Activation of protein kinase a contributes to the expression but not the induction of long-term hyperexcitability caused by axotomy of Aplysia sensory neurons

Journal of Neuroscience

Volumn 19, Issue 4, 1999, Pages 1247-1256

  Liao, Xiaogang ^a   Gunstream, John D ^a   Lewin, Matthew R ^a   Ambron, Richard T ^b   Walters, Edgar T ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

cAMP; Cell dissociation; Long term memory; Nerve injury; Protein kinase inhibitor (PKI); Sensitization

Indexed keywords

CYCLIC AMP; CYCLIC AMP DERIVATIVE; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; SEROTONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APLYSIA; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; LONG TERM MEMORY; MEMORY; NERVE EXCITABILITY; NERVE FIBER TRANSECTION; NERVE INJURY; NEURITE; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; SENSORY NERVE CELL;

EID: 0033558311     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-04-01247.1999     Document Type: Article

References (59)

1. Abel T, Kandel E (1998) Positive and negative regulatory mechanisms that mediate long-term memory storage. Brain Res Brain Res Rev 26:360-378.
2. Alberini CM, Ghirardi M, Metz R, Kandel ER (1994) C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76:1099-1114.
3. Ambron RT, Walters ET (1996) Priming events and retrograde injury signals: a new perspective on the cellular and molecular biology of nerve regeneration. Mol Neurobiol 13:61-79.
4. Ambron RT, Dulin MF, Zhang X-P, Schmied R, Walters ET (1995) Axoplasm enriched in a protein mobilized by nerve injury elicits memory-like alterations in Aplysia neurons. J Neurosci 15:3440-3446.
5. Ambron RT, Zhang X-P, Gunstream JD, Povelones M, Walters ET (1996) Intrinsic injury signals enhance growth, survival, and excitability of Aplysia neurons. J Neurosci 16:7469-7477.
6. Bailey CH, Montarolo P, Chen M, Kandel ER, Schacher S (1992) Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia. Neuron 9:749-758.
7. Baxter DA, Byrne JH (1990) Differential effects of cAMP and serotonin on membrane current, action-potential duration, and excitability in somata of pleural sensory neurons of Aplysia. J Neurophysiol 64:978-990.
8. Bedi SS, Salim A, Chen S, Glanzman DL (1998) Long-term effects of axotomy on excitability and growth of isolated Aplysia sensory neurons in cell culture: potential role of cAMP. J Neurophysiol 79:1371-1383.
9. Berra E, Diaz-Meco MT, Lozano J, Frutos S, Municio MM, Sanchez P, Sanz L, Moscat J (1995) Evidence for a role of MEK and MAPK during signal transduction by protein kinase C zeta. EMBO J 14:6157-6163.
10. Clatworthy AL, Walters ET (1994) Comparative analysis of hyperexcitability and synaptic facilitation induced by nerve injury in two populations of mechanosensory neurones of Aplysia californica. J Exp Biol 190:217-238.
11. Dale N, Kandel ER, 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.
12. Dale N, Schacher S, Kandel ER (1988) Long-term facilitation in Aplysia involves increase in transmitter release. Science 239:282-285.
13. Dash PK, Tian LM, Moore AN (1998) Sequestration of cAMP response element-binding proteins by transcription factor decoys causes collateral elaboration of regenerating Aplysia motor neuron axons. Proc Natl Acad Sci USA 95:8339-8344.
14. Dubnau J, Tully T (1998) Gene discovery in Drosophila: new insights for learning and memory. Annu Rev Neurosci 21:407-444.
15. Gasull X, Gunstream JD, Lewin MR, Walters ET (1997) Long-term hyperexcitability of Aplysia sensory neurons after nerve injury involves activity-dependent induction signals. Soc Neurosci Abstr 23:1958.
16. Ghirardi M, Braha O, Hochner B, Montarolo PG, Kandel ER, Dale N (1992) Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in Aplysia sensory neurons. Neuron 9:479-489.
17. Goda Y (1995) Memory mechanisms. A common cascade for long-term memory. Curr Biol 5:136-138.
18. Goldsmith BA, Abrams TW (1992) cAMP modulates multiple K+ currents, increasing spike duration and excitability in Aplysia sensory neurons. Proc Natl Acad Sci USA 89:11481-11485.
19. Greenberg SM, Castellucci VF, Bayley H, Schwartz JH (1987) A molecular mechanism for long-term sensitization in Aplysia. Nature 329:62-65.
20. Gunstream JD, Castro GA, Walters ET (1995) Retrograde transport of plasticity signals in Aplysia sensory neurons following axonal injury. J Neurosci 15:439-448.
21. Gunstream JD, Castro GA, Walters ET (1997) Region-specific, protein synthesis-dependent long-term hyperexcitability of Aplysia sensory neurons suggests local tagging of axons by 5HT. Soc Neurosci Abstr 23:1958.
22. Hegde AN, Goldberg AL, Schwartz JH (1993) Regulatory subunits of 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.
23. Hegde AN, Inokuchi K, Pei W, Casadio A, Ghirardi M, Chain DG, Martin KC, Kandel ER, Schwartz JH (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89:115-126.
24. + current in the pleural sensory neurons of Aplysia by serotonin and cAMP: implications for spike broadening. Proc Natl Acad Sci USA 89:11476-11480.
25. Hochner B, Klein M, Schacher S, Kandel ER (1986) Action-potential duration and the modulation of transmitter release from the sensory neurons of Aplysia in presynaptic facilitation and behavioral sensitization. Proc Natl Acad Sci USA 83:8410-8414.
