Peripheral nerve regeneration: Experimental strategies and future perspectives

Advanced Drug Delivery Reviews

Volumn 82, Issue , 2015, Pages 160-167

  Faroni, Alessandro ^a   Mobasseri, S Atefeh ^a,b   Kingham, Paul J ^c   Reid, Adam J ^a,d  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UMEÅ UNIVERSITY   (Sweden)

^d MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Muscle denervation; Neuronal survival; Peripheral nerve regeneration; Reinnervation; Scaffold; Stem cell

Indexed keywords

CYTOLOGY; SCAFFOLDS; SCAFFOLDS (BIOLOGY); STEM CELLS;

AXONAL REGENERATION; CELL BASED THERAPIES; DENERVATION; EXPERIMENTAL STRATEGY; NERVE TISSUE ENGINEERING; NEURONAL SURVIVAL; PERIPHERAL NERVE REGENERATION; REINNERVATION;

CELL ENGINEERING;

AGENTS ACTING ON THE PERIPHERAL NERVOUS AND NEUROMUSCULAR SYSTEMS; GROWTH FACTOR;

CELL SURVIVAL; EXPERIMENTAL STUDY; HUMAN; MUSCLE REGENERATION; NERVE CELL LESION; NERVE FIBER REGENERATION; NERVE REGENERATION; NEUROBIOLOGY; NEUROMUSCULAR DISEASE; NONHUMAN; PERIKARYON; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; REINNERVATION; REVIEW; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TISSUE SCAFFOLD; TREATMENT RESPONSE; ANIMAL; DRUG EFFECTS; PATHOPHYSIOLOGY; PERIPHERAL NERVE INJURIES; PHYSIOLOGY; PROCEDURES; TISSUE REGENERATION; TRENDS;

ANIMALS; GUIDED TISSUE REGENERATION; HUMANS; NERVE REGENERATION; PERIPHERAL NERVE INJURIES; TISSUE ENGINEERING;

EID: 84927129591     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.11.010     Document Type: Review

References (130)

1. Brushart T.M. Nerve repair 2011, Oxford University Press, New York; Oxford.
2. Millesi H. Bridging defects: autologous nerve grafts. Acta Neurochir. 2007, 100:37-38. (Supplement).
3. Jivan S., Kumar N., Wiberg M., Kay S. The influence of pre-surgical delay on functional outcome after reconstruction of brachial plexus injuries. J. Plast. Reconstr. Aesthet. Surg. 2009, 62:472-479.
4. Gordon T., Tyreman N., Raji M.A. The basis for diminished functional recovery after delayed peripheral nerve repair. J. Neurosci. Off. J. Soc. Neurosci. 2011, 31:5325-5334.
5. Lundborg G. A 25-year perspective of peripheral nerve surgery: evolving neuroscientific concepts and clinical significance. J. Hand Ther. 2000, 25:391-414.
6. Dahlin L.B. The biology of nerve injury and repair. J. Am. Soc Surg. Hand 2004, 4:143-155.
7. McKay Hart A., Brannstrom T., Wiberg M., Terenghi G. Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat: timecourse of cell death and elimination. Exp. Brain Res. 2002, 142:308-318.
8. Groves M.J., Christopherson T., Giometto B., Scaravilli F. Axotomy-induced apoptosis in adult rat primary sensory neurons. J. Neurocytol. 1997, 26:615-624.
9. Chen Z.L., Yu W.M., Strickland S. Peripheral regeneration. Annu. Rev. Neurosci. 2007, 30:209-233.
10. Geuna S., Raimondo S., Ronchi G., Di Scipio F., Tos P., Czaja K., Fornaro M. Chapter 3: histology of the peripheral nerve and changes occurring during nerve regeneration. Int. Rev. Neurobiol. 2009, 87:27-46.
