3-Methylcholanthrene, an AhR agonist, caused cell-cycle arrest by histone deacetylation through a RhoA-dependent recruitment of HDAC1 and pRb2 to E2F1 complex

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Chang, Chih Cheng ^a,b   Sue, Yuh Mou ^b   Yang, Nian Jie ^a,b   Lee, Yi Hsuan ^c   Juan, Shu Hui ^a,b  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLCHOLANTHRENE; CYCLIN D3; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN E; HISTONE; HISTONE DEACETYLASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PRAVASTATIN; RAF PROTEIN; RAS PROTEIN; RETINOBLASTOMA 2 PROTEIN; RETINOBLASTOMA PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SIMVASTATIN; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL CYCLE ARREST; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; DEACETYLATION; DNA MODIFICATION; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; EPIGENETICS; GEL MOBILITY SHIFT ASSAY; HISTONE MODIFICATION; IMMUNOPRECIPITATION; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN HYPOPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; UPREGULATION;

ACETYLATION; ANIMALS; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; E2F1 TRANSCRIPTION FACTOR; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE 1; HISTONES; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; INTRACELLULAR SPACE; MALE; METHYLCHOLANTHRENE; MICE; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-RAF; PROTO-ONCOGENE PROTEINS P21(RAS); PTEN PHOSPHOHYDROLASE; RECEPTORS, ARYL HYDROCARBON; RETINOBLASTOMA-LIKE PROTEIN P130; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84899048744     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092793     Document Type: Article

References (36)

