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Home / Equine Research Bank / Animals (Basel) / Nanoparticles from Equine Fetal Bone Marrow-Derived Cells En...
Animals : an open access journal from MDPI2020; 10(10); doi: 10.3390/ani10101723

Nanoparticles from Equine Fetal Bone Marrow-Derived Cells Enhance the Survival of Injured Chondrocytes.

Abstract: Recent studies have shown that mesenchymal stem cells (MSCs) can play a restorative role against degenerative joint diseases in horses. The purpose of this study was to investigate whether fetal bone marrow-derived cells (BMC)-derived nanoparticles (BMC-NPs) can stimulate the survival of equine chondrocytes. Equine fetal BMCs were isolated and characterized, and the role of BMC-NPs s in equine chondrocytes undergoing inflammatory cell death was examined. BMCs have several characteristics, such as the potential to differentiate into chondrocytes and osteocytes. Additionally, BMCs expressed immunoregulatory genes in response to treatment with tumor necrosis factor-alpha (TNF-α) and Interleukin 1 beta (IL-1β). We found that BMC-NPs were taken up by equine chondrocytes. Functionally, BMC-NPs promoted the growth of chondrocytes, and reduced apoptosis induced by inflammatory cytokines. Furthermore, we observed that BMC-NPs upregulated the phosphorylation of protein kinase B (Akt) in the presence of IL-1β, and reduced the phosphorylation of TNF-α-induced activation of extracellular signal-regulated kinase 1/2 (ERK1/2) in the chondrocytes. Cumulatively, our study demonstrated that equine fetal BMC-NPs have the potential to stimulate the survival of chondrocytes damaged by inflammatory cytokines. Thus, BMC-NPs may become an alternative cell-free allogenic therapeutic for degenerative joint diseases in horses.
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Publication Date: 2020-09-23 PubMed ID: 32977476PubMed Central: PMC7598183DOI: 10.3390/ani10101723Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article reports on the potential of nanoparticles derived from equine fetal bone marrow cells to enhance the survival and growth of damaged cartilage cells in horses. The study suggests these nanoparticles could offer a cell-free treatment option for degenerative joint diseases in horses.

Introduction

  • The article begins by discussing the role of mesenchymal stem cells (MSCs) in combating degenerative joint diseases in horses.
  • The study aims to investigate the potential of nanoparticles from fetal bone marrow-derived cells (BMCs) to enhance the survival of equine cartilage cells, also known as chondrocytes.

Methodology

  • Equine fetal BMCs were isolated and characterized to study their behavior and effects.
  • The researchers checked how these BMCs react to treatment with tumor necrosis factor-alpha (TNF-α) and Interleukin 1 beta (IL-1β), which are two proteins that play crucial roles in stimulating the immune response.
  • The researchers also examined the uptake of these BMC-derived nanoparticles (BMC-NPs) by chondrocytes, and their influence on the growth and survival of these cells.

Findings

  • The study found that BMC-NPs stimulate the growth of chondrocytes, and reduce their death triggered by inflammation-causing proteins.
  • BMC-NPs were found to upregulate the activation of a protein kinase B (Akt) in the presence of IL-1β.
  • They also reduce the activation of signal-regulated proteins (ERK1/2) stimulated by TNF-α in chondrocytes.

Conclusion

  • Ultimately, the research demonstrates the potential of equine fetal BMC-NPs to promote the survival of chondrocytes damaged by inflammatory proteins.
  • Therefore, BMC-NPs could serve as an alternative cell-free, allogeneic therapeutic strategy for degenerative joint diseases in horses.

