A bisanthracycline (WP631) represses uPAR gene expression and cell migration of RKO colon cancer cells by interfering with transcription factor binding to a chromatin-accessible -148/-124 promoter region

Oncology Research

Volumn 15, Issue 5, 2005, Pages 265-279

  Nair, Rajesh R ^a   Wang, Heng ^a   Jamaluddin, Md S ^a   Fokt, Izabella ^a   Priebe, Waldemar ^a   Boyd, Douglas D ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Gene expression; Sp1; Transcription; uPAR

Indexed keywords

ANTHRACYCLINE DERIVATIVE; BISANTHRACYCLINE; DEOXYRIBONUCLEASE I; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; UNCLASSIFIED DRUG; UROKINASE RECEPTOR; VITRONECTIN; WP 629; WP 631;

ALLELE; ARTICLE; BINDING AFFINITY; CANCER CELL; CELL LEVEL; CELL MIGRATION; CHROMATIN; COLON CANCER; DNA BINDING; DNA FOOTPRINTING; DNA SEQUENCE; DRUG INHIBITION; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; GC RICH SEQUENCE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; TRANSCRIPTION INITIATION;

EID: 26244438166     PISSN: 09650407     EISSN: None     Source Type: Journal    
DOI: 10.3727/096504005776404571     Document Type: Article

References (61)

