FK506-binding protein 1b/12.6: A key to aging-related hippocampal Ca2+ dysregulation?

European Journal of Pharmacology

Volumn 739, Issue C, 2014, Pages 74-82

  Gant, J C ^a   Blalock, E M ^a   Chen, K C ^a   Kadish, I ^a   Porter, N M ^a   Norris, C M ^a   Thibault, O ^a   Landfield, P W ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Aging; Calcium; FKBP1b; Ryanodine receptor

Indexed keywords

ADENOVIRUS VECTOR; CALCIUM CHANNEL L TYPE; CALCIUM ION; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 1B 12.6; MAMMALIAN TARGET OF RAPAMYCIN; RYANODINE RECEPTOR; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CALCIUM; TACROLIMUS BINDING PROTEIN 1B;

AFTERHYPERPOLARIZATION; AGING; ALZHEIMER DISEASE; BRAIN SLICE; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME INHIBITION; FKBP1B GENE; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; HIPPOCAMPUS; MENTAL DETERIORATION; MICROARRAY ANALYSIS; MOLECULAR MODEL; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SLOW AFTERHYPERPOLARIZATION; ANIMAL; CYTOLOGY; DEFICIENCY; GENETICS; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY;

AGING; ANIMALS; CALCIUM; HIPPOCAMPUS; HUMANS; NEURONS; TACROLIMUS BINDING PROTEINS;

EID: 84907696755     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.10.070     Document Type: Review

References (115)

1. D.H. Aitken, and M.J. Meaney Temporally graded, age-related impairments in spatial memory in the rat Neurobiol. Aging 10 1989 273 276
2. M.E. Bach, M. Barad, H. Son, M. Zhuo, Y.F. Lu, R. Shih, I. Mansuy, R.D. Hawkins, and E.R. Kandel Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway Proc. Natl. Acad. Sci. U.S.A. 96 1999 5280 5285
3. M.J. Berridge Elementary and global aspects of calcium signalling J. Physiol. 499 Pt 2 1997 291 306
4. J. Berrout, and M. Isokawa Homeostatic and stimulus-induced coupling of the L-type Ca2+ channel to the ryanodine receptor in the hippocampal neuron in slices Cell Calcium 46 2009 30 38
5. E.M. Blalock, K.C. Chen, K. Sharrow, J.P. Herman, N.M. Porter, T.C. Foster, and P.W. Landfield Gene microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment J. Neurosci. 23 2003 3807 3819
6. E.M. Blalock, K.C. Chen, A.J. Stromberg, C.M. Norris, I. Kadish, S.D. Kraner, N.M. Porter, and P.W. Landfield Harnessing the power of gene microarrays for the study of brain aging and Alzheimer's disease: statistical reliability and functional correlation Ageing Res. Rev. 4 2005 481 512
7. E.M. Blalock, R. Grondin, K.C. Chen, O. Thibault, V. Thibault, J.D. Pandya, A. Dowling, Z. Zhang, P. Sullivan, N.M. Porter, and P.W. Landfield Aging-related gene expression in hippocampus proper compared with dentate gyrus is selectively associated with metabolic syndrome variables in rhesus monkeys J. Neurosci. 30 2010 6058 6071
8. L.D. Brewer, A.L. Dowling, M.A. Curran-Rauhut, P.W. Landfield, N.M. Porter, and E.M. Blalock Estradiol reverses a calcium-related biomarker of brain aging in female rats J. Neurosci. 29 2009 6058 6067
9. A.B. Brillantes, K. Ondrias, A. Scott, E. Kobrinsky, E. Ondriasova, M.C. Moschella, T. Jayaraman, M. Landers, B.E. Ehrlich, and A.R. Marks Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein Cell 77 1994 513 523
