Pharmacologic reversal of neurogenic and neuroplastic abnormalities and cognitive impairments without affecting Aβ and tau pathologies in 3xTg-AD mice

Acta Neuropathologica

Volumn 120, Issue 5, 2010, Pages 605-621

  Blanchard, Julie ^a   Wanka, Lukas ^a,c   Tung, Yunn Chyn ^a   Cárdenas Aguayo, María Del Carmen ^a   Laferla, Frank M ^b   Iqbal, Khalid ^a   Grundke Iqbal, Inge ^a  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Alzheimer disease; CNTF; Cognition; Neurogenesis; Neuronal plasticity; Tau hyperphosphorylation

Indexed keywords

AMYLOID BETA PROTEIN; CENTRAL NERVOUS SYSTEM AGENTS; CILIARY NEUROTROPHIC FACTOR; TAU PROTEIN; UNCLASSIFIED DRUG; VALYLGLYCYLASPARTYLGLYCYLGLYCYLLEUCYLPHENYLALANYLGLUTAMYLLYSYLLYSYLLEUCINE;

ALZHEIMER DISEASE; AMYLOID NEUROPATHY; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BODY WEIGHT; CHRONIC DRUG ADMINISTRATION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ASSOCIATION; DISEASE COURSE; DRUG DESIGN; DRUG EFFECT; DRUG MECHANISM; DRUG STRUCTURE; DRUG SYNTHESIS; EXPLORATORY BEHAVIOR; FEMALE; GRANULAR CELL; HIPPOCAMPUS; LOCOMOTION; MOTOR COORDINATION; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROFIBRILLARY TANGLE; NONHUMAN; PHYSICAL CAPACITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECOGNITION; REFERENCE MEMORY; SHORT TERM MEMORY; SPATIAL MEMORY; TASK PERFORMANCE; TAUOPATHY; TRANSGENIC MOUSE; TREATMENT DURATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BLOTTING, WESTERN; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CILIARY NEUROTROPHIC FACTOR; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; MAZE LEARNING; MEMORY; MICE; MICE, TRANSGENIC; NEUROFIBRILLARY TANGLES; NEUROGENESIS; NEURONAL PLASTICITY; NEUROPROTECTIVE AGENTS; PEPTIDES; PLAQUE, AMYLOID; PROTEIN STRUCTURE, SECONDARY; TAU PROTEINS;

EID: 78149414428     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-010-0734-6     Document Type: Article

References (76)

1. MA Aberg ND Aberg H Hedbacker J Oscarsson PS Eriksson 2000 Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus J Neurosci 20 2896 2903 1:CAS:528:DC%2BD3cXisVertLY%3D 10751442
2. Abrous DN, Wojtowics JM (2008) Neurogenesis and hippocampal memory system. In: Adult neurogenesis. Cold Spring Harbor Press, New York
3. ACTSG 1996 A double-blind placebo-controlled clinical trial of subcutaneous recombinant human ciliary neurotrophic factor (rHCNTF) in amyotrophic lateral sclerosis. ALS CNTF Treatment Study Group Neurology 46 1244 1249
4. JB Aimone J Wiles FH Gage 2006 Potential role for adult neurogenesis in the encoding of time in new memories Nat Neurosci 9 723 727 1:CAS:528: DC%2BD28XltVeqtLg%3D 10.1038/nn1707 16732202
5. MF Anderson MA Aberg M Nilsson PS Eriksson 2002 Insulin-like growth factor-I and neurogenesis in the adult mammalian brain Brain Res Dev Brain Res 134 115 122 1:CAS:528:DC%2BD38Xis1Oqtbw%3D 10.1016/S0165-3806(02)00277-8 11947942 (Pubitemid 34310242)
6. S Artero MC Tierney J Touchon K Ritchie 2003 Prediction of transition from cognitive impairment to senile dementia: a prospective, longitudinal study Acta Psychiatr Scand 107 390 393 1:STN:280:DC%2BD3s3lvFWitA%3D%3D 10.1034/j.1600-0447.2003.00081.x 12752036 (Pubitemid 36606157)
