Critical analysis of the potential for the therapeutic targeting of the Sp1 transcription factor in pancreatic cancer

References

• Weinberg RA. Oncogenes, antioncogenes, and the molecular bases of multistep carcinogenesis. Cancer Res. 1989;49(14):3713–3721.
   Web of Science ®Google Scholar
• Weinberg F, Chandel NS. Mitochondrial metabolism and cancer. Ann N Y Acad Sci. 2009;1177:66–73.
   PubMed Web of Science ®Google Scholar
• Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin. 2009;59(4):225–249.
   PubMed Web of Science ®Google Scholar
• Siegel R, Naishadham D, Jemal A. Cancer Statistics, 2013. CA Cancer J Clin. 2013;63(1):11–30.
   PubMed Web of Science ®Google Scholar
• Ottenhof NA, Milne AN, Morsink FH, et al. Pancreatic intraepithelial neoplasia and pancreatic tumorigenesis: of mice and men. Arch Pathol Lab Med. 2009;133(3):375–381.
   Web of Science ®Google Scholar
• Nkondjock A, Krewski D, Johnson KC, Ghadirian P; Canadian Cancer Registries Epidemiology Research Group. Dietary patterns and risk of pancreatic cancer. Int J Cancer. 2005;114(5):817–823.
   Google Scholar
• Nkondjock A, Krewski D, Johnson KC, Ghadirian P; Canadian Cancer Registries Epidemiology Research Group. Specific fatty acid intake and the risk of pancreatic cancer in Canada. Br J Cancer. 2005;92(5):971–977.
   Google Scholar
• Ghadirian P, Nkondjock A. Consumption of food groups and the risk of pancreatic cancer: a case-control study. J Gastrointest Cancer. 2010;41(2):121–129.
   PubMedGoogle Scholar
• Shi C, Hruban RH, Klein AP. Familial pancreatic cancer. Arch Pathol Lab Med. 2009;133(3):365–374.
   Web of Science ®Google Scholar
• Hruban RH, Adsay NV. Molecular classification of neoplasms of the pancreas. Hum Pathol. 2009;40(5):612–623.
   PubMed Web of Science ®Google Scholar
• Hruban RH, Maitra A, Schulick R, et al. Emerging molecular biology of pancreatic cancer. Gastrointest Cancer Res. 2008;2(Suppl 4):S10–S15.
   Google Scholar
• Gidekel Friedlander SY, Chu GC, Snyder EL, et al. Context-dependent transformation of adult pancreatic cells by oncogenic K-Ras. Cancer Cell. 2009;16(5):379–389.
   Web of Science ®Google Scholar
• Hingorani SR, Petricoin EF, Maitra A, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell. 2003;4(6):437–450.
   PubMed Web of Science ®Google Scholar
• Maitra A, Hruban RH. Pancreatic cancer. Annu Rev Pathol. 2008;3:157–188.
   PubMed Web of Science ®Google Scholar
• Xing HR, Cordon-Cardo C, Deng X, et al. Pharmacologic inactivation of kinase suppressor of ras-1 abrogates Ras-mediated pancreatic cancer. Nat Med. 2003;9(10):1266–1268.
   Web of Science ®Google Scholar
• Maitra A, Kern SE, Hruban RH. Molecular pathogenesis of pancreatic cancer. Best Pract Res Clin Gastroenterol. 2006;20(2):211–226.
   PubMed Web of Science ®Google Scholar
• Hingorani SR, Wang L, Multani AS, et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell. 2005;7(5):469–483.
   PubMed Web of Science ®Google Scholar
• Hansel DE, Kern SE, Hruban RH. Molecular pathogenesis of pancreatic cancer. Annu Rev Genomics Hum Genet. 2003;4:237–256.
   PubMed Web of Science ®Google Scholar
• Fernandez-Zapico ME, Gonzalez-Paz NC, Weiss E, et al. Ectopic expression of VAV1 reveals an unexpected role in pancreatic cancer tumorigenesis. Cancer Cell. 2005;7(1):39–49.
   Web of Science ®Google Scholar
• Bertone P, Stolc V, Royce TE, et al. Global identification of human transcribed sequences with genome tiling arrays. Science. 2004; 306(5705):2242–2246.
