Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins

Journal of Lipid Research

Volumn 51, Issue 8, 2010, Pages 2105-2120

  Subra, Caroline ^a,b   Grand, David ^a   Laulagnier, Karine ^c   Stella, Alexandre ^d   Lambeau, Gérard ^e   Paillasse, Michael ^a,b   De Medina, Philippe ^a,b   Monsarrat, Bernard ^d   Perret, Bertrand ^a   Silvente Poirot, Sandrine ^a,b   Poirot, Marc ^a,b   Record, Michel ^a,b  

^a CHU PURPAN   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^e INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Arachidonic acid; Docosahexaenoic acid; Exosome; Phosphatidate phosphatase; Prostaglandin

Indexed keywords

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; ARACHIDONIC ACID; CALCIUM INDEPENDENT PHOSPHOLIPASE A2; DIACYLGLYCEROL; FATTY ACID BINDING PROTEIN; FRUCTOSE BISPHOSPHATE ALDOLASE; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); HEAT SHOCK PROTEIN 70; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PROSTAGLANDIN E2; RAS PROTEIN; SCRAMBLASE; SECRETORY PHOSPHOLIPASE A2; 9-DEOXY-DELTA-9-PROSTAGLANDIN D2; GUANOSINE TRIPHOSPHATE; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPASE; PHOSPHOLIPASE A2; PHOSPHOLIPASE D2; PROSTAGLANDIN; PROSTAGLANDIN D2; PROTEOME;

ARTICLE; BIOLOGICAL ACTIVITY; CELL ACTIVATION; CELL COMPARTMENTALIZATION; CELL LEVEL; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; EXOSOME; INTERNALIZATION; LIPOGENESIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSCYTOSIS; ANALOGS AND DERIVATIVES; CELL LINE; DRUG EFFECTS; HUMAN; LIPOLYSIS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CELL LINE; DINOPROSTONE; ENDOSOMES; ENZYME ACTIVATION; EXOSOMES; GUANOSINE TRIPHOSPHATE; HUMANS; LIPOLYSIS; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPASE D; PHOSPHOLIPASES; PHOSPHOLIPASES A2; PROSTAGLANDIN D2; PROSTAGLANDINS; PROTEOME;

EID: 77956867597     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M003657     Document Type: Article

References (75)

