Phorbol 12-myristate 13-acetate potentiation of N-methyl-D-aspartate- induced currents in primary cultured cerebellar granule cells is mediated by protein kinase Cα

Journal of Pharmacology and Experimental Therapeutics

Volumn 330, Issue 2, 2009, Pages 641-649

  Reneau, Jason C ^a   Reyland, Mary E ^c   Phillips, Jonathan ^a   Kindy, Carissa ^a   Popp, R Lisa ^a,b  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C GAMMA; PROTEIN KINASE C THETA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG POTENTIATION; DRUG RECEPTOR BINDING; ENZYME ACTIVATION; GRANULE CELL; MEMBRANE CURRENT; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CELLS, CULTURED; CEREBELLUM; DRUG SYNERGISM; ENZYME ACTIVATION; N-METHYLASPARTATE; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C-ALPHA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; TETRADECANOYLPHORBOL ACETATE;

EID: 67651014866     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.109.153163     Document Type: Article

References (39)

1. Bartz AE (1976) Introduction to the analysis of variance, in Basic Statistical Concepts in Education and the Behavioral Sciences, p 287, Burgess Publishing Co., Minneapolis, MN.
2. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA, and Zhang D (2002) Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415:793-798. (Pubitemid 34150501)
3. Chen L and Huang LY (1991) Sustained potentiation of NMDA receptor-mediated glutamate responses through activation of protein kinase C by a μ opioid. Neuron 7:319-326.
4. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356:521-523.
5. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S, and Sevarino KA (1995) Cloning and characterization of x-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J Neurosci 15:6498-6508. (Pubitemid 3001297)
6. Cuevas J and Berg DK (1998) Mammalian nicotinic receptors with alpha7 subunits that slowly desensitize and rapidly recover from alpha-bungarotoxin blockade. J Neurosci 18:10335-10344. (Pubitemid 29016553)
7. Cuevas J, Roth AL, and Berg DK (2000) Two distinct classes of functional 7-containing nicotinic receptor on rat superior cervical ganglion neurons. J Physiol 525: 735-746. (Pubitemid 30426793)
8. Farrant M, Feldmeyer D, Takahashi T, and Cull-Candy SG (1994) NMDA-receptor channel diversity in the developing cerebellum. Nature 368:335-339. (Pubitemid 24104267)
9. Gallo V, Kingsbury A, Balázs R, and Jørgensen OS (1987) The role in depolarization in the survival and differentiation of cerebellar granule cells in culture. J Neurosci 7:2203-2213. (Pubitemid 17114929)
10. Gerber G, Kangrga I, Ryu PD, Larew JS, and Randic M (1989) Multiple effects of phorbol esters in the rat spinal dorsal horn. J Neurosci 9:3606-3617. (Pubitemid 19260034)
11. Grant ER, Bacskai BJ, Anegawa NJ, Pleasure DE, and Lynch DR (1998) Opposing contributions of NR1 and NR2 to protein kinase C modulation of NMDA receptors. J Neurochem 71:1471-1481.
12. Jackson MF, Konarski JZ, Weerapura M, Czerwinski W, and MacDonald JF (2006) Protein kinase C enhances glycine-insensitive desensitization of NMDA receptors independently of previously identified protein kinase C sites. J Neurochem 96: 1509-1518. (Pubitemid 43351611)
13. Kleckner NW and Dingledine R (1988) Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241:835-837.
14. Lan JY, Skeberdis VA, Jover T, Grooms SY, Lin Y, Araneda RC, Zheng X, Bennett MV, and Zukin RS (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat Neurosci 4:382-390. (Pubitemid 32260114)
15. Leonard AS and Hell JW (1997) Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N-methyl-D-aspartate receptors at different sites. J Biol Chem 272:12107-12115. (Pubitemid 27202791)
16. Liao GY, Wagner DA, Hsu MH, and Leonard JP (2001) Evidence for direct protein kinase-C mediated modulation of N-methyl-D-aspartate receptor current. Mol Pharmacol 59:960-964.
17. Logan SM, Rivera FE, and Leonard JP (1999) Protein kinase C modulation of recombinant NMDA receptor currents: roles for the C-terminal C1 exon and calcium ions. J Neurosci 19:974-986.