   PubMed Web of Science ®Google Scholar
• Cheng J, Kapranov P, Drenkow J, et al. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science. 2005; 308(5725):1149–1154.
   PubMed Web of Science ®Google Scholar
• Kapranov P, Cheng J, Dike S, et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science. 2007;316(5830):1484–1488.
   PubMed Web of Science ®Google Scholar
• American Cancer Society. Cancer Facts and Figures 2013 [webpage on the Internet]. Atlanta: American Cancer Society; 2013. Available from: http://www.cancer.org/research/cancerfactsstatistics/cancerfactsfigures2013/index. Accessed December, 2013.
   Google Scholar
• Hawes RH, Xiong Q, Waxman I, Chang KJ, Evans DB, Abbruzzese JL. A multispecialty approach to the diagnosis and management of pancreatic cancer. Am J Gastroenterol. 2000;95(1):17–31.
   PubMed Web of Science ®Google Scholar
• Lau WY, Lai EC. Development and controversies of adjuvant therapy for pancreatic cancer. Hepatobiliary Pancreat Dis Int. 2008;7(2):121–125.
   Web of Science ®Google Scholar
• Pliarchopoulou K, Pectasides D. Pancreatic cancer: current and future treatment strategies. Cancer Treat Rev. 2009;35(5):431–436.
   Web of Science ®Google Scholar
• Mahalingam D, Kelly KR, Swords RT, Carew J, Nawrocki ST, Giles FJ. Emerging drugs in the treatment of pancreatic cancer. Expert Opin Emerg Drugs. 2009;14(2):311–328.
   PubMed Web of Science ®Google Scholar
• Sezgin C, Karabulut B, Uslu R, et al. Gemcitabine treatment in patients with inoperable locally advanced/metastatic pancreatic cancer and prognostic factors. Scand J Gastroenterol. 2005;40(12):1486–1492.
   PubMed Web of Science ®Google Scholar
• Wong HH, Lemoine NR. Pancreatic cancer: molecular pathogenesis and new therapeutic targets. Nat Rev Gastroenterol Hepatol. 2009;6(7):412–422.
   PubMed Web of Science ®Google Scholar
• Lemons D, McGinnis W. Genomic evolution of Hox gene clusters. Science. 2006;313(5795):1918–1922.
   Web of Science ®Google Scholar
• Courey AJ, Tjian R. Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell. 1988;55(5):887–898.
   Web of Science ®Google Scholar
• Bouwman P, Philipsen S. Regulation of the activity of Sp1-related transcription factors. Mol Cell Endocrinol. 2002;195(1–2):27–38.
   Web of Science ®Google Scholar
• Suske G. The Sp-family of transcription factors. Gene. 1999;238(2):291–300.
   PubMed Web of Science ®Google Scholar
• Wierstra I. Sp1: emerging roles – beyond constitutive activation of TATA-less housekeeping genes. Biochem Biophys Res Commun. 2008;372(1):1–13.
   PubMed Web of Science ®Google Scholar
• Abdelrahim M, Smith R, Burghardt R, Safe S. Role of Sp proteins in regulation of vascular endothelial growth factor expression and proliferation of pancreatic cancer cells. Cancer Res. 2004;64(18):6740–6749.
   PubMed Web of Science ®Google Scholar
• Marin M, Karis A, Visser P, Grosveld F, Philipsen S. Transcription factor Sp1 is essential for early embryonic development but dispensable for cell growth and differentiation. Cell. 1997;89(4):619–628.
   PubMed Web of Science ®Google Scholar
• Lou Z, O’Reilly S, Liang H, Maher VM, Sleight SD, McCormick JJ. Down-regulation of overexpressed sp1 protein in human fibrosarcoma cell lines inhibits tumor formation. Cancer Res. 2005;65(3):1007–1017.
   PubMed Web of Science ®Google Scholar
• Abdelrahim M, Baker CH, Abbruzzese JL, et al. Regulation of vascular endothelial growth factor receptor-1 expression by specificity proteins 1, 3, and 4 in pancreatic cancer cells. Cancer Res. 2007;67(7):3286–3294.
   PubMed Web of Science ®Google Scholar
• Higgins KJ, Abdelrahim M, Liu S, Yoon K, Safe S. Regulation of vascular endothelial growth factor receptor-2 expression in pancreatic cancer cells by Sp proteins. Biochem Biophys Res Commun. 2006;345(1):292–301.
