695
Views
71
CrossRef citations to date
0
Altmetric
Review

Platelet-rich plasma, a source of autologous growth factors and biomimetic scaffold for peripheral nerve regeneration

, , , , , & show all
Pages 197-212 | Received 25 Jul 2016, Accepted 08 Nov 2016, Published online: 28 Nov 2016

References

  • Griffin JW, Hogan MV, Chhabra AB, et al. Peripheral nerve repair and reconstruction. J Bone Joint Surg Am. 2013;95:2144–2151. DOI:10.2106/JBJS.L.00704
  • Fowler JR, Lavasani M, Huard J, et al. Biologic strategies to improve nerve regeneration after peripheral nerve repair. J Reconstr Microsurg. 2015;31:243–248. DOI:10.1055/s-0034-1394091
  • Faroni A, Mobasseri SA, Kingham PJ, et al. Peripheral nerve regeneration: experimental strategies and future perspectives. Adv Drug Deliv Rev. 2015;82-83:160–167. DOI:10.1016/j.addr.2014.11.010
  • Evans GR. Peripheral nerve injury: a review and approach to tissue engineered constructs. Anat Rec. 2001;263:396–404.
  • Belkas JS, Shoichet MS, Midha R. Peripheral nerve regeneration through guidance tubes. Neurol Res. 2004;26:151–160. DOI:10.1179/016164104225013798
  • Hoke A. Mechanisms of Disease: what factors limit the success of peripheral nerve regeneration in humans? Nat Clin Pract Neurol. 2006;2:448–454. DOI:10.1038/ncpneuro0262
  • Allodi I, Udina E, Navarro X. Specificity of peripheral nerve regeneration: interactions at the axon level. Prog Neurobiol. 2012;98:16–37. DOI:10.1016/j.pneurobio.2012.05.005 .
  • Pfister BJ, Gordon T, Loverde JR, et al. Biomedical engineering strategies for peripheral nerve repair: surgical applications, state of the art, and future challenges. Crit Rev Biomed Eng. 2011;39:81–124.
  • Scheib J, Hoke A. Advances in peripheral nerve regeneration. Nat Rev Neurol. 2013;9:668–676. DOI:10.1038/nrneurol.2013.227
  • Painter MW, Brosius Lutz A, Cheng YC, et al. Diminished Schwann cell repair responses underlie age-associated impaired axonal regeneration. Neuron. 2014;83:331–343. DOI:10.1016/j.neuron.2014.06.016
  • Zochodne DW. The challenges and beauty of peripheral nerve regrowth. J Peripher Nerv Syst. 2012;17:1–18. DOI:10.1111/j.1529-8027.2012.00378.x
  • Lu P, Wang Y, Graham L, et al. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell. 2012;150:1264–1273. DOI:10.1016/j.cell.2012.08.020
  • Marquardt LM, Sakiyama-Elbert SE. Engineering peripheral nerve repair. Curr Opin Biotechnol. 2013;24:887–892. DOI:10.1016/j.copbio.2013.05.006
  • Daly WT, Knight AM, Wang H, et al. Comparison and characterization of multiple biomaterial conduits for peripheral nerve repair. Biomaterials. 2013;34:8630–8639. DOI:10.1016/j.biomaterials.2013.07.086
  • Deumens R, Bozkurt A, Meek MF, et al. Repairing injured peripheral nerves: bridging the gap. Prog Neurobiol. 2010;92:245–276. DOI:10.1016/j.pneurobio.2010.10.002
  • Sanchez M, Yoshioka T, Ortega M, et al. Ultrasound-guided platelet-rich plasma injections for the treatment of common peroneal nerve palsy associated with multiple ligament injuries of the knee. Knee Surg Sports Traumatol Arthrosc. 2014;22:1084–1089. DOI:10.1007/s00167-013-2479-y
  • Sanchez M, Anitua E, Delgado D, et al. Ultrasound-guided plasma rich in growth factors injections and scaffolds hasten motor nerve functional recovery in an ovine model of nerve crush injury. J Tissue Eng Regen Med. 2015. DOI:10.1002/term.2079
  • Kuffler DP. An assessment of current techniques for inducing axon regeneration and neurological recovery following peripheral nerve trauma. Prog Neurobiol. 2014;116:1–12. DOI:10.1016/j.pneurobio.2013.12.004
  • Giannessi E, Coli A, Stornelli MR, et al. An autologously generated platelet-rich plasma suturable membrane may enhance peripheral nerve regeneration after neurorraphy in an acute injury model of sciatic nerve neurotmesis. J Reconstr Microsurg. 2014;30:617–626. DOI:10.1055/s-0034-1372483
  • Zheng C, Zhu Q, Liu X, et al. Effect of platelet-rich plasma (PRP) concentration on proliferation, neurotrophic function and migration of Schwann cells in vitro. J Tissue Eng Regen Med. 2016;10:428–436. DOI:10.1002/term.1756
  • Young J, Medawar P. Fibrin suture of peripheral nerves: measurement of the rate of regeneration. The Lancet. 1940;236:126–128. DOI:10.1016/S0140-6736(01)07978-8 .
