Hippocampal Gene Expression Meta-Analysis Identifies Aging and Age-Associated Spatial Learning Impairment (ASLI) Genes and Pathways

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Uddin, Raihan K ^a   Singh, Shiva M ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AGE ASSOCIATED SPATIAL LEARNING IMPAIRMENT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASLI GENE; CELL INTERACTION; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; DEGENERATIVE DISEASE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ASSOCIATION; HIPPOCAMPUS; LEARNING DISORDER; MALE; MEMORY DISORDER; META ANALYSIS (TOPIC); MICROARRAY ANALYSIS; MOLECULAR GENETICS; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NEUROLOGIC DISEASE; NONHUMAN; RAT; SIGNAL TRANSDUCTION;

AGING; ANIMALS; GENE EXPRESSION REGULATION; GENES; HIPPOCAMPUS; LEARNING DISORDERS; MEMORY DISORDERS; META-ANALYSIS AS TOPIC; MICROARRAY ANALYSIS; NEURONAL PLASTICITY; RATS;

EID: 84880418980     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069768     Document Type: Article

References (95)

1. Landfield PW, Thibault O, Mazzanti ML, Porter NM, Kerr DS, (1992) Mechanisms of neuronal death in brain aging and Alzheimer's disease: role of endocrine-mediated calcium dyshomeostasis. J Neurobiol 23: 1247-1260.
2. Tanzi RE, Bertram L, (2001) New frontiers in Alzheimer's disease genetics. Neuron 32: 181-184.
3. Mattson MP, Magnus T, (2006) Ageing and neuronal vulnerability. Nat Rev Neurosci 7: 278-294.
4. Burger C, Lopez MC, Feller JA, Baker HV, Muzyczka N, et al. (2007) Changes in transcription within the CA1 field of the hippocampus are associated with age-related spatial learning impairments. Neurobiol Learn Mem 87: 21-41.
5. Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, et al. (2010) Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328: 753-756.
6. Glorioso C, Oh S, Douillard GG, Sibille E, (2011) Brain molecular aging, promotion of neurological disease and modulation by Sirtuin5 longevity gene polymorphism. Neurobiol Dis 41: 279-290.
7. Morris RG, Garrud P, Rawlins JN, O'Keefe J, (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297: 681-683.
8. Burgess N, (2002) The hippocampus, space, and viewpoints in episodic memory. Q J Exp Psychol A 55: 1057-1080.
9. Verbitsky M, Yonan AL, Malleret G, Kandel ER, Gilliam TC, et al. (2004) Altered hippocampal transcript profile accompanies an age-related spatial memory deficit in mice. Learn Mem 11: 253-260.
10. Mesulam MM, (1999) Neuroplasticity failure in Alzheimer's disease: bridging the gap between plaques and tangles. Neuron 24: 521-529.
11. Small SA, Tsai WY, DeLaPaz R, Mayeux R, Stern Y, (2002) Imaging hippocampal function across the human life span: is memory decline normal or not? Ann Neurol 51: 290-295.
12. Pawlowski TL, Bellush LL, Wright AW, Walker JP, Colvin RA, et al. (2009) Hippocampal gene expression changes during age-related cognitive decline. Brain Res 1256: 101-110.
13. Lu T, Pan Y, Kao SY, Li C, Kohane I, et al. (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429: 883-891.
14. Glorioso C, Sibille E, (2011) Between destiny and disease: Genetics and molecular pathways of human central nervous system aging. Prog Neurobiol 93: 165-181.
15. Burger C, Lopez MC, Baker HV, Mandel RJ, Muzyczka N, (2008) Genome-wide analysis of aging and learning-related genes in the hippocampal dentate gyrus. Neurobiol Learn Mem 89: 379-396.
16. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to Meta-Analysis: Wiley. 421 p.
17. Li C, Wong W, (2001) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2: RESEARCH0032.
18. Bolstad BM, Collin F, Brettschneider J, Simpson K, Cope L, et al. (2005) Quality assessment of affymetrix GeneChip data. In: Gentleman R, Irizarry RA, Carey VJ, Dudoit S, Huber W, editors. Bioinformatics and computational biology solutions using R and Bioconductor. First ed. New York: Springer. 33-48.
19. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
20. Gautier L, Cope L, Bolstad BM, Irizarry RA, (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
21. Johnson WE, Li C, Rabinovic A, (2007) Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8: 118-127.
22. Chen C, Grennan K, Badner J, Zhang D, Gershon E, et al. (2011) Removing batch effects in analysis of expression microarray data: an evaluation of six batch adjustment methods. PLoS One 6: e17238.
