TXR1-mediated thrombospondin repression: A novel mechanism of resistance to taxanes?

Genes and Development

Volumn 20, Issue 15, 2006, Pages 1975-1981

  Van Amerongen, Renée ^a   Berns, Anton ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; ANTINEOPLASTIC AGENT; BETA TUBULIN; CD36 ANTIGEN; CD47 ANTIGEN; CISPLATIN; CYCLOPHOSPHAMIDE; DOCETAXEL; FAS ANTIGEN; GLYCOPROTEIN P; GLYCOPROTEIN P INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; N ACETYLSARCOSYLGLYCYLVALYL DEXTRO ALLOISOLEUCYLTHREONYLNORVALYLISOLEUCYLARGINYLPROLINE ETHYLAMIDE; PACLITAXEL; PEPTIDE; PEPTIDE 4N1K; PROTEIN; PROTEIN BCL 2; PROTEIN P53; PROTEIN TAXOL RESISTANCE 1; RAF PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TAXANE DERIVATIVE; TETRACYCLINE; THROMBOSPONDIN; THROMBOSPONDIN 1; TUBULIN; UNCLASSIFIED DRUG;

APOPTOSIS; CANCER; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CELL CYCLE ARREST; CLINICAL TRIAL; COMBINATION CHEMOTHERAPY; CYTOTOXICITY; DOSE RESPONSE; DRUG DOSE REGIMEN; DRUG ELIMINATION; DRUG MECHANISM; DRUG POTENTIATION; DRUG PROTEIN BINDING; DRUG SENSITIVITY; GENE MUTATION; HUMAN; METRONOMIC CHEMOTHERAPY; MICROTUBULE ASSEMBLY; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; UNSPECIFIED SIDE EFFECT;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BRIDGED COMPOUNDS; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; PROSTATIC NEOPLASMS; REPRESSOR PROTEINS; TAXOIDS; THROMBOSPONDIN 1;

EID: 33746598247     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1460806     Document Type: Review

References (49)

