Sp1 transcription factor: A long-standing target in cancer chemotherapy

Pharmacology and Therapeutics

Volumn 152, Issue , 2015, Pages 111-124

  Vizcaíno, Carolina ^a   Mansilla, Sylvia ^a   Portugal, José ^a  

^a INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

Author keywords

Anticancer drugs; Prognosis; Sp1; Sp3; Targeted therapy; Transcription factors

Indexed keywords

ANTINEOPLASTIC AGENT; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SP1; SP1 PROTEIN, HUMAN;

ARTICLE; BLADDER CANCER; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CARCINOGENESIS; CELL GROWTH; CELL PROLIFERATION; COLORECTAL CANCER; DNA BINDING; DOWN REGULATION; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN TARGETING; STOMACH CANCER; ANIMAL; BINDING SITE; DRUG DELIVERY SYSTEM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASMS; PHYSIOLOGY; PROCEDURES; PROMOTER REGION;

ANIMALS; ANTINEOPLASTIC AGENTS; BINDING SITES; DRUG DELIVERY SYSTEMS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TARGETING; HUMANS; NEOPLASMS; PROMOTER REGIONS, GENETIC; SP1 TRANSCRIPTION FACTOR;

EID: 84933675531     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2015.05.008     Document Type: Review

References (180)

1. M. Abdelrahim, C.H. Baker, J.L. Abbruzzese, and S. Safe Tolfenamic acid and pancreatic cancer growth, angiogenesis, and Sp protein degradation J Natl Cancer Inst 98 2006 855 868
2. M. Abdelrahim, and S. Safe Cyclooxygenase-2 inhibitors decrease vascular endothelial growth factor expression in colon cancer cells by enhanced degradation of Sp1 and Sp4 proteins Mol Pharmacol 68 2005 317 329
3. M. Abdelrahim, R. Smith 3rd, R. Burghardt, and S. Safe Role of Sp proteins in regulation of vascular endothelial growth factor expression and proliferation of pancreatic cancer cells Cancer Res 64 2004 6740 6749
4. V. Albertini, A. Jain, S. Vignati, S. Napoli, A. Rinaldi, and I. Kwee Novel GC-rich DNA-binding compound produced by a genetically engineered mutant of the mithramycin producer Streptomyces argillaceus exhibits improved transcriptional repressor activity: implications for cancer therapy Nucleic Acids Res 34 2006 1721 1734
5. S. Ammanamanchi, J.W. Freeman, and M.G. Brattain Acetylated Sp3 is a transcriptional activator J Biol Chem 278 2003 35775 35780
6. J.C. Azizkhan, D.E. Jensen, A.J. Pierce, and M. Wade Transcription from TATA-less promoters: dihydrofolate reductase as a model Crit Rev Eukaryot Gene Expr 3 1993 229 254
7. F. Barceló, M. Ortiz-Lombardía, M. Martorell, M. Oliver, C. Méndez, and J.A. Salas DNA binding characteristics of mithramycin and chromomycin analogues obtained by combinatorial biosynthesis Biochemistry 49 2010 10543 10552
8. F. Barceló, C. Scotta, M. Ortiz-Lombardía, C. Méndez, J.A. Salas, and J. Portugal Entropically-driven binding of mithramycin in the minor groove of C/G-rich DNA sequences Nucleic Acids Res 35 2007 2215 2226
9. R. Basha, S.B. Ingersoll, U.T. Sankpal, S. Ahmad, C.H. Baker, and J.R. Edwards Tolfenamic acid inhibits ovarian cancer cell growth and decreases the expression of c-Met and survivin through suppressing specificity protein transcription factors Gynecol Oncol 122 2011 163 170
10. M. Bataller, C. Méndez, J.A. Salas, and J. Portugal Mithramycin SK modulates polyploidy and cell death in colon carcinoma cells Mol Cancer Ther 7 2008 2988 2997
11. R.G. Bedolla, J. Gong, T.J. Prihoda, I.T. Yeh, I.M. Thompson, and R. Ghosh Predictive value of Sp1/Sp3/FLIP signature for prostate cancer recurrence PLoS One 7 2012 e44917
12. K. Beishline, and J. Azizkhan-Clifford Sp1 and the 'hallmarks of cancer' FEBS J 282 2015 224 258
13. A.R. Black, D. Jensen, S.Y. Lin, and J.C. Azizkhan Growth/Cell cycle regulation of Sp1 phosphorylation J Biol Chem 274 1999 1207 1215
14. L.M. Botella, T. Sánchez-Elsner, C. Rius, A. Corbi, and C. Bernabéu Identification of a critical Sp1 site within the endoglin promoter and its involvement in the transforming growth factor-β stimulation J Biol Chem 276 2001 34486 34494
15. G. Bretones, M.D. Delgado, and J. León Myc and cell cycle control Biochim Biophys Acta 1849 2015 506 516
16. M.J. Bywater, R.B. Pearson, G.A. McArthur, and R.D. Hannan Dysregulation of the basal RNA polymerase transcription apparatus in cancer Nat Rev Cancer 13 2013 299 314
17. G. Chadalapaka, I. Jutooru, S. Chintharlapalli, S. Papineni, R. Smith 3rd, and X. Li Curcumin decreases specificity protein expression in bladder cancer cells Cancer Res 68 2008 5345 5354
