Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer's Ddisease

PLoS ONE

Volumn 3, Issue 8, 2008, Pages

  Rodríguez, José J ^a   Jones, Victoria C ^a   Tabuchi, Masashi ^a   Allan, Stuart M ^a   Knight, Elysse M ^a   LaFerla, Frank M ^b   Oddo, Salvatore ^b   Verkhratsky, Alexei ^a,c  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HISTONE H3; PRESENILIN 1; TAU PROTEIN; PRESENILIN; SERUM AMYLOID A;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LABELING; CELL PROLIFERATION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DISEASE SEVERITY; FEMALE; GLIA CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PREVALENCE; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SEX DIFFERENCE; TRANSGENIC MOUSE; AGING; AMINO ACID SUBSTITUTION; ANIMAL; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; PATHOLOGY;

MAMMALIA; MUS; MUS MUSCULUS;

AGING; ALZHEIMER DISEASE; AMINO ACID SUBSTITUTION; ANIMALS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; PRESENILINS; SERUM AMYLOID A PROTEIN; TAU PROTEINS;

EID: 51849123324     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002935     Document Type: Article

References (54)

1. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319-335.
2. Ramón y Cajal S (1913) Estudios sobre la degeneración y regeneración del sistema nervioso. Madrid: Imprenta de Hijos de Nicolás Moya.
3. Gross CG (2000) Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1: 67-73.
4. Taupin P, Gage FH (2002) Adult neurogenesss and neural stem cells of the central nervous system in mammals. J Neurosci Res 69: 745-749.
5. Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85: 523-569.
6. Paterson JA, Privat A, Ling EA, Leblond CP (1973) Investigation of glial cells in semithin sections. 3. Transformation of subependymal cells into glial cells, as shown by radioautography after 3 H-thymidine injection into the lateral ventricle of the brain of young rats. J Comp Neurol. 149: 83-102.
7. Levison SW, Goldman JE (1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron. 10: 201-12.
8. Kempermann G, Gage FH (1999) New nerve cells for the adult brain. Sci Am 280: 48-53.
9. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, et al. (2002) Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
10. Mayo W, Lemaire V, Malaterre J, Rodriguez JJ, Cayre M, et al. (2005) Pregnenolone sulfate enhances neurogenesis and PSA-NCAM in young and aged hippocampus. Neurobiol Aging 26: 103-114.
11. Tatebayashi Y, Lee MH, Li L, Iqbal K, Grundke-Iqbal I (2003) The dentate gyrus neurogenesis: a therapeutic target for Alzheimer's disease. Acta Neuropathol 105: 225-232.
12. Price DL, Struble RG, Whiteouse PJ, Kitt CA, Cork LC, et al. (1986) Alzheimer's disease: a multisystem disorder. Res Publ Assoc Res Nerv Dis 64: 209-214.
13. Braak R, Braak H (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 82: 239-259.
14. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH (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.
15. Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18: 3206-3212.
16. Verret L, Jankowsky JL, Xu GM, Borchelt DR, Rampon C (2007) Alzheimer's-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hippocampal neurogenesis. J Neurosci 27: 6771-6780.
17. Gage FH, Kempermann G, Palmer TD, Peterson DA, Ray J (1998) Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 36: 249-266.
18. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, et al. (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 101: 343-347.
19. Feng R, Rampon C, Tang YP, Shrom D, Jin J, et al. (2001) Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 32: 911-926.
20. Haughey NJ, Nath A, Chan SL, Borchard AC, Rao MS, et al. (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.
21. Haughey NJ, Liu D, Nath A, Borchard AC, Mattson MP (2002) Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amnyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease. Neuromolecular Med 1: 125-135.
22. Wen PH, Shao X, Shao Z, Hof PR, Wisniewski T, et al. (2002) Overexpression of wild type but not an FAD mutant presenilin-1 promotes neurogenesis in the hippocampus of adult mice. Neurobiol Dis 10: 8-19.
23. Caillé I, Allinquant B, Dupont E, Bouillot C, Langer A, et al. (2004) Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development 131: 2173-2181.
24. Dong H, Goico B, Martin M, Csernansky CA, Bertchume A, et al. (2004) Modulation of hippocampal cell proliferation, memory, and amyloid plaque deposition in APPsw (Tg2576) mutant mice by isolation stress. Neuroscience 127: 601-609.
