Chapter Summary

In this chapter, we explored several of the fundamentally important issues related to information storage in neurons. How is a persisting biochemical signal generated? How is that signal transmitted to an effector system to alter neuronal function? If there are multiple biochemical mechanisms for information storage, how might one mechanism transition into the next? In addressing these critical issues, a number of specific molecular mechanisms were proposed in the context of E-LTP at Schaffer-collateral synapses. Our models focused on persistent post-translational modifications as maintenance mechanisms, and on postsynaptic receptors as target effectors of these maintenance signals. Some of the models proposed may be wrong in their particulars, and likely some of the models are relevant to some types of LTP but not others. Future studies will refine and clarify these issues.

Nevertheless, the three decades-worth of studies on mechanisms of E-LTP stand as meaningful contributions to our understanding of the basics of molecular information storage in the nervous system. Much, much progress has been made in defining the basic biochemical mechanisms available to the neuron that allow it to generate a persisting signal and translate that signal into a persisting effect. This work also has begun to define the biochemical processes that can be used by any central synapse for augmenting the strength of its synaptic connections. Thus, investigations into the biochemistry of E-LTP have given us insights into the fundamental cell biology of the neuron.

References

1. Frey, U., Krug, M., Reymann, K. G., and Matthies, H. (1988). "Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro." Brain Res. 452:57-65.

2. Stanton, P. K., and Sarvey, J. M. (1984). "Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis." J. Neurosci. 4:3080-3088.

3. Lu, K. P., Liou, Y. C., and Zhou, X. Z. (2002). "Pinning down proline-directed phosphorylation signaling." Trends Cell Biol. 12:164-172.

4. Duman, R. S., Terwilliger, R. Z., and Nestler, E. J. (1993). "Alterations in nitric oxide-stimulated endogenous ADP-ribosylation associated with long-term potentiation in rat hippocampus." J. Neurochem. 61:1542-1545.

5. Schuman, E. M., Meffert, M. K., Schulman, H., and Madison, D. V. (1994). "An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation." Proc. Natl. Acad. Sci. USA 91:11958-11962.

6. Lisman, J., Schulman, H., and Cline, H. (2002). "The molecular basis of CaMKII function in synaptic and behavioural memory." Nat. Rev. Neurosci. 3:175-190.

7. Strack, S., and Colbran, R. J. (1998). "Autophosphorylation-dependent targeting of calcium/calmodulin- dependent protein kinase II by the NR2B subunit of the N-methyl- D- aspartate receptor." J. Biol. Chem. 273:20689-20692.

8. Leonard, A. S., Lim, I. A., Hemsworth, D. E., Horne, M. C., and Hell, J. W. (1999). "Calcium/ calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor." Proc. Natl. Acad. Sci. USA 96:3239-3244.

9. Lisman, J. E., and Zhabotinsky, A. M. (2001). "A model of synaptic memory: a CaMKII/PPl switch that potentiates transmission by organizing an AMPA receptor anchoring assembly." Neuron 31:191-201.

10. Hvalby, O., Hemmings, H. C. Jr, Paulsen, O., Czernik, A. J., Nairn, A. C., Godfraind, J. M., Jensen, V., Raastad, M., Storm, J. F., Andersen, P., and Greengard, P. (1994). "Specificity of protein kinase inhibitor peptides and induction of long-term potentiation." Proc. Natl. Acad. Sci. USA 91:4761-4765.

11. Otmakhov, N., Griffith, L. C., and Lisman, J. E.

(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.

12. Silva, A. J., Stevens, C. F., Tonegawa, S., and Wang, Y. (1992). "Deficient hippocampal long-term potentiation in alpha-calcium- calmodulin kinase II mutant mice." Science 257:201-206.

(1998). "CA1 long-term potentiation is diminished but present in hippocampal slices from alpha-CaMKII mutant mice." Learn. Mem. 5:344-354.

14. Mayford, M., Wang, J., Kandel, E. R., and O'Dell, T. J. (1995). "CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP." Cell 81:891-904.