  • Anitua E, Pascual C, Perez-Gonzalez R, et al. Intranasal delivery of plasma and platelet growth factors using PRGF-Endoret system enhances neurogenesis in a mouse model of Alzheimer’s disease. PLoS One. 2013;8:e73118. DOI:10.1371/journal.pone.0073118
  • Anitua E, Pascual C, Perez-Gonzalez R, et al. Intranasal PRGF-Endoret enhances neuronal survival and attenuates NF-kappaB-dependent inflammation process in a mouse model of Parkinson’s disease. J Control Release. 2015;203:170–180. DOI:10.1016/j.jconrel.2015.02.030
  • Anjayani S, Wirohadidjojo YW, Adam AM, et al. Sensory improvement of leprosy peripheral neuropathy in patients treated with perineural injection of platelet-rich plasma. Int J Dermatol. 2014;53:109–113. DOI:10.1111/ijd.12162
  • Zheng C, Zhu Q, Liu X, et al. Improved peripheral nerve regeneration using acellular nerve allografts loaded with platelet-rich plasma. Tissue Eng Part A. 2014;20:3228–3240. DOI:10.1089/ten.TEA.2013.0729
  • Kuffler DP. Platelet-rich plasma promotes axon regeneration, wound healing, and pain reduction: fact or fiction. Mol Neurobiol. 2015;52:990–1014. DOI:10.1007/s12035-015-9251-x
  • Malahias MA, Johnson EO, Babis GC, et al. Single injection of platelet-rich plasma as a novel treatment of carpal tunnel syndrome. Neural Regen Res. 2015;10:1856–1859. DOI:10.4103/1673-5374.165322
  • Seddon H, Medawar P. Fibrin suture of human nerves. Lancet. 1942;240:87–88. DOI:10.1016/S0140-6736(00)62286-9
  • Dalton P, Harvey A, Oudega M, et al. Tissue engineering of the nervous system. Tissue Eng. 2008;611–647. DOI:10.1016/B978-0-12-370869-4.00020-3
  • Mueller M, Wacker K, Ringelstein EB, et al. Rapid response of identified resident endoneurial macrophages to nerve injury. Am J Pathol. 2001;159:2187–2197. DOI:10.1016/S0002-9440(10)63070-2
  • Raimondo S, Fornaro M, Tos P, et al. Perspectives in regeneration and tissue engineering of peripheral nerves. Ann Anat. 2011;193:334–340. DOI:10.1016/j.aanat.2011.03.001
  • Parrinello S, Napoli I, Ribeiro S, et al. EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell. 2010;143:145–155. DOI:10.1016/j.cell.2010.08.039
  • Cattin AL, Burden JJ, Van Emmenis L, et al. Macrophage-induced blood vessels guide schwann cell-mediated regeneration of peripheral nerves. Cell. 2015;162:1127–1139. DOI:10.1016/j.cell.2015.07.021 .
