Identification of mitogen-activated protein kinase-activated protein kinase-2 as a vimentin kinase activated by okadaic acid in 9L rat brain tumor cells

Journal of Cellular Biochemistry

Volumn 71, Issue 2, 1998, Pages 169-181

  Cheng, Ting Jen ^a   Lai, Yiu Kay ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

Intermediate filaments; Kinase activated protein kinase 2; Mitogen activated protein; Okadaic acid; Phosphorylation; Vimentin

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; OKADAIC ACID; PHOSPHATASE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; VIMENTIN; VIMENTIN KINASE;

AMINO ACID ANALYSIS; ANIMAL CELL; ARTICLE; BRAIN TUMOR; CYTOSKELETON; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; BRAIN NEOPLASMS; CYTOSOL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME ACTIVATION; GLIOSARCOMA; IMIDAZOLES; KINETIN; OKADAIC ACID; PEPTIDE MAPPING; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PURINES; PYRIDINES; RATS; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0031668989     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(19981101)71:2<169::AID-JCB3>3.0.CO;2-T     Document Type: Article

References (61)

1. Ando S, Tanabe K, Gonda Y, Sato C, Inagaki M (1989): Domain-and sequence-specific phosphorylation of vimentin induces diassembly of the filament structure. Biochemistry 28:2974-2979.
2. Ando S, Tokui T, Yamauchi T, Sugiura H, Tanabe K, Inagaki M (1991): Evidence that ser-82 is a unique phosphorylation site on vimentin for Ca2+-calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 175: 955-962.
3. Bialojan C, Takai A (1988): Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem J 256:283-290.
4. Boyle WJ, van der Geer P, Hunter T (1991): Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. In Hunter T, Sefton BM, eds. "Protein Phosphorylation," Part B. San Diego: Academic Press, pp 110-148.
5. Bradford MM (1976): A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
6. Cano E, Doza YN, Ben-Levy R, Cohen P, Mahadevan LC (1996): Identification of anisomycin-activated kinases p45 and p55 in murine cells as MAPKAP kinase-2. Oncogene 12:805-812.
7. Chou Y-H, Opal P, Quinlan RA, Goldman RD (1996): The relative roles of specific N-and C-terminal phosphorylation sites in the disassembly of intermediate filament in mitotic BHK-21 cells. J Cell Sci 109:817-826.
8. Cohen P (1992): Signal integration at the level of protein kinases, protein phosphatases and their substrates. Trends Biochem Sci 17:408-413.
9. Couldwell WT, Hinton DR, He S, Chen TC, Sebat I, Weiss MH, Law RE (1994): Protein kinase C inhibitors induce apoptosis in human malignant glioma cell lines. FEBS Lett 345:43-46.
10. Engel K, Ahlers A, Brach MA, Herrmann F, Gaestel M (1995): MAPKAP kinase 2 is activated by heat shock and TNF-α: In vivo phosphorylation of small heat shock protein results from stimulation of the MAP kinase cascade. J Cell Biochem 57:321-330.
11. Eriksson JE, Brautigan DL, Valle R, Olmsted J, Fujiki H, Goldman RD (1992a): Cytoskeletal integrity in interphase cells requires protein phosphatase activity. Proc Natl Acad Sci USA 89:11093-11097.
12. Eriksson JE, Opal P, Goldman RD (1992b): Intermediate filament dynamics. Curr Opin Cell Biol 4:99-104.
13. Gadbois DM (1992): Staurosporine is a potent inhibitor of p34 cdc2 and p34 cdc2-like kinases. Biochem Biophys Res Commun 184:80-85.
14. Gaestel M, Schroder W, Benndorf R, Lippmann C, Buchner K, Hucho F, Erdmann VA, Bielka H (1991): Identification of the phosphorylation sites of the murine small heat-shock protein hsp25. J Biol Chem 266:14721-14724.
15. Gard DL, Lazarides E (1982): Analysis of desmin and vimentin phosphopeptides in cultured avian myogenic cells and their modulation by 8-bromo-adenosine 3′,5′-cyclic monophosphate. Proc Natl Acad Sci USA 79:6912-6916.
16. Giasson BI, Cromlish JA, Athlan ES, Mushynske WE (1996): Activation of cyclic AMP-dependent protein kinase in okadaic acid-treated neurons potentiates neurophilament fragmentation and stimulates phosphorylation of Ser-2 in the low-molecular-mass neurofilament subunit. J Neurochem 66:1207-1213.
17. Guy GR, Philip R, Tan YH (1995): Activation of protein kinases and the inactivation of protein phosphatase 2A in tumor necrosis factor and interleukin-1 signal-transduction pathways. Eur J Biochem 229:503-511.
