Neurotoxicity Research

, Volume 4, Issue 2, pp 95–101 | Cite as

Novel cellular approaches to repair of neurodegenerative disease: From Sertoli cells to umbilical cord blood stem cells

  • Paul R. Sanberg
  • Alison E. Willing
  • David W. Cahill
Article

Abstract

Neural transplantation is a promising approach to the treatment of neurodegenerative diseases and brain injury that has been shown to be efficacious in many animal models. However, the use of fetal tissue limits the acceptability and widespread application of this technique. In this review we discuss possible alternatives cell sources that may be used to repair the brain and spinal cord, with a focus on Sertoli cells, hNT Neurons, bone marrow and umbilical cord blood derived stem cells.

Keywords

Sertoli cells hNT neurons Neural stem cells Bone marrow Umbilical cord blood Transplantation 

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References

  1. Allison, J., Georgios, H.M., Strasser, A. and Vaux, D.L. (1997) “Transgenic expression of CD95ligand on islet B cells induces a granulocytic infiltration but does not confer immune privilege upon islet allografts”, Proc. Natl. Acad. Sci. USA 94, 3943–3947.PubMedCrossRefGoogle Scholar
  2. Avallet, O., Vigier, M., Leduque, P., Dubois, P.M. and Saez, J.M. (1994) “Expression and regulation of transforming growth factor-beta 1 messenger ribonucleic acid and protein in cultured porcine Leydig and Sertoli cells”, Endocrinology 134, 2079–2087.PubMedCrossRefGoogle Scholar
  3. Azizi, S.A., Stokes, D., Augelli, B.J., DiGirolamo, C. and Prockop, D.J. (1998) “Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats-similarities to astrocyte grafts”, Proc. Natl. Acad. Sci. USA 95, 3908–3913.PubMedCrossRefGoogle Scholar
  4. Baker, K.A., Hong, M., Sadi, D. and Mendez, I. (2000) “Intrastriatal and intranigral grafting of hNT neurons in the 6-OHDA rat model of Parkinson’s disease”, Exp. Neurol. 162, 350–360.PubMedCrossRefGoogle Scholar
  5. Bellgrau, D., Gold, D., Selawry, H., Moore, J., Franzusoff, A. and Duke, R.C. (1995) “A role for CD95 ligand in preventing graft rejection”, Nature 377, 630–632.PubMedCrossRefGoogle Scholar
  6. Bender, J.G., Unversagt, K.L., Walker, D.E., Lee, W., Van Epps, D.E., Smith, D.H., Stewart, C.C. and To, L.B. (1991) “Identification and comparison of CD34-positive cells and their subpopulations from normal peripheral blood and bone marrow using multicolor flow cytometry”, Blood 77, 2591–2596.PubMedGoogle Scholar
  7. Bjornson, C.R.R., Rietze, R., Reynolds, B.A., Magli, M.C. and Vescovi, A.L. (2000) “Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo”, Science 283, 534–537.CrossRefGoogle Scholar
  8. Borlongan, C.V., Tajima, Y., Trojanowski, J.Q., Lee, V.M. and Sanberg, P.R. (1998) “Transplantation of cryopreserved human embryonal carcinoma-derived neurons (NT2N cells) promotes functional recovery in ischemic rats”, Exp. Neurol. 149, 310–321.PubMedCrossRefGoogle Scholar
  9. Brazelton, T.R., Rossi, F.M., Keshet, G.I. and Blau, H.M. (2000) “From marrow to brain: expression of neuronal phenotypes in adult mice”, Science 290, 1775–1779.PubMedCrossRefGoogle Scholar
  10. Cameron, D.F., Othberg, A.I., Borlongan, C.V., Rashed, S., Anton, A., Saporta, S. and Sanberg, P.R. (1997) “Post-thaw viability and functionality of cryopreserved rat fetal brain cells cocultured with Sertoli cells”, Cell Transplant. 6, 185–189.PubMedCrossRefGoogle Scholar
  11. Chen, J., Li, Y. and Chopp, M. (2000) “Intracerebral transplantation of bone marrow with BDNF after MCAo in rat”, Neuropharmacology 39, 711–716.PubMedCrossRefGoogle Scholar