  • Chen P, Piao X, Bonaldo P. Role of macrophages in Wallerian degeneration and axonal regeneration after peripheral nerve injury. Acta Neuropathol. 2015;130:605–618. DOI:10.1007/s00401-015-1482-4
  • Chen YY, McDonald D, Cheng C, et al. Axon and Schwann cell partnership during nerve regrowth. J Neuropathol Exp Neurol. 2005;64:613–622.
  • Sakiyama-Elbert SE, Hubbell JA. Controlled release of nerve growth factor from a heparin-containing fibrin-based cell ingrowth matrix. J Control Release. 2000;69:149–158.
  • Yao L, Damodaran G, Nikolskaya N, et al. The effect of laminin peptide gradient in enzymatically cross-linked collagen scaffolds on neurite growth. J Biomed Mater Res A. 2010;92:484–492. DOI:10.1002/jbm.a.32359
  • Dubovy P. Wallerian degeneration and peripheral nerve conditions for both axonal regeneration and neuropathic pain induction. Ann Anat. 2011;193:267–275. DOI:10.1016/j.aanat.2011.02.011
  • Jessen KR, Mirsky R, Lloyd AC. Schwann cells: development and role in nerve repair. Cold Spring Harb Perspect Biol. 2015;7:a020487. DOI:10.1101/cshperspect.a020487
  • Arthur-Farraj PJ, Latouche M, Wilton DK, et al. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron. 2012;75:633–647. DOI:10.1016/j.neuron.2012.06.021
  • Gaudet AD, Popovich PG, Ramer MS. Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. J Neuroinflammation. 2011;8:110. DOI:10.1186/1742-2094-8-72
  • Martini R, Fischer S, Lopez-Vales R, et al. Interactions between Schwann cells and macrophages in injury and inherited demyelinating disease. Glia. 2008;56:1566–1577. DOI:10.1002/glia.20766
  • Hall S. The response to injury in the peripheral nervous system. J Bone Joint Surg Br. 2005;87:1309–1319. DOI:10.1302/0301-620X.87B10.16700
  • Lutz AB, Barres BA. Contrasting the glial response to axon injury in the central and peripheral nervous systems. Dev Cell. 2014;28:7–17. DOI:10.1016/j.devcel.2013.12.002
  • Mokarram N, Merchant A, Mukhatyar V, et al. Effect of modulating macrophage phenotype on peripheral nerve repair. Biomaterials. 2012;33:8793–8801. DOI:10.1016/j.biomaterials.2012.08.050
  • Geuna S, Raimondo S, Ronchi G, et al. Chapter 3: histology of the peripheral nerve and changes occurring during nerve regeneration. Int Rev Neurobiol. 2009;87:27–46. DOI:10.1016/S0074-7742(09)87003-7
  • Borselli C, Storrie H, Benesch-Lee F, et al. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc Natl Acad Sci U S A. 2010;107:3287–3292. DOI:10.1073/pnas.0903875106
  • Clements IP, Kim YT, English AW, et al. Thin-film enhanced nerve guidance channels for peripheral nerve repair. Biomaterials. 2009;30:3834–3846. DOI:10.1016/j.biomaterials.2009.04.022
  • Jain A, Valmikinathan CM, Bellamkonda RV. Peripheral Nerve Regeneration. In: Ducheyne P (ed). Comprehensive Biomaterials. 5. Oxford: Elsevier; 2011:421–434. DOI:10.1016/B978-0-08-055294-1.00183-5
  • Krick K, Tammia M, Martin R, et al. Signaling cue presentation and cell delivery to promote nerve regeneration. Curr Opin Biotechnol. 2011;22:741–746. DOI:10.1016/j.copbio.2011.04.002
  • Hart AM, Terenghi G, Wiberg M. Neuronal death after peripheral nerve injury and experimental strategies for neuroprotection. Neurol Res. 2008;30:999–1011. DOI:10.1179/174313208X362479
  • Konofaos P, Ver Halen JP. Nerve repair by means of tubulization: past, present, future. J Reconstr Microsurg. 2013;29:149–164. DOI:10.1055/s-0032-1333316
  • Itoh S, Takakuda K, Samejima H, et al. Synthetic collagen fibers coated with a synthetic peptide containing the YIGSR sequence of laminin to promote peripheral nerve regeneration in vivo. J Mater Sci Mater Med. 1999;10:129–134.
