Reversal of aging-related neuronal Ca2+ dysregulation and cognitive impairment by delivery of a transgene encoding FK506-binding protein 12.6/1b to the hippocampus

Journal of Neuroscience

Volumn 35, Issue 30, 2015, Pages 10878-10887

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

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Aging; Alzheimer s disease; Calcium; FKBP; Memory; Ryanodine receptor

Indexed keywords

CALCIUM ION; FK 506 BINDING PROTEIN; PARVOVIRUS VECTOR; CALCIUM; FKBP1B PROTEIN, RAT;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; HIPPOCAMPUS; MORRIS WATER MAZE TEST; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY TEST; YOUNG ADULT; ANIMAL; COGNITION; COGNITION DISORDERS; FISCHER 344 RAT; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; NERVE CELL; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENE; TRANSGENIC RAT;

AGING; ANIMALS; CALCIUM; COGNITION; COGNITION DISORDERS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, INBRED F344; RATS, TRANSGENIC; REAL-TIME POLYMERASE CHAIN REACTION; TACROLIMUS BINDING PROTEINS; TRANSGENES;

EID: 84938488959     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1248-15.2015     Document Type: Article

References (77)

1. Andrade R, Foehring RC, Tzingounis AV (2012) The calcium-activated slow AHP: cutting through the Gordian knot. Front Cell Neurosci 6:47. Medline
2. Andreasen M, Lambert JD (1995) The excitability of CA1 pyramidal cell dendrites is modulated by a local Ca(2+)-dependent K(+)-conductance. Brain Res 698:193-203. CrossRef Medline
3. Aschauer DF, Kreuz S, Rumpel S (2013) Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLoS One 8:e76310. CrossRef Medline
4. Betley JN, Sternson SM (2011) Adeno-associated viral vectors for mapping, monitoring, and manipulating neural circuits. Hum Gene Ther 22:669- 677. CrossRef Medline
5. Bezprozvanny I, Mattson MP (2008) Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease. Trends Neurosci 31:454-463. CrossRef Medline
6. 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. CrossRef Medline
7. Bosch MK, Nerbonne JM, Ornitz DM (2014) Dual transgene expression in murine cerebellar Purkinje neurons by viral transduction in vivo. PLoS One 9:e104062. CrossRef Medline
8. Broekman ML, Comer LA, Hyman BT, Sena-Esteves M (2006) Adenoassociated virus vectors serotyped with AAV8 capsid are more efficient than AAV-1 or -2 serotypes for widespread gene delivery to the neonatal mouse brain. Neuroscience 138:501-510. CrossRef Medline
9. Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130 -138. CrossRef Medline
10. Cartford MC, Gemma C, Bickford PC (2002) Eighteen-month-old Fischer 344 rats fed a spinach-enriched diet show improved delay classical eyeblink conditioning and reduced expression of tumor necrosis factor alpha (TNFalpha) and TNFbeta in the cerebellum. J Neurosci 22:5813-5816. Medline
11. Castle MJ, Gershenson ZT, Giles AR, Holzbaur EL, Wolfe JH (2014) Adenoassociated virus serotypes 1, 8, and 9 share conserved mechanisms for anterograde and retrograde axonal transport. Hum Gene Ther 25:705- 720. CrossRef Medline
12. Cearley CN, Wolfe JH (2006) Transduction characteristics of adenoassociated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther 13:528 -537. CrossRef Medline
13. Disterhoft JF, Oh MM (2006) Pharmacological and molecular enhancement of learning in aging and Alzheimer's disease. J Physiol Paris 99:180- 192. CrossRef Medline
14. Disterhoft JF, Oh MM (2007) Alterations in intrinsic neuronal excitability during normal aging. Aging Cell 6:327-336. CrossRef Medline
15. Disterhoft JF, Thompson LT, Moyer JR Jr, Mogul DJ (1996) Calciumdependent afterhyperpolarization and learning in young and aging hippocampus. Life Sci 59:413- 420. CrossRef Medline
16. Falkow S (2004) Molecular Koch's postulates applied to bacterial pathogenicity- a personal recollection 15 years later. Nat Rev Microbiol 2:67-72. CrossRef Medline
17. Foster TC, NorrisCM (1997) Age-associated changes in Ca(2+)-dependent processes: relation to hippocampal synaptic plasticity. Hippocampus 7:602- 612. CrossRef Medline
18. Gallagher M, Rapp PR (1997) The use of animal models to study the effects of aging on cognition. Annu Rev Psychol 48:339 -370. CrossRef Medline
19. Gant JC, Sama MM, Landfield PW, Thibault O (2006) Early and simultaneous emergence of multiple hippocampal biomarkers of aging is mediated by Ca2+-induced Ca2+ release. J Neurosci 26:3482-3490. CrossRef Medline
