Calcium-dependent phosphorylation regulates neuronal stability and plasticity in a highly precise pacemaker nucleus

Journal of Neurophysiology

Volumn 106, Issue 1, 2011, Pages 319-331

  George, Andrew A ^a   Macleod, Gregory T ^b   Zakon, Harold H ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Calcineurin; Intrinsic excitability; Protein kinase C; Sensorimotor adaptation

Indexed keywords

CALCINEURIN; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE; PROTEIN KINASE C;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTRIC FISH; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PACEMAKER NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CALCINEURIN; CALCIUM; ELECTRIC FISH; FEMALE; ISOENZYMES; MALE; MEDULLA OBLONGATA; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; PROTEIN KINASE C; RECEPTORS, N-METHYL-D-ASPARTATE; SEX FACTORS;

EID: 79959933633     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00741.2010     Document Type: Article

References (64)

1. Aizenman CD, Linden DJ. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat Neurosci 3: 109-111, 2000.
2. Alroy G, Su H, Yaari Y. Protein kinase C mediates muscarinic block of intrinsic bursting in rat hippocampal neurons. J Physiol 518: 71-79, 1999.
3. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, Traynelis SF. Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20: 89-102, 2000.
4. Blackwell KT. Subcellular, cellular, and circuit mechanisms underlying classical conditioning in Hermissenda crassicornis. Anat Rec 1: 25-37, 2006.
5. Bullock TH. Species differences in effect of electroreceptor input on electric organ pacemakers and other aspects of behavior in electric fish. Brain Behav Evol 2: 85-118, 1969.
6. Chen G, Greengard P, Yan Z. Potentiation of NMDA receptor currents by dopamine D1 receptors in prefrontal cortex. Proc Natl Acad Sci USA 101: 2596-2600, 2004.
7. Chen Y, Yu FH, Surmeier DJ, Scheuer T, Catterall WA. Neuromodulation of Na_ channel slow inactivation via cAMP-dependent protein kinase and protein kinase C. Neuron 49: 409-420, 2006.
8. Conn PJ, Strong JA, Azhderian EM, Nairn AC, Greengard P, Kaczmarek LK. Protein kinase inhibitors selectively block phorbol ester- or forskolininduced changes in excitability of Aplysia neurons. J Neurosci 9: 473-479, 1989.
9. Dembrow NC, Pettit DL, Zakon HH. Calcium dynamics encode the magnitude of a graded memory underlying sensorimotor adaptation. J Neurophysiol 103: 2372-2381, 2010.
10. Desai R, Kronengold J, Mei J, Forman SA, Kaczmarek LK. Protein kinase C modulates inactivation of Kv3.3 channels. J Biol Chem 283: 22283-22294, 2008.
11. Dye J. Dynamics and stimulus-dependence of pacemaker control during behavioral modulations in the weakly electric fish, Apteronotus. J Comp Physiol A 161: 175-185, 1987.
12. Dye J. An in vitro physiological preparation of a vertebrate communicatory behavior: chirping in the weakly electric fish, Apteronotus. J Comp Physiol A 163: 445-458, 1988.
13. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA. Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178, 2002.
14. Hagedorn M, Heiligenberg W. Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Behav 33: 254-265, 1985.
15. Halpain S, Girault JA, Greengard P. Activation of NMDA receptors induces dephosphorylation of DARPP-32 in rat striatal slices. Nature 343: 369-372, 1990.
16. Harvey-Girard E, Dunn RJ, Maler L. Regulated expression of N-methyl-D-aspartate receptors and associated proteins in teleost electrosensory system and telencephalon. J Comp Neurol 505: 644-668, 2007.
17. + channels by G proteins, voltage-dependent facilitation, protein kinase C, and Cav beta subunits. Proc Natl Acad Sci USA 98: 4699-4704, 2001.