1. Thery, C., S. Amigorena, G. Raposo, and A. Clayton. 2006. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chapter 3: Unit 3.22.
2. Raposo, G., H. W. Nijman, W. Stoorvogel, R. Liejendekker, C. V. Harding, C. J. Melief, and H. J. Geuze. 1996. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183: 1161-1172.
3. Hess, C., S. Sadallah, A. Hefti, R. Landmann, and J. A. Schifferli. 1999. Ectosomes released by human neutrophils are specialized functional units. J. Immunol. 163: 4564-4573.
4. Werner, N., S. Wassmann, P. Ahlers, S. Kosiol, and G. Nickenig. 2006. Circulating CD31+/annexin V+ apoptotic microparticles correlate with coronary endothelial function in patients with coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 26: 112-116.
5. Valadi, H., K. Ekstrom, A. Bossios, M. Sjostrand, J. J. Lee, and J. O. Lotvall. 2007. Exosome-mediated transfer of mRNAs and micro-RNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9: 654-659.
6. Skokos, D., H. G. Botros, C. Demeure, J. Morin, R. Peronet, G. Birkenmeier, S. Boudaly, and S. Mecheri. 2003. Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. J. Immunol. 170: 3037-3045.
7. Zakharova, L., M. Svetlova, and A. F. Fomina. 2007. T cell exosomes induce cholesterol accumulation in human monocytes via phosphatidylserine receptor. J. Cell. Physiol. 212: 174-181.
8. Miyanishi, M., K. Tada, M. Koike, Y. Uchiyama, T. Kitamura, and S. Nagata. 2007. Identification of Tim4 as a phosphatidylserine receptor. Nature. 450: 435-439.
9. Ristorcelli, E., E. Beraud, S. Mathieu, D. Lombardo, and A. Verine. 2009. Essential role of Notch signaling in apoptosis of human pancreatic tumoral cells mediated by exosomal nanoparticles. Int. J. Cancer. 125: 1016-1026.
10. Alais, S., S. Simoes, D. Baas, S. Lehmann, G. Raposo, J. L. Darlix, and P. Leblanc. 2008. Mouse neuroblastoma cells release prion infectivity associated with exosomal vesicles. Biol. Cell. 100: 603-615.
11. Schorey, J. S., and S. Bhatnagar. 2008. Exosome function: from tumor immunology to pathogen biology. Traffic. 9: 871-881.
12. Sharples, R. A., L. J. Vella, R. M. Nisbet, R. Naylor, K. Perez, K. J. Barnham, C. L. Masters, and A. F. Hill. 2008. Inhibition of gamma-secretase causes increased secretion of amyloid precursor protein C-terminal fragments in association with exosomes. FASEB J. 22: 1469-1478.
13. Perrin-Cocon, L., S. Agaugue, F. Coutant, A. Masurel, S. Bezzine, G. Lambeau, P. Andre, and V. Lotteau. 2004. Secretory phospholipase A2 induces dendritic cell maturation. Eur. J. Immunol. 34: 2293-2302.
14. Thurnher, M. 2007. Lipids in dendritic cell biology: messengers, effectors, and antigens. J. Leukoc. Biol. 81: 154-160.
15. Laulagnier, K., C. Motta, S. Hamdi, S. Roy, F. Fauvelle, J. F. Pageaux, T. Kobayashi, J. P. Salles, B. Perret, C. Bonnerot, et al. 2004. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem. J. 380: 161-171.
16. Laulagnier, K., D. Grand, A. Dujardin, S. Hamdi, H. Vincent-Schneider, D. Lankar, J. P. Salles, C. Bonnerot, B. Perret, and M. Record. 2004. PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes. FEBS Lett. 572: 11-14.
17. Scher, J. U., and M. H. Pillinger. 2005. 15d-PGJ2: the anti-inflammatory prostaglandin? Clin. Immunol. 114: 100-109.
18. Gandarillas, N. L., T. D. Bunney, M. B. Josephs, P. Gierschik, and M. Katan. 2009. In vitro reconstitution of activation of PLCepsilon by Ras and Rho GTPases. Methods Mol. Biol. 462: 379-389.
19. Scher, J. U., and M. H. Pillinger. 2009. The anti-inflammatory effects of prostaglandins. J. Investig. Med. 57: 703-708.
20. Rouault, M., C. Le Calvez, E. Boilard, F. Surrel, A. Singer, F. Ghomashchi, S. Bezzine, S. Scarzello, J. Bollinger, M. H. Gelb, et al. 2007. Recombinant production and properties of binding of the full set of mouse secreted phospholipases A2 to the mouse M-type receptor. Biochemistry. 46: 1647-1662.