1. Nielsen, L.; Kellerman, G. M.; Behrendt, N.; Picone, R.; Dano, K.; Blasi, F. A 55,000-60,000 Mr receptor protein for urokinase-type plasminogen activator. J. Biol. Chem. 263:2358-2363; 1988.
2. Behrendt, N.; Ronne, E.; Ploug, M.; Petri, T.; Lober, D.; Nielsen, L.; Schleuning, W.; Blasi, F.; Appella, E.; Dano, K. The human receptor for urokinase plasminogen activator. J. Biol. Chem. 265:6453-6460; 1990.
3. Wei, Y.; Waltz, D. A.; Rao, N.; Drummond, R. J.; Rosenberg, S.; Chapman, H. A. Identification of the urokinase receptor as an adhesion receptor for vitronectin. J. Biol. Chem. 269:32380-32388; 1994.
4. Ghiso, J. A.; Kovalski, K.; Ossowski, L. Tumor dormancy induced by downregulation of urokinase receptor in human carcinoma involves integrin and MAPK signaling. J. Cell Biol. 147:89-103; 1999.
5. Resnati, M.; Pallavicini, I.; Wang, J. M.; Oppenheim, J.; Serhan, C. N.; Romano, M.; Blasi, F. The fibrinolytic receptor for urokinase activates the G protein-coupled chemotactin receptor FPRL1/LXA4R. Proc. Natl. Acad. Sci. USA 99:1359-1364; 2002.
6. Wei, Y.; Lukashev, M.; Simon, D. I.; Bodary, S. C.; Rosenberg, S.; Doyle, M. V.; Chapman, H. A. Regulation of integrin function by the urokinase receptor. Science 273: 1551-1555; 1996.
7. 2-macroglobulin receptor. J. Biol. Chem. 269:17886-17892; 1994.
8. Ellis, V.; Behrendt, N.; Dano, K. Plasminogen activation by receptor-bound urokinase. J. Biol. Chem. 266:12752-12758; 1991.
9. Nestl, A.; Von Stein, O. D.; Zatloukal, K.; Thies, W.-G.; Herrlich, P.; Hofmann, M.; Sleeman, J. P. Gene expression patterns associated with the metastatic phenotype in rodent and human tumors. Cancer Res. 61:1569-1577; 2001.
10. Suzuki, S.; Hayashi, Y.; Wang, Y.; Nakamura, T.; Morita, Y.; Kawasaki, K.; Aoyama, N.; Kim, S. R.; Itoh, H.; Kuroda, Y.; Doe, W. F. Urokinase type plasminogen activator receptor expression in colorectal neoplasias. Gut 43: 798-805; 1999.
11. Ganesh, S.; Sier, C. F. M.; Heerding, M. M.; Griffioen, G.; Lamers, C. B. H.; Verspaget, H. W. Urokinase receptor and colorectal cancer survival. Lancet 344:401-402; 1994.
12. Kobayashi, H.; Ohi, H.; Shinohara, H.; Fujii, T.; Schmitt, M.; Goretzki, L.; Chucholowski, N.; Janicke, F.; Graeff, H. Saturation of tumour cell surface receptors for urokinase-type plasminogen activator by ammo-terminal fragment and subsequent effect of on reconstituted basement membrane invasion. Br. J. Cancer 67:537-544; 1993.
13. Rabbani, S. A.; Gladu, J. Urokinase receptor antibody can reduce tumor volume and detect the presence of occult tumor metastases in vivo. Cancer Res. 62:2390-2397; 2002.
14. Lakka, S. S.; Gondi, C. S.; Yanamandra, N.; Dinh, D. H.; Olivero, W. C.; Gujrati, M.; Rao, J. S. Synergistic downregulation of urokinase activator receptor and matrix metalloproteinase-9 in SNB19 glioblastoma cells efficiently inhibits glioma cell invasion, angiogenesis, and tumor growth. Cancer Res. 63:2454-2461; 2003.
15. Wilhelm, O.; Weidle, U.; Rettenberger, S.; Schmitt, M.; Graeff, H. Recombinant soluble urokinase receptor as a scavenger for urokinase-type plasminogen activator (uPA). Inhibition of proliferation and invasion of human ovarian cancer cells. FEBS Lett. 337:131-134; 1994.
16. Lund, L. R.; Romer, J.; Ellis, V.; Blasi, F.; Dano, K. Urokinase-receptor biosynthesis, mRNA levels and gene transcription are increased by transforming growth factor-b1 in human A549 lung carcinoma cells. EMBO J. 10:3399-3407; 1992.
