Aromatase activity induction in human adipose fibroblasts by retinoic acids via retinoic acid receptor α

Journal of Molecular Endocrinology

Volumn 51, Issue 2, 2013, Pages 247-260

  Wilde, Jan ^a   Erdmann, Maria ^a   Mertens, Michael ^a   Eiselt, Gabriele ^a   Schmidt, Martin ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

9 cis retinoic acid; Adipose tissue; All trans retinoic acid; Emsa; Estrogen synthesis; Promoter; Retinoic acid receptor ; Site directed mutagenesis

Indexed keywords

ALITRETINOIN; AROMATASE; MESSENGER RNA; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA;

ADIPOSE TISSUE; ARTICLE; CELL FRACTIONATION; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CYTOSOLIC FRACTION; DNA RESPONSIVE ELEMENT; ENZYME ACTIVATION; ENZYME ACTIVITY; ESTROGEN SYNTHESIS; FIBROBLAST; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; MUTATION; PRIORITY JOURNAL; PROADIPOCYTE; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE; SITE DIRECTED MUTAGENESIS; SUBCUTANEOUS FAT;

9-CIS-RETINOIC ACID; ADIPOSE TISSUE; ALL-TRANS-RETINOIC ACID; EMSA; ESTROGEN SYNTHESIS; PROMOTER; RETINOIC ACID RECEPTOR Α; SITE-DIRECTED MUTAGENESIS;

ADIPOSE TISSUE; AROMATASE; BASE SEQUENCE; BINDING SITES; ENZYME ACTIVATION; FEMALE; FIBROBLASTS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES, REPORTER; HUMANS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, RETINOIC ACID; TRANSCRIPTIONAL ACTIVATION; TRETINOIN;

EID: 84884246071     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-12-0129     Document Type: Article

References (45)

