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. 1996 Aug;74(4):546–554. doi: 10.1038/bjc.1996.399

Enhancement of sensitivity of human lung adenocarcinoma cells to growth-inhibitory activity of interferon alpha by differentiation-inducing agents.

I Goto 1, Y Yamamoto-Yamaguchi 1, Y Honma 1
PMCID: PMC2074667  PMID: 8761368

Abstract

A low concentration of differentiation inducers such as dimethylsulphoxide (DMSO), sodium butyrate, hexamethylene bisacetamide and sodium phenylacetate greatly enhanced the antiproliferative effect in vitro and in vivo of interferon alpha (IFN-alpha) to several human lung adenocarcinoma cells. The agents induced morphological changes in the adenocarcinoma cells and the agents together with IFN-alpha-induced alkaline phosphatase activity, which is a typical marker of type II pneumocyte maturation. To understand the mechanism of the DMSO-enhanced interferon sensitivity, we examined the effect of DMSO on high-affinity IFN-alpha receptor and interferon-stimulated promoter-binding factors. The lung adenocarcinoma cells were not impaired in IFN-alpha receptor and interferon-stimulated gene transactivation factor 3 (ISGF-3). Our data suggest that the enhancement of interferon sensitivity in the lung adenocarcinoma cells acts downstream of the activation of ISGF-3.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agarwala S. S., Kirkwood J. M. Interferons in the therapy of solid tumors. Oncology. 1994 Mar-Apr;51(2):129–136. doi: 10.1159/000227327. [DOI] [PubMed] [Google Scholar]
  2. Arnold A., Ayoub J., Douglas L., Hoogendoorn P., Skingley L., Gelmon K., Hirsh V., Eisenhauer E. Phase II trial of 13-cis-retinoic acid plus interferon alpha in non-small-cell lung cancer. The National Cancer Institute of Canada Clinical Trials Group. J Natl Cancer Inst. 1994 Feb 16;86(4):306–309. doi: 10.1093/jnci/86.4.306. [DOI] [PubMed] [Google Scholar]
  3. Azuma A., Yamano Y., Yoshimura A., Hibino T., Nishida T., Yagita H., Okumura K., Seya T., Kannagi R., Shibuya M. Augmented lung adenocarcinoma cytotoxicity by the combination of a genetically modified anti-Lewis Y antibody and antibodies to complement regulatory proteins. Scand J Immunol. 1995 Aug;42(2):202–208. doi: 10.1111/j.1365-3083.1995.tb03646.x. [DOI] [PubMed] [Google Scholar]
  4. Dale T. C., Rosen J. M., Guille M. J., Lewin A. R., Porter A. G., Kerr I. M., Stark G. R. Overlapping sites for constitutive and induced DNA binding factors involved in interferon-stimulated transcription. EMBO J. 1989 Mar;8(3):831–839. doi: 10.1002/j.1460-2075.1989.tb03444.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Degos L. Differentiating agents in the treatment of leukemia and myelodysplastic syndromes. Leuk Res. 1990;14(8):731–733. doi: 10.1016/0145-2126(90)90103-g. [DOI] [PubMed] [Google Scholar]
  6. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edelson J. D., Shannon J. M., Mason R. J. Alkaline phosphatase: a marker of alveolar type II cell differentiation. Am Rev Respir Dis. 1988 Nov;138(5):1268–1275. doi: 10.1164/ajrccm/138.5.1268. [DOI] [PubMed] [Google Scholar]
  8. Giard D. J., Aaronson S. A., Todaro G. J., Arnstein P., Kersey J. H., Dosik H., Parks W. P. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst. 1973 Nov;51(5):1417–1423. doi: 10.1093/jnci/51.5.1417. [DOI] [PubMed] [Google Scholar]
  9. Goto I., Hozumi M., Honma Y. Selective effect of O-alkyl lysophospholipids on the growth of a human lung giant cell carcinoma cell line. Anticancer Res. 1994 Mar-Apr;14(2A):357–362. [PubMed] [Google Scholar]
  10. Guchelaar H. J., Timmer-Bosscha H., Dam-Meiring A., Uges D. R., Oosterhuis J. W., de Vries E. G., Mulder N. H. Enhancement of cisplatin and etoposide cytotoxicity after all-trans retinoic-acid-induced cellular differentiation of a murine embryonal carcinoma cell line. Int J Cancer. 1993 Sep 30;55(3):442–447. doi: 10.1002/ijc.2910550320. [DOI] [PubMed] [Google Scholar]