10. R.D. Brinton Estrogen regulation of glucose metabolism and mitochondrial function: therapeutic implications for prevention of Alzheimer's disease Adv. Drug Deliv. Rev. 60 2008 1504 1511
11. M.R. Brown, J.W. Geddes, and P.G. Sullivan Brain region-specific, age-related, alterations in mitochondrial responses to elevated calcium J. Bioenergy Biomembr. 36 2004 401 406
12. A.M. Bruno, J.Y. Huang, D.A. Bennett, R.A. Marr, M.L. Hastings, and G.E. Stutzmann Altered ryanodine receptor expression in mild cognitive impairment and Alzheimer's disease Neurobiol. Aging 33 2012 (1001 e1001-1006)
13. A. Caccamo, S. Majumder, A. Richardson, R. Strong, and S. Oddo Molecular interplay between mTOR, A{beta} and tau: effects on cognitive impairments J. Biol. Chem. 285 2010 13107 13120
14. S. Chakroborty, I. Goussakov, M.B. Miller, and G.E. Stutzmann Deviant ryanodine receptor-mediated calcium release resets synaptic homeostasis in presymptomatic 3xTg-AD mice J. Neurosci. 29 2009 9458 9470
15. P. Chavis, L. Fagni, J.B. Lansman, and J. Bockaert Functional coupling between ryanodine receptors and L-type calcium channels in neurons Nature 382 1996 719 722
16. Chen, K.C.; Blalock, E.M.; Curran-Rauhut, M.A.; Kadish, I.; Blalock, S.J.; Brewer, L.; Porter, N.M.; Landfield, P.W.; 2013. Glucocorticoid-dependent hippocampal transcriptome in male rats: pathway-specific alterations with aging. Endocrinology.
17. K.C. Chen, E.M. Blalock, O. Thibault, P. Kaminker, and P.W. Landfield Expression of alpha 1D subunit mRNA is correlated with L-type Ca2+ channel activity in single neurons of hippocampal «zipper» slices Proc. Natl. Acad. Sci. U.S.A. 97 2000 4357 4362
18. G.V. Clodfelter, N.M. Porter, P.W. Landfield, and O. Thibault Sustained Ca2+-induced Ca2+-release underlies the post-glutamate lethal Ca2+ plateau in older cultured hippocampal neurons Eur. J. Pharmacol. 447 2002 189 200
19. C. Corona, A. Pensalfini, V. Frazzini, and S.L. Sensi New therapeutic targets in Alzheimer's disease: brain deregulation of calcium and zinc Cell Death Dis. 2 2011 e176
20. R.A. Deyo, K.T. Straube, and J.F. Disterhoft Nimodipine facilitates associative learning in aging rabbits Science 243 1989 809 811
21. J.F. Disterhoft, and M.M. Oh Alterations in intrinsic neuronal excitability during normal aging Aging Cell 6 2007 327 336
22. J.F. Disterhoft, L.T. Thompson, J.R. Moyer Jr.; and D.J. Mogul Calcium-dependent afterhyperpolarization and learning in young and aging hippocampus Life Sci. 59 1996 413 420
23. M. Eitoku, L. Sato, T. Senda, and M. Horikoshi Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly Cell Mol. Life Sci. 65 2008 414 444
24. L. Fedrizzi, and E. Carafoli Ca2+ dysfunction in neurodegenerative disorders: Alzheimer's disease Biofactors 37 2011 189 196
25. W. Fischer, K.S. Chen, F.H. Gage, and A. Bjorklund Progressive decline in spatial learning and integrity of forebrain cholinergic neurons in rats during aging Neurobiol. Aging 13 1992 9 23
26. F. Forette, M.L. Seux, J.A. Staessen, L. Thijs, M.R. Babarskiene, S. Babeanu, A. Bossini, R. Fagard, B. Gil-Extremera, T. Laks, Z. Kobalava, C. Sarti, J. Tuomilehto, H. Vanhanen, J. Webster, Y. Yodfat, and W.H. Birkenhager The prevention of dementia with antihypertensive treatment: new evidence from the Systolic Hypertension in Europe (Syst-Eur) study Arch. Intern. Med. 162 2002 2046 2052