23. Sirbu A, Ruskin HJ, Crane M, (2010) Cross-platform microarray data normalisation for regulatory network inference. PLoS One 5: e13822.
24. Ramasamy A, Mondry A, Holmes CC, Altman DG, (2008) Key issues in conducting a meta-analysis of gene expression microarray datasets. PLoS Med 5: e184.
25. Moreau Y, Aerts S, De Moor B, De Strooper B, Dabrowski M, (2003) Comparison and meta-analysis of microarray data: from the bench to the computer desk. Trends Genet 19: 570-577.
26. Cochran W (1937) Problems arising in the analysis of a series of similar experiments. J R Stat Soc: 102-118.
27. Fleiss JL (1993) The statistical basis of meta-analysis. Stat methods Med Res: 121-145.
28. Rhodes DR, Barrette TR, Rubin MA, Ghosh D, Chinnaiyan AM, (2002) Meta-analysis of microarrays: interstudy validation of gene expression profiles reveals pathway dysregulation in prostate cancer. Cancer Res 62: 4427-4433.
29. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B 57: 299-314.
30. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
31. Blalock EM, Chen KC, Sharrow K, Herman JP, Porter NM, et al. (2003) Gene microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment. J Neurosci 23: 3807-3819.
32. Rowe WB, Blalock EM, Chen KC, Kadish I, Wang D, et al. (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.
33. Kadish I, Thibault O, Blalock EM, Chen KC, Gant JC, et al. (2009) Hippocampal and cognitive aging across the lifespan: a bioenergetic shift precedes and increased cholesterol trafficking parallels memory impairment. J Neurosci 29: 1805-1816.
34. Goldstein DR, Guerra R (2010) A brief introduction to meta-analysis, genetics and genomics. In: Goldstein DR, Guerra R, editors. Meta-analysis and combining information in genetics and genomics: CRC Press. 3-20.
35. Leek JT, Scharpf RB, Bravo HC, Simcha D, Langmead B, et al. (2010) Tackling the widespread and critical impact of batch effects in high-throughput data. Nat Rev Genet 11: 733-739.
36. Donnelly N, Gorman AM, Gupta S, Samali A (2013) The eIF2alpha kinases: their structures and functions. Cell Mol Life Sci.
37. Ishii N, Takahashi T, Soroosh P, Sugamura K, (2010) OX40-OX40 ligand interaction in T-cell-mediated immunity and immunopathology. Adv Immunol 105: 63-98.
38. Cazander G, Jukema GN, Nibbering PH, (2012) Complement activation and inhibition in wound healing. Clin Dev Immunol 2012: 534291.
39. Maier M, Peng Y, Jiang L, Seabrook TJ, Carroll MC, et al. (2008) Complement C3 deficiency leads to accelerated amyloid beta plaque deposition and neurodegeneration and modulation of the microglia/macrophage phenotype in amyloid precursor protein transgenic mice. J Neurosci 28: 6333-6341.
40. Borghese F, Clanchy FI, (2011) CD74: an emerging opportunity as a therapeutic target in cancer and autoimmune disease. Expert Opin Ther Targets 15: 237-251.
41. Mihelic M, Dobersek A, Guncar G, Turk D, (2008) Inhibitory fragment from the p41 form of invariant chain can regulate activity of cysteine cathepsins in antigen presentation. J Biol Chem 283: 14453-14460.
42. Arnold AC, Gallagher PE, Diz DI, (2013) Brain renin-angiotensin system in the nexus of hypertension and aging. Hypertens Res 36: 5-13.
43. Moscarello MA, Mastronardi FG, Wood DD, (2007) The role of citrullinated proteins suggests a novel mechanism in the pathogenesis of multiple sclerosis. Neurochem Res 32: 251-256.
44. Wyeth MS, Zhang N, Houser CR, (2012) Increased cholecystokinin labeling in the hippocampus of a mouse model of epilepsy maps to spines and glutamatergic terminals. Neuroscience 202: 371-383.
45. Zwanzger P, Domschke K, Bradwejn J, (2012) Neuronal network of panic disorder: the role of the neuropeptide cholecystokinin. Depress Anxiety 29: 762-774.
46. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, et al. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261: 921-923.
47. Bu G, (2009) Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 10: 333-344.
48. Maeda S, Sahara N, Saito Y, Murayama S, Ikai A, et al. (2006) Increased levels of granular tau oligomers: an early sign of brain aging and Alzheimer's disease. Neurosci Res 54: 197-201.
49. O'Neill C, Kiely AP, Coakley MF, Manning S, Long-Smith CM, (2012) Insulin and IGF-1 signalling: longevity, protein homoeostasis and Alzheimer's disease. Biochem Soc Trans 40: 721-727.