25. Wang R, Dineley KT, Sweatt JD, Zheng H (2004) Presenilin 1 familial Alzheimer's disease mutation leads to defective associative learning and impaired adult neurogenesis. Neuroscience 126: 305-312.
26. Wolf SA, Kronenberg G, Lehmann K, Blankenship A, Overall R, et al. (2006) Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer's disease. Biol Psychiatry 60: 1314-1323.
27. Chevallier NL, Soriano S, Kang DE, Masliah E, Hu G, et al. (2005) Perturbed neurogenesis in the adult hippocampus associated with presenilin-1 A246E mutation. Am J Pathol 167: 151-159.
28. Donovan MH, Yazdani U, Norris RD, Games D, German DC, et al. (2006) Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol 495: 70-83.
29. Jin K, Galvan V, Xie L, Mao XO, Gorostiza OF, et al. (2004) Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw, Ind) mice. Proc Natl Acad Sci U S A 101: 13363-13367.
30. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, et al. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-421.
31. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24: 1063-1070.
32. Frazer ME, Hughes JE, Mastrangelo MA, Tibbens JL, Federoff HJ, et al. (2008) Reduced pathology and improved behavioral performance in Alzheimer's disease mice vaccinated with HSV amplicons expressing amyloid-beta and interleukin-4. Mol Ther. 16: 845-853.
33. McKee AC, Carreras I, Hossain L, Ryu H, Klein WL, et al. (2008) Ibuprofen reduces Abeta, hyperphosphorylated tau and memory deficits in Alzheimer mice. Brain Res. 1207: 225-236.
34. Carroll JC, Rosario ER, Chang L, Stanczyk FZ, Oddo S, et al. (2007) Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3xTg-AD mice. J Neurosci. 27: 13357-13365.
35. Baum LW (2005) Sex, hormones, and Alzheimer's disease. J Gerontol A Biol Sci Med Sci 60: 736-743.
36. Webber KM, Casadesus G, Perry G, Atwood CS, Bowen R, et al. (2005) Gender differences in Alzheimer disease: the role of luteinizing hormone in disease pathogenesis. Alzheimer Dis Assoc Disord 19: 95-99.
37. Clinton LK, Billings LM, Green KN, Caccamo A, Ngo J, et al. (2007) Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice. Neurobiol Dis. 28: 76-82.
38. Eng LF, Ghirnikar RS, Lee YL (2000) Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 25: 1439-1451.
39. Hsu S, Raine L, Franger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577-580.
40. Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.
41. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, et al. (2004) Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev. 28: 273-283.
42. Syková E, Vorísek I, Antonova T, Mazel T, Meyer-Luehmann M, et al. (2005), Jucker M (2005) Changes in extracellular space size and geometry in APP23 transgenic mice: a model of Alzheimer's disease. Proc Natl Acad Sci U S A. 102: 479-484.
43. Shoes TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, et al. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410: 372-376.
44. Boekhoorn K, Joels M, Lucassen PJ (2006) Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol Dis. 24: 1-14.
45. Cooper-Kuhn CM, Kuhn HG (2002) Is it all DNA repair? Methodological considerations for detecting neurogenesis in the adult brain. Brain Res Dev Brain Res 134: 13-21.
46. Rakic P (2002) Adult neurogenesis in mammals: an identity crisis. J Neurosci 22: 614-618.
47. Manly JJ, Merchant CA, Jacobs DM, Small SA, Bell K, et al. (2000) Endogenous estrogen levels and Alzheimer's disease among postmenopausal women. Neurology 54: 833-837.
48. Galea LA, Spritzer MD, Barker JM, Pawluski JL (2006) Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 16: 225-232.
49. Tanapat P, Hastings NB, Reeves AJ, Gould E (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19: 5792-5801.
50. Jacobsen JS, Wu CC, Redwine JM, Comery TA, Arias R, et al. (2006) Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 103: 5161-5166.
51. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis Cell 132: 645-660.
52. Lagace DC, Fischer SJ, Eisch AJ (2007) Gender and endogenous levels of estradiol do not influence adult hippocampal neurogeneais in mice. Hippocampus 17: 175-180.
53. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, et al. (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439: 589-593.
54. Olson AK, Eadie BD, Ernst C, Christie BR (2006) Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16: 250-260.