Cellular microparticles and pathophysiology of traumatic brain injury

Zilong Zhao, Yuan Zhou, Ye Tian, Min Li, Jing-fei Dong, Jianning Zhang

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Protein Cell ›› 2017, Vol. 8 ›› Issue (11) : 801-810. DOI: 10.1007/s13238-017-0414-6
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REVIEW

Cellular microparticles and pathophysiology of traumatic brain injury

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Abstract

Traumatic brain injury (TBI) is a leading cause of death and disability worldwide. The finding that cellular microparticles (MPs) generated by injured cells profoundly impact on pathological courses of TBI has paved the way for new diagnostic and therapeutic strategies. MPs are subcellular fragments or organelles that serve as carriers of lipids, adhesive receptors, cytokines, nucleic acids, and tissue-degrading enzymes that are unique to the parental cells. Their sub-micron sizes allow MPs to travel to areas that parental cells are unable to reach to exercise diverse biological functions. In this review, we summarize recent developments in identifying a casual role of MPs in the pathologies of TBI and suggest that MPs serve as a new class of therapeutic targets for the prevention and treatment of TBI and associated systemic complications.

Keywords

traumatic brain injury / cellular microparticles / coagulopathy / inflammation

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Zilong Zhao, Yuan Zhou, Ye Tian, Min Li, Jing-fei Dong, Jianning Zhang. Cellular microparticles and pathophysiology of traumatic brain injury. Protein Cell, 2017, 8(11): 801‒810 https://doi.org/10.1007/s13238-017-0414-6

References

[1]
AlkhamisTM, Beissinger RL, ChediakJR (1990) Artificial surface effect on red blood cells and platelets in laminar shear flow.Blood75:1568–1575
[2]
AndrewsAM, LuttonEM, MerkelSF, Razmpour R, RamirezSH (2016) Mechanical injury induces brain endothelial-derived microvesicle release: implications for cerebral vascular injury during traumatic brain injury.Front Cell Neurosci10:43
CrossRef Google scholar
[3]
ArthurJF, Gardiner EE, KennyD , AndrewsRK, BerndtMC (2008) Platelet receptor redox regulation.Platelets19:1–8
CrossRef Google scholar
[4]
AuerLM, OttE (1979) Disturbances of the coagulatory system in patients with severe cerebral trauma. II Platelet function.Acta Neurochir (Wien)49:219–226
CrossRef Google scholar
[5]
AwasthiD, RockWA, CareyME, Farrell JB (1991) Coagulation changes after an experimental missile wound to the brain in the cat.Surg Neurol36:441–446
CrossRef Google scholar
[6]
BayirH, TyurinVA, TyurinaYY, Viner R, RitovV , AmoscatoAA, ZhaoQ, ZhangXJ, Janesko-Feldman KL, AlexanderH , BasovaLV, ClarkRS, KochanekPM, Kagan VE (2007) Selective early cardiolipin peroxidation after traumatic brain injury: an oxidative lipidomics analysis.Ann Neurol62:154–169
CrossRef Google scholar
[7]
BegonjaAJ,Gambaryan S, GeigerJ , AktasB, Pozgajova M, NieswandtB , WalterU(2005) Platelet NAD(P)H-oxidase-generated ROS production regulates alphaIIbbeta3-integrin activation independent of the NO/cGMP pathway.Blood106:2757–2760
CrossRef Google scholar
[8]
BetaneliV, PetrovEP, SchwilleP (2012) The role of lipids in VDAC oligomerization. Biophys J102:523–531
CrossRef Google scholar
[9]
BiancoF, Pravettoni E, ColomboA , SchenkU, MollerT, MatteoliM, Verderio C (2005) Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia.J Immunol174:7268–7277
CrossRef Google scholar
[10]