11. Clarke D., Richardson P. Peripheral nerve injury. Curr. Opin. Neurol. 1994, 7:415-421.
12. Makwana M., Raivich G. Molecular mechanisms in successful peripheral regeneration. FEBS J. 2005, 272:2628-2638.
13. Berdan R.C., Easaw J.C., Wang R. Alterations in membrane potential after axotomy at different distances from the soma of an identified neuron and the effect of depolarization on neurite outgrowth and calcium channel expression. J. Neurophysiol. 1993, 69:151-164.
14. Zheng J.Q., Kelly T.K., Chang B., Ryazantsev S., Rajasekaran A.K., Martin K.C., Twiss J.L. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J. Neurosci. Off. J. Soc. Neurosci. 2001, 21:9291-9303.
15. Reid A.J., Shawcross S.G., Hamilton A.E., Wiberg M., Terenghi G. N-acetylcysteine alters apoptotic gene expression in axotomised primary sensory afferent subpopulations. Neurosci. Res. 2009, 65:148-155.
16. Terenghi G., Hart A., Wiberg M. The nerve injury and the dying neurons: diagnosis and prevention. J. Hand. Surg. Eur. Vol. 2011, 36:730-734.
17. Calenda G., Strong T.D., Pavlovich C.P., Schaeffer E.M., Burnett A.L., Yu W., Davies K.P., Bivalacqua T.J. Whole genome microarray of the major pelvic ganglion after cavernous nerve injury: new insights into molecular profile changes after nerve injury. BJU Int. 2012, 109:1552-1564.
18. Burnett M.G., Zager E.L. Pathophysiology of peripheral nerve injury: a brief review. Neurosurg. Focus. 2004, 16:E1.
19. Ide C. Peripheral nerve regeneration. Neurosci. Res. 1996, 25:101-121.
20. Griffin J.W., Hogan M.V., Chhabra A.B., Deal D.N. Peripheral nerve repair and reconstruction. J. Bone Joint Surg. Am. 2013, 95:2144-2151.
21. Jessen K.R., Mirsky R. Negative regulation of myelination: relevance for development, injury, and demyelinating disease. Glia 2008, 56:1552-1565.
22. Scheib J., Hoke A. Advances in peripheral nerve regeneration. Nat. Rev. Neurol. 2013, 9:668-676.
23. Allodi I., Udina E., Navarro X. Specificity of peripheral nerve regeneration: interactions at the axon level. Prog. Neurobiol. 2012, 98:16-37.
24. Gutmann E. Denervation and disuse atrophy in crosstriated muscle. Rev. Can. Biol. 1962, 21:353-365.
25. Hart A.M., Terenghi G., Wiberg M. Neuronal death after peripheral nerve injury and experimental strategies for neuroprotection. Neurol. Res. 2008, 30:999-1011.
26. McArthur J.C., Yiannoutsos C., Simpson D.M., Adornato B.T., Singer E.J., Hollander H., Marra C., Rubin M., Cohen B.A., Tucker T., Navia B.A., Schifitto G., Katzenstein D., Rask C., Zaborski L., Smith M.E., Shriver S., Millar L., Clifford D.B., Karalnik I.J. A phase II trial of nerve growth factor for sensory neuropathy associated with HIV infection. AIDS Clinical Trials Group Team 291. Neurology 2000, 54:1080-1088.
27. Novikova L.N., Novikov L.N., Kellerth J.O. BDNF abolishes the survival effect of NT-3 in axotomized Clarke neurons of adult rats. J. Comp. Neurol. 2000, 428:671-680.
28. Hart A.M., Terenghi G., Kellerth J.O., Wiberg M. Sensory neuroprotection, mitochondrial preservation, and therapeutic potential of N-acetyl-cysteine after nerve injury. Neuroscience 2004, 125:91-101.
29. Wilson A.D., Hart A., Brannstrom T., Wiberg M., Terenghi G. Primary sensory neuronal rescue with systemic acetyl-l-carnitine following peripheral axotomy. A dose-response analysis. Br. J. Plast. Surg. 2003, 56:732-739.
