Taxol induces concomitant hyperphosphorylation and reorganization of vimentin intermediate filaments in 9L rat brain tumor cells

Journal of Cellular Biochemistry

Volumn 68, Issue 4, 1998, Pages 472-483

  Chu, Jao Jia ^a,b   Chen, Kuang Den ^a   Lin, Yi Liang ^a   Fei, Chyn Yi ^a   Chiang, Ann Shyn ^a   Chiang, Chi Der ^b   Lai, Yiu Kay ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

Cytoskeleton; Inhibitors; Intermediate filaments; Microtubules; Protein kinases; Protein phosphorylation; Taxol; Vimentin

Indexed keywords

PACLITAXEL; VIMENTIN;

ANIMAL CELL; ARTICLE; BRAIN TUMOR; CYTOSKELETON; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BRAIN NEOPLASMS; CELL CYCLE; CELL SIZE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; INTERMEDIATE FILAMENTS; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; MICROTUBULES; PACLITAXEL; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; RATS; TUMOR CELLS, CULTURED; VIMENTIN;

ANIMALIA;

EID: 0032521088     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(19980315)68:4<472::AID-JCB7>3.0.CO;2-N     Document Type: Article

References (77)

1. Ando S, Tanabe K, Gonda Y, Sato C, Inagaki M (1989): Domain and sequence specific phosphorylation of vimentin induces disassembly of the filament structure. Biochemistry 28:2974-2979.
2. 2(+)-calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 175: 955-962.
3. Bershadsky AD, Vasiliev JM (1988): "Cytoskeleton." New York: Plenum Press.
4. Blagosklonny MV, Schulte TW, Nguyen P, Mimnaugh EG, Trepel J, Neckers L (1995): Taxol induction of p21WAF1 and p53 requires c-raf-1. Cancer Res 55:4623-4626.
5. Blagosklonny MV, Schulte T, Nguyen P, Trepel J, Neckers LM (1996): Taxol-induced apoptosis and phosphorylation of Bcl-2 protein involves c-Raf-1 and represents a novel c-Raf-1 signal transduction pathway. Cancer Res 56:1851-1854.
6. Blagosklonny MV, Giannakakou P, el-Deiry WS, Kingston DG, Higgs PI, Neckers L, Fojo T (1997): Raf-1/bcl-2 phosphorylation: A step from microtubule damage to cell death. Cancer Res 57:130-135.
7. Bloom GS, Vallee RB (1983): Association of microtubule associated protein 2 MAP2 with microtubules and intermediate filaments in cultured brain cells. J Cell Biol 96:1523-1531.
8. Cabral F, Gottesman MM (1979): Phosphorylation of the 10-nm filament protein from Chinese hamster ovary cells. J Biol Chem 254:6203-6206.
9. Chen KD, Chu JJ, Lai YK (1996): Modulation of protein phosphorylation and stress protein expression by okadaic acid on heat-shock cells. J Cell Biochem 61:255-265.
10. Cheng TJ, Lai YK (1994): Transient increase in vimentin phosphorylation and vimentin-HSC70 association in 9L rat brain tumor cells experiencing heat-shock. J Cell Biochem 54:100-109.
11. cdc2 phosphorylation of vimentin. Cell 62:1063-1071.
12. Chou YH, Ngai KL, Goldman RD (1991): The regulation of intermediate filament reorganization in mitosis. J Biol Chem 266:7325-7328.
13. Chou YH, 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.
14. Cooper JA, Sefton BM, Hunter T (1983): Detection and quantification of phosphotyrosine in proteins. Methods Enzymol 99:387-403.
15. Das KC, White CW (1997) Activation of NF-kappaB by antineoplastic agents. Role of protein kinase C. J Biol Chem 272:14914-14920.
16. Ding A, Chen B, Fuortes M, Blum E (1996): Association of mitogen-activated protein kinases with microtubules in mouse macrophages. J Exp Med 183:1899-1904.
