β-Catenin and peroxisome proliferator-activated receptor- δcoordinate dynamic chromatin loops for the transcription of vascular endothelial growth factor A gene in colon cancer cells

Journal of Biological Chemistry

Volumn 287, Issue 49, 2012, Pages 41364-41373

  Hwang, Injoo ^a   Kim, Jeeho ^a   Jeong, Sunjoo ^a  

^a Dankook University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; CANCER CELLS; CELL ENGINEERING; CHEMICAL ACTIVATION; CYTOLOGY; DISEASES; DYNAMICS; ENDOTHELIAL CELLS; PLANTS (BOTANY);

CHROMATIN IMMUNOPRECIPITATION; COLON CANCER CELLS; COLORECTAL CARCINOMA; DOWN-STREAM; LUCIFERASE ASSAYS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; TARGET GENES; UPSTREAM SITES; VASCULAR ENDOTHELIAL GROWTH FACTOR; Β-CATENIN;

TRANSCRIPTION;

BETA CATENIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; T CELL FACTOR 4 PROTEIN; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER CELL; CARCINOGENESIS; CELL STRAIN HCT116; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; COLON CANCER; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A GENE;

EID: 84870331037     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.377739     Document Type: Article

References (65)

1. Grothey, A., and Galanis, E. (2009) Targeting angiogenesis. Progress with anti- VEGFA treatment with large molecules. Nat. Rev. Clin. Oncol. 6, 507-518
2. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732
3. Wouters, B. G., and Koritzinsky, M. (2008) Hypoxia signaling through mTOR and the unfolded protein response in cancer. Nat. Rev. Cancer 8, 851-864
4. Zhang, X., Gaspard, J. P., and Chung, D. C. (2001) Regulation of vascular endothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res. 61, 6050-6054 (Pubitemid 32762538)
5. Easwaran, V., Lee, S. H., Inge, L., Guo, L., Goldbeck, C., Garrett, E., Wiesmann, M., Garcia, P. D., Fuller, J. H., Chan, V., Randazzo, F., Gundel, R., Warren, R. S., Escobedo, J., Aukerman, S. L., Taylor, R. N., and Fantl, W. J. (2003) β-Catenin regulates vascular endothelial growth factor expression in colon cancer. Cancer Res. 63, 3145-3153 (Pubitemid 36735866)
6. Rao, T. P., and Kühl, M. (2010) An updated overview on Wnt signaling pathways. A prelude for more. Circulation Res. 106, 1798-1806
7. Wagner, N., Jehl-Piétri, C., Lopez, P., Murdaca, J., Giordano, C., Schwartz, C., Gounon, P., Hatem, S. N., Grimaldi, P., and Wagner, K. D. (2009) Peroxisome proliferator-activated receptor b stimulation induces rapid cardiac growth and angiogenesis via direct activation of calcineurin. Cardiovasc. Res. 83, 61-71
8. Goodwin, A. M., and D'Amore, P. A. (2002) Wnt signaling in the vasculature. Angiogenesis 5, 1-9 (Pubitemid 36076918)
9. Fauconnet, S., Lascombe, I., Chabannes, E., Adessi, G. L., Desvergne, B., and Wahli, W. (2002) Differential regulation of vascular endothelial growth factor expression by peroxisome proliferator-activated receptors in bladder cancer cells. J. Biol. Chem. 277, 23534-23543 (Pubitemid 34952189)
10. Stephen, R. L., Gustafsson, M. C., Jarvis, M., Tatoud, R., Marshall, B. R., and Knight, D. (2004) Activation of peroxisome proliferator-activated receptor δ stimulates the proliferation of human breast and prostate cancer cell lines. Cancer Res. 64, 3162-3170 (Pubitemid 38581418)
11. Zuo, X., Peng, Z., Moussalli, M. J., Morris, J. S., Broaddus, R. R., Fischer, S. M., and Shureiqi, I. (2009) Targeted genetic disruption of peroxisome proliferator-activated receptor δ and colonic tumorigenesis. J. Natl. Cancer Inst. 101, 762-767
12. Wang, D., Wang, H., Guo, Y., Ning, W., Katkuri, S., Wahli, W., Desvergne, B., Dey, S. K., and DuBois, R. N. (2006) Cross-talk between peroxisome proliferator-activated receptor δ and VEGFA stimulates cancer progression. Proc. Natl. Acad. Sci. U.S.A. 103, 19069-19074 (Pubitemid 350002829)
