Skip to main content

Advertisement

SpringerLink
Log in

Aligned collagen–GAG matrix as a 3D substrate for Schwann cell migration and dendrimer-based gene delivery

  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

The development of artificial off-the-shelf conduits that facilitate effective nerve regeneration and recovery after repair of traumatic nerve injury gaps is of fundamental importance. Collagen–glycosaminoglycan (GAG) matrix mimicking Schwann cell (SC) basal lamina has been proposed as a suitable and biologically rational substrate for nerve regeneration. In the present study, we have focused on the permissiveness of this matrix type for SC migration and repopulation, as these events play an essential role in nerve remodeling. We have also demonstrated that SCs cultured within collagen–GAG matrix are compatible with non-viral dendrimer-based gene delivery, that may allow conditioning of matrix-embedded cells for future gene therapy applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Noble J, Munro CA, Prasad VSSV, Midha R. Analysis of upper and lower extremity peripheral nerve injuries in a population of patients with multiple injuries. J Trauma. 1998;45:116–22.

    Article  Google Scholar 

  2. Millesi H, Meissl G, and Berger A The interfasicular nerve-grafting of the median and ulnar nerves. J Bone Joint Surg Am. 1972; 54-A:727-750.

  3. Belkas J, Shoichet MS, Midha R. Axonal guidance channels in peripheral nerve regeneration. Oper Tech Orthop. 2005;14:190–8.

    Article  Google Scholar 

  4. Raheja A, Suri V, Suri A, Sarkar C, Srivastava A, Mohanty S, Jain KG, Sharma MC, Mallick HN, Yadav PK, Kalaivani M, Pandey RM. Dose-dependent facilitation of peripheral nerve regeneration by bone marrow-derived mononuclear cells: a randomized controlled study: laboratory investigation. J Neurosurg. 2012;117:1170–81.

    Article  Google Scholar 

  5. Shakhbazau A, Martinez JA, Xu QG, Kawasoe J, Van Minnen MJ, Midha R. Evidence for a systemic regulation of neurotrophin synthesis in response to peripheral nerve injury. J Neurochem. 2012;122:501–11.

    Article  Google Scholar 

  6. Singh B, Xu QG, Franz CK, Zhang R, Dalton C, Gordon T, Verge VM, Midha R, Zochodne DW. Accelerated axon outgrowth, guidance, and target reinnervation across nerve transection gaps following a brief electrical stimulation paradigm. J Neurosurg. 2012;116:498–512.

    Article  Google Scholar 

  7. Yang DY, Sheu ML, Su HL, Cheng FC, Chen YJ, Chen CJ, Chiu WT, Yiin JJ, Sheehan J, Pan HC. Dual regeneration of muscle and nerve by intravenous administration of human amniotic fluid-derived mesenchymal stem cells regulated by stromal cell-derived factor-1alpha in a sciatic nerve injury model. J Neurosurg. 2012;116:1357–67.

    Article  Google Scholar 

  8. Yang Y, De LL, Rives CB, Jang JH, Lin WC, Shull KR, Shea LD. Neurotrophin releasing single and multiple lumen nerve conduits. J Control Release. 2005;104:433–46.

    Article  Google Scholar 

  9. Pabari A, Yang SY, Mosahebi A, Seifalian AM. Recent advances in artificial nerve conduit design: strategies for the delivery of luminal fillers. J Control Release. 2011;156:2–10.

    Article  Google Scholar 

  10. Tan A, Rajadas J, Seifalian AM. Biochemical engineering nerve conduits using peptide amphiphiles. J Control Release. 2012;163:342–52.

    Article  Google Scholar 

  11. Sun M, McGowan M, Kingham PJ, Terenghi G, Downes S. Novel thin-walled nerve conduit with microgrooved surface patterns for enhanced peripheral nerve repair. J Mater Sci Mater Med. 2010;21:2765–74.

    Article  Google Scholar 

  12. Chen X, Yang Y, Yao J, Lin W, Li Y, Chen Y, Gao Y, Yang Y, Gu X, Wang X. Bone marrow stromal cells-loaded chitosan conduits promote repair of complete transection injury in rat spinal cord. J Mater Sci Mater Med. 2011;22:2347–56.

