Expression and up-regulation of retinoic acid receptor-β is associated with retinoid sensitivity and colony formation in esophageal cancer cell lines

Cancer Research

Volumn 59, Issue 10, 1999, Pages 2477-2483

  Xu, Xiao Chun ^a   Liu, Xiaoming ^a   Tahara, Eiichi ^b   Lippman, Scott M ^a   Lotan, Reuben ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b HIROSHIMA UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RETINOIC ACID RECEPTOR; RETINOID;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; COLONY FORMATION; CONTROLLED STUDY; ESOPHAGUS CANCER; GROWTH INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RECEPTOR UPREGULATION;

APOPTOSIS; CELL DIFFERENTIATION; CELL DIVISION; DRUG RESISTANCE; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; NEOPLASM PROTEINS; RECEPTORS, RETINOIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, NEOPLASM; TRETINOIN; TUMOR CELLS, CULTURED; TUMOR STEM CELL ASSAY; UP-REGULATION;

EID: 0033563248     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Coia, L. R., and Sauter, E. R. Esophageal cancer. Curr. Probl. Cancer, 18: 189-247, 1994.
2. Luketich, J. D., Schauer, P., Urso, K., Kassis, E., Ferson, P., Keenan, R., and Landreneau, R. Future directions in esophageal cancer. Chest, 113: 120S-122S, 1998.
3. Hoff, S. J., Sawyers, J. L., Blanke, C. D., Choy, H., and Stewart, J. R. Prognosis of adenocarcinoma arising in Barrett's esophagus. Ann. Thorac. Surg., 65: 176-181, 1998.
4. Ajani, J. A. Current status of new drugs and multidisciplinary approaches in patients with carcinoma of the esophagus. Chest, 113: 112S-119S, 1998.
5. Sharma, V. K., Chockalingam, H., Homung, C. A., Vasudeva, R., and Howden, C. W. Changing trends in esophageal cancer: a 15-year experience in a single center. Am. J. Gastroenterol., 93: 702-705, 1998.
6. Landis, S. H., Murray, T., Bolden, S., and Wingo, P. A. Cancer statistics 1998. CA Cancer J. Clin., 48: 6-29, 1998.
7. Kelloff, G. J., Boone, C. W., Steele, V. K., Perloff, M., Crowell, J., and Doody, L. A. Development of chemopreventive agents for lung and upper aerodigestive tract cancers. J. Cell. Biochem., 17 (Suppl. F): 2-17, 1993.
8. Moon, R. C., and Mehta, R. G. Retinoid inhibition of experimental carcinogenesis. In: M. I. Dawson and W. H. Okamura (eds.), Chemistry and Biology of Synthetic Retinoids, pp. 501-518. Boca Raton, FL: CRC Press, 1990.
9. Han, J. Highlights of the cancer chemoprevention studies in China. Prev. Med., 22: 712-722, 1993.
10. DeVita, V. T., Jr., Hellman, S., and Rosenberg, S. A (eds). Cancer: Principles and Practice of Oncology, pp. 231-258, 585-608, 980-1020. Philadelphia and New York: Lippincott-Raven Publishers, 1997.
11. Wolbach, S. B. Effects of vitamin A deficiency and hypervitaminosis in animals. In: W. H. Sebrell and R. S. Harris (eds.), The Vitamins, Vol. 1, pp. 106-137. New York: Academic Press, 1956.
12. Sporn, M. B., and Newton, D. L. Chemoprevention of cancer with retinoids. Fed. Proc., 38: 2528-2534, 1979.
13. Shklar, G., Schwartz, J., Grau, D., Trickier, D. P., and Wallace, K. D. Inhibition of hamster buccal pouch carcinogenesis by 13-cis-retinoic acid. Oral Surg. Oral. Med. Oral Pathol., 50: 45-52, 1980.
14. Lippman, S. M., Benner, S. E., and Hong, W. K. Cancer chemoprevention. J. Clin. Oncol., 12: 851-873, 1994.
15. Hong, W., Endicott, J., Itri, L. M., Doos, W., Batsakis, J. G., Bell, R., Fofonoff, S., Byers, R., Atkinson, E. N., Vaughan, C., Toth, B. B., Kramer, A., Dimery, I. W., Skipper, P., and Strong, S. 13-cis retinoic acid in the treatment of oral leukoplakia. N. Engl. J. Med., 315: 1501-1505, 1986.
16. Hong, W. K., Lippman, S. M., Itri, L. M., Karp, D. D., Lee, J. S., Byers, R. M., Schantz, S. S., Kramer, A. M., Lotan, R., Peters, L. L., Dimery, I. W., Brown, B. W., and Goepfert, H. Prevention of second primary tumors with isotretinoin in squamous-cell carcinoma of the head and neck. N. Engl. J. Med., 323: 795-801, 1990.