18. Lu WY, Jackson MF, Bai D, Orser BA, and MacDonald JF (2000) In CA1 pyramidal neurons of the hippocampus protein kinase C regulates calcium-dependent inactivation of NMDA receptors. J Neurosci 20:4452-4461. (Pubitemid 30396610)
19. Lu WY, Xiong ZG, Lei S, Orser BA, Dudek E, Browning MD, and MacDonald JF (1999) G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat Neurosci 2:331-338. (Pubitemid 30491275)
20. Matthies HJ, Palfrey HC, Hirning LD, and Miller RJ (1987) Down-regulation of protein kinase C in neuronal cells: effects on neurotransmitter release. J Neurosci 7:1198-1206. (Pubitemid 17055362)
21. Monyer H, Burnashev N, Laurie DJ, Sakmann B, and Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540. (Pubitemid 24100885)
22. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, and Nakanishi S (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37. (Pubitemid 21896774)
23. Newton AC (2001) Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem Rev 101:2353-2364.
24. Ohno S and Nishizuka Y (2002) Protein kinase C isotypes and their specific functions: prologue. J Biochem 132:509-511. (Pubitemid 35238901)
25. Popp RL, Lickteig RL, and Lovinger DM (1999) Factors that enhance ethanol inhibition of N-methyl-D-aspartate receptors in cerebellar granule cells. J Pharmacol Exp Ther 289:1564-1574.
26. Popp RL, Velasquez O, Bland J, and Hughes P (2006) Characterization of protein kinase C isoforms in primary cultured cerebellar granule cells. Brain Res 1083: 70-84.
27. Popp RL and Dertien JS (2008) Actin depolymerization contributes to ethanol inhibition of NMDA receptors in primary cultured cerebellar granule cells. Alcohol 42:525-539.
28. Popp RL, Reneau JC, and Brotherton BJ (2008a) Activation of protein kinase C enhances NMDA-induced currents in primary cultured cerebellar granule cells: effect of temperature and NMDA NR2 subunit composition. Eur J Pharmacol 599:1-10.
29. Popp RL, Reneau JC, and Dertien JS (2008b) Cerebellar granule cells cultured from adolescent rats express functional N-methyl-D-aspartate receptors: an in vitro model for studying the developing cerebellum. J Neurochem 106:900-911.
30. Sánchez-Pérez AM and Felipo V (2005) Serines 890 and 896 of the NMDA receptor subunit NR1 are differentially phosphorylated by protein kinase C isoforms. Neurochem Int 47:84-91.
31. Scott DB, Blanpied TA, Swanson GT, Zhang C, and Ehlers MD (2001) An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J Neurosci 21:3063-3072. (Pubitemid 32323488)
32. Sigel E, Baur R, and Malherbe P (1994) Protein kinase C transiently activates heteromeric N-methyl-D-aspartate receptor channels independent of the phosphorylatable C-terminal splice domain and of consensus phosphorylation sites. J Biol Chem 269:8204-8208. (Pubitemid 24200232)
33. Tingley WG, Ehlers MD, Kameyama K, Doherty C, Ptak JB, Riley CT, and 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.
34. Tingley WG, Roche KW, Thompson AK, and Huganir RL (1993) Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364:70-73. (Pubitemid 23233458)
35. Tyszkiewicz JP, Gu Z, Wang X, Cai X, and Yan Z (2004) Group II metabotropic glutamate receptors enhance NMDA receptor currents via a protein kinase C-dependent mechanism in pyramidal neurones of rat prefrontal cortex. J Physiol 554:765-777. (Pubitemid 38219890)
36. Xiong ZG, Raouf R, Lu WY, Wang LY, Orser BA, Dudek EM, Browning MD, and MacDonald JF (1998) Regulation of N-methyl-D-aspartate receptor function by constitutively active protein kinase C. Mol Pharmacol 54:1055-1063. (Pubitemid 29002049)
37. Yamakura T, Mori H, Shimoji K, and Mishina M (1993) Phosphorylation of the carboxyl-terminal domain of the ζ1 subunit is not responsible for potentiation by TPA of the NMDA receptor channel. Biochem Biophys Res Commun 196:1537-1544. (Pubitemid 23347623)
38. 2+ influx amplifies protein kinase C potentiation of recombinant NMDA receptors. J Neurosci 17:8676-8686.
39. Zheng X, Zhang L, Wang AP, Bennett MV, and Zukin RS (1999) Protein kinase C potentiation of N-methyl-D-aspartate receptor activity is not mediated by phosphorylation of N-methyl-D-aspartate receptor subunits. Proc Natl Acad Sci U S A 96:15262-15267.