Acid sphingomyelinase deactivation post-ischemia promotes brain angiogenesis and remodeling by small extracellular vesicles.


Journal

Basic research in cardiology
ISSN: 1435-1803
Titre abrégé: Basic Res Cardiol
Pays: Germany
ID NLM: 0360342

Informations de publication

Date de publication:
12 2022
Historique:
received: 19 07 2021
accepted: 08 08 2022
revised: 17 07 2022
entrez: 29 8 2022
pubmed: 30 8 2022
medline: 1 9 2022
Statut: ppublish

Résumé

Antidepressants have been reported to enhance stroke recovery independent of the presence of depressive symptoms. They have recently been proposed to exert their mood-stabilizing actions by inhibition of acid sphingomyelinase (ASM), which catalyzes the hydrolysis of sphingomyelin to ceramide. Their restorative action post-ischemia/reperfusion (I/R) still had to be defined. Mice subjected to middle cerebral artery occlusion or cerebral microvascular endothelial cells exposed to oxygen-glucose deprivation were treated with vehicle or with the chemically and pharmacologically distinct antidepressants amitriptyline, fluoxetine or desipramine. Brain ASM activity significantly increased post-I/R, in line with elevated ceramide levels in microvessels. ASM inhibition by amitriptyline reduced ceramide levels, and increased microvascular length and branching point density in wildtype, but not sphingomyelinase phosphodiesterase-1 ([Smpd1]

Identifiants

pubmed: 36038749
doi: 10.1007/s00395-022-00950-7
pii: 10.1007/s00395-022-00950-7
pmc: PMC9424180
doi:

Substances chimiques

Antidepressive Agents 0
Ceramides 0
Fluoxetine 01K63SUP8D
Amitriptyline 1806D8D52K
Desipramine TG537D343B

