Oral carcinogenesis induced by 4-nitroquinoline 1-oxide in lecithin: Retinol acyltransferase gene knockout mice

Journal of Nutritional Biochemistry

Volumn 21, Issue 10, 2010, Pages 975-982

  Liu, Limin ^a   Tang, Xiao Han ^a   Scognamiglio, Theresa ^a   Gudas, Lorraine J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Cancer prevention; Nutrition; Retinoic acid; Retinol; Squamous cell carcinoma of the head and neck; Stem cell

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; BROXURIDINE; CYCLIN D1; CYCLOOXYGENASE 2; LECITHIN RETINOL ACYLTRANSFERASE; PROTEIN P21; RETINOIC ACID RECEPTOR; RETINOL; SECRETED FRIZZLED RELATED PROTEIN 1; SECRETED FRIZZLED RELATED PROTEIN 2; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INCIDENCE; CARCINOGENESIS; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; EPITHELIUM CELL; FEMALE; KNOCKOUT MOUSE; MALE; MOUSE; MOUTH CANCER; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RETINOL DEFICIENCY; SIGNAL TRANSDUCTION; TONGUE; WILD TYPE;

4-NITROQUINOLINE-1-OXIDE; ACYLTRANSFERASES; ANIMALS; BASE SEQUENCE; CARCINOGENS; CARCINOMA, SQUAMOUS CELL; DNA PRIMERS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOUTH NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VITAMIN A;

MUS;

EID: 77956647797     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2009.07.012     Document Type: Article

References (69)

