Protein kinase Mζ enhances excitatory synaptic transmission by increasing the number of active postsynaptic AMPA receptors

Hippocampus

Volumn 16, Issue 5, 2006, Pages 443-452

  Ling, Douglas S F ^a   Benardo, Larry S ^b   Sacktor, Todd C ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

^b Department of Neurology ^*

Author keywords

AMPAR; Atypical PKC; Long term potentiation; LTP; PKM ; Trafficking

Indexed keywords

AMPA RECEPTOR; PROTEIN KINASE C; PROTEIN KINASE M; UNCLASSIFIED DRUG; PROTEIN KINASE M ZETA, RAT;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; RAT STRAIN; RECEPTOR DENSITY; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ANIMAL; DENDRITE; DRUG EFFECT; ELECTROPHYSIOLOGY; IN VITRO STUDY; KINETICS; MALE; PATCH CLAMP; SPRAGUE DAWLEY RAT;

ANIMALS; DENDRITES; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; KINETICS; LONG-TERM POTENTIATION; MALE; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SYNAPTIC TRANSMISSION;

EID: 33745133729     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20171     Document Type: Article

References (69)

1. Abet T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R. 1997. Genetic demonstration of a role for PKA in the late phase of LTP, in hippocampus-based long-term memory. Cell 88:615-626.
2. Ambros-Ingerson J, Xiao P, Larson J, Lynch G. 1993. Waveform. analysis suggests that LTP alters the kinetics of synaptic receptor channels. Brain Res 620:237-244.
3. Andrasfalvy BK, Magee JC. 2004. Changes in AMPA receptor currents following LTP induction on rat CA1 pyramidal neurones. J Physiol 559:543-554.
4. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, Traynelis SF. 2000. Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20:89-102.
5. Benke TA, Luthi A, Isaac JT, Collingridge GL. 1998. Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393:793-797.
6. Bolshakov VY, Seigelbaum SA. 1995. Regulation of hippocampal transmitter release during development and long-term potentiation. Science 264:1730-1734.
7. Bolshakov VY, Golan H, Kandel ER, Siegelbaum SA. 1997. Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron 19:635-651.
8. Burgard EC, Hablitz JJ. 1993. NMDA receptor-mediated components of miniature excitatory synaptic currents in developing rat neocortex. J Neurophysiol 70:1841-1852.
9. Carroll RC, Nicoll RA, Malenka RC. 1998. Effects of PKA, PKC on miniature excitatory postsynaptic currents in CA1 pyramidal cells. J Neurophysiol 80:2797-2800.
10. Choi S, Klingauf J, Tsien RW. 2000. Postfusional regulation of cleft glutamate concentration during LTP at 'silent synapses'. Nat Neurosci 3:330-336.
11. Daw MI, Chittajallu R, Bortolotto ZA, Dev KK, Duprat F, Henley JM, Collingridge GL, Isaac JT. 2000. PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron 28:873-886.
12. 2+/ calmodulin-kinase II enhances channel conductance of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci USA 96:3269-3274.
13. Drier EA, Tello MK, Cowan M, Wu P, Blace N, Sacktor TC, Yin JC. 2002. Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster. Nat Neurosci 5:316-324.
14. Durand GM, Kovalchuk Y, Konnerth A. 1996. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381:71-75.
15. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R. 2003. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143.
16. Faber DS, Korn H. 1991. Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60:1288-1294.
17. Frey U, Huang Y-Y, Kandel ER. 1993. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
18. Frick A, Magee J, Johnston D. 2004. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7:126-135.
19. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. 2000. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