1. Ackerman GE, Smith ME, Mendelson CR, MacDonald PC & Simpson ER 1981 Aromatization of androstenedione by human adipose tissue stromal cells in monolayer culture. Journal of Clinical Endocrinology and Metabolism 53 412-417.(doi:10.1210/jcem-53-2-412)
2. Agarwal VR, Bulun SE, Leitch M, Rohrich R & Simpson ER 1996 Use of alternative promoters to express the aromatase cytochrome P450 (CYP19) gene in breast adipose tissues of cancer-free and breast cancer patients. Journal of Clinical Endocrinology and Metabolism 81 3843-3849.(doi:10.1210/jc.81.11.3843)
3. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W & Lipman DJ 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25 3389-3402.(doi:10.1093/nar/25.17.3389)
4. Antras J, Lasnier F & Pairault J 1991 Adipsin gene expression in 3T3-F442A adipocytes is posttranscriptionally down-regulated by retinoic acid. Journal of Biological Chemistry 266 1157-1161.
5. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 248-254.(doi:10.1016/0003-2697(76)90527-3)
6. Bulun SE & Simpson ER 1994 Regulation of aromatase expression in human tissues. Breast Cancer Research and Treatment 30 19-29.(doi:10.1007/ BF00682738)
7. Bulun SE, Price TM, Aitken J, Mahendroo MS & Simpson ER 1993 A link between breast cancer and local estrogen biosynthesis suggested by quantification of breast adipose tissue aromatase cytochrome P450 transcripts using competitive polymerase chain reaction after reverse transcription. Journal of Clinical Endocrinology and Metabolism 77 1622-1628.(doi:10.1210/jc.77.6.1622)
8. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M & Werner T 2005 MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21 2933-2942.(doi:10.1093/bioinformatics/bti473)
9. Chen D, Reierstad S, Lu M, Lin Z, Ishikawa H & Bulun SE 2009 Regulation of breast cancer-associated aromatase promoters. Cancer Letters 273 15-27.(doi:10.1016/j.canlet.2008.05.038)
10. Clyne CD, Speed CJ, Zhou J & Simpson ER 2002 Liver receptor homologue-1 (LRH-1) regulates expression of aromatase in preadipocytes. Journal of Biological Chemistry 277 20591-20597.(doi:10.1074/jbc.M201117200)
11. Green H & Meuth M 1974 An established pre-adipose cell line and its differentiation in culture. Cell 3 127-133.(doi:10.1016/0092-8674(74)90116-0)
12. Kamei Y, Kawada T, Kazuki R & Sugimoto E 1993 Retinoic acid receptor g2 gene expression is up-regulated by retinoic acid in 3T3-L1 preadipocytes. Biochemical Journal 293 807-812.
13. Kawada T, Kamei Y, Fujita A, Hida Y, Takahashi N, Sugimoto E & Fushiki T 2000 Carotenoids and retinoids as suppressors on adipocyte differentiation via nuclear receptors. Biofactors 13 103-109.(doi:10.1002/biof.5520130117)
14. Kiefer FW, Vernochet C, O'Brien P, Spoerl S, Brown JD, Nallamshetty S, Zeyda M, Stulnig TM, Cohen DE, Kahn CR et al. 2012 Retinaldehyde dehydrogenase 1 regulates a thermogenic program in white adipose tissue. Nature Medicine 18 918-925.(doi:10.1038/nm.2757)
15. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680-685.(doi:10.1038/ 227680a0)
16. Liu X, Nugoli M, Laferriere J, Saleh SM, Rodrigue-Gervais IG, Saleh M, Park M, Hallett MT, Muller WJ & Giguere V 2011 Stromal retinoic acid receptor b promotes mammary gland tumorigenesis. PNAS 108 774-779.(doi:10.1073/pnas.1011845108)
17. Meng L, Zhou J, Sasano H, Suzuki T, Zeitoun KM & Bulun SE 2001 Tumor necrosis factor a and interleukin 11 secreted by malignant breast epithelial cells inhibit adipocyte differentiation by selectively down-regulating CCAAT/enhancer binding protein a and peroxisome proliferator-activated receptor g: mechanism of desmoplastic reaction. Cancer Research 61 2250-2255.
18. Mu YM, Yanase T, Nishi Y, Hirase N, Goto K, Takayanagi R & Nawata H 2000 A nuclear receptor system constituted by RAR and RXR induces aromatase activity in MCF-7 human breast cancer cells. Molecular and Cellular Endocrinology 166 137-145.(doi:10.1016/S0303-7207 (00)00273-2)
19. O'Neill JS, Elton RA & Miller WR 1988 Aromatase activity in adipose tissue from breast quadrants: a link with tumour site. BMJ 296 741-743.(doi:10.1136/bmj.296.6624.741)
20. Pfaffl MW 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29 e45.(doi:10.1093/nar/ 29.9.e45)
21. Rubin GL, Zhao Y, Kalus AM & Simpson ER 2000 Peroxisome proliferator-activated receptor g ligands inhibit estrogen biosynthesis in human breast adipose tissue: possible implications for breast cancer therapy. Cancer Research 60 1604-1608.
22. Rubin GL, Duong JH, Clyne CD, Speed CJ, Murata Y, Gong C & Simpson ER 2002 Ligands for the peroxisomal proliferator-activated receptor g and the retinoid X receptor inhibit aromatase cytochrome P450 (CYP19) expression mediated by promoter II in human breast adipose. Endocrinology 143 2863-2871.(doi:10.1210/en.143.8.2863)
23. Safi R, Kovacic A, Gaillard S, Murata Y, Simpson ER, McDonnell DP & Clyne CD 2005 Coactivation of liver receptor homologue-1 by peroxisome proliferator-activated receptor g coactivator-1a on aromatase promoter II and its inhibition by activated retinoid X receptor suggest a novel target for breast-specific antiestrogen therapy. Cancer Research 65 11762-11770.(doi:10.1158/0008-5472.CAN-05-2792)