BiancoF, Perrotta C, NovellinoL , FrancoliniM, Riganti L, MennaE , SagliettiL, Schuchman EH, FurlanR , ClementiE, Matteoli M, VerderioC (2009) Acid sphingomyelinase activity triggers microparticle release from glial cells.EMBO J28:1043–1054
CrossRef Google scholar
[11]
BiroE, Akkerman JW, HoekFJ , GorterG, PronkLM, SturkA, Nieuwland R (2005) The phospholipid composition and cholesterol content of platelet-derived microparticles: a comparison with platelet membrane fractions.J Thromb Haemost3:2754–2763
CrossRef Google scholar
[12]
BirtsCN, BartonCH, WiltonDC (2010) Catalytic and non-catalytic functions of human IIA phospholipase A2.Trends Biochem Sci35:28–35
CrossRef Google scholar
[13]
BochkovVN, Oskolkova OV, BirukovKG , LevonenAL, BinderCJ, StocklJ (2010) Generation and biological activities of oxidized phospholipids.Antioxid Redox Signal12:1009–1059
CrossRef Google scholar
[14]
BohmanLE,RileyJ, MilovanovaTN , SanbornMR, ThomSR, ArmsteadWM (2016) Microparticles impair hypotensive cerebrovasodilation and cause hippocampal neuronal cell injury after traumatic brain injury.J Neurotrauma33:168–174
CrossRef Google scholar
[15]
BoudreauLH, DuchezAC, CloutierN, Soulet D, MartinN , BollingerJ, PareA, RousseauM, Naika GS, LevesqueT , LaflammeC, Marcoux G, LambeauG , FarndaleRW, Pouliot M, Hamzeh- CognasseH , CognasseF, Garraud O, NigrovicPA , GuderleyH, Lacroix S, ThibaultL , SempleJW, GelbMH, BoilardE (2014) Platelets release mitochondria serving as substrate for bactericidal group IIA-secreted phospholipase A2 to promote inflammation.Blood124:2173–2183
CrossRef Google scholar
[16]
BrownSB, ClarkeMC, MagowanL, Sanderson H, SavillJ (2000) Constitutive death of platelets leading to scavenger receptormediated phagocytosis.A caspase-independent cell clearance program. J Biol Chem275:5987–5996
CrossRef Google scholar
[17]
BudnikV, Ruiz-Canada C, WendlerF (2016) Extracellular vesicles round off communication in the nervous system.Nat Rev Neurosci17:160–172
CrossRef Google scholar
[18]
CaiJ, HanY, RenH, Chen C, HeD , ZhouL, EisnerGM, AsicoLD, Jose PA, ZengC (2013) Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells.J Mol Cell Biol5:227–238
CrossRef Google scholar
[19]
CavallucciV, Bisicchia E, CencioniMT , FerriA, LatiniL, NobiliA, Biamonte F, NazioF , FanelliF, MorenoS, MolinariM, Viscomi MT, D’AmelioM (2014) Acute focal brain damage alters mitochondrial dynamics and autophagy in axotomized neurons.Cell Death Dis5:e1545
CrossRef Google scholar
[20]
ChangR, Cardenas JC, WadeCE , HolcombJB (2016) Advances in the understanding of trauma-induced coagulopathy.Blood128:1043–1049
CrossRef Google scholar
[21]
ChengG, KongRH, ZhangLM, Zhang JN (2012) Mitochondria in traumatic brain injury and mitochondrial-targeted multipotential therapeutic strategies.Br J Pharmacol167:699–719
CrossRef Google scholar
[22]
ChivetM, Javalet C, LaulagnierK , BlotB, Hemming FJ, SadoulR (2014) Exosomes secreted by cortical neurons upon glutamatergic synapse activation specifically interact with neurons.J Extracell Vesicles3:24722
CrossRef Google scholar
[23]
CocucciE, Racchetti G, MeldolesiJ (2009) Shedding microvesicles: artefacts no more.Trends Cell Biol19:43–51
CrossRef Google scholar
[24]
CorpsKN, RothTL, McGavernDB (2015) Inflammation and neuroprotection in traumatic brain injury.JAMA Neurol72:355–362
CrossRef Google scholar
[25]
CuthbertJP, Harrison-Felix C, CorriganJD , KreiderS, BellJM, CoronadoVG, Whiteneck GG (2015) Epidemiology of adults receiving acute inpatient rehabilitation for a primary diagnosis of traumatic brain injury in the United States.J Head Trauma Rehabil30:122–135
