Inhibition of Spleen Tyrosine Kinase Potentiates Paclitaxel-Induced Cytotoxicity in Ovarian Cancer Cells by Stabilizing Microtubules

Cancer Cell

Volumn 28, Issue 1, 2015, Pages 82-96

  Yu, Yu ^a   Gaillard, Stephanie ^a,h   Phillip, JudeM ^c   Huang, Tai Chung ^b   Pinto, SnehaM ^b   Tessarollo, NayaraG ^a,d   Zhang, Zhen ^a   Pandey, Akhilesh ^a,b   Wirtz, Denis ^a,c   Ayhan, Ayse ^a,e   Davidson, Ben ^f,g   Wang, Tian Li ^a   Shih, Ie Ming ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d FEDERAL UNIVERSITY OF ESPÍRITO SANTO   (Brazil)

^e HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f OSLO UNIVERSITY HOSPITAL   (Norway)

^g UNIVERSITY OF OSLO   (Norway)

^h DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOPLATIN; DOCETAXEL; DOXORUBICIN; FLUOROURACIL; FOSTAMATINIB; METHOTREXATE; MICROTUBULE ASSOCIATED PROTEIN; MITOMYCIN; PACLITAXEL; PHOSPHOTYROSINE; PROTEIN KINASE SYK; TUBULIN; N4-(2,2-DIMETHYL-3-OXO-4H-PYRID(1,4)OXAZIN-6-YL)-5-FLUORO-N2-(3,4,5-TRIMETHOXYPHENYL)-2,4-PYRIMIDINEDIAMINE; OXAZINE DERIVATIVE; PROTEIN TYROSINE KINASE; PYRIDINE DERIVATIVE; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENTIATION; DRUG RESISTANCE; DRUG SENSITIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROTUBULE; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR RECURRENCE; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG SCREENING; FEMALE; GENE SILENCING; GENETICS; METABOLISM; OVARIAN NEOPLASMS; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE; UPREGULATION;

CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; OVARIAN NEOPLASMS; OXAZINES; PACLITAXEL; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PYRIDINES; TUBULIN; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84937441218     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.05.009     Document Type: Article

References (52)

