Age-related loss of calcium buffering and selective neuronal vulnerability in Alzheimer's disease

Acta Neuropathologica

Volumn 122, Issue 5, 2011, Pages 565-576

  Riascos, David ^a   De Leon, Dianne ^a   Baker Nigh, Alaina ^a   Nicholas, Alexander ^b   Yukhananov, Rustam ^c   Bu, Jing ^b,e   Wu, Chuang Kuo ^d   Geula, Changiz ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c Precision Biosystems   (United States)

^d TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^e BERKSHIRE MEDICAL CENTER   (United States)

Author keywords

Aging; Alzheimer's disease; Calcium dysregulation; Cholinergic basal forebrain neurons; Selective neuronal vulnerability; Tangle pathology

Indexed keywords

CALBINDIN; MESSENGER RNA;

ADULT; AGED; AGING; ALZHEIMER DISEASE; ARTICLE; CELL LOSS; CELL PROTECTION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MALE; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NEUROPROTECTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS;

ADULT; AGED; AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; AUTOPSY; CALCIUM; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CHOLINERGIC NEURONS; FEMALE; HUMANS; MALE; MIDDLE AGED; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; PROSENCEPHALON;

EID: 82355169652     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0865-4     Document Type: Article

References (45)

1. T Arendt V Bigl A Arendt A Tennstdet 1983 Loss of neurons in the nucleus basalis of Meynert in Alzheimer's disease, paralysis agitans and Korsakoffs disease Acta Neuropathol 61 101 108 6637393 10.1007/BF00697388 1:STN:280:DyaL2c%2FkvVaksg%3D%3D (Pubitemid 13048358)
2. T Arikuni K Kubota 1984 Substantia innominata projection to caudate nucleus in macaque monkeys Brain Res 302 184 189 6203613 10.1016/0006-8993(84) 91299-X 1:STN:280:DyaL2c3jtlersg%3D%3D (Pubitemid 14095426)
3. DM Armstrong MD Ikonomovic R Sheffield RJ Wenthold 1994 AMPA-selective glutamate receptor subtype immunoreactivity in the entorhinal cortex of non-demented elderly and patients with Alzheimer's disease Brain Res 639 207 216 8205474 10.1016/0006-8993(94)91732-9 1:CAS:528:DyaK2cXitFCgu78%3D (Pubitemid 24078557)
4. J Baudier RD Cole 1987 Phosphorylation of tau proteins to a state like that in Alzheimer's brain is catalyzed by a calcium/calmodulin-dependent kinase and modulated by phospholipids J Biol Chem 262 17577 17583 3121601 1:CAS:528:DyaL1cXkt1Cn (Pubitemid 18032243)
5. J Biernat N Gustke G Drewes EM Mandelkow E Mandelkow 1993 Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding Neuron 11 153 163 8393323 10.1016/0896-6273(93)90279-Z 1:CAS:528:DyaK2cXhs1SlsL4%3D (Pubitemid 23222542)
6. H Braak E Braak 1991 Neuropathological staging of Alzheimer's disease Acta Neuropathol 82 239 259 1759558 10.1007/BF00308809 1:STN:280: DyaK387gtFOiug%3D%3D
7. J Bu V Sathyendra N Nagykery C Geula 2003 Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex Exp Neurol 182 220 231 12821392 10.1016/S0014-4886(03)00094-3 1:CAS:528:DC%2BD3sXkvVCnsrY%3D (Pubitemid 36776265)
8. R Bullock H Bergman J Touchon, et al. 2006 Effect of age on response to rivastigmine or donepezil in patients with Alzheimer's disease Curr Med Res Opin 22 483 494 16574032 10.1185/030079906X89685 1:CAS:528:DC%2BD28XjvV2ht7o%3D
9. E Buritica L Villamil F Guzman, et al. 2009 Changes in calcium-binding protein expression in human cortical contusion tissue J Neurotrauma 26 2145 2155 19645526 10.1089/neu.2009.0894
10. C D'Orlando B Fellay B Schwaller, et al. 2001 Calretinin and calbindin D-28k delay the onset of cell death after excitotoxic stimulation in transfected P19 cells Brain Res 909 145 158 11478931 10.1016/S0006-8993(01)02671-3 (Pubitemid 32710128)
11. N de Talamoni CA Smith RH Wasserman, et al. 1993 Immunocytochemical localization of the plasma membrane calcium pump, calbindin-D28k, and parvalbumin in Purkinje cells of avian and mammalian cerebellum Proc Natl Acad Sci USA 90 11949 11953 8265654 10.1073/pnas.90.24.11949 (Pubitemid 24008757)
