Deletion of the lifespan determinant p66Shc improves performance in a spatial memory task, decreases levels of oxidative stress markers in the hippocampus and increases levels of the neurotrophin BDNF in adult mice

Experimental Gerontology

Volumn 43, Issue 3, 2008, Pages 200-208

  Berry, A ^a,c   Greco, A ^a   Giorgio, M ^b   Pelicci, P G ^b   de Kloet, R ^c   Alleva, E ^a   Minghetti, L ^a   Cirulli, F ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Aging; Anxiety; BDNF; Mice; Morris water maze; Neurodegeneration; Open field; Oxidative stress; p66Shc; Pain sensitivity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIN; PROTEIN P66;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; COGNITION; CONTROLLED STUDY; GENE DELETION; HIPPOCAMPUS; LIFESPAN; MALE; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NOCICEPTION; NONHUMAN; OPEN FIELD TEST; OXIDATIVE STRESS; PAIN THRESHOLD; PHYSICAL PERFORMANCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPATIAL MEMORY; TAIL FLICK TEST; TASK PERFORMANCE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGING; ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MICE, KNOCKOUT; OXIDATIVE STRESS; PAIN; PAIN THRESHOLD; SIGNAL TRANSDUCTION; SPATIAL BEHAVIOR;

MUS;

EID: 39149141395     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2007.10.016     Document Type: Article

References (38)