   Web of Science ®Google Scholar
• Abdelrahim M, Baker CH, Abbruzzese JL, Safe S. Tolfenamic acid and pancreatic cancer growth, angiogenesis, and Sp protein degradation. J Natl Cancer Inst. 2006;98(12):855–868.
   PubMedGoogle Scholar
• Chintharlapalli S, Papineni S, Abdelrahim M, et al. Oncogenic microRNA-27a is a target for anticancer agent methyl 2-cyano-3,11-dioxo-18beta-olean-1,12-dien-30-oate in colon cancer cells. Int J Cancer. 2009;125(8):1965–1974.
   PubMed Web of Science ®Google Scholar
• Mertens-Talcott SU, Chintharlapalli S, Li X, Safe S. 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. 2007;67(22):11001–11011.
   PubMed Web of Science ®Google Scholar
• Chadalapaka G, Jutooru I, Chintharlapalli S, et al. Curcumin decreases specificity protein expression in bladder cancer cells. Cancer Res. 2008;68(13):5345–5354.
   PubMed Web of Science ®Google Scholar
• Jutooru I, Chadalapaka G, Sreevalsan S, et al. Arsenic trioxide downregulates specificity protein (Sp) transcription factors and inhibits bladder cancer cell and tumor growth. Exp Cell Res. 2010;316(13):2174–2188.
   PubMed Web of Science ®Google Scholar
• Ammendola R, Mesuraca M, Russo T, Cimino F. Sp1 DNA binding efficiency is highly reduced in nuclear extracts from aged rat tissues. J Biol Chem. 1992;267(25):17944–17948.
   PubMed Web of Science ®Google Scholar
• Oh JE, Han JA, Hwang ES. Downregulation of transcription factor, Sp1, during cellular senescence. Biochem Biophys Res Commun. 2007;353(1):86–91.
   PubMed Web of Science ®Google Scholar
• Chintharlapalli S, Papineni S, Ramaiah SK, Safe S. Betulinic acid inhibits prostate cancer growth through inhibition of specificity protein transcription factors. Cancer Res. 2007;67(6):2816–2823.
   PubMed Web of Science ®Google Scholar
• Jiang NY, Woda BA, Banner BF, Whalen GF, Dresser KA, Lu D. Sp1, a new biomarker that identifies a subset of aggressive pancreatic ductal adenocarcinoma. Cancer Epidemiol Biomarkers Prev. 2008;17(7):1648–1652.
   PubMed Web of Science ®Google Scholar
• Black AR, Black JD, Azizkhan-Clifford J. Sp1 and krüppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol. 2001;188(2):143–160.
   PubMed Web of Science ®Google Scholar
• Xie K, Wei D, Huang S. Transcriptional anti-angiogenesis therapy of human pancreatic cancer. Cytokine Growth Factor Rev. 2006;17(3):147–156.
   Web of Science ®Google Scholar
• Shi Q, Le X, Abbruzzese JL, et al. Constitutive Sp1 activity is essential for differential constitutive expression of vascular endothelial growth factor in human pancreatic adenocarcinoma. Cancer Res. 2001;61(10):4143–4154.
   PubMed Web of Science ®Google Scholar
• Jia Z, Zhang J, Wei D, et al. Molecular basis of the synergistic antiangiogenic activity of bevacizumab and mithramycin A. Cancer Res. 2007;67(10):4878–4885.
   PubMed Web of Science ®Google Scholar
• Jungert K, Buck A, von Wichert G, et al. Sp1 is required for transforming growth factor-beta-induced mesenchymal transition and migration in pancreatic cancer cells. Cancer Res. 2007;67(4):1563–1570.
   Web of Science ®Google Scholar
• Gao Y, Jia Z, Kong X, et al. Combining betulinic acid and mithramycin a effectively suppresses pancreatic cancer by inhibiting proliferation, invasion, and angiogenesis. Cancer Res. 2011;71(15):5182–5193.
   PubMed Web of Science ®Google Scholar
• Jutooru I, Chadalapaka G, Abdelrahim M, et al. 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. 2010;78(2):226–236.
   PubMed Web of Science ®Google Scholar
• Jutooru I, Chadalapaka G, Lei P, Safe S. Inhibition of NFkappaB and pancreatic cancer cell and tumor growth by curcumin is dependent on specificity protein down-regulation. J Biol Chem. 2010;285(33):25332–25344.
