Chapter 21 Use of Stem Cells for Improving Nerve Regeneration

International Review of Neurobiology

Volumn 87, Issue C, 2009, Pages 393-403

  Terenghi, Giorgio ^a   Wiberg, Mikael ^b,c   Kingham, Paul J ^a,b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UMEÅ UNIVERSITY   (Sweden)

^c UMEÅ UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN; POLY(3 HYDROXYBUTYRIC ACID);

ALLOGENEIC STEM CELL TRANSPLANTATION; BIOENGINEERING; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; MATERIAL COATING; NERVE CELL; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; REVIEW; SCHWANN CELL; UPREGULATION; ANIMAL; METHODOLOGY; PERIPHERAL NERVE; PHYSIOLOGY; STEM CELL; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

ANIMALS; HUMANS; NERVE REGENERATION; PERIPHERAL NERVES; SCHWANN CELLS; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 70349784343     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7742(09)87021-9     Document Type: Review

References (85)

1. Aberg M., Ljungberg C., Edin E., Millqvist H., Nordh E., Terenghi G., and Wiberg M. Clinical evaluation of a resorbable wrap-around implant as an alternative to nerve repair. J. Plast. Reconstr. Aesthet. Surg. (2009) in press
2. Alison M.R., Poulsom R., Forbes S., and Wright N.A. An introduction to stem cells. J. Pathol. 197 (2002) 419-423
3. Armstrong S.J., Wiberg M., Terenghi G., and Kingham P.J. ECM Molecules mediate both Schwann cell proliferation and activation to enhance neurite outgrowth. Tissue Eng. 13 12 (2007) 2863-2870
4. Banfi A., Bianchi G., Galotto M., Cancedda R., and Quarto R. Bone marrow stromal damage after chemo/radiotherapy: Occurrence, consequences and possibilities of treatment. Leuk. Lymphoma 42 (2001) 863-870
5. Barbash I.M., Chouraqui P., Baron J., Feinberg M.S., Etzion S., Tessone A., Miller L., Guetta E., Zipori D., Kedes L.H., Kloner R.A., and Leor J. Systemic delivery of bone-marrow derived mesenchymal stem cells to the infarcted myocardium. Circulation 108 (2003) 863-868
6. Bossolasco P., Cova L., Calzaross C., Rimoldi S.G., Borsotti C., Deliliers G.L., Silani V., and Soligo D. Polli. Neuro-glial differentiation of human bone marrow stem cells in vitro. Exp. Neurol. 193 2 (2005) 312-325
7. Brohlin M., Mahay D., Novikov L.N., Terenghi G., Wiberg M., Shawcross S.G., and Novikova L.N. Characterisation of human mesenchymal stem cells following differentiation into Schwann cell-like cells. Neurosci. Res. 64 (2009) 41-49
8. Burdick J.A., and Vunjak-Novakovic G. Engineered microenvironments for controlled stem cell differentiation. Tissue Eng. 15 (2009) 205-219
9. Caddick J., Kingham P.J., Gardiner N.J., Wiberg M., and Terenghi G. Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54 8 (2006) 840-849
10. Chen C.J., Ou Y.C., Liao S.L., Chen W.Y., Chen S.Y., Wu C.W., Wang C.C., Wang W.Y., Huang Y.S., and Hsu S.H. Transplantation of bone marrow stromal cells for peripheral nerve repair. Exp. Neurol. 204 (2007) 443-453
11. Chen X., Wang X.D., Chen G., Liu W.W., Yao J., and Gu X.S. Study of in vivo differentiation of rat bone marrow stromal cells into Schwann cell-like cells. Microsurgery 26 2 (2006) 111-115
12. Chew S.Y., Mi R., Hoke A., and Leong K.W. The effect of the alignment of electrospun fibrous scaffolds on Schwann cell maturation. Biomat 29 6 (2008) 653-661
13. Choi B.H., Zhu S.J., Kim B.Y., Huh Y.H., Lee S.H., and Jung J.H. Transplantation of cultured bone marrow stromal cells to improve peripheral nerve regeneration. Int. J. Oral Maxillofac. Surg. 34 (2005) 537-542
