Disrupting function of FK506-binding protein 1b/12.6 induces the Ca 2+-dysregulation aging phenotype in hippocampal neurons

Journal of Neuroscience

Volumn 31, Issue 5, 2011, Pages 1693-1703

  Gant, John C ^a   Chen, Kuey Chu ^a   Norris, Christopher M ^a   Kadish, Inga ^b   Thibault, Olivier ^a   Blalock, Eric M ^a   Porter, Nada M ^a   Landfield, Philip W ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 1B; MAMMALIAN TARGET OF RAPAMYCIN; NIMODIPINE; RAPAMYCIN; RYANODINE RECEPTOR 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS VECTOR; VOLTAGE GATED CALCIUM CHANNEL;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN; BRAIN SLICE; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL AGING; CONTROLLED STUDY; CORRELATION ANALYSIS; DOWN REGULATION; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; JUVENILE ANIMAL; MALE; MEMORY; MICROINJECTION; MUSCLE CELL; NERVE CELL; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; PYRAMIDAL NERVE CELL; RAT; RNA INTERFERENCE; UPREGULATION;

AGING; ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CELLS, CULTURED; ELECTROPHYSIOLOGY; GENE KNOCKDOWN TECHNIQUES; GENETIC VECTORS; HIPPOCAMPUS; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE POTENTIALS; MICROINJECTIONS; PATCH-CLAMP TECHNIQUES; POLYMERASE CHAIN REACTION; PYRAMIDAL CELLS; RATS; RATS, INBRED F344; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SIROLIMUS; TACROLIMUS BINDING PROTEINS;

EID: 79551505854     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4805-10.2011     Document Type: Article

References (99)

1. Berridge MJ (1997) Elementary and global aspects of calcium signalling. J Physiol 499:291-306. (Pubitemid 27129414)
2. 2+ channel to the ryanodine receptor in the hippocampal neuron in slices. Cell Calcium 46:30-38.
3. Bezprozvanny I, Mattson MP (2008) Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease. Trends Neurosci 31:454-463.
4. Blalock EM, Porter NM, Landfield PW (1999) Decreased G-protein-mediated regulation and shift in calcium channel types with age in hippocampal cultures. J Neurosci 19:8674-8684.
5. Blalock EM, Geddes JW, Chen KC, Porter NM, Markesbery WR, Landfield PW (2004) Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses. Proc Natl Acad Sci U S A 101:2173-2178.
6. Blalock EM, Grondin R, Chen KC, Thibault O, Thibault V, Pandya JD, Dowling A, Zhang Z, Sullivan P, Porter NM, Landfield PW (2010) Agingrelated gene expression in hippocampus proper compared with dentate gyrus is selectively associated with metabolic syndrome variables in rhesus monkeys. J Neurosci 30:6058-6071.
7. Blundell J, Kouser M, Powell CM (2008) Systemic inhibition of mammalian target of rapamycin inhibits fear memory reconsolidation. Neurobiol Learn Mem 90:28-35.
8. Brewer LD, Thibault V, Chen KC, Langub MC, Landfield PW, Porter NM (2001) Vitamin D hormone confers neuroprotection in parallel with downregulation of L-type calcium channel expression in hippocampal neurons. J Neurosci 21:98-108.
9. Brinton RD (2008) Estrogen regulation of glucose metabolism and mitochondrial function: therapeutic implications for prevention of Alzheimer's disease. Adv Drug Deliv Rev 60:1504-1511.
10. Brown TH, Jaffe DB (1994) Calcium imaging in hippocampal neurons using confocal microscopy. Ann N Y Acad Sci 747:313-324.
11. Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7:30-40.
12. Caccamo A, Majumder S, Richardson A, Strong R, Oddo S (2010) Molecular interplay between mTOR, Aβ and tau: effects on cognitive impairments. J Biol Chem 285:13107-13120.