18. G. Chadalapaka, I. Jutooru, S. Sreevalsan, S. Pathi, K. Kim, and C. Chen Inhibition of rhabdomyosarcoma cell and tumor growth by targeting specificity protein (Sp) transcription factors Int J Cancer 132 2013 795 806
19. J.B. Chaires, J.E. Herrera, and M.J. Waring Preferential binding of daunomycin to 5′ATCG and 5′ATGC sequences revealed by footprinting titration experiments Biochemistry 29 1990 6145 6153
20. J.B. Chaires, F.F. Leng, T. Przewloka, I. Fokt, Y.H. Ling, and R. Perez-Soler Structure-based design of a new bisintercalating anthracycline antibiotic J Med Chem 40 1997 261 266
21. S.Y. Chiang, J.C. Azizkhan, and T.A. Beerman A comparison of DNA-binding drugs as inhibitors of E2F1- and Sp1-DNA complexes and associated gene expression Biochemistry 37 1998 3109 3115
22. S. Chintharlapalli, S. Papineni, S.O. Lee, P. Lei, U.H. Jin, and S.I. Sherman Inhibition of pituitary tumor-transforming gene-1 in thyroid cancer cells by drugs that decrease specificity proteins Mol Carcinog 50 2011 655 667
23. S. Chintharlapalli, S. Papineni, P. Lei, S. Pathi, and S. Safe Betulinic acid inhibits colon cancer cell and tumor growth and induces proteasome-dependent and -independent downregulation of specificity proteins (Sp) transcription factors BMC Cancer 11 2011 371
24. S. Chintharlapalli, S. Papineni, S.K. Ramaiah, and S. Safe Betulinic acid inhibits prostate cancer growth through inhibition of specificity protein transcription factors Cancer Res 67 2007 2816 2823
25. E.S. Choi, J.S. Nam, J.Y. Jung, N.P. Cho, and S.D. Cho Modulation of specificity protein 1 by mithramycin A as a novel therapeutic strategy for cervical cancer Sci Rep 4 2014 7162
26. S. Chu Transcriptional regulation by post-transcriptional modification - role of phosphorylation in Sp1 transcriptional activity Gene 508 2012 1 8
27. J. Colon, M.R. Basha, R. Madero-Visbal, S. Konduri, C.H. Baker, and L.J. Herrera Tolfenamic acid decreases c-Met expression through Sp proteins degradation and inhibits lung cancer cells growth and tumor formation in orthotopic mice Invest New Drugs 29 2011 41 51
28. A.J. Courey, D.A. Holtzman, S.P. Jackson, and R. Tjian Synergistic activation by the glutamine-rich domains of human transcription factor Sp1 Cell 59 1989 827 836
29. A.P. Crijns, R.S. Fehrmann, S. de Jong, F. Gerbens, G.J. Meersma, and H.G. Klip Survival-related profile, pathways, and transcription factors in ovarian cancer PLoS Med 6 2009 e1000024
30. M. Dalvai, O. Mondesert, B. Bugler, S. Manenti, B. Ducommun, and C. Dozier Doxorubicin promotes transcriptional upregulation of Cdc25B in cancer cells by releasing Sp1 from the promoter Oncogene 32 2013 5123 5128
31. K. Deacon, D. Onion, R. Kumari, S.A. Watson, and A.J. Knox 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 J Biol Chem 287 2012 39967 39981
32. E. Deniaud, J. Baguet, R. Chalard, B. Blanquier, L. Brinza, and J. Meunier Overexpression of transcription factor Sp1 leads to gene expression perturbations and cell cycle inhibition PLoS One 4 2009 e7035
33. E. Deniaud, J. Baguet, A.L. Mathieu, G. Pages, J. Marvel, and Y. Leverrier Overexpression of Sp1 transcription factor induces apoptosis Oncogene 25 2006 7096 7105
34. M. D'Incalci, D. Brunelli, E. Marangon, M. Simone, M. Tavecchio, and A. Gescher Modulation of gene transcription by natural products - a viable anticancer strategy Curr Pharm Des 13 2007 2744 2750
35. A. Doetzlhofer, H. Rotheneder, G. Lagger, M. Koranda, V. Kurtev, and G. Brosch Histone deacetylase 1 can repress transcription by binding to Sp1 Mol Cell Biol 19 1999 5504 5511
36. K. Essafi-Benkhadir, S. Grosso, A. Puissant, G. Robert, M. Essafi, and M. Deckert Dual role of Sp3 transcription factor as an inducer of apoptosis and a marker of tumour aggressiveness PLoS One 4 2009 e4478
37. P.O. Estève, H.G. Chin, and S. Pradhan Molecular mechanisms of transactivation and doxorubicin-mediated repression of survivin gene in cancer cells J Biol Chem 282 2007 2615 2625
38. C. Fandos, M. Sánchez-Feutrie, T. Santalucía, F. Viñals, J. Cadefau, and A. Gumà GLUT1 glucose transporter gene transcription is repressed by Sp3. Evidence for a regulatory role of Sp3 during myogenesis J Mol Biol 294 1999 103 119
39. X.H. Feng, X. Lin, and R. Derynck Smad2, Smad3 and Smad4 cooperate with Sp1 to induce p15(Ink4B) transcription in response to TGF-β EMBO J 19 2000 5178 5193
40. A. Fernández-Guizán, S. Mansilla, F. Barceló, C. Vizcaíno, L.E. Núñez, and F. Morís The activity of a novel mithramycin analog is related to its binding to DNA, cellular accumulation, and inhibition of Sp1-driven gene transcription Chem Biol Interact 219 2014 123 132