30. Zhang C.G., Welin D., Novikov L., Kellerth J.O., Wiberg M., Hart A.M. Motorneuron protection by N-acetyl-cysteine after ventral root avulsion and ventral rhizotomy. Br. J. Plast. Surg. 2005, 58:765-773.
31. Hlaing S.M., Garcia L.A., Kovanecz I., Martinez R.A., Shah S., Artaza J.N., Ferrini M.G. Sildenafil promotes neuroprotection of the pelvic ganglia neurones after bilateral cavernosal nerve resection in the rat. BJU Int. 2013, 111:159-170.
32. Reid A.J., Sun M., Wiberg M., Downes S., Terenghi G., Kingham P.J. Nerve repair with adipose-derived stem cells protects dorsal root ganglia neurons from apoptosis. Neuroscience 2011, 199:515-522.
33. Schlosshauer B., Dreesmann L., Schaller H.E., Sinis N. Synthetic nerve guide implants in humans: a comprehensive survey. Neurosurgery 2006, 59:740-747. (discussion 747-748).
34. Evans G.R.D. Peripheral nerve injury: a review and approach to tissue engineered constructs. Anat. Rec. 2001, 263:396-404.
35. Wang P.-H., Tseng I.L., Hsu S.-h. Review: bioengineering approaches for guided peripheral nerve regeneration. J. Med. Biol. Eng. 2011, 31:151-159.
36. Pabari A., Lloyd-Hughes H., Seifalian A.M., Mosahebi A. Nerve conduits for peripheral nerve surgery. Plast. Reconstr. Surg. 2014, 133:1420-1430.
37. Gu X., Ding F., Williams D.F. Neural tissue engineering options for peripheral nerve regeneration. Biomaterials 2014, 35:6143-6156.
38. Curtis A., Wilkinson C. Topographical control of cells. Biomaterials 1997, 18:1573-1583.
39. Bell J.H., Haycock J.W. Next generation nerve guides: materials, fabrication, growth factors, and cell delivery. Tissue Eng. B Rev. 2012, 18:116-128.
40. Daud M.F., Pawar K.C., Claeyssens F., Ryan A.J., Haycock J.W. An aligned 3D neuronal-glial co-culture model for peripheral nerve studies. Biomaterials 2012, 33:5901-5913.
41. Mobasseri S.A., Terenghi G., Downes S. Micro-structural geometry of thin films intended for the inner lumen of nerve conduits affects nerve repair. J. Mater. Sci. Mater. Med. 2013, 24:1639-1647.
42. Sun M., McGowan M., Kingham P.J., Terenghi G., Downes S. Novel thin-walled nerve conduit with microgrooved surface patterns for enhanced peripheral nerve repair. J. Mater. Sci. Mater. Med. 2010, 21:2765-2774.
43. Hersel U., Dahmen C., Kessler H. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 2003, 24:4385-4415.
44. de Luca A.C., Terenghi G., Downes S. Chemical surface modification of poly-epsilon-caprolactone improves Schwann cell proliferation for peripheral nerve repair. J. Tissue Eng. Regen. Med. 2014, 8:153-163.
45. Armstrong S.J., Wiberg M., Terenghi G., Kingham P.J. ECM molecules mediate both Schwann cell proliferation and activation to enhance neurite outgrowth. Tissue Eng. 2007, 13:2863-2870.
46. Santos X., Rodrigo J., Hontanilla B., Bilbao G. Evaluation of peripheral nerve regeneration by nerve growth factor locally administered with a novel system. J. Neurosci. Methods 1998, 85:119-127.
47. Rich K.M., Alexander T.D., Pryor J.C., Hollowell J.P. Nerve growth factor enhances regeneration through silicone chambers. Exp. Neurol. 1989, 105:162-170.
48. Derby A., Engleman V.W., Frierdich G.E., Neises G., Rapp S.R., Roufa D.G. Nerve growth factor facilitates regeneration across nerve gaps: morphological and behavioral studies in rat sciatic nerve. Exp. Neurol. 1993, 119:176-191.