  11. Hanai N., Ishihara T., Uchino F., Imada N., Fujihara S., Ikegami J. Effects of dimethyl sulfoxide and colchicine on the resorption of experimental amyloid. Virchows Arch A Pathol Anat Histol. 1979;384(1):45–52. doi: 10.1007/BF00427150. [DOI] [PubMed] [Google Scholar]
  12. Harrison E. F., Hawke J. E., Hunter H. L., Costanzi J. J., Morgan L. R., Plotkin D., Tucker W. G., Worrall P. M. Single-dose ifosfamide: efficacy studies in non-small cell lung cancer. Semin Oncol. 1982 Dec;9(4 Suppl 1):56–60. [PubMed] [Google Scholar]
  13. Honma Y., Onozuka Y., Okabe-Kado J., Kasukabe T., Hozumi M. Hemin enhances the sensitivity of erythroleukemia cells to 1-beta-D-arabinofuranosylcytosine by both activation of deoxycytidine kinase and reduction of cytidine deaminase activity. Cancer Res. 1991 Sep 1;51(17):4535–4538. [PubMed] [Google Scholar]
  14. Hozumi M. Fundamentals of chemotherapy of myeloid leukemia by induction of leukemia cell differentiation. Adv Cancer Res. 1983;38:121–169. doi: 10.1016/s0065-230x(08)60189-x. [DOI] [PubMed] [Google Scholar]
  15. Huang M. E., Ye Y. C., Chen S. R., Chai J. R., Lu J. X., Zhoa L., Gu L. J., Wang Z. Y. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood. 1988 Aug;72(2):567–572. [PubMed] [Google Scholar]
  16. Iwasaki T., Hamano T., Aizawa K., Kobayashi K., Kakishita E. A case of pulmonary amyloidosis associated with multiple myeloma successfully treated with dimethyl sulfoxide. Acta Haematol. 1994;91(2):91–94. doi: 10.1159/000204262. [DOI] [PubMed] [Google Scholar]
  17. Kasahara K., Fujiwara Y., Nishio K., Ohmori T., Sugimoto Y., Komiya K., Matsuda T., Saijo N. Metallothionein content correlates with the sensitivity of human small cell lung cancer cell lines to cisplatin. Cancer Res. 1991 Jun 15;51(12):3237–3242. [PubMed] [Google Scholar]
  18. Kessler D. S., Pine R., Pfeffer L. M., Levy D. E., Darnell J. E., Jr Cells resistant to interferon are defective in activation of a promoter-binding factor. EMBO J. 1988 Dec 1;7(12):3779–3783. doi: 10.1002/j.1460-2075.1988.tb03262.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Klastersky J., Sculier J. P., Nicaise C., Weerts D., Mairesse M., Libert P., Rocmans P., Michel J., Ferremans W. Combination chemotherapy with cisplatin, etoposide, and vindesine in non-small cell lung carcinoma: a clinical trial of the EORTC lung cancer working party. Cancer Treat Rep. 1983 Jul-Aug;67(7-8):727–730. [PubMed] [Google Scholar]
  20. Koyama H., Ono T. Induction by short-chain fatty acids of alkaline phosphatase activity in cultured mammalian cells. J Cell Physiol. 1976 May;88(1):49–56. doi: 10.1002/jcp.1040880107. [DOI] [PubMed] [Google Scholar]
  21. Levy D. E., Kessler D. S., Pine R., Darnell J. E., Jr Cytoplasmic activation of ISGF3, the positive regulator of interferon-alpha-stimulated transcription, reconstituted in vitro. Genes Dev. 1989 Sep;3(9):1362–1371. doi: 10.1101/gad.3.9.1362. [DOI] [PubMed] [Google Scholar]
  22. Levy D. E., Kessler D. S., Pine R., Reich N., Darnell J. E., Jr Interferon-induced nuclear factors that bind a shared promoter element correlate with positive and negative transcriptional control. Genes Dev. 1988 Apr;2(4):383–393. doi: 10.1101/gad.2.4.383. [DOI] [PubMed] [Google Scholar]
  23. Lippman S. M., Kavanagh J. J., Paredes-Espinoza M., Delgadillo-Madrueño F., Paredes-Casillas P., Hong W. K., Holdener E., Krakoff I. H. 13-cis-retinoic acid plus interferon alpha-2a: highly active systemic therapy for squamous cell carcinoma of the cervix. J Natl Cancer Inst. 1992 Feb 19;84(4):241–245. doi: 10.1093/jnci/84.4.241. [DOI] [PubMed] [Google Scholar]
