Regulation of ERK1/2 phosphorylation by acute and chronic morphine - Implications for the role of cAMP-responsive element binding factor (CREB)-dependent and Ets-like protein-1 (Elk-1)-dependent transcription; small interfering RNA-based strategy

FEBS Journal

Volumn 275, Issue 15, 2008, Pages 3836-3849

  Ligeza, Agnieszka ^a   Wawrzczak Bargiela, Agnieszka ^a   Kaminska, Dorota ^a   Korostynski, Michal ^a   Przewlocki, Ryszard ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

ERK; Opioids; Protein kinases; Protein phosphatases; RNA interference

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MORPHINE; MU OPIATE RECEPTOR; NALOXONE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR ELK 1;

ARTICLE; CELL FUNCTION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; RNA INTERFERENCE;

BLOTTING, WESTERN; CELL LINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ETS-DOMAIN PROTEIN ELK-1; GENE SILENCING; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MORPHINE; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC;

RATTUS;

EID: 47249125866     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06531.x     Document Type: Article

References (57)

1. Nestler EJ Aghajanian GK (1997) Molecular and cellular basis of addiction. Science 278, 58 63.
2. Nestler EJ (1997) Molecular mechanisms of opiate and cocaine addiction. Curr Opin Neurobiol 7, 713 719.
3. Granados-Soto V, Kalcheva I, Hua X, Newton A Yaksh TL (2000) Spinal PKC activity and expression: role in tolerance produced by continuous spinal morphine infusion. Pain 85, 395 404.
4. Parkitna JR, Obara I, Wawrzczak-Bargiela A, Makuch W, Przewlocka B Przewlocki R (2006) Effects of glycogen synthase kinase 3beta and cyclin-dependent kinase 5 inhibitors on morphine-induced analgesia and tolerance in rats. J Pharmacol Exp Ther 319, 832 839.
5. Fan GH, Wang LZ, Qiu HC, Ma L Pei G (1999) Inhibition of calcium/calmodulin-dependent protein kinase II in rat hippocampus attenuates morphine tolerance and dependence. Mol Pharmacol 56, 39 45.
6. Gutstein HB, Rubie EA, Mansour A, Akil H Woodgett JR (1997) Opioid effects on mitogen-activated protein kinase signaling cascades. Anesthesiology 87, 1118 1126.
7. Asensio VJ, Miralles A Garcia-Sevilla JA (2006) Stimulation of mitogen-activated protein kinase kinases (MEK1/2) by mu-, delta- and kappa-opioid receptor agonists in the rat brain: regulation by chronic morphine and opioid withdrawal. Eur J Pharmacol 539, 49 56.
8. Schulz S Hollt V (1998) Opioid withdrawal activates MAP kinase in locus coeruleus neurons in morphine-dependent rats in vivo. Eur J Neurosci 10, 1196 1201.
9. English JD Sweatt JD (1996) Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271, 24329 24332.
10. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1, 602 609.
11. Kelly A, Laroche S Davis S (2003) Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J Neurosci 23, 5354 5360.
12. Mazzucchelli C, Vantaggiato C, Ciamei A, Fasano S, Pakhotin P, Krezel W, Welzl H, Wolfer DP, Pages G, Valverde O et al. (2002) Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 34, 807 820.
13. Davis S, Vanhoutte P, Pages C, Caboche J Laroche S (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci 20, 4563 4572.
14. Ferrer-Alcon M, Garcia-Fuster J, La Harpe R Garcia-Sevilla JA (2004) Long-term regulation of signalling components of adenylyl cyclase and mitogen-activated protein kinase in the pre-frontal cortex of human opiate addicts. J Neurochem 90, 220 230.
15. Valjent E, Corvol JC, Pages C, Besson MJ, Maldonado R Caboche J (2000) Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J Neurosci 20, 8701 8709.
16. Valjent E, Pages C, Herve D, Girault JA Caboche J (2004) Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. Eur J Neurosci 19, 1826 1836.
17. Berhow MT, Hiroi N Nestler EJ (1996) Regulation of ERK (extracellular signal regulated kinase), part of the neurotrophin signal transduction cascade, in the rat mesolimbic dopamine system by chronic exposure to morphine or cocaine. J Neurosci 16, 4707 4715.