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

43

Subventions

Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Abe T, Niizuma K, Kanoke A, Saigusa D, Saito R, Uruno A, Fujimura M, Yamamoto M, Tominaga T (2018) Metabolomic Analysis of Mouse Brain after a Transient Middle Cerebral Artery Occlusion by Mass Spectrometry Imaging. Neurol Med Chir (Tokyo) 58:384–392. https://doi.org/10.2176/nmc.oa.2018-0054
doi: 10.2176/nmc.oa.2018-0054
Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, Carson AP, Chamberlain AM, Chang AR, Cheng S, Das SR, Delling FN, Djousse L, Elkind MSV, Ferguson JF, Fornage M, Jordan LC, Khan SS, Kissela BM, Knutson KL, Kwan TW, Lackland DT, Lewis TT, Lichtman JH, Longenecker CT, Loop MS, Lutsey PL, Martin SS, Matsushita K, Moran AE, Mussolino ME, O’Flaherty M, Pandey A, Perak AM, Rosamond WD, Roth GA, Sampson UKA, Satou GM, Schroeder EB, Shah SH, Spartano NL, Stokes A, Tirschwell DL, Tsao CW, Turakhia MP, VanWagner LB, Wilkins JT, Wong SS, Virani SS, American Heart Association Council on E, Prevention Statistics C, Stroke Statistics S (2019) Heart Disease and stroke statistics-2019 update: a report from the American Heart Association. Circulation 139:e56–e528. https://doi.org/10.1161/CIR.0000000000000659
doi: 10.1161/CIR.0000000000000659
Brunkhorst R, Friedlaender F, Ferreiros N, Schwalm S, Koch A, Grammatikos G, Toennes S, Foerch C, Pfeilschifter J, Pfeilschifter W (2015) Alterations of the ceramide metabolism in the peri-infarct cortex are independent of the sphingomyelinase pathway and not influenced by the acid sphingomyelinase inhibitor fluoxetine. Neural Plast. https://doi.org/10.1155/2015/503079
doi: 10.1155/2015/503079
Burkhart JM, Schumbrutzki C, Wortelkamp S, Sickmann A, Zahedi RP (2012) Systematic and quantitative comparison of digest efficiency and specificity reveals the impact of trypsin quality on MS-based proteomics. J Proteom 75:1454–1462. https://doi.org/10.1016/j.jprot.2011.11.016
doi: 10.1016/j.jprot.2011.11.016
Chabriat H, Bassetti CL, Marx U, Audoli-Inthavong ML, Sors A, Lambert E, Wattez M, Hermann DM, investigators RBs (2020) Safety and efficacy of GABAA alpha5 antagonist S44819 in patients with ischaemic stroke: a multicentre, double-blind, randomised, placebo-controlled trial. Lancet Neurol 19:226–233. https://doi.org/10.1016/S1474-4422(20)30004-1
doi: 10.1016/S1474-4422(20)30004-1
Chao HC, Lee TH, Chiang CS, Yang SY, Kuo CH, Tang SC (2019) Sphingolipidomics investigation of the temporal dynamics after ischemic brain injury. J Proteome Res 18:3470–3478. https://doi.org/10.1021/acs.jproteome.9b00370
doi: 10.1021/acs.jproteome.9b00370
Chollet F, Tardy J, Albucher JF, Thalamas C, Berard E, Lamy C, Bejot Y, Deltour S, Jaillard A, Niclot P, Guillon B, Moulin T, Marque P, Pariente J, Arnaud C, Loubinoux I (2011) Fluoxetine for motor recovery after acute ischaemic stroke (FLAME): a randomised placebo-controlled trial. Lancet Neurol 10:123–130. https://doi.org/10.1016/S1474-4422(10)70314-8
doi: 10.1016/S1474-4422(10)70314-8
Clark WM, Lessov NS, Dixon MP, Eckenstein F (1997) Monofilament intraluminal middle cerebral artery occlusion in the mouse. Neurol Res 19:641–648. https://doi.org/10.1080/01616412.1997.11740874
doi: 10.1080/01616412.1997.11740874
Deng X, Yin X, Allan R, Lu DD, Maurer CW, Haimovitz-Friedman A, Fuks Z, Shaham S, Kolesnick R (2008) Ceramide biogenesis is required for radiation-induced apoptosis in the germ line of C. elegans. Science 322:110–115. https://doi.org/10.1126/science.1158111
doi: 10.1126/science.1158111
Doeppner TR, Herz J, Gorgens A, Schlechter J, Ludwig AK, Radtke S, de Miroschedji K, Horn PA, Giebel B, Hermann DM (2015) Extracellular vesicles improve post-stroke neuroregeneration and prevent postischemic immunosuppression. Stem Cells Transl Med 4:1131–1143. https://doi.org/10.5966/sctm.2015-0078
doi: 10.5966/sctm.2015-0078
EFFECTS Trial Collaboration (2020) Safety and efficacy of fluoxetine on functional recovery after acute stroke (EFFECTS): a randomised, double-blind, placebo-controlled trial. Lancet Neurol 19:661–669. https://doi.org/10.1016/S1474-4422(20)30219-2
