LIF removal increases CRABPI and CRABPII transcripts in embryonic stem cells cultured in retinol or 4-oxoretinol

Molecular and Cellular Endocrinology

Volumn 280, Issue 1-2, 2008, Pages 63-74

  Lane, Michelle A ^a   Xu, Juliana ^c,d   Wilen, Elana W ^c   Sylvester, Renia ^c   Derguini, Fadila ^b   Gudas, Lorraine J ^c,d  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b INSTITUT DE RECHERCHE PIERRE FABRE   (France)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

Cell differentiation; Cytochrome P450; Embryonic stem cells; LIF; Retinoic acid binding proteins; Retinol metabolism

Indexed keywords

4 OXORETINOIC ACID; CELLULAR RETINOIC ACID BINDING PROTEIN 1; CELLULAR RETINOIC ACID BINDING PROTEIN 2; CYTOCHROME A1; LEUKEMIA INHIBITORY FACTOR; MESSENGER RNA; RETINOIC ACID BINDING PROTEIN; RETINOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS REGULATION; TRANSCRIPTION INITIATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CYTOCHROME P-450 ENZYME SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYONIC STEM CELLS; ENZYME INDUCTION; LEUKEMIA INHIBITORY FACTOR; MICE; PROTEIN BINDING; RECEPTORS, RETINOIC ACID; RNA, MESSENGER; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; TRETINOIN; UP-REGULATION; VITAMIN A;

EID: 36649016663     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2007.09.010     Document Type: Article

References (49)