Cite This Article

APA
Kim KH, Park TS, Cho BW, Kim TM. (2020). Nanoparticles from Equine Fetal Bone Marrow-Derived Cells Enhance the Survival of Injured Chondrocytes. Animals (Basel), 10(10). https://doi.org/10.3390/ani10101723

Publication

Animals : an open access journal from MDPI
ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 10
Issue: 10

Researcher Affiliations

Kim, Ki Hoon
  • Graduate School of International Agricultural Technology, Seoul National University, Pyeongchang Daero 1447, Pyeongchang, Gangwon-do 25354, Korea.
Park, Tae Sub
  • Graduate School of International Agricultural Technology, Seoul National University, Pyeongchang Daero 1447, Pyeongchang, Gangwon-do 25354, Korea.
  • Institutes of Green-Bio Science and Technology, Seoul National University, Pyeongchang Daero 1447, Pyeongchang, Gangwon-do 25354, Korea.
Cho, Byung-Wook
  • Department of Animal Science, College of Natural Resources and Life Sciences, Pusan National University, Samnangin-ro 1268-50, Miryang, Gyeongsangnam-do 50463, Korea.
Kim, Tae Min
  • Graduate School of International Agricultural Technology, Seoul National University, Pyeongchang Daero 1447, Pyeongchang, Gangwon-do 25354, Korea.
  • Institutes of Green-Bio Science and Technology, Seoul National University, Pyeongchang Daero 1447, Pyeongchang, Gangwon-do 25354, Korea.

Grant Funding

  • 2018R1D1A1A02085481 / National Research Foundation of Korea
  • 1403-20180039 / Seoul National University

