Takayanagi, R., The lack of the C-terminal domain of adipose triglyceride lipase causes neutral lipid storage disease through impaired interactions with lipid droplets. J. Clin. Endocrinol. Metab. 93 (2008), 2877–2884 doi:10.1210/jc.2007-2247; 10.1210/jc.2007-2247.
81. Kovanen, P.T., Mast cells: multipotent local effector cells in atherothrombosis. Immunol. Rev. 217 (2007), 105–122 doi:IMR515 [pii] 10.1111/j.1600-065X.2007.00515.x.
82. Kumar, V., Butcher, S.J., Öörni, K., Engelhardt, P., Heikkonen, J., Kaski, K., Ala-Korpela, M., Kovanen, P.T., Three-dimensional cryoEM reconstruction of native LDL particles to 16 Å resolution at physiological body temperature. PLoS One, 6, 2011, e18841, 10.1371/journal.pone.0018841.
83. Lappalainen, J., Lindstedt, K.A., Kovanen, P.T., A protocol for generating high numbers of mature and functional human mast cells from peripheral blood. Clin. Exp. Allergy 37 (2007), 1404–1414 doi:CEA2778 [pii] 10.1111/j.1365-2222.2007.02778.x.
84. Le Lay, S., C, M.B., Hajduch, E., Dugail, I., Filling up adipocytes with lipids. Lessons from caveolin-1 deficiency. Biochim. Biophys. Acta 1791 (2009), 514–518.
85. Lennartsson, J., Rönnstrand, L., Stem cell factor receptor/c-Kit: from basic science to clinical implications. Physiol. Rev. 92 (2012), 1619–1649, 10.1152/physrev.00046.2011.
86. Li, L., Meng, X.W., Krilis, S.A., Mast cells expressing chymase but not tryptase can be derived by culturing human progenitors in conditioned medium obtained from a human mastocytosis cell strain with c-kit ligand. J. Immunol. 156 (1996), 4839–4844.
87. Li, L.O., Klett, E.L., Coleman, R.A., Acyl-CoA synthesis, lipid metabolism and lipotoxicity. Biochim. Biophys. Acta 1801 (2010), 246–251, 10.1016/j.bbalip.2009.09.024.
88. Liu, F.-T., Goodarzi, H., Chen, H.-Y., IgE, mast cells, and eosinophils in atopic dermatitis. Clin. Rev. Allergy Immunol. 41 (2011), 298–310, 10.1007/s12016-011-8252-4.
89. Liu, P., Ying, Y., Zhao, Y., Mundy, D.I., Zhu, M., Anderson, R.G.W., Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 279 (2004), 3787–3792, 10.1074/jbc.M311945200.
90. Lundstrom, S.L., Saluja, R., Adner, M., Haeggstrom, J.Z., Nilsson, G.P., Wheelock, C.E., Lipid mediator metabolic profiling demonstrates differences in eicosanoid patterns in two phenotypically distinct mast cell populations. J. Lipid Res. 54 (2013), 116–126 doi:jlr.M030171 [pii] 10.1194/jlr.M030171.
91. Maaninka, K., Lappalainen, J., Kovanen, P.T., Human mast cells arise from a common circulating progenitor. J. Allergy Clin. Immunol., 132, 2013 463–469.e3.
92. Maloberti, P.M., Duarte, A.B., Orlando, U.D., Pasqualini, M.E., Solano, A.R., López-Otín, C., Podestá, E.J., Functional interaction between acyl-CoA synthetase 4, lipooxygenases and cyclooxygenase-2 in the aggressive phenotype of breast cancer cells. PLoS One, 5, 2010, e15540, 10.1371/journal.pone.0015540.
93. Massey, W.A., Guo, C.B., Dvorak, A.M., Hubbard, W.C., Bhagavan, B.S., Cohan, V.L., Warner, J.A., Kagey-Sobotka, A., Lichtenstein, L.M., Human uterine mast cells. Isolation, purification, characterization, ultrastructure, and pharmacology. J. Immunol. 147 (1991), 1621–1627.