41. K.A. Fitzgerald, J.C. Evans, J. McCarthy, J. Guo, M. Prencipe, and M. Kearney The role of transcription factors in prostate cancer and potential for future RNA interference therapy Expert Opin Ther Targets 18 2014 633 649
42. P. Fojas-de-Borja, N.K. Collins, P. Du, J. Azizkhan-Clifford, and M. Mudryj Cyclin A-CDK phosphorylates Sp1 and enhances Sp1-mediated transcription EMBO J 20 2001 5737 5747
43. D.A. Frank Targeting transcription factors for cancer therapy IDrugs 12 2009 29 33
44. C.A. Frederick, L.D. Williams, G. Ughetto, G.A. van der Marel, J.H. van Boom, and A. Rich Structural comparison of anticancer drug-DNA complexes: adriamycin and daunomycin Biochemistry 29 1990 2538 2549
45. M. Fulciniti, S. Amin, P. Nanjappa, S. Rodig, R. Prabhala, and C. Li Significant biological role of Sp1 transactivation in multiple myeloma Clin Cancer Res 17 2011 6500 6509
46. A. Gajek, M. Denel, B. Bukowska, A. Rogalska, and A. Marczak Pro-apoptotic activity of new analog of anthracyclines - WP631 in advanced ovarian cancer cell line Toxicol In Vitro 28 2014 273 281
47. Y. Gao, Z. Jia, X. Kong, Q. Li, D.Z. Chang, and D. Wei Combining betulinic acid and mithramycin a effectively suppresses pancreatic cancer by inhibiting proliferation, invasion, and angiogenesis Cancer Res 71 2011 5182 5193
48. J. Gilmour, S.A. Assi, U. Jaegle, D. Kulu, H. van de Werken, and D. Clarke A crucial role for the ubiquitously expressed transcription factor Sp1 at early stages of hematopoietic specification Development 141 2014 2391 2401
49. M. Gniazdowski, W.A. Denny, S.M. Nelson, and M. Czyz Effects of anticancer drugs on transcription factor-DNA interactions Expert Opin Ther Targets 9 2005 471 489
50. H. Göllner, C. Dani, B. Phillips, S. Philipsen, and G. Suske Impaired ossification in mice lacking the transcription factor Sp3 Mech Dev 106 2001 77 83
51. P.J. Grohar, and L.J. Helman Prospects and challenges for the development of new therapies for Ewing sarcoma Pharmacol Ther 137 2013 216 224
52. H. Guan, J. Cai, N. Zhang, J. Wu, J. Yuan, and J. Li Sp1 is upregulated in human glioma, promotes MMP-2-mediated cell invasion and predicts poor clinical outcome Int J Cancer 130 2012 593 601
53. N.P. Gullett, A.R. Ruhul Amin, S. Bayraktar, J.M. Pezzuto, D.M. Shin, and F.R. Khuri Cancer prevention with natural compounds Semin Oncol 37 2010 258 281
54. G. Hagen, S. Muller, M. Beato, and G. Suske Cloning by recognition site screening of two novel GT box binding proteins: a family of Sp1 related genes Nucleic Acids Res 20 1992 5519 5525
55. H. Hagiwara, M. Iyo, and K. Hashimoto Mithramycin protects against dopaminergic neurotoxicity in the mouse brain after administration of methamphetamine Brain Res 1301 2009 189 196
56. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
57. S. He, and J.R. Davie Sp1 and Sp3 foci distribution throughout mitosis J Cell Sci 119 2006 1063 1070
58. B.T. Hennessy, R.L. Coleman, and M. Markman Ovarian cancer Lancet 374 2009 1371 1382
59. H. Honda, M.J. Pazin, H. Ji, R.P. Wernyj, and P.J. Morin Crucial roles of Sp1 and epigenetic modifications in the regulation of the CLDN4 promoter in ovarian cancer cells J Biol Chem 281 2006 21433 21444
60. C. Hong, H.A. Kim, G.L. Firestone, and L.F. Bjeldanes 3,3′-Diindolylmethane (DIM) induces a G(1) cell cycle arrest in human breast cancer cells that is accompanied by Sp1-mediated activation of p21(WAF1/CIP1) expression Carcinogenesis 23 2002 1297 1305
61. T.I. Hsu, M.C. Wang, S.Y. Chen, Y.M. Yeh, W.C. Su, and W.C. Chang Sp1 expression regulates lung tumor progression Oncogene 31 2012 3973 3988
62. L.H. Hurley DNA and its associated processes as targets for cancer therapy Nat Rev Cancer 2 2002 188 200
63. H. Ishibashi, K. Nakagawa, M. Onimaru, E.J. Castellanous, Y. Kaneda, and Y. Nakashima Sp1 decoy transfected to carcinoma cells suppresses the expression of vascular endothelial growth factor, transforming growth factor β1, and tissue factor and also cell growth and invasion activities Cancer Res 60 2000 6531 6536
64. Z. Jia, Y. Gao, L. Wang, Q. Li, J. Zhang, and X. Le Combined treatment of pancreatic cancer with mithramycin A and tolfenamic acid promotes Sp1 degradation and synergistic antitumor activity Cancer Res 70 2010 1111 1119
65. Z. Jia, J. Zhang, D. Wei, L. Wang, P. Yuan, and X. Le Molecular basis of the synergistic antiangiogenic activity of bevacizumab and mithramycin A Cancer Res 67 2007 4878 4885