18. Narita M, Ioka M, Suzuki M, Narita M Suzuki T (2002) Effect of repeated administration of morphine on the activity of extracellular signal regulated kinase in the mouse brain. Neurosci Lett 324, 97 100.
19. Chalmers CJ, Gilley R, March HN, Balmanno K Cook SJ (2007) The duration of ERK1/2 activity determines the activation of c-Fos and Fra-1 and the composition and quantitative transcriptional output of AP-1. Cell Signal 19, 695 704.
20. Traverse S, Seedorf K, Paterson H, Marshall CJ, Cohen P Ullrich A (1994) EGF triggers neuronal differentiation of PC12 cells that overexpress the EGF receptor. Curr Biol 4, 694 701.
21. Traverse S, Gomez N, Paterson H, Marshall C Cohen P (1992) Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem J 288, 351 355.
22. Camps M, Nichols A Arkinstall S (2000) Dual specificity phosphatases: a gene family for control of MAP kinase function. FASEB J 14, 6 16.
23. Choe ES, Parelkar NK, Kim JY, Cho HW, Kang HS, Mao L Wang JQ (2004) The protein phosphatase 1/2A inhibitor okadaic acid increases CREB and Elk-1 phosphorylation and c-fos expression in the rat striatum in vivo. J Neurochem 89, 383 390.
24. Casillas AM, Amaral K, Chegini-Farahani S Nel AE (1993) Okadaic acid activates p42 mitogen-activated protein kinase (MAP kinase; ERK-2) in B-lymphocytes but inhibits rather than augments cellular proliferation: contrast with phorbol 12-myristate 13-acetate. Biochem J 290, 545 550.
25. Gabra BH, Bailey CP, Kelly E, Sanders AV, Henderson G, Smith FL Dewey WL (2007) Evidence for an important role of protein phosphatases in the mechanism of morphine tolerance. Brain Res 1159, 86 93.
26. Brondello JM, Brunet A, Pouyssegur J McKenzie FR (1997) The dual specificity mitogen-activated protein kinase phosphatase-1 and -2 are induced by the p42/p44MAPK cascade. J Biol Chem 272, 1368 1376.
27. 2+-dependent signal pathways in Rat-1 cells. J Biol Chem 272, 13309 13319.
28. Bilecki W, Zapart G, Ligeza A, Wawrzczak-Bargiela A, Urbanski MJ Przewlocki R (2005) Regulation of the extracellular signal-regulated kinases following acute and chronic opioid treatment. Cell Mol Life Sci 62, 2369 2375.
29. Sgambato V, Pages C, Rogard M, Besson MJ Caboche J (1998) Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation. J Neurosci 18, 8814 8825.
30. Nestler EJ (2004) Molecular mechanisms of drug addiction. Neuropharmacology 47 (Suppl. 1 24 32.
31. Hipskind RA, Rao VN, Mueller CG, Reddy ES Nordheim A (1991) Ets-related protein Elk-1 is homologous to the c-fos regulatory factor p62TCF. Nature 354, 531 534.
32. Bot G, Blake AD, Li S Reisine T (1997) Opioid regulation of the mouse delta-opioid receptor expressed in human embryonic kidney 293 cells. Mol Pharmacol 52, 272 281.
33. Eisinger DA Schulz R (2004) Extracellular signal-regulated kinase/mitogen-activated protein kinases block internalization of delta-opioid receptors. J Pharmacol Exp Ther 309, 776 785.
34. Johnson EA, Oldfield S, Braksator E, Gonzalez-Cuello A, Couch D, Hall KJ, Mundell SJ, Bailey CP, Kelly E Henderson G (2006) Agonist-selective mechanisms of mu-opioid receptor desensitization in human embryonic kidney 293 cells. Mol Pharmacol 70, 676 685.
35. Pfeiffer M, Koch T, Schroder H, Laugsch M, Hollt V Schulz S (2002) Heterodimerization of somatostatin and opioid receptors cross-modulates phosphorylation, internalization, and desensitization. J Biol Chem 277, 19762 19772.
36. Koch T, Schulz S, Pfeiffer M, Klutzny M, Schroder H, Kahl E Hollt V (2001) C-terminal splice variants of the mouse mu-opioid receptor differ in morphine-induced internalization and receptor resensitization. J Biol Chem 276, 31408 31414.
37. Arden JR, Segredo V, Wang Z, Lameh J Sadee W (1995) Phosphorylation and agonist-specific intracellular trafficking of an epitope-tagged mu-opioid receptor expressed in HEK 293 cells. J Neurochem 65, 1636 1645.