27. T.C. Foster Role of estrogen receptor alpha and beta expression and signaling on cognitive function during aging Hippocampus 22 2012 656 669
28. T.C. Foster, and C.M. Norris Age-associated changes in Ca(2+)-dependent processes: relation to hippocampal synaptic plasticity Hippocampus 7 1997 602 612
29. K.M. Frick, M.G. Baxter, A.L. Markowska, D.S. Olton, and D.L. Price Age-related spatial reference and working memory deficits assessed in the water maze Neurobiol. Aging 16 1995 149 160
30. A.E. Gamelli, B.C. McKinney, J.A. White, and G.G. Murphy Deletion of the L-type calcium channel Ca(V) 1.3 but not Ca(V) 1.2 results in a diminished sAHP in mouse CA1 pyramidal neurons Hippocampus 21 2011 133 141
31. J.C. Gant, K.C. Chen, C.M. Norris, I. Kadish, O. Thibault, E.M. Blalock, N.M. Porter, and P.W. Landfield Disrupting function of FK506-binding protein 1b/12.6 induces the Ca(2)+-dysregulation aging phenotype in hippocampal neurons J. Neurosci. 31 2011 1693 1703
32. J.C. Gant, M.M. Sama, P.W. Landfield, and O. Thibault Early and simultaneous emergence of multiple hippocampal biomarkers of aging is mediated by Ca2+-induced Ca2+ release J. Neurosci. 26 2006 3482 3490
33. G.E. Gibson, and C. Peterson Calcium and the aging nervous system Neurobiol. Aging 8 1987 329 343
34. A.M. Gomez, A. Rueda, Y. Sainte-Marie, L. Pereira, S. Zissimopoulos, X. Zhu, R. Schaub, E. Perrier, R. Perrier, C. Latouche, S. Richard, M.C. Picot, F. Jaisser, F.A. Lai, H.H. Valdivia, and J.P. Benitah Mineralocorticoid modulation of cardiac ryanodine receptor activity is associated with downregulation of FK506-binding proteins Circulation 119 2009 2179 2187
35. W.V. Goodison, V. Frisardi, and P.G. Kehoe Calcium channel blockers and Alzheimer's disease: potential relevance in treatment strategies of metabolic syndrome J. Alzheimer's Dis. 30 Suppl 2 2012 S269 282
36. I. Goussakov, M.B. Miller, and G.E. Stutzmann NMDA-mediated Ca(2+) influx drives aberrant ryanodine receptor activation in dendrites of young Alzheimer's disease mice J. Neurosci. 30 2010 12128 12137
37. D.E. Harrison, R. Strong, Z.D. Sharp, J.F. Nelson, C.M. Astle, K. Flurkey, N.L. Nadon, J.E. Wilkinson, K. Frenkel, C.S. Carter, M. Pahor, M.A. Javors, E. Fernandez, and R.A. Miller Rapamycin fed late in life extends lifespan in genetically heterogeneous mice Nature 460 2009 392 395
38. J.P. Herman, K.C. Chen, R. Booze, and P.W. Landfield Up-regulation of alpha1D Ca2+ channel subunit mRNA expression in the hippocampus of aged F344 rats Neurobiol. Aging 19 1998 581 587
39. C.A. Hoeffer, W. Tang, H. Wong, A. Santillan, R.J. Patterson, L.A. Martinez, M.V. Tejada-Simon, R. Paylor, S.L. Hamilton, and E. Klann Removal of FKBP12 enhances mTOR-Raptor interactions, LTP, memory, and perseverative/repetitive behavior Neuron 60 2008 832 845
40. M.C. Holmes, and J.R. Seckl The role of 11beta-hydroxysteroid dehydrogenases in the brain Mol. Cell Endocrinol. 248 2006 9 14
41. E. Jacinto, and M.N. Hall Tor signalling in bugs, brain and brawn Nat. Rev. Mol. Cell Biol. 4 2003 117 126
42. R.P. Jakob, G. Zoldak, T. Aumuller, and F.X. Schmid Chaperone domains convert prolyl isomerases into generic catalysts of protein folding Proc. Natl. Acad. Sci. U.S.A. 106 2009 20282 20287
