Retinoic acid receptors and GATA transcription factors activate the transcription of the human lecithin:retinol acyltransferase gene

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 3, 2009, Pages 546-553

  Cai, Kun ^a   Gudas, Lorraine J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Cancer; GATA; LRAT; Promoter analysis; Prostate; Retinoic acid; Retinoic acid receptor; Retinol; STRA6; Transcription; Tumor cell

Indexed keywords

LECITHIN RETINOL ACYLTRANSFERASE; MESSENGER RNA; RETINOIC ACID RECEPTOR BETA; RETINOIC ACID RECEPTOR BETA 2; RETINOIC ACID RECEPTOR GAMMA; RETINOL; TRANSCRIPTION FACTOR GATA; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL CULTURE; CELL LINE; GENE; GENE ACTIVATION; GENE CONTROL; GENE DELETION; GENE SEQUENCE; HUMAN; HUMAN CELL; LECITHIN RETINOL ACYLTRANSFERASE GENE; PROMOTER REGION; PROSTATE CANCER; PROSTATE EPITHELIUM; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ACYLTRANSFERASES; CELL LINE, TUMOR; EPITHELIAL CELLS; GATA4 TRANSCRIPTION FACTOR; HUMANS; MALE; MEMBRANE PROTEINS; PROMOTER REGIONS, GENETIC; PROSTATE; PROSTATIC NEOPLASMS; PROTEIN BINDING; RECEPTORS, RETINOIC ACID; RESPONSE ELEMENTS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; VITAMIN A;

EID: 58149284254     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2008.06.007     Document Type: Article

References (80)

1. Arapshian A., Kuppumbatti Y.S., and Mira-y-Lopez R. Methylation of conserved CpG sites neighboring the beta retinoic acid response element may mediate retinoic acid receptor beta gene silencing in MCF-7 breast cancer cells. Oncogene 19 (2000) 4066-4070
2. Arceci R.J., King A.A., Simon M.C., Orkin S.H., and Wilson D.B. Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol Cell Biol 13 (1993) 2235-2246
3. Blutt S.E., Allegretto E.A., Pike J.W., and Weigel N.L. 1,25-dihydroxyvitamin D3 and 9-cis-retinoic acid act synergistically to inhibit the growth of LNCaP prostate cells and cause accumulation of cells in G1. Endocrinology 138 (1997) 1491-1497
4. Bohnsack B.L., and Hirschi K.K. Nutrient regulation of cell cycle progression. Ann Rev Nutr 24 (2004) 433-453
5. Boorjian S., Tickoo S.K., Mongan N.P., Yu H., Bok D., Rando R.R., et al. Reduced lecithin: retinol acyltransferase expression correlates with increased pathologic tumor stage in bladder cancer. Clin Cancer Res 10 (2004) 3429-3437
6. Bouillet P., Sapin V., Chazaud C., Messaddeq N., Decimo D., Dolle P., et al. Developmental expression pattern of Stra6, a retinoic acid-responsive gene encoding a new type of membrane protein. Mech Dev 63 (1997) 173-186
7. Campbell M.J., Park S., Uskokovic M.R., Dawson M.I., and Koeffler H.P. Expression of retinoic acid receptor-beta sensitizes prostate cancer cells to growth inhibition mediated by combinations of retinoids and a 19-nor hexafluoride vitamin D3 analog. Endocrinology 139 (1998) 1972-1980
8. Chen A.C., Guo X., Derguini F., and Gudas L.J. Human breast cancer cells and normal mammary epithelial cells: retinol metabolism and growth inhibition by the retinol metabolite 4-oxoretinol. Cancer Res 57 (1997) 4642-4651
9. Chiba H., Clifford J., Metzger D., and Chambon P. Distinct retinoid X receptor-retinoic acid receptor heterodimers are differentially involved in the control of expression of retinoid target genes in F9 embryonal carcinoma cells. Mol Cell Biol 17 (1997) 3013-3020