1. Abubaker K., Luwor R.B., Escalona R., McNally O., Quinn M.A., Thompson E.W., Findlay J.K., Ahmed N. Targeted disruption of the JAK2/STAT3 pathway in combination with systemic administration of paclitaxel inhibits the priming of ovarian cancer stem cells leading to a reduced tumor burden. Front Oncol 2014, 4:75.
2. Ahmed A.A., Wang X., Lu Z., Goldsmith J., Le X.F., Grandjean G., Bartholomeusz G., Broom B., Bast R.C. Modulating microtubule stability enhances the cytotoxic response of cancer cells to Paclitaxel. Cancer Res. 2011, 71:5806-5817.
3. Braselmann S., Taylor V., Zhao H., Wang S., Sylvain C., Baluom M., Qu K., Herlaar E., Lau A., Young C., et al. R406, an orally available spleen tyrosine kinase inhibitor blocks fc receptor signaling and reduces immune complex-mediated inflammation. J.Pharmacol. Exp. Ther. 2006, 319:998-1008.
4. Buchner M., Fuchs S., Prinz G., Pfeifer D., Bartholomé K., Burger M., Chevalier N., Vallat L., Timmer J., Gribben J.G., et al. Spleen tyrosine kinase is overexpressed and represents a potential therapeutic target in chronic lymphocytic leukemia. Cancer Res. 2009, 69:5424-5432.
5. Chang W., Gruber D., Chari S., Kitazawa H., Hamazumi Y., Hisanaga S., Bulinski J.C. Phosphorylation of MAP4 affects microtubule properties and cell cycle progression. J.Cell Sci. 2001, 114:2879-2887.
6. Chen C.L., Cen L., Kohout J., Hutzen B., Chan C., Hsieh F.C., Loy A., Huang V., Cheng G., Lin J. Signal transducer and activator of transcription 3 activation is associated with bladder cancer cell growth and survival. Mol. Cancer 2008, 7:78.
7. Cheng S., Coffey G., Zhang X.H., Shaknovich R., Song Z., Lu P., Pandey A., Melnick A.M., Sinha U., Wang Y.L. SYK inhibition and response prediction in diffuse large B-cell lymphoma. Blood 2011, 118:6342-6352.
8. Cho K.R., Shih IeM. Ovarian cancer. Annu. Rev. Pathol. 2009, 4:287-313.
9. Coopman P.J., Do M.T., Barth M., Bowden E.T., Hayes A.J., Basyuk E., Blancato J.K., Vezza P.R., McLeskey S.W., Mangeat P.H., Mueller S.C. The Syk tyrosine kinase suppresses malignant growth of human breast cancer cells. Nature 2000, 406:742-747.
10. Couture C., Songyang Z., Jascur T., Williams S., Tailor P., Cantley L.C., Mustelin T. Regulation of the Lck SH2 domain by tyrosine phosphorylation. J.Biol. Chem. 1996, 271:24880-24884.
11. Currie K.S., Kropf J.E., Lee T., Blomgren P., Xu J., Zhao Z., Gallion S., Whitney J.A., Maclin D., Lansdon E.B., et al. Discovery of GS-9973, a selective and orally efficacious inhibitor of spleen tyrosine kinase. J.Med. Chem. 2014, 57:3856-3873.
12. Daniels B.R., Perkins E.M., Dobrowsky T.M., Sun S.X., Wirtz D. Asymmetric enrichment of PIE-1 in the Caenorhabditis elegans zygote mediated by binary counterdiffusion. J.Cell Biol. 2009, 184:473-479.
13. Faruki S., Geahlen R.L., Asai D.J. Syk-dependent phosphorylation of microtubules in activated B-lymphocytes. J.Cell Sci. 2000, 113:2557-2565.
14. Feldman A.L., Sun D.X., Law M.E., Novak A.J., Attygalle A.D., Thorland E.C., Fink S.R., Vrana J.A., Caron B.L., Morice W.G., et al. Overexpression of Syk tyrosine kinase in peripheral T-cell lymphomas. Leukemia 2008, 22:1139-1143.
15. Friedberg J.W., Sharman J., Sweetenham J., Johnston P.B., Vose J.M., Lacasce A., Schaefer-Cutillo J., De Vos S., Sinha R., Leonard J.P., et al. Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia. Blood 2010, 115:2578-2585.
16. Geahlen R.L. Getting Syk: spleen tyrosine kinase as a therapeutic target. Trends Pharmacol. Sci. 2014, 35:414-422.