  12. Cheung, W.M., Chu, P.W., Lung, C.H. and Ip, N.Y. (2000) “Expression of retinoid receptors during the retinoic acid-induced neuronal differentiation of human embryonal carcinoma cells”, J. Neurochem. 75, 34–40.PubMedCrossRefGoogle Scholar
  13. Compagnone, N.A., Zhang, P., Vigne, J.L. and Mellon, S.H. (2000) “Novel role for the nuclear phosphoprotein SET in transcriptional activation of P450c17 and initiation of neurosteroidogenesis”, Mol. Endocrinol. 14, 875–888.PubMedCrossRefGoogle Scholar
  14. Coughlan, C.M., McManus, C.M., Sharron, M., Gao, Z., Murphy, D., Jaffer, S., Choe, W., Chen, W., Hesselgesser, J., Gaylord, H., Kalyuzhny, A., Lee, V.M., Wolf, B., Doms, R.W. and Kolson, D.L. (2000) “Expression of multiple functional chemokine receptors and monocyte chemoattractant protein-1 in human neurons”, Neuroscience 97, 591–600.PubMedCrossRefGoogle Scholar
  15. Cudicini, C., Lejeune, H., Gomez, E., Bosmans, E., Ballet, F., Saez, J. and Jegou, B. (1997) “Human Leydig cells and Sertoli cells are producers of interleukins-1 and-6”, J. Clin Endocrinol. Metab. 82, 1426–1433.PubMedCrossRefGoogle Scholar
  16. De Cesaris, P., Filippini, A., Cervelli C., Riccioli, A., Muci, S., Starace, G., Stefanini, M. and Ziparo, E. (1992) “Immunosuppressive molecules produced by Sertoli cells cultured in vitro: biological effects on lymphocytes”, Biochem. Biophys. Res. Commun. 186, 1639–1645.PubMedCrossRefGoogle Scholar
  17. Dombrowicz, D., Hooghe-Peters, E.L., Gothot, A., Sente, B., Vanhaelst, L., Closset, J. and Hennen, G. (1992) “Cellular localization of IGF-I and IGF-II mRNAs in immature hypophysectomized rat testis and epididymis after in vivo hormonal treatment”, Arch. Int. Physiol. Biochim. Biophys. 100, 303–308.PubMedCrossRefGoogle Scholar
  18. Eglitis, M.A. and Mezey, E. (1997) “Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice”, Proc. Natl. Acad Sci. USA 94, 4080–4085.PubMedCrossRefGoogle Scholar
  19. Emerich, D.F. (in press) “Cell transplantation for Parkinson’s disease; A commentary.” Cell Transplant.Google Scholar
  20. Flax, J.D., Aurora, S., Yang, C., Simonin, C., Wills, A.M., Billinghurst, L.L., Jendoubi, M., Sidman, R.L., Wolfe, J.H., Kim, S.U. and Snyder, E.Y. (1998) “Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes”, Nat. Biotech. 16, 1033–1039.CrossRefGoogle Scholar
  21. Freed, C.R., Greene, P.E., Breeze, R.E., Tsai, W.Y., DuMouchel, W., Kao, R., Dillon, S., Winfield, H., Culver, S., Trojanowski, J.Q., Eidelberg, D. and Fahn, S. (2001) “Transplantation of embryonic dopamine neurons for severe Parkinson’s disease”, N. Engl. J. Med. 344, 710–719.PubMedCrossRefGoogle Scholar
  22. Globerson, A. (1999) “Hematopoietic stem cells and aging”, Exp. Gerontol. 34, 137–146.PubMedCrossRefGoogle Scholar
  23. Guillemain, I.G., Alonso, G., Patey, G., Privat, A. and Chaudieu, I. (2000) “Human NT2 Neurons express a large variety of neurotransmission phenotypes in vitro”, J. Comp. Neurol. 422, 380–385.PubMedCrossRefGoogle Scholar
  24. Hammang, J.P., Archer, D.R. and Duncan, I.D. (1997) “Myelination following transplantation of EGF-responsive neural stem cells into a myelin-deficient environment”, Exp. Neurol. 147, 84–95.PubMedCrossRefGoogle Scholar
  25. Harrison, D.E. and Astle, C.M. (1982) “Loss of stem cell repopulating ability upon transplantation. Effects of donor age, cell number, and transplantation procedure”, J. Exp. Med. 156, 1767–1779.PubMedCrossRefGoogle Scholar
  26. Hartley, R.S., Margulis, M., Lee, V.M.-Y. and Tang, C.M. (1999) “Astrocytes are required for the formation of functional synapses between human NT2N neurons in vitro”, J. Comp. Neurol. 407, 1–10.PubMedCrossRefGoogle Scholar