20. Hernandez AI, Blace N, Crary JF, Serrano PA, Leitges M, Libien JM, Weinstein G, Tcherapanov A, Sacktor TC. 2003. Protein kinase Mζ synthesis from a brain mRNA encoding an independent protein kinase Cζ catalytic domain. Implications for the molecular mechanism of memory. J Biol Chem 278:40305-40316.
21. Isaac JT. 2003. Postsynaptic silent synapses: evidence and mechanisms. Neuropharmacology 45:450-460.
22. Isaac JT, Nicoll RA, Malenka RC. 1995. Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
23. Jensen V, Kaiser KM, Borchardt T, Adelmann G, Rozov A, Burnashev N, Brix C, Frotscher M, Andersen P, Hvalby O, Sakmann B, Seeburg PH, Sprengel R. 2003. A juvenile form of postsynaptic hippocampal long-term potentiation in mice deficient for the AMPA receptor subunit GluR-A. J Physiol 553:843-856.
24. Kolleker A, Zhu JJ, Schupp BJ, Qin Y, Mack V, Borchardt T, Kohr G, Malinow R, Seeburg PH, Osten R 2003. Glutamatergic plasticity by synaptic delivery of GluR-B(long)-containing AMPA receptors. Neuron 40:1199-1212.
25. Levenson J, Weeber E, Selcher JC, Kategaya LS, Sweatt JD, Eskin A. 2002. Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake. Nat Neurosci 5:155-161.
26. Liao D, Jones A, Malinow R. 1995. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slices. Nature 375:400-404.
27. Linden DJ. 2001. The expression of cerebellar LTD in culture is not associated with changes in AMPA-receptor kinetics, agonist affinity, or unitary conductance. Proc Natl Acad Sci USA 98:14066-14071.
28. Ling DS, Benardo, LS. 1999. Restrictions on inhibitory circuits contribute to limited recruitment of fast inhibition in rat neocortical pyramidal cells. J Neurophysiol 82:1793-1807.
29. Ling DS, Benardo LS, Serrano PA, Blace N, Kelly MT, Crary JF, Sacktor TC. 2002. Protein kinase Mζ is necessary and sufficient for LTP maintenance. Nat Neurosci 5:295-296.
30. Lynch G, Baudry M. 1984. The biochemistry of memory: a new and specific hypothesis. Science 224:1057-1063.
31. Lynch MA, Errington ML, Bliss TV. 1985. Long-term potentiation of synaptic transmission in the dentate gyrus: increased release of [14C]glutamate without increase in receptor binding. Neurosci Lett 62:123-129.
32. Malinow R, Malenka RC. 2002. AMPA receptor trafficking and synaptic plasticity. Anon Rev Neurosci 25:103-126.
33. Malinow R, Madison DV, Tsien RW. 1988. Persistent protein kinase activity underlying long-term potentiation. Nature 335:820-824.
34. Matthies H, Reymann KG. 1993. Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation. Neuroreport 4:712-714.
35. McBain CJ, Dingledine R. 1993. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiaturn interneurones of rat hippocampus. J Physiol 462:373-392.
36. Muslimov IA, Nimmrich V, Hernandez AI, Tcherepanov A, Sacktor TC, Tiedge H. 2004. Dendritic transport and localization of protein kinase Mζ mRNA: implications for molecular memory consolidation. J Biol Chem 279:52613-52622.
37. Nayak A, Zastrow DJ, Lickteig R, Zahniser NR, Browning MD. 1998. Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394:680-683.
38. Nelder JA, Mead R. 1965. A simplex method for function minimization. Computer J 7:308-313.
39. Newton AC. 2001. Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem Rev 101:2353-2364.
40. Nishimune A, Isaac JT Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM. 1998. NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97.
41. Osten P, Valsamis L, Harris A, Sacktor TC. 1996. Protein synthesis-dependent formation of protein kinase Mζ in LTP. J Neurosci 16:2444-2451.
42. Osten P, Srivastava S, Inman GJ, Vilim FS, Khatri L, Lee LM, States BA, Einheber S, Milner TA, Hanson PI, Ziff EB. 1998. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF, α and β-SNAPs. Neuron 21:99-110.
