Proteomic analysis of the dorsal and ventral hippocampus of rats maintained on a high fat and refined sugar diet

Proteomics

Volumn 13, Issue 20, 2013, Pages 3076-3091

  Francis, Heather M ^a   Mirzaei, Mehdi ^a   Pardey, Margery C ^a   Haynes, Paul A ^a   Cornish, Jennifer L ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

Animal proteomics; Diet; Fat; Label free quantitative proteomics; Nanoflow LC MS MS; Sugar

Indexed keywords

ADENOSINE KINASE; ALPHA CATENIN; ALPHA TROPOMYOSIN; BETA TUBULIN; CALBINDIN; CASEIN KINASE II; CASEIN KINASE IIALPHA; CELL ADHESION MOLECULE; CLAUDIN; CLAUDIN 10; CULLIN; CULLIN 3; CYSTATIN B; FOCAL ADHESION KINASE 1; GLUTAMINASE; INITIATION FACTOR 5A; ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE 2; LAMIN A; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN 6; NITRILASE; PARVALBUMIN; PROFILIN; RETINOL DEHYDROGENASE; RETINOL DEHYDROGENASE 11; SEPTIN; SEPTIN 8; SYNAPTOPHYSIN; UBIQUINONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BIOSYNTHESIS; BODY WEIGHT; CALCIUM SIGNALING; CALORIC INTAKE; CELL FUNCTION; CELL INTERACTION; CITRIC ACID CYCLE; CONTROLLED STUDY; DIETARY INTAKE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DORSAL HIPPOCAMPUS; DOWN REGULATION; ENERGY METABOLISM; HIPPOCAMPUS; LEARNING; LIPID DIET; MALE; MAZE TEST; MEMORY; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RAT; RECOGNITION; REINFORCEMENT; SIGNAL TRANSDUCTION; TASK PERFORMANCE; UBIQUITINATION; UPREGULATION; VENTRAL HIPPOCAMPUS;

ANIMAL PROTEOMICS; DIET; FAT; LABEL-FREE QUANTITATIVE PROTEOMICS; NANOFLOW LC-MS/MS; SUGAR;

ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; CONDITIONING, OPERANT; DIET, HIGH-FAT; DIETARY CARBOHYDRATES; ENERGY INTAKE; ESCAPE REACTION; EXPLORATORY BEHAVIOR; EXTINCTION, PSYCHOLOGICAL; HIPPOCAMPUS; MALE; MAZE LEARNING; PROTEOLYSIS; PROTEOME; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84885392794     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201300124     Document Type: Article

References (103)

1. Scoville, W. B., Milner, B., Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 1957, 20, 11-21.
2. Squire, L. R., Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 1992, 99, 195-231.
3. Tulving, E., Markowitsch, H. J., Episodic and declarative memory: role of the hippocampus. Hippocampus 1998, 8, 198-204.
4. Jarrard, L. E., Selective hippocampal lesions: differential effects on performance by rats of a spatial task with preoperative versus postoperative training. J. Comp. Physiol. Psychol. 1978, 92, 1119-1127.
5. Morris, R. G., Garrud, P., Rawlins, J. N., O'Keefe, J., Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297, 681-683.
6. Francis, H. M., Stevenson, R. J., Higher reported saturated fat and refined sugar intake is associated with reduced hippocampal-dependent memory and sensitivity to interoceptive signals. Behav. Neurosci. 2011, 125, 943-955.
7. Eskelinen, M. H., Ngandu, T., Helkala, E. L., Tuomilehto, J. etal., Fat intake at midlife and cognitive impairment later in life: a population-based CAIDE study. Int. J. Geriatr. Psychiatry 2008, 23, 741-747.
8. Knopman, D., Boland, L. L., Mosley, T., Howard, G. etal., Cardiovascular risk factors and cognitive decline in middle-aged adults. Neurology 2001, 56, 42-48.
