Retinoic acid inhibits endometrial cancer cell growth via multiple genomic mechanisms

Journal of Molecular Endocrinology

Volumn 46, Issue 2, 2011, Pages 139-153

  Cheng, You Hong ^a   Utsunomiya, Hiroki ^a   Pavone, Mary Ellen ^b   Yin, Ping ^b   Bulun, Serdar E ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 [(5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 NAPHTHYL)CARBOXAMIDO]BENZOIC ACID; COMPLEMENTARY RNA; ESTRADIOL; PROGESTERONE; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; RETINOID X RECEPTOR; RNA; SMALL INTERFERING RNA;

ARTICLE; CANCER CELL; CELL GROWTH; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENDOMETRIUM CANCER; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENOMICS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MICROARRAY ANALYSIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZOATES; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; ENDOMETRIAL NEOPLASMS; ENDOMETRIUM; FEMALE; GENE EXPRESSION PROFILING; GENE KNOCKDOWN TECHNIQUES; GENOME; HUMANS; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; RECEPTORS, RETINOIC ACID; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TETRAHYDRONAPHTHALENES; TRETINOIN;

EID: 79953689271     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-10-0064     Document Type: Article

References (59)

1. Bachner D, Ahrens M, Schroder D, Hoffmann A, Lauber J, Betat N, Steinert P, Flohe L & Gross G 1998 Bmp-2 downstream targets in mesenchymal development identified by subtractive cloning from recombinant mesenchymal progenitors (C3H10T1/2). Developmental Dynamics 213 398-411. (doi:10.1002/(SICI)1097-0177(199812)213:4<398::AID-AJA5>3.0.CO;2-T)
2. Backes C, Keller A, Kuentzer J, Kneissl B, Comtesse N, Elnakady YA, Muller R, Meese E & Lenhof HP 2007 GeneTrail-advanced gene set enrichment analysis. Nucleic Acids Research 35 W186-W192. (doi:10.1093/nar/gkm323)
3. Bastien J & Rochette-Egly C 2004 Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 328 1-16. (doi:10.1016/ j.gene.2003.12.005)
4. Bergeron RM, Thompson TB, Leonard LS, Pluta L & Gaido KW 1999 Estrogenicity of bisphenol A in a human endometrial carcinoma cell line. Molecular and Cellular Endocrinology 150 179-187. (doi:10. 1016/S0303-7207(98)00202-0)
5. Brand C, Segard P, Plouvier P, Formstecher P, Danze PM & Lefebvre P 2002 Selective alteration of gene expression in response to natural and synthetic retinoids. BMC Pharmacology 2 13. (doi:10.1186/1471-2210-2-13)
6. Bruckheimer EM & Kyprianou N 2000 Apoptosis in prostate carcinogenesis. A growth regulator and a therapeutic target. Cell and Tissue Research 301 153-162. (doi:10.1007/s004410000196)
7. Bucco RA, Zheng WL, Davis JT, Sierra-Rivera E, Osteen KG, Chaudhary AK & Ong DE 1997 Cellular retinoic acid-binding protein(II) presence in rat uterine epithelial cells correlates with their synthesis of retinoic acid. Biochemistry 36 4009-4014. (doi:10.1021/bi962094o)
8. Bulun SE, Yang S, Fang Z, Gurates B, Tamura M & Sebastian S 2002 Estrogen production and metabolism in endometriosis. Annals of the New York Academy of Sciences 955 75-85. (doi:10.1111/j.1749-6632.2002.tb02767.x)
9. Carter CA 2003 Retinoic acid signaling through PI3-kinase induces differentiation of human endometrial adenocarcinoma cells. Experimental and Molecular Pathology 75 34-44. (doi:10.1016/S0014-4800(03)00033-9)
10. Carter CA & Madden VJ 2000 A newly characterized human endometrial adenocarcinoma cell line (CAC-1) differentiates in response to retinoic acid treatment. Experimental and Molecular Pathology 69 175-191. (doi:10.1006/exmp.2000.2334)
11. Carter CA & Shaw BL 2000 Retinoic acid affects the EGF-R signaling pathway during differentiation induction of human endometrial adenocarcinoma cells. Experimental and Molecular Pathology 68 170-186. (doi:10.1006/exmp.2000.2301)
