Osteoimmune Modulation and Guided Osteogenesis Promoted by Barrier Membranes Incorporated with S-Nitrosoglutathione (GSNO) and Mesenchymal Stem Cell-Derived Exosomes

References

• Wang X, Friis T, Glatt V, Crawford R, Xiao Y. Structural properties of fracture haematoma: current status and future clinical implications. J Tissue Eng Regen Med. 2017;11(10):2864–2875. doi:10.1002/term.219027401283
   PubMed Web of Science ®Google Scholar
• Gomez-Barrena E, Rosset P, Lozano D, Stanovici J, Ermthaller C, Gerbhard F. Bone fracture healing: cell therapy in delayed unions and nonunions. Bone. 2015;70:93–101. doi:10.1016/j.bone.2014.07.03325093266
   PubMed Web of Science ®Google Scholar
• Goulet JA, Senunas LE, DeSilva GL, Greenfield ML. Autogenous iliac crest bone graft. Complications and functional assessment. Clin Orthop Relat Res. 1997;339:76–81. doi:10.1097/00003086-199706000-00011
   PubMed Web of Science ®Google Scholar
• Xu XY, Li X, Wang J, He XT, Sun HH, Chen FM. Concise review: periodontal tissue regeneration using stem cells: strategies and translational considerations. Stem Cells Transl Med. 2018.
   Web of Science ®Google Scholar
• Ma Y, Zhou Y, Wu F, Ji W, Zhang J, Wang X. The bidirectional interactions between inflammation and coagulation in fracture hematoma. Tissue Eng Part B Rev. 2019;25(1):46–54. doi:10.1089/ten.teb.2018.015730129875
   PubMed Web of Science ®Google Scholar
• Galliot B, Crescenzi M, Jacinto A, Tajbakhsh S. Trends in tissue repair and regeneration. Development. 2017;144(3):357–364. doi:10.1242/dev.14427928143842
   PubMed Web of Science ®Google Scholar
• Ciuffi S, Zonefrati R, Brandi ML. Adipose stem cells for bone tissue repair. Clin Cases Miner Bone Metab. 2017;14(2):217–226. doi:10.11138/ccmbm/2017.14.1.21729263737
   PubMedGoogle Scholar
• Yang Y, Rossi FMV, Putnins EE. Periodontal regeneration using engineered bone marrow mesenchymal stromal cells. Biomaterials. 2010;31(33):8574–8582. doi:10.1016/j.biomaterials.2010.06.02620832109
   PubMed Web of Science ®Google Scholar
• Iwata T, Washio K, Yoshida T, et al. Cell sheet engineering and its application for periodontal regeneration. J Tissue Eng Regen Med. 2015;9(4):343–356. doi:10.1002/term.178523881816
   PubMed Web of Science ®Google Scholar
• Mazini L, Rochette L, Amine M, Malka G. Regenerative capacity of adipose derived stem cells (ADSCs), comparison with mesenchymal stem cells (MSCs). Int J Mol Sci. 2019;20(10):2523. doi:10.3390/ijms20102523
   PubMed Web of Science ®Google Scholar
• Sarko DK, McKinney CE. Exosomes: origins and therapeutic potential for neurodegenerative disease. Front Neurosci. 2017;11:82. doi:10.3389/fnins.2017.0008228289371
   PubMed Web of Science ®Google Scholar
• Wortzel I, Dror S, Kenific CM, Lyden D. Exosome-mediated metastasis: communication from a distance. Dev Cell. 2019;49(3):347–360. doi:10.1016/j.devcel.2019.04.01131063754
   PubMed Web of Science ®Google Scholar
• Teng X, Chen L, Chen W, Yang J, Yang Z, Shen Z. Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation. Cell Physiol Biochem. 2015;37(6):2415–2424. doi:10.1159/00043859426646808
   PubMed Web of Science ®Google Scholar
• Lou GH, Chen Z, Zheng M, Liu YN. Mesenchymal stem cell-derived exosomes as a new therapeutic strategy for liver diseases. Exp Mol Med. 2017;49(6):e346–e346. doi:10.1038/emm.2017.6328620221