7. CP Arthur MH Stowell 2007 Structure of synaptophysin: a hexameric MARVEL-domain channel protein Structure 15 707 714 1:CAS:528: DC%2BD2sXmtlahtbo%3D 10.1016/j.str.2007.04.011 17562317 (Pubitemid 46874081)
8. A Bensadoun D Weinstein 1976 Assay of proteins in the presence of interfering materials Anal Biochem 70 241 250 1:CAS:528:DyaE28Xos1emsA%3D%3D 10.1016/S0003-2697(76)80064-4 1259145
9. LM Billings S Oddo KN Green JL McGaugh FM LaFerla 2005 Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice Neuron 45 675 688 1:CAS:528:DC%2BD2MXis1yrs7s%3D 10.1016/j.neuron.2005.01.040 15748844 (Pubitemid 40320703)
10. M Blurton-Jones M Kitazawa H Martinez-Coria NA Castello FJ Muller JF Loring, et al. 2009 Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease Proc Natl Acad Sci USA 106 13594 13599 1:CAS:528:DC%2BD1MXhtVKksrfE 10.1073/pnas.0901402106 19633196
11. V Boissonneault M Filali M Lessard J Relton G Wong S Rivest 2009 Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease Brain 132 1078 1092 10.1093/brain/awn331 19151372
12. DS Bredt RA Nicoll 2003 AMPA receptor trafficking at excitatory synapses Neuron 40 361 379 1:CAS:528:DC%2BD3sXosFCqsrY%3D 10.1016/S0896-6273(03)00640-8 14556714 (Pubitemid 37244101)
13. MJ Butte 2001 Neurotrophic factor structures reveal clues to evolution, binding, specificity and receptor activation Cell Mol Life Sci 58 1003 1013 1:CAS:528:DC%2BD3MXmvFWhsb4%3D 10.1007/PL00000915 11529493
14. HA Cameron RD McKay 1999 Restoring production of hippocampal neurons in old age Nat Neurosci 2 894 897 1:CAS:528:DyaK1MXmsVyjsrw%3D 10.1038/13197 10491610 (Pubitemid 30602603)
15. NL Chevallier S Soriano DE Kang E Masliah G Hu EH Koo 2005 Perturbed neurogenesis in the adult hippocampus associated with presenilin-1 A246E mutation Am J Pathol 167 151 159 1:CAS:528:DC%2BD2MXms1eitrs%3D 15972961
16. Chohan MO, Li B, Blanchard J, Tung YC, Heaney AT, Rabe A et al (2009) Enhancement of dentate gyrus neurogenesis, dendritic and synaptic plasticity and memory by a neurotrophic peptide. Neurobiol Aging (in press)
17. RE Clark SM Zola LR Squire 2000 Impaired recognition memory in rats after damage to the hippocampus J Neurosci 20 8853 8860 1:CAS:528:DC%2BD3MXpslWn 11102494
18. GL Collingridge JT Isaac YT Wang 2004 Receptor trafficking and synaptic plasticity Nat Rev Neurosci 5 952 962 1:CAS:528:DC%2BD2cXpvFWrsbw%3D 10.1038/nrn1556 15550950 (Pubitemid 39593358)
19. ST DeKosky SW Scheff 1990 Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity Ann Neurol 27 457 464 1:STN:280:DyaK3c3pslGntg%3D%3D 10.1002/ana.410270502 2360787
20. ST DeKosky SW Scheff SD Styren 1996 Structural correlates of cognition in dementia: quantification and assessment of synapse change Neurodegeneration 5 417 421 1:STN:280:DyaK2s7nvFGktA%3D%3D 10.1006/neur.1996.0056 9117556 (Pubitemid 27077903)
21. M Demars YS Hu A Gadadhar O Lazarov 2010 Impaired neurogenesis is an early event in the etiology of familial Alzheimer's disease in transgenic mice J Neurosci Res 88 2103 2117 1:CAS:528:DC%2BC3cXnsVWitLg%3D 10.1002/jnr.22387 20209626