12. Carter CA, Pogribny M, Davidson A, Jackson CD, McGarrity LJ & Morris SM 1996 Effects of retinoic acid on cell differentiation and reversion toward normal in human endometrial adenocarcinoma (RL95-2) cells. Anticancer Research 16 17-24.
13. Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L, Privalsky ML, Nakatani Y & Evans RM 1997 Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90 569-580. (doi:10.1016/S0092-8674(00)80516-4)
14. Cheng YH, Imir A, Suzuki T, Fenkci V, Yilmaz B, Sasano H & Bulun SE 2006 SP1 and SP3 mediate progesterone-dependent induction of the 17b-hydroxysteroid dehydrogenase type 2 gene in human endometrium. Biology of Reproduction 75 605-614. (doi:10.1095/biolreprod.106.051912)
15. Cheng YH, Yin P, Xue Q, Yilmaz B, Dawson MI & Bulun SE 2008 Retinoic acid (RA) regulates 17β-hydroxysteroid dehydrogenase type 2 expression in endometrium: interaction of RA receptors with specificity protein (SP) 1/SP3 for estradiol metabolism. Journal of Clinical Endocrinology and Metabolism 93 1915-1923. (doi:10.1210/jc.2007-1536)
16. Cristillo AD, Heximer SP, Russell L & Forsdyke DR 1997 Cyclosporin A inhibits early mRNA expression of G0/G1 switch gene 2 (G0S2) in cultured human blood mononuclear cells. DNA and Cell Biology 16 1449-1458. (doi:10.1089/dna.1997.16.1449)
17. Dardes RC, Schafer JM, Pearce ST, Osipo C, Chen B & Jordan VC 2002 Regulation of estrogen target genes and growth by selective estrogen-receptor modulators in endometrial cancer cells. Gynecologic Oncology 85 498-506. (doi:10.1006/gyno.2002.6659)
18. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC & Lempicki RA 2003 DAVID: database for annotation, visualization, and integrated discovery. Genome Biology 4 P3. (doi:10.1186/gb-2003-4-5-p3)
19. Hartwell L, Weinert T, Kadyk L & Garvik B 1994 Cell cycle checkpoints, genomic integrity, and cancer. Cold Spring Harbor Symposia on Quantitative Biology 59 259-263.
20. Hochberg Y & Benjamini Y 1990 More powerful procedures for multiple significance testing. Statistics in Medicine 9 811-818. (doi:10.1002/sim.4780090710)
21. Holinka CF, Hata H, Gravanis A, Kuramoto H & Gurpide E 1986 Effects of estradiol on proliferation of endometrial adenocarci-noma cells (Ishikawa line). Journal of Steroid Biochemistry 25 781-786. (doi:10.1016/0022-4731(86)90308-0)
22. Hosack DA, Dennis G Jr, Sherman BT, Lane HC & Lempicki RA 2003 Identifying biological themes within lists of genes with EASE. Genome Biology 4 R70. (doi:10.1186/gb-2003-4-10-r70)
23. Jacobberger JW, Sizemore N, Gorodeski G & Rorke EA 1995 Transforming growth factor β regulation of epidermal growth factor receptor in ectocervical epithelial cells. Experimental Cell Research 220 390-396. (doi:10.1006/excr.1995.1330)
24. Klipper-Aurbach Y, Wasserman M, Braunspiegel-Weintrob N, Borstein D, Peleg S, Assa S, Karp M, Benjamini Y, Hochberg Y & Laron Z 1995 Mathematical formulae for the prediction of the residual beta cell function during the first two years of disease in children and adolescents with insulin-dependent diabetes mellitus. Medical Hypotheses 45 486-490. (doi:10.1016/0306-9877(95)90228-7)
25. Kudelka AP, Freedman RS, Edwards CL, Lippman SM, Tornos CS, Krakoff IH & Kavanagh JJ 1993 Metastatic adenocarcinoma of the endometrium treated with 13-cis-retinoic acid plus interferon-α. Anticancer Drugs 4 335-337. (doi:10.1097/00001813-199306000-00007)
26. Kumarendran MK, Loughney AD, Prentice A, Thomas EJ & Redfern CP 1996 Nuclear retinoid receptor expression in normal human endometrium throughout the menstrual cycle. Molecular Human Reproduction 2 123-129. (doi:10.1093/molehr/2.2.123)