  24. Lippman S. M., Parkinson D. R., Itri L. M., Weber R. S., Schantz S. P., Ota D. M., Schusterman M. A., Krakoff I. H., Gutterman J. U., Hong W. K. 13-cis-retinoic acid and interferon alpha-2a: effective combination therapy for advanced squamous cell carcinoma of the skin. J Natl Cancer Inst. 1992 Feb 19;84(4):235–241. doi: 10.1093/jnci/84.4.235. [DOI] [PubMed] [Google Scholar]
  25. Loehrer P. J., Einhorn L. H. Drugs five years later. Cisplatin. Ann Intern Med. 1984 May;100(5):704–713. doi: 10.7326/0003-4819-100-5-704. [DOI] [PubMed] [Google Scholar]
  26. Martyré M. C., Wietzerbin J. Characterization of specific functional receptors for HuIFN-alpha on a human megakaryocytic cell line (Dami): expression related to differentiation. Br J Haematol. 1994 Feb;86(2):244–252. doi: 10.1111/j.1365-2141.1994.tb04722.x. [DOI] [PubMed] [Google Scholar]
  27. McCormick C., Freshney R. I., Speirs V. Activity of interferon alpha, interleukin 6 and insulin in the regulation of differentiation in A549 alveolar carcinoma cells. Br J Cancer. 1995 Feb;71(2):232–239. doi: 10.1038/bjc.1995.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Okabe-Kado J., Hayashi M., Honma Y., Hozumi M. Enhancement by hemin of the sensitivity of K562 human leukemic cells to 1-beta-D-arabinofuranosylcytosine. Cancer Res. 1986 Mar;46(3):1239–1243. [PubMed] [Google Scholar]
  29. Okabe-Kado J., Hayashi M., Honma Y., Hozumi M., Tsuruo T. Inhibition by erythroid differentiation factor (activin A) of P-glycoprotein expression in multidrug-resistant human K562 erythroleukemia cells. Cancer Res. 1991 May 15;51(10):2582–2586. [PubMed] [Google Scholar]
  30. Reuben R. C., Wife R. L., Breslow R., Rifkind R. A., Marks P. A. A new group of potent inducers of differentiation in murine erythroleukemia cells. Proc Natl Acad Sci U S A. 1976 Mar;73(3):862–866. doi: 10.1073/pnas.73.3.862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rutherford M. N., Hannigan G. E., Williams B. R. Interferon-induced binding of nuclear factors to promoter elements of the 2-5A synthetase gene. EMBO J. 1988 Mar;7(3):751–759. doi: 10.1002/j.1460-2075.1988.tb02872.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sakiyama S., Nakamura Y., Yasuda S. Expression of epidermal growth factor receptor gene in cultured human lung cancer cells. Jpn J Cancer Res. 1986 Oct;77(10):965–969. [PubMed] [Google Scholar]
  33. Samid D., Shack S., Sherman L. T. Phenylacetate: a novel nontoxic inducer of tumor cell differentiation. Cancer Res. 1992 Apr 1;52(7):1988–1992. [PubMed] [Google Scholar]
  34. Terasaki T., Shimosato Y., Nakajima T., Tsumuraya M., Morinaga S., Hirohashi S., Yamaguchi K., Kato K., Ichinose H., Nagatsu T. Changes in cell characteristics due to culture conditions in cell lines from human small cell lung cancer. Jpn J Clin Oncol. 1986 Sep;16(3):203–212. [PubMed] [Google Scholar]
  35. Xu B., Grandér D., Sangfelt O., Einhorn S. Primary leukemia cells resistant to alpha-interferon in vitro are defective in the activation of the DNA-binding factor interferon-stimulated gene factor 3. Blood. 1994 Sep 15;84(6):1942–1949. [PubMed] [Google Scholar]
  36. Yamada T., Hirohashi S., Shimosato Y., Kodama T., Hayashi S., Ogura T., Gamou S., Shimizu N. Giant cell carcinomas of the lung producing colony-stimulating factor in vitro and in vivo. Jpn J Cancer Res. 1985 Oct;76(10):967–976. [PubMed] [Google Scholar]
  37. Young C. W., Fanucchi M. P., Declan Walsh T., Baltzer L., Yaldaei S., Stevens Y. W., Gordon C., Tong W., Rifkind R. A., Marks P. A. Phase I trial and clinical pharmacological evaluation of hexamethylene bisacetamide administration by ten-day continuous intravenous infusion at twenty-eight-day intervals. Cancer Res. 1988 Dec 15;48(24 Pt 1):7304–7309. [PubMed] [Google Scholar]

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