1. Achkar C.C., Derguini F., Blumberg B., Langston A., Levin A.A., Speck J., Evans R.M., Bolado Jr. 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. U.S.A. 93 (1996) 4879-4884
2. Astrom A., Pettersson U., and Voorhees J.J. Structure of the human cellular retinoic acid-binding protein II gene. Early transcriptional regulation by retinoic acid. J. Biol. Chem. 267 (1992) 25251-25255
3. Astrom A., Pettersson U., Chambon P., and Voorhees J.J. Retinoic acid induction of human cellular retinoic acid-binding protein-II gene transcription is mediated by retinoic acid receptor-retinoid X receptor heterodimers bound to one far upstream retinoic acid-responsive element with 5-base pair spacing. J. Biol. Chem. 269 (1994) 22334-22339
4. Bhatt H., Brunet L.J., and Stewart C.L. Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 11408-11412
5. Blumberg B., Bolado Jr. J., Derguini F., Craig A.G., Moreno T.A., Chakravarti D., Heyman R.A., Buck J., and Evans R.M. Novel retinoic acid receptor ligands in Xenopus embryos. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 4873-4878
6. 3H]-3-diazo-4-keto-all-trans-retinal. J. Am. Chem. Soc. 112 (1990) 7779-7782
7. Boylan J.F., and Gudas L.J. Overexpression of the cellular retinoic acid binding protein-I (CRABP-I) results in a reduction in differentiation-specific gene expression in F9 teratocarcinoma cells. J. Cell Biol. 112 (1991) 965-979
8. Boylan J.F., and Gudas L.J. The level of CRABP-I expression influences the amounts and types of all-trans-retinoic acid metabolites in F9 teratocarcinoma stem cells. J. Biol. Chem. 267 (1992) 21486-21491
9. Bucco R.A., Melner M.H., Gordon D.S., Leers-Sucheta S., and Ong D.E. Inducible expression of cellular retinoic acid-binding protein II in rat ovary: gonadotropin regulation during luteal development. Endocrinology 136 (1995) 2730-2740
10. Bucco R.A., Zheng W.L., Wardlaw S.A., Davis J.T., Sierra-Rivera E., Osteen K.G., Melner M.H., Kakkad B.P., and Ong D.E. Regulation and localization of cellular retinol-binding protein, retinol-binding protein, cellular retinoic acid-binding protein (CRABP), and CRABP II in the uterus of the pseudopregnant rat. Endocrinology 137 (1996) 3111-3122
11. 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. 271 (1996) 14971-14980
12. 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
13. Cornic M., Delva L., Castaigne S., Lefebvre P., Balitrand N., Degos L., and Chomienne C. In vitro all-trans-retinoic acid (ATRA) sensitivity and cellular retinoic acid binding protein (CRABP) levels in relapse leukemic cells after remission induction by ATRA in acute promyelocytic leukemia. Leukemia 8 Suppl. 2 (1994) S16-S19
14. Delva L., Bastie J.N., Rochette-Egly C., Kraiba R., Balitrand N., Despouy G., Chambon P., and Chomienne C. Physical and functional interactions between cellular retinoic acid binding protein II and the retinoic acid-dependent nuclear complex. Mol. Cell. Biol. 19 (1999) 7158-7167
15. Dong D., Ruuska S.E., Levinthal D.J., and Noy N. Distinct roles for cellular retinoic acid-binding proteins I and II in regulating signaling by retinoic acid. J. Biol. Chem. 274 (1999) 23695-23698
16. Durand B., Saunders M., Leroy P., Leid M., and Chambon P. All-trans and 9-cis-retinoic acid induction of CRABPII transcription is mediated by RAR-RXR heterodimers bound to DR1 and DR2 repeated motifs. Cell 71 (1992) 73-85
17. Faria T.N., Rivi R., Derguini F., Pandolfi P.P., and Gudas L.J. 4-Oxoretinol, a metabolite of retinol in the human promyelocytic leukemia cell line NB4, induces cell growth arrest and granulocytic differentiation. Cancer Res. 58 (1998) 2007-2013
18. Fiorella P.D., Giguere V., and Napoli J.L. Expression of cellular retinoic acid-binding protein (type II) in Escherichia coli. Characterization and comparison to cellular retinoic acid-binding protein (type I). J. Biol. Chem. 268 (1993) 21545-21552
19. Fogh K., Voorhees J.J., and Astrom A. Expression, purification, and binding properties of human cellular retinoic acid-binding protein type I and type II. Arch. Biochem. Biophys. 300 (1993) 751-755
20. Giguere V. Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocr. Rev. 15 (1994) 61-79
21. Grippo J.F., and Gudas L.J. The effect of dibutyryl cyclic AMP and butyrate on F9 teratocarcinoma cellular retinoic acid-binding protein activity. J. Biol. Chem. 262 (1987) 4492-4500
22. Guo X., and Gudas L.J. 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 Res. 58 (1998) 166-176
23. Lane M.A., Chen A.C., Roman S.D., Derguini F., and Gudas L.J. Removal of LIF (leukemia inhibitory factor) results in increased vitamin A (retinol) metabolism to 4-oxoretinol in embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13524-13529
24. Langston A.W., and Gudas L.J. Identification of a retinoic acid responsive enhancer 3′ of the murine homeobox gene Hox-1.6. Mech. Dev. 38 (1992) 217-227
