Stage-specific changes in neurogenic and glial markers in Alzheimer's disease

Biological Psychiatry

Volumn 77, Issue 8, 2015, Pages 711-719

  Ekonomou, Antigoni ^a   Savva, George M ^b   Brayne, Carol ^b   Forster, Gillian ^c   Francis, Paul T ^a   Johnson, Mary ^d   Perry, Elaine K ^d   Attems, Johannes ^d   Somani, Alyma ^a   Minger, Stephen L ^a   Ballard, Clive G ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Alzheimer's disease; Glia; Human brain; Neural progenitors; Neurogenesis; Tangles

Indexed keywords

CYCLINE; GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE PROTEIN; NEURONAL PROTEIN C; NEURONAL PROTEIN D; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ARTICLE; ASTROCYTE; CELL NUCLEUS; CONTROLLED STUDY; DENTATE GYRUS; DISEASE SEVERITY; EPENDYMA CELL; FEMALE; GLIA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROPATHOLOGY; PRIORITY JOURNAL; SUBVENTRICULAR ZONE; ANIMAL; CELL COUNT; LATERAL BRAIN VENTRICLE; METABOLISM; NERVE CELL; PATHOLOGY; STEM CELL; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; CELL COUNT; DENTATE GYRUS; HUMANS; LATERAL VENTRICLES; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; STEM CELLS;

EID: 84933066893     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.05.021     Document Type: Article

References (59)