18. Hoffman DA, Johnston D. Downregulation of transient K_ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci 10: 3521-3528, 1998.
19. Hopkins CD. Neuroethology of electric communication. Annu Rev Neurosci 11: 497-535, 1988.
20. +/calmodulin-dependent protein kinase II. J Biochem 364: 593-611, 2002.
21. Ikegami S, Kato A, Kudo Y, Kuno T, Ozawa F, Inokuchi K. A facilitatory effect on the induction of long-term potentiation in vivo by chronic administration of antisense oligodeoxynucleotides against catalytic subunits of calcineurin. Brain Res Mol Brain Res 41: 183-191, 1996.
22. Jacinto E, Werlen G, Karin M. Cooperation between Syk and Rac1 leads to synergistic JNK activation in T lymphocytes. Immunity 8: 31-41, 1998.
23. Kelly MT, Crary JF, Sacktor TC. Regulation of protein kinase Mzeta synthesis by multiple kinases in long-term potentiation. J Neurosci 27: 3439-3444, 2007.
24. Lan JY, Skeberdis VA, Jover T, Grooms SY, Lin Y, Araneda RC, Zheng X, Bennett MV, Zukin RS. Protein kinase C modulates NMDA receptor trafficking and gating. Nat Neurosci 4: 382-390, 2001.
25. +-binding protein CaBP4 by protein kinase Czeta in photoreceptors. J Neurosci 27: 12743-12754, 2007.
26. Lisman J, Malenka RC, Nicoll RA, Malinow R. Learning mechanisms: the case for CaM-KII. Science 276: 2001-2002, 1997.
27. Lisman J, Schulman H, Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3: 175-190, 2002.
28. Magoski NS. Regulation of an Aplysia bag-cell neuron cation channel by closely associated protein kinase A and a protein phosphatase. J Neurosci 30: 6833-6841, 2004.
29. Malenka RC, Madison DV, Nicoll RA. Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature 321: 175-177, 1986.
30. Maler L, Hincke MT. Distribution of calcium/calmodulin-dependent kinase 2 in the brain of Apteronotus leptorhynchus. J Comp Neurol 408: 177-203, 1999.
31. Maler L, Sas E, Johnston S, Ellis W. An atlas of the brain of the electric fish Apteronotus leptorhynchus. J Chem Neuroanat 4: 1-38, 1991.
32. Malleret G, Haditsch U, Genoux D, Jones MW, Bliss TV, Vanhoose AM, Weitlauf C, Kandel ER, Winder DG, Mansuy IM. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell 104: 675-686, 2001.
33. Manseau F, Sossin WS, Castellucci VF. Long-term changes in excitability induced by protein kinase C activation in Aplysia sensory neurons. J Neurophysiol 79: 1210-1218, 1998.
34. Metzner W. The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci 13: 1862-1878, 1993.
35. Meyer JH, Leong M, Keller CH. Hormone-induced and maturational changes in electric organ discharges and electroreceptor tuning in the weakly electric fish Apteronotus. J Comp Physiol A 160: 385-394, 1987.
36. Misonou H, Mohapatra DP, Park EW, Leung V, Zhen D, Misonou K, Anderson AE, Trimmer JS. Regulation of ion channel localization and phosphorylation by neuronal activity. Nat Neurosci 7: 711-718, 2004.
37. Moortgat KT, Bullock TH, Sejnowski TJ. Precision of the pacemaker nucleus in a weakly electric fish: network versus cellular influences. J Neurophysiol 83: 971-983, 2000.
38. Nelson AB, Gittis AH, du Lac S. Decreases in CaMKII activity trigger persistent potentiation of intrinsic excitability in spontaneously firing vestibular nucleus neurons. Neuron 46: 623-631, 2005.
39. Numann R, Catterall WA, Scheuer T. Functional modulation of brain sodium channels by protein kinase C phosphorylation. Science 254: 115-118, 1991.
40. Oestreich J, Dembrow NC, George AA, Zakon HH. A "sample-and-hold" pulse-counting integrator as a mechanism for graded memory underlying sensorimotor adaptation. Neuron 49: 577-588, 2006.
41. Oestreich J, Zakon HH. The long-term resetting of a brainstem pacemaker nucleus by synaptic input: a model for sensorimotor adaptation. J Neurosci 22: 8287-8296, 2002.