  • Armstrong SJ, Wiberg M, Terenghi G, et al. ECM molecules mediate both Schwann cell proliferation and activation to enhance neurite outgrowth. Tissue Eng. 2007;13:2863–2870. DOI:10.1089/ten.2007.0055.
  • Patel S, Kurpinski K, Quigley R, et al. Bioactive nanofibers: synergistic effects of nanotopography and chemical signaling on cell guidance. Nano Lett. 2007;7:2122–2128. DOI:10.1021/nl071182z
  • Bell JH, Haycock JW. Next generation nerve guides: materials, fabrication, growth factors, and cell delivery. Tissue Eng Part B Rev. 2012;18:116–128. DOI:10.1089/ten.TEB.2011.0498
  • Hobson MI, Green CJ, Terenghi G. VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy. J Anat. 2000;197(Pt 4):591–605.
  • Emel E, Ergun SS, Kotan D, et al. Effects of insulin-like growth factor-I and platelet-rich plasma on sciatic nerve crush injury in a rat model. J Neurosurg. 2011;114:522–528. DOI:10.3171/2010.9.JNS091928
  • Kokai LE, Bourbeau D, Weber D, et al. Sustained growth factor delivery promotes axonal regeneration in long gap peripheral nerve repair. Tissue Eng Part A. 2011;17:1263–1275. DOI:10.1089/ten.TEA.2010.0507
  • Boyd JG, Gordon T. Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Mol Neurobiol. 2003;27:277–324. DOI:10.1385/MN:27:3:277
  • Strauch B, Rodriguez DM, Diaz J, et al. Autologous Schwann cells drive regeneration through a 6-cm autogenous venous nerve conduit. J Reconstr Microsurg. 2001;17:589–595; discussion 96–97. DOI:10.1055/s-2001-18812
  • Mobasseri A, Faroni A, Minogue BM, et al. Polymer scaffolds with preferential parallel grooves enhance nerve regeneration. Tissue Eng Part A. 2015;21:1152–1162. DOI:10.1089/ten.TEA.2014.0266
  • Zhang F, Blain B, Beck J, et al. Autogenous venous graft with one-stage prepared Schwann cells as a conduit for repair of long segmental nerve defects. J Reconstr Microsurg. 2002;18:295–300. DOI:10.1055/s-2002-30186
  • Hess JR, Brenner MJ, Fox IK, et al. Use of cold-preserved allografts seeded with autologous Schwann cells in the treatment of a long-gap peripheral nerve injury. Plast Reconstr Surg. 2007;119:246–259. DOI:10.1097/01.prs.0000245341.71666.97
  • Ruff RL, McKerracher L, Selzer ME. Repair and neurorehabilitation strategies for spinal cord injury. Ann N Y Acad Sci. 2008;1142:1–20. DOI:10.1196/annals.1444.004
  • Anitua E, Pelacho B, Prado R, et al. Infiltration of plasma rich in growth factors enhances in vivo angiogenesis and improves reperfusion and tissue remodeling after severe hind limb ischemia. J Control Release. 2015;202:31–39. DOI:10.1016/j.jconrel.2015.01.029
  • Schaakxs D, Kalbermatten DF, Raffoul W, et al. Regenerative cell injection in denervated muscle reduces atrophy and enhances recovery following nerve repair. Muscle Nerve. 2013;47:691–701. DOI:10.1002/mus.23662
  • Dodla M, Bellamkond R. Peripheral nerve regeneration. In: Atala A, editor. Foundations of Regenerative Medicine: Clinical & Therapeutic Applications. Burlington: Academic Press; 2009:672–687.