17. Shetty, S.; Kumar, A.; Idell, S. Posttranscriptional regulation of urokinase receptor mRNA: identification of a novel urokinase receptor mRNA binding protein in human mesothelioma cells. Mol. Cell. Biol. 17:1075-1083; 1997.
18. Mahoney, T. S.; Weyrich, A. S.; Dixon, D. A.; McIntyre, T.; Prescott, S. M.; Zimmerman, G. A. Cell adhesion regulates gene expression at translational checkpoints in human myeloid leukocytes. Proc. Natl. Acad. Sci. USA 98: 10284-10289; 2001.
19. Nykjaer, A.; Conese, M.; Cremona, O.; Gliemann, J.; Blasi, F. Recycling of the urokinase receptor upon internalization of the uPA:serpin complexes. EMBO J. 16: 2610-2620; 1997.
20. Wang, H.; Skibber, J.; Juarez, J.; Boyd, D. Transcriptional activation of the urokinase receptor gene in invasive colon cancer. Int. J. Cancer 58:650-657; 1994.
21. Wang, Y.; Dang, J.; Wang, H.; Allgayer, H.; Murrell, G. A.; Boyd, D. Identification of a novel nuclear factor-kappa B sequence involved in expression of the urokinase-type plasminogen activator receptor. Eur. J. Biochem. 267:3248-3254; 2000.
22. Lengyel, E.; Wang, H.; Stepp, E.; Juarez, J.; Doe, W.; Pfarr, C. M.; Boyd, D. Requirement of an upstream AP-1 motif for the constitutive and phorbol ester-inducible expression of the urokinase-type plasminogen activator receptor gene. J. Biol. Chem. 271:23176-23184; 1996.
23. Allgayer, H.; Wang, H.; Wang, Y.; Heiss, M. M.; Bauer, R.; Nyormoi, O.; Boyd, D. D. Transactivation of the urokinase-type plasminogen activator receptor gene through a novel promoter motif bound with an activator protein-2α-related factor. J. Biol. Chem. 274:4702-4714; 1999.
24. Hapke, S.; Gawaz, M.; Dehne, K.; Kohler, J.; Marshall, J. F.; Graeff, H.; Schmitt, M.; Reuning, U.; Lengyel, E. β3A-integrin downregulates the urokinase-type plasminogen activator receptor (uPAR) through a PEA3/ets transcriptional silencing element in the uPAR promoter. Mol. Cell. Biol. 21:2118-2132; 2001.
25. Soravia, E.; Grebe, A.; De Luca, P.; Helin, K.; Suh, T. T.; Degen, J. L.; Blasi, F. A conserved TATA-less proximal promoter drives basal transcription from the urokinase-type plasminogen activator receptor gene. Blood 86:624-635; 1995.
26. Trisciuoglio, D.; Iervolino, A.; Candiloro, A.; Fibbi, G.; Fanciulli, M.; Zangemeister-Wittke, U.; Zupi, G.; Del Bufalo, D. bcl-2 induction of urokinase plasminogen activator receptor expression in human cancer cells through Sp1 activation. J. Biol. Chem. 279:6737-6745; 2004.
27. Allgayer, H.; Wang, H.; Gallick, G. E.; Crabtree, A.; Mazar, A.; Jones, T.; Kraker, A. J.; Boyd, D. D. Transcriptional induction of the urokinase receptor gene by a constitutively active Src. Requirement of an upstream motif (-152/-135) bound with Sp1. J. Biol. Chem. 274:18428-18445; 1999.
28. Wang, H.; Yang, L.; Jamaluddin, M. d. S.; Boyd, D. D. The Kruppel-like KLF4 transcription factor, a novel regulator of urokinase receptor expression, drives synthesis of this binding site in colonic crypt luminal surface epithelial cells. J. Biol. Chem. 279:22674-22683; 2004.
29. Schewe, D.; Leupold, J. H.; Boyd, D. D.; Lengyel, E.; Gruetzner, K. U.; Schildberg, F. W.; Janch, K. W.; Allgayer, H. Tumor-specific transcription factor binding to an AP-2/Sp1 promoter element of the urokinase-receptor uPAR promoter in a first large series of resected gastrointestinal cancers. Clin. Cancer Res. 9:2267-2276; 2003.
30. Mohanam, S.; Chintala, S. K.; Go, Y.; Bhattarcharya, A.; Boyd, D.; Rao, J. S. In vitro inhibition of human glioblastoma cell line invasiveness by antisense uPA receptor. Oncogene 14:1351-1359; 1997.