17. Gioia R., Leroy C., Drullion C., Lagarde V., Etienne G., Dulucq S., Lippert E., Roche S., Mahon F.X., Pasquet J.M. Quantitative phosphoproteomics revealed interplay between Syk and Lyn in the resistance to nilotinib in chronic myeloid leukemia cells. Blood 2011, 118:2211-2221.
18. Goold R.G., Owen R., Gordon-Weeks P.R. Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J.Cell Sci. 1999, 112:3373-3384.
19. Gundersen G.G., Kalnoski M.H., Bulinski J.C. Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently invivo. Cell 1984, 38:779-789.
20. Hoellenriegel J., Coffey G.P., Sinha U., Pandey A., Sivina M., Ferrajoli A., Ravandi F., Wierda W.G., O'Brien S., Keating M.J., Burger J.A. Selective, novel spleen tyrosine kinase (Syk) inhibitors suppress chronic lymphocytic leukemia B-cell activation and migration. Leukemia 2012, 26:1576-1583.
21. Holgado-Madruga M., Wong A.J. Gab1 is an integrator of cell death versus cell survival signals in oxidative stress. Mol. Cell. Biol. 2003, 23:4471-4484.
22. Holohan C., Van Schaeybroeck S., Longley D.B., Johnston P.G. Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer 2013, 13:714-726.
23. Hutchcroft J.E., Harrison M.L., Geahlen R.L. B lymphocyte activation is accompanied by phosphorylation of a 72-kDa protein-tyrosine kinase. J.Biol. Chem. 1991, 266:14846-14849.
24. Jinawath N., Vasoontara C., Yap K.L., Thiaville M.M., Nakayama K., Wang T.L., Shih I.M. NAC-1, a potential stem cell pluripotency factor, contributes to paclitaxel resistance in ovarian cancer through inactivating Gadd45 pathway. Oncogene 2009, 28:1941-1948.
25. Jinawath N., Vasoontara C., Jinawath A., Fang X., Zhao K., Yap K.L., Guo T., Lee C.S., Wang W., Balgley B.M., et al. Oncoproteomic analysis reveals co-upregulation of RELA and STAT5 in carboplatin resistant ovarian carcinoma. PLoS ONE 2010, 5:e11198.
26. Keshvara L.M., Isaacson C., Harrison M.L., Geahlen R.L. Syk activation and dissociation from the B-cell antigen receptor is mediated by phosphorylation of tyrosine 130. J.Biol. Chem. 1997, 272:10377-10381.
27. Koti M., Gooding R.J., Nuin P., Haslehurst A., Crane C., Weberpals J., Childs T., Bryson P., Dharsee M., Evans K., et al. Identification of the IGF1/PI3K/NF κB/ERK gene signalling networks associated with chemotherapy resistance and treatment response in high-grade serous epithelial ovarian cancer. BMC Cancer 2013, 13:549.
28. Krisenko M.O., Cartagena A., Raman A., Geahlen R.L. Nanomechanical property maps of breast cancer cells as determined by multiharmonic atomic force microscopy reveal Syk-dependent changes in microtubule stability mediated by MAP1B. Biochemistry 2014, 54:60-68.
29. L'Hernault S.W., Rosenbaum J.L. Reversal of the posttranslational modification on Chlamydomonas flagellar alpha-tubulin occurs during flagellar resorption. J.Cell Biol. 1985, 100:457-462.
30. Law C.L., Chandran K.A., Sidorenko S.P., Clark E.A. Phospholipase C-gamma1 interacts with conserved phosphotyrosyl residues in the linker region of Syk and is a substrate for Syk. Mol. Cell. Biol. 1996, 16:1305-1315.
31. Lin Y.H., Chen B.Y., Lai W.T., Wu S.F., Guh J.H., Cheng A.L., Hsu L.C. The Akt inhibitor MK-2206 enhances the cytotoxicity of paclitaxel (Taxol) and cisplatin in ovarian cancer cells. Naunyn Schmiedebergs Arch. Pharmacol. 2015, 388:19-31.
32. Liu Y.M., Chen H.L., Lee H.Y., Liou J.P. Tubulin inhibitors: a patent review. Expert Opin Ther Pat 2014, 24:69-88.
33. Luangdilok S., Box C., Patterson L., Court W., Harrington K., Pitkin L., Rhŷs-Evans P., O-charoenrat P., Eccles S. Syk tyrosine kinase is linked to cell motility and progression in squamous cell carcinomas of the head and neck. Cancer Res. 2007, 67:7907-7916.