13. Röhrl, C., Kaindl, U., Koneczny, I., Hudec, X., Baron, D. M., König, J. S., and Marian, B. (2011) Peroxisome proliferator-activated receptor γ and β/δ mediate vascular endothelial growth factor production in colorectal tumor cells. J. Cancer Res. Clin. Oncol. 137, 29-39
14. Barker, N., and Clevers, H. (2006) Mining the Wnt pathway for cancer therapeutics. Nat. Rev. Drug Discov. 5, 997-1014 (Pubitemid 44835127)
15. Clevers, H. (2006) Wnt/β-catenin signaling in development and disease. Cell 127, 469-480
16. Saif, M. W., and Chu, E. (2010) Biology of colorectal cancer. Cancer J. 16, 196-201
17. Castrillo, A., and Tontonoz, P. (2004) Nuclear receptors in macrophage biology. At the cross-roads of lipid metabolism and inflammation. Annu. Rev. Cell Dev. Biol. 20, 455-480 (Pubitemid 39488646)
18. Berger, J., and Moller, D. E. (2002) The mechanisms of action of PPARs. Annu. Rev. Med. 53, 409-435 (Pubitemid 34177889)
19. Wang, D., and Dubois, R. N. (2008) Peroxisome proliferator-activated receptors and progression of colorectal cancer. PPAR Res. 2008, 931074
20. Park, B. H., Vogelstein, B., and Kinzler, K. W. (2001) Genetic disruption of PPAR-δ decrease the tumorigenicity of human colon cancer cells. Proc. Natl. Acad. Sci. U.S.A. 98, 2598-2603 (Pubitemid 32209528)
21. Wang, D., Wang, H., Shi, Q., Katkuri, S., Walhi, W., Desvergne, B., Das, S. K., Dey, S. K., and DuBois, R. N. (2004) Prostaglandin E2 promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor δ. Cancer Cell 6, 285-295 (Pubitemid 39222041)
22. Reed, K. R., Sansom, O. J., Hayes, A. J., Gescher, A. J., Winton, D. J., Peters, J. M., and Clarke, A. R. (2004) PPAR-δ status and Apc-mediated tumourigenesis in the mouse intestine. Oncogene 23, 8992-8996 (Pubitemid 39657790)
23. Harman, F. S., Nicol, C. J., Marin, H. E., Ward, J. M., Gonzalez, F. J., and Peters, J. M. (2004) Peroxisome proliferator-activated receptor-δ attenuates colon carcinogenesis. Nat. Med. 10, 481-483 (Pubitemid 38667905)
24. Kim, D. J., Bility, M. T., Billin, A. N., Willson, T. M., Gonzalez, F. J., and Peters, J. M. (2006) PPARβ/δ selectively induces differentiation and inhibits cell proliferation. Cell Death Differ. 13, 53-60
25. Hollingshead, H. E., Killins, R. L., Borland, M. G., Girroir, E. E., Billin, A. N., Willson, T. M., Sharma, A. K., Amin, S., Gonzalez, F. J., and Peters, J. M. (2007) Peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) ligands do not potentiate growth of human cancer cell lines. Carcinogenesis 28, 2641-2649 (Pubitemid 350238968)
26. Foreman, J. E., Chang, W. C., Palkar, P. S., Zhu, B., Borland, M. G., Williams, J. L., Kramer, L. R., Clapper, M. L., Gonzalez, F. J., and Peters, J. M. (2011) Functional characterization of peroxisome proliferator-activated receptor-β/δ expression in colon cancer. Mol. Carcinog. 50, 884-900
27. Müller, R. (2004) Cross-talk of oncogenic and prostanoid signaling pathways. J. Cancer Res. Clin. Oncol. 130, 429-444
28. Wang, D., and DuBois, R. N. (2007) Inflammatory mediators and nuclear receptor signaling in colorectal cancer. Cell Cycle 6, 682-685 (Pubitemid 46535680)
29. Han, C., Lim, K., Xu, L., Li, G., and Wu, T. (2008) Regulation of Wnt/β-catenin pathway by cPLA2α and PPAR-δ. J. Cell Biochem. 105, 534-545
30. Li, Q., Barkess, G., and Qian, H. (2006) Chromatin looping and the probability of transcription. Trends Genet. 22, 197-202
31. Kleinjan, D. A., and van Heyningen, V. (2005) Long range control of gene expression. Emerging mechanisms and disruption in disease. Am. J. Hum. Genet. 76, 8-32 (Pubitemid 40023762)
32. Yochum, G. S., McWeeney, S., Rajaraman, V., Cleland, R., Peters, S., and Goodman, R. H. (2007) Serial analysis of chromatin occupancy identifies β-catenin target genes in colorectal carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 104, 3324-3329 (Pubitemid 46364158)