49. Utley D.S., Lewin S.L., Cheng E.T., Verity A.N., Sierra D., Terris D.J. Brain-derived neurotrophic factor and collagen tubulization enhance functional recovery after peripheral nerve transection and repair. Arch. Otolaryngol. Head Neck Surg. 1996, 122:407-413.
50. Sahenk Z., Seharaseyon J., Mendell J.R. CNTF potentiates peripheral nerve regeneration. Brain Res. 1994, 655:246-250.
51. Lewin S.L., Utley D.S., Cheng E.T., Verity A.N., Terris D.J. Simultaneous treatment with BDNF and CNTF after peripheral nerve transection and repair enhances rate of functional recovery compared with BDNF treatment alone. Laryngoscope 1997, 107:992-999.
52. Ho P.R., Coan G.M., Cheng E.T., Niell C., Tarn D.M., Zhou H., Sierra D., Terris D.J. Repair with collagen tubules linked with brain-derived neurotrophic factor and ciliary neurotrophic factor in a rat sciatic nerve injury model. Arch. Otolaryngol. Head Neck Surg. 1998, 124:761-766.
53. Kanje M., Skottner A., Sjoberg J., Lundborg G. Insulin-like growth factor I (IGF-I) stimulates regeneration of the rat sciatic nerve. Brain Res. 1989, 486:396-398.
54. Fujimoto E., Mizoguchi A., Hanada K., Yajima M., Ide C. Basic fibroblast growth factor promotes extension of regenerating axons of peripheral nerve. In vivo experiments using a Schwann cell basal lamina tube model. J. Neurocytol. 1997, 26:511-528.
55. Fine E.G., Decosterd I., Papaloizos M., Zurn A.D., Aebischer P. GDNF and NGF released by synthetic guidance channels support sciatic nerve regeneration across a long gap. Eur. J. NeuroSci. 2002, 15:589-601.
56. Danielsen N., Pettmann B., Vahlsing H.L., Manthorpe M., Varon S. Fibroblast growth factor effects on peripheral nerve regeneration in a silicone chamber model. J. Neurosci. Res. 1988, 20:320-330.
57. La Marca R., Cerri F., Horiuchi K., Bachi A., Feltri M.L., Wrabetz L., Blobel C.P., Quattrini A., Salzer J.L., Taveggia C. TACE (ADAM17) inhibits Schwann cell myelination. Nat. Neurosci. 2011, 14:857-865.
58. Boyd J.G., Gordon T. A dose-dependent facilitation and inhibition of peripheral nerve regeneration by brain-derived neurotrophic factor. Eur. J. NeuroSci. 2002, 15:613-626.
59. Boyd J.G., Gordon T. The neurotrophin receptors, trkB and p75, differentially regulate motor axonal regeneration. J. Neurobiol. 2001, 49:314-325.
60. Magnaghi V., Procacci P., Tata A.M. Chapter 15: novel pharmacological approaches to Schwann cells as neuroprotective agents for peripheral nerve regeneration. Int. Rev. Neurobiol. 2009, 87:295-315.
61. Zeng W., Rong M., Hu X., Xiao W., Qi F., Huang J., Luo Z. Incorporation of Chitosan Microspheres into Collagen-Chitosan Scaffolds for the Controlled Release of Nerve Growth Factor. PLoS ONE 2014, 9:e101300.
62. Melcangi R.C., Cavarretta I.T., Ballabio M., Leonelli E., Schenone A., Azcoitia I., Miguel Garcia-Segura L., Magnaghi V. Peripheral nerves: a target for the action of neuroactive steroids, Brain research. Brain Res. Rev. 2005, 48:328-338.
63. Faroni A., Magnaghi V. The neurosteroid allopregnanolone modulates specific functions in central and peripheral glial cells. Front. Endocrinol. 2011, 2:103.
64. Mercier G., Turque N., Schumacher M. Rapid effects of triiodothyronine on immediate-early gene expression in Schwann cells. Glia 2001, 35:81-89.
