Cited by 51Extracellular vesicles in diseaseBarrier Structure and Function StudiesMesenchymal stem cell research

Mesenchymal stem cell derived extracellular vesicles for repairing the neurovascular unit after ischemic stroke

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Davis, Courtney, Savitz, Sean I., Satani, Nikunj·2021·Cells

Abstract

Ischemic stroke is a debilitating disease and one of the leading causes of long-term disability. During the early phase after ischemic stroke, the blood-brain barrier (BBB) exhibits increased permeability and disruption, leading to an influx of immune cells and inflammatory molecules that exacerbate the damage to the brain tissue. Mesenchymal stem cells have been investigated as a promising therapy to improve the recovery after ischemic stroke. The therapeutic effects imparted by MSCs are mostly paracrine. Recently, the role of extracellular vesicles released by these MSCs have been studied as possible carriers of information to the brain. This review focuses on the potential of MSC derived EVs to repair the components of the neurovascular unit (NVU) controlling the BBB, in order to promote overall recovery from stroke. Here, we review the techniques for increasing the effectiveness of MSC-based therapeutics, such as improved homing capabilities, bioengineering protein expression, modified culture conditions, and customizing the contents of EVs. Combining multiple techniques targeting NVU repair may provide the basis for improved future stroke treatment paradigms.

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  • MSCs have emerged as a promising platform for neurovascular repair due to their perivascular origin and paracrine capacity to modulate endothelial, metabolic, and neuronal function.

    “Simultaneously, MSCs have emerged as a promising platform for neurovascular repair due to their perivascular origin and paracrine capacity to modulate endothelial, metabolic, and neuronal function (Davis et al., 2021).”

    From APOE3-Christchurch variant enhances neurovascular support functions of iPSC-derived mesenchymal stromal cells (2026) · cites this paper as Davis et al., 2021

    The Introduction and Section 4 describe MSCs as a promising potential stroke therapy whose effects are believed to arise largely from paracrine signaling. Sections 6.1 and 6.5 discuss effects of MSC-derived vesicles on endothelial cells and neurons. The copy does not establish a perivascular origin for MSCs or show that they modulate metabolic function; Section 6.3 notes similarities between MSCs and pericytes, not a shared origin. Page numbers are unavailable in our copy. (LLM, conf=0.85)

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  1. [1]Virani S.S. Alonso A. Aparicio H.J. Benjamin E.J. Bittencourt M.S. Callaway C.W. Carson A.P. Chamberlain A.M. Cheng S. Delling F.N. Heart Disease and Stroke Statistics-2021 Update: A Report From the American Heart Association Circulation 2021 143 e254 e743 10.1161/CIR.0000000000000950 33501848 PMC13036842 · DOI · Paper page
  2. [2]Prevalence and Most Common Causes of Disability Among Adults—United States, 2005 Morb. Mortal. Wkly. Rep. 2009 58 421 426 19407734
  3. [3]Diseases G.B.D. Injuries C. Global burden of 369 diseases and injuries in 204 countries and territories, 1990-2019: A systematic analysis for the Global Burden of Disease Study 2019 Lancet 2020 396 1204 1222 10.1016/S0140-6736(20)30925-9 33069326 PMC7567026 · DOI · Paper page
  4. [4]Collaborators G.B.D.S. Global, regional, and national burden of stroke, 1990-2016: A systematic analysis for the Global Burden of Disease Study 2016 Lancet Neurol. 2019 18 439 458 10.1016/S1474-4422(19)30034-1 30871944 PMC6494974 · DOI
  5. [5]Kim S.Y. Buckwalter M. Soreq H. Vezzani A. Kaufer D. Blood-brain barrier dysfunction-induced inflammatory signaling in brain pathology and epileptogenesis Epilepsia 2012 53 Suppl. S6 37 44 10.1111/j.1528-1167.2012.03701.x 23134494 PMC3703535 · DOI · Paper page
  6. [6]Sakadzic S. Lee J. Boas D.A. Ayata C. High-resolution in vivo optical imaging of stroke injury and repair Brain Res 2015 1623 174 192 10.1016/j.brainres.2015.04.044 25960347 PMC4569527 · DOI
  7. [7]DiNapoli V.A. Huber J.D. Houser K. Li X. Rosen C.L. Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery following stroke in aged rats Neurobiol. Aging 2008 29 753 764 10.1016/j.neurobiolaging.2006.12.007 17241702 PMC2683361 · DOI
  8. [8]Satani N. Savitz S.I. Is Immunomodulation a Principal Mechanism Underlying How Cell-Based Therapies Enhance Stroke Recovery? Neurotherapeutics 2016 13 775 782 10.1007/s13311-016-0468-9 27485235 PMC5081125 · DOI
  9. [9]Drago D. Cossetti C. Iraci N. Gaude E. Musco G. Bachi A. Pluchino S. The stem cell secretome and its role in brain repair Biochimie 2013 95 2271 2285 10.1016/j.biochi.2013.06.020 23827856 PMC4061727 · DOI
  10. [10]Maumus M. Jorgensen C. Noel D. Mesenchymal stem cells in regenerative medicine applied to rheumatic diseases: Role of secretome and exosomes Biochimie 2013 95 2229 2234 10.1016/j.biochi.2013.04.017 23685070 · DOI
  11. [11]Van Niel G. D’Angelo G. Raposo G. Shedding light on the cell biology of extracellular vesicles Nat. Rev. Mol. Cell Biol. 2018 19 213 228 10.1038/nrm.2017.125 29339798 · DOI · Paper page
  12. [12]Raposo G. Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles, and friends J. Cell Biol. 2013 200 373 383 10.1083/jcb.201211138 23420871 PMC3575529 · DOI · Paper page
  13. [14]Jiang X. Andjelkovic A.V. Zhu L. Yang T. Bennett M.V.L. Chen J. Keep R.F. Shi Y. Blood-brain barrier dysfunction and recovery after ischemic stroke Prog. Neurobiol. 2018 163–164 144 171 10.1016/j.pneurobio.2017.10.001 28987927 PMC5886838 · DOI
  14. [15]Keaney J. Campbell M. The dynamic blood-brain barrier FEBS J. 2015 282 4067 4079 10.1111/febs.13412 26277326 · DOI · Paper page
  15. [16]Xue Q. Liu Y. Qi H. Ma Q. Xu L. Chen W. Chen G. Xu X. A novel brain neurovascular unit model with neurons, astrocytes and microvascular endothelial cells of rat Int. J. Biol. Sci. 2013 9 174 189 10.7150/ijbs.5115 23412420 PMC3572400 · DOI
  16. [17]Canfield S.G. Stebbins M.J. Faubion M.G. Gastfriend B.D. Palecek S.P. Shusta E.V. An isogenic neurovascular unit model comprised of human induced pluripotent stem cell-derived brain microvascular endothelial cells, pericytes, astrocytes, and neurons Fluids Barriers CNS 2019 16 25 10.1186/s12987-019-0145-6 31387594 PMC6685239 · DOI
  17. [18]Underly R.G. Levy M. Hartmann D.A. Grant R.I. Watson A.N. Shih A.Y. Pericytes as Inducers of Rapid, Matrix Metalloproteinase-9-Dependent Capillary Damage during Ischemia J. Neurosci. 2017 37 129 140 10.1523/JNEUROSCI.2891-16.2016 28053036 PMC5214626 · DOI