42. Oestreich J, Zakon HH. Species-specific differences in sensorimotor adaptation are correlated with differences in social structure. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191: 845-856, 2005.
43. O'Leary T, van Rossum MC, Wyllie DJ. Homeostasis of intrinsic excitability in hippocampal neurones: dynamics and mechanism of the response to chronic depolarization. J Physiol 588: 157-170, 2010.
44. Pratt KG, Aizenman CD. Homeostatic regulation of intrinsic excitability and synaptic transmission in a developing visual circuit. J Neurosci 27: 8268-8277, 2007.
45. Schaefer J, Zakon HH. Opposing actions of androgen and estrogen on in vitro firing frequency of neuronal oscillators in the electromotor system. J Neurosci 16: 2860-2868, 1996.
46. Seroussi Y, Brosh I, Barkai E. Learning-induced reduction in post-burst after-hyperpolarization (AHP) is mediated by activation of PKC. Eur J Neurosci 16: 965-969, 2002.
47. Smith MR, Nelson AB, Du Lac S. Regulation of firing response gain by calcium-dependent mechanisms in vestibular nucleus neurons. J Neurophysiol 4: 2031-2042, 2002.
48. Smith GT. Pharmacological characterization of ionic currents that regulate high-frequency spontaneous activity of electromotor neurons in the weakly electric fish, Apteronotus leptorhynchus. J Neurobiol 66: 1-18, 2006.
49. Suh YH, Pelkey KA, Lavezzari G, Roche PA, Huganir RL, McBain CJ, Roche KW. Corequirement of PICK1 binding and PKC phosphorylation for stable surface expression of the metabotropic glutamate receptor mGluR7. Neuron 58: 736-748, 2008.
50. Tong G, Shepherd D, Jahr CE. Synaptic desensitization of NMDA receptors by calcineurin. Science 267: 1510-1512, 1995.
51. Tsien RW, Tsien RY. Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6: 715-760, 1990.
52. +/calmodulin-dependent kinases in posttetanic potentiation at input selective glutamatergic pathways. Proc Natl Acad Sci USA 95: 7133-7138, 1998.
53. +-dependent protein kinase and phosphatase activities controlling synaptic strength. Learn Mem 3: 170-181, 1996.
54. Wierenga CJ, Ibata K, Turrigiano GG. Postsynaptic expression of homeostatic plasticity at neocortical synapses. J Neurosci 25: 2895-2905, 2005.
55. Wilson GF, Magoski NS, Kaczmarek LK. Modulation of a calcium-sensitive nonspecific cation channel by closely associated protein kinase and phosphatase activities. Proc Natl Acad Sci USA 95: 10938-10943, 1998.
56. Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER. Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell 92: 25-37, 1998.
57. Yakel JL. Calcineurin regulation of synaptic function: from ion channels to transmitter release and gene transcription. Trends Pharmacol Sci 18: 124-134, 1997.
58. Yawo H. Protein kinase C potentiates transmitter release from the chick ciliary presynaptic terminal by increasing the exocytotic fusion probability. J Physiol 515: 169-180, 1999.
59. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22: 4860169-4868, 2002.
60. Zakon HH, Dunlap KD. Sex steroids and communication signals in electric fish: a tale of two species. Brain Behav Evol 54: 61-69, 1999.
61. Zakon H, Oestreich J, Tallarovic S, Triefenbach F. EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips. J Physiol (Paris) 96: 451-458, 2002.
62. Zamponi GW, Bourinet E, Nelson D, Nargeot J, Snutch TP. Crosstalk between G proteins and protein kinase C mediated by the calcium channel alpha1 subunit. Nature 385: 442-446, 1997.
63. Zhang M, Hung FS, Zhu Y, Xie Z, Wang JH. Calcium signal-dependent plasticity of neuronal excitability developed postnatally. J Neurobiol 61: 277-287, 2004.
64. Zupanc GK, Horschke I. A distinct population of neurons in the central posterior/prepacemaker nucleus project to the nucleus preopticus periventricularis in the weakly electric gymnotiform fish, Apteronotus leptorhynchus. Brain Res 776: 117-125, 1997.