Schwann cells seeded in acellular nerve grafts improve functional recovery

Muscle and Nerve

Volumn 49, Issue 2, 2014, Pages 267-276

  Jesuraj, Nithya J ^a   Santosa, Katherine B ^b   Macewan, Matthew R ^a   Moore, Amy M ^b   Kasukurthi, Rahul ^b   Ray, Wilson Z ^b   Flagg, Eric R ^b   Hunter, Daniel A ^b   Borschel, Gregory H ^b   Johnson, Philip J ^b   Mackinnon, Susan E ^b   Sakiyama Elbert, Shelly E ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell transplantation; Growth factor; Nerve regeneration; Peripheral nerve injury; Reinnervation

Indexed keywords

GROWTH FACTOR;

ACELLULAR NERVE GRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; EVOKED MUSCLE RESPONSE; FEMORAL NERVE; FREEZE THAWING; GENE EXPRESSION; MALE; MUSCLE REGENERATION; MUSCLE STRENGTH; NERVE FIBER REGENERATION; NERVE GRAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SCHWANN CELL; SCIATIC NERVE; SCIATIC NERVE INJURY;

CELL TRANSPLANTATION; GROWTH FACTOR; NERVE REGENERATION; PERIPHERAL NERVE INJURY; REINNERVATION;

ANIMALS; CELL TRANSPLANTATION; DISEASE MODELS, ANIMAL; FEMORAL NERVE; ISOGRAFTS; MALE; NERVE GROWTH FACTOR; NERVE REGENERATION; PERIPHERAL NERVE INJURIES; RATS; RATS, INBRED LEW; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SCHWANN CELLS; SCIATIC NERVE; TIME FACTORS;

EID: 84892522144     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.23885     Document Type: Article

References (72)