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 67 references
  1. Ekstrand C, Bondesson U, Giving E, Hedeland M, Ingvast-Larsson C, Jacobsen S, Lofgren M, Moen L, Rhodin M, Saetra T. Disposition and effect of intra-articularly administered dexamethasone on lipopolysaccharide induced equine synovitis.. Acta Vet. Scand. 2019;61:28.
    doi: 10.1186/s13028-019-0464-2pmc: PMC6585085pubmed: 31221173google scholar: lookup
  2. Hardingham T.E.. Fell-Muir lecture: Cartilage 2010—the known unknowns.. Int. J. Exp. Pathol. 2010;91:203–209.
    doi: 10.1111/j.1365-2613.2010.00719.xpmc: PMC2884088pubmed: 20602640google scholar: lookup
  3. Neundorf R.H., Lowerison M.B., Cruz A.M., Thomason J.J., McEwen B.J., Hurtig M.B.. Determination of the prevalence and severity of metacarpophalangeal joint osteoarthritis in Thoroughbred racehorses via quantitative macroscopic evaluation.. Am. J. Vet. Res. 2010;71:1284–1293.
    doi: 10.2460/ajvr.71.11.1284pubmed: 21034319google scholar: lookup
  4. Reed S.R., Jackson B.F., Mc Ilwraith C.W., Wright I.M., Pilsworth R., Knapp S., Wood J.L., Price J.S., Verheyen K.L.. Descriptive epidemiology of joint injuries in Thoroughbred racehorses in training.. Equine Vet. J. 2012;44:13–19.
    doi: 10.1111/j.2042-3306.2010.00352.xpubmed: 21496103google scholar: lookup
  5. Broeckx S.Y., Seys B., Suls M., Vandenberghe A., Marien T., Adriaensen E., Declercq J., Van Hecke L., Braun G., Hellmann K.. Equine Allogeneic Chondrogenic Induced Mesenchymal Stem Cells Are an Effective Treatment for Degenerative Joint Disease in Horses.. Stem Cells Dev. 2019;28:410–422.
    doi: 10.1089/scd.2018.0061pmc: PMC6441287pubmed: 30623737google scholar: lookup
  6. Colbath A.C., Dow S.W., McIlwraith C.W., Goodrich L.R.. Mesenchymal stem cells for treatment of musculoskeletal disease in horses: Relative merits of allogeneic versus autologous stem cells.. Equine Vet. J. 2020;52:654–663.
    doi: 10.1111/evj.13233pubmed: 31971273google scholar: lookup
  7. Marinas-Pardo L., Garcia-Castro J., Rodriguez-Hurtado I., Rodriguez-Garcia M.I., Nunez-Naveira L., Hermida-Prieto M.. Allogeneic Adipose-Derived Mesenchymal Stem Cells (Horse Allo 20) for the Treatment of Osteoarthritis-Associated Lameness in Horses: Characterization, Safety, and Efficacy of Intra-Articular Treatment.. Stem Cells Dev. 2018;27:1147–1160.
    doi: 10.1089/scd.2018.0074pubmed: 29978736google scholar: lookup
  8. Broeckx S.Y., Martens A.M., Bertone A.L., Van Brantegem L., Duchateau L., Van Hecke L., Dumoulin M., Oosterlinck M., Chiers K., Hussein H.. The use of equine chondrogenic-induced mesenchymal stem cells as a treatment for osteoarthritis: A randomised, double-blinded, placebo-controlled proof-of-concept study.. Equine Vet. J. 2019;51:787–794.
    doi: 10.1111/evj.13089pmc: PMC6850029pubmed: 30815897google scholar: lookup
  9. Ardanaz N., Vazquez F.J., Romero A., Remacha A.R., Barrachina L., Sanz A., Ranera B., Vitoria A., Albareda J., Prades M.. Inflammatory response to the administration of mesenchymal stem cells in an equine experimental model: Effect of autologous, and single and repeat doses of pooled allogeneic cells in healthy joints.. BMC Vet. Res. 2016;12:65.
    doi: 10.1186/s12917-016-0692-xpmc: PMC4815220pubmed: 27029614google scholar: lookup
  10. Zayed M., Adair S., Ursini T., Schumacher J., Misk N., Dhar M.. Concepts and challenges in the use of mesenchymal stem cells as a treatment for cartilage damage in the horse.. Res. Vet. Sci. 2018;118:317–323.