18. Hagiwara M, Inagaki M, Hidaka H (1987): Specific binding of a novel compound, N-[2-(methylamino)ethyl]-5-isoquinolinesulfonamide (H-8) to the active site of cAMP-dependent protein kinase. Mol Pharmacol 31:523-528.
19. Han J, Lee JD, Bibbs L, Ulevitch RJ (1994): A Map kinase targeted by endotoxin and hyperosmolarity in mammalian-cells. Science 265:808-811.
20. Hidaka H, Inagaki M, Kawamato S, Sasaki Y (1984): Isoquinolinesulfonamide, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23:5036-5041.
21. Hirano K, Hartshorne DJ (1993): Phosphorylation of vimentin in the C-terminal domain after exposure to calculin-A. Eur J Cell Biol 62:59-65.
22. Ho DT, Roberge M (1996): The antitumor drug fostriecin induces vimentin hyperphosphorylation and intermediate filament reorganization. Carcinogen 17:967-972.
23. 411 in vimentin and thereby inhibits cytoskeletal intermediate filament assembly. J Protein Chem 13:517-525.
24. Huot J, Lambert H, Lavoie JN, Guimond A, Houle F, Landry J (1995): Characterization of 45-kDa/54-kDa HSP27 kinase, a stress-sensitive kinase which may activate the phosphorylation-dependent protective function of mammalian 27-kDa heat-shock protein HSP27. Eur J Biochem 227:416-427.
25. Ido M, Nagao Y, Higashigawa M, Shibata T, Taniguchi K, Hamazaki M, Sakurai M (1991): Differential growth inhibition of isoquinolinesulfonamides H-8 and H-7 towards multidrug-resistant P388 murine leukaemia cells. Br J Cancer 64:1103-1107.
26. Inagaki M, Kawamato S, Itoh H, Saitoh M, Hagiwara M, Takahashi J, Hidaka H (1986): Naphthalenesulfonamides as calmodulin antagonists and protein kinase inhibitors. Mol Pharmacol 29:577-581.
27. Inagaki M, Matsuoka Y, Isujimura K, Ando S, Tokui T, Takahashi T, Inagaki N (1996): Dynamic property of intermediate filaments: Regulation by phosphorylation. BioEssays 18:481-487.
28. Inagaki M, Nishi Y, Nishizawa K, Matsuyama M, Sato C (1987): Site-specific phosphorylation induces disassembly of vimentin in vitro. Nature 328:649-652.
29. Inagaki N, Ito M, Nakano T, Inagaki M (1994): Spatiotemporal distribution of protein kinase and phosphatase activities. Trends Biochem Sci 19:448-452.
30. Jarvis WD, Turner AJ, Povrik LF, Taylor RS, Grant S (1994): Induction of apoptotic DNA fragmentation and cell death in HL-60 human promyelocytic leukemia cells by pharmacological inhibitors of protein kinase C. Cancer Res 54:1707-1714.
31. Kasahara K, Kartasova T, Ren X-q, Ikuta T, Chida K, Kuroki T (1993): Hyperphosphorylation of keratins by treatment of okadaic acid of BALB/MK-2 mouse keratinocytes. J Biol Chem 268:23531-23537.
32. Kase H, Iwahashi K, Nakanishi S, Matsuda Y, Yamada K (1987): K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochem Biophys Res Commun 142:436-440.
33. Kawamato S, Hidaka H (1984): 1-(5-Isoquinolinesulfonyl)-2-methylpiperazine (H-7) is a selective inhibitor of protein kinase C in rabbit platelets. Biochem Biophys Res Commun 125:258-264.
34. Laemmli UK (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Lai Y-K, Lee W-C, Chen K-D (1993): Vimentin serves as a phosphate sink during the apparent activation of protein kinases by okadaic acid in mammalian cells. J Cell Biochem 53:161-168.
36. Lamb NJC, Fernandez A, Feramisco JR, Welch WJ (1989): Modulation of vimentin containing intermediate filament distribution and phosphorylation in living fibroblasts by the cAMP-dependent protein kinases. J Cell Biol 108:2409-2422.
37. Lee W-C, Yu J-S, Yang S-D, Lai Y-K (1992): Reversible hyperphosphorylation and reorganization of vimentin intermediate filaments by okadaic acid in 9L rat brain tumor cells. J Cell Biochem 50:1-16.
38. Liauw S, Steinberg RA (1996): Dephosphorylation of catalytic subunit of cAMP-dependent protein kinase at Thr-197 by a cellular protein phosphatase and by purified protein phosphatase 2A. J Biol Chem 271:258-263.
39. Matsuzawa K, Kosaki H, Inagaki N, Shibata H, Mukai H, Ono Y, Amano M, Kaibuchi K, Matsuura Y, Azuma I, Inagaki M (1997): Domain-specific phosphorylation of vimentin and glial fibrillary acidic protein by PKN. Biochem Biophys Res Commun 234:621-625.
40. Maulik N, Watanabe M, Zu Y-L, Huang C-K, Cordis GA, Schley JA, Das DK (1996): Ischemic preconditioning triggers the activation of MAP kinases and MAPKAP kinase 2 in rat hearts. FEBS Lett 396:233-237.