10. Dahiya R., Boyle B., Park H.D., Kurhanewicz J., Macdonald J.M., and Narayan P. 13-cis-retinoic acid-mediated growth inhibition of DU-145 human prostate cancer cells. Biochem Mol Biol Int 32 (1994) 1-12
11. de Vos S., Dawson M.I., Holden S., Le T., Wang A., Cho S.K., et al. Effects of retinoid X receptor-selective ligands on proliferation of prostate cancer cells. Prostate 32 (1997) 115-121
12. DiPaola R.S., Rafi M.M., Vyas V., Toppmeyer D., Rubin E., Patel J., et al. Phase I clinical and pharmacologic study of 13-cis-retinoic acid, interferon alfa, and paclitaxel in patients with prostate cancer and other advanced malignancies. J Clin Oncol 17 (1999) 2213-2218
13. Gillespie R.F., and Gudas L.J. Retinoic acid receptor isotype specificity in F9 teratocarcinoma stem cells results from the differential recruitment of coregulators to retinoic response elements. J Biol Chem 282 (2007) 33421-33434
14. Goodman D.S. Plasma retinol-binding protein. Ann N Y Acad Sci 348 (1980) 378-390
15. Gudas L.J., Sporn M.B., and Roberts A.B. Cellular biology and biochemistry of the retinoids. In: M.B.a.R Sporn A.B., and Goodman D.S. (Eds). The retinoids: biology, chemistry, and medicine (1994), Raven Press, New York 443-520
16. 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 62 (2002) 1654-1661
17. Guo X., Nanus D.M., Ruiz A., Rando R.R., Bok D., and Gudas L.J. Reduced levels of retinyl esters and vitamin A in human renal cancers. Cancer Res 61 (2001) 2774-2781
18. Guo X., Ruiz A., Rando R.R., Bok D., and 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 21 (2000) 1925-1933
19. Hayashi K., Yokozaki H., Goodison S., Oue N., Suzuki T., Lotan R., et al. Inactivation of retinoic acid receptor beta by promoter CpG hypermethylation in gastric cancer. Differentiation 68 (2001) 13-21
20. Herr F.M., MacDonald P.N., and Ong D.E. Solubilization and partial characterization of lecithin-retinol acyltransferase from rat liver. J Nutr Biochem (1991) 503-511
21. 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 (1991) 3972-3981
22. Huang D., Chen S.W., Langston A.W., and Gudas L.J. A conserved retinoic acid responsive element in the murine Hoxb-1 gene is required for expression in the developing gut. Development 125 (1998) 3235-3246
23. Jones H.E., Eaton C.L., Barrow D., Dutkowski C., and Griffiths K. Response of cell growth and retinoic acid receptor expression to retinoic acid in neoplastic and non-neoplastic prostate cell lines. Prostate 30 (1997) 174-182
24. Kastner P., Grondona J.M., Mark M., Gansmuller A., LeMeur M., Decimo D., et al. Genetic analysis of RXR alpha developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 78 (1994) 987-1003
25. Kawaguchi R., Yu J., Honda J., Hu J., Whitelegge J., Ping P., et al. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 315 (2007) 820-825
26. Kim H., Lapointe J., Kaygusuz G., Ong D.E., Li C., van de Rijn M., et al. The retinoic acid synthesis gene ALDH1a2 is a candidate tumor suppressor in prostate cancer. Cancer Res 65 (2005) 8118-8124
27. Kim Y.K., Wassef L., Hamberger L., Piantedosi R., Palczewski K., Blaner W.S., et al. Retinyl ester formation by lecithin:retinol acyltransferase (LRAT) is a key regulator of retinoid homeostasis in mouse embryogenesis. J Biol Chem 283 (2007) 5611-5621
