Homer-1a immediate early gene expression correlates with better cognitive performance in aging

Age

Volumn 35, Issue 5, 2013, Pages 1799-1808

  Kaja, Simon ^a   Sumien, Nathalie ^b   Borden, Priscilla K ^a   Khullar, Nitasha ^a   Iqbal, Maaz ^a   Collins, Julie L ^a   Forster, Michael J ^b   Koulen, Peter ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

Behavior; Cognition; Cognitive aging; Learning; Memory; Synapse

Indexed keywords

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PROTEIN HOMER 1A; PROTEIN HOMER 1B; PROTEIN HOMER 1C;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; FOREBRAIN; GENE CLUSTER; GENE EXPRESSION; HOMER 1A GENE; IMMEDIATE EARLY GENE; IMMUNOBLOTTING; MALE; MAZE TEST; MEMORY; MOLECULAR PATHOLOGY; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NONHUMAN; SPATIAL LEARNING; SYNAPSE; TASK PERFORMANCE;

AGING; ANIMALS; BEHAVIOR, ANIMAL; CARRIER PROTEINS; COGNITION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOBLOTTING; MALE; MICE; MICE, INBRED C57BL; TIME FACTORS;

EID: 84892604040     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9479-6     Document Type: Article

References (45)

1. Aarts MM, Arundine M, Tymianski M (2003) Novel concepts in excitotoxic neurodegeneration after stroke. Expert Rev Mol Med 5:1-22
2. Baxter MG, Gallagher M (1996) Neurobiological substrates of behavioral decline: models and data analytic strategies for individual differences in aging. Neurobiol Aging 17:491-495
3. Brakeman PR, Lanahan AA, O'Brien R, Roche K, Barnes CA, Huganir RL, Worley PF (1997) Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386:284-288
4. Brayton CF, Treuting PM, Ward JM (2012) Pathobiology of aging mice and GEM: background strains and experimental design. Vet Pathol 49:85-105
5. Burroughs SL, Kaja S, Koulen P (2011) Quantification of deficits in spatial visual function of mouse models for glaucoma. Invest Ophthalmol Vis Sci 52:3654-3659
6. Calhoun ME, Kurth D, Phinney AL, Long JM, Hengemihle J, Mouton PR, Ingram DK, Jucker M (1998) Hippocampal neuron and synaptophysin-positive bouton number in aging C57BL/6 mice. Neurobiol Aging 19:599-606
7. Chen T, Fei F, Jiang XF, Zhang L, Qu Y, Huo K, Fei Z (2012) Down-regulation of Homer1b/c attenuates glutamatemediated excitotoxicity through endoplasmic reticulum and mitochondria pathways in rat cortical neurons. Free Radic Biol Med 52:208-217
8. Collier TJ, Coleman PD (1991) Divergence of biological and chronological aging: evidence from rodent studies. Neurobiol Aging 12:685-693
9. Dubey A, Forster MJ, Lal H, Sohal RS (1996) Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of the mouse. Arch Biochem Biophys 333:189-197
10. Duncan RS, Hwang SY, Koulen P (2005) Effects of Vesl/Homer proteins on intracellular signaling. Exp Biol Med (Maywood) 230:527-535
11. Erickson CA, Barnes CA (2003) The neurobiology of memory changes in normal aging. Exp Gerontol 38:61-69
12. Forster MJ, Dubey A, Dawson KM, Stutts WA, Lal H, Sohal RS (1996) Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc Natl Acad Sci U S A 93:4765-4769
13. Gallagher M, Rapp PR (1997) The use of animal models to study the effects of aging on cognition. Annu Rev Psychol 48:339-370
14. Ghasemzadeh MB, Mueller C, Vasudevan P (2009) Behavioral sensitization to cocaine is associated with increased glutamate receptor trafficking to the postsynaptic density after extended withdrawal period. Neuroscience 159:414-426
15. Giuffrida R, Musumeci S, D'Antoni S, Bonaccorso CM, Giuffrida-Stella AM, Oostra BA, Catania MV (2005) A reduced number of metabotropic glutamate subtype 5 receptors are associated with constitutive homer proteins in a mouse model of fragile X syndrome. J Neurosci 25:8908-8916
16. Goh JO, Park DC (2009) Neuroplasticity and cognitive aging: the scaffolding theory of aging and cognition. Restor Neurol Neurosci 27:391-403
17. Hatsopoulos NG, Suminski AJ (2011) Sensing with the motor cortex. Neuron 72:477-487
18. Haucke V, Neher E, Sigrist SJ (2011) Protein scaffolds in the coupling of synaptic exocytosis and endocytosis. Nat Rev Neurosci 12:127-138
19. Hayashi MK, Tang C, Verpelli C, Narayanan R, Stearns MH, Xu RM, Li H, Sala C, Hayashi Y (2009) The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 137:159-171
20. Hayflick L (2007) Biological aging is no longer an unsolved problem. Annals of the New York Academy of Sciences 1100:1-13
21. Hwang SY, Wei J, Westhoff JH, Duncan RS, Ozawa F, Volpe P, Inokuchi K, Koulen P (2003) Differential functional interaction of two Vesl/Homer protein isoforms with ryanodine receptor type 1: a novel mechanism for control of intracellular calcium signaling. Cell Calcium 34:177-184