66. Y. Jiang, L. Wang, W. Gong, D. Wei, X. Le, and J. Yao A high expression level of insulin-like growth factor I receptor is associated with increased expression of transcription factor Sp1 and regional lymph node metastasis of human gastric cancer Clin Exp Metastasis 21 2004 755 764
67. N.Y. Jiang, B.A. Woda, B.F. Banner, G.F. Whalen, K.A. Dresser, and D. Lu Sp1, a new biomarker that identifies a subset of aggressive pancreatic ductal adenocarcinoma Cancer Epidemiol Biomarkers Prev 17 2008 1648 1652
68. I. Jutooru, G. Chadalapaka, M. Abdelrahim, M.R. Basha, I. Samudio, and M. Konopleva Methyl 2-cyano-3,12-dioxooleana-1,9-dien-28-oate decreases specificity protein transcription factors and inhibits pancreatic tumor growth: role of microRNA-27a Mol Pharmacol 78 2010 226 236
69. I. Jutooru, G. Chadalapaka, P. Lei, and S. Safe Inhibition of NFκB and pancreatic cancer cell and tumor growth by curcumin is dependent on specificity protein down-regulation J Biol Chem 285 2010 25332 25344
70. I. Jutooru, G. Chadalapaka, S. Sreevalsan, P. Lei, R. Barhoumi, and R. Burghardt Arsenic trioxide downregulates specificity protein (Sp) transcription factors and inhibits bladder cancer cell and tumor growth Exp Cell Res 316 2010 2174 2188
71. I. Jutooru, A.S. Guthrie, G. Chadalapaka, S. Pathi, K. Kim, and R. Burghardt Mechanism of action of phenethylisothiocyanate and other reactive oxygen species-inducing anticancer agents Mol Cell Biol 34 2014 2382 2395
72. J.T. Kadonaga, K.A. Jones, and R. Tjian Promoter-specific activation of RNA polymerase II transcription by Sp1 Trends Biochem Sci 11 1986 20 23
73. S.B. Kennett, A.J. Udvadia, and J.M. Horowitz Sp3 encodes multiple proteins that differ in their capacity to stimulate or repress transcription Nucleic Acids Res 25 1997 3110 3117
74. K. Kim, G. Chadalapaka, S.O. Lee, D. Yamada, X. Sastre-Garau, and P.A. Defossez Identification of oncogenic microRNA-17-92/ZBTB4/specificity protein axis in breast cancer Oncogene 31 2012 1034 1044
75. M.K. Kim, J.S. Lee, and J.H. Chung In vivo transcription factor recruitment during thyroid hormone receptor-mediated activation Proc Natl Acad Sci U S A 96 1999 10092 10097
76. P.D. King, and M.C. Perry Hepatotoxicity of chemotherapy Oncologist 6 2001 162 176
77. L.M. Kong, C.G. Liao, F. Fei, X. Guo, J.L. Xing, and Z.N. Chen Transcription factor Sp1 regulates expression of cancer-associated molecule CD147 in human lung cancer Cancer Sci 101 2010 1463 1470
78. G. Koutsodontis, and D. Kardassis Inhibition of p53-mediated transcriptional responses by mithramycin A Oncogene 23 2004 9190 9200
79. G. Koutsodontis, A. Moustakas, and D. Kardassis The role of Sp1 family members, the proximal GC-rich motifs, and the upstream enhancer region in the regulation of the human cell cycle inhibitor p21WAF-1/Cip1 gene promoter Biochemistry 41 2002 12771 12784
80. I. Krüger, M. Vollmer, D.G. Simmons, H.P. Elsasser, S. Philipsen, and G. Suske Sp1/Sp3 compound heterozygous mice are not viable: impaired erythropoiesis and severe placental defects Dev Dyn 236 2007 2235 2244
81. T.J. Lee, E.M. Jung, J.T. Lee, S. Kim, J.W. Park, and K.S. Choi Mithramycin A sensitizes cancer cells to TRAIL-mediated apoptosis by down-regulation of XIAP gene promoter through Sp1 sites Mol Cancer Ther 5 2006 2737 2746
82. W.R. Lee, K.H. Kim, H.J. An, Y.Y. Park, K.S. Kim, and C.K. Lee Effects of chimeric decoy oligodeoxynucleotide in the regulation of transcription factors NF-kB and Sp1 in an animal model of atherosclerosis Basic Clin Pharmacol Toxicol 112 2013 236 243
83. W.S. Lee, J. Kwon, D.H. Yun, Y.N. Lee, E.Y. Woo, and M.J. Park Specificity protein 1 expression contributes to Bcl-w-induced aggressiveness in glioblastoma multiforme Mol Cells 37 2014 17 23
84. K.A. Lee, Y.J. Lee, J.O. Ban, Y.J. Lee, S.H. Lee, and M.K. Cho The flavonoid resveratrol suppresses growth of human malignant pleural mesothelioma cells through direct inhibition of specificity protein 1 Int J Mol Med 30 2012 21 27
85. K. Lee, D.Z. Qian, S. Rey, H. Wei, J.O. Liu, and G.L. Semenza Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells Proc Natl Acad Sci U S A 106 2009 2353 2358
86. B. Lemon, and R. Tjian Orchestrated response: a symphony of transcription factors for gene control Genes Dev 14 2000 2551 2569
87. F. Leng, W. Priebe, and J.B. Chaires Ultratight DNA binding of a new bisintercalating anthracycline antibiotic Biochemistry 37 1998 1743 1753
