Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysia

Neuron

Volumn 22, Issue 1, 1999, Pages 147-156

  Chain, Daniel G ^a   Casadio, Andrea ^a   Schacher, Samuel ^a   Hegde, Ashok N ^a   Valbrun, Mireille ^a   Yamamoto, Naoki ^a   Goldberg, Alfred L ^b   Bartsch, Dusan ^a   Kandel, Eric R ^a   Schwartz, James H ^a  

^a Coll of Physicians and Surg ^*  (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LACTACYSTIN; PROTEASOME; SEROTONIN; UBIQUITIN;

ALLOSTERISM; ANIMAL CELL; ANIMAL TISSUE; APLYSIA; ARTICLE; CONFORMATIONAL TRANSITION; FACILITATION; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; SENSORY NERVE CELL;

EID: 0032911634     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80686-8     Document Type: Article

References (67)

1. Alberini, C.M., Ghirardi, M., Metz, R., and Kandel, E.R. (1994). C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76, 1099-1114.
2. l alpha protein levels in protein kinase A mutant mice. J. Biol. Chem. 272, 3993-3998.
3. Bacskai, B.J., Hochner, B., Mahaut-Smith, M., Adams, S.R., Kaang, B.K., Kandel, E.R., and Tsien, R.Y. (1993). Spatially resolved dynamics of cAmp and protein kinase A subunits in Aplysia sensory neurons. Science 260, 222-226.
4. Bartsch, D., Ghirardi, M., Skehel, P.A., Karl, K.A., Herder, S.P., Chen, M., Bailey, C.H., and Kandel, E.R. (1995). Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change. Cell 83, 979-992.
5. Bartsch, D., Casadio, A., Karl, K., Serodio, P., and Kandel, E.R. (1998). CREB-1 encodes a nuclear activator, a represser, and a cytoplasmic modulator that constitute a regulatory unit critical for long-term facilitation in Aplysia. Cell 95, 211-223.
6. Barzilai, A., Kennedy, T.E., Sweatt, J.D., and Kandel, E.R. (1989). 5-HT modulates protein synthesis and the expression of specific proteins during long-term facilitation in Aplysia sensory neurons. Neuron 2, 1577-1586.
7. Baumeister, W., Walz, J., Zühl, F., and Seemüller, E. (1998). The proteasome: Paradigm for a self-compartmentalizing protease. Cell 92, 367-380.
8. Bergold, P.J., Sweatt, J.D., Winicov, I., Weiss, K.R., Kandel, E.R., and Schwartz, J.H. (1990). Protein synthesized during acquisition of long-term facilitation is needed for the persistent loss of regulatory subunits of the Aplysia cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 87, 3788-3791.
9. Bergold, P.J., Beushausen, S.A., Sacktor, T.C., Cheley, S., Bayley, H., and Schwartz, J.H. (1992). Identification of a regulatory subunit of the cAMP-dependent protein kinase down-regulated in Aplysia sensory neurons during long-term sensitization. Neuron 8, 387-397.
10. Bernier, L., Castellucci, V.F., Kandel, E.R., and Schwartz, J.H. (1982). Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′:5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia. J. Neurosci. 2, 1682-1691.
11. Bubis, J., Neitzel, J.J., Saraswat, L.D., and Taylor, S.S. (1988). A point mutation abolishes binding of cAmp to site A in the regulatory subunit of cAMP-dependent protein kinase. J. Biol. Chem. 263, 9668-9673.
12. Byrne, J.H., and Kandel, E.R. (1996). Presynaptic facilitation revisited: State and time dependence. J. Neurosci. 16, 425-435.
13. Byrne, J.H., Zwartjes, R., Homayouni, R., Critz, S.S., and Eskin, A. (1993). Roles of second messenger pathways in neuronal plasticity and in learning and memory. Insights gained from Aplysia. Adv. Second Messengers Phosphoprotein Res. 27, 47-108.
14. Castellucci, V.F., Kandel, E.R., Schwanz, J.H., Wilson, F.D., Nairn, A.C., and Greengard, P. (1980). Intracellular injection of the catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. Proc. Natl. Acad. Sci. USA 77, 7492-7496.
15. Chain, D.G., Hegde, A.N., Yamamoto, N., Liu-Marsh, B., and Schwartz, J.H. (1995). Persistent activation of cAMP-dependent protein kinase by regulated proteolysis suggests a neuron-specific function of the ubiquitin system in Aplysia. J. Neurosci. 15, 7592-7603.
16. Craiu, A., Gaczynska, M., Akopian, T., Gramm, C.F., Fenteany, G., and Goldberg, A.L. (1997). Lactacystin and clasto-lactacystin beta-lactone modify multiple proteasome beta-subunits and inhibit intracellular protein degradation and major histocompatibility complex class I antigen presentation. J. Biol. Chem. 272, 13437-13445.
17. Dale, N., Kandel, E.R., and Schacher, S. (1987). Serotonin produces long-term changes in the excitability of Aplysia sensory neurons in culture that depend on new protein synthesis. J. Neurosci. 7, 2232-2238.