    Article  Google Scholar 

  13. Zheng L, Cui HF. Enhancement of nerve regeneration along a chitosan conduit combined with bone marrow mesenchymal stem cells. J Mater Sci Mater Med. 2012;23:2291–302.

    Article  Google Scholar 

  14. Mobasseri SA, Terenghi G, Downes S. Micro-structural geometry of thin films intended for the inner lumen of nerve conduits affects nerve repair. J Mater Sci Mater Med. 2013;24:1639–47.

    Article  Google Scholar 

  15. Kehoe S, Zhang XF, Boyd D. Composition–property relationships for an experimental composite nerve guidance conduit: evaluating cytotoxicity and initial tensile strength. J Mater Sci Mater Med. 2011;22:945–59.

    Article  Google Scholar 

  16. Yahyouche A, Zhidao X, Triffitt JT, Czernuszka JT, Clover AJ. Improved angiogenic cell penetration in vitro and in vivo in collagen scaffolds with internal channels. J Mater Sci Mater Med. 2013;24:1571–80.

    Article  Google Scholar 

  17. Steele TW, Huang CL, Nguyen E, Sarig U, Kumar S, Widjaja E, Loo JS, Machluf M, Boey F, Vukadinovic Z, Hilfiker A, Venkatraman SS. Collagen–cellulose composite thin films that mimic soft-tissue and allow stem-cell orientation. J Mater Sci Mater Med. 2013;24:2013–27.

    Article  Google Scholar 

  18. Archibald SJ, Shefner J, Krarup C, Madison RD. Monkey median nerve repaired by nerve graft or collagen nerve guide tube. J Neurosci. 1995;15:4109–23.

    Google Scholar 

  19. Kemp SWP, Syed S, Walsh SK, Zochodne DW, Midha R. Collagen nerve conduits promote enhanced axonal regeneration, Schwann cell association, and neovascularization compared to silicone conduits. Tissue Eng A. 2009;15(8):1975–88.

    Article  Google Scholar 

  20. Archibald SJ, Krarup C, Shefner J, Li ST, Madison RD. A collagen-based nerve guide conduit for peripheral nerve repair: an electrophysiological study of nerve regeneration in rodents and nonhuman primates. J Comp Neurol. 1991;306:685–96.

    Article  Google Scholar 

  21. Mahmood A, Wu H, Qu C, Xiong Y, Chopp M. Effects of treating traumatic brain injury with collagen scaffolds and human bone marrow stromal cells on sprouting of corticospinal tract axons into the denervated side of the spinal cord. J Neurosurg. 2013;118:381–9.

    Article  Google Scholar 

  22. Aronson JP, Mitha AP, Hoh BL, Auluck PK, Pomerantseva I, Vacanti JP, Ogilvy CS. A novel tissue engineering approach using an endothelial progenitor cell-seeded biopolymer to treat intracranial saccular aneurysms. J Neurosurg. 2012;117:546–54.

    Article  Google Scholar 

  23. Hudson AR, Morris J, Weddell G, Drury A. Peripheral nerve autografts. J Surg Res. 1972;12:267–74.

    Article  Google Scholar 

  24. Zhao Q, Dahlin LB, Kanje M, Lundborg G. The formation of a ‘pseudo-nerve’ in silicone chambers in the absence of regenerating axons. Brain Res. 1992;592:106–14.

    Article  Google Scholar 

  25. Richardson PM. Neurotrophic factors in regeneration. Curr Opin Neurobiol. 1991;1:401–6.

    Article  Google Scholar 

  26. Brushart TME. In: Gelberman RH, editor. Operative nerve repair and reconstruction. Philadelphia: J.B. Lippincott; 1991. p. 215–30.

    Google Scholar 

  27. Martini R. Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J Neurocytol. 1994;23:1–28.

    Article  Google Scholar 

  28. Fu SY, Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol. 1997;14:67–116.

    Article  Google Scholar 

  29. Chen YY, McDonald D, Cheng C, Magnowski B, Durand J, Zochodne DW. Axon and Schwann cell partnership during nerve regrowth. J Neuropathol Exp Neurol. 2005;64:613–22.

