A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons

Journal of Neuroscience

Volumn 24, Issue 34, 2004, Pages 7583-7595

  Sung, Ying Ju ^a   Walters, Edgar T ^b   Ambron, Richard T ^a  

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

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

CGMP; Chronic pain; Nerve injury; Nitric oxide; Positive injury signal; Retrograde transport

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; GUANYLATE CYCLASE; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE SYNTHASE; PHOSPHATE; THREONINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APLYSIA; ARTICLE; CELL NUCLEUS; CHRONIC PAIN; CLONING; CONTROLLED STUDY; DRUG TARGETING; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; NERVE CRUSH; NERVE EXCITABILITY; NERVE FIBER; NERVE FIBER TRANSECTION; NERVE INJURY; NEUROPATHIC PAIN; NEUROPATHOLOGY; NOCICEPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SENSORY NERVE; SEQUENCE HOMOLOGY; VERTEBRA;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; APLYSIA; AXONS; AXOTOMY; BINDING SITES; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; MITOGEN-ACTIVATED PROTEIN KINASES; MITOGENS; NEURONS, AFFERENT; NITRIC OXIDE; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN KINASES; PROTEIN TRANSPORT; TIME FACTORS;

EID: 4444325794     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1445-04.2004     Document Type: Article

References (82)

