Cancer Treatment Reviews
Volume 25, Issue 6 , Pages 377-386 , December 1999

Twenty-five years of chemotherapy in small cell lung cancer sends us back to the laboratory

  • P.B. Jensen

      Affiliations

    • Laboratory of Experimental Medical Oncology, The Laboratory Center, National University Hospital, 9 Blegdamsvej, Copenhagen, DK-2100, Denmark
  • ,
  • M. Sehested

      Affiliations

    • Department of Oncology, The Finsen Center, and Department of Pathology, The Laboratory Center, National University Hospital, 9 Blegdamsvej, Copenhagen, DK-2100, Denmark
  • ,
  • S.W. Langer

      Affiliations

    • Laboratory of Experimental Medical Oncology, The Laboratory Center, National University Hospital, 9 Blegdamsvej, Copenhagen, DK-2100, Denmark
  • ,
  • H.H. Hansen

References 

    REFERENCES
  1. Green RA, Humphrey E, Close H. Alkylating agents in bronchogenic carcinoma. Am J Med. 1969;46:516
  2. Kokron O, Titscher R, Micksche M. Klinische erfarungen mit holoxan beim kleinzelligen bronchuskarzinom. Oest Z Onkol. 1978;4:103–106
  3. Aisner J. Extensive-disease small-cell lung cancer: The thrill of victory; The agony of defeat. J Clin Oncol. 1996;14:658–665
  4. Hansen HH. The management of small cell lung cancer. Lancet. 1992;339:846–849
  5. Turrisi AT, Kim K, Blum R, Sause WT, Livingston RB, Komaki R, et al. Twice-daily compared with once-daily thoracic radiotherapy in limited small-cell lung cancer treated concurrently with cisplatin and etoposide. N Engl J Med. 1999;340:265–271
  6. Auperin A, Arriagada R, Pignon JP, Le Péchoux C, Gregor A, Stephens RJ, et al. Prophylactic cranial irradiation for patients with small-cell lung cancer in complete remission. N Eng J Med. 1999;341:476–484
  7. Lassen U, Hansen HH. Surgery in limited stage small cell lung cancer. Cancer Treat Rev. 1999;25:67–72
  8. Lassen UN, Hirsch FR, Osterlind K, Bergman B and Dombernowsky P. Outcome of combination chemotherapy in extensive stage small-cell lung cancer: any treatment related progress?. Lung Cancer. 1998;20:151–160
  9. Chute JP, Chen T, Feigal E, Simon R, Johnson BE. Twenty years of phase III trials for patients with extensive-stage small-cell lung cancer: percetible progress. J Clin Oncol. 1999;17:1794–1801
  10. Bonomi P. Review of selected randomized trials in small cell lung cancer. Sem Oncol. 1998;25:suppl 9, 70–78
  11. Chen AY and Liu LF. DNA topoisomerases – Essential enzymes and lethal targets. Annu Rev Pharmacol Toxicol. 1994;34:191–218
  12. Danø K. Active outward transport of daunomycin in resistant Ehrlich ascites tumor cells. Biochim Biophys Acta. 1973;323:466–483
  13. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta. 1976;455:152–162
  14. Sehested M, Friche E, Jensen PB, Demant EJF. Relationship of VP-16 to the classical multidrug resistance (MDR) phenotype. Cancer Research. 1992;52:2874–2879
  15. Cole SPC, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science. 1992;258:1650–1654
  16. Zaman GJR, Flens MJ, van Leusden MR, de Haas M, Mulder HS, Lankelma J, et al. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc Natl Acad Sci (USA). 1994;91:8822–8826
  17. Danks MK, Schmidt CA, Cirtain MC, Suttle DP, Beck WT. Altered Catalytic Activity of and DNA Cleavage by DNA Topoisomerase II from Human Leukemic Cells Selected for Resistance to VM-26. Biochemistry. 1988;27:8861–8869
  18. Guinee DG, Holden JA, Benfield JR, Woodward ML, Przygodzki RM, Fishback NF, et al. Comparison of DNA topoisomerase liα expression in small cell and non small cell carcinoma of the lung. In search of a mechanism of chemotherapeutic response. Cancer. 1996;78:729–735