    doi: 10.1016/j.rvsc.2018.03.011pubmed: 29601969google scholar: lookup
  11. Kourembanas S.. Exosomes: Vehicles of intercellular signaling, biomarkers, and vectors of cell therapy.. Annu. Rev. Physiol. 2015;77:13–27.
    doi: 10.1146/annurev-physiol-021014-071641pubmed: 25293529google scholar: lookup
  12. Murphy C., Withrow J., Hunter M., Liu Y., Tang Y.L., Fulzele S., Hamrick M.W.. Emerging role of extracellular vesicles in musculoskeletal diseases.. Mol. Asp. Med. 2018;60:123–128.
    doi: 10.1016/j.mam.2017.09.006pmc: PMC5856577pubmed: 28965750google scholar: lookup
  13. Burke J., Hunter M., Kolhe R., Isales C., Hamrick M., Fulzele S.. Therapeutic potential of mesenchymal stem cell based therapy for osteoarthritis.. Clin. Transl. Med. 2016;5:27.
    doi: 10.1186/s40169-016-0112-7pmc: PMC4980326pubmed: 27510262google scholar: lookup
  14. Joo H.S., Suh J.H., Lee H.J., Bang E.S., Lee J.M.. Current Knowledge and Future Perspectives on Mesenchymal Stem Cell-Derived Exosomes as a New Therapeutic Agent.. Int. J. Mol. Sci. 2020;21:727.
    doi: 10.3390/ijms21030727pmc: PMC7036914pubmed: 31979113google scholar: lookup
  15. Li J.J., Hosseini-Beheshti E., Grau G.E., Zreiqat H., Little C.B.. Stem Cell-Derived Extracellular Vesicles for Treating Joint Injury and Osteoarthritis.. Nanomaterials (Basel) 2019;9:261.
    doi: 10.3390/nano9020261pmc: PMC6409698pubmed: 30769853google scholar: lookup
  16. Liu Y., Lin L., Zou R., Wen C., Wang Z., Lin F.. MSC-derived exosomes promote proliferation and inhibit apoptosis of chondrocytes via lncRNA-KLF3-AS1/miR-206/GIT1 axis in osteoarthritis.. Cell Cycle. 2018;17:2411–2422.
    doi: 10.1080/15384101.2018.1526603pmc: PMC6342066pubmed: 30324848google scholar: lookup
  17. Zhang S., Teo K.Y.W., Chuah S.J., Lai R.C., Lim S.K., Toh W.S.. MSC exosomes alleviate temporomandibular joint osteoarthritis by attenuating inflammation and restoring matrix homeostasis.. Biomaterials. 2019;200:35–47.
    doi: 10.1016/j.biomaterials.2019.02.006pubmed: 30771585google scholar: lookup
  18. Zhang S., Chuah S.J., Lai R.C., Hui J.H.P., Lim S.K., Toh W.S.. MSC exosomes mediate cartilage repair by enhancing proliferation, attenuating apoptosis and modulating immune reactivity.. Biomaterials. 2018;156:16–27.
    doi: 10.1016/j.biomaterials.2017.11.028pubmed: 29182933google scholar: lookup
  19. Mao G., Zhang Z., Hu S., Zhang Z., Chang Z., Huang Z., Liao W., Kang Y.. Exosomes derived from miR-92a-3p-overexpressing human mesenchymal stem cells enhance chondrogenesis and suppress cartilage degradation via targeting WNT5A.. Stem Cell Res. 2018;9:247.
    doi: 10.1186/s13287-018-1004-0pmc: PMC6158854pubmed: 30257711google scholar: lookup
  20. Cosenza S., Toupet K., Maumus M., Luz-Crawford P., Blanc-Brude O., Jorgensen C., Noel D.. Mesenchymal stem cells-derived exosomes are more immunosuppressive than microparticles in inflammatory arthritis.. Theranostics. 2018;8:1399–1410.
    doi: 10.7150/thno.21072pmc: PMC5835945pubmed: 29507629google scholar: lookup
  21. Livak K.J., Schmittgen T.D.. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.. Methods. 2001;25:402–408.
    doi: 10.1006/meth.2001.1262pubmed: 11846609google scholar: lookup
  22. Xie L., Xie H., Chen C., Tao Z., Zhang C., Cai L.. Inhibiting the PI3K/AKT/NF-κB signal pathway with nobiletin for attenuating the development of osteoarthritis: In vitro and in vivo studies.. Food Funct. 2019;10:2161–2175.