1. Abdulla FA, Smith PA (2001) Axotomy- and autotomy-induced changes in the excitability of rat dorsal root ganglion neurons. J Neurophysiol 85:630-643.
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 RI, 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, Schmied R, Huang CC, Smedman M (1992) A signal sequence mediates the retrograde transport of proteins from the axon periphery to the cell body and then into the nucleus. J Neurosci 12:2813-2818.
5. Ambron RT, Dulin MF, Zhang XP, Schmied R, Walters ET (1995) Axoplasm enriched in a protein mobilized by nerve injury induces memory-like alterations in Aplysia neurons. J Neurosci 15:3440-3446.
6. Ambron RT, Zhang XP, Gunstream JD, Povelones M, Walters ET (1996) Intrinsic injury signals enhance growth, survival, and excitability of Aplysia neurons. J Neurosci 16:7469-7477.
7. Antonov I, Antonova I, Kandel ER, Hawkins RD (2003) Activity-dependent presynaptic facilitation and hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37:135-147.
8. Bartsch D, Ghirardi M, Skehel PA, Karl KA, Herder SP, Chen M, Bailey CH, Kandel ER (1995) Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83:979-992.
9. 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.
10. Billy AJ, Walters ET (1989) Long-term expansion and sensitization of mechanosensory receptive fields in Aplysia support an activity-dependent model of whole-cell sensory plasticity. J Neurosci 9:1254-1262.
11. Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 87:682-685.
12. Brunet JF, Shapiro E, Foster SA, Kandel ER, Iino Y (1991) Identification of a peptide specific for Aplysia sensory neurons by PCR-based differential screening. Science 252:856-859.
13. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425-435.
14. 2/M phase of the cell cycle: evidence for regulation of Golgi structure. J Cell Biol 153:1355-1367.
15. Chain DG, Casadio A, Schacher S, Hegde AN, Valbrun M, Yamamoto N, Goldberg AL, Bartsch D, Kandel ER, Schwartz JH (1999) Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysia. Neuron 22:147-156.
16. Chen Y, Devor M (1998) Ectopic mechanosensitivity in injured sensory axons arises from the site of spontaneous electrogenesis. Eur J Pain 2:165-178.
17. Clatworthy AL, Grose E (1999) Immune-mediated alterations in nociceptive sensory function in Aplysia californica. J Exp Biol 202:623-630.
18. Clatworthy AL, Illich PA, Castro GA, Walters ET (1995) Role of peri-axonal inflammation in the development of thermal hyperalgesia and guarding behavior in a rat model of neuropathic pain. Neurosci Lett 184:5-8.
19. Dagan D, Levitan IB (1981) Isolated identified Aplysia neurons in cell culture. J Neurosci 1:736-740.
20. Dale N, Schacher S, Kandel ER (1988) Long-term facilitation in Aplysia involves increase in transmitter release. Science 239:282-285.
21. 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.
22. DesGroseillers L, Auclair D, Wickham L, Maalouf M (1994) A novel actin cDNA is expressed in the neurons of Aplysia californica. Biochim Biophys Acta 1217:322-324.
23. Farr M, Mathews J, Zhu DF, Ambron RT (1999) Inflammation causes a long-term hyperexcitability in the nociceptive sensory neurons of Aplysia. Learn Mem 6:331-340.
24. Farr M, Zhu DF, Povelones M, Valcich D, Ambron RT (2001) Direct interactions between immunocytes and neurons after axotomy in Aplysia. J Neurobiol 46:89-96.
25. Fiallos-Estrada CE, Kummer W, Mayer B, Bravo R, Zimmermann M, Herdegen T (1993) Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and c-JUN co-expression in rat dorsal root ganglion neurons following sciatic nerve transection. Neurosci Lett 150:169-173.
26. Francis SH, Corbin JD (1994) Structure and function of cyclic nucleotide-dependent protein kinases. Annu Rev Physiol 56:237-272.
27. 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.
28. Glanzman DL, Kandel ER, Schacher S (1989) Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron 3:441-450.
29. Glass DB, Krebs EG (1982) Phosphorylation by guanosine 3′:5′-monophosphate-dependent protein kinase of synthetic peptide analogs of a site phosphorylated in histone H2B. J Biol Chem 257:1196-1200.
30. + currents, increasing spike duration and excitability in Aplysia sensory neurons. Proc Natl Acad Sci USA 89:11481-11485.
31. Gracely RH, Lynch SA, Bennett GJ (1992) Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 51:175-194.
32. Gudi T, Lohmann SM, Pilz RB (1997) Regulation of gene expression by cyclic GMP-dependent protein kinase requires nuclear translocation of the kinase: identification of a nuclear localization signal. Mol Cell Biol 17:5244-5254.
33. Gunstream JD, Castro GA, Walters ET (1995) Retrograde transport of plasticity signals in Aplysia sensory neurons following axonal injury. J Neurosci 15:439-448.
34. Hall KU, Collins SP, Gamm DM, Massa E, DePaoli-Roach AA, Uhler MD (1999) Phosphorylation-dependent inhibition of protein phosphatase-1 by G-substrate. A Purkinje cell substrate of the cyclic GMP-dependent protein kinase. J Biol Chem 274:3485-3495.
35. Hanz S, Perlson E, Willis D, Zheng JQ, Massarwa R, Huerta JJ, Koltzenburg M, Kohler M, van-Minnen J, Twiss JL, Fainzilber M (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40:1095-1104.
36. Ji RR, Woolf CJ (2001) Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol Dis 8:1-10.
37. Johanson SO, Crouch MF, Hendry IA (1995) Retrograde axonal transport of signal transduction proteins in rat sciatic nerve. Brain Res 690:55-63.
38. Karin M (1994) Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr Opin Cell Biol 6:415-424.
39. Kim YI, Na HS, Kim SH, Han HC, Yoon YW, Sung B, Nam HJ, Shin SL, Hong SK (1998) Cell type-specific changes of the membrane properties of peripherally-axotomized dorsal root ganglion neurons in a rat model of neuropathic pain. Neuroscience 86:301-309.
40. Lewin MR, Walters ET (1999) Cyclic GMP pathway is critical for inducing long-term sensitization of nociceptive sensory neurons. Nat Neurosci 2:18-23.
41. Liao X, Gunstream JD, Lewin MR, Ambron RT, Walters ET (1999) Activation of protein kinase A contributes to the expression but not the induction of long-term hyperexcitability caused by axotomy of Aplysia sensory neurons. J Neurosci 19:1247-1256.
42. Lin H, Bao J, Sung YJ, Walters ET, Ambron RT (2003) Rapid electrical and delayed molecular signals regulate the serum response element after nerve injury: convergence of injury and learning signals. J Neurobiol 57:204-220.
43. Marais R, Wynne J, Treisman R (1993) The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell 73:381-393.