27. Kurita T, Wang YZ, Donjacour AA, Zhao C, Lydon JP, O'Malley BW, Isaacs JT, Dahiya R & Cunha GR 2001a Paracrine regulation of apoptosis by steroid hormones in the male and female reproductive system. Cell Death and Differentiation 8 192-200. (doi:10.1038/sj.cdd. 4400797)
28. Kurita T, Cooke PS & Cunha GR 2001b Epithelial-stromal tissue interaction in paramesonephric (Mullerian) epithelial differentiation. Developmental Biology 240 194-211. (doi:10.1006/dbio.2001.0458)
29. Lee CH, Chinpaisal C & Wei LN 1998 Cloning and characterization of mouse RIP140, a corepressor for nuclear orphan receptor TR2. Molecular and Cellular Biology 18 6745-6755.
30. Letwin NE, Kafkafi N, Benjamini Y, Mayo C, Frank BC, Luu T, Lee NH & Elmer GI 2006 Combined application of behavior genetics and microarray analysis to identify regional expression themes and gene-behavior associations. Journal of Neuroscience 26 5277-5287. (doi:10.1523/JNEUROSCI.4602-05.2006)
31. Levi F, Franceschi S, Negri E & La Vecchia C 1993 Dietary factors and the risk of endometrial cancer. Cancer 71 3575-3581. (doi:10.1002/ 1097-0142(19930601)71:11<3575::AID-CNCR2820711119>3.0. CO;2-0)
32. Lohnes D, Mark M, Mendelsohn C, Dolle P, Dierich A, Gorry P, Gansmuller A & Chambon P 1994 Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Development 120 2723-2748.
33. Lohnes D, Mark M, Mendelsohn C, Dolle P, Decimo D, LeMeur M, Dierich A, Gorry P & Chambon P 1995 Developmental roles of the retinoic acid receptors. Journal of Steroid Biochemistry and Molecular Biology 53 475-486. (doi:10.1016/0960-0760(95)00094-G)
34. Mendelsohn C, Lohnes D, Decimo D, Lufkin T, LeMeur M, Chambon P & Mark M 1994 Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120 2749-2771.
35. Meunier B, Dumas E, Piec I, Bechet D, Hebraud M & Hocquette JF 2007 Assessment of hierarchical clustering methodologies for proteomic data mining. Journal of Proteome Research 6 358-366. (doi:10.1021/pr060343h)
36. Meyer M, Sonntag-Buck V, Keaveney M & Stunnenberg HG 1996 Retinoid-dependent transcription: the RAR/RXR-TBP-EIA/EIA-LA connection. Biochemical Society Symposium 62 97-109.
37. Morriss-Kay GM & Ward SJ 1999 Retinoids and mammalian development. International Review of Cytology 188 73-131. (doi:10. 1016/S0074-7696(08)61566-1)
38. Negri E, La Vecchia C, Franceschi S, Levi F & Parazzini F 1996 Intake of selected micronutrients and the risk of endometrial carcinoma. Cancer 77 917-923. (doi:10.1002/(SICI)1097-0142(19960301) 77:5<917::AID-CNCR17>3.0.CO;2-6)
39. Njar VC, Gediya L, Purushottamachar P, Chopra P, Vasaitis TS, Khandelwal A, Mehta J, Huynh C, Belosay A & Patel J 2006 Retinoic acid metabolism blocking agents (RAMBAs) for treatment of cancer and dermatological diseases. Bioorganic & Medicinal Chemistry 14 4323-4340. (doi:10.1016/j.bmc.2006.02.041)
40. Obel JC, Friberg G & Fleming GF 2006 Chemotherapy in endometrial cancer. Clinical Advances in Hematology and Oncology 4 459-468.
41. Patel JB, Huynh CK, Handratta VD, Gediya LK, Brodie AM, Goloubeva OG, Clement OO, Nanne IP, Soprano DR, & Njar VC, 2004 Novel retinoic acid metabolism blocking agents endowed with multiple biological activities are efficient growth inhibitors of human breast and prostate cancer cells in vitro and a human breast tumor xenograft in nude mice. Journal of Medicinal Chemistry 47 6716-6729. (doi:10.1021/jm0401457)
42. Pavone ME, Reierstad S, Sun H, Milad M, Bulun SE & Cheng YH 2010 Altered retinoid uptake and action contributes to cell survival in endometriosis. Journal of Clinical Endocrinology and Metabolism 95 E300-E309. (doi:10.1210/jc.2010-0459)
43. Pierro E, Minici F, Alesiani O, Miceli F, Proto C, Screpanti I, Mancuso S & Lanzone A 2001 Stromal-epithelial interactions modulate estrogen responsiveness in normal human endome-trium. Biology of Reproduction 64 831-838. (doi:10.1095/biolre-prod64.3.831)
