Adult neurogenesis, neural stem cells and Alzheimer's disease: Developments, limitations, problems and promises

Current Alzheimer Research

Volumn 6, Issue 6, 2009, Pages 461-470

  Taupin, Philippe ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

Amyloid; Aneuploidy; Cellular therapy; Neurodegenerative diseases; Pathogenesis; Presenilin

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; ANTIINFLAMMATORY AGENT; APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; BETA AMYLOID VACCINE; BINDING PROTEIN; GALANTAMINE; GRB ASSOCIATED BINDING PROTEIN 2; HOMOTAURINE; HYPOCHOLESTEROLEMIC AGENT; MEMANTINE; METAL CHELATE; PEPTIDE VACCINE; PRESENILIN 1; PRESENILIN 2; PROTEINASE INHIBITOR; RIVASTIGMINE; SECRETASE INHIBITOR; SORTILIN; SORTILIN RELATED RECEPTOR; TACRINE; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANEUPLOIDY; BEHAVIOR CHANGE; BRAIN DEGENERATION; CELL CYCLE PROGRESSION; CELL DIVISION; CHROMOSOME 21; COGNITION; DIAGNOSTIC TEST; DISEASE MODEL; DOWN SYNDROME; DRUG EFFECT; EARLY DIAGNOSIS; FAMILIAL DISEASE; GENE EXPRESSION; GENE IDENTIFICATION; GENE MUTATION; GENETIC RISK; HUMAN; MOLECULAR MECHANICS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; OCCUPATIONAL THERAPY; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; REGENERATION; REVIEW; STEM CELL TRANSPLANTATION; ADULT STEM CELL; BRAIN; GENETICS; METHODOLOGY; PATHOLOGY; PHYSIOLOGY;

ADULT STEM CELLS; ALZHEIMER DISEASE; BRAIN; HUMANS; NEUROFIBRILLARY TANGLES; NEUROGENESIS; STEM CELL TRANSPLANTATION;

EID: 73949086520     PISSN: 15672050     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720509790147151     Document Type: Review

References (138)

1. Alzheimer A. Uber einen eigenartigen schweren erkrankungsprozeb der hirnrinde. Neurolog Cenrealbl 23: 1129-1136 (1906).
2. Caselli RJ, Beach TG, Yaari R, Reiman EM. Alzheimer's disease a century later. J Clin Psychiatry 67: 1784-1800 (2006).
3. Jellinger KA. Alzheimer 100 - highlights in the history of Alzheimer research. J Neural Transm 113: 1603-1623 (2006).
4. Burns A, Byrne EJ and Maurer K. Alzheimer's disease. Lancet 360: 163-165 (2002).
5. Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, et al. Alzheimer's Disease International. Global prevalence of dementia: a Delphi consensus study. Lancet 366: 2112-2117 (2005).
6. Gross CG. Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1: 67-73 (2000).
7. Taupin P. Neurogenesis in the adult central nervous system. C R Biol 329: 465-475 (2006).
8. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317 (1998).
9. Bedard A and Parent A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151: 159-168 (2004).
10. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243-1249 (2007).
11. Taupin P and Gage FH. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 69: 745-749 (2002).
12. Gage FH. Mammalian neural stem cells. Science 287: 1433-1438 (2000).
13. Parent JM, Tada E, Fike JR, Lowenstein DH. Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J Neurosci 19: 4508-4519 (1999).
14. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410: 372-376 (2001). Erratum in: Nature 414, 938 (2001).
15. 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 101: 343-347 (2004).
16. Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, Kitabatake Y, et al. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130: 1146-1158 (2007).
17. Taupin P. Adult neurogenesis and neuroplasticity. Restor Neurol Neurosci 24: 9-15 (2006).
18. Taupin P. Adult neurogenesis pharmacology in neurological diseases and disorders. Exp Rev Neurother 8: 311-320 (2008).
