Pharmacogenomic and molecular docking studies on the cytotoxicity of the natural steroid wortmannin against multidrug-resistant tumor cells

Phytomedicine

Volumn 22, Issue 1, 2015, Pages 120-127

  Kuete, Victor ^a,b   Saeed, Mohamed E M ^a   Kadioglu, Onat ^a   Börtzler, Jonas ^a   Khalid, Hassan ^c   Greten, Henry Johannes ^d,e   Efferth, Thomas ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF DSCHANG   (Cameroon)

^c UNIVERSITY OF KHARTOUM   (Sudan)

^d UNIVERSITY OF PORTO   (Portugal)

^e Heidelberg School of Chinese Medicine   (Germany)

Author keywords

ABC transporter; Cluster analysis; Drug resistance; Fusarium oxysporum; Kinase inhibitor; Microarrays; Molecular docking; Wortmannin

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MULTIDRUG RESISTANCE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE ALPHA; PROTEIN KINASE B; UNCLASSIFIED DRUG; WORTMANNIN; ABCB1 PROTEIN, HUMAN; ANDROSTANE DERIVATIVE; ANTINEOPLASTIC AGENT; PIK3CA PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; GENE MUTATION; HUMAN; HUMAN CELL; MOLECULAR DOCKING; MULTIDRUG RESISTANCE; NUCLEOTIDE SEQUENCE; PHARMACOGENOMICS; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TUMOR CELL; UNINDEXED SEQUENCE; CLUSTER ANALYSIS; DNA MICROARRAY; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; PHARMACOGENETICS; TUMOR CELL LINE;

FUNGI; FUSARIUM OXYSPORUM; PENICILLIUM; PENICILLIUM FUNICULOSUM;

ANDROSTADIENES; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CLUSTER ANALYSIS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; MOLECULAR DOCKING SIMULATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; P-GLYCOPROTEINS; PHARMACOGENETICS; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION;

EID: 84916940655     PISSN: 09447113     EISSN: 1618095X     Source Type: Journal    
DOI: 10.1016/j.phymed.2014.11.011     Document Type: Article

References (57)