88. J. Letovsky, and W.S. Dynan Measurement of the binding of transcription factor Sp1 to a single GC box recognition sequence Nucleic Acids Res 17 1989 2639 2653
89. L. Li, and J.R. Davie The role of Sp1 and Sp3 in normal and cancer cell biology Ann Anat 192 2010 275 283
90. L. Li, P. Gao, Y. Li, Y. Shen, J. Xie, and D. Sun JMJD2A-dependent silencing of Sp1 in advanced breast cancer promotes metastasis by downregulation of DIRAS3 Breast Cancer Res Treat 147 2014 487 500
91. L. Li, S. He, J.M. Sun, and J.R. Davie Gene regulation by Sp1 and Sp3 Biochem Cell Biol 82 2004 460 471
92. H. Li, Y. Zhang, A. Strose, D. Tedesco, K. Gurova, and G. Selivanova Integrated high-throughput analysis identifies Sp1 as a crucial determinant of p53-mediated apoptosis Cell Death Differ 21 2014 1493 1502
93. A. López-Soto, A. Quiñones-Lombrana, R. López-Arbesu, C. López-Larrea, and S. González Transcriptional regulation of ULBP1, a human ligand of the NKG2D receptor J Biol Chem 281 2006 30419 30430
94. Z. Lou, S. O'Reilly, H. Liang, V.M. Maher, S.D. Sleight, and J.J. McCormick Down-regulation of overexpressed Sp1 protein in human fibrosarcoma cell lines inhibits tumor formation Cancer Res 65 2005 1007 1017
95. K.L. MacQuarrie, A.P. Fong, R.H. Morse, and S.J. Tapscott Genome-wide transcription factor binding: beyond direct target regulation Trends Genet 27 2011 141 148
96. B. Majello, P. De Luca, G. Suske, and L. Lania Differential transcriptional regulation of c-myc promoter through the same DNA binding sites targeted by Sp1-like proteins Oncogene 10 1995 1841 1848
97. A. Malek, L.E. Núñez, M. Magistri, L. Brambilla, S. Jovic, and G.M. Carbone Modulation of the activity of Sp transcription factors by mithramycin analogues as a new strategy for treatment of metastatic prostate cancer PLoS One 7 2012 e35130
98. U. Manne, R.G. Srivastava, and S. Srivastava Recent advances in biomarkers for cancer diagnosis and treatment Drug Discov Today 10 2005 965 976
99. S. Mansilla, and J. Portugal Sp1 transcription factor as a target for anthracyclines: effects on gene transcription Biochimie 90 2008 976 987
100. S. Mansilla, W. Priebe, and J. Portugal Sp1-targeted inhibition of gene transcription by WP631 in transfected lymphocytes Biochemistry 43 2004 7584 7592
101. S. Mansilla, W. Priebe, and J. Portugal Mitotic catastrophe results in cell death by caspase-dependent and caspase-independent mechanisms Cell Cycle 5 2006 53 60
102. S. Mansilla, W. Priebe, and J. Portugal Transcriptional changes facilitate mitotic catastrophe in tumour cells that contain functional p53 Eur J Pharmacol 540 2006 34 45
103. S. Mansilla, W. Priebe, and J. Portugal Changes in gene expression induced by Sp1 knockdown differ from those caused by challenging Sp1 binding to gene promoters Biochim Biophys Acta 1809 2011 327 336
104. S. Mansilla, M. Rojas, M. Bataller, W. Priebe, and J. Portugal Circumvention of the multidrug-resistance protein (MRP-1) by an antitumor drug through specific inhibition of gene transcription in breast tumor cells Biochem Pharmacol 73 2007 934 942
105. M. Marin, A. Karis, P. Visser, F. Grosveld, and S. Philipsen Transcription factor Sp1 is essential for early embryonic development but dispensable for cell growth and differentiation Cell 89 1997 619 628
106. B. Martín, A. Vaquero, W. Priebe, and J. Portugal Bisanthracycline WP631 inhibits basal and Sp1-activated transcription initiation in vitro Nucleic Acids Res 27 1999 3402 3409
107. S.U. Mertens-Talcott, S. Chintharlapalli, X. Li, and S. Safe The oncogenic microRNA-27a targets genes that regulate specificity protein transcription factors and the G2-M checkpoint in MDA-MB-231 breast cancer cells Cancer Res 67 2007 11001 11011
108. G. Minotti, P. Menna, E. Salvatorelli, G. Cairo, and L. Gianni Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity Pharmacol Rev 56 2004 185 229
109. M. Minuzzo, S. Marchini, M. Broggini, G. Faircloth, M. D'Incalci, and R. Mantovani Interference of transcriptional activation by the antineoplastic drug ecteinascidin-743 Proc Natl Acad Sci U S A 97 2000 6780 6784
110. K. Miyata, F. Yotsumoto, S.O. Nam, T. Odawara, S. Manabe, and T. Ishikawa Contribution of transcription factor, Sp1, to the promotion of HB-EGF expression in defense mechanism against the treatment of irinotecan in ovarian clear cell carcinoma Cancer Med 3 2014 1159 1169
111. M. Mobahat, A. Narendran, and K. Riabowol Survivin as a preferential target for cancer therapy Int J Mol Sci 15 2014 2494 2516