  18. [19]Chen J. Leak R.K. Yang G.Y. Perspective for stroke and brain injury research: Mechanisms and potential therapeutic targets CNS Neurosci. Ther. 2015 21 301 303 10.1111/cns.12392 25809674 PMC6495936 · DOI
  19. [20]Iadecola C. Anrather J. The immunology of stroke: From mechanisms to translation Nat. Med. 2011 17 796 808 10.1038/nm.2399 21738161 PMC3137275 · DOI · Paper page
  20. [21]Lai T.W. Zhang S. Wang Y.T. Excitotoxicity and stroke: Identifying novel targets for neuroprotection Prog. Neurobiol. 2014 115 157 188 10.1016/j.pneurobio.2013.11.006 24361499 · DOI · Paper page
  21. [22]Anrather J. Iadecola C. Inflammation and Stroke: An Overview Neurotherapeutics 2016 13 661 670 10.1007/s13311-016-0483-x 27730544 PMC5081118 · DOI
  22. [23]Nahirney P.C. Reeson P. Brown C.E. Ultrastructural analysis of blood-brain barrier breakdown in the peri-infarct zone in young adult and aged mice J. Cereb. Blood Flow. Metab. 2016 36 413 425 10.1177/0271678X15608396 26661190 PMC4759675 · DOI
  23. [24]Krueger M. Hartig W. Reichenbach A. Bechmann I. Michalski D. Blood-brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions PLoS ONE 2013 8 e56419 10.1371/journal.pone.0056419 23468865 PMC3582567 · DOI
  24. [25]Willis C.L. Meske D.S. Davis T.P. Protein kinase C activation modulates reversible increase in cortical blood-brain barrier permeability and tight junction protein expression during hypoxia and posthypoxic reoxygenation J. Cereb. Blood Flow Metab. 2010 30 1847 1859 10.1038/jcbfm.2010.119 20700133 PMC3023932 · DOI
  25. [26]Rochfort K.D. Cummins P.M. Cytokine-mediated dysregulation of zonula occludens-1 properties in human brain microvascular endothelium Microvasc. Res. 2015 100 48 53 10.1016/j.mvr.2015.04.010 25953589 · DOI
  26. [27]Andjelkovic A.V. Xiang J. Stamatovic S.M. Hua Y. Xi G. Wang M.M. Keep R.F. Endothelial Targets in Stroke: Translating Animal Models to Human Arterioscler. Thromb. Vasc. Biol. 2019 39 2240 2247 10.1161/ATVBAHA.119.312816 31510792 PMC6812626 · DOI
  27. [28]Knowland D. Arac A. Sekiguchi K.J. Hsu M. Lutz S.E. Perrino J. Steinberg G.K. Barres B.A. Nimmerjahn A. Agalliu D. Stepwise recruitment of transcellular and paracellular pathways underlies blood-brain barrier breakdown in stroke Neuron 2014 82 603 617 10.1016/j.neuron.2014.03.003 24746419 PMC4016169 · DOI · Paper page
  28. [29]Armulik A. Genove G. Mae M. Nisancioglu M.H. Wallgard E. Niaudet C. He L. Norlin J. Lindblom P. Strittmatter K. Pericytes regulate the blood-brain barrier Nature 2010 468 557 561 10.1038/nature09522 20944627 · DOI · Paper page
  29. [30]Simpkins A.N. Dias C. Leigh R. National Institutes of Health Natural History of Stroke Investigators Identification of Reversible Disruption of the Human Blood-Brain Barrier Following Acute Ischemia Stroke 2016 47 2405 2408 10.1161/STROKEAHA.116.013805 27462115 PMC5111547 · DOI
  30. [31]Wang C.X. Shuaib A. Critical role of microvasculature basal lamina in ischemic brain injury Prog. Neurobiol. 2007 83 140 148 10.1016/j.pneurobio.2007.07.006 17868971 · DOI
  31. [32]Rosell A. Foerch C. Murata Y. Lo E.H. Mechanisms and markers for hemorrhagic transformation after stroke Acta Neurochir. Suppl. 2008 105 173 178 10.1007/978-3-211-09469-3_34 19066105 · DOI
  32. [33]Pfefferkorn T. Rosenberg G.A. Closure of the blood-brain barrier by matrix metalloproteinase inhibition reduces rtPA-mediated mortality in cerebral ischemia with delayed reperfusion Stroke 2003 34 2025 2030 10.1161/01.STR.0000083051.93319.28 12855824 · DOI
  33. [34]De Meyer S.F. Denorme F. Langhauser F. Geuss E. Fluri F. Kleinschnitz C. Thromboinflammation in Stroke Brain Damage Stroke 2016 47 1165 1172 10.1161/STROKEAHA.115.011238 26786115 · DOI
  34. [35]Eltzschig H.K. Collard C.D. Vascular ischaemia and reperfusion injury Br. Med. Bull. 2004 70 71 86 10.1093/bmb/ldh025 15494470 · DOI
  35. [36]Wang Z. Wang Y. Ye J. Lu X. Cheng Y. Xiang L. Chen L. Feng W. Shi H. Yu X. bFGF attenuates endoplasmic reticulum stress and mitochondrial injury on myocardial ischaemia/reperfusion via activation of PI3K/Akt/ERK1/2 pathway J. Cell Mol. Med. 2015 19 595 607 10.1111/jcmm.12346 25533999 PMC4369816 · DOI
  36. [37]Yu H.C. Qin H.Y. He F. Wang L. Fu W. Liu D. Guo F.C. Liang L. Dou K.F. Han H. Canonical notch pathway protects hepatocytes from ischemia/reperfusion injury in mice by repressing reactive oxygen species production through JAK2/STAT3 signaling Hepatology 2011 54 979 988 10.1002/hep.24469 21633967 · DOI
  37. [38]Yang G.Y. Betz A.L. Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats Stroke 1994 25 1658 1664 10.1161/01.STR.25.8.1658 8042219 · DOI
  38. [39]Yin K.J. Hamblin M. Chen Y.E. Angiogenesis-regulating microRNAs and Ischemic Stroke Curr. Vasc. Pharmacol. 2015 13 352 365 10.2174/15701611113119990016 26156265 PMC4079753 · DOI
  39. [40]Ames A. 3rd Wright R.L. Kowada M. Thurston J.M. Majno G. Cerebral ischemia. II. The no-reflow phenomenon Am. J. Pathol. 1968 52 437 453 5635861 PMC2013326
  40. [41]Reffelmann T. Hale S.L. Dow J.S. Kloner R.A. No-reflow phenomenon persists long-term after ischemia/reperfusion in the rat and predicts infarct expansion Circulation 2003 108 2911 2917 10.1161/01.CIR.0000101917.80668.E1 14656914 · DOI
  41. [42]Ito U. Hakamata Y. Kawakami E. Oyanagi K. Temporary [corrected] cerebral ischemia results in swollen astrocytic end-feet that compress microvessels and lead to delayed [corrected] focal cortical infarction J. Cereb. Blood Flow Metab. 2011 31 328 338 10.1038/jcbfm.2010.97 20588315 PMC3049496 · DOI
  42. [43]Ito U. Hakamata Y. Watabe K. Oyanagi K. Astrocytic involvement in the maturation phenomenon after temporary cerebral ischemia Acta Neurochir. Suppl. 2013 118 23 29 10.1007/978-3-7091-1434-6_4 23564099 · DOI
  43. [44]Leigh R. Jen S.S. Hillis A.E. Krakauer J.W. Barker P.B. Albers G.W. Davis S.M. Donnan G.A. Fisher M. Furlan A.J. Pretreatment blood-brain barrier damage and post-treatment intracranial hemorrhage in patients receiving intravenous tissue-type plasminogen activator Stroke 2014 45 2030 2035 10.1161/STROKEAHA.114.005249 24876245 PMC4120660 · DOI
  44. [45]Nadareishvili Z. Simpkins A.N. Hitomi E. Reyes D. Leigh R. Post-Stroke Blood-Brain Barrier Disruption and Poor Functional Outcome in Patients Receiving Thrombolytic Therapy Cerebrovasc. Dis. 2019 47 135 142 10.1159/000499666 30970357 PMC6610790 · DOI
  45. [46]Wei X. Yang X. Han Z.P. Qu F.F. Shao L. Shi Y.F. Mesenchymal stem cells: A new trend for cell therapy Acta Pharmacol. Sin. 2013 34 747 754 10.1038/aps.2013.50 23736003 PMC4002895 · DOI
  46. [47]Kehl D. Generali M. Mallone A. Heller M. Uldry A.C. Cheng P. Gantenbein B. Hoerstrup S.P. Weber B. Proteomic analysis of human mesenchymal stromal cell secretomes: A systematic comparison of the angiogenic potential NPJ Regen. Med. 2019 4 8 10.1038/s41536-019-0070-y 31016031 PMC6467904 · DOI
