Synaptic distributions of GluA2 and PKMζ in the monkey dentate gyrus and their relationships with aging and memory

Journal of Neuroscience

Volumn 32, Issue 21, 2012, Pages 7336-7344

  Hara, Yuko ^a   Punsoni, Michael ^a   Yuk, Frank ^a   Sehwan Park, C ^a   Janssen, William G M ^a   Rapp, Peter R ^b   Morrison, John H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 2; PROTEIN KINASE C ZETA;

AGING; AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; COGNITION; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS; ELECTRON MICROSCOPY; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD LABELING; LEARNING; MEMORY; MEMORY CONSOLIDATION; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RECOGNITION; RHESUS MONKEY; SYNAPSE; TRANSMISSION ELECTRON MICROSCOPY;

AGING; ANIMALS; DENDRITIC SPINES; DENTATE GYRUS; FEMALE; MACACA MULATTA; MEMORY; MEMORY DISORDERS; NEURONS; PROTEIN KINASE C; PROTEIN TRANSPORT; PSYCHOMOTOR PERFORMANCE; RECEPTORS, AMPA; RECOGNITION (PSYCHOLOGY); SYNAPSES;

EID: 84861324086     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0605-12.2012     Document Type: Article

References (63)

1. Cabalka LM, Hyman BT, Goodlett CR, Ritchie TC, Van Hoesen GW (1992) Alteration in the pattern of nerve terminal protein immunoreactivity in the perforant pathway in Alzheimer's disease and in rats after entorhinal lesions. Neurobiol Aging 13:283-291.
2. Calhoun ME, Mao Y, Roberts JA, Rapp PR (2004) Reduction in hippocampal cholinergic innervation is unrelated to recognition memory impairment in aged rhesus monkeys. J Comp Neurol 475:238-246.
3. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
4. Crary JF, Shao CY, Mirra SS, Hernandez AI, Sacktor TC (2006) Atypical protein kinase C in neurodegenerative disease I: PKMzeta aggregates with limbic neurofibrillary tangles and AMPA receptors in Alzheimer disease. J Neuropathol Exp Neurol 65:319-326.
5. Dumitriu D, Hao J, Hara Y, Kaufmann J, Janssen WG, Lou W, Rapp PR, Morrison JH (2010) Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J Neurosci 30:7507-7515.
6. Flood DG, Buell SJ, Horwitz GJ, Coleman PD (1987) Dendritic extent in human dentate gyrus granule cells in normal aging and senile dementia. Brain Res 402:205-216.
7. Gazzaley AH, Siegel SJ, Kordower JH, Mufson EJ, Morrison JH (1996) Circuit-specific alterations of N-methyl-D-aspartate receptor subunit 1 in the dentate gyrus of aged monkeys. Proc Natl Acad Sci U S A 93:3121-3125.
8. Gearing M, Tigges J, Mori H, Mirra SS (1996) A beta40 is a major form of beta-amyloid in nonhuman primates. Neurobiol Aging 17:903-908.
9. Geinisman Y, de Toledo-Morrell L, Morrell F (1986) Loss of perforated synapses in the dentate gyrus: morphological substrate of memory deficit in aged rats. Proc Natl Acad Sci U S A 83:3027-3031.
10. Gilardi KV, Shideler SE, Valverde CR, Roberts JA, Lasley BL (1997) Characterization of the onset of menopause in the rhesus macaque. Biol Reprod 57:335-340.
11. Groc L, Choquet D (2006) AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell Tissue Res 326:423-438.
12. Hanley JG, Khatri L, Hanson PI, Ziff EB (2002) NSF ATPase and alpha-/ beta-SNAPs disassemble the AMPA receptor-PICK1 complex. Neuron 34:53-67.
13. Hara Y, Park CS, Janssen WG, Punsoni M, Rapp PR, Morrison JH (2011a) Synaptic characteristics of dentate gyrus axonal boutons and their relationships with aging, menopause, and memory in female rhesus monkeys. J Neurosci 31:7737-7744.
14. Hara Y, Rapp PR, Morrison JH (2011b) Neuronal and morphological bases of cognitive decline in aged rhesus monkeys. Age (Dordr). Jun 28 [Epub ahead of print] PubMed.
15. Hara Y, Park CS, Janssen WG, Roberts MT, Morrison JH, Rapp PR (2012) Synaptic correlates of memory and menopause in the hippocampal dentate gyrus in rhesus monkeys. Neurobiol Aging 33:421.e417-421.e428.
16. Hardt O, Migues PV, Hastings M, Wong J, Nader K (2010) PKMzeta maintains 1-day- and 6-day-old long-term object location but not object identity memory in dorsal hippocampus. Hippocampus 20:691-695.