22. H Dong B Goico M Martin CA Csernansky A Bertchume JG Csernansky 2004 Modulation of hippocampal cell proliferation, memory, and amyloid plaque deposition in APPsw (Tg2576) mutant mice by isolation stress Neuroscience 127 601 609 1:CAS:528:DC%2BD2cXmt1Oht7o%3D 10.1016/j.neuroscience.2004.05.040 15283960 (Pubitemid 38993164)
23. MH Donovan U Yazdani RD Norris D Games DC German AJ Eisch 2006 Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease J Comp Neurol 495 70 83 10.1002/cne.20840 16432899 (Pubitemid 43238052)
24. Ennaceur A (2010) One-trial objects recognition in rats and mice: methodological and theoretical issues. Behav Brain Res (in press)
25. A Ennaceur JP Aggleton 1997 The effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat Behav Brain Res 88 181 193 1:STN:280:DyaK1c%2FmvVCgug%3D%3D 10.1016/S0166-4328(97)02297-3 9404627 (Pubitemid 27498504)
26. A Ennaceur N Neave JP Aggleton 1997 Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex the cingulum bundle and the fornix Exp Brain Res 113 509 519 1:STN:280:DyaK2s3mtFyjsQ%3D%3D 10.1007/PL00005603 9108217 (Pubitemid 27140274)
27. P Garcia I Youssef JK Utvik S Florent-Bechard V Barthelemy C Malaplate-Armand, et al. 2010 Ciliary neurotrophic factor cell-based delivery prevents synaptic impairment and improves memory in mouse models of Alzheimer's disease J Neurosci 30 7516 7527 1:CAS:528:DC%2BC3cXovVOitrc%3D 10.1523/JNEUROSCI.4182-09.2010 20519526
28. GG Glenner CW Wong 1984 Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein Biochem Biophys Res Commun 120 885 890 1:CAS:528:DyaL2cXitVOntLw%3D 10.1016/S0006-291X(84)80190-4 6375662
29. I Grundke-Iqbal K Iqbal YC Tung M Quinlan HM Wisniewski LI Binder 1986 Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology Proc Natl Acad Sci USA 83 4913 4917 1:CAS:528:DyaL28XksFyqtrg%3D 10.1073/pnas.83.13.4913 3088567
30. NJ Haughey D Liu A Nath AC Borchard MP Mattson 2002 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 1 125 135 1:CAS:528:DC%2BD38XjtFWms7k%3D 10.1385/NMM:1:2:125 12025858 (Pubitemid 37012521)
31. NJ Haughey A Nath SL Chan AC Borchard MS Rao MP Mattson 2002 Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis in models of Alzheimer's disease J Neurochem 83 1509 1524 1:CAS:528:DC%2BD3sXjsFyg 10.1046/j.1471-4159.2002.01267.x 12472904 (Pubitemid 35477489)
32. M Inoue H Karita C Nakayama H Noguchi 1997 Construction and characterization of ciliary neurotrophic factor (CNTF) antagonists: microenvironmental difference in the CNTF receptor between rat and chicken cells for recognizing the D1 cap region J Neurochem 69 95 101 1:CAS:528: DyaK2sXktV2nu7k%3D 10.1046/j.1471-4159.1997.69010095.x 9202298
33. R Janz TC Sudhof RE Hammer V Unni SA Siegelbaum VY Bolshakov 1999 Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I Neuron 24 687 700 1:CAS:528:DyaK1MXnvFyjsr8%3D 10.1016/S0896-6273(00)81122-8
34. K Jin AL Peel XO Mao L Xie BA Cottrell DC Henshall, et al. 2004 Increased hippocampal neurogenesis in Alzheimer's disease Proc Natl Acad Sci USA 101 343 347 1:CAS:528:DC%2BD2cXjvFaltg%3D%3D 10.1073/pnas.2634794100 14660786 (Pubitemid 38084252)
