Clinical relevance of human cancer xenografts as a tool for preclinical assessment: Example of in-vivo evaluation of topotecan-based chemotherapy in a panel of human small-cell lung cancer xenografts

Anti-Cancer Drugs

Volumn 21, Issue 1, 2010, Pages 25-32

  Némati, Fariba ^a   Daniel, Catherine ^a   Arvelo, Francisco ^a,d   Legrier, Marie Emmanuelle ^a   Froget, Benoît ^a   Livartowski, Alain ^a   Assayag, Franck ^a   Bourgeois, Yveline ^a   Poupon, Marie France ^a,c   Decaudin, Didier ^a,b  

^a Department of Translational Research ^*

^b INSTITUT CURIE   (France)

^c Centre Universitaire   (France)

^d FACULTAD DE CIENCIAS   (Venezuela)

Author keywords

Small cell lung cancer; Topotecan; Xenografts

Indexed keywords

CISPLATIN; DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); ETOPOSIDE; GLUTATHIONE TRANSFERASE P1; IFOSFAMIDE; LUNG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; TOPOTECAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER RESEARCH; CANCER RESISTANCE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG RESEARCH; FEMALE; HUMAN; HUMAN CELL; LUNG SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CISPLATIN; DRUG RESISTANCE, NEOPLASM; ETOPOSIDE; FEMALE; GENE EXPRESSION; HUMANS; IFOSFAMIDE; LUNG NEOPLASMS; MICE; MICE, NUDE; SMALL CELL LUNG CARCINOMA; TOPOTECAN; TREATMENT OUTCOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 74349117865     PISSN: 09594973     EISSN: None     Source Type: Journal    
DOI: 10.1097/CAD.0b013e3283300a29     Document Type: Article

References (48)