doi: 10.1016/S1474-4422(20)30219-2
Ermini L, Ausman J, Melland-Smith M, Yeganeh B, Rolfo A, Litvack ML, Todros T, Letarte M, Post M, Caniggia I (2017) A single sphingomyelin species promotes exosomal release of endoglin into the maternal circulation in preeclampsia. Sci Rep 7:12172. https://doi.org/10.1038/s41598-017-12491-4
doi: 10.1038/s41598-017-12491-4
Focus Trial Collaboration (2019) Effects of fluoxetine on functional outcomes after acute stroke (FOCUS): a pragmatic, double-blind, randomised, controlled trial. Lancet (London, England) 393:265–274. https://doi.org/10.1016/S0140-6736(18)32823-X
doi: 10.1016/S0140-6736(18)32823-X
Gorgens A, Bremer M, Ferrer-Tur R, Murke F, Tertel T, Horn PA, Thalmann S, Welsh JA, Probst C, Guerin C, Boulanger CM, Jones JC, Hanenberg H, Erdbrugger U, Lannigan J, Ricklefs FL, El-Andaloussi S, Giebel B (2019) Optimisation of imaging flow cytometry for the analysis of single extracellular vesicles by using fluorescence-tagged vesicles as biological reference material. J Extracell Vesicles 8:1587567. https://doi.org/10.1080/20013078.2019.1587567
doi: 10.1080/20013078.2019.1587567
Gulbins A, Grassme H, Hoehn R, Wilker B, Soddemann M, Kohnen M, Edwards MJ, Kornhuber J, Gulbins E (2016) Regulation of neuronal stem cell proliferation in the hippocampus by endothelial ceramide. Cell Physiol Biochem 39:790–801. https://doi.org/10.1159/000447789
doi: 10.1159/000447789
Gulbins A, Schumacher F, Becker KA, Wilker B, Soddemann M, Boldrin F, Muller CP, Edwards MJ, Goodman M, Caldwell CC, Kleuser B, Kornhuber J, Szabo I, Gulbins E (2018) Antidepressants act by inducing autophagy controlled by sphingomyelin-ceramide. Mol Psychiatry 23:2324–2346. https://doi.org/10.1038/s41380-018-0090-9
doi: 10.1038/s41380-018-0090-9
Gulbins E, Palmada M, Reichel M, Luth A, Bohmer C, Amato D, Muller CP, Tischbirek CH, Groemer TW, Tabatabai G, Becker KA, Tripal P, Staedtler S, Ackermann TF, van Brederode J, Alzheimer C, Weller M, Lang UE, Kleuser B, Grassme H, Kornhuber J (2013) Acid sphingomyelinase-ceramide system mediates effects of antidepressant drugs. Nat Med 19:934–938. https://doi.org/10.1038/nm.3214
doi: 10.1038/nm.3214
Hacke W, Kaste M, Bluhmki E, Brozman M, Davalos A, Guidetti D, Larrue V, Lees KR, Medeghri Z, Machnig T, Schneider D, von Kummer R, Wahlgren N, Toni D, Investigators E (2008) Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 359:1317–1329. https://doi.org/10.1056/NEJMoa0804656
doi: 10.1056/NEJMoa0804656
Herr I, Martin-Villalba A, Kurz E, Roncaioli P, Schenkel J, Cifone MG, Debatin KM (1999) FK506 prevents stroke-induced generation of ceramide and apoptosis signaling. Brain Res 826:210–219
doi: 10.1016/S0006-8993(99)01288-3
Herz J, Reitmeir R, Hagen SI, Reinboth BS, Guo Z, Zechariah A, ElAli A, Doeppner TR, Bacigaluppi M, Pluchino S, Kilic U, Kilic E, Hermann DM (2012) Intracerebroventricularly delivered VEGF promotes contralesional corticorubral plasticity after focal cerebral ischemia via mechanisms involving anti-inflammatory actions. Neurobiol Dis 45:1077–1085. https://doi.org/10.1016/j.nbd.2011.12.026
doi: 10.1016/j.nbd.2011.12.026
Jernigan PL, Makley AT, Hoehn RS, Edwards MJ, Pritts TA (2015) The role of sphingolipids in endothelial barrier function. Biol Chem 396:681–691. https://doi.org/10.1515/hsz-2014-0305
doi: 10.1515/hsz-2014-0305
Jin F, Hagemann N, Brockmeier U, Schafer ST, Zechariah A, Hermann DM (2013) LDL attenuates VEGF-induced angiogenesis via mechanisms involving VEGFR2 internalization and degradation following endosome-trans-Golgi network trafficking. Angiogenesis 16:625–637. https://doi.org/10.1007/s10456-013-9340-2
doi: 10.1007/s10456-013-9340-2
Jin F, Hagemann N, Sun L, Wu J, Doeppner TR, Dai Y, Hermann DM (2018) High-density lipoprotein (HDL) promotes angiogenesis via S1P3-dependent VEGFR2 activation. Angiogenesis 21:381–394. https://doi.org/10.1007/s10456-018-9603-z
doi: 10.1007/s10456-018-9603-z