CrossRef Google scholar
[26]
DaleGL, FrieseP (2006) Bax activators potentiate coated-platelet formation.J Thromb Haemost4:2664–2669
CrossRef Google scholar
[27]
DavizonP, MundayAD, LopezJA (2010) Tissue factor, lipid rafts, and microparticles.Semin Thromb Hemost36:857–864
CrossRef Google scholar
[28]
de KroonAI, DolisD, MayerA, Lill R, de KruijffB (1997) Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa.Is cardiolipin present in the mitochondrial outer membrane? Biochem Biophys Acta1325:108–116
CrossRef Google scholar
[29]
Del CondeI, Shrimpton CN, ThiagarajanP , LopezJA (2005) Tissuefactor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation.Blood106:1604–1611
CrossRef Google scholar
[30]
DevauxPF (1992) Protein involvement in transmembrane lipid asymmetry.Annu Rev Biophys Biomol Struct21:417–439
CrossRef Google scholar
[31]
DingW, KouJ, MengH, Kou Y, HeZ , CaoM, WangL, BiY, ThatteHS, ShiJ (2015) Procoagulant activity induced by transcatheter closure of atrial septal defects is associated with exposure of phosphatidylserine on microparticles, platelets and red blood cells.Thromb Res136:354–360
CrossRef Google scholar
[32]
DongJF (2014) Platelet microparticles are not created equal.Blood124:2161–2162
CrossRef Google scholar
[33]
DuanS, NearyJT (2006) P2X(7) receptors: properties and relevance to CNS function. Glia54:738–746
CrossRef Google scholar
[34]
FaureJ, Lachenal G, CourtM , HirrlingerJ, Chatellard-Causse C, BlotB , GrangeJ, Schoehn G, GoldbergY , BoyerV, Kirchhoff F, RaposoG , GarinJ, SadoulR (2006) Exosomes are released by cultured cortical neurones.Mol Cell Neurosci31:642–648
CrossRef Google scholar
[35]
FerrariD, Chiozzi P, FalzoniS , Dal SusinoM, ColloG, BuellG, Di Virgilio F (1997) ATP-mediated cytotoxicity in microglial cells.Neuropharmacology36:1295–1301
CrossRef Google scholar
[36]
FoxJE, AustinCD, BoylesJK, Steffen PK (1990) Role of the membrane skeleton in preventing the shedding of procoagulantrich microvesicles from the platelet plasma membrane.J Cell Biol111:483–493
CrossRef Google scholar
[37]
FoxJE, AustinCD, ReynoldsCC, Steffen PK (1991) Evidence that agonist-induced activation of calpain causes the shedding of procoagulant-containing microvesicles from the membrane of aggregating platelets.J Biol Chem266:13289–13295
[38]
FrostegardJ, Svenungsson E, WuR , GunnarssonI, Lundberg IE, KlareskogL , HorkkoS, Witztum JL (2005) Lipid peroxidation is enhanced in patients with systemic lupus erythematosus and is associated with arterial and renal disease manifestations.Arthritis Rheum52:192–200
CrossRef Google scholar
[39]
GasserO, Schifferli JA (2004) Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis.Blood104:2543–2548
CrossRef Google scholar
[40]
GasserO, HessC, MiotS, Deon C, SanchezJC , SchifferliJA (2003) Characterisation and properties of ectosomes released by human polymorphonuclear neutrophils.Exp Cell Res285:243–257
CrossRef Google scholar
[41]
GhajarJ (2000) Traumatic brain injury.Lancet356:923–929
CrossRef Google scholar
[42]
HarhangiBS, Kompanje EJ, LeebeekFW , MaasAI (2008) Coagulation disorders after traumatic brain injury.Acta Neurochir150:165–175; discussion 175
CrossRef Google scholar
[43]
HarrisonEB, Hochfelder CG, LambertyBG , MeaysBM, MorseyBM, KelsoML, Fox HS, YelamanchiliSV (2016) Traumatic brain injury increases levels of miR-21 in extracellular vesicles: implications for neuroinflammation.FEBS Open Bio6:835–846