  • Sondell M, Lundborg G, Kanje M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci. 1999;19:5731–5740.
  • Ray WZ, Mackinnon SE. Management of nerve gaps: autografts, allografts, nerve transfers, and end-to-side neurorrhaphy. Exp Neurol. 2010;223:77–85. DOI:10.1016/j.expneurol.2009.03.031
  • Wang Y, Jia H, Li WY, et al. Synergistic effects of bone mesenchymal stem cells and chondroitinase ABC on nerve regeneration after acellular nerve allograft in rats. Cell Mol Neurobiol. 2012;32:361–371. DOI:10.1007/s10571-011-9764-4
  • di Summa PG, Kingham PJ, Raffoul W, et al. Adipose-derived stem cells enhance peripheral nerve regeneration. J Plast Reconstr Aesthet Surg. 2010;63:1544–1552. DOI:10.1016/j.bjps.2009.09.012
  • Hutchison N, Fligny C, Duffield JS. Resident mesenchymal cells and fibrosis. Biochim Biophys Acta. 2013;1832:962–971. DOI:10.1016/j.bbadis.2012.11.015
  • Ceccarelli J, Putnam AJ. Sculpting the blank slate: how fibrin’s support of vascularization can inspire biomaterial design. Acta Biomater. 2014;10:1515–1523. DOI:10.1016/j.actbio.2013.07.043
  • Gessmann J, Seybold D, Peter E, et al. Alignment of the fibrin network within an autologous plasma clot. Tissue Eng Part C Methods. 2016;22:30–37. DOI:10.1089/ten.tec.2015.0207
  • Janmey PA, Winer JP, Weisel JW. Fibrin gels and their clinical and bioengineering applications. J R Soc Interface. 2009;6:1–10. DOI:10.1098/rsif.2008.0327
  • Martino MM, Briquez PS, Guc E, et al. Growth factors engineered for super-affinity to the extracellular matrix enhance tissue healing. Science. 2014;343:885–888. DOI:10.1126/science.1247663
  • Brown AC, Barker TH. Fibrin-based biomaterials: modulation of macroscopic properties through rational design at the molecular level. Acta Biomater. 2014;10:1502–1514. DOI:10.1016/j.actbio.2013.09.008
  • Wood MD, Moore AM, Hunter DA, et al. Affinity-based release of glial-derived neurotrophic factor from fibrin matrices enhances sciatic nerve regeneration. Acta Biomater. 2009;5:959–968. DOI:10.1016/j.actbio.2008.11.008
  • Dalamagkas K, Tsintou M, Seifalian A. Advances in peripheral nervous system regenerative therapeutic strategies: a biomaterials approach. Mater Sci Eng C Mater Biol Appl. 2016;65:425–432. DOI:10.1016/j.msec.2016.04.048
  • Mosahebi A, Fuller P, Wiberg M, et al. Effect of allogeneic Schwann cell transplantation on peripheral nerve regeneration. Exp Neurol. 2002;173:213–223. DOI:10.1006/exnr.2001.7846
  • Cheng HL, Russell JW, Feldman EL. IGF-I promotes peripheral nervous system myelination. Ann N Y Acad Sci. 1999;883:124–130.
  • Hoffman-Kim D, Mitchel JA, Bellamkonda RV. Topography, cell response, and nerve regeneration. Annu Rev Biomed Eng. 2010;12:203–231. DOI:10.1146/annurev-bioeng-070909-105351
  • Kalbermatten DF, Erba P, Mahay D, et al. Schwann cell strip for peripheral nerve repair. J Hand Surg Eur Vol. 2008;33:587–594. DOI:10.1177/1753193408090755
  • Madduri S, Gander B. Schwann cell delivery of neurotrophic factors for peripheral nerve regeneration. J Peripher Nerv Syst. 2010;15:93–103. DOI:10.1111/j.1529-8027.2010.00257.x
  • Schlosshauer B, Muller E, Schroder B, et al. Rat Schwann cells in bioresorbable nerve guides to promote and accelerate axonal regeneration. Brain Res. 2003;963:321–326.
