Plasmalogen enrichment in exosomes secreted by a nematode parasite versus those derived from its mouse host: Implications for exosome stability and biology

Journal of Extracellular Vesicles

Volumn 5, Issue 1, 2016, Pages

  Simbari, Fabio ^a   McCaskill, Jana ^a   Coakley, Gillian ^a   Millar, Marissa ^a   Maizels, Rick M ^a,b   Fabriás, Gemma ^c   Casas, Josefina ^c   Buck, Amy H ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c INSTITUTE OF ADVANCED CHEMISTRY OF CATALONIA IQAC CSIC   (Spain)

Author keywords

Cholesterol; Cross species communication; Dynamic light scattering; Ether lipids; Extracellular vesicles; Helminth; Host pathogen

Indexed keywords

CHOLESTEROL; GLYCEROPHOSPHOLIPID; SPHINGOLIPID; SPHINGOMYELIN;

ACIDITY; ARTICLE; CELL MEMBRANE; CELL SIZE; CELLULAR SECRETION; ENDOCYTOSIS; EPITHELIUM CELL; EXOSOME; HELIGMOSOMOIDES POLYGYRUS; INTESTINE CELL; LIPID BILAYER; LIPID COMPOSITION; LIPIDOMICS; MEMBRANE STRUCTURE; NEMATODE; NONHUMAN; PH; PHAGOCYTOSIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TANDEM MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ZETA POTENTIAL;

EID: 84997353960     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.3402/jev.v5.30741     Document Type: Article

References (80)

1. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200:373-83
2. Fevrier B, Raposo G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol. 2004; 16:415-21
3. Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255-89
4. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem. 1987;262:9412-20
5. Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell. 1983;33:967-78
6. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol. 1983;97:329-39
7. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, et al. B lymphocytes secrete antigenpresenting vesicles. J Exp Med. 1996;183:1161-72
8. De Toro J, Herschlik L, Waldner C, Mongini C. Emerging roles of exosomes in normal and pathological conditions: new insights for diagnosis and therapeutic applications. Front Immunol. 2015;6:203
9. Marcilla A, Martin-Jaular L, Trelis M, de Menezes-Neto A, Osuna A, Bernal D, et al. Extracellular vesicles in parasitic diseases. J Extracell Vesicles. 2014;3:25040, doi: http://dx.doi. org/10.3402/jev.v3.25040
10. Coakley G, Maizels RM, Buck AH. Exosomes and other extracellular vesicles: the new communicators in parasite infections. Trends Parasitol. 2015;31:477-89
11. Mu JY, Zhuang XY, Wang QL, Jiang H, Deng ZB, Wang BM, et al. Interspecies communication between plant and mouse gut host cells through edible plant derived exosome-like nanoparticles. Mol Nutr Food Res. 2014;58:1561-73
12. Ju S, Mu J, Dokland T, Zhuang X, Wang Q, Jiang H, et al. Grape exosome-like nanoparticles induce intestinal stem cells and protect mice from DSS-induced colitis. Mol Ther. 2013;21:1345-57
13. Regente M, Pinedo M, Elizalde M, de la Canal L. Apoplastic exosome-like vesicles: a new way of protein secretion in plants? Plant Signal Behav. 2012;7:544-6
14. Buck AH, Coakley G, Simbari F, McSorley HJ, Quintana JF, Le Bihan T, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun. 2014;5:5488
15. Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012; 10:e1001450
16. Lydic TA, Townsend S, Adda CG, Collins C, Mathivanan S, Reid GE. Rapid and comprehensive ''shotgun'' lipidome profiling of colorectal cancer cell derived exosomes. Methods. 2015;87:83-95
17. Carayon K, Chaoui K, Ronzier E, Lazar I, Bertrand-Michel J, Roques V, et al. Proteolipidic composition of exosomes changes during reticulocyte maturation. J Biol Chem. 2011; 286:34426-39
18. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Mobius W, Hoernschemeyer J, et al. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem. [Research Support, Non-U.S. Gov't]. 2003; 278:10963-72
19. Laulagnier K, Motta C, Hamdi S, Roy S, Fauvelle F, Pageaux JF, et al. Mast cell-and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J. 2004;380(Pt 1):161-71
20. Llorente A, Skotland T, Sylvanne T, Kauhanen D, Rog T, Orlowski A, et al. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta. 2013;1831:1302-9
21. Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066, doi: http://dx.doi.org/10.3402/jev.v4.27066
22. Barenholz Y. Sphingomyelin and cholesterol: from membrane biophysics and rafts to potential medical applications. Subcell Biochem. 2004;37:167-215
23. Record M, Carayon K, Poirot M, Silvente-Poirot S. Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies. Biochim Biophys Acta. 2014;1841:108-20
24. Chitwood DJ, Lusby WR. Metabolism of plant sterols by nematodes. Lipids. 1991;26:619-27
25. Lee DL. The biology of nematodes. London: Taylor & Francis; 2002
26. Bankov I, Timanova A, Barrett J. Sphingomyelin synthesis in helminths: a minireview. Folia Parasitol (Praha). 1998;45: 257-60
27. Johnston CJ, Robertson E, Harcus Y, Grainger JR, Coakley G, Smyth DJ, et al. Cultivation of Heligmosomoides polygyrus: an immunomodulatory nematode parasite and its secreted products. J Vis Exp. 2015;98:e52412
28. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006; Chapter 3: Unit 3 22
29. Vidal K, Grosjean I, Evillard JP, Gespach C, Kaiserlian D. Immortalization of mouse intestinal epithelial cells by the SV40-large T gene. Phenotypic and immune characterization of the MODE-K cell line. J Immunol Methods. 1993;166: 63-73
30. Garanto A, Mandal NA, Egido-Gabas M, Marfany G, Fabrias G, Anderson RE, et al. Specific sphingolipid content decrease in Cerkl knockdown mouse retinas. Exp Eye Res. 2013;110: 96-106
31. Gorrochategui E, Casas J, Perez-Albaladejo E, Jauregui O, Porte C, Lacorte S. Characterization of complex lipid mixtures in contaminant exposed JEG-3 cells using liquid chromatography and high-resolution mass spectrometry. Environ Sci Pollut Res Int. 2014;21:11907-16
32. Palleschi S, Silvestroni L. Laurdan fluorescence spectroscopy reveals a single liquid-crystalline lipid phase and lack of thermotropic phase transitions in the plasma membrane of living human sperm. Biochim Biophys Acta. 1996;1279:197-202
33. Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem. 2009;284:34211-22
34. Rappleye CA, Paredez AR, Smith CW, McDonald KL, Aroian RV. The coronin-like protein POD-1 is required for anterior-posterior axis formation and cellular architecture in the nematode Caenorhabditis elegans. Genes Dev. 1999;13:2838-51
35. Armenti ST, Chan E, Nance J. Polarized exocyst-mediated vesicle fusion directs intracellular lumenogenesis within the C. elegans excretory cell. Dev Biol. 2014;394:110-21
36. Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science. 2009;323:1718-22
37. Roger E, Lagarce F, Benoit JP. The gastrointestinal stability of lipid nanocapsules. Int J Pharm. 2009;379:260-5
38. Honary S, Zahir F. Effect of zeta potential on the properties of nano-drug delivery systems-a review (Part 1). Trop J Pharm Res. 2013;12:255-64
39. Honary S, Zahir F. Effect of zeta potential on the properties of nano-drug delivery systems-a review (Part 2). Trop J Pharm Res. 2013;12:265-73
40. Marimpietri D, Petretto A, Raffaghello L, Pezzolo A, Gagliani C, Tacchetti C, et al. Proteome profiling of neuroblastomaderived exosomes reveal the expression of proteins potentially involved in tumor progression. PLoS One. 2013;8:e75054
41. Kaszuba M, Corbett J, Watson FM, Jones A. High-concentration zeta potential measurements using light-scattering techniques. Philos Trans A Math Phys Eng Sci. 2010;368:4439-51