Jorge RE, Robinson RG, Arndt S, Starkstein S (2003) Mortality and poststroke depression: a placebo-controlled trial of antidepressants. Am J Psychiatry 160:1823–1829. https://doi.org/10.1176/appi.ajp.160.10.1823
doi: 10.1176/appi.ajp.160.10.1823
Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, Sawamoto K (2010) Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells 28:545–554. https://doi.org/10.1002/stem.306
doi: 10.1002/stem.306
Kornhuber J, Muller CP, Becker KA, Reichel M, Gulbins E (2014) The ceramide system as a novel antidepressant target. Trends Pharmacol Sci 35:293–304. https://doi.org/10.1016/j.tips.2014.04.003
doi: 10.1016/j.tips.2014.04.003
Kornhuber J, Tripal P, Reichel M, Terfloth L, Bleich S, Wiltfang J, Gulbins E (2008) Identification of new functional inhibitors of acid sphingomyelinase using a structure-property-activity relation model. J Med Chem 51:219–237. https://doi.org/10.1021/jm070524a
doi: 10.1021/jm070524a
Li WL, Cai HH, Wang B, Chen L, Zhou QG, Luo CX, Liu N, Ding XS, Zhu DY (2009) Chronic fluoxetine treatment improves ischemia-induced spatial cognitive deficits through increasing hippocampal neurogenesis after stroke. J Neurosci Res 87:112–122. https://doi.org/10.1002/jnr.21829
doi: 10.1002/jnr.21829
Lim CM, Kim SW, Park JY, Kim C, Yoon SH, Lee JK (2009) Fluoxetine affords robust neuroprotection in the postischemic brain via its anti-inflammatory effect. J Neurosci Res 87:1037–1045. https://doi.org/10.1002/jnr.21899
doi: 10.1002/jnr.21899
Lin DJ, Finklestein SP, Cramer SC (2018) New directions in treatments targeting stroke recovery. Stroke 49:3107–3114. https://doi.org/10.1161/STROKEAHA.118.021359
doi: 10.1161/STROKEAHA.118.021359
Ludwig KR, Schroll MM, Hummon AB (2018) Comparison of In-solution, FASP, and S-trap based digestion methods for bottom-up proteomic studies. J Proteome Res 17:2480–2490. https://doi.org/10.1021/acs.jproteome.8b00235
doi: 10.1021/acs.jproteome.8b00235
Lugo-Hernandez E, Squire A, Hagemann N, Brenzel A, Sardari M, Schlechter J, Sanchez-Mendoza EH, Gunzer M, Faissner A, Hermann DM (2017) 3D visualization and quantification of microvessels in the whole ischemic mouse brain using solvent-based clearing and light sheet microscopy. J Cereb Blood Flow Metab 37:3355–3367. https://doi.org/10.1177/0271678X17698970
doi: 10.1177/0271678X17698970
Manoonkitiwongsa PS, Jackson-Friedman C, McMillan PJ, Schultz RL, Lyden PD (2001) Angiogenesis after stroke is correlated with increased numbers of macrophages: the clean-up hypothesis. J Cereb Blood Flow Metab 21:1223–1231. https://doi.org/10.1097/00004647-200110000-00011
doi: 10.1097/00004647-200110000-00011
Menck K, Sonmezer C, Worst TS, Schulz M, Dihazi GH, Streit F, Erdmann G, Kling S, Boutros M, Binder C, Gross JC (2017) Neutral sphingomyelinases control extracellular vesicles budding from the plasma membrane. J Extracell Vesicles 6:1378056. https://doi.org/10.1080/20013078.2017.1378056
doi: 10.1080/20013078.2017.1378056
Merz SF, Korste S, Bornemann L, Michel L, Stock P, Squire A, Soun C, Engel DR, Detzer J, Lorchner H, Hermann DM, Kamler M, Klode J, Hendgen-Cotta UB, Rassaf T, Gunzer M, Totzeck M (2019) Contemporaneous 3D characterization of acute and chronic myocardial I/R injury and response. Nat Commun 10:2312. https://doi.org/10.1038/s41467-019-10338-2
doi: 10.1038/s41467-019-10338-2
Naser E, Kadow S, Schumacher F, Mohamed ZH, Kappe C, Hessler G, Pollmeier B, Kleuser B, Arenz C, Becker KA, Gulbins E, Carpinteiro A (2020) Characterization of the small molecule ARC39, a direct and specific inhibitor of acid sphingomyelinase in vitro. J Lipid Res 61:896–910. https://doi.org/10.1194/jlr.RA120000682
doi: 10.1194/jlr.RA120000682
Nielsen MM, Lambertsen KL, Clausen BH, Meyer M, Bhandari DR, Larsen ST, Poulsen SS, Spengler B, Janfelt C, Hansen HS (2016) Mass spectrometry imaging of biomarker lipids for phagocytosis and signalling during focal cerebral ischaemia. Sci Rep 6:39571. https://doi.org/10.1038/srep39571
doi: 10.1038/srep39571