1. Abidin I., Yargicoglu P., Agar A., Gumuslu S., Aydin S., Ozturk O., and Sahin E. The effect of chronic restraint stress on spatial learning and memory: relation to oxidant stress. Int. J. Neurosci. 114 (2004) 683-699
2. Balogh S.A., McDowell C.S., Stavnezer A.J., and Denenberg V.H. A behavioral and neuroanatomical assessment of an inbred substrain of 129 mice with behavioral comparisons to C57BL/6J mice. Brain Res. 836 (1999) 38-48
3. Berry A., Capone F., Giorgio M., Pelicci P.G., de Kloet E.R., Alleva E., Minghetti L., and Cirulli F. Deletion of the life span determinant p66Shc prevents age-dependent increases in emotionality and pain sensitivity in mice. Exp. Gerontol. 42 (2007) 37-45
4. Bert B., Fink H., Hortnagl H., Veh R.W., Davies B., Theuring F., and Kusserow H. Mice over-expressing the 5-HT(1A) receptor in cortex and dentate gyrus display exaggerated locomotor and hypothermic response to 8-OH-DPAT. Behav. Brain Res. 167 (2006) 328-341
5. Bimonte H.A., Nelson M.E., and Granholm A.C. Age-related deficits as working memory load increases: relationships with growth factors. Neurobiol. Aging 24 (2003) 37-48
6. Castren E., Voikar V., and Rantamaki T. Role of neurotrophic factors in depression. Curr. Opin. Pharmacol. 7 (2007) 18-21
7. Cattaneo E., and Pelicci P.G. Emerging roles for SH2/PTB-containing Shc adaptor proteins in the developing mammalian brain. Trends Neurosci. 21 (1998) 476-481
8. Chavko M., Auker C.R., and McCarron R.M. Relationship between protein nitration and oxidation and development of hyperoxic seizures. Nitric Oxide 9 (2003) 18-23
9. Cirulli F., Berry A., and Alleva E. Intracerebroventricular administration of brain-derived neurotrophic factor in adult rats affects analgesia and spontaneous behaviour but not memory retention in a Morris Water Maze task. Neurosci. Lett. 287 (2000) 207-210
10. Cirulli F., Berry A., Chiarotti F., and Alleva E. Intrahippocampal administration of BDNF in adult rats affects short-term behavioral plasticity in the Morris water maze and performance in the elevated plus-maze. Hippocampus 14 (2004) 802-807
11. Cirulli F., De Acetis L., and Alleva E. Pain assessment in rodents by standard laboratory techniques: an ethological perspective aimed at reducing suffering. In: Balls M., van Zeller A.-M., and Halder M. (Eds). Progress in the Reduction Refinement and Replacement of Animal Experimentation vol. 31B (2000), Elsevier 1127-1136
12. Coyle J.T., and Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science 262 (1993) 689-695
13. Crisp T., Minus T.O., Coleman M.L., Giles J.R., Cibula C., and Finnerty E.P. Aging, peripheral nerve injury and nociception: effects of the antioxidant 16-desmethyltirilazad. Behav. Brain Res. 166 (2006) 159-165
14. Durany N., Michel T., Kurt J., Cruz-Sanchez F.F., Cervas-Navarro J., and Riederer P. Brain-derived neurotrophic factor and neurotrophin-3 levels in Alzheimer's disease brains. Int. J. Dev. Neurosci. 18 (2000) 807-813
15. Finkel T., and Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 408 (2000) 239-247
16. Floyd R.A., and Hensley K. Oxidative stress in brain aging. Implications for therapeutics of neurodegenerative diseases. Neurobiol. Aging 23 (2002) 795-807
17. Francia P., delli Gatti C., Bachschmid M., Martin-Padura I., Savoia C., Migliaccio E., Pelicci P.G., Schiavoni M., Luscher T.F., Volpe M., and Cosentino F. Deletion of p66shc gene protects against age-related endothelial dysfunction. Circulation 110 (2004) 2889-2895
18. Giorgio M., Migliaccio E., Orsini F., Paolucci D., Moroni M., Contursi C., Pelliccia G., Luzi L., Minucci S., Marcaccio M., Pinton P., Rizzuto R., Bernardi P., Paolucci F., and Pelicci P.G. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122 (2005) 221-233
19. Hock C., Heese K., Hulette C., Rosenberg C., and Otten U. Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch. Neurol. 57 (2000) 846-851
20. King T.E., Joynes R.L., and Grau J.W. Tail-flick test: II. The role of supraspinal systems and avoidance learning. Behav. Neurosci. 111 (1997) 754-767
21. Liu J., and Mori A. Stress, aging, and brain oxidative damage. Neurochem. Res. 24 (1999) 1479-1497
22. Madrigal J.L., Garcia-Bueno B., Caso J.R., Perez-Nievas B.G., and Leza J.C. Stress-induced oxidative changes in brain. CNS Neurol. Disord. Drug Targets 5 (2006) 561-568
23. Martin-Iverson M.T., Todd K.G., and Altar C.A. Brain-derived neurotrophic factor and neurotrophin-3 activate striatal dopamine and serotonin metabolism and related behaviors: interactions with amphetamine. J. Neurosci. 14 (1994) 1262-1270
24. Mattson M.P., Maudsley S., and Martin B. BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 27 (2004) 589-594
25. Migliaccio E., Giorgio M., Mele S., Pelicci G., Reboldi P., Pandolfi P.P., Lanfrancone L., and Pelicci P.G. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402 (1999) 309-313
26. Minghetti L., Greco A., Cardone F., Puopolo M., Ladogana A., Almonti S., Cunningham C., Perry V.H., Pocchiari M., and Levi G. Increased brain synthesis of prostaglandin E2 and F2-isoprostane in human and experimental transmissible spongiform encephalopathies. J. Neuropathol. Exp. Neurol. 59 (2000) 866-871
27. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11 (1984) 47-60
28. Murer M.G., Yan Q., and Raisman-Vozari R. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog. Neurobiol. 63 (2001) 71-124
29. Napoli C., Martin-Padura I., de Nigris F., Giorgio M., Mansueto G., Somma P., Condorelli M., Sica G., De Rosa G., and Pelicci P. Deletion of the p66Shc longevity gene reduces systemic and tissue oxidative stress, vascular cell apoptosis, and early atherogenesis in mice fed a high-fat diet. Proc. Natl. Acad. Sci. USA 100 (2003) 2112-2116
30. Ogden C.A., Rich M.E., Schork N.J., Paulus M.P., Geyer M.A., Lohr J.B., Kuczenski R., and Niculescu A.B. Candidate genes, pathways and mechanisms for bipolar (manic-depressive) and related disorders: an expanded convergent functional genomics approach. Mol. Psychiatry 9 (2004) 1007-1029
31. Pellmar T.C., Hollinden G.E., and Sarvey J.M. Free radicals accelerate the decay of long-term potentiation in field CA1 of guinea-pig hippocampus. Neuroscience 44 (1991) 353-359
32. Siesjo B.K., Agardh C.D., and Bengtsson F. Free radicals and brain damage. Cerebrovasc. Brain Metab. Rev. 1 (1989) 165-211
33. Silva R.H., Abilio V.C., Takatsu A.L., Kameda S.R., Grassl C., Chehin A.B., Medrano W.A., Calzavara M.B., Registro S., Andersen M.L., Machado R.B., Carvalho R.C., Ribeiro Rde A., Tufik S., and Frussa-Filho R. Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacology 46 (2004) 895-903
34. Thoenen H. Neurotrophins and neuronal plasticity. Science 270 (1995) 593-598
35. Trinei M., Giorgio M., Cicalese A., Barozzi S., Ventura A., Migliaccio E., Milia E., Padura I.M., Raker V.A., Maccarana M., Petronilli V., Minucci S., Bernardi P., Lanfrancone L., and Pelicci P.G. A p53-p66Shc signalling pathway controls intracellular redox status, levels of oxidation-damaged DNA and oxidative stress-induced apoptosis. Oncogene 21 (2002) 3872-3878
36. Williams J.H., and Bliss T.V. An in vitro study of the effect of lipoxygenase and cyclo-oxygenase inhibitors of arachidonic acid on the induction and maintenance of long-term potentiation in the hippocampus. Neurosci. Lett. 107 (1989) 301-306
37. Wolfer D.P., Stagljar-Bozicevic M., Errington M.L., and Lipp H.P. Spatial memory and learning in transgenic mice: fact or artifact?. News Physiol. Sci. 13 (1998) 118-123
38. Yan Q., Rosenfeld R.D., Matheson C.R., Hawkins N., Lopez O.T., Bennett L., and Welcher A.A. Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience 78 (1997) 431-448