Dual treatment with shikonin and temozolomide reduces glioblastoma tumor growth, migration and glial-to-mesenchymal transition

Cellular Oncology

Volumn 40, Issue 3, 2017, Pages 247-261

  Matias, Diana ^a,b   Balça Silva, Joana ^a,c,d   Dubois, Luiz Gustavo ^a   Pontes, Bruno ^b   Ferrer, Valéria Pereira ^a   Rosário, Luciane ^a   do Carmo, Anália ^c,e   Echevarria Lima, Juliana ^b   Sarmento Ribeiro, Ana Bela ^c,d,e   Lopes, Maria Celeste ^c,f   Moura Neto, Vivaldo ^a  

^a Secretaria de Estado da Saude de Sao Paulo   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

^f UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Glial to mesenchymal transition; Glioblastoma; Migration; Shikonin; Temozolomide

Indexed keywords

BETA3 INTEGRIN; F ACTIN; GELATINASE A; GELATINASE B; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; PROTEIN KINASE B; SHIKONIN; TEMOZOLOMIDE; VIMENTIN; ANTINEOPLASTIC AGENT; DACARBAZINE; NAPHTHOQUINONE;

ACTIN FILAMENT; ANISOTROPY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER GROWTH; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL TRANSFORMATION; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOSKELETON; GLIAL TO MESENCHYMAL TRANSITION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; MICROTUBULE; MTT ASSAY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; BRAIN TUMOR; CELL MOTION; DRUG EFFECT; DRUG RESISTANCE; EPITHELIAL MESENCHYMAL TRANSITION; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DACARBAZINE; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; GLIOBLASTOMA; HUMANS; NAPHTHOQUINONES;

EID: 85017446157     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-017-0320-1     Document Type: Article

References (47)