33. Yochum, G. S., Cleland, R., and Goodman, R. H. (2008) A genome-wide screen for β-catenin binding sites identifies a downstream enhancer element that controls c-Myc gene expression. Mol. Cell. Biol. 28, 7368-7379
34. Hatzis, P., van der Flier, L. G., van Driel, M. A., Guryev, V., Nielsen, F., Denissov, S., Nijman, I. J., Koster, J., Santo, E. E., Welboren, W., Versteeg, R., Cuppen, E., van de Wetering, M., Clevers, H., and Stunnenberg, H. G. (2008) Genome-wide pattern of TCF7L2/TCF-4 chromatin occupancy in colorectal cancer cells. Mol. Cell. Biol. 28, 2732-2744 (Pubitemid 351542371)
35. Yochum, G. S., Sherrick, C. M., Macpartlin, M., and Goodman, R. H. (2010) A β-catenin/TCF-coordinated chromatin loop at MYC integrates 5′ and 3′ Wnt responsive enhancers. Proc. Natl. Acad. Sci. U.S.A. 107, 145-150
36. Choi, Y. S., Hur, J., and Jeong, S. (2007) β-Catenin binds to the downstream region and regulates the expression C-reactive protein gene. Nucleic Acids Res. 35, 5511-5519 (Pubitemid 47423924)
37. Mosimann, C., Hausmann, G., and Basler, K. (2009) β-Catenin hits chromatin. Regulation of Wnt target gene activation. Nat. Rev. Mol. Cell Biol. 10, 276-286
38. Valenta, T., Hausmann, G., and Basler, K. (2012) The many faces and functions of β-catenin. EMBO J. 31, 2714-2736
39. Dekker, J. (2006) The three C's of chromosome conformation capture. Controls, controls, controls. Nat. Methods 3, 17-21
40. Hwang, I., Choi, Y. S., Jeon, M. Y., and Jeong, S. (2010) NF-κB p65 represses β-catenin-activated transcription of cyclin D1. Biochem. Biophys. Res. Commun. 403, 79-84
41. Aarenstrup, L., Flindt, E. N., Otkjaer, K., Kirkegaard, M., Andersen, J. S., and Kristiansen, K. (2008) HDAC activity is required for p65/RelA-dependent repression of PPAR δ-mediated transactivation in human keratinocytes. J. Invest. Dermatol. 128, 1095-1106 (Pubitemid 351543195)
42. Peeters, L. L., Vigne, J. L., Tee, M. K., Zhao, D., Waite, L. L., and Taylor, R. N. (2005) PPARγ represses VEGFA expression in human endometrial cells: implication for uterine angiogenesis. Angiogenesis 8, 373-379
43. Chandra, V., Huang, P., Hamuro, Y., Raghuram, S., Wang, Y., Burris, T. P., and Rastinejad, F. (2008) Structure of the intact PPAR-γ-RXR-nuclear receptor complex on DNA. Nature 456, 350-356
44. Allred, C. D., Talbert, D. R., Southard, R. C., Wang, X., and Kilgore, M. W. (2008) PPARγ as a molecular target of eicosapentaenoic acid in human colon cancer (HT-29) cells. J. Nutr. 138, 250-256 (Pubitemid 351213635)
45. Ignatenko, N. A., Babbar, N., Mehta, D., Casero, R. A., Jr., and Gerner, E. W. (2004) Suppression of polyamine catabolism by activated Ki-ras in human colon cancer cells. Mol. Carcinog 39, 91-102 (Pubitemid 38167113)
46. Babbar, N., Ignatenko, N. A., Casero, R. A., Jr., and Gerner, E. W. (2003) Cyclooxygenase-independent induction of apoptosis by sulindac sulfone is mediated by polyamines in colon cancer. J. Biol. Chem. 278, 47762-47775 (Pubitemid 37523223)
47. Billin, A. N., Thirlwell, H., and Ayer, D. E. (2000) β-Catenin- histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator. Mol. Cell. Biol. 20, 6882-6890
48. Margariti, A., Zampetaki, A., Xiao, Q., Zhou, B., Karamariti, E., Martin, D., Yin, X., Mayr, M., Li, H., Zhang, Z., De Falco, E., Hu, Y., Cockerill, G., Xu, Q., and Zeng, L. (2010) Histone Deacetylase 7 controls endothelial cell growth through modulation of β-catenin. Circ. Res. 106, 1202-1211
49. Hsu, P. Y., Hsu, H. K., Singer, G. A., Yan, P. S., Rodriguez, B. A., Liu, J. C., Weng, Y. I., Deatherage, D. E., Chen, Z., Pereira, J. S., Lopez, R., Russo, J., Wang, Q., Lamartiniere, C. A., Nephew, K. P., and Huang, T. H. (2010) Estrogen-mediated epigenetic repression of large chromatin regions through DNA looping. Genome Res. 20, 733-744