17. Lippman, S. M., Batsakis, J. G., Toth, B. B., Weber, R. S., Lee, J. J., Martin, J. W., Hays, G. J., Goepfert, H., and Hong, W. K. Comparison of low-dose isotretinoin with β carotene to prevent oral carcinogenesis. N. Engl. J. Med., 328: 15-20, 1993.
18. Inayama, Y., Kitamura, H., Shibagaki, T., Usuda, Y., Ito, T., Nakatani, Y., and Kanisawa, M. In vivo growth and differentiation potential of tracheal basal cells of rabbits in vitamin A deficiency. Int. J. Exp. Pathol., 77: 89-97, 1996.
19. Han, R. Studies on cancer chemoprevention in China (Abstract). Fourth International Conference on Prevention of Human Cancer: Nutrition and Chemoprevention Controversies (Tucson, AZ), p. A20, 1992.
20. Blot, W. J., Li, J. Y., and Taylor, P. R. Nutritional intervention trials in Linxian, China: supplementation with specific vitamin/mineral combination, cancer incidence and disease-specific mortality in the general population. J. Natl. Cancer Inst., 85: 1483-1492, 1993.
21. Li, J. Y., Taylor, P. R., and Li, B. Nutrition intervention trials in Linxian, China: multiple vitamin/mineral supplementation, cancer incidence and disease-specific mortality among adults with esophageal dysplasia. J. Natl. Cancer Inst., 85: 1492-1498, 1993.
22. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J., 10: 940-954, 1996.
23. Mangelsdorf, D. J., Umesono, K., and Evans, R. M. The retinoid receptors. In: M. B. Sporn, A. B. Roberts, and D. S. Goodman (eds.), The Retinoids. pp. 319-349. New York: Raven Press, 1994.
24. Chambon, P. The retinoid signaling pathway: molecular and genetic analyses. Semin. Cell Biol., 5: 115-125, 1994.
25. Gudas, L. J., Sporn, M. B., and Roberts, A. B. Cellular biology and biochemistry of the retinoids. In: M. B. Sporn, A. B. Roberts, and D. S. Goodman (eds.), The Retinoids. pp. 443-520, New York: Raven Press, 1994.
26. DeLuca, L. M. Retinoids and their receptors in differentiation, embryogenesis and neoplasia. FASEB J., 5: 2924-2933, 1991.
27. Lotan, R., and Clifford, J. L. Nuclear receptors for retinoids: mediators of retinoic acid effects on normal and malignant cells. Biomed. Pharmacother., 45: 145-156, 1994.
28. Xu, X-C., Ro, J. Y., Lee, J. S., Shin, D. M., Hong, W. K., and Lotan, R. Differential expression of nuclear retinoic acid receptors in normal, premalignant, and malignant head and neck tissues. Cancer Res., 54: 3580-3587, 1994.
29. Lotan, R., Xu, X-C., Lippman, S. M., Ro, J. Y., Lee, J. S., Lee, J. J., and Hong, W. K. Suppression of retinoic acid receptor β in premalignant oral lesions and its up-regulation by isotretinoin. N. Engl. J. Med., 332: 1405-1410, 1995.
30. Xu, X-C., Sozzi, G., Lee, J. S., Lee, J. J., Pastorino, U., Pilotti, S., Kurie, J. M., Hong, W. K., and Lotan, R. Suppression of nuclear retinoic acid receptor β in non-small cell lung cancer in vivo: implications in lung cancer development. J. Natl. Cancer Inst., 89: 624-629, 1997.
31. Xu, X-C., Sneige, N., Liu, X., Nandagiri, R., Lee, J. J., Lukmanji, F., Hortobagyi, G., Lippman, S. M., Dhingra, K., and Lotan, R. Progressive decrease in nuclear retinoic acid receptor β messenger RNA level during breast carcinogenesis. Cancer Res., 57: 4992-4996, 1997.
32. Xu, X-C., Stier, U., Rosewicz, S., El-Naggar, A-K., and Lotan, R. Selective suppression of nuclear retinoic acid receptor β gene expression in human pancreatic cancers. Int. J. Oncol., 8: 445-451, 1996.
33. Zou, C., Clifford, J. L., Xu, X-C., Sacks, P. G., Chambon, P., Hong, W. K., and Lotan, R. Modulation by retinoic acid of squamous cell differentiation, cellular RA-binding proteins, and nuclear RA receptors in human head and neck squamous carcinoma cell lines. Cancer Res., 54: 5479-5487, 1994.