  19. Kreisholt J, Sorensen M, Jensen PB, Nielsen BS, Andersen CB, Sehested M. Immunohistochemical detection of DNA topoisomerase II α. P-glycoprotein and Multi Drug Resistance related protein (MRP) in small cell and non-small cell lung cancer. British Journal of Cancer. 1998;77:1469–1473
  20. Giaccone G. MRP is frequently expressed in human lung cancer cell lines, in non small cell lung cancer and in normal lungs. Int J Cancer. 1996;66:760–767
  21. Holmes JA, West RR. The effect of MDR-1 gene expression on outcome in acute myeloblastic leukaemia. Br J Cancer. 1994;69:382–384
  22. Trock BJ, Leonessa F, Clarke R. Multidrug resistance in breast cancer: a meta-analysis of MDR1/gp170 expression and its possible functional significance. J Natl Cancer Inst. 1997;89:917–931
  23. Scheper RJ, Broxterman HJ, Scheffer GL, Kaaijk P, Dalton WS, van Heijningen THM, et al. Overexpression of a M 110,000 vesicular protein in non-p-glycoprotein-mediated multidrug resistance. Cancer Res. 1993;53:1475–1479
  24. Schinkel AH, Mayer U, Wagenaar E, Mol CA, van Demter L, Smit JJ, et al. Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins. Proc Natl Acad Sci USA. 1997;94:4028–4033
  25. Sikic BI, Fisher GA, Lum BL, Halsey J, Beketic-Oreskovic L, Chen G. Modulation and prevention of multidrug resistance by inhibitors of P-glycoprotein. Cancer Chemother Pharmacol. 1997;40:Suppl: S13–9
  26. Pusztai L, Hortobagyi GN. High dose chemotherapy: how resistant is breast cancer. Drug resistance updates. 1998;1:62–72
  27. Grant SC, Gralla RJ, Kris MG, Orazem J, Kitsis EA. Single-agent chemotherapy trials in small-cell lung cancer, 1970 to 1990: The case for studies in previously treated patients. J Clin Oncol. 1992;10:484–498
  28. Dombernowsky P, Sorensen S, Aisner J, Hansen HH. Cis-Dichlorodiammineplatinum (II) in small cell anaplastic bronchogenic carcinoma: a phase II study. Cancer Treat Rep. 1979;63:534–545
  29. Von Hoff DD, Elson D. Clinical results with cisplatin in lung cancer. In:  Prestayko AW,  Crooke ST,  Carter SK editor. Cisplatin current status and new developments. New York: Academic Press; 1980;p. 445–456
  30. Rosenberg B. In: Prestayko , Crooke ,  and Carter editor. Cisplatin: its history and possible mechanism of action, in: Cisplatin, current status and new developments.. New York: Academic Press; 1980;p. 9–20
  31. Frei E. The national cancer chemotherapy program. Science. 1982;217:600–606
  32. Zubrod CG. Origins and developments of chemotherapy research at the National Cancer Institute. Cancer Treat Rep. 1984;68:9–20
  33. Driscoll JS. The preclinical new drug research program of the National Cancer Institute. Cancer Treat Rep. 1984;68:63–66
  34. Estey E, Hoth D, Simon R, Marsoni S, Leyland-Jones B, Wittes R. Therapeutic response in Phase I trials of antineoplastic agents. Cancer Treat Rep. 1986;70:1105–1115
  35. Marsoni S, Hoth D, Simon R, Leyland-Jones B, De Rosa M and Wittes R. Clinical drug development: An analysis of Phase II trials. Cancer Treat Rep. 1987;71:71–80
  36. Wani MC, Taylor HL, Wall ME. Plant antitumor agents: VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevefolia. J Am Chem Soc. 1971;93:2325–2327
  37. Wall ME, Wani MC, Cook CE, Palmer KH, McPhail AT, Sim GA. Plant antitumor agents: I. The isolation and structure of camptothecin, a novel alkaloid leukemia and tumor inhibitor from Camptotheca acuminata. J Am Chem Soc. 1966;88:3888–3890
  38. Moody TW, Cuttitta F. Growth factors and peptide receptors in small cell lung cancer. Life sci. 1993;52:1161–1173