35. K Jin L Xie J Childs Y Sun XO Mao A Logvinova, et al. 2003 Cerebral neurogenesis is induced by intranasal administration of growth factors Ann Neurol 53 405 409 1:CAS:528:DC%2BD3sXit1ynurw%3D 10.1002/ana.10506 12601711 (Pubitemid 36258647)
36. KK Karishma J Herbert 2002 Dehydroepiandrosterone (DHEA) stimulates neurogenesis in the hippocampus of the rat promotes survival of newly formed neurons and prevents corticosterone-induced suppression Eur J Neurosci 16 445 453 1:STN:280:DC%2BD38vjs1Snug%3D%3D 10.1046/j.1460-9568.2002.02099.x 12193187 (Pubitemid 35471862)
37. N Kee CM Teixeira AH Wang PW Frankland 2007 Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus Nat Neurosci 10 355 362 1:CAS:528:DC%2BD2sXitVGku78%3D 10.1038/nn1847 17277773
38. G Kempermann HG Kuhn FH Gage 1998 Experience-induced neurogenesis in the senescent dentate gyrus J Neurosci 18 3206 3212 1:CAS:528:DyaK1cXivFCht7w%3D 9547229
39. KS Kim DL Miller VJ Sapienza J Chen C-M C Bai I Grundke-Iqbal, et al. 1988 Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid peptide Neurosci Res Commun 2 121 130 1:CAS:528:DyaL1MXhsFSrsbs%3D
40. HG Kuhn H Dickinson-Anson FH Gage 1996 Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation J Neurosci 16 2027 2033 1:CAS:528:DyaK28XhvVGnsro%3D 8604047
41. HG Kuhn J Winkler G Kempermann LJ Thal FH Gage 1997 Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain J Neurosci 17 5820 5829 1:CAS:528: DyaK2sXkvFynu7o%3D 9221780
42. B Leuner E Gould TJ Shors 2006 Is there a link between adult neurogenesis and learning? Hippocampus 16 216 224 10.1002/hipo.20153 16421862
43. B Li H Yamamori Y Tatebayashi B Shafit-Zagardo H Tanimukai S Chen, et al. 2008 Failure of neuronal maturation in Alzheimer disease dentate gyrus J Neuropathol Exp Neurol 67 78 84 1:CAS:528:DC%2BD1cXhtlyisr4%3D 10.1097/nen.0b013e318160c5db 18091557
44. RJ Lichtenwalner ME Forbes SA Bennett CD Lynch WE Sonntag DR Riddle 2001 Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis Neuroscience 107 603 613 1:CAS:528:DC%2BD3MXosFKnsLo%3D 10.1016/S0306-4522(01)00378-5 11720784 (Pubitemid 33097497)
45. PM Lledo M Alonso MS Grubb 2006 Adult neurogenesis and functional plasticity in neuronal circuits Nat Rev Neurosci 7 179 193 1:CAS:528: DC%2BD28Xhs1Gqt78%3D 10.1038/nrn1867 16495940 (Pubitemid 43292464)
46. R Malinow RC Malenka 2002 AMPA receptor trafficking and synaptic plasticity Annu Rev Neurosci 25 103 126 1:CAS:528:DC%2BD38XmtF2hsLw%3D 10.1146/annurev.neuro.25.112701.142758 12052905 (Pubitemid 34748013)
47. E Masliah M Mallory L Hansen R DeTeresa M Alford R Terry 1994 Synaptic and neuritic alterations during the progression of Alzheimer's disease Neurosci Lett 174 67 72 1:CAS:528:DyaK2cXltlWnurk%3D 10.1016/0304-3940(94)90121-X 7970158 (Pubitemid 24205235)
48. W Mayo O George S Darbra JJ Bouyer M Vallee M Darnaudery, et al. 2003 Individual differences in cognitive aging: implication of pregnenolone sulfate Prog Neurobiol 71 43 48 1:CAS:528:DC%2BD3sXovVWhtLc%3D 10.1016/j.pneurobio.2003. 09.006 14611866 (Pubitemid 37377934)
49. HY McDonald JM Wojtowicz 2005 Dynamics of neurogenesis in the dentate gyrus of adult rats Neurosci Lett 385 70 75 1:CAS:528:DC%2BD2MXlslyltrg%3D 10.1016/j.neulet.2005.05.022 15967575 (Pubitemid 40909984)