  27. Ho, A.D., Young, D., Maruyama, M., Corringham, R.E.T., Mason, J.R., Thompson, P., Grenier, K., Law, P., Terstappen, L.W.M.M. and Lane, T. (1996) “Pluripotent and lineage-committed CD34+ subsets in leukapheresis products mobilized by G-CSF. GM-CSF versus a combination of both”, Exp. Hematol. 24, 1460.PubMedGoogle Scholar
  28. Hunt, P. and Eardley, D.D. (1986) “Suppressive effects of insulin and insulin-like growth factor I (IGF I) on immune responses”, J. Immunol. 136, 3994–3999.PubMedGoogle Scholar
  29. Hurlbert, M.S., Gianani, R.I., Hutt, C., Freed, C.R. and Kaddis, F.G. (1999) “Neural transplantation of hNT neurons for Huntington’s disease”, Cell Transplant. 8, 143–151.PubMedGoogle Scholar
  30. Kang, S.M., Schneider, D.B. and Lin, Z. (1997) “Fas ligand expression in islets of Langerhans does not confer immune privilege and instead targets them for rapid destruction”, Nat. Med. 3, 738–743.PubMedCrossRefGoogle Scholar
  31. Kirschenbaum, B., Nedergaard, M., Preuss, A., Barami, K., Fraser, R. and Goldman, S. (1994) “In vitro neuronal production by precursor cells derived from the adult human brain”, Cerebral Cortex. 4, 576–589.PubMedCrossRefGoogle Scholar
  32. Kleppner, S.R., Robinson, K.A., Trojanowski, J.Q. and Lee, V.M.-Y. (1995) “Transplanted human neurons derived from a teratocarcinoma cell line (NTera-2) mature, integrate, and survive for over 1 year in the nude mouse brain”, J. Comp. Neurol. 357, 618–632.PubMedCrossRefGoogle Scholar
  33. Kondziolka, D., Wechsler, L., Goldstein, S., Meltzer, C., Thulborn, K.R., Gebel, J., Jannetta, P., DeCesare, S., Elder, E.M., McGrogan, M., Reitman, M.A. and Bynum, L. (2000) “Transplantation of cultured human neuronal cells for patients with stroke”, Neurology 55, 565–569.PubMedGoogle Scholar
  34. Kopen, G.C., Prockop, D.J. and Phinney, D.G. (1999) “Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains”, Proc. Natl. Acad. Sci. USA 96, 10711–10716.PubMedCrossRefGoogle Scholar
  35. Korbutt, G.S., Suarez-Pinzon, W.L., Power, R.F., Rajotte, R.V. and Rabinovitch, A. (2000) “Testicular Sertoli cells exert both protective and destructive effects on syngeneic islet grafts in non-obese diabetic mice”, Diabetologia 43, 474–480.PubMedCrossRefGoogle Scholar
  36. Kukekov, V.G., Laywell, E.D., Suslov, O., Davies, K., Scheffler, B., Thomas, L.B., O’Brien, T.F., Kusakabe, M. and Steindler, D.A. (1999) “Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain”, Exp. Neurol. 156, 333–344.PubMedCrossRefGoogle Scholar
  37. Kvinlaug, B., Brat, S. and Gloster, A. (2000) “Production of central nervous system cell types from adult and postnatal murine precursor cells”, Soc. Neurosci. Abst. 26, 829.Google Scholar
  38. Lansdorp, P.M. (1997) “Self-renewal of stem cells”, Biol. Blood Marrow Transplant. 3, 171–178.PubMedGoogle Scholar
  39. Laywell, E.D., Kukekov, V.G. and Steindler, D.A. (1999) “Multipotent neurospheres can be derived from forebrain subependymal zone and spinal cord of adult mice after protracted postmortem intervals”, Exp. Neurol. 156, 430–433.PubMedCrossRefGoogle Scholar
  40. Li, Y., Chen, J. and Chopp, M. (2001) “Adult bone marrow transplantation after stroke in adult rats”, Cell Transplant. 10, 31–40.PubMedGoogle Scholar
  41. Lin, S.Z., Hayashi, T., Su, T.-P., Chiang, Y.H., Sanberg, P.R., Hoffer, B.J., Wang, Y. and Borlongan, C.V. (2000) “Detection of GDNF in cultured and grafted hNT Neurons”, Exp. Neurol. 164, 447.Google Scholar