1. F.B. Furnari, T. Fenton, R.M. Bachoo, A. Mukasa, J.M. Stommel, A. Stegh, W.C. Hahn, K.L. Ligon, D.N. Louis, C. Brennan, L. Chin, R.A. DePinho, W.K. Cavenee, Malignant astrocytic glioma: Genetics, biology, and paths to treatment. Genes. Dev. 21, 2683–2710 (2007). doi:10.1101/gad.1596707
2. F.R. Lima, S.A. Kahn, R.C. Soletti, D. Biasoli, T. Alves, A.C. da Fonseca, C. Garcia, L. Romao, J. Brito, R. Holanda-Afonso, J. Faria, H. Borges, V. Moura-Neto, Glioblastoma: Therapeutic challenges, what lies ahead. Biochim. Biophys. Acta. 1826, 338–349 (2012). doi:10.1016/j.bbcan.2012.05.004
3. R. Stupp, M. E. Hegi, W. P. Mason, M. J. van den Bent, M. J. Taphoorn, R. C. Janzer, S. K. Ludwin, A. Allgeier, B. Fisher, K. Belanger, P. Hau, A. A. Brandes, J. Gijtenbeek, C. Marosi, C. J. Vecht, K. Mokhtari, P. Wesseling, S. Villa, E. Eisenhauer, T. Gorlia, M. Weller, D. Lacombe, J. G. Cairncross, R. O. Mirimanoff, European Organisation for Research, Treatment of Cancer Brain Tumour and Radiation Oncology Groups, National Cancer Institute of Canada Clinical Trials Group. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet. Oncol. 10, 459–466 (2009) doi: 10.1016/S1470–2045(09)70025–7
4. S.A. Kahn, D. Biasoli, C. Garcia, L.H. Geraldo, B. Pontes, M. Sobrinho, A.C. Frauches, L. Romao, R.C. Soletti, S. Assuncao Fdos, F. Tovar-Moll, J.M. de Souza, F.R. Lima, G. Anderluh, V. Moura-Neto, Equinatoxin II potentiates temozolomide- and etoposide-induced glioblastoma cell death. Current. Top. Med. Chem. 12, 2082–2093 (2012)
5. V. Moura-Neto, L. Campanati, D. Matias, C.M. Pereira, C. Freitas, J. M. Coelho-Aguiar, T.C.L.S. Spohr, A.L. Tavares-Gomes, D. Pinheiro-Aguiar, S.A. Kahn, J. Balça-Silva, B. Pontes, I. Porto-Carreiro, J. Faria, R.A.P. Martins, S. Lima-Costa, M. F. Dias-Costa, M.C. Lopes, F.R.S. Lima. Glioblastoma and the special role of adhesion molecules in their invasion, ed. by A. Sedo, R. Mentlein (Springer-Verlag Wien, 2014), p. 293. doi:10.1007/978–3–7091-1431-5
6. H.J. Anderson, D.S. Galileo, Small-molecule inhibitors of FGFR, integrins and FAK selectively decrease L1CAM-stimulated glioblastoma cell motility and proliferation. Cell. Oncol. 39, 229–242 (2016). doi:10.1007/s13402-016-0267-7
7. B.N. Smith, N.A. Bhowmick, Role of EMT in metastasis and therapy resistance. J. Clin. Med. 5, pii:E17 (2016). doi:10.3390/jcm5020017
8. J.S. Desgrosellier, D.A. Cheresh, Integrins in cancer: Biological implications and therapeutic opportunities. Nat. Rev. Cancer 10, 9–22 (2010). doi:10.1038/nrc2748
9. F.A. Mamuya, M.K. Duncan, aV integrins and TGF-β-induced EMT: A circle of regulation. J. Cell. Mol. Med. 16, 445–455 (2012). doi:10.1111/j.1582-4934.2011.01419.x
10. C.Y. Liu, H.H. Lin, M.J. Tang, Y.K. Wang. Vimentin contributes to epithelial-mesenchymal transition cancer cell mechanics by mediating cytoskeletal organization and focal adhesion maturation. Oncotarget 6, 15966–15983 (2015) doi:10.18632/oncotarget.3862
11. L.J. McCawley, L.M. Matrisian, Matrix metalloproteinases: Multifunctional contributors to tumor progression. Mol. Med. Today 6, 149–156 (2000). doi:10.1016/S1357-4310(00)01686-5
12. E. Godefroy, A. Moreau-Aubry, E. Diez, B. Dreno, F. Jotereau, Y. Guilloux. alpha v beta3-dependent cross-presentation of matrix metalloproteinase-2 by melanoma cells gives rise to a new tumor antigen. J. Exp. Med. 202, 61–72 (2005) doi: 10.1084/jem.20042138
13. R.C. Soletti, G.P. de Faria, J. Vernal, H. Terenzi, G. Anderluh, H.L. Borges, V. Moura-Neto, N.H. Gabilan, Potentiation of anticancer-drug cytotoxicity by sea anemone pore-forming proteins in human glioblastoma cells. Anti-Cancer Drugs 19, 517–525 (2008). doi:10.1097/CAD.0b013e3282faa704
14. B.L. Santos, M.N. Oliveira, P.L. Coelho, B.P. Pitanga, A.B. da Silva, T. Adelita, V.D. Silva, F. Costa Mde. R.S. El-Bacha, M. Tardy, H. Chneiweiss, M.P. Junier, V. Moura-Neto, S.L. Costa. Flavonoids suppress human glioblastoma cell growth by inhibiting cell metabolism, migration, and by regulating extracellular matrix proteins and metalloproteinases expression. Chem. Biol. Interact. 242, 123–138 (2015) doi: 10.1016/j.cbi.2015.07.014