    doi: 10.1039/C8FO01786Gpubmed: 30938722google scholar: lookup
  23. Viatour P., Merville M.P., Bours V., Chariot A.. Phosphorylation of NF-kappaB and IkappaB proteins: Implications in cancer and inflammation.. Trends Biochem. Sci. 2005;30:43–52.
    doi: 10.1016/j.tibs.2004.11.009pubmed: 15653325google scholar: lookup
  24. Park M.H., Hong J.T.. Roles of NF-kappaB in Cancer and Inflammatory Diseases and Their Therapeutic Approaches.. Cells. 2016;5:15.
    doi: 10.3390/cells5020015pmc: PMC4931664pubmed: 27043634google scholar: lookup
  25. Nejadnik H., Hui J.H., Feng Choong E.P., Tai B.-C., Lee E.H.. Autologous bone marrow–derived mesenchymal stem cells versus autologous chondrocyte implantation: An observational cohort study.. Am. J. Sports Med. 2010;38:1110–1116.
    doi: 10.1177/0363546509359067pubmed: 20392971google scholar: lookup
  26. Lim C.T., Ren X., Afizah M.H., Tarigan-Panjaitan S., Yang Z., Wu Y., Chian K.S., Mikos A.G., Hui J.H.. Repair of osteochondral defects with rehydrated freeze-dried oligo[poly(ethylene glycol) fumarate] hydrogels seeded with bone marrow mesenchymal stem cells in a porcine model.. Tissue Eng. Part A. 2013;19:1852–1861.
    doi: 10.1089/ten.tea.2012.0621pubmed: 23517496google scholar: lookup
  27. Bjorge I.M., Kim S.Y., Mano J.F., Kalionis B., Chrzanowski W.. Extracellular vesicles, exosomes and shedding vesicles in regenerative medicine—A new paradigm for tissue repair.. Biomater. Sci. 2017;6:60–78.
    doi: 10.1039/C7BM00479Fpubmed: 29184934google scholar: lookup
  28. Toh W.S., Lai R.C., Hui J.H.P., Lim S.K.. MSC exosome as a cell-free MSC therapy for cartilage regeneration: Implications for osteoarthritis treatment.. Semin. Cell Dev. Biol. 2017;67:56–64.
    doi: 10.1016/j.semcdb.2016.11.008pubmed: 27871993google scholar: lookup
  29. Chen K., Man C., Zhang B., Hu J., Zhu S.S.. Effect of in vitro chondrogenic differentiation of autologous mesenchymal stem cells on cartilage and subchondral cancellous bone repair in osteoarthritis of temporomandibular joint.. Int. J. Oral Maxillofac. Surg. 2013;42:240–248.
    doi: 10.1016/j.ijom.2012.05.030pubmed: 22763137google scholar: lookup
  30. Toh W.S., Foldager C.B., Pei M., Hui J.H.. Advances in mesenchymal stem cell-based strategies for cartilage repair and regeneration.. Stem Cell Rev. Rep. 2014;10:686–696.
    doi: 10.1007/s12015-014-9526-zpubmed: 24869958google scholar: lookup
  31. Hofer H.R., Tuan R.S.. Secreted trophic factors of mesenchymal stem cells support neurovascular and musculoskeletal therapies.. Stem Cell Res. 2016;7:131.
    doi: 10.1186/s13287-016-0394-0pmc: PMC5016979pubmed: 27612948google scholar: lookup
  32. Tao S.C., Yuan T., Zhang Y.L., Yin W.J., Guo S.C., Zhang C.Q.. Exosomes derived from miR-140-5p-overexpressing human synovial mesenchymal stem cells enhance cartilage tissue regeneration and prevent osteoarthritis of the knee in a rat model.. Theranostics. 2017;7:180–195.
    doi: 10.7150/thno.17133pmc: PMC5196895pubmed: 28042326google scholar: lookup
  33. Wang Y., Yu D., Liu Z., Zhou F., Dai J., Wu B., Zhou J., Heng B.C., Zou X.H., Ouyang H.. Exosomes from embryonic mesenchymal stem cells alleviate osteoarthritis through balancing synthesis and degradation of cartilage extracellular matrix.. Stem Cell Res. 2017;8:189.
