Neurobiology of Aging
Volume 27, Issue 7 , Pages 909-917 , July 2006

Isolation of neural precursor cells from Alzheimer's disease and aged control postmortem brain

  • Mark A. Lovell

      Affiliations

    • From the Sanders-Brown Center on Aging and Alzheimer's Disease Research Center, 800 S. Limestone St., 101 Sanders-Brown Bldg., University of Kentucky, Lexington, KY 40536-0230, USA
    • Department of Chemistry, University of Kentucky, Lexington, KY 40506, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 859 257 1412x251; fax: +1 859 323 2866.
    • ,
  • Hartmut Geiger

      Affiliations

    • Department of Internal Medicine, University of Kentucky, Lexington, KY 40536, USA
    • ,
  • Gary E. Van Zant

      Affiliations

    • Department of Internal Medicine, University of Kentucky, Lexington, KY 40536, USA
    • ,
  • Bert C. Lynn

      Affiliations

    • From the Sanders-Brown Center on Aging and Alzheimer's Disease Research Center, 800 S. Limestone St., 101 Sanders-Brown Bldg., University of Kentucky, Lexington, KY 40536-0230, USA
    • Department of Chemistry, University of Kentucky, Lexington, KY 40506, USA
    • ,
  • William R. Markesbery

      Affiliations

    • From the Sanders-Brown Center on Aging and Alzheimer's Disease Research Center, 800 S. Limestone St., 101 Sanders-Brown Bldg., University of Kentucky, Lexington, KY 40536-0230, USA
    • Departments of Neurology and Pathology, University of Kentucky, Lexington, KY 40536-0230, USA

Received 11 January 2005 ,Revised 25 April 2005 ,Accepted 2 May 2005.

