Cytokine-induced release of ceramide-enriched exosomes as a mediator of cell death signaling in an oligodendroglioma cell line

Suk, 2001, IFN-gamma/TNF-alpha synergism as the final effector in autoimmune diabetes: a key role for STAT1/IFN regulatory factor-1 pathway in pancreatic beta cell death, J. Immunol., 166, 4481, 10.4049/jimmunol.166.7.4481 Barthson, 2011, Cytokines tumor necrosis factor-alpha and interferon-gamma induce pancreatic beta-cell apoptosis through STAT1-mediated Bim protein activation, J. Biol. Chem., 286, 39632, 10.1074/jbc.M111.253591 Kiaer, 2009, Serum albumin protects from cytokine-induced pancreatic beta cell death by a phosphoinositide 3-kinase-dependent mechanism, Endocrine., 35, 325, 10.1007/s12020-009-9161-7 Sasagawa, 2000, Synergistic induction of apoptosis in murine hepatoma Hepa1–6 cells by IFN-gamma and TNF-alpha, Biochem. Biophys. Res. Commun., 272, 674, 10.1006/bbrc.2000.2835 Kamachi, 2002, Regulation of apoptotic cell death by cytokines in a human salivary gland cell line: distinct and synergistic mechanisms in apoptosis induced by tumor necrosis factor alpha and interferon gamma, J. Lab. Clin. Med., 139, 13, 10.1067/mlc.2002.120648 Takuma, 1987, Synergism of tumor necrosis factor and interferon-gamma in induction of differentiation of human myeloblastic leukemic ML-1 cells, Biochem. Biophys. Res. Commun., 145, 514, 10.1016/0006-291X(87)91351-9 Craig, 1989, Differentiation-inducing and cytotoxic effects of tumor necrosis factor and interferon-gamma in myeloblastic ML-1 cells, J. Cell. Physiol., 141, 46, 10.1002/jcp.1041410108 Andrews, 1998, TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors, J. Neurosci. Res., 54, 574, 10.1002/(SICI)1097-4547(19981201)54:5<574::AID-JNR2>3.0.CO;2-0 Buntinx, 2004, Cytokine-induced cell death in human oligodendroglial cell lines: I. Synergistic effects of IFN-gamma and TNF-alpha on apoptosis, J. Neurosci. Res., 76, 834, 10.1002/jnr.20118 Testai, 2004, Regulation of sphingomyelinases in cells of the oligodendrocyte lineage, J. Neurosci. Res., 75, 66, 10.1002/jnr.10816 Scurlock, 1999, Differential responses of oligodendrocytes to tumor necrosis factor and other pro-apoptotic agents: role of ceramide in apoptosis, J. Neurosci. Res., 55, 514, 10.1002/(SICI)1097-4547(19990215)55:4<514::AID-JNR11>3.0.CO;2-V Buntinx, 2004, Cytokine-induced cell death in human oligodendroglial cell lines. II: alterations in gene expression induced by interferon-gamma and tumor necrosis factor-alpha, J. Neurosci. Res., 76, 846, 10.1002/jnr.20117 Larocca, 1997, Induction of oligodendrocyte apoptosis by C2-ceramide, Neurochem. Res., 22, 529, 10.1023/A:1027332415877 Haimovitz-Friedman, 1997, Ceramide signaling in apoptosis, Br. Med. Bull., 53, 539, 10.1093/oxfordjournals.bmb.a011629 Lee, 2004, Amyloid-beta peptide induces oligodendrocyte death by activating the neutral sphingomyelinase-ceramide pathway, J. Cell Biol., 164, 123, 10.1083/jcb.200307017 Jana, 2009, Ceramide and neurodegeneration: susceptibility of neurons and oligodendrocytes to cell damage and death, J. Neurol. Sci., 278, 5, 10.1016/j.jns.2008.12.010 Novgorodov, 2011, Developmentally regulated ceramide synthase 6 increases mitochondrial Ca2+ loading capacity and promotes apoptosis, J. Biol. Chem., 286, 4644, 10.1074/jbc.M110.164392 Yoon, 1998, Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival, J. Neurosci., 18, 3273, 10.1523/JNEUROSCI.18-09-03273.1998 Ge, 2012, Exosomes in cancer microenvironment and beyond: have we overlooked these extracellular messengers?, Cancer Microenviron., 5, 323, 10.1007/s12307-012-0110-2 Kowal, 2014, Biogenesis and secretion of exosomes, Curr. Opin. Cell Biol., 29, 116, 10.1016/j.ceb.2014.05.004 Raposo, 2013, Extracellular vesicles: exosomes, microvesicles, and friends, J. Cell Biol., 200, 373, 10.1083/jcb.201211138 Colombo, 2014, Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles, Annu. Rev. Cell Dev. Biol., 30, 255, 10.1146/annurev-cellbio-101512-122326 Simons, 2009, Exosomes–vesicular carriers for intercellular communication, Curr. Opin. Cell Biol., 21, 575, 10.1016/j.ceb.2009.03.007 Bobrie, 2011, Exosome secretion: molecular mechanisms and roles in immune responses, Traffic., 12, 1659, 10.1111/j.1600-0854.2011.01225.x Trajkovic, 2008, Ceramide triggers budding of exosome vesicles into multivesicular endosomes, Science., 319, 1244, 10.1126/science.1153124 Simons, 2006, Neuron-glia