  47. [48]Colombo M. Raposo G. Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles Annu. Rev. Cell Dev. Biol. 2014 30 255 289 10.1146/annurev-cellbio-101512-122326 25288114 · DOI · Paper page
  48. [49]Veziroglu E.M. Mias G.I. Characterizing Extracellular Vesicles and Their Diverse RNA Contents Front. Genet. 2020 11 700 10.3389/fgene.2020.00700 32765582 PMC7379748 · DOI
  49. [50]Zaborowski M.P. Balaj L. Breakefield X.O. Lai C.P. Extracellular Vesicles: Composition, Biological Relevance, and Methods of Study Bioscience 2015 65 783 797 10.1093/biosci/biv084 26955082 PMC4776721 · DOI
  50. [51]Hristov M. Erl W. Linder S. Weber P.C. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro Blood 2004 104 2761 2766 10.1182/blood-2003-10-3614 15242875 · DOI
  51. [52]Heijnen H.F.G. Schiel A.E. Fijnheer R. Geuze H.J. Sixma J.J. Activated Platelets Release Two Types of Membrane Vesicles: Microvesicles by Surface Shedding and Exosomes Derived From Exocytosis of Multivesicular Bodies and α-Granules Blood 1999 94 3791 3799 10.1182/blood.V94.11.3791 10572093 · DOI
  52. [53]Purvinsh L. Gorshkov A. Brodskaia A. Vasin A. Extracellular Vesicles in Viral Pathogenesis: A Case of Dr. Jekyll and Mr. Hyde Life 2021 11 45 10.3390/life11010045 33450847 PMC7828316 · DOI
  53. [54]Haraszti R.A. Didiot M.C. Sapp E. Leszyk J. Shaffer S.A. Rockwell H.E. Gao F. Narain N.R. DiFiglia M. Kiebish M.A. High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources J. Extracell Vesicles 2016 5 32570 10.3402/jev.v5.32570 27863537 PMC5116062 · DOI · Paper page
  54. [55]Witwer K.W. Van Balkom B.W.M. Bruno S. Choo A. Dominici M. Gimona M. Hill A.F. De Kleijn D. Koh M. Lai R.C. Defining mesenchymal stromal cell (MSC)-derived small extracellular vesicles for therapeutic applications J. Extracell Vesicles 2019 8 1609206 10.1080/20013078.2019.1609206 31069028 PMC6493293 · DOI
  55. [56]Minciacchi V.R. You S. Spinelli C. Morley S. Zandian M. Aspuria P.J. Cavallini L. Ciardiello C. Reis Sobreiro M. Morello M. Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles Oncotarget 2015 6 11327 11341 10.18632/oncotarget.3598 25857301 PMC4484459 · DOI
  56. [57]Hatakeyama M. Ninomiya I. Kanazawa M. Angiogenesis and neuronal remodeling after ischemic stroke Neural. Regen. Res. 2020 15 16 19 10.4103/1673-5374.264442 31535636 PMC6862417 · DOI
  57. [58]Teng H. Zhang Z.G. Wang L. Zhang R.L. Zhang L. Morris D. Gregg S.R. Wu Z. Jiang A. Lu M. Coupling of angiogenesis and neurogenesis in cultured endothelial cells and neural progenitor cells after stroke J. Cereb. Blood Flow Metab. 2008 28 764 771 10.1038/sj.jcbfm.9600573 17971789 PMC2744583 · DOI · Paper page
  58. [59]Szpak G.M. Lechowicz W. Lewandowska E. Bertrand E. Wierzba-Bobrowicz T. Dymecki J. Border zone neovascularization in cerebral ischemic infarct Folia Neuropathol. 1999 37 264 268 10705649
  59. [60]Krupinski J. Kaluza J. Kumar P. Kumar S. Wang J.M. Role of angiogenesis in patients with cerebral ischemic stroke Stroke 1994 25 1794 1798 10.1161/01.STR.25.9.1794 7521076 · DOI
  60. [61]Ding R. Hase Y. Ameen-Ali K.E. Ndung’u M. Stevenson W. Barsby J. Gourlay R. Akinyemi T. Akinyemi R. Uemura M.T. Loss of capillary pericytes and the blood-brain barrier in white matter in poststroke and vascular dementias and Alzheimer’s disease Brain Pathol. 2020 30 1087 1101 10.1111/bpa.12888 32705757 PMC8018063 · DOI
  61. [62]Schmidt R. Schmidt H. Fazekas F. Vascular risk factors in dementia J. Neurol. 2000 247 81 87 10.1007/s004150050021 10751108 · DOI
  62. [63]Doeppner T.R. Herz J. Gorgens A. Schlechter J. Ludwig A.K. Radtke S. de Miroschedji K. Horn P.A. Giebel B. Hermann D.M. Extracellular Vesicles Improve Post-Stroke Neuroregeneration and Prevent Postischemic Immunosuppression Stem Cells Transl. Med. 2015 4 1131 1143 10.5966/sctm.2015-0078 26339036 PMC4572905 · DOI
  63. [64]Xin H. Li Y. Cui Y. Yang J.J. Zhang Z.G. Chopp M. Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats J. Cereb. Blood Flow Metab. 2013 33 1711 1715 10.1038/jcbfm.2013.152 23963371 PMC3824189 · DOI
  64. [65]Zhang Y. Zhang Y. Chopp M. Zhang Z.G. Mahmood A. Xiong Y. Mesenchymal Stem Cell-Derived Exosomes Improve Functional Recovery in Rats After Traumatic Brain Injury: A Dose-Response and Therapeutic Window Study Neurorehabilit. Neural. Repair. 2020 34 616 626 10.1177/1545968320926164 PMC7329589 32462980 · DOI
  65. [66]Kaminski N. Koster C. Mouloud Y. Borger V. Felderhoff-Muser U. Bendix I. Giebel B. Herz J. Mesenchymal Stromal Cell-Derived Extracellular Vesicles Reduce Neuroinflammation, Promote Neural Cell Proliferation and Improve Oligodendrocyte Maturation in Neonatal Hypoxic-Ischemic Brain Injury Front. Cell Neurosci. 2020 14 601176 10.3389/fncel.2020.601176 33362471 PMC7758466 · DOI
  66. [67]Doeppner T.R. Bahr M. Giebel B. Hermann D.M. Immunological and non-immunological effects of stem cell-derived extracellular vesicles on the ischaemic brain Ther. Adv. Neurol. Disord. 2018 11 1756286418789326 10.1177/1756286418789326 30083231 PMC6071165 · DOI
  67. [68]Xin H. Li Y. Liu Z. Wang X. Shang X. Cui Y. Zhang Z.G. Chopp M. MiR-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles Stem Cells 2013 31 2737 2746 10.1002/stem.1409 23630198 PMC3788061 · DOI
  68. [69]Zhang Y. Chopp M. Meng Y. Katakowski M. Xin H. Mahmood A. Xiong Y. Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury J. Neurosurg. 2015 122 856 867 10.3171/2014.11.JNS14770 25594326 PMC4382456 · DOI · Paper page
  69. [70]Rahmani A. Saleki K. Javanmehr N. Khodaparast J. Saadat P. Nouri H.R. Mesenchymal stem cell-derived extracellular vesicle-based therapies protect against coupled degeneration of the central nervous and vascular systems in stroke Ageing Res. Rev. 2020 62 101106 10.1016/j.arr.2020.101106 32565329 · DOI
  70. [71]Romanov Y.A. Volgina N.E. Vtorushina V.V. Romanov A.Y. Dugina T.N. Kabaeva N.V. Sukhikh G.T. Comparative Analysis of Secretome of Human Umbilical Cord- and Bone Marrow-Derived Multipotent Mesenchymal Stromal Cells Bull. Exp. Biol. Med. 2019 166 535 540 10.1007/s10517-019-04388-1 30793233 · DOI
  71. [72]Baberg F. Geyh S. Waldera-Lupa D. Stefanski A. Zilkens C. Haas R. Schroeder T. Stuhler K. Secretome analysis of human bone marrow derived mesenchymal stromal cells Biochim. Biophys. Acta 2019 1867 434 441 10.1016/j.bbapap.2019.01.013 30716505 · DOI
  72. [73]Fatima F. Ekstrom K. Nazarenko I. Maugeri M. Valadi H. Hill A.F. Camussi G. Nawaz M. Non-coding RNAs in Mesenchymal Stem Cell-Derived Extracellular Vesicles: Deciphering Regulatory Roles in Stem Cell Potency, Inflammatory Resolve, and Tissue Regeneration Front. Genet. 2017 8 161 10.3389/fgene.2017.00161 29123544 PMC5662888 · DOI
