Xenograft models for preclinical drug testing: Implications for adrenocortical cancer

Molecular and Cellular Endocrinology

Volumn 351, Issue 1, 2012, Pages 71-77

  Luconi, Michaela ^a   Mannelli, Massimo ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Adrenocortical carcinoma; IGF system; In vivo animal model; Orthotopic; Xenograft

Indexed keywords

ANTINEOPLASTIC AGENT; DOXORUBICIN; EVEROLIMUS; MITOTANE; PACLITAXEL; PIOGLITAZONE; PLACEBO; ROSIGLITAZONE; SORAFENIB; SUNITINIB;

ADRENAL CORTEX CARCINOMA; ANTINEOPLASTIC ACTIVITY; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER RECURRENCE; CANCER SURVIVAL; CARCINOGENICITY; CYTOTOXICITY; DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG DISTRIBUTION; DRUG EXCRETION; DRUG METABOLISM; DRUG POTENCY; DRUG SCREENING; DRUG TARGETING; GENE EXPRESSION PROFILING; GENETIC TRANSFECTION; METABOLOMICS; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; TUMOR VOLUME; TUMOR XENOGRAFT;

ADRENAL CORTEX NEOPLASMS; ADRENOCORTICAL CARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; HUMANS; MICE; MITOTANE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84857120981     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.09.043     Document Type: Review

References (60)