   PubMed Web of Science ®Google Scholar
• Yuan P, Wang L, Wei D, et al. Therapeutic inhibition of Sp1 expression in growing tumors by mithramycin a correlates directly with potent antiangiogenic effects on human pancreatic cancer. Cancer. 2007;110(12):2682–2690.
   PubMed Web of Science ®Google Scholar
• Osada N, Kosuge Y, Ishige K, Ito Y. Mithramycin, an agent for developing new therapeutic drugs for neurodegenerative diseases. J Pharmacol Sci. 2013;122(4):251–256.
   PubMed Web of Science ®Google Scholar
• Lee TJ, Jung EM, Lee JT, et al. Mithramycin A sensitizes cancer cells to TRAIL-mediated apoptosis by down-regulation of XIAP gene promoter through Sp1 sites. Mol Cancer Ther. 2006;5(11):2737–2746.
   PubMed Web of Science ®Google Scholar
• Taylor DJ, Parsons CE, Han H, Jayaraman A, Rege K. Parallel screening of FDA-approved antineoplastic drugs for identifying sensitizers of TRAIL-induced apoptosis in cancer cells. BMC Cancer. 2011;11:470.
   PubMed Web of Science ®Google Scholar
• Konduri S, Colon J, Baker CH, et al. Tolfenamic acid enhances pancreatic cancer cell and tumor response to radiation therapy by inhibiting survivin protein expression. Mol Cancer Ther. 2009;8(3):533–542.
   PubMed Web of Science ®Google Scholar
• Jia Z, Gao Y, Wang L, et al. Combined treatment of pancreatic cancer with mithramycin A and tolfenamic acid promotes Sp1 degradation and synergistic antitumor activity. Cancer Res. 2010;70(3):1111–1119.
   PubMed Web of Science ®Google Scholar
• Gandhy SU, Kim K, Larsen L, Rosengren RJ, Safe S. Curcumin and synthetic analogs induce reactive oxygen species and decreases specificity protein (Sp) transcription factors by targeting microRNAs. BMC Cancer. 2012;12:564.
   PubMed Web of Science ®Google Scholar
• Safe SH, Prather PL, Brents LK, Chadalapaka G, Jutooru I. Unifying mechanisms of action of the anticancer activities of triterpenoids and synthetic analogs. Anticancer Agents Med Chem. 2012;12(10):1211–1220.
   PubMed Web of Science ®Google Scholar
• Deeb D, Gao X, Liu Y, Varma NR, Arbab AS, Gautam SC. Inhibition of telomerase activity by oleanane triterpenoid CDDO-Me in pancreatic cancer cells is ROS-dependent. Molecules. 2013;18(3):3250–3265.
   Web of Science ®Google Scholar
• El-Jurdi NH, Saif MW. Diabetes and pancreatic cancer. JOP. 2013; 14(4):363–366.
   Google Scholar
• Evans JM, Donnelly LA, Emslie-Smith AM, Alessi DR, Morris AD. Metformin and reduced risk of cancer in diabetic patients. BMJ. 2005;330(7503):1304–1305.
   PubMed Web of Science ®Google Scholar
• Libby G, Donnelly LA, Donnan PT, Alessi DR, Morris AD, Evans JM. New users of metformin are at low risk of incident cancer: a cohort study among people with type 2 diabetes. Diabetes Care. 2009;32(9):1620–1625.
   PubMed Web of Science ®Google Scholar
• Nair V, Pathi S, Jutooru I, et al. Metformin inhibits pancreatic cancer cell and tumor growth and downregulates Sp transcription factors. Carcinogenesis. 2013;34(12):2870–2879.
   PubMed Web of Science ®Google Scholar
• Banerjee S, Sangwan V, McGinn O, et al. Triptolide-induced cell death in pancreatic cancer is mediated by O-GlcNAc modification of transcription factor Sp1. J Biol Chem. 2013;288(47):33927–33938.
   PubMed Web of Science ®Google Scholar
• Jutooru I, Guthrie A, Chadalapaka G, et al. Mechanism of Action of Phenethylisothiocyanate and Other ROS-Inducing Anticancer Agents. Moll Cell Biol. Epub 2014 Apr 14.
   Google Scholar