1. Ma Q, Whitlock JP Jr (1997) A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Biol Chem 272: 8878-8884. (Pubitemid 27154882)
2. Denison MS, Whitlock JP Jr (1995) Xenobiotic-inducible transcription of cytochrome P450 genes. J Biol Chem 270: 18175-18178.
3. Chang CC, Tsai SY, Lin H, Li HF, Lee YH, et al. (2009) Aryl-hydrocarbon receptor-dependent alteration of FAK/RhoA in the inhibition of HUVEC motility by 3-methylcholanthrene. Cell Mol Life Sci 66: 3193-3205.
4. Pang PH, Lin YH, Lee YH, Hou HH, Hsu SP, et al. (2008) Molecular mechanisms of p21 and p27 induction by 3-methylcholanthrene, an aryl-hydrocarbon receptor agonist, involved in antiproliferation of human umbilical vascular endothelial cells. J Cell Physiol 215: 161-171.
5. Chang CC, Lee PS, Chou Y, Hwang LL, Juan SH (2012) Mediating effects of aryl-hydrocarbon receptor and RhoA in altering brain vascular integrity: the therapeutic potential of statins. Am J Pathol 181: 211-221.
6. Lees E (1995) Cyclin dependent kinase regulation. Curr Opin Cell Biol 7: 773-780.
7. Sherr CJ (1993) Mammalian G1 cyclins. Cell 73: 1059-1065.
8. Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512. (Pubitemid 29297917)
9. Wang S, Ghosh RN, Chellappan SP (1998) Raf-1 physically interacts with Rb and regulates its function: a link between mitogenic signaling and cell cycle regulation. Mol Cell Biol 18: 7487-7498. (Pubitemid 28533067)
10. DeGregori J (2006) Surprising dependency for retinoblastoma protein in ras-mediated tumorigenesis. Mol Cell Biol 26: 1165-1169.
11. Dudler T, Gelb MH (1996) Palmitoylation of Ha-Ras facilitates membrane binding, activation of downstream effectors, and meiotic maturation in Xenopus oocytes. J Biol Chem 271: 11541-11547. (Pubitemid 26155999)
12. Claudio PP, Stiegler P, Howard CM, Bellan C, Minimo C, et al. (2001) RB2/p130 gene-enhanced expression down-regulates vascular endothelial growth factor expression and inhibits angiogenesis in vivo. Cancer Res 61: 462-468. (Pubitemid 32128598)
13. Garrison PM, Rogers JM, Brackney WR, Denison MS (2000) Effects of histone deacetylase inhibitors on the Ah receptor gene promoter. Arch Biochem Biophys 374: 161-171. (Pubitemid 30120249)
14. Latchney SE, Lioy DT, Henry EC, Gasiewicz TA, Strathmann FG, et al. (2011) Neural precursor cell proliferation is disrupted through activation of the aryl hydrocarbon receptor by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Stem Cells Dev 20: 313-326.
15. Puga A (2011) Perspectives on the potential involvement of the AH receptordioxin axis in cardiovascular disease. Toxicol Sci 120: 256-261.
16. Ge NL, Elferink CJ (1998) A direct interaction between the aryl hydrocarbon receptor and retinoblastoma protein. Linking dioxin signaling to the cell cycle. J Biol Chem 273: 22708-22713.
17. Puga A, Barnes SJ, Dalton TP, Chang C, Knudsen ES, et al. (2000) Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell cycle arrest. J Biol Chem 275: 2943-2950. (Pubitemid 30082071)
18. Weiss C, Kolluri SK, Kiefer F, Gottlicher M (1996) Complementation of Ah receptor deficiency in hepatoma cells: negative feedback regulation and cell cycle control by the Ah receptor. Exp Cell Res 226: 154-163. (Pubitemid 26238939)
19. Elferink CJ, Ge NL, Levine A (2001) Maximal aryl hydrocarbon receptor activity depends on an interaction with the retinoblastoma protein. Mol Pharmacol 59: 664-673. (Pubitemid 32273994)
20. Zhang HS, Dean DC (2001) Rb-mediated chromatin structure regulation and transcriptional repression. Oncogene 20: 3134-3138. (Pubitemid 32553569)
21. Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144: 1235-1244. (Pubitemid 29157301)
22. Fazal F, Bijli KM, Minhajuddin M, Rein T, Finkelstein JN, et al. (2009) Essential role of cofilin-1 in regulating thrombin-induced RelA/p65 nuclear translocation and intercellular adhesion molecule 1 (ICAM-1) expression in endothelial cells. J Biol Chem 284: 21047-21056.
23. Xu J, He L, Ahmed SH, Chen SW, Goldberg MP, et al. (2000) Oxygen-glucose deprivation induces inducible nitric oxide synthase and nitrotyrosine expression in cerebral endothelial cells. Stroke 31: 1744-1751. (Pubitemid 30437532)
24. Lin H, Lee JL, Hou HH, Chung CP, Hsu SP, et al. (2008) Molecular mechanisms of the antiproliferative effect of beraprost, a prostacyclin agonist, in murine vascular smooth muscle cells. J Cell Physiol 214: 434-441. (Pubitemid 350309000)
25. Lam EW, Bennett JD, Watson RJ (1995) Cell-cycle regulation of human B-myb transcription. Gene 160: 277-281.
26. Shih CM, Lin H, Liang YC, Lee WS, Bi WF, et al. (2004) Concentration-dependent differential effects of quercetin on rat aortic smooth muscle cells. Eur J Pharmacol 496: 41-48. (Pubitemid 39024314)
27. Juan SH, Lee JL, Ho PY, Lee YH, Lee WS (2006) Antiproliferative and antiangiogenic effects of 3-methylcholanthrene, an aryl-hydrocarbon receptor agonist, in human umbilical vascular endothelial cells. Eur J Pharmacol 530: 1-8.
28. Pierre S, Bats AS, Chevallier A, Bui LC, Ambolet-Camoit A, et al. (2011) Induction of the Ras activator Son of Sevenless 1 by environmental pollutants mediates their effects on cellular proliferation. Biochem Pharmacol 81: 304-313.
29. Mulero-Navarro S, Pozo-Guisado E, Perez-Mancera PA, Alvarez-Barrientos A, Catalina-Fernandez I, et al. (2005) Immortalized mouse mammary fibroblasts lacking dioxin receptor have impaired tumorigenicity in a subcutaneous mouse xenograft model. J Biol Chem 280: 28731-28741. (Pubitemid 41105774)
30. Brennan P, Babbage JW, Burgering BM, Groner B, Reif K, et al. (1997) Phosphatidylinositol 3-kinase couples the interleukin-2 receptor to the cell cycle regulator E2F. Immunity 7: 679-689. (Pubitemid 28156635)
31. Klippel A, Escobedo MA, Wachowicz MS, Apell G, Brown TW, et al. (1998) Activation of phosphatidylinositol 3-kinase is sufficient for cell cycle entry and promotes cellular changes characteristic of oncogenic transformation. Mol Cell Biol 18: 5699-5711. (Pubitemid 28450521)
32. Gu J, Tamura M, Yamada KM (1998) Tumor suppressor PTEN inhibits integrin- and growth factor-mediated mitogen-activated protein (MAP) kinase signaling pathways. J Cell Biol 143: 1375-1383. (Pubitemid 28559837)
33. Paramio JM, Navarro M, Segrelles C, Gomez-Casero E, Jorcano JL (1999) PTEN tumour suppressor is linked to the cell cycle control through the retinoblastoma protein. Oncogene 18: 7462-7468. (Pubitemid 30035047)
34. Davis RK, Chellappan S (2008) Disrupting the Rb-Raf-1 interaction: a potential therapeutic target for cancer. Drug News Perspect 21: 331-335.
35. Gomez-Duran A, Ballestar E, Carvajal-Gonzalez JM, Marlowe JL, Puga A, et al. (2008) Recruitment of CREB1 and histone deacetylase 2 (HDAC2) to the mouse Ltbp-1 promoter regulates its constitutive expression in a dioxin receptor-dependent manner. J Mol Biol 380: 1-16.
36. Martinez-Balbas MA, Bauer UM, Nielsen SJ, Brehm A, Kouzarides T (2000) Regulation of E2F1 activity by acetylation. EMBO J 19: 662-671. (Pubitemid 30093739)