CrossRef Google scholar
[44]
HasselmannDO, RapplG, TilgenW, Reinhold U (2001) Extracellular tyrosinase mRNA within apoptotic bodies is protected from degradation in human serum.Clin Chem47:1488–1489
[45]
HayakawaK, Esposito E, WangX , TerasakiY, LiuY, XingC, Ji X, LoEH (2016) Transfer of mitochondria from astrocytes to neurons after stroke.Nature535:551–555
CrossRef Google scholar
[46]
HeJ,GuD, WuX, Reynolds K, DuanX , YaoC, WangJ, ChenCS, Chen J, WildmanRP , KlagMJ, Whelton PK (2005) Major causes of death among men and women in China.N Engl J Med353:1124–1134
CrossRef Google scholar
[47]
HeemskerkJW, VuistWM, FeijgeMA, Reutelingsperger CP, LindhoutT (1997) Collagen but not fibrinogen surfaces induce bleb formation, exposure of phosphatidylserine, and procoagulant activity of adherent platelets: evidence for regulation by protein tyrosine kinase-dependent Ca2+ responses.Blood90:2615–2625
[48]
HessC, Sadallah S, HeftiA , LandmannR, Schifferli JA (1999) Ectosomes released by human neutrophils are specialized functional units.J Immunol163:4564–4573
[49]
HiebertJB, ShenQ, ThimmeschAR , PierceJD (2015) Traumatic brain injury and mitochondrial dysfunction.Am Journal Med Sci350:132–138
CrossRef Google scholar
[50]
HoffmanSW, RoofRL, SteinDG (1996) A reliable and sensitive enzyme immunoassay method for measuring 8-isoprostaglandin F2 alpha: a marker for lipid peroxidation after experimental brain injury.J Neurosci Methods68:133–136
CrossRef Google scholar
[51]
HorstmanLL, JyW, JimenezJJ, Bidot C, AhnYS (2004) New horizons in the analysis of circulating cell-derived microparticles.Keio J Med53:210–230
CrossRef Google scholar
[52]
HoviusR, Lambrechts H, NicolayK , de KruijffB (1021) Improved methods to isolate and subfractionate rat liver mitochondria.Lipid composition of the inner and outer membrane. Biochim Biophys Acta1990:217–226
CrossRef Google scholar
[53]
HugelB, Martinez MC, KunzelmannC , FreyssinetJM (2005) Membrane microparticles: two sides of the coin.Physiology (Bethesda)20:22–27
CrossRef Google scholar
[54]
HulkaF, Mullins RJ, FrankEH (1996) Blunt brain injury activates the coagulation process.Arch Surg131:923–927; discussion 927–928
CrossRef Google scholar
[55]
HuvaereK, Cardoso DR, Homem-de-MelloP , WestermannS, Skibsted LH (2010) Light-induced oxidation of unsaturated lipids as sensitized by flavins.J Phys Chem B114:5583–5593
CrossRef Google scholar
[56]
JacobyRC, OwingsJT, HolmesJ,Battistella FD, GosselinRC , PaglieroniTG (2001) Platelet activation and function after trauma.J Trauma51:639–647
CrossRef Google scholar
[57]
JiJ, KlineAE, AmoscatoA, Samhan-Arias AK, SparveroLJ , TyurinVA, Tyurina YY, FinkB , ManoleMD, PuccioAM, OkonkwoDO, Cheng JP, AlexanderH , ClarkRS, Kochanek PM, WipfP , KaganVE, BayirH (2012) Lipidomics identifies cardiolipin oxidation as a mitochondrial target for redox therapy of brain injury.Nat Neurosci15:1407–1413
CrossRef Google scholar
[58]
JimenezJJ, JyW, MauroLM, Horstman LL, SoderlandC , AhnYS (2003) Endothelial microparticles released in thrombotic thrombocytopenic purpura express von Willebrand factor and markers of endothelial activation.Br J Haematol123:896–902
CrossRef Google scholar
[59]
KaganVE, TyurinVA, JiangJ, Tyurina YY, RitovVB , AmoscatoAA, OsipovAN, BelikovaNA, Kapralov AA, KiniV , VlasovaII, ZhaoQ, ZouM, Di P, SvistunenkoDA , KurnikovIV, Borisenko GG (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors.Nat Chem Biol1:223–232
CrossRef Google scholar