17. Harris KM, Stevens JK (1989) Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9:2982-2997.
18. He Y, Janssen WG, Rothstein JD, Morrison JH (2000) Differential synaptic localization of the glutamate transporter EAAC1 and glutamate receptor subunit GluR2 in the rat hippocampus. J Comp Neurol 418:255-269.
19. He Y, Hof PR, Janssen WG, Rothstein JD, Morrison JH (2001) Differential synaptic localization of GluR2 and EAAC1 in the macaque monkey entorhinal cortex: a postembedding immunogold study. Neurosci Lett 311:161-164.
20. Henley JM, Barker EA, Glebov OO (2011) Routes, destinations and delays: recent advances in AMPA receptor trafficking. Trends Neurosci 34:258-268.
21. Hernandez AI, Blace N, Crary JF, Serrano PA, Leitges M, Libien JM, Weinstein G, Tcherapanov A, Sacktor TC (2003) Protein kinase M zeta synthesis from a brainmRNAencoding an independent protein kinaseCzeta catalytic domain. Implications for the molecular mechanism of memory. J Biol Chem 278:40305-40316.
22. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279-291.
23. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci 26:360-368.
24. Kelly MT, Crary JF, Sacktor TC (2007) Regulation of protein kinase Mzeta synthesis by multiple kinases in long-term potentiation. J Neurosci 27:3439-3444.
25. Kessels HW, Malinow R (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61:340-350.
26. Keuker JI, Luiten PG, Fuchs E (2003) Preservation of hippocampal neuron numbers in aged rhesus monkeys. Neurobiol Aging 24:157-165.
27. Kimura N, Tanemura K, Nakamura S, Takashima A, Ono F, Sakakibara I, Ishii Y, Kyuwa S, Yoshikawa Y (2003) Age-related changes of Alzheimer's disease-associated proteins in cynomolgus monkey brains. Biochem Biophys Res Commun 310:303-311.
28. Lee SH, Simonetta A, Sheng M (2004) Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron 43:221-236.
29. Man HY, Lin JW, Ju WH, Ahmadian G, Liu L, Becker LE, Sheng M, Wang YT (2000) Regulation ofAMPAreceptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25:649-662.
30. Mead AN, Stephens DN (2003) Involvement of AMPA receptor GluR2 subunits in stimulus-reward learning: evidence from glutamate receptor gria2 knock-out mice. J Neurosci 23:9500-9507.
31. Migues PV, Hardt O, Wu DC, Gamache K, Sacktor TC, Wang YT, Nader K (2010) PKMzeta maintains memories by regulating GluR2-dependent AMPA receptor trafficking. Nat Neurosci 13:630-634.
32. Morrison JH, Hof PR (1997) Life and death of neurons in the aging brain. Science 278:412-419.
33. Moss MB, Rosene DL, Peters A (1988) Effects of aging on visual recognition memory in the rhesus monkey. Neurobiol Aging 9:495-502.
34. Noel J, Ralph GS, Pickard L, Williams J, Molnar E, Uney JB, Collingridge GL, Henley JM (1999) Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23:365-376.
35. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545-559.
36. Oster H, Eichele G, Leitges M (2004) Differential expression of atypical PKCs in the adult mouse brain. Brain Res Mol Brain Res 127:79-88.
37. Pagliusi SR, Gerrard P, Abdallah M, Talabot D, Catsicas S (1994) Age-related changes in expression of AMPA-selective glutamate receptor subunits: is calcium-permeability altered in hippocampal neurons? Neuroscience 61:429-433.
38. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141-1144.
39. Peters A, Jones EG, Morrison JH (1999) Cerebral cortex: neurodegenerative and age-related changes in structure and function of cerebral cortex. New York: Springer.
40. Presty SK, Bachevalier J, Walker LC, Struble RG, Price DL, Mishkin M, Cork LC (1987) Age differences in recognition memory of the rhesus monkey (Macaca mulatta). Neurobiol Aging 8:435-440.
41. Rapp PR, Amaral DG (1991) Recognition memory deficits in a subpopulation of aged monkeys resemble the effects of medial temporal lobe damage. Neurobiol Aging 12:481-486.
42. Rapp PR, Morrison JH, Roberts JA (2003) Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci 23:5708-5714.