15. Chen, H. X., Otmakhov, N., Strack, S., Colbran, R. J., and Lisman, J. E. (2001). "Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP?" J. Neurophysiol. 85:1368-1376.

16. De Koninck, P., and Schulman, H. (1998). "Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations." Science 279:227-230.

17. Poser, S., and Storm, D. R. (2001). "Role of Ca2+-stimulated adenylyl cyclases in LTP and memory formation." Int. J. Dev. Neurosci. 19:387-394.

18. Roberson, E. D., and Sweatt, J. D. (1996). "Transient activation of cyclic AMP-dependent protein kinase during hippocampal long-term potentiation." J. Biol. Chem. 271:30436-30441.

19. Garthwaite, J., and Boulton, C. L. (1995). "Nitric oxide signaling in the central nervous system." Annu. Rev. Physiol. 57:683-706.

20. Kleppisch, T., Pfeifer, A., Klatt, P., Ruth, P., Montkowski, A., Fassler, R., and Hofmann, F.

(1999). "Long-term potentiation in the hippocam-pal CA1 region of mice lacking cGMP-dependent kinases is normal and susceptible to inhibition of nitric oxide synthase." J. Neurosci. 19:48-55.

21. Bon, C. L., and Garthwaite, J. (2001). "Nitric oxide-induced potentiation of CA1 hippocampal synaptic transmission during baseline stimulation is strictly frequency-dependent." Neuropharmacology 40:501-507.

22. Selig, D. K., Segal, M. R., Liao, D., Malenka, R. C., Malinow, R., Nicoll, R. A., and Lisman, J. E. (1996). "Examination of the role of cGMP in long-term potentiation in the CA1 region of the hippocampus." Learn. Mem. 3:42-48.

23. Schuman, E. M., and Madison, D. V. (1991). "A requirement for the intercellular messenger nitric oxide in long-term potentiation." Science 254:1503-1506.

24. Arancio, O., Antonova, I., Gambaryan, S., Lohmann, S. M., Wood, J. S., Lawrence, D. S., and Hawkins, R. D. (2001). "Presynaptic role of cGMP-dependent protein kinase during long-lasting potentiation." J. Neurosci. 1:143-149.

25. Lovinger, D. M., Wong, K. L., Murakami, K., and Routtenberg, A. (1987). "Protein kinase C inhibitors eliminate hippocampal long-term potentiation." Brain. Res. 436:177-183.

26. Colley, P. A., Sheu, F. S., and Routtenberg, A. (1990). "Inhibition of protein kinase C blocks two components of LTP persistence, leaving initial potentiation intact." J. Neurosci. 10:3353-3360.

27. Malinow, R., Madison, D. V., and Tsien, R. W. (1988). "Persistent protein kinase activity underlying long-term potentiation." Nature 335:820-824.

28. Wang, J. H., and Feng, D. P. (1992). "Postsynaptic protein kinase C essential to induction and maintenance of long-term potentiation in the hippocampal CA1 region." Proc. Natl. Acad. Sci. USA 89:2576-2580.

29. Klann, E., Chen, S. J., and Sweatt, J. D. (1991). "Persistent protein kinase activation in the maintenance phase of long-term potentiation." J. Biol. Chem. 266:24253-24256.

30. Klann, E., Chen, S. J., and Sweatt, J. D. (1993). "Mechanism of protein kinase C activation during the induction and maintenance of long-term potentiation probed using a selective peptide substrate." Proc. Natl. Acad. Sci. USA 90:8337-8341.

31. Leahy, J. C., Luo, Y., Kent, C. S., Meiri, K. F., and Vallano, M. L. (1993). "Demonstration of presynaptic protein kinase C activation following long-term potentiation in rat hippocampal slices." Neuroscience 52:563-574.

32. Lovinger, D. M., Akers, R. F., Nelson, R. B., Barnes, C. A., McNaughton, B. L., and Routtenberg, A. (1985). "A selective increase in phosporylation of protein F1, a protein kinase C substrate, directly related to three day growth of long term synaptic enhancement." Brain Res. 343:137-143.