65. Devesa P., Gelabert M., Gonzlez-Mosquera T., Gallego R., Relova J.L., Devesa J., Arce V.M. Growth hormone treatment enhances the functional recovery of sciatic nerves after transection and repair. Muscle Nerve 2012, 45:385-392.
66. Magnaghi V., Ballabio M., Camozzi F., Colleoni M., Consoli A., Gassmann M., Lauria G., Motta M., Procacci P., Trovato A.E., Bettler B. Altered peripheral myelination in mice lacking GABAB receptors. Mol. Cell. Neurosci. 2008, 37:599-609.
67. Faroni A., Smith R.J., Procacci P., Castelnovo L.F., Puccianti E., Reid A.J., Magnaghi V., Verkhratsky A. Purinergic signaling mediated by P2X receptors controls myelination in sciatic nerves. J. Neurosci. Res. 2014, 92(10):1259-1269.
68. Faroni A., Castelnovo L.F., Procacci P., Caffino L., Fumagalli F., Melfi S., Gambarotta G., Bettler B., Wrabetz L., Magnaghi V. Deletion of GABA-B receptor in Schwann cells regulates remak bundles and small nociceptive C-fibers. Glia 2014, 62:548-565.
69. Guenard V., Kleitman N., Morrissey T.K., Bunge R.P., Aebischer P. Syngeneic Schwann cells derived from adult nerves seeded in semipermeable guidance channels enhance peripheral nerve regeneration. J. Neurosci. Off. J. Soc. Neurosci. 1992, 12:3310-3320.
70. Kalbermatten D.F., Erba P., Mahay D., Wiberg M., Pierer G., Terenghi G. Schwann cell strip for peripheral nerve repair. J. Hand. Surg. Eur. Vol. 2008, 33:587-594.
71. Mosahebi A., Fuller P., Wiberg M., Terenghi G. Effect of allogeneic Schwann cell transplantation on peripheral nerve regeneration. Exp. Neurol. 2002, 173:213-223.
72. Mosahebi A., Woodward B., Wiberg M., Martin R., Terenghi G. Retroviral labeling of Schwann cells: in vitro characterization and in vivo transplantation to improve peripheral nerve regeneration. Glia 2001, 34:8-17.
73. Dombrowski M.A., Sasaki M., Lankford K.L., Kocsis J.D., Radtke C. Myelination and nodal formation of regenerated peripheral nerve fibers following transplantation of acutely prepared olfactory ensheathing cells. Brain Res. 2006, 1125:1-8.
74. Radtke C., Vogt P.M. Peripheral nerve regeneration: a current perspective. Eplasty 2009, 9:e47.
75. Tohill M., Terenghi G. Stem-cell plasticity and therapy for injuries of the peripheral nervous system. Biotechnol. Appl. Biochem. 2004, 40:17-24.
76. Cui L., Jiang J., Wei L., Zhou X., Fraser J.L., Snider B.J., Yu S.P. Transplantation of embryonic stem cells improves nerve repair and functional recovery after severe sciatic nerve axotomy in rats. Stem Cells 2008, 26:1356-1365.
77. Ziegler L., Grigoryan S., Yang I.H., Thakor N.V., Goldstein R.S. Efficient generation of Schwann cells from human embryonic stem cell-derived neurospheres. Stem Cell Rev. 2011, 7:394-403.
78. Guo B.F., Dong M.M. Application of neural stem cells in tissue-engineered artificial nerve. Otolaryngol. Head Neck Surg. 2009, 140:159-164.
79. Xiong Y., Zeng Y.S., Zeng C.G., Du B.L., He L.M., Quan D.P., Zhang W., Wang J.M., Wu J.L., Li Y., Li J. Synaptic transmission of neural stem cells seeded in 3-dimensional PLGA scaffolds. Biomaterials 2009, 30:3711-3722.
80. Shi Y., Zhou L., Tian J., Wang Y. Transplantation of neural stem cells overexpressing glia-derived neurotrophic factor promotes facial nerve regeneration. Acta Otolaryngol. 2009, 129:906-914.