[60]
KasprzakHA, Wozniak A, DrewaG, WozniakB (2001) Enhanced lipid peroxidation processes in patients after brain contusion.J Neurotrauma18:793–797
CrossRef Google scholar
[61]
KaufmanHH, HuiKS, MattsonJC, Borit A, ChildsTL , HootsWK, Bernstein DP, MakelaME , WagnerKA, KahanBD (1984) Clinicopathological correlations of disseminated intravascular coagulation in patients with head injury.Neurosurgery15:34–42
CrossRef Google scholar
[62]
KorytowskiW, BasovaLV, PilatA, Kernstock RM, GirottiAW (2011) Permeabilization of the mitochondrial outer membrane by Bax/ truncated Bid (tBid) proteins as sensitized by cardiolipin hydroperoxide translocation: mechanistic implications for the intrinsic pathway of oxidative apoptosis.J Biol Chem286:26334–26343
CrossRef Google scholar
[63]
KumarA, LoaneDJ (2012) Neuroinflammation after traumatic brain injury: opportunities for therapeutic intervention.Brain Behav Immun26:1191–1201
CrossRef Google scholar
[64]
Kunzelmann-MarcheC, Satta N, TotiF , ZhangY, Nawroth PP, MorrisseyJH , FreyssinetJM (2000) The influence exerted by a restricted phospholipid microenvironment on the expression of tissue factor activity at the cell plasma membrane surface.Thromb Haemost83:282–289
[65]
LachenalG, Pernet-Gallay K, ChivetM , HemmingFJ, BellyA, BodonG, Blot B, HaaseG , GoldbergY, SadoulR (2011) Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity.Mol Cell Neurosci46:409–418
CrossRef Google scholar
[66]
LentzBR (2003) Exposure of platelet membrane phosphatidylserine regulates blood coagulation.Prog Lipid Res42:423–438
CrossRef Google scholar
[67]
LiAE, ItoH, RoviraII, Kim KS, TakedaK , YuZY, Ferrans VJ, FinkelT (1999) A role for reactive oxygen species in endothelial cell anoikis.Circ Res85:304–310
CrossRef Google scholar
[68]
LuD, Mahmood A, GoussevA , QuC, ZhangZG, ChoppM (2004) Delayed thrombosis after traumatic brain injury in rats.J Neurotrauma21:1756–1766
CrossRef Google scholar
[69]
MaaniCV, DeSocio PA,HolcombJB (2009) Coagulopathy in trauma patients: what are the main influence factors?Curr Opin Anaesthesiol22:255–260
CrossRef Google scholar
[70]
MaasAI,Roozenbeek B, ManleyGT (2010) Clinical trials in traumatic brain injury: past experience and current developments.Neurotherapeutics7:115–126
CrossRef Google scholar
[71]
MackM, Kleinschmidt A, BruhlH , KlierC, NelsonPJ, CihakJ, Plachy J, StangassingerM , ErfleV, Schlondorff D (2000) Transfer of the chemokine receptor CCR5 between cells by membranederived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection.Nat Med6:769–775
CrossRef Google scholar
[72]
MacKenzieA, WilsonHL, Kiss-TothE, Dower SK, NorthRA , SurprenantA (2001) Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity15:825–835
CrossRef Google scholar
[73]
MaedaT, Katayama Y, KawamataT , AoyamaN, MoriT (1997)Hemodynamic depression and microthrombosis in the peripheral areas of cortical contusion in the rat: role of platelet activating factor.Acta Neurochir Suppl70:102–105
CrossRef Google scholar
[74]
MakiRA, TyurinVA, LyonRC, Hamilton RL, DeKoskyST , KaganVE, Reynolds WF (2009) Aberrant expression of myeloperoxidase in astrocytes promotes phospholipid oxidation and memory deficits in a mouse model of Alzheimer disease.J BiolChem284:3158–3169
CrossRef Google scholar
[75]
MesriM, Altieri DC (1999) Leukocyte microparticles stimulate endothelial cell cytokine release and tissue factor induction in a JNK1 signaling pathway.J Biol Chem274:23111–23118
CrossRef Google scholar
[76]
