MAPKAP kinase-2 is a primary response gene induced by depolarization in PC12 cells and in brain

Journal of Neuroscience Research

Volumn 78, Issue 3, 2004, Pages 315-328

  Vician, Linda J ^a,b   Xu, Guoping ^b   Liu, Wei ^a,b   Feldman, Jonathan D ^b   Machado, Hidevaldo B ^a,c   Herschman, Harvey R ^a,b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Depolarization; Immediate early gene; MAPKAPK2; PC12 cells

Indexed keywords

COMPLEMENTARY DNA; FORSKOLIN; GENE PRODUCT; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE ACTIVATED PROTEIN KINASE 2; PROLINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BRAIN CELL; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE DEPOLARIZATION; CELL STRAIN; CONTROLLED STUDY; DENTATE GYRUS; DIFFERENTIAL DISPLAY; ENZYME INDUCTION; ENZYME REPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE INDUCTION; GENE LIBRARY; GENETIC TRANSCRIPTION; HIPPOCAMPUS; INTRON; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT; SEIZURE;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, NORTHERN; BLOTTING, SOUTHERN; BRAIN; CALCIUM; CELL DIFFERENTIATION; CLONING, MOLECULAR; CYCLOHEXIMIDE; DRUG INTERACTIONS; ENZYME ACTIVATION; EXCITATORY AMINO ACID AGONISTS; FORSKOLIN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IN SITU HYBRIDIZATION; KAINIC ACID; MALE; MOLECULAR SEQUENCE DATA; PC12 CELLS; POTASSIUM CHLORIDE; PROTEIN SYNTHESIS INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TIME FACTORS;

EID: 8444224709     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20251     Document Type: Article

References (70)

