Human embryonic stem cell-derived neural precursor transplants in collagen scaffolds promote recovery in injured rat spinal cord

References

• Ben-Hur T, Idelson M, Khaner H, Pera M, Reinhartz E, Itzik A, et al. Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats. Stem Cells. 2004; 22:1246–55.
   PubMed Web of Science ®Google Scholar
• Roy NS, Cleren C, Singh SK, Yang L, Beal MF, Goldman SA. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat Med. 2006; 12:1259–68.
   PubMed Web of Science ®Google Scholar
• Haruta M, Sasai Y, Kawasaki H, Amemiya K, Ooto S, Kitada M, et al. In vitro and in vivo characterization of pigment epithelial cells differentiated from primate embryonic stem cells. Invest Ophthalmol Vis Sci. 2004; 45:1020–5.
   PubMed Web of Science ®Google Scholar
• Lund RD, Wang S, Klimanskaya I, Holmes T, Ramos-Kelsey R, Lu B, et al. Human embryonic stem cell-derived cells rescue visual function in dystrophic RCS rats. Cloning Stem Cells. 2006; 8:189–99.
   PubMedGoogle Scholar
• 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; 5:1410–2.
   PubMed Web of Science ®Google Scholar
• Kerr DA, Llado J, Shamblott MJ, Maragakis NJ, Irani DN, Crawford TO, et al. Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J Neurosci. 2003; 23:5131–40.
   PubMed Web of Science ®Google Scholar
• Chiba S, Iwasaki Y, Sekino H, Suzuki N. Transplantation of motoneuron-enriched neural cells derived from mouse embryonic stem cells improves motor function of hemiplegic mice. Cell Transplant. 2003; 12:457–68.
   Google Scholar
• Deshpande DM, Kim YS, Martinez T, Carmen J, Dike S, Shats I, et al. Recovery from paralysis in adult rats using embryonic stem cells. Ann Neurol. 2006; 60:32–44.
   PubMed Web of Science ®Google Scholar
• McDonald JW, Becker D, Holekamp TF, Howard M, Liu S, Lu A, et al. Repair of the injured spinal cord and the potential of embryonic stem cell transplantation. J Neurotrauma. 2004; 21:383–93.
   PubMed Web of Science ®Google Scholar
• Cai C, Grabel L. Directing the differentiation of embryonic stem cells to neural stem cells. Dev Dyn. 2007; 236:3255–66.
   PubMed Web of Science ®Google Scholar
• Kulbatski I, Mothe AJ, Nomura H, Tator CH. Endogenous and exogenous CNS derived stem/progenitor cell approaches for neurotrauma. Curr Drug Targets. 2005; 6:111–26.
   PubMed Web of Science ®Google Scholar
• Hosseinkhani H, Hosseinkhani M, Tian F, Kobayashi H, Tabata Y. Osteogenic differentiation of mesenchymal stem cells in self-assembled peptide-amphiphile nanofibers. Biomaterials. 2006; 27:4079–86.
   PubMed Web of Science ®Google Scholar
• Hosseinkhani H, Hosseinkhani M, Kobayashi H. Proliferation and differentiation of mesenchymal stem cells using self-assembled peptide amphiphile nanofibers. Biomed Mater. 2006; 1:8–15.
   PubMed Web of Science ®Google Scholar
• Hosseinkhani H, Hosseinkhani M, Tian F, Kobayashi H, Tabata Y. Bone regeneration on a collagen sponge self-assembled peptide-amphiphile nanofiber hybrid scaffold. Tissue Eng. 2007; 13:11–9.
   PubMedGoogle Scholar
• Baharvand H, Mehrjardi NZ, Hatami M, Kiani S, Rao M, Haghighi MM. Neural differentiation from human embryonic stem cells in a defined adherent culture condition. Int J Dev Biol. 2007; 51:371–8.
   PubMed Web of Science ®Google Scholar
• Teng YD, Lavik EB, Qu X, Park KI, 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 USA. 2002; 99:3024–9.