17. Draberova E, Draber P (1993): A microtubule-interacting protein involved in coalignment of vimentin intermediate filaments with microtubules. J Cell Sci 106:1263-1273.
18. Dunton CJ (1997) New options for the treatment of advanced ovarian cancer. Semin Oncol 24 (1 suppl 5):S5-S2S511.
19. Eriksson JE, Brautigan DL, Vallee R, Olmsted J, Fujiki H, Goldman RD (1992): Cytoskeletal integrity in interphase cells requires protein phosphatase activity. Proc Natl Acad Sci USA 89:11093-11097.
20. Escribano J, Rozengurt E (1988) cyclic AMP increasing agents rapidly stimulate vimentin phosphorylation in quiescent cultures of Swiss 3T3 cells. J Cell Physiol 137:223-234.
21. Evans RM (1988): Cyclic AMP-dependent protein kinase-induced vimentin filament disassembly involves modification of the N-terminal domain of intermediate filament subunits. FEBS Lett 234:73-78.
22. Foisner R (1997): Dynamic organization of intermediate filaments and associated proteins during the cell cycle. Bioessays 19:297-305.
23. Fuchs E, Weber K (1994): Intermediate filaments: structure, dynamics, function and disease. Annu Rev Biochem 63:345-382.
24. Gard KL, Lazarides E (1982): Analysis of desmin and vimentin phosphopeptide in cultured avian myogenic cells and their modulation by 8-bromo-adenosine 3′.5′-cyclic monophosphate. Proc Natl Acad Sci USA 79:6912-6916.
25. Goldman RD (1971): The role of three cytoplasmic fibers in BHK-21 cell motility. I. Microtubules and the effects of colchicine. J Cell Biol 51:752-762.
26. Goldman RD, Hill B, Steinert P, Whitman MJ, Zackroff RV (1980): Intermediate filament-microtubule interaction: Evidence in support of common organization center. In Debrabander, DeMey (eds): "Microtubules and Microtubule Inhibitor." Netherlands: Elsevier-North Holland, pp 91-102.
27. Goldman RD, Khuon S, Chou YH, Opal P, Steinert PM (1996): The function of intermediate filaments in cell shape and cytoskeletal integrity. J Cell Biol 134:971-983.
28. Gurland G, Gundersen GG (1995): Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J Cell Biol 131:1275-1290.
29. Gyoeva FK, Gelfand VI (1991): Coalignment of vimentin intermediate filaments with microtubules depends on kinesin. Nature 353:445-448.
30. Harrison BC, Mobley PL (1991): Phorbol myristate acetate and 8-bromo-cyclic AMP-induced phosphorylation of glial fibrillary acidic protein and vimentin in astrocytes: Comparison of phosphorylation sites. J Neurochem 56:1724-1730.
31. Henricson BE, Carboni JM, Burkhardt AL, Vogel SN (1995): LPS and Taxol activate Lyn kinase autophosphorylation in Lps(n), but not in Lps(d), macrophages. Mol Med 1:428-435.
32. Ho DT, Roberge M (1997): The antitumor drug fostriecin induces vimentin hyperphosphorylation and intermediate filament reorganization. Carcinogenesis 17:967-972.
33. Hollenbeck PJ, Bershadsky AD, Pletjushkina OY, Tint IS, Vasiliev JM (1989): Intermediate filament collapse is an ATP-dependent and actin-dependent process. J Cell Sci 92:621-631.
34. Horwitz SB (1992): Mechanism of action of taxol. Trends Pharmacol Sci 13:134-136.
35. Huang CK, Devanne JF, Kennedy SP (1988): Vimentin, a cytoskeletal substrate of protein kinase C. Biochem Biophys Res Commun 150:1006-1011.
36. 411, in vimentin and thereby inhibits cytoskeletal intermediate filament assembly. J Prot Chem 13:417-525.