9. Kalmijn, S., Launer, L. J., Ott, A., Witteman, J. C. etal., Dietary fat intake and the risk of incident dementia in the Rotterdam Study. Ann. Neurol. 1997, 42, 776-782.
10. Grant, W. B., Campbell, A., Itzhaki, R. F., Savory, J., The significance of environmental factors in the etiology of Alzheimer's disease. J. Alzheimers Dis. 2002, 4, 179-189.
11. Morris, M. C., Evans, D. A., Bienias, J. L., Tangney, C. C. etal., Dietary fats and the risk of incident Alzheimer disease. Arch. Neurol. 2003, 60, 194-200.
12. Molteni, R., Barnard, R. J., Ying, Z., Roberts, C. K., Gomez-Pinilla, F., A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 2002, 112, 803-814.
13. Valladolid-Acebes, I., Stucchi, P., Cano, V., Fernandez-Alfonso, M. S. etal., High-fat diets impair spatial learning in the radial-arm maze in mice. Neurobiol. Learn Mem. 2011, 95, 80-85.
14. Kanoski, S. E., Davidson, T. L., Different patterns of memory impairments accompany short- and longer-term maintenance on a high-energy diet. J. Exp. Psychol. Anim. Behav. Process 2010, 36, 313-319.
15. Greenwood, C. E., Winocur, G., Learning and memory impairment in rats fed a high saturated fat diet. Behav. Neural. Biol. 1990, 53, 74-87.
16. Jurdak, N., Kanarek, R. B., Sucrose-induced obesity impairs novel object recognition learning in young rats. Physiol. Behav. 2009, 96, 1-5.
17. Kanoski, S. E., Meisel, R. L., Mullins, A. J., Davidson, T. L., The effects of energy-rich diets on discrimination reversal learning and on BDNF in the hippocampus and prefrontal cortex of the rat. Behav. Brain Res. 2007, 182, 57-66.
18. Dillon, G. M., Qu, X., Marcus, J. N., Dodart, J. C., Excitotoxic lesions restricted to the dorsal CA1 field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice. Neurobiol. Learn Mem. 2008, 90, 426-433.
19. Winocur, G., Olds, J., Effects of context manipulation on memory and reversal learning in rats with hippocampal lesions. J. Comp. Physiol. Psychol. 1978, 92, 312-321.
20. Linnarsson, S., Bjorklund, A., Ernfors, P., Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 1997, 9, 2581-2587.
21. Wu, A., Ying, Z., Gomez-Pinilla, F., The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. Eur. J. Neurosci. 2004, 19, 1699-1707.
22. Souza, C. G., Moreira, J. D., Siqueira, I. R., Pereira, A. G. etal., Highly palatable diet consumption increases protein oxidation in rat frontal cortex and anxiety-like behavior. Life Sci. 2007, 81, 198-203.
23. Jurdak, N., Lichtenstein, A. H., Kanarek, R. B., Diet-induced obesity and spatial cognition in young male rats. Nutr. Neurosci. 2008, 11, 48-54.
24. Messier, C., Whately, K., Liang, J., Du, L., Puissant, D., The effects of a high-fat, high-fructose, and combination diet on learning, weight, and glucose regulation in C57BL/6 mice. Behav. Brain Res. 2007, 178, 139-145.
25. Nishikawa, T., Edelstein, D., Du, X. L., Yamagishi, S. etal., Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404, 787-790.
26. Thompson, C. L., Pathak, S. D., Jeromin, A., Ng, L. L. etal., Genomic anatomy of the hippocampus. Neuron 2008, 60, 1010-1021.
27. Dong, H. W., Swanson, L. W., Chen, L., Fanselow, M. S., Toga, A. W., Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. USA 2009, 106, 11794-11799.