1. Achiwa, H., Sato, S., Shimizu, S., Maeda, H., Niimi, T., Takahashi, T., Ueda, R., and Mitsudomi, T. 2003. Analysis of β-tubulin gene alteration in human lung cancer cell lines. Cancer Lett. 201: 211-216.
2. Asch, A.S., Barnwell, J., Silverstein, R.L., and Nachman, R.L. 1987. Isolation of the thrombospondin membrane receptor. J. Clin. Invest. 79: 1054-1061.
3. Bocci, G., Francia, G., Man, S., Lawler, J., and Kerbel, R.S. 2003. Thrombospondin 1, a mediator of the antiangiogenic effects of low-dose metronomic chemotherapy. Proc. Natl. Acad. Sci. 100: 12917-12922.
4. Browder, T., Butterfield, C.E., Kraling, B.M., Shi, B., Marshall, B., O'Reilly, M.S., and Folkman, J. 2000. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res. 60: 1878-1886.
5. Castedo, M., Perfettini, J.L., Roumier, T., Andreau, K., Medema, R., and Kroemer, G. 2004. Cell death by mitotic catastrophe: A molecular definition. Oncogene 23: 2825-2837.
6. Chen, J.G., Yang, C.P., Cammer, M., and Horwitz, S.B. 2003. Gene expression and mitotic exit induced by microtubule-stabilizing drugs. Cancer Res. 63: 7891-7899.
7. Damber, J.E., Vallbo, C., Albertsson, P., Lennernas, B., and Norrby, K. 2005. The anti-tumour effect of low-dose continuous chemotherapy may partly be mediated by thrombospondin. Cancer Chemother. Pharmacol. 58: 1-7.
8. Dawson, D.W., Pearce, S.F., Zhong, R., Silverstein, R.L., Frazier, W.A., and Bouck, N.P. 1997. CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol. 138: 707-717.
9. Dumontet, C., Isaac, S., Souquet, P.J., Bejui-Thivolet, F., Pacheco, Y., Peloux, N., Frankfurter, A., Luduena, R., and Perol, M. 2005. Expression of class III β tubulin in non-small cell lung cancer is correlated with resistance to taxane chemotherapy. Bull. Cancer 92: E25-E30.
10. Giannakakou, P., Sackett, D.L., Kang, Y.K., Zhan, Z., Buters, J.T., Fojo, T., and Poruchynsky, M.S. 1997. Paclitaxel-resistant human ovarian cancer cells have mutant β-tubulins that exhibit impaired paclitaxel-driven polymerization. J. Biol. Chem. 272: 17118-17125.
11. Gligorov, J. and Lotz, J.P. 2004. Preclinical pharmacology of the taxanes: Implications of the differences. Oncologist (Suppl. 2) 9: 3-8.
12. Guo, N., Krutzsch, H.C., Inman, J.K., and Roberts, D.D. 1997. Thrombospondin 1 and type I repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells. Cancer Res. 57: 1735-1742.
13. 26Glu) and less stable microtubules. Mol. Cancer Ther. 5: 270-278.
14. He, L., Yang, C.P., and Horwitz, S.B. 2001. Mutations in β-tubulin map to domains involved in regulation of microtubule stability in epothilone-resistant cell lines. Mol. Cancer Ther. 1: 3-10.
15. Hennequin, C., Giocanti, N., and Favaudon, V. 1995. S-phase specificity of cell killing by docetaxel (Taxotere) in synchronised HeLa cells. Br. J. Cancer 71: 1194-1198.
16. Hoekstra, R., de Vos, F.Y., Eskens, F.A., Gietema, J.A., van der Gaast, A., Groen, H.J., Knight, R.A., Carr, R.A., Humerickhouse, R.A., Verweij, J., et al. 2005. Phase I safety, pharmacokinetic, and pharmacodynamic study of the thrombospondin-1-mimetic angiogenesis inhibitor ABT-510 in patients with advanced cancer. J. Clin. Oncol. 23: 5188-5197.
17. Hoekstra, R., de Vos, F.Y., Eskens, F.A., de Vries, E.G., Uges, D.R., Knight, R., Carr, R.A., Humerickhouse, R., Verweij, J., and Gietema, J.A. 2006. Phase I study of the thrombospondin-1-mimetic angiogenesis inhibitor ABT-510 with 5-fluorouracil and leucovorin: A safe combination. Eur. J. Cancer 42: 467-472.
18. Isenberg, J.S., Calzada, M.J., Zhou, L., Guo, N., Lawler, J., Wang, X.Q., Frazier, W.A., and Roberts, D.D. 2005. Endogenous thrombospondin-1 is not necessary for proliferation but is permissive for vascular smooth muscle cell responses to platelet-derived growth factor. Matrix Biol. 24: 110-123.
19. Jimenez, B., Volpert, O.V., Crawford, S.E., Febbraio, M., Silverstein, R.L., and Bouck, N. 2000. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat. Med. 6: 41-48.
20. Jimenez, B., Volpert, O.V., Reiher, F., Chang, L., Munoz, A., Karin, M., and Bouck, N. 2001. c-Jun N-terminal kinase activation is required for the inhibition of neovascularization by thrombospondin-1. Oncogene 20: 3443-3448.
21. Kerbel, R.S. and Kamen, B.A. 2004. The anti-angiogenic basis of metronomic chemotherapy. Nat. Rev. Cancer 4: 423-436.
22. Li, L. and Cohen, S.N. 1996. Tsg101: A novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85: 319-329.
23. Lih, C.-J., Wei, W., and Cohen, S.N. 2006. Txr1: A transcriptional regulator of thrombospondin-1 that modulates cellular sensitivity to taxanes. Genes & Dev. (this issue).
24. Maeno, K., Ito, K., Hama, Y., Shingu, K., Kimura, M., Sano, M., Nakagomi, H., Tsuchiya, S., and Fujimori, M. 2003. Mutation of the class I β-tubulin gene does not predict response to paclitaxel for breast cancer. Cancer Lett. 198: 89-97.
25. Manna, P.P. and Frazier, W.A. 2003. The mechanism of CD47-dependent killing of T cells: Heterotrimeric Gi-dependent inhibition of protein kinase A. J. Immunol. 170: 3544-3553.
26. Manna, P.P., Dimitry, J., Oldenborg, P.A., and Frazier, W.A. 2005. CD47 augments Fas/CD95-mediated apoptosis. J. Biol. Chem. 280: 29637-29644.