15. J. Balca-Silva, D. Matias, A. do Carmo, H. Girao, V. Moura-Neto, A.B. Sarmento-Ribeiro, M.C. Lopes. Tamoxifen in combination with temozolomide induce a synergistic inhibition of PKC-pan in GBM cell lines. Biochim. Biophys. Acta 1850, 722–732 (2015) doi:10.1016/j.bbagen.2014.12.022
16. X. Chen, L. Yang, J.J. Oppenheim, M.Z. Howard, Cellular pharmacology studies of shikonin derivatives. Phytother. Res. 16, 199–209 (2002). doi:10.1002/ptr.1100
17. Y. Chen, L. Zheng, J. Liu, Z. Zhou, X. Cao, X. Lv, F. Chen, Shikonin inhibits prostate cancer cells metastasis by reducing matrix metalloproteinase-2/−9 expression via AKT/mTOR and ROS/ERK1/2 pathways. Int. Immunopharmacol. 21, 447–455 (2014). doi:10.1016/j.intimp.2014.05.026
18. H. Wang, C. Wu, S. Wan, H. Zhang, S. Zhou, G. Liu, Shikonin attenuates lung cancer cell adhesion to extracellular matrix and metastasis by inhibiting integrin β1 expression and the ERK1/2 signaling pathway. Toxicology 308, 104–112 (2013). doi:10.1016/j.tox.2013.03.015
19. Q. Zhao, N. Kretschmer, R. Bauer, T. Efferth, Shikonin and its derivatives inhibit the epidermal growth factor receptor signaling and synergistically kill glioblastoma cells in combination with erlotinib. Int. J. Cancer 137, 1446–1456 (2015). doi:10.1002/ijc.29483
20. F.L. Zhang, P. Wang, Y.H. Liu, L.B. Liu, X.B. Liu, Z. Li, Y.X. Xue, Topoisomerase I inhibitors, shikonin and topotecan, inhibit growth and induce apoptosis of glioma cells and glioma stem cells. PLoS One 8, e81815 (2013). doi:10.1371/journal.pone.0081815
21. D. Hong, S.Y. Jang, E.H. Jang, B. Jung, I.H. Cho, M.J. Park, S.Y. Jeong, J.H. Kim, Shikonin as an inhibitor of the LPS-induced epithelial-to-mesenchymal transition in human breast cancer cells. Int. J. Mol. Med. 36, 1601–1606 (2015). doi:10.3892/ijmm.2015.2373
22. R. Mahabir, M. Tanino, A. Elmansuri, L. Wang, T. Kimura, T. Itoh, Y. Ohba, H. Nishihara, H. Shirato, M. Tsuda, S. Tanaka, Sustained elevation of snail promotes glial-mesenchymal transition after irradiation in malignant glioma. Neuro-Oncology 16, 671–685 (2014). doi:10.1093/neuonc/not239
23. J. Faria, L. Romao, S. Martins, T. Alves, F.A. Mendes, G.P. de Faria, R. Hollanda, C. Takiya, L. Chimelli, V. Morandi, J.M. de Souza, J.G. Abreu, V. Moura Neto, Interactive properties of human glioblastoma cells with brain neurons in culture and neuronal modulation of glial laminin organization. Differentiation 74, 562–572 (2006). doi:10.1111/j.1432-0436.2006.00090.x
24. L.F. Romao, F.A. Mendes, N.M. Feitosa, J.C. Faria, J.M. Coelho-Aguiar, J.M. de Souza, V. Moura-Neto, J.G. Abreu, Connective tissue growth factor (CTGF/CCN2) is negatively regulated during neuron-glioblastoma interaction. PLoS One 8, e55605 (2013). doi:10.1371/journal.pone.0055605
25. C.C. Liang, A.Y. Park, J.L. Guan, In vitro scratch assay: A convenient and inexpensive method for analysis of cell migration in vitro. Nat. Protoc. 2, 329–333 (2007). doi:10.1038/nprot.2007.30
26. A. Boudaoud, A. Burian, D. Borowska-Wykret, M. Uyttewaal, R. Wrzalik, D. Kwiatkowska, O. Hamant, FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nat. Protoc. 9, 457–463 (2014). doi:10.1038/nprot.2014.024
27. H. Towbin, T. Staehelin, J. Gordon, Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Biotechnology 24, 145–149 (1979)
28. K.A. McDowell, G.J. Riggins, G.L. Gallia, Targeting the AKT pathway in glioblastoma. Curr. Pharm. Des. 17, 2411–2420 (2011)
29. N. Fenouille, M. Tichet, M. Dufies, A. Pottier, A. Mogha, J.K. Soo, S. Rocchi, A. Mallavialle, M.D. Galibert, A. Khammari, J.P. Lacour, R. Ballotti, M. Deckert, S. Tartare-Deckert, The epithelial-mesenchymal transition (EMT) regulatory factor SLUG (SNAI2) is a downstream target of SPARC and AKT in promoting melanoma cell invasion. PLoS One 7, e40378 (2012). doi:10.1371/journal.pone.0040378
30. Y. Iwadate, Epithelial-mesenchymal transition in glioblastoma progression. Oncol. Lett. 11, 1615–1620 (2016). doi:10.3892/ol.2016.4113
