Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-26T07:04:34.125Z Has data issue: false hasContentIssue false
  • English
  • Français

White Matter Repair: Skin-Derived Precursors as a Source of Myelinating Cells

Published online by Cambridge University Press:  02 December 2014

Jeff Biernaskie  and
Freda D. Miller
Jeff Biernaskie*
Affiliation:
Department of Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada.
Freda D. Miller
Affiliation:
Developmental and Stem Cell Biology Group, University of Toronto, Toronto, Ontario, Canada. Departments of Molecular and Medical Genetics and Physiology, University of Toronto, Toronto, Ontario, Canada.
*
Department of Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine, Room HM220, University of Calgary, 3300 Hospital Drive NW, Calgary, Alberta, T2N 4N1, Canada.
Rights & Permissions [Opens in a new window]

Abstract:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Stem cell based therapies hold great promise for repair and functional restoration following neurological injury and disease. Skin-derived precursors (or “SKPs”) are a novel, multipotent somatic stem cell that resides within the mammalian dermis. SKPs persist within the skin throughout adulthood and yet intriguingly, exhibit many similarities to embryonic neural crest stem cells (NCSCs). For example, SKPs give rise to both neural and mesodermal cell types, and the former appear biased to peripheral nervous system fates. As such, SKPs are capable of generating Schwann cells, the myelinating glial cell of the peripheral nervous system. Here we discuss our current understanding of the biological origin of SKPs and specifically the potential therapeutic utility of SKPs as a highly accessible and autologous source of Schwann cells for remyelination and repair of the injured or diseased nervous system.

Résumé:

RÉSUMÉ:

Les traitements à base de cellules souches pour la réparation et le rétablissement fonctionnel suite à une lésion neurologique ou à une maladie sont très prometteurs. Les précurseurs dérivés de la peau (PDP) sont de nouvelles cellules souches somatiques pluripotentes qu'on retrouve dans le derme des mammifères. Les PDP persistent dans la peau pendant toute la vie adulte et, ce qui est intriguant, présentent plusieurs caractéristiques similaires à celles des cellules souches de la crête neurale embryonnaire. À titre d'exemple, les PDP donnent naissance à des cellules de type nerveux et de type mésodermique et les premières semblent biaisées en faveur du système nerveux périphérique. Elles sont donc capables de générer des cellules de Schwann qui sont les cellules gliales myélinisantes du système nerveux périphérique. Nous discutons ici de notre compréhension actuelle de l'origine biologique des PDP et spécifiquement de leur utilité thérapeutique potentielle comme source autologue très accessibles de cellules de Schwann pour la remyélinisation et la réparation du système nerveux malade ou qui a subi une lésion.

Type
Research Article
Information
Canadian Journal of Neurological Sciences , Volume 37 , supplement S2 , September 2010 , pp. S34 - S41
Copyright
Copyright © Canadian Neurological Sciences Federation 2010