19. Lederman RJ. What tests are necessary to diagnose Alzheimer disease? Cleve Clin J Med 67: 615-618 (2000).
20. Dubois B, Feldman HH, Jacova C, DeKosky ST, Barberger-Gateau P, Cummings J, et al. Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS-ADRDA criteria. Lancet Neurol 6: 734-746 (2007).
21. Patterson C, Feightner JW, Garcia A, Hsiung GY, MacKnight C, Sadovnick AD. Diagnosis and treatment of dementia: 1. Risk assessment and primary prevention of Alzheimer disease. CMAJ 178: 548-556 (2008).
22. Cankurtaran M, Yavuz BB, Cankurtaran ES, Halil M, Ulger Z, Ariogul S. Risk factors and type of dementia: Vascular or Alzheimer? Arch Gerontol Geriatr 47: 25-34 (2008).
23. Terry RD. The pathogenesis of Alzheimer disease: an alternative to the amyloid hypothesis. J Neuropathol Exp Neurol 55: 1023-1025 (1996).
24. St George-Hyslop PH. Piecing together Alzheimer's. Sci Am 283: 76-83 (2000).
25. Brun A, Gustafson L. Distribution of cerebral degeneration in Alzheimer's disease. A clinico-pathological study. Arch Psychiatr Nervenkr 223: 15-33 (1976).
26. Anderson DH, Talaga KC, Rivest AJ, Barron E, Hageman GS and Johnson LV. Characterization of beta amyloid assemblies in drusen: the deposits associated with aging and age-related macular degeneration. Exp Eye Res 78: 243-256 (2004).
27. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, et al. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325: 733-736 (1987).
28. Goldgaber D, Lerman MI, McBride OW, Saffiotti U, Gajdusek DC. Characterization and chromosomal localization of a cDNA encoding brain amyloid of Alzheimer's disease. Science 235: 877-880 (1987).
29. Schellenberg GD, Bird TD, Wijsman EM, Orr HT, Anderson L, Nemens E, et al. Genetic linkage evidence for a familial Alzheimer's disease locus on chromosome 14. Science 258: 668-671 (1992).
30. Serpell LC, Sunde M, Blake CC. The molecular basis of amyloidosis. Cell Mol Life Sci 53: 871-887 (1997).
31. Dobson CM. Protein misfolding, evolution and disease. Trends Biochem Sci 24: 329-332 (1999).
32. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356 (2002). Erratum in: Science 297: 2209 (2002).
33. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E, et al. Science 313: 1781-1784 (2006).
34. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM. Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45: 675-688 (2005).
35. Fukutani Y, Kobayashi K, Nakamura I, Watanabe K, Isaki K, Cairns NJ. Neurons, intracellular and extra cellular neurofibrillary tangles in subdivisions of the hippocampal cortex in normal ageing and Alzheimer's disease. Neurosci Lett 200: 57-60 (1995).
36. Kim H, Jensen CG, Rebhun LI. The binding of MAP-2 and tau on brain microtubules in vitro: implications for microtubule structure. Ann N Y Acad Sci 466: 218-239 (1986).
37. Drubin DG, Kirschner MW. Tau protein function in living cells. J Cell Biol 103: 2739-2746 (1986).
38. Iqbal K, Grundke-Iqbal I, Smith AJ, George L, Tung YC, Zaidi T. Identification and localization of a tau peptide to paired helical filaments of Alzheimer disease. Proc Natl Acad Sci USA 86: 5646-5650 (1989).
39. Wang JZ, Grundke-Iqbal I, Iqbal K. Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur J Neurosci 25: 59-68 (2007).
40. Iqbal K, Alonso AC, Gong CX, Khatoon S, Pei JJ, Wang JZ, et al. Mechanisms of neurofibrillary degeneration and the formation of neurofibrillary tangles. J Neural Transm Suppl 53: 169-180 (1998).
41. Alonso A, Zaidi T, Novak M, Grundke-Iqbal I, Iqbal K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc Natl Acad Sci USA 98: 6923-6928 (2001).