43. Otmakhov N, Griffith LC, Lisman JE. 1997. Postsynaptic inhibitors of calcium/calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. J Neurosci 17:5357-5365.
44. Otmakhova NA, Otmakhov N, Mortenson LH, Lisman JE. 2000. Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses. J Neurosci 20:4446-4451.
45. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD. 2004. Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975.
46. Passafaro M, Piech V, Sheng M. 2001. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4:917-926.
47. 2+/ calmudulin-dependent protein kinase II. J Neurosci 22:4406-4411.
48. Pratt KG, Watt AJ, Griffith LC, Nelson SB, Turrigiano GG. 2003. Activity-dependent remodeling of pfesynaptic inputs by postsynaptic expression of activated CaMKII. Neuron 39:269-281.
49. Raghavachari S, Lisman JE. 2004. Properties of quantal transmission at CA1 synapses. J Neurophysiol 92:2456-2467.
50. Rall W. 1969a. Distributions of potential in cylindrical coordinates and time constants for a membrane cylinder. Biophys J 9:1509-1541.
51. Rall W. 1969b. Time constants and electrotonic length of membrane cylinders and neurons. Biophys J 9:1483-1508.
52. Sacktor TC, Osten P, Valsamis H, Jiang X, Naik MU, Sublette E. 1993. Persistent activation of the ζ isoform of protein kinase C in the maintenance of long-term potentiation. Proc Natl Acad Sci USA 90:8342-8346.
53. Sajikumar S, Navakkode S, Sacktor TC, Frey JU. 2005. Synaptic tagging and cross-tagging: the role of protein kinase Mζ in maintaining long-term potentiation but not long-term depression. J Neurosci 25:5750-5756.
54. Sanes JR, Lichtman JW. 1999. Can molecules explain long-term potentiation? Nat Neurosci 2:597-604.
55. Serrano P, Yao Y, Sacktor TC. 2005. Persistent phosphorylation by protein kinase Mζ maintains late-phase long-term potentiation. J Neurosci 25:1979-1984.
56. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R. 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-1816.
57. Sigworth FJ. 1980. The variance of sodium current fluctuations at the node of Ranvier. J Physiol 307:97-129.
58. Song I, Huganir RL. 2002. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25:578-588.
59. Song I, Kamboj S, Xia J, Dong H, Liao D, Huganir RL. 1998. Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21:393-400.
60. Sweatt JD. 1999. Toward a molecular explanation for long-term potentiation. Learn Mem 6:399-416.
61. Tang CM, Shi QY, Katchman A, Lynch G. 1991. Modulation of the time course of fast EPSCs and glutamate channel kinetics by aniracetam. Science 254:288-290.
62. Tang CM, Margulis M, Shi QY, Fielding A. 1994. Saturation of post-synaptic glutamate receptors after quantal release of transmitter. Neuron 13:1385-1393.
63. Traynelis SF, Silver RA, Cull-Candy SG. 1993. Estimated conductance of glutamate receptor channels activated during EPSCs at the cerebellar mossy fiber-granule cell synapse. Neuron 11:279-289.
64. Trussell LO, Fischbach GD. 1989. Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3:209-218.
65. Voronin LL, Cherubini E. 2004. "Deaf, mute and whispering" silent synapses: their role in synaptic plasticity. J Physiol 557:3-12.
66. Vyklicky L Jr, Patneau DK, Mayer ML. 1991. Modulation of excitatory synaptic transmission by drugs that reduce desensitization at AMPA/ kainate receptors. Neuron 7:971-984.
67. Wang LY, Salter MW, MacDonald JF. 1991. Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 253:1132-1135.
68. Zakharenko SS, Zablow L, Siegelbaum SA. 2001. Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat Neurosci 4:711-717.
69. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Koster HJ, Borchardt T. Worley P, Lubke J, Frotscher M, Kelly PH, Sommer B, Andersen P. Seeburg PH, Sakmann B. 1999. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284:1805-1811.