Molecular mechanism for age-related memory loss: The histone-binding protein RbAp48

Science Translational Medicine

Volumn 5, Issue 200, 2013, Pages

  Pavlopoulos, Elias ^a   Jones, Sidonie ^a,b   Kosmidis, Stylianos ^a   Close, Maggie ^a   Kim, Carla ^a   Kovalerchik, Olga ^a   Small, Scott A ^a,b   Kandel, Eric R ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOBLASTOMA BINDING PROTEIN 4;

AGE; AGING; ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; AUTOPSY; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; FOREBRAIN; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE EXPRESSION; GENE IDENTIFICATION; HIPPOCAMPUS; HISTONE ACETYLATION; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVIEW; TRANSGENIC MOUSE; UPREGULATION;

ACETYLATION; ADULT; AGED; AGED, 80 AND OVER; AGING; ANIMALS; DENTATE GYRUS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DOMINANT; HISTONE ACETYLTRANSFERASES; HISTONES; HUMANS; MALE; MEMBRANE PROTEINS; MEMORY DISORDERS; MICE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; PHOSPHOPROTEINS; PROTEIN BINDING; RETINOBLASTOMA-BINDING PROTEIN 4; RNA, MESSENGER;

EID: 84883889160     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3006373     Document Type: Review

References (51)