1. Siemionow M, Brzezicki G. Chapter 8: current techniques and concepts in peripheral nerve repair. Int Rev Neurobiol 2009;87:141-172.
2. Burnett MG, Zager EL. Pathophysiology of peripheral nerve injury: a brief review. Neurosurg Focus 2004;16:E1.
3. Schmidt CE, Leach JB. Neural tissue engineering: strategies for repair and regeneration. Annu Rev Biomed Eng 2003;5:293-347.
4. Bain JR, Mackinnon SE, Hudson AR, Falk RE, Falk JA, Hunter DA, et al. Preliminary report of peripheral nerve allografting in primates immunosuppressed with cyclosporin A. Transplant Proc 1989;21(Pt 3):3176-3177.
5. Midha R, Mackinnon SE, Evans PJ, Best TJ, Hare GM, Hunter DA, et al. Comparison of regeneration across nerve allografts with temporary or continuous cyclosporin A immunosuppression. J Neurosurg 1993;78:90-100.
6. Nakao Y, Mackinnon SE, Mohanakumar T, Miyasaka M, Nakayama K, Nakafusa Y, et al. Monoclonal antibodies against ICAM-1 and LFA-1 (CD11A) induce specific tolerance to peripheral nerve allograft in rats. Transplant Proc 1995;27:373-377.
7. Strasberg SR, Hertl MC, Mackinnon SE, Lee CK, Watanabe O, Tarasidis G, et al. Peripheral nerve allograft preservation improves regeneration and decreases systemic cyclosporin A requirements. Exp Neurol 1996;139:306-316.
8. Strasberg SR, Mackinnon SE, Genden EM, Bain JR, Purcell CM, Hunter DA, et al. Long-segment nerve allograft regeneration in the sheep model: experimental study and review of the literature. J Reconstr Microsurg 1996;12:529-537.
9. Gulati AK, Cole GP. Immunogenicity and regenerative potential of acellular nerve allografts to repair peripheral nerve in rats and rabbits. Acta Neurochir (Wien) 1994;126:158-164.
10. Zalewski AA, Gulati AK. Evaluation of histocompatibility as a factor in the repair of nerve with a frozen nerve allograft. J Neurosurg 1982;56:550-554.
11. Hudson TW, Liu SY, Schmidt CE. Engineering an improved acellular nerve graft via optimized chemical processing. Tissue Eng 2004;10:1346-1358.
12. Hudson TW, Zawko S, Deister C, Lundy S, Hu CY, Lee K, et al. Optimized acellular nerve graft is immunologically tolerated and supports regeneration. Tissue Eng 2004;10:1641-1651.
13. Johnson PJ, Newton P, Hunter DA, Mackinnon SE. Nerve endoneurial microstructure facilitates uniform distribution of regenerative fibers: a post hoc comparison of midgraft nerve fiber densities. J Reconstr Microsurg 2011;27:83-90.
14. Moore AM, MacEwan M, Santosa KB, Chenard KE, Ray WZ, Hunter DA, et al. Acellular nerve allografts in peripheral nerve regeneration: a comparative study. Muscle Nerve 2011;44:221-234.
15. Whitlock EL, Tuffaha SH, Luciano JP, Yan Y, Hunter DA, Magill CK, et al. Processed allografts and type I collagen conduits for repair of peripheral nerve gaps. Muscle Nerve 2009;39:787-799.
16. Mackinnon SE, Dellon AL. A study of nerve regeneration across synthetic (Maxon) and biologic (collagen) nerve conduits for nerve gaps up to 5 cm in the primate. J Reconstr Microsurg 1990;6:117-121.
17. Mackinnon SE, Dellon AL. Clinical nerve reconstruction with a bioabsorbable polyglycolic acid tube. Plast Reconstr Surg 1990;85:419-424.
18. Meek MF, Coert JH. Clinical use of nerve conduits in peripheral-nerve repair: review of the literature. J Reconstr Microsurg 2002;18:97-109.
19. Karabekmez FE, Duymaz A, Moran SL. Early clinical outcomes with the use of decellularized nerve allograft for repair of sensory defects within the hand. Hand (N Y) 2009;4:245-249.
20. Brenner MJ, Lowe JB III, Fox IK, Mackinnon SE, Hunter DA, Darcy MD, et al. Effects of Schwann cells and donor antigen on long-nerve allograft regeneration. Microsurgery 2005;25:61-70.
21. Bunge RP. The role of the Schwann cell in trophic support and regeneration. J Neurol 1994;242(Suppl 1):S19-S21.
22. Nagarajan R, Le N, Mahoney H, Araki T, Milbrandt J. Deciphering peripheral nerve myelination by using Schwann cell expression profiling. Proc Natl Acad Sci U S A 2002;99:8998-9003.
23. Reynolds ML, Woolf CJ. Reciprocal Schwann cell-axon interactions. Curr Opin Neurobiol 1993;3:683-693.