33. Gianotti, C., Nunzi, M. G., Gispen, W. H., and Corradetti, R. (1992). "Phosphorylation of the presynaptic protein B-50 (GAP-43) is increased during electrically induced long-term poten-tiation." Neuron 8:843-848.

34. Sacktor, T. C., Osten, P., Valsamis, H., Jiang, X., Naik, M. U., and Sublette, E. (1993). "Persistent activation of the zeta isoform of protein kinase C in the maintenance of long-term potentiation." Proc. Natl. Acad. Sci. USA 90:8342-8346.

35. Schwartz, J. H. (1993). "Cognitive kinases." Proc. Natl. Acad. Sci. USA 90:8310-8313.

36. Powell, C. M., Johnston, D., and Sweatt, J. D. (1994). "Autonomously active protein kinase C in the maintenance phase of N-methyl-D-aspartate receptor-independent long term potentiation." J. Biol. Chem. 269:27958-27963.

37. Malenka, R. C., Madison, D. V., and Nicoll, R. A.

(1986). "Potentiation of synaptic transmission in the hippocampus by phorbol esters." Nature 321:175-177.

38. Malenka, R. C., Ayoub, G. S., and Nicoll, R. A.

(1987). "Phorbol esters enhance transmitter release in rat hippocampal slices." Brain Res. 403:198-203.

39. Hvalby, O., Reymann, K., and Andersen, P. (1988). "Intracellular analysis of potentiation of CA1 hippocampal synaptic transmission by phorbol ester application." Exp. Brain Res. 71:588-596.

40. Hu, G. Y., Hvalby, O., Walaas, S. I., Albert, K. A., Skjeflo, P., Andersen, P., and Greengard, P. (1987). "Protein kinase C injection into hippocampal pyramidal cells elicits features of long term potentiation." Nature 328:426-429.

41. Abeliovich, A., Chen, C., Goda, Y., Silva, A. J., Stevens, C. F., and Tonegawa, S. (1993). "Modified hippocampal long-term potentiation in PKC gamma-mutant mice." Cell 75:1253-1262.

42. Weeber, E. J., Atkins, C. M., Selcher, J. C., Varga, A. W., Mirnikjoo, B., Paylor, R., Leitges, M., and Sweatt, J. D. (2000). "A role for the beta isoform of protein kinase C in fear conditioning." J. Neurosci. 20:5906-5914.

43. Goda, Y., Stevens, C. F., and Tonegawa, S. (1996). "Phorbol ester effects at hippocampal synapses act independently of the gamma isoform of PKC." Learn. Mem. 3:182-187.

44. Klann, E., and Thiels, E. (1999). "Modulation of protein kinases and protein phosphatases by reactive oxygen species: implications for hippocam-pal synaptic plasticity." Prog. Neuropsychopharmacol. Biol. Psychiatry 23:359-376.

45. Knapp, L. T., and Klann, E. (2002). "Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C." J. Neurosci. 22:674-683.

46. Sweatt, J. D., Atkins, C. M., Johnson, J., English, J. D., Roberson, E. D., Chen, S. J., Newton, A., and Klann, E. (1998). "Protected-site phosphorylation of protein kinase C in hippocampal long-term potentiation." J. Neurochem. 71:1075-1085.

47. Flint, A. J., Paladini, R. D., and Koshland, D. E. Jr. (1990). "Autophosphorylation of protein kinase C at three separated regions of its primary sequence." Science 249:408-411.

48. Orr, J. W., Keranen, L. M., and Newton, A. C. (1992). "Reversible exposure of the pseudosubstrate domain of protein kinase C by phos-phatidylserine and diacylglycerol." J. Biol. Chem. 267:15263-15266.

49. Keranen, L. M., Dutil, E. M., and Newton, A. C.

(1995). "Protein kinase C is regulated in vivo by three functionally distinct phosphorylations." Curr. Biol. 5:1394-1403.

50. Dutil, E. M., Keranen, L. M., DePaoli-Roach, A. A., and Newton, A. C. (1994). "In vivo regulation of protein kinase C by trans-phosphorylation followed by autophosphorylation." J. Biol. Chem. 269:29359-29362.