81. Heine W., Conant K., Griffin J.W., Hoke A. Transplanted neural stem cells promote axonal regeneration through chronically denervated peripheral nerves. Exp. Neurol. 2004, 189:231-240.
82. Ikeda M., Uemura T., Takamatsu K., Okada M., Kazuki K., Tabata Y., Ikada Y., Nakamura H. Acceleration of peripheral nerve regeneration using nerve conduits in combination with induced pluripotent stem cell technology and a basic fibroblast growth factor drug delivery system. J. Biomed. Mater. Res. A 2014, 102:1370-1378.
83. Kreitzer F.R., Salomonis N., Sheehan A., Huang M., Park J.S., Spindler M.J., Lizarraga P., Weiss W.A., So P.L., Conklin B.R. A robust method to derive functional neural crest cells from human pluripotent stem cells. Am. J. Stem Cells 2013, 2:119-131.
84. Lee G., Chambers S.M., Tomishima M.J., Studer L. Derivation of neural crest cells from human pluripotent stem cells. Nat. Protoc. 2010, 5:688-701.
85. Wakao S., Hayashi T., Kitada M., Kohama M., Matsue D., Teramoto N., Ose T., Itokazu Y., Koshino K., Watabe H., Iida H., Takamoto T., Tabata Y., Dezawa M. Long-term observation of auto-cell transplantation in non-human primate reveals safety and efficiency of bone marrow stromal cell-derived Schwann cells in peripheral nerve regeneration. Exp. Neurol. 2010, 223:537-547.
86. di Summa P.G., Kalbermatten D.F., Pralong E., Raffoul W., Kingham P.J., Terenghi G. Long-term in vivo regeneration of peripheral nerves through bioengineered nerve grafts. Neuroscience 2011, 181:278-291.
87. Matsuse D., Kitada M., Kohama M., Nishikawa K., Makinoshima H., Wakao S., Fujiyoshi Y., Heike T., Nakahata T., Akutsu H., Umezawa A., Harigae H., Kira J., Dezawa M. Human umbilical cord-derived mesenchymal stromal cells differentiate into functional Schwann cells that sustain peripheral nerve regeneration. J. Neuropathol. Exp. Neurol. 2010, 69:973-985.
88. McKenzie I.A., Biernaskie J., Toma J.G., Midha R., Miller F.D. Skin-derived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J. Neurosci. Off. J. Soc. Neurosci. 2006, 26:6651-6660.
89. Martens W., Sanen K., Georgiou M., Struys T., Bronckaers A., Ameloot M., Phillips J., Lambrichts I. Human dental pulp stem cells can differentiate into Schwann cells and promote and guide neurite outgrowth in an aligned tissue-engineered collagen construct in vitro. FEBS J. 2014, 28:1634-1643.
90. Barry F.P., Murphy J.M. Mesenchymal stem cells: clinical applications and biological characterization. Int. J. Biochem. Cell Biol. 2004, 36:568-584.
91. Bajada S., Mazakova I., Richardson J.B., Ashammakhi N. Updates on stem cells and their applications in regenerative medicine. J. Tissue Eng. Regen. Med. 2008, 2:169-183.
92. Garcia-Castro J., Trigueros C., Madrenas J., Perez-Simon J.A., Rodriguez R., Menendez P. Mesenchymal stem cells and their use as cell replacement therapy and disease modelling tool. J. Cell. Mol. Med. 2008, 12:2552-2565.
93. Caddick J., Kingham P.J., Gardiner N.J., Wiberg M., Terenghi G. Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 2006, 54:840-849.
94. Dezawa M., Takahashi I., Esaki M., Takano M., Sawada H. Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur. J. NeuroSci. 2001, 14:1771-1776.
95. Oliveira J.T., Mostacada K., de Lima S., Martinez A.M. Bone marrow mesenchymal stem cell transplantation for improving nerve regeneration. Int. Rev. Neurobiol. 2013, 108:59-77.