20. Gant JC, Chen KC, Norris CM, Kadish I, Thibault O, Blalock EM, Porter NM, LandfieldPW (2011) Disrupting function of FK506-binding protein 1b/ 12.6 induces the Ca(2)+-dysregulation aging phenotype in hippocampal neurons. J Neurosci 31:1693-1703. CrossRef Medline
21. Gant JC, Blalock EM, Chen KC, Kadish I, Porter NM, Norris CM, Thibault O, Landfield PW (2014) FK506-binding protein 1b/12.6: a key to agingrelated hippocampal Ca2+ dysregulation? Eur J Pharmacol 739:74-82. CrossRef Medline
22. Gibson GE, Peterson C (1987) Calcium and the aging nervous system. Neurobiol Aging 8:329 -343. CrossRef Medline
23. Gibson GE, Zhang H, Toral-Barza L, Szolosi S, Tofel-Grehl B (1996) Calcium stores in cultured fibroblasts and their changes with Alzheimer's disease. Biochim Biophys Acta 1316:71-77. CrossRef Medline
24. Hausch F, Kozany C, Theodoropoulou M, Fabian AK (2013) FKBPs and the Akt/mTOR pathway. Cell Cycle 12:2366 -2370. CrossRef Medline
25. Hebert LE, Weuve J, Scherr PA, Evans DA (2013) Alzheimer disease in the United States (2010 -2050) estimated using the 2010 census. Neurology 80:1778 -1783. CrossRef Medline
26. Hemond P, Jaffe DB (2005) Caloric restriction prevents aging-associated changes in spike-mediated Ca2+ accumulation and the slow afterhyperpolarization in hippocampal CA1 pyramidal neurons. Neuroscience 135: 413-420. CrossRef Medline
27. Hoeffer CA, Klann E (2010) mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci 33:67-75. CrossRef Medline
28. 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. CrossRef Medline
29. Hudry E, Wu HY, Arbel-Ornath M, Hashimoto T, Matsouaka R, Fan Z, Spires-Jones TL, Betensky RA, Bacskai BJ, Hyman BT (2012) Inhibition of the NFAT pathway alleviates amyloid beta neurotoxicity in a mouse model of Alzheimer's disease. J Neurosci 32:3176 -3192. CrossRef Medline
30. 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. CrossRef Medline
31. Kang CM, Hong Y, Dhe-Paganon S, Yoon HS (2008) FKBP family proteins: immunophilins with versatile biological functions. Neurosignals 16:318- 325. CrossRef Medline
32. 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. CrossRef Medline
33. Khachaturian ZS (1989) The role of calcium regulation in brain aging: reexamination of a hypothesis. Aging (Milano) 1:17-34.
34. Kuchibhotla KV, Goldman ST, Lattarulo CR, Wu HY, Hyman BT, Bacskai BJ (2008) Aß plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron 59:214 -225. CrossRef Medline
35. Kumar A, Foster TC (2005) Intracellular calcium stores contribute to increased susceptibility to LTD induction during aging. Brain Res 1031: 125-128. CrossRef Medline
36. Lancaster B, Hu H, Ramakers GM, Storm JF (2001) Interaction between synaptic excitation and slow afterhyperpolarization current in rat hippocampal pyramidal cells. J Physiol 536:809-823. CrossRef Medline
37. Landfield PW (1987) "Increased calcium-current" hypothesis of brain aging. Neurobiol Aging 8:346 -347. CrossRef Medline
38. Landfield PW, Pitler TA (1984) Prolonged Ca2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226:1089 -1092. CrossRef Medline
39. Lima PA, Marrion NV (2007) Mechanisms underlying activation of the slow AHP in rat hippocampal neurons. Brain Res 1150:74-82. CrossRef Medline
40. Luebke JI, Amatrudo JM (2012) Age-related increase of sI(AHP) in prefrontal pyramidal cells of monkeys: relationship to cognition. Neurobiol Aging 33:1085-1095. CrossRef Medline
41. Lynch G, BaudryM (1987) Brain spectrin, calpain and long-term changes in synaptic efficacy. Brain Res Bull 18:809-815. CrossRef Medline
42. Lynch G, Rex CS, Gall CM (2006) Synaptic plasticity in early aging. Ageing Res Rev 5:255-280. CrossRef Medline
43. MacMillanD (2013) FK506 binding proteins: cellular regulators of intracellular Ca2+ signalling. Eur J Pharmacol 700:181-193. CrossRef Medline
44. MacMillan D, McCarron JG (2009) Regulation by FK506 and rapamycin of Ca2+ release from the sarcoplasmic reticulum in vascular smooth muscle: the role of FK506 binding proteins and mTOR. Br J Pharmacol 158: 1112-1120. CrossRef Medline
45. Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol 354:319 -331. CrossRef Medline
46. Magee JC, Johnston D (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275:209 -213. CrossRef Medline
47. Markowska AL (1999) Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J Neurosci 19:8122- 8133. Medline
48. Masliah E, Crews L, Hansen L (2006) Synaptic remodeling during aging and in Alzheimer's disease. J Alzheimers Dis 9:91-99. Medline
49. McCown TJ (2010) The future of epilepsy treatment: focus on adenoassociated virus vector gene therapy. Drug News Perspect 23:281-286. CrossRef Medline
