Metabolism of all-trans-retinol in normal human cell strains and squamous cell carcinoma (SCC) lines from the oral cavity and skin: Reduced esterification of retinol in SCC lines

Cancer Research

Volumn 58, Issue 1, 1998, Pages 166-176

  Guo, Xiaojia ^a   Gudas, Lorraine J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 OXORETINOIC ACID; BENZYLSULFONYL FLUORIDE; DEHYDRORETINOL; DRUG METABOLITE; DRUG VEHICLE; PALMITOYL COENZYME A; RETINAL; RETINOIC ACID; RETINOIC ACID BINDING PROTEIN; RETINOID; RETINOL; RETINOL ACYLTRANSFERASE; RETINOL BINDING PROTEIN; RETINOL DERIVATIVE; RETINOL ESTER;

ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; DRUG EFFICACY; DRUG METABOLISM; ESTERIFICATION; FACE CANCER; HUMAN; HUMAN CELL; MOUTH CARCINOMA; PRIORITY JOURNAL; SKIN CARCINOMA; SOFT PALATE; SQUAMOUS CELL CARCINOMA;

CARCINOMA, SQUAMOUS CELL; HUMANS; MOUTH NEOPLASMS; SKIN NEOPLASMS; TRETINOIN; TUMOR CELLS, CULTURED;

EID: 0031975456     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Bertram, J. S., Kolonel, L-C., and Meyskens, F. R., Jr. Rationale and strategies for chemoprevention of cancer in humans. Cancer Res., 47: 3012-3031, 1987
2. Chen, L-C., Sly, L., and De Luca, L. M. High dietary retinoic acid prevents malignant conversion of skin papillomas induced by a two-stage carcinogenesis in female SENCAR mice. Carcinogenesis (Lond.), 15: 2383-2386, 1994.
3. Pollard, M., Luckert, P. H., and Sporn, M. B. Prevention of primary prostate cancer in Lobund-Wistar rats by N-(4-hydroxyphenyl) retinamide. Cancer Res., 51: 3610-3611, 1991.
4. Moon, R. C., Mehta, R. G., and Rao, K. V. N. Retinoids and cancer in experimental animals. In: M. B. Sporn, A. B. Roberts, and D. S. Goodman (eds.), The Retinoids: Biology, Chemistry and Medicine, pp. 573-596. New York: Raven Press, 1994.
5. Abemayor, E. The effects of retinoic acid on the in vitro and in vivo growth of neuroblastoma cells. Laryngoscope, 102: 1133-1149, 1992.
6. Lippman, S. M., Kavanagh, J. J., Paredes-Espinoza, M., Delgadillo-Madrueno, F., Paredes-Casillas, P., Hong, W. K., Massimini, G., Holdener, E. E., and Krakoff, I. H. 13-cis-retinoic acid plus interferon-α2 in locally advanced squamous cell carcinoma carcinoma of the cervix. J. Natl. Cancer Inst., 85: 499-500, 1993.
7. Hong, W. K., and Itri, L. M. Retinoids and human cancer. In: M. B. Sporn, A. B. Roberts and D. S. Goodman (eds.), The Retinoids: Biology, Chemistry, and Medicine, pp. 597-630. New York: Raven Press, 1994.
8. Lotan, R. Effects of vitamin A and its analogs (retinoids) on normal and neoplastic cells. Biochim. Biophys. Acta, 605: 33-91, 1980.
9. 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: Biology, Chemistry, and Medicine, pp. 443-520. New York: Raven Press, 1994.
10. Darmon, M. Retinoic acid in skin and epithelia. Semin. Dev. Biol., 2: 219-228, 1991.
11. Ong, D. E., Newcomer, M. E., and Chytil, F. Cellular retinoid-binding proteins. In: M. B. Sporn, A. B. Roberts and D. S. Goodman (eds.), The Retinoids: Biology, Chemistry, and Medicine, pp. 283-318. New York: Raven Press, 1994.
12. Törma, H., and Vahlquist, A. Vitamin A esterification in human epidermis: a relationship to keratinocyte differentiation. J. Invest. Dermatol., 94: 132-138, 1990.
13. Napoli, J. L., Harris, S., Shields, C., and Cummings, C. Retinol metabolism in LLC-PK1 cells: characterization of retinoic acid synthesis by an established mammalian cell line. J. Biol. Chem., 261: 13592-13597, 1986.
