Development of a novel, physiologically relevant cytotoxicity model: Application to the study of chemotherapeutic damage to mesenchymal stromal cells

Toxicology and Applied Pharmacology

Volumn 263, Issue 3, 2012, Pages 374-389

  May, Jennifer E ^a   Morse, H Ruth ^a   Xu, Jinsheng ^a   Donaldson, Craig ^a  

^a UNIVERSITY OF THE WEST OF ENGLAND   (United Kingdom)

Author keywords

Chemotherapy; HepG2 spheroids; In vitro model; Mesenchymal stem cell; Toxicity testing

Indexed keywords

ANTIINFECTIVE AGENT; CYTOCHROME P450;

ARTICLE; CELL CULTURE; CELL DAMAGE; CELL STRAIN HEPG2; CELL TYPE; CHEMOTHERAPY; CYTOTOXICITY; DRUG MECHANISM; ENZYME ACTIVITY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STROMA CELL; PROCESS OPTIMIZATION;

ANIMAL TESTING ALTERNATIVES; ANTINEOPLASTIC AGENTS; COCULTURE TECHNIQUES; CYTOCHROME P-450 ENZYME SYSTEM; HEP G2 CELLS; HUMANS; MESENCHYMAL STEM CELLS; MESENCHYMAL STROMAL CELLS; MODELS, BIOLOGICAL; PRODRUGS; TOXICITY TESTS;

ANIMALIA;

EID: 84865412978     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.07.013     Document Type: Article

References (48)