21. Kobayashi, T., E. Stang, K. S. Fang, P. de Moerloose, R. G. Parton, and J. Gruenberg. 1998. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature. 392: 193-197.
22. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.
23. Laulagnier, K., H. Vincent-Schneider, S. Hamdi, C. Subra, D. Lankar, and M. Record. 2005. Characterization of exosome subpopulations from RBL-2H3 cells using fluorescent lipids. Blood Cells Mol. Dis. 35: 116-121.
24. Allal, C., C. Buisson-Brenac, V. Marion, C. Claudel-Renard, T. Faraut, P. Dal Monte, D. Streblow, M. Record, and J. L. Davignon. 2004. Human cytomegalovirus carries a cell-derived phospholipase A2 required for infectivity. J. Virol. 78: 7717-7726.
25. Gubern, A., J. Casas, M. Barcelo-Torns, D. Barneda, X. de la Rosa, R. Masgrau, F. Picatoste, J. Balsinde, M. A. Balboa, and E. Claro. 2008. Group IVA phospholipase A2 is necessary for the biogenesis of lipid droplets. J. Biol. Chem. 283: 27369-27382.
26. Gayral, S., P. Deleris, K. Laulagnier, M. Laffargue, J. P. Salles, B. Perret, M. Record, and M. Breton-Douillon. 2006. Selective activation of nuclear phospholipase D-1 by g protein-coupled receptor agonists in vascular smooth muscle cells. Circ. Res. 99: 132-139.
27. Bouyssie, D., A. Gonzalez de Peredo, E. Mouton, R. Albigot, L. Roussel, N. Ortega, C. Cayrol, O. Burlet-Schiltz, J. P. Girard, and B. Monsarrat. 2007. Mascot file parsing and quantification (MFPaQ), a new software to parse, validate, and quantify proteomics data generated by ICAT and SILAC mass spectrometric analyses: application to the proteomics study of membrane proteins from primary human endothelial cells. Mol. Cell. Proteomics. 6: 1621-1637.
28. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
29. Payre, B., P. de Medina, N. Boubekeur, L. Mhamdi, J. Bertrand-Michel, F. Terce, I. Fourquaux, D. Goudouneche, M. Record, M. Poirot, et al. 2008. Microsomal antiestrogen-binding site ligands induce growth control and differentiation of human breast cancer cells through the modulation of cholesterol metabolism. Mol. Cancer Ther. 7: 3707-3718.
30. Soares, A. F., O. Nosjean, D. Cozzone, D. D'Orazio, M. Becchi, M. Guichardant, G. Ferry, J. A. Boutin, M. Lagarde, and A. Geloen. 2005. Covalent binding of 15-deoxy-delta12,14-prostaglandin J2 to PPARgamma. Biochem. Biophys. Res. Commun. 337: 521-525.
31. Kitanaka, N., Y. Owada, R. Okuyama, H. Sakagami, M. R. Nourani, S. Aiba, H. Furukawa, M. Watanabe, M. Ono, T. Ohteki, et al. 2006. Epidermal-type fatty acid binding protein as a negative regulator of IL-12 production in dendritic cells. Biochem. Biophys. Res. Commun. 345: 459-466.
32. Stipp, C. S., D. Orlicky, and M. E. Hemler. 2001. FPRP, a major, highly stoichiometric, highly specific CD81- and CD9-associated protein. J. Biol. Chem. 276: 4853-4862.
33. Orlicky, D. J., R. Berry, and J. M. Sikela. 1996. Human chromosome 1 localization of the gene for a prostaglandin F2alpha receptor negative regulatory protein. Hum. Genet. 97: 655-658.
34. Kim, J. H., S. Lee, T. G. Lee, M. Hirata, P. G. Suh, and S. H. Ryu. 2002. Phospholipase D2 directly interacts with aldolase via Its PH domain. Biochemistry. 41: 3414-3421.
35. Ganley, I. G., S. J. Walker, M. Manifava, D. Li, H. A. Brown, and N. T. Ktistakis. 2001. Interaction of phospholipase D1 with a casein-kinase-2-like serine kinase. Biochem. J. 354: 369-378.
36. Shimoyama, Y., R. Sakamoto, T. Akaboshi, M. Tanaka, and K. Ohtsuki. 2001. Characterization of secretory type IIA phospholipase A2 (sPLA2-IIA) as a glycyrrhizin (GL)-binding protein and the GL-induced inhibition of the CK-II-mediated stimulation of sPLA2-IIA activity in vitro. Biol. Pharm. Bull. 24: 1004-1008.
37. Mancuso, D. J., C. M. Jenkins, and R. W. Gross. 2000. The genomic organization, complete mRNA sequence, cloning, and expression of a novel human intracellular membrane-associated calcium-independent phospholipase A(2). J. Biol. Chem. 275: 9937-9945.