1. Jackman DM, Johnson BE. Small-cell lung cancer. Lancet 2005; 366:1385-1396.
2. Simon GR,Wagner H. Small cell lung cancer. Chest 2003; 123:259S-271S.
3. Mascaux C, Paesmans M, Berghmans T, Branle F, Lafitte JJ, Lemaitre F, et al. A systematic review of the role of etoposide and cisplatin in the chemotherapy of small cell lung cancer with methodology assessment and meta-analysis. Lung Cancer 2000; 30:23-36.
4. Pommier Y. Eukaryotic DNA topoisomerase I: genome gatekeeper and its intruders, camptothecins. Semin Oncol 1996; 23:3-10.
5. Pommier Y, Pourquier P, Fan Y, Strumberg D. Mechanism of action of eukaryotic DNA topoisomerase I and drugs targeted to the enzyme. Biochim Biophys Acta 1998; 1400:83-105.
6. Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 2006; 6:789-802.
7. Slichenmyer WJ, Rowinsky EK, Donehower RC, Kaufmann SH. The current status of camptothecin analogues as antitumor agents. J Natl Cancer Inst 1993; 85:271-291.
8. Puppo M, Battaglia F, Ottaviano C, Delfino S, Ribatti D, Varesio L, et al. Topotecan inhibits vascular endothelial growth factor production and angiogenic activity induced by hypoxia in human neuroblastoma by targeting hypoxia-inducible factor-1alpha and -2alpha. Mol Cancer Ther 2008; 7:1974-1984.
9. Clements M, Jones C, Cumming M, Daoud S. Antiangiogenic potential of camptothecin and topotecan. Cancer Chemother Pharmacol 1999; 44:411-416.
10. Beppu K, Nakamura K, Linehan WM, Rapisarda A, Thiele CJ. Topotecan blocks hypoxia-inducible factor-1alpha and vascular endothelial growth factor expression induced by insulin-like growth factor-I in neuroblastoma cells. Cancer Res 2005; 65:4775-4781.
11. Lund EL, Hansen LT, Kristjansen PE. Augmenting tumor sensitivity to topotecan by transient hypoxia. Cancer Chemother Pharmacol 2005; 56:473-480.
12. Ardizzoni A, Hansen H, Dombernowsky P, Gamucci T, Kaplan S, Postmus P, et al. Topotecan, a new active drug in the second-line treatment of small-cell lung cancer: a phase II study in patients with refractory and sensitive disease. The European Organization for Research and Treatment of Cancer Early Clinical Studies Group and New Drug Development Office, and the Lung Cancer Cooperative Group. J Clin Oncol 1997; 15:2090-2096.
13. Eckardt J, Gralla RJ, Palmer MC, Gandara D, Laplante J, Sandler A, et al. Topotecan as second-line therapy in patients with small cell lung cancer (SCLC): a phase II study. Ann Oncol 1996; 7:107a.
14. Depierre A, von Pawel J, Hans K, Moro D, Clark P, Gatzemeier U, et al. Evaluation of topotecan in relapsed small cell lung cancer. A multicentre phase II study [abstract]. Lung Cancer 1997; 18:35.
15. Von Pawel J, Gatzemeier U, Pujol JL, Moreau L, Bildat S, Ranson M, et al. Phase II comparator study of oral versus intravenous topotecan in patients with chemosensitive small-cell lung cancer. J Clin Oncol 2001; 19:1743-1749.
16. O'Brien ME, Ciuleanu TE, Tsekov H, Shparyk Y, Cucevia B, Juhasz G, et al. Phase III trial comparing supportive care alone with supportive care with oral topotecan in patients with relapsed small-cell lung cancer. J Clin Oncol 2006; 24:5441-5447.
17. Von Pawel J, Schiller JH, Shepherd FA, Fields SZ, Kleisbauer JP, Chrysson NG, et al. Topotecan versus cyclophosphamide, doxorubicin, and vincristine for the treatment of recurrent small-cell lung cancer. J Clin Oncol 1999; 17:658-667.
18. Eckardt JR, von Pawel J, Pujol JL, Papai Z, Quoix E, Ardizzoni A, et al. Phase III study of oral compared with intravenous topotecan as second-line therapy in small-cell lung cancer. J Clin Oncol 2007; 25:2086-2092.
19. Ardizzoni A. Topotecan in the treatment of recurrent small cell lung cancer: an update. Oncologist 2004; 9 (Suppl 6):4-13.
20. Houghton PJ, Cheshire PJ, Hallman JD II, Lutz L, Friedman HS, Danks MK, et al. Efficacy of topoisomerase I inhibitors, topotecan and irinotecan, administered at low dose levels in protracted schedules to mice bearing xenografts of human tumors. Cancer Chemother Pharmacol 1995; 36:393-403.
21. Nemati F, Livartowski A, De CP, Bourgeois Y, Arvelo F, Pouillart P, et al. Distinctive potentiating effects of cisplatin and/or ifosfamide combined with etoposide in human small cell lung carcinoma xenografts. Clin Cancer Res 2000; 6:2075-2086.
22. Poupon M, Arvelo F, Goguel A, Bourgeois Y, Jacrot M, Hanania N, et al. Response of small-cell lung cancer xenografts to chemotherapy: multidrug resistance and direct clinical correlates. J Natl Cancer Inst 1993; 85:2023-2029.
23. Arvelo F, Poupon M, Goguel A, Lizard G, Bourgeois Y, Arriagada R, et al. Response of a multidrug-resistant human small-cell lung cancer xenograft to chemotherapy. J Cancer Res Clin Oncol 1993; 120:17-23.
24. Arvelo F, Poupon M, Le CT. Establishment and characterization of five human small cell lung cancer cell lines from early tumor xenografts. Anticancer Res 1994; 14:1893-1901.
25. Gralla RJ, Eckardt J, Grotzinger KM. Quality of life with single agent oral topotecan versus intravenous TPT in patients with chemosensitive small cell lung cancer (SCLC): an international phase III study. Lung Cancer 2003; 41:S237.