43. T. Jayaraman, A.M. Brillantes, A.P. Timerman, S. Fleischer, H. Erdjument-Bromage, P. Tempst, and A.R. Marks FK506 binding protein associated with the calcium release channel (ryanodine receptor) J. Biol. Chem. 267 1992 9474 9477
44. M. Joels, and E.R. de Kloet Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus Science (New York, N.Y 245 1989 1502 1505
45. T. Kadar, I. Arbel, M. Silbermann, and A. Levy Morphological hippocampal changes during normal aging and their relation to cognitive deterioration J. Neural Transm. Suppl. 44 1994 133 143
46. I. Kadish, O. Thibault, E.M. Blalock, K.C. Chen, J.C. Gant, N.M. Porter, and P.W. Landfield Hippocampal and cognitive aging across the lifespan: a bioenergetic shift precedes and increased cholesterol trafficking parallels memory impairment J. Neurosci. 29 2009 1805 1816
47. C.B. Kang, Y. Hong, S. Dhe-Paganon, and H.S. Yoon FKBP family proteins: immunophilins with versatile biological functions Neurosignals 16 2008 318 325
48. D.S. Kerr, L.W. Campbell, S.Y. Hao, and P.W. Landfield Corticosteroid modulation of hippocampal potentials: increased effect with aging Science (New York, N.Y 245 1989 1505 1509
49. A.S. Khachaturian, P.P. Zandi, C.G. Lyketsos, K.M. Hayden, I. Skoog, M.C. Norton, J.T. Tschanz, L.S. Mayer, K.A. Welsh-Bohmer, and J.C. Breitner Antihypertensive medication use and incident Alzheimer disease: the Cache County Study Arch. Neurol. 63 2006 686 692
50. Z.S. Khachaturian Towards theories of brain aging D.S. Kay, G.W. Burrows, Handbook of Studies on Psychiatry and Old Age 1984 Elsevier Amsterdam 7 30
51. S. Kim, H.M. Yun, J.H. Baik, K.C. Chung, S.Y. Nah, and H. Rhim Functional interaction of neuronal Cav1.3 L-type calcium channel with ryanodine receptor type 2 in the rat hippocampus J. Biol. Chem. 282 2007 32877 32889
52. S. Kirischuk, N. Voitenko, P. Kostyuk, and A. Verkhratsky Age-associated changes of cytoplasmic calcium homeostasis in cerebellar granule neurons in situ: investigation on thin cerebellar slices Exp. Gerontol. 31 1996 475 487
53. M.G. Knuttinen, A.E. Gamelli, C. Weiss, J.M. Power, and J.F. Disterhoft Age-related effects on eyeblink conditioning in the F344 × BN F1 hybrid rat Neurobiol. Aging 22 2001 1 8
54. A. Kumar, and T.C. Foster Enhanced long-term potentiation during aging is masked by processes involving intracellular calcium stores J. Neurophysiol. 91 2004 2437 2444
55. A. Kumar, and T.C. Foster Intracellular calcium stores contribute to increased susceptibility to LTD induction during aging Brain Res. 1031 2005 125 128
56. P.W. Landfield 'Increased calcium-current' hypothesis of brain aging Neurobiol. Aging 8 1987 346 347
57. P.W. Landfield, E.M. Blalock, K.C. Chen, and N.M. Porter A new glucocorticoid hypothesis of brain aging: implications for Alzheimer's disease Curr. Alzheimer Res. 4 2007 205 212
58. P.W. Landfield, and T.A. Pitler Prolonged Ca2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats Science (New York, N.Y 226 1984 1089 1092
59. S.E. Lehnart, F. Huang, S.O. Marx, and A.R. Marks Immunophilins and coupled gating of ryanodine receptors Curr. Top. Med. Chem. 3 2003 1383 1391
60. M.A. Leissring, Y. Akbari, C.M. Fanger, M.D. Cahalan, M.P. Mattson, and F.M. LaFerla Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice J. Cell Biol. 149 2000 793 798
