Loss of calbindin-D28K is associated with the full range of tangle pathology within basal forebrain cholinergic neurons in Alzheimer's disease

Neurobiology of Aging

Volumn 36, Issue 12, 2015, Pages 3163-3170

  Ahmadian, Saman S ^a   Rezvanian, Aras ^a   Peterson, Melanie ^a   Weintraub, Sandra ^a   Bigio, Eileen H ^a   Mesulam, Marek Marsel ^a   Geula, Changiz ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Basal forebrain cholinergic neurons; Calbindin D28k; Selective neuronal vulnerability; Tangles; Tau epitope

Indexed keywords

CALBINDIN 1; EPITOPE; CALBINDIN; TAU PROTEIN;

ADULT; AGE; AGED; ALZHEIMER DISEASE; ARTICLE; BASAL FOREBRAIN CHOLINERGIC NEURON; BINDING AFFINITY; CHOLINERGIC NERVE CELL; CLINICAL ARTICLE; DISEASE REGISTRY; FEMALE; FOREBRAIN; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MIDDLE AGED; NEUROFIBRILLARY TANGLE; NEUROMODULATION; NEUROPIL; PATHOGENESIS; PRIORITY JOURNAL; PROBABILITY; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RISK FACTOR; STEREOLOGY; VERY ELDERLY; AGING; BASAL FOREBRAIN; CYTOLOGY; DEFICIENCY; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; PATHOLOGY;

AGED; AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; BASAL FOREBRAIN; CALBINDINS; CHOLINERGIC NEURONS; EPITOPES; FEMALE; GENETIC ASSOCIATION STUDIES; HUMANS; MALE; MIDDLE AGED; NEUROFIBRILLARY TANGLES; TAU PROTEINS;

EID: 84947029569     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.09.001     Document Type: Article

References (76)