13. Campbell LW, Hao SY, Thibault O, Blalock EM, Landfield PW (1996) Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J Neurosci 16:6286-6295. (Pubitemid 26314001)
14. Cearley CN, Wolfe JH (2006) Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther 13:528-537.
15. Chavis P, Fagni L, Lansman JB, Bockaert J (1996) Functional coupling between ryanodine receptors and L-type calcium channels in neurons. Nature 382:719-722.
16. 2+ channel activity in single neurons of hippocampal "zipper" slices. Proc Natl Acad Sci U S A 97:4357-4362.
17. 2+ plateau in older cultured hippocampal neurons. Eur J Pharmacol 447:189-200.
18. Cracco JB, Serrano P, Moskowitz SI, Bergold PJ, Sacktor TC (2005) Protein synthesis-dependent LTP in isolated dendrites of CA1 pyramidal cells. Hippocampus 15:551-556.
19. Crystal RG, Sondhi D, Hackett NR, Kaminsky SM, Worgall S, Stieg P, Souweidane M, Hosain S, Heier L, Ballon D, Dinner M, Wisniewski K, Kaplitt M, Greenwald BM, Howell JD, Strybing K, Dyke J, Voss H (2004) Clinical protocol. Administration of a replication-deficient adeno-associated virus gene transfer vector expressing the human CLN2 cDNA to the brain of children with late infantile neuronal ceroid lipofuscinosis. Hum Gene Ther 15:1131-1154.
20. Disterhoft JF, Oh MM (2007) Alterations in intrinsic neuronal excitability during normal aging. Aging Cell 6:327-336.
21. Disterhoft JF, Thompson LT, Moyer JR Jr, Mogul DJ (1996) Calcium-dependent afterhyperpolarization and learning in young and aging hippocampus. Life Sci 59:413-420.
22. Eitoku M, Sato L, Senda T, Horikoshi M (2008) Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell Mol Life Sci 65:414-444.
23. Fitzsimons HL, Bland RJ, During MJ (2002) Promoters and regulatory elements that improve adeno-associated virus transgene expression in the brain. Methods 28:227-236.
24. 2+ release. J Neurosci 26:3482-3490.
25. Gibson GE, Peterson C (1987) Calcium and the aging nervous system. Neurobiol Aging 8:329-343.
26. Gómez AM, Rueda A, Sainte-Marie Y, Pereira L, Zissimopoulos S, Zhu X, Schaub R, Perrier E, Perrier R, Latouche C, Richard S, Picot MC, Jaisser F, Lai FA, Valdivia HH, Benitah JP (2009) Mineralocorticoid modulation of cardiac ryanodine receptor activity is associated with downregulation of FK506-binding proteins. Circulation 119:2179-2187.
27. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460:392-395.
28. 2+ accumulation and the slow afterhyperpolarization in hippocampal CA1 pyramidal neurons. Neuroscience 135:413-420.
29. 2+ channel subunit mRNA expression in the hippocampus of aged F344 rats. Neurobiol Aging 19:581-587.
30. Hoeffer CA, Tang W, Wong H, Santillan A, Patterson RJ, Martinez LA, Tejada-Simon MV, Paylor R, Hamilton SL, Klann E (2008) Removal of FKBP12 enhances mTOR-Raptor interactions, LTP, memory, and perseverative/repetitive behavior. Neuron 60:832-845.
31. Holmes MC, Seckl JR (2006) The role of 11beta-hydroxysteroid dehydrogenases in the brain. Mol Cell Endocrinol 248:9-14.
32. Jacinto E, Hall MN (2003) Tor signalling in bugs, brain and brawn. Nat Rev Mol Cell Biol 4:117-126.
33. 2+ transients in hippocampal brain slices during simultaneous current- and voltage-clamp recording. Microsc Res Tech 29:279-289.
34. 2+ entry into hippocampal neurons. Nature 357:244-246.