112. K.S. Moorefield, H. Yin, T.D. Nichols, C. Cathcart, S.O. Simmons, and J.M. Horowitz Sp2 localizes to subnuclear foci associated with the nuclear matrix Mol Biol Cell 17 2006 1711 1722
113. D. Mottet, S. Pirotte, V. Lamour, M. Hagedorn, S. Javerzat, and A. Bikfalvi HDAC4 represses p21(WAF1/Cip1) expression in human cancer cells through a Sp1-dependent, p53-independent mechanism Oncogene 28 2009 243 256
114. V. Nair, S. Pathi, I. Jutooru, S. Sreevalsan, R. Basha, and M. Abdelrahim Metformin inhibits pancreatic cancer cell and tumor growth and downregulates Sp transcription factors Carcinogenesis 34 2013 2870 2879
115. V. Nair, S. Sreevalsan, R. Basha, M. Abdelrahim, A. Abudayyeh, and A. Rodrigues Hoffman Mechanism of metformin-dependent inhibition of mammalian target of rapamycin (mTOR) and Ras activity in pancreatic cancer: role of specificity protein (Sp) transcription factors J Biol Chem 289 2014 27692 27701
116. M. Nicolás, V. Noé, and C.J. Ciudad Transcriptional regulation of the human Sp1 gene promoter by the specificity protein (Sp) family members nuclear factor Y (NF-Y) and E2F Biochem J 371 2003 265 275
117. F. Nikulenkov, C. Spinnler, H. Li, C. Tonelli, Y. Shi, and M. Turunen Insights into p53 transcriptional function via genome-wide chromatin occupancy and gene expression analysis Cell Death Differ 19 2012 1992 2002
118. V. Noé, C. Alemany, L.A. Chasin, and C.J. Ciudad Retinoblastoma protein associates with Sp1 and activates the hamster dihydrofolate reductase promoter Oncogene 16 1998 1931 1938
119. G.D. Noratto, I. Jutooru, S. Safe, G. Angel-Morales, and S.U. Mertens-Talcott The drug resistance suppression induced by curcuminoids in colon cancer SW-480 cells is mediated by reactive oxygen species-induced disruption of the microRNA-27a-ZBTB10-Sp axis Mol Nutr Food Res 57 2013 1638 1648
120. L.E. Núñez, S.E. Nybo, J. González-Sabín, M. Pérez, N. Menéndez, and A.F. Braña A novel mithramycin analogue with high antitumor activity and less toxicity generated by combinatorial biosynthesis J Med Chem 55 2012 5813 5825
121. M. Oeggerli, Y. Tian, C. Ruiz, B. Wijker, G. Sauter, and E. Obermann Role of KCNMA1 in breast cancer PLoS One 7 2012 e41664
122. G. O'Sullivan-Coyne, G.C. O'Sullivan, T.R. O'Donovan, K. Piwocka, and S.L. McKenna Curcumin induces apoptosis-independent death in oesophageal cancer cells Br J Cancer 101 2009 1585 1595
123. S. Papineni, S. Chintharlapalli, M. Abdelrahim, S.O. Lee, R. Burghardt, and A. Abudayyeh Tolfenamic acid inhibits esophageal cancer through repression of specificity proteins and c-Met Carcinogenesis 30 2009 1193 1201
124. J.H. Park, D.C. McMillan, P.G. Horgan, and C.S. Roxburgh The impact of anti-inflammatory agents on the outcome of patients with colorectal cancer Cancer Treat Rev 40 2014 68 77
125. S. Pathi, I. Jutooru, G. Chadalapaka, V. Nair, S.O. Lee, and S. Safe Aspirin inhibits colon cancer cell and tumor growth and downregulates specificity protein (Sp) transcription factors PLoS One 7 2012 e48208
126. F.J. Piedrafita, and M. Pfahl Retinoid-induced apoptosis and Sp1 cleavage occur independently of transcription and require caspase activation Mol Cell Biol 17 1997 6348 6358
127. J. Portugal, S. Mansilla, C. Vizcaíno, and F. Barceló Promoter-specific transcriptional interference by DNA-binding drugs In Recent Research Developments in Biochemistry Vol. 8 2011 Research Signpost Kerala 45 63
128. J. Portugal, B. Martín, A. Vaquero, N. Ferrer, S. Villamarín, and W. Priebe Analysis of the effects of daunorubicin and WP631 on transcription Curr Med Chem 8 2001 1 8
129. S. Previdi, A. Malek, V. Albertini, C. Riva, C. Capella, and M. Broggini Inhibition of Sp1-dependent transcription and antitumor activity of the new aureolic acid analogues mithramycin SDK and SK in human ovarian cancer xenografts Gynecol Oncol 118 2010 182 188
130. W. Priebe, I. Fokt, T. Przewloka, J.B. Chaires, J. Portugal, and J.O. Trent Exploiting anthracycline scaffold for designing DNA-targeting agents Methods Enzymol 340 2001 529 555
131. B.F. Pugh, and R. Tjian Mechanism of transcriptional activation by Sp1: evidence for coactivators Cell 61 1990 1187 1197
132. R.G. Roeder The eukaryotic transcriptional machinery: complexities and mechanisms unforeseen Nat Med 9 2003 1239 1244
133. S. Safe, and M. Abdelrahim Sp transcription factor family and its role in cancer Eur J Cancer 41 2005 2438 2448