  73. [74]Maffioli E. Nonnis S. Angioni R. Santagata F. Cali B. Zanotti L. Negri A. Viola A. Tedeschi G. Proteomic analysis of the secretome of human bone marrow-derived mesenchymal stem cells primed by pro-inflammatory cytokines J. Proteom. 2017 166 115 126 10.1016/j.jprot.2017.07.012 28739509 · DOI
  74. [75]Yilmaz G. Alexander J.S. Erkuran Yilmaz C. Granger D.N. Induction of neuro-protective/regenerative genes in stem cells infiltrating post-ischemic brain tissue Exp. Transl. Stroke Med. 2010 2 11 10.1186/2040-7378-2-11 20509949 PMC2893124 · DOI
  75. [76]Qu R. Li Y. Gao Q. Shen L. Zhang J. Liu Z. Chen X. Chopp M. Neurotrophic and growth factor gene expression profiling of mouse bone marrow stromal cells induced by ischemic brain extracts Neuropathology 2007 27 355 363 10.1111/j.1440-1789.2007.00792.x 17899689 PMC2593420 · DOI
  76. [77]Zacharek A. Shehadah A. Chen J. Cui X. Roberts C. Lu M. Chopp M. Comparison of bone marrow stromal cells derived from stroke and normal rats for stroke treatment Stroke 2010 41 524 530 10.1161/STROKEAHA.109.568881 20056925 PMC2847444 · DOI
  77. [78]Eirin A. Zhu X.Y. Jonnada S. Lerman A. van Wijnen A.J. Lerman L.O. Mesenchymal Stem Cell-Derived Extracellular Vesicles Improve the Renal Microvasculature in Metabolic Renovascular Disease in Swine Cell Transplant. 2018 27 1080 1095 10.1177/0963689718780942 29954220 PMC6158551 · DOI
  78. [79]Guo H. Ingolia N.T. Weissman J.S. Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels Nature 2010 466 835 840 10.1038/nature09267 20703300 PMC2990499 · DOI · Paper page
  79. [80]Qiu G. Zheng G. Ge M. Wang J. Huang R. Shu Q. Xu J. Mesenchymal stem cell-derived extracellular vesicles affect disease outcomes via transfer of microRNAs Stem Cell Res. Ther. 2018 9 320 10.1186/s13287-018-1069-9 30463593 PMC6249826 · DOI
  80. [81]Gatti S. Bruno S. Deregibus M.C. Sordi A. Cantaluppi V. Tetta C. Camussi G. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury Nephrol. Dial. Transplant. 2011 26 1474 1483 10.1093/ndt/gfr015 21324974 · DOI
  81. [82]Muraca M. Cappariello A. The Role of Extracellular Vesicles (EVs) in the Epigenetic Regulation of Bone Metabolism and Osteoporosis Int. J. Mol. Sci. 2020 21 8682 10.3390/ijms21228682 33213099 PMC7698531 · DOI
  82. [83]Born L.J. Harmon J.W. Jay S.M. Therapeutic potential of extracellular vesicle-associated long noncoding RNA Bioeng. Transl. Med. 2020 5 e10172 10.1002/btm2.10172 33005738 PMC7510462 · DOI
  83. [84]Nolte-’t Hoen E.N. Buermans H.P. Waasdorp M. Stoorvogel W. Wauben M.H. t Hoen P.A. Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions Nucleic Acids Res. 2012 40 9272 9285 10.1093/nar/gks658 22821563 PMC3467056 · DOI
  84. [85]Kim K.M. Abdelmohsen K. Mustapic M. Kapogiannis D. Gorospe M. RNA in extracellular vesicles Wiley Interdiscip. Rev. RNA 2017 8 e1413 10.1002/wrna.1413 28130830 PMC5474163 · DOI
  85. [86]Melki I. Tessandier N. Zufferey A. Boilard E. Platelet microvesicles in health and disease Platelets 2017 28 214 221 10.1080/09537104.2016.1265924 28102737 · DOI
  86. [87]Abels E.R. Breakefield X.O. Introduction to Extracellular Vesicles: Biogenesis, RNA Cargo Selection, Content, Release, and Uptake Cell. Mol. Neurobiol. 2016 36 301 312 10.1007/s10571-016-0366-z 27053351 PMC5546313 · DOI
  87. [88]Kalra H. Drummen G.P. Mathivanan S. Focus on Extracellular Vesicles: Introducing the Next Small Big Thing Int. J. Mol. Sci. 2016 17 170 10.3390/ijms17020170 26861301 PMC4783904 · DOI
  88. [89]Spees J.L. Olson S.D. Whitney M.J. Prockop D.J. Mitochondrial transfer between cells can rescue aerobic respiration Proc. Nat. Acad. Sci. USA 2006 103 1283 1288 10.1073/pnas.0510511103 16432190 PMC1345715 · DOI
  89. [90]Lin H.Y. Liou C.W. Chen S.D. Hsu T.Y. Chuang J.H. Wang P.W. Huang S.T. Tiao M.M. Chen J.B. Lin T.K. Mitochondrial transfer from Wharton’s jelly-derived mesenchymal stem cells to mitochondria-defective cells recaptures impaired mitochondrial function Mitochondrion 2015 22 31 44 10.1016/j.mito.2015.02.006 25746175 · DOI
  90. [91]Liu K. Ji K. Guo L. Wu W. Lu H. Shan P. Yan C. Mesenchymal stem cells rescue injured endothelial cells in an in vitro ischemia-reperfusion model via tunneling nanotube like structure-mediated mitochondrial transfer Microvasc. Res. 2014 92 10 18 10.1016/j.mvr.2014.01.008 24486322 · DOI
  91. [92]Hayakawa K. Chan S.J. Mandeville E.T. Park J.H. Bruzzese M. Montaner J. Arai K. Rosell A. Lo E.H. Protective Effects of Endothelial Progenitor Cell-Derived Extracellular Mitochondria in Brain Endothelium Stem Cells 2018 36 1404 1410 10.1002/stem.2856 29781122 PMC6407639 · DOI
  92. [93]He Z. Ning N. Zhou Q. Khoshnam S.E. Farzaneh M. Mitochondria as a therapeutic target for ischemic stroke Free Radic. Biol. Med. 2020 146 45 58 10.1016/j.freeradbiomed.2019.11.005 31704373 · DOI
  93. [94]Fuhrmann D.C. Brune B. Mitochondrial composition and function under the control of hypoxia Redox Biol. 2017 12 208 215 10.1016/j.redox.2017.02.012 28259101 PMC5333533 · DOI
  94. [95]Sousa Fialho M.D.L. Abd Jamil A.H. Stannard G.A. Heather L.C. Hypoxia-inducible factor 1 signalling, metabolism and its therapeutic potential in cardiovascular disease Biochim. Biophys. Acta Mol. Basis Dis. 2019 1865 831 843 10.1016/j.bbadis.2018.09.024 30266651 · DOI
  95. [96]Fan P. Yu X.Y. Xie X.H. Chen C.H. Zhang P. Yang C. Peng X. Wang Y.T. Mitophagy is a protective response against oxidative damage in bone marrow mesenchymal stem cells Life Sci. 2019 229 36 45 10.1016/j.lfs.2019.05.027 31085242 · DOI
  96. [97]Huang J.L. Manaenko A. Ye Z.H. Sun X.J. Hu Q. Hypoxia therapy--a new hope for the treatment of mitochondrial dysfunctions Med. Gas. Res. 2016 6 174 176 10.4103/2045-9912.191365 27867487 PMC5110142 · DOI
  97. [98]Borlongan C.V. Nguyen H. Lippert T. Russo E. Tuazon J. Xu K. Lee J.Y. Sanberg P.R. Kaneko Y. Napoli E. May the force be with you: Transfer of healthy mitochondria from stem cells to stroke cells J. Cereb. Blood Flow Metab. 2019 39 367 370 10.1177/0271678X18811277 30375940 PMC6365599 · DOI
  98. [99]Boilard E. Extracellular vesicles and their content in bioactive lipid mediators: More than a sack of microRNA J. Lipid Res. 2018 59 2037 2046 10.1194/jlr.R084640 29678959 PMC6210911 · DOI
  99. [100]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 108 120 10.1016/j.bbalip.2013.10.004 24140720 · DOI
  100. [101]Pathan M. Fonseka P. Chitti S.V. Kang T. Sanwlani R. Van Deun J. Hendrix A. Mathivanan S. Vesiclepedia 2019: A compendium of RNA, proteins, lipids and metabolites in extracellular vesicles Nucleic Acids Res. 2019 47 D516 D519 10.1093/nar/gky1029 30395310 PMC6323905 · DOI
  101. [102]Keerthikumar S. Chisanga D. Ariyaratne D. Al Saffar H. Anand S. Zhao K. Samuel M. Pathan M. Jois M. Chilamkurti N. ExoCarta: A Web-Based Compendium of Exosomal Cargo J. Mol. Biol. 2016 428 688 692 10.1016/j.jmb.2015.09.019 26434508 PMC4783248 · DOI