28. Fanselow, M. S., Dong, H. W., Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 2010, 65, 7-19.
29. Pardey, M. C., Homewood, J., Taylor, A., Cornish, J. L., Re-evaluation of an animal model for ADHD using a free-operant choice task. J. Neurosci. Methods 2009, 176, 166-171.
30. Gammulla, C. G., Pascovici, D., Atwell, B. J., Haynes, P. A., Differential metabolic response of cultured rice (Oryza sativa) cells exposed to high- and low-temperature stress. Proteomics 2010, 10, 3001-3019.
31. Mirzaei, M., Soltani, N., Sarhadi, E., Pascovici, D. etal., Shotgun proteomic analysis of long-distance drought signaling in rice roots. J. Proteome Res. 2012, 11, 348-358.
32. Mirzaei, M., Pascovici, D., Atwell, B. J., Haynes, P. A., Differential regulation of aquaporins, small GTPases and V-ATPases proteins in rice leaves subjected to drought stress and recovery. Proteomics 2012, 12, 864-877.
33. Voelckel, C., Mirzaei, M., Reichelt, M., Luo, Z. etal., Transcript and protein profiling identify candidate gene sets of potential adaptive significance in New Zealand Pachycladon. BMC Evol. Biol. 2010, 10, 151.
34. Zybailov, B., Mosley, A. L., Sardiu, M. E., Coleman, M. K. etal., Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 2006, 5, 2339-2347.
35. Neilson, K. A., Ali, N. A., Muralidharan, S., Mirzaei, M. etal., Less label, more free: approaches in label-free quantitative mass spectrometry. Proteomics 2011, 11, 535-553.
36. Mirzaei, M., Pascovici, D., Keighley, T., George, I. etal., Shotgun proteomic profiling of five species of New Zealand Pachycladon. Proteomics 2011, 11, 166-171.
37. Neilson, K. A., Keighley, T., Pascovici, D., Cooke, B., Haynes, P. A., Label-free quantitative shotgun proteomics using normalized spectral abundance factors. Methods Mol. Biol. 2013, 1002, 205-222.
38. Kanoski, S. E., Zhang, Y., Zheng, W., Davidson, T. L., The effects of a high-energy diet on hippocampal function and blood-brain barrier integrity in the rat. J. Alzheimers Dis. 2010, 21, 207-219.
39. Stranahan, A. M., Norman, E. D., Lee, K., Cutler, R. G. etal., Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 2008, 18, 1085-1088.
40. Avena, N. M., Hoebel, B. G., A diet promoting sugar dependency causes behavioral cross-sensitization to a low dose of amphetamine. Neuroscience 2003, 122, 17-20.
41. Lindqvist, A., Mohapel, P., Bouter, B., Frielingsdorf, H. etal., High-fat diet impairs hippocampal neurogenesis in male rats. Eur. J. Neurol. 2006, 13, 1385-1388.
42. Nguyen JCD, Bongiorno, D., Killcross, A. S., Jenkins, T. A. (Eds.), Effect of Western diet Consumption on Spatial Alternation and Brain Serotonin Measures in the Rat, Australian Neuroscience Society, Melbourne, Australia 2013.
43. Mielke, J. G., Nicolitch, K., Avellaneda, V., Earlam, K. etal., Longitudinal study of the effects of a high-fat diet on glucose regulation, hippocampal function, and cerebral insulin sensitivity in C57BL/6 mice. Behav. Brain Res. 2006, 175, 374-382.
44. la Fleur, S. E., Vanderschuren, L. J., Luijendijk, M. C., Kloeze, B. M. etal., A reciprocal interaction between food-motivated behavior and diet-induced obesity. Int. J. Obes. (Lond). 2007, 31, 1286-1294.
45. Davis, J. F., Tracy, A. L., Schurdak, J. D., Tschop, M. H. etal., Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav. Neurosci. 2008, 122, 1257-1263.
46. Sclafani, A., Springer, D., Dietary obesity in adult rats: similarities to hypothalamic and human obesity syndromes. Physiol. Behav. 1976, 17, 461-471.