24. Waller AV. Experiments on the glossopharyngeal and hypoglossal nerves of the frog and observations produced thereby in the structure of their primative fibres. Philos Trans R Soc Lond 1850;140(423).
25. Chan JR, Cosgaya JM, Wu YJ, Shooter EM. Neurotrophins are key mediators of the myelination program in the peripheral nervous system. Proc Natl Acad Sci U S A 2001;98:14661-14668.
26. Iwase T, Jung CG, Bae H, Zhang M, Soliven B. Glial cell line-derived neurotrophic factor-induced signaling in Schwann cells. J Neurochem 2005;94:1488-1499.
27. Frostick SP, Yin Q, Kemp GJ. Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 1998;18:397-405.
28. Guenard V, Kleitman N, Morrissey TK, Bunge RP, Aebischer P. Syngeneic Schwann cells derived from adult nerves seeded in semipermeable guidance channels enhance peripheral nerve regeneration. J Neurosci 1992;12:3310-3320.
29. Kim DH, Connolly SE, Kline DG, Voorhies RM, Smith A, Powell M, et al. Labeled Schwann cell transplants versus sural nerve grafts in nerve repair. J Neurosurg 1994;80:254-260.
30. Levi AD, Guenard V, Aebischer P, Bunge RP. The functional characteristics of Schwann cells cultured from human peripheral nerve after transplantation into a gap within the rat sciatic nerve. J Neurosci 1994;14(Pt 1):1309-1319.
31. Aszmann OC, Korak KJ, Luegmair M, Frey M. Bridging critical nerve defects through an acellular homograft seeded with autologous schwann cells obtained from a regeneration neuroma of the proximal stump. J Reconstr Microsurg 2008;24:151-158.
32. Brushart TM. Preferential reinnervation of motor nerves by regenerating motor axons. J Neurosci 1988;8:1026-1031.
33. Brushart TM. Motor axons preferentially reinnervate motor pathways. J Neurosci 1993;13:2730-2738.
34. Madison RD, Archibald SJ, Brushart TM. Reinnervation accuracy of the rat femoral nerve by motor and sensory neurons. J Neurosci 1996;16:5698-5703.
35. Madison RD, Archibald SJ, Lacin R, Krarup C. Factors contributing to preferential motor reinnervation in the primate peripheral nervous system. J Neurosci 1999;19:11007-11016.
36. Madison RD, Robinson GA, Chadaram SR. The specificity of motor neurone regeneration (preferential reinnervation). Acta Physiol (Oxf) 2007;189:201-206.
37. Madison RD, Sofroniew MV, Robinson GA. Schwann cell influence on motor neuron regeneration accuracy. Neuroscience 2009;163:213-221.
38. Hoke A, Redett R, Hameed H, Jari R, Zhou C, Li ZB, et al. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci 2006;26:9646-9655.
39. Jesuraj NJ, Nguyen PK, Wood MD, Moore AM, Borschel GH, Mackinnon SE, et al. Differential gene expression in motor and sensory Schwann cells in the rat femoral nerve. J Neurosci Res 2012;90:96-104.
40. Southard JH, Belzer FO. Organ preservation. Annu Rev Med 1995;46:235-247.
41. Fox IK, Jaramillo A, Hunter DA, Rickman SR, Mohanakumar T, Mackinnon SE. Prolonged cold-preservation of nerve allografts. Muscle Nerve 2005;31:59-69.
42. Brockes JP, Raff MC. Studies on cultured rat Schwann cells. II. Comparison with a rat Schwann cell line. In Vitro 1979;15:772-778.
43. Pruss RM. The potential use of cultured cells to detect non-neuronal targets of neuropeptide action. Peptides 1982;3:231-233.
44. Raff MC, Abney E, Brockes JP, Hornby-Smith A. Schwann cell growth factors. Cell 1978;15:813-822.
45. Jesuraj NJ, Santosa KB, Newton P, Liu Z, Hunter DA, Mackinnon SE, et al. A systematic evaluation of Schwann cell injection into acellular cold-preserved nerve grafts. J Neurosci Methods 2011;197:209-215.
46. Aguayo AJ, Charron L, Bray GM. Potential of Schwann cells from unmyelinated nerves to produce myelin: a quantitative ultrastructural and radiographic study. J Neurocytol 1976;5:565-573.
47. Aguayo AJ, Epps J, Charron L, Bray GM. Multipotentiality of Schwann cells in cross-anastomosed and grafted myelinated and unmyelinated nerves: quantitative microscopy and radioautography. Brain Res 1976;104:1-20.
48. Hunter DA, Moradzadeh A, Whitlock EL, Brenner MJ, Myckatyn TM, Wei CH, et al. Binary imaging analysis for comprehensive quantitative histomorphometry of peripheral nerve. J Neurosci Methods 2007;166:116-124.