50. Morrison JH, Hof PR (2007) Life and death of neurons in the aging cerebral cortex. Int Rev Neurobiol 81:41-57. CrossRef Medline
51. Moser MB, Moser EI, Forrest E, Andersen P, Morris RG (1995) Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci U S A 92:9697-9701. CrossRef Medline
52. 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. Medline
53. Murchison D, Griffith WH (2007) Calcium buffering systems and calcium signaling in aged rat basal forebrain neurons. Aging Cell 6:297-305. CrossRef Medline
54. Murphy GG, Shah V, Hell JW, Silva AJ (2006) Investigation of age-related cognitive decline using mice as a model system: neurophysiological correlates. Am J Geriatr Psychiatry 14:1012-1021. CrossRef Medline
55. Nixon RA, Saito KI, Grynspan F, Griffin WR, Katayama S, Honda T, Mohan PS, Shea TB, BeermannM (1994) Calcium-activated neutral proteinase (calpain) system in aging and Alzheimer's disease. Ann N Y Acad Sci 747:77-91. Medline
56. OhMM, Oliveira FA, Waters J, Disterhoft JF (2013) Altered calcium metabolism in aging CA1 hippocampal pyramidal neurons. J Neurosci 33:7905- 7911. CrossRef Medline
57. Overk CR, Cartier A, Shaked G, Rockenstein E, Ubhi K, Spencer B, Price DL, Patrick C, Desplats P, Masliah E (2014) Hippocampal neuronal cells that accumulate alpha-synuclein fragments are more vulnerable to Aß oligomer toxicity via mGluR5-implications for dementia with Lewy bodies. Mol Neurodegener 9:18. CrossRef Medline
58. Peters A, Rosene DL, Moss MB, Kemper TL, Abraham CR, Tigges J, AlbertMS (1996) Neurobiological bases of age-related cognitive decline in the rhesus monkey. J Neuropathol Exp Neurol 55:861- 874. CrossRef Medline
59. Reitz C, Brayne C, Mayeux R (2011) Epidemiology of Alzheimer disease. Nat Rev Neurol 7:137-152. CrossRef Medline
60. Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69: 143-179. CrossRef Medline
61. 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. CrossRef Medline
62. Rozkalne A, Hyman BT, Spires-Jones TL (2011) Calcineurin inhibition with FK506 ameliorates dendritic spine density deficits in plaque-bearing Alzheimer model mice. Neurobiol Dis 41:650-654. CrossRef Medline
63. Sah P, Bekkers JM (1996) Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of long-term potentiation. J Neurosci 16:4537- 4542. Medline
64. Salegio EA, Samaranch L, Kells AP, Forsayeth J, Bankiewicz K (2012) Guided delivery of adeno-associated viral vectors into the primate brain. Adv Drug Deliv Rev 64:598-604. CrossRef Medline
65. Scharfman HE, MacLusky NJ (2006) Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front Neuroendocrinol 27:415- 435. CrossRef Medline
66. Scharfman HE, Schwartzkroin PA (1989) Protection of dentate hilar cells from prolonged stimulation by intracellular calcium chelation. Science 246:257-260. CrossRef Medline
67. Scheff SW, Price DA, Schmitt FA, DeKosky ST, Mufson EJ (2007) Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 68:1501-1508. CrossRef Medline
68. Stutzmann GE, Smith I, Caccamo A, Oddo S, Laferla FM, Parker I (2006) Enhanced ryanodine receptor recruitment contributes to Ca2+ disruptions in young, adult, and aged Alzheimer's disease mice. J Neurosci 26: 5180-5189. CrossRef Medline
69. Thibault O, LandfieldPW (1996) Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272:1017-1020. CrossRef Medline
70. Thibault O, Hadley R, Landfield PW (2001) Elevated postsynaptic [Ca2+]i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J Neurosci 21:9744 -9756. Medline
71. 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. CrossRef Medline
72. Thibault O, Pancani T, Landfield PW, NorrisCM (2012) Reduction in neuronal L-type calcium channel activity in a double knock-in mouse model of Alzheimer's disease. Biochim Biophys Acta 1822:546 -549. CrossRef Medline
73. Toescu EC, Verkhratsky A (2007) The importance of being subtle: small changes in calcium homeostasis control cognitive decline in normal aging. Aging Cell 6:267-273. CrossRef Medline
74. 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. CrossRef Medline
75. Verkhratsky A (2005) Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 85:201-279. CrossRef Medline
76. Wang Y, Mattson MP (2014) L-type Ca2+ currents at CA1 synapses, but not CA3 or dentate granule neuron synapses, are increased in 3xTgAD mice in an age-dependent manner. Neurobiol Aging 35:88 -95. CrossRef Medline
77. Zalk R, Lehnart SE, Marks AR (2007) Modulation of the ryanodine receptor and intracellular calcium. Annu Rev Biochem 76:367-385. CrossRef Medline