1. Alzheimer's Disease International. World Alzheimer report 2009. Available at: http://www.alz.co.uk/research/world-report. Accessed March 2010.
2. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996): Chain migration of neuronal precursors. Science 271:978-981.
3. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997): Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17: 5046-5061.
4. Palmer TD, Takahashi J, Gage FH (1997): The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8:389-404.
5. Ma DK, Bonaguidi MA, Ming GL, Song H (2009): Adult neural stem cells in the mammalian central nervous system. Cell Res 19:672-682.
6. Rochefort C, Gheusi G, Vincent JD, Lledo PM (2002): Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22:2679-2689.
7. Magavi SS, Mitchell BD, Szentirmai O, Carter BS, Macklis JD (2005): Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J Neurosci 25:10729-10739.
8. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, et al. (2008): Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153-1161.
9. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007): A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559-566.
10. Kee N, Teixeira CM, Wang AH, Frankland PW (2007): Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355-362.
11. Tashiro A, Makino H, Gage FH (2007): Experience-specific functional modification of the dentate gyrus through adult neurogenesis: A critical period during an immature stage. J Neurosci 27:3252-3259.
12. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. (1998): Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
13. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, et al. (2004): Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427: 740-744.
14. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, et al. (2006): Cellular composition and cytoarchitecture of the adult human subventricular zone: A niche of neural stem cells. J Comp Neurol 494:415-434.
15. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, et al. (2007): Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243-1249.
16. Abrous DN, Koehl M, Le Moal M (2005): Adult neurogenesis: From precursors to network and physiology. Physiol Rev 85:523-569.
17. Vaidya VA, Vadodaria KC, Jha S (2007): Neurotransmitter regulation of adult neurogenesis: Putative therapeutic targets. CNS Neurol Disord Drug Targets 6:358-374.
18. Ziabreva I, Perry E, Perry R, Minger SL, Ekonomou A, Przyborski S, Ballard C (2006): Altered neurogenesis in Alzheimer's disease. J Psychosom Res 61:311-316.
19. Perry EK, Johnson M, Ekonomou A, Perry RH, Ballard C, Attems J (2012): Neurogenic abnormalities in Alzheimer's disease differ between stages of neurogenesis and are partly related to cholinergic pathology. Neurobiol Dis 47:155-162.
20. Li B, Yamamori H, Tatebayashi Y, Shafit-Zagardo B, Tanimukai H, Chen S, et al. (2008): Failure of neuronal maturation in Alzheimer disease dentate gyrus. J Neuropathol Exp Neurol 67:78-84.
21. 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.
22. Ekonomou A, Ballard CG, Pathmanaban ON, Perry RH, Perry EK, Kalaria RN, Minger SL (2011): Increased neural progenitors in vascular dementia. Neurobiol Aging 32:2152-2161.
23. Ekonomou A, Johnson M, Perry RH, Perry EK, Kalaria RN, Minger SL, Ballard CG (2012): Increased neural progenitors in individuals with cerebral small vessel disease. Neuropathol Appl Neurobiol 38: 344-353.
24. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, et al. (2006): Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci U S A 103:13198-13202.
25. Macas J, Nern C, Plate KH, Momma S (2006): Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci 26:13114-13119.
26. Minger SL, Ekonomou A, Carta EM, Chinoy A, Perry RH, Ballard CG (2007): Endogenous neurogenesis in the human brain following cerebral infarction. Regen Med 2:69-74.
27. Johnson M, Ekonomou A, Hobbs C, Ballard CG, Perry RH, Perry EK (2011): Neurogenic marker abnormalities in the hippocampus in dementia with Lewy bodies. Hippocampus 21:1126-1136.
28. Demars M, Hu YS, Gadadhar A, Lazarov O (2010): Impaired neurogenesis is an early event in the etiology of familial Alzheimer's disease in transgenic mice. J Neurosci Res 88:2103-2117.
29. Hamilton LK, Aumont A, Julien C, Vadnais A, Calon F, Fernandes KJ (2010): Widespread deficits in adult neurogenesis precede plaque and tangle formation in the 3xTg mouse model of Alzheimer's disease. Eur J Neurosci 32:905-920.
30. Jin K, Galvan V, Xie L, Mao XO, Gorostiza OF, Bredesen DE, Greenberg DA (2004): Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice. Proc Natl Acad Sci U S A 101: 13363-13367.
31. Wen PH, Hof PR, Chen X, Gluck K, Austin G, Younkin SG, et al. (2004): The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp Neurol 188:224-237.
32. Ermini FV, Grathwohl S, Radde R, Yamaguchi M, Staufenbiel M, Palmer TD, Jucker M (2008): Neurogenesis and alterations of neural stem cells in mouse models of cerebral amyloidosis. Am J Pathol 172: 1520-1528.
33. Brayne C, McCracken C, Matthews FE (2006): Cohort profile: The Medical Research Council Cognitive Function and Ageing Study (CFAS). Int J Epidemiol 35:1140-1145.
34. Matthews FE, Brayne C, Lowe J, McKeith I, Wharton SB, Ince P (2009): Epidemiological pathology of dementia: Attributable-risks at death in the Medical Research Council Cognitive Function and Ageing Study. PLoS Med 6:e1000180.
35. Braak H, Braak E (1991): Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239-259.
36. Braak H, Alafuzoff I, Arzberger T, Kretzschmanr H, Del Tredici K (2006): Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunohistochemistry. Acta Neuropathol 112:389-404.
37. Savva GM, Wharton SB, Ince PG, Forster G, Matthews FE, Brayne C, Medical Research Council Cognitive Function and Ageing Study (2009): Age, neuropathology and dementia. N Engl J Med 360:2302-2309.
38. Benjamini Y, Hochberg Y (1995): Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289-300.
39. Verwer RW, Sluiter AA, Balesar RA, Baayen JC, Noske DP, Dirven CM, et al. (2007): Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin. Brain 130(Pt 12):3321-3335.
40. Ziabreva I, Ballard C, Johnson M, Larsen JP, McKeith I, Perry R, et al. (2007): Loss of Musashi1 in Lewy body dementia associated with cholinergic deficit. Neuropathol Appl Neurobiol 33:586-590.
41. Kremer T, Jagasia R, Herrmann A, Matile H, Borroni E, Francis F, et al. (2013): Analysis of adult neurogenesis: Evidence for a prominent "nonneurogenic" DCX-protein pool in rodent brain. PLoS One 8:e59269.
42. Martí-Mengual U, Varea E, Crespo C, Blasco-Ibáñez JM, Nacher J (2013): Cells expressing markers of immature neurons in the amygdala of adult humans. Eur J Neurosci 37:10-22.
43. Kempermann G, Gast D, Gage FH (2002): Neuroplasticity in old age: Sustained fivefold induction of hippocampal neurogenesis by longterm environmental enrichment. Ann Neurol 52:135-143.
44. van Praag H, Shubert T, Zhao C, Gage FH (2005): Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25: 8680-8685.
45. Leem YH, Lim HJ, Shim SB, Cho JY, Kim BS, Han PL (2009): Repression of tau hyperphosphorylation by chronic endurance exercise in aged transgenic mouse model of tauopathies. J Neurosci Res 87:2561-2570.
46. Marlatt MW, Lucassen PJ (2010): Neurogenesis and Alzheimer's disease: Biology and pathophysiology in mice and men. Curr Alzheimer Res 7:113-125.
47. Belarbi K, Burnouf S, Fernandez-Gomez FJ, Laurent C, Lestavel S, Figeac M, et al. (2011): Beneficial effects of exercise in a transgenic mouse model of Alzheimer's disease-like tau pathology. Neurobiol Dis 43:486-494.
48. García-Mesa Y, López-Ramos JC, Giménez-Llort L, Revilla S, Guerra R, Gruart A, et al. (2011): Physical exercise protects against Alzheimer's disease in 3xTg-AD mice. J Alzheimers Dis 24:421-454.
49. Marlatt MW, Potter MC, Lucassen PJ, van Praag H (2012): Running throughout middle-age improves memory function, hippocampal neurogenesis, and BDNF levels in female C57BL/6J mice. Dev Neurobiol 72:943-952.
50. Marlatt MW, Potter MC, Bayer TA, van Praag H, Lucassen PJ (2013): Prolonged running, not fluoxetine treatment, increases neurogenesis, but does not alter neuropathology, in the 3xTg mouse model of Alzheimer's disease. Curr Top Behav Neurosci 15:313-340.
51. Voss MW, Vivar C, Kramer AF, van Praag H (2013): Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn Sci 17:525-544.
52. Yang Y, Mufson EJ, Herrup K (2003): Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J Neurosci 23:2557-2563.
53. Hong XP, Peng CX, Wei W, Tian Q, Liu YH, Yao XQ, et al. (2010): Essential role of tau phosphorylation in adult hippocampal neurogenesis. Hippocampus 20:1339-1349.
54. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, et al. (2010): Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483-495.
55. Ekdahl CT (2012): Microglial activation - tuning and pruning adult neurogenesis. Front Pharmacol 3:411-419.
56. Verkhratsky A, Olabarria M, Noristani HN, Yeh CY, Rodriguez JJ (2012): Astrocytes in Alzheimer's disease. Neurotherapeutics 7: 399-412.
57. Nyffeler M, Yee BK, Feldon J, Knuesel I (2010): Abnormal differentiation of newborn granule cells in age-related working memory impairments. Neurobiol Aging 31:1956-1974.
58. Kim SE, Ko IG, Kim BK, Shin MS, Cho S, Kim CJ, et al. (2010): Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol 45:357-365.
59. Déry N, Pilgrim M, Gibala M, Gillen J, Wojtowicz JM, Macqueen G, Becker S (2013): Adult hippocampal neurogenesis reduces memory interference in humans: Opposing effects of aerobic exercise and depression. Front Neurosci 7:66.