MiduraEF, Jernigan PL, KuetheJW , FriendLA, VeileR, MakleyAT, Caldwell CC, GoodmanMD (2015) Microparticles impact coagulation after traumatic brain injury.J Surg Res197:25–31
CrossRef Google scholar
[77]
MirandaKC, BondDT, McKeeM, Skog J, PaunescuTG , Da SilvaN, BrownD, RussoLM (2010) Nucleic acids within urinary exosomes/microvesicles are potential biomarkers for renal disease.Kidney Int78:191–199
CrossRef Google scholar
[78]
MorelN, MorelO, PetitL, Hugel B, CochardJF , FreyssinetJM, SztarkF, DabadieP (2008) Generation of procoagulant microparticles in cerebrospinal fluid and peripheral blood after traumatic brain injury.J Trauma64:698–704
CrossRef Google scholar
[79]
MorelL, ReganM, HigashimoriH , NgSK, EsauC, VidenskyS, Rothstein J, YangY (2013) Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1.J Biol Chem288:7105–7116
CrossRef Google scholar
[80]
MoskovichO, Fishelson Z (2007) Live cell imaging of outward and inward vesiculation induced by the complement c5b-9 complex.J Biol Chem282:29977–29986
CrossRef Google scholar
[81]
MurphyMP (2009) How mitochondria produce reactive oxygen species.Biochem J417:1–13
CrossRef Google scholar
[82]
NagataS, Hanayama R, KawaneK (2010) Autoimmunity and the clearance of dead cells.Cell140:619–630
CrossRef Google scholar
[83]
NautaAJ,TrouwLA, DahaMR, Tijsma O, NieuwlandR , SchwaebleWJ, Gingras AR, MantovaniA , HackEC, RoosA (2002) Direct binding of C1q to apoptotic cells and cell blebs induces complement activation.Eur J Immunol32:1726–1736
CrossRef Google scholar
[84]
NekludovM, Bellander BM, BlombackM , WallenHN (2007) Platelet dysfunction in patients with severe traumatic brain injury.J Neurotrauma24:1699–1706
CrossRef Google scholar
[85]
NekludovM, Mobarrez F, GrythD , BellanderBM, WallenH (2014) Formation of microparticles in the injured brain of patients with severe isolated traumatic brain injury.J Neurotrauma31:1927–1933
CrossRef Google scholar
[86]
NesheimME, MannKG(1983) The kinetics and cofactor dependence of the two cleavages involved in prothrombin activation.J Biol Chem258:5386–5391
[87]
ObermeierB, Daneman R, RansohoffRM (2013) Development, maintenance and disruption of the blood-brain barrier.Nat Med19:1584–1596
CrossRef Google scholar
[88]
OwensAP III, Mackman N (2011) Microparticles in hemostasis and thrombosis.Circ Res108:1284–1297
CrossRef Google scholar
[89]
PanQ, HeC, LiuH, Liao X, DaiB , ChenY, YangY, ZhaoB, Bihl J, MaX (2016) Microvascular endothelial cells-derived microvesicles imply in ischemic stroke by modulating astrocyte and blood brain barrier function and cerebral blood flow.Mol Brain9:63
CrossRef Google scholar
[90]
PatzS, Trattnig C, GrunbacherG , EbnerB, GullyC, NovakA, Rinner B, LeitingerG , AbsengerM, Tomescu OA, ThallingerGG , FaschingU, WissaS, Archelos-GarciaJ , SchaferU (2013) More than cell dust: microparticles isolated from cerebrospinal fluid of brain injured patients are messengers carrying mRNAs, miRNAs, and proteins.J Neurotrauma30:1232–1242
CrossRef Google scholar
[91]
PearlsteinDP, AliMH, MungaiPT, Hynes KL, GewertzBL , SchumackerPT (2002) Role of mitochondrial oxidant generation in endothelial cell responses to hypoxia.Arterioscler Thromb Vasc Biol22:566–573
CrossRef Google scholar
[92]
PetrosilloG, Casanova G, MateraM , RuggieroFM, Paradies G (2006) Interaction of peroxidized cardiolipin with rat-heart mitochondrial membranes: induction of permeability transition and cytochrome c release.FEBS Lett580:6311–6316
CrossRef Google scholar
[93]