37. Hyams JS, Lloyd CW (1994): Microtubules. New York: Wiley-Liss.
38. Jordan MA, Toso RJ, Thrower D, Wilson L (1993): Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc Natl Acad Sci USA 90:9552-9556.
39. Jun CD, Choi BM, Kim HM, Chung HT (1995): Involvement of protein kinase C during taxol-induced activation of murine peritoneal macrophages. J Immunol 154:6541-6547.
40. Kelly RB (1990): Microtubules, membrane traffic, and cell organization. Cell 61:5-7.
41. Ku NO, Liao J, Chou CF, Omary MB (1996): Implications of intermediate filament protein phosphorylation. Cancer Metastasis Rev 15:429-444.
42. Laemmli UK (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage. Nature 227: 680-685.
43. Lai YK, Lee WC, Chen KD (1994): 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.
44. Lai YK, Shen CH, Cheng TJ, Hou MC, Lee WC (1993): Enhanced phosphorylation of a 65 kDa protein is associated with rapid induction of stress proteins in 9L rat brain tumor cells. J Cell Biochem 51:369-379.
45. Lamb NJC, Fernandex A, Feramisco JR, Welch WJ (1989): Modulation of vimentin containing intermediate filament distribution and phosphorylation in living fibroblasts by the cAMP-dependent protein kinase. J Cell Biol 108:2409-2422.
46. Lee WC, Yu JS, Yang SD, Lai YK (1992): Reversible hyperphosphorylation and reorganization of vimentin intermediate filaments by okadaic acid in 9L rat brain tumor cell. J Cell Biochem 49:373-393.
47. Lee WC, Lee YC, Perng MD, Chen CM, Lai YK (1993): Induction of vimentin modification and vimentin-HSP72 association by withangulatin A in 9L rat brain tumor cells. J Cell Biochem 53:1-13.
48. Lee LF, Schuerer-Maly CC, Lofquist AK, van Haaften-Day C, Ting JP, White CM, Martin BK, Haskill JS (1996): Taxol-dependent transcriptional activation of IL-8 expression in a subset of human ovarian cancer. Cancer Res 56:1303-1308.
49. Long BH, Fairchild CR (1994): Paclitaxel inhibits progression of mitotic cells to G1 phase by interference with spindle formation without affecting other microtubule functions during anaphase and telophase. Cancer Res 54:4355-4361.
50. Maniotis AJ, Chen CS, Ingber DE (1997): Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci USA 94:849-854.
51. Matsuoka Y, Nishizawa K, Yano T, Shibata M, Ando S, Takahashi T, Inagaki M (1992): Two different protein kinases act on a different time schedule as glial filament kinases during mitosis. EMBO J 11:2895-2902.
52. Matsuzawa K, Kosako 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.
53. 2+-activated proteinase specific for these intermediate filament proteins. Mol Cell Biol 3:1146-1156.
54. Nishio K, Arioka H, Ishida T, Fukumoto H, Kurokawa H, Sata M, Ohata M, Saijo N (1995): Enhanced interaction between tubulin and microtubule-associated protein 2 via inhibition of MAP kinase and CDC2 kinase by paclitaxel. Int J Cancer 63:688-693.
55. Nogales E, Wolf SG, Khan IA, Luduena RF, Downing KH (1995): Structure of tubulin at 6.5Å and location of the taxol-binding sites. Nature 375:424-427.
56. O'Connor CM, Gard DL, Lazarides E (1981): Phosphorylation of intermediate filament proteins by cAMP-dependent protein kinases. Cell 23:135-143.
57. Perng MD, Cheng TJ, Chen CM, Lai YK (1994): Induction of aggregation and augmentation of protein kinase mediated phosphorylation of purified vimentin intermediate filaments by withangulatin A. Mol Pharmacol 46:612-617.
