Three-dimensional and co-culture models for preclinical evaluation of metal-based anticancer drugs

Investigational New Drugs

Volumn 33, Issue 4, 2015, Pages 835-847

  Schreiber Brynzak, Ekaterina ^a   Klapproth, Erik ^a   Unger, Christine ^b   Lichtscheidl Schultz, Irene ^a   Göschl, Simone ^a   Schweighofer, Sarah ^b   Trondl, Robert ^a   Dolznig, Helmut ^b   Jakupec, Michael A ^a   Keppler, Bernhard K ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

3D models; Anti invasive properties; Hypoxia; Metal based drugs; Multicellular spheroids

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANTINEOPLASTIC AGENT; CISPLATIN; DIMETHYL SULFOXIDE; GALLIUM; KP 1339; KP 1537; KP 46; KP 772; LANTHANUM; OXALIPLATIN; PLATINUM COMPLEX; RUTHENIUM COMPLEX; UNCLASSIFIED DRUG; 8 QUINOLINOL; ORGANOMETALLIC COMPOUND; PHENANTHROLINE DERIVATIVE; TRIS(1,10-PHENANTHROLINE)LANTHANUM(III); TRIS(8-QUINOLINOLATO)GALLIUM (III);

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL CONTRACTION ASSAY; CELL INVASION ASSAY; COCULTURE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG SCREENING; DRUG SELECTIVITY; DRUG STRUCTURE; EXPERIMENTAL MODEL; FIBROBLAST; HUMAN; HUMAN CELL; METASTASIS; MONOLAYER CULTURE; MULTICELLULAR SPHEROID; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RELIABILITY; RESAZURIN ASSAY; THREE DIMENSIONAL IMAGING; TUMOR INVASION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANOXIA; CELL CYCLE; CELL LINE; CELL MOTION; DRUG EFFECTS; PHYSIOLOGY; TUMOR CELL CULTURE; TUMOR CELL LINE;

ANOXIA; ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CISPLATIN; COCULTURE TECHNIQUES; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; ORGANOMETALLIC COMPOUNDS; ORGANOPLATINUM COMPOUNDS; OXYQUINOLINE; PHENANTHROLINES; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 84944153428     PISSN: 01676997     EISSN: 15730646     Source Type: Journal    
DOI: 10.1007/s10637-015-0260-4     Document Type: Article

References (56)