1. Abbas, H.K., Mirocha, C.J., 1988. Isolation and purification of a hemorrhagic factor (wortmannin) from Fusarium oxysporum (N17B). Appl. Environ. Microbiol. 54, 1268-1274.
2. Abdou, R., Scherlach, K., Dahse, H.M., Sattler, I., Hertweck, C., 2010. Botryorhodines A-D, antifungal and cytotoxic depsidones from Botryosphaeria rhodina, an endophyte of the medicinal plant Bidens pilosa. Phytochemistry 71, 110-116.
3. Alley, M.C., Scudiero, D.A., Monks, A., Hursey, M.L., Czerwinski, M.J., Fine, D.L., Abbott, B.J., Mayo, J.G., Shoemaker, R.H., Boyd, M.R., 1988. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res. 48, 589-601.
4. Berns, K., Horlings, H.M., Hennessy, B.T., Madiredjo, M., Hijmans, E.M., Beelen, K., Linn, S.C., Gonzalez-Angulo, A.M., Stemke-Hale, K., Hauptmann, M., Beijersbergen, R.L., Mills, G.B., van de Vijver, M.J., Bernards, R., 2007. A functional genetic approach identifies the PI3K pathway as amajor determinant of trastuzumab resistance in breast cancer. Cancer Cell 12, 395-402.
5. Bertelsen, C.A., Sondak, V.K., Mann, B.D., Korn, E.L., Kern, D.H., 1984. Chemosensitivity testing of human solid tumors. A review of 1582 assays with 258 clinical correlations. Cancer 53, 1240-1245.
6. Blumenthal, R.D., Goldenberg, D.M., 2007.Methods and goals for the use of in vitro and in vivo chemosensitivity testing. Mol. Biotechnol. 35, 185-197.
7. Bonnefoi, H., Underhill, C., Iggo, R., Cameron, D., 2009. Predictive signatures for chemotherapy sensitivity in breast cancer: are they ready for use in the clinic? Eur. J. Cancer 45, 1733-1743.
8. Cree, I.A., 2009. Chemosensitivity and chemoresistance testing in ovarian cancer. Curr. Opin. Obstet. Gynecol. 21, 39-43.
9. Cui, Y., Yi, D., Bai, X., Sun, B., Zhao, Y., Zhang, Y., 2012. Ginkgolide B produced endophytic fungus (Fusarium oxysporum) isolated from Ginkgo biloba. Fitoterapia 83, 913-920.
10. De Roock, W., Claes, B., Bernasconi, D., De Schutter, J., Biesmans, B., Fountzilas, G., Kalogeras, K.T., Kotoula, V., Papamichael, D., Laurent-Puig, P., Penault-Llorca, F., Rougier, P., Vincenzi, B., Santini, D., Tonini, G., Cappuzzo, F., Frattini, M., Molinari, F., Saletti, P., De Dosso, S., Martini, M., Bardelli, A., Siena, S., Sartore-Bianchi, A., Tabernero, J., Macarulla, T., Di Fiore, F., Gangloff, A.O., Ciardiello, F., Pfeiffer, P., Qvortrup, C., Hansen, T.P., Van Cutsem, E., Piessevaux, H., Lambrechts, D., Delorenzi, M., Tejpar, S., 2010. Effects of KRAS, BRAF, NRAS, and PIK3CA mutations on the efficacy of cetuximab plus chemotherapy in chemotherapy-refractory metastatic colorectal cancer: a retrospective consortium analysis. Lancet Oncol. 11, 753-762.
11. Efferth, T., 2012. Signal transduction pathways of the epidermal growth factor receptor in colorectal cancer and their inhibition by small molecules. Curr. Med. Chem. 19, 5735-5744.
12. Efferth, T., Fabry, U., Osieka, R., 1997. Apoptosis and resistance to daunorubicin in human leukemic cells. Leukemia 11, 1180-1186.
13. Efferth, T., Gebhart, E., Ross, D.D., Sauerbrey, A., 2003. Identification of gene expression profiles predicting tumor cell response to l-alanosine. Biochem. Pharmacol. 66, 613-621.
14. Efferth, T., Konkimalla, V.B., Wang, Y.F., Sauerbrey, A., Meinhardt, S., Zintl, F., Mattern, J., Volm, M., 2008. Prediction of broad spectrum resistance of tumors towards anticancer drugs. Clin. Cancer Res. 14, 2405-2412.
15. Fiser, A., Sali, A., 2003. Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol. 374, 461-491.
16. Gallorini, M., Cataldi, A., di Giacomo, V., 2012. Cyclin-dependent kinase modulators and cancer therapy. BioDrugs 26, 377-391.
17. Ganesan, P., Janku, F., Naing, A., Hong, D.S., Tsimberidou, A.M., Falchook, G.S., Wheler, J.J., Piha-Paul, S.A., Fu, S., Stepanek, V.M., Lee, J.J., Luthra, R., Overman, M.J., Kopetz, E.S., Wolff, R.A., Kurzrock, R., 2013. Target-based therapeutic matching in early-phase clinical trials in patients with advanced colorectal cancer and PIK3CA mutations. Mol. Cancer Ther. 12, 2857-2863.
18. Garcia-Carbonero, R., Carnero, A., Paz-Ares, L., 2013. Inhibition of HSP90 molecular chaperones: moving into the clinic. Lancet Oncol. 14, e358-e369.
19. Gillet, J.P., Efferth, T., Steinbach, D., Hamels, J., de Longueville, F., Bertholet, V., Remacle, J., 2004.Microarray-based detection of multidrug resistance in human tumor cells by expression profiling of ATP-binding cassette transporter genes. Cancer Res. 64, 8987-8993.
