Elevated SP-1 transcription factor expression and activity drives basal and hypoxia-induced Vascular Endothelial Growth Factor (VEGF) expression in non-small cell lung cancer

Journal of Biological Chemistry

Volumn 287, Issue 47, 2012, Pages 39967-39981

  Deacon, Karl ^a   Onion, David ^a   Kumari, Rajendra ^a   Watson, Susan A ^a   Knox, Alan J ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINOMYCIN D; AIRWAY EPITHELIAL CELLS; ANGIOGENESIS; BASE PAIRS; CHROMATIN IMMUNOPRECIPITATION ASSAY; CONSTITUTIVELY ACTIVES; DOMINANT NEGATIVE; EXPRESSION LEVELS; HISTONE ACETYLTRANSFERASES; HISTONE H4; HYPERACETYLATION; IMMUNOHISTOCHEMISTRY; MICROVASCULAR; MITHRAMYCIN; NON SMALL CELL LUNG CANCER; OVER-EXPRESSION; PROMOTER ACTIVITIES; STRONG CORRELATION; TRANSCRIPTION FACTOR EXPRESSION; TRANSCRIPTION START SITE; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR;

BIOLOGICAL ORGANS; CYTOLOGY; DISEASES; TRANSCRIPTION FACTORS; TUMORS;

CELLS;

DACTINOMYCIN; E1A ASSOCIATED P300 PROTEIN; HISTONE ACETYLTRANSFERASE PCAF; HISTONE H4; MESSENGER RNA; MITHRAMYCIN; MITHRAMYCIN A; RIBOZYME; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; BINDING SITE; CANCER CELL; CELL HYPOXIA; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; EX VIVO STUDY; FLUORESCENCE; GENE EXPRESSION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; TRANSCRIPTION INITIATION SITE;

ANOXIA; CARCINOMA, NON-SMALL-CELL LUNG; CELL HYPOXIA; CELL LINE, TUMOR; DACTINOMYCIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; LUNG NEOPLASMS; MALE; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; NUCLEIC ACID SYNTHESIS INHIBITORS; P300-CBP TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SP1 TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84869224268     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.397042     Document Type: Article

References (52)