1. Unger C, Kramer N, Walzl A, Scherzer M, Hengstschläger M, Dolznig H (2014) Modeling human carcinomas: physiologically relevant 3D models to improve anti-cancer drug development. Adv Drug Deliv Rev 79-80:50-67
2. Sutherland RM (1988) Cell and environment interactions in tumor microregions: the multicell spheroid model. Science 240(4849): 177-184
3. Friedrich J, Ebner R, Kunz-Schughart LA (2007) Experimental anti-tumor therapy in 3-D: spheroids-old hat or new challenge? Int J Radiat Biol 83(11-12):849-871
4. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA (2010) Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 148(1):3-15
5. Kim H, Phung Y, Ho M (2012) Changes in global gene expression associated with 3D structure of tumors: an ex vivo matrix-free mesothelioma spheroid model. PLoS One 7(6), e39556
6. Mehta G, Hsiao AY, Ingram M, Luker GD, Takayama S (2012) Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J Control Release 164(2):192-204
7. Durand RE, Olive PL (2001) Resistance of tumor cells to chemo- and radiotherapy modulated by the three-dimensional architecture of solid tumors and spheroids. Methods Cell Biol 64:211-233
8. Desoize B, Jardillier JK (2000) Multicellular resistance: a paradigm for clinical resistance? Crit Rev Oncol Hematol 36(2-3):193-207
9. Shannon AM, Bouchier-Hayes DJ, Condron CM, Toomey D (2003) Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev 29(4):297-307
10. Bertout JA, Patel SA, Simon MC (2008) The impact of O2 availability on human cancer. Nat Rev Cancer 8(12):967-975
11. Brown JM (1999) The hypoxic cell: a target for selective cancer therapy-eighteenth Bruce F. Cain Memorial award lecture. Cancer Res 59:5863-5870
12. Ma HL, Jiang Q, Han S, Wu Y, Cui Tomshine J, Wang D, Gan Y, Zou G, Liang XJ (2012) Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration. Mol Imaging 11(6):487-498
13. Trédan O, Galmarini CM, Patel K, Tannock IF (2006) Drug resistance and the solid tumor microenvironment. Nat Rev Cancer 6(8): 583-592
14. Phillips RM, Loadman PM, Cronin BP (1998) Evaluation of a novel in vitro assay for assessing drug penetration into avascular regions of tumours. Br J Cancer 77(12):2112-2119
15. Wilson WR, Hay MP (2011) Targeting hypoxia in cancer therapy. Nat Rev Cancer 11(6):393-410
16. Semenza GL (2012) Molecular mechanisms mediating metastasis of hypoxic breast cancer cells. Trends Mol Med 18(9):534-543
17. Chang Q, Jurisica I, Do T, Hedley DW (2011) Hypoxia predicts aggressive growth and spontaneous metastasis formation from orthotopically grown primary xenografts of human pancreatic cancer. Cancer Res 71(8):3110-3120
18. Vaupel P (2009) Prognostic potential of the pre-therapeutic tumor oxygenation status. Adv Exp Med Biol 645:241-246
19. Nagelkerke A, Bussink J, Mujcic H, Wouters BG, Lehmann S, Sweep FC, Span PN (2013) Hypoxia stimulates migration of breast cancer cells via the PERK/ATF4/LAMP3-arm of the unfolded protein response. Breast Cancer Res 15(1):R2
20. Tian X, Wang W, Zhang Q, Zhao L, Wei J, Xing H, Song Y, Wang S, Ma D, Meng L, Chen G (2010) Hypoxia-inducible factor-1α enhances the malignant phenotype of multicellular spheroid HeLa cells in vitro. Oncol Lett 1(5):893-897
21. Korch C, Spillman MA, Jackson TA, Jacobsen BM, Murphy SK, Lessey BA, Jordan VC, Bradfrod AP (2012) DNA profiling analysis of endometrial and ovarian cell lines reveals misidentification, redundancy and contamination. Gynecol Oncol 127:241-248
22. Hart FA, Laming FP (1964) Complexes of 1,10-phenanthroline with lanthanide chlorides and thiocyanates. J Inorg Nucl Chem 26:579-585
23. Peti W, Pieper T, Sommer M, Keppler BK, Giester G (1999) Synthesis of tumor-inhibiting complex salts containing the anion trans-tetrachlorobis(indazole)ruthenate(III) and crystal structure of the tetraphenylphosphonium salt. Eur J Inorg Chem 1551-1555
24. Collery P, Jakupec MA, Kynast B, Keppler BK (2006) Preclinical and early clinical development of the antitumor gallium complex KP46 (FFC11). In: Alpoim MC, Morais PC, Santos MA, Cristóvão AJ, Centeno JA, Collery P (eds.) Metal ions in biology and medicine 9: 521-524
25. Abramkin SA, Jungwirth U, Valiahdi SM, Dworak C, Habala L, Meelich K, Berger W, Jakupec MA, Hartinger CG, Nazarov AA, Galanski M, Keppler BK (2010) {(1R,2R,4R)-4-methyl-1,2-cyclohexanediamine}oxalatoplatinum(II): a novel enantiomerically pure oxaliplatin derivative showing improved anticancer activity in vivo. J Med Chem 53:7356-7364
26. Dhara SC (1970) Rapid method for the synthesis of cis-[Pt(NH3)2Cl2]. Indian J Chem 8:193-194
27. Kidani Y, Inagaki K, Iigo M, Hoshi A, Kuretani K (1978) Antitumor activity of 1,2-diaminocyclohexane-platinum complexes against sarcoma-180 ascites form. J Med Chem 21:1315-1318
28. Albini A, Iwamoto Y, Kleinman HK (1987) A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 47(12):3239-3245
29. Vinci M, Gowan S, Boxall F, Patterson L, Zimmermann M, Court W, Lomas C et al (2012) Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biol 10(1):29
30. Liu WD, Zhang T, Wang CL, Meng HM, Song YW, Zhao Z, Li ZM (2012) Sphere-forming tumor cells possess stem-like properties in human fibrosarcoma primary tumors and cell lines. Oncol Lett 4(6):1315-1320
31. Bjørge L, Junnikkala S, Kristoffersen EK, Hakulinen J, Matre R, Meri S (1997) Resistance of ovarian teratocarcinoma cell spheroids to complement-mediated lysis. Br J Cancer 75(9):1247-1255