14. Siegenthaler, G., Saurat, J-H., and Ponec, M. Retinol and retinal metabolism: relationship to the state of differentiation of cultured human keratinocytes. Biochem. J., 268: 371-378, 1990.
15. Achkar, C. C., Derguini, F., Blumberg, B., Langston, A., Levin, A. A., Speck, J., Evans, R. M., Bolado, J., J., Nakanishi, K., Buck, J., and Gudas, L. J. 4-Oxoretinol, a new natural ligand and transactivator of the retinoic acid receptors. Proc. Natl. Acad. Sci. USA, 93: 4879-4884, 1996.
16. Chen, H., Namkung, M. J., and Juchau, M. R. Biotransformation of all-trans-retinol and all-trans-retinal to all-trans-retinoic acid in rat conceptal homogenates. Biochem. Pharmacol., 50: 1257-1264, 1995.
17. Buck, J., Derguini, F., Levi, E., Nakanishi, K., and Hammerling, U. Intracellular signalling by 14-hydroxy-4,14-retro-retinol. Science (Washington DC), 254: 1654-1656, 1991.
18. Buck, J., Grün, F., Kimura, S., Noy, N., Derguini, F., and Hammerling, U. Anhydroretinol: a naturally occurring inhibitor of lymphocyte physiology. J. Exp. Med., 178: 675-680, 1993.
19. Hong, W. K., and Lotan, R. Retinoids in Oncology. New York: Marcel Dekker, 1993.
20. Warrell, R. P., Jr., Stanley, R., Frankel, S. R., Miller, W. H., Jr., Scheinberg, D. A., Itri, L. M., Hittelman, W. N., Vyas, R., Andreeff, M., Tafuri, A., Jakubowski, A., Gabrilove, J., Gordon, M. S., and Dmitrovsky, E. Differentiation therapy of acute promyelocytic leukemia with tretinoin (all-trans retinoic acid). N. Engl. J. Med., 324: 1385-1393, 1991.
21. 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: Biology, Chemistry and Medicine, pp. 319-350. New York: Raven Press, 1994.
22. Krust, A., Kastrier, P., Petkovich, M., Zelent, A., and Chambon, P. A third human retinoic acid receptor, hRAR-γ Proc. Natl. Acad. Sci. USA, 86: 5310-5314, 1989.
23. Elder, J. T., Fisher, G. J., Zhang, Q. Y., Eisen, D., Krust, A., Kastner, P., Chambon, P., and Voorhees, J. J. Retinoic acid receptor gene expression in human skin. J. Invest. Dermatol., 96: 425-433, 1991.
24. Elder, J. T., Aström, A., Pettersson, U., Tavakkol, A., Griffiths, C. E., Krust, A., Kastner, P., Chambon, P., and Voorhees, J. J. Differential regulation of retinoic acid receptors and binding proteins in human skin. J. Invest. Dermatol., 98: 673-679, 1992.
25. Fisher, G. J., Talwar, H. S., Xiao, J-H., Datta, S. C., Reddy, A. P., Gaub, M. P., Rochette-Egly, C., Chambon, P., and Voorhees, J. J. Immunological identification and functional quantitation of retinoic acid and retinoid X receptor proteins in human skin. J. Biol. Chem., 269: 20629-20635, 1995.
26. Xiao, J-H., Durand, B., Chambon, P., and Voorhees, J. J. Endogenous retinoic acid receptor (RAR)-retinoid X receptor (RXR) heterodimers are the major functional forms regulating retinoid-responsive elements in adult human keratinocytes. Binding of ligands to RAR only is sufficient for RAR-RXR heterodimers to confer ligand-dependent activation of hRAR β 2/RARE (DR5). J. Biol. Chem., 270: 3001-3011, 1995.
27. Vollberg, T. M., Nervi, C., George, M. D., Fujimoto, W., Krust, A., and Jetten, A. M. Retinoic acid receptors as regulators of human epidermal keratinocyte differentiation. Mol. Endocrinol., 6: 667-676, 1992.
28. 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.
29. Randolph, R. K., and Simon, M. Characterization of retinol metabolism in cultured human epidermal keratinocytes. J. Biol. Chem., 268: 9198-9205, 1993.
30. Vahlquist, A. Vitamin A in human skin: I. Detection and identification of retinoids in normal epidermis. J. Invest. Dermatol., 79: 89-93, 1982.