61. C. Long, L.G. Cook, G.Y. Wu, and B.M. Mitchell Removal of FKBP12/12.6 from endothelial ryanodine receptors leads to an intracellular calcium leak and endothelial dysfunction Arterioscler. Thromb. Vasc. Biol. 27 2007 1580 1586
62. C.B. Lu, J.B. Hamilton, A.D. Powell, E.C. Toescu, and M. Vreugdenhil Effect of ageing on CA3 interneuron sAHP and gamma oscillations is activity-dependent Neurobiol. Aging 32 2011 956 965
63. W. Lutz, W. Sanderson, and S. Scherbov The coming acceleration of global population ageing Nature 451 2008 716 719
64. G. Lynch, C.S. Rex, L.Y. Chen, and C.M. Gall The substrates of memory: defects, treatments, and enhancement Eur. J. Pharmacol. 585 2008 2 13
65. A.L. Markowska Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle J. Neurosci. 19 1999 8122 8133
66. A.R. Marks Intracellular calcium-release channels: regulators of cell life and death Am. J. Physiol. 272 1997 H597 605
67. M.P. Mattson, Q. Guo, K. Furukawa, and W.A. Pedersen Presenilins, the endoplasmic reticulum, and neuronal apoptosis in Alzheimer's disease J. Neurochem. 70 1998 1 14
68. G. Meissner Regulation of mammalian ryanodine receptors Front. Biosci. 7 2002 d2072 2080
69. M.L. Michaelis, K. Johe, and T.E. Kitos Age-dependent alterations in synaptic membrane systems for Ca2+ regulation Mech. Ageing Dev. 25 1984 215 225
70. S. Moriguchi, M. Nishi, S. Komazaki, H. Sakagami, T. Miyazaki, H. Masumiya, S.Y. Saito, M. Watanabe, H. Kondo, H. Yawo, K. Fukunaga, and H. Takeshima Functional uncoupling between Ca2+ release and afterhyperpolarization in mutant hippocampal neurons lacking junctophilins Proc. Natl. Acad. Sci. U.S.A. 103 2006 10811 10816
71. J.H. Morrison, and P.R. Hof Selective vulnerability of corticocortical and hippocampal circuits in aging and Alzheimer's disease Prog. Brain Res. 136 2002 467 486
72. J.R. Moyer Jr.; S.C. Furtak, J.P. McGann, and T.H. Brown Aging-related changes in calcium-binding proteins in rat perirhinal cortex Neurobiol. Aging 32 2011 1693 1706
73. J.R. Moyer Jr.; L.T. Thompson, J.P. Black, and J.F. Disterhoft Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner J. Neurophysiol. 68 1992 2100 2109
74. D. Murchison, and W.H. Griffith Calcium buffering systems and calcium signaling in aged rat basal forebrain neurons Aging Cell 6 2007 297 305
75. D. Murchison, A.N. McDermott, C.L. Lasarge, K.A. Peebles, J.L. Bizon, and W.H. Griffith Enhanced calcium buffering in F344 rat cholinergic basal forebrain neurons is associated with age-related cognitive impairment J. Neurophysiol. 102 2009 2194 2207
76. R.A. Nixon The calpains in aging and aging-related diseases Ageing Res Rev 2 2003 407 418
77. C.M. Norris, E.M. Blalock, K.C. Chen, N.M. Porter, and P.W. Landfield Calcineurin enhances L-type Ca(2+) channel activity in hippocampal neurons: increased effect with age in culture Neuroscience 110 2002 213 225
78. C.M. Norris, E.M. Blalock, K.C. Chen, N.M. Porter, O. Thibault, S.D. Kraner, and P.W. Landfield Hippocampal 'zipper' slice studies reveal a necessary role for calcineurin in the increased activity of L-type Ca(2+) channels with aging Neurobiol. Aging 31 2010 328 338
79. M.M. Oh, F.A. Oliveira, J. Waters, and J.F. Disterhoft Altered calcium metabolism in aging CA1 hippocampal pyramidal neurons J. Neurosci. 33 2013 7905 7911
