Differentiated adipose-derived stem cells promote myelination and enhance functional recovery in a rat model of chronic denervation

Journal of Neuroscience Research

Volumn 90, Issue 7, 2012, Pages 1392-1402

  Tomita, Koichi ^a,b   Madura, Tomas ^a   Mantovani, Cristina ^a   Terenghi, Giorgio ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Adipose derived stem cell; Chronic denervation; Myelination; Peripheral nerve; Schwann cell differentiation

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN BASIC PROTEIN; PROTEIN S 100;

ADIPOSE DERIVED STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; DENERVATION; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOTOR PERFORMANCE; MYELIN SHEATH; MYELINATION; NERVE FIBER REGENERATION; NERVE REGENERATION; NEURITE; NONHUMAN; PERONEUS NERVE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL GANGLION;

ADIPOSE TISSUE; ANIMALS; CHRONIC DISEASE; COCULTURE TECHNIQUES; DENERVATION; DISEASE MODELS, ANIMAL; GANGLIA, SPINAL; MYELIN SHEATH; NERVE REGENERATION; PRIMARY CELL CULTURE; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SCIATIC NEUROPATHY; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84860917828     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23002     Document Type: Article

References (48)

1. Bain JR, Mackinnon SE, Hunter DA. 1989. Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 83: 129-138.
2. Boyd JG, Gordon T. 2002. A dose-dependent facilitation and inhibition of peripheral nerve regeneration by brain-derived neurotrophic factor. Eur J Neurosci 15: 613-626.
3. Boyd JG, Gordon T. 2003. Glial cell line-derived neurotrophic factor and brain-derived neurotrophic factor sustain the axonal regeneration of chronically axotomized motoneurons in vivo. Exp Neurol 183: 610-619.
4. Bunge RP. 1993. Expanding roles for the Schwann cell: ensheathment, myelination, trophism and regeneration. Curr Opin Neurobiol 3: 805-809.
5. Caddick J, Kingham PJ, Gardiner NJ, Wiberg M, Terenghi G. 2006. Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54: 840-849.
6. Chan JR, Cosgaya JM, Wu YJ, Shooter EM. 2001. Neurotrophins are key mediators of the myelination program in the peripheral nervous system. Proc Natl Acad Sci U S A 98: 14661-14668.
7. Croft AP, Przyborski SA. 2006. Formation of neurons by non-neural adult stem cells: potential mechanism implicates an artifact of growth in culture. Stem Cells 24: 1841-1851.
8. di Summa PG, Kingham PJ, Raffoul W, Wiberg M, Terenghi G, Kalbermatten DF. 2010. Adipose-derived stem cells enhance peripheral nerve regeneration. J Plast Reconstr Aesthet Surg 63: 1544-1552.
9. di Summa PG, Kalbermatten DF, Pralong E, Raffoul W, Kingham PJ, Terenghi G. 2011. Long-term in vivo regeneration of peripheral nerves through bioengineered nerve grafts. Neuroscience 181: 278-291.
10. Eccleston PA, Mirsky R, Jessen KR, Sommer I, Schachner M. 1987. Postnatal development of rat peripheral nerves: an immunohistochemical study of membrane lipids common to non-myelin forming Schwann cells, myelin forming Schwann cells and oligodendrocytes. Brain Res 432: 249-256.
11. Erba P, Mantovani C, Kalbermatten DF, Pierer G, Terenghi G, Kingham PJ. 2010. Regeneration potential and survival of transplanted undifferentiated adipose tissue-derived stem cells in peripheral nerve conduits. J Plast Reconstr Aesthet Surg 63: e811-e817.
12. Fu SY, Gordon T. 1995. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J Neurosci 15: 3886-3895.
13. Funakoshi H, Frisen J, Barbany G, Timmusk T, Zachrisson O, Verge VM, Persson H. 1993. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123: 455-465.
14. Gimble J, Guilak F. 2003. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 5: 362-369.
15. Gordon T, Sulaiman O, Boyd JG. 2003. Experimental strategies to promote functional recovery after peripheral nerve injuries. J Peripher Nerv Syst 8: 236-250.
16. Gordon T, Tyreman N, Raji MA. 2011. The basis for diminished functional recovery after delayed peripheral nerve repair. J Neurosci 31: 5325-5334.
17. Haastert K, Mauritz C, Chaturvedi S, Grothe C. 2007. Human and rat adult Schwann cell cultures: fast and efficient enrichment and highly effective non-viral transfection protocol. Nat Protoc 2: 99-104.
18. Hare GM, Evans PJ, Mackinnon SE, Best TJ, Bain JR, Szalai JP, Hunter DA. 1992. Walking track analysis: a long-term assessment of peripheral nerve recovery. Plast Reconstr Surg 89: 251-258.
19. Heumann R, Korsching S, Bandtlow C, Thoenen H. 1987. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J Cell Biol 104: 1623-1631.
20. Hoke A, Ho T, Crawford TO, LeBel C, Hilt D, Griffin JW. 2003. Glial cell line-derived neurotrophic factor alters axon Schwann cell units and promotes myelination in unmyelinated nerve fibers. J Neurosci 23: 561-567.