    doi: 10.1186/s13287-017-0632-0pmc: PMC5556343pubmed: 28807034google scholar: lookup
  34. Zhu Y., Wang Y., Zhao B., Niu X., Hu B., Li Q., Zhang J., Ding J., Chen Y., Wang Y.. Comparison of exosomes secreted by induced pluripotent stem cell-derived mesenchymal stem cells and synovial membrane-derived mesenchymal stem cells for the treatment of osteoarthritis.. Stem Cell Res. 2017;8:64.
    doi: 10.1186/s13287-017-0510-9pmc: PMC5345222pubmed: 28279188google scholar: lookup
  35. Zhang S., Chu W.C., Lai R.C., Lim S.K., Hui J.H., Toh W.S.. Exosomes derived from human embryonic mesenchymal stem cells promote osteochondral regeneration.. Osteoarthr. Cartil. 2016;24:2135–2140.
    doi: 10.1016/j.joca.2016.06.022pubmed: 27390028google scholar: lookup
  36. Mao Z., Li Y., Yang Y., Fang Z., Chen X., Wang Y., Kang J., Qu X., Yuan W., Dai K.. Osteoinductivity and Antibacterial Properties of Strontium Ranelate-Loaded Poly(Lactic-co-Glycolic Acid) Microspheres With Assembled Silver and Hydroxyapatite Nanoparticles.. Front. Pharm. 2018;9:368.
    doi: 10.3389/fphar.2018.00368pmc: PMC5915458pubmed: 29720940google scholar: lookup
  37. Wu J., Kuang L., Chen C., Yang J., Zeng W.-N., Li T., Chen H., Huang S., Fu Z., Li J.. miR-100-5p-abundant exosomes derived from infrapatellar fat pad MSCs protect articular cartilage and ameliorate gait abnormalities via inhibition of mTOR in osteoarthritis.. Biomaterials. 2019;206:87–100.
    doi: 10.1016/j.biomaterials.2019.03.022pubmed: 30927715google scholar: lookup
  38. Zavatti M., Beretti F., Casciaro F., Bertucci E., Maraldi T.. Comparison of the therapeutic effect of amniotic fluid stem cells and their exosomes on monoiodoacetate-induced animal model of osteoarthritis.. Biofactors. 2020;46:106–117.
    doi: 10.1002/biof.1576pubmed: 31625201google scholar: lookup
  39. Guillot P.V., Gotherstrom C., Chan J., Kurata H., Fisk N.M.. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC.. Stem Cells. 2007;25:646–654.
    doi: 10.1634/stemcells.2006-0208pubmed: 17124009google scholar: lookup
  40. Stenderup K., Justesen J., Clausen C., Kassem M.. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells.. Bone. 2003;33:919–926.
    doi: 10.1016/j.bone.2003.07.005pubmed: 14678851google scholar: lookup
  41. Zhang Z.Y., Teoh S.H., Chong M.S., Schantz J.T., Fisk N.M., Choolani M.A., Chan J.. Superior osteogenic capacity for bone tissue engineering of fetal compared with perinatal and adult mesenchymal stem cells.. Stem Cells. 2009;27:126–137.
    doi: 10.1634/stemcells.2008-0456pubmed: 18832592google scholar: lookup
  42. Campagnoli C., Roberts I.A., Kumar S., Bennett P.R., Bellantuono I., Fisk N.M.. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow.. Blood. 2001;98:2396–2402.
    doi: 10.1182/blood.V98.8.2396pubmed: 11588036google scholar: lookup
  43. Caplan A.I.. The mesengenic process.. Clin. Plast. Surg. 1994;21:429–435.
    doi: 10.1016/S0094-1298(20)31020-8pubmed: 7924141google scholar: lookup
  44. Mattar P., Bieback K.. Comparing the immunomodulatory properties of bone marrow, adipose tissue, and birth-associated tissue mesenchymal stromal cells.. Front. Immunol. 2015;6:560.
    doi: 10.3389/fimmu.2015.00560pmc: PMC4630659pubmed: 26579133google scholar: lookup
  45. Ullah I., Subbarao R.B., Rho G.J.. Human mesenchymal stem cells-current trends and future prospective.. Biosci. Rep. 2015.
    doi: 10.1042/BSR20150025pmc: PMC4413017pubmed: 25797907google scholar: lookup