   PubMed Web of Science ®Google Scholar
• Aghajani Nargesi A, Lerman LO, Eirin A. Mesenchymal stem cell-derived extracellular vesicles for kidney repair: current status and looming challenges. Stem Cell Res Ther. 2017;8(1):273. doi:10.1186/s13287-017-0727-729202871
   PubMed Web of Science ®Google Scholar
• Lee JH, Park J, Lee JW. Therapeutic use of mesenchymal stem cell-derived extracellular vesicles in acute lung injury. Transfusion. 2019;59(S1):876–883. doi:10.1111/trf.1483830383895
   PubMedGoogle Scholar
• De Jong OG, Van Balkom BW, Schiffelers RM, Bouten CV, Verhaar MC. Extracellular vesicles: potential roles in regenerative medicine. Front Immunol. 2014;5:608. doi:10.3389/fimmu.2014.0060825520717
   PubMed Web of Science ®Google Scholar
• Bateman RM, Ellis CG, Suematsu M, Walley KR. S-nitrosoglutathione acts as a small molecule modulator of human fibrin clot architecture. PLoS One. 2012;7(8):e43660. doi:10.1371/journal.pone.004366022916291
   PubMed Web of Science ®Google Scholar
• de Menezes AM, de Souza GF, Gomes AS, et al. S-nitrosoglutathione decreases inflammation and bone resorption in experimental periodontitis in rats. J Periodontol. 2012;83(4):514–521. doi:10.1902/jop.2011.11033221910597
   PubMed Web of Science ®Google Scholar
• Wang X, Friis TE, Masci PP, Crawford RW, Liao W, Xiao Y. Alteration of blood clot structures by interleukin-1 beta in association with bone defects healing. Sci Rep. 2016;6:35645. doi:10.1038/srep3564527767056
   PubMed Web of Science ®Google Scholar
• Lima B, Lam GK, Xie L, et al. Endogenous S-nitrosothiols protect against myocardial injury. Proc Natl Acad Sci U S A. 2009;106(15):6297–6302. doi:10.1073/pnas.090104310619325130
   PubMed Web of Science ®Google Scholar
• Shahrezaee M, Salehi M, Keshtkari S, Oryan A, Kamali A, Shekarchi B. In vitro and in vivo investigation of PLA/PCL scaffold coated with metformin-loaded gelatin nanocarriers in regeneration of critical-sized bone defects. Nanomedicine. 2018;14(7):2061–2073. doi:10.1016/j.nano.2018.06.00729964218
   PubMed Web of Science ®Google Scholar
• Kamath MS, Ahmed SS, Dhanasekaran M, Santosh SW. Polycaprolactone scaffold engineered for sustained release of resveratrol: therapeutic enhancement in bone tissue engineering. Int J Nanomedicine. 2014;9:183–195. doi:10.2147/IJN.S49460
   PubMed Web of Science ®Google Scholar
• Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101–1108. doi:10.1038/nprot.2008.7318546601
   PubMed Web of Science ®Google Scholar
• Wei F, Li Z, Crawford R, Xiao Y, Zhou Y. Immunoregulatory role of exosomes derived from differentiating mesenchymal stromal cells on inflammation and osteogenesis. J Tissue Eng Regen Med. 2019;13(11):1978–1991. doi:10.1002/term.294731359542
   PubMed Web of Science ®Google Scholar
• Jimi E, Hirata S, Osawa K, Terashita M, Kitamura C, Fukushima H. The current and future therapies of bone regeneration to repair bone defects. Int J Dent. 2012;2012:148261. doi:10.1155/2012/14826122505894
   PubMedGoogle Scholar
• Wang J, Wang L, Zhou Z, et al. Biodegradable polymer membranes applied in guided bone/tissue regeneration: a review. Polymers (Basel). 2016;8(4):115.