80. X. Peng, C.L. Wood, E.M. Blalock, K.C. Chen, P.W. Landfield, and A.J. Stromberg Statistical implications of pooling RNA samples for microarray experiments BMC Bioinformatics 4 2003 26
81. C. Peterson, and G.E. Gibson Synaptosomal calcium metabolism during hypoxia and 3,4-diaminopyridine treatment J. Neurochem. 42 1984 248 253
82. T.A. Pitler, and P.W. Landfield Aging-related prolongation of calcium spike duration in rat hippocampal slice neurons Brain Res. 508 1990 1 6
83. N.M. Porter, and P.W. Landfield Stress hormones and brain aging: adding injury to insult? Nat. Neurosci. 1 1998 3 4
84. B. Potier, Y. Lamour, and P. Dutar Age-related alterations in the properties of hippocampal pyramidal neurons among rat strains Neurobiol. Aging 14 1993 17 25
85. F. Protasi Structural interaction between RYRs and DHPRs in calcium release units of cardiac and skeletal muscle cells Front. Biosci. 7 2002 d650 658
86. J.N. Reynolds, and P.L. Carlen Diminished calcium currents in aged hippocampal dentate gyrus granule neurones Brain Res. 479 1989 384 390
87. D. Riascos, D. de Leon, A. Baker-Nigh, A. Nicholas, R. Yukhananov, J. Bu, C.K. Wu, and C. Geula Age-related loss of calcium buffering and selective neuronal vulnerability in Alzheimer's disease Acta Neuropathol. 122 2011 565 576
88. H.L. Roderick, M.J. Berridge, and M.D. Bootman Calcium-induced calcium release Curr. Biol. 13 2003 R425
89. W.B. Rowe, E.M. Blalock, K.C. Chen, I. Kadish, D. Wang, J.E. Barrett, O. Thibault, N.M. Porter, G.M. Rose, and P.W. Landfield Hippocampal expression analyses reveal selective association of immediate-early, neuroenergetic, and myelinogenic pathways with cognitive impairment in aged rats J. Neurosci. 27 2007 3098 3110
90. M. Samso, W. Feng, I.N. Pessah, and P.D. Allen Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating PLoS Biol. 7 2009 e85
91. H.E. Scharfman, and N.J. MacLusky Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS Front. Neuroendocrinol. 27 2006 415 435
92. F. Sedarat, L. Xu, E.D. Moore, and G.F. Tibbits Colocalization of dihydropyridine and ryanodine receptors in neonate rabbit heart using confocal microscopy Am. J. Physiol. Heart Circ Physiol. 279 2000 H202 209
93. J.W. Simpkins, and M. Singh More than a decade of estrogen neuroprotection Alzheimer's Dementia: J. Alzheimer's Assoc. 4 2008 S131 136
94. F. Sohrabji, and S. Bake Age-related changes in neuroprotection: is estrogen pro-inflammatory for the reproductive senescent brain? Endocrine 29 2006 191 197
95. G.E. Stutzmann, I. Smith, A. Caccamo, S. Oddo, F.M. Laferla, and I. Parker Enhanced ryanodine receptor recruitment contributes to Ca2+ disruptions in young, adult, and aged Alzheimer's disease mice J. Neurosci. 26 2006 5180 5189
96. C. Supnet, and I. Bezprozvanny Presenilins function in ER calcium leak and Alzheimer's disease pathogenesis Cell Calcium 50 2011 303 309
97. H. Takeshima, S. Komazaki, M. Nishi, M. Iino, and K. Kangawa Junctophilins: a novel family of junctional membrane complex proteins Molecular Cell 6 2000 11 22
98. O. Thibault, J.C. Gant, and P.W. Landfield Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store Aging Cell 6 2007 307 317
99. O. Thibault, R. Hadley, and P.W. Landfield Elevated postsynaptic [Ca2+]i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity J. Neurosci. 21 2001 9744 9756