1. Arendt T., Bigl V., Tennstedt A., Arendt A. Neuronal loss in different parts of the nucleus basalis is related to neuritic plaque formation in cortical target areas in Alzheimer's disease. Neuroscience 1985, 14:1-14.
2. Arriagada P.V., Marzloff K., Hyman B.T. Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease. Neurology 1992, 42:1681-1688.
3. Augustinack J.C., Schneider A., Mandelkow E.M., Hyman B.T. Specific Tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. 2002, 103:26-35.
4. Ballatore C., Lee V.M., Trojanowski J.Q. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat. Rev. Neurosci. 2007, 8:663-672.
5. Baumann K., Mandelkow E.M., Biernat J., Piwnica-Worms H., Mandelkow E. Abnormal Alzheimer-like phosphorylation of Tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett. 1993, 336:417-424.
6. Bellido T., Huening M., Raval-Pandya M., Manolagas S.C., Christakos S. Calbindin-D28k is expressed in osteoblastic cells and suppresses their apoptosis by inhibiting caspase-3 activity. J. Biol. Chem. 2000, 275:26328-26332.
7. Berger-Sweeney J., Heckers S., Mesulam M.M., Wiley R.G., Lappi D.A., Sharma M. Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. J. Neurosci. 1994, 14:4507-4519.
8. Braak E., Braak H., Mandelkow E.M. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol. 1994, 87:554-567.
9. Bu J., Sathyendra V., Nagykery N., Geula C. Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp. Neurol. 2003, 182:220-231.
10. 28K and parvalbumin in the rat nervous system. Neuroscience 1990, 35:375-475.
11. Chalfie M., Wolinsky E. The identification and suppression of inherited neurodegeneration in Caenorhabditis elegans. Nature 1990, 345:410-416.
12. Choi D.W. Cerebral hypoxia: some new approaches and unanswered questions. J. Neurosci. 1990, 10:2493-2501.
13. Choi W.S., Lee E., Lim J., Oh Y.J. Calbindin-D28K prevents drug-induced dopaminergic neuronal death by inhibiting caspase and calpain activity. Biochem. Biophys. Res. Commun. 2008, 371:127-131.
14. Chun W., Johnson G.V. The role of Tau phosphorylation and cleavage in neuronal cell death. Front. Biosci. 2007, 12:733-756.
15. Drewes G., Lichtenberg-Kraag B., Doring F., Mandelkow E.M., Biernat J., Goris J., Doree M., Mandelkow E. Mitogen activated protein (MAP) kinase transforms Tau protein into an Alzheimer-like state. EMBO J. 1992, 11:2131-2138.
16. Ekinci F.J., Shea T.B. Hyperactivation of mitogen-activated protein kinase increases phospho-Tau immunoreactivity within human neuroblastoma: additive and synergistic influence of alteration of additional kinase activities. Cell Mol. Neurobiol. 1999, 19:249-260.
17. Fine A., Hoyle C., Maclean C.J., Levatte T.L., Baker H.F., Ridley R.M. Learning impairments following injection of a selective cholinergic immunotoxin, ME20.4 IgG-saporin, into the basal nucleus of Meynert in monkeys. Neuroscience 1997, 81:331-343.
18. Geula C., Bu J., Nagykery N., Scinto L.F., Chan J., Joseph J., Parker R., Wu C.K. Loss of calbindin-D28k from aging human cholinergic basal forebrain: relation to neuronal loss. J. Comp. Neurol. 2003, 455:249-259.
19. Geula C., Mesulam M.M. Cortical cholinergic fibers in aging and Alzheimer's disease: a morphometric study. Neuroscience 1989, 33:469-481.
20. Geula C., Mesulam M.M. Cholinergic systems in Alzheimer disease. Alzheimer Disease 1999, 269-292. Lippincott Williams & Wilkins, Philadelphia. second ed. R.D. Terry, R. Katzman, K.L. Bick, S.S. Sisodia (Eds.).
21. Geula C., Nagykery N., Nicholas A., Wu C.K. Cholinergic neuronal and axonal abnormalities are present early in aging and in Alzheimer disease. J. Neuropathol. Exp. Neurol. 2008, 67:309-318.
22. Geula C., Schatz C.R., Mesulam M.M. 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 1993, 54:461-476.
23. Guillozet-Bongaarts A.L., Garcia-Sierra F., Reynolds M.R., Horowitz P.M., Fu Y., Wang T., Cahill M.E., Bigio E.H., Berry R.W., Binder L.I. Tau truncation during neurofibrillary tangle evolution in Alzheimer's disease. Neurobiol. Aging 2005, 26:1015-1022.
24. Hashiguchi M., Saito T., Hisanaga S., Hashiguchi T. Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser202/Thr205 of human Tau. J. Biol. Chem. 2002, 277:44525-44530.
25. Hisanaga S., Ishiguro K., Uchida T., Okumura E., Okano T., Kishimoto T. Tau protein kinase II has a similar characteristic to cdc2 kinase for phosphorylating neurofilament proteins. J. Biol. Chem. 1993, 268:15056-15060.
26. Hof P.R., Morrison J.H. Neocortical neuronal subpopulations labeled by a monoclonal antibody to calbindin exhibit differential vulnerability in Alzheimer's disease. Exp. Neurol. 1991, 111:293-301.
27. Hosoi T., Uchiyama M., Okumura E., Saito T., Ishiguro K., Uchida T., Okuyama A., Kishimoto T., Hisanaga S. Evidence for cdk5 as a major activity phosphorylating Tau protein in porcine brain extract. J. Biochem. 1995, 117:741-749.