50. NQ McDonald N Panayotatos WA Hendrickson 1995 Crystal structure of dimeric human ciliary neurotrophic factor determined by MAD phasing EMBO J 14 2689 2699 1:CAS:528:DyaK2MXms1Cktrk%3D 7796798
51. JB Mitchell J Laiacona 1998 The medial frontal cortex and temporal memory: tests using spontaneous exploratory behaviour in the rat Behav Brain Res 97 107 113 1:STN:280:DyaK1M%2FotlWhtw%3D%3D 10.1016/S0166-4328(98)00032-1 9867236 (Pubitemid 28558854)
52. AV Molofsky S He M Bydon SJ Morrison R Pardal 2005 Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways Genes Dev 19 1432 1437 1:CAS:528:DC%2BD2MXlslChurc%3D 10.1101/gad.1299505 15964994 (Pubitemid 41003009)
53. D Morgan S Munireddy J Alamed J DeLeon DM Diamond P Bickford, et al. 2008 Apparent behavioral benefits of tau overexpression in P301L tau transgenic mice J Alzheimers Dis 15 605 614 1:CAS:528:DC%2BD1cXhsFSmt7jK 19096159
54. RG Morris P Garrud JN Rawlins J O'Keefe 1982 Place navigation impaired in rats with hippocampal lesions Nature 297 681 683 1:STN:280:DyaL383itVSguw%3D%3D 10.1038/297681a0 7088155 (Pubitemid 12096189)
55. J Nacher G Alonso-Llosa DR Rosell BS McEwen 2003 NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus Neurobiol Aging 24 273 284 1:CAS:528:DC%2BD38XpslSlt7Y%3D 10.1016/S0197-4580(02) 00096-9 12498961 (Pubitemid 36005408)
56. AH Nagahara DA Merrill G Coppola S Tsukada BE Schroeder GM Shaked, et al. 2009 Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease Nat Med 15 331 337 1:CAS:528: DC%2BD1MXhsFeqsbg%3D 10.1038/nm.1912 19198615
57. G Neves SF Cooke TV Bliss 2008 Synaptic plasticity, memory and the hippocampus: a neural network approach to causality Nat Rev Neurosci 9 65 75 1:CAS:528:DC%2BD2sXhsVGjsbbI 10.1038/nrn2303 18094707 (Pubitemid 350295694)
58. S Oddo A Caccamo JD Shepherd MP Murphy TE Golde R Kayed, et al. 2003 Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction Neuron 39 409 421 1:CAS:528:DC%2BD3sXmsFOksro%3D 10.1016/S0896-6273(03)00434-3 12895417 (Pubitemid 36937044)
59. S Pellow P Chopin SE File M Briley 1985 Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat J Neurosci Methods 14 149 167 1:STN:280:DyaL28%2Fht12htw%3D%3D 10.1016/0165-0270(85)90031-7 2864480 (Pubitemid 16239568)
60. KS Rai B Hattiangady AK Shetty 2007 Enhanced production and dendritic growth of new dentate granule cells in the middle-aged hippocampus following intracerebroventricular FGF-2 infusions Eur J Neurosci 26 1765 1779 10.1111/j.1460-9568.2007.05820.x 17883411 (Pubitemid 47493203)
61. MS Rao B Hattiangady AK Shetty 2006 The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus Aging Cell 5 545 558 1:CAS:528:DC%2BD2sXhsF2nsg%3D%3D 10.1111/j.1474-9726.2006.00243.x 17129216 (Pubitemid 44782623)
62. G Riedel J Micheau AG Lam EL Roloff SJ Martin H Bridge, et al. 1999 Reversible neural inactivation reveals hippocampal participation in several memory processes Nat Neurosci 2 898 905 1:CAS:528:DyaK1MXmsVyjsr0%3D 10.1038/13202 10491611 (Pubitemid 30602604)