  42. Loveland, K.L., Zlatic, K., Stein-Oakley, A., Risbridger, G. and Kretser, D.M. (1995) “Platelet-derived growth factor ligand and receptor subunit mRNA in the Sertoli and Leydig cells of the rat testis”, Mol. Cell. Endocrinol. 1108, 155–159.CrossRefGoogle Scholar
  43. Makoui, A.S., Saporta, S., Willing, A.E., Zigova, T., Khan, T., Cahill, D. and Sanberg, P.R. (2000) “Recovery of motor and sensory evoked potentials after transplantation of hNT neurons in rats with complete spinal cord contusion injury”, Exp. Neurol. 164, 455.Google Scholar
  44. Mezey, E., Chandross, K.J., Harta, G., Maki, R.A. and McKercher, S.R. (2000) “Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow”, Science 290, 1779–1782.PubMedCrossRefGoogle Scholar
  45. Miyazono, M., Nowell, P.C., Finan, J.L., Lee, V.M.-Y. and Trojanowski, J.Q. (1996) “Long-term integration and neuronal differentiation of human embryonal carcinoma cells (NTera-2) transplanted into the caudoputamen of nude mice”, J. Comp. Neurol. 376, 602–613.CrossRefGoogle Scholar
  46. Muir, J.K., Raghupathi, R., Saatman, K.E., Wilson, C.A., Lee, V.M., Trojanowski, J.Q., Philips, M.F. and McIntosh, T.K. (1999) “Terminally differentiated human neurons survive and integrate following transplantation into the traumatically injured rat brain”, J. Neurotrauma. 16, 403–414.PubMedCrossRefGoogle Scholar
  47. Muruve, D.A., Nicolson, A.B., Manfro, R.C., Strom, T.B., Sukhatme, V.P. and Liberman, T.A. (1997) “Adenovirusmediated expression of Fas ligand induces hepatic apoptosis after systemic administration and apoptosis of ex vivo-infected pancreatic islet allografts and isografts”, Human Gene Therapy 8, 955–963.PubMedCrossRefGoogle Scholar
  48. Othberg, A., Willing, A.E., Cameron, D.F., Anton, A., Saporta, S. and Sanberg, P.R. (1998) “Porcine Sertoli cells enhance survival of dopaminergic rat embryonic ventral mesencephalic and human teratocarcinoma-derived neurons in vitro”, Cell Transplant. 7, 57–64.CrossRefGoogle Scholar
  49. Philips, M.F., Muir, J.K., Saatman, K.E., Raghupathi, R., Lee, V.M., Trojanowski, J.Q. and McIntosh, T.K. (1999) “Survival and integration of transplanted postmitotic human neurons following experimental brain injury in immunocompetent rats”, J. Neurosurg. 90, 116–124.PubMedCrossRefGoogle Scholar
  50. Piccirillo, C.A., Chang, Y. and Prud’homme, G.J. (1998) “TGF-B1 somatic gene therapy prevents autoimmune disease in nonobese diabetic mice”, J. Immunol. 161, 3950–3956.PubMedGoogle Scholar
  51. Pleasure, S.J. and Lee, V.M.-Y. (1993) “NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell”, J. Neurosci. Res. 35, 585–602.PubMedCrossRefGoogle Scholar
  52. Pollanen, P. and Maddocks, S. (1988) “Macrophages, lymphocytes and MHC II antigen in the ram and the rat testis”, J. Reprod. Fert. 32, 437–445.CrossRefGoogle Scholar
  53. Pollanen, P. and Niemi, M. (1987) “Immunohistochemical identification of macrophages, lymphoid cells and HLA antigens in the human testis”, Int. J. Androl. 10, 37–42.PubMedCrossRefGoogle Scholar
  54. Prockop, D.J. (1997) “Marrow stromal cells as stem cells for nonhematopoietic tissues”, Science 276, 71–74.PubMedCrossRefGoogle Scholar
  55. Ren, R.F., Lah, J.J., Diehlmann, A., Kim, E.S., Hawver, D.B., Levey, A.I., Beyreuther, K. and Flanders, K.C. (1999) “Differential effects of transforming growth factor-beta(s) and glial cell line-derived neurotrophic factor on gene expression of presenilin-1 in human post-mitotic neurons and astrocytes”, Neuroscience 93, 1041–1049.PubMedCrossRefGoogle Scholar
  56. Reynolds, B.A., Tetzlaff, W. and Weiss, S. (1992) “A multipotential EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes”, J. Neurosci. 12, 4565–4574.PubMedGoogle Scholar