  39. Wistuba II, Bryant D, Behrens C, Milchgrub S, Virmani AK, Ashfaq R, et al. Comparison of features of human lung cancer cell lines and their corresponding tumors. Clin Cancer Res. 1999;5:991–1000
  40. Tsai C, Ihde DC, Kadoyama C, Venzon D, Gazdar AF. Correlation of in vitro drug sensitivity testing of long-term small cell lung cancer cell lines with response and survival. Eur J Cancer. 1990;26:1148–1152
  41. Giaccone G, Gazdar AF, Beck H, Zunino F, Capranico G. Multidrug sensitivity phenotype of human lung cancer cells associated with topoisomerase II expression. Cancer Res. 1992;52:1666–1674
  42. Jensen PB, Holm B, Sorensen M, Christensen IJ, Sehested M. In vitro cross-resistance and collateral sensitivity in seven resistant small cell lung cancer cell lines. Preclinical identification of suitable drug partners to taxotere, taxol, topotecan & gemcitabine. Br J Cancer. 1997;75:869–877
  43. Jensen PB, Christensen IJ, Sehested M, Hansen HH, videløv L. Differential cytotoxicity of 19 anticancer agents in wild type and etoposide resistant small cell lung cancer cell lines. Br J Cancer. 1993;67:311–320
  44. Weinstein JN, Kohn KW, Grever MR, Viswanadhan VN, Rubinstein LV, Monks AP, et al. Neural computing in cancer drug development: predicting mechanism of action. Science. 1992;258:447–451
  45. Weinstein JN. An information-intensive approach to the molecular pharmacology of cancer. Science. 1997;275:343–349
  46. Monks A, Scudiero DA, Johnson GS, Paull KD, Sausville EA. The NCI anti-cancer drug screen: a smart screen to identify effectors of novel targets. Anticancer Drug Design. 1997;12:533–547
  47. Boyd MR, Paull KD. Some practical considerations and applications of the National Cancer Institute in vitro anticancer drug discovery screen. Drug Development Research; 1995; p. 91–109
  48. Monks A, Scudiero D, Skehan P, Shoemaker R, Paull K, Vistica D, et al. Feasibility of a high-flux anticancer drug screen utilizing a diverse panel of cultured human tumor cell lines. Journal of the National Cancer Institute; 1991; p. 757–766
  49. Roed H, Vindeløv LL, Christensen IJ, Spang-Thomsen M, Hansen HH. The cytotoxic activity of cisplatin, carboplatin, and teniposide alone and combined determined on four human small cell lung cancer cell lines. Eur J Clin Oncol. 1988;24:247–253
  50. Jensen PB, Sørensen BS, Sehested M, Grue P, Demant EJF, Hansen HH. Targeting the cytotoxicity of topoisomerase Ii directed epipodophyllotoxins to tumour cells in acidic environments. Cancer Research. 1994;54:2959–2963
  51. Paull KD, Lin CM, Malspeis L, Hamel E. Identification of novel antimitotic agents acting at the tubulin level by computer-assisted evaluation of differential cytotoxicity data. Cancer Res. 1992;52:3892–3900
  52. Pettit GR, Cichacz ZA, Gao F, Herald CL, Boyd MR, Schmidt JM, et al. Isolation and structure of Spongistatin 1. J Org Chem. 1993;58:1302–1304
  53. Sorensen M, Sehested M, Jensen PB. Characterization of a human small cell lung cancer cell line resistant to the topoisomerase I directed drug topothecan. Br J Cancer. 1995;72:399–404
  54. Brock I, Hipfner DR, Nielsen BS, Jensen PB, Deeley RG, Cole SPC, et al. Sequential co-expression of the multidrug resistance genes, MRP and mdr1 and their products in VP-16 (etoposide) selected H69 small cell lung cancer cells. Cancer Res. 1995;55:459–462
  55. Wessel I, Jensen PB, Falck J, Mirski S, Cole SPC, Sehested M. Alternative splicing leading to a deletion of bp 4468–76 coding for lys-ser-lys in topoisomerase II alpha (topo II) in small cell lung cancer H69/VP cells resistant to etoposide (VP-16) results in an extranuclear enzyme localisation. Cancer Research. 1997;57:4451–5541