43. Sacktor TC (2011) How does PKMzeta maintain long-term memory? Nat Rev Neurosci 12:9-15.
44. Sacktor TC, Osten P, Valsamis H, Jiang X, Naik MU, Sublette E (1993) Persistent activation of the zeta isoform of protein kinase C in the maintenance of long-term potentiation. Proc Natl Acad SciU S A90:8342-8346.
45. Serrano P, Friedman EL, Kenney J, Taubenfeld SM, Zimmerman JM, Hanna J, Alberini C, Kelley AE, Maren S, Rudy JW, Yin JC, Sacktor TC, Fenton AA (2008) PKMzeta maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biol 6:2698-2706.
46. Shamy JL, Buonocore MH, Makaron LM, Amaral DG, Barnes CA, Rapp PR (2006) Hippocampal volume is preserved and fails to predict recognition memory impairment in aged rhesus monkeys (Macaca mulatta). Neurobiol Aging 27:1405-1415.
47. Shao CY, Sondhi R, van de Nes PS, Sacktor TC (2011) PKMzeta is necessary and sufficient for synaptic clustering of PSD-95. Hippocampus. Advance online publication. Retrieved March 6, 2012. doi: 2010.1002/hipo.20996.
48. Shema R, Hazvi S, Sacktor TC, Dudai Y (2009) Boundary conditions for the maintenance of memory by PKMzeta in neocortex. Learn Mem 16:122-128.
49. Shema R, Haramati S, Ron S, Hazvi S, Chen A, Sacktor TC, Dudai Y (2011) Enhancement of consolidated long-term memory by overexpression of protein kinase Mzeta in the neocortex. Science 331:1207-1210.
50. Sloane JA, Pietropaolo MF, Rosene DL, Moss MB, Peters A, Kemper T, Abraham CR (1997) Lack of correlation between plaque burden and cognition in the aged monkey. Acta Neuropathol 94:471-478.
51. Small SA, Chawla MK, Buonocore M, Rapp PR, Barnes CA (2004) Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. Proc Natl Acad Sci U S A 101:7181-7186.
52. Tanabe K, Kani S, Shimizu T, Bae YK, Abe T, Hibi M (2010) Atypical protein kinase C regulates primary dendrite specification of cerebellar Purkinje cells by localizing Golgi apparatus. J Neurosci 30:16983-16992.
53. Tigges J, Gordon TP, McClure HM, Hall EC, Peters A (1988) Survival rate and life span of rhesus monkeys at the Yerkes regional primate research center. Am J Primatol 15:263-273.
54. Tisdale EJ (2002) Glyceraldehyde-3-phosphate dehydrogenase is phosphorylated by protein kinase Ciota /lambda and plays a role in microtubule dynamics in the early secretory pathway. J Biol Chem 277:3334-3341.
55. Toni N, Buchs PA, Nikonenko I, Povilaitite P, Parisi L, Muller D (2001) Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci 21:6245-6251.
56. Vissavajjhala P, Janssen WG, Hu Y, Gazzaley AH, Moran T, Hof PR, Morrison JH (1996) Synaptic distribution of the AMPA-GluR2 subunit and its colocalization with calcium-binding proteins in rat cerebral cortex: an immunohistochemical study using a GluR2-specific monoclonal antibody. Exp Neurol 142:296-312.
57. Walker ML, Herndon JG (2008) Menopause in nonhuman primates? Biol Reprod 79:398-406.
58. White WO, Seibenhener ML, Wooten MW (2002) Phosphorylation of tyrosine 256 facilitates nuclear import of atypical protein kinase C. J Cell Biochem 85:42-53.
59. Witter MP, Van Hoesen GW, Amaral DG (1989) Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J Neurosci 9:216-228.
60. Yao Y, Kelly MT, Sajikumar S, Serrano P, Tian D, Bergold PJ, Frey JU, Sacktor TC (2008) PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J Neurosci 28:7820-7827.
61. Yassa MA, Muftuler LT, Stark CE (2010) Ultrahigh-resolution microstructural diffusion tensor imaging reveals perforant path degradation in aged humans in vivo. Proc Natl Acad Sci U S A 107:12687-12691.
62. Yildirim M, Janssen WG, Tabori NE, Adams MM, Yuen GS, Akama KT, McEwen BS, Milner TA, Morrison JH (2008) Estrogen and aging affect synaptic distribution of phosphorylated LIM kinase (pLIMK) in CA1 region of female rat hippocampus. Neuroscience 152:360-370.
63. Yildirim M, Janssen WG, Lou WY, Akama KT, McEwen BS, Milner TA, Morrison JH (2011) Effects of estrogen and aging on the synaptic distribution of phosphorylated Akt-immunoreactivity in the CA1 region of the female rat hippocampus. Brain Res 1379:98-108.