94. Melo, R.C., D'Avila, H., Wan, H.C., Bozza, P.T., Dvorak, A.M., Weller, P.F., Lipid bodies in inflammatory cells: structure, function, and current imaging techniques. J. Histochem. Cytochem. 59 (2011), 540–556 doi:0022155411404073 [pii] 10.1369/0022155411404073.
95. Mikl, C., Peters, J., Trapp, M., Kornmueller, K., Schneider, W.J., Prassl, R., Softness of atherogenic lipoproteins: a comparison of very low density lipoprotein (VLDL) and low density lipoprotein (LDL) using elastic incoherent neutron scattering (EINS). J. Am. Chem. Soc. 133 (2011), 13213–13215, 10.1021/ja203679g.
96. Minai-Fleminger, Y., Elishmereni, M., Vita, F., Soranzo, M.R., Mankuta, D., Zabucchi, G., Levi-Schaffer, F., Ultrastructural evidence for human mast cell-eosinophil interactions in vitro. Cell Tissue Res. 341 (2010), 405–415, 10.1007/s00441-010-1010-8.
97. Miyamoto, T., Sasaguri, Y., Sasaguri, T., Azakami, S., Yasukawa, H., Kato, S., Arima, N., Sugama, K., Morimatsu, M., Expression of stem cell factor in human aortic endothelial and smooth muscle cells. Atherosclerosis 129 (1997), 207–213.
98. Moon, T.C., Befus, A.D., Kulka, M., Mast cell mediators: their differential release and the secretory pathways involved. Front. Immunol., 5, 2014, 569, 10.3389/fimmu.2014.00569.
99. Moos, M.P.W., Funk, C.D., Endothelial cysteinyl leukotriene 2 receptor expression and myocardial ischemia/reperfusion injury. Trends Cardiovasc. Med. 18 (2008), 268–273, 10.1016/j.tcm.2008.11.009.
100. Mounier, C.M., Ghomashchi, F., Lindsay, M.R., James, S., Singer, A.G., Parton, R.G., Gelb, M.H., Arachidonic acid release from mammalian cells transfected with human groups IIA and X secreted phospholipase A(2) occurs predominantly during the secretory process and with the involvement of cytosolic phospholipase A(2)-alpha. J. Biol. Chem. 279 (2004), 25024–25038, 10.1074/jbc.M313019200.
101. Müller, G., Jung, C., Straub, J., Wied, S., Kramer, W., Induced release of membrane vesicles from rat adipocytes containing glycosylphosphatidylinositol-anchored microdomain and lipid droplet signalling proteins. Cell Signal. 21 (2009), 324–338, 10.1016/j.cellsig.2008.10.021.
102. Muoio, D.M., Lewin, T.M., Wiedmer, P., Coleman, R.A., Acyl-CoAs are functionally channeled in liver: potential role of acyl-CoA synthetase. Am. J. Physiol. Endocrinol. Metab. 279 (2000), E1366–E1373.
103. Murakami, M., Kudo, I., Umeda, M., Matsuzawa, A., Takeda, M., Komada, M., Fujimori, Y., Takahashi, K., Inoue, K., Detection of three distinct phospholipases A2 in cultured mast cells. J. Biochem. 111 (1992), 175–181.
104. Murakami, M., Taketomi, Y., Miki, Y., Sato, H., Hirabayashi, T., Yamamoto, K., Recent progress in phospholipase A(2) research: from cells to animals to humans. Prog. Lipid Res. 50 (2011), 152–192 doi:S0163-7827(10)00065-2 [pii] 10.1016/j.plipres.2010.12.001.
105. Murphy, S., Martin, S., Parton, R.G., Lipid droplet-organelle interactions; sharing the fats. Biochim. Biophys. Acta 1791 (2009), 441–447.
106. Nilsson, G., Butterfield, J.H., Nilsson, K., Siegbahn, A., Stem cell factor is a chemotactic factor for human mast cells. J. Immunol. 153 (1994), 3717–3723.
