Encapsulation of bone marrow-MSCs in PRP-derived fibrin microbeads and preliminary evaluation in a volumetric muscle loss injury rat model: modular muscle tissue engineering

References

• Pollot BE, Corona BT. Volumetric muscle loss. Methods Mol Biol. 2016;1460:19–31.
   PubMedGoogle Scholar
• Corona BT, Wenke JC, Ward CL. Pathophysiology of volumetric muscle loss injury. Cells Tissues Org. 2016;202:180–188.
   PubMed Web of Science ®Google Scholar
• Lipman A, Strauss E. Treatment of pectoralis major muscle ruptures. Bull Hosp Jt Dis. 2016;74:63–72.
   Web of Science ®Google Scholar
• Greising SM, Dearth CL, Corona BT. Regenerative and rehabilitative medicine: a necessary synergy for functional recovery from volumetric muscle loss injury. Cells Tissues Org. 2016;202:237–249.
   PubMed Web of Science ®Google Scholar
• Qazi TH, Mooney DJ, Pumberger M, et al. Biomaterials based strategies for skeletal muscle tissue engineering: existing technologies and future trends. Biomaterials. 2015;53:502–521.
   PubMed Web of Science ®Google Scholar
• Quarta MC, Chacon R, Blonigan J, et al. Bioengineered constructs combined with exercise enhance stem cell-mediated treatment of volumetric muscle loss. Nat Commun. 2017;8:15613.
   PubMed Web of Science ®Google Scholar
• Bian W, Bursac N. Tissue engineering of functional skeletal muscle: challenges and recent advances. IEEE Eng Med Biol Mag. 2008;27:109.
   PubMedGoogle Scholar
• Longo UG, Loppini M, Berton A, et al. Tissue engineered strategies for skeletal muscle injury. Stem Cells Int. 2012;2012:1.
   Web of Science ®Google Scholar
• Danna NR, Beutel BG, Campbell KA, et al. Therapeutic approaches to skeletal muscle repair and healing. Sports Health. 2014;6:348–355.
   PubMedGoogle Scholar
• Grasman JM, Zayas MJ, Page RL, et al. Biomimetic scaffolds for regeneration of volumetric muscle loss in skeletal muscle injuries. Acta Biomater. 2015;25:2–15.
   PubMed Web of Science ®Google Scholar
• Brazelton TR, Nystrom M, Blau HM. Significant differences among skeletal muscles in the incorporation of bone marrow-derived cells. Dev Biol. 2003;262:64–74.
   PubMed Web of Science ®Google Scholar
• Peçanha R, Bagno LL, Ribeiro MB, et al. Adipose-derived stem-cell treatment of skeletal muscle injury. J Bone Joint Surg Am. 2012;94:609–617.
   PubMed Web of Science ®Google Scholar
• Caseiro AR, Pereira T, Bártolo PJ, et al. Mesenchymal stem cells and biomaterials systems—perspectives for skeletal muscle tissue repair and regeneration. Proc Eng. 2015;110:90–97.
   Google Scholar
• Goldman SM, Henderson B.E.P, et al. Evaluation of bone marrow mononuclear cells as an adjunct therapy to minced muscle graft for the treatment of volumetric muscle loss injuries. Stem Cell Res Ther. 2017;8:142.
   PubMed Web of Science ®Google Scholar
• Parmaksiz M, Elçin AE, Elçin YM. Decellularization of bovine small intestinal submucosa and its use for the healing of a critical‐sized full‐thickness skin defect, alone and in combination with stem cells, in a small rodent model. J Tissue Eng Regen Med. 2017;11:1754–1765.
   PubMed Web of Science ®Google Scholar
• Eppley BL, Woodell JE, Higgins J. Platelet quantification and growth factor analysis from platelet-rich plasma: implications for wound healing. Plast Reconstr Surg. 2004;114:1502–1508.
   PubMed Web of Science ®Google Scholar
• Alsousou J, Thompson M, Hulley P, et al. The biology of platelet-rich plasma and its application in trauma and orthopaedic surgery. J Bone Jt Surg Br. 2009;91-B:987–996.