1. Hanahan, D., and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70 (Pubitemid 30046295)
2. Yuan, A., Yu, C. J., Chen, W. J., Lin, F. Y., Kuo, S. H., Luh, K. T., and Yang, P. C. (2000) Correlation of total VEGFmRNAand protein expression with histologic type, tumor angiogenesis, patient survival and timing of relapse in non-small-cell lung cancer. Int. J. Cancer 89, 475-483
3. Yuan, A., Yu, C. J., Kuo, S. H., Chen, W. J., Lin, F. Y., Luh, K. T., Yang, P. C., and Lee, Y. C. (2001) Vascular endothelial growth factor 189 mRNA isoform expression specifically correlates with tumor angiogenesis, patient survival, and postoperative relapse in non-small-cell lung cancer. J. Clin. Oncol. 19, 432-441 (Pubitemid 32112856)
4. Han, H., Silverman, J. F., Santucci, T. S., Macherey, R. S., d'Amato, T. A., Tung, M. Y., Weyant, R. J., and Landreneau, R. J. (2001) Vascular endothelial growth factor expression in stage I non-small cell lung cancer correlates with neoangiogenesis and a poor prognosis. Ann. Surg. Oncol. 8, 72-79 (Pubitemid 32126827)
5. Decaussin, M., Sartelet, H., Robert, C., Moro, D., Claraz, C., Brambilla, C., and Brambilla, E. (1999) Expression of vascular endothelial growth factor (VEGF) and its two receptors (VEGF-R1-Flt1 and VEGF-R2-Flk1/KDR) in non-small cell lung carcinomas (NSCLCs). Correlation with angiogenesis and survival. J. Pathol. 188, 369-377 (Pubitemid 29327434)
6. Graves, E. E., Vilalta, M., Cecic, I. K., Erler, J. T., Tran, P. T., Felsher, D., Sayles, L., Sweet-Cordero, A., Le, Q. T., and Giaccia, A. J. (2010) Hypoxia in models of lung cancer. Implications for targeted therapeutics. Clin. Cancer Res. 16, 4843-4852
7. Tsai, J. C., Goldman, C. K., and Gillespie, G. Y. (1995) Vascular endothelial growth factor in human glioma cell lines. Induced secretion by EGF, PDGF-BB, and bFGF. J. Neurosurg. 82, 864-873
8. De Luca, A., Carotenuto, A., Rachiglio, A., Gallo, M., Maiello, M. R., Aldinucci, D., Pinto, A., and Normanno, N. (2008) The role of the EGFR signaling in tumor microenvironment. J. Cell Physiol. 214, 559-567 (Pubitemid 351224199)
9. Gately, S. (2000) The contributions of cyclooxygenase-2 to tumor angiogenesis. Cancer Metastasis Rev. 19, 19-27
10. Textor, B., Sator-Schmitt, M., Richter, K. H., Angel, P., and Schorpp-Kistner, M. (2006) c-Jun and JunB are essential for hypoglycemia- mediated VEGF induction. Ann. N.Y. Acad. Sci. 1091, 310-318 (Pubitemid 47092246)
11. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K. S., Powell-Braxton, L., Hillan, K. J., and Moore, M. W. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442 (Pubitemid 26102720)
12. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C., Declercq, C., Pawling, J., Moons, L., Collen, D., Risau, W., and Nagy, A. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439 (Pubitemid 26102719)
13. Kim, K. J., Li, B., Winer, J., Armanini, M., Gillett, N., Phillips, H. S., and Ferrara, N. (1993) Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 362, 841-844 (Pubitemid 23132159)
14. Gerber, H. P., and Ferrara, N. (2005) Pharmacology and pharmacodynamics of bevacizumab as monotherapy or in combination with cytotoxic therapy in preclinical studies. Cancer Res. 65, 671-680
15. Yoo, P. S., Mulkeen, A. L., and Cha, C. H. (2006) Post-transcriptional regulation of vascular endothelial growth factor. Implications for tumor angiogenesis. World J. Gastroenterol. 12, 4937-4942 (Pubitemid 44323260)
16. Ferrara, N. (2010) Binding to the extracellular matrix and proteolytic processing. Two key mechanisms regulating vascular endothelial growth factor action. Mol. Biol. Cell 21, 687-690
17. Ladomery, M. R., Harper, S. J., and Bates, D. O. (2007) Alternative splicing in angiogenesis. The vascular endothelial growth factor paradigm. Cancer Lett. 249, 133-142 (Pubitemid 46452926)
18. Folkman, J., Long, D. M., Jr., and Becker, F. F. (1963) Growth and metastasis of tumor in organ culture. Cancer 16, 453-467
19. Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J. M., Lane, W. S., and Kaelin, W. G., Jr. (2001) HIFα targeted for VHL-mediated destruction by proline hydroxylation. Implications for O2 sensing. Science 292, 464-468 (Pubitemid 32335941)
20. 2-regulated prolyl hydroxylation. Science 292, 468-472
21. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275 (Pubitemid 29246458)
22. Mizukami, Y., Li, J., Zhang, X., Zimmer, M. A., Iliopoulos, O., and Chung, D. C. (2004) Hypoxia-inducible factor-1-independent regulation of vascular endothelial growth factor by hypoxia in colon cancer. Cancer Res. 64, 1765-1772 (Pubitemid 38428700)
23. Arany, Z., Wagner, B. K., Ma, Y., Chinsomboon, J., Laznik, D., and Spiegelman, B. M. (2008) Gene expression-based screening identifies microtubule inhibitors as inducers of PGC-1α and oxidative phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 105, 4721-4726 (Pubitemid 351753813)
24. Clark, P. E. (2009) The role ofVHLin clear-cell renal cell carcinoma and its relation to targeted therapy. Kidney Int. 76, 939-945
25. Rak, J., Yu, J. L., Klement, G., and Kerbel, R. S. (2000) Oncogenes and angiogenesis. Signaling three-dimensional tumor growth. J. Investig. Dermatol. Symp. Proc. 5, 24-33 (Pubitemid 32044086)
26. Spinella, F., Rosanò, L., Di Castro, V., Natali, P. G., and Bagnato, A. (2004) Endothelin-1-induced prostaglandin E2-EP2, EP4 signaling regulates vascular endothelial growth factor production and ovarian carcinoma cell invasion. J. Biol. Chem. 279, 46700-46705 (Pubitemid 39523128)
27. Kaluz, S., Kaluzová, M., and Stanbridge, E. J. (2003) Expression of the hypoxia marker carbonic anhydrase IX is critically dependent on SP1 activity. Identification of a novel type of hypoxia-responsive enhancer. Cancer Res. 63, 917-922 (Pubitemid 36278419)
28. Xu, Q., Ji, Y. S., and Schmedtje, J. F., Jr. (2000) Sp1 increases expression of cyclooxygenase-2 in hypoxic vascular endothelium. Implications for the mechanisms of aortic aneurysm and heart failure. J. Biol. Chem. 275, 24583-24589 (Pubitemid 30626555)
29. Koshiji, M., To, K. K., Hammer, S., Kumamoto, K., Harris, A. L., Modrich, P., and Huang, L. E. (2005) HIF-1α induces genetic instability by transcriptionally downregulating MutSalpha expression. Mol. Cell 17, 793-803 (Pubitemid 40386941)
30. 2)/cy-clooxygenase- 2 (COX-2)/prostacyclin receptor-dependent autocrine loop. J. Biol. Chem. 285, 25913-25927
31. 2-terminal kinase 1 and MKK3/p38 pathways regulated by MEK kinases 2 and 3. MEK kinase 3 activates MKK3 but does not cause activation of p38 kinase in vivo. J. Biol. Chem. 272, 14489-14496
32. Bradbury, D., Clarke, D., Seedhouse, C., Corbett, L., Stocks, J., and Knox, A. (2005) Vascular endothelial growth factor induction by prostaglandin E2 in human airway smooth muscle cells is mediated by E prostanoid EP2/EP4 receptors and SP-1 transcription factor binding sites. J. Biol. Chem. 280, 29993-30000 (Pubitemid 41216174)
33. Finkenzeller, G., Technau, A., and Marmé, D. (1995) Hypoxia-induced transcription of the vascular endothelial growth factor gene is independent of functional AP-1 transcription factor. Biochem. Biophys. Res. Commun. 208, 432-439
34. Finkenzeller, G., Sparacio, A., Technau, A., Marmé, D., and Siemeister, G. (1997) Sp1 recognition sites in the proximal promoter of the human vascular endothelial growth factor gene are essential for platelet-derived growth factor-induced gene expression. Oncogene 15, 669-676 (Pubitemid 27389929)
35. Blume, S. W., Snyder, R. C., Ray, R., Thomas, S., Koller, C. A., and Miller, D. M. (1991) Mithramycin inhibits SP1 binding and selectively inhibits transcriptional activity of the dihydrofolate reductase gene in vitro and in vivo. J. Clin. Invest. 88, 1613-1621
36. Black, A. R., Black, J. D., and Azizkhan-Clifford, J. (2001) Sp1 and Kruppel-like factor family of transcription factors in cell growth regulation and cancer. J. Cell Physiol. 188, 143-160 (Pubitemid 32622905)