References 

  1. Ahmed S, Reynolds BA, Weiss S. BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J Neurosci. 1995;15:5765–5778
  2. Arsenijevic Y, Weiss S. Insulin-like growth factor-I is a differentiation factor for postmitotic CNS stem cell-derived neuronal precursors: distinct actions from those of brain-derived neurotrophic factor. J Neurosci. 1998;18:2118–2128
  3. Baird A. Fibroblast growth factors: activities and significance of non-neurotrophin neurotrophic growth factors. Curr Opin Neurobiol. 1994;4:78–86
  4. Carpenter MK, Cui X, Hu ZY, Jackson J, Sherman S, Seiger A, et al. In vitro expansion of a multipotent population of human neural progenitor cells. Exp Neurol. 1999;158:265–278
  5. Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci. 1999;19:4462–4471
  6. Davis AA, Temple S. A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature. 1994;372:263–266
  7. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97:703–716
  8. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4:1313–1317
  9. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL, et al. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol. 1998;16:1033–1039
  10. Gerdes J. Ki-67 and other proliferation markers useful for immunohistological diagnostic and prognostic evaluations in human malignancies. Semin Cancer Biol. 1990;1:199–206
  11. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol. 1984;133:1710–1715
  12. Gerdes J, Schwab U, Lemke H, Stein H. Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int J Cancer. 1983;31:13–20
  13. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, et al. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci. 1996;16:1091–1100
  14. Gross RE, Mehler MF, Mabie PC, Zang Z, Santschi L, Kessler JA. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron. 1996;17:595–606
  15. Haughey NJ, Liu D, Nath A, Borchard AC, Mattson MP. Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease. Neuromolecular Med. 2002;1:125–135
  16. Haughey NJ, Nath A, Chan SL, Borchard AC, Rao MS, Mattson MP. Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J Neurochem. 2002;83:1509–1524
  17. Herzlinger D. Renal stem cells and the lineage of the nephron. Annu Rev Physiol. 1994;56:671–689
  18. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, et al. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci USA. 2004;101:343–347
  19. Johansson CB, Svensson M, Wallstedt L, Janson AM, Frisen J. Neural stem cells in the adult human brain. Exp Cell Res. 1999;253:733–736
  20. 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
  21. Kalyani A, Hobson K, Rao MS. Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev Biol. 1997;186:202–223
  22. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature. 1997;386:493–495
  23. Keyoung HM, Roy NS, Benraiss A, Louissaint A, Suzuki A, Hashimoto M, et al. High-yield selection and extraction of two promoter-defined phenotypes of neural stem cells from the fetal human brain. Nat Biotechnol. 2001;19:843–850
  24. Kirschenbaum B, Nedergaard M, Preuss A, Barami K, Fraser RA, Goldman SA. In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb Cortex. 1994;4:576–589
  25. Magavi SS, Leavitt BR, Macklis JD. Induction of neurogenesis in the neocortex of adult mice. Nature. 2000;405:951–955
  26. Magavi SS, Macklis JD. Manipulation of neural precursors in situ: induction of neurogenesis in the neocortex of adult mice. Neuropsychopharmacology. 2001;25:816–835
  27. Mayer-Proschel M, Kalyani AJ, Mujtaba T, Rao MS. Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron. 1997;19:773–785
  28. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM . Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34:939–944
  29. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, et al. The consortium to establish a registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology. 1991;41:479–486
  30. Morshead CM, Craig CG, van der Kooy D. In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development. 1998;125:2251–2261
  31. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron. 1994;13:1071–1082
  32. Murrell W, Bushell GR, Livesey J, McGrath J, MacDonald KP, Bates PR, et al. Neurogenesis in adult human. Neuroreport. 1996;7:1189–1194
  33. Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G, Jiang L, et al. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med. 2003;9:439–447
  34. Okano H, Imai T, Okabe M. Musashi: a translational regulator of cell fate. J Cell Sci. 2002;115:1355–1359
  35. Pagano SF, Impagnatiello F, Girelli M, Cova L, Grioni E, Onofri M, et al. Isolation and characterization of neural stem cells from the adult human olfactory bulb. Stem Cells. 2000;18:295–300
  36. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci. 1999;19:8487–8497
  37. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH. Cell culture. Progenitor cells from human brain after death. Nature. 2001;411:42–43
  38. Pincus DW, Keyoung HM, Harrison-Restelli C, Goodman RR, Fraser RA, Edgar M, et al. Fibroblast growth factor-2/brain-derived neurotrophic factor-associated maturation of new neurons generated from adult human subependymal cells. Ann Neurol. 1998;43:576–585
  39. Rao MS, Noble M, Mayer-Proschel M. A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci USA. 1998;95:3996–4001
  40. Reynolds BA, Tetzlaff W, Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci. 1992;12:4565–4574
  41. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255:1707–1710
  42. Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol. 1996;175:1–13
  43. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, Harrison-Restelli C, et al. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med. 2000;6:271–277
  44. Sakakibara S, Nakamura Y, Satoh H, Okano H. Rna-binding protein Musashi2: developmentally regulated expression in neural precursor cells and subpopulations of neurons in mammalian CNS. J Neurosci. 2001;21:8091–8107
  45. Sakakibara S, Nakamura Y, Yoshida T, Shibata S, Koike M, Takano H, et al. RNA-binding protein Musashi family: roles for CNS stem cells and a subpopulation of ependymal cells revealed by targeted disruption and antisense ablation. Proc Natl Acad Sci USA. 2002;99:15194–15199
  46. Sakakibara S, Okano H. Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J Neurosci. 1997;17:8300–8312
  47. Scharff C, Kirn JR, Grossman M, Macklis JD, Nottebohm F. Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron. 2000;25:481–492
  48. Shimazaki T, Arsenijevic Y, Ryan AK, Rosenfeld MG, Weiss S. A role for the POU-III transcription factor Brn-4 in the regulation of striatal neuron precursor differentiation. Embo J. 1999;18:444–456
  49. Sigal SH, Brill S, Fiorino AS, Reid LM. The liver as a stem cell and lineage system. Am J Physiol. 1992;263:G139–G148
  50. The National Institute on Aging and Reagan Institute Working Group . Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. Neurobiol Aging. 1997;18:S1–S2
  51. Uchida N, Fleming WH, Alpern EJ, Weissman IL. Heterogeneity of hematopoietic stem cells. Curr Opin Immunol. 1993;5:177–184
  52. Vescovi AL, Parati EA, Gritti A, Poulin P, Ferrario M, Wanke E, et al. 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. 1999;156:71–83
  53. Vescovi AL, Reynolds BA, Fraser DD, Weiss S. bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron. 1993;11:951–966
  54. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, et al. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci. 1996;16:7599–7609
  55. Wen PH, Shao X, Shao Z, Hof PR, Wisniewski T, Kelley K, et al. Overexpression of wild type but not an FAD mutant presenilin-1 promotes neurogenesis in the hippocampus of adult mice. Neurobiol Dis. 2002;10:8–19

PII: S0197-4580(05)00116-8

doi: 10.1016/j.neurobiolaging.2005.05.004

Neurobiology of Aging
Volume 27, Issue 7 , Pages 909-917 , July 2006

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