   Google Scholar
• Vu TD, Pal SN, Ti LK, et al. An autologous platelet-rich plasma hydrogel compound restores left ventricular structure, function and ameliorates adverse remodeling in a minimally invasive large animal myocardial restoration model: a translational approach: Vu and Pal “Myocardial Repair: PRP, Hydrogel and Supplements”. Biomaterials. 2015;45:27–35.
   PubMed Web of Science ®Google Scholar
• Fernandez-Moure JS, Van Eps JL, Cabrera FJ, et al. Platelet-rich plasma: a biomimetic approach to enhancement of surgical wound healing. J Surg Res. 2017;207:33–44.
   PubMed Web of Science ®Google Scholar
• Kasten P, Vogel J, Geiger F, et al. The effect of platelet-rich plasma on healing in critical-size long-bone defects. Biomaterials. 2008;29:3983–3992.
   PubMed Web of Science ®Google Scholar
• Zhao T, Yan W, Xu K, et al. Combined treatment with platelet-rich plasma and brain-derived neurotrophic factor-overexpressing bone marrow stromal cells supports axonal remyelination in a rat spinal cord hemi-section model. Cytotherapy. 2013;15:792–804.
   PubMed Web of Science ®Google Scholar
• Chen WH, Lo WC, Hsu WC, et al. Synergistic anabolic actions of hyaluronic acid and platelet-rich plasma on cartilage regeneration in osteoarthritis therapy. Biomaterials. 2014;35:9599–9607.
   PubMed Web of Science ®Google Scholar
• Dimauro I, Grasso L, Fittipaldi S, et al. Platelet-rich plasma and skeletal muscle healing: a molecular analysis of the early phases of the regeneration process in an experimental animal model. PLoS One. 2014;9:e102993.
   PubMed Web of Science ®Google Scholar
• McClure MJ, Garg K, Simpson DG, et al. The influence of platelet‐rich plasma on myogenic differentiation. J Tissue Eng Regen Med. 2016;10:E239–E249.
   PubMed Web of Science ®Google Scholar
• Bacakova M, Musilkova J, Riedel T, et al. The potential applications of fibrin-coated electrospun polylactide nanofibers in skin tissue engineering. Int J Nanomed. 2016;11:771–789. DOI:10.2147/IJN.S99317
   PubMed Web of Science ®Google Scholar
• Ahmed TAE, Dare EV, Hincke M. Fibrin: a versatile scaffold for tissue engineering applications. Tissue Eng B. 2008;14:199–215.
   PubMed Web of Science ®Google Scholar
• Dahlstrøm KK, Weis-Fogh US, Medgyesi S, et al. The use of autologous fibrin adhesive in skin transplantation. Plast Reconstr Surg. 1992;89:968–972.
   PubMed Web of Science ®Google Scholar
• Ahmed TAE, Giulivi A, Griffith M, et al. Fibrin glues in combination with mesenchymal stem cells to develop a tissue-engineered cartilage substitute. Tissue Eng A. 2011;17:323–335.
   PubMed Web of Science ®Google Scholar
• Pripatnanont P, Nuntanaranont T, Vongvatcharanon S, et al. The primacy of platelet-rich fibrin on bone regeneration of various grafts in rabbit’s calvarial defects. J Craniomaxillofac Surg. 2013;41:191–200.
   PubMed Web of Science ®Google Scholar
• Zhou H, Xu HHK. The fast release of stem cells from alginate-fibrin microbeads in injectable scaffolds for bone tissue engineering. Biomaterials. 2011;32:7503–7513.
   PubMed Web of Science ®Google Scholar
• Wang W, Li B, Yang J, et al. The restoration of full-thickness cartilage defects with BMSCs and TGF-beta 1 loaded PLGA/fibrin gel constructs. Biomaterials. 2010;31:8964–8973.