42. Hardy J and Orr H. The genetics of neurodegenerative diseases. J Neurochem 97: 1690-1699 (2006).
43. Hardy J. The genetic causes of neurodegenerative diseases. J Alzheimers Dis 3: 109-116 (2001).
44. Schellenberg GD. Genetic dissection of Alzheimer disease, a heterogeneous disorder. Proc Natl Acad Sci USA 92: 8552-8559 (1995).
45. Thomas P, Fenech M. A review of genome mutation and Alzheimer's disease. Mutagenesis 22: 15-33 (2007).
46. Minghetti L. Role of inflammation in neurodegenerative diseases. Curr Opin Neurol 18: 315-321 (2005).
47. Filipcik P, Cente M, Ferencik M, Hulin I, Novak M. The role of oxidative stress in the pathogenesis of Alzheimer's disease. Bratisl Lek Listy 107: 384-394 (2006).
48. Onyango IG, Khan SM. Oxidative stress, mitochondrial dysfunction, and stress signaling in Alzheimer's disease. Curr Alzheimer Res 3: 339-349 (2006).
49. Zilka N, Ferencik M, Hulin I. Neuroinflammation in Alzheimer's disease: protector or promoter? Bratisl Lek Listy 107: 374-383 (2006).
50. Malinski T. Nitric oxide and nitroxidative stress in Alzheimer's disease. J Alzheimers Dis 11: 207-218 (2007).
51. Raber J, Huang Y, Ashford JW. ApoE genotype accounts for the vast majority of AD risk and AD pathology. Neurobiol Aging 25: 641-650 (2004).
52. Nishimura M, Yu G, St George-Hyslop PH. Biology of presenilins as causative molecules for Alzheimer disease. Clin Genet 55: 219-225 (1999).
53. Newman M, Musgrave FI, Lardelli M. Alzheimer disease: amyloidogenesis, the presenilins and animal models. Biochim Biophys Acta 1772: 285-297 (2007).
54. Goedert M, Strittmatter WJ, Roses AD. Alzheimer's disease. Risky apolipoprotein in brain. Nature 372: 45-46 (1994).
55. Rogaeva E, Meng Y, Lee JH, Gu Y, Kawarai T, Zou F, et al. The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat Genet 39: 168-177 (2007).
56. Mahley RW. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240: 622-630 (1988).
57. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, et al. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in lateonset familial Alzheimer disease. Proc Natl Acad Sci USA 90: 1977-1981 (1993).
58. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261: 921-923 (1993).
59. Ma J, Yee A, Brewer HB Jr, Das S, Potter H. Amyloid-associated proteins alpha 1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer beta-protein into filaments. Nature 372: 92-94 (1994).
60. Seaman MN. Recycle your receptors with retromer. Trends Cell Biol 15: 68-75 (2005).
61. Finckh U, von der Kammer H, Velden J, Michel T, Andresen B, Deng A, et al. Genetic association of a cystatin C gene polymorphism with late-onset Alzheimer disease. Arch Neurol 57: 1579-1583 (2000).
62. Wakutani Y, Kowa H, Kusumi M, Nakaso K, Yasui K, Isoe-Wada K, et al. A haplotype of the methylenetetrahydrofolate reductase gene is protective against late-onset Alzheimer's disease. Neurobiol Aging 25: 291-294 (2004).
63. Beyer K, Lao JI, Latorre P, Riutort N, Matute B, Fernández- Figueras MT, et al. Methionine synthase polymorphism is a risk factor for Alzheimer disease. Neuroreport 14: 1391-1394 (2003).
64. Holgado-Madruga M, Emlet DR, Moscatello DK, Godwin AK, Wong AJ. A Grb2-associated docking protein in EGF- and insulin-receptor signaling. Nature 379: 560-564 (1996).
65. Reiman EM, Webster JA, Myers AJ, Hardy J, Dunckley T, Zismann VL, et al. GAB2 Alleles Modify Alzheimer's Risk in APOE varepsilon4 Carriers. Neuron 54: 713-720 (2007).