51. Zhang, J., Wang, L., Petrin, J., Bishop, W. R., and Bond, R. W. (1993). "Characterization of site-specific mutants altered at protein kinase C beta 1 isozyme autophosphorylation sites." Proc. Natl. Acad. Sci. USA 90:6130-6134.

52. Zhang, J., Wang, L., Schwartz, J., Bond, R. W., and Bishop, W. R. (1994). "Phosphorylation of Thr642 is an early event in the processing of newly synthesized protein kinase C beta 1 and is essential for its activation." J. Biol. Chem. 269:19578-19584.

53. Newton, A. C., and Koshland, D. E. Jr. (1987). "Protein kinase C autophosphorylates by an intrapeptide reaction." J. Biol. Chem. 262:10185-10188.

54. Osten, P., Valsamis, L., Harris, A., and Sacktor, T. C.

(1996). "Protein synthesis-dependent formation of protein kinase Mzeta in long-term potentiation." J. Neurosci. 16:2444-2451.

55. Ling, D. S., Benardo, L. S., Serrano, P. A., Blace, N., Kelly, M. T., Crary, J. F., and Sacktor, T. C. (2002). "Protein kinase Mzeta is necessary and sufficient for LTP maintenance." Nat. Neurosci. 5:295-296.

56. Hrabetova, S., and Sacktor, T. C. (1996). "Bidirectional regulation of protein kinase M zeta in the maintenance of long-term potentiation and long-term depression." J. Neurosci. 16:5324-5333.

57. Williams, J. H., Errington, M. L., Lynch, M. A., and Bliss, T. V. (1989). "Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus." Nature 341:739-742.

58. O'Dell, T. J., Hawkins, R. D., Kandel, E. R., and Arancio, O. (1991). "Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger." Proc. Natl. Acad. Sci. USA 88:11285-11289.

59. Scannevin, R. H., and Huganir, R. L. (2000). "Postsynaptic organization and regulation of excitatory synapses." Nat. Rev. Neurosci. 1:133-141.

60. Derkach, V., Barria, A., and Soderling, T. R. (1999). "Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors." Proc. Natl. Acad. Sci. USA 96:3269-3274.

61. Benke ,T. A., Luthi, A., Isaac, J. T., and Collingridge, G. L. (1998). "Modulation of AMPA receptor unitary conductance by synaptic activity." Nature 393:793-797.

62. Barria, A., Muller, D., Derkach, V., Griffith, L. C., and Soderling, T. R. (1997). "Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation." Science 276:2042-2045.

63. Shi, S. H. (2001). "Amersham Biosciences & Science Prize. AMPA receptor dynamics and synaptic plasticity." Science 294:1851-1852.

64. Malinow, R., and Malenka, R. C. (2002). "AMPA receptor trafficking and synaptic plasticity." Annu. Rev. Neurosci. 25:103-126.

65. Poncer, J. C., Esteban, J. A., and Malinow, R. (2002). "Multiple mechanisms for the potentiation of AMPA receptor-mediated transmission by alpha-Ca2+/ calmodulin-dependent protein kinase II." J. Neurosci. 22:4406-4411.

66. Lee, H. K., Barbarosie, M., Kameyama, K., Bear, M. F., and Huganir, R. L. (2000). "Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity." Nature 405:955-959.

67. Montgomery, J. M., and Madison, D. V. (2002). "State-dependent heterogeneity in synaptic depression between pyramidal cell pairs." Neuron 33:765-777.

68. Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., Poncer, J. C., and Malinow, R. (2000). "Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction." Science 287:2262-2267.

69. Ehlers, M. D. (2000). "Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting." Neuron 28:511-525.

70. Luscher, C., Xia, H., Beattie, E. C., Carroll, R. C., von Zastrow, M., Malenka, R. C., and Nicoll, R. A.

(1999). "Role of AMPA receptor cycling in synaptic transmission and plasticity." Neuron 24:649-658.

71. Grosshans, D. R., Clayton, D. A., Coultrap, S. J., and Browning, M. D. (2002). "LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1." Nat. Neurosci. 5:27-33.