1. Argiris A., Karamouzis M.V., Raben D., Ferris R.L. Head and neck cancer. Lancet 2008, 371:1695-1709.
2. Haddad R.I., Shin D.M. Recent advances in head and neck cancer. N Engl J Med 2008, 359:1143-1154.
3. Gudas L.J., Sporn M.B., Roberts A. Cellular biology and biochemistry of retinoids. The retinoids: biology, chemistry, and medicine 1994, 443-520. Raven Press, New York. M.B. Sporn, A.B. Roberts, D.S. Goodman (Eds.).
4. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996, 10:940-954.
5. Mangelsdorf D.J., Thummel C., Beato M., Herrlich P., Schutz G., Umesono K., et al. The nuclear receptor superfamily: the second decade. Cell 1995, 83:835-839.
6. Hu L., Crowe D.L., Rheinwald J.G., Chambon P., Gudas L.J. Abnormal expression of retinoic acid receptors and keratin 19 by human oral and epidermal squamous cell carcinoma cell lines. Cancer Res 1991, 51:3972-3981.
7. Lotan R. Retinoids and their receptors in modulation of differentiation, development, and prevention of head and neck cancers. Anticancer Res 1996, 16:2415-2419.
8. Love J.M., Gudas L.J., Vitamin A differentiation and cancer. Curr Opin Cell Biol 1994, 6:825-831.
9. Xu X.C., Ro J.Y., Lee J.S., Shin D.M., Hong W.K., Lotan R. Differential expression of nuclear retinoid receptors in normal, premalignant, and malignant head and neck tissues. Cancer Res 1994, 54:3580-3587.
10. Soprano D.R., Qin P., Soprano K.J. Retinoic acid receptors and cancers. Annu Rev Nutr 2004, 24:201-221.
11. Sun S.Y., Lotan R. Retinoids and their receptors in cancer development and chemoprevention. Crit Rev Oncol Hematol 2002, 41:41-55.
12. Youssef E.M., Lotan D., Issa J.P., Wakasa K., Fan Y.H., Mao L., et al. Hypermethylation of the retinoic acid receptor-beta(2) gene in head and neck carcinogenesis. Clin Cancer Res 2004, 10:1733-1742.
13. Ha P.K., Califano J.A. Promoter methylation and inactivation of tumour-suppressor genes in oral squamous-cell carcinoma. Lancet Oncol 2006, 7:77-82.
14. Giannini F., Maestro R., Vukosavljevic T., Pomponi F., Boiocchi M. All-trans, 13-cis and 9-cis retinoic acids induce a fully reversible growth inhibition in HNSCC cell lines: implications for in vivo retinoic acid use. Int J Cancer 1997, 70:194-200.
15. Lotan R., Xu X.C., Lippman S.M., Ro J.Y., Lee J.S., Lee J.J., et al. Suppression of retinoic acid receptor-beta in premalignant oral lesions and its up-regulation by isotretinoin. N Engl J Med 1995, 332:1405-1410.
16. Altucci L., Leibowitz M.D., Ogilvie K.M., de Lera A.R., Gronemeyer H. RAR and RXR modulation in cancer and metabolic disease. Nat Rev Drug Discov 2007, 6:793-810.
17. Clarke N., Germain P., Altucci L., Gronemeyer H. Retinoids: potential in cancer prevention and therapy. Expert Rev Mol Med 2004, 6:1-23.
18. Lippman S.M., Sudbo J., Hong W.K. Oral cancer prevention and the evolution of molecular-targeted drug development. J Clin Oncol 2005, 23:346-356.
19. Mongan N.P., Gudas L.J. Diverse actions of retinoid receptors in cancer prevention and treatment. Differentiation 2007, 75:853-870.
20. Harrison E.H. Lipases and carboxylesterases: possible roles in the hepatic utilization of vitamin A. J Nutr 2000, 130:340S-344S.
21. Harrison E.H. Mechanisms of digestion and absorption of dietary vitamin A. Annu Rev Nutr 2005, 25:87-103.
22. Blomhoff R., Rasmussen M., Nilsson A., Norum K.R., Berg T., Blaner W.S. Hepatic retinol metabolism. Distribution of retinoids, enzymes, and binding proteins in isolated rat liver cells. J Biol Chem 1985, 260:13560-13565.
23. Matsuura T., Gad M.Z., Harrison E.H., Ross A.C. Lecithin:retinol acyltransferase and retinyl ester hydrolase activities are differentially regulated by retinoids and have distinct distributions between hepatocyte and nonparenchymal cell fractions of rat liver. J Nutr 1997, 127:218-224.
24. Ong D.E., MacDonald P.N., Gubitosi A.M. Esterification of retinol in rat liver. Possible participation by cellular retinol-binding protein and cellular retinol-binding protein II. J Biol Chem 1988, 263:5789-5796.
25. Ross A.C., Zolfaghari R. Regulation of hepatic retinol metabolism: perspectives from studies on vitamin A status. J Nutr 2004, 134:269S-275S.
