The Role of the Theta Isoform of Protein Kinase C (PKC) in Activity-Dependent Synapse Elimination: Evidence from the PKC Theta Knock-Out Mouse In Vivo and In Vitro

Journal of Neuroscience

Volumn 24, Issue 15, 2004, Pages 3762-3769

  Li, Min Xu ^a   Jia, Min ^a   Yang, Li Xia ^a   Jiang, Hao ^b   Lanuza, Maria A ^c   Gonzalez, Carmen M ^c   Nelson, Phillip G ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b HENRY FORD HEALTH SYSTEM   (United States)

^c UNIVERSITAT ROVIRA I VIRGILI   (Spain)

Author keywords

In vitro; In vivo; Knock out; Neuromuscular junction; PKC theta; Synapse elimination

Indexed keywords

MUSCLE ENZYME; PROTEIN KINASE C THETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA MODIFICATION; ENZYME ACTIVITY; ENZYME DEFICIENCY; KNOCKOUT MOUSE; MOUSE; MUSCLE CELL; NERVE CELL; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPSE; SYNAPSE ELIMINATION;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; DIFFUSION CHAMBERS, CULTURE; ISOENZYMES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROELECTRODES; MUSCLES; NEUROMUSCULAR JUNCTION; PHORBOL ESTERS; PROTEIN KINASE C; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 1942521770     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3930-03.2004     Document Type: Article

References (36)