96. Fraser J.K., Schreiber R., Strem B., Zhu M., Alfonso Z., Wulur I., Hedrick M.H. Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes, Nature clinical practice. Cardiovasc. Med. 2006, 3(Suppl. 1):S33-S37.
97. Kern S., Eichler H., Stoeve J., Kluter H., Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006, 24:1294-1301.
98. Locke M., Windsor J., Dunbar P.R. Human adipose-derived stem cells: isolation, characterization and applications in surgery. ANZ J. Surg. 2009, 79:235-244.
99. Aust L., Devlin B., Foster S.J., Halvorsen Y.D., Hicok K., du Laney T., Sen A., Willingmyre G.D., Gimble J.M. Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 2004, 6:7-14.
100. Gronthos S., Franklin D.M., Leddy H.A., Robey P.G., Storms R.W., Gimble J.M. Surface protein characterization of human adipose tissue-derived stromal cells. J. Cell. Physiol. 2001, 189:54-63.
101. Zuk P.A., Zhu M., Ashjian P., De Ugarte D.A., Huang J.I., Mizuno H., Alfonso Z.C., Fraser J.K., Benhaim P., Hedrick M.H. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 2002, 13:4279-4295.
102. Zuk P.A., Zhu M., Mizuno H., Huang J., Futrell J.W., Katz A.J., Benhaim P., Lorenz H.P., Hedrick M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001, 7:211-228.
103. Gimble J., Guilak F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 2003, 5:362-369.
104. Kingham P.J., Kolar M.K., Novikova L.N., Novikov L.N., Wiberg M. Stimulating the neurotrophic and angiogenic properties of human adipose-derived stem cells enhances nerve repair. Stem Cells Dev. 2014, 23:741-754.
105. Kingham P.J., Kalbermatten D.F., Mahay D., Armstrong S.J., Wiberg M., Terenghi G. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp. Neurol. 2007, 207:267-274.
106. Faroni A., Terenghi G., Reid A.J. Adipose-derived stem cells and nerve regeneration: promises and pitfalls. Int. Rev. Neurobiol. 2013, 108:121-136.
107. Faroni A., Smith R.J., Reid A.J. Adipose derived stem cells and nerve regeneration. Neural Regen Res. 2014, 9(14):1341-1346.
108. Shiotani A., O'Malley B.W., Coleman M.E., Alila H.W., Flint P.W. Reinnervation of motor endplates and increased muscle fiber size after human insulin-like growth factor I gene transfer into the paralyzed larynx. Hum. Gene Ther. 1998, 9:2039-2047.
109. Nakagawa H., Shiotani A., O'Malley B.W., Coleman M.E., Flint P.W. Timing of human insulin-like growth factor-1 gene transfer in reinnervating laryngeal muscle. Laryngoscope 2004, 114:726-732.
110. Nagata K., Itaka K., Baba M., Uchida S., Ishii T., Kataoka K. Muscle-targeted hydrodynamic gene introduction of insulin-like growth factor-1 using polyplex nanomicelle to treat peripheral nerve injury. J. Control. Release 2014, 183:27-34.
111. Herzog R.W. AAV-mediated gene transfer to skeletal muscle. Methods Mol. Biol. 2004, 246:179-194.
112. Moimas S., Novati F., Ronchi G., Zacchigna S., Fregnan F., Zentilin L., Papa G., Giacca M., Geuna S., Perroteau I., Arnez Z.M., Raimondo S. Effect of vascular endothelial growth factor gene therapy on post-traumatic peripheral nerve regeneration and denervation-related muscle atrophy. Gene Ther. 2013, 20:1014-1021.
113. Chen J., Chu Y.F., Chen J.M., Li B.C. Synergistic effects of NGF, CNTF and GDNF on functional recovery following sciatic nerve injury in rats. Adv. Med. Sci. 2010, 55:32-42.