47. Dheilly, N. M., Haynes, P. A., Raftos, D. A., Nair, S. V., Time course proteomic profiling of cellular responses to immunological challenge in the sea urchin, Heliocidaris erythrogramma. Dev. Comp. Immunol. 2012, 37, 243-256.
48. Lee, A., Chick, J. M., Kolarich, D., Haynes, P. A. etal., Liver membrane proteome glycosylation changes in mice bearing an extra-hepatic tumor. Mol. Cell Proteomics. 2011, 10, M900538MCP200.
49. Thompson, E. L., Taylor, D. A., Nair, S. V., Birch, G. etal., A proteomic analysis of the effects of metal contamination on Sydney Rock Oyster (Saccostrea glomerata) haemolymph. Aquat. Toxicol. 2011, 103, 241-249.
50. Pascovici, D., Keighley, T., Mirzaei, M., Haynes, P. A., Cooke, B., PloGO: plotting gene ontology annotation and abundance in multi-condition proteomics experiments. Proteomics 2012, 12, 406-410.
51. Koizumi, S., Rosa, P., Willars, G. B., Challiss, R. A. etal., Mechanisms underlying the neuronal calcium sensor-1-evoked enhancement of exocytosis in PC12 cells. J. Biol. Chem. 2002, 277, 30315-30324.
52. Takida, S., Elmquist, B. J., Trachte, G. J., C-type natriuretic peptide attenuates evoked dopamine efflux by influencing Goalpha. Hypertension 1999, 33, 124-129.
53. Icard-Liepkalns, C., Ravassard, P., Liepkalns, V. A., Chatail, F., Mallet, J., An ADP-ribosylation-factor(ARF)-like protein involved in regulated secretion. Eur. J. Biochem. 1997, 246, 388-393.
54. Ragozzino, M. E., Unick, K. E., Gold, P. E., Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc. Natl. Acad. Sci. USA 1996, 93, 4693-4698.
55. Izquierdo, I., Medina, J. H., Memory formation: The sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn Mem. 1997, 68, 285-316.
56. Jerusalinsky, D., Kornisiuk, E., Izquierdo, I., Cholinergic neurotransmission and synaptic plasticity concerning memory processing. Neurochem. Res. 1997, 22, 507-515.
57. Huang, X. F., Zavitsanou, K., Huang, X., Yu, Y. etal., Dopamine transporter and D2 receptor binding densities in mice prone or resistant to chronic high fat diet-induced obesity. Behav. Brain Res. 2006, 175, 415-419.
58. South, T., Huang, X. F., High-fat diet exposure increases dopamine D2 receptor and decreases dopamine transporter receptor binding density in the nucleus accumbens and caudate putamen of mice. Neurochem. Res. 2008, 33, 598-605.
59. Chen, Y., Yang, Z., Meng, M., Zhao, Y. etal., Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement. Mol. Cell. 2009, 35, 841-855.
60. Bitko, V., Oldenburg, A., Garmon, N. E., Barik, S., Profilin is required for viral morphogenesis, syncytium formation, and cell-specific stress fiber induction by respiratory syncytial virus. BMC Microbiol. 2003, 3:9.
61. Avalos, A. M., Arthur, W. T., Schneider, P., Quest, A. F. etal., Aggregation of integrins and RhoA activation are required for Thy-1-induced morphological changes in astrocytes. J. Biol. Chem. 2004, 279, 39139-39145.
62. Vanhauwe, J. F., Thomas, T. O., Minshall, R. D., Tiruppathi, C. etal., Thrombin receptors activate G(o) proteins in endothelial cells to regulate intracellular calcium and cell shape changes. J. Biol. Chem. 2002, 277, 34143-34119.