31. Kurlandsky, S. B., Xiao, J. H., Duell, E. A., Voorhees, J. J., and Fisher, G. J. Biological activity of all-trans retinol requires metabolic conversion to all-trans retinoic acid and is mediated through activation of nuclear retinoid receptors in human keratinocytes. J. Biol. Chem., 269: 32821-32827, 1994.
32. Blumberg, B., Bolado, J., Jr., Derguini, F., Craig, A. G., Moreno, T. A., Charkaravarti, D., Heyman, R. A., Buck, J., and Evans, R. M. Novel RAR ligands in Xenopus embryos. Proc. Natl. Acad. Sci. USA, 93: 4873-4878, 1996.
33. Kaulsky, M. B., Fleckman, P., and Dale, B. A. Retinoic acid regulates oral epithelial differentiation by two mechanisms. J. Invest. Dermatol., 104: 224-230, 1995.
34. Lindberg, K., and Rheinwald, J. G. Three distinct keratinocyte subtypes identified in human oral epithelium by their patterns of keratin expression in culture and in xenografts. Differentiation, 45: 230-241, 1990.
35. Shafer, W. G., Hine, M. A., and Levy, B. M. Oral Pathology. Philadelphia: W. B. Saunders, 1976.
36. Hong, W. K., 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., Lippman, S. M., Skipper, P., and Strong, S. 13-cis-retinoic acid in the treatment of oral leukoplakia. N. Engl. J. Med., 315: 1501-1505, 1986.
37. Hong, W. K., Lippman, S. M., Itri, L. M., Karp, D. D., Lee, J. S., Byers, R. M., Schantz, S. P., Kramer, A. M., Lotan, R., Peters, L. J., 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.
38. 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.
39. de Thé, H., Marchio, P., Tiollais, P., and Dejean, A. Differential expression and ligand regulation of the retinoic acid receptor a and β genes. EMBO J., 8: 429-433, 1987.
40. Hu, L., and Gudas, L. J. Cyclic AMP analogs and retinoic acid influence the expression of RARα, β, and γ mRNAs in F9 murine teratocarcinoma cells. Mol. Cell. Biol., 10: 391-396, 1990.
41. Rheinwald, J. G., and Beckett, M. A. Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultured from human squamous cell carcinomas. Cancer Res., 41: 1657-1663, 1981.
42. Crowe, D. L., Hu, L., Gudas, L. J., and Rheinwald, J. Variable expression of retinoic acid receptor β (RAR β) mRNA in human oral and epidermal keratinocytes: relation to keratin 19 expression and keratinization potential. Differentiation, 48: 199-208, 1991.
43. De Leenheer, A. P., Lambert, W. E., and Claeys, I. All-trans-retinoic acid: measurement of reference values in human serum by high performance liquid chromatography. J. Lipid Res., 23: 1362-1367, 1982.
44. Fuchs, E., and Green, H. Regulation of terminal differentiation of cultured human keratinocytes by vitamin A. Cell, 25: 617-625, 1981.
45. McLean, S. W., Ruddel, M. E., Gross, E. G., DiGiovanna, J. J., and Peck, G. L. Liquid chromatographic assay for retinol (vitamin A) and retinol analogs in therapeutic trials. Clin. Chem., 28: 693-696, 1982.
46. Chen, A. C., and Gudas, L. J. An analysis of retinoic acid-induced gene expression and metabolism in AB1 embryonic stem cells. J. Biol. Chem., 14971-14980, 1996.
47. Ball, M. D. Acyl coenzyme A-dependent retinol esterification. In: L. Packer (ed.), Methods in Enzymology, pp. 446-449. New York: Academic Press, 1990.
48. Ottonello, S., Scita, G., Mantovani, G., Cavazzini, D., and Rossi, G. L. Retinol bound to cellular retinol-binding protein is a substrate for cytosolic retinoic acid synthesis. J. Biol. Chem., 268: 27133-27142, 1993.
49. Chai, X., Boerman, M. H. E. M., Zhai, Y., and Napoli, J. L. Cloning of a cDNA for liver microsomal retinol dehydrogenase. A tissue-specific, short-chain alcohol dehydrogenase. J. Biol. Chem., 270: 3900-3904, 1995.
50. Boerman, M. H. E. M., and Napoli, J. L. Cellular retinol-binding protein-supported retinoic acid synthesis. Relative roles of microsomes and cytosol. J. Biol. Chem., 271: 5610-5616, 1996.