35. Jakob RP, Zoldák G, Aumüller T, Schmid FX (2009) Chaperone domains convert prolyl isomerases into generic catalysts of protein folding. Proc Natl Acad Sci U S A 106:20282-20287.
36. Joëls M, de Kloet ER (1989) Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. Science 245:1502-1505.
37. Johnston LC, Eberling J, Pivirotto P, Hadaczek P, Federoff HJ, Forsayeth J, Bankiewicz KS (2009) Clinically relevant effects of convection-enhanced delivery of AAV2-GDNF on the dopaminergic nigrostriatal pathway in aged rhesus monkeys. Hum Gene Ther 20:497-510.
38. Kadish I, Van Groen T (2002) Low levels of estrogen significantly diminish axonal sprouting after entorhinal cortex lesions in the mouse. J Neurosci 22:4095-4102. (Pubitemid 37465717)
39. Kadish I, Thibault O, Blalock EM, Chen KC, Gant JC, Porter NM, Landfield PW (2009) Hippocampal and cognitive aging across the lifespan: a bioenergetic shift precedes and increased cholesterol trafficking parallels memory impairment. J Neurosci 29:1805-1816.
40. Kang CB, Hong Y, Dhe-Paganon S, Yoon HS (2008) FKBP family proteins: immunophilins with versatile biological functions. Neurosignals 16:318-325.
41. Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, Lawlor PA, Bland RJ, Young D, Strybing K, Eidelberg D, During MJ (2007) Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 369:2097-2105.
42. Kato H, Oikawa T, Otsuka K, Takahashi A, Itoyama Y (2000) Postischemic changes in the immunophilin FKBP12 in the rat brain. Brain Res Mol Brain Res 84:58-66.
43. Kells AP, Eberling J, Su X, Pivirotto P, Bringas J, Hadaczek P, Narrow WC, Bowers WJ, Federoff HJ, Forsayeth J, Bankiewicz KS (2010) Regeneration of the MPTP-lesioned dopaminergic system after convection-enhanced delivery of AAV2-GDNF. J Neurosci 30:9567-9577.
44. Kerr DS, Campbell LW, Hao SY, Landfield PW (1989) Corticosteroid modulation of hippocampal potentials: increased effect with aging. Science 245:1505-1509.
45. Khachaturian ZS (1989) The role of calcium regulation in brain aging: re-examination of a hypothesis. Aging (Milano) [Erratum (1989) 1:II] 1:17-34.
46. Kim S, Yun HM, Baik JH, Chung KC, Nah SY, Rhim H (2007) Functional interaction of neuronal Cav1.3 L-type calcium channel with ryanodine receptor type 2 in the rat hippocampus. J Biol Chem 282:32877-32889.
47. Kirischuk S, Voitenko N, Kostyuk P, Verkhratsky A (1996) Age-associated changes of cytoplasmic calcium homeostasis in cerebellar granule neurons in situ: investigation on thin cerebellar slices. Exp Gerontol 31:475-487. (Pubitemid 26234903)
48. Klein RL, Hamby ME, Gong Y, Hirko AC, Wang S, Hughes JA, King MA, Meyer EM (2002) Dose and promoter effects of adeno-associated viral vector for green fluorescent protein expression in the rat brain. Exp Neurol 176:66-74.
49. Klein RL, Dayton RD, Tatom JB, Henderson KM, Henning PP (2008) AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol Ther 16:89-96.
50. Kumar A, Foster TC (2004) Enhanced long-term potentiation during aging is masked by processes involving intracellular calcium stores. J Neurophysiol 91:2437-2444.
51. Kumar A, Foster TC (2005) Intracellular calcium stores contribute to increased susceptibility to LTD induction during aging. Brain Res 1031:125-128.
52. Landfield PW (1987) "Increased calcium-current" hypothesis of brain aging. Neurobiol Aging 8:346-347.
53. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226:1089-1092.