References

1. Fernandes, KJL, McKenzie, IA, Mill, P, et al. A dermal niche for mutipotent adult skin-derived precursor cells. Nature Cell Biol. 2004;6(11):1082–93.CrossRefGoogle Scholar
2. Toma, JG, Ahkavan, M, Fernandes, KJL, et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nature Cell Biol. 2001;3:778–84.CrossRefGoogle ScholarPubMed
3. Joannides, A, Gaughwin, P, Schwiening, C, et al. Efficient generation of neural precursors from adult human skin: astrocytes promote neurogenesis from skin-derived stem cells. Lancet. 2004 Jul 10–16;364(9429):172–8.CrossRefGoogle ScholarPubMed
4. McKenzie, IA, Biernaskie, J, Toma, JG, et al. Skin-derived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J Neurosci. 2006 Jun 14;26(24): 6651–60.Google ScholarPubMed
5. Gago, N, Perez-Lopez, V, Sanz-Jaka, JP, et al. Age-dependent depletion of human skin-derived progenitor cells. Stem Cells. 2009 May;27(5):1164–72.Google ScholarPubMed
6. Fernandes, KJ, Toma, JG, Miller, FD. Multipotent skin-derived precursors: adult neural crest-related precursors with therapeutic potential. Philos Trans R Soc Lond B Biol Sci. 2008 Jan 12;363(1489):185–98.CrossRefGoogle ScholarPubMed
7. Hunt, DP, Morris, PN, Sterling, J, et al. A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells. 2008 Jan;26(1): 163–72.CrossRefGoogle ScholarPubMed
8. Toma, JG, McKenzie, IA, Bagli, D, et al. Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells. 2005 Jun-Jul;23(6):727–37.CrossRefGoogle ScholarPubMed
9. Lavoie, JF, Biernaskie, JA, Chen, Y, et al. Skin-derived precursors differentiate into skeletogenic cell types and contribute to bone repair. Stem Cells Dev. 2009 Jul-Aug;18(6):893–906.CrossRefGoogle ScholarPubMed
10. Fernandes, KJ, Kobayashi, NR, Gallagher, CJ, et al. Analysis of the neurogenic potential of multipotent skin-derived precursors. Exp Neurol. 2006 Sep;201(1):32–48.Google ScholarPubMed
11. Taveggia, C, Zanazzi, G, Petrylak, A, et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron. 2005 Sep 1;47(5):681–94.Google ScholarPubMed
12. Le Douarin, N, Kalcheim, C. The neural crest. 2nd ed. Cambridge; New York: Cambridge University Press; 1999.Google Scholar
13. Dong, Z, Brennan, A, Liu, N, et al. Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron. 1995 Sep;15(3):585–96.Google ScholarPubMed
14. Jessen, KR, Mirsky, R. Embryonic Schwann cell development: the biology of Schwann cell precursors and early Schwann cells. J Anat. 1997 Nov;191 ( Pt 4):501–5.Google ScholarPubMed
15. Jessen, KR, Mirsky, R. Signals that determine Schwann cell identity. J Anat. 2002 Apr;200(4):367–76.Google ScholarPubMed
16. Meier, C, Parmantier, E, Brennan, A, et al. Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor, neurotrophin-3, and platelet-derived growth factor-BB. J Neurosci. 1999 May 15;19(10):3847–59.CrossRefGoogle ScholarPubMed
17. Leimeroth, R, Lobsiger, C, Lussi, A, et al. Membrane-bound neuregulin1 type III actively promotes Schwann cell differentiation of multipotent progenitor cells. Dev Biol. 2002 Jun 15;246(2):245–58.CrossRefGoogle ScholarPubMed
18. Shah, NM, Marchionni, MA, Isaacs, I, et al. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell. 1994 May 6;77(3):349–60.CrossRefGoogle ScholarPubMed
19. Biernaskie, J, McKenzie, IA, Toma, JG, et al. Isolation of skinderived precursors (SKPs) and differentiation and enrichment of their Schwann cell progeny. Nat Protocols. 2006;1(6):2803–12.CrossRefGoogle ScholarPubMed
20. Walsh, SK, Gordon, T, Addas, BM, et al. Skin-derived precursor cells enhance peripheral nerve regeneration following chronic denervation. Exp Neurol. 2009 May 27.Google ScholarPubMed
21. Fawcett, JW, Asher, RA. The glial scar and central nervous system repair. Brain Res Bull. 1999 Aug;49(6):377–91.Google ScholarPubMed
22. Aguayo, AJ, David, S, Bray, GM. Influences of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents. J Exp Biol. 1981 Dec;95:231–40.Google ScholarPubMed