28. Lane M.A., Xu J., Wilen E.W., Sylvester R., Derguini F., and Gudas L.J. LIF removal increases CRABPI and CRABPII transcripts in embryonic stem cells cultured in retinol or 4-oxoretinol. Mol Cell Endocrinol 280 (2008) 63-74
29. Langston A.W., Thompson J.R., and Gudas L.J. Retinoic acid-responsive enhancers located 3′ of the Hox A and Hox B homeobox gene clusters. Functional analysis. J Biol Chem 272 (1997) 2167-2175
30. Leonard M., Brice M., Engel J.D., and Papayannopoulou T. Dynamics of GATA transcription factor expression during erythroid differentiation. Blood 82 (1993) 1071-1079
31. Liu C., Glasser S.W., Wan H., and Whitsett J.A. GATA-6 and thyroid transcription factor-1 directly interact and regulate surfactant protein-C gene expression. J Biol Chem 277 (2002) 4519-4525
32. Liu L., and Gudas L.J. Disruption of the lecithin:retinol acyltransferase gene makes mice more susceptible to vitamin A deficiency. J Biol Chem 280 (2005) 40226-40234
33. Liu L., Tang X.H., and Gudas L.J. Homeostasis of retinol in lecithin:retinol acyltransferase gene knockout mice fed a high retinol diet. Biochem Pharmacol 75 (2008) 2316-2324
34. Lotan R. Effect of vitamin A and its analogs (retinoids) on normal and neplastic cells. Biochim Biophys Acta 605 (1981) 33-91
35. Lotan Y., Xu X.C., Shalev M., Lotan R., Williams R., Wheeler T.M., et al. Differential expression of nuclear retinoid receptors in normal and malignant prostates. J Clin Oncol 18 (2000) 116-121
36. Loudig O., Babichuk C., White J., Abu-Abed S., Mueller C., and Petkovich M. Cytochrome P450RAI(CYP26) promoter: a distinct composite retinoic acid response element underlies the complex regulation of retinoic acid metabolism. Mol Endocrinol 14 (2000) 1483-1497
37. Loudig O., Maclean G.A., Dore N.L., Luu L., and Petkovich M. Transcriptional co-operativity between distant retinoic acid response elements in regulation of Cyp26A1 inducibility. Biochem J 392 (2005) 241-248
38. Mader S., Leroy P., Chen J.Y., and Chambon P. Multiple parameters control the selectivity of nuclear receptors for their response elements. Selectivity and promiscuity in response element recognition by retinoic acid receptors and retinoid X receptors. J Biol Chem 268 (1993) 591-600
39. Mangelsdorf D.J. Vitamin A receptors. Nutr Rev 52 (1994) S32-44
40. Martin D.I., Zon L.I., Mutter G., and Orkin S.H. Expression of an erythroid transcription factor in megakaryocytic and mast cell lineages. Nature 344 (1990) 444-447
41. Mongan N.P., and Gudas L.J. Valproic acid, in combination with all-trans-retinoic acid and 5-aza-2′-deoxycytidine, restores expression of silenced RARbeta2 in breast cancer cells. Mol Cancer Ther 4 (2005) 477-486
42. Mongan N.P., and Gudas L.J. Diverse actions of retinoid receptors in cancer prevention and treatment. Differentiation 75 (2007) 853-870
43. Mouthon M.A., Bernard O., Mitjavila M.T., Romeo P.H., Vainchenker W., and Mathieu-Mahul D. Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood 81 (1993) 647-655
44. Nakayama T., Watanabe M., Yamanaka M., Hirokawa Y., Suzuki H., Ito H., et al. The role of epigenetic modifications in retinoic acid receptor beta2 gene expression in human prostate cancers. Lab Invest 81 (2001) 1049-1057
45. Nanus D.M., and Gudas L.J. Retinoids and prostate cancer. Prostate J 2 (2000) 68-73
46. Niles R.M. Signaling pathways in retinoid chemoprevention and treatment of cancer. Mutat Res 555 (2004) 81-96