25. Li X.H., and Ong D.E. Cellular retinoic acid-binding protein II gene expression is directly induced by estrogen, but not retinoic acid, in rat uterus. J. Biol. Chem. 278 (2003) 35819-35825
26. Li R., Faria T.N., Boehm M., Nabel E.G., and Gudas L.J. Retinoic acid causes cell growth arrest and an increase in p27 in F9 wild type but not in F9 retinoic acid receptor beta2 knockout cells. Exp. Cell Res. 294 (2004) 290-300
27. MacGregor T.M., Copeland N.G., Jenkins N.A., and Giguere V. The murine gene for cellular retinoic acid-binding protein type II. Genomic organization, chromosomal localization, and post-transcriptional regulation by retinoic acid. J. Biol. Chem. 267 (1992) 7777-7783
28. Martinez-Ceballos E., Chambon P., and Gudas L.J. Differences in gene expression between wild type and Hoxa1 knockout embryonic stem cells after retinoic acid treatment or leukemia inhibitory factor (LIF) removal. J. Biol. Chem. 280 (2005) 16484-16498
29. Martin-Ibanez R., Urban N., Sergent-Tanguy S., Pineda J.R., Garrido-Clua N., Alberch J., and Canals J.M. Interplay of leukemia inhibitory factor and retinoic acid on neural differentiation of mouse embryonic stem cells. J. Neurosci. Res. 85 (2007) 2686-2701
30. McClean S.W., Ruddel M.E., Gross E.G., DeGiovanna J.J., and Peck G.L. Liquid-chromatographic assay for retinol (vitamin A) and retinol analogs in therapeutic trials. Clin. Chem. 28 (1982) 693-696
31. Means A.L., and Gudas L.J. The roles of retinoids in vertebrate development. Annu. Rev. Biochem. 64 (1995) 201-233
32. Means A.L., and Gudas L.J. The CRABP I gene contains two separable, redundant regulatory regions active in neural tissues in transgenic mouse embryos. Dev. Dyn. 209 (1997) 59-69
33. Means A.L., Thompson J.R., and Gudas L.J. Transcriptional regulation of the cellular retinoic acid binding protein I gene in F9 teratocarcinoma cells. Cell Growth Differ. 11 (2000) 71-82
34. Murray P., and Edgar D. The regulation of embryonic stem cell differentiation by leukaemia inhibitory factor (LIF). Differentiation 68 (2001) 227-234
35. Napoli J.L., Posch K.P., Fiorella P.D., and Boerman M.H. Physiological occurrence, biosynthesis and metabolism of retinoic acid: evidence for roles of cellular retinol-binding protein (CRBP) and cellular retinoic acid-binding protein (CRABP) in the pathway of retinoic acid homeostasis. Biomed. Pharmacother. 45 (1991) 131-143
36. Nichols J., Davidson D., Taga T., Yoshida K., Chambers I., and Smith A. Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mech. Dev. 57 (1996) 123-131
37. Noy N. Retinoid-binding proteins: mediators of retinoid action. Biochem. J. 348 Pt 3 (2000) 481-495
38. Ong D.E., Newcomer M.E., and Chytil F. Cellular retinoid-binding proteins. In: Sporn M.B., et al. (Ed). The Retinoids: Biology, Chemistry, and Medicine (1994), Raven Press, New York 283-318
39. Park S.W., Li G., Lin Y.P., Barrero M.J., Ge K., Roeder R.G., and Wei L.N. Thyroid hormone-induced juxtaposition of regulatory elements/factors and chromatin remodeling of CRABP1 dependent on MED1/TRAP220. Mol. Cell 19 (2005) 643-653
40. Penniston K.L., and Tanumihardjo S.A. Elevated serum concentrations of beta-glucuronide metabolites and 4-oxoretinol in lactating sows after treatment with vitamin A: a model for evaluating supplementation in lactating women. Am. J. Clin. Nutr. 81 (2005) 851-858
41. Rathjen P.D., Nichols J., Toth S., Edwards D.R., Heath J.K., and Smith A.G. Developmentally programmed induction of differentiation inhibiting activity and the control of stem cell populations. Genes Dev. 4 (1990) 2308-2318
42. Ruff S.J., and Ong D.E. Cellular retinoic acid binding protein is associated with mitochondria. FEBS Lett. 487 (2000) 282-286
43. Sauter C.N., McDermid R.L., Weinberg A.L., Greco T.L., Xu X., Murdoch F.E., and Fritsch M.K. Differentiation of murine embryonic stem cells induces progesterone receptor gene expression. Exp. Cell Res. 311 (2005) 251-264
44. Sessler R.J., and Noy N. A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II. Mol. Cell 18 (2005) 343-353
45. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Kontgen F., and Abbondanzo S.J. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359 (1992) 76-79
46. Tighe A.P., and Gudas L.J. Retinoic acid inhibits leukemia inhibitory factor signaling pathways in mouse embryonic stem cells. J. Cell. Physiol. 198 (2004) 223-229
47. 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. 86 (1989) 9099-9103
48. White J.A., Beckett-Jones B., Guo Y.D., Dilworth F.J., Bonasoro J., Jones G., and Petkovich M. cDNA cloning of human retinoic acid-metabolizing enzyme (hP450RAI) identifies a novel family of cytochromes P450. J. Biol. Chem. 272 (1997) 18538-18541
49. Zheng W.L., Bucco R.A., Schmitt M.C., Wardlaw S.A., and Ong D.E. Localization of cellular retinoic acid-binding protein (CRABP) II and CRABP in developing rat testis. Endocrinology 137 (1996) 5028-5035