   PubMed Web of Science ®Google Scholar
• Wendler S, Schlundt C, Bucher CH, et al. Immune modulation to enhance bone healing-a new concept to induce bone using prostacyclin to locally modulate immunity. Front Immunol. 2019;10:713. doi:10.3389/fimmu.2019.0071331024548
   PubMed Web of Science ®Google Scholar
• Diwan AD, Wang MX, Jang D, Zhu W, Murrell GA. Nitric oxide modulates fracture healing. J Bone Miner Res. 2000;15(2):342–351. doi:10.1359/jbmr.2000.15.2.34210703937
   PubMed Web of Science ®Google Scholar
• Zhou X, Zhang J, Feng G, Shen J, Kong D, Zhao Q. Nitric oxide-releasing biomaterials for biomedical applications. Curr Med Chem. 2016;23(24):2579–2601. doi:10.2174/092986732366616072910464727480214
   PubMed Web of Science ®Google Scholar
• Liang H, Nacharaju P, Friedman A, Friedman JM. Nitric oxide generating/releasing materials. Future Sci OA. 2015;1(1). doi:10.4155/fso.15.54
   PubMedGoogle Scholar
• Pelegrino MT, De Araujo Lima B, Do Nascimento MHM, Lombello CB, Brocchi M, Seabra AB. Biocompatible and antibacterial nitric oxide-releasing pluronic F-127/chitosan hydrogel for topical applications. Polymers (Basel). 2018;10(4):452. doi:10.3390/polym10040452
   PubMed Web of Science ®Google Scholar
• Yoo JW, Acharya G, Lee CH. In vivo evaluation of vaginal films for mucosal delivery of nitric oxide. Biomaterials. 2009;30(23–24):3978–3985. doi:10.1016/j.biomaterials.2009.04.00419409611
   PubMed Web of Science ®Google Scholar
• Ramadass SK, Nazir LS, Thangam R, et al. Type I collagen peptides and nitric oxide releasing electrospun silk fibroin scaffold: a multifunctional approach for the treatment of ischemic chronic wounds. Colloids Surf B Biointerfaces. 2019;175:636–643. doi:10.1016/j.colsurfb.2018.12.02530583219
   PubMed Web of Science ®Google Scholar
• Won JS, Kim J, Annamalai B, Shunmugavel A, Singh I, Singh AK. Protective role of S-nitrosoglutathione (GSNO) against cognitive impairment in rat model of chronic cerebral hypoperfusion. J Alzheimers Dis. 2013;34(3):621–635. doi:10.3233/JAD-12178623254638
   PubMed Web of Science ®Google Scholar
• Khan M, Sekhon B, Giri S, et al. S-Nitrosoglutathione reduces inflammation and protects brain against focal cerebral ischemia in a rat model of experimental stroke. J Cereb Blood Flow Metab. 2005;25(2):177–192. doi:10.1038/sj.jcbfm.960001215647746
   PubMed Web of Science ®Google Scholar
• Khan M, Sakakima H, Dhammu TS, et al. S-nitrosoglutathione reduces oxidative injury and promotes mechanisms of neurorepair following traumatic brain injury in rats. J Neuroinflammation. 2011;8:78. doi:10.1186/1742-2094-8-7821733162
   PubMed Web of Science ®Google Scholar
• Khan M, Im YB, Shunmugavel A, et al. Administration of S-nitrosoglutathione after traumatic brain injury protects the neurovascular unit and reduces secondary injury in a rat model of controlled cortical impact. J Neuroinflammation. 2009;6:32. doi:10.1186/1742-2094-6-3219889224
   PubMed Web of Science ®Google Scholar
• Yamagata K, Nakayamada S, Tanaka Y. Use of mesenchymal stem cells seeded on the scaffold in articular cartilage repair. Inflamm Regen. 2018;38:4. doi:10.1186/s41232-018-0061-129560045
   PubMed Web of Science ®Google Scholar
• Lin Y, Umebayashi M, Abdallah MN, et al. Combination of polyetherketoneketone scaffold and human mesenchymal stem cells from temporomandibular joint synovial fluid enhances bone regeneration. Sci Rep. 2019;9(1):472. doi:10.1038/s41598-018-36778-230679553
   PubMedGoogle Scholar
• Kaigler D, Pagni G, Park CH, et al. Stem cell therapy for craniofacial bone regeneration: a randomized, controlled feasibility trial. Cell Transplant. 2013;22(5):767–777. doi:10.3727/096368912X65296822776413
   PubMed Web of Science ®Google Scholar
• Squillaro T, Peluso G, Galderisi U. Clinical trials with mesenchymal stem cells: an update. Cell Transplant. 2016;25(5):829–848. doi:10.3727/096368915X68962226423725