38. Blake AD, Bot G, Freeman JC Reisine T (1997) Differential opioid agonist regulation of the mouse mu opioid receptor. J Biol Chem 272, 782 790.
39. Quillan JM, Carlson KW, Song C, Wang D Sadee W (2002) Differential effects of mu-opioid receptor ligands on Ca(2+) signaling. J Pharmacol Exp Ther 302, 1002 1012.
40. Belcheva MM, Szucs M, Wang D, Sadee W Coscia CJ (2001) mu-Opioid receptor-mediated ERK activation involves calmodulin-dependent epidermal growth factor receptor transactivation. J Biol Chem 276, 33847 33853.
41. Tso PH Wong YH (2001) Opioid-induced adenylyl cyclase supersensitization in human embryonic kidney 293 cells requires pertussis toxin-sensitive G proteins other than G(i1) and G(i3). Neurosci Lett 299, 25 28.
42. Schmidt H, Schulz S, Klutzny M, Koch T, Handel M Hollt V (2000) Involvement of mitogen-activated protein kinase in agonist-induced phosphorylation of the mu-opioid receptor in HEK 293 cells. J Neurochem 74, 414 422.
43. Zheng H, Loh HH Law PY (2008) Beta-arrestin-dependent mu-opioid receptor-activated extracellular signal-regulated kinases (ERKs) translocate to nucleus in contrast to G protein-dependent ERK activation. Mol Pharmacol 73, 178 190.
44. Rios C, Gomes I Devi LA (2006) mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br J Pharmacol 148, 387 395.
45. Belcheva MM, Wong YH Coscia CJ (2000) Evidence for transduction of mu but not kappa opioid modulation of extracellular signal-regulated kinase activity by G(z) and G(12) proteins. Cell Signal 12, 481 489.
46. Kodama M, Russell DS Duman RS (2005) Electroconvulsive seizures increase the expression of MAP kinase phosphatases in limbic regions of rat brain. Neuropsychopharmacology 30, 360 371.
47. Levinthal DJ Defranco DB (2005) Reversible oxidation of ERK-directed protein phosphatases drives oxidative toxicity in neurons. J Biol Chem 280, 5875 5883.
48. Vickers ER, Kasza A, Kurnaz IA, Seifert A, Zeef LA, O'Donnell A, Hayes A Sharrocks AD (2004) Ternary complex factor-serum response factor complex-regulated gene activity is required for cellular proliferation and inhibition of apoptotic cell death. Mol Cell Biol 24, 10340 10351.
49. Cesari F, Brecht S, Vintersten K, Vuong LG, Hofmann M, Klingel K, Schnorr JJ, Arsenian S, Schild H, Herdegen T et al. (2004) Mice deficient for the ets transcription factor elk-1 show normal immune responses and mildly impaired neuronal gene activation. Mol Cell Biol 24, 294 305.
50. 2+ rise and subsequent cyclic AMP response element-binding protein activation in hippocampal neurons: a potential initiation mechanism for estrogen neurotrophism. Neuroscience 132, 299 311.
51. Levenson JM, Choi S, Lee SY, Cao YA, Ahn HJ, Worley KC, Pizzi M, Liou HC Sweatt JD (2004) A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel. J Neurosci 24, 3933 3943.
52. Kwak SP, Hakes DJ, Martell KJ Dixon JE (1994) Isolation and characterization of a human dual specificity protein-tyrosine phosphatase gene. J Biol Chem 269, 3596 3604.
53. Takaki M, Ujike H, Kodama M, Takehisa Y, Nakata K Kuroda S (2001) Two kinds of mitogen-activated protein kinase phosphatases, MKP-1 and MKP-3, are differentially activated by acute and chronic methamphetamine treatment in the rat brain. J Neurochem 79, 679 688.
54. Camps M, Chabert C, Muda M, Boschert U, Gillieron C Arkinstall S (1998) Induction of the mitogen-activated protein kinase phosphatase MKP3 by nerve growth factor in differentiating PC12. FEBS Lett 425, 271 276.
55. Grill C, Gheyas F, Dayananth P, Jin W, Ding W, Qiu P, Wang L, Doll RJ English JM (2004) Analysis of the ERK1,2 transcriptome in mammary epithelial cells. Biochem J 381, 635 644.
56. Ryser S, Massiha A, Piuz I Schlegel W (2004) Stimulated initiation of mitogen-activated protein kinase phosphatase-1 (MKP-1) gene transcription involves the synergistic action of multiple cis-acting elements in the proximal promoter. Biochem J 378, 473 484.
57. Chomczynski P Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162, 156 159.