14. Chu C., Schmidt J.J., Carnes K., Zhang Z., Kong H.J., and Hofmann M.C. Three-dimensional synthetic niche components to control germ cell proliferation. Tissu Eng. 15 (2009) 255-262
15. Chung C., and Burdick J.A. Influence of three-dimensional hyaluronic acid microenvironments on mesenchymal stem cell chondrogenesis. Tissue Eng. 15 (2009) 243-254
16. Ciardelli G., and Chiono V. Materials for peripheral nerve regeneration. Macromol. Biosci. 6 (2006) 13-26
17. Crigler L., Robey R.C., Asawachaicharn A., Gaupp D., and Phinney D.G. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp. Neurol. 198 (2006) 54-64
18. Cuevas P., Carceller F., Dujovny M., Garcia-Gomez I., Cuevas B., Gonzalez-Corrochano R., Diaz-Gonzalez D., and Reimers D. Peripheral nerve regeneration by bone marrow stromal cells. Neurol. Res. 24 (2002) 634-638
19. Da L., Sand T.T., Harman R.J., Lennon D.P., and Caplan A.I. MSC frequency correlates with blood vessel density in equine adipose tissue. Tissue Eng. 15 (2009) 221-229
20. De Ugarte D.A., Morizono K., Elbarbary A., Alfonso Z., Zuk P.A., Zhu M., Dragoo J.L., Ashjian P., Thomas B., Benhaim P., Chen I., Fraser J., et al. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174 (2003) 101-109
21. Dezawa M., Takahashi I., Esaki M., Takano M., and Sawada H. Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur. J. Neurosci. 14 (2001) 1771-1776
22. Evans G.R.D. Peripheral nerve injury: A review and approach to engineered constructs. Anat. Rec. 263 (2001) 396-404
23. Galderisi U., Helmbold H., Squillaro T., Alessio N., Komm N., Khadang B., Cipollaro M., Bohn W., and Giordano A. In vitro senescence of rat mesenchymal stem cells is accompanied by downregulation of stemness-related and DNA damage repair genes. Stem Cell Dev. (2008) [e-pub ahead of print]
24. Gimble J., and Guilak F. Adipose-derived adult stem cells, Isolation, characterization, and differentiation potential. Cytotherapy 5 (2003) 362-369
25. Gojo S., Gojo N., Mori T., Abe H., Kyo S., Hata J., and Umezawa A. In vivo cardiovasculogeneis by direct injection of isolated adult mesenchymal stem cells. Exp. Cell Res. 288 (2003) 51-59
26. Hadlock T., Sundback C., Hunter D., Cheney M., and Vacanti J. A polymer foam conduit seeded with Schwann cells promotes guided peripheral nerve regeneration. Tissue Eng. 6 (2000) 119-127
27. Hall S. Nerve repair: A neurobiologist's view. J. Hand Surg. 26B (2001) 129-136
28. Hart A., Brannstrom T., Wiberg M., and Terenghi G. Timecourse of primary sensory neuron and satellite cell death after peripheral axotomy in adult rat. Exp. Brain Res. 142 (2002) 308-318
29. Hart A.M., Terenghi G., and Wiberg M. Neuronal death after peripheral nerve injury and experimental strategies for neuroprotection. Neurol. Res. 30 (2008) 999-1011
30. Hou S.Y., Zhang H.Y., Quan D.P., Liu X.L., and Zhu J.K. Tissue-engineered peripheral nerve grafting by differentiated bone marrow stromal cells. Neuroscience 140 (2006) 101-110
31. Hu J., Zhu Q.T., Liu X.L., Xu Y.B., and Zhu J.K. Repair of extended peripheral nerve lesions in rhesus monkeys using acellular allogenic nerve grafts implanted with autologous mesenchymal stem cells. Exp. Neurol. 204 2 (2007) 658-666
32. Izadpanah R., Trygg C., Patel B., Christopher K., Dufour J., Gimble J.M., and Bunnell B.A. Biological properties od mesenchymal stem cells derived from bone marrow and adipose tissue. J. Cell Biochem. 99 (2006) 1285-1297