27. Martello, L.A., Verdier-Pinard, P., Shen, H.J., He, L., Torres, K., Orr, G.A., and Horwitz, S.B. 2003. Elevated levels of microtubule destabilizing factors in a Taxol-resistant/dependent A549 cell line with an β-tubulin mutation. Cancer Res. 63: 1207-1213.
28. Mateo, V., Lagneaux, L., Bron, D., Biron, G., Armant, M., Delespesse, G., and Sarfati, M. 1999. CD47 ligation induces caspase-independent cell death in chronic lymphocytic leukemia. Nat. Med. 5: 1277-1284.
29. Mateo, V., Brown, E.J., Biron, G., Rubio, M., Fischer, A., Deist, F.L., and Sarfati, M. 2002. Mechanisms of CD47-induced caspase-independent cell death in normal and leukemic cells: Link between phosphatidylserine exposure and cytoskeleton organization. Blood 100: 2882-2890.
30. Mesquita, B., Veiga, I., Pereira, D., Tavares, A., Pinto, I.M., Pinto, C., Teixeira, M.R., and Castedo, S. 2005. No significant role for beta tubulin mutations and mismatch repair defects in ovarian cancer resistance to paclitaxel/cisplatin. BMC Cancer 5: 101.
31. Monzó, M., Rosell, R., Sánchez, J.J., Lee, J.S., O'Brate, A., González-Larriba, J.L., Alberola, V., Lorenzo, J.C., Núñez, L., Ro, J.Y., et al. 1999. Paclitaxel resistance in non-small-cell lung cancer associated with beta-tubulin gene mutations. J. Clin. Oncol. 17: 1786-1793.
32. Mozzetti, S., Ferlini, C., Concolino, P., Filippetti, F., Raspaglio, G., Prislei, S., Gallo, D., Martinelli, E., Ranelletti, F.O., Ferrandina, G., et al. 2005. Class III β-tubulin overexpression is a prominent mechanism of paclitaxel resistance in ovarian cancer patients. Clin. Cancer Res. 11: 298-305.
33. Quesada, A.J., Nelius, T., Yap, R., Zaichuk, T.A., Alfranca, A., Filleur, S., Volpert, O.V., and Redondo, J.M. 2005. In vivo upregulation of CD95 and CD95L causes synergistic inhibition of angiogenesis by TSP1 peptide and metronomic doxorubicin treatment. Cell Death Differ. 12: 649-658.
34. Ranganathan, S., Benetatos, C.A., Colarusso, P.J., Dexter, D.W., and Hudes, G.R. 1998. Altered beta-tubulin isotype expression in paclitaxel-resistant human prostate carcinoma cells. Br. J. Cancer 77: 562-566.
35. Riou, J.F., Naudin, A., and Lavelle, F. 1992. Effects of Taxotere on murine and human tumor cell lines. Biochem. Biophys. Res. Commun. 187: 164-170.
36. Saumet, A., Slimane, M.B., Lanotte, M., Lawler, J., and Dubernard, V. 2005. Type 3 repeat/C-terminal domain of thrombospondin-1 triggers caspase-independent cell death through CD47/αvβ3 in promyelocytic leukemia NB4 cells. Blood 106: 658-667.
37. Sève, P., Mackey, J., Isaac, S., Tredan, O., Souquet, P.J., Perol, M., Lai, R., Voloch, A., and Dumontet, C. 2005. Class III β-tubulin expression in tumor cells predicts response and outcome in patients with non-small cell lung cancer receiving paclitaxel. Mol. Cancer Ther. 4: 2001-2007.
38. Sid, B., Sartelet, H., Bellon, G., El Btaouri, H., Rath, G., Delorme, N., Haye, B., and Martiny, L. 2004. Thrombospondin 1: A multifunctional protein implicated in the regulation of tumor growth. Crit. Rev. Oncol. Hematol. 49: 245-258.
39. Swanton, C., Tomlinson, I., and Downward, J. 2006. Chromosomal instability, colorectal cancer and taxane resistance. Cell Cycle 5: 818-823.
40. Torres, K. and Horwitz, S.B. 1998. Mechanisms of Taxol-induced cell death are concentration dependent. Cancer Res. 58: 3620-3626.
41. van Ark-Otte, J., Samelis, G., Rubio, G., Lopez Saez, J.B., Pinedo, H.M., and Giaccone, G. 1998. Effects of tubulin-inhibiting agents in human lung and breast cancer cell lines with different multidrug resistance phenotypes. Oncol. Rep. 5: 249-255.
42. Wang, Y., O'Brate, A., Zhou, W., and Giannakakou, P. 2005. Resistance to microtubule-stabilizing drugs involves two events: β-tubulin mutation in one allele followed by loss of the second allele. Cell Cycle 4: 1847-1853.
43. Wang, Y., Yin, S., Blade, K., Cooper, G., Menick, D.R., and Cabral, F. 2006. Mutations at leucine 215 of β-tubulin affect paclitaxel sensitivity by two distinct mechanisms. Biochemistry 45: 185-194.
44. Yap, R., Veliceasa, D., Emmenegger, U., Kerbel, R.S., McKay, L.M., Henkin, J., and Volpert, O.V. 2005. Metronomic low-dose chemotherapy boosts CD95-dependent antiangiogenic effect of the thrombospondin peptide ABT-510: A complementation antiangiogenic strategy. Clin. Cancer Res. 11: 6678-6685.
45. Yeh, J.J., Hsu, W.H., Wang, J.J., Ho, S.T., and Kao, A. 2003. Predicting chemotherapy response to paclitaxel-based therapy in advanced non-small-cell lung cancer with P-glycoprotein expression. Respiration 70: 32-35.
46. Yeung, T.K., Germond, C., Chen, X., and Wang, Z. 1999. The mode of action of taxol: Apoptosis at low concentration and necrosis at high concentration. Biochem. Biophys. Res. Commun. 263: 398-404.
47. Yoo, G.H., Piechocki, M.P., Ensley, J.F., Nguyen, T., Oliver, J., Meng, H., Kewson, D., Shibuya, T.Y., Lonardo, F., and Tainsky, M.A. 2002. Docetaxel induced gene expression patterns in head and neck squamous cell carcinoma using cDNA microarray and PowerBlot. Clin. Cancer Res. 8: 3910-3921.
48. Zhou, J. and Giannakakou, P. 2005. Targeting microtubules for cancer chemotherapy. Curr. Med. Chem. Anticancer Agents 5: 65-71.
49. Zhao, J., Kim, J.E., Reed, E., and Li, Q.Q. 2005. Molecular mechanism of antitumor activity of taxanes in lung cancer (Review). Int. J. Oncol. 27: 247-256.