Young blood reverses age-related impairments in cognitive function and synaptic plasticity in mice

Nature Medicine

Volumn 20, Issue 6, 2014, Pages 659-663

  Villeda, Saul A ^a,b,c   Plambeck, Kristopher E ^a   Middeldorp, Jinte ^c   Castellano, Joseph M ^c   Mosher, Kira I ^c   Luo, Jian ^c   Smith, Lucas K ^a   Bieri, Gregor ^a,c   Lin, Karin ^a,b   Berdnik, Daniela ^c   Wabl, Rafael ^c   Udeochu, Joe ^a,b   Wheatley, Elizabeth G ^a,b   Zou, Bende ^d   Simmons, Danielle A ^c   Xie, Xinmin S ^d   Longo, Frank M ^c   Wyss Coray, Tony ^c,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d AfaSci Research Laboratory   (United States)

^e VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

ADULT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL DENSITY; COGNITION; COGNITIVE DEFECT; CONDITIONING; CONTROLLED STUDY; DENDRITIC SPINE; EXPOSURE; FEAR; GROUPS BY AGE; HIPPOCAMPUS; MEMORY; MICROARRAY ANALYSIS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OUTCOME ASSESSMENT; PARABIOSIS; PLASMA; PRIORITY JOURNAL; SPATIAL LEARNING;

ANIMALIA; MUS;

AGE FACTORS; AGING; ANIMALS; BLOOD TRANSFUSION; BLOTTING, WESTERN; CELL LINE; COGNITION DISORDERS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA PRIMERS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; NEURONAL PLASTICITY; PARABIOSIS; POLYMERASE CHAIN REACTION;

EID: 84902075251     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3569     Document Type: Article

References (35)

1. Hebert, L.E., Scherr, P.A., Bienias, J.L., Bennett, D.A. & Evans, D.A. Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch. Neurol. 60, 1119-1122 (2003). (Pubitemid 36975801)
2. Bishop, N.A., Lu, T. & Yankner, B.A. Neural mechanisms of ageing and cognitive decline. Nature 464, 529-535 (2010).
3. Hedden, T. & Gabrieli, J.D. Insights into the ageing mind: a view from cognitive neuroscience. Nat. Rev. Neurosci. 5, 87-96 (2004). (Pubitemid 38160284)
4. Raz, N., Gunning-Dixon, F.M., Head, D., Dupuis, J.H. & Acker, J.D. Neuroanatomical correlates of cognitive aging: evidence from structural magnetic resonance imaging. Neuropsychology 12, 95-114 (1998). (Pubitemid 28070401)
5. Mattson, M.P. & Magnus, T. Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 7, 278-294 (2006).
6. Rapp, P.R. & Heindel, W.C. Memory systems in normal and pathological aging. Curr. Opin. Neurol. 7, 294-298 (1994). (Pubitemid 24243731)
7. Andrews-Hanna, J.R. et al. Disruption of large-scale brain systems in advanced aging. Neuron 56, 924-935 (2007). (Pubitemid 350181355)
8. Scheff, S.W., Price, D.A., Schmitt, F.A., DeKosky, S.T. & Mufson, E.J. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 68, 1501-1508 (2007). (Pubitemid 46685921)
9. Nicholson, D.A., Yoshida, R., Berry, R.W., Gallagher, M. & Geinisman, Y. Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J. Neurosci. 24, 7648-7653 (2004). (Pubitemid 39186819)
10. Smith, T.D., Adams, M.M., Gallagher, M., Morrison, J.H. & Rapp, P.R. Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J. Neurosci. 20, 6587-6593 (2000).
11. Morrison, J.H. & Baxter, M.G. The ageing cortical synapse: hallmarks and implications for cognitive decline. Nat. Rev. Neurosci. 13, 240-250 (2012).
12. Villeda, S.A. et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477, 90-94 (2011).
13. Pavlopoulos, E. et al. Molecular mechanism for age-related memory loss: the histone-binding protein RbAp48. Sci. Transl. Med. 5, 200ra115 (2013).
14. Conboy, I.M. et al. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760-764 (2005). (Pubitemid 40292986)
15. Brack, A.S. et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807-810 (2007). (Pubitemid 47257918)
16. Ruckh, J.M. et al. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 10, 96-103 (2012).
17. Loffredo, F.S. et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell 153, 828-839 (2013).
18. Geinisman, Y., de Toledo-Morrell, L. & Morrell, F. Loss of perforated synapses in the dentate gyrus: morphological substrate of memory deficit in aged rats. Proc. Natl. Acad. Sci. USA 83, 3027-3031 (1986). (Pubitemid 16041794)
19. Rosenzweig, E.S. & Barnes, C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog. Neurobiol. 69, 143-179 (2003). (Pubitemid 36577321)
20. Small, S.A., Schobel, S.A., Buxton, R.B., Witter, M.P. & Barnes, C.A. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 12, 585-601 (2011).
21. Alberini, C.M. Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev. 89, 121-145 (2009).
22. Bliss, T.V. & Collingridge, G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39 (1993). (Pubitemid 23020772)
23. Frey, U. & Morris, R.G. Synaptic tagging and long-term potentiation. Nature 385, 533-536 (1997). (Pubitemid 27074671)
24. Jeong, H. et al. Sirt1 mediates neuroprotection from mutant huntingtin by activation of the TORC1 and CREB transcriptional pathway. Nat. Med. 18, 159-165 (2012).
25. Merrill, D.A., Karim, R., Darraq, M., Chiba, A.A. & Tuszynski, M.H. Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J. Comp. Neurol. 459, 201-207 (2003). (Pubitemid 36384320)
26. Bizon, J.L. & Gallagher, M. Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline. Eur. J. Neurosci. 18, 215-219 (2003). (Pubitemid 36920862)
27. Drapeau, E. et al. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl. Acad. Sci. USA 100, 14385-14390 (2003). (Pubitemid 37499246)
28. Smolinsky, A.N. et al. Analysis of grooming behavior and its utility in studying animal stress, anxiety, and depression. in Mouse Models of Mood and Anxiety Disorders (ed. Gould, T.) 21-36 (Humana Press, NY, 2009).
29. Gould, T.D. Mood and Anxiety Related Phenotypes in Mice: Characterization Using Behavioral Tests (Humana Press, New York, 2009).
30. Luo, J. et al. Glia-dependent TGF-β signaling, acting independently of the TH17 pathway, is critical for initiation of murine autoimmune encephalomyelitis. J. Clin. Invest. 117, 3306-3315 (2007). (Pubitemid 350096987)
31. Xie, X. & Smart, T.G. Modulation of long-term potentiation in rat hippocampal pyramidal neurons by zinc. Pflugers Arch. 427, 481-486 (1994). (Pubitemid 24219030)
32. Grimm, D. et al. In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J. Virol. 82, 5887-5911 (2008). (Pubitemid 351822263)
33. Xu, W. et al. Distinct neuronal coding schemes in memory revealed by selective erasure of fast synchronous synaptic transmission. Neuron 73, 990-1001 (2012).
34. Raber, J. et al. Irradiation enhances hippocampus-dependent cognition in mice deficient in extracellular superoxide dismutase. Hippocampus 21, 72-80 (2011).
35. Alamed, J., Wilcock, D.M., Diamond, D.M., Gordon, M.N. & Morgan, D. Two-day radial-arm water maze learning and memory task; robust resolution of amyloid-related memory deficits in transgenic mice. Nat. Protoc. 1, 1671-1679 (2006). (Pubitemid 46773288)