38. Konstantinopoulos, P. A., M. V. Karamouzis, and A. G. Papavassiliou. 2007. Post-translational modifications and regulation of the RAS superfamily of GTPases as anticancer targets. Nat. Rev. Drug Discov. 6: 541-555.
39. Bae, C. D., D. S. Min, I. N. Fleming, and J. H. Exton. 1998. Determination of interaction sites on the small G protein RhoA for phospholipase D. J. Biol. Chem. 273: 11596-11604.
40. Hiroyama, M., and J. H. Exton. 2005. Localization and regulation of phospholipase D2 by ARF6. J. Cell. Biochem. 95: 149-164.
41. Le Stunff, H., L. Dokhac, S. Bourgoin, M. F. Bader, and S. Harbon. 2000. Phospholipase D in rat myometrium: occurrence of a membrane-bound ARF6 (ADP-ribosylation factor 6)-regulated activity controlled by betagamma subunits of heterotrimeric G-proteins. Biochem. J. 352: 491-499.
42. Lambeau, G., and M. H. Gelb. 2008. Biochemistry and physiology of mammalian secreted phospholipases A2. Annu. Rev. Biochem. 77: 495-520.
43. Singer, A. G., F. Ghomashchi, C. Le Calvez, J. Bollinger, S. Bezzine, M. Rouault, M. Sadilek, E. Nguyen, M. Lazdunski, G. Lambeau, et al. 2002. Interfacial kinetic and binding properties of the complete set of human and mouse groups I, II, V, X, and XII secreted phospholipases A2. J. Biol. Chem. 277: 48535-48549.
44. Blanc, L., C. Barres, P. Bette-Bobillo, and M. Vidal. 2007. Reticulocyte-secreted exosomes bind natural IgM antibodies: involvement of a ROS-activatable endosomal phospholipase iPLA2. Blood. 110: 3407-3416.
45. Lauber, K., E. Bohn, S. M. Krober, Y. J. Xiao, S. G. Blumenthal, R. K. Lindemann, P. Marini, C. Wiedig, A. Zobywalski, S. Baksh, et al. 2003. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell. 113: 717-730.
46. Barbu, A. E., and I. Pecht. 2005. Desensitization of mast cells' secretory response to an immuno-receptor stimulus. Immunol. Lett. 100: 78-87.
47. Amano, T., T. Furuno, N. Hirashima, N. Ohyama, and M. Nakanishi. 2001. Dynamics of intracellular granules with CD63-GFP in rat basophilic leukemia cells. J Biochem. 129: 739-744.
48. Grimberg, E., Z. Peng, I. Hammel, and R. Sagi-Eisenberg. 2003. Synaptotagmin III is a critical factor for the formation of the perinuclear endocytic recycling compartment and determination of secretory granules size. J. Cell Sci. 116: 145-154.
49. Tadokoro, S., T. Kurimoto, M. Nakanishi, and N. Hirashima. 2007. Munc18-2 regulates exocytotic membrane fusion positively interacting with syntaxin-3 in RBL-2H3 cells. Mol. Immunol. 44: 3427-3433.
50. Simons, M., and G. Raposo. 2009. Exosomes - vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21: 575-581.
51. Bhatnagar, S., K. Shinagawa, F. J. Castellino, and J. S. Schorey. 2007. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood. 110: 3234-3244.
52. Santos, T. G., D. O. Souza, and C. I. Tasca. 2006. GTP uptake into rat brain synaptic vesicles. Brain Res. 1070: 71-76.
53. Lee, C. S., I. S. Kim, J. B. Park, M. N. Lee, H. Y. Lee, P. G. Suh, and S. H. Ryu. 2006. The phox homology domain of phospholipase D activates dynamin GTPase activity and accelerates EGFR endocytosis. Nat. Cell Biol. 8: 477-484.
54. Petry, C., G. Fritz, J. Pfeilschifter, and A. Huwiler. 2004. Inhibition of Rho modulates cytokine-induced prostaglandin E2 formation in renal mesangial cells. Biochim. Biophys. Acta. 1636: 108-118.
55. Maeda, A., Y. Ozaki, S. Sivakumaran, T. Akiyama, H. Urakubo, A. Usami, M. Sato, K. Kaibuchi, and S. Kuroda. 2006. Ca2+ -independent phospholipase A2-dependent sustained Rho-kinase activation exhibits all-or-none response. Genes Cells. 11: 1071-1083.
56. Wijewickrama, G. T., J. H. Kim, Y. J. Kim, A. Abraham, Y. Oh, B. Ananthanarayanan, M. Kwatia, S. J. Ackerman, and W. Cho. 2006. Systematic evaluation of transcellular activities of secretory phospholipases A2. High activity of group V phospholipases A2 to induce eicosanoid biosynthesis in neighboring inflammatory cells. J. Biol. Chem. 281: 10935-10944.
