Subcellular organization of camkii in rat hippocampal pyramidal neurons

Journal of Comparative Neurology

Volumn 521, Issue 15, 2013, Pages 3570-3583

  Ding, Jin Dong ^a   Kennedy, Mary B ^b   Weinberg, Richard J ^c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Hypoxia; Immunogold electron microscopy; Postsynaptic density; Synaptic plasticity

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL LABELING; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; HIPPOCAMPUS; IN VIVO STUDY; INTRACELLULAR SIGNALING; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STRATUM RADIATUM; SYNAPSE; TISSUE LEVEL;

HYPOXIA; IMMUNOGOLD ELECTRON MICROSCOPY; POSTSYNAPTIC DENSITY; SYNAPTIC PLASTICITY;

ANIMALS; ANTIBODIES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL MEMBRANE; CYTOPLASM; DATA INTERPRETATION, STATISTICAL; DENDRITES; DENDRITIC SPINES; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MICROSCOPY, IMMUNOELECTRON; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SUBCELLULAR FRACTIONS; SYNAPSES; TISSUE EMBEDDING; TISSUE FIXATION;

EID: 84882939684     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23372     Document Type: Article

References (53)

1. 2+/calmodulin-dependent protein kinase II: potential role in neuronal damage. J Neurochem 58:1743-1753.
2. Barria A, Malinow R. 2005. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48:289-301.
3. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR. 1997. Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276:2042-2045.
4. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, Somogyi P. 1993. The metabotropic glutamate receptor (mGluR1 α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
5. Bayer KU, Lohler J, Schulman H, Harbers K. 1999. Developmental expression of the CaM kinase II isoforms: ubiquitous γ- and δ-CaM kinase II are the early isoforms and most abundant in the developing nervous system. Brain Res Mol Brain Res 70:147-154.
6. Bennett MK, Erondu NE, Kennedy MB. 1983. Purification and characterization of a calmodulin-dependent protein kinase that is highly concentrated in brain. J Biol Chem 258:12735-12744.
7. Burette AC, Lesperance T, Crum J, Martone M, Volkmann N, Ellisman MH, Weinberg RJ. 2012. Electron tomographic analysis of synaptic ultrastructure. J Comp Neurol 520:2697-2711.
8. 2+/calmodulin-dependent protein kinase in developing rat brain. J Neurosci 10:1788-1798.
9. Chen X, Vinade L, Leapman RD, Petersen JD, Nakagawa T, Phillips TM, Sheng M, Reese TS. 2005. Mass of the postsynaptic density and enumeration of three key molecules. Proc Natl Acad Sci U S A 102:11551-11556.
10. Domańska-Janik K, Zalewska T, Zablocka B, Ostrowski J. 1999. Ischemia-induced modifications of protein components of rat brain postsynaptic densities. Neurochem Int 34:329-336.
11. 2+/calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 391:78-84.
12. 2+/calmodulin-dependent protein kinase II in neurons. J Neurosci 20:3076-3084.
13. Dosemeci A, Tao-Cheng JH, Vinade L, Winters CA, Pozzo-Miller L, Reese TS. 2001. Glutamate-induced transient modification of the postsynaptic density. Proc Natl Acad Sci U S A 98:10428-10432.
14. 2+/calmodulin-dependent protein kinase in rat brain. J Neurosci 5:3270-3277.
15. Fera A, Dosemeci A, Sousa AA, Yang C, Leapman RD, Reese TS. 2012. Direct visualization of CaMKII at postsynaptic densities by electron microscopy tomography. J Comp Neurol 520:4218-4225
16. Goldenring JR, McGuire JS Jr, DeLorenzo RJ. 1984. Identification of the major postsynaptic density protein as homologous with the major calmodulin-binding subunit of a calmodulin-dependent protein kinase. J Neurochem 42:1077-1084.
17. Halt AR, Dallapiazza RF, Zhou Y, Stein IS, Qian H, Juntti S, Wojcik S, Brose N, Silva AJ, Hell JW. 2012. CaMKII binding to GluN2B is critical during memory consolidation. EMBO J 31:1203-1216.
18. Hill TC, Zito K. 2013. LTP-induced long-term stabilization of individual nascent dendritic spines. J Neurosci 33:678-686.
19. Honkura N, Matsuzaki M, Noguchi J, Ellis-Davies GC, Kasai H. 2008. The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57:719-729.
20. 2+/calmodulin-dependent protein kinase II to synaptic junctions in the vulnerable hippocampal CA1 region following transient ischemia. J Neurochem 64:277-284.
21. Hu BR, Park M, Martone ME, Fischer WH, Ellisman MH, Zivin JA. 1998. Assembly of proteins to postsynaptic densities after transient cerebral ischemia. J Neurosci 18:625-633.