31. W.Y. Cheng, J.J. Kandel, D.J. Yamashiro, P. Canoll, D. Anastassiou, A multi-cancer mesenchymal transition gene expression signature is associated with prolonged time to recurrence in glioblastoma. PLoS One 7, e34705 (2012). doi:10.1371/journal.pone.0034705
32. E.M. Goellner, B. Grimme, A.R. Brown, Y.C. Lin, X.H. Wang, K.F. Sugrue, L. Mitchell, R.N. Trivedi, J.B. Tang, R.W. Sobol, Overcoming temozolomide resistance in glioblastoma via dual inhibition of NAD+ biosynthesis and base excision repair. Cancer Res. 71, 2308–2317 (2011). doi:10.1158/0008-5472.CAN-10-3213
33. H. Wu, J. Xie, Q. Pan, B. Wang, D. Hu, X. Hu, Anticancer agent shikonin is an incompetent inducer of cancer drug resistance. PLoS One 8, e52706 (2013). doi:10.1371/journal.pone.0052706
34. W. Li, J. Liu, K. Jackson, R. Shi, Y. Zhao, Sensitizing the therapeutic efficacy of taxol with shikonin in human breast cancer cells. PLoS One 9, e94079 (2014). doi:10.1371/journal.pone.0094079
35. M.E. Hegi, A.C. Diserens, T. Gorlia, M.F. Hamou, N. de Tribolet, M. Weller, J.M. Kros, J.A. Hainfellner, W. Mason, L. Mariani, J.E. Bromberg, P. Hau, R.O. Mirimanoff, J.G. Cairncross, R.C. Janzer, R. Stupp, MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352, 997–1003 (2005). doi:10.1056/NEJMoa043331
36. C. Kubelt, K. Hattermann, S. Sebens, H.M. Mehdorn, J. Held-Feindt, Epithelial-to-mesenchymal transition in paired human primary and recurrent glioblastomas. Int. J. Oncol. 46, 2515–2525 (2015). doi:10.3892/ijo.2015.2944
37. Y.W. Heng, H.H. Lim, T. Mina, P. Utomo, S. Zhong, C.T. Lim, C.G. Koh, TPPP acts downstream of RhoA-ROCK-LIMK2 to regulate astral microtubule organization and spindle orientation. J. Cell. Sci. 125, 1579–1590 (2012). doi:10.1242/jcs.096818
38. M. Silginer, M. Weller, U. Ziegler, P. Roth, Integrin inhibition promotes atypical anoikis in glioma cells. Cell. Death Dis. 5, e1012 (2014). doi:10.1038/cddis.2013.543
39. M. Rolli, E. Fransvea, J. Pilch, A. Saven, B. Felding-Habermann, Activated integrin alphavbeta3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells. Proc. Natl. Acad. Sci. U S A 100, 9482–9487 (2003). doi:10.1073/pnas.1633689100
40. S.S. Lakka, C.S. Gondi, N. Yanamandra, W.C. Olivero, D.H. Dinh, M. Gujrati, J.S. Rao, Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduces tumor cell invasion, tumor growth and angiogenesis. Oncogene 23, 4681–4689 (2004). doi:10.1038/sj.onc.1207616
41. C. Chetty, S.S. Lakka, P. Bhoopathi, J.S. Rao, MMP-2 alters VEGF expression via alphaVbeta3 integrin-mediated PI3K/AKT signaling in A549 lung cancer cells. Int. J. Cancer 127, 1081–1095 (2010). doi:10.1002/ijc.25134
42. A.V. Fonseca, D. Corbeil, The hematopoietic stem cell polarization and migration: A dynamic link between RhoA signaling pathway, microtubule network and ganglioside-based membrane microdomains. Commun. Integr. Biol. 4, 201–204 (2011). doi:10.4161/cib.4.2.14419
43. U. Jadhav, S. Chigurupati, S.S. Lakka, S. Mohanam, Inhibition of matrix metalloproteinase-9 reduces in vitro invasion and angiogenesis in human microvascular endothelial cells. Int. J. Oncol. 25, 1407–1414 (2004)
44. Y. Jiao, X. Feng, Y. Zhan, R. Wang, S. Zheng, W. Liu, X. Zeng, Matrix metalloproteinase-2 promotes αvβ3 integrin-mediated adhesion and migration of human melanoma cells by cleaving fibronectin. PLoS One 7, e41591 (2012). doi:10.1371/journal.pone.0041591
45. J.M. Yang, Z. Xu, H. Wu, H. Zhu, X. Wu, W.N. Hait, Overexpression of extracellular matrix metalloproteinase inducer in multidrug resistant cancer cells. Mol. Cancer Res. 1, 420–427 (2003)
46. F.Y. Zhang, Y. Hu, Z.Y. Que, P. Wang, Y.H. Liu, Z.H. Wang, Y.X. Xue, Shikonin inhibits the migration and invasion of human glioblastoma cells by targeting phosphorylated β-catenin and phosphorylated PI3K/Akt: A potential mechanism for the anti-glioma efficacy of a traditional Chinese herbal medicine. Int. J. Mol. Sci. 16, 23823–23848 (2015). doi:10.3390/ijms161023823
47. P.L. Wei, C.C. Tu, C.H. Chen, Y.S. Ho, C.T. Wu, H.Y. Su, W.Y. Chen, J.J. Liu, Y.J. Chang, Shikonin suppresses the migratory ability of hepatocellular carcinoma cells. J. Agric. Food Chem. 61, 8191–8197 (2013). doi:10.1021/jf4009586