  102. [104]Chen F. Ohashi N. Li W. Eckman C. Nguyen J.H. Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure Hepatology 2009 50 1914 1923 10.1002/hep.23203 19821483 PMC2925168 · DOI
  103. [105]Cheng Z. Wang L. Qu M. Liang H. Li W. Li Y. Deng L. Zhang Z. Yang G.Y. Mesenchymal stem cells attenuate blood-brain barrier leakage after cerebral ischemia in mice J. Neuroinflamm. 2018 15 135 10.1186/s12974-018-1153-1 29724240 PMC5932816 · DOI
  104. [106]Wang N. Chen C. Yang D. Liao Q. Luo H. Wang X. Zhou F. Yang X. Yang J. Zeng C. Mesenchymal stem cells-derived extracellular vesicles, via miR-210, improve infarcted cardiac function by promotion of angiogenesis Biochim. Biophys. Acta Mol. Basis Dis. 2017 1863 2085 2092 10.1016/j.bbadis.2017.02.023 28249798 · DOI
  105. [107]Lou Y.L. Guo F. Liu F. Gao F.L. Zhang P.Q. Niu X. Guo S.C. Yin J.H. Wang Y. Deng Z.F. miR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia Mol. Cell Biochem. 2012 370 45 51 10.1007/s11010-012-1396-6 22833359 · DOI
  106. [109]Fujioka T. Kaneko N. Sawamoto K. Blood vessels as a scaffold for neuronal migration Neurochem. Int. 2019 126 69 73 10.1016/j.neuint.2019.03.001 30851365 · DOI
  107. [110]Eichmann A. Thomas J.L. Molecular parallels between neural and vascular development Cold Spring Harb. Perspect. Med. 2013 3 a006551 10.1101/cshperspect.a006551 23024177 PMC3530036 · DOI · Paper page
  108. [111]Freitas-Andrade M. Raman-Nair J. Lacoste B. Structural and Functional Remodeling of the Brain Vasculature Following Stroke Front. Physiol. 2020 11 948 10.3389/fphys.2020.00948 32848875 PMC7433746 · DOI
  109. [112]Todorova D. Simoncini S. Lacroix R. Sabatier F. Dignat-George F. Extracellular Vesicles in Angiogenesis Circ. Res. 2017 120 1658 1673 10.1161/CIRCRESAHA.117.309681 28495996 PMC5426696 · DOI
  110. [113]Anderson J.D. Johansson H.J. Graham C.S. Vesterlund M. Pham M.T. Bramlett C.S. Montgomery E.N. Mellema M.S. Bardini R.L. Contreras Z. Comprehensive Proteomic Analysis of Mesenchymal Stem Cell Exosomes Reveals Modulation of Angiogenesis via Nuclear Factor-KappaB Signaling Stem Cells 2016 34 601 613 10.1002/stem.2298 26782178 PMC5785927 · DOI
  111. [114]Yang Y. Cai Y. Zhang Y. Liu J. Xu Z. Exosomes Secreted by Adipose-Derived Stem Cells Contribute to Angiogenesis of Brain Microvascular Endothelial Cells Following Oxygen-Glucose Deprivation In Vitro Through MicroRNA-181b/TRPM7 Axis J. Mol. Neurosci. 2018 65 74 83 10.1007/s12031-018-1071-9 29705934 · DOI
  112. [115]Zeng Z. Inoue K. Sun H. Leng T. Feng X. Zhu L. Xiong Z.G. TRPM7 regulates vascular endothelial cell adhesion and tube formation Am. J. Physiol. Cell Physiol. 2015 308 C308 C318 10.1152/ajpcell.00275.2013 25472964 PMC4329423 · DOI
  113. [117]Liddelow S.A. Barres B.A. Reactive Astrocytes: Production, Function, and Therapeutic Potential Immunity 2017 46 957 967 10.1016/j.immuni.2017.06.006 28636962 · DOI · Paper page
  114. [118]Jensen C.J. Massie A. De Keyser J. Immune players in the CNS: The astrocyte J. Neuroimmune Pharmacol. 2013 8 824 839 10.1007/s11481-013-9480-6 23821340 · DOI
  115. [119]Zamanian J.L. Xu L. Foo L.C. Nouri N. Zhou L. Giffard R.G. Barres B.A. Genomic analysis of reactive astrogliosis J. Neurosci. 2012 32 6391 6410 10.1523/JNEUROSCI.6221-11.2012 22553043 PMC3480225 · DOI · Paper page
  116. [120]Hira K. Ueno Y. Tanaka R. Miyamoto N. Yamashiro K. Inaba T. Urabe T. Okano H. Hattori N. Astrocyte-Derived Exosomes Treated With a Semaphorin 3A Inhibitor Enhance Stroke Recovery via Prostaglandin D2 Synthase Stroke 2018 49 2483 2494 10.1161/STROKEAHA.118.021272 30355116 · DOI
  117. [122]Hayakawa K. Pham L.D. Katusic Z.S. Arai K. Lo E.H. Astrocytic high-mobility group box 1 promotes endothelial progenitor cell-mediated neurovascular remodeling during stroke recovery Proc. Natl. Acad. Sci. USA 2012 109 7505 7510 10.1073/pnas.1121146109 22529378 PMC3358881 · DOI
  118. [123]Hayakawa K. Esposito E. Wang X. Terasaki Y. Liu Y. Xing C. Ji X. Lo E.H. Transfer of mitochondria from astrocytes to neurons after stroke Nature 2016 535 551 555 10.1038/nature18928 27466127 PMC4968589 · DOI · Paper page
  119. [124]Chen S.H. Oyarzabal E.A. Sung Y.F. Chu C.H. Wang Q. Chen S.L. Lu R.B. Hong J.S. Microglial regulation of immunological and neuroprotective functions of astroglia Glia 2015 63 118 131 10.1002/glia.22738 25130274 PMC4237670 · DOI
  120. [125]Zhang D. Hu X. Qian L. O’Callaghan J.P. Hong J.S. Astrogliosis in CNS pathologies: Is there a role for microglia? Mol. Neurobiol. 2010 41 232 241 10.1007/s12035-010-8098-4 20148316 PMC3629545 · DOI
  121. [126]Drago F. Lombardi M. Prada I. Gabrielli M. Joshi P. Cojoc D. Franck J. Fournier I. Vizioli J. Verderio C. ATP Modifies the Proteome of Extracellular Vesicles Released by Microglia and Influences Their Action on Astrocytes Front. Pharmacol. 2017 8 910 10.3389/fphar.2017.00910 29321741 PMC5733563 · DOI
  122. [127]Kim E. Otgontenger U. Jamsranjav A. Kim S.S. Deleterious Alteration of Glia in the Brain of Alzheimer’s Disease Int. J. Mol. Sci. 2020 21 6676 10.3390/ijms21186676 PMC7555758 32932623 · DOI
  123. [128]Li T. Liu T. Chen X. Li L. Feng M. Zhang Y. Wan L. Zhang C. Yao W. Microglia induce the transformation of A1/A2 reactive astrocytes via the CXCR7/PI3K/Akt pathway in chronic post-surgical pain J. Neuroinflamm. 2020 17 211 10.1186/s12974-020-01891-5 32665021 PMC7362409 · DOI
  124. [129]Jha M.K. Jo M. Kim J.H. Suk K. Microglia-Astrocyte Crosstalk: An Intimate Molecular Conversation Neuroscientist 2019 25 227 240 10.1177/1073858418783959 29931997 · DOI · Paper page
  125. [130]He M. Dong H. Huang Y. Lu S. Zhang S. Qian Y. Jin W. Astrocyte-Derived CCL2 is Associated with M1 Activation and Recruitment of Cultured Microglial Cells Cell Physiol. Biochem. 2016 38 859 870 10.1159/000443040 26910882 · DOI
  126. [131]Xie C. Gao X. Luo Y. Pang Y. Li M. Electroacupuncture modulates stromal cell-derived factor-1alpha expression and mobilization of bone marrow endothelial progenitor cells in focal cerebral ischemia/reperfusion model rats Brain Res. 2016 1648 119 126 10.1016/j.brainres.2016.07.038 27453543 · DOI
  127. [132]Xin H. Wang F. Li Y. Lu Q.E. Cheung W.L. Zhang Y. Zhang Z.G. Chopp M. Secondary Release of Exosomes From Astrocytes Contributes to the Increase in Neural Plasticity and Improvement of Functional Recovery After Stroke in Rats Treated With Exosomes Harvested From MicroRNA 133b-Overexpressing Multipotent Mesenchymal Stromal Cells Cell Transplant. 2017 26 243 257 10.3727/096368916×693031 27677799 PMC5303172 · DOI
  128. [134]Mills S.J. Cowin A.J. Kaur P. Pericytes, mesenchymal stem cells and the wound healing process Cells 2013 2 621 634 10.3390/cells2030621 24709801 PMC3972668 · DOI
  129. [135]Tian X. Brookes O. Battaglia G. Pericytes from Mesenchymal Stem Cells as a model for the blood-brain barrier Sci. Rep. 2017 7 39676 10.1038/srep39676 28098158 PMC5241806 · DOI · Paper page