  56. Cormier Y, Eisenhauer E, Muldal A, Gregg R, Ayoub J, Goss G, et al. Gemcitabine is an active new agent in previously untreated extensive small cell lung cancer (SCLC). A study of the National Cancer Institute of Canada Clinical Trials Group. Ann Oncol. 1994;5:283–285
  57. Earle CC, Stewart DJ, Cormier Y, Evans WK, Gertler SZ, Mihalcioiu C, et al. A phase I study of gemcitabine/cisplatin/etoposide in the treatment of small-cell lung cancer. Lung Cancer. 1998;22:235–241
  58. Groen HJ, Fokkema E, Biesma B, Kwa B, van Putten JW, Postmus PE, et al. Paclitaxel and carboplatin in the treatment of small-cell lung cancer patients resistant to cyclophosphamide, doxorubicin, and etoposide: a non-cross-resistant schedule. J Clin Oncol. 1999;17:927–932
  59. Birch R, Weaver CH, Hainsworth JD, Bobo C and Greco FA. A randomized study of etoposide and carboplatin with or without paclitaxel in the treatment of small cell lung cancer. Semin Oncol. 1997;24:S12–S12
  60. Ardizzoni, A. Hansen, H. Dombernowsky, P. Gamucci, T. Kaplan, S. Postmus, P. Giaccone, G. Schaefer, B, Wanders, J, Verweij, J. 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. J Clin Oncol, 15
  61. Sehested M, Wessel I, Jensen LH, Holm B, Oliveri RS, Kenwrick S, et al. Chinese hamster ovary resistant to the topoisomerase II catalytic inhibitor ICRF-159: A Tyr49Phe mutation confers high-level resistance to bisdioxopiperazines. Cancer Research. 1998;58:1460–1468
  62. Holm B, Jensen PB, Sehested M. Use of the bisdioxopiperazine ICRF-187 as an antidote to etoposide (VP-16) in vivo. A model for administering high-dose topoisomerase II targeting agents. Cancer Chemother Pharmacol. 1996;38:203–209
  63. Holm B, Sehested M, Jensen PB. Improved targeting of brain tumors using dexrazoxane rescue of topoisomerase II combined with supralethal doses of etoposide and teniposide. Clinical Cancer Research. 1998;4:1367–1373
  64. Gelmon KA, Eisenhauer EA, Harris AL, Ratain MJ, Workman P. Anticancer agents targeting signaling molecules and cancer cell environment: Challenges for drug development. J Natl Cancer Inst. 1999;91:1281–1287
  65. Maurer-Spurej E, Wong KF, Maurer N, Fenske DB and Cullis PR. Factors influencing uptake and retention of amino-containing drugs in large unilamellar vesicles exhibiting transmembrane pH gradients. Biochim Biophys Acta. 1999;1416:1–10
  66. Demant EJ and Friche E. Equilibrium binding of anthracycline cytostatics to serum albumin and small unilamellar phospholipid vesicles as measured by gel filtration. Biochem Pharmacol. 1998;55:27–32
  67. Gerweck LE, Kozin SV, Stocks SJ. The pH partition theory predicts the accumulation and toxicity of doxorubicin in normal and low-pH-adapted cells. Br J Cancer. 1999;79:838–842
  68. Sorensen M, Sehested M, Jensen PB. pH-dependent regulation of camptothecin induced cytotoxicity and cleavable complex formation by the antimalarial agent chloroquine. Biochem Pharmacol. 1997;54:373–380
  69. O’Leary JJ, Shapiro RL, Ren CJ, Chuang N, Cohen HW, Potmesil M. Antiangiogenic effects of camptothecin analogues 9-amino-20(S)-camptothecin, topotecan, and CPT-11 studied in the mouse cornea model. Clin Cancer Res. 1999;5:181–187
  70. Belotti D, Vergani V, Drudis T, Borsotti P, Pitelli MR, Viale G, et al. The microtubule-affecting drug paclitaxel has anntangiogenic activity. Clin Cancer Res. 1996;2:1843–1849

PII: S0305-7372(99)90142-1

doi: 10.1053/ctrv.1999.0142

Cancer Treatment Reviews
Volume 25, Issue 6 , Pages 377-386 , December 1999