PhillisJW, Horrocks LA, FarooquiAA (2006) Cyclooxygenases, lipoxygenases, and epoxygenases in CNS: their role and involvement in neurological disorders.Brain Res Rev52:201–243
CrossRef Google scholar
[94]
PilitsisJG, CoplinWM, O’ReganMH, WellwoodJM, DiazFG, FairfaxMR, Michael DB, PhillisJW (2003) Free fatty acids in cerebrospinal fluids from patients with traumatic brain injury.Neurosci Lett349:136–138
CrossRef Google scholar
[95]
ReichCF III, Pisetsky DS (2009) The content of DNA and RNA in microparticles released by Jurkat and HL-60 cells undergoing in vitro apoptosis.Exp Cell Res315:760–768
CrossRef Google scholar
[96]
RostovtsevaTK, KazemiN, WeinrichM, Bezrukov SM (2006) Voltage gating of VDAC is regulated by nonlamellar lipids of mitochondrial membranes.J Biol Chem281:37496–37506
CrossRef Google scholar
[97]
RozmyslowiczT, MajkaM, KijowskiJ, Murphy SL, ConoverDO , PonczM, Ratajczak J, GaultonGN , RatajczakMZ (2003) Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV.AIDS17:33–42
CrossRef Google scholar
[98]
SaatmanKE, CreedJ, RaghupathiR (2010) Calpain as a therapeutic target in traumatic brain injury.Neurotherapeutics7:31–42
CrossRef Google scholar
[99]
Saenz-CuestaM, IrizarH, Castillo-TrivinoT , Munoz-CullaM, Osorio-Querejeta I, PradaA , SepulvedaL, Lopez-Mato MP, Lopez de MunainA , ComabellaM, VillarLM, OlascoagaJ, Otaegui D (2014) Circulating microparticles reflect treatment effects and clinical status in multiple sclerosis.Biomark Med8:653–661
CrossRef Google scholar
[100]
SchnurigerB, InabaK, AbdelsayedGA , LustenbergerT, EberleBM, BarmparasG, Talving P, DemetriadesD (2010) The impact of platelets on the progression of traumatic intracranial hemorrhage.J Trauma68:881–885
CrossRef Google scholar
[101]
SeifmanMA, Adamides AA, NguyenPN , VallanceSA, CooperDJ, KossmannT, Rosenfeld JV, Morganti-KossmannMC (2008) Endogenous melatonin increases in cerebrospinal fluid of patients after severe traumatic brain injury and correlates with oxidative stress and metabolic disarray.J Cereb Blood Flow Metab28:684–696
CrossRef Google scholar
[102]
ShcherbinaA, Remold-O’Donnell E (1999) Role of caspase in a subset of human platelet activation responses.Blood93:4222–4231
[103]
ShettyAK, MishraV, KodaliM, Hattiangady B (2014) Blood brain barrier dysfunction and delayed neurological deficits in mild traumatic brain injury induced by blast shock waves.Front Cell Neurosci8:232
[104]
ShlosbergD, Benifla M, KauferD , FriedmanA (2010) Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury.Nat Rev Neurol6:393–403
CrossRef Google scholar
[105]
SiljanderP, Farndale RW,FeijgeMA , ComfuriusP, KosS, BeversEM, Heemskerk JW (2001) Platelet adhesion enhances the glycoprotein VI-dependent procoagulant response: involvement of p38 MAP kinase and calpain.Arterioscler Thromb Vasc Biol21:618–627
CrossRef Google scholar
[106]
SparveroLJ, Amoscato AA, KochanekPM , PittBR, KaganVE, BayirH (2010) Mass-spectrometry based oxidative lipidomics and lipid imaging: applications in traumatic brain injury.J Neurochem115:1322–1336
CrossRef Google scholar
[107]
SteinSC, SmithDH (2004) Coagulopathy in traumatic brain injury.Neurocrit Care1:479–488
CrossRef Google scholar
[108]
SteinSC, ChenXH, SinsonGP, Smith DH (2002) Intravascular coagulation: a major secondary insult in nonfatal traumatic brain injury.J Neurosurg97:1373–1377
CrossRef Google scholar
[109]
SteinSC,GrahamDI, ChenXH, Smith DH (2004) Association between intravascular microthrombosis and cerebral ischemia in traumatic brain injury.Neurosurgery54:687–691; discussion 691