1. Aden D.P., Fogel A., Plotkin S., Damjanov I., Knowles B.B. Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature 1979, 282:615-616.
2. Afsharian P., Terelius Y., Hassan Z., Nilsson C., Lundgren S., Hassan M. The effect of repeated administration of cyclophosphamide P450 2B in rats. Clin. Cancer Res. 2007, 13(14):4218-4224.
3. Alarcon R.A. Fluorometric determination of acrolein and related compounds with m-aminophenol. Anal. Chem. 1968, 40(11):1704-1708.
4. Anderson D., Bishop J.B., Garner R.C., Ostrosky-Wegman P., Selby P. Cyclophosphamide: review of its mutagenicity for an assessment of potential germ cell risks. Mutat. Res. 1995, 330:115-181.
5. Berg N., De Wever B., Fuchs H.W., Gaca M., Krul C., Roggen E.L. Toxicology in the 21st century - working our way towards a visionary reality. Toxicol. In Vitro 2011, 25(4):874-881.
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
7. Brandon E.F.A., Bosch T.M., Deenen M.J., Levink R., van der Wal E., van Meerveld J.B.M., Bijl M., Beijnen J.H., Schellens J.H.M., Meijerman I. Validation of in vitro cell models used in drug metabolism and transport studies; genotyping of cytochrome P450, phase II enzymes and drug transporter polymorphisms in the human hepatoma (HepG2), ovarian carcinoma (IGROV-1) and colon carcinoma (Caco-2, LS180) cell lines. Toxicol. Appl. Pharmacol. 2006, 211:1-10.
8. Breithaupt H., Dammann A., Aigner K. Pharmacokinetics of dacarbazine (DTIC) and its metabolite 5-aminoimidazole-4-carboxamide (AIC) following different dose schedules. Cancer Chemother. Pharmacol. 1982, 9(2):103-109.
9. Chang T.T., Hughes-Fulford M. Monolayer and spheroid culture of human liver hepatocellular carcinoma cell line cells demonstrate distinct global gene expression patterns and functional phenotypes. Tissue Eng. A 2009, 15(3):559-567.
10. De Lima Prata K., Orellana M.D., De Santis G.C., Kashima S., Fontes A.M., Carrara R., Palma P.V., Neder L., Covas D.T. Effects of high-dose chemotherapy on bone marrow multipotent mesenchymal stromal cells isolated from lymphoma patients. Exp. Hematol. 2010, 38:292-300.
11. Deutsch W.A., Kukreja A., Shane B., Hedge V. Phenobarbital, oxazepam and Wyeth 14,643 cause DNA damage as measured by the Comet assay. Mutagenesis 2001, 16(5):439-442.
12. Directive 2010/63/EU of the European Parliament and of the Council Off. J. Eur. Union 2010, 53:33-79. (22 September).
13. Dix D.J., Houck K.A., Martin M.T., Richard A.M., Setzer R.W., Kavlock R.J. The ToxCast program for prioritizing toxicity testing of environmental chemicals. Toxicol. Sci. 2007, 95(1):5-12.
14. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F.C., Krause D.S., Deans R.J., Keating A., Prockop D.J., Horwitz E.M. Minimum criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8(4):315-317.
15. Fellows M.D., O'Donovan M.R. Etoposide, cadmium chloride, benzo[a]pyrene, cyclophosphamide and colchicine tested in the in vitro mammalian cell micronucleus test (MNvit) in the presence and absence of cytokinesis block using L5178Y mouse lymphoma cells and 2-aminoanthracene tested in MNvit in the absence of cytokinesis block using TK6 cells at AstraZeneca UK, in support of OECD draft Test Guideline 4872009. Mutat. Res. 2009, 702(2):163-170.
16. Freyer J.P. Role of necrosis in regulating the growth saturation of multicellular spheroids. Cancer Res. 1998, 48:2432-2439.
17. Frith J.E., Thomson B., Genever P.G. Dynamic three-dimensional culture methods enhance mesenchymal stem cell properties and increase therapeutic potential. Tissue Eng. C Meth. 2010, 16(4):735-749.
18. Hall T.J., Cambridge G., James P.R. Development of a co-culture system with induced HepG2 cells and K562 cells for examining drug metabolism in vitro. Studies with cyclophosphamide, ondansetron and cisplatin. Res. Commun. Chem. Pathol. 1991, 72(2):161-168.
19. Hashizume T., Yoshitomi S., Asahi S., Matsumura S., Chatani F., Oda H. In vitro micronucleus test in HepG2 transformants expressing a series of human cytochrome P450 isoforms with chemicals requiring metabolic activation. Mutat. Res. 2009, 677(1-2):1-7.
20. Hewitt N.J., Hewitt P. Phase I and II enzyme characterization of two sources of HepG2 cell lines. Xenobiotica 2004, 34(3):243-256.
21. Huitema A.D.R., Tibben M.M., Kerbusch T., Kettenes-van den Bosch J.J., Rodenhuis S., Beijnen J.H. Simple and selective determination of the cyclophosphamide metabolite phosphoramide mustard in human plasma using high-performance liquid chromatography. J. Chromatogr. B 2003, 745:345-355.
22. Kemp K., Morse R., Wexler S., Cox C., Mallam E., Hows J., Donaldson C. Chemotherapy-induced mesenchymal stem cell damage in patients with haematological malignancy. Ann. Hematol. 2010, 89:701-713.
23. Kemp K., Morse R., Sanders K., Hows J., Donaldson C. Alkylating chemotherapeutic agents cyclophosphamide and melphalan cause functional injury to human bone marrow-derived mesenchymal stem cells. Ann. Hematol. 2011, 90(7):777-789.
24. Ku W.W., Bigger A., Brambilla G., Glatt H., Gocke E., Guzzie P.J., Hakura A., Honma M., Martus H.J., Obach R.S., Roberts S. Strategy for genotoxicity testing - metabolic considerations. Mutat. Res. 2007, 627:59-77.