    Article  Google Scholar 

  30. Lavdas AA, Franceschini I, Dubois-Dalcq M, Matsas R. Schwann cells genetically engineered to express PSA show enhanced migratory potential without impairment of their myelinating ability in vitro. Glia. 2006;53:868–78.

    Article  Google Scholar 

  31. Hu Y, Leaver SG, Plant GW, Hendriks WT, Niclou SP, Verhaagen J, Harvey AR, Cui Q. Lentiviral-mediated transfer of CNTF to Schwann cells within reconstructed peripheral nerve grafts enhances adult retinal ganglion cell survival and axonal regeneration. Mol Ther. 2005;11:906–15.

    Article  Google Scholar 

  32. Bachelin C, Zujovic V, Buchet D, Mallet J, Baron-Van EA. Ectopic expression of polysialylated neural cell adhesion molecule in adult macaque Schwann cells promotes their migration and remyelination potential in the central nervous system. Brain. 2010;133:406–20.

    Article  Google Scholar 

  33. Weidner N, Blesch A, Grill RJ, Tuszynski MH. Nerve growth factor-hypersecreting Schwann cell grafts augment and guide spinal cord axonal growth and remyelinate central nervous system axons in a phenotypically appropriate manner that correlates with expression of L1. J Comp Neurol. 1999;413:495–506.

    Article  Google Scholar 

  34. Walsh S, Biernaskie J, Kemp SW, Midha R. Supplementation of acellular nerve grafts with skin derived precursor cells promotes peripheral nerve regeneration. Neuroscience. 2009;164:1097–107.

    Article  Google Scholar 

  35. Komiyama T, Nakao Y, Toyama Y, Asou H, Vacanti CA, Vacanti MP. A novel technique to isolate adult Schwann cells for an artificial nerve conduit. J Neurosci Methods. 2003;122:195–200.

    Article  Google Scholar 

  36. Yannas IV, Lee E, Orgill DP, Skrabut EM, Murphy GF. Synthesis and characterization of a model extracellular matrix that induces partial regeneration of adult mammalian skin. Proc Natl Acad Sci USA. 1989;86:933–7.

    Article  Google Scholar 

  37. Szulc J, Wiznerowicz M, Sauvain MO, Trono D, Aebischer P. A versatile tool for conditional gene expression and knockdown. Nat Methods. 2006;3:109–16.

    Article  Google Scholar 

  38. Shakhbazau A, Shcharbin D, Petyovka N, Goncharova N, Seviaryn I, Kosmacheva S, Bryszewska M, Potapnev M. Non-virally modified human mesenchymal stem cells produce ciliary neurotrophic factor in biodegradable fibrin-based 3D scaffolds. J Pharm Sci. 2012;101:1546–54.

    Article  Google Scholar 

  39. Parrinello S, Napoli I, Ribeiro S, Wingfield DP, Fedorova M, Parkinson DB, Doddrell RD, Nakayama M, Adams RH, Lloyd AC. EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell. 2010;143:145–55.

    Article  Google Scholar 

  40. Napoli I, Noon LA, Ribeiro S, Kerai AP, Parrinello S, Rosenberg LH, Collins MJ, Harrisingh MC, White IJ, Woodhoo A, Lloyd AC. A central role for the ERK-signaling pathway in controlling Schwann cell plasticity and peripheral nerve regeneration in vivo. Neuron. 2012;73:729–42.

    Article  Google Scholar 

  41. Tohill MP, Mann DJ, Mantovani CM, Wiberg M, Terenghi G. Green fluorescent protein is a stable morphological marker for Schwann cell transplants in bioengineered nerve conduits. Tissue Eng. 2004;10:1359–67.

    Article  Google Scholar 

  42. Weber N, Ortega P, Clemente MI, Shcharbin D, Bryszewska M, de la Mata FJ, Gomez R, Munoz-Fernandez MA. Characterization of carbosilane dendrimers as effective carriers of siRNA to HIV-infected lymphocytes. J Control Release. 2008;132:55–64.