134. S. Safe, P. Imanirad, S. Sreevalsan, V. Nair, and I. Jutooru Transcription factor Sp1, also known as specificity protein 1 as a therapeutic target Expert Opin Ther Targets 18 2014 759 769
135. S. Saha, S. Mukherjee, M. Mazumdar, A. Manna, P. Khan, and A. Adhikary Mithramycin A sensitizes therapy-resistant breast cancer stem cells toward genotoxic drug doxorubicin Transl Res 165 2015 558 577
136. U.T. Sankpal, S. Goodison, M. Abdelrahim, and R. Basha Targeting Sp1 transcription factors in prostate cancer therapy Med Chem 7 2011 518 525
137. U.T. Sankpal, C.M. Lee, S.F. Connelly, O. Kayaleh, D. Eslin, and R. Sutphin Cellular and organismal toxicity of the anti-cancer small molecule, tolfenamic acid: a pre-clinical evaluation Cell Physiol Biochem 32 2013 675 686
138. U.T. Sankpal, P. Maliakal, D. Bose, O. Kayaleh, D. Buchholz, and R. Basha Expression of specificity protein transcription factors in pancreatic cancer and their association in prognosis and therapy Curr Med Chem 19 2012 3779 3786
139. T.J. Shaw, E.C. Lacasse, J.P. Durkin, and B.C. Vanderhyden Downregulation of XIAP expression in ovarian cancer cells induces cell death in vitro and in vivo Int J Cancer 122 2008 (1430-1034)
140. C.J. Sherr, and J.M. Roberts CDK inhibitors: positive and negative regulators of G1-phase progression Genes Dev 13 1999 1501 1512
141. R.L. Siegel, K.D. Miller, and A. Jemal Cancer statistics, 2015 CA Cancer J Clin 65 2015 5 29
142. S.F. Sleiman, B.C. Langley, M. Basso, J. Berlin, L. Xia, and J.B. Payappilly Mithramycin is a gene-selective Sp1 Inhibitor that identifies a biological intersection between cancer and neurodegeneration J Neurosci 31 2011 6858 6870
143. R.C. Snyder, R. Ray, S. Blume, and D.M. Miller Mithramycin blocks transcriptional initiation of the c-myc P1 and P2 promoters Biochemistry 30 1991 4290 4297
144. E. Sorianello, F.X. Soriano, S. Fernández-Pascual, A. Sancho, D. Naon, and M. Vila-Caballer The promoter activity of human Mfn2 depends on Sp1 in vascular smooth muscle cells Cardiovasc Res 94 2012 38 47
145. S. Sreevalsan, and S. Safe The cannabinoid WIN 55,212-2 decreases specificity protein transcription factors and the oncogenic cap protein eIF4E in colon cancer cells Mol Cancer Ther 12 2013 2483 2493
146. C. Stevens, L. Smith, and N.B. La Thangue Chk2 activates E2F-1 in response to DNA damage Nat Cell Biol 5 2003 401 409
147. G. Suske The Sp-family of transcription factors Gene 238 1999 291 300
148. R.M. Sutphin, S.F. Connelly, C.M. Lee, U.T. Sankpal, D. Eslin, and M. Khan Anti-leukemic response of a NSAID, tolfenamic acid Target Oncol 9 2014 135 144
149. A. Tapias, C.J. Ciudad, I.B. Roninson, and V. Noé Regulation of Sp1 by cell cycle related proteins Cell Cycle 7 2008 2856 2867
150. G. Terrados, F. Finkernagel, B. Stielow, D. Sadic, J. Neubert, and O. Herdt Genome-wide localization and expression profiling establish Sp2 as a sequence-specific transcription factor regulating vitally important genes Nucleic Acids Res 40 2012 7844 7857
151. L. Tora, and H.T. Timmers The TATA box regulates TATA-binding protein (TBP) dynamics in vivo Trends Biochem Sci 35 2010 309 314
152. L.A. Torre, F. Bray, R.L. Siegel, J. Ferlay, J. Lortet-Tieulent, and A. Jemal Global cancer statistics, 2012 CA Cancer J Clin 65 2015 87 108
153. A. Vaquero, and J. Portugal Modulation of DNA-protein interactions in the P1 and P2 c-myc promoters by two intercalating drugs Eur J Biochem 251 1998 435 442
154. C. Vizcaíno, S. Mansilla, L.E. Núñez, C. Méndez, J.A. Salas, and F. Morís Novel mithramycins abrogate the involvement of protein factors in the transcription of cell cycle control genes Biochem Pharmacol 84 2012 1133 1142
155. C. Vizcaíno, L.E. Nuñez, F. Morís, and J. Portugal Genome-wide modulation of gene transcription in ovarian carcinoma cells by a new mithramycin analogue PLoS One 9 2014 e104687
156. Y.T. Wang, J.Y. Chuang, M.R. Shen, W.B. Yang, W.C. Chang, and J.J. Hung Sumoylation of specificity protein 1 augments its degradation by changing the localization and increasing the specificity protein 1 proteolytic process J Mol Biol 380 2008 869 885
157. L. Wang, X. Guan, J. Zhang, Z. Jia, D. Wei, and Q. Li Targeted inhibition of Sp1-mediated transcription for antiangiogenic therapy of metastatic human gastric cancer in orthotopic nude mouse models Int J Oncol 33 2008 161 167
158. B.S. Wang, Z. Liu, S.L. Sun, and Y. Zhao Identification of genes and candidate agents associated with pancreatic cancer Tumour Biol 35 2014 81 88