12. A Demuro E Mina R Kayed, et al. 2005 Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers J Biol Chem 280 17294 17300 15722360 10.1074/jbc.M500997200 1:CAS:528: DC%2BD2MXjsFOguro%3D (Pubitemid 41389198)
13. A Fine C Hoyle CJ Maclean TL Levatte HF Baker RM Ridley 1997 Learning impairments following injection of a selective cholinergic immunotoxin, ME20.4 IgG-saporin, into the basal nucleus of Meynert in monkeys Neurosci 81 331 343 10.1016/S0306-4522(97)00208-X 1:CAS:528:DyaK2sXmtVKmsbg%3D (Pubitemid 27381991)
14. C Geula J Bu N Nagykery 2003 Loss of calbindin-D28k from aging human cholinergic basal forebrain: relation to neuronal loss J Comp Neurol 455 249 259 12454989 10.1002/cne.10475 1:CAS:528:DC%2BD38Xps1yrt70%3D (Pubitemid 35424261)
15. Geula C, Mesulam M-M (1999) Cholinergic systems in Alzheimer disease. In: Terry RD, Katzman R, Bick KL, Sisodia SS (eds) Alzheimer disease, 2nd edn. Lippincott Williams and Wilkins, Philadelphia, pp 269-292
16. C Geula N Nagykery A Nicholas CK Wu 2008 Cholinergic neuronal and axonal abnormalities are present early in aging and in Alzheimer disease J Neuropathol Exp Neurol 67 309 318 18379437 10.1097/NEN.0b013e31816a1df3 (Pubitemid 351507486)
17. C Geula CR Schatz MM Mesulam 1993 Differential localization of NADPH-diaphorase and calbindin-D28k within the cholinergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human Neuroscience 54 461 476 8336832 10.1016/0306-4522(93)90266-I 1:CAS:528:DyaK3sXks1yksbs%3D (Pubitemid 23153755)
18. T Gomez-Isla JL Price DWJ McKeel JC Morris JH Growdon BT Hyman 1996 Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease J Neurosci 16 4491 4500 8699259 1:CAS:528:DyaK28XktlamsLs%3D (Pubitemid 26243044)
19. JA Hartigan GV Johnson 1999 Transient increases in intracellular calcium result in prolonged site-selective increases in tau phosphorylation through a glycogen synthase kinase 3beta-dependent pathway J Biol Chem 274 21395 21401 10409701 10.1074/jbc.274.30.21395 1:CAS:528:DyaK1MXkvVKrtL8%3D (Pubitemid 29350614)
20. AM Iacopino EM Quintero EK Miller 1994 Calbindin-D28K: a potential neuroprotective protein Neurodegeneration 3 1 20
21. MD Ikonomovic R Nocera K Mizukami DM Armstrong 2000 Age-related loss of the AMPA receptor subunits GluR2/3 in the human nucleus basalis of Meynert Exp Neurol 166 363 375 11085901 10.1006/exnr.2000.7544 1:CAS:528: DC%2BD3cXotFCrsbY%3D
22. ZS Khachaturian 1994 Calcium hypothesis of Alzheimer's disease and brain aging Ann N Y Acad Sci 747 1 11 7847664 10.1111/j.1749-6632.1994.tb44398.x 1:CAS:528:DyaK2MXovVSjs7c%3D
23. +-loaded calbindin-D(28K) Nat Struct Mol Biol 13 641 647 16799559 10.1038/nsmb1112 1:CAS:528:DC%2BD28Xms1eltLo%3D (Pubitemid 44036475)
24. CA Lasagna-Reeves DL Castillo-Carranza MJ Guerrero-Muoz GR Jackson R Kayed 2010 Preparation and characterization of neurotoxic tau oligomers Biochemistry 49 10039 10041 21047142 10.1021/bi1016233 1:CAS:528: DC%2BC3cXhtlynsbnF
25. S Lehericy EC Hirsch P Cervera-Pierot, et al. 1993 Heterogeneity and selectivity of the degeneration of cholinergic neurons in the basal forebrain of patients with Alzheimer's disease J Comp Neurol 330 15 31 8468401 10.1002/cne.903300103 1:STN:280:DyaK3s3isVKiuw%3D%3D (Pubitemid 23095311)
26. AI Levey JP Bolam DB Rye 1986 A light and electron microscopic procedure for sequential double antigen localization using diaminobenzidine and benzidine dihydrochloride J Histochem Cytochem 34 1449 1457 2430010 10.1177/34.11.2430010 1:CAS:528:DyaL2sXmtlyjsg%3D%3D (Pubitemid 16005397)
27. DH Lowenstein RP Gwinn MS Seren RP Simon TK McIntosh 1994 Increased expression of mRNA encoding calbindin-D28K, the glucose-regulated proteins, or the 72 kDa heat-shock protein in three models of acute CNS injury Mol Brain Res 22 299 308 8015387 10.1016/0169-328X(94)90058-2 1:CAS:528:DyaK2cXivFGkur8%3D (Pubitemid 24063651)
28. MP Mattson RE Rydel I Lieberburg VL Smith-Swintosky 1993 Altered calcium signaling and neuronal injury: stroke and Alzheimer's disease as examples. Review Ann New York Acad Sci 679 1 21 10.1111/j.1749-6632.1993.tb18285.x 1:CAS:528:DyaK3sXkvFaqtr0%3D (Pubitemid 23202395)