24. Sambrook J & Russell DW 2001 In Molecular Cloning: A Laboratory Manual, Edn3. Cold Spring Harbor, NY,USA: Cold Spring Harbor Laboratory Press.
25. Schmidt M & Loffler G 1994 Induction of aromatase in stromal vascular cells from human breast adipose tissue depends on cortisol and growth factors. FEBS Letters 341 177-181.(doi:10.1016/0014-5793(94)80452-4)
26. Schmidt M & Loffler G 1998 Induction of aromatase activity in human adipose tissue stromal cells by extracellular nucleotides - evidence for P2-purinoceptors in adipose tissue. European Journal of Biochemistry 252 147-154.(doi:10.1046/j.1432-1327.1998.2520147.x)
27. Schmidt M, Renner C & Loffler G 1998 Progesterone inhibits glucocorti-coid-dependent aromatase induction in human adipose fibroblasts. Journal of Endocrinology 158 401-407.(doi:10.1677/joe.0.1580401)
28. Simpson ER 2003 Sources of estrogen and their importance. Journal of Steroid Biochemistry and Molecular Biology 86 225-230.(doi:10.1016/ S0960-0760(03)00360-1)
29. Simpson ER 2004 Aromatase: biologic relevance of tissue-specific expression. Seminars in Reproductive Medicine 22 11-23.(doi:10.1055/ s-2004-823023)
30. Simpson ER, Ackerman GE, Smith ME & Mendelson CR 1981 Estrogen formation in stromal cells of adipose tissue of women: induction by glucocorticosteroids. PNAS 78 5690-5694.(doi:10.1073/pnas.78.9.5690)
31. Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, Amarneh B, Ito Y, Fisher CR, Michael MD et al. 1994 Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocrine Reviews 15 342-355.(doi:10.1210/edrv-15-3-342)
32. Stone RL & Bernlohr DA 1990 The molecular basis for inhibition of adipose conversion of murine 3T3-L1 cells by retinoic acid. Differentiation 45 119-127.(doi:10.1111/j.1432-0436.1990.tb00465.x)
33. Strom K, Gundersen TE, Hansson O, Lucas S, Fernandez C, Blomhoff R & Holm C 2009 Hormone-sensitive lipase (HSL) is also a retinyl ester hydrolase: evidence from mice lacking HSL. FASEB Journal 23 2307-2316.(doi:10.1096/fj.08-120923)
34. Sun T, Zhao Y, Mangelsdorf DJ & Simpson ER 1998 Characterization of a region upstream of exon I.1 of the human CYP19 (aromatase) gene that mediates regulation by retinoids in human choriocarcinoma cells. Endocrinology 139 1684-1691.(doi:10.1210/en.139.4.1684)
35. Taylor JD, Ackroyd AJ & Halford SE 1994 The gel shift assay for the analysis of DNA-protein interactions. In DNA-Protein Interactions: Principles and Protocols, pp 263-279. Ed GG Kneale. Totowa, NJ: Humana Press.
36. Uysal KT, Wiesbrock SM, Marino MW & Hotamisligil GS 1997 Protection from obesity-induced insulin resistance in mice lacking TNF-a function. Nature 389 610-614.(doi:10.1038/39335)
37. Weiske J & Huber O 2006 The histidine triad protein Hint1 triggers apoptosis independent of its enzymatic activity. Journal of Biological Chemistry 281 27356-27366.(doi:10.1074/jbc.M513452200)
38. Zaroukian S, Pineault R, Gandini S, Lacroix A & Ghadirian P 2005 Correlation between nutritional biomarkers and breast cancer: a case- control study. Breast 14 209-223.(doi:10.1016/j.breast.2005.01.001)
39. Zhang S, Tang G, Russell RM, Mayzel KA, Stampfer MJ, Willett WC & Hunter DJ 1997 Measurement of retinoids and carotenoids in breast adipose tissue and a comparison of concentrations in breast cancer cases and control subjects. American Journal of Clinical Nutrition 66 626-632.
40. Zhao Y, Mendelson CR & Simpson ER 1995a Characterization of the sequences of the human CYP19 (aromatase) gene that mediate regulation by glucocorticoids in adipose stromal cells and fetal hepatocytes. Molecular Endocrinology 9 340-349.(doi:10.1210/me.9.3.340)
41. Zhao Y, Nichols JE, Bulun SE, Mendelson CR & Simpson ER 1995b Aromatase P450 gene expression in human adipose tissue. Role of a Jak/STAT pathway in regulation of the adipose-specific promoter. Journal of Biological Chemistry 270 16449-16457.(doi:10.1074/jbc.270. 27.16449)
42. Zhao Y, Agarwal VR, Mendelson CR & Simpson ER 1996a Estrogen biosynthesis proximal to a breast tumor is stimulated by PGE2 via cyclic AMP, leading to activation of promoter II of the CYP19 (aromatase) gene. Endocrinology 137 5739-5742.(doi:10.1210/en.137.12.5739)
43. Zhao Y, Nichols JE, Valdez R, Mendelson CR & Simpson ER 1996b Tumor necrosis factor-a stimulates aromatase gene expression in human adipose stromal cells through use of an activating protein-1 binding site upstream of promoter 1.4. Molecular Endocrinology 10 1350-1357.(doi:10.1210/me.10.11.1350)
44. Zhou J, Gurates B, Yang S, Sebastian S & Bulun SE 2001 Malignant breast epithelial cells stimulate aromatase expression via promoter II in human adipose fibroblasts: an epithelial-stromal interaction in breast tumors mediated by CCAAT/enhancer binding protein b. Cancer Research 61 2328-2334.
45. Zhu ZR, Parviainen M, Mannisto S, Pietinen P, Eskelinen M, Syrjanen K & Uusitupa M 1995 Vitamin A concentration in breast adipose tissue of breast cancer patients. Anticancer Research 15 1593-1596.