32. Laurent J, Frongia C, Cazales M, Mondesert O, Ducommun B, Lobjois V (2013) Multicellular tumor spheroid models to explore cell cycle checkpoints in 3D. BMC Cancer 13:73
33. Ke Q, Costa M (2006) Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70(5):1469-1480
34. Maxwell PH, Dachs GU, Gleadle JM, Nicholls LG, Harris AL, Stratford IJ, Hankinson O, Pugh CW, Ratcliffe PJ (1997) Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc Natl Acad Sci U S A 94:8104-8109
35. Hofheinz RD, Dittrich C, Jakupec MA, Drescher A, Jaehde U, Gneist M, Graf von Keyserlingk N, Keppler BK, Hochhaus A (2005) Early results from a phase I study on orally administered tris(8-quinolinolato)gallium(III) (FFC11, KP46) in patients with solid tumors - a CESAR study (Central European Society for Anticancer Drug Research - EWIV). Int J Clin Pharmacol Ther 43(12):590-591
36. Collery P, Domingo JL, Keppler BK (1996) Preclinical toxicology and tissue gallium distribution of a novel antitumour gallium compound: tris(8-quinolinolato)gallium (III). Anticancer Res 16:687-692
37. Thompson DS, Weiss GJ, Jones SF, Burris HA, Ramanathan RK, Infante RJ, Bendell JC, Ogden A, Von Hoff DD (2012) NKP-1339: maximum tolerated dose defined for first-in-human GRP78 targeted agent. J Clin Oncol 30, Suppl., abstr. 3033
38. Bergamo A, Masi A, Jakupec MA, Keppler BK, Sava G (2009) Inhibitory effects of the ruthenium complex KP1019 in models of mammary cancer cell migration and invasion. Met-Based Drugs 681270
39. Dolznig H, Rupp C, Puri C, Haslinger C, Schweifer N, Kerjaschki D, Garin-Chesa P (2011) Modeling adenocarcinomas in vitro: a novel 3D co-culture system induces cancer relevant pathways upon tumour-stroma interaction. Am J Path 179(1):487-501
40. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C (2001) Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 12(9):2730-2741
41. Christian MM, Moy RL, Wagner RF, Yen-Moore A (2001) A correlation of alpha-smooth muscle actin and invasion in micronodular basal cell carcinoma. Dermatol Surg 27(5):441-445
42. de Wever O, Demetter P, Mareel M, Brack M (2008) Stromal myofibroblasts are drivers of invasive cancer growth Int. J Cancer 123:2229-2238
43. Valiahdi SM, Heffeter P, Jakupec MA, Marculescu R, Berger W, Rappersberger K, Keppler BK (2009) The gallium complex KP46 exerts strong activity against primary explanted melanoma cells and induces apoptosis in melanoma cell lines. Melanoma Res 19(5): 283-293
44. Desoize B, Collery P, Akéli JC, Keppler B (2000) Tris(8-quinolinolato)Ga(III) is active against unicellular and multicellular resistance. Met Ions Biol Med 6:573-576
45. Carlsson J, Nederman T (1989) Tumour spheroid technology in cancer therapy research. Eur J Cancer 25(8):1127-1133
46. Hazlehurst LA, Dalton WS (2001) Mechanisms associated with cell adhesion mediated drug resistance (CAM-DR) in hematopoietic malignancies. Cancer Metastasis Rev 20(1-2):43-50
47. Erler JT, Cawthorne CJ, Williams KJ, Koritzinsky M, Wouters BG, Wilson C, Miller C, Demonacos C, Stratford IJ, Dive C (2004) Hypoxia-mediated down-regulation of Bid and Bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance. Mol Cell Biol 24: 2875-2889
48. Enyedi ÉA, Dömötör O, Bali K, Hetényi A, Tuccinardi T, Keppler BK (2015) Interaction of the anticancer gallium(III) complexes of 8-hydroxyquinoline and maltol with human serum proteins. J Biol Inorg Chem 20:77-88
49. Rainaldi G, Calcabrini A, Arancia G, Santini MT (1999) Differential expression of adhesion molecules (CD44, ICAM-1 and LFA-3) in cancer cells grown in monolayer or as multicellular spheroids. Anticancer Res 19(3A):1769-1778
50. Jungwirth U, Gojo J, Tuder T, Walko G, Holcmann M, Schöfl T, Nowikovsky K, Wilfinger N, Schoonhoven S, Kowol CR, Lemmens-Gruber R, Heffeter P, Keppler BK, Berger W (2014) Calpain-mediated integrin deregulation as a novel mode of action for the anticancer gallium compound KP46. Mol Cancer Ther 13(10):2436-2449
51. Heffeter P, Jakupec MA, Körner W, Wild S, von Keyserlingk NG, Elbling L, Zorbas H, Korynevska A, Knasmüller S, Sutterlüty H, Micksche M, Keppler BK, Berger W (2006) Anticancer activity of the lanthanum compound [tris(1,10-phenanthroline)lanthanum(III)]trithiocyanate (KP772; FFC24). Biochem Pharmacol 71(4):426-440
52. Trondl R, Heffeter P, Kowol CR, Jakupec MA, Berger W, Keppler BK (2014) NKP-1339, the first ruthenium-based anticancer drug on the edge to clinical application. Chem Sci 5:2925-2932
53. Heffeter P, Atil B, Kryeziu K, Groza D, Koellensperger G, Körner W, Jungwirth U, Mohr T, Keppler BK, Berger W (2013) The ruthenium compound KP1339 potentiates the anticancer activity of sorafenib in vitro and in vivo. Eur J Cancer 49(15):3366-3375
54. Bytzek AK, Boeck K, Hermann G, Hann S, Keppler BK, Hartinger CG, Koellensperger G (2011) LC- and CZE-ICP-MS approaches for the in vivo analysis of the anticancer drug candidate sodium trans-[tetrachloridobis(1H-indazole)ruthenate(III)] (KP1339) in mouse plasma. Metallomics 3(10):1049-1055
55. Dömötör O, Hartinger CG, Bytzek AK, Kiss T, Keppler BK, Enyedy EA (2013) Characterization of the binding sites of the anticancer ruthenium(III) complexes KP1019 and KP1339 on human serum albumin via competition studies. J Biol Inorg Chem 18(1):9-17
56. Roberts DL, Williams KJ, Cowen RL, Barathova M, Eustace AJ, Brittain-Dissont S, Tilby MJ, Pearson DG, Ottley CJ, Stratford IJ, Dive C (2009) Contribution of HIF-1 and drug penetrance to oxaliplatin resistance in hypoxic colorectal cancer cells. Br J Cancer 101(8):1290-1297