29. M Mesulam P Shaw D Mash S Weintraub 2004 Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum Ann Neurol 55 815 828 15174015 10.1002/ana.20100 1:CAS:528:DC%2BD2cXlsVCkur8%3D (Pubitemid 38702576)
30. M-M Mesulam EJ Mufson AI Levey BH Wainer 1983 Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey J Comp Neurol 214 170 197 6841683 10.1002/cne.902140206 1:STN:280:DyaL3s7os12hsQ%3D%3D (Pubitemid 13162962)
31. M-M Mesulam EJ Mufson BH Wainer 1986 Three-dimensional representation and cortical projection topography of the nucleus basalis (Ch4) in the macaque: concurrent demonstration of choline acetyltransferase and retrograde transport with a stabilized tetramethylbenzidine method for horseradish peroxidase Brain Res 367 301 308 3516304 10.1016/0006-8993(86)91607-0 1:CAS:528: DyaL28XitVSrtrs%3D (Pubitemid 16011692)
32. RJ Miller 1991 The control of neuronal Ca2 + homeostasis Prog Neurobiol 37 255 285 1947178 10.1016/0301-0082(91)90028-Y 1:CAS:528:DyaK3MXmslKhur8%3D
33. SS Mirra A Heyman D McKeel, et al. 1991 The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease Neurology 41 479 486 2011243 1:STN:280:DyaK3M7oslajsQ%3D%3D
34. JC Morris A Heyman RC Mohs, et al. 1989 CERAD Investigators. The Consortium to establish a Registry for Alzheimer's Disease. Part I. Clinical and neuropsychological assessment of Alzheimer's disease Neurology 39 1159 1165 2771064 1:STN:280:DyaL1MzmsFGqsQ%3D%3D (Pubitemid 19239715)
35. EJ Mufson SY Ma EJ Cochran, et al. 2000 Loss of nucleus basalis neurons containing trkA immunoreactivity in individuals with mild cognitive impairment and early Alzheimer's disease J Comp Neurol 427 19 30 11042589 10.1002/1096-9861(20001106)427:1<19::AID-CNE2>3.0.CO;2-A 1:STN:280:DC%2BD3crgtVKmsw%3D%3D
36. EK Perry D Irving JM Kerwin, et al. 1993 Cholinergic transmitter and neurotrophic activities in Lewy body dementia: similarity to Parkinson's and distinction from Alzheimer disease Alzheimer Dis Assoc Disord 7 2 69 79 8347330 10.1097/00002093-199307020-00002 1:STN:280:DyaK3szkvFCqtg%3D%3D (Pubitemid 23222509)
37. GL Rintoul LA Raymond KG Baimbridge 2001 Calcium buffering and protection from excitotoxic cell death by exogenous calbindin-D28k in HEK 293 cells Cell Calcium 29 277 287 11243935 10.1054/ceca.2000.0190 1:CAS:528: DC%2BD3MXisFSktrw%3D (Pubitemid 32266394)
38. WA Samuel VW Henderson CA Miller 1991 Severity of dementia in Alzheimer disease and neurofibrillary tangles in multiple brain regions Alzhemier Dis Assoc Disor 5 1 11 10.1097/00002093-199100510-00001 1:STN:280: DyaK3M3it1GhtQ%3D%3D
39. HE Scharfman PA Schwartzkroin 1989 Protection of dentate hilar cells from prolonged stimulation by intracellular calcium chelation Science 246 249 262 10.1126/science.2508225
40. Schliebs R, Arendt T (2011) The cholinergic system in aging and neuronal degeneration. Behav Brain Res (in press)
41. JD Stoehr SL Mobley D Roice, et al. 1997 The effects of selective cholinergic basal forebrain lesions and aging upon expectancy in the rat Neurobiol Lear Mem 67 214 227 10.1006/nlme.1997.3768 1:CAS:528: DyaK2sXjs1ekt7c%3D (Pubitemid 27424458)
42. U Wagner M Utton JM Gallo CC Miller 1996 Cellular phosphorylation of tau by GSK-3 beta influences tau binding to microtubules and microtubule organisation J Cell Sci 109 1537 1543 8799840 1:CAS:528:DyaK28XktValsrk%3D (Pubitemid 26190502)
43. CK Wu N Nagykery LB Hersh LF Scinto C Geula 2003 Selective age-related loss of calbindin-D28k from basal forebrain cholinergic neurons in the common marmoset (Callithrix jacchus) Neuroscience 120 249 259 12849757 10.1016/S0306-4522(03)00248-3 1:CAS:528:DC%2BD3sXkvFylt7Y%3D (Pubitemid 36782647)
44. C-K Wu LB Hersh C Geula 2000 Cyto- and chemoarchitecture of basal forebrain cholinergic neurons in the common marmoset (Callithirx jacchus) Exp Neurol 165 306 326 10993691 10.1006/exnr.2000.7468 1:STN:280: DC%2BD3M%2FhtVOktQ%3D%3D
45. C-K Wu M-M Mesulam C Geula 1997 Age-related loss of calbindin from human basal forebrain cholinergic neurons Neuroreport 8 2209 2213 9243613 10.1097/00001756-199707070-00024 1:CAS:528:DyaK2sXlt1Wgsbw%3D (Pubitemid 27319674)