44. Roberts LM, Hirokawa Y, Nachtigal MW & Ingraham HA 1999 Paracrine-mediated apoptosis in reproductive tract development. Developmental Biology 208 110-122. (doi:10.1006/dbio.1998.9190)
45. Rorke EA & Jacobberger JW 1995 Transforming growth factor-β1 (TGFb1) enhances apoptosis in human papillomavirus type 16-immortalized human ectocervical epithelial cells. Experimental Cell Research 216 65-72. (doi:10.1006/excr.1995.1008)
46. Rorke EA, Zhang D, Choo CK, Eckert RL & Jacobberger JW 2000 TGF-β-mediated cell cycle arrest of HPV16-immortalized human ectocervical cells correlates with decreased E6/E7 mRNA and increased p53 and p21(WAF-1) expression. Experimental Cell Research 259 149-157. (doi:10.1006/excr.2000.4953)
47. Rotello RJ, Lieberman RC, Purchio AF & Gerschenson LE 1991 Coordinated regulation of apoptosis and cell proliferation by transforming growth factor β1 in cultured uterine epithelial cells. PNAS 88 3412-3415. (doi:10.1073/pnas.88.8.3412)
48. Rusiniak ME, Yu M, Ross DT, Tolhurst EC & Slack JL 2000 Identification of B94 (TNFAIP2) as a potential retinoic acid target gene in acute promyelocytic leukemia. Cancer Research 60 1824-1829.
49. Saidi SA, Holland CM, Charnock-Jones DS & Smith SK 2006 In vitro and in vivo effects of the PPAR-a agonists fenofibrate and retinoic acid in endometrial cancer. Molecular Cancer 5 13. (doi:10.1186/ 1476-4598-5-13)
50. Schulman IG, Li C, Schwabe JW & Evans RM 1997 The phantom ligand effect: allosteric control of transcription by the retinoid X receptor. Genes and Development 11 299-308. (doi:10.1101/ gad.11.3.299)
51. Smyth GK 2004 Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 3 Article3. (doi:10.2202/1544-6115.1027)
52. Tarrade A, Bastien J, Bruck N, Bauer A, Gianni M & Rochette-Egly C 2005 Retinoic acid and arsenic trioxide cooperate for apoptosis through phosphorylated RXRα. Oncogene 24 2277-2288. (doi:10. 1038/sj.onc.1208402)
53. Teyssier C, Belguise K, Galtier F, Cavailles V & Chalbos D 2003 Receptor-interacting protein 140 binds c-Jun and inhibits estradiol-induced activator protein-1 activity by reversing glucocorticoid receptor-interacting protein 1 effect. Molecular Endocrinology 17 287-299. (doi:10.1210/me.2002-0324)
54. Wada K, Nomura S, Morii E, Kitamura Y, Nishizawa Y, Miyake A & Terada N 1996 Changes in levels of mRNAs of transforming growth factor (TGF)-beta1,-beta2,-beta3, TGF-beta type II receptor and sulfated glycoprotein-2 during apoptosis of mouse uterine epithelium. Journal of Steroid Biochemistry and Molecular Biology 59 367-375. (doi:10.1016/S0960-0760(96)00139-2)
55. Weinert TA & Hartwell LH 1993 Cell cycle arrest of cdc mutants and specificity of the RAD9 checkpoint. Genetics 134 63-80.
56. Witcher M, Ross DT, Rousseau C, Deluca L & Miller WH Jr 2003 Synergy between all-trans retinoic acid and tumor necrosis factor pathways in acute leukemia cells. Blood 102 237-245. (doi:10.1182/ blood-2002-09-2725)
57. Woodworth CD, Chung J, McMullin E, Plowman GD, Simpson S & Iglesias M 1996 Transforming growth factor β1 supports autonomous growth of human papillomavirus-immortalized cervical keratinocytes under conditions promoting squamous differentiation. Cell Growth and Differentiation 7 811-820.
58. Yang S, Fang Z, Gurates B, Tamura M, Miller J, Ferrer K & Bulun SE 2001 Stromal PRs mediate induction of 17β-hydroxysteroid dehydrogenase type 2 expression in human endometrial epithelium: a paracrine mechanism for inactivation of E2. Molecular Endocrinology 15 2093-2105. (doi:10.1210/me.15.12.2093)
59. Zheng WL, Sierra-Rivera E, Luan J, Osteen KG & Ong DE 2000 Retinoic acid synthesis and expression of cellular retinol-binding protein and cellular retinoic acid-binding protein type II are concurrent with decidualization of rat uterine stromal cells. Endocrinology 141 802-808. (doi:10.1210/en.141.2.802)