33. Jurgens W.J.F.M., Oedayrajsingh-Varma M.J., Helder M.N., Zandich Doulabi B., Schouten T.E., Kuik D.J., Ritt M.J.P.F., and van Milligen F.J. Effect of tissue harvesting site on yield of stem cells derived from adipose tissue: Implications for cell-based therapies. Cell Tissue Res. 332 (2008) 415-426
34. Kalbermatten D.F., Kingham P.J., Mahay D., Mantovani C., Pettersson J., Raffoul W., Balchin H., Pierer G., and Terenghi G. Fibrin matrix for suspension of regenerative cells in an artificial nerve conduit. J. Plast. Reconstr. Aesthet. Surg. 61 (2008) 669-675
35. Kalbermatten D.F., Pettersson J., Kingham P.J., Mahay D., Erba P., Pierer G., and Terenghi H. New fibrin conduit for peripheral nerve repair. J. Recontr. Microsurg. 25 (2009) 27-33
36. Keilhoff G., Stang F., Goihl A., Wolf G., and Fansa H. Mesenchymal stem cells as alternative therapy in supporting nerve regeneration and myelination. Cell Mol. Neurobiol. 26 (2006) 1233-1250
37. Kim B.J., Seo J.H., Bubien J.K., and Oh Y.S. Differentiation of adult bone marrow stem cells into neuroprogenitor cells in vitro. Neuroreport 13 (2002) 1185-1188
38. Kingham P.J., Kalbermatten D.F., Mahay D., Armstrong S.J., Wiberg M., and Terenghi G. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp. Neurol. 207 2 (2007) 267-274
39. Kretlow J.D., Jin Y.Q., Liu W., Zhang W.J., Hong T.H., Zhou G., Baggett L.S., Mikos A.G., and Cao Y. Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol. 9 (2008) 60
40. Kvist M., Danielsen N., and Dahlin L.B. Effects of FK506 on regeneration and macrophages in injured rat sciatic nerve. J. Peripher. Nerv. Syst. 8 (2003) 251-259
41. Labrador R.O., Buti M., and Navarros X. Influence of collagen and laminin gels concentration on nerve regeneration after resection and tube repair. Exp. Neurol. 149 (1998) 243-252
42. Li Q., Ping P., Jiang H., and Liu K. Nerve conduit filled with GDNF gene-modified Schwann cells enhances regeneration of the peripheral nerve. Microsurgery 26 (2006) 116-121
43. Lin G., Garcia M., Ning H., Banie L., Guo Y.L., Lue T.F., and Lin C.S. Defining stem and progenitor cells within adipose tissue. Stem Cells Dev. 17 (2008) 1053-1064
44. Lutolf M.P., and Hubbell J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in engineering. Nat. Biotechnol. 23 (2005) 47-55
45. Mackinnon S.E., Doolabh V.B., Novak C.B., and Trulock E.P. Clinical outcome following nerve allograft transplantation. Plast. Reconstr. Surg. 107 (2001) 1419-1429
46. Madison R., da Silva C.F., Dikkes P., Chiu T.H., and Sidman R.L. Increased rate of peripheral nerve regeneration using bioresorbable nerve guides and a laminin-containing gel. Exp. Neurol. 88 (1985) 767-772
47. Mahay D., Terenghi G., and Shawcross S. Growth factors in mesenchymal stem cells following glial cell differentiation. Biotechnol. Appl. Biochem. 51 (2008) 167-176
48. Mahay D., Terenghi G., and Shawcross S.G. Schwann cell mediated trophic effects by differentiated mesenchymal stem cells. Exp. Cell Res. 314 (2008) 2692-2701
49. Mantovani C., Mahay D., Shawcross S., Terenghi G., and Wiberg M. Development of an in vitro co-culture model to investigate peripheral myelin formation. Neurosci. Res. (2009) (submitted for publication)
50. Matsumoto K., Ohnishi K., Kiyotani T., Sekine T., Ueda H., Nakamura T., Eo K., and Shimizu Y. Peripheral nerve regeneration across an 80 mm gap bridged by a polyglycolic acid (PGA)-collagen tube filled with laminin-coated fibres: A histological and electrophysiological evaluation of regenerated nerves. Brain Res. 868 (2000) 325-328
51. Midha R., Nag S., Munro C.A., and Ang L.C. Differential response of sensory and motor axons in nerve allografts after withdrawal of immunosuppressive therapy. J. Neurosurg. 94 (2001) 102-110