72. Lu, X. , Wyszynski, M., Sheng, M., and Baudry, M. (2001). "Proteolysis of glutamate receptor-interacting protein by calpain in rat brain: implications for synaptic plasticity." J. Neurochem. 77:1553-1560.

73. Vanderklish, P., Bednarski, E., and Lynch, G. (1996). "Translational suppression of calpain blocks long-term potentiation." Learn. Mem. 3:209-217.

74. Vanderklish, P., Saido, T. C., Gall, C., Arai, A., and Lynch, G. (1995). "Proteolysis of spectrin by calpain accompanies theta-burst stimulation in cultured hippocampal slices." Brain Res. Mol. Brain Res. 32:25-35.

75. Pavlidis, P., Montgomery, J., and Madison, D. V.

(2000). "Presynaptic protein kinase activity supports long-term potentiation at synapses between individual hippocampal neurons." J. Neurosci. 20:4497-4505.

76. Routtenberg, A. (1990). "Trans-synaptophobia." Adv. Exp. Med. Biol. 268:401-403.

77. Linden, D. J., Wong, K. L., Sheu, F. S., and Routtenberg, A. (1988). "NMDA receptor blockade prevents the increase in protein kinase C substrate (protein F1) phosphorylation produced by long-term potentiation." Brain Res. 458:142-146.

78. Parfitt, K. D., and Madison, D. V. (1993). "Phorbol esters enhance synaptic transmission by a presy-naptic, calcium-dependent mechanism in rat hippocampus." J. Physiol. 471:245-268.

79. Ryan, T. A., Ziv, N. E., and Smith, S. J. (1996). "Potentiation of evoked vesicle turnover at individually resolved synaptic boutons." Neuron 17:125-134.

80. Malgaroli, A., Ting, A. E., Wendland, B., Bergamaschi, A., Villa, A., Tsien, R. W., and Scheller, R. H. (1995). "Presynaptic component of long-term potentiation visualized at individual hippocampal synapses." Science 268:1624-1628.

81. Zakharenko, S. S., Zablow, L., and Siegelbaum, S. A. (2001). "Visualization of changes in presynaptic function during long-term synaptic plasticity." Nat. Neurosci. 4:711-717.

82. Braun, J. E., and Madison, D. V. (2000). "A novel SNAP25-caveolin complex correlates with the onset of persistent synaptic potentiation." J. Neurosci. 20:5997-6006.

83. Antonova, I., Arancio, O., Trillat, A. C., Wang, H. G., Zablow, L., Udo, H., Kandel, E. R., and Hawkins, R. D. (2001). "Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation." Science 294:1547-1550.

84. Martin, K. C., Casadio, A., Zhu, H., E. Y., Rose, J. C., Chen, M., Bailey, C. H., and Kandel, E. R. (1997). "Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage." Cell 91:927-938.

85. Ouyang, Y., Rosenstein, A., Kreiman, G., Schuman, E. M., and Kennedy, M. B. (1999). "Tetanic stimulation leads to increased accumulation of Ca(2+)/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons." J. Neurosci. 19:7823-7833.

86. Steward, O., and Worley, P. F. (2001). "A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites." Proc. Natl. Acad. Sci. USA 98:7062-7068.

87. Steward, O., and Schuman, E. M. (2001). "Protein synthesis at synaptic sites on dendrites." Annu. Rev. Neurosci. 24:299-325.

88. Raught, B., Gingras, A. C., and Sonenberg, N. (2001). "The target of rapamycin (TOR) proteins." Proc. Natl. Acad. Sci. USA98:7037-7044.

89. Angenstein, F., Greenough, W. T., and Weiler, I. J. (1998). "Metabotropic glutamate receptor-initiated translocation of protein kinase p90rsk to polyribo-somes: a possible factor regulating synaptic protein synthesis." Proc. Natl. Acad. Sci. USA 95:15078-15083.

90. Greenough, W. T., Klintsova, A. Y., Irwin, S. A., Galvez, R., Bates, K. E., and Weiler, I. J. (2001). "Synaptic regulation of protein synthesis and the fragile X protein." Proc. Natl. Acad. Sci. USA 98:7101-7106.