1. Balice-Gordon RJ, Lichtman JW (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372:519-524.
2. Blackstone C, Murphy T, Moss S, Baraban J, Huganir R (1994) Cyclic AMP and synaptic activity-dependent phosphorylation of AMPA-preferring glutamate receptors. J Neurosci 14:7585-7593.
3. Brown MC, Jansen JK, Van Essen D (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol (Lond) 261:387-422.
4. Cabelli RJ, Shelton DL, Segal RA, Shatz CJ (1997) Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19:63-76.
5. Cantrell A, Tibbs V, Westenbroek R, Scheuer T, Catterall WA (1999) Dopaminergic modulation of voltage-gated Na+ current in rat hippocampal neurons requires anchoring of cAMP-dependent protein kinase. J Neurosci 19:RC21(1-6).
6. Csillik B, Knyihar-Csillik E, Kreutzberg GW, Tajti L, Kereszturi A, Kovacs T (1992) Calcitonin gene-related peptide is released from cholinergic synapses. Ann NY Acad Sci 657:466-468.
7. D'Angelo E, Rossi P, Tanzi F, Taglietti V (1992) Protein kinase C facilitation of acetylcholine release at the rat neuromuscular junction. Eur J Neurosci 4:823-831.
8. Fields RD, Nelson PG (1992) Activity-dependent development of the vertebrate nervous system. Int Rev Neurobiol 34:133-214.
9. Ghirardi M, Braha O, Hochner B, Montarolo P, Kandel E, 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.
10. Hebb DO (1949) The organization of behavior. New York: Wiley.
11. Hilgenberg L, Miles K (1995) Developmental regulation of a protein kinase C isoform localized in the neuromuscular junction. J Cell Sci 108:51-61.
12. Hilgenberg L, Yearwood S, Milstein S, Miles K (1996) Neural influence on protein kinase C isoform expression in skeletal muscle. J Neurosci 16:4994-5003.
13. Jia M, Li MX, Dunlap V, Nelson PG (1999) The thrombin receptor mediates functional activity-dependent neuromuscular synapse reduction via protein kinase C activation in vitro. J Neurobiol 38:369-381.
14. Kim S, Bondeva T, Nelson PG (2002) Activation of protein kinase C isozymes in primary mouse myotubes by carbachol. Brain Res Dev Brain Res 137:13-21.
15. Lanuza MA, Li MX, Jia M, Kim S, Davenport R, Dunlap V, Nelson PG (2000) Protein kinase C mediated changes in synaptic efficacy at the neuromuscular junction in vitro: the role of postsynaptic acetylcholine receptors. J Neurosci Res 61:616-625.
16. Lanuza MA, Garcia N, Santafe M, Nelson PG, Fenoll-Brunet MR, Tomas J (2001) Pertussis toxin-sensitive G-protein and protein kinase C activity are involved in normal synapse elimination in the neonatal rat muscle. J Neurosci Res 63:330-340.
17. Lanuza MA, Garcia N, Santafe M, Gonzalez CM, Alonso I, Nelson PG, Tomas J (2002) Pre- and postsynaptic maturation of the neuromuscular junction during neonatal synapse elimination depends on protein kinase C. J Neurosci Res 67:607-617.
18. Li MX, Jia M, Jiang H, Dunlap V, Nelson PG (2001a) Opposing actions of protein kinase A and C mediate Hebbian synaptic plasticity. Nat Neurosci 4:871-872.
19. Li MX, Jia M, Yang LX, Dunlap V, Nelson PG (2001b) The role of PKC theta in synapse loss in neuro-muscular junction in vitro. Soc Neurosci Abstr 27:799.3.
20. Li MX, Jia M, Yang LX, Dunlap V, Nelson PG (2002) Pre- and postsynaptic mechanisms in Hebbian activity-dependent synapse modification. J Neurobiol 52:241-250.
21. Malenka R, Madison D, Nicoll R (1986) Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature 321:175-177.
22. Miles K, Greengard P, Huganir RL (1989) Calcitonin gene-related peptide regulates phosphorylation of the nicotinic acetylcholine receptor in rat myotubes. Neuron 2:1517-1524.
23. Nelson PG, Jia M, Li MX (2003) Protein kinases and Hebbian function. The Neurosientist 9:110-116.
24. Newton A (1995) Protein kinase C: structure, function, and regulation. J Biol Chem 270:28495-28498.
25. O'Brien RA, Ostberg AJ, Vrbova G (1978) Observations on the elimination of polyneuronal innervation in developing mammalian skeletal muscle. J Physiol (Lond) 282:571-582.
26. Pfeifhofer C, Kofler K, Gruber T, Tabrizi NG, Lutz C, Maly K, Leitges M, Baier G (2003) Protein kinase C theta affects Ca2+ mobilization and NFAT cell activation in primary mouse T cells. J Exp Med 197:1525-1535.
27. Piehl F, Arvidsson U, Hokfelt T, Cullheim S (1993) Calcitoningene-related peptide-like immunoreactivity in motoneuron pools innervating different hind limb muscles in the rat. Exp Brain Res 96:291-303.
28. Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
29. Shatz CJ (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5:745-756.
30. Sik A, Gulacsi A, Lai Y, Doyle W, Pacia S, Mody I, Freund T (2000) Localization of the A kinase anchoring protein AKAP79 in the human hippocampus. Eur J Neurosci 12:1155-1164.
31. Sun Z, Arendt C, Ellmeier W, Schaeffer E, Sunshine M, Gandhi L, Annes J, Petrzilka D, Kupfer A, Schwartzberg P, Littman D (2000) PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes. Nature 404:402-407.
32. Swope SL, Moss SJ, Raymond LA, Huganir RL (1999) Regulation of ligand-gated ion channels by protein phosphorylation. Adv Second Messenger Phosphoprotein Res 33:49-78.
33. Tanaka C, Nishizuka Y (1994) The protein kinase C family for neuronal signaling. Annu Rev Neurosci 17:551-567.
34. Thompson WJ (1985) Activity and synapse elimination at the neuromuscular junction. Cell Mol Neurobiol 5:167-182.
35. Tingley WG, Ehlers MD, Kameyama K, Doherty C, Ptak JB, Riley CT, Huganir RL (1997) Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J Biol Chem 272:5157-5166.
36. Vaello ML, Ruiz-Gomez A, Lerma J, Mayor Jr F (1994) Modulation of inhibitory glycine receptors by phosphorylation by protein kinase C and cAMP-dependent protein kinase. J Biol Chem 269:2002-2008.