Nogueira RG, Jadhav AP, Haussen DC, Bonafe A, Budzik RF, Bhuva P, Yavagal DR, Ribo M, Cognard C, Hanel RA, Sila CA, Hassan AE, Millan M, Levy EI, Mitchell P, Chen M, English JD, Shah QA, Silver FL, Pereira VM, Mehta BP, Baxter BW, Abraham MG, Cardona P, Veznedaroglu E, Hellinger FR, Feng L, Kirmani JF, Lopes DK, Jankowitz BT, Frankel MR, Costalat V, Vora NA, Yoo AJ, Malik AM, Furlan AJ, Rubiera M, Aghaebrahim A, Olivot JM, Tekle WG, Shields R, Graves T, Lewis RJ, Smith WS, Liebeskind DS, Saver JL, Jovin TG, Investigators DT (2018) Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct. N Engl J Med 378:11–21. https://doi.org/10.1056/NEJMoa1706442
doi: 10.1056/NEJMoa1706442
Ohtani R, Tomimoto H, Kondo T, Wakita H, Akiguchi I, Shibasaki H, Okazaki T (2004) Upregulation of ceramide and its regulating mechanism in a rat model of chronic cerebral ischemia. Brain Res 1023:31–40. https://doi.org/10.1016/j.brainres.2004.07.024
doi: 10.1016/j.brainres.2004.07.024
Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, Pesch R, Makarov A, Lange O, Horning S, Mann M (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteom 4:2010–2021. https://doi.org/10.1074/mcp.T500030-MCP200
doi: 10.1074/mcp.T500030-MCP200
Pariente J, Loubinoux I, Carel C, Albucher JF, Leger A, Manelfe C, Rascol O, Chollet F (2001) Fluoxetine modulates motor performance and cerebral activation of patients recovering from stroke. Ann Neurol 50:718–729
doi: 10.1002/ana.1257
Park MH, Lee JY, Park KH, Jung IK, Kim KT, Lee YS, Ryu HH, Jeong Y, Kang M, Schwaninger M, Gulbins E, Reichel M, Kornhuber J, Yamaguchi T, Kim HJ, Kim SH, Schuchman EH, Jin HK, Bae JS (2018) Vascular and neurogenic rejuvenation in aging mice by modulation of ASM. Neuron 100:762. https://doi.org/10.1016/j.neuron.2018.10.038
doi: 10.1016/j.neuron.2018.10.038
Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, Coscia C, Iessi E, Logozzi M, Molinari A, Colone M, Tatti M, Sargiacomo M, Fais S (2009) Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 284:34211–34222. https://doi.org/10.1074/jbc.M109.041152
doi: 10.1074/jbc.M109.041152
Reitmeir R, Kilic E, Kilic U, Bacigaluppi M, ElAli A, Salani G, Pluchino S, Gassmann M, Hermann DM (2011) Post-acute delivery of erythropoietin induces stroke recovery by promoting perilesional tissue remodelling and contralesional pyramidal tract plasticity. Brain 134:84–99. https://doi.org/10.1093/brain/awq344
doi: 10.1093/brain/awq344
Robinson RG, Schultz SK, Castillo C, Kopel T, Kosier JT, Newman RM, Curdue K, Petracca G, Starkstein SE (2000) Nortriptyline versus fluoxetine in the treatment of depression and in short-term recovery after stroke: a placebo-controlled, double-blind study. Am J Psychiatry 157:351–359. https://doi.org/10.1176/appi.ajp.157.3.351
doi: 10.1176/appi.ajp.157.3.351
Salomon C, Ryan J, Sobrevia L, Kobayashi M, Ashman K, Mitchell M, Rice GE (2013) Exosomal signaling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis. PLoS ONE 8:e68451. https://doi.org/10.1371/journal.pone.0068451
doi: 10.1371/journal.pone.0068451
Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338–1340. https://doi.org/10.1126/science.1095505
doi: 10.1126/science.1095505
Shin TK, Kang MS, Lee HY, Seo MS, Kim SG, Kim CD, Lee WS (2009) Fluoxetine and sertraline attenuate postischemic brain injury in mice. Korean J Physiol Pharmacol 13:257–263. https://doi.org/10.4196/kjpp.2009.13.3.257
doi: 10.4196/kjpp.2009.13.3.257
Sokolova V, Ludwig AK, Hornung S, Rotan O, Horn PA, Epple M, Giebel B (2011) Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf B Biointerfaces 87:146–150. https://doi.org/10.1016/j.colsurfb.2011.05.013
doi: 10.1016/j.colsurfb.2011.05.013
Stinear CM, Lang CE, Zeiler S, Byblow WD (2020) Advances and challenges in stroke rehabilitation. Lancet Neurol 19:348–360. https://doi.org/10.1016/S1474-4422(19)30415-6
doi: 10.1016/S1474-4422(19)30415-6
Sun P, Zhang K, Hassan SH, Zhang X, Tang X, Pu H, Stetler RA, Chen J, Yin KJ (2020) Endothelium-targeted deletion of microRNA-15a/16-1 promotes poststroke angiogenesis and improves long-term neurological recovery. Circ Res 126:1040–1057. https://doi.org/10.1161/CIRCRESAHA.119.315886