159. X.B. Wang, W.Q. Peng, Z.J. Yi, S.L. Zhu, and Q.H. Gan Expression and prognostic value of transcriptional factor sp1 in breast cancer Ai Zheng 26 2007 996 1000
160. L. Wang, D. Wei, S. Huang, Z. Peng, X. Le, and T.T. Wu Transcription factor Sp1 expression is a significant predictor of survival in human gastric cancer Clin Cancer Res 9 2003 6371 6380
161. I. Wierstra Sp1: emerging roles - beyond constitutive activation of TATA-less housekeeping genes Biochem Biophys Res Commun 372 2008 1 13
162. C. Wright, B. Angus, J. Napier, M. Wetherall, Y. Udagawa, and J.R. Sainsbury Prognostic factors in breast cancer: immunohistochemical staining for SP1 and NCRC 11 related to survival, tumour epidermal growth factor receptor and oestrogen receptor status J Pathol 153 1987 325 331
163. J. Wu, X. Ling, D. Pan, P. Apontes, L. Song, and P. Liang Molecular mechanism of inhibition of survivin transcription by the GC-rich sequence-selective DNA binding antitumor agent, hedamycin: evidence of survivin down-regulation associated with drug sensitivity J Biol Chem 280 2005 9745 9751
164. Q. Xu, M. Liu, N. Xu, and H. Zhu Variation in Sp1 binding sites correlates with expression of survivin in breast cancer Mol Med Rep 10 2014 1395 1399
165. R. Xu, P. Zhang, J. Huang, S. Ge, J. Lu, and G. Qian Sp1 and Sp3 regulate basal transcription of the survivin gene Biochem Biophys Res Commun 356 2007 286 292
166. C. Yan, and P.J. Higgins Drugging the undruggable: transcription therapy for cancer Biochim Biophys Acta 1835 2013 76 85
167. W.S. Yang, G. Chadalapaka, S.G. Cho, S.O. Lee, U.H. Jin, and I. Jutooru The transcriptional repressor ZBTB4 regulates EZH2 through a MicroRNA-ZBTB4-specificity protein signaling axis Neoplasia 16 2014 1059 1069
168. H.C. Yang, J.Y. Chuang, W.Y. Jeng, C.I. Liu, A.H. Wang, and P.J. Lu Pin1-mediated Sp1 phosphorylation by CDK1 increases Sp1 stability and decreases its DNA-binding activity during mitosis Nucleic Acids Res 42 2014 13573 13587
169. J.C. Yao, L. Wang, D. Wei, W. Gong, M. Hassan, and T.T. Wu 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 2004 4109 4117
170. B. Yu, P.K. Datta, and S. Bagchi Stability of the Sp3-DNA complex is promoter-specific: Sp3 efficiently competes with Sp1 for binding to promoters containing multiple Sp-sites Nucleic Acids Res 31 2003 5368 5376
171. P. Yuan, L. Wang, D. Wei, J. Zhang, Z. Jia, and Q. Li Therapeutic inhibition of Sp1 expression in growing tumors by mithramycin a correlates directly with potent antiangiogenic effects on human pancreatic cancer Cancer 110 2007 2682 2690
172. A. Zannetti, S. Del Vecchio, M.V. Carriero, R. Fonti, P. Franco, and G. Botti Coordinate up-regulation of Sp1 DNA-binding activity and urokinase receptor expression in breast carcinoma Cancer Res 60 2000 1546 1551
173. M. Zhang, A. Mathur, Y. Zhang, S. Xi, S. Atay, and J.A. Hong Mithramycin represses basal and cigarette smoke-induced expression of ABCG2 and inhibits stem cell signaling in lung and esophageal cancer cells Cancer Res 72 2012 4178 4192
174. Y. Zhang, M. Sun, W. Shi, Q. Yang, C. Chen, and Z. Wang Arsenic trioxide suppresses transcription of hTERT through down-regulation of multiple transcription factors in HL-60 leukemia cells Toxicol Lett 232 2015 481 489
175. J.P. Zhang, H. Zhang, H.B. Wang, Y.X. Li, G.H. Liu, and S. Xing Down-regulation of Sp1 suppresses cell proliferation, clonogenicity and the expressions of stem cell markers in nasopharyngeal carcinoma J Transl Med 12 2014 222
176. J. Zhang, Z.G. Zhu, J. Ji, F. Yuan, Y.Y. Yu, and B.Y. Liu Transcription factor Sp1 expression in gastric cancer and its relationship to long-term prognosis World J Gastroenterol 11 2005 2213 2217
177. C. Zhao, and A. Meng Sp1-like transcription factors are regulators of embryonic development in vertebrates Dev Growth Differ 47 2005 201 211
178. S. Zhao, J. Wu, F. Zheng, Q. Tang, L. Yang, and L. Li β-Elemene inhibited expression of DNA methyltransferase 1 through activation of ERK1/2 and AMPKalpha signalling pathways in human lung cancer cells: the role of Sp1 J Cell Mol Med 19 2015 630 641
179. Y. Zhao, W. Zhang, Z. Guo, F. Ma, Y. Wu, and Y. Bai Inhibition of the transcription factor Sp1 suppresses colon cancer stem cell growth and induces apoptosis in vitro and in nude mouse xenografts Oncol Rep 30 2013 1782 1792
180. G.H. Zhu, M. Lenzi, and E.L. Schwartz The Sp1 transcription factor contributes to the tumor necrosis factor-induced expression of the angiogenic factor thymidine phosphorylase in human colon carcinoma cells Oncogene 21 2002 8477 8485