  57. Sanberg, P.R., Borlongan, C.V., Saporta, S. and Cameron, D.F. (1996) “Testis-derived Sertoli cells survive and provide localized immunoprotection for xenografts in rat brain”, Nat. Biotech. 14, 1692–1695.CrossRefGoogle Scholar
  58. Sanberg, P.R., Borlongan, C.V., Othberg, A.I., Saporta, S., Freeman, T.B. and Cameron, D.F. (1997) “Testis-derived Sertoli cells have a trophic effect on dopamine neurons and alleviate hemiparkinsonism in rats”, Nat. Med. 3, 1129–1132.PubMedCrossRefGoogle Scholar
  59. Sanchez-Ramos, J., Song, S., Cardozo-Pelaez, F., Hazzi, C., Stedeford, T., Willing, A., Freeman, T.B., Saporta, S., Janssen, W., Patel, N., Cooper, D.R. and Sanberg, P.R. (2000) “Adult bone marrow stromal cells differentiate into neural cells in vitro”, Exp. Neurol. 164, 247–256.PubMedCrossRefGoogle Scholar
  60. Saporta, S., Borlongan, C.V. and Sanberg, P.R. (1999) “Neural transplantation of human post-mitotic cell line-derived NT2 (hNT) neurons into ischemic rats. A dose-response study”, Neuroscience 91, 519–525.PubMedCrossRefGoogle Scholar
  61. Satoh, J. and Kuroda, Y. (2000) “Differential gene expression between human neurons and neuronal progenitor cells in culture: an analysis of arrayed cDNA clones in NTera2 human embryonal carcinoma cell line as a model system”, J. Neurosci. Meth. 94, 155–164.CrossRefGoogle Scholar
  62. Selawry, H., Fajaco, R. and Whittington, K. (1985) “Intratesticular islet allografts in the spontaneously diabetic BB/W rat”, Diabetes 34, 1019–1024.PubMedCrossRefGoogle Scholar
  63. Selawry, H., Whittington, K. and Fajaco, R. (1986) “Effect of cyclosporine on islet xenograft survival in the BB/W rat”, Transplantation 42, 568–570.PubMedGoogle Scholar
  64. Selawry, H., Fojaco, R. and Whittington, K. (1987) “Extended survival of MHC-compatible islet grafts from diabetes-resistant donors in spontaneously diabetic BB/W rat”, Diabetes 36, 1061–1067.PubMedCrossRefGoogle Scholar
  65. Selawry, H.P., Whittington, K.B. and Bellgrau, D. (1989) “Abdominal intratesticular islet-xenograft survival in rats”, Diabetes 38, 220–223.PubMedGoogle Scholar
  66. Selawry, H.P., Kotb, M., Herrod, H.G. and Lu, Z.N. (1991) “Production of a factor, or factors, suppressing IL-2 production and T cell proliferation by Sertoli cell-enriched preparations. A potential role for islet transplantation in an immunologically privileged site”, Transplantation 52, 846–850.PubMedCrossRefGoogle Scholar
  67. Sheridan, K.M. and Maltese, W.A. (1998) “Expression of Rab3A GTPase and other synaptic proteins is induced in differentiated NT2N neurons”, J. Mol. Neurosci. 10, 121–128.PubMedCrossRefGoogle Scholar
  68. Sirchia, G. and Rebulla, P. (1999) “Placental/umbilical cord blood transplantation”, Haematologica 84, 738–747.PubMedGoogle Scholar
  69. Smith, E.P., Hall, S.H., Monaco, L., French, F.S., Wilson, E.M. and Conti, M. (1989) “A rat Sertoli cell factor similar to basic fibroblast growth factor increases c-fos messenger ribonucleic acid in cultured Sertoli cells”, Mol. Endocrinol. 3, 954–961.PubMedCrossRefGoogle Scholar
  70. Talbot, K., Young, R.A., Jolly-Tornetta, C., Lee, V.M., Trojanowski, J.Q. and Wolf, B.A. (2000) “A frontal variant of Alzheimer’s disease exhibits decreased calcium-independent phospholipase A2 activity in the prefrontal cortex”, Neurochem. Int. 37, 17–31.PubMedCrossRefGoogle Scholar
  71. Toma, J.G., Akhavan, M., Fernandes, K., Fortier, M., Sadikot, A. and Miller, F.D. (2000) Skin Tissue: A Source for Multipotent Neural Stem Cells (Society for Neuroscience, New Orleans), 26, 828.Google Scholar