44. 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.
45. Michael D, Martin KC, Seger R, Ning MM, Baston R, Kandel ER (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.
46. Millan MJ (1999) The induction of pain: an integrative review. Prog Neurobiol 57:1-164.
47. Monfort P, Munoz MD, Kosenko E, Felipo V (2002) Long-term potentiation in hippocampus involves sequential activation of soluble guanylate cyclase, cGMP-dependent protein kinase, and cGMP-degrading phosphodiesterase. J Neurosci 22:10116-10122.
48. Moroz LL, Chen D, Gillette MU, Gillette R (1996) Nitric oxide synthase activity in the molluscan CNS. J Neurochem 66:873-876.
49. Muller U, Carew TJ (1998) Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons. Neuron 21:1423-1434.
50. Park SY, Choi IY, Kim RU, Lee YS, Cho HJ, Kim DS (2003) Downregulation of voltage-gated potassium channel a gene expression by axotomy and neurotrophins in rat dorsal root ganglia. Mol Cells 16:256-259.
51. Pohler D, Butt E, Meissner J, Muller S, Lohse M, Walter U, Lohmann SM, Jarchau T (1995) Expression, purification, and characterization of the cGMP-dependent protein kinases 1β and II using the baculovirus system. FEBS Lett 374:419-425.
52. Schlossmann I, Feil R, Hofmann F (2003) Signaling through NO and cGMP-dependent protein kinases. Ann Med 35:21-27.
53. Schmied R, Ambron RT (1997) A nuclear localization signal targets proteins to the retrograde transport system, thereby evading uptake into organelles in Aplysia axons. J Neurobiol 33:151-160.
54. Schmied R, Huang CC, Zhang XP, 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.
55. + currents. Science 240:1664-1666.
56. Scott JD (1991) Cyclic nucleotide-dependent protein kinases. Pharmacol Ther 50:123-145.
57. Smolenski A, Bachmann C, Reinhard K, Honig-Liedl P, Jarchau T, Hoschuetzky H, Walter U (1998) Analysis and regulation of vasodilator-stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J Biol Chem 273:20029-20035.
58. Study RE, Kral MG (1996) Spontaneous action potential activity in isolated dorsal root ganglion neurons from rats with a painful neuropathy. Pain 65:235-242.
59. Sung YJ, Ambron RT (2004) Pathways that elicit long-term changes in gene expression in nociceptive neurons following nerve injury: contributions to neuropathic pain. Neurol Res 26:195-203.
60. Sung YJ, Hwang MC, Hwang YW (1996) The dominant negative effects of H-Ras harboring a Gly to Ala mutation at position 60. J Biol Chem 271:30537-30543.
61. Sung YJ, Conti J, Currie JR, Brown WT, Denman RB (2000) RNAs that interact with the fragile X syndrome RNA binding protein FMRP. Biochem Biophys Res Commun 275:973-980.
62. Sung YJ, Povelones M, Ambron RT (2001) RISK-1: a novel MAPK homologue in axoplasm that is activated and retrogradely transported after nerve injury. J Neurobiol 47:67-79.
63. Sung YJ, Dolzhanskaya N, Nolin SL, Brown T, Currie JR, Denman RB (2003) The fragile X mental retardation protein FMRP binds elongation factor 1A mRNA and negatively regulates its translation in vivo. J Biol Chem 278:15669-15678.
64. Sutton MA, Carew TJ (2000) Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory-motor synapses in Aplysia. Neuron 26:219-231.
65. Ungless MA, Gasull X, Walters ET (2002) Long-term alteration of S-type potassium current and passive membrane properties in Aplysia sensory neurons following axotomy. J Neurophysiol 87:2408-2420.
66. Verge VM, Xu Z, Xu XJ, Wiesenfeld-Hallin Z, Hokfelt T (1992) Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc Natl Acad Sci USA 89:11617-11621.
67. Wall PD, Devor M (1983) Sensory afferent impulses originate from dorsal root ganglia as well as from the periphery in normal and nerve injured rats. Pain 17:321-339.
68. Walters ET (1994) Injury-related behavior and neuronal plasticity: an evolutionary perspective on sensitization, hyperalgesia, and analgesia. Int Rev Neurobiol 36:325-427.
69. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983a) Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. J Neurophysiol 50:1522-1542.
70. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983b) Mechanoafferent neurons innervating tail of Aplysia. II. Modulation by sensitizing stimulation. J Neurophysiol 50:1543-1559.
71. Walters ET, Alizadeh H, Castro GA (1991) Similar neuronal alterations induced by axonal injury and learning in Aplysia. Science 253:797-799.
72. Walters ET, Bodnarova M, Billy AJ, Dulin MF, Diaz-Rios M, Miller MW, Moroz LL (2004) Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin-A mRNA in Aplysia californica. J Comp Neurol 471:219-240.
73. Wang H, Sun H, Della Penna K, Benz RJ, Xu J, Gerhold DL, Holder DJ, Koblan KS (2002) Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience 114:529-546.
74. Waxman SG, Kocsis JD, Black JA (1994) Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is re-expressed following axotomy. J Neurophysiol 72:466-470.
75. Whitmarsh AJ, Shore P, Sharrocks AD, Davis RJ (1995) Integration of MAP kinase signal transduction pathways at the serum response element. Science 269:403-407.
76. Xu S, Robbins D, Frost J, Dang A, Lange-Carter C, Cobb MH (1995) MEKK1 phosphorylates MEK1 and MEK2 but does not cause activation of mitogen-activated protein kinase. Proc Natl Acad Sci USA 92:6808-6812.
77. Yao Z, Dolginov Y, Hanoch T, Yung Y, Ridner G, Lando Z, Zharhary D, Seger R (2000) Detection of partially phosphorylated forms of ERK by monoclonal antibodies reveals spatial regulation of ERK activity by phosphatases. FEBS Lett 468:37-42.
78. Zaragoza C, Soria E, Lopez E, Browning D, Balbin M, Lopez-Otin C, Lamas S (2002) Activation of the mitogen activated protein kinase extracellular signal-regulated kinase 1 and 2 by the nitric oxide-cGMP-cGMP-dependent protein kinase axis regulates the expression of matrix metalloproteinase 13 in vascular endothelial cells. Mol Pharmacol 62:927-935.
79. Zhang JM, Donnelly DF, Song XJ, Lamotte RH (1997) Axotomy increases the excitability of dorsal root ganglion cells with unmyelinated axons. J Neurophysiol 78:2790-2794.
80. Zhang X, Verge V, Wiesenfeld-Hallin Z, Ju G, Bredt D, Synder SH, Hokfelt T (1993) Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J Comp Neurol 335:563-575.
81. Zhou B, Zhang ZY (2002) The activity of the extracellular signal-regulated kinase 2 is regulated by the differential phosphorylation in the activation loop. J Biol Chem 277:13889-13899.
82. Zimmermann M (2001) Pathobiology of neuropathic pain. Eur J Pharmacol 429:23-37.