22. Ingram DK (1996) Brain-behavior linkages in aged rodent models: strategies for examining individual differences. Neurobiol Aging 17:497-499, discussion 500
23. Inoue N, Nakao H, Migishima R, Hino T, Matsui M, Hayashi F, Nakao K, Manabe T, Aiba A, Inokuchi K (2009) Requirement of the immediate early gene vesl-1S/homer- 1a for fear memory formation. Mol Brain 2:7
24. Jaubert PJ, Golub MS, Lo YY, Germann SL, Dehoff MH, Worley PF, Kang SH, Schwarz MK, Seeburg PH, Berman RF (2007) Complex, multimodal behavioral profile of the Homer1 knockout mouse. Genes Brain Behav 6:141-154
25. Kaja S, Duncan RS, Longoria S, Hilgenberg JD, Payne AJ, Desai NM, Parikh RA, Burroughs SL, Gregg EV, Goad DL, Koulen P (2011) Novel mechanism of increased Ca2+ release following oxidative stress in neuronal cells involves type 2 inositol-1, 4, 5-trisphosphate receptors. Neuroscience 175:281-291
26. Kaja S, Yang SH, Wei J, Fujitani K, Liu R, Brun-Zinkernagel AM, Simpkins JW, Inokuchi K, Koulen P (2003) Estrogen protects the inner retina from apoptosis and ischemiainduced loss of Vesl-1L/Homer 1c immunoreactive synaptic connections. Invest Ophthalmol Vis Sci 44:3155-3162
27. Kato A, Ozawa F, Saitoh Y, Fukazawa Y, Sugiyama H, Inokuchi K (1998) Novel members of the Vesl/Homer family of PDZ proteins that bind metabotropic glutamate receptors. J Biol Chem 273:23969-23975
28. Klugmann M, Symes CW, Leichtlein CB, Klaussner BK, Dunning J, Fong D, Young D, During MJ (2005) AA Vmediated hippocampal expression of short and long Homer 1 proteins differentially affect cognition and seizure activity in adult rats. Mol Cell Neurosci 28:347-360
29. Lamont MG, Weber JT (2012) The role of calcium in synaptic plasticity and motor learning in the cerebellar cortex. Neurosci Biobehav Rev 36:1153-1162
30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
31. Mao L, Yang L, Tang Q, Samdani S, Zhang G, Wang JQ (2005) The scaffold protein Homer1b/c links metabotropic glutamate receptor 5 to extracellular signal-regulated protein kinase cascades in neurons. J Neurosci 25:2741-2752
32. McDonald SR, Forster MJ (2005) Lifelong vitamin E intake retards age-associated decline of spatial learning ability in apoE-deficient mice. Age 27:5-16
33. Menard C, Quirion R (2012) Successful cognitive aging in rats: a role for mGluR5 glutamate receptors, homer 1 proteins and downstream signaling pathways. PLoS One 7:e28666
34. Mufson EJ, Binder L, Counts SE, DeKosky ST, de Toledo- Morrell L, Ginsberg SD, Ikonomovic MD, Perez SE, Scheff SW (2012) Mild cognitive impairment: pathology and mechanisms. Acta Neuropathol 123:13-30
35. Nguyen PV (2006) Comparative plasticity of brain synapses in inbred mouse strains. J Exp Biol 209:2293-2303
36. Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y (2004) Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and agerelated spatial learning impairments. J Neurosci 24:7648-7653
37. Park DC, Reuter-Lorenz P (2009) The adaptive brain: aging and neurocognitive scaffolding. Annu Rev Psychol 60:173-196
38. Proctor DT, Coulson EJ, Dodd PR (2010) Reduction in postsynaptic scaffolding PSD-95 and SAP-102 protein levels in the Alzheimer inferior temporal cortex is correlated with disease pathology. J Alzheimers Dis 21:795-811
39. Rapp PR, Amaral DG (1992) Individual differences in the cognitive and neurobiological consequences of normal aging. Trends Neurosci 15:340-345
40. Rowe WB, Blalock EM, Chen KC, Kadish I, Wang D, Barrett JE, Thibault O, Porter NM, Rose GM, Landfield PW (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
41. Sumien N, Heinrich KR, Sohal RS, Forster MJ (2004) Shortterm vitamin E intake fails to improve cognitive or psychomotor performance of aged mice. Free Radic Biol Med 36:1424-1433
42. Sumien N, Sims MN, Taylor HJ, Forster MJ (2006) Profiling psychomotor and cognitive aging in four-way cross mice. Age 28:265-282
43. Tappe A, Kuner R (2006) Regulation of motor performance and striatal function by synaptic scaffolding proteins of the Homer1 family. Proc Natl Acad Sci U S A 103:774-779
44. Tu JC, Xiao B, Yuan JP, Lanahan AA, Leoffert K, Li M, Linden DJ, Worley PF (1998) Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21:717-726
45. Westhoff JH, Hwang SY, Duncan RS, Ozawa F, Volpe P, Inokuchi K, Koulen P (2003) Vesl/Homer proteins regulate ryanodine receptor type 2 function and intracellular calcium signaling. Cell Calcium 34:261-269