  130. [136]De Souza L.E. Malta T.M. Kashima Haddad S. Covas D.T. Mesenchymal Stem Cells and Pericytes: To What Extent Are They Related? Stem Cells Dev. 2016 25 1843 1852 10.1089/scd.2016.0109 27702398 · DOI
  131. [137]Helms H.C. Abbott N.J. Burek M. Cecchelli R. Couraud P.O. Deli M.A. Forster C. Galla H.J. Romero I.A. Shusta E.V. In vitro models of the blood-brain barrier: An overview of commonly used brain endothelial cell culture models and guidelines for their use J. Cereb. Blood Flow Metab. 2016 36 862 890 10.1177/0271678X16630991 26868179 PMC4853841 · DOI · Paper page
  132. [138]Lu Y. Zhou Y. Zhang R. Wen L. Wu K. Li Y. Yao Y. Duan R. Jia Y. Bone Mesenchymal Stem Cell-Derived Extracellular Vesicles Promote Recovery Following Spinal Cord Injury via Improvement of the Integrity of the Blood-Spinal Cord Barrier Front. Neurosci. 2019 13 209 10.3389/fnins.2019.00209 30914918 PMC6423165 · DOI
  133. [139]Jean LeBlanc N. Guruswamy R. ElAli A. Vascular Endothelial Growth Factor Isoform-B Stimulates Neurovascular Repair After Ischemic Stroke by Promoting the Function of Pericytes via Vascular Endothelial Growth Factor Receptor-1 Mol. Neurobiol. 2018 55 3611 3626 10.1007/s12035-017-0478-6 28290152 · DOI
  134. [140]Denker S.P. Ji S. Dingman A. Lee S.Y. Derugin N. Wendland M.F. Vexler Z.S. Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke J. Neurochem. 2007 100 893 904 10.1111/j.1471-4159.2006.04162.x 17212701 PMC2262099 · DOI
  135. [141]Zhao S.C. Ma L.S. Chu Z.H. Xu H. Wu W.Q. Liu F. Regulation of microglial activation in stroke Acta Pharmacol. Sin. 2017 38 445 458 10.1038/aps.2016.162 28260801 PMC5386316 · DOI
  136. [142]Durafourt B.A. Moore C.S. Zammit D.A. Johnson T.A. Zaguia F. Guiot M.C. Bar-Or A. Antel J.P. Comparison of polarization properties of human adult microglia and blood-derived macrophages Glia 2012 60 717 727 10.1002/glia.22298 22290798 · DOI
  137. [143]Yin J. Valin K.L. Dixon M.L. Leavenworth J.W. The Role of Microglia and Macrophages in CNS Homeostasis, Autoimmunity, and Cancer J. Immunol. Res. 2017 2017 5150678 10.1155/2017/5150678 29410971 PMC5749282 · DOI
  138. [144]Boche D. Perry V.H. Nicoll J.A. Review: Activation patterns of microglia and their identification in the human brain Neuropathol. Appl. Neurobiol. 2013 39 3 18 10.1111/nan.12011 23252647 · DOI
  139. [145]Hu X. Li P. Guo Y. Wang H. Leak R.K. Chen S. Gao Y. Chen J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia Stroke 2012 43 3063 3070 10.1161/STROKEAHA.112.659656 22933588 · DOI
  140. [146]Faustino J.V. Wang X. Johnson C.E. Klibanov A. Derugin N. Wendland M.F. Vexler Z.S. Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke J. Neurosci. 2011 31 12992 13001 10.1523/JNEUROSCI.2102-11.2011 21900578 PMC3539822 · DOI
  141. [148]Pusic K.M. Pusic A.D. Kemme J. Kraig R.P. Spreading depression requires microglia and is decreased by their M2a polarization from environmental enrichment Glia 2014 62 1176 1194 10.1002/glia.22672 24723305 PMC4081540 · DOI · Paper page
  142. [150]Pan J. Jin J.L. Ge H.M. Yin K.L. Chen X. Han L.J. Chen Y. Qian L. Li X.X. Xu Y. Malibatol A regulates microglia M1/M2 polarization in experimental stroke in a PPARgamma-dependent manner J. Neuroinflamm. 2015 12 51 10.1186/s12974-015-0270-3 PMC4378556 25889216 · DOI
  143. [151]Wang J. Xia J. Huang R. Hu Y. Fan J. Shu Q. Xu J. Mesenchymal stem cell-derived extracellular vesicles alter disease outcomes via endorsement of macrophage polarization Stem Cell Res. Ther. 2020 11 424 10.1186/s13287-020-01937-8 32993783 PMC7522905 · DOI
  144. [152]Chen X. Yang B. Tian J. Hong H. Du Y. Li K. Li X. Wang N. Yu X. Wei X. Dental Follicle Stem Cells Ameliorate Lipopolysaccharide-Induced Inflammation by Secreting TGF-beta3 and TSP-1 to Elicit Macrophage M2 Polarization Cell Physiol. Biochem. 2018 51 2290 2308 10.1159/000495873 30537736 · DOI
  145. [153]Go V. Bowley B.G.E. Pessina M.A. Zhang Z.G. Chopp M. Finklestein S.P. Rosene D.L. Medalla M. Buller B. Moore T.L. Extracellular vesicles from mesenchymal stem cells reduce microglial-mediated neuroinflammation after cortical injury in aged Rhesus monkeys Geroscience 2020 42 1 17 10.1007/s11357-019-00115-w 31691891 PMC7031476 · DOI
  146. [154]Goncalves F.D.C. Luk F. Korevaar S.S. Bouzid R. Paz A.H. Lopez-Iglesias C. Baan C.C. Merino A. Hoogduijn M.J. Membrane particles generated from mesenchymal stromal cells modulate immune responses by selective targeting of pro-inflammatory monocytes Sci. Rep. 2017 7 12100 10.1038/s41598-017-12121-z 28935974 PMC5608915 · DOI
  147. [155]Zhao J. Li X. Hu J. Chen F. Qiao S. Sun X. Gao L. Xie J. Xu B. Mesenchymal stromal cell-derived exosomes attenuate myocardial ischaemia-reperfusion injury through miR-182-regulated macrophage polarization Cardiovasc. Res. 2019 115 1205 1216 10.1093/cvr/cvz040 30753344 PMC6529919 · DOI
  148. [156]Xin D. Li T. Chu X. Ke H. Yu Z. Cao L. Bai X. Liu D. Wang Z. Mesenchymal stromal cell-derived extracellular vesicles modulate microglia/macrophage polarization and protect the brain against hypoxia-ischemic injury in neonatal mice by targeting delivery of miR-21a-5p Acta Biomater. 2020 113 597 613 10.1016/j.actbio.2020.06.037 32619670 · DOI
  149. [157]He X. Dong Z. Cao Y. Wang H. Liu S. Liao L. Jin Y. Yuan L. Li B. MSC-Derived Exosome Promotes M2 Polarization and Enhances Cutaneous Wound Healing Stem Cells Int. 2019 2019 7132708 10.1155/2019/7132708 31582986 PMC6754952 · DOI
  150. [158]He S. Liu R. Li B. Huang L. Fan W. Tembachako C.R. Zheng X. Xiong X. Miyata M. Xu B. Propagermanium, a CCR2 inhibitor, attenuates cerebral ischemia/reperfusion injury through inhibiting inflammatory response induced by microglia Neurochem. Int. 2019 125 99 110 10.1016/j.neuint.2019.02.010 30794846 · DOI
  151. [159]Voloboueva L.A. Sun X. Xu L. Ouyang Y.B. Giffard R.G. Distinct Effects of miR-210 Reduction on Neurogenesis: Increased Neuronal Survival of Inflammation But Reduced Proliferation Associated with Mitochondrial Enhancement J. Neurosci. 2017 37 3072 3084 10.1523/JNEUROSCI.1777-16.2017 28188219 PMC5354339 · DOI
  152. [160]Meng Z.Y. Kang H.L. Duan W. Zheng J. Li Q.N. Zhou Z.J. MicroRNA-210 Promotes Accumulation of Neural Precursor Cells Around Ischemic Foci After Cerebral Ischemia by Regulating the SOCS1-STAT3-VEGF-C Pathway J. Am. Heart Assoc. 2018 7 10.1161/JAHA.116.005052 29478968 PMC5866312 · DOI
  153. [161]Zeng L. He X. Wang Y. Tang Y. Zheng C. Cai H. Liu J. Wang Y. Fu Y. Yang G.Y. MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain Gene Ther. 2014 21 37 43 10.1038/gt.2013.55 24152581 · DOI
  154. [162]Ayanlaja A.A. Xiong Y. Gao Y. Ji G. Tang C. Abdikani Abdullah Z. Gao D. Distinct Features of Doublecortin as a Marker of Neuronal Migration and Its Implications in Cancer Cell Mobility Front. Mol. Neurosci. 2017 10 199 10.3389/fnmol.2017.00199 28701917 PMC5487455 · DOI