  • Zurita M, Otero L, Aguayo C, et al. Cell therapy for spinal cord repair: optimization of biologic scaffolds for survival and neural differentiation of human bone marrow stromal cells. Cytotherapy. 2010;12:522–537. DOI:10.3109/14653241003615164
  • Vaquero J, Otero L, Bonilla C, et al. Cell therapy with bone marrow stromal cells after intracerebral hemorrhage: impact of platelet-rich plasma scaffolds. Cytotherapy. 2013;15:33–43. DOI:10.1016/j.jcyt.2012.10.005
  • Cho HH, Jang S, Lee SC, et al. Effect of neural-induced mesenchymal stem cells and platelet-rich plasma on facial nerve regeneration in an acute nerve injury model. Laryngoscope. 2010;120:907–913. DOI:10.1002/lary.20860
  • 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. DOI:10.1016/j.jcyt.2013.04.004
  • Ye F, Li H, Qiao G, et al. Platelet-rich plasma gel in combination with Schwann cells for repair of sciatic nerve injury. Neural Regen Res. 2012;7:2286.
  • de Winter F, Hoyng S, Tannemaat M, et al. Gene therapy approaches to enhance regeneration of the injured peripheral nerve. Eur J Pharmacol. 2013;719:145–152. DOI:10.1016/j.ejphar.2013.04.057
  • Hoyng SA, De Winter F, Gnavi S, et al. A comparative morphological, electrophysiological and functional analysis of axon regeneration through peripheral nerve autografts genetically modified to overexpress BDNF, CNTF, GDNF, NGF, NT3 or VEGF. Exp Neurol. 2014;261:578–593. DOI:10.1016/j.expneurol.2014.08.002
  • Sandquist EJ, Uz M, Sharma AD, et al. Stem Cells, Bioengineering, and 3-D Scaffolds for Nervous System Repair and Regeneration. In: Zhang LG, Kaplan DL, (eds). Neural Engineering: From Advanced Biomaterials to 3D Fabrication Techniques. Cham: Springer International Publishing; 2016. p. 25–81. DOI:10.1007/978-3-319-31433-4_2
  • Hoyng SA, de Winter F, Tannemaat MR, et al. Gene therapy and peripheral nerve repair: a perspective. Front Mol Neurosci. 2015;8:32. DOI:10.3389/fnmol.2015.00032
  • Sanchez M, Anitua E, Orive G, et al. Platelet-rich therapies in the treatment of orthopaedic sport injuries. Sports Med. 2009;39:345–354.
  • Anitua E, Alkhraisat MH, Orive G. Perspectives and challenges in regenerative medicine using plasma rich in growth factors. J Control Release. 2012;157:29–38. DOI:10.1016/j.jconrel.2011.07.004
  • Anitua E, Zalduendo MM, Prado R, et al. Morphogen and proinflammatory cytokine release kinetics from PRGF-Endoret fibrin scaffolds: evaluation of the effect of leukocyte inclusion. J Biomed Mater Res A. 2015;103:1011–1020. DOI:10.1002/jbm.a.35244
  • Shworak N. Heparan Sulfate. In: Aird W, editor. Endothelial Biomedicine. New York: Cambridge University Press; 2007:947–959.
  • Sanchez M, Anitua E, Delgado D, et al. A new strategy to tackle severe knee osteoarthritis: combination of intra-articular and intraosseous injections of platelet rich plasma. Expert Opin Biol Ther. 2016;16:627–643. DOI:10.1517/14712598.2016.1157162
  • Scala M, Mereu P, Spagnolo F, et al. The use of platelet-rich plasma gel in patients with mixed tumour undergoing superficial parotidectomy: a randomized study. Vivo. 2014;28:121–124.