100. O. Thibault, and P.W. Landfield Increase in single L-type calcium channels in hippocampal neurons during aging Science (New York, N.Y.) 272 1996 1017 1020
101. O. Thibault, T. Pancani, P.W. Landfield, and C.M. Norris Reduction in neuronal L-type calcium channel activity in a double knock-in mouse model of Alzheimer's disease Biochim. Biophys. Acta 1822 2012 546 549
102. E.C. Toescu, and A. Verkhratsky Ca2+ and mitochondria as substrates for deficits in synaptic plasticity in normal brain ageing J. Cell. Mol. Med. 8 2004 181 190
103. G.C. Tombaugh, W.B. Rowe, and G.M. Rose The slow afterhyperpolarization in hippocampal CA1 neurons covaries with spatial learning ability in aged Fisher 344 rats J. Neurosci. 25 2005 2609 2616
104. H. Tu, O. Nelson, A. Bezprozvanny, Z. Wang, S.F. Lee, Y.H. Hao, L. Serneels, B. De Strooper, G. Yu, and I. Bezprozvanny Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimer's disease-linked mutations Cell 126 2006 981 993
105. L.M. Veng, M.H. Mesches, and M.D. Browning Age-related working memory impairment is correlated with increases in the L-type calcium channel protein alpha1D (Cav1.3) in area CA1 of the hippocampus and both are ameliorated by chronic nimodipine treatment Brain Res. Mol. Brain Res. 110 2003 193 202
106. A. Verkhratsky Endoplasmic reticulum calcium signaling in nerve cells Biol. Res. 37 2004 693 699
107. A. Verkhratsky Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons Physiol. Rev. 85 2005 201 279
108. T. Wagenknecht, M. Radermacher, R. Grassucci, J. Berkowitz, H.B. Xin, and S. Fleischer Locations of calmodulin and FK506-binding protein on the three-dimensional architecture of the skeletal muscle ryanodine receptor J. Biol. Chem. 272 1997 32463 32471
109. X. Wang, M.L. Michaelis, and E.K. Michaelis Functional genomics of brain aging and Alzheimer's disease: focus on selective neuronal vulnerability Curr. Genom. 11 2010 618 633
110. G. Watfa, P. Rossignol, A. Kearney-Schwartz, R. Fay, S. Bracard, J. Felblinger, J.M. Boivin, P. Lacolley, F. Zannad, and A. Benetos Use of calcium channel blockers is associated with better cognitive performance in older hypertensive patients with subjective memory complaints J. Hypertens 28 2010 2485 2493
111. J.E. Wilkinson, L. Burmeister, S.V. Brooks, C.C. Chan, S. Friedline, D.E. Harrison, J.F. Hejtmancik, N. Nadon, R. Strong, L.K. Wood, M.A. Woodward, and R.A. Miller Rapamycin slows aging in mice Aging Cell 11 2012 675 682
112. N.T. Wright, B.L. Prosser, K.M. Varney, D.B. Zimmer, M.F. Schneider, and D.J. Weber S100A1 and calmodulin compete for the same binding site on ryanodine receptor J. Biol. Chem. 283 2008 26676 26683
113. H.B. Xin, T. Senbonmatsu, D.S. Cheng, Y.X. Wang, J.A. Copello, G.J. Ji, M.L. Collier, K.Y. Deng, L.H. Jeyakumar, M.A. Magnuson, T. Inagami, M.I. Kotlikoff, and S. Fleischer Oestrogen protects FKBP12.6 null mice from cardiac hypertrophy Nature 416 2002 334 338
114. J.L. Yau, and J.R. Seckl Local amplification of glucocorticoids in the aging brain and impaired spatial memory Front. Aging Neurosci. 4 2012 24
115. R. Zalk, S.E. Lehnart, and A.R. Marks Modulation of the ryanodine receptor and intracellular calcium Annu. Rev. Biochem. 76 2007 367 385