26. Liu L., Gudas L.J. Disruption of the lecithin:retinol acyltransferase gene makes mice more susceptible to vitamin A deficiency. J Biol Chem 2005, 280:40226-40234.
27. Zolfaghari R., Ross A.C. Lecithin:retinol acyltransferase expression is regulated by dietary vitamin A and exogenous retinoic acid in the lung of adult rats. J Nutr 2002, 132:1160-1164.
28. Herr F.M., Wardlaw S.A., Kakkad B., Albrecht A., Quick T.C., Ong D.E. Intestinal vitamin A metabolism: coordinate distribution of enzymes and CRBP(II). J Lipid Res 1993, 34:1545-1554.
29. MacDonald P.N., Ong D.E. Evidence for a lecithin-retinol acyltransferase activity in the rat small intestine. J Biol Chem 1988, 263:12478-12482.
30. Gollapalli D.R., Rando R.R. All-trans-retinyl esters are the substrates for isomerization in the vertebrate visual cycle. Biochemistry 2003, 42:5809-5818.
31. Saari J.C., Bredberg D.L. Lecithin:retinol acyltransferase in retinal pigment epithelial microsomes. J Biol Chem 1989, 264:8636-8640.
32. Saari J.C., Bredberg D.L., Farrell D.F. Retinol esterification in bovine retinal pigment epithelium: reversibility of lecithin:retinol acyltransferase. Biochem J 1993, 291(Pt 3):697-700.
33. Shingleton J.L., Skinner M.K., Ong D.E. Retinol esterification in Sertoli cells by lecithin-retinol acyltransferase. Biochemistry 1989, 28:9647-9653.
34. Guo X., Ruiz A., Rando R.R., Bok D., Gudas L.J. Esterification of all-trans-retinol in normal human epithelial cell strains and carcinoma lines from oral cavity, skin and breast: reduced expression of lecithin:retinol acyltransferase in carcinoma lines. Carcinogenesis 2000, 21:1925-1933.
35. Kurlandsky S.B., Duell E.A., Kang S., Voorhees J.J., Fisher G.J. Auto-regulation of retinoic acid biosynthesis through regulation of retinol esterification in human keratinocytes. J Biol Chem 1996, 271:15346-15352.
36. Randolph R.K., Winkler K.E., Ross A.C. Fatty acyl CoA-dependent and -independent retinol esterification by rat liver and lactating mammary gland microsomes. Arch Biochem Biophys 1991, 288:500-508.
37. Guo X., Knudsen B.S., Peehl D.M., Ruiz A., Bok D., Rando R.R., et al. Retinol metabolism and lecithin:retinol acyltransferase levels are reduced in cultured human prostate cancer cells and tissue specimens. Cancer Res 2002, 62:1654-1661.
38. Batten M.L., Imanishi Y., Maeda T., Tu D.C., Moise A.R., Bronson D., et al. Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J Biol Chem 2004, 279:10422-10432.
39. O'Byrne S.M., Wongsiriroj N., Libien J., Vogel S., Goldberg I.J., Baehr W., et al. Retinoid absorption and storage is impaired in mice lacking lecithin:retinol acyltransferase (LRAT). J Biol Chem 2005, 280:35647-35657.
40. Kim Y.K., Wassef L., Hamberger L., Piantedosi R., Palczewski K., Blaner W.S., et al. Retinyl ester formation by lecithin:retinol acyltransferase is a key regulator of retinoid homeostasis in mouse embryogenesis. J Biol Chem 2008, 283:5611-5621.
41. Liu L., Tang X.H., Gudas L.J. Homeostasis of retinol in lecithin: retinol acyltransferase gene knockout mice fed a high retinol diet. Biochem Pharmacol 2008, 75:2316-2324.
42. Tang X.H., Knudsen B., Bemis D., Tickoo S., Gudas L.J. Oral cavity and esophageal carcinogenesis modeled in carcinogen-treated mice. Clin Cancer Res 2004, 10:301-313.
43. Makita H., Tanaka T., Fujitsuka H., Tatematsu N., Satoh K., Hara A., et al. Chemoprevention of 4-nitroquinoline 1-oxide-induced rat oral carcinogenesis by the dietary flavonoids chalcone, 2-hydroxychalcone, and quercetin. Cancer Res 1996, 56:4904-4909.
44. Tanaka T., Makita H., Ohnishi M., Mori H., Satoh K., Hara A., et al. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis in rats by flavonoids diosmin and hesperidin, each alone and in combination. Cancer Res 1997, 57:246-252.
45. Gillespie R.F., Gudas L.J. Retinoid regulated association of transcriptional co-regulators and the polycomb group protein SUZ12 with the retinoic acid response elements of Hoxa1, RARbeta(2), and Cyp26A1 in F9 embryonal carcinoma cells. J Mol Biol 2007, 372:298-316.
46. Mortensen R.M., Conner D.A., Chao S., Geisterfer-Lowrance A.A., Seidman J.G. Production of homozygous mutant ES cells with a single targeting construct. Mol Cell Biol 1992, 12:2391-2395.