66. Wragg M, Hutton M, Talbot C. Genetic association between intronic polymorphism in presenilin-1 gene and late-onset Alzheimer's disease. Alzheimer's Disease Collaborative Group. Lancet 347: 509-512 (1996).
67. Migliore L, Testa A, Scarpato R, Pavese N, Petrozzi L, Bonuccelli U. Spontaneous and induced aneuploidy in peripheral blood lymphocytes of patients with Alzheimer's disease. Hum Genet 101: 299-305 (1997).
68. Migliore L, Botto N, Scarpato R, Petrozzi L, Cipriani G, Bonuccelli U. Preferential occurrence of chromosome 21 malsegregation in peripheral blood lymphocytes of Alzheimer disease patients. Cytogenet Cell Genet 87: 41-46 (1999).
69. Geller LN, Potter H. Chromosome missegregation and trisomy 21 mosaicism in Alzheimer's disease. Neurobiol Dis 6: 167-179 (1999).
70. Potter H. Review and hypothesis: Alzheimer disease and Down syndrome--chromosome 21 nondisjunction may underlie both disorders. Am J Hum Genet 48: 1192-1200 (1991).
71. Olson MI, Shaw CM. Presenile dementia and Alzheimer's disease in mongolism. Brain 92: 147-156 (1969).
72. Glenner GG, Wong CW. Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 122: 1131-1135 (1984).
73. Wisniewski HM, Rabe A. Discrepancy between Alzheimer-type neuropathology and dementia in persons with Down's syndrome. Ann N Y Acad Sci 477: 247-260 (1986).
74. Roizen NJ, Patterson D. Down's syndrome. Lancet 361: 1281-1289 (2003).
75. Torres EM, Williams BR, Amon A. Aneuploidy: cells losing their balance. Genetics 179: 737-746 (2008).
76. Li J, Xu M, Zhou H, Ma J, Potter H. Alzheimer presenilins in the nuclear membrane, interphase kinetochores, and centrosomes suggest a role in chromosome segregation. Cell 90: 917-927 (1997).
77. Ramírez MJ, Puerto S, Galofré P, Parry EM, Parry JM, Creus A, et al. Multicolour FISH detection of radioactive iodine-induced 17cen-p53 chromosomal breakage in buccal cells from therapeutically exposed patients. Carcinogenesis 21: 1581-1586 (2000).
78. Chen Y, McPhie DL, Hirschberg J, Neve RL. The amyloid precursor protein-binding protein APP-BP1 drives the cell cycle through the S-M checkpoint and causes apoptosis in neurons. J Biol Chem 275: 8929-8935 (2000).
79. 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 6: 1509-1524 (2002).
80. Klein JA, Ackerman SL. Oxidative stress, cell cycle, and neurodegeneration. J Clin Invest 111: 785-793 (2003).
81. Langley B, Ratan RR. Oxidative stress-induced death in the nervous system: cell cycle dependent or independent? J Neurosci Res 77: 621-629 (2004).
82. Zhu X, Raina AK, Perry G, Smith MA. Alzheimer's disease: the two-hit hypothesis. Lancet Neurol 3: 219-226 (2004).
83. 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 101: 343-347 (2004).
84. Jin K, Galvan V, Xie L, Mao XO, Gorostiza OF, Bredesen DE, et al. Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice. Proc Natl Acad Sci USA 101: 13363-13367 (2004).
85. Feng R, Rampon C, Tang YP, Shrom D, Jin J, Kyin M, et al. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 32: 911-926 (2001). Erratum in: Neuron 33: 313 (2002).
86. 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 10: 8-19 (2002).
87. Verret L, Jankowsky JL, Xu GM, Borchelt DR, Rampon C. Alzheimer's-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hippocampal neurogenesis. J Neurosci 27: 6771-6780 (2007).
88. Zhang C, McNeil E, Dressler L, Siman R. Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer's disease. Exp Neurol 204: 77-87 (2007).