57. Sawada, H., M. Murakami, A. Enomoto, S. Shimbara, and I. Kudo. 1999. Regulation of type V phospholipase A2 expression and function by proinflammatory stimuli. Eur. J. Biochem. 263: 826-835.
58. Salvado, M. D., A. Alfranca, A. Escolano, J. Z. Haeggstrom, and J. M. Redondo. 2009. COX-2 limits prostanoid production in activated HUVECs and is a source of PGH2 for transcellular metabolism to PGE2 by tumor cells. Arterioscler. Thromb. Vasc. Biol. 29: 1131-1137.
59. Folco, G., and R. C. Murphy. 2006. Eicosanoid transcellular biosynthesis: from cell-cell interactions to in vivo tissue responses. Pharmacol. Rev. 58: 375-388.
60. Zarini, S., M. A. Gijon, A. E. Ransome, R. C. Murphy, and A. Sala. 2009. Transcellular biosynthesis of cysteinyl leukotrienes in vivo during mouse peritoneal inflammation. Proc. Natl. Acad. Sci. USA. 106: 8296-8301.
61. Kondo, H., R. Shirakawa, T. Higashi, M. Kawato, M. Fukuda, T. Kita, and H. Horiuchi. 2006. Constitutive GDP/GTP exchange and secretion-dependent GTP hydrolysis activity for Rab27 in platelets. J. Biol. Chem. 281: 28657-28665.
62. van der Goot, F. G., and J. Gruenberg. 2006. Intra-endosomal membrane traffic. Trends Cell Biol. 16: 514-521.
63. Falguieres, T., P. P. Luyet, and J. Gruenberg. 2009. Molecular assemblies and membrane domains in multivesicular endosome dynamics. Exp. Cell Res. 315: 1567-1573.
64. Shinozaki, K., and M. Waite. 1999. A novel phosphatidylglycerol-selective phospholipase A2 from macrophages. Biochemistry. 38: 1669-1675.
65. Hullin-Matsuda, F., K. Kawasaki, I. Delton-Vandenbroucke, Y. Xu, M. Nishijima, M. Lagarde, M. Schlame, and T. Kobayashi. 2007. De novo biosynthesis of the late endosome lipid, bis(monoacylglycero) phosphate. J. Lipid Res. 48: 1997-2008.
66. van Blitterswijk, W. J., and H. Hilkmann. 1993. Rapid attenuation of receptor-induced diacylglycerol and phosphatidic acid by phospholipase D-mediated transphosphatidylation: formation of bisphosphatidic acid. EMBO J. 12: 2655-2662.
67. Sattar, A. A., and R. Haque. 2007. Cytosolic PLA2 in zymogen granule fusion and amylase release: inhibition of GTP-induced fusion by arachidonyl trifluoromethyl ketone points to cPLA2 in G-protein-mediated secretory vesicle fusion. J Biochem. 141: 77-84.
68. Blackwood, R. A., J. E. Smolen, A. Transue, R. J. Hessler, D. M. Harsh, R. C. Brower, and S. French. 1997. Phospholipase D activity facilitates Ca2+-induced aggregation and fusion of complex liposomes. Am. J. Physiol. 272: C1279-C1285.
69. van Rossum, D. B., D. Oberdick, Y. Rbaibi, G. Bhardwaj, R. K. Barrow, N. Nikolaidis, S. H. Snyder, K. Kiselyov, and R. L. Patterson. 2008. TRP-2, a lipid/trafficking domain that mediates diacylglycerol-induced vesicle fusion. J. Biol. Chem. 283: 34384-34392.
70. Boyce, J. A. 2007. Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunol. Rev. 217: 168-185.
71. Looze, C., D. Yui, L. Leung, M. Ingham, M. Kaler, X. Yao, W. W. Wu, R. F. Shen, M. P. Daniels, and S. J. Levine. 2009. Proteomic profiling of human plasma exosomes identifies PPARgamma as an exosome-associated protein. Biochem. Biophys. Res. Commun. 378: 433-438.
72. Tan, N. S., N. S. Shaw, N. Vinckenbosch, P. Liu, R. Yasmin, B. Desvergne, W. Wahli, and N. Noy. 2002. Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Mol. Cell. Biol. 22: 5114-5127.
73. Reue, K., and D. N. Brindley. 2008. Thematic Review Series: Glycerolipids. Multiple roles for lipins/phosphatidate phosphatase enzymes in lipid metabolism. J. Lipid Res. 49: 2493-2503.
74. Cerbone, A., C. Toaldo, S. Laurora, F. Briatore, S. Pizzimenti, M. U. Dianzani, C. Ferretti, and G. Barrera. 2007. 4-Hydroxynonenal and PPARgamma ligands affect proliferation, differentiation, and apoptosis in colon cancer cells. Free Radic. Biol. Med. 42: 1661-1670.
75. Szanto, A., and L. Nagy. 2008. The many faces of PPARgamma: anti-inflammatory by any means? Immunobiology. 213: 789-803.