91. Gao, F. B. (2002). "Understanding fragile X syndrome: insights from retarded flies." Neuron 34:859-862.

92. Huber, K. M., Gallagher, S. M., Warren, S. T., and Bear, M. F. (2002). "Altered synaptic plasticity in a mouse model of fragile X mental retardation." Proc. Natl. Acad. Sci. USA 99:7746-7750.

93. Raymond, C. R., Thompson, V. L., Tate, W. P., and Abraham, W. C. (2000). "Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation." J. Neurosci. 20:969-976.

94. Frey, U., and Morris, R. G. (1998). "Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation." Trends Neurosci. 21:181-188.

95. Martin, S. J., Grimwood, P. D., and Morris, R. G.

(2000). "Synaptic plasticity and memory: an evaluation of the hypothesis." Annu. Rev.Neurosci. 23:649-711.

96. Sanna, P. P., Cammalleri, M., Berton, F., Simpson, C., Lutjens, R., Bloom, F. E., and Francesconi, W. (2002). "Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region." J. Neurosci. 22:3359-3365.

97. Sweatt, J. D. (2001). "Protooncogenes subserve memory formation in the adult CNS." Neuron 31:671-674.

(2001). "Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway." Curr. Opin. Neurobiol. 11:297-305.

99. Kelly, A., and Lynch, M. A. (2000). "Long-term potentiation in dentate gyrus of the rat is inhibited by the phosphoinositide 3-kinase inhibitor, wortmannin." Neuropharmacology 39:643-651.

100. Silva, A. J., Stevens, C. F., Tonegawa, S., and Wang, Y. (1992). "Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice." Science 257:201-206.

101. Pettit, D. L., Perlman, S., and Malinow, R. (1994). "Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons." Science 266:1881-1885.

102. Ouyang, Y., Kantor, D., Harris, K. M., Schuman, E. M., and Kennedy, M. B. (1997). "Visualization of the distribution of autophosphorylated calcium/calmodulin-dependent protein kinase II after tetanic stimulation in the CA1 area of the hippocampus." J. Neurosci. 17:5416-5427.

103. Malinow, R., Schulman, H., and Tsien, R. W. (1989). "Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP." Science 245:862-866.

104. Wang, J. H., and Kelly, P. T. (1995). "Postsynaptic injection of CA2+/CaM induces synaptic poten-tiation requiring CaMKII and PKC activity." Neuron 15:443-452.

105. Fukunaga, K., Stoppini, L., Miyamoto, E., and Muller, D. (1993). "Long-term potentiation is associated with an increased activity of Ca2+/ calmodulin-dependent protein kinase II." J. Biol. Chem. 268:7863-7867.

106. Matthies, H. Jr, Behnisch, T., Kase, H., Matthies, H., and Reymann, K. G. (1991). "Differential effects of protein kinase inhibitors on pre-established long-term potentiation in rat hippocampal neurons in vitro." Neurosci. Lett. 121:259-262.

107. Matthies, H., and Reymann, K. G. (1993). "Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation." Neuroreport 4:712-714.

108. Reymann, K. G., Brodemann, R., Kase, H., and Matthies, H. (1988). "Inhibitors of calmodulin and protein kinase C block different phases of hippocampal long-term potentiation." Brain Res. 461:388-392.

109. Reymann, K. G., Frey, U., Jork, R., and Matthies, H. (1988). "Polymyxin B, an inhibitor of protein kinase C, prevents the maintenance of synaptic long-term potentiation in hippocampal CA1 neurons." Brain Res. 440:305-314.

110. Blitzer, R. D., Wong, T., Nouranifar, R., Iyengar, R., and Landau, E. M. (1995). "Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region." Neuron 15:1403-1414.

111. Blitzer, R. D., Connor, J. H., Brown, G. P., Wong, T., Shenolikar, S., Iyengar, R., and Landau, E. M. (1998). "Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP." Science 280:1940-1942.