28. Hung K.S., Hwang S.L., Liang C.L., Chen Y.J., Lee T.H., Liu J.K., Howng S.L., Wang C.H. Calpain inhibitor inhibits p35-p25-Cdk5 activation, decreases Tau hyperphosphorylation, and improves neurological function after spinal cord hemisection in rats. J. Neuropathol. Exp. Neurol. 2005, 64:15-26.
29. Hyman B.T., Phelps C.H., Beach T.G., Bigio E.H., Cairns N.J., Carrillo M.C., Dickson D.W., Duyckaerts C., Frosch M.P., Masliah E., Mirra S.S., Nelson P.T., Schneider J.A., Thal D.R., Thies B., Trojanowski J.Q., Vinters H.V., Montine T.J. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease. Alzheimers Dement. 2012, 8:1-13.
30. Ikonomovic M.D., Mizukami K., Davies P., Hamilton R., Sheffield R., Armstrong D.M. The loss of GluR2(3) immunoreactivity precedes neurofibrillary tangle formation in the entorhinal cortex and hippocampus of Alzheimer brains. J. Neuropathol. Exp. Neurol. 1997, 56:1018-1027.
31. Ikonomovic M.D., Nocera R., Mizukami K., Armstrong D.M. Age-related loss of the AMPA receptor subunits GluR2/3 in the human nucleus basalis of Meynert. Exp. Neurol. 2000, 166:363-375.
32. Kang H.J., Yoon W.J., Moon G.J., Kim D.Y., Sohn S., Kwon H.J., Gwag B.J. Caspase-3-mediated cleavage of PHF-1 Tau during apoptosis irrespective of excitotoxicity and oxidative stress: an implication to Alzheimer's disease. Neurobiol. Dis. 2005, 18:450-458.
33. Katz B. Neural transmitter release: from quantal secretion to exocytosis and beyond. The Fenn Lecture. J. Neurocytol. 1996, 25:677-686.
34. Kobayashi S., Ishiguro K., Omori A., Takamatsu M., Arioka M., Imahori K., Uchida T. A cdc2-related kinase PSSALRE/cdk5 is homologous with the 30 kDa subunit of Tau protein kinase II, a proline-directed protein kinase associated with microtubule. FEBS Lett. 1993, 335:171-175.
35. Kojetin D.J., Venters R.A., Kordys D.R., Thompson R.J., Kumar R., Cavanagh J. Structure, binding interface and hydrophobic transitions of Ca2+-loaded calbindin-D(28K). Nat. Struct. Mol. Biol. 2006, 13:641-647.
36. Lauckner J., Frey P., Geula C. Comparative distribution of Tau phosphorylated at Ser262 in pre-tangles and tangles. Neurobiol. Aging 2003, 24:767-776.
37. Lee M.S., Kwon Y.T., Li M., Peng J., Friedlander R.M., Tsai L.H. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 2000, 405:360-364.
38. Levey A.I., Bolam J.P., Rye D.B., Hallanger A.E., Demuth R.M., Mesulam M.M., Wainer B.H. A light and electron microscopic procedure for sequential double antigen localization using diaminobenzidine and benzidine dihydrochloride. J. Histochem. Cytochem. 1986, 34:1449-1457.
39. Liu J., Liu M.C., Wang K.K. Calpain in the CNS: from synaptic function to neurotoxicity. Sci. Signal 2008, 1:re1.
40. Luna-Munoz J., Garcia-Sierra F., Falcon V., Menendez I., Chavez-Macias L., Mena R. Regional conformational change involving phosphorylation of Tau protein at the Thr231, precedes the structural change detected by Alz-50 antibody in Alzheimer's disease. J. Alzheimers Dis. 2005, 8:29-41.
41. Lutz W., Frank E.M., Craig T.A., Thompson R., Venters R.A., Kojetin D., Cavanagh J., Kumar R. Calbindin D28K interacts with Ran-binding protein M: identification of interacting domains by NMR spectroscopy. Biochem. Biophys. Res. Commun. 2003, 303:1186-1192.
42. Malenka R.C., Kauer J.A., Perkel D.J., Nicoll R.A. The impact of postsynaptic calcium on synaptic transmission-its role in long-term potentiation. Trends Neurosci. 1989, 12:444-450.
43. Markesbery W.R., Wang H.Z., Kowall N.W., Kosik K.S., McKee A.C. Morphometric image analysis of neuropil threads in Alzheimer's disease. Neurobiol. Aging 1993, 14:303-307.
44. Marty A. The physiological role of calcium-dependent channels. Trends Neurosci. 1989, 12:420-424.
45. Mattson M.P., Rychlik B., Chu C., Christakos S. Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron 1991, 6:41-51.
46. McKhann G.M., Knopman D.S., Chertkow H., Hyman B.T., Jack C.R., Kawas C.H., Klunk W.E., Koroshetz W.J., Manly J.J., Mayeux R., Mohs R.C., Morris J.C., Rossor M.N., Scheltens P., Carrillo M.C., Thies B., Weintraub S., Phelps C.H. The diagnosis of dementia due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 2011, 7:263-269.
47. Meldrum B., Garthwaite J. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol. Sci. 1990, 11:379-387.
48. Mesulam M.M., Geula C. Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J. Comp. Neurol. 1988, 275:216-240.
49. Mesulam M.M., Mufson E.J., Levey A.I., Wainer B.H. 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. 1983, 214:170-197.
50. Mesulam M.M., Mufson E.J., Wainer B.H., Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 1983, 10:1185-1201.
51. Mesulam M.M., Shaw P., Mash D., Weintraub S. Cholinergic nucleus basalis Tauopathy emerges early in the aging-MCI-AD continuum. Ann. Neurol. 2004, 55:815-828.