  72. Velardo, M.J., O’Steen, B.E., McGrogan, M. and Reier, P.J. (2000) “hNT cells and transplantation repair of rat cervical spinal cord contusions”, Exp. Neurol. 164, 454.Google Scholar
  73. Vescovi, A.L., Parati, E.A., Gritti, A., Poulin, P., Ferrario, M., Wanke, E., Frolichsthal-Schoeller, P., Cova, L., Arcellana-Panlilio, M., Colombo, A. and Galli, R. (1999) “Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation”, Exp. Neurol. 156, 71–83.PubMedCrossRefGoogle Scholar
  74. Weima, S.M., van Rooijen, M.A., Mummery, C.L., Feijen, A., Kruijer, W., de Laat, S.W. and van Zoelen, E.J. (1988) “Differentially regulated production of platelet-derived growth factor and of transforming growth factor beta by a human teratocarcinoma cell line”, Differentiation 38, 203–210.PubMedCrossRefGoogle Scholar
  75. Widenfalk, J., Nosrat, C., Tomac, A., Westphal, H., Hoffer, B. and Olson, L. (1997) “Neurturin and glial cell line-derived neurotrophic factor receptor-b (GDNFR-b), novel proteins related to GDNF and GDNFR-a with specific cellular patterns of expression suggesting roles in the developing and adult nervous system and in peripheral organs”, J. Neurosci. 17, 8506–8519.PubMedGoogle Scholar
  76. Willing, A.E., Othberg, A.I., Saporta, S., Anton, A., Sinibaldi, S., Poulos, S.G., Cameron, D.F., Freeman, T.B. and Sanberg, P.R. (1999a) “Sertoli cells enhance the survival of co-transplanted dopamine neurons”, Brain Res. 822, 246–250.PubMedCrossRefGoogle Scholar
  77. Willing, A.E., Sudberry, J.J., Othberg, A.I., Saporta, S., Poulos, S.B., Cameron, D.F., Freeman, T.B. and Sanberg, P.R. (1999b) “Sertoli cells decrease microglial response and increase engraftment of human hNT neurons in the hemiparkinsonian rat striatum”, Brain Res. Bull. 48, 441–444.PubMedCrossRefGoogle Scholar
  78. Woodbury, D., Schwarz, E.J., Prockop, D.J. and Black, I.B. (2000) “Adult rat and human bone marrow stromal cells differentiate into neurons”, J. Neurosci. Res. 61, 364–370.PubMedCrossRefGoogle Scholar
  79. Wu, A.G., Michejda, M., Mazumder, A., Meehan, K.R., Menendez, F.A., Tchabo, J.G., Slack, R., Johnson, M.P. and Bellanti, J.A. (1999) “Analysis and characterization of hematopoietic progenitor cells from fetal bone marrow, adult bone marrow, peripheral blood, and cord blood”, Pediatr. Res. 46, 163–169.PubMedCrossRefGoogle Scholar
  80. Yandava, B.D., Billinghurst, L.L. and Snyder, E.Y. (1999), “Global cell replacement is feasible via neural stem cell trans plantation: evidence from the dysmyelinated shiverer mouse brain”, Proc. Natl. Acad. Sci. USA 96, 7029–7034.PubMedCrossRefGoogle Scholar
  81. Zeller, M. and Strauss, W.L. (1995) “Retinoic acid induces cholinergic differentiation of NTera2 human embryonal carcinoma cells”, Int. J. Dev. Neurosci. 13, 437–445.PubMedCrossRefGoogle Scholar
  82. Zhao, L.-R., Duan, W.-M., Reyes, M., Keene, C.D., Nussbaum, E.S., Verfaille, C.M. and Low, W.C. (2000) “Human bone marrow stem cells exhibit neural phenotypes after transplantation and ameliorate neurological deficits with ischemic brain injury in rats”, Soc. Neurosci. Abst. 26, 2291.Google Scholar
  83. Zigova, T., Barroso, L.F., Willing, A.E., Saporta, S., McGrogan, M.P., Freeman, T.B. and Sanberg, P.R. (2000) “Dopaminergic phenotype of hNT cells in vitro”, Dev. Brain Res. 122, 87–90.CrossRefGoogle Scholar

Copyright information

© Springer 2002

Authors and Affiliations

  • Paul R. Sanberg
    • 1
  • Alison E. Willing
    • 1
  • David W. Cahill
    • 1
  1. 1.Center for Aging and Brain Repair, Department of NeurosurgeryUniversity of South Florida College of MedicineTampaUSA

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