    Article  Google Scholar 

  43. Shcharbin D, Pedziwiatr E, Nowacka O, Kumar M, Zaborski M, Ortega P, de la Mata FJ, Gomez R, Munoz-Fernandez MA, Bryszewska M. Carbosilane dendrimers NN8 and NN16 form a stable complex with siGAG1. Colloids Surf B. 2011;83:388–91.

    Article  Google Scholar 

  44. Shakhbazau A, Shcharbin D, Bryszewska M, Kumar R, Wobma HM, Kallos MS, Goncharova N, Seviaryn I, Kosmacheva S, Potapnev M, Midha R. Non-viral engineering of skin precursor-derived Schwann cells for enhanced NT-3 production in adherent and microcarrier culture. Curr Med Chem. 2012;19:5572–9.

    Article  Google Scholar 

  45. Santos JL, Oramas E, Pego AP, Granja PL, Tomas H. Osteogenic differentiation of mesenchymal stem cells using PAMAM dendrimers as gene delivery vectors. J Control Release. 2009;134:141–8.

    Article  Google Scholar 

  46. Schlosshauer B, Dreesmann L, Schaller HE, Sinis N. Synthetic nerve guide implants in humans: a comprehensive survey. Neurosurgery. 2006;59(4):740–7.

    Article  Google Scholar 

  47. Armstrong SJ, Wiberg M, Terenghi G, Kingham PJ. Laminin activates NF-kappaB in Schwann cells to enhance neurite outgrowth. Neurosci Lett. 2008;439:42–6.

    Article  Google Scholar 

  48. Webber C, Zochodne D. The nerve regenerative microenvironment: early behavior and partnership of axons and Schwann cells. Exp Neurol. 2010;223:51–9.

    Article  Google Scholar 

  49. Lee JY, Giusti G, Friedrich PF, Archibald SJ, Kemnitzer JE, Patel J, Desai N, Bishop AT, Shin AY. The effect of collagen nerve conduits filled with collagen–glycosaminoglycan matrix on peripheral motor nerve regeneration in a rat model. J Bone Jt Surg Am. 2012;94:2084–91.

    Article  Google Scholar 

  50. Chamberlain LJ, Yannas IV, Hsu HP, Strichartz G, Spector M. Collagen–GAG substrate enhances the quality of nerve regeneration through collagen tubes up to level of autograft. Exp Neurol. 1998;154:315–29.

    Article  Google Scholar 

  51. Chamberlain LJ, Yannas IV, Hsu HP, Strichartz GR, Spector M. Near-terminus axonal structure and function following rat sciatic nerve regeneration through a collagen–GAG matrix in a ten-millimeter gap. J Neurosci Res. 2000;60:666–77.

    Article  Google Scholar 

  52. Harley BA, Kim HD, Zaman MH, Yannas IV, Lauffenburger DA, Gibson LJ. Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions. Biophys J. 2008;95:4013–24.

    Article  Google Scholar 

  53. Zochodne D. Neurobiology of peripheral nerve regeneration. 1st ed. New York: Cambridge University Press; 2008.

    Book  Google Scholar 

  54. Harrisingh MC, Perez-Nadales E, Parkinson DB, Malcolm DS, Mudge AW, Lloyd AC. The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation. EMBO J. 2004;23:3061–71.

    Article  Google Scholar 

  55. Pieper JS, van Wachem PB, van Luyn MJA, Brouwer LA, Hafmans T, Veerkamp JH, van Kuppevelt TH. Attachment of glycosaminoglycans to collagenous matrices modulates the tissue response in rats. Biomaterials. 2000;21:1689–99.

    Article  Google Scholar 

  56. Liu J, Chau CH, Liu H, Jang BR, Li X, Chan YS, Shum DK. Upregulation of chondroitin 6-sulphotransferase-1 facilitates Schwann cell migration during axonal growth. J Cell Sci. 2006;119:933–42.

    Article  Google Scholar 

  57. Cragnolini AB, Friedman WJ. The function of p75NTR in glia. Trends Neurosci. 2008;31:99–104.

    Article  Google Scholar 

  58. Roux PP, Barker PA. Neurotrophin signaling through the p75 neurotrophin receptor. Prog Neurobiol. 2002;67:203–33.

    Article  Google Scholar 

  59. Taniuchi M, Clark HB, Johnson EM Jr. Induction of nerve growth factor receptor in Schwann cells after axotomy. Proc Natl Acad Sci USA. 1986;83:4094–8.