47. 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 280 (2005) 35647-35657
48. Ong D.E., MacDonald P.N., and 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 263 (1988) 5789-5796
49. Peehl D.M., Sellers R.G., Arnstein P., Kung H.F., and Rhim J.S. Altered growth regulation and loss of response to retinoic acid accompany tumorigenic transformation of prostatic cells. Anticancer Res 19 (1999) 3857-3864
50. Peehl D.M., Wong S.T., and Stamey T.A. Vitamin A regulates proliferation and differentiation of human prostatic epithelial cells. Prostate 23 (1993) 69-78
51. Quandt K., Frech K., Karas H., Wingender E., and Werner T. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23 (1995) 4878-4884
52. Randolph R.K., and Ross A.C. Vitamin A status regulates hepatic lecithin:retinol acyltransferase activity in rats. J Biol Chem 266 (1991) 16453-16457
53. Sambrook J., Fritsch E.F., and Maniatis T. Molecular cloning: a laboratory manual (1989), Cold Spring Harber Laboratory Press, New York
54. Sheren-Manoff M., Shin S.J., Su D., Bok D., Rando R.R., and Gudas L.J. Reduced lecithin:retinol acyltransferase expression in human breast cancer. Int J Oncol 29 (2006) 1193-1199
55. Soprano D.R., Qin P., and Soprano K.J. Retinoic acid receptors and cancers. Annu Rev Nutr 24 (2004) 201-221
56. Su D., and 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 75 (2008) 1129-1160
57. Su D., and Gudas L.J. Retinoic acid receptor gamma activates receptor tyrosine kinase Tie1 gene transcription through transcription factor GATA4 in F9 stem cells. Exp Hematol 36 (2008) 624-641
58. Suh Y.A., Lee H.Y., Virmani A., Wong J., Mann K.K., Miller Jr. W.H., et al. Loss of retinoic acid receptor beta gene expression is linked to aberrant histone H3 acetylation in lung cancer cell lines. Cancer Res 62 (2002) 3945-3949
59. Sumi K., Tanaka T., Uchida A., Magoori K., Urashima Y., Ohashi R., et al. Cooperative interaction between hepatocyte nuclear factor 4 alpha and GATA transcription factors regulates ATP-binding cassette sterol transporters ABCG5 and ABCG8. Mol Cell Biol 27 (2007) 4248-4260
60. Sun S.Y., and Lotan R. Retinoids and their receptors in cancer development and chemoprevention. Crit Rev Oncol Hematol 41 (2002) 41-55
61. Swisshelm K., Ryan K., Lee X., Tsou H.C., Peacocke M., and Sager R. Down-regulation of retinoic acid receptor beta in mammary carcinoma cell lines and its up-regulation in senescing normal mammary epithelial cells. Cell Growth Differ 5 (1994) 133-141
62. Szeto W., Jiang W., Tice D.A., Rubinfeld B., Hollingshead P.G., Fong S.E., et al. Overexpression of the retinoic acid-responsive gene Stra6 in human cancers and its synergistic induction by Wnt-1 and retinoic acid. Cancer Res 61 (2001) 4197-4205
63. Taneja R., Bouillet P., Boylan J.F., Gaub M.P., Roy B., Gudas L.J., et al. Reexpression of retinoic acid receptor (RAR) gamma or overexpression of RAR alpha or RAR beta in RAR gamma-null F9 cells reveals a partial functional redundancy between the three RAR types. Proc Natl Acad Sci USA 92 (1995) 7854-7858
64. Thalasila A., Poplin E., Shih J., Dvorzhinski D., Capanna T., Doyle-Lindrud S., et al. A phase I trial of weekly paclitaxel, 13-cis-retinoic acid, and interferon alpha in patients with prostate cancer and other advanced malignancies. Cancer Chemother Pharmacol 52 (2003) 119-124