54. Landfield PW, Blalock EM, Chen KC, Porter NM (2007) A new glucocorticoid hypothesis of brain aging: implications for Alzheimer's disease. Curr Alzheimer Res 4:205-212.
55. Lehnart SE, Huang F, Marx SO, Marks AR (2003) Immunophilins and coupled gating of ryanodine receptors. Curr Top Med Chem 3:1383-1391.
56. Long C, Cook LG, Wu GY, Mitchell BM (2007) Removal of FKBP12/12.6 from endothelial ryanodine receptors leads to an intracellular calcium leak and endothelial dysfunction. Arterioscler Thromb Vasc Biol 27:1580-1586. (Pubitemid 46986113)
57. Lynch G, Rex CS, Gall CM (2006) Synaptic plasticity in early aging. Ageing Res Rev 5:255-280.
58. 2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol 487:67-90.
59. Magnusson KR, Kresge D, Supon J (2006) Differential effects of aging on NMDA receptors in the intermediate versus the dorsal hippocampus. Neurobiol Aging 27:324-333.
60. Marks AR (1997) Intracellular calcium-release channels: regulators of cell life and death. Am J Physiol 272:H597-H605.
61. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101:365-376.
62. McPhee SW, Janson CG, Li C, Samulski RJ, Camp AS, Francis J, Shera D, Lioutermann L, Feely M, Freese A, Leone P (2006) Immune responses to AAV in a phase I study for Canavan disease. J Gene Med 8:577-588.
63. 2+ regulation. Mech Ageing Dev 25:215-225.
64. 2+ channels. Neuron 9:1163-1173.
65. Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8:608-619.
66. Mouravlev A, Dunning J, Young D, During MJ (2006) Somatic gene transfer of cAMP response element-binding protein attenuates memory impairment in aging rats. Proc Natl Acad Sci U S A 103:4705-4710.
67. Moyer JR Jr, Thompson LT, Black JP, Disterhoft JF (1992) Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. J Neurophysiol 68:2100-2109.
68. Murchison D, Griffith WH (2007) Calcium buffering systems and calcium signaling in aged rat basal forebrain neurons. Aging Cell 6:297-305. (Pubitemid 46785135)
69. Nicotera P, Zhivotovsky B, Orrenius S (1994) Nuclear calcium transport and the role of calcium in apoptosis. Cell Calcium 16:279-288. (Pubitemid 24300838)
70. 2+ channels. J Neurosci 18:3171-3179.
71. 2+ channel activity in hippocampal neurons: increased effect with age in culture. Neuroscience 110:213-225.
72. Oh MM, McKay BM, Power JM, Disterhoft JF (2009) Learning-related postburst afterhyperpolarization reduction in CA1 pyramidal neurons is mediated by protein kinase A. Proc Natl Acad Sci U S A 106:1620-1625.
73. Parsons RG, Gafford GM, Helmstetter FJ (2006) Translational control via the mammalian target of rapamycin pathway is critical for the formation and stability of long-term fear memory in amygdala neurons. J Neurosci 26:12977-12983.
74. Porter NM, Landfield PW (1998) Stress hormones and brain aging: adding injury to insult? Nat Neurosci 1:3-4.
75. Porter NM, Thibault O, Thibault V, Chen KC, Landfield PW (1997) Calcium channel density and hippocampal cell death with age in long-term culture. J Neurosci 17:5629-5639.
76. Protasi F (2002) Structural interaction between RYRs and DHPRs in calcium release units of cardiac and skeletal muscle cells. Front Biosci 7:d650-d658.
77. 2+ channels in rat central and peripheral neurons: high-threshold current resistant to dihydropyridine blockers and omega-conotoxin. Neuron 6:269-280.
78. Reynolds JN, Carlen PL (1989) Diminished calcium currents in aged hippocampal dentate gyrus granule neurones. Brain Res 479:384-390.