25. Li J., Law H.K.W., Lau Y.L., Chan G.C.F. Differential damage and recovery of human mesenchymal stem cells after exposure to chemotherapeutic agents. Br. J. Haematol. 2004, 127:326-334.
26. Li Y., Schilling T., Benisch P., Zeck S., Meissner-Weigl J., Schneider D., Limbert C., Seufert J., Kassem M., Schutze N., Jacob F., Ebert R. Effects of high glucose on mesenchymal stem cell proliferation and differentiation. Biochem. Biophys. Res. Commun. 2007, 363:209-215.
27. Li C.L., Tian T., Nan K.J., Zhao N., Guo Y.H., Cui J., Wang J., Zhang W.G. Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro. Oncol. Rep. 2008, 20(6):1465-1471.
28. Lubberstedt M., Muller-Vieira Mayer M., Km Biemel, Knospel F., Knobeloch D., Nussler A.K., Gerlach J.C., Zeilinger K. HepaRG human hepatic cell line utility as a surrogate for primary human hepatocytes in drug metabolism assessment in vitro. J. Pharmacol. Toxicol. 2011, 63(1):59-68.
29. Marchesi F., Turriziani M., Tortorelli G., Avvisati G., Torino F., De Vecchis L. Triazene compounds: mechanism of action and related DNA repair systems. Pharmacol. Res. 2007, 56:275-287.
30. Moore A., Pinkerton R. Vincristine: can its therapeutic index be enhanced?. Pediatr. Blood Cancer 2009, 53:1180-1187.
31. Nakamura K., Mizutani R., Sanbe A., Enosawa S., Kasahara M., Nakagawa A., Ejiri Y., Murayama N., Miyamoto Y., Torii T., Kusakawa S., Yamauchi J., Fukuda M., Yamazaki H., Tanoue A. Evaluation of drug toxicity with hepatocytes cultured in a micro-space cell culture system. J. Biosci. Bioeng. 2011, 111(1):78-84.
32. Olson H., Betton G., Robinson D., Thomas K., Monro A., Kolaia G., Lilly P., Sanders J., Sipes G., Bracken W., Dorato M., Van Deun K., Smith P., Berger B., Heller A. Concordance of the toxicity of pharmaceuticals in humans and animals. Regul. Toxicol. Pharmacol. 2000, 32:56-67.
33. Pass G.J., Carrie D., Boylan M., Lorimore S., Wright E., Houston B., Henderson C.J., Wolf C.R. Role of hepatic cytochrome P450s in the pharmacokinetics and toxicity of cyclophosphamide: studies with the hepatic cytochrome P450 reductase null mouse. Cancer Res. 2005, 65(10):4211-4217.
34. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284(5411):143-147.
35. Price P.S., Keenan R.E., Swartout J.C. Characterising interspecies uncertainty using data from studies of anti-neoplastic agents in animals and humans. Toxicol. Appl. Pharmacol. 2008, 233(1):64-70.
36. Renbarger J.L., McCammack K.C., Rouse C.E., Hall S.D. Effect of race on vincristine-associated neurotoxicity in pediatric acute lymphoblastic leukemia patients. Pediatr. Blood Cancer 2008, 50:769-771.
37. Ringdén O., Le Blanc K. Allogeneic haematopoietic stem cell transplantation: state of the art and new perspectives. APMIS 2005, 113:813-830.
38. Rooseboom M., Commandeur J.N.M., Vermeulen N.P.E. Enzyme-catalyzed activation of anticancer prodrugs. Pharmacol. Rev. 2004, 56(1):53-102.
39. Seaton M.J., Schlosser P.M., Medinsky M.A. In vitro conjugation of benzene metabolites by human liver: potential influence of interindividual variability on benzene toxicity. Carcinogenesis 1995, 16(7):1519-1527.
40. Sung J.H., Kam C., Shuler M.L. A microfluidic device for a pharmacokinetic-pharmacodynamic (PK-PD) model on a chip. Lab Chip 2010, 10:446-455.
41. Ukelis U., Kramer P.J., Olejniczak K., Mueller S.O. Replacement of in vivo acute oral toxicity studies by in vitro cytotoxicity methods: opportunities, limits and regulatory status. Regul. Toxicol. Pharmacol. 2008, 51:108-118.
42. Ullrich A., Stolz D.B., Ellis E.C., Strom S.C., Michalopoulos G.K., Hengstler J.G., Runge D. Long term cultures of primary human hepatocytes as an alternative to drug testing in animals. ALTEX 2009, 26(4):295-302.
43. Wang W., Itaka K., Ohba S., Nishiyama N., Chung U., Yamasaki Y., Kataoka K. 3D spheroid culture system on micropatterned substrates for improved differentiation efficiency of multipotent mesenchymal stem cells. Biomaterials 2009, 30:2705-2715.
44. Wexler S.A., Donaldson C., Denning-Kendall P., Rice C., Bradley B., Hows J. Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord blood and mobilized adult blood are not. Br. J. Haematol. 2003, 121:368-374.
45. Wilkening S., Bader A. Influence of culture time on the expression of drug-metabolizing enzymes in primary human hepatocytes and hepatoma cell line HepG2. J. Biochem. Mol. Toxicol. 2003, 17(4):207-213.
46. Wilkening S., Stahl F., Bader A. Comparison of primary human hepatocytes and hepatoma cell line HepG2 with regard to their biotransformation properties. Drug Metab. Dispos. 2003, 31(8):1035-1042.
47. Xu J., Ma M., Purcell W.M. Characterization of some cytotoxic endpoints using rat liver and HepG2 spheroids as in vitro models and their application in hepatotoxicity studies. I. Glucose metabolism and enzyme release as cytotoxic markers. Toxicol. Appl. Pharmacol. 2003, 189:100-111.
48. Xu J., Ma M., Purcell W.M. Characterisation of some cytotoxic endpoints using rat liver and HepG2 spheroids as in vitro models and their application in hepatotoxicity studies. II. Spheroid cell spreading inhibition as a new cytotoxic marker. Toxicol. Appl. Pharmacol. 2003, 189:112-119.