22. 2+/calmodulin-dependent protein kinase. Proc Natl Acad Sci U S A 81:945-949.
23. Kennedy MB, Bennett MK, Erondu NE. 1983. Biochemical and immunochemical evidence that the "major postsynaptic density protein" is a subunit of a calmodulin-dependent protein kinase. Proc Natl Acad Sci U S A 80:7357-7361.
24. Kennedy MJ, Davison IG, Robinson CG, Ehlers MD. 2010. Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 141:524-535.
25. Kharazia VN, Weinberg RJ. 1999. Immunogold localization of AMPA and NMDA receptors in somatic sensory cortex of albino rat. J Comp Neurol 412:292-302.
26. 2+/calmodulin kinase II translocates in a hippocampal slice model of ischemia. J Neurochem 64:2147-2156.
27. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R. 2009. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458:299-304.
28. Lisman J, Schulman H, Cline H. 2002. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190.
29. Lisman J, Yasuda R, Raghavachari S. 2012. Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 13:169-182.
30. Lledo PM, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, Nicoll RA. 1995. Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci U S A 92:11175-11179.
31. 2+/calmodulin-dependent protein kinase associate differently with the postsynaptic density fraction. J Biol Chem 260:9039-9046.
32. Mizutani A, Kuroda Y, Futatsugi A, Furuichi T, Mikoshiba K. 2008. Phosphorylation of Homer3 by calcium/calmodulin-dependent kinase II regulates a coupling state of its target molecules in Purkinje cells. J Neurosci 28:5369-5382.
33. Newpher TM, Ehlers MD. 2009. Spine microdomains for postsynaptic signaling and plasticity. Trends Cell Biol 19:218-227.
34. 2+/calmodulin-dependent protein kinase II. J Biol Chem 279:17980-17988.
35. Okamoto K, Nagai T, Miyawaki A, Hayashi Y. 2004. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112.
36. Okamoto K, Narayanan R, Lee SH, Murata K, Hayashi Y. 2007. The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure. Proc Natl Acad Sci U S A 104:6418-6423.
37. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, De Koninck P, Choquet D. 2010. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67:239-252.
38. Otmakhov N, Tao-Cheng JH, Carpenter S, Asrican B, Dosemeci A, Reese TS, Lisman J. 2004. Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation. J Neurosci 24:9324-9331.
39. 2+/calmodulin-dependent protein kinase II at the PSD. J Neurosci 23:11270-11278.
40. Petralia RS, Sans N, Wang YX, Wenthold RJ. 2005. Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol Cell Neurosci 29:436-452.
41. Phend KD, Rustioni A, Weinberg RJ. 1995. An osmium-free method of Epon embedment that preserves both ultrastructure and antigenicity for post-embedding immunocytochemistry. J Histochem Cytochem 43:283-292.
42. Sato T. 1968. A modified method for lead staining of thin sections. J Electron Microsc (Tokyo) 17:158-159.
43. Shin SM, Zhang N, Hansen J, Gerges NZ, Pak DT, Sheng M, Lee SH. 2012. GKAP orchestrates activity-dependent postsynaptic protein remodeling and homeostatic scaling. Nat Neurosci 15:1655-1666.
44. 2+ signaling pathway in GABAergic neurons of the hippocampus. Proc Natl Acad Sci U S A 95:3245-3250.
45. Soderling TR. 2000. CaM-kinases: modulators of synaptic plasticity. Curr Opin Neurobiol 10:375-380.
46. 2+/calmodulin-dependent protein kinase II into postsynaptic density after decapitation. J Neurochem 63:1529-1537.
47. 2+/calmodulin-dependent protein kinase II clusters in hippocampal neurons. Neuroscience 106:69-78.
48. Tao-Cheng JH, Vinade L, Pozzo-Miller LD, Reese TS, Dosemeci A. 2002. Calcium/calmodulin-dependent protein kinase II clusters in adult rat hippocampal slices. Neuroscience 115:435-440.
49. Tao-Cheng JH, Gallant PE, Brightman MW, Dosemeci A, Reese TS. 2007. Structural changes at synapses after delayed perfusion fixation in different regions of the mouse brain. J Comp Neurol 501:731-740.
50. Valtschanoff JG, Weinberg RJ. 2001. Laminar organization of the NMDA receptor complex within the postsynaptic density. J Neurosci 21:1211-1217.
51. Wu GY, Cline HT. 1998. Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279:222-226.
52. Zito K, Knott G, Shepherd GM, Shenolikar S, Svoboda K. 2004. Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron 44:321-334.
53. Zou DJ, Cline HT. 1999. Postsynaptic calcium/calmodulin-dependent protein kinase II is required to limit elaboration of presynaptic and postsynaptic neuronal arbors. J Neurosci 19:8909-8918.