  46. Gotherstrom C., Ringden O., Westgren M., Tammik C., Le Blanc K.. Immunomodulatory effects of human foetal liver-derived mesenchymal stem cells.. Bone Marrow Transpl. 2003;32:265–272.
    doi: 10.1038/sj.bmt.1704111pubmed: 12858197google scholar: lookup
  47. Götherström C., Lundqvist A., Duprez I.R., Childs R., Berg L., le Blanc K.J.C.. Fetal and adult multipotent mesenchymal stromal cells are killed by different pathways.. Cytotherapy. 2011;13:269–278.
    doi: 10.3109/14653249.2010.523077pubmed: 20942778google scholar: lookup
  48. Gotherstrom C., Ringden O., Tammik C., Zetterberg E., Westgren M., Le Blanc K.. Immunologic properties of human fetal mesenchymal stem cells.. Am. J. Obs. Gynecol. 2004;190:239–245.
    doi: 10.1016/j.ajog.2003.07.022pubmed: 14749666google scholar: lookup
  49. Kim M., Kim C., Choi Y.S., Kim M., Park C., Suh Y.. Age-related alterations in mesenchymal stem cells related to shift in differentiation from osteogenic to adipogenic potential: Implication to age-associated bone diseases and defects.. Mech. Ageing Dev. 2012;133:215–225.
    doi: 10.1016/j.mad.2012.03.014pubmed: 22738657google scholar: lookup
  50. Guillot P.V., De Bari C., Dell’Accio F., Kurata H., Polak J., Fisk N.M.. Comparative osteogenic transcription profiling of various fetal and adult mesenchymal stem cell sources.. Differentiation. 2008;76:946–957.
    doi: 10.1111/j.1432-0436.2008.00279.xpubmed: 18557767google scholar: lookup
  51. Kim S., Lee S.K., Kim H., Kim T.M.. Exosomes Secreted from Induced Pluripotent Stem Cell-Derived Mesenchymal Stem Cells Accelerate Skin Cell Proliferation.. Int. J. Mol. Sci. 2018;19:3119.
    doi: 10.3390/ijms19103119pmc: PMC6213597pubmed: 30314356google scholar: lookup
  52. Zhang J., Liu X., Li H., Chen C., Hu B., Niu X., Li Q., Zhao B., Xie Z., Wang Y.. Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway.. Stem Cell Res. 2016;7:136.
    doi: 10.1186/s13287-016-0391-3pmc: PMC5028974pubmed: 27650895google scholar: lookup
  53. Arslan F., Lai R.C., Smeets M.B., Akeroyd L., Choo A., Aguor E.N., Timmers L., van Rijen H.V., Doevendans P.A., Pasterkamp G.. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury.. Stem Cell Res. 2013;10:301–312.
    doi: 10.1016/j.scr.2013.01.002pubmed: 23399448google scholar: lookup
  54. Barberini D.J., Freitas N.P.P., Magnoni M.S., Maia L., Listoni A.J., Heckler M.C., Sudano M.J., Golim M.A., da Cruz Landim-Alvarenga F., Amorim R.M.. Equine mesenchymal stem cells from bone marrow, adipose tissue and umbilical cord: Immunophenotypic characterization and differentiation potential.. Stem Cell Res. 2014;5:25.
    doi: 10.1186/scrt414pmc: PMC4055040pubmed: 24559797google scholar: lookup
  55. Ranera B., Lyahyai J., Romero A., Vazquez F.J., Remacha A.R., Bernal M.L., Zaragoza P., Rodellar C., Martin-Burriel I.. Immunophenotype and gene expression profiles of cell surface markers of mesenchymal stem cells derived from equine bone marrow and adipose tissue.. Vet. Immunol. Immunopathol. 2011;144:147–154.
    doi: 10.1016/j.vetimm.2011.06.033pubmed: 21782255google scholar: lookup
  56. Xie L., Zhang N., Marsano A., Vunjak-Novakovic G., Zhang Y., Lopez M.J.. In vitro mesenchymal trilineage differentiation and extracellular matrix production by adipose and bone marrow derived adult equine multipotent stromal cells on a collagen scaffold.. Stem Cell Rev. Rep. 2013;9:858–872.