42. Sokolova V, Ludwig AK, Hornung S, Rotan O, Horn PA, Epple M, et al. Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf B Biointerfaces. 2011;87: 146-50
43. Lohner K, Balgavy P, Hermetter A, Paltauf F, Laggner P. Stabilization of non-bilayer structures by the etherlipid ethanolamine plasmalogen. Biochim Biophys Acta. 1991;1061: 132-40
44. Lohner K. Is the high propensity of ethanolamine plasmalogens to form non-lamellar lipid structures manifested in the properties of biomembranes? Chem Phys Lipids. 1996;81: 167-84
45. Braverman NE, Moser AB. Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta. 2012;1822:1442-52
46. Subra C, Laulagnier K, Perret B, Record M. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie. 2007;89:205-12
47. Ito J, Nagayasu Y, Yokoyama S. Cholesterol-sphingomyelin interaction in membrane and apolipoprotein-mediated cellular cholesterol efflux. J Lipid Res. 2000;41:894-904
48. Sonnino S, Prinetti A. Membrane domains and the ''lipid raft'' concept. Curr Med Chem. 2013;20:4-21
49. Ikonen E. Roles of lipid rafts in membrane transport. Curr Opin Cell Biol. 2001;13:470-7
50. Trajkovic K. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319:1244-7
51. Slotte JP, Hedstrom G, Rannstrom S, Ekman S. Effects of sphingomyelin degradation on cell cholesterol oxidizability and steady-state distribution between the cell-surface and the cell interior. Biochim Biophys Acta. 1989;985:90-6
52. Harmala AS, Porn MI, Mattjus P, Slotte JP. Cholesterol transport from plasma-membranes to intracellular membranes is inhibited by 3-beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. Biochim Biophys Acta. 1994;1211:317-25
53. Weber G, Farris FJ. Synthesis and spectral properties of a hydrophobic fluorescent probe: 6-propionyl-2-(dimethylamino) naphthalene. Biochemistry. 1979;18:3075-8
54. Parasassi T, Gratton E. Membrane lipid domains and dynamics as detected by Laurdan fluorescence. J Fluoresc. 1995;5: 59-69
55. Sanchez SA, Tricerri MA, Gratton E. Laurdan generalized polarization fluctuations measures membrane packing microheterogeneity in vivo. Proc Natl Acad Sci USA. 2012;109: 7314-9
56. Han XL, Gross RW. Plasmenylcholine and phosphatidylcholine membrane bilayers possess distinct conformational motifs. Biochemistry. 1990;29:4992-6
57. Paltauf F. Ether lipids in biomembranes. Chem Phys Lipids. 1994;74:101-39
58. Breckenridge WC, Morgan IG, Zanetta JP, Vincendon G. Adult rat brain synaptic vesicles. II. Lipid composition. Biochim Biophys Acta. 1973;320:681-6
59. Glaser PE, Gross RW. Plasmenylethanolamine facilitates rapid membrane fusion: a stopped-flow kinetic investigation correlating the propensity of a major plasma membrane constituent to adopt an HII phase with its ability to promote membrane fusion. Biochemistry. 1994;33:5805-12
60. Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles. 2014;3:24641, doi: http://dx.doi.org/10.3402/jev.v3.24641
61. Jayachandran R, BoseDasgupta S, Pieters J. Surviving the macrophage: tools and tricks employed by Mycobacterium tuberculosis. Curr Top Microbiol Immunol. 2013;374:189-209
62. Jayachandran R, Sundaramurthy V, Combaluzier B, Mueller P, Korf H, Huygen K, et al. Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin. Cell. 2007;130:37-50
63. Pieters J, Muller P, Jayachandran R. On guard: coronin proteins in innate and adaptive immunity. Nat Rev Immunol. 2013;13:510-8
64. Zheng PY, Jones NL. Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein. Cell Microbiol. 2003;5:25-40
65. Lv MM, Zhu XY, Chen WX, Zhong SL, Hu Q, Ma TF, et al. Exosomes mediate drug resistance transfer in MCF-7 breast cancer cells and a probable mechanism is delivery of Pglycoprotein. Tumor Biol. 2014;35:10773-9
66. Lespine A, Menez C, Bourguinat C, Prichard RK. P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. Int J Parasitol Drugs Drug Resist. 2012;2:58-75
67. de Gassart A, Geminard C, Fevrier B, Raposo G, Vidal M. Lipid raft-associated protein sorting in exosomes. Blood. 2003;102:4336-44
68. Valapala M, Vishwanatha JK. Lipid raft endocytosis and exosomal transport facilitate extracellular trafficking of annexin A2. J Biol Chem. 2011;286:30911-25
69. Phuyal S, Skotland T, Hessvik NP, Simolin H, Overbye A, Brech A, et al. The ether lipid precursor hexadecylglycerol stimulates the release and changes the composition of exosomes derived from PC-3 cells. J Biol Chem. 2015;290:4225-37
70. Han XL, Holtzman DM, McKeel DW. Plasmalogen deficiency in early Alzheimer's disease subjects and in animal models: molecular characterization using electrospray ionization mass spectrometry. J Neurochem. 2001;77:1168-80
71. Farooqui AA, Horrocks LA. Plasmalogens: workhorse lipids of membranes in normal and injured neurons and glia. Neuroscientist. 2001;7:232-45
72. Maeba R, Maeda T, Kinoshita M, Takao K, Takenaka H, Kusano J, et al. Plasmalogens in human serum positively correlate with high-density lipoprotein and decrease with aging. J Atheroscler Thromb. 2007;14:12-8
73. Sugiura T, Fukuda T, Miyamoto T, Waku K. Distribution of alkyl and alkenyl ether-linked phospholipids and platelet-activating factor-like lipid in various species of invertebrates. Biochim Biophys Acta. 1992;1126:298-308
74. Brouwers JFHM, Van Hellemond JJ, van Golde LMG, Tielens AGM. Ether lipids and their possible physiological function in adult Schistosoma mansoni. Mol Biochem Parasitol. 1998;96: 49-58
75. Chitwood DJ, Krusberg LR. Diacyl, alkylacyl, and alkenylacyl phospholipids of Meloidogyne javanica females. J Nematol. 1981;13:105-11
76. Chitwood DJ, Krusberg LR. Diacyl, alkylacyl and alkenylacyl phospholipids of the nematode Turbatrix aceti. Comp Biochem Physiol B Biochem Mol Biol. 1981;69:115-20
77. Coutant F, Perrin-Cocon L, Agaugue S, Delair T, Andre P, Lotteau V. Mature dendritic cell generation promoted by lysophosphatidylcholine. J Immunol. 2002;169:1688-95
78. Rappa G, Mercapide J, Anzanello F, Pope RM, Lorico A. Biochemical and biological characterization of exosomes containing prominin-1/CD133. Mol Cancer. 2013;12:62
79. van der Kleij D, Latz E, Brouwers JF, Kruize YC, Schmitz M, Kurt-Jones EA, et al. A novel host-parasite lipid crosstalk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J Biol Chem. 2002; 277:48122-9
80. Spector AA, Yorek MA. Membrane lipid composition and cellular function. J Lipid Res. 1985;26:1015-35