   PubMed Web of Science ®Google Scholar
• Park KI, Teng YD, Snyder EY. The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue. Nat Biotechnol. 2002; 20:1111–7.
   PubMed Web of Science ®Google Scholar
• Silva GA, Czeisler C, Niece KL, Beniash E, Harrington DA, Kessler JA, et al. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science. 2004; 303:1352–5.
   PubMed Web of Science ®Google Scholar
• Hosseinkhani H, Hosseinkhani M, Tian F, Kobayashi H, Tabata Y. Ectopic bone formation in collagen sponge self-assembled peptide–amphiphile nanofibers hybrid scaffold in a perfusion culture bioreactor. Biomaterials. 2006; 27:5089–98.
   PubMed Web of Science ®Google Scholar
• Baharvand H, Ashtiani SK, Taee A, Massumi M, Valojerdi MR, Yazdi PE, et al. Generation of new human embryonic stem cell lines with diploid and triploid karyotypes. Dev Growth Differ. 2006; 48:117–28.
   PubMed Web of Science ®Google Scholar
• Levenstein ME, Ludwig TE, Xu RH, Llanas RA, VanDenHeuvel-Kramer K, Manning D, et al. Basic fibroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells. 2006; 24:568–74.
   PubMed Web of Science ®Google Scholar
• Cohen MA, Itsykson P, Reubinoff BE. Neural differentiation of human ES cells. Curr Protoc Cell Biol. 2007; 23:23–7.
   Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001; 25:402–8.
   PubMed Web of Science ®Google Scholar
• Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma. 1995; 12:1–21.
   PubMed Web of Science ®Google Scholar
• Pevny LH, Sockanathan S, Placzek M, Lovell-Badge R. A role for SOX1 in neural determination. Development. 1998; 125:1967–78.
   PubMedGoogle Scholar
• Guillaume DJ, Johnson MA, Li XJ, Zhang SC. Human embryonic stem cell-derived neural precursors develop into neurons and integrate into the host brain. J Neurosci Res. 2006; 84:1165–76.
   PubMed Web of Science ®Google Scholar
• Guillaume DJ, Zhang SC. Human embryonic stem cells: a potential source of transplantable neural progenitor cells. Neurosurg Focus. 2008; 24:E3–.
   Google Scholar
• Tabar V, Panagiotakos G, Greenberg ED, Chan BK, Sadelain M, Gutin PH, et al. Migration and differentiation of neural precursors derived from human embryonic stem cells in the rat brain. Nat Biotechnol. 2005; 23:601–6.
   PubMed Web of Science ®Google Scholar
• Wei L, Cui L, Snider BJ, Rivkin M, Yu SS, Lee CS, et al. Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol Dis. 2005; 19:183–93.
   PubMed Web of Science ®Google Scholar
• Ikeda R, Kurokawa MS, Chiba S, Yoshikawa H, Ide M, Tadokoro M, et al. Transplantation of neural cells derived from retinoic acid-treated cynomolgus monkey embryonic stem cells successfully improved motor function of hemiplegic mice with experimental brain injury. Neurobiol Dis. 2005; 20:38–48.
   PubMedGoogle Scholar
• Daadi MM, Maag AL, Steinberg GK. Adherent self-renewable human embryonic stem cell-derived neural stem cell line: functional engraftment in experimental stroke model. PLoS ONE. 2008; 3:e1644–
   PubMed Web of Science ®Google Scholar
• Yan J, Xu L, Welsh AM, Hatfield G, Hazel T, Johe K, et al. Extensive neuronal differentiation of human neural stem cell grafts in adult rat spinal cord. PLoS Med. 2007; 4:e39–.
   PubMed Web of Science ®Google Scholar
• Wu S, Suzuki Y, Kitada M, Kitaura M, Kataoka K, Takahashi J, et al. Migration, integration, and differentiation of hippocampus-derived neurosphere cells after transplantation into injured rat spinal cord. Neurosci Lett. 2001; 312:173–6.