1. S. A. Small, S. A. Schobel, R. B. Buxton, M. P. Witter, C. A. Barnes, A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 12, 585-601 (2011).
2. H. Braak, I. Alafuzoff, T. Arzberger, H. Kretzschmar, K. Del Tredici, Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 112, 389-404 (2006).
3. T. Gómez-Isla, J. L. Price, D. W. McKeel Jr., J. C. Morris, J. H. Growdon, B. T. Hyman, Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J. Neurosci. 16, 4491-4500 (1996).
4. D. R. Thal, U. Rüb, M. Orantes, H. Braak, Phases of Ab-deposition in the human brain and its relevance for the development of AD. Neurology 58, 1791-1800 (2002).
5. M. J. West, Regionally specific loss of neurons in the aging human hippocampus. Neurobiol. Aging 14, 287-293 (1993).
6. S. A. Small, G. M. Perera, R. DeLaPaz, R. Mayeux, Y. Stern, Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer's disease. Ann. Neurol. 45, 466-472 (1999).
7. S. A. Small, W. Y. Tsai, R. DeLaPaz, R. Mayeux, Y. Stern, Imaging hippocampal function across the human life span: Is memory decline normal or not? Ann. Neurol. 51, 290-295 (2002).
8. H. Moreno, F. Hua, T. Brown, S. Small, Longitudinal mapping of mouse cerebral blood volume with MRI. NMR Biomed. 19, 535-543 (2006).
9. H. Moreno, W. E. Wu, T. Lee, A. Brickman, R. Mayeux, T. R. Brown, S. A. Small, Imaging the Ab-related neurotoxicity of Alzheimer disease. Arch. Neurol. 64, 1467-1477 (2007).
10. S. A. Small, M. K. Chawla, M. Buonocore, P. R. Rapp, C. A. Barnes, Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. Proc. Natl. Acad. Sci. U.S.A. 101, 7181-7186 (2004).
11. C. K. Toner, E. Pirogovsky, C. B. Kirwan, P. E. Gilbert, Visual object pattern separation deficits in nondemented older adults. Learn. Mem. 16, 338-342 (2009).
12. M. A. Yassa, J. W. Lacy, S. M. Stark, M. S. Albert, M. Gallagher, C. E. Stark, Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus 21, 968-979 (2011).
13. S. M. Stark, M. A. Yassa, C. E. Stark, Individual differences in spatial pattern separation performance associated with healthy aging in humans. Learn. Mem. 17, 284-288 (2010).
14. A. M. Brickman, Y. Stern, S. A. Small, Hippocampal subregions differentially associate with standardized memory tests. Hippocampus 21, 923-928 (2011).
15. N. M. Lewandowski, S. A. Small, Brain microarray: Finding needles in molecular haystacks. J. Neurosci. 25, 10341-10346 (2005).
16. S. A. Small, K. Kent, A. Pierce, C. Leung, M. S. Kang, H. Okada, L. Honig, J. P. Vonsattel, T. W. Kim, Model-guided microarray implicates the retromer complex in Alzheimer's disease. Ann. Neurol. 58, 909-919 (2005).
17. Q. Zhang, N. Vo, R. H. Goodman, Histone binding protein RbAp48 interacts with a complex of CREB binding protein and phosphorylated CREB. Mol. Cell. Biol. 20, 4970-4978 (2000).
18. +/-mice: A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42, 947-959 (2004).
19. E. Korzus, M. G. Rosenfeld, M. Mayford, CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42, 961-972 (2004).
20. C. G. Vecsey, J. D. Hawk, K. M. Lattal, J. M. Stein, S. A. Fabian, M. A. Attner, S. M. Cabrera, C. B. McDonough, P. K. Brindle, T. Abel, M. A. Wood, Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 27, 6128-6140 (2007).
21. Y. H. Chung, E. J. Kim, C. M. Shin, K. M. Joo, M. J. Kim, H. W. Woo, C. I. Cha, Age-related changes in CREB binding protein immunoreactivity in the cerebral cortex and hippocampus of rats. Brain Res. 956, 312-318 (2002).
22. S. Trompet, A. J. Craen, J. W. Jukema, D. Pons, P. E. Slagboom, D. Kremer, E. L. Bollen, R. G. Westendorp, Variation in the CBP gene involved in epigenetic control associates with cognitive function. Neurobiol. Aging 32, 549.e541-549.e548 (2011).
23. S. Peleg, F. Sananbenesi, A. Zovoilis, S. Burkhardt, S. Bahari-Javan, R. C. Agis-Balboa, P. Cota, J. L. Wittnam, A. Gogol-Doering, L. Opitz, G. Salinas-Riester, M. Dettenhofer, H. Kang, L. Farinelli, W. Chen, A. Fischer, Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328, 753-756 (2010).
24. D. Vermaak, P. A. Wade, P. L. Jones, Y. B. Shi, A. P. Wolffe, Functional analysis of the SIN3-histone deacetylase RPD3-RbAp48-histone H4 connection in the Xenopus oocyte. Mol. Cell. Biol. 19, 5847-5860 (1999).
25. M. Mayford, M. E. Bach, Y. Y. Huang, L. Wang, R. D. Hawkins, E. R. Kandel, Control of memory formation through regulated expression of a CaMKII transgene. Science 274, 1678-1683 (1996).
26. S. M. Resnick, K. M. Trotman, C. Kawas, A. B. Zonderman, Age-associated changes in specific errors on the Benton Visual Retention Test. J. Gerontol. B Psychol. Sci. Soc. Sci. 50, P171-P178 (1995).
27. D. L. Schacter, L. A. Cooper, M. Valdiserri, Implicit and explicit memory for novel visual objects in older and younger adults. Psychol. Aging 7, 299-308 (1992).
28. C. L. Grady, A. R. McIntosh, B. Horwitz, J. M. Maisog, L. G. Ungerleider, M. J. Mentis, P. Pietrini, M. B. Schapiro, J. V. Haxby, Age-related reductions in human recognition memory due to impaired encoding. Science 269, 218-221 (1995).
29. M. B. Moss, D. L. Rosene, A. Peters, Effects of aging on visual recognition memory in the rhesus monkey. Neurobiol. Aging 9, 495-502 (1988).
30. P. R. Rapp, D. G. Amaral, Evidence for task-dependent memory dysfunction in the aged monkey. J. Neurosci. 9, 3568-3576 (1989).
31. C. A. Erickson, C. A. Barnes, The neurobiology of memory changes in normal aging. Exp. Gerontol. 38, 61-69 (2003).