107. Obata, T., Nagakura, T., Masaki, T., Maekawa, K., Yamashita, K., Eicosapentaenoic acid inhibits prostaglandin D2 generation by inhibiting cyclo-oxygenase-2 in cultured human mast cells. Clin. Exp. Allergy 29 (1999), 1129–1135.
108. Olofsson, S.-O., Andersson, L., Håversen, L., Olsson, C., Myhre, S., Rutberg, M., Mobini, R., Li, L., Lu, E., Borén, J., Boström, P., The formation of lipid droplets: possible role in the development of insulin resistance/type 2 diabetes. Prostaglandins. Leukot. Essent. Fatty Acids 85 (2011), 215–218, 10.1016/j.plefa.2011.04.019.
109. Olofsson, S.-O., Boström, P., Andersson, L., Rutberg, M., Perman, J., Borén, J., Lipid droplets as dynamic organelles connecting storage and efflux of lipids. Biochim. Biophys. Acta 1791 (2009), 448–458, 10.1016/j.bbalip.2008.08.001.
110. Oörni, K., Kovanen, P.T., Lipoprotein modification by secretory phospholipase A(2) enzymes contributes to the initiation and progression of atherosclerosis. Curr. Opin. Lipidol. 20 (2009), 421–427, 10.1097/MOL.0b013e32832fa14d.
111. Patella, V., Marinò, I., Lampärter, B., Arbustini, E., Adt, M., Marone, G., Human heart mast cells. Isolation, purification, ultrastructure, and immunologic characterization. J. Immunol. 154 (1995), 2855–2865.
112. Peters, S.P., MacGlashan, D.W., Schleimer, R.P., Hayes, E.C., Adkinson, N.F., Lichtenstein, L.M., The pharmacologic modulation of the release of arachidonic acid metabolites from purified human lung mast cells. Am. Rev. Respir. Dis. 132 (1985), 367–373.
113. Poeckel, D., Funk, C.D., The 5-lipoxygenase/leukotriene pathway in preclinical models of cardiovascular disease. Cardiovasc. Res. 86 (2010), 243–253, 10.1093/cvr/cvq016.
114. Pulimood, A.B., Mathan, M.M., Mathan, V.I., Quantitative and ultrastructural analysis of rectal mucosal mast cells in acute infectious diarrhea. Dig. Dis. Sci. 43 (1998), 2111–2116.
115. Qadri, F., Bhuiyan, T.R., Dutta, K.K., Raqib, R., Alam, M.S., Alam, N.H., Svennerholm, A.-M., Mathan, M.M., Acute dehydrating disease caused by Vibrio cholerae serogroups O1 and O139 induce increases in innate cells and inflammatory mediators at the mucosal surface of the gut. Gut 53 (2004), 62–69.
116. Razin, E., Ihle, J.N., Seldin, D., Mencia-Huerta, J.M., Katz, H.R., LeBlanc, P.A., Hein, A., Caulfield, J.P., Austen, K.F., Stevens, R.L., Interleukin 3: a differentiation and growth factor for the mouse mast cell that contains chondroitin sulfate E proteoglycan. J. Immunol. 132 (1984), 1479–1486.
117. Rivera, J., Gilfillan, A.M., Molecular regulation of mast cell activation. J. Allergy Clin. Immunol. 117 (2006), 1214–1225, 10.1016/j.jaci.2006.04.015 quiz 1226.
118. Robenek, H., Buers, I., Hofnagel, O., Robenek, M.J., Troyer, D., Severs, N.J., Compartmentalization of proteins in lipid droplet biogenesis. Biochim. Biophys. Acta 1791 (2009), 408–418.
119. Rodríguez, N.E., Wilson, M.E., Eosinophils and mast cells in leishmaniasis. Immunol. Res. 59 (2014), 129–141, 10.1007/s12026-014-8536-x.
120. Schaloske, R.H., Dennis, E.A., The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta 1761 (2006), 1246–1259 doi:S1388-1981(06)00220-4 [pii] 10.1016/j.bbalip.2006.07.011.