CrossRef Google scholar
[110]
StoicaBA, FadenAI(2010) Cell death mechanisms and modulation in traumatic brain injury.Neurotherapeutics7:3–12
CrossRef Google scholar
[111]
SuzukiJ,UmedaM, SimsPJ,Nagata S (2010) Calcium-dependent phospholipid scrambling by TMEM16F.Nature468:834–838
CrossRef Google scholar
[112]
TianY, Salsbery B, WangM , YuanH, YangJ, ZhaoZ, Wu X, ZhangY , KonkleBA, Thiagarajan P, LiM , ZhangJ, DongJF (2015) Brain-derived microparticles induce systemic coagulation in a murine model of traumatic brain injury.Blood125:2151–2159
CrossRef Google scholar
[113]
TschuorC, AsmisLM, LenzlingerPM , TannerM, HarterL, KeelM, Stocker R, StoverJF (2008) In vitro norepinephrine significantly activates isolated platelets from healthy volunteers and critically ill patients following severe traumatic brain injury.Crit Care12: R80
CrossRef Google scholar
[114]
TyurinVA, Tyurina YY, KochanekPM , HamiltonR, DeKosky ST, GreenbergerJS , BayirH, KaganVE (2008) Oxidative lipidomics of programmed cell death.Methods Enzymol442:375–393
CrossRef Google scholar
[115]
van der SandeJJ, Emeis JJ, LindemanJ (1981) Intravascular coagulation: a common phenomenon in minor experimental head injury.J Neurosurg54:21–25
CrossRef Google scholar
[116]
VerderioC, MuzioL, TurolaE, Bergami A, NovellinoL , RuffiniF, Riganti L, CorradiniI, FrancoliniM, Garzetti L, MaiorinoC , ServidaF, Vercelli A, RoccaM, Dalla LiberaD, Martinelli V,ComiG , MartinoG, Matteoli M, FurlanR (2012) Myeloid microvesicles are a marker and therapeutic target for neuroinflammation.Ann Neurol72:610–624
CrossRef Google scholar
[117]
VisavadiyaNP, PatelSP, VanRooyenJL , SullivanPG, Rabchevsky AG (2016) Cellular and subcellular oxidative stress parameters following severe spinal cord injury.Redox Biol8:59–67
CrossRef Google scholar
[118]
WafaisadeA, Wutzler S, LeferingR , TjardesT, Banerjee M, PaffrathT, BouillonB, Maegele M, TraumaRegistry of D.G.U. (2010) Drivers of acute coagulopathy after severe trauma: a multivariate analysis of 1987 patients.Emerg Medicine Journal (EMJ)27:934–939
CrossRef Google scholar
[119]
WarrenBA, ValesO (1972) The release of vesicles from platelets following adhesion to vessel walls in vitro.Br J Exp Pathol53:206–215
[120]
YasuiH, Donahue DL, WalshM , CastellinoFJ,PloplisVA (2016) Early coagulation events induce acute lung injury in a rat model of blunt traumatic brain injury.Am J Physiol Lung Cell Mol Physiol311:L74–L86
CrossRef Google scholar
[121]
ZappulliV, FriisKP, FitzpatrickZ , MaguireCA, Breakefield XO (2016) Extracellular vesicles and intercellular communication within the nervous system.J Clin Invest126:1198–1207
CrossRef Google scholar
[122]
ZetterbergH, SmithDH, BlennowK (2013) Biomarkers of mild traumatic brain injury in cerebrospinal fluid and blood.Nat Rev Neurol9:201–210
CrossRef Google scholar
[123]
ZhangJ,JiangR, LiuL, Watkins T, ZhangF , DongJF (2012) Traumatic brain injury-associated coagulopathy.J Neurotrauma29:2597–2605
CrossRef Google scholar
[124]
ZhaoZ, WangM, TianY, Hilton T, SalsberyB, ZhouEZ, WuX, ThiagarajanP , BoilardE, LiM, ZhangJ, Dong JF (2016) Cardiolipin-mediated procoagulant activity of mitochondria contributes to traumatic brain injury-associated coagulopathy in mice.Blood127:2763–2772
CrossRef Google scholar
[125]
ZwaalRF, Comfurius P, van DeenenLL (1977) Membrane asymmetry and blood coagulation.Nature268:358–360
CrossRef Google scholar

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