26. Bahadori HR, Green MR, Catapano CV. Synergistic interaction between topotecan and microtubule-interfering agents. Cancer Chemother Pharmacol 2001; 48:188-196.
27. Jonsson E, Fridborg H, Nygren P, Larsson R. Synergistic interactions of combinations of topotecan with standard drugs in primary cultures of human tumor cells from patients. Eur J Clin Pharmacol 1998; 54:509-514.
28. Nagourney RA, Sommers BL, Harper SM, Radecki S, Evans SS. Ex vivo analysis of topotecan: advancing the application of laboratory-based clinical therapeutics. Br J Cancer 2003; 89:1789-1795.
29. Whitacre C, Zborowska E, Gordon N, Mackay W, Berger N. Topotecan increases topoisomerase IIalpha levels and sensitivity to treatment with etoposide in schedule-dependent process. Cancer Res 1997; 57:1425-1428.
30. Kaufmann S, Peereboom D, Buckwalter C, Svingen P, Grochow L, Donehower R, et al. Cytotoxic effects of topotecan combined with various anticancer agents in human cancer cell lines [see comments]. J Natl Cancer Inst 1996; 88:734-741.
31. Jensen P, Holm B, Sorensen M, Christensen I, Sehested M. In vitro crossresistance and collateral sensitivity in seven resistant small-cell lung cancer cell lines: preclinical identification of suitable drug partners to taxotere, taxol, topotecan and gemcitabin. Br J Cancer 1997; 75:869-877.
32. Bonner J, Kozelsky T. The significance of the sequence of administration of topotecan and etoposide. Cancer Chemother Pharmacol 1996; 39:109-112.
33. Ciuleanu TE, Curca R, Iancu D, Todor N, Cebotaru C, Radulescu I, et al. First-line chemotherapy with topotecan and etoposide in advanced small cell lung cancer. A phase II study. J Buon 2002; 7:43-46.
34. Saraiya B, Gounder M, Dutta J, Saleem A, Collazo C, Zimmerman L, et al. Sequential topoisomerase targeting and analysis of mechanisms of resistance to topotecan in patients with acute myelogenous leukemia. Anticancer Drugs 2008; 19:411-420.
35. Van Waardenburg RC, de Jong LA, van Eijndhoven MA, Verseyden C, Pluim D, Jansen LE, et al. Platinated DNA adducts enhance poisoning of DNA topoisomerase I by camptothecin. J Biol Chem 2004; 279:54502-54509.
36. Quoix E, Breton JL, Gervais R, Wilson J, Schramel F, Cardenal F, et al. A randomised phase II study of the efficacy and safety of intravenous topotecan in combination with either cisplatin or etoposide in patients with untreated extensive disease small-cell lung cancer. Lung Cancer 2005; 49:253-261.
37. Seifart U, Jensen K, Ukena J, Mueller C, Schroder M, Fuhr HG, et al. Randomized phase II study comparing topotecan/cisplatin administration for 5 days Versus 3 days in the treatment of extensive stage small cell lung cancer (SCLC). Lung Cancer 2005; 48:415-422.
38. Lyss AP, Herndon JE II, Lynch TJ Jr, Turrisi AT,Watson DM, Grethlein SJ, et al. Novel doublets in extensive-stage small-cell lung cancer: a randomized phase II study of topotecan plus cisplatin or paclitaxel (CALGB 9430). Clin Lung Cancer 2002; 3:205-210; discussion 211-212.
39. Rowinsky EK, Kaufmann SH, Baker SD, Grochow LB, Chen TL, Peereboom D, et al. Sequences of topotecan and cisplatin: phase I, pharmacologic, and in vitro studies to examine sequence dependence. J Clin Oncol 1996; 14:3074-3084.
40. Sorensen M, Jensen PB, Herrstedt J, Hirsch FR, Hansen HH. A dose escalating study of topotecan preceding cisplatin in previously untreated patients with small-cell lung cancer. Ann Oncol 2000; 11:829-835.
41. Eckardt JR, von Pawel J, Papai Z, Tomova A, Tzekova V, Crofts TE, et al. Open-label, multicenter, randomized, phase III study comparing oral topotecan/cisplatin versus etoposide/cisplatin as treatment for chemotherapy-naive patients with extensive-disease small-cell lung cancer. J Clin Oncol 2006; 24:2044-2051.
42. Fischer B, Arcaro A. Current status of clinical trials for small cell lung cancer. Rev Recent Clin Trials 2008; 3:40-61.
43. Hao X,Widersten M, Ridderstrom M, Hellman U, Mannervik B. Co-variation of glutathione transferase expression and cytostatic drug resistance in HeLa cells: establishment of class Mu glutathione transferase M3-3 as the dominating isoenzyme. Biochem J 1994; 297:59-67.
44. Sharma R, Singhal S, Srivastava S, Bajpai K, Frenkel E, Awasthi S. Glutathione and glutathione linked enzymes in human small cell lung cancer cell lines. Cancer Lett 1993; 75:111-119.
45. Ma J, Maliepaard M, Nooter K, Loos W, Kolker H, Verweij J, et al. Reduced cellular accumulation of topotecan: a novel mechanism of resistance in a human ovarian cancer cell line. Br J Cancer 1998; 77:1645-1652.
46. Emerson D, Besterman J, Brown H, Evans M, Leitner P, Luzzio M, et al. In vivo antitumor activity of two new seven-substituted water-soluble camptothecin analogues. Cancer Res 1995; 55:603-609.
47. Marchetti S, Oostendorp RL, Pluim D, van Eijndhoven M, van Tellingen O, Schinkel AH, et al. In vitro transport of gimatecan (7-t- butoxyiminomethylcamptothecin) by breast cancer resistance protein, P-glycoprotein, and multidrug resistance protein 2. Mol Cancer Ther 2007; 6:3307-3313.
48. Gounder MK, Nazar AS, Saleem A, Pungaliya P, Kulkarni D, Versace R, et al. Effects of drug efflux proteins and topoisomerase I mutations on the camptothecin analogue gimatecan. Invest New Drugs 2008; 26: 205-213.