34. de Thè, H., Chomienne, C., Lanotte, M., Dego, L., and Dejean, A. The t(15;17) translocation of acute promyelocytic leukemia fuses the retinoic acid receptor a gene to a novel transcribed locus. Nature (Lond.), 347: 558-561, 1990.
35. Hu, L., Crowe, D. L., Rheinwald, J. G., Chambon, P., and Gudas, L. J. Abnormal expression of retinoic acid receptors and keratin 19 by human oral and epidermal squamous cell carcinoma cell lines. Cancer Res., 51: 3972-3981, 1991.
36. Gebert, J. F., Moghal, N., Frangioni, J. V., Sugarbaker, D. J., and Neel, B. G. High frequency of retinoic acid receptor β abnormalities in human lung cancer. Oncogene, 6: 1859-1868, 1991.
37. Houle, B., Leduc, F., and Bradley, W. E. Implication of RAR-β in epidermoid (squamous) lung cancer. Genes Chromosomes Cancer, 3: 358-366, 1991.
38. Houle, B., Rochette-Egly, C., and Bradley, W. E. Tumor-suppressive effect of the retinoic acid receptor β in human epidermoid lung cancer cells. Proc. Natl. Acad. Sci. USA, 90: 985-989, 1993.
39. Geradts, J., Chen, J-Y., Russell, E. K., Yankaskas, J. R., Nieves, L., and Minna, J. D. Human lung cancer cell lines exhibit resistance to retinoic acid treatment. Cell Growth Differ., 4: 799-809, 1993.
40. Swisshelm, K., Ryan, K., Lee, X., Tsou, H. C., Peacocke, M., and Sager, R. Down-regulation of retinoic acid receptor β in mammary carcinoma cell lines and its up-regulation in senescing normal mammary epithelial cells. Cell Growth Differ., 5: 133-141, 1994.
41. de Thè, H. Altered retinoic acid receptor. FASEB J., 10: 955-960, 1996.
42. Oridate, N., Lotan, D., Xu, X-C., Hong, W. K., and Lotan, R. Differential induction of apoptosis by all-trans-retinoic acid and N-(4-hydroxyphenyl)retinamide in human head and neck squamous cell carcinoma cell lines. Clin. Cancer Res., 2: 855-863, 1996.
43. Xu, X-C., Clifford, J. L., Hong, W. K., and Lotan, R. Detection of nuclear retinoic acid receptor mRNA in histological tissue sections using nonradioactive in situ hybridization histochemistry. Diagn. Mol. Pathol., 3: 122-131, 1994.
44. Hoffmann, W., Schiebe, M., Hirnle, P., Souchon, R., Clemens, M., Adamietz, I., and Bamberg, M. 13-cis retinoic acid and interferon-α ± irradiation in the treatment of squamous-cell carcinomas. Int. J. Cancer., 70: 475-477, 1997.
45. Slabber, C. F., Falkson, G., Burger, W., and Schoeman, L. 13-Cis-retinoic acid and interferon α-2a in patients with advanced esophageal cancer: a phase II trial. Invest. New Drugs., 14: 391-394, 1996.
46. Lotan, R. Effects of vitamin A and its analogs (retinoids) on normal and neoplastic cells. Biochem. Biophys. Acta, 605: 33-91, 1980.
47. Lotan, R. Squamous cell differentiation markers in normal, premalignant, and malignant epithelium: effects of retinoids. J. Cell. Biochem., 17 (Suppl. F): 167-174, 1993.
48. Jetten, A. M., Kim, J. S., Sacks, P. G., Rearick, J. I., Lotan, D., Hong, W. K., and Lotan, R. Suppression of growth and squamous cell differentiation markers in cultured human head and neck squamous carcinoma cells by β-all-trans-retinoic acid. Int. J. Cancer, 45: 195-202, 1990.
49. Sacks, P. G., Oke, V., Amos, B., Vasey, T., and Lotan, R. Modulation of growth, differentiation, and glycoprotein synthesis by β-all-trans retinoic acid in a multicellular tumor spheroid model for squamous carcinoma of the head and neck. Int. J. Cancer, 45: 926-933, 1989.
50. Muller, A., Nakagawa, H., and Rustgi, A. K. Retinoic acid and N-(4-hydroxy-phenyl) retinamide suppress growth of esophageal squamous carcinoma cell lines. Cancer Lett., 113: 95-101, 1997.
51. Seewaldt, V. L., Johnson, B. S., Parker, M. B., Collins, S. J., and Swisshelm, K. Expression of retinoic acid receptor β mediates retinoic acid-induced growth arrest and apoptosis in breast cells. Cell Growth Differ., 6: 1077-1088, 1995.