47. Doetschman T.C., Eistetter H., Katz M., Schmidt W., Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 1985, 87:27-45.
48. Kurosawa H. Methods for inducing embryoid body formation: in vitro differentiation system of embryonic stem cells. J Biosci Bioeng 2007, 103:389-398.
49. Mohn D., Chen S.W., Dias D.C., Weinstein D.C., Dyer M.A., Sahr K., et al. Mouse Mix gene is activated early during differentiation of ES and F9 stem cells and induces endoderm in frog embryos. Dev Dyn 2003, 226:446-459.
50. Desbaillets I., Ziegler U., Groscurth P., Gassmann M. Embryoid bodies: an in vitro model of mouse embryogenesis. Exp Physiol 2000, 85:645-651.
51. Rathjen J., Rathjen P.D. Mouse ES cells: experimental exploitation of pluripotent differentiation potential. Curr Opin Genet Dev 2001, 11:587-594.
52. Chan G., Boyle J.O., Yang E.K., Zhang F., Sacks P.G., Shah J.P., et al. Cyclooxygenase-2 expression is up-regulated in squamous cell carcinoma of the head and neck. Cancer Res 1999, 59:991-994.
53. Shiotani H., Denda A., Yamamoto K., Kitayama W., Endoh T., Sasaki Y., et al. Increased expression of cyclooxygenase-2 protein in 4-nitroquinoline-1-oxide-induced rat tongue carcinomas and chemopreventive efficacy of a specific inhibitor, nimesulide. Cancer Res 2001, 61:1451-1456.
54. Gimenez-Conti I.B., Collet A.M., Lanfranchi H., Itoiz M.E., Luna M., Xu H.J., et al. p53, Rb, and cyclin D1 expression in human oral verrucous carcinomas. Cancer 1996, 78:17-23.
55. Kotelnikov V.M., Coon J.S., Mundle S., Kelanic S., LaFollette S., Taylor S.I., et al. Cyclin D1 expression in squamous cell carcinomas of the head and neck and in oral mucosa in relation to proliferation and apoptosis. Clin Cancer Res 1997, 3:95-101.
56. Schoelch M.L., Regezi J.A., Dekker N.P., Ng I.O., McMillan A., Ziober B.L., et al. Cell cycle proteins and the development of oral squamous cell carcinoma. Oral Oncol 1999, 35:333-342.
57. Todd R., Hinds P.W., Munger K., Rustgi A.K., Opitz O.G., Suliman Y., et al. Cell cycle dysregulation in oral cancer. Crit Rev Oral Biol Med 2002, 13:51-61.
58. Fong D., Spizzo G., Gostner J.M., Gastl G., Moser P., Krammel C., et al. TROP2: a novel prognostic marker in squamous cell carcinoma of the oral cavity. Mod Pathol 2008, 21:186-191.
59. Jones S.E., Jomary C. Secreted frizzled-related proteins: searching for relationships and patterns. Bioessays 2002, 24:811-820.
60. Rattner A., Hsieh J.C., Smallwood P.M., Gilbert D.J., Copeland N.G., Jenkins N.A., et al. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc Natl Acad Sci USA 1997, 94:2859-2863.
61. Sogabe Y., Suzuki H., Toyota M., Ogi K., Imai T., Nojima M., et al. Epigenetic inactivation of SFRP genes in oral squamous cell carcinoma. Int J Oncol 2008, 32:1253-1261.
62. Marsit C.J., McClean M.D., Furniss C.S., Kelsey K.T. Epigenetic inactivation of the SFRP genes is associated with drinking, smoking and HPV in head and neck squamous cell carcinoma. Int J Cancer 2006, 119:1761-1766.
63. Gratzner H.G. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 1982, 218:474-475.
64. Lippman S.M., Batsakis J.G., Toth B.B., Weber R.S., Lee J.J., Martin J.W., et al. Comparison of low-dose isotretinoin with beta carotene to prevent oral carcinogenesis. N Engl J Med 1993, 328:15-20.
65. Lotan R. Retinoids and chemoprevention of aerodigestive tract cancers. Cancer Metastasis Rev 1997, 16:349-356.
66. Rhee C.S., Sen M., Lu D., Wu C., Leoni L., Rubin J., et al. Wnt and frizzled receptors as potential targets for immunotherapy in head and neck squamous cell carcinomas. Oncogene 2002, 21:6598-6605.
67. Uraguchi M., Morikawa M., Shirakawa M., Sanada K., Imai K. Activation of WNT family expression and signaling in squamous cell carcinomas of the oral cavity. J Dent Res 2004, 83:327-332.
68. Su D., Gudas L.J. Retinoic acid receptor gamma activates receptor tyrosine kinase Tie1 gene transcription through transcription factor GATA4 in F9 stem cells. Exp Hematol 2008, 36:624-641.
69. Su D., Gudas L.J. Gene expression profiling elucidates a specific role for RARgamma in the retinoic acid-induced differentiation of F9 teratocarcinoma stem cells. Biochem Pharmacol 2008, 75:1129-1160.