89. Rodríguez JJ, Jones VC, Tabuchi M, Allan SM, Knight EM, LaFerla FM, et al. Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer's disease. PLoS ONE 3: e2935 (2008).
90. Donovan MH, Yazdani U, Norris RD, Games D, German DC, Eisch AJ. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol 495: 70-83 (2006).
91. German DC, Eisch AJ. Mouse models of Alzheimer's disease: insight into treatment. Rev Neurosci 15: 353-369 (2004).
92. Heo C, Chang KA, Choi HS, Kim HS, Kim S, Liew H, et al. Effects of the monomeric, oligomeric, and fibrillar Abeta42 peptides on the proliferation and differentiation of adult neural stem cells from subventricular zone. J Neurochem 102: 493-500 (2007).
93. Taupin P. Adult neurogenesis and neural stem cells in mammals. Nova Science Publishers. New York. First Edition (2007).
94. Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, et al. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann Neurol 55: 306-319 (2004).
95. Small GW, Kepe V, Ercoli LM, Siddarth P, Bookheimer SY, Miller KJ, et al. PET of brain amyloid and tau in mild cognitive impairment. N Engl J Med 355: 2652-2663 (2006).
96. van Oijen M, Hofman A, Soares HD, Koudstaal PJ, Breteler MM. Plasma Abeta(1-40) and Abeta(1-42) and the risk of dementia: a prospective case-cohort study. Lancet Neurol 5: 655-660 (2006).
97. Finehout EJ, Franck Z, Choe LH, Relkin N and Lee KH. Cerebrospinal fluid proteomic biomarkers for Alzheimer's disease. Ann Neurol 61: 120-129 (2007).
98. Forsberg A, Engler H, Almkvist O, Blomquist G, Hagman G, Wall A, et al. PET imaging of amyloid deposition in patients with mild cognitive impairment. Neurobiol Aging 29: 1456-1465 (2007).
99. Nordberg A. Amyloid imaging in Alzheimer's disease. Curr Opin Neurol 20: 398-402 (2007).
100. Kawas CH. Clinical practice. Early Alzheimer's disease. N Engl J Med 349: 1056-1063 (2003).
101. Scarpini E, Scheltens P, Feldman H. Treatment of Alzheimer's disease: current status and new perspectives. Lancet Neurol 2: 539-547 (2003).
102. Arrieta JL, Artalejo FR. Methodology, results and quality of clinical trials of tacrine in the treatment of Alzheimer's disease: a systematic review of the literature. Age Ageing 27: 161-179 (1998).
103. Wilkinson DG, Francis PT, Schwam E, Payne-Parrish J. Cholinesterase inhibitors used in the treatment of Alzheimer's disease: the relationship between pharmacological effects and clinical efficacy. Drugs Aging 21: 453-478 (2004).
104. Aisen PS. The development of anti-amyloid therapy for Alzheimer's disease : from secretase modulators to polymerisation inhibitors. CNS Drugs 19: 989-996 (2005).
105. Creeley C, Wozniak DF, Labruyere J, Taylor GT, Olney JW. Low doses of memantine disrupt memory in adult rats. J Neurosci 26: 3923-3932 (2006).
106. McShane R, Areosa Sastre A, Minakaran N. Memantine for dementia. Cochrane Database Syst Rev 2: CD003154 (2006).
107. Estrada LD, Soto C. Disrupting beta-amyloid aggregation for Alzheimer disease treatment. Curr Top Med Chem 7: 115-126 (2007).
108. Janus C. Vaccines for Alzheimer's disease: how close are we? CNS Drugs 17: 457-474 (2003).
109. Solomon B. Intravenous immunoglobulin and Alzheimer's disease immunotherapy. Curr Opin Mol Ther 9: 79-85 (2007).
110. Rehen SK, McConnell MJ, Kaushal D, Kingsbury MA, Yang AH, Chun J. Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proc Natl Acad Sci USA 98: 13361-13366 (2001).
111. Rehen SK, Yung YC, McCreight MP, Kaushal D, Yang AH, Almeida BS, et al. Constitutional aneuploidy in the normal human brain. J Neurosci 25: 2176-2180 (2005).
112. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, et al. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425: 968-973 (2003).
113. Yang Y, Geldmacher DS, Herrup K. DNA replication precedes neuronal cell death in Alzheimer's disease. J Neurosci 21: 2661-2668 (2001).
114. Busser J, Geldmacher DS, Herrup K. Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J Neurosci 18; 2801-2807 (1998).
115. Vincent I, Rosado M, Davies P. Mitotic mechanisms in Alzheimer's disease? J Cell Biol 132: 413-425 (1996).
116. Herrup K, Neve R, Ackerman SL, Copani A. Divide and die: cell cycle events as triggers of nerve cell death. J Neurosci 24: 9232-9239 (2004).
117. Yang Y, Mufson EJ, Herrup K. Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J Neurosci 23: 2557-2563 (2003).
118. Herrup K, Arendt T. Re-expression of cell cycle proteins induces neuronal cell death during Alzheimer's disease. J Alzheimers Dis 4: 243-247 (2002).
119. Morshead CM, van der Kooy D. Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J Neurosci 12: 249-256 (1992).
120. Cameron HA, McKay RD. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435: 406-417 (2001).
121. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495 (1997).
122. Miller MW and Nowakowski RS. Use of bromodeoxyuridine- immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 457: 44-52 (1988).
123. del Rio JA and Soriano E. Immunocytochemical detection of 5′-bromodeoxyuridine incorporation in the central nervous system of the mouse. Brain Res. Dev Brain Res 49: 311-317 (1989).
124. Nowakowski RS and Hayes NL. New neurons: extraordinary evidence or extraordinary conclusion? Science 288: 771 (2000).
125. Gould E and Gross CG. Neurogenesis in adult mammals: some progress and problems. J Neurosci 22: 619-623 (2002).
126. Rakic P. Adult neurogenesis in mammals: an identity crisis. J Neurosci 22: 614-618 (2002).
127. Taupin P. BrdU Immunohistochemistry for Studying Adult Neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 53: 198-214 (2007).
128. Taupin P. Protocols for studying adult neurogenesis: insights and recent developments. Reg Med 2: 51-62 (2007).
129. Poduslo JF, Curran GL, Wengenack TM, Malester B, Duff K. Permeability of proteins at the blood-brain barrier in the normal adult mouse and double transgenic mouse model of Alzheimer's disease. Neurobiol Dis 8: 555-567 (2001).
130. Desai BS, Monahan AJ, Carvey PM, Hendey B. Blood-brain barrier pathology in Alzheimer's and Parkinson's disease: implications for drug therapy. Cell Transplant 16: 285-299 (2007).
131. Taupin P. The therapeutic potential of adult neural stem cells. Curr Opin Mol Ther 8: 225-231 (2006).
132. Mitsiadis TA, Barrandon O, Rochat A, Barrandon Y, De Bari C. Stem cell niches in mammals. Exp Cell Res 313: 3377-3385 (2007).
133. Ninkovic J, Götz M. Signaling in adult neurogenesis: from stem cell niche to neuronal networks. Curr Opin Neurobiol 17: 338-344 (2007).
134. Taupin P. Adult neural stem cells, neurogenic niches and cellular therapy. Stem Cell Rev 2: 213-220 (2006).
135. Chin VI, Taupin P, Sanga S, Scheel J, Gage FH, Bhatia SN. Microfabricated platform for studying stem cell fates. Biotechnol Bioeng 88: 399-415 (2004).
136. Brown AB, Yang W, Schmidt NO, Carroll R, Leishear KK, Rainov NG, et al. Intravascular delivery of neural stem cell lines to target intracranial and extracranial tumors of neural and non-neural origin. Hum Gene Ther 14: 1777-1785 (2003).
137. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, et al. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422: 688-694 (2003).
138. Taupin P. Consideration of adult neurogenesis from basic science to therapy. Med Sci Monit 11: LE16-LE17 (2005).