52. Miller R.J. The control of neuronal Ca2+ homeostasis. Prog. Neurobiol. 1991, 37:255-285.
53. Montine T.J., Phelps C.H., Beach T.G., Bigio E.H., Cairns N.J., Dickson D.W., Duyckaerts C., Frosch M.P., Masliah E., Mirra S.S., Nelson P.T., Schneider J.A., Thal D.R., Trojanowski J.Q., Vinters H.V., Hyman B.T. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: a practical approach. Acta Neuropathol. 2012, 123:1-11. National Institute on Aging, Alzheimer's Association.
54. Morris J.C., Heyman A., Mohs R.C., Hughes J.P., van Belle G., Fillenbaum G., Mellits E.D., Clark C. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology 1989, 39:1159-1165.
55. Nairn A.C., Hemmings H.C., Greengard P. Protein kinases in the brain. Ann. Rev. Biochem. 1985, 54:931-976.
56. Newell K.L., Hyman B.T., Growdon J.H., Hedley-Whyte E.T. Application of the National Institute on Aging (NIA)-Reagan Institute criteria for the neuropathological diagnosis of Alzheimer disease. J. Neuropathol. Exp. Neurol. 1999, 58:1147-1155.
57. Patterson K.R., Remmers C., Fu Y., Brooker S., Kanaan N.M., Vana L., Ward S., Reyes J.F., Philibert K., Glucksman M.J., Binder L.I. Characterization of prefibrillar Tau oligomers in vitro and in Alzheimer disease. J. Biol. Chem. 2011, 286:23063-23076.
58. Perry E.K., Irving D., Kerwin J.M., McKeith I.G., Thompson P., Collerton D., Fairbairn A.F., Ince P.G., Morris C.M., Cheng A.V. Cholinergic transmitter and neurotrophic activities in Lewy body dementia: similarity to Parkinson's and distinction from Alzheimer disease. Alzheimer Dis. Assoc. Disord. 1993, 7:69-79.
59. Price J.L., Morris J.C. Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann. Neurol. 1999, 45:358-368.
60. Riascos D., de Leon D., Baker-Nigh A., Nicholas A., Yukhananov R., Bu J., Wu C.K., Geula C. Age-related loss of calcium buffering and selective neuronal vulnerability in Alzheimer's disease. Acta Neuropathol. 2011, 122:565-576.
61. 2+-responsive proteins within cholinergic neurons in aging and Alzheimer's disease. Neurobiol. Aging 2014, 35:1325-1333.
62. Rintoul G.L., Raymond L.A., Baimbridge K.G. Calcium buffering and protection from excitotoxic cell death by exogenous calbindin-D28k in HEK 293 cells. Cell Calcium 2001, 29:277-287.
63. Rissman R.A., Poon W.W., Blurton-Jones M., Oddo S., Torp R., Vitek M.P., LaFerla F.M., Rohn T.T., Cotman C.W. Caspase-cleavage of Tau is an early event in Alzheimer disease tangle pathology. J. Clin. Invest. 2004, 114:121-130.
64. Roberts W.M. Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J. Neurosci. 1994, 14:3246-3262.
65. Saito K., Elce J.S., Hamos J.E., Nixon R.A. Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:2628-2632.
66. Sarter M., Parikh V. Choline transporters, cholinergic transmission and cognition. Nat. Rev. Neurosci. 2005, 6:48-56.
67. Schliebs R., Arendt T. The cholinergic system in aging and neuronal degeneration. Behav. Brain Res. 2011, 221:555-563.
68. Stoehr J.D., Mobley S.L., Roice D., Brooks R., Baker L.M., Wiley R.G., Wenk G.L. The effects of selective cholinergic basal forebrain lesions and aging upon expectancy in the rat. Neurobiol. Learn Mem. 1997, 67:214-227.
69. Szekely A.M., Costa E., Grayson D.R. Transcriptional program coordination by N-methyl-D-aspartate-sensitive glutamate receptor stimulation in primary cultures of cerebellar neurons. Mol. Pharmacol. 1990, 38:624-633.
70. Tsuji T., Shimohama S., Kimura J., Shimizu K. m-Calpain (calcium-activated neutral proteinase) in Alzheimer's disease brains. Neurosci. Lett. 1998, 248:109-112.
71. Vana L., Kanaan N.M., Ugwu I.C., Wuu J., Mufson E.J., Binder L.I. Progression of Tau pathology in cholinergic basal forebrain neurons in mild cognitive impairment and Alzheimer's disease. Am. J. Pathol. 2011, 179:2533-2550.
72. Wang J.Z., Wu Q., Smith A., Grundke-Iqbal I., Iqbal K. Tau is phosphorylated by GSK-3 at several sites found in Alzheimer disease and its biological activity markedly inhibited only after it is prephosphorylated by A-kinase. FEBS Lett. 1998, 436:28-34.
73. Whitehouse P.J., Struble R.G., Hedreen J.C., Clark A.W., Price D.L. Alzheimer's disease and related dementias: selective involvement of specific neuronal systems. CRC Crit. Rev. Clin. Neurobiol. 1985, 1:319-339.
74. Wu C.K., Mesulam M.M., Geula C. Age-related loss of calbindin from human basal forebrain cholinergic neurons. Neuroreport 1997, 8:2209-2213.
75. Wu C.K., Nagykery N., Hersh L.B., Scinto L.F., Geula C. Selective age-related loss of calbindin-D28k from basal forebrain cholinergic neurons in the common marmoset (Callithrix jacchus). Neuroscience 2003, 120:249-259.
76. Zakharov V.V., Mosevitsky M.I. M-calpain-mediated cleavage of GAP-43 near Ser41 is negatively regulated by protein kinase C, calmodulin and calpain-inhibiting fragment GAP-43-3. J. Neurochem. 2007, 101:1539-1551.