1. Abraham J., Bakke S., Rutt A., Meadows B., Merino M., Alexander R., Schrump D., Bartlett D., Choyke P., Robey R., Hung E., Steinberg S.M., Bates S., Fojo T. A phase II trial of combination chemotherapy and surgical resection for the treatment of metastatic adrenocortical carcinoma: continuous infusion doxorubicin, vincristine, and etoposide with daily mitotane as a P-glycoprotein antagonist. Cancer 2002, 94:2333-2343.
2. Allolio B., Fassnacht M. Clinical review: adrenocortical carcinoma: clinical update. Journal of Clinical and Endocrinology Metabolism 2006, 91:2027-2037.
3. Barlaskar F.M., Spalding A.C., Heaton J.H., Kuick R., Kim A.C., Thomas D.G., Giordano T.J., Ben-Josef E., Hammer G.D. Preclinical targeting of the type I insulin-like growth factor receptor in adrenocortical carcinoma. Journal of Clinical and Endocrinology Metabolism 2009, 94:204-212.
4. Berruti A., Terzolo M., Sperone P., Pia A., Casa S.D., Gross D.J., Carnaghi C., Casali P., Porpiglia F., Mantero F., Reimondo G., Angeli A., Dogliotti L. Etoposide, doxorubicin and cisplatin plus mitotane in the treatment of advanced adrenocortical carcinoma: a large prospective phase II trial. Endocrine Related Cancer 2005, 12:657-666.
5. Betz M.J., Shapiro I., Fassnacht M., Hahner S., Reincke M., Beuschlein F. Peroxisome proliferator-activated receptor-gamma agonists suppress adrenocortical tumor cell proliferation and induce differentiation. Journal of Clinical and Endocrinology Metabolism 2005, 90:3886-3896. The German and Austrian Adrenal Network.
6. Bibby M.C. Orthotopic models of cancer for preclinical drug evaluation: advantages and disadvantages. European Journal of Cancer 2004, 4:852-857.
7. Bonacci R., Gigliotti A., Baudin E., Wion-Barbot N., Emy P., Bonnay M., Cailleux A.F., Nakib I., Schlumberger M., Comète Réseau. Cytotoxic therapy with etoposide and cisplatin in advanced adrenocortical carcinoma. British Journal of Cancer 1998, 78:546-549.
8. Bukowski R.M., Wolfe M., Levine H.S., Crawford D.E., Stephens R.L., Gaynor E., Harker W.G. Phase II trial of mitotane and cisplatin in patients with adrenal carcinoma: southwest oncology group study. Journal of Clinical Oncology 1993, 11:161-165.
9. Cantini G., Lombardi A., Piscitelli E., Poli G., Ceni E., Marchiani S., Ercolino T., Galli A., Serio M., Mannelli M., Luconi M. Rosiglitazone inhibits adrenocortical cancer cell proliferation by interfering with the IGF-IR intracellular signaling. PPAR Research 2008, 904041.
10. Cardoso C.C., Bornstein S.R., Hornsby P.J. Optimizing orthotopic cell transplantation in the mouse adrenal gland. Cell Transplant 2010, 19:565-572.
11. Cellai I., Petrangolini G., Tortoreto M., Pratesi G., Luciani P., Deledda C., Benvenuti S., Ricordati C., Gelmini S., Ceni E., Galli A., Balzi M., Faraoni P., Serio M., Peri A. In vivo effects of rosiglitazone in a human neuroblastoma xenograft. British Journal of Cancer 2010, 102:685-692.
12. Decker R.A., Kuehner M.E. Adrenocortical carcinoma. American Surgeon 1991, 57:502-513.
13. De Francia S., Pirro E., Zappia F., De Martino F., Sprio A.E., Daffara F., Terzolo M., Berruti A., Di Carlo F., Ghezzo F. A new simple HPLC method for measuring mitotane and its two principal metabolites Tests in animals and mitotane-treated patients. Journal of Chromatography. B. Analytical Technologies in the Biomedical and Life Sciences 2006, 837:69-75.
14. DiMasi J.A., Hansen R.W., Grabowski H.G. The price of innovation: new estimates of drug development costs. Journal of Health Economics 2003, 22:151-185.
15. Doghman M., El Wakil A., Cardinaud B., Thomas E., Wang J., Zhao W., Peralta-Del Valle M.H., Figueiredo B.C., Zambetti G.P., Lalli E. Regulation of insulin-like growth factor-mammalian target of rapamycin signaling by microRNA in childhood adrenocortical tumors. Cancer Research 2010, 70:4666-4675.
16. Guertin D.A., Sabatini D.M. Defining the role of mTOR in cancer. Cancer Cell 2007, 12:9-22.
17. El Hilali N., Rubio N., Martinez-Villacampa M., Blanco J. Combined noninvasive imaging and luminometric quantification of luciferase-labeled human prostate tumors and metastases. Laboratory Investigation 2002, 82:1563-1571.
18. Fassnacht M., Johanssen S., Quinkler M., Bucsky P., Willenberg H.S., Beuschlein F., Terzolo M., Mueller H.H., Hahner S., Allolio B. Limited prognostic value of the 2004 International Union Against Cancer staging classification for adrenocortical carcinoma: proposal for a Revised TNM Classification. Cancer 2009, 115:243-250.
19. Feng Z., Levine A.J. The regulation of energy metabolism and the IGF-1/mTOR pathways by the p53 protein. Trends In Cell Biology 2010, 20:427-434.