   PubMed Web of Science ®Google Scholar
• Wang J, Sun X, Zhao J, et al. Exosomes: a novel strategy for treatment and prevention of diseases. Front Pharmacol. 2017;8:300. doi:10.3389/fphar.2017.0030028659795
   PubMed Web of Science ®Google Scholar
• Willis GR, Kourembanas S, Mitsialis SA. Toward exosome-based therapeutics: isolation, heterogeneity, and fit-for-purpose potency. Front Cardiovasc Med. 2017;4:63. doi:10.3389/fcvm.2017.0006329062835
   PubMed Web of Science ®Google Scholar
• Liang X, Zhang L, Wang S, Han Q, Zhao RC. Exosomes secreted by mesenchymal stem cells promote endothelial cell angiogenesis by transferring miR-125a. J Cell Sci. 2016;129(11):2182–2189. doi:10.1242/jcs.17037327252357
   PubMed Web of Science ®Google Scholar
• Zhang S, Teo KYW, Chuah SJ, Lai RC, Lim SK, Toh WS. MSC exosomes alleviate temporomandibular joint osteoarthritis by attenuating inflammation and restoring matrix homeostasis. Biomaterials. 2019;200:35–47. doi:10.1016/j.biomaterials.2019.02.00630771585
   PubMed Web of Science ®Google Scholar
• Damania A, Jaiman D, Teotia AK, Kumar A. Mesenchymal stromal cell-derived exosome-rich fractionated secretome confers a hepatoprotective effect in liver injury. Stem Cell Res Ther. 2018;9(1):31. doi:10.1186/s13287-017-0752-629409540
   PubMedGoogle Scholar
• Xu N, Shao Y, Ye K, et al. Mesenchymal stem cell-derived exosomes attenuate phosgene-induced acute lung injury in rats. Inhal Toxicol. 2019;31(2):52–60. doi:10.1080/08958378.2019.159722031068039
   PubMed Web of Science ®Google Scholar
• Ni H, Yang S, Siaw-Debrah F, et al. Exosomes derived from bone mesenchymal stem cells ameliorate early inflammatory responses following traumatic brain injury. Front Neurosci. 2019;13:14. doi:10.3389/fnins.2019.0001430733666
   PubMed Web of Science ®Google Scholar
• Patel GK, Khan MA, Zubair H, et al. Comparative analysis of exosome isolation methods using culture supernatant for optimum yield, purity and downstream applications. Sci Rep. 2019;9(1):5335. doi:10.1038/s41598-019-41800-230926864
   PubMed Web of Science ®Google Scholar
• Lobb RJ, Becker M, Wen SW, et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J Extracell Vesicles. 2015;4:27031. doi:10.3402/jev.v4.2703126194179
   PubMed Web of Science ®Google Scholar
• Di Trapani M, Bassi G, Midolo M, et al. Differential and transferable modulatory effects of mesenchymal stromal cell-derived extracellular vesicles on T, B and NK cell functions. Sci Rep. 2016;6:24120. doi:10.1038/srep2412027071676
   PubMed Web of Science ®Google Scholar
• Ferguson SW, Wang J, Lee CJ, et al. The microRNA regulatory landscape of MSC-derived exosomes: a systems view. Sci Rep. 2018;8(1):1419. doi:10.1038/s41598-018-19581-x29362496
   PubMed Web of Science ®Google Scholar
• Caponnetto F, Manini I, Skrap M, et al. Size-dependent cellular uptake of exosomes. Nanomedicine. 2017;13(3):1011–1020. doi:10.1016/j.nano.2016.12.00927993726
   PubMed Web of Science ®Google Scholar
• Zhang J, Liu X, Li H, et al. Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway. Stem Cell Res Ther. 2016;7(1):136. doi:10.1186/s13287-016-0391-327650895
   PubMedGoogle Scholar
• Wang X, Shah FA, Vazirisani F, et al. Exosomes influence the behavior of human mesenchymal stem cells on titanium surfaces. Biomaterials. 2020;230:119571. doi:10.1016/j.biomaterials.2019.11957131753474
   PubMed Web of Science ®Google Scholar
• Wei F, Li M, Crawford R, Zhou Y, Xiao Y. Exosome-integrated titanium oxide nanotubes for targeted bone regeneration. Acta Biomater. 2019;86:480–492. doi:10.1016/j.actbio.2019.01.00630630122
   PubMed Web of Science ®Google Scholar
• Takeuchi R, Katagiri W, Endo S, Kobayashi T. Exosomes from conditioned media of bone marrow-derived mesenchymal stem cells promote bone regeneration by enhancing angiogenesis. PLoS One. 2019;14(11):e0225472. doi:10.1371/journal.pone.022547231751396
   PubMed Web of Science ®Google Scholar