26. Hooper SL, Probst WC, Cropper EC, Kupfermann I, Weiss KR (1994a) Myomodulin application increases cAMP and activates cAMP-dependent protein kinase in the accessory radula closer muscle of Aplysia. Neurosci Lett 179:167-170.
27. Hooper SL, Probst WC, Cropper EC, Kupfermann I, Weiss KR (1994b) SCP application or B15 stimulation activates cAPK in the ARC muscle of Aplysia. Brain Res 657:337-341.
28. Kemp BE, Cheng HC, Walsh DA (1988) Peptide inhibitors of cAMP-dependent protein kinase. Methods Enzymol 159:173-183.
29. 2+ and other signals. Soc Neurosci Abstr 22:1445.
30. Lewin MR, Walters ET (1999) Cyclic GMP pathway is critical for inducing long-term sensitization of nociceptive sensory neurons. Nature Neurosci 2:18-23.
31. Liao X, Gunstream JD, Lewin MR, Ambron RT, Walters ET (1997) Injury-induced long-term hyperexcitability of Aplysia sensory neurons is not due to persistent activation of PKA: differences between Rp-cAMPS and PKI treatments. Soc Neurosci Abstr 23:1332.
32. Liao X, Grose E, Walters ET (1998) Activity of PKC but not PKA is important for induction of dissociation-induced long-term hyperexcitability of Aplysia sensory neurons. Soc Neurosci Abstr 24:701.
33. Manseau F, Sossin WS, Castellucci VF (1998) Long-term changes in excitability induced by protein kinase C activation in Aplysia sensory neurons. J Neurophysiol 79:1210-1218.
34. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912.
35. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234:1249-1254.
36. Müeller U, Carew TJ (1998) Serotonin induces temporally and mechanistically distinct phases of persistent PKA activaty in Aplysia sensory neurons. Neuron 21:1423-1434.
37. Rayport SG, Schacher S (1986) Synaptic plasticity in vitro: cell culture of identified Aplysia neurons mediating short-term habituation and sensitization. J Neurosci 6:759-763.
38. Schacher S, 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 12:2403-2413.
39. Schacher S, Castellucci VF, Kandel ER (1988) cAMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis. Science 240:1667-1669.
40. Schacher S, Kandel ER, Montarolo P (1993) cAMP and arachidonic acid simulate long-term structural and functional changes produced by neurotransmitters in Aplysia sensory neurons. Neuron 10:1079-1088.
41. Schmied R, Huang C-C, Zhang X-P, Ambron DA, Ambron RT (1993) Endogenous axoplasmic proteins and proteins containing nuclear localization signal sequences use the retrograde axonal transport/nuclear import pathway in Aplysia neurons. J Neurosci 13:4064-4071.
42. Scholz KP, Byrne JH (1987) Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science 235:685-687.
43. Scholz KP, Byrne JH (1988) Intracellular injection of cAMP induces a long-term reduction of neuronal K+ currents. Science 240:1664-1666.
44. Siegelbaum SA, Camardo JS, Kandel ER (1982) Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones. Nature 299:413-417.
45. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127-148.
46. Steffensen I, Dulin MF, Walters ET, Morris CE (1995) Peripheral regeneration and central sprouting of sensory neurone axons in Aplysia following nerve injury. J Exp Biol 198:2067-2078.
47. Sung YJ, Povelones M, Zhang X-P, Zhu D-F, Ambron RT (1998) Injury-activated kinase (IAK-1): a MAPK homologue that is retrogradely transported after injury and which recognizes the transcription factor C/EBP. Soc Neurosci Abstr 24:65.
48. Titmus MJ, Faber DS (1990) Axotomy-induced alterations in the electrophysiological characteristics of neurons. Prog Neurobiol 35:1-51.
49. Van Haastert PJ, Van Driel R, Jastorff B, Baraniak J, Stec WJ, De Wit RJ (1984) Competitive cAMP antagonists for cAMP-receptor proteins. J Biol Chem 259:10020-10024.
50. Walters ET (1987) Multiple sensory neuronal correlates of site-specific sensitization in Aplysia. J Neurosci 7:408-417.
51. Walters ET (1991) A functional, cellular, and evolutionary model of nociceptive plasticity in Aplysia. Biol Bull 180:241-251.
52. Walters ET (1994) Injury-related behavior and neuronal plasticity: an evolutionary perspective on sensitization, hyperalgesia and analgesia. Int Rev Neurobiol 36:325-427.
53. Walters ET, Ambron RT (1995) Long-term alterations induced by injury and by 5-HT in Aplysia sensory neurons: convergent pathways and common signals? Trends Neurosci 18:137-142.
54. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983) Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. J Neurophysiol 50:1522-1542.
55. Walters ET, Alizadeh H, Castro GA (1991) Similar neuronal alterations induced by axonal injury and learning in Aplysia. Science 253:797-799.
56. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA (1994) Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265:1878-1882.
57. Zimmermann M, Herdegen T (1996) Plasticity of the nervous system at the systemic, cellular and molecular levels: a mechanism of chronic pain and hyperalgesia. Prog Brain Res 110:233-259.
58. Zhang ZS, Fang B, Marshak DW, Byrne JH, Cleary LJ (1991) Serotoninergic varicosities make synaptic contacts with pleural sensory neurons of Aplysia. J Comp Neurol 311:259-270.
59. Ziv NE, Spira ME (1993) Spatiotemporal distribution of Ca2+ following axotomy and throughout the recovery process of cultured Aplysia neurons. Eur J Neurosci 5:657-668.