20. Hanker, A.B., Pfefferle, A.D., Balko, J.M., Kuba, M.G., Young, C.D., Sanchez, V., Sutton, C.R., Cheng, H., Perou, C.M., Zhao, J.J., Cook, R.S., Arteaga, C.L., 2013. Mutant PIK3CA accelerates HER2-driven transgenic mammary tumors and induces resistance to combinations of anti-HER2 therapies. Proc. Natl. Acad. Sci. U. S. A. 110, 14372-14377.
21. Janku, F., Wheler, J.J., Naing, A., Falchook, G.S., Hong, D.S., Stepanek, V.M., Fu, S., Piha- Paul, S.A., Lee, J.J., Luthra, R., Tsimberidou, A.M., Kurzrock, R., 2013. PIK3CA mutation H1047R is associated with response to PI3K/AKT/mTOR signaling pathway inhibitors in early-phase clinical trials. Cancer Res. 73, 276-284.
22. Kimmig, A., Gekeler, V., Neumann, M., Frese, G., Handgretinger, R., Kardos, G., Diddens, H., Niethammer, D., 1990. Susceptibility of multidrug-resistant human leukemia cell lines to human interleukin 2-activated killer cells. Cancer Res. 50, 6793-6799.
23. Konkimalla, V.B., Blunder, M., Bauer, R., Efferth, T., 2010. Inhibition of inducible nitric oxide synthase by bis(helenalinyl)glutarate in RAW264.7 macrophages. Biochem. Pharmacol. 79, 1573-1580.
24. Konkimalla, V.B., Efferth, T., 2010. Inhibition of epidermal growth factor receptor overexpressing cancer cells by the aphorphine-type isoquinoline alkaloid, dicentrine. Biochem. Pharmacol. 79, 1092-1099.
25. Konkimalla, V.B., McCubrey, J.A., Efferth, T., 2009. The role of downstream signaling pathways of the epidermal growth factor receptor for artesunate's activity in cancer cells. Curr. Cancer Drug Targets 9, 72-80.
26. Kubota, T., Weisenthal, L., 2006. Chemotherapy sensitivity and resistance testing: to be "standard" or to be individualized, that is the question. Gastric Cancer 9, 82-87.
27. Kuete, V., Efferth, T., 2013. Molecular determinants of cancer cell sensitivity and resistance towards the sesquiterpene farnesol. Pharmazie 68, 608-615.
28. Kumar, A., Patil, D., Rajamohanan, P.R., Ahmad, A., 2013. Isolation, purification and characterization of vinblastine and vincristine from endophytic fungus Fusarium oxysporum isolated from Catharanthus roseus. PLoS One 8, e71805.
29. Kumara, P.M., Soujanya, K.N., Ravikanth, G., Vasudeva, R., Ganeshaiah, K.N., Shaanker, R.U., 2014. Rohitukine, a chromone alkaloid and a precursor of flavopiridol, is produced by endophytic fungi isolated from Dysoxylum binectariferum Hook.f and Amoora rohituka (Roxb).Wight & Arn. Phytomedicine 21, 541-546.
30. Leber, M.F., Efferth, T., 2009. Molecular principles of cancer invasion and metastasis (review). Int. J. Oncol. 34, 881-895.
31. Liu, X.L., Huang, K.H., Zhou, J.Z., Meng, L., Wang, Y., Zhang, L.X., 2012. Identification and antibacterial characteristics of an endophytic fungus Fusarium oxysporum from Lilium lancifolium. Lett. Appl. Microbiol. 55, 399-406.
32. Ludovini, V., Bianconi, F., Pistola, L., Chiari, R., Minotti, V., Colella, R., Giuffrida, D., Tofanetti, F.R., Siggillino, A., Flacco, A., Baldelli, E., Iacono, D., Mameli, M.G., Cavaliere, A., Crino, L., 2011. Phosphoinositide-3-kinase catalytic alpha and KRAS mutations are important predictors of resistance to therapy with epidermal growth factor receptor tyrosine kinase inhibitors in patients with advanced non-small cell lung cancer. J. Thorac. Oncol. 6, 707-715.
33. Mattern, J., Wayss, K., Volm, M., 1986. Predicting chemosensitivity of tumors. Breast Cancer Res. Treat. 8, 157-159.
34. Mishra, A., Gond, S.K., Kumar, A., Sharma, V.K., Verma, S.K., Kharwar, R.N., Sieber, T.N., 2012. Season and tissue type affect fungal endophyte communities of the Indian medicinal plant Tinospora cordifolia more strongly than geographic location. Microb. Ecol. 64, 388-398.
35. Morris, G.M., Huey, R., Lindstrom, W., Sanner, M.F., Belew, R.K., Goodsell, D.S., Olson, A.J., 2009. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791.
36. Musavi, S.F., Dhavale, A., Balakrishnan, R.M., 2015. Optimization and kinetic modeling of cell-associated camptothecin production from an endophytic Fusarium oxysporum NFX06. Prep. Biochem. Biotechnol. 45, 158-172.
37. Newman, D.J., Cragg, G.M., 2007. Natural products as sources of new drugs over the last 25 years. J. Nat. Prod. 70, 461-477.
38. O'Brien, J., Wilson, I., Orton, T., Pognan, F., 2000. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem. 267, 5421-5426.