1. Bailey CH, Giustetto M, Huang YY, Hawkins RD, Kandel ER. 2000. Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nat Rev Neurosci 1:11-20.
2. Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, Kumar S, Badger AM, White RF, McVey MJ, Legos JJ, Erhardt JA, Nelson AH, Ohlstein EH, Hunter AJ, Ward K, Smith BR, Adams JL, Parsons AA. 2001. SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia. J Pharmacol Exp Ther 296:312-321.
3. Blanquet PR, Mariani J, Derer P. 2003. A calcium/calmodulin kinase pathway connects brain-derived neurotrophic factor to the cyclic AMP-responsive transcription factor in the rat hippocampus. Neuroscience 118:477-490.
4. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term memory in mice with a targeted mutation of the cAMP- responsive element-binding protein. Cell 79:59-68.
5. Carballo E, Cao H, Lai WS, Kennington EA, Campbell D, Blackshear PJ. 2001. Decreased sensitivity of tristetraprolin-deficient cells to p38 inhibitors suggests the involvement of tristetraprolin in the p38 signaling pathway. J Biol Chem 276:42580-42587.
6. Chang L, Karin M. 2001. Mammalian MAP kinase signalling cascades. Nature 410:37-40.
7. Chen CY, Gherzi R, Ong SE, Chan EL, Raijmakers R, Pruijn GJ, Stoecklin G, Moroni C, Mann M, Karin M. 2001. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107:451-464.
8. Chen CY, Shyu AB. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20:465-470.
9. Cheng TJ, Lai YK. 1998. Identification of mitogen-activated protein kinase-activated protein kinase-2 as a vimentin kinase activated by okadaic acid in 9L rat brain tumor cells. J Cell Biochem 71:169-181.
10. Clifton AD, Young PR, Cohen P. 1996. A comparison of the substrate specificity of MAPKAP kinase-2 and MAPKAP kinase-3 and their activation by cytokines and cellular stress. FEBS Lett 392:209-214.
11. Cohen P. 1996. Dissection of protein kinase cascades that mediate cellular response to cytokines and cellular stress. Adv Pharmacol 36:15-27.
12. Crispino M, Tocco G, Feldman JD, Herschman HR, Baudry M. 1998. Nurr1 mRNA expression in neonatal and adult rat brain following kainic acid-induced seizure activity. Brain Res Mol Brain Res 59:178-188.
13. Dean JL, Brook M, Clark AR, Saklatvala J. 1999. p38 mitogen-activated protein kinase regulates cyclooxygenase-2 mRNA stability and transcription in lipopolysaccharide-treated human monocytes. J Biol Chem 274:264-269.
14. Donohue PJ, Alberts GF, Guo Y, Winkles JA. 1995. Identification by targeted differential display of an immediate early gene encoding a putative serine/threonine kinase. J Biol Chem 270:10351-10357.
15. Engel K, Plath K, Gaestel M. 1993. The MAP kinase-activated protein kinase 2 contains a proline-rich SH3- binding domain. FEBS Lett 336:143-147.
16. Fambrough D, McClure K, Kazlauskas A, Lander ES. 1999. Diverse signaling pathways activated by growth factor receptors induce broadly overlapping, rather than independent, sets of genes. Cell 97:727-741.
17. Feldman JD, Vician L, Crispino M, Tocco G, Baudry M, Herschman HR. 1998a. Seizure activity induces PIM-1 expression in brain. J Neurosci Res 53:502-509.
18. Feldman JD, Vician L, Crispino M, Tocco G, Marcheselli VL, Bazan NG, Baudry M, Herschman HR. 1998b. KID-1, a protein kinase induced by depolarization in brain. J Biol Chem 273:16535-16543.
19. Feldman JD, Vician L, Crispino M, Hoe W, Baudry M, Herschman HR. 2000a. rTLE3, a newly identified transducin-like enhancer of split, is induced by depolarization in brain. J Neurochem 74:1838-1847.
20. Feldman JD, Vician L, Crispino M, Hoe W, Baudry M, Herschman HR. 2000b. The salt-inducible kinase, SIK, is induced by depolarization in brain. J Neurochem 74:2227-2238.
21. Ferguson GD, Anagnostaras SG, Silva AJ, Herschman HR. 2000. Deficits in memory and motor performance in synaptotagmin IV mutant mice. Proc Natl Acad Sci USA 97:5598-5603.
22. Fort P, Marty L, Piechaczyk M, el Sabrouty S, Dani C, Jeanteur P, Blanchard JM. 1985. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res 13:1431-1442.
23. Hanks SK, Quinn AM. 1991. Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Methods Enzymol 200:38-62.