31. 19-31 is a potent competitive antagonist of the interaction of urokinase-type plasminogen activator with its receptor (CD87). Biol. Chem. 382:1197-1205; 2001.
32. Muehlenweg, B.; Assfalg-Machleid, I.; Parrado, S. G.; Burgle, M.; Creutzburg, S.; Schmitt, M.; Auerswald, E. A.; Machleidt, W.; Magdolen, V. A novel type of bifunctional inhibitor directed against proteolytic activity and receptor/ligand interaction. J. Biol. Chem. 275:33562-33566; 2000.
33. Schmiedeberg, N.; Schmitt, M.; Rolz, C.; Truffault, V.; Sukopp, M.; Burgle, M.; Wilhelm, O.; Schmalix, W.; Magdolen, V.; Kessler, H. Synthesis, solution structure, and biological evaluation of urokinase-type plasminogen activator (uPA)-derived receptor binding domain mimetics. J. Med. Chem. 45:4984-4994; 2002.
34. Xing, R. H.; Mazar, A.; Henkin, J.; Rabbani, S. A. Prevention of breast cancer growth, invasion and metastasis by antiestrogen tamoxifen alone or in combination with urokinase inhibitor B-428. Cancer Res. 57:3585-3593; 1997.
35. Chakrabarti, S. K.; James, J. C.; Mirmira, R. G. Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic transcription factor, Pdx1. J. Biol. Chem. 277:13286-13293; 2002.
36. Nawrocki, A. R.; Goldring, C. E.; Kostadinova, R. M.; Frey, F. J.; Frey, B. M. In vivo footprinting of the human 11β-hydroxysteroid dehydrogenase type 2 promoter. J. Biol. Chem. 277:14647-14656; 2002.
37. Martin, B.; Vaquero, A.; Priebe, W.; Portugal, J. Bisanthracycline WP631 inhibits basal and Sp1-activated transcription initiation in vitro. Nucleic Acids Res. 27:3402-3409; 1999.
38. Chaires, J. B.; Leng, F.; Przewloka, T.; Fokt, I.; Ling, Y.-H.; Perez-Soler, R.; Priebe, W. Structure-based design of a new bisintercalating anthracycline antibiotic. J. Med. Chem. 40:261-266; 1997.
39. Ibanez-Tallon, I.; Caretti, G.; Blasi, F.; Crippa, M. P. In vivo analysis of the state o the human uPA enhancer following stimulation by TPA. Oncogene 18:2836-2845; 1999.
40. Yan, C.; Wang, H.; Aggarwal, B. B.; Boyd, D. D. A novel homologous recombination system to study 92 kDa type IV collagenase transcription demonstrates that the NFkB motif drives the transition from a repressed to an activated state of gene expression. FASEB J. 18:540-541; 2004.
41. Boyd, D. D.; Wang, H.; Avila, H.; Parikh, N. U.; Kessler, H.; Magdolen, V.; Gallick, G. E. Combination of a Src kinase inhibitor with a novel pharmacological antagonist of the urokinase receptor diminishes in vitro colon cancer invasiveness. Clin. Cancer Res. 10:1544-1554; 2004.
42. Boyd, D.; Levine, A.; Brattain, D. E.; McKnight, M. K.; Brattain, M. G. Comparison of growth requirements of two human intratumoral colon carcinoma cell lines in monolayer and soft agarose. Cancer Res. 48:2469-2474; 1988.
43. Haggerty, T. J.; Zeller, K. I.; Osthus, R. C.; Wonsey, D. R.; Dang, C. V. A strategy for identifying transcription factor binding sites reveals two classes of genomic c-Myc target sites. Proc. Natl. Acad. Sci. USA 100:5313-5318; 2003.
44. Ercolani, L.; Florence, B.; Denaro, M.; Alexander, M. Isolation and complete sequence of functional human glyceraldehyde-3-phosphate dehydrogenase gene. J. Biol. Chem. 263:15335-15341; 1988.
45. Dani, C.; Piechaczyk, M.; Audigier, Y.; El Sabouty, S.; Cathala, G.; Marty, L.; Fort, P.; Blanchard, J. M.; Jeanteur, P. Characterization of the transcription products of glyceraldehyde 3-phosphate-dehydrogenase gene in HeLa cells. Eur. J. Biochem. 145:299-304; 1984.