121. Schleimer, R.P., MacGlashan, D.W., Peters, S.P., Pinckard, R.N., Adkinson, N.F., Lichtenstein, L.M., Characterization of inflammatory mediator release from purified human lung mast cells. Am. Rev. Respir. Dis. 133 (1986), 614–617.
122. Schreiber, R., Zechner, R., Lipolysis meets inflammation: arachidonic acid mobilization from fat. J. Lipid Res. 55 (2014), 2447–2449, 10.1194/jlr.C055673.
123. Schumann, J., Basiouni, S., Gück, T., Fuhrmann, H., Treating canine atopic dermatitis with unsaturated fatty acids: the role of mast cells and potential mechanisms of action. J. Anim. Physiol. Anim. Nutr. 98 (2014), 1013–1020, 10.1111/jpn.12181.
124. Simons, K., Gerl, M.J., Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11 (2010), 688–699, 10.1038/nrm2977.
125. Smirnova, E., Goldberg, E.B., Makarova, K.S., Lin, L., Brown, W.J., Jackson, C.L., ATGL has a key role in lipid droplet/adiposome degradation in mammalian cells. EMBO Rep. 7 (2006), 106–113, 10.1038/sj.embor.7400559.
126. Soupene, E., Kuypers, F.A., Mammalian long-chain acyl-CoA synthetases. Exp. Biol. Med. 233 (2008), 507–521 doi:0710-MR-287 [pii] 10.3181/0710-MR-287.
127. Sztalryd, C., Xu, G., Dorward, H., Tansey, J.T., Contreras, J.A., Kimmel, A.R., Londos, C., Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation. J. Cell Biol. 161 (2003), 1093–1103 doi:10.1083/jcb.200210169 jcb.200210169 [pii].
128. Testerink, N., Ajat, M., Houweling, M., Brouwers, J.F., Pully, V.V., van Manen, H.J., Otto, C., Helms, J.B., Vaandrager, A.B., Replacement of retinyl esters by polyunsaturated triacylglycerol species in lipid droplets of hepatic stellate cells during activation. PLoS One, 7, 2012, e34945.
129. Theoharides, T.C., Kempuraj, D., Tagen, M., Conti, P., Kalogeromitros, D., Differential release of mast cell mediators and the pathogenesis of inflammation. Immunol. Rev. 217 (2007), 65–78, 10.1111/j.1600-065X.2007.00519.x.
130. Triggiani, M., Oriente, A., Seeds, M.C., Bass, D.A., Marone, G., Chilton, F.H., Migration of human inflammatory cells into the lung results in the remodeling of arachidonic acid into a triglyceride pool. J. Exp. Med. 182 (1995), 1181–1190.
131. Tuohetahuntila, M., Spee, B., Kruitwagen, H.S., Wubbolts, R., Brouwers, J.F., van de Lest, C.H., Molenaar, M.R., Houweling, M., Helms, J.B., Vaandrager, A.B., Role of long-chain acyl-CoA synthetase 4 in formation of polyunsaturated lipid species in hepatic stellate cells. Biochim. Biophys. Acta 1851 (2015), 220–230, 10.1016/j.bbalip.2014.12.003.
132. Umlauf, E., Csaszar, E., Moertelmaier, M., Schuetz, G.J., Parton, R.G., Prohaska, R., Association of stomatin with lipid bodies. J. Biol. Chem. 279 (2004), 23699–23709 doi:10.1074/jbc.M310546200 M310546200 [pii].
133. Valent, P., Cerny-Reiterer, S., Herrmann, H., Mirkina, I., George, T.I., Sotlar, K., Sperr, W.R., Horny, H.-P., Phenotypic heterogeneity, novel diagnostic markers, and target expression profiles in normal and neoplastic human mast cells. Best Pract. Res. Clin. Haematol. 23 (2010), 369–378, 10.1016/j.beha.2010.07.003.
134. Van den Elsen, L.W.J., Nusse, Y., Balvers, M., Redegeld, F.A., Knol, E.F., Garssen, J., Willemsen, L.E.M., n-3 Long-chain PUFA reduce allergy-related mediator release by human mast cells in vitro via inhibition of reactive oxygen species. Br. J. Nutr. 109 (2013), 1821–1831, 10.1017/S0007114512003959.