63. Round, J. L., Tomassian, T., Zhang, M., Patel, V. etal., Dlgh1 coordinates actin polymerization, synaptic T cell receptor and lipid raft aggregation, and effector function in T cells. J. Exp. Med. 2005, 201, 419-430.
64. Shah, V., Bharadwaj, S., Kaibuchi, K., Prasad, G. L., Cytoskeletal organization in tropomyosin-mediated reversion of ras-transformation: evidence for Rho kinase pathway. Oncogene 2001, 20, 2112-2121.
65. Lamprecht, R., LeDoux, J., Structural plasticity and memory. Nat. Rev. Neurosci. 2004, 5, 45-54.
66. Matus, A., Actin-based plasticity in dendritic spines. Science 2000, 290, 754-758.
67. Kim, C. H., Lisman, J. E., A role of actin filament in synaptic transmission and long-term potentiation. J. Neurosci. 1999, 19, 4314-4324.
68. Krucker, T., Siggins, G. R., Halpain, S., Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc. Natl. Acad. Sci. USA 2000, 97, 6856-6861.
69. Zafra, F., Lindholm, D., Castren, E., Hartikka, J., Thoenen, H., Regulation of brain-derived neurotrophic factor and nerve growth factor mRNA in primary cultures of hippocampal neurons and astrocytes. J. Neurosci. 1992, 12, 4793-4799.
70. Takeuchi, Y., Yamamoto, H., Miyakawa, T., Miyamoto, E., Increase of brain-derived neurotrophic factor gene expression in NG108-15 cells by the nuclear isoforms of Ca2+/calmodulin-dependent protein kinase II. J. Neurochem. 2000, 74, 1913-1922.
71. Kamata, A., Takeuchi, Y., Fukunaga, K., Identification of the isoforms of Ca2+/calmodulin-dependent protein kinase II and expression of brain-derived neurotrophic factor mRNAs in the substantia nigra. J. Neurochem. 2006, 96, 195-203.
72. Malinow, R., Malenka, R. C., AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 2002, 25, 103-126.
73. Caldeira, M. V., Melo, C. V., Pereira, D. B., Carvalho, R. F. etal., BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol. Cell Neurosci. 2007, 35, 208-219.
74. Foster, T. C., Sharrow, K. M., Masse, J. R., Norris, C. M., Kumar, A., Calcineurin links Ca2 +dysregulation with brain aging. J. Neurosci. 2001, 21, 4066-4073.
75. Thibault, O., Porter, N. M., Chen, K. C., Blalock, E. M. etal., Calcium dysregulation in neuronal aging and Alzheimer's disease: history and new directions. Cell Calcium 1998, 24, 417-433.
76. LaFerla, F. M., Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat. Rev. Neurosci. 2002, 3, 862-872.
77. Senior, A. E., ATP synthesis by oxidative phosphorylation. Physiol. Rev. 1988, 68, 177-231.
78. Bowling, A. C., Mutisya, E. M., Walker, L. C., Price, D. L. etal., Age-dependent impairment of mitochondrial function in primate brain. J. Neurochem. 1993, 60, 1964-1967.
79. Mutisya, E. M., Bowling, A. C., Beal, M. F., Cortical cytochrome oxidase activity is reduced in Alzheimer's disease. J. Neurochem. 1994, 63, 2179-2184.
80. Valla, J., Schneider, L., Niedzielko, T., Coon, K. D. etal., Impaired platelet mitochondrial activity in Alzheimer's disease and mild cognitive impairment. Mitochondrion 2006, 6, 323-330.
81. Vaynman, S., Ying, Z., Wu, A., Gomez-Pinilla, F., Coupling energy metabolism with a mechanism to support brain-derived neurotrophic factor-mediated synaptic plasticity. Neuroscience 2006, 139, 1221-1234.
82. Ding, Q., Vaynman, S., Souda, P., Whitelegge, J. P., Gomez-Pinilla, F., Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis. Eur. J. Neurosci. 2006, 24, 1265-1276.
