Nanomedicine: Nanotechnology, Biology and Medicine
Volume 3, Issue 4 , Pages 311-321 , December 2007

Reknitting the injured spinal cord by self-assembling peptide nanofiber scaffold

  • Jiasong Guo, PhD

      Affiliations

    • Department of Anatomy, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • Department of Histology and Embryology, Southern Medical University, Guangzhou, China
    • ,
  • Huanxing Su, MD

      Affiliations

    • Department of Anatomy, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • ,
  • Yuanshan Zeng, MD, PhD

      Affiliations

    • Department of Histology and Embryology, Zhongshan Medical College, Sun Yat-sen University, Guangzhou, China
    • ,
  • Yu-Xiang Liang, PhD

      Affiliations

    • Department of Anatomy, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • State Key Laboratory for Brain and Cognitive Sciences, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • ,
  • Wai Man Wong, MS

      Affiliations

    • Department of Anatomy, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • ,
  • Rutledge G. Ellis-Behnke, PhD

      Affiliations

    • Department of Anatomy, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • State Key Laboratory for Brain and Cognitive Sciences, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
    • ,
  • Kwok-Fai So, PhD

      Affiliations

    • Department of Anatomy, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • State Key Laboratory for Brain and Cognitive Sciences, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • Research Centre of Heart, Brain, Hormone and Healthy Aging, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • ,
  • Wutian Wu, MD, PhD

      Affiliations

    • Department of Anatomy, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • State Key Laboratory for Brain and Cognitive Sciences, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • Research Center of Reproduction, Development and Growth, The University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China
    • Corresponding Author InformationCorresponding author. Department of Anatomy, University of Hong Kong Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong SAR, China.

Received 1 July 2007 ,Accepted 20 September 2007.