24. Heidenreich O, Neininger A, Schratt G, Zinck R, Cahill MA, Engel K, Kotlyarov A, Kraft R, Kostka S, Gaestel M, Nordheim A. 1999. MAPKAP kinase 2 phosphorylates serum response factor in vitro and in vivo. J Biol Chem 274:14434-14443.
25. Herschman HR. 1991. Primary response genes induced by growth factors and tumor promoters. Annu Rev Biochem 60:281-319.
26. Herschman HR, Ferguson GD, Feldman JD, Farias-Eisner R, Vician L. 2000. Searching for depolarization-induced genes that modulate synaptic plasticity and neurotrophin-induced genes that mediate neuronal differentiation. Neurochem Res 25:591-602.
27. Hoover HE, Thuerauf DJ, Martindale JJ, Glembotski CC. 2000. Alpha B-crystallin gene induction and phosphorylation by MKK6-activated p38. A potential role for alpha 13 crystallin as a target of the p38 branch of the cardiac stress response. J Biol Chem 275:23825-23833.
28. Hsu DK, Donohue PJ, Alberts GF, Winkles JA. 1993. Fibroblast growth factor-1 induces phosphofructokinase, fatty acid synthase and Ca(2+)-ATPase mRNA expression in NIH 3T3 cells. Biochem Biophys Res Commun 197:1483-1491.
29. Huang CK, Zhan L, Ai Y, Jongstra J. 1997. LSP1 is the major substrate for mitogen-activated protein kinase- activated protein kinase 2 in human neutrophils. J Biol Chem 272:17-19.
30. Huang YY, Kandel ER. 1994. Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1:74-82.
31. Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR. 1998. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1:595-601.
32. Konat GW, Laszkiewiewicz I, Grubinska B, Wiggins RC. 1994. Generation of labeled DNA probes by PCR. In: Griffin GH, Griffin AM, editors. PCR technology: current innovations. Boca Raton: CRC Press, p 37-42.
33. Konietzko U, Kauselmann G, Scafidi J, Staubli U, Mikkers H, Berns A, Schweizer M, Waltereit R, Kuhl D. 1999. Pim kinase expression is induced by LTP stimulation and required for the consolidation of enduring LTP. EMBO J 18:3359-3369.
34. Kontoyiannis D, Kotlyarov A, Carballo E, Alexopoulou L, Blackshear PJ, Gaestel M, Davis R, Flavell R, Kollias G. 2001. Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J 20:3760-3770.
35. Kotlyarov A, Neininger A, Schubert C, Eckert R, Birchmeier C, Volk HD, Gaestel M. 1999. MAPKAP kinase 2 is essential for LPS-induced TNF-alpha biosynthesis. Nat Cell Biol 1:94-97.
36. Kyriakis JM, Avruch J. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807-869.
37. Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ. 1999. Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19:4311-4323.
38. Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ. 2000. Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA. J Biol Chem 275:17827-17837.
39. Lasa M, Mahtani KR, Finch A, Brewer G, Saklatvala J, Clark AR. 2000. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol Cell Biol 20:4265-4274.
40. Lipson KE, Baserga R. 1989. Transcriptional activity of the human thymidine kinase gene determined by a method using the polymerase chain reaction and an intron-specific probe. Proc Natl Acad Sci USA 86:9774-9777.
41. Mahtani KR, Brook M, Dean JL, Sully G, Saklatvala J, Clark AR. 2001. Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability. Mol Cell Biol 21:6461-6469.
42. Maizels ET, Mukherjee A, Sithanandam G, Peters CA, Cottom J, Mayo KE, Hunzicker-Dunn M. 2001. Developmental regulation of mitogen-activated protein kinase-activated kinases-2 and -3 (MAPKAPK-2/-3) in vivo during corpus luteum formation in the rat. Mol Endocrinol 15:716-733.
43. Martin SJ, Grimwood PD, Morris RG. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
44. McLaughlin MM, Kumar S, McDonnell PC, Van Horn S, Lee JC, Livi GP, Young PR. 1996. Identification of mitogen-activated protein (MAP) kinase-activated protein kinase-3, a novel substrate of CSBP p38 MAP kinase. J Biol Chem 271:8488-8492.
45. Michel AD, Grahames CB, Humphrey PP. 1996. Functional characterisation of P2 purinoceptors in PC12 cells by measurement of radiolabelled calcium influx. Naunyn Schmiedebergs Arch Pharmacol 354:562-571.
46. Ming XF, Stoecklin G, Lu M, Looser R, Moroni C. 2001. Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol Cell Biol 21:5778-5789.
47. Morris DR, Geballe AP. 2000. Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20:8635-8642.