135. Walther, T.C., Farese, R.V., Lipid droplets and cellular lipid metabolism. Annu. Rev. Biochem. 81 (2012), 687–714, 10.1146/annurev-biochem-061009-102430.
136. Walther, T.C., Farese, R.V., The life of lipid droplets. Biochim. Biophys. Acta 1791 (2009), 459–466 doi:S1388-1981(08)00193-5 [pii] 10.1016/j.bbalip.2008.10.009.
137. Wan, H.-C., Melo, R.C.N., Jin, Z., Dvorak, A.M., Weller, P.F., Roles and origins of leukocyte lipid bodies: proteomic and ultrastructural studies. FASEB J. 21 (2007), 167–178, 10.1096/fj.06-6711com.
138. Wang, X., Kulka, M., n-3 Polyunsaturated fatty acids and mast cell activation. J. Leukoc. Biol., 2015, 10.1189/jlb.2RU0814-388R.
139. Weise, C., Ernst, D., van Tol, E.A.F., Worm, M., Dietary polyunsaturated fatty acids and non-digestible oligosaccharides reduce dermatitis in mice. Pediatr. Allergy Immunol. 24 (2013), 361–367, 10.1111/pai.12073.
140. Weller, P.F., Bozza, P.T., Yu, W., Dvorak, A.M., Cytoplasmic lipid bodies in eosinophils: central roles in eicosanoid generation. Int. Arch. Allergy Immunol. 118 (1999), 450–452.
141. Wendell, S.G., Baffi, C., Holguin, F., Fatty acids, inflammation, and asthma. J. Allergy Clin. Immunol. 133 (2014), 1255–1264, 10.1016/j.jaci.2013.12.1087.
142. Wernersson, S., Pejler, G., Mast cell secretory granules: armed for battle. Nat. Rev. Immunol. 14 (2014), 478–494, 10.1038/nri3690.
143. Westerberg, C.M., Ekoff, M., Nilsson, G., Regulation of mast cell survival and apoptosis. Methods Mol. Biol. 1220 (2015), 257–267, 10.1007/978-1-4939-1568-2_16.
144. Williams, D.E., Morrissey, P.J., Mochizuki, D.Y., de Vries, P., Anderson, D., Cosman, D., Boswell, H.S., Cooper, S., Grabstein, K.H., Broxmeyer, H.E., T-cell growth factor P40 promotes the proliferation of myeloid cell lines and enhances erythroid burst formation by normal murine bone marrow cells in vitro. Blood 76 (1990), 906–911.
145. Xu, J.-M., Shi, G.-P., Emerging role of mast cells and macrophages in cardiovascular and metabolic diseases. Endocr. Rev. 33 (2012), 71–108, 10.1210/er.2011-0013.
146. Yamada, K., Okano, Y., Miura, K., Nozawa, Y., A major role for phospholipase A2 in antigen-induced arachidonic acid release in rat mast cells. Biochem. J. 247 (1987), 95–99.
147. Zechner, R., Kienesberger, P.C., Haemmerle, G., Zimmermann, R., Lass, A., Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J. Lipid Res. 50 (2009), 3–21.
148. Zechner, R., Zimmermann, R., Eichmann, T.O., Kohlwein, S.D., Haemmerle, G., Lass, A., Madeo, F., FAT SIGNALS – lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 15 (2012), 279–291 doi:S1550-4131(12)00018-6 [pii] 10.1016/j.cmet.2011.12.018.
149. Zehmer, J.K., Huang, Y., Peng, G., Pu, J., Anderson, R.G., Liu, P., A role for lipid droplets in inter-membrane lipid traffic. Proteomics 9 (2009), 914–921.
150. Zimmermann, R., Strauss, J.G., Haemmerle, G., Schoiswohl, G., Birner-Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., Zechner, R., Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306 (2004), 1383–1386 doi:306/5700/1383 [pii] 10.1126/science.1100747.