doi: 10.1161/CIRCRESAHA.119.315886
Thery C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, Antoniou A, Arab T, Archer F, Atkin-Smith GK, Ayre DC, Bach JM, Bachurski D, Baharvand H, Balaj L, Baldacchino S, Bauer NN, Baxter AA, Bebawy M, Beckham C, Bedina Zavec A, Benmoussa A, Berardi AC, Bergese P, Bielska E, Blenkiron C, Bobis-Wozowicz S, Boilard E, Boireau W, Bongiovanni A, Borras FE, Bosch S, Boulanger CM, Breakefield X, Breglio AM, Brennan MA, Brigstock DR, Brisson A, Broekman ML, Bromberg JF, Bryl-Gorecka P, Buch S, Buck AH, Burger D, Busatto S, Buschmann D, Bussolati B, Buzas EI, Byrd JB, Camussi G, Carter DR, Caruso S, Chamley LW, Chang YT, Chen C, Chen S, Cheng L, Chin AR, Clayton A, Clerici SP, Cocks A, Cocucci E, Coffey RJ, Cordeiro-da-Silva A, Couch Y, Coumans FA, Coyle B, Crescitelli R, Criado MF, D’Souza-Schorey C, Das S, Datta Chaudhuri A, de Candia P, De Santana EF, De Wever O, Del Portillo HA, Demaret T, Deville S, Devitt A, Dhondt B, Di Vizio D, Dieterich LC, Dolo V, Dominguez Rubio AP, Dominici M, Dourado MR, Driedonks TA, Duarte FV, Duncan HM, Eichenberger RM, Ekstrom K, El Andaloussi S, Elie-Caille C, Erdbrugger U, Falcon-Perez JM, Fatima F, Fish JE, Flores-Bellver M, Forsonits A, Frelet-Barrand A et al (2018) Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles 7:1535750. https://doi.org/10.1080/20013078.2018.1535750
doi: 10.1080/20013078.2018.1535750
Thery C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2:569–579. https://doi.org/10.1038/nri855
doi: 10.1038/nri855
Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B, Simons M (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319:1244–1247. https://doi.org/10.1126/science.1153124
doi: 10.1126/science.1153124
Umezu T, Tadokoro H, Azuma K, Yoshizawa S, Ohyashiki K, Ohyashiki JH (2014) Exosomal miR-135b shed from hypoxic multiple myeloma cells enhances angiogenesis by targeting factor-inhibiting HIF-1. Blood 124:3748–3757. https://doi.org/10.1182/blood-2014-05-576116
doi: 10.1182/blood-2014-05-576116
Verderio C, Gabrielli M, Giussani P (2018) Role of sphingolipids in the biogenesis and biological activity of extracellular vesicles. J Lipid Res 59:1325–1340. https://doi.org/10.1194/jlr.R083915
doi: 10.1194/jlr.R083915
Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, Birrer MJ, Szabo E, Zon LI, Kyriakis JM, Haimovitz-Friedman A, Fuks Z, Kolesnick RN (1996) Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380:75–79. https://doi.org/10.1038/380075a0
doi: 10.1038/380075a0
Wang YC, Dzyubenko E, Sanchez-Mendoza EH, Sardari M, Silva de Carvalho T, Doeppner TR, Kaltwasser B, Machado P, Kleinschnitz C, Bassetti CL, Hermann DM (2018) Postacute delivery of GABAA alpha5 antagonist promotes postischemic neurological recovery and peri-infarct brain remodeling. Stroke 49:2495–2503. https://doi.org/10.1161/STROKEAHA.118.021378
doi: 10.1161/STROKEAHA.118.021378
Ward NS (2017) Restoring brain function after stroke - bridging the gap between animals and humans. Nat Rev Neurol 13:244–255. https://doi.org/10.1038/nrneurol.2017.34
doi: 10.1038/nrneurol.2017.34
Xin H, Li Y, Cui Y, Yang JJ, Zhang ZG, Chopp M (2013) Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. J Cereb Blood Flow Metab 33:1711–1715. https://doi.org/10.1038/jcbfm.2013.152
doi: 10.1038/jcbfm.2013.152
Yu ZF, Nikolova-Karakashian M, Zhou D, Cheng G, Schuchman EH, Mattson MP (2000) Pivotal role for acidic sphingomyelinase in cerebral ischemia-induced ceramide and cytokine production, and neuronal apoptosis. J Mol Neurosci 15:85–97. https://doi.org/10.1385/JMN:15:2:85
doi: 10.1385/JMN:15:2:85
Zhang WH, Wang H, Wang X, Narayanan MV, Stavrovskaya IG, Kristal BS, Friedlander RM (2008) Nortriptyline protects mitochondria and reduces cerebral ischemia/hypoxia injury. Stroke 39:455–462. https://doi.org/10.1161/STROKEAHA.107.496810
doi: 10.1161/STROKEAHA.107.496810
Zhang ZG, Chopp M (2015) Promoting brain remodeling to aid in stroke recovery. Trends Mol Med 21:543–548. https://doi.org/10.1016/j.molmed.2015.07.005
doi: 10.1016/j.molmed.2015.07.005