49. Wood MD, Macewan MR, French AR, Moore AM, Hunter DA, Mackinnon SE, et al. Fibrin matrices with affinity-based delivery systems and neurotrophic factors promote functional nerve regeneration. Biotechnol Bioeng 2010;106:970-979.
50. Wilfinger WW, Mackey K, Chomczynski P. Effect of pH and ionic strength on the spectrophotometric assessment of nucleic acid purity. Biotechniques 1997;22:474-476, 478-481.
51. Salonen V, Aho H, Roytta M, Peltonen J. Quantitation of Schwann cells and endoneurial fibroblast-like cells after experimental nerve trauma. Acta Neuropathol 1988;75:331-336.
52. Gaumond G, Tyropolis A, Grodzicki S, Bushmich S. Comparison of direct fluorescent antibody staining and real-time polymerase chain reaction for the detection of Borrelia burgdorferi in Ixodes scapularis ticks. J Vet Diagn Invest 2006;18:583-586.
53. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-408.
54. Henderson CE, Camu W, Mettling C, Gouin A, Poulsen K, Karihaloo M, et al. Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 1993;363:266-270.
55. Li L, Wu W, Lin LF, Lei M, Oppenheim RW, Houenou LJ. Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc Natl Acad Sci U S A 1995;92:9771-9775.
56. Lee AC, Yu VM, Lowe JB III, Brenner MJ, Hunter DA, Mackinnon SE, et al. Controlled release of nerve growth factor enhances sciatic nerve regeneration. Exp Neurol 2003;184:295-303.
57. Wood MD, Moore AM, Hunter DA, Tuffaha S, Borschel GH, Mackinnon SE, et al. Affinity-based release of glial-derived neurotrophic factor from fibrin matrices enhances sciatic nerve regeneration. Acta Biomater 2009;5:959-968.
58. Xu X, Yu H, Gao S, Ma HQ, Leong KW, Wang S. Polyphosphoester microspheres for sustained release of biologically active nerve growth factor. Biomaterials 2002;23:3765-3772.
59. Yan Q, Matheson C, Lopez OT. In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 1995;373:341-344.
60. Mackinnon SE, Dellon AL, O'Brien JP. Changes in nerve fiber numbers distal to a nerve repair in the rat sciatic nerve model. Muscle Nerve 1991;14:1116-1122.
61. Mirsky R, Jessen KR. Schwann cell development, differentiation and myelination. Curr Opin Neurobiol 1996;6:89-96.
62. Jessen KR, Mirsky R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 2005;6:671-682.
63. Aitken JT, Sharman M, Young JZ. Maturation of regenerating nerve fibres with various peripheral connexions. J Anat 1947;81:1-22.
64. Williams PL, Wendell-Smith CP. Some additional parametric variations between peripheral nerve fibre populations. J Anat 1971;109(Pt 3):505-526.
65. Fraher J, Dockery P. A strong myelin thickness-axon size correlation emerges in developing nerves despite independent growth of both parameters. J Anat 1998;193(Pt 2):195-201.
66. Parrinello S, Napoli I, Ribeiro S, Digby PW, Fedorova M, Parkinson DB, et al. EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell;143:145-155.
67. Urbanchek MS, Chung KC, Asato H, Washington LN, Kuzon WM Jr. Rat walking tracks do not reflect maximal muscle force capacity. J Reconstr Microsurg 1999;15:143-149.
68. Viguie CA, Lu DX, Huang SK, Rengen H, Carlson BM. Quantitative study of the effects of long-term denervation on the extensor digitorum longus muscle of the rat. Anat Rec 1997;248:346-354.
69. Dellon AL, Mackinnon SE. An alternative to the classical nerve graft for the management of the short nerve gap. Plast Reconstr Surg 1988;82:849-856.
70. Hirata H, Hibasami H, Yoshida T, Ogawa M, Matsumoto M, Morita A, et al. Nerve growth factor signaling of p75 induces differentiation and ceramide-mediated apoptosis in Schwann cells cultured from degenerating nerves. Glia 2001;36:245-258.
71. Galla TJ, Vedecnik SV, Halbgewachs J, Steinmann S, Friedrich C, Stark GB. Fibrin/Schwann cell matrix in poly-epsilon-caprolactone conduits enhances guided nerve regeneration. Int J Artif Organs 2004;27:127-136.
72. Suri S, Schmidt CE. Cell-laden hydrogel constructs of hyaluronic acid, collagen, and laminin for neural tissue engineering. Tissue Eng Part A 2010;16:1703-1716.