   PubMed Web of Science ®Google Scholar
• Thomson KS, Korte FS, Giachelli CM, et al. Prevascularized microtemplated fibrin scaffolds for cardiac tissue engineering applications. Tissue Eng A. 2013;19:967–977.
   PubMed Web of Science ®Google Scholar
• Scott JB, Afshari M, Kotek R, et al. The promotion of axon extension in vitro using polymer-templated fibrin scaffolds. Biomaterials. 2011;32:4830–4839.
   PubMed Web of Science ®Google Scholar
• Page RL, Malcuit C, Vilner L, et al. Restoration of skeletal muscle defects with adult human cells delivered on fibrin microthreads. Tissue Eng A. 2011;17:2629–2640.
   PubMed Web of Science ®Google Scholar
• Koc A, Emin N, Elcin AE, et al. In vitro osteogenic differentiation of rat mesenchymal stem cells in a microgravity bioreactor. J Bioact Comp Polym. 2008;23:244–261.
   Web of Science ®Google Scholar
• Emin N, Koc A, Durkut S, et al. Engineering of rat articular cartilage on porous sponges: effects of TGF-beta 1 and microgravity bioreactor culture. Artif Cell Blood Sub. 2008;36:123–137.
   PubMed Web of Science ®Google Scholar
• Durkut S, Elcin AE, Elcin YM. In vitro evaluation of encapsulated primary rat hepatocytes pre- and post-cryopreservation at-80 degrees C and in liquid nitrogen. Artif Cell Nanomed Biotechnol. 2015;43:50–61.
   PubMed Web of Science ®Google Scholar
• Fernandes G, Yang S. Application of platelet-rich plasma with stem cells in bone and periodontal tissue engineering. Bone Res. 2016;4:16036.
   PubMed Web of Science ®Google Scholar
• Celebi B, Elcin YM. Proteome analysis of rat bone marrow mesenchymal stem cell subcultures. J Proteome Res. 2009;8:2164–2172.
   PubMed Web of Science ®Google Scholar
• Celebi B, Elcin AE, Elcin YM. Proteome analysis of rat bone marrow mesenchymal stem cell differentiation. J Proteome Res. 2010;9:5217–5227.
   PubMed Web of Science ®Google Scholar
• Perka C, Arnold U, Spitzer RS, et al. The use of fibrin beads for tissue engineering and subsequential transplantation. Tissue Eng. 2001;7:359–361.
   PubMedGoogle Scholar
• Murphy MB, Blashki D, Buchanan RM, et al. Adult and umbilical cord blood-derived platelet-rich plasma for mesenchymal stem cell proliferation, chemotaxis, and cryo-preservation. Biomaterials. 2012;33:5308–5316.
   PubMed Web of Science ®Google Scholar
• Man Y, Wang P, Guo Y, et al. Angiogenic and osteogenic potential of platelet-rich plasma and adipose-derived stem cell laden alginate microspheres. Biomaterials. 2012;33:8802–8811.
   PubMed Web of Science ®Google Scholar
• Simman R, Hoffmann A, Bohinc RJ, et al. Role of platelet-rich plasma in acceleration of bone fracture healing. Ann Plast Surg. 2008;61:337–344.
   PubMed Web of Science ®Google Scholar
• Suzuki Y, Kuroda Y, Morita A, et al. Fibrin glue sealing for the prevention of pancreatic fistulas following distal pancreatectomy. Arch Surg. 1995;130:952–955.
   PubMed Web of Science ®Google Scholar
• Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–111.
   PubMed Web of Science ®Google Scholar
• Gurevich O, Vexler A, Marx G, et al. Fibrin microbeads for isolating and growing bone marrow-derived progenitor cells capable of forming bone tissue. Tissue Eng. 2002;8:661–672.
   PubMedGoogle Scholar
• Lee KY, Mooney DJ. Alginate: properties and biomedical applications. Prog Polym Sci. 2012;37:106–126.
   PubMed Web of Science ®Google Scholar
• Huang H, Zeng X, Li W, et al. Reinforced conducting hydrogels prepared from in-situ polymerization of aniline in an aqueous solution of sodium alginate. J Mater Chem A. 2014;2:16516–16522.