  • Anitua E, Prado R, Orive G. Endogenous morphogens and fibrin bioscaffolds for stem cell therapeutics. Trends Biotechnol. 2013;31:364–374. DOI:10.1016/j.tibtech.2013.04.003
  • Kuffler DP, Reyes O, Sosa IJ, et al. Neurological recovery across a 12-cm-long ulnar nerve gap repaired 3.25 years post trauma: case report. Neurosurgery. 2011;69:E1321–e1326. DOI:10.1227/NEU.0b013e31822a9fd2 .
  • Sabongi RG, De Rizzo LALM, Fernandes M, et al. Nerve regeneration: is there an alternative to nervous graft? J Reconstr Microsurg. 2014;30:607–616. DOI:10.1055/s-0034-1372477
  • Hibner M, Castellanos ME, Drachman D, et al. Repeat operation for treatment of persistent pudendal nerve entrapment after pudendal neurolysis. J Minim Invasive Gynecol. 2012;19:325–330. DOI:10.1016/j.jmig.2011.12.022
  • Wu CC, Wu YN, Ho HO, et al. The neuroprotective effect of platelet-rich plasma on erectile function in bilateral cavernous nerve injury rat model. J Sex Med. 2012;9:2838–2848. DOI:10.1111/j.1743-6109.2012.02881.x
  • Anitua E, Pascual C, Antequera D, et al. Plasma rich in growth factors (PRGF-Endoret) reduces neuropathologic hallmarks and improves cognitive functions in an Alzheimer’s disease mouse model. Neurobiol Aging. 2014;35:1582–1595. DOI:10.1016/j.neurobiolaging.2014.01.009
  • Kim JY, Jeon WJ, Kim DH, et al. An inside-out vein graft filled with platelet-rich plasma for repair of a short sciatic nerve defect in rats. Neural Regen Res. 2014;9:1351–1357. DOI:10.4103/1673-5374.137587
  • Takeuchi M, Kamei N, Shinomiya R, et al. Human platelet-rich plasma promotes axon growth in brain-spinal cord coculture. Neuroreport. 2012;23:712–716. DOI:10.1097/WNR.0b013e3283567196
  • Kaplan S, Piskin A, Ayyildiz M, et al. The effect of melatonin and platelet gel on sciatic nerve repair: an electrophysiological and stereological study. Microsurgery. 2011;31:306–313. DOI:10.1002/micr.20876
  • Farrag TY, Lehar M, Verhaegen P, et al. Effect of platelet rich plasma and fibrin sealant on facial nerve regeneration in a rat model. Laryngoscope. 2007;117:157–165. DOI:10.1097/01.mlg.0000249726.98801.77
  • Sariguney Y, Yavuzer R, Elmas C, et al. Effect of platelet-rich plasma on peripheral nerve regeneration. J Reconstr Microsurg. 2008;24:159–167. DOI:10.1055/s-2008-1076752
  • Park GY, Kwon DR. Platelet-rich plasma limits the nerve injury caused by 10% dextrose in the rabbit median nerve. Muscle Nerve. 2014;49:56–60. DOI:10.1002/mus.23863
  • Alcaraz J, Oliver A, Sanchez JM. Platelet-rich plasma in a patient with cerebral palsy. Am J Case Rep. 2015;16:469–472. DOI:10.12659/AJCR.893805
  • Anitua E, Prado R, Azkargorta M, et al. High-throughput proteomic characterization of plasma rich in growth factors (PRGF-Endoret)-derived fibrin clot interactome. J Tissue Eng Regen Med. 2015;9:E1–E12. DOI:10.1002/term.1721
  • Jiang H, Qu W, Li Y, et al. Platelet-derived growth factors-BB and fibroblast growth factors-base induced proliferation of Schwann cells in a 3D environment. Neurochem Res. 2013;38:346–355. DOI:10.1007/s11064-012-0925-8
  • Luo H, Zhang Y, Zhang Z, et al. The protection of MSCs from apoptosis in nerve regeneration by TGFβ1 through reducing inflammation and promoting VEGF-dependent angiogenesis. Biomaterials. 2012;33:4277–4287. DOI:10.1016/j.biomaterials.2012.02.042.