References 

  1. Schwab ME, Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev. 1996;76:319–370
  2. Dusart I, Schwab ME. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci. 1994;6:712–724
  3. Hulsebosch C. Recent advances in pathophysiology and treatment of spinal cord injury. Adv Physiol Educ. 2002;26:238–255
  4. Lu P, Jones L, Snyder E, Tuszynsky M. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol. 2003;181:115–129
  5. Vroemen M, Aigner L, Winkler J, Weidner N. Adult neural progenitor cells grafts survival after acute spinal cord injury and integrate along axonal pathways. Eur J Neurosci. 2003;18:743–751
  6. Deumens R, Koopmans GC, Honig WM, Maquet V, Jerome R, Steinbusch HW, et al. Chronically injured corticospinal axons do not cross large spinal lesion gaps after a multifactorial transplantation strategy using olfactory ensheathing cell/olfactory nerve fibroblast-biomatrix bridges. J Neurosci Res. 2006;83:811–820
  7. Reier PJ, Stokes BT, Thompson FJ, Anderson DK. Fetal cell grafts into resection and contusion/compression injuries of the rat and cat spinal cord. Exp Neurol. 1992;115:177–188
  8. David S, Aguayo A. Axonal elongation into peripheral nervous system “bridges” after central nervous system injury in adult rats. Science. 1981;215:931–933
  9. Oudega M, Xu X. SC transplantation for repair of the adult spinal cord. J Neurotrauma. 2006;23:453–467
  10. Li Y, Decherchi P, Raisman G. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J Neurosci. 2003;23:727–731
  11. Mcdonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D, et al. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med. 1999;5:1410–1412
  12. Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ, et al. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A. 2002;99:2199–2204
  13. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Morshead C, Fehlings M. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci. 2006;26:3377–3389
  14. Guo JS, Zeng YS, Li H, Huang WL, Liu RY, Li XB, et al. Co-transplant of neural stem cells and NT-3 gene modified Schwann cells promote the recovery of transected spinal cord injury. Spinal Cord. 2007;45:15–24
  15. Mitsui T, Fischer I, Shumsky JS, Murray M. Transplants of fibroblasts expressing BDNF and NT-3 promote recovery of bladder and hindlimb function following spinal contusion injury in rats. Exp Neurol. 2005;194:410–431
  16. Schmidt C, Leach J. Neural tissue engineering: strategies for repair and regeneration. Ann Rev Eng. 2003;5:295–347
  17. Geller H, Fawcett J. Building a bridge: engineering spinal cord repair. Exp Neurol. 2002;174:125–136
  18. Scott M, Will R, Ironside J, Nguyen H, Tremblay P, DeArmond S, et al. Compelling transgenetic evidence for transmission of bovine spongiform encephalopathy prions to humans. Proc Natl Acad Sci U S A. 1999;96:15137–15142
  19. Holmes T. Novel peptide-based biomaterial scaffolds for tissue engineering. Trends Biotechnol. 2002;20:16–21
  20. Nomura H, Tator C, Shoichet M. Bioengineered strategies for spinal cord repair. J Neurotrauma. 2006;23:496–507
  21. Moore M, Friedman J, Lewellyn E, Mantila S, Krych A, Ameenuddin S, et al. Multiple-channel scaffolds to promote spinal cord axon regeneration. Biomaterials. 2006;27:419–429
  22. Zhang S, Gelain F, Zhao X. Designer self-assembling peptide nanofiber scaffolds for 3D tissue cell cultures. Semin Cancer Biol. 2005;15:413–420
  23. Stokols S, Tuszynski M. Freeze-dried agarose scaffolds with uniaxial channels stimulate and guide linear axonal growth following spinal cord injury. Biomaterials. 2006;27:443–451
  24. Prang P, Muller R, Eljaouhari A, Heckmann K, Kunz W, Weber T, et al. The promotion of oriented axonal regrowth in the injured spinal cord by alginate-based anisotropic capillary hydrogels. Biomaterials. 2006;27:3560–3569
  25. Ellis-Behnke RG, Liang YX, You SW, Tay DK, Zhang S, So K, et al. Nano neuro knitting: peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. Proc Natl Acad Sci U S A. 2006;103:5054–5059
  26. Lupi O. Prions in dermatology. J Am Acad Dermatol. 2002;46:790–793
  27. Holmes T, Lacalle S, Su X, Liu G, Rich A, Zhang S. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc Natl Acad Sci U S A. 2000;97:6728–6733
  28. Zhang S. Fabrication of novel biomaterials through molecular self-assembly. Nat Biotechnol. 2003;21:1171–1178
  29. Garreta E, Genove E, Borros S, Semino C. Osteogenic differentiation of mouse embryonic stem cells and mouse embryonic fibroblasts in a three-dimensional self-assembling peptide scaffold. Tissue Eng. 2006;12:2215–2227
  30. Davis M, Hsieh P, Takahashi T, Song Q, Zhang S, Kamm R, et al. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc Natl Acad Sci U S A. 2006;103:8055–8060
  31. Zhang S, Holmes T, Lockshin C, Rich A. Spontaneous assembly of a self-complementary oligopeptide to form a stable macroscopic membrane. Proc Natl Acad Sci U S A. 1993;90:3334–3338
  32. Zhang S, Holmes T, DiPersio C, Hynes R, Su X, Rich A. Self-complementary oligopeptide matrices support mammalian cell attachment. Biomaterials. 1995;16:1385–1393
  33. Caplan M, Moore P, Zhang S, Kamm R, Lauffenburger D. Self-assembly of a beta-sheet oligopeptide is governed by electrostatic repulsion. Biomacromolecules. 2000;1:627–631
  34. Marini D, Hwang W, Lauffenburger D, Zhang S, Kamm D. Left-handed helical ribbon intermediates in the self-assembly of a β-sheet peptide. Nano Lett. 2002;2:295–299
  35. Morrissey TK, Kleitman N, Bunge RP. Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J Neurosci. 1991;11:2433–2442
  36. Xu XM, Guénard V, Kleitman N, Bunge M. Axonal regeneration into SC-seeded guidance channels grafted into transected adult rat spinal cord. J Comp Neurol. 1995;351:145–160
  37. Johe KK, Hazel TG, Muller T, Dugich-Djordjevic MM, Mckay RD. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 1996;10:3129–3140
  38. Enomoto M, Shinomiya K, Okabe S. Migration and differentiation of neural progenitor cells from two different regions of embryonic central nervous system after transplantation into the intact spinal cord. Eur J Neurosci. 2003;17:1223–1232
  39. Challa VR, Moody DM, Brown WR, Zagzag D. A morphologic study of the vasculature of malignant gliomas using thick celloidin sections and alkaline phosphatase stain. Clin Neuropathol. 2004;23:167–172
  40. Hsu JY, Xu XM. Early profiles of axonal growth and astroglial response after spinal cord hemisection and implantation of Schwann cell-seeded guidance channels in adult rats. J Neurosci Res. 2005;82:472–483
  41. Kamada T, Koda M, Dezawa M, Yoshinaga K, Hashimoto M, Koshizuka S, et al. Transplantation of bone marrow stromal cell–derived Schwann cells promotes axonal regeneration and functional recovery after complete transection of adult rat spinal cord. J Neuropathol Exp Neurol. 2005;64:37–45
  42. Burge M, Pearse D. Transplantation strategies to promote repair of the injured spinal cord. J Rehabil Res Dev. 2003;40:55–62
  43. Teng Y, Lavik E, Qu X, Park K, Ourednik J, Zurakowski D, et al. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc Natl Acad Sci U S A. 2002;99:3024–3029
  44. Patista C, Mulder M, Gautier S, Maquet V, Jerome R, Oudega M. Freeze-dried poly(d,l-lactic acid) macroporous guidance scaffolds impregnated with brain-derived neurotrophic factor in the transected adult rat thoracic spinal cord. Biomaterials. 2004;25:1569–1582
  45. Ellis-Behnke RG, Liang YX, Tay DK, Kau PF, Schneider GE, Zhang S, et al. Nano hemostat solution: immediate hemostasis at the nanoscale. Nanomedicine. 2006;2:207–215
  46. Zeng YS, Ding Y, Wu LZ, Guo JS, Li HB, Wong WM, et al. Co-transplantation of SC promotes the survival and differentiation of neural stem cells transplanted into the injured spinal cord. Dev Neurosci. 2005;27:20–26
  47. Enzmann G, Benton R, Talbott J, Cao Q, Whittemore S. Functional considerations of stem cell transplantation therapy for spinal cord repair. J Neurotrauma. 2006;23:479–495
  48. Toda H, Tsuji M, Nakano I, Kobuke K, Hayashi T, Kasahara H, et al. Stem cell–derived neural stem/progenitor cell supporting factor is an autocrine/paracrine survival factor for adult neural stem/progenitor cells. J Biol Chem. 2003;278:35491–35500
  49. Silva G, Czeisler C, Niece K, Beniash E, Harrington D, Kessler J, et al. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science. 2004;303:1352–1355

 R.G.E.-B. has a financial interest in Clear Nano Solutions, Inc. and in 3D Matrix, manufacturer of the material distributed by BD Biosciences.

PII: S1549-9634(07)00123-2

doi: 10.1016/j.nano.2007.09.003

Nanomedicine: Nanotechnology, Biology and Medicine
Volume 3, Issue 4 , Pages 311-321 , December 2007

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