    doi: 10.1007/s12015-013-9456-1pmc: PMC3834181pubmed: 23892935google scholar: lookup
  57. Hillmann A., Ahrberg A.B., Brehm W., Heller S., Josten C., Paebst F., Burk J.. Comparative Characterization of Human and Equine Mesenchymal Stromal Cells: A Basis for Translational Studies in the Equine Model.. Cell Transpl. 2016;25:109–124.
    doi: 10.3727/096368915X687822pubmed: 25853993google scholar: lookup
  58. Capomaccio S., Cappelli K., Bazzucchi C., Coletti M., Gialletti R., Moriconi F., Passamonti F., Pepe M., Petrini S., Mecocci S.. Equine Adipose-Derived Mesenchymal Stromal Cells Release Extracellular Vesicles Enclosing Different Subsets of Small RNAs.. Stem Cells Int. 2019;2019:4957806.
    doi: 10.1155/2019/4957806pmc: PMC6442443pubmed: 31011332google scholar: lookup
  59. Pascucci L., Alessandri G., Dall’Aglio C., Mercati F., Coliolo P., Bazzucchi C., Dante S., Petrini S., Curina G., Ceccarelli P.. Membrane vesicles mediate pro-angiogenic activity of equine adipose-derived mesenchymal stromal cells.. Vet. J. 2014;202:361–366.
    doi: 10.1016/j.tvjl.2014.08.021pubmed: 25241947google scholar: lookup
  60. Klymiuk M.C., Balz N., Elashry M.I., Heimann M., Wenisch S., Arnhold S.. Exosomes isolation and identification from equine mesenchymal stem cells.. BMC Vet. Res. 2019;15:42.
    doi: 10.1186/s12917-019-1789-9pmc: PMC6348641pubmed: 30691449google scholar: lookup
  61. Kojima M., Gimenes-Junior J.A., Langness S., Morishita K., Lavoie-Gagne O., Eliceiri B., Costantini T.W., Coimbra R.. Exosomes, not protein or lipids, in mesenteric lymph activate inflammation: Unlocking the mystery of post-shock multiple organ failure.. J. Trauma Acute Care Surg. 2017;82:42–50.
    doi: 10.1097/TA.0000000000001296pubmed: 27779585google scholar: lookup
  62. Kowal J., Arras G., Colombo M., Jouve M., Morath J.P., Primdal-Bengtson B., Dingli F., Loew D., Tkach M., Thery C.. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes.. Proc. Natl. Acad. Sci. USA. 2016;113:E968–E977.
    doi: 10.1073/pnas.1521230113pmc: PMC4776515pubmed: 26858453google scholar: lookup
  63. Xiao B., Chai Y., Lv S., Ye M., Wu M., Xie L., Fan Y., Zhu X., Gao Z.. Endothelial cell-derived exosomes protect SH-SY5Y nerve cells against ischemia/reperfusion injury.. Int. J. Mol. Med. 2017;40:1201–1209.
    doi: 10.3892/ijmm.2017.3106pmc: PMC5593464pubmed: 28849073google scholar: lookup
  64. Schey K.L., Luther J.M., Rose K.L.. Proteomics characterization of exosome cargo.. Methods. 2015;87:75–82.
    doi: 10.1016/j.ymeth.2015.03.018pmc: PMC4591097pubmed: 25837312google scholar: lookup
  65. Kim J., Shin H., Kim J., Kim J., Park J.. Isolation of High-Purity Extracellular Vesicles by Extracting Proteins Using Aqueous Two-Phase System.. PLoS ONE. 2015;10:e0129760.
    doi: 10.1371/journal.pone.0129760pmc: PMC4475045pubmed: 26090684google scholar: lookup
  66. Shin H., Park Y.H., Kim Y.G., Lee J.Y., Park J.. Aqueous two-phase system to isolate extracellular vesicles from urine for prostate cancer diagnosis.. PLoS ONE. 2018;13:e0194818.
    doi: 10.1371/journal.pone.0194818pmc: PMC5870972pubmed: 29584777google scholar: lookup
  67. Skotland T., Sagini K., Sandvig K., Llorente A.. An emerging focus on lipids in extracellular vesicles.. Adv. Drug Deliv. Rev. 2020.
    doi: 10.1016/j.addr.2020.03.002pubmed: 32151658google scholar: lookup
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