Auteurs

Ayan Mohamud Yusuf (A)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.

Nina Hagemann (N)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.

Xiaoni Zhang (X)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.

Maria Zafar (M)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.

Tanja Hussner (T)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.

Carolin Bromkamp (C)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.

Carlotta Martiny (C)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.

Tobias Tertel (T)

Institute of Transfusion Medicine, University Hospital Essen, Essen, Germany.

Verena Börger (V)

Institute of Transfusion Medicine, University Hospital Essen, Essen, Germany.

Fabian Schumacher (F)

Institute of Molecular Biology, University Hospital Essen, Essen, Germany.
Department of Toxicology, University of Potsdam, Nuthetal, Germany.
Institute of Pharmacy, Freie Universität Berlin, Berlin, Germany.

Fiorella A Solari (FA)

Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., Dortmund, Germany.

Mike Hasenberg (M)

Institute of Immunology and Experimental Imaging, University Hospital Essen, Essen, Germany.

Christoph Kleinschnitz (C)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.

Thorsten R Doeppner (TR)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany.
Department of Neurology, University Medicine Göttingen, Göttingen, Germany.

Burkhard Kleuser (B)

Department of Toxicology, University of Potsdam, Nuthetal, Germany.

Albert Sickmann (A)

Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., Dortmund, Germany.
Medizinisches Proteom-Center (MPC), Ruhr University, Bochum, Germany.
Department of Chemistry, College of Physical Sciences, University of Aberdeen, Aberdeen, Scotland, UK.

Matthias Gunzer (M)

Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., Dortmund, Germany.
Institute of Immunology and Experimental Imaging, University Hospital Essen, Essen, Germany.

Bernd Giebel (B)

Institute of Transfusion Medicine, University Hospital Essen, Essen, Germany.

Richard Kolesnick (R)

Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Erich Gulbins (E)

Institute of Molecular Biology, University Hospital Essen, Essen, Germany.

Dirk M Hermann (DM)

Department of Neurology, University Hospital Essen, Hufelandstr. 55, 45122, Essen, Germany. dirk.hermann@uk-essen.de.
Center for Translational and Behavioral Neurosciences, University Hospital Essen, Essen, Germany. dirk.hermann@uk-essen.de.

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