112. Winder, D. G., Mansuy, I. M., Osman, M., Moallem, T. M., and Kandel, E. R. (1998). "Genetic and pharmacological evidence for a novel, intermediate phase of long-term poten-tiation suppressed by calcineurin." Cell 92:25-37.

113. Frey, U., Huang, Y. Y., and Kandel, E. R. (1993). "Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons." Science 260:1661-1664.

114. Chetkovich, D. M., and Sweatt, J. D. (1993). "NMDA receptor activation increases cyclic AMP in area CA1 of the hippocampus via calcium/ calmodulin stimulation of adenylyl cyclase." J. Neurochem. 61:1933-1942.

115. Chetkovich, D. M., Gray, R., Johnston, D., and Sweatt, J. D. (1991). "N-methyl-D-aspartate receptor activation increases cAMP levels and voltage-gated Ca2+ channel activity in area CA1 of hippocampus." Proc. Natl. Acad. Sci. USA 88:6467-6471.

116. Chavez-Noriega, L. E., and Stevens, C. F. (1992). "Modulation of synaptic efficacy in field CA1 of the rat hippocampus by forskolin." Brain Res. 574:85-92.

117. Pockett, S., Slack, J. R., and Peacock, S. (1993). "Cyclic AMP and long-term potentiation in the CA1 region of rat hippocampus." Neuroscience 52:229-236.

118. Roberson, E. D. (1999). Roles for the cyclic AMP dependent protein kinase and superoxide in the induction of hippocampel long-term potentia-tion. Eric Roberson, PhD Thesis. Houston: Baylor College of Medicine.

119. English, J. D., and Sweatt, J. D. (1997). "A requirement for the mitogen-activated protein kinase Cascade in hippocampal long term potentiation." J. Biol. Chem. 272:19103-19106.

120. Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., and Sweatt, J. D. (1998). "The MAPK cascade is required for mammalian associative learning." Nat. Neurosci. 1:602-609.

121. Impey, S., Obrietan, K., Wong, S. T., Poser, S., Yano, S., Wayman, G., Deloulme, J. C., Chan, G., and Storm, D. R. (1998). "Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation." Neuron 21:869-883.

122. English, J. D., and Sweatt, J. D. (1996). "Activation of p42 mitogen-activated protein kinase in hip-pocampal long term potentiation." J. Biol. Chem. 271:24329-24332.

123. Roberson, E. D., English, J. D., Adams, J. P., Selcher, J. C., Kondratick, C., and Sweatt, J. D. (1999). "The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus." J. Neurosci. 19:4337-4348.

124. Verdaguer, N., Corbalan-Garcia, S., Ochoa, W. F., Fita, I., and Gomez-Fernandez, J. C. (1999). "Ca(2+) bridges the C2 membrane-binding domain of protein kinase Calpha directly to phosphatidylserine." Embo. J. 18:6329-6338.

125. Kolodziej, S. J., Hudmon, A., Waxham, M. N., and Stoops, J. K. (2000). "Three-dimensional reconstructions of calcium /calmodulin-dependent (CaM) kinase IIalpha and truncated CaM kinase IIalpha reveal a unique organization for its structural core and functional domains." J. Biol. Chem. 275:14354-14359.

126. Dineley, K. T., Weeber, E. J., Atkins, C., Adams, J. P., Anderson, A. E., and Sweatt, J. D. (2001). "Leitmotifs in the biochemistry of LTP induction: amplification, integration and coordination." J. Neurochem. 77:961-971.

127. Wong, S. T., Athos, J., Figueroa, X. A., Pineda, V. V., Schaefer, M. L., Chavkin, C. C., Muglia, L. J., and Storm, D. R. (1999). "Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP." Neuron 23:787-798.

Genomic Regulation in Memory Formation J. David Sweatt, Acrylic on canvas, 2002

Brain Battalion

Brain Battalion

Get All The Support And Guidance You Need To Be A Success At Beefing Up Your Brain. This Book Is One Of The Most Valuable Resources In The World When It Comes To Understanding Your Brain to Come Up With A Battle Plan For Intelligence.

Get My Free Ebook


Post a comment