   Web of Science ®Google Scholar
• Aarimaa V, Kaariainen M, Vaittinen S, et al. Restoration of myofiber continuity after transection injury in the rat soleus. Neuromuscul Disord. 2004;14:421–428.
   PubMed Web of Science ®Google Scholar
• Pieri F, Lucarelli E, Corinaldesi G, et al. Effect of mesenchymal stem cells and platelet-rich plasma on the healing of standardized bone defects in the alveolar ridge: a comparative histomorphometric study in minipigs. J Oral Maxillofac Surg. 2009;67:265–272.
   PubMed Web of Science ®Google Scholar
• Teng C, Zhou C, Xu D, et al. Combination of platelet-rich plasma and bone marrow mesenchymal stem cells enhances tendon–bone healing in a rabbit model of anterior cruciate ligament reconstruction. J Orthop Surg Res. 2016;11:96.
   PubMed Web of Science ®Google Scholar
• Ogino Y, Ayukawa Y, Kukita T, et al. The contribution of platelet-derived growth factor, transforming growth factor-β1, and insulin-like growth factor-I in platelet-rich plasma to the proliferation of osteoblast-like cells. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol. 2006;101:724–729.
   PubMed Web of Science ®Google Scholar
• Tidball JG. Mechanisms of muscle injury, repair, and regeneration. Compr Physiol. 2011;1:2029–2062.
   PubMed Web of Science ®Google Scholar
• Jeong W, Yang CE, Roh TS, et al. Scar prevention and enhanced wound healing induced by polydeoxyribonucleotide in a rat incisional wound-healing model. IJMS. 2017;18:1698.
   Web of Science ®Google Scholar
• Ruehle MA, Stevens HY, Beedle AM, et al. Aggregate mesenchymal stem cell delivery ameliorates the regenerative niche for muscle repair. J Tissue Eng Regen Med. 2018;12(8):1867–1876. DOI:10.1002/term.2707 [Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Su N, Gao P-L, Wang K, et al. Fibrous scaffolds potentiate the paracrine function of mesenchymal stem cells: a new dimension in cell-material interaction. Biomaterials. 2017;141:74–85.
   PubMed Web of Science ®Google Scholar
• Mosca MJ, Rodeo SA. Platelet-rich plasma for muscle injuries: game over or time out? Curr Rev Musculoskelet Med. 2015;8:145–153.
   PubMed Web of Science ®Google Scholar
• Lyras DN, Kazakos K, Agrogiannis G, et al. Experimental study of tendon healing early phase: is IGF-1 expression influenced by platelet rich plasma gel? Orthop Traumatol Surg Res. 2010;96:381–387.
   PubMed Web of Science ®Google Scholar
• Mishra A, Tummala P, King A, et al. Buffered platelet-rich plasma enhances mesenchymal stem cell proliferation and chondrogenic differentiation. Tissue Eng Part C Methods. 2009;15:431–435.
   PubMed Web of Science ®Google Scholar
• Sassoli C, Vallone L, Tani A, et al. Combined use of bone marrow-derived mesenchymal stromal cells (BM-MSCs) and platelet rich plasma (PRP) stimulates proliferation and differentiation of myoblasts in vitro: new therapeutic perspectives for skeletal muscle repair/regeneration. Cell Tissue Res. 2018;372:549–570.
   PubMed Web of Science ®Google Scholar
• D'Esposito V, Passaretti F, Perruolo G, et al. Platelet‐rich plasma increases growth and motility of adipose tissue‐derived mesenchymal stem cells and controls adipocyte secretory function. J Cell Biochem. 2015;116:2408–2418.
   PubMed Web of Science ®Google Scholar
• Rubio-Azpeitia E, Andia I. Partnership between platelet-rich plasma and mesenchymal stem cells: in vitro experience. Muscles Ligaments Tendons J. 2014;4:52–62.
   PubMedGoogle Scholar