20. Ferruzzi P., Ceni E., Tarocchi M., Grappone C., Milani S., Galli A., Fiorelli G., Serio M., Mannelli M. Thiazolidinediones inhibit growth and invasiveness of the human adrenocortical cancer cell line H295R. Journal of Clinical and Endocrinology Metabolism 2005, 90:1332-1339.
21. Fidler I.J., Ellis L.M. The implications of angiogenesis for the biology and therapy of cancer metastasis. Cell 1994, 79:185-188.
22. Fiebig H.H., Burger A.M. Human tumor xenografts and explants. Tumor Models in Cancer Research 2002, 113-137. Humana Press Inc., Totowa. B.A. Teicher (Ed.).
23. Fiebig H.H., Maier A., Burger A.M. Clonogenic assay with established human tumour xenografts: correlation of in vitro to in vivo activity as a basis for anticancer drug discovery. European Journal of Cancer 2004, 40:802-820.
24. Fichtner I., Slisow W., Gill J., Becker M., Elbe B., Hillebrand T., Bibby M. Anticancer drug response and expression of molecular markers in early-passage xenotransplanted colon carcinomas. European Journal of Cancer 2004, 40:298-307.
25. Fu X.Y., Besterman J.M., Monosov A., Hoffman R.M. Models of human metastatic colon cancer in nude mice orthotopically constructed by using histologically intact patient specimens. Proceedings of The National Academy of Sciences of The United States of America 1991, 88:9345-9349.
26. Gicquel C., Bertagna X., Schneid H., Francillard-Leblond M., Luton J.P., Girard F., Le Bouc Y. Rearrangements at the 11p15 locus and overexpression of insulin-like growth factor-II gene in sporadic adrenocortical tumors. Journal of Clinical Endocrinology and Metabolism 1994, 78:1444-1453.
27. Heaney A.P., Fernando M., Yong W.H., Melmed S. Functional PPAR-gamma receptor is a novel therapeutic target for ACTH-secreting pituitary adenomas. Nature Medicine 2002, 8:1281-1287.
28. Henriquez N.V., van Overveld P.G., Que I., Buijs J.T., Bachelier R., Kaijzel E.L., Löwik C.W., Clezardin P., van der Pluijm G. Advances in optical imaging and novel model systems for cancer metastasis research. Clinical and Experimental Metastasis 2007, 24:699-705.
29. Hermansson V., Cantillana T., Hovander L., Bergman A., Ljungvall K., Magnusson U., Törneke K., Brandt I. Pharmacokinetics of the adrenocorticolytic compounds 3-methylsulphonyl-DDE and o, p'-DDD (mitotane) in Minipigs. Cancer Chemotherapy and Pharmacology 2008, 61:267-274.
30. Hermsen I.G., Fassnacht M., Terzolo M., Houterman S., den Hartigh J., Leboulleux S., Daffara F., Berruti A., Chadarevian R., Schlumberger M., Allolio B., Haak H.R., Baudin E. Plasma concentrations of o, p'DDD, o, p'DDA, and o, p'DDE as predictors of tumor response to mitotane in adrenocortical carcinoma: results of a retrospective ENS@T multicenter study. Journal of Clinical Endocrinology and Metabolism 2011, 96:1844-1851.
31. Hoffman R. Green fluorescent protein imaging of tumour growth, metastasis, and angiogenesis in mouse models. The Lancet Oncology 2002, 3:546-556.
32. Hoffman R.M. Orthotopic metastatic mouse models for anticancer drug discovery and evaluation: a bridge to the clinic. Investigational New Drugs 1999, 17:343-359.
33. Johnson J.I., Decker S., Zaharevitz D., Rubinstein L.V., Venditti J.M., Schepartz S., Kalyandrug S., Christian M., Arbuck S., Hollingshead M., Sausville E.A. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. British Journal of Cancer 2001, 84:1424-1431.
34. Kelland L.R., Jones M., Abel G., Valenti M., Gwynne J., Harrap K.R. Human ovarian-carcinoma cell lines and companion xenografts: a disease-oriented approach to new platinum anticancer drug discovery. Cancer Chemotherapy and Pharmacology 1992, 30:43-50.
35. Kelland L.R. Of mice and men: values and liabilities of the athymic nude mouse model in anticancer drug development. European Journal of Cancer 2004, 40:827-836.
36. Kerbel R.S. Human tumor xenografts as predictive preclinical models for anticancer drug activity in humans: better than commonly perceived-but they can be improved. Cancer Biology and Therapy 2003, 2:S134-S139.
37. Khan T.S., Imam H., Juhlin C., Skogseid B., Gröndal S., Tibblin S., Wilander E., Oberg K., Eriksson B. Streptozocin and o, p'DDD in the treatment of adrenocortical cancer patients: long-term survival in its adjuvant use. Annals of Oncology 2000, 11:1281-1287.
38. Lin W.C., Pretlow T.P., Pretlow T.G., Culp L.A. Bacterial lacZ gene as a highly sensitive marker to detect micrometastasis formation during tumor progression. Cancer Research 1990, 50:2808-2817.
39. Lindhe O., Skogseid B., Brandt I. Cytochrome P450-catalyzed binding of 3-methylsulfonyl-DDE and o, p'-DDD in human adrenal zona fasciculata/reticularis. Journal of Clinical Endocrinology and Metabolism 2002, 87:1319-1326.
40. Logié A., Boudou P., Boccon-Gibod L., Baudin E., Vassal G., Schlumberger M., Le Bouc Y., Gicquel C. Establishment and characterization of a human adrenocortical carcinoma xenograft model. Endocrinology 2000, 141:3165-3171.