41. Mumby MC, Walter G (1993): Protein serine/threonine phosphatases: Structure, regulation and functions in cell growth. Physiol Rev 73:673-699.
42. Perng M-D, Cheng T-J, Chen C-M, Lai Y-K (1994): Induction of aggregation and augmentation of protein kinase-mediated phosphorylation of purified vimentin intermediate filaments by Withangulatin A. Mol Pharmacol 46: 612-617.
43. Pryzwansky KB, Wyatt TA, Lincoln TM (1995): Cyclic guanosine monophosphate-dependent protein kinase is targeted to intermediate filaments and phosphorylates vimentin in A23187-stimulated human neutrophils. Blood 85:222-230.
44. Roberge M, Tudan C, Hung SMF, Harder KW, Jirik FR (1994): Antitumor drug fostriecin inhibits the mitotic entry checkpoint and protein phosphatases 1 and 2A. Cancer Res 54:6115-6121.
45. Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, Hunt T, Nebreda AR (1994): A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78:1027-1037.
46. Saklatvala J, Rawlinson L, Waller RJ, Sarsfield S, Lee JC, Morton LF, Barnes, MJ, Farndale RW (1996): Role of the p38 mitogen-activated protein kinase in platelet aggregation caused by collagen or a thromboxane analogues. J Biol Chem 271:6586-6589.
47. Schachtele C, Seifert R, Osswald H (1988): Stimulus-dependent inhibition of platelet aggregation caused by collagen or a thromboxane analogue. Biochem Biophys Res Commun 151:542-547.
48. Stokoe D, Campbell DG, Nakielny S, Hidaka H, Leevers SJ, Marshall C, Cohen P (1992): MAPKAP kinase-2, a novel protein kinase activated by mitogen-activated protein kinase. EMBO J 11:3985-3994.
49. 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 kinase-1 and kinase-2. Eur J Biochem 217:715-722.
50. Toivola DM, Goldman RD, Garrod DR, Eriksson JE (1997): Protein phosphatases maintain the organization and structural interactions of hepatic keratin intermediate filaments. J Cell Sci 110:23-33.
51. Tokumitsu H, Chijiwa T, Hagiwara M, Mizuitani A, Terusawa M, Hidaka H (1990): KN-62, 1-[N,O-bis(5-isoquinolinesulfonyl)-N-methyl-L-tyrosyl]-4-phenylpiperazine, a specific inhibitor of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 265:4315-4320.
52. Tsujimura K, Ogawara M, Takeuchi Y, Imajoh-Ohmi S, Ha MH, Inagaki M (1994): Visualization and function of vimentin phosphorylation by cdc2 kinase during mitosis. J Biol Chem 269:31097-31106.
53. Vesely J, Havlicek L, Strnad M, Blow JJ, Donella-Deana A, Dinna L, Letham DS, Kato J, Detivand L, Leclerc S, Al E (1994): Inhibition of cyclin-dependent kinases by purine analogues. Eur J Biochem 224:771-786.
54. Vitale ML, Rodriguez Del Castillo A, Trifaro JM (1992): Protein kinase C activation by phorbol esters induces chromaffin cell cortical filamentous actin disassembly and increases the initial rate of exocytosis in response to nicotinic receptor stimulation. Neuroscience 51:463-474.
55. Walker TP, Watson SP (1992): Okadaic acid inhibits activation of phospholipase C in human platelets by mimicking the actions of protein kinases A and C. Br J Pharmacol 105:627-631.
56. Weizsaecker M, Deen DF, Rosenblum ML, Hoshino T, Gutin PH, Barker M (1981): The 9L rat brain tumor: Description and application of an animal model. J Neurol 224: 183-192.
57. Yamashita K, Yasuda H, Pines J, Yasumoto K, Nishitani H, Ohtsubo M, Hunter T, Sugimura T, Nishimoto T (1990): Okadaic acid, a potent inhibitor of type 1 and type A protein phosphatases, activates cdc2/H1 kinase and transiently induces a premature mitosis-like state in BHK21 cells. EMBO J 9:4331-4338.
58. Yatsunami J, Fujiki H, Suganuma M, Yoshizawa S, Eriksson JE, Olson MOJ, Goldman RD (1991): Vimentin is hyperphosphorylated in primary human fibroblasts treated with okadaic acid. Biochem Biophys Res Comm 177:1165-1170.
59. Zheng B, Woo CF, Kuo JF (1991): Mitotic arrest and enhanced nuclear protein phosphorylation inhibitor and tumor promoter. J Biol Chem 266:10031-10034.
60. Zhu DM, Tekle E, Chock PB, Huang CY (1996): Reversible phosphorylation as a controlling factor for sustaining calcium oscillations in HeLa cells: Involvement of calmodulin-dependent kinase II and a calyculin A-inhibitable phosphatases. Biochemstry 35:7214-7223.
61. Zu Y-L, Gilchrist A, Lacadia ME, Sha'afi RI, Huang C-K (1996): Activation of MAP kinase-activated protein kinase 2 in human neutrophils after phorbol ester or fMLP peptide stimulation. Blood 12:5287-5296.