50. Olson, L. E., Tollkuhn, J., Scafoglio, C., Krones, A., Zhang, J., Ohgi, K. A., Wu, W., Taketo, M. M., Kemler, R., Grosschedl, R., Rose, D., Li, X., and Rosenfeld, M. G. (2006) Homeodomain-mediated β-catenin-dependent switching events dictate cell-lineage determination. Cell 125, 593-605
51. Kim, Y. J., Cecchini, K. R., and Kim, T. H. (2011) Conserved, developmentally regulated mechanism couples chromatin looping and heterochromatin barrier activity at the homeobox gene A locus. Proc. Natl. Acad. Sci. U.S.A. 108, 7391-7396
52. Oishi, Y., Manabe, I., Tobe, K., Ohsugi, M., Kubota, T., Fujiu, K., Maemura, K., Kubota, N., Kadowaki, T., and Nagai, R. (2008) SUMOylation of Krüppel-like transcription factor 5 acts as a molecular switch in transcriptional programs of lipid metabolism involving PPAR-δ. Nat. Med. 14, 656-666 (Pubitemid 351809542)
53. Gupta, R. A., Tan, J., Krause, W. F., Geraci, M. W., Willson, T. M., Dey, S. K., and DuBois, R. N. (2000) Prostacyclin-mediated activation of peroxisome proliferator activated receptor δ in colorectal cancer. Proc. Natl. Acad. Sci. U.S.A. 97, 13275-13280
54. Takayama, O., Yamamoto, H., Damdinsuren, B., Sugita, Y., Ngan, C. Y., Xu, X., Tsujino, T., Takemasa, I., Ikeda, M., Sekimoto, M., Matsuura, N., and Monden, M. (2006) Expression of PPAR-δ in multistage carcinogenesis of the colorectum. Implications of malignant cancer morphology. Br. J. Cancer 95, 889-895 (Pubitemid 44498105)
55. Moraes, L. A., Piqueras, L., and Bishop-Bailey, D. (2006) Peroxisome proliferator-activated receptors and inflammation. Pharmacol. Ther. 110, 371-385
56. Notterman, D. A., Alon, U., Sierk, A. J., and Levine, A. J. (2001) Transcriptional gene expression profiles of colorectal adenoma, adenocarcinoma, and normal tissue examined by oligonucleotide arrays. Cancer Res. 61, 3124-3130 (Pubitemid 32691964)
57. Hao, C. Y., Moore, D. H., Wong, P., Bennington, J. L., Lee, N. M., and Chen, L. C. (2005) Alteration of gene expression in macroscopically normal colonic mucosa from individuals with a family history of sporadic colon cancer. Clin. Cancer Res. 11, 1400-1407 (Pubitemid 40315219)
58. Essers, M. A., de Vries-Smits, L. M., Barker, N., Polderman, P. E., Burgering, B. M., and Korswagen, H. C. (2005) Functional interaction between β-catenin and FOXO in oxidative stress signaling. Science 308, 1181-1184 (Pubitemid 40696437)
59. Kioussi, C., Briata, P., Baek, S. H., Rose, D. W., Hamblet, N. S., Herman, T., Ohgi, K. A., Lin, C., Gleiberman, A., Wang, J., Brault, V., Ruiz-Lozano, P., Nguyen, H. D., Kemler, R., Glass, C. K., Wynshaw-Boris, A., and Rosenfeld, M. G. (2002) Identification of a Wnt/Dvl/β-catenin → Pitx2 pathway mediating cell type-specific proliferation during development. Cell 111, 673-685 (Pubitemid 35441249)
60. Kwak, H., Hwang, I., Kim, J. H., Kim, M. Y., Yang, J. S., and Jeong, S. (2009) Modulation of transcription by the peroxisome proliferator-activated receptor-δ binding RNA aptamer in colon cancer cells. Mol. Cancer Ther. 8, 2664-2673
61. Wu, C. W., Yu, J., and Sung, J. J. (2009) Peroxisome proliferator- activated receptor δ and gastric cancer. Oncol. Rep. 22, 451-457
62. Handeli, S., and Simon, J. A. (2008) A small molecule inhibitor of Tcf/β-catenin signaling down-regulates PPARγ and PPAR-δ activities. Mol. Cancer Ther. 7, 521-529 (Pubitemid 351482135)
63. He, T. C., Chan, T. A., Vogelstein, B., and Kinzler, K. W. (1999) PPAR-δ is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell 99, 335-345 (Pubitemid 29519912)
64. de Laat, W., and Grosveld, F. (2003) Spatial organization of gene expression. The active chromatin hub. Chromosome Res. 11, 447-459
65. Hampsey, M., Singh, B. N., Ansari, A., Lainé, J. P., and Krishnamurthy, S. (2011) Control of eukaryotic gene expression. Gene loops and transcriptional memory. Adv. Enzyme Regul. 51, 118-125