18. Dash, P.K., Hochner, B., and Kandel, E.R. (1990). Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345, 718-721.
19. Dohrman, D.P., Diamond, I., and Gordon, A.S. (1996). Ethanol causes translocation of cAMP-dependent protein kinase catalytic subunit to the nucleus. Proc. Natl. Acad. Sci. USA 93, 10217-10221.
20. Eytan, E., Armon, T., Heller, H., Beck, S., and Hershko, A. (1993). Ubiquitin-carboxy-terminal hydrolase activity associated with 26S protease complex. J. Biol. Chem. 268, 4668-4674.
21. Fenteany, G., Standaert, R.F., Lane, W.S., Choi, S., Corey, E.J., and Schreiber, S.L. (1995). Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268, 726-731.
22. Frost, W.N., Castellucci, V.F., Hawkins, R.D., and Kandel, E.R. (1985). Monosynaptic connections made by the sensory neurons of the gill-and siphon-withdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization. Proc. Natl. Acad. Sci. USA 82, 8266-8269.
23. Ghirardi, M., Monterolo, P.G., and Kandel, E.R. (1995). A novel intermediate stage in the transition between short-and long-term facilitation in the sensory to motor neuron synapse of Aplysia. Neuron 14, 413-420.
24. Gjertsen, B.T., Mellgren, G., Otten, A., Maronde, E., Genieser, H.G., Jastorf, B., Vintermyr, O.K., McKnight, G.S., and Doskeland, S.O. (1995). Novel Rp-cAmp analogs as tools for inhibition of cAmp-kinase in cell culture. J. Biol. Chem. 270, 20599-20607.
25. Greenberg, S.M., Castellucci, V.F., Bayley, H., and Schwartz, J.H. (1987a). A molecular mechanism for long-term sensitization in Aplysia. Nature 329, 62-65.
26. Greenberg, S.M., Bernier, L, and Schwartz, J.H. (1987b). Distribution of cAmp and cAMP-dependent protein kinases in Aplysia sensory neurons. J. Neurosci. 7, 291-301.
27. Haas, A.L., and Siepmann, T.J. (1997). Pathways of ubiquitin conjugation. FASEB J. 11, 1257-1268.
28. Hale, A.J., Smith, C.A., Sutherland, L.C., Stoneman, V.E.A., LongThorne, V.L., Culhane, A.C., and Williams, G.T. (1996). Apoptosis: molecular regulation of cell death. Eur. J. Biochem. 236, 1-26.
29. Hegde, A.N., Goldberg, A.L., and Schwartz, J.H. (1993). Regulatory subunits of the cAMP-dependent protein kinases are degraded after conjugation to ubiquitin: A molecular mechanism underlying long-term synaptic plasticity. Proc. Natl. Acad. Sci. USA 90, 7436-7440.
30. Hegde, A.N., Inokuchi, K., Pei, W., Casadio, A., Ghirardi, M., Chain, D.G., Martin, K.C., Kandel, E.R., and Schwartz, J.H. (1997). Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89, 115-126.
31. Herberg, F.W., Taylor, S.S., and Dostmann, W.R. (1996). Active site mutations define the pathway for the cooperative activation of cAMP-dependent protein kinase. Biochemistry 35, 2934-2942.
32. Hershko, A., and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
33. Hofmann, F., Bechtel, P.J., and Krebs, E.G. (1977). Concentrations of cyclic AMP-dependent protein kinase subunits in various tissues. J. Biol. Chem. 252, 1441-1447.
34. Kaang, B.-K., Kandel, E.R., and Grant, S.G. (1993). Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons. Neuron 10, 427-435.
35. Kandel, E.R., and Schwartz, J.H. (1982). Molecular biology of learning: Modulation of transmitter release. Science 218, 433-443.
36. Lee, D.H., and Goldberg, A.L. (1996). Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J. Biol. Chem. 271, 27280-27284.
37. McKnight, G.S., Clegg, C.H., Uhler, M.D., Chrivia, J.C., Cadd, G.G., Correll, L.A., and Otten, A.D. (1988). Analysis of the cAMP-dependent protein kinase system using molecular genetic approaches. Rec. Prog. Hormone Res. 44, 307-335.
38. Michael, D., Martin, K.C., Seger, R., Ning, M.-M., Baston, R., and Kandel, E.R. (1998). Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia. Proc. Natl. Acad. Sci. USA 95, 1864-1869.
39. Mitch, W.E., and Goldberg, A.L. (1996). Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N. Engl. J. Med. 335, 1897-1905.
40. Montarolo, P.G., Castellucci, V.F., Morgan, J., Kandel, E.R., and Schacher, S. (1986). A critical period for macromolecular synthesis in long-term heterosynaptic facilitation. Science 244, 1249-1254.
41. Müller, U., and Carew, T.J. (1998). Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons. Neuron 21, 1423-1434.
42. Muralidhar, M.G., and Thomas, J.B. (1993). The Drosophila bendless gene encodes a neural protein related to ubiquitin-conjugating enzymes. Neuron 11, 253-266.