52. Liu, Y., Lee, M. O., Wang, H. G., Li, Y., Hashimoto, Y., Klaus, M., Reed, J. C., and Zhang, X. K. Retinoic acid receptor β mediates the growth-inhibitory effect of retinoic acid by promoting apoptosis in human breast cancer cells. Mol. Cell Biol., 16: 1138-1149, 1996.
53. Zhang, M., Martin, K. J., Sheng, S., and Sager, R. Expression genetics: a different approach to cancer diagnosis and prognosis. Trends Biotechnol., 16: 66-71, 1998.
54. Berard, J., Laboune, F., Mukuna, M., Masse, S., Kothary, R., and Bradley, W. E. C. Lung tumors in mice expressing an antisense RAR-β2 transgene. FASEB J., 10: 1091-1097, 1996.
55. Ogasawara, S., Maesawa, C., Tamura, G., and Satodate, R. Frequent microsatellite alterations on chromosome 3p in esophageal squamous cell carcinoma. Cancer Res., 55: 891-894, 1995.
56. Bartsch, D., Boye, B., Baust, C., zur Hausen, H., and Schwarz, E. Retinoic acid-mediated repression of human papillomavirus 18 transcription and different ligand regulation of the retinoic acid receptor β gene in non-tumorigenic and tumorigenic HeLa hybrid cells. EMBO J., 11: 2283-2291, 1992.
57. Halachmi, S., Marden, E., Martin, G., MacKay, H., Abbondanza, C., and Brown, M. Estrogen receptor-associated proteins: possible mediators of hormone-induced transcription. Science (Washington DC), 264: 1455-1458, 1994.
58. Zhang, X-K., Liu, Y., Lee, M-O., and Pfahl, M. A specific defect in the retinoic acid response associated with human lung cancer cell lines. Cancer Res. 54: 5663-5669, 1994.
59. Oridate, N., Zou, C. P., Mitchell, M. F., Hong, W. K., and Lotan, R. Activation by retinoic acid of native retinoic acid receptor β2 promoter is suppressed in human oral squamous cell carcinoma SqCC/Y1 cells. Mol. Cell. Differ., 2: 413-431, 1994.
60. Zhang, X. K., Liu, Y., and Lee, M. O. Retinoid receptors in human lung cancer and breast cancer. Mutat. Res., 350: 267-277, 1996.
61. Xu, X-C., Zile, M. H., Lippman, S. M., Lee, J. S., Lee, J. J., Hong, W. K., and Lotan, R. Anti-retinoic acid antibody binding to human premalignant oral lesions is lower than to normal tissue, is increased after 13-cis-retinoic acid treatment in vivo, and is related to retinoic acid receptor beta expression. Cancer Res., 55: 5507-5511, 1995.
62. Verma, A. K., Shoemaker, A., Simsiman, R., Denning, M., and Zachman, R. D. Expression of retinoic acid nuclear receptors and tissue transglutaminase is altered in various tissues of rats fed a vitamin A-deficient diet. J. Nutr., 122: 2144-2152, 1992.
63. Kato, S., Mano, H. M., Kumazawa, T., Yoshizawa, Y., Kojima, R., and Masushige, S. Effect of retinoid status on α, β, and y retinoic acid receptor mRNA levels in various rat tissues. Biochem. J., 286: 755-760, 1992.
64. Aoki, T., Mori, T., Du, X., Nisihira, T., Matsubara, T., and Nakamura, Y. Allelotype study of esophageal carcinoma. Genes, Chromosomes Cancer, 10: 177-182, 1994.
65. Montesano, R., Hollstein, M., and Hainaut, P. Genetic alterations in esophageal cancer and their relevance to etiology and pathogenesis: a review. Int. J. Cancer, 69: 225-235, 1996.
66. Bennett, W. P., von Brevern, M. C., Zhu, S. M., Bartsch, H., Muehlbauer, K. R., and Hollstein, M. C. p53 mutations in esophageal tumors from a high incidence area of China in relation to patient diet and smoking history. Cancer Epidemiol. Biomark. Prev., 6: 963-966, 1997.
67. Takeuchi, H., Ozawa, S., Ando, N., Shih, C-H., Koyanagi, K., Ueda, M., and Kitajima, M. Altered p16/MTS1/CDKN2 and cyclin DI/PRAD-I gene expression is associated with the prognosis of squamous cell carcinoma of the esophagus. Clin. Cancer Res., 3: 2229-2236, 1997.
68. Yoshida, K., Kuniyasu, H., Yasui, W., Kitadai, Y., Toge, T., and Tahara, E. Expression of growth factors and their receptors in human esophageal carcinomas: regulation of expression by epidermal growth factor and transforming growth factor α. J. Cancer Res. Clin. Oncol., 119: 401-407, 1993.