32. E. Pavlopoulos, P. Trifilieff, V. Chevaleyre, L. Fioriti, S. Zairis, A. Pagano, G. Malleret, E. R. Kandel, Neuralized1 activates CPEB3: A function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell 147, 1369-1383 (2011).
33. N. J. Broadbent, S. Gaskin, L. R. Squire, R. E. Clark, Object recognition memory and the rodent hippocampus. Learn. Mem. 17, 5-11 (2010).
34. F. Pacifico, M. Paolillo, G. Chiappetta, E. Crescenzi, S. Arena, A. Scaloni, M. Monaco, C. Vascotto, G. Tell, S. Formisano, A. Leonardi, RbAp48 is a target of nuclear factor-kB activity in thyroid cancer. J. Clin. Endocrinol. Metab. 92, 1458-1466 (2007).
35. L. Kong, X. P. Yu, X. H. Bai, W. F. Zhang, Y. Zhang, W. M. Zhao, J. H. Jia, W. Tang, Y. B. Zhou, C. J. Liu, RbAp48 is a critical mediator controlling the transforming activity of human papillomavirus type 16 in cervical cancer. J. Biol. Chem. 282, 26381-26391 (2007).
36. R. G. Morris, P. Garrud, J. N. Rawlins, J. O'Keefe, Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683 (1982).
37. J. R. Keith, Y. Wu, J. R. Epp, R. J. Sutherland, Fluoxetine and the dentate gyrus: Memory, recovery of function, and electrophysiology. Behav. Pharmacol. 18, 521-531 (2007).
38. N. Sumien, M. N. Sims, H. J. Taylor, M. J. Forster, Profiling psychomotor and cognitive aging in four-way cross mice. Age 28, 265-282 (2006).
39. M. Verbitsky, A. L. Yonan, G. Malleret, E. R. Kandel, T. C. Gilliam, P. Pavlidis, Altered hippocampal transcript profile accompanies an age-related spatial memory deficit in mice. Learn. Mem. 11, 253-260 (2004).
40. W. Lin, A. Celik, R. P. Paczynski, Regional cerebral blood volume: A comparison of the dynamic imaging and the steady state methods. J. Magn. Reson. Imaging 9, 44-52 (1999).
41. I. Gaisler-Salomon, G. M. Miller, N. Chuhma, S. Lee, H. Zhang, F. Ghoddoussi, N. Lewandowski, S. Fairhurst, Y. Wang, A. Conjard-Duplany, J. Masson, P. Balsam, R. Hen, O. Arancio, M. P. Galloway, H. M. Moore, S. A. Small, S. Rayport, Glutaminase-deficient mice display hippocampal hypoactivity, insensitivity to pro-psychotic drugs and potentiated latent inhibition: Relevance to schizophrenia. Neuropsychopharmacology 34, 2305-2322 (2009).
42. W. Wu, S. A. Small, Imaging the earliest stages of Alzheimer's disease. Curr. Alzheimer Res. 3, 529-539 (2006).
43. Y. J. Chen, M. A. Johnson, M. D. Lieberman, R. E. Goodchild, S. Schobel, N. Lewandowski, G. Rosoklija, R. C. Liu, J. A. Gingrich, S. Small, H. Moore, A. J. Dwork, D. A. Talmage, L. W. Role, Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components. J. Neurosci. 28, 6872-6883 (2008).
44. L. M. Valor, M. M. Pulopulos, M. Jimenez-Minchan, R. Olivares, B. Lutz, A. Barco, Ablation of CBP in forebrain principal neurons causes modest memory and transcriptional defects and a dramatic reduction of histone acetylation but does not affect cell viability. J. Neurosci. 31, 1652-1663 (2011).
45. A. Cvekl, M. K. Duncan, Genetic and epigenetic mechanisms of gene regulation during lens development. Prog. Retin. Eye Res. 26, 555-597 (2007).
46. A. Sahay, K. N. Scobie, A. S. Hill, C. M. O'Carroll, M. A. Kheirbek, N. S. Burghardt, A. A. Fenton, A. Dranovsky, R. Hen, Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466-470 (2011).
47. N. C. Berchtold, D. H. Cribbs, P. D. Coleman, J. Rogers, E. Head, R. Kim, T. Beach, C. Miller, J. Troncoso, J. Q. Trojanowski, H. R. Zielke, C. W. Cotman, Gene expression changes in the course of normal brain aging are sexually dimorphic. Proc. Natl. Acad. Sci. U.S.A. 105, 15605-15610 (2008).
48. M. E. Bach, M. Barad, H. Son, M. Zhuo, Y. F. Lu, R. Shih, I. Mansuy, R. D. Hawkins, 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, 5280-5285 (1999).
49. A. J. Silva, E. M. Simpson, J. S. Takahashi, H.-P. Lipp, S. Nakanishi, J. M. Wehner, K. P. Giese, T. Tully, T. Abel, P. F. Chapman, K. Fox, S. Grant, S. Itohara, R. Lathe, M. Mayford, J. O. McNamara, R. J. Morris, M. Picciotto, J. Roder, H.-S. Shin, P. A. Slesinger, D. R. Storm, M. P. Stryker, S. Tonegawa, Y. Wang, D. P. Wolfer, Mutant mice and neuroscience: Recommendations concerning genetic background. Banbury Conference on Genetic Background in Mice. Neuron 19, 755-759 (1997).
50. M. J. Hawrylycz, E. S. Lein, A. L. Guillozet-Bongaarts, E. H. Shen, L. Ng, J. A. Miller, L. N. van de Lagemaat, K. A. Smith, A. Ebbert, Z. L. Riley, C. Abajian, C. F. Beckmann, A. Bernard, D. Bertagnolli, A. F. Boe, P. M. Cartagena, M. M. Chakravarty, M. Chapin, J. Chong, R. A. Dalley, B. D. Daly, C. Dang, S. Datta, N. Dee, T. A. Dolbeare, V. Faber, D. Feng, D. R. Fowler, J. Goldy, B. W. Gregor, Z. Haradon, D. R. Haynor, J. G. Hohmann, S. Horvath, R. E. Howard, A. Jeromin, J. M. Jochim, M. Kinnunen, C. Lau, E. T. Lazarz, C. Lee, T. A. Lemon, L. Li, Y. Li, J. A. Morris, C. C. Overly, P. D. Parker, S. E. Parry, M. Reding, J. J. Royall, J. Schulkin, P. A. Sequeira, C. R. Slaughterbeck, S. C. Smith, A. J. Sodt, S. M. Sunkin, B. E. Swanson, M. P. Vawter, D. Williams, P. Wohnoutka, H. R. Zielke, D. H. Geschwind, P. R. Hof, S. M. Smith, C. Koch, S. G. Grant, A. R. Jones, An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489, 391-399 (2012).
51. E. Pavlopoulos, S. Jones, S. Kosmidis, M. Close, C. Kim, O. Kovalerchik, S. A. Small, E. R. Kandel, Molecular mechanism for age-related memory loss: The histone-binding protein RbAp48. Sci. Transl. Med. 5, 200ra115 (2013).