52. Mosahebi A., Woodward B., Wiberg M., Martin R., and Terenghi G. Retroviral labelling of Schwann cells: In vitro characterisation and in vivo transplantation to improve peripheral nerve regeneration. Glia 34 (2001) 8-17
53. Mosahebi A., Simon M., Wiberg M., and Terenghi G. A novel use of alginate hydrogel as Schwann cell matrix. Tissue Eng. 7 (2001) 525-534
54. Mosahebi A., Fuller P., Wiberg M., and Terenghi G. Effect of allogeneic Schwann cell transplantation on peripheral nerve regeneration. Exp. Neurol. 173 (2002) 213-223
55. Mohanna P.N., Young R.C., Wiberg M., and Terenghi G. A composite poly-hydroxybutyrate-glial growth factor conduit for long nerve gap repair. J. Anat. 203 (2003) 553-565
56. Mohanna P.N., Terenghi G., and Wiberg M. Composite PHB-GGF conduit for long nerve gap repair: A long-term evaluation. Scan. J. Plast. Reconstr. Hand Surg. 39 (2005) 129-137
57. Muraglia A., Cacedda R., and Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J. Cell Sci. 113 (2000) 1161-1166
58. Muschler G.F., Nitto H., Boehm C.A., and Easley K.A. Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J. Orthop. Res. 19 (2001) 117-125
59. Novikova L.N., Mosahebi A., Wiberg M., Terenghi G., Kellerth J.O., and Novikov L.N. Alginate hydrogel and matrigel as potential cell carrier for neurotransplantation. J. Biomed. Mat. Res. 77A (2006) 242-252
60. Ngo T.T.B., Waggoner P.J., Romero A.A., Nelson K.D., Eberhart R.C., and Smith G.M. Poly-l-lactide microfilaments enhance peripheral nerve regeneration across extended nerve lesions. J. Neurosci. Res. 72 (2003) 227-238
61. Pereira Lopes F.R., de Moura Campos L.C., Correa Jr. J.D., Balduino A., Lora S., Langone F., Borojevic R., and Martinez A.M.B. Bone marrow stromal cells and resorbable collagen guidance tubes enhance sciatic nerve regeneration in mice. Exp. Neurol. 198 (2006) 457-468
62. Raimondo S., Penna C., Pagliaro P., and Geuna S. Morphological characterisation of GFP stably transfected adult mesenchymal bone marrow stem cells. J. Anat. 208 (2006) 3-12
63. Schallmoser K., Rodhe E., Reinisch A., Bartmann C., Thaler D., Drexler C., Obenauf A.C., Lanzer G., Linkesch W., and Strunk D. Rapid large-scale expansion of functional mesenchymal stem cells from unmanipulated bone marrow without animal serum. Tissue Eng. 14 (2008) 185-196
64. Schlosshauer B., Dreesmann L., Schaller H.E., and Sinis N. Synthetic nerve guide implants in humans: A comprehensive survey. Neurosurgery 59 4 (2006) 740-748
65. Seckel B.R., Jones D., Hekimian K.J., Wang K.K., Chakalis D.P., and Costas P.D. Hyaluronic acid through a new injectable nerve guide delivery stem enhances peripheral nerve regeneration in the rat. J. Neurosci. Res. 40 (1995) 3138-3324
66. Shimizu S., Kitada M., Ishikawa H., Itokazu Y., Wakao S., and Dezawa M. Peripheral nerve regeneration by the in vitro differentiated human bone marrow stromal cells with Schwann cell property. Biochem. Biophys. Res. Commun. 359 (2007) 915-920
67. Strem B.M., Hicok K.C., Zhu M., Wulur I., Alfonso Z., Schreiber R.E., Fraser J.K., and Hedrick M.H. Multipotential differentiation of adipose tissue-derived stem cells. Keio J. Med. 54 (2005) 132-141
68. Sulaiman O.A., Voda J., Gold B.G., and Gordon T. FK506 increases peripheral nerve regeneration after chronic axotomy but not after chronic Schwann cell denervation. Exp. Neurol. 175 (2002) 127-137
69. Tholpady S.S., Katz A.J., and Ogle R.C. Mesenchymal stem cells from rat visceral fat exhibit multipotential differentiation in vitro. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 272 (2003) 398-402