34. Mócsai A., Ruland J., Tybulewicz V.L. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 2010, 10:387-402.
35. Nakashima H., Natsugoe S., Ishigami S., Okumura H., Matsumoto M., Hokita S., Aikou T. Clinical significance of nuclear expression of spleen tyrosine kinase (Syk) in gastric cancer. Cancer Lett. 2006, 236:89-94.
36. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
37. Peters J.D., Furlong M.T., Asai D.J., Harrison M.L., Geahlen R.L. Syk, activated by cross-linking the B-cell antigen receptor, localizes to the cytosol where it interacts with and phosphorylates alpha-tubulin on tyrosine. J.Biol. Chem. 1996, 271:4755-4762.
38. Piperno G., Fuller M.T. Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J.Cell Biol. 1985, 101:2085-2094.
39. Podolanczuk A., Lazarus A.H., Crow A.R., Grossbard E., Bussel J.B. Of mice and men: an open-label pilot study for treatment of immune thrombocytopenic purpura by an inhibitor of Syk. Blood 2009, 113:3154-3160.
40. Ruzza P., Biondi B., Calderan A. Therapeutic prospect of Syk inhibitors. Expert Opin Ther Pat 2009, 19:1361-1376.
41. Thompson W.C. Post-translational addition of tyrosine to alpha tubulin invivo in intact brain and in myogenic cells in culture. FEBS Lett. 1977, 80:9-13.
42. Trivedi N., Marsh P., Goold R.G., Wood-Kaczmar A., Gordon-Weeks P.R. Glycogen synthase kinase-3beta phosphorylation of MAP1B at Ser1260 and Thr1265 is spatially restricted to growing axons. J.Cell Sci. 2005, 118:993-1005.
43. Uckun F.M., Ek R.O., Jan S.T., Chen C.L., Qazi S. Targeting SYK kinase-dependent anti-apoptotic resistance pathway in B-lineage acute lymphoblastic leukaemia (ALL) cells with a potent SYK inhibitory pentapeptide mimic. Br. J. Haematol. 2010, 149:508-517.
44. Uckun F.M., Qazi S., Ma H., Tuel-Ahlgren L., Ozer Z. STAT3 is a substrate of SYK tyrosine kinase in B-lineage leukemia/lymphoma cells exposed to oxidative stress. Proc. Natl. Acad. Sci. USA 2010, 107:2902-2907.
45. Vogelstein B., Papadopoulos N., Velculescu V.E., Zhou S., Diaz L.A., Kinzler K.W. Cancer genome landscapes. Science 2013, 339:1546-1558.
46. Wang W.H., Childress M.O., Geahlen R.L. Syk interacts with and phosphorylates nucleolin to stabilize Bcl-x(L) mRNA and promote cell survival. Mol. Cell. Biol. 2014, 34:3788-3799.
47. Weinblatt M.E., Kavanaugh A., Burgos-Vargas R., Dikranian A.H., Medrano-Ramirez G., Morales-Torres J.L., Murphy F.T., Musser T.K., Straniero N., Vicente-Gonzales A.V., Grossbard E. Treatment of rheumatoid arthritis with a Syk kinase inhibitor: a twelve-week, randomized, placebo-controlled trial. Arthritis Rheum. 2008, 58:3309-3318.
48. Weinblatt M.E., Kavanaugh A., Genovese M.C., Musser T.K., Grossbard E.B., Magilavy D.B. An oral spleen tyrosine kinase (Syk) inhibitor for rheumatoid arthritis. N.Engl. J. Med. 2010, 363:1303-1312.
49. Xue L., Wang W.H., Iliuk A., Hu L., Galan J.A., Yu S., Hans M., Geahlen R.L., Tao W.A. Sensitive kinase assay linked with phosphoproteomics for identifying direct kinase substrates. Proc. Natl. Acad. Sci. USA 2012, 109:5615-5620.
50. Xue L., Geahlen R.L., Tao W.A. Identification of direct tyrosine kinase substrates based on protein kinase assay-linked phosphoproteomics. Mol Cell Proteomics 2013, 12:2969-2980.
51. Zioncheck T.F., Harrison M.L., Geahlen R.L. Purification and characterization of a protein-tyrosine kinase from bovine thymus. J.Biol. Chem. 1986, 261:15637-15643.
52. Zioncheck T.F., Harrison M.L., Isaacson C.C., Geahlen R.L. Generation of an active protein-tyrosine kinase from lymphocytes by proteolysis. J.Biol. Chem. 1988, 263:19195-19202.