79. Rowe WB, Blalock EM, Chen KC, Kadish I, Wang D, Barrett JE, Thibault O, Porter NM, Rose GM, Landfield PW (2007) Hippocampal expression analyses reveal selective association of immediate-early, neuroenergetic, and myelinogenic pathways with cognitive impairment in aged rats. J Neurosci 27:3098-3110.
80. Rüegg S, Baybis M, Juul H, Dichter M, Crino PB (2007) Effects of rapamycin on gene expression, morphology, and electrophysiological properties of rat hippocampal neurons. Epilepsy Res 77:85-92.
81. Sedarat F, Xu L, Moore ED, Tibbits GF (2000) Colocalization of dihydropyridine and ryanodine receptors in neonate rabbit heart using confocal microscopy. Am J Physiol Heart Circ Physiol 279:H202-H209.
82. Smith CC, Vedder LC, McMahon LL (2009) Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses. Psychoneuroendocrinology 34 [Suppl 1]:S130-S142.
83. Stutzmann GE, Smith I, Caccamo A, Oddo S, Parker I, Laferla F (2007) Enhanced ryanodine-mediated calcium release in mutant PS1-expressing Alzheimer's mouse models. Ann N Y Acad Sci 1097:265-277.
84. Su X, Kells AP, Huang EJ, Lee HS, Hadaczek P, Beyer J, Bringas J, Pivirotto P, Penticuff J, Eberling J, Federoff HJ, Forsayeth J, Bankiewicz KS (2009) Safety evaluation of AAV2-GDNF gene transfer into the dopaminergic nigrostriatal pathway in aged and parkinsonian rhesus monkeys. Hum Gene Ther 20:1627-1640.
85. Tang SJ, Reis G, Kang H, Gingras AC, Sonenberg N, Schuman EM (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci U S A 99:467-472. (Pubitemid 34060384)
86. + channel is modulated by FK506 and rapamycin. Brain Res 786:255-258.
87. Thibault O, Landfield PW (1996) Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272:1017-1020. (Pubitemid 26259320)
88. 2+]i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J Neurosci 21:9744-9756.
89. Thibault O, Gant JC, Landfield PW (2007) Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store. Aging Cell 6:307-317.
90. Toescu EC, Verkhratsky A (2003) Neuronal ageing from an intraneuronal perspective: roles of endoplasmic reticulum and mitochondria. Cell Calcium 34:311-323.
91. Tombaugh GC, Rowe WB, Rose GM (2005) The slow afterhyperpolarization in hippocampal CA1 neurons covaries with spatial learning ability in aged Fisher 344 rats. J Neurosci 25:2609-2616.
92. Tonkikh A, Janus C, El-Beheiry H, Pennefather PS, Samoilova M, McDonald P, Ouanounou A, Carlen PL (2006) Calcium chelation improves spatial learning and synaptic plasticity in aged rats. Exp Neurol 197:291-300.
93. Tsien RW, Lipscombe D, Madison DV, Bley KR, Fox AP (1988) Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11:431-438.
94. Tsien RY (1988) Fluorescence measurement and photochemical manipulation of cytosolic free calcium. Trends Neurosci 11:419-424.
95. v1.3) of L-type calcium channels in the hippocampus of aged rats. Brain Res Mol Brain Res 107:120-127.
96. Verkhratsky A (2004) Endoplasmic reticulum calcium signaling in nerve cells. Biol Res 37:693-699.
97. Watabe AM, O'Dell TJ (2003) Age-related changes in theta frequency stimulation-induced long-term potentiation. Neurobiol Aging 24:267-272.
98. Zaiss AK, Muruve DA (2005) Immune responses to adeno-associated virus vectors. Curr Gene Ther 5:323-331.
99. Zalk R, Lehnart SE, Marks AR (2007) Modulation of the ryanodine receptor and intracellular calcium. Annu Rev Biochem 76:367-385.