    Article  Google Scholar 

  60. Notterpek L. Neurotrophins in myelination: a new role for a puzzling receptor. Trends Neurosci. 2003;26:232–4.

    Article  Google Scholar 

  61. Khursigara G, Bertin J, Yano H, Moffett H, DiStefano PS, Chao MV. A prosurvival function for the p75 receptor death domain mediated via the caspase recruitment domain receptor-interacting protein 2. J Neurosci. 2001;21:5854–63.

    Google Scholar 

  62. Cosgaya JM, Chan JR, Shooter EM. The neurotrophin receptor p75NTR as a positive modulator of myelination. Science. 2002;298:1245–8.

    Article  Google Scholar 

  63. Yamashita T, Tucker KL, Barde YA. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron. 1999;24:585–93.

    Article  Google Scholar 

  64. Fernandez-Valle C, Gorman D, Gomez AM, Bunge MB. Actin plays a role in both changes in cell shape and gene-expression associated with Schwann cell myelination. J Neurosci. 1997;17:241–50.

    Google Scholar 

  65. Bentley CA, Lee KF. p75 is important for axon growth and Schwann cell migration during development. J Neurosci. 2000;20:7706–15.

    Google Scholar 

  66. Anton ES, Weskamp G, Reichardt LF, Matthew WD. Nerve growth factor and its low-affinity receptor promote Schwann cell migration. Proc Natl Acad Sci USA. 1994;91:2795–9.

    Article  Google Scholar 

  67. Sachs BD, Baillie GS, McCall JR, Passino MA, Schachtrup C, Wallace DA, Dunlop AJ, MacKenzie KF, Klussmann E, Lynch MJ, Sikorski SL, Nuriel T, Tsigelny I, Zhang J, Houslay MD, Chao MV, Akassoglou K. p75 neurotrophin receptor regulates tissue fibrosis through inhibition of plasminogen activation via a PDE4/cAMP/PKA pathway. J Cell Biol. 2007;177:1119–32.

    Article  Google Scholar 

  68. Gordon T, Brushart TM, Amirjani N, Chan KM. The potential of electrical stimulation to promote functional recovery after peripheral nerve injury—comparisons between rats and humans. Acta Neurochir Suppl. 2007;100:3–11.

    Article  Google Scholar 

  69. Bianchi BR, Zhang XF, Reilly RM, Kym PR, Yao BB, Chen J. Species comparison and pharmacological characterization of human, monkey, rat and mouse TRPA1 channels. J Pharmacol Exp Ther. 2012;341(2):360–8.

    Article  Google Scholar 

  70. Harries LW, Brown JE, Gloyn AL. Species-specific differences in the expression of the HNF1A, HNF1B and HNF4A genes. PLoS ONE. 2009;4:e7855.

    Article  Google Scholar 

  71. Holden PR, Tugwood JD. Peroxisome proliferator-activated receptor alpha: role in rodent liver cancer and species differences. J Mol Endocrinol. 1999;22:1–8.

    Article  Google Scholar 

  72. Shakhbazau A, Shcharbin D, Seviaryn I, Goncharova N, Kosmacheva S, Potapnev M, Bryszewska M, Kumar R, Biernaskie J, Midha R. Dendrimer-driven neurotrophin expression differs in temporal patterns between rodent and human stem cells. Mol Pharm. 2012;9:1521–8.

    Google Scholar 

  73. Gassmann K, Abel J, Bothe H, Haarmann-Stemmann T, Merk HF, Quasthoff KN, Rockel TD, Schreiber T, Fritsche E. Species-specific differential AhR expression protects human neural progenitor cells against developmental neurotoxicity of PAHs. Environ Health Perspect. 2010;118:1571–7.