  155. [163]Wang C. Liu F. Liu Y.Y. Zhao C.H. You Y. Wang L. Zhang J. Wei B. Ma T. Zhang Q. Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain Cell Res. 2011 21 1534 1550 10.1038/cr.2011.83 21577236 PMC3365638 · DOI
  156. [164]Han M. Cao Y. Xue H. Chu X. Li T. Xin D. Yuan L. Ke H. Li G. Wang Z. Neuroprotective Effect of Mesenchymal Stromal Cell-Derived Extracellular Vesicles Against Cerebral Ischemia-Reperfusion-Induced Neural Functional Injury: A Pivotal Role for AMPK and JAK2/STAT3/NF-kappaB Signaling Pathway Modulation Drug Des. Devel. Ther. 2020 14 2865 2876 10.2147/DDDT.S248892 32764885 PMC7381771 · DOI
  157. [165]Moon G.J. Sung J.H. Kim D.H. Kim E.H. Cho Y.H. Son J.P. Cha J.M. Bang O.Y. Application of Mesenchymal Stem Cell-Derived Extracellular Vesicles for Stroke: Biodistribution and MicroRNA Study Transl. Stroke Res. 2019 10 509 521 10.1007/s12975-018-0668-1 30341718 · DOI · Paper page
  158. [166]Zhang Y. Chopp M. Liu X.S. Katakowski M. Wang X. Tian X. Wu D. Zhang Z.G. Exosomes Derived from Mesenchymal Stromal Cells Promote Axonal Growth of Cortical Neurons Mol. Neurobiol. 2017 54 2659 2673 10.1007/s12035-016-9851-0 26993303 PMC5028236 · DOI
  159. [167]Zhou L. Lin Q. Wang P. Yao L. Leong K. Tan Z. Huang Z. Enhanced neuroprotective efficacy of bone marrow mesenchymal stem cells co-overexpressing BDNF and VEGF in a rat model of cardiac arrest-induced global cerebral ischemia Cell Death Dis. 2017 8 e2774 10.1038/cddis.2017.184 28492549 PMC5520708 · DOI
  160. [168]Nakajima M. Nito C. Sowa K. Suda S. Nishiyama Y. Nakamura-Takahashi A. Nitahara-Kasahara Y. Imagawa K. Hirato T. Ueda M. Mesenchymal Stem Cells Overexpressing Interleukin-10 Promote Neuroprotection in Experimental Acute Ischemic Stroke Mol. Ther. 2017 6 102 111 10.1016/j.omtm.2017.06.005 28725658 PMC5502709 · DOI
  161. [169]Cho G.W. Koh S.H. Kim M.H. Yoo A.R. Noh M.Y. Oh S. Kim S.H. The neuroprotective effect of erythropoietin-transduced human mesenchymal stromal cells in an animal model of ischemic stroke Brain Res. 2010 1353 1 13 10.1016/j.brainres.2010.06.013 20547143 · DOI
  162. [170]Toyama K. Honmou O. Harada K. Suzuki J. Houkin K. Hamada H. Kocsis J.D. Therapeutic benefits of angiogenetic gene-modified human mesenchymal stem cells after cerebral ischemia Exp. Neurol. 2009 216 47 55 10.1016/j.expneurol.2008.11.010 19094989 · DOI
  163. [173]Bak R.O. Porteus M.H. CRISPR-Mediated Integration of Large Gene Cassettes Using AAV Donor Vectors Cell Rep. 2017 20 750 756 10.1016/j.celrep.2017.06.064 28723575 PMC5568673 · DOI
  164. [174]Lee J. Bayarsaikhan D. Arivazhagan R. Park H. Lim B. Gwak P. Jeong G.B. Lee J. Byun K. Lee B. CRISPR/Cas9 Edited sRAGE-MSCs Protect Neuronal Death in Parkinsons Disease Model Int. J. Stem Cells 2019 12 114 124 10.15283/ijsc18110 30836725 PMC6457706 · DOI
  165. [175]Nihongaki Y. Kawano F. Nakajima T. Sato M. Photoactivatable CRISPR-Cas9 for optogenetic genome editing Nat. Biotechnol. 2015 33 755 760 10.1038/nbt.3245 26076431 · DOI
  166. [176]Polstein L.R. Gersbach C.A. A light-inducible CRISPR-Cas9 system for control of endogenous gene activation Nat. Chem. Biol. 2015 11 198 200 10.1038/nchembio.1753 25664691 PMC4412021 · DOI
  167. [177]Qi L.S. Larson M.H. Gilbert L.A. Doudna J.A. Weissman J.S. Arkin A.P. Lim W.A. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression Cell 2013 152 1173 1183 10.1016/j.cell.2013.02.022 23452860 PMC3664290 · DOI · Paper page
  168. [178]Strutt S.C. Torrez R.M. Kaya E. Negrete O.A. Doudna J.A. RNA-dependent RNA targeting by CRISPR-Cas9 Elife 2018 7 10.7554/eLife.32724 29303478 PMC5796797 · DOI
  169. [179]Dow L.E. Fisher J. O’Rourke K.P. Muley A. Kastenhuber E.R. Livshits G. Tschaharganeh D.F. Socci N.D. Lowe S.W. Inducible in vivo genome editing with CRISPR-Cas9 Nat. Biotechnol. 2015 33 390 394 10.1038/nbt.3155 25690852 PMC4390466 · DOI
  170. [180]Morshed M. Hasan A. Sharifi M. Nejadi Babadaei M.M. Bloukh S.H. Islam M.A. Chowdhury E.H. Falahati M. Non-viral delivery systems of DNA into stem cells: Promising and multifarious actions for regenerative medicine J. Drug Deliv. Sci. Technol. 2020 60 101861 10.1016/j.jddst.2020.101861 · DOI
  171. [181]Bucher C. Gazdhar A. Benneker L.M. Geiser T. Gantenbein-Ritter B. Nonviral Gene Delivery of Growth and Differentiation Factor 5 to Human Mesenchymal Stem Cells Injected into a 3D Bovine Intervertebral Disc Organ Culture System Stem Cells Int. 2013 2013 326828 10.1155/2013/326828 24454406 PMC3885261 · DOI
  172. [182]Lim J.Y. Park S.H. Jeong C.H. Oh J.H. Kim S.M. Ryu C.H. Park S.A. Ahn J.G. Oh W. Jeun S.S. Microporation is a valuable transfection method for efficient gene delivery into human umbilical cord blood-derived mesenchymal stem cells BMC Biotechnol. 2010 10 38 10.1186/1472-6750-10-38 20462460 PMC2883955 · DOI
  173. [183]Huang X. Zhang F. Wang H. Niu G. Choi K.Y. Swierczewska M. Zhang G. Gao H. Wang Z. Zhu L. Mesenchymal stem cell-based cell engineering with multifunctional mesoporous silica nanoparticles for tumor delivery Biomaterials 2013 34 1772 1780 10.1016/j.biomaterials.2012.11.032 23228423 PMC3538138 · DOI
  174. [184]Kim T.H. Kim M. Eltohamy M. Yun Y.R. Jang J.H. Kim H.W. Efficacy of mesoporous silica nanoparticles in delivering BMP-2 plasmid DNA for in vitro osteogenic stimulation of mesenchymal stem cells J. Biomed. Mater. Res. Part A 2013 101 1651 1660 10.1002/jbm.a.34466 23184619 · DOI
  175. [185]Moon H.H. Joo M.K. Mok H. Lee M. Hwang K.C. Kim S.W. Jeong J.H. Choi D. Kim S.H. MSC-based VEGF gene therapy in rat myocardial infarction model using facial amphipathic bile acid-conjugated polyethyleneimine Biomaterials 2014 35 1744 1754 10.1016/j.biomaterials.2013.11.019 24280192 · DOI
  176. [186]Koren E. Torchilin V.P. Cell-penetrating peptides: Breaking through to the other side Trends Mol. Med. 2012 18 385 393 10.1016/j.molmed.2012.04.012 22682515 · DOI
  177. [187]Jang Y.L. Yun U.J. Lee M.S. Kim M.G. Son S. Lee K. Chae S.Y. Lim D.W. Kim H.T. Kim S.H. Cell-penetrating peptide mimicking polymer-based combined delivery of paclitaxel and siRNA for enhanced tumor growth suppression Int. J. Pharm. 2012 434 488 493 10.1016/j.ijpharm.2012.04.083 22613208 · DOI
  178. [188]Peng L.H. Huang Y.F. Zhang C.Z. Niu J. Chen Y. Chu Y. Jiang Z.H. Gao J.Q. Mao Z.W. Integration of antimicrobial peptides with gold nanoparticles as unique non-viral vectors for gene delivery to mesenchymal stem cells with antibacterial activity Biomaterials 2016 103 137 149 10.1016/j.biomaterials.2016.06.057 27376562 · DOI
  179. [189]Tian H. Guo Z. Chen J. Lin L. Xia J. Dong X. Chen X. PEI conjugated gold nanoparticles: Efficient gene carriers with visible fluorescence Adv. Healthc Mater. 2012 1 337 341 10.1002/adhm.201200033 23184751 · DOI