43. Mykles, D.L. (1998). Intracellular proteinases of invertebrates: Calcium-dependent and proteasome/ubiquitin-dependent systems. Int. Rev. Cytol. 184, 157-289.
44. Neitzel. J.J., Dostmann, W.R., and Taylor, S.S. (1991). Role of MgAtp in the activation and reassociation of cAMP-dependent protein kinase I: Consequences of replacing the essential arginine in cAmp binding site A. Biochemistry 30, 733-739.
45. Oh, C.E., McMahon, R., Benzer, S., and Tanouye, M. (1994). Bendless, a Drosophila gene affecting neuronal connectivity, encodes a ubiquitin-conjugating enzyme homolog. J. Neurosci. 14, 3166-3179.
46. O'Leary, F.A., Byrne, J.H., and Cleary, L.J. (1995). Long-term structural rendering in Aplysia sensory neurons requires de novo protein synthesis during a critical time period. J. Neurosci. 15, 3519-3525.
47. Pagano, M. (1997). Cell cycle regulation by the ubiquitin pathway. FASEB J. 11, 1067-1075.
48. Rock, K.L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D., and Goldberg, A.L. (1994). Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78, 761-771.
49. Sacktor, T.C., and Schwartz, J.H. (1990). Sensitizing stimuli cause translocation of protein kinase C in Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA 87, 2036-2039.
50. 2+/calmodulin binding protein in neurons of Aplysia. Proc. Natl. Acad. Sci. USA 80, 6708-6712.
51. 2+/calmodulin-dependent protein kinase produces an autonomous enzyme in Aplysia neurons. J. Cell Biol. 100, 835-842.
52. Schacher, S., and Proshansky, E. (1983). Neurite regeneration by Aplysia neurons in dissociated cell culture: Modulation by Aplysia hemolymph and the presence of the initial axonal segment. J. NeuRosci. 3, 2403-2413.
53. Scholtz, K.P., and Byrne, J.H. (1987). Long-term sensitization in Aplysia: Biophysical correlates in tail sensory neurons. Science 235, 685-687.
54. Schwartz, J.H., and Greenberg, S.M. (1989). Turtles all the way down: some molecular mechanisms underlying long-term sensitization in Aplysia. In Neural Models of Plasticity, J.H. Byrne, ed. (New York: Academic Press), pp. 46-57.
55. Sossin, W.S., Sacktor, T.C., and Schwartz, J.H. (1994). Persistent activation of protein kinase C during the development of long-term facilitation in Aplysia. Learn. Mem. 1, 189-202.
56. Squire, L. (1987). Memory and Brain (New York: Oxford University Press).
57. Su, Y., Dostmann, W.R., Herberg, F.W., Durick, K., Xuong, N.H., Ten Eyck, L., Taylor, S.S., and Varughese, K.I. (1995). Regulatory subunit of protein kinase A: Structure of deletion mutant with cAmp binding domains. Science 269, 807-813.
58. Sudakin, V., Ganoth, D., Dahan, A., Heller, H., Hershko, J., Luca, F.C., Ruderman, J.V., and Hershko, A. (1995). The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell 6, 185-197.
59. Sweatt, J.D., and Kandel, E R. (1989). Persistent and transcriptionally-dependent increase in protein phosphorylation upon long-term facilitation in Aplysia sensory neurons. Nature 339, 51-54.
60. Tawa, N.E., Odessey, R., and Goldberg, A.L. (1997). Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J. Clin. Invest. 100, 197-203.
61. Taylor, S.S., Buechler, J.A., and Yonemoto, W. (1990). camp-dependent protein kinase: Framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59, 971-1005.
62. Vanderklish, P., Bednarski, E., and Lynch, G. (1996). Translational suppression of calpain blocks long-term potentiation. Learn. Mem. 3, 209-217.
63. Verma, I.M., Stevenson, J.K., Schwartz, E.M., Van Antwerp, D., and Miyamoto, S. (1995). Rel/NF-κB/l-κB family: Intimate tales of association and dissociation. Genes Dev. 9, 2723-2735.
64. Wang, K.K., Nath, R., Posner, A., Raser, K.D., Buroker-Kilgore, M., Hajimohammadresza, I., Probert, J.W.A., Marcoux, F.W., Ye, Q., Takano, E., et al. (1996). An alpha-mercaptoacrylic acid derivative is a selective nonpeptide cell-permeable calpain inhibitor and is neuroprotective. Proc. Natl. Acad. Sci. USA 93, 6687-6692.
65. Wilkinson, K.D. (1997). Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J. 11, 1245-1256.
66. Yin, J.C., and Tully, T. (1996). CREB and the formation of long-term memory. Curr. Opin. Neurobiol. 6, 264-268.
67. Zhu, Y., Carroll, M., Papa, F., Hochstrasser, M., and D'Andrea, A.D. (1996). DUB-1, a deubiquitinating enzyme with growth-suppressing activity. Proc. Natl. Acad. Sci. USA 93, 3275-3279.