23. David, S, Aguayo, AJ. Axonal elongation into peripheral nervous system “bridges” after central nervous system injury in adult rats. Science. 1981 Nov 20;214(4523):931–3.CrossRefGoogle ScholarPubMed
24. Barakat, DJ, Gaglani, SM, Neravetla, SR, et al. Survival, integration, and axon growth support of glia transplanted into the chronically contused spinal cord. Cell Transplant. 2005;14(4):225–40.CrossRefGoogle ScholarPubMed
25. Takami, T, Oudega, M, Bates, ML, et al. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci. 2002 Aug 1;22(15):6670–81.CrossRefGoogle Scholar
26. Schaal, SM, Kitay, BM, Cho, KS, et al. Schwann cell transplantation improves reticulospinal axon growth and forelimb strength after severe cervical spinal cord contusion. Cell Transplant. 2007;16(3):207–28.CrossRefGoogle ScholarPubMed
27. Jessen, KR, Mirsky, R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci. 2005 Sep;6(9):671–82.CrossRefGoogle ScholarPubMed
28. Biernaskie, J, Sparling, JS, Liu, J, et al. Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci. 2007 Sep 5;27(36):9545–59.Google ScholarPubMed
29. Parr, AM, Kulbatski, I, Tator, CH. Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J Neurotrauma. 2007 May;24(5):835–45.CrossRefGoogle ScholarPubMed
30. Karimi-Abdolrezaee, S, Eftekharpour, E, Wang, J, et al. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci. 2006 Mar 29;26(13):3377–89.CrossRefGoogle ScholarPubMed
31. Jessen, KR, Mirsky, R. Why do Schwann cells survive in the absence of axons? Ann N Y Acad Sci. 1999 Sep 14;883:109–15.CrossRefGoogle ScholarPubMed
32. Aggarwal, S, Pittenger, MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005 Feb 15;105(4):1815–22.CrossRefGoogle ScholarPubMed
33. Le Blanc, K, Rasmusson, I, Sundberg, B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 2004 May 1;363(9419): 1439–41.CrossRefGoogle ScholarPubMed
34. Plant, GW, Bates, ML, Bunge, MB. Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-transected spinal cord interface. Mol Cell Neurosci. 2001 Mar;17(3):471–87.CrossRefGoogle Scholar
35. Barritt, AW, Davies, M, Marchand, F, et al. Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci. 2006 Oct 18;26(42):10856–67.Google ScholarPubMed
36. Cafferty, WB, Yang, SH, Duffy, PJ, et al. Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci. 2007 Feb 28;27(9):2176–85.CrossRefGoogle ScholarPubMed
37. Liebscher, T, Schnell, L, Schnell, D, et al. Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann Neurol. 2005 Nov;58(5):706–19.CrossRefGoogle ScholarPubMed
38. Pearse, DD, Marcillo, AE, Oudega, M, et al. Transplantation of Schwann cells and olfactory ensheathing glia after spinal cord injury: does pretreatment with methylprednisolone and interleukin-10 enhance recovery? J Neurotrauma. 2004 Sep;21(9):1223–39.CrossRefGoogle ScholarPubMed
39. Hill, CE, Hurtado, A, Blits, B, et al. Early necrosis and apoptosis of Schwann cells transplanted into the injured rat spinal cord. Eur J Neurosci. 2007 Sep;26(6):1433–45.CrossRefGoogle ScholarPubMed
40. Hill, CE, Moon, LD, Wood, PM, et al. Labeled Schwann cell transplantation: cell loss, host Schwann cell replacement, and strategies to enhance survival. Glia. 2006 Feb;53(3):338–43.CrossRefGoogle ScholarPubMed
41. Pearse, DD, Sanchez, AR, Pereira, FC, et al. Transplantation of Schwann cells and/or olfactory ensheathing glia into the contused spinal cord: Survival, migration, axon association, and functional recovery. Glia. 2007 Jul;55(9):976–1000.CrossRefGoogle ScholarPubMed
42. Hofstetter, CP, Holmstrom, NA, Lilja, JA, et al. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci. 2005 Mar;8(3): 346–53.Google Scholar
43. Woodhoo, A, Sahni, V, Gilson, J, et al. Schwann cell precursors: a favourable cell for myelin repair in the Central Nervous System. Brain. 2007 Aug;130(Pt 8):2175–85.CrossRefGoogle ScholarPubMed