  180. [190]Hu C. Peng Q. Chen F. Zhong Z. Zhuo R. Low molecular weight polyethylenimine conjugated gold nanoparticles as efficient gene vectors Bioconjug. Chem. 2010 21 836 843 10.1021/bc900374d 20438071 · DOI
  181. [191]Guidotti G. Brambilla L. Rossi D. Cell-Penetrating Peptides: From Basic Research to Clinics Trends Pharmacol. Sci. 2017 38 406 424 10.1016/j.tips.2017.01.003 28209404 · DOI
  182. [192]Bechara C. Sagan S. Cell-penetrating peptides: 20 years later, where do we stand? FEBS Lett. 2013 587 1693 1702 10.1016/j.febslet.2013.04.031 23669356 · DOI
  183. [193]Heitz F. Morris M.C. Divita G. Twenty years of cell-penetrating peptides: From molecular mechanisms to therapeutics Br. J. Pharmacol. 2009 157 195 206 10.1111/j.1476-5381.2009.00057.x 19309362 PMC2697800 · DOI
  184. [194]Hu Y. Chen W. Wu L. Jiang L. Qin H. Tang N. Hypoxic preconditioning improves the survival and neural effects of transplanted mesenchymal stem cells via CXCL12/CXCR4 signalling in a rat model of cerebral infarction Cell Biochem. Funct. 2019 37 504 515 10.1002/cbf.3423 31368195 · DOI
  185. [195]Liu H. Xue W. Ge G. Luo X. Li Y. Xiang H. Ding X. Tian P. Tian X. Hypoxic preconditioning advances CXCR4 and CXCR7 expression by activating HIF-1alpha in MSCs Biochem. Biophys. Res. Commun. 2010 401 509 515 10.1016/j.bbrc.2010.09.076 20869949 · DOI
  186. [196]Wei L. Fraser J.L. Lu Z.Y. Hu X. Yu S.P. Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats Neurobiol. Dis. 2012 46 635 645 10.1016/j.nbd.2012.03.002 22426403 PMC3353023 · DOI
  187. [197]Chen J. Liu Z. Hong M.M. Zhang H. Chen C. Xiao M. Wang J. Yao F. Ba M. Liu J. Proangiogenic compositions of microvesicles derived from human umbilical cord mesenchymal stem cells PLoS ONE 2014 9 e115316 10.1371/journal.pone.0115316 25514634 PMC4267846 · DOI
  188. [199]Kim E.H. Kim D.H. Kim H.R. Kim S.Y. Kim H.H. Bang O.Y. Stroke Serum Priming Modulates Characteristics of Mesenchymal Stromal Cells by Controlling the Expression miRNA-20a Cell Transplant. 2016 25 1489 1499 10.3727/096368916X690430 26762119 · DOI
  189. [200]Jeon E.S. Shin J.H. Hwang S.J. Moon G.J. Bang O.Y. Kim H.H. Cobalt chloride induces neuronal differentiation of human mesenchymal stem cells through upregulation of microRNA-124a Biochem. Biophys. Res. Commun. 2014 444 581 587 10.1016/j.bbrc.2014.01.114 24491559 · DOI
  190. [201]Choi Y.J. Li W.Y. Moon G.J. Lee P.H. Ahn Y.H. Lee G. Bang O.Y. Enhancing trophic support of mesenchymal stem cells by ex vivo treatment with trophic factors J. Neurol. Sci. 2010 298 28 34 10.1016/j.jns.2010.09.003 20864125 · DOI
  191. [202]Wei Z.Z. Gu X. Ferdinand A. Lee J.H. Ji X. Ji X.M. Yu S.P. Wei L. Intranasal delivery of bone marrow mesenchymal stem cells improved neurovascular regeneration and rescued neuropsychiatric deficits after neonatal stroke in rats Cell Transplant. 2015 24 391 402 10.3727/096368915X686887 25647744 · DOI
  192. [203]Park H.W. Moon H.E. Kim H.S. Paek S.L. Kim Y. Chang J.W. Yang Y.S. Kim K. Oh W. Hwang J.H. Human umbilical cord blood-derived mesenchymal stem cells improve functional recovery through thrombospondin1, pantraxin3, and vascular endothelial growth factor in the ischemic rat brain J. Neurosci. Res. 2015 93 1814 1825 10.1002/jnr.23616 26332684 · DOI
  193. [204]Wei N. Yu S.P. Gu X. Taylor T.M. Song D. Liu X.F. Wei L. Delayed intranasal delivery of hypoxic-preconditioned bone marrow mesenchymal stem cells enhanced cell homing and therapeutic benefits after ischemic stroke in mice Cell Transplant. 2013 22 977 991 10.3727/096368912X657251 23031629 · DOI
  194. [205]Wang J.W. Qiu Y.R. Fu Y. Liu J. He Z.J. Huang Z.T. Transplantation with hypoxia-preconditioned mesenchymal stem cells suppresses brain injury caused by cardiac arrest-induced global cerebral ischemia in rats J. Neurosci. Res. 2017 95 2059 2070 10.1002/jnr.24025 28186348 · DOI
  195. [206]Zhang Y. Ma L. Su Y. Su L. Lan X. Wu D. Han S. Li J. Kvederis L. Corey S. Hypoxia conditioning enhances neuroprotective effects of aged human bone marrow mesenchymal stem cell-derived conditioned medium against cerebral ischemia in vitro Brain Res. 2019 1725 146432 10.1016/j.brainres.2019.146432 31491422 · DOI
  196. [207]Kang T. Jones T.M. Naddell C. Bacanamwo M. Calvert J.W. Thompson W.E. Bond V.C. Chen Y.E. Liu D. Adipose-Derived Stem Cells Induce Angiogenesis via Microvesicle Transport of miRNA-31 Stem Cells Transl. Med. 2016 5 440 450 10.5966/sctm.2015-0177 26933040 PMC4798737 · DOI
  197. [208]Francois M. Romieu-Mourez R. Li M. Galipeau J. Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation Mol. Ther. 2012 20 187 195 10.1038/mt.2011.189 21934657 · DOI
  198. [209]Sivanathan K.N. Gronthos S. Rojas-Canales D. Thierry B. Coates P.T. Interferon-gamma modification of mesenchymal stem cells: Implications of autologous and allogeneic mesenchymal stem cell therapy in allotransplantation Stem Cell Rev. Rep. 2014 10 351 375 10.1007/s12015-014-9495-2 24510581 · DOI
  199. [210]Redondo-Castro E. Cunningham C. Miller J. Martuscelli L. Aoulad-Ali S. Rothwell N.J. Kielty C.M. Allan S.M. Pinteaux E. Interleukin-1 primes human mesenchymal stem cells towards an anti-inflammatory and pro-trophic phenotype in vitro Stem Cell Res. Ther 2017 8 79 10.1186/s13287-017-0531-4 28412968 PMC5393041 · DOI
  200. [211]Gorin C. Rochefort G.Y. Bascetin R. Ying H. Lesieur J. Sadoine J. Beckouche N. Berndt S. Novais A. Lesage M. Priming Dental Pulp Stem Cells With Fibroblast Growth Factor-2 Increases Angiogenesis of Implanted Tissue-Engineered Constructs Through Hepatocyte Growth Factor and Vascular Endothelial Growth Factor Secretion Stem Cells Transl. Med. 2016 5 392 404 10.5966/sctm.2015-0166 26798059 PMC4807665 · DOI

200 of 218 shown

Cited by

Sorted by citations

Authors
Davis, C., Savitz, S. I., & Satani, N.
Affiliations
The University of Texas Health Science Center at Houston (US)
Corresponding author
Satani, Nikunj
Venue
Cells
Publisher
MDPI AG
Published
2021-03-31
Volume
10
Issue
4
Pages
767
ISSN
2073-4409 (ISSN-L)
OpenAlex
W3139989032
Cited by
51
References
11
Citations by year
2026: 11 · 2025: 7 · 2024: 8 · 2023: 8 · 2022: 11 · 2021: 6
FWCI
0.87
Type
journal article
Language
en
Open access
Locations
  • Cells (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
  • Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
  • Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
Keywords
mesenchymal stem cells, extracellular vesicles, ischemic stroke, neurovascular unit, blood-brain barrier permeability, paracrine signaling, stroke recovery, stem cell homing, neuroinflammation
MeSH terms
Extracellular Vesicles, Ischemic Stroke, Animals, Blood-Brain Barrier, Brain, Humans, Nerve Regeneration, Mesenchymal Stem Cells

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