58. Rao S, Krauss NE, Heerding JM, Swindell CS, Ringel I, Orr GA, Horwitz SB (1994): 3′-(p-azidobenzamido) taxol photolabeleds the N-terminal 31 amino acids of beta-tubulin. J Biol Chem 269:3132-3124.
59. Rao S, Orr GA, Chaudhary AG, Kingston DGI, Horwitz SB (1995): Characterization of the taxol binding site on the microtubule. J Biol Chem 270:20235-20238.
60. Schiff PB, Horwitz SB (1980): Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci USA 77:1561-1565.
61. Schiff PB, Horwitz SB (1981): Taxol assembles tubulin in the absence of exogenous quanosine 5′-triphosphate or microtubule-associated proteins. Biochemistry 20:3247-3252.
62. Seidman AD, Hudis CA, Raptis G, Baselga J, Fennelly D, Norton L (1997): Paclitaxel for breast cancer: The Memorial Sloan-Kettering Cancer Center experience. Oncology 11(3 suppl 2):20-28.
63. Skalli O, Goldman RD (1991): Recent insights into the assembly, dynamics, and function of intermediate filament networks. Cell Motil Cytoskeleton 19:67-79.
64. Spruill WA, Steiner AL, Tres LL, Kierszenbaum AL (1983): Follicle-stimulating hormone-dependent phosphorylation of vimentin in cultures of rat Sertoli cells. Proc Natl Acad Sci USA 80:993-997.
65. Sternberger LA, Sternberger NH (1983): Monoclonal antibodies distinguish phosphorylated and non-phosphorylated neurofilaments in situ. Proc Natl Acad Sci USA 80:6126-6130.
66. Stewart M (1993): Intermediate filament structure and assembly. Curr Opin Cell Biol 5:3-11.
67. Svitkina TM, Verkhovsky AB, Borisy GG (1996): Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton. J Cell Biol 135:991-1007.
68. Takai Y, Ogawara M, Tomono Y, Moritoh C, Imajoh-Ohmi S, Tsutsumi O, Taketani Y, Inagaki M (1996): Mitosis-specific phosphorylation of vimentin by protein kinase C coupled with reorganization of intracellular membranes. J Cell Biol 133:141-149.
69. Thompson WC, Wilson L, Purich DL (1981): Taxol induces microtubule assembly at low temperatures. Cell Motil Cytoskeleton 1:445-454.
70. Trevor KT, McGurire JG, Leonova EV (1995): Association of vimentin intermediate filaments with the centrosome. J Cell Sci 108:343-356.
71. Tsujimura K, Oagawara 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.
72. Wani MC, Taylor HL, Wall ME, Coggan P, Mcphail AT (1971): Plant antitumor agents VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc 93:2325-2327.
73. Weizsaecker M, Deen DF, Rosenblum ML, Hoshino T, Gutin PH, Baker M (1981): The 9L rat brain tumor: Description and application of animal model. J Neurol 224:183-192.
74. Wolfson M, Yang CP, Horwitz SB (1997): Taxol induces tyrosine phosphorylation of She and its association with Grb2 in murine RAW 264.7 cells. Int J Cancer 70:248-252.
75. Wyatt A, Lincoln TM, Pryzwansky KB (1991): Vimentin is transiently co-localized with and phosphorylated by cyclic GMP-dependent protein kinase in formyl peptide stimulated neutrophils. J Biol Chem 266:21274-21280.
76. Yang HY, Lieska N, Goldman A, Goldman RD (1992): Colchicine-sensitive and colchicine-insensitive intermediate filament system distinguished by a new intermediate filament-associated protein, IFAP-70/280kD. Cell Motil Cytoskeleton 22:185-199.
77. Yatsunami J, Fujiki H, Suganuma M, Yoshizawa S, Eriksson JE, Olson MO, Goldman RD (1991): Vimentin is hyperphosphorylated in primary human fibroblasts treated with okadaic acid. Biochem Biophys Res Commun 177:1165-1170.