  • Lee AC, Yu VM, Lowe JB 3rd, et al. Controlled release of nerve growth factor enhances sciatic nerve regeneration. Exp Neurol. 2003;184:295–303.
  • Rao SN, Pearse DD. Regulating axonal responses to injury: the intersection between signaling pathways involved in axon myelination and the inhibition of axon regeneration. Front Mol Neurosci. 2016;9:33. DOI:10.3389/fnmol.2016.00098
  • Yokota K, Ishida O, Sunagawa T, et al. Platelet-rich plasma accelerated surgical angio-genesis in vascular-implanted necrotic bone: an experimental study in rabbits. Acta Orthop. 2008;79:106–110. DOI:10.1080/17453670710014842
  • Bosch G, Moleman M, Barneveld A, et al. The effect of platelet-rich plasma on the neovascularization of surgically created equine superficial digital flexor tendon lesions. Scand J Med Sci Sports. 2011;21:554–561. DOI:10.1111/j.1600-0838.2009.01070.x
  • Sanchez M, Anitua E, Azofra J, et al. Ligamentization of tendon grafts treated with an endogenous preparation rich in growth factors: gross morphology and histology. Arthroscopy. 2010;26:470–480. DOI:10.1016/j.arthro.2009.08.019
  • Hall H. Modified fibrin hydrogel matrices: both, 3D-scaffolds and local and controlled release systems to stimulate angiogenesis. Curr Pharm Des. 2007;13:3597–3607.
  • Lichtenfels M, Colome L, Sebben AD, et al. Effect of platelet rich plasma and platelet rich fibrin on sciatic nerve regeneration in a rat model. Microsurgery. 2013;33:383–390. DOI:10.1002/micr.22105
  • Renn TY, Kao YH, Wang CC, et al. Anti-inflammatory effects of platelet biomaterials in a macrophage cellular model. Vox Sang. 2015. DOI:10.1111/vox.12264
  • Vasina EM, Cauwenberghs S, Feijge MA, et al. Microparticles from apoptotic platelets promote resident macrophage differentiation. Cell Death Dis. 2011;2:e211. DOI:10.1038/cddis.2011.82
  • Coudriet GM, He J, Trucco M, et al. Hepatocyte growth factor modulates interleukin-6 production in bone marrow derived macrophages: implications for inflammatory mediated diseases. PLoS One. 2010;5:e15384. DOI:10.1371/journal.pone.0015384
  • Ma CH, Omura T, Cobos EJ, et al. Accelerating axonal growth promotes motor recovery after peripheral nerve injury in mice. J Clin Invest. 2011;121:4332–4347. DOI:10.1172/JCI58675
  • Shavlakadze T, White JD, Davies M, et al. Insulin-like growth factor I slows the rate of denervation induced skeletal muscle atrophy. Neuromuscul Disord. 2005;15:139–146. DOI:10.1016/j.nmd.2004.10.013
  • Sulaiman OA, Gordon T. Transforming growth factor-beta and forskolin attenuate the adverse effects of long-term Schwann cell denervation on peripheral nerve regeneration in vivo. Glia. 2002;37:206–218.
  • Akassoglou K, Yu WM, Akpinar P, et al. Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron. 2002;33:861–875.
  • Akassoglou K, Akpinar P, Murray S, et al. Fibrin is a regulator of Schwann cell migration after sciatic nerve injury in mice. Neurosci Lett. 2003;338:185–188.
  • Chernousov MA, Carey DJ. alphaVbeta8 integrin is a Schwann cell receptor for fibrin. Exp Cell Res. 2003;291:514–524.
  • Martino MM, Briquez PS, Ranga A, et al. Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc Natl Acad Sci U S A. 2013;110:4563–4568. DOI:10.1073/pnas.1221602110.
  • Akassoglou K, Kombrinck KW, Degen JL, et al. Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury. J Cell Biol. 2000;149:1157–1166.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.