46. Yebra, M.; Parry, G. C. N.; Stromblad, S.; Mackman, N.; Rosenberg, S.; Mueller, B. M.; Cheresh, D. A. Requirement of receptor-bound urokinase-type plasminogen activator for integrin αvβ5-directed cell migration. J. Biol. Chem. 271:29393-29399; 1996.
47. Boyd, D.; Florent, G.; Kim, P.; Brattain, M. G. Determination of the levels of urokinase and its receptor in human colon carcinoma cell lines. Cancer Res. 48:3112-3116; 1988.
48. Borgatti, M.; Lampronti, B.; Romanelli, A.; Pedone, C.; Saviano, M.; Bianchi, N.; Mischiati, C.; Gambari, R. Transcription factor decoy molecules based on a peptide nucleic acid (PNA)-DNA chimera mimicking sp1 binding sites. J. Biol. Chem. 278:7500-7509; 2003.
49. Ishibashi, H.; Nakagawa, K.; Onimaru, M.; Castellanous, E. J.; Kaneda, Y.; Nakashima, Y.; Shirasuna, K.; Sueishi, K. Sp1 decoy transfected to carcinoma cells suppresses the expression of vascular endothelial growth factor, transforming growth factor β, and tissue factor and also cell growth and invasion activities. Cancer Res. 60:6531-6536; 2000.
50. Blume, S. W.; Snyder, R. C.; Ray, R.; Thomas, S.; Koller, C. A.; Miller, D. M. 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; 1991.
51. Binaschi, M.; Bigioni, M.; Cipollone, A.; Rossi, C.; Goso, C.; Maggi, C. A.; Capranico, G.; Animati, F. Anthracyclines: Selected new developments. Curr. Med. Chem. Anticancer Agents 1:113-130; 2001.
52. Binaschi, M.; Farinosi, R.; Borgnetto, M. E.; Capranico, G. In vivo site specificity and human isoenzyme selectivity of two topoisomerase II-poisoining anthracyclines. Cancer Res. 60:3770-3776; 2000.
53. Yu, Y.; Khan, J.; Khanna, C.; Helman, L.; Meltzer, P. S.; Merlino, G. Expression profiling identifies the cytoskeletal organizer ezrin and the developmental homeoprotein Six-1 as key metastatic regulators. Nat. Med. 10:175-181; 2004.
54. Zannetti, A.; Del Vecchio, S.; Carriero, M. V.; Fonti, R.; Franco, P.; Botti, G.; D-Aiuto, G.; Stoppelli, M. P.; Salvatore, M. Coordinate up-regulation of Sp1 DNA-binding activity and urokinase receptor expression in breast carcinoma. Cancer Res. 60:1546-1551; 2000.
55. Saffer, J. D.; Jackson, S. P.; Annarella, M. B. Developmental expression of Sp1 in the mouse. Mol. Cell. Biol. 11:2189-2199; 1991.
56. Han, I.; Kudlow, J. E. Reduced glycosylation of Sp1 is associated with increased proteasome susceptibility. Mol. Cell. Biol. 17:2550-2558; 1997.
57. Minuzzo, M.; Marchini, S.; Broggini, M.; Faircloth, G.; D'Incalci, M.; Mantovani, R. Interference of transcriptional activation by the antineoplastic drug ecteinascidin-743. Proc. Natl. Acad. Sci. USA 97:6780-6784; 2000.
58. Natarajan, K.; Singh, S.; Burke, T. R.; Grunberger, D.; Aggarwal, B. B. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-κB. Proc. Natl. Acad. Sci. USA 93:9090-9095; 1996.
59. Guo, Y.; Higazi, A.; Arakelian, A.; Sachais, B. S.; Cines, D.; Goldfarb, R.; Jones, T.; Kwaan, H.; Mazar, A.; Rabbani, S. A. A peptide derived from the nonreceptor binding region of urokinase plasminogen activator (uPA) inhibits tumor progression and angiogenesis and induces tumor cell death in vivo. FASEB J. 14:1400-1410; 2000.
60. Guo, Y.; Mazar, A.; Lebrun, J.; Rabbani, S. A. An antiangiogenic urokinase-derived peptide combined with tamoxifen decreases tumor growth and metastasis in a syngenic model of breast cancer. Cancer Res. 62:4678-4684; 2002.
61. Boyd, D. D.; Kim, S. J.; Wang, H.; Jones, T. R.; Gallick, G. E. A urokinase-derived peptide (Angstrom 6) increases survival of mice bearing orthotopically grown prostate cancer and reduces lymph node metastasis. Am. J. Pathol. 162:619-626; 2003.