    Article  Google Scholar 

  74. Smith AM, Dragunow M. The human side of microglia. Trends Neurosci. 2014;37:125–35.

    Article  Google Scholar 

  75. Steffenhagen C, Kraus S, Dechant FX, Kandasamy M, Lehner B, Poehler AM, Furtner T, Siebzehnrubl FA, Couillard-Despres S, Strauss O, Aigner L, Rivera FJ. Identity, fate and potential of cells grown as neurospheres: species matters. Stem Cell Rev. 2011;7:815–35.

    Article  Google Scholar 

  76. Granowitz C, Berkowitz RD, Goff SP. Mutations affecting the cytoplasmic domain of the Moloney murine leukemia virus envelope protein: rapid reversion during replication. Virus Res. 1996;41:25–42.

    Article  Google Scholar 

  77. Taddeo B, Carlini F, Verani P, Engelman A. Reversion of a human immunodeficiency virus type 1 integrase mutant at a second site restores enzyme function and virus infectivity. J Virol. 1996;70:8277–84.

    Google Scholar 

  78. Kang HC, Huh KM, Bae YH. Polymeric nucleic acid carriers: current issues and novel design approaches. J Control Release. 2012;164:256–64.

    Article  Google Scholar 

  79. Dandekar P, Jain R, Keil M, Loretz B, Muijs L, Schneider M, Auerbach D, Jung G, Lehr CM, Wenz G. Cellular delivery of polynucleotides by cationic cyclodextrin polyrotaxanes. J Control Release. 2012;164:387–93.

    Article  Google Scholar 

  80. Martello F, Piest M, Engbersen JF, Ferruti P. Effects of branched or linear architecture of bioreducible poly(amido amine)s on their in vitro gene delivery properties. J Control Release. 2012;164:372–9.

    Article  Google Scholar 

  81. Bonner DK, Zhao X, Buss H, Langer R, Hammond PT. Crosslinked linear polyethylenimine enhances delivery of DNA to the cytoplasm. J Control Release. 2013;167:101–7.

    Article  Google Scholar 

  82. Tomalia DA. Dendrimer research. Science. 1991;252:1231.

    Article  Google Scholar 

  83. Pandita D, Santos JL, Rodrigues J, Pego AP, Granja PL, Tomas H. Gene delivery into mesenchymal stem cells: a biomimetic approach using RGD nanoclusters based on poly(amidoamine) dendrimers. Biomacromolecules. 2011;12:472–81.

    Article  Google Scholar 

  84. Shakhbazau AV, Shcharbin DG, Goncharova NV, Seviaryn IN, Kosmacheva SM, Kartel NA, Bryszewska M, Majoral JP, Potapnev MP. Neurons and stromal stem cells as targets for polycation-mediated transfection. Bull Exp Biol Med. 2011;151:126–9.

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by CIHR Grant #163322, by the Center for Excellence in Nerve Regeneration (partnership between the Hotchkiss Brain Institute, University of Calgary and Integra LifeSciences), and by Alberta Innovates-Health Solutions (fellowship support for A.S.). The authors thank Ranjan Kumar and Indranil Dey for their kind assistance.

Author information

Authors and Affiliations

  1. Department of Clinical Neuroscience, Faculty of Medicine, University of Calgary, HMRB 109-3330 Hospital Drive NW, Calgary, AB, T2N4N1, Canada

    Antos Shakhbazau & Rajiv Midha

  2. Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada

    Antos Shakhbazau & Rajiv Midha

  3. Integra LifeSciences Corporation, Plainsboro, NJ, USA

    Simon J. Archibald

  4. Institute of Biophysics and Cell Engineering, National Academy of Sciences of Belarus, Minsk, Belarus

    Dzmitry Shcharbin

  5. Department of General Biophysics, University of Lodz, Lodz, Poland

    Maria Bryszewska

Authors
  1. Antos Shakhbazau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simon J. Archibald
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dzmitry Shcharbin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Bryszewska
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rajiv Midha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antos Shakhbazau.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 549 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shakhbazau, A., Archibald, S.J., Shcharbin, D. et al. Aligned collagen–GAG matrix as a 3D substrate for Schwann cell migration and dendrimer-based gene delivery. J Mater Sci: Mater Med 25, 1979–1989 (2014). https://doi.org/10.1007/s10856-014-5224-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10856-014-5224-2

Keywords

Search

Navigation