48. Neininger A, Kontoyiannis D, Kotlyarov A, Winzen R, Eckert R, Volk HD, Holtmann H, Kollias G, Gaestel M. 2002. MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post- transcriptional levels. J Biol Chem 277:3065-3068.
49. Neufeld B, Grosse-Wilde A, Hoffmeyer A, Jordan BW, Chen P, Dinev D, Ludwig S, Rapp UR. 2000. Serine/threonine kinases 3pK and MAPK-activated protein kinase 2 interact with the basic helix-loop-helix transcription factor E47 and repress its transcriptional activity. J Biol Chem 275:20239-20242.
50. Poser S, Storm DR. 2001. Role of Ca2+-stimulated adenylyl cyclases in LTP and memory formation. Int J Dev Neurosci 19:387-394.
51. Rane MJ, Coxon PY, Powell DW, Webster R, Klein JB, Pierce W, Ping P, McLeish KR. 2001. p38 Kinase-dependent MAPKAPK-2 activation functions as 3-phosphoinositide-dependent kinase-2 for Akt in human neutrophils. J Biol Chem 276:3517-3523.
52. Reynolds LJ, Richards RJ. 2001. Can toxicogenomics provide information on the bioreactivity of diesel exhaust particles? Toxicology 165:145-152.
53. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Plainview, NY: Cold Spring Harbor Laboratory Press.
54. Sithanandam G, Latif F, Duh FM, Bernal R, Smola U, Li H, Kuzmin I, Wixler V, Geil L, Shrestha S. 1996. 3pK, a new mitogen-activated protein kinase-activated protein kinase located in the small cell lung cancer tumor suppressor gene region. Mol Cell Biol 16:868-876.
55. Stokoe D, Campbell DG, Nakielny S, Hidaka H, Leevers SJ, Marshall C, Cohen P. 1992a. MAPKAP kinase-2; a novel protein kinase activated by mitogen-activated protein kinase. EMBO J 11:3985-3994.
56. Stokoe D, Caudwell B, Cohen PT, Cohen P. 1993. The substrate specificity and structure of mitogen-activated protein (MAP) kinase-activated protein kinase-2. Biochem J 296:843-849.
57. Stokoe D, Engel K, Campbell DG, Cohen P, Gaestel M. 1992b. Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Lett 313:307-313.
58. Sutherland C, Alterio J, Campbell DG, Le Bourdelles B, Mallet J, Haavik J, Cohen P. 1993. Phosphorylation and activation of human tyrosine hydroxylase in vitro by mitogen-activated protein (MAP) kinase and MAP-kinase-activated kinases 1 and 2. Eur J Biochem 217:715-722.
59. Tan Y, Rouse J, Zhang A, Cariati S, Cohen P, Comb MJ. 1996. FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase-2. EMBO J 15:4629-4642.
60. Vician L, Lim IK, Ferguson G, Tocco G, Baudry M, Herschman HR. 1995. Synaptotagmin IV is an immediate early gene induced by depolarization in PC12 cells and in brain. Proc Natl Acad Sci USA 92:2164-2168.
61. Vician L, Silver AL, Farias-Eisner R, Herschman HR. 2001. NID67, a small putative membrane protein, is preferentially induced by NGF in PC12 pheochromocytoma cells. J Neurosci Res 64:108-120.
62. Wang X, Xu L, Wang H, Young PR, Gaestel M, Feuerstein GZ. 2002. Mitogen-activated protein kinase-activated protein (MAPKAP) kinase 2 deficiency protects brain from ischemic injury in mice. J Biol Chem 277:43968-43972.
63. Werz O, Klemm J, Samuelsson B, Radmark O. 2000. 5-Lipoxygenase is phosphorylated by p38 kinase-dependent MAPKAP kinases. Proc Natl Acad Sci USA 97:5261-5266.
64. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, Takasu MA, Tao X, Greenberg ME. 2001. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 98:11024-11031.
65. Wingett D, Reeves R, Magnuson NS. 1991. Stability changes in pim-1 proto-oncogene mRNA after mitogen stimulation of normal lymphocytes. J Immunol 147:3653-3659.
66. Winzen R, Kracht M, Ritter B, Wilhelm A, Chen CY, Shyu AB, Muller M, Gaestel M, Resell K, Holtmann H. 1999. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J 18:4969-4980.
67. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
68. Xing J, Kornhauser JM, Xia Z, Thiele EA, Greenberg ME. 1998. Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol Cell Biol 18:1946-1955.
69. Zhu W, Brauchle MA, Di Padova F, Gram H, New L, Ono K, Downey JS, Han J. 2001. Gene suppression by tristetraprolin and release by the p38 pathway. Am J Physiol Lung Cell Mol Physiol 281:499-508.
70. Zu YL, Wu F, Gilchrist A, Ai Y, Labadia ME, Huang CK. 1994. The primary structure of a human MAP kinase activated protein kinase 2. Biochem Biophys Res Commun 200:1118-1124.