83. Santini, E., Muller, R. U., Quirk, G. J., Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. J. Neurosci. 2001, 21, 9009-9017.
84. Morris, R. G., Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J. Neurosci. 1989, 9, 3040-3057.
85. Verhage, M., Maia, A. S., Plomp, J. J., Brussaard, A. B. etal., Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000, 287, 864-869.
86. Leube, R. E., Expression of the synaptophysin gene family is not restricted to neuronal and neuroendocrine differentiation in rat and human. Differentiation 1994, 56, 163-171.
87. Wiedenmann, B., Franke, W. W., Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38, 000 characteristic of presynaptic vesicles. Cell 1985, 41, 1017-1028.
88. Tang, Y. P., Shimizu, E., Dube, G. R., Rampon, C. etal., Genetic enhancement of learning and memory in mice. Nature 1999, 401, 63-69.
89. Sandi, C., Davies, H. A., Cordero, M. I., Rodriguez, J. J. etal., Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. Eur. J. Neurosci. 2003, 17, 2447-2456.
90. De Bruin, J. P., Sanchez-Santed, F., Heinsbroek, R. P., Donker, A., Postmes, P., A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res. 1994, 652, 323-333.
91. Salazar, R. F., White, W., Lacroix, L., Feldon, J., White, I. M., NMDA lesions in the medial prefrontal cortex impair the ability to inhibit responses during reversal of a simple spatial discrimination. Behav. Brain Res. 2004, 152, 413-424.
92. Lee, M. K., Tuttle, J. B., Rebhun, L. I., Cleveland, D. W., Frankfurter, A., The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskeleton. 1990, 17, 118-132.
93. Park, S. Y., Avraham, H., Avraham, S., Characterization of the tyrosine kinases RAFTK/Pyk2 and FAK in nerve growth factor-induced neuronal differentiation. J. Biol. Chem. 2000, 275, 19768-19777.
94. Ivankovic-Dikic, I., Gronroos, E., Blaukat, A., Barth, B. U., Dikic, I., Pyk2 and FAK regulate neurite outgrowth induced by growth factors and integrins. Nat. Cell Biol. 2000, 2, 574-581.
95. Huang, Y., Lu, W., Ali, D. W., Pelkey, K. A. etal., CAKbeta/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 2001, 29, 485-496.
96. Choeiri, C., Staines, W., Messier, C., Immunohistochemical localization and quantification of glucose transporters in the mouse brain. Neuroscience 2002, 111, 19-34.
97. Hooijmans, C. R., Graven, C., Dederen, P. J., Tanila, H. etal., Amyloid beta deposition is related to decreased glucose transporter-1 levels and hippocampal atrophy in brains of aged APP/PS1 mice. Brain Res. 2007, 1181, 93-103.
98. Kiang, J. G., Tsokos, G. C., Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol. Ther. 1998, 80, 183-201.
99. Lenaz, G., Bovina, C., Castelluccio, C., Fato, R. etal., Mitochondrial complex I defects in aging. Mol. Cell Biochem. 1997, 174, 329-333.
100. Baloyannis, S. J., Costa, V., Michmizos, D., Mitochondrial alterations in Alzheimer's disease. Am. J. Alzheimers Dis. Other Demen. 2004, 19, 89-93.
101. Baloyannis, S. J., Mitochondrial alterations in neurons of various areas of the brain in Parkinson's disease: an electron microscopy study. Parkinsonism Related Disorders 2001, 7, S10-S17.
102. Calabrese, V., Scapagnini, G., Ravagna, A., Colombrita, C. etal., Increased expression of heat shock proteins in rat brain during aging: relationship with mitochondrial function and glutathione redox state. Mech. Ageing Dev. 2004, 125, 325-335.
103. Vizcaíno, J. A., Côté, R. G., Csordas, A., Dianes, J. A. etal., The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 2012, doi: 10.1093/nar/gks1262.