41. Luconi M., Mangoni M., Gelmini S., Poli G., Nesi G., Francalanci M., Prates N., Cantini G., Lombardi A., Pepi M., Ercolino T., Serio M., Orlando C., Mannelli M. Rosiglitazone impairs proliferation of human adrenocortical cancer: preclinical study in a xenograft mouse model. Endocrine-Related Cancer 2010, 17:169-177.
42. Luton J.P., Cerdas S., Billaud L., Thomas G., Guilhaume B., Bertagna X., Laudat M.H., Louvel A., Chapuis Y., Blondeau P., Bonnin A., Bricaire H. Clinical features of adrenocortical carcinoma, prognostic factors, and the effect of mitotane therapy. New England Journal Medicine 1990, 322:1195-1201.
43. Lyons S.K. Advances in imaging mouse tumour models in vivo. Journal of Pathology 2005, 205:194-205.
44. Mahmood I. Prediction of clearance, volume of distribution and half-life by allometric scaling and by use of plasma concentrations predicted from pharmacokinetic constants: a comparative study. Journal of Pharmacy and Pharmacology 1999, 51:905-910.
45. Mariniello, B., Rosato, A., Zuccolotto, G., Rubin, B., Pezzani, R., Cicala, M.V., Finco, I., Iacobone, M., Fassina, A., Mantero, F., 2011. Combination of Sorafenib and Everolimus Impacts Therapeutically on Adrenal Tumor Models. In: 93rd Annual Meeting and Expo of the Endocrine Society, ENDO 2011, Abst OR13-3.
46. Peterson J.K., Houghton P.J. Integrating pharmacology and in vivo cancer models in preclinical and clinical drug development. European Journal of Cancer 2004, 40:837-844.
47. Poulin P., Theil F.P. Prediction of pharmacokinetics prior to in vivo studies. II. Generic physiologically based pharmacokinetic models of drug disposition. Journal of Pharmaceutical Sciences 2002, 91:1358-1370.
48. Ritschel W.A., Vachharajani N.N., Johnson R.D., Hussain A.S. The allometric approach for interspecies scaling of pharmacokinetic parameters. Comparative Biochemistry and Physiology C 1992, 103:249-253.
49. Rygaard J., Povlsen C.O. Heterotransplantation of a human malignant tumour to " Nude" mice. Acta Pathologica Et Microbiologica Scandinavica 1969, 77:758-760.
50. Sausville E.A., Feigal E. Evolving approaches to cancer drug discovery and development at the National Cancer Institute, USA. Annals Of Oncology 1999, 10:1287-1291.
51. Schlumberger M., Brugieres L., Gicquel C., Travagli J.P., Droz J.P., Parmentier C. 5-Fluorouracil, doxorubicin, and cisplatin as treatment for adrenal cortical carcinoma. Cancer 1991, 67:2997-3000.
52. Suggitt M., Bibby M.C. 50years of preclinical anticancer drug screening: empirical to target-driven approaches. Clinical Cancer Research 2005, 11:971-981.
53. Terzolo M., Angeli A., Fassnacht M., Daffara F., Tauchmanova L., Conton P.A., Rossetto R., Buci L., Sperone P., Grossrubatscher E., Reimondo G., Bollito E., Papotti M., Saeger W., Hahner S., Koschker A.C., Arvat E., Ambrosi B., Loli P., Lombardi G., Mannelli M., Bruzzi P., Mantero F., Allolio B., Dogliotti L., Berruti A. Adjuvant mitotane treatment for adrenocortical carcinoma. New England Journal Medicine 2007, 356:2372-2380.
54. van Erp N.P., Guchelaar H.J., Ploeger B.A., Romijn J.A., Hartigh J., Gelderblom H. Mitotane has a strong and a durable inducing effect on CYP3A4 activity. European Journal of Endocrinology 2011, 164:621-626.
55. van Slooten H., van Oosterom A.T. CAP (cyclophosphamide, doxorubicin, and cisplatin) regimen in adrenal cortical carcinoma. Cancer Treatment Reports 1983, 67:377-379.
56. Veytsman I., Nieman L., Fojo T. Management of endocrine manifestations and the use of mitotane as a chemotherapeutic agent for adrenocortical carcinoma. Journal of Clinical Oncology 2009, 27:4619-4629.
57. Wilhelm S., Carter C., Lynch M., Lowinger T., Dumas J., Smith R.A., Schwartz B., Simantov R., Kelley S. Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nature Reviews Drug Discovery 2006, 5:835-844.
58. Wilhelm S.M., Carter C., Tang L., Wilkie D., McNabola A., Rong H., Chen C., Zhang X., Vincent P., McHugh M., Cao Y., Shujath J., Gawlak S., Eveleigh D., Rowley B., Liu L., Adnane L., Lynch M., Auclair D., Taylor I., Gedrich R., Voznesensky A., Riedl B., Post L.E., Bollag G., Trail P.A. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Research 2004, 64:7099-7109.
59. Williamson S.K., Lew D., Miller G.J., Balcerzak S.P., Baker L.H., Crawford E.D. Phase II evaluation of cisplatin and etoposide followed by mitotane at disease progression in patients with locally advanced or metastatic adrenocortical carcinoma: a Southwest Oncology Group Study. Cancer 2000, 88:1159-1165.
60. Wu Y.W., Chik C.L., Knazek R.A. An in vitro and in vivo study of antitumor effects of gossypol on human SW-13 adrenocortical carcinoma. Cancer Research 1989, 49:3754-3758.