51. Kurlandsky, S. B., Duell, E. A., Kang, S., Voorhees, J. J., and Fisher, G. J. Autoregulation of retinoic acid biosynthesis through regulation of retinol esterification in human keratinocytes. J. Biol. Chem., 271: 15346-15352, 1996.
52. MacDonald, P. N., and Ong, D. E. A lecithin:retinol acyltransferase activity in human and rat liver. Biochem. Biophys. Res. Commun., 156: 157-163, 1988.
53. Törma, H., and Vahlquist, A. Retinol esterification by mouse epidermal microsomes: evidence for acyl-CoA:retinol acyltransferase activity. J. Invest. Dermatol., 88: 398-402, 1987.
54. Berne, B., Torma, H., Staberg, B., Mikkelsen, S., and Vahlquist, A. Decreased retinyl ester concentrations in UV-induced murine squamous cell carcinomas. Acta Dermato-Venereol., 69: 503-508, 1989.
55. Bhat, P. V., and Jetten, A. M. Metabolism of all-trans-retinol and all-trans-retinoic acid in rabbit tracheal epithelial cells in culture. Biochim. Biophys. Acta, 922: 18-27, 1987.
56. Rollman, O., Wood, E. J., Olsson, M. J., and Cunliffe, W. J. Biosynthesis of 3,4-didehydroretinol from retinol by human skin keratinocytes in culture. Biochem. J., 293: 675-682, 1993.
57. Creek, K. E., St. Hilaire, P., and Hodam, J. R. A comparison of the uptake, metabolism and biologic effects of retinol delivered to human keratinocytes either free or bound to serum retinol-binding protein. J. Nutr., 123: 356-361, 1993.
58. Blaner, W. S., and Olson, J. A. Retinol and retinoic acid metabolism. In: M. B. Sporn Roberts, A. B., and Goodman, D. S. (eds.), The Retinoids: Biology, Chemistry, and Medicine, pp. 229-256. New York: Raven Press, 1994.
59. Ross, A. C. Retinol esterification by mammary gland microsomes from the lactating rat. J. Lipid Res., 23: 133-144, 1982.
60. Randolph, R. K., and Simon, M. Metabolic regulation of active retinoid concentrations in cultured human epidermal keratinocytes by exogenous fatty acids. Arch. Biochem. Biophys., 318: 6-14, 1995.
61. Randolph, R. K., and Simon, M. All-trans-retinoic acid regulates retinol and 3,4-didehydroretinol metabolism in cultured human epidermal keratinocytes. J. Invest. Dermatol., 106: 168-175, 1996.
62. Xu, X-C., Ro, J. Y., Shin, D. M., Hong, W. K., and Lotan, R. Differential expression of nuclear retinoid receptors in normal, premalignant, and malignant head and neck tissues. Cancer Res., 54: 3580-3587, 1994.
63. 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.
64. 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.
65. 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.
66. Seewaldt, V. L., Johnson, B. S., Parker, M. B., and Collins, S. J. Expression of retinoic acid receptor β mediates retinoic acid-induced growth arrest and apoptosis in breast cancer cells. Cell Growth Differ., 6: 1077-1088, 1995.
67. Blomhoff, R., Green, M. H., Berg, T., and Norum, K. R. Transport and storage of vitamin A. Science (Washington DC), 250: 399-404, 1990.
68. Törma, H., and Vahlquist, A. Retinol uptake and metabolism to 3,4-didehydroretinol in human keratinocytes at various stages of differentiation. Skin Pharmacol., 4: 154-157, 1991.
69. Vahlquist, A., Andersson, E., Coble, B. I., Rollman, O., and Törma, H. Increased concentrations of 3,4-didehydroretinol and retinoic acid-binding protein (CRABP II) in human squamous cell carcinoma and keratoacanthoma but not in basal cell carcinoma of the skin. J. Invest. Dermatol., 106: 1070-1074, 1996.
70. Andersson, E., Bjorklind, C., Torma, H., and Vahlquist, A. The metabolism of vitamin A to 3,4-didehydroretinol can be demonstrated in human keratinocytes, melanoma cells and HeLa cells, and is correlated to cellular retinoid-binding protein expression. Biochim. Biophys. Acta, 1224: 349-359, 1994.
71. Labrecque, J., Bhat, P. V., and Lacroix, A. Purification and partial characterization of a rat kidney aldehyde dehydrogenase that oxidizes retinal to retinoic acid. Biochem. Cell Biol., 71: 85-89, 1993.