50. Ferrari R, Moreno JH, Minhajuddin AT, O'Bryant SE, Reisch JS, et al. (2012) Implication of common and disease specific variants in CLU, CR1, and PICALM. Neurobiol Aging 33: 1846 e1847-1818.
51. Chen LH, Kao PY, Fan YH, Ho DT, Chan CS, et al. (2012) Polymorphisms of CR1, CLU and PICALM confer susceptibility of Alzheimer's disease in a southern Chinese population. Neurobiol Aging 33: 210 e211-217.
52. Shukla V, Skuntz S, Pant HC, (2012) Deregulated Cdk5 activity is involved in inducing Alzheimer's disease. Arch Med Res 43: 655-662.
53. Miller BC, Eckman EA, Sambamurti K, Dobbs N, Chow KM, et al. (2003) Amyloid-beta peptide levels in brain are inversely correlated with insulysin activity levels in vivo. Proc Natl Acad Sci U S A 100: 6221-6226.
54. Alzheimer's A, (2012) 2012 Alzheimer's disease facts and figures. 8, 131-168 (2012). Alzheimers Dement 8: 131-168.
55. Liu CC, Kanekiyo T, Xu H, Bu G (2013) Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat Rev Neurol.
56. Angelo M, Plattner F, Giese KP, (2006) Cyclin-dependent kinase 5 in synaptic plasticity, learning and memory. J Neurochem 99: 353-370.
57. Nalivaeva NN, Beckett C, Belyaev ND, Turner AJ, (2012) Are amyloid-degrading enzymes viable therapeutic targets in Alzheimer's disease? J Neurochem 120Suppl 1: 167-185.
58. Scotland PB, Heath JL, Conway AE, Porter NB, Armstrong MB, et al. (2012) The PICALM protein plays a key role in iron homeostasis and cell proliferation. PLoS One 7: e44252.
59. Xiao Q, Gil SC, Yan P, Wang Y, Han S, et al. (2012) Role of phosphatidylinositol clathrin assembly lymphoid-myeloid leukemia (PICALM) in intracellular amyloid precursor protein (APP) processing and amyloid plaque pathogenesis. J Biol Chem 287: 21279-21289.
60. Lin JF, Pan HC, Ma LP, Shen YQ, Schachner M, (2012) The cell neural adhesion molecule contactin-2 (TAG-1) is beneficial for functional recovery after spinal cord injury in adult zebrafish. PLoS One 7: e52376.
61. Derfuss T, Parikh K, Velhin S, Braun M, Mathey E, et al. (2009) Contactin-2/TAG-1-directed autoimmunity is identified in multiple sclerosis patients and mediates gray matter pathology in animals. Proc Natl Acad Sci U S A 106: 8302-8307.
62. He HJ, Wang Y, Le Y, Duan KM, Yan XB, et al. (2012) Surgery upregulates high mobility group box-1 and disrupts the blood-brain barrier causing cognitive dysfunction in aged rats. CNS Neurosci Ther 18: 994-1002.
63. Klune JR, Dhupar R, Cardinal J, Billiar TR, Tsung A, (2008) HMGB1: endogenous danger signaling. Mol Med 14: 476-484.
64. Romaniello R, Tonelli A, Arrigoni F, Baschirotto C, Triulzi F, et al. (2012) A novel mutation in the beta-tubulin gene TUBB2B associated with complex malformation of cortical development and deficits in axonal guidance. Dev Med Child Neurol 54: 765-769.
65. Cushion TD, Dobyns WB, Mullins JG, Stoodley N, Chung SK, et al. (2013) Overlapping cortical malformations and mutations in TUBB2B and TUBA1A. Brain 136: 536-548.
66. Bartus K, Pigott B, Garthwaite J, (2013) Cellular targets of nitric oxide in the hippocampus. PLoS One 8: e57292.
67. Shen F, Li YJ, Shou XJ, Cui CL, (2012) Role of the NO/sGC/PKG signaling pathway of hippocampal CA1 in morphine-induced reward memory. Neurobiol Learn Mem 98: 130-138.
68. Menard C, Quirion R, (2012) Group 1 metabotropic glutamate receptor function and its regulation of learning and memory in the aging brain. Front Pharmacol 3: 182.
69. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, et al. (2010) The Arc of synaptic memory. Exp Brain Res 200: 125-140.
70. Shepherd JD, Bear MF, (2011) New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14: 279-284.
71. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, et al. (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52: 437-444.
72. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, et al. (2000) Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20: 3993-4001.
73. Timofeeva OA, Eddins D, Yakel JL, Blackshear PJ, Levin ED, (2010) Hippocampal infusions of MARCKS peptides impair memory of rats on the radial-arm maze. Brain Res 1308: 147-152.