39. Paull, K.D., Shoemaker, R.H., Hodes, L., Monks, A., Scudiero, D.A., Rubinstein, L., Plowman, J., Boyd, M.R., 1989. Display and analysis of patterns of differential activity of drugs against human tumor cell lines: development of mean graph and COMPARE algorithm. J. Natl. Cancer Inst. 81, 1088-1092.
40. Raviraja, N.S., 2005. Fungal endophytes in five medicinal plant species from Kudremukh Range, Western Ghats of India. J. Basic Microbiol. 45, 230-235.
41. Rubinstein, L.V., Shoemaker, R.H., Paull, K.D., Simon, R.M., Tosini, S., Skehan, P., Scudiero, D.A., Monks, A., Boyd, M.R., 1990. Comparison of in vitro anticancer-drugs-creening data generated with a tetrazolium assay versus a protein assay against a diverse panel of human tumor cell lines. J. Natl. Cancer Inst. 82, 1113-1118.
42. Sartore-Bianchi, A., Martini, M., Molinari, F., Veronese, S., Nichelatti, M., Artale, S., Di Nicolantonio, F., Saletti, P., De Dosso, S., Mazzucchelli, L., Frattini, M., Siena, S., Bardelli, A., 2009. PIK3CA mutations in colorectal cancer are associated with clinical resistance to EGFR-targeted monoclonal antibodies. Cancer Res. 69, 1851-1857.
43. Scherf, U., Ross, D.T., Waltham, M., Smith, L.H., Lee, J.K., Tanabe, L., Kohn, K.W., Reinhold, W.C., Myers, T.G., Andrews, D.T., Scudiero, D.A., Eisen, M.B., Sausville, E.A., Pommier, Y., Botstein, D., Brown, P.O., Weinstein, J.N., 2000. A gene expression database for the molecular pharmacology of cancer. Nat. Genet. 24, 236-244.
44. Siena, S., Sartore-Bianchi, A., Di Nicolantonio, F., Balfour, J., Bardelli, A., 2009. Biomarkers predicting clinical outcome of epidermal growth factor receptor-targeted therapy in metastatic colorectal cancer. J. Natl. Cancer Inst. 101, 1308-1324.
45. Spano, D., Heck, C., De Antonellis, P., Christofori, G., Zollo, M., 2012. Molecular networks that regulate cancer metastasis. Semin. Cancer Biol. 22, 234-249.
46. Staunton, J.E., Slonim, D.K., Coller, H.A., Tamayo, P., Angelo, M.J., Park, J., Scherf, U., Lee, J.K., Reinhold, W.O., Weinstein, J.N., Mesirov, J.P., Lander, E.S., Golub, T.R., 2001. Chemosensitivity prediction by transcriptional profiling. Proc. Natl. Acad. Sci. U. S. A. 98, 10787-10792.
47. Tan, S.H., Lee, S.C., 2012. An update on chemotherapy and tumor gene expression profiles in breast cancer. Expert Opin. Drug Metab. Toxicol. 8, 1083-1113.
48. Tiwari, S., Singh, S., Pandey, P., Saikia, S.K., Negi, A.S., Gupta, S.K., Pandey, R., Banerjee, S., 2014. Isolation, structure determination, and antiaging effects of 2,3-pentanediol from endophytic fungus of Curcuma amada and docking studies. Protoplasma 251, 1089-1098.
49. Van Nguyen, M., Clark, G.M., Mascorro, D., Von Hoff, D.D., 1991. In vitro chemosensitivity testing of human gastric adenocarcinoma. Cancer Treat. Res. 55, 133-142.
50. Venkatachalam, T.K., Qazi, S., Samuel, P., Uckun, F.M., 2003. Inhibition of mast cell leukotriene release by thiourea derivatives. Bioorg. Med. Chem. Lett. 13, 485-488.
51. Volm, M., Koomagi, R., Mattern, J., Efferth, T., 2002. Protein expression profiles indicative for drug resistance of non-small cell lung cancer. Br. J. Cancer 87, 251-257.
52. Walkinshaw, D.R., Yang, X.J., 2008. Histone deacetylase inhibitors as novel anticancer therapeutics. Curr. Oncol. 15, 237-243.
53. Wang, Q.X., Li, S.F., Zhao, F., Dai, H.Q., Bao, L., Ding, R., Gao, H., Zhang, L.X., Wen, H.A., Liu, H.W., 2011. Chemical constituents from endophytic fungus Fusarium oxysporum. Fitoterapia 82, 777-781.
54. Wee, S., Jagani, Z., Xiang, K.X., Loo, A., Dorsch, M., Yao, Y.M., Sellers, W.R., Lengauer, C., Stegmeier, F., 2009. PI3K pathway activationmediates resistance to MEK inhibitors in KRAS mutant cancers. Cancer Res. 69, 4286-4293.
55. Workman, P., Clarke, P.A., Raynaud, F.I., van Montfort, R.L., 2010. Drugging the PI3 kinome: from chemical tools to drugs in the clinic. Cancer Res. 70, 2146-2157.
56. Wosikowski, K., Schuurhuis, D., Johnson, K., Paull, K.D., Myers, T.G., Weinstein, J.N., Bates, S.E., 1997. Identification of epidermal growth factor receptor and c-erbB2 pathway inhibitors by correlation with gene expression patterns. J. Natl. Cancer Inst. 89, 1505-1515.
57. Zeino, M., Zhao, Q., Eichhorn, T., Hermann, J., Müller, R., Efferth, T., 2013. Molecular docking studies of myxobacterial disorazoles and tubulysins to tubulin. J. Biosci. Med. 3, 31-43.