114. Haase G., Pettmann B., Vigne E., Castelnau-Ptakhine L., Schmalbruch H., Kahn A. Adenovirus-mediated transfer of the neurotrophin-3 gene into skeletal muscle of pmn mice: therapeutic effects and mechanisms of action. J. Neurol. Sci. 1998, 160(Suppl. 1):S97-S105.
115. Lazerges C., Daussin P.A., Coulet B., Boubaker el A.R., Micallef J.P., Chammas M., Reyne Y., Bacou F. Transplantation of primary satellite cells improves properties of reinnervated skeletal muscles. Muscle Nerve 2004, 29:218-226.
116. Cesar M., Roussanne-Domergue S., Coulet B., Gay S., Micallef J.P., Chammas M., Reyne Y., Bacou F. Transplantation of adult myoblasts or adipose tissue precursor cells by high-density injection failed to improve reinnervated skeletal muscles. Muscle Nerve 2008, 37.
117. Halum S.L., Naidu M., Delo D.M., Atala A., Hingtgen C.M. Injection of autologous muscle stem cells (myoblasts) for the treatment of vocal fold paralysis: a pilot study. Laryngoscope 2007, 117:917-922.
118. Craff M.N., Zeballos J.L., Johnson T.S., Ranka M.P., Howard R., Motarjem P., Randolph M.A., Winograd J.M. Embryonic stem cell-derived motor neurons preserve muscle after peripheral nerve injury. Plast. Reconstr. Surg. 2007, 119:235-245.
119. Schaakxs D., Kalbermatten D.F., Raffoul W., Wiberg M., Kingham P.J. Regenerative cell injection in denervated muscle reduces atrophy and enhances recovery following nerve repair. Muscle Nerve 2013, 47:691-701.
120. Jiang J., Yao P., Gu Y., Xu L., Xu J., Tan H. Adult rat mesenchymal stem cells delay denervated muscle atrophy. Cell. Mol. Neurobiol. 2012, 32:1287-1298.
121. Hogendoorn S., Duijnisveld B.J., van Duinen S.G., Stoel B.C., van Dijk J.G., Fibbe W.E., Nelissen R.G. Local injection of autologous bone marrow cells to regenerate muscle in patients with traumatic brachial plexus injury: a pilot study. Bone Joint Res. 2014, 3:38-47.
122. Fishman J.M., Tyraskis A., Maghsoudlou P., Urbani L., Totonelli G., Birchall M.A., De Coppi P. Skeletal muscle tissue engineering: which cell to use?. Tissue Eng. B Rev. 2013, 19(6):503-515.
123. Koning M., Harmsen M.C., van Luyn M.J., Werker P.M. Current opportunities and challenges in skeletal muscle tissue engineering. J. Tissue Eng. Regen. Med. 2009, 3:407-415.
124. Kumbar S.G., James R., Nukavarapu S.P., Laurencin C.T. Electrospun nanofiber scaffolds: engineering soft tissues. Biomed. Mater. 2008, 3:034002.
125. Borschel G.H., Dow D.E., Dennis R.G., Brown D.L. Tissue-engineered axially vascularized contractile skeletal muscle. Plast. Reconstr. Surg. 2006, 117:2235-2242.
126. Morimoto Y., Kato-Negishi M., Onoe H., Takeuchi S. Three-dimensional neuron-muscle constructs with neuromuscular junctions. Biomaterials 2013, 34:9413-9419.
127. Artico M., Cervoni L., Nucci F., Giuffre R. Birthday of peripheral nervous system surgery: the contribution of Gabriele Ferrara (1543-1627). Neurosurgery 1996, 39:380-382. (discussion 382-383).
128. Seddon H.J. Nerve grafting and other unusual forms of nerve repair. Spec. Rep. Ser. 1954, 282:389-417.
129. Millesi H., Meissl G., Berger A. The interfascicular nerve-grafting of the median and ulnar nerves. J. Bone Joint Surg. Am. 1972, 54:727-750.
130. Moore A.M. Nerve transfers to restore upper extremity function: a paradigm shift. Front. Neurol. 2014, 5:40.