74. Gay EA, Klein RC, Melton MA, Blackshear PJ, Yakel JL, (2008) Inhibition of native and recombinant nicotinic acetylcholine receptors by the myristoylated alanine-rich C kinase substrate peptide. J Pharmacol Exp Ther 327: 884-890.
75. Park H, Poo MM, (2013) Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 14: 7-23.
76. Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, et al. (2011) A critical role for IGF-II in memory consolidation and enhancement. Nature 469: 491-497.
77. Osterwalder T, Contartese J, Stoeckli ET, Kuhn TB, Sonderegger P, (1996) Neuroserpin, an axonally secreted serine protease inhibitor. EMBO J 15: 2944-2953.
78. Lee TW, Coates LC, Birch NP, (2008) Neuroserpin regulates N-cadherin-mediated cell adhesion independently of its activity as an inhibitor of tissue plasminogen activator. J Neurosci Res 86: 1243-1253.
79. Monfort P, Munoz MD, Kosenko E, Llansola M, Sanchez-Perez A, et al. (2004) Sequential activation of soluble guanylate cyclase, protein kinase G and cGMP-degrading phosphodiesterase is necessary for proper induction of long-term potentiation in CA1 of hippocampus. Alterations in hyperammonemia. Neurochem Int 45: 895-901.
80. Poulin P, Pittman QJ, (1993) Arginine vasopressin-induced sensitization in brain: facilitated inositol phosphate production without changes in receptor number. J Neuroendocrinol 5: 23-31.
81. Montmayeur JP, Barr TP, Kam SA, Packer SJ, Strichartz GR, (2011) ET-1 induced Elevation of intracellular calcium in clonal neuronal and embryonic kidney cells involves endogenous endothelin-A receptors linked to phospholipase C through Galpha(q/11). Pharmacol Res 64: 258-267.
82. Roesler R, Schwartsmann G, (2012) Gastrin-releasing peptide receptors in the central nervous system: role in brain function and as a drug target. Front Endocrinol (Lausanne) 3: 159.
83. Smogorzewski M, Islam A, (1995) Parathyroid hormone stimulates the generation of inositol 1,4,5-triphosphate in brain synaptosomes. Am J Kidney Dis 26: 814-817.
84. Ramsdell JS, Tashjian AH Jr, (1986) Thyrotropin-releasing hormone (TRH) elevation of inositol trisphosphate and cytosolic free calcium is dependent on receptor number. Evidence for multiple rapid interactions between TRH and its receptor. J Biol Chem 261: 5301-5306.
85. Ebstein RP, Knafo A, Mankuta D, Chew SH, Lai PS, (2012) The contributions of oxytocin and vasopressin pathway genes to human behavior. Horm Behav 61: 359-379.
86. Finch EA, Augustine GJ, (1998) Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396: 753-756.
87. Foster TC, (2012) Dissecting the age-related decline on spatial learning and memory tasks in rodent models: N-methyl-D-aspartate receptors and voltage-dependent Ca2+ channels in senescent synaptic plasticity. Prog Neurobiol 96: 283-303.
88. Daniels MP, (2012) The role of agrin in synaptic development, plasticity and signaling in the central nervous system. Neurochem Int 61: 848-853.
89. Kenwrick S, Watkins A, De Angelis E, (2000) Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum Mol Genet 9: 879-886.
90. Maness PF, Schachner M, (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10: 19-26.
91. Poplawski GH, Tranziska AK, Leshchyns'ka I, Meier ID, Streichert T, et al. (2012) L1CAM increases MAP2 expression via the MAPK pathway to promote neurite outgrowth. Mol Cell Neurosci 50: 169-178.
92. Iida Y, Yamamori S, Itakura M, Miyaoka H, Takahashi M (2013) Protein phosphatase 2A dephosphorylates SNAP-25 through two distinct mechanisms in mouse brain synaptosomes. Neurosci Res.
93. Genoud S, Pralong W, Riederer BM, Eder L, Catsicas S, et al. (1999) Activity-dependent phosphorylation of SNAP-25 in hippocampal organotypic cultures. J Neurochem 72: 1699-1706.
94. Sass B, Rabstein LS, Madison R, Nims RM, Peters RL, et al. (1975) Incidence of spontaneous neoplasms in F344 rats throughout the natural life-span. J Natl Cancer Inst 54: 1449-1456.
95. Coleman GL, Barthold W, Osbaldiston GW, Foster SJ, Jonas AM, (1977) Pathological changes during aging in barrier-reared Fischer 344 male rats. J Gerontol 32: 258-278.