65. Touma S.E., Goldberg J.S., Moench P., Guo X., Tickoo S.K., Gudas L.J., et al. Retinoic acid and the histone deacetylase inhibitor trichostatin a inhibit the proliferation of human renal cell carcinoma in a xenograft tumor model. Clin Cancer Res 11 (2005) 3558-3566
66. Tsuzuki S., Kitajima K., Nakano T., Glasow A., Zelent A., and Enver T. Cross talk between retinoic acid signaling and transcription factor GATA-2. Mol Cell Biol 24 (2004) 6824-6836
67. Umesono K., Murakami K.K., Thompson C.C., and Evans R.M. Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell 65 (1991) 1255-1266
68. van Wering H.M., Huibregtse I.L., van der Zwan S.M., de Bie M.S., Dowling L.N., Boudreau F., et al. Physical interaction between GATA-5 and hepatocyte nuclear factor-1alpha results in synergistic activation of the human lactase-phlorizin hydrolase promoter. J Biol Chem 277 (2002) 27659-27667
69. Vasios G.W., Gold J.D., Petkovich M., Chambon P., and Gudas L.J. A retinoic acid-responsive element is present in the 5′ flanking region of the laminin B1 gene. Proc Natl Acad Sci USA 86 (1989) 9099-9103
70. Wongsiriroj N., Piantedosi R., Palczewski K., Goldberg I.J., Johnston T.P., Li E., et al. The molecular basis of retinoid absorption: a genetic dissection. J Biol Chem 283 (2008) 13510-13519
71. Wu Q., Li Y., Liu R., Agadir A., Lee M.O., Liu Y., et al. Modulation of retinoic acid sensitivity in lung cancer cells through dynamic balance of orphan receptors nur77 and COUP-TF and their heterodimerization. EMBO J 16 (1997) 1656-1669
72. Wu S., Zhang D., Zhang Z.P., Soprano D.R., and Soprano K.J. Critical role of both retinoid nuclear receptors and retinoid-X-receptors in mediating growth inhibition of ovarian cancer cells by all-trans-retinoic acid. Oncogene 17 (1998) 2839-2849
73. Yost R.W., Harrison E.H., and Ross A.C. Esterification by rat liver microsomes of retinol bound to cellular retinol-binding protein. J Biol Chem 263 (1988) 18693-18701
74. Zhan H.C., Gudas L.J., Bok D., Rando R., Nanus D.M., and Tickoo S.K. Differential expression of the enzyme that esterifies retinol, lecithin:retinol acyltransferase, in subtypes of human renal cancer and normal kidney. Clin Cancer Res 9 (2003) 4897-4905
75. Zheng X., Chang R.L., Cui X.X., Avila G.E., Lee S., Lu Y.P., et al. Inhibitory effect of 12-O-tetradecanoylphorbol-13-acetate alone or in combination with all-trans-retinoic acid on the growth of LNCaP prostate tumors in immunodeficient mice. Cancer Res 64 (2004) 1811-1820
76. Zochbauer-Muller S., Fong K.M., Virmani A.K., Geradts J., Gazdar A.F., and Minna J.D. Aberrant promoter methylation of multiple genes in non-small cell lung cancers. Cancer Res 61 (2001) 249-255
77. Zolfaghari R., and Ross A.C. Lecithin:retinol acyltransferase from mouse and rat liver. CDNA cloning and liver-specific regulation by dietary vitamin a and retinoic acid. J Lipid Res 41 (2000) 2024-2034
78. Zolfaghari R., and 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 132 (2002) 1160-1164
79. Zolfaghari R., and Ross A.C. Cloning, gene organization and identification of an alternative splicing process in lecithin:retinol acyltransferase cDNA from human liver. Gene 341 (2004) 181-188
80. Zon L.I., Mather C., Burgess S., Bolce M.E., Harland R.M., and Orkin S.H. Expression of GATA-binding proteins during embryonic development in Xenopus laevis. Proc Natl Acad Sci USA 88 (1991) 10642-10646