70. Thompson D.M., and Buettner H.M. Neurite outgrowth is directed by Schwann cell alignment in the absence of other guidance cues. Ann. Biomed. Eng. 34 (2006) 161-168
71. Tohill M., Mantovani C., Wiberg M., and Terenghi G. Rat bone marrow mesenchymal stem cells express glial markers and stimulate nerve regeneration. Neurosci. Lett. 362 (2004) 200-203
72. Tohill M.P., Mann D.J., Mantovani C., Wiberg M., and Terenghi G. Green fluorescent protein is a stable morphological marker for Schwann cell transplants in bioengineered nerve conduits. Tissue Eng. 10 (2004) 1359-1367
73. Tohill M., and Terenghi G. Stem-cell plasticity and therapy for injuries of the peripheral nervous system. Biotechnol. Appl. Biochem. 40 (2004) 17-24
74. Tong X.J., Hirai K.I., Shimada H., Mizutani Y., Izumi T., Toda N., and Yu P. Sciatic nerve regeneration navigated by laminin-fibronectin double coated biodegradable collagen grafts in rats. Brain. Res. 663 (1994) 155-162
75. Valentini R.F., and Aebischer P. Strategies for the engineering of peripheral nervous tissue regeneration. In: Lanza R.P., Langer R., and Chick W.L. (Eds). Principles of Tissue Engineering (1997) 671-684 Academic Press, Austin
76. Vilalta M., Degano I.R., Bago J., Gould D., Santos M., Garcia-Arranz M., Ayatas R., Fuster C., Chernajovsky Y., Garcia-Olmo D., Rubio N., and Blanco J. Biodistribution, long term survival and safety of human adipose tissue-derived mesenchymal stem cells transplanted in nude mice by high sensitivity non-invasive bioluminescence imaging. Stem. Cell Dev. 17 (2008) 993-1003
77. Wang D., Liu X.L., Zhu J.K., Jiang L., Hu J., Zhang Y., Yang L.M., Wang H.G., and Yi J.H. Bridging small-gap peripheral nerve defects using acellular nerve allograft implanted with autologous bone marrow stromal cells in primates. Brain Res. 1188 (2008) 44-53
78. Wang W., Itoh S., Konno K., Kikkawa T., Ichinose S., Sakai K., Ohkuma T., and Watabe K. Effects of Schwann cell allignment along the oriented electrospun chitosan nanofibres on nerve regeneration. J. Biomed. Mater. Res. (2008) [Epub ahead of print]
79. Welin D., Novikova L.N., Wiberg M., Kellerth J.O., and Novikov L.N. Survival and regeneration of cutaneous and muscular afferent neurons after peripheral nerve injury in adult rats. Exp. Brain. Res. 186 (2008) 315-323
80. Wen X., and Tresco P.A. Effect of filament diameter and extracellular matrix molecule precoating on neurite outgrowth and Schwann cell behaviour on multifilament entubulation bridging device in vitro. J. Biomed. Mat. Res. 76 (2006) 626-637
81. Woodbury D., Schwarz E.J., Prockop D.J., and Black I.B. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 61 (2000) 364-370
82. Wu J., and Chiu D.T. Painful neuromas: a review of treatment modalities. Ann. Plast. Surg. 43 (1999) 661-667
83. Yamakawa T., Kakinoki R., Ikeguchi R., Nakayama K., Morimoto Y., and Nakamura T. Nerve regeneration promoted in a tube with vascularity containing bone marrow-derived cells. Cell Transplant 16 (2007) 811-822
84. Zhang P., He X., Liu K., Fu Z., Zhang D., Zhang Q., and Jiang B. Bone marrow stromal cells differentiated into functional Schwann cells in injured rat sciatic nerve. Artif. Cells Blood Substit. Immobil. Biotechnol. 32 (2004) 509-518
85. Zhang P., He X., Zhao F., Zhang D., Fu Z., and Jiang B. Bridging small-gap peripheral nerve defects using biodegradable chitin conduits with cultured Schwann and bone marrow stromal cells in rats. J. Reconstr. Microsurg. 21 (2005) 565-572