communication in the control of oligodendrocyte function and myelin biogenesis, J. Cell Sci., 119, 4381, 10.1242/jcs.03242 Trajkovic, 2006, Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites, J. Cell Biol., 172, 937, 10.1083/jcb.200509022 Frühbeis, 2012, Emerging roles of exosomes in neuron-glia communication, Front. Physiol., 3, 119, 10.3389/fphys.2012.00119 Turola, 2012, Microglial microvesicle secretion and intercellular signaling, Front. Physiol., 3, 149, 10.3389/fphys.2012.00149 Robbins, 2014, Regulation of immune responses by extracellular vesicles, Nat. Rev. Immunol., 14, 195, 10.1038/nri3622 Candelario, 2014, The role of extracellular vesicles in the progression of neurodegenerative disease and cancer, Trends Mol. Med., 20, 368, 10.1016/j.molmed.2014.04.003 Record, 2014, Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies, Biochim. Biophys. Acta., 1841, 108, 10.1016/j.bbalip.2013.10.004 Buzas, 2014, Emerging role of extracellular vesicles in inflammatory diseases, Nat. Rev. Rheumatol., 10, 356, 10.1038/nrrheum.2014.19 Chen, 2014, Exosomes from drug-resistant breast cancer cells transmit chemoresistance by a horizontal transfer of microRNAs, PLoS One., 9, e95240, 10.1371/journal.pone.0095240 Rajendran, 2014, Emerging roles of extracellular vesicles in the nervous system, J. Neurosci., 34, 15482, 10.1523/JNEUROSCI.3258-14.2014 Post, 1992, Characterization of a cell line derived from a human oligodendroglioma, Mol. Chem. Neuropathol., 16, 303, 10.1007/BF03159976 Bakhti, 2011, Inhibition of myelin membrane sheath formation by oligodendrocyte-derived exosome-like vesicles, J. Biol. Chem., 286, 787, 10.1074/jbc.M110.190009 Smith, 1985, Measurement of protein using bicinchoninic acid, Anal. Biochem., 150, 76, 10.1016/0003-2697(85)90442-7 Bielawski, 2009, Comprehensive quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry, Methods Mol. Biol., 579, 443, 10.1007/978-1-60761-322-0_22 Bielawski, 2010, Sphingolipid analysis by high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS), Adv. Exp. Med. Biol., 688, 46, 10.1007/978-1-4419-6741-1_3 Krysko, 2008, Apoptosis and necrosis: detection, discrimination and phagocytosis, Methods., 44, 205, 10.1016/j.ymeth.2007.12.001 Li, 1991, Shedding of human neuroblastoma gangliosides, Biochim. Biophys. Acta., 1083, 57, 10.1016/0005-2760(91)90124-Z Kjellberg, 2015, Metabolic conversion of ceramides in HeLa cells - a cholesteryl phosphocholine delivery approach, PLoS One., 10, e0143385, 10.1371/journal.pone.0143385 Qin, 2010, Neurons and oligodendrocytes recycle sphingosine 1-phosphate to ceramide: significance for apoptosis and multiple sclerosis, J. Biol. Chem., 285, 14134, 10.1074/jbc.M109.076810 Kim, 2012, Aberrant upregulation of astroglial ceramide potentiates oligodendrocyte injury, Brain Pathol., 22, 41, 10.1111/j.1750-3639.2011.00501.x Osawa, 2005, Roles for C16-ceramide and sphingosine 1-phosphate in regulating hepatocyte apoptosis in response to tumor necrosis factor-alpha, J. Biol. Chem., 280, 27879, 10.1074/jbc.M503002200 White-Gilbertson, 2009, Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells, Oncogene., 28, 1132, 10.1038/onc.2008.468 D'Agostino, 2006, Membrane vesicles shed by oligodendroglioma cells induce neuronal apoptosis, Int. J. Oncol., 29, 1075 Merrill, 2011, Sphingolipid and glycosphingolipid metabolic pathways in the era of sphingolipidomics, Chem. Rev., 111, 6387, 10.1021/cr2002917 Mencarelli, 2013, Ceramide function in the brain: when a slight tilt is enough, Cell. Mol. Life Sci., 70, 181, 10.1007/s00018-012-1038-x Wheeler, 2008, A defect of sphingolipid metabolism modifies the properties of normal appearing white matter in multiple sclerosis, Brain., 131, 3092, 10.1093/brain/awn190 Vidaurre, 2014, Cerebrospinal fluid ceramides from patients with multiple sclerosis impair neuronal bioenergetics, Brain., 137, 2271, 10.1093/brain/awu139 Mathivanan, 2009, ExoCarta: A compendium of exosomal proteins and RNA, Proteomics., 9, 4997, 10.1002/pmic.200900351 Mathivanan, 2012, ExoCarta 2012: database of exosomal proteins, RNA and lipids, Nucleic Acids Res., 40, D1241, 10.1093/nar/gkr828 Lakhal, 2011, Exosome nanotechnology: an emerging paradigm shift in drug delivery: exploitation of exosome nanovesicles for systemic in vivo delivery of RNAi heralds new horizons for drug delivery across biological barriers, BioEssays., 33, 737, 10.1002/bies.201100076