63. F Rousseau JF Gauchat JG McLeod S Chevalier C Guillet F Guilhot, et al. 2006 Inactivation of cardiotrophin-like cytokine, a second ligand for ciliary neurotrophic factor receptor, leads to cold-induced sweating syndrome in a patient Proc Natl Acad Sci USA 103 10068 10073 1:CAS:528:DC%2BD28XmvVaju7s%3D 10.1073/pnas.0509598103 16782820 (Pubitemid 43993624)
64. J Sanchez-Ramos S Song V Sava B Catlow X Lin T Mori, et al. 2009 Granulocyte colony stimulating factor decreases brain amyloid burden and reverses cognitive impairment in Alzheimer's mice Neuroscience 163 55 72 1:CAS:528:DC%2BD1MXhtVSmsr3N 10.1016/j.neuroscience.2009.05.071 19500657
65. F Sargolini P Roullet A Oliverio A Mele 2003 Effects of intra-accumbens focal administrations of glutamate antagonists on object recognition memory in mice Behav Brain Res 138 153 163 1:CAS:528:DC%2BD3sXjtF2hug%3D%3D 10.1016/S0166-4328(02)00238-3 12527446 (Pubitemid 36071354)
66. CI Sze JC Troncoso C Kawas P Mouton DL Price LJ Martin 1997 Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease J Neuropathol Exp Neurol 56 933 944 1:STN:280:DyaK2svgt1yrtw%3D%3D 10.1097/00005072-199708000-00011 9258263
67. RD Terry E Masliah DP Salmon N Butters R DeTeresa R Hill, et al. 1991 Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment Ann Neurol 30 572 580 1:STN:280:DyaK387mtFOntw%3D%3D 10.1002/ana.410300410 1789684
68. JL Trejo E Carro I Torres-Aleman 2001 Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus J Neurosci 21 1628 1634 1:CAS:528:DC%2BD3MXjslClurs%3D 11222653
69. KJ Tsai YC Tsai CK Shen 2007 G-CSF rescues the memory impairment of animal models of Alzheimer's disease J Exp Med 204 1273 1280 1:CAS:528:DC%2BD2sXms1aktrk%3D 10.1084/jem.20062481 17517969 (Pubitemid 46919864)
70. H van Praag AF Schinder BR Christie N Toni TD Palmer FH Gage 2002 Functional neurogenesis in the adult hippocampus Nature 415 1030 1034 10.1038/4151030a 11875571 (Pubitemid 34193451)
71. Verret L, Trouche S, Zerwas M, Rampon C (2007) Hippocampal neurogenesis during normal and pathological aging. Psychoneuroendocrinology 32(Suppl 1):S26-S30
72. JM Wang C Singh L Liu RW Irwin S Chen EJ Chung, et al. 2010 Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease Proc Natl Acad Sci USA 107 6498 6503 1:CAS:528: DC%2BC3cXkslynu7Y%3D 10.1073/pnas.1001422107 20231471
73. KA Welsh N Butters JP Hughes RC Mohs A Heyman 1992 Detection and staging of dementia in Alzheimer's disease. Use of the neuropsychological measures developed for the Consortium to Establish a Registry for Alzheimer's Disease Arch Neurol 49 448 452 1:STN:280:DyaK383lsFGmtw%3D%3D 1580805
74. PH Wen PR Hof X Chen K Gluck G Austin SG Younkin, et al. 2004 The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice Exp Neurol 188 224 237 1:CAS:528:DC%2BD2cXlsFygt7Y%3D 10.1016/j.expneurol.2004.04.002 15246822 (Pubitemid 38891583)
75. MJ West L Slomianka HJ Gundersen 1991 Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator Anat Rec 231 482 497 1:STN:280:DyaK387ntFWrtw%3D%3D 10.1002/ar.1092310411 1793176
76. M Windisch A Gschanes B Hutter-Paier 1998 Neurotrophic activities and therapeutic experience with a brain derived peptide preparation J Neural Transm Suppl 53 289 298 1:CAS:528:DyaK1cXmvVWnt7Y%3D 9700665