21. Jessen KR, Mirsky R. 1999. Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci 22: 402-410.
22. Jessen KR, Mirsky R. 2005. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6: 671-682.
23. Jivan S, Novikova LN, Wiberg M, Novikov LN. 2006. The effects of delayed nerve repair on neuronal survival and axonal regeneration after seventh cervical spinal nerve axotomy in adult rats. Exp Brain Res 170: 245-254.
24. Kaewkhaw R, Scutt AM, Haycock JW. 2011. Anatomical site influences the differentiation of adipose-derived stem cells for Schwann-cell phenotype and function. Glia 59: 734-749.
25. Kalbermatten DF, Schaakxs D, Kingham PJ, Wiberg M. 2011. Neurotrophic activity of human adipose stem cells isolated from deep and superficial layers of abdominal fat. Cell Tissue Res 344: 251-260.
26. Keilhoff G, Goihl A, Langnase K, Fansa H, Wolf G. 2006a. Transdifferentiation of mesenchymal stem cells into Schwann cell-like myelinating cells. Eur J Cell Biol 85: 11-24.
27. Keilhoff G, Goihl A, Stang F, Wolf G, Fansa H. 2006b. Peripheral nerve tissue engineering: autologous Schwann cells vs. transdifferentiated mesenchymal stem cells. Tissue Eng 12: 1451-1465.
28. Kingham PJ, Kalbermatten DF, Mahay D, Armstrong SJ, Wiberg M, Terenghi G. 2007. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol 207: 267-274.
29. Mantovani C, Mahay D, Kingham M, Terenghi G, Shawcross SG, Wiberg M. 2010. Bone marrow- and adipose-derived stem cells show expression of myelin mRNAs and proteins. Regen Med 5: 403-410.
30. Martini R, Mohajeri MH, Kasper S, Giese KP, Schachner M. 1995. Mice doubly deficient in the genes for P0 and myelin basic protein show that both proteins contribute to the formation of the major dense line in peripheral nerve myelin. J Neurosci 15: 4488-4495.
31. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H. 1992. Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol 119: 45-54.
32. Quattrini A, Previtali S, Feltri ML, Canal N, Nemni R, Wrabetz L. 1996. Beta 4 integrin and other Schwann cell markers in axonal neuropathy. Glia 17: 294-306.
33. Roytta M, Salonen V. 1988. Long-term endoneurial changes after nerve transection. Acta Neuropathol 76: 35-45.
34. Scherer SS, Xu YT, Roling D, Wrabetz L, Feltri ML, Kamholz J. 1994. Expression of growth-associated protein-43 kD in Schwann cells is regulated by axon-Schwann cell interactions and cAMP. J Neurosci Res 38: 575-589.
35. Shea GK, Tsui AY, Chan YS, Shum DK. 2010. Bone marrow-derived Schwann cells achieve fate commitment-a prerequisite for remyelination therapy. Exp Neurol 224: 448-458.
36. Son YJ, Thompson WJ. 1995. Schwann cell processes guide regeneration of peripheral axons. Neuron 14: 125-132.
37. Stoll G, Muller HW. 1999. Nerve injury, axonal degeneration and neural regeneration: basic insights. Brain Pathol 9: 313-325.
38. Strem BM, Hicok KC, Zhu M, Wulur I, Alfonso Z, Schreiber RE, Fraser JK, Hedrick MH. 2005. Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med 54: 132-141.
39. Sulaiman OA, Gordon T. 2000. Effects of short- and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia 32: 234-246.
40. Temporin K, Tanaka H, Kuroda Y, Okada K, Yachi K, Moritomo H, Murase T, Yoshikawa H. 2008. Interleukin-1 beta promotes sensory nerve regeneration after sciatic nerve injury. Neurosci Lett 440: 130-133.
41. Terenghi G. 1999. Peripheral nerve regeneration and neurotrophic factors. J Anat 194: 1-14.
42. Tomita K, Hata Y, Kubo T, Fujiwara T, Yano K, Hosokawa K. 2009. Effects of the in vivo predegenerated nerve graft on early Schwann cell migration: quantitative analysis using S100-GFP mice. Neurosci Lett 461: 36-40.
43. Walsh SK, Gordon T, Addas BM, Kemp SW, Midha R. 2010. Skin-derived precursor cells enhance peripheral nerve regeneration following chronic denervation. Exp Neurol 223: 221-228.
44. Weir C, Morel-Kopp MC, Gill A, Tinworth K, Ladd L, Hunyor SN, Ward C. 2008. Mesenchymal stem cells: isolation, characterisation and in vivo fluorescent dye tracking. Heart Lung Circ 17: 395-403.
45. Wright KT, El Masri W, Osman A, Chowdhury J, Johnson WE. 2010. Bone marrow for the treatment of spinal cord injury: mechanisms and clinical application. Stem Cells (in press).
46. You S, Petrov T, Chung PH, Gordon T. 1997. The expression of the low affinity nerve growth factor receptor in long-term denervated Schwann cells. Glia 20: 87-100.
47. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. 2002. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13: 4279-4295.
48. Zurita M, Bonilla C, Otero L, Aguayo C, Vaquero J. 2008. Neural transdifferentiation of bone marrow stromal cells obtained by chemical agents is a short-time reversible phenomenon. Neurosci Res 60: 275-280.