   PubMed Web of Science ®Google Scholar
• Chow SY, Moul J, Tobias CA, Himes BT, Liu Y, Obrocka M, et al. Characterization and intraspinal grafting of EGF/bFGF-dependent neurospheres derived from embryonic rat spinal cord. Brain Res. 2000; 874:87–106.
   PubMed Web of Science ®Google Scholar
• Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, Nakamura M, et al. Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res. 2002; 69:925–33.
   PubMed Web of Science ®Google Scholar
• Lee KH, Yoon DH, Park YG, Lee BH. Effects of glial transplantation on functional recovery following acute spinal cord injury. J Neurotrauma. 2005; 22:575–89.
   PubMed Web of Science ®Google Scholar
• Lu P, Jones LL, Snyder EY, Tuszynski MH. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol. 2003; 181:115–29.
   PubMed Web of Science ®Google Scholar
• Hofstetter CP, Holmstrom NA, Lilja JA, Schweinhardt P, Hao J, Spenger C, et al. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci. 2005; 8:346–53.
   PubMed Web of Science ®Google Scholar
• Akiyama Y, Honmou O, Kato T, Uede T, Hashi K, Kocsis JD. Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp Neurol. 2001; 167:27–39.
   PubMed Web of Science ®Google Scholar
• O'Shaughnessy TJ, Lin HJ, Ma W. Functional synapse formation among rat cortical neurons grown on three-dimensional collagen gels. Neurosci Lett. 2003; 340:169–72.
   PubMed Web of Science ®Google Scholar
• Klapka N, Muller HW. Collagen matrix in spinal cord injury. J Neurotrauma. 2006; 23:422–35.
   PubMed Web of Science ®Google Scholar
• Joosten EA, Veldhuis WB, Hamers FP. Collagen containing neonatal astrocytes stimulates regrowth of injured fibers and promotes modest locomotor recovery after spinal cord injury. J Neurosci Res. 2004; 77:127–42.
   PubMed Web of Science ®Google Scholar
• Schulz TC, Noggle SA, Palmarini GM, Weiler DA, Lyons IG, Pensa KA, et al. Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture. Stem Cells. 2004; 22:1218–38.
   PubMed Web of Science ®Google Scholar
• Sonntag KC, Pruszak J, Yoshizaki T, van Arensbergen J, Sanchez-Pernaute R, Isacson O. Enhanced yield of neuroepithelial precursors and midbrain-like dopaminergic neurons from human embryonic stem cells using the bone morphogenic protein antagonist noggin. Stem Cells. 2007; 25:411–8.
   PubMed Web of Science ®Google Scholar
• Brederlau A, Correia AS, Anisimov SV, Elmi M, Paul G, Roybon L, et al. Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson's disease: effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells. 2006; 24:1433–40.
   PubMed Web of Science ®Google Scholar
• Erdo F, Buhrle C, Blunk J, Hoehn M, Xia Y, Fleischmann B, et al. Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J Cereb Blood Flow Metab. 2003; 23:780–5.
   PubMed Web of Science ®Google Scholar
• Hayashi J, Takagi Y, Fukuda H, Imazato T, Nishimura M, Fujimoto M, et al. Primate embryonic stem cell-derived neuronal progenitors transplanted into ischemic brain. J Cereb Blood Flow Metab. 2006; 26:906–14.
   PubMed Web of Science ®Google Scholar
• Dihne M, Bernreuther C, Hagel C, Wesche KO, Schachner M. Embryonic stem cell-derived neuronally committed precursor cells with reduced teratoma formation after transplantation into the lesioned adult mouse brain. Stem Cells. 2006; 24:1458–66.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126:663–76.
   PubMed Web of Science ®Google Scholar
• Nishikawa S, Goldstein RA, Nierras CR. The promise of human induced pluripotent stem cells for research and therapy. Nat Rev Mol Cell Biol. 2008; 9:725–9.
   PubMed Web of Science ®Google Scholar