37. Lou, Z., O'Reilly, S., Liang, H., Maher, V. M., Sleight, S. D., and McCormick, J. J. (2005) Down-regulation of overexpressed sp1 protein in human fibrosarcoma cell lines inhibits tumor formation. Cancer Res. 65, 1007-1017 (Pubitemid 40216463)
38. Li, L., and Davie, J. R. (2010) The role of Sp1 and Sp3 in normal and cancer cell biology. Ann. Anat. 192, 275-283
39. Wierstra, I. (2008) Sp1. Emerging roles. Beyond constitutive activation of TATA-less housekeeping genes. Biochem. Biophys. Res. Commun 372, 1-13
40. Brown, L. M., Cowen, R. L., Debray, C., Eustace, A., Erler, J. T., Sheppard, F. C., Parker, C. A., Stratford, I. J., and Williams, K. J. (2006) Reversing hypoxic cell chemoresistance in vitro using genetic and small molecule approaches targeting hypoxia inducible factor-1. Mol. Pharmacol. 69, 411-418 (Pubitemid 43121938)
41. Lee, C. G., Yoon, H. J., Zhu, Z., Link, H., Wang, Z., Gwaltney, J. M., Landry, M., and Elias, J. A. (2000) Respiratory syncytial virus stimulation of vascular endothelial cell growth factor/vascular permeability factor. Am. J. Respir. Cell Mol. Biol. 23, 662-669
42. Takayama, K., Reynolds, P. N., Adachi, Y., Kaliberova, L., Uchino, J., Nakanishi, Y., and Curiel, D. T. (2007) Vascular endothelial growth factor promoter-based conditionally replicative adenoviruses for pan-carcinoma application. Cancer Gene. Ther. 14, 105-116 (Pubitemid 44952240)
43. Shimoyamada, H., Yazawa, T., Sato, H., Okudela, K., Ishii, J., Sakaeda, M., Kashiwagi, K., Suzuki, T., Mitsui, H., Woo, T., Tajiri, M., Ohmori, T., Ogura, T., Masuda, M., Oshiro, H., and Kitamura, H. (2010) Early growth response-1 induces and enhances vascular endothelial growth factor-A expression in lung cancer cells. Am. J. Pathol. 177, 70-83
44. Bouchard, F., Bélanger, S. D., Biron-Pain, K., and St-Pierre, Y. (2010) EGR-1 activation by EGF inhibits MMP-9 expression and lymphoma growth. Blood 116, 759-766
45. Lim, J. H., Jung, C. R., Lee, C. H., and Im, D. S. (2008) Egr-1 and serum response factor are involved in growth factors- and serum-mediated induction of E2-EPF UCP expression that regulates the VHL-HIF pathway. J. Cell Biochem. 105, 1117-1127
46. Kamimura, M., Bea, F., Akizawa, T., Katus, H. A., Kreuzer, J., and Viedt, C. (2004) Platelet-derived growth factor induces tissue factor expression in vascular smooth muscle cells via activation of Egr-1. Hypertension 44, 944-951 (Pubitemid 39577426)
47. Kong, L. M., Liao, C. G., Fei, F., Guo, X., Xing, J. L., and Chen, Z. N. (2010) Transcription factor Sp1 regulates expression of cancer-associated molecule CD147 in human lung cancer. Cancer Sci. 101, 1463-1470
48. Yao, J. C., Wang, L., Wei, D., Gong, W., Hassan, M., Wu, T. T., Mansfield, P., Ajani, J., and Xie, K. (2004) Association between expression of transcription factor Sp1 and increased vascular endothelial growth factor expression, advanced stage, and poor survival in patients with resected gastric cancer. Clin. Cancer Res. 10, 4109-4117 (Pubitemid 38812490)
49. Shi, Q., Le, X., Abbruzzese, J. L., Peng, Z., Qian, C. N., Tang, H., Xiong, Q., Wang, B., Li, X. C., and Xie, K. (2001) Constitutive Sp1 activity is essential for differential constitutive expression of vascular endothelial growth factor in human pancreatic adenocarcinoma. Cancer Res. 61, 4143-4154 (Pubitemid 32720983)
50. Zannetti, A., Del Vecchio, S., Carriero, M. V., Fonti, R., Franco, P., Botti, G., D'Aiuto, G., Stoppelli, M. P., and Salvatore, M. (2000) Coordinate up-regulation of Sp1 DNA-binding activity and urokinase receptor expression in breast carcinoma. Cancer Res. 60, 1546-1551 (Pubitemid 30183423)
51. Guan, H., Cai, J., Zhang, N., Wu, J., Yuan, J., Li, J., and Li, M. (2012) Sp1 is upregulated in human glioma, promotes MMP-2-mediated cell invasion and predicts poor clinical outcome. Int. J. Cancer 130, 593-601
52. Discher, D. J., Bishopric, N. H., Wu, X., Peterson, C. A., and Webster, K. A. (1998) Hypoxia regulates β-enolase and pyruvate kinase-M promoters by modulating Sp1/Sp3 binding to a conserved GC element. J. Biol. Chem. 273, 26087-26093 (Pubitemid 28475843)