Specificity protein (Sp) transcription factors Sp1, Sp3 and Sp4 are non-oncogene addiction genes in cancer cells

Oncotarget

Volumn 7, Issue 16, 2016, Pages 22245-22256

  Hedrick, Erik ^a   Cheng, Yating ^a   Jin, Un Ho ^a   Kim, Kyounghyun ^b   Safe, Stephen ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Cancer; Non oncogene addiction; Sp transcription factors

Indexed keywords

SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3; TRANSCRIPTION FACTOR SP4; SP1 PROTEIN, HUMAN; SP3 PROTEIN, HUMAN; SP4 PROTEIN, HUMAN;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER CELL LINE; CANCER CELL; CANCER CELL LINE; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; COLON CANCER CELL LINE; CONTROLLED STUDY; CORRELATIONAL STUDY; FEMALE; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC REGULATION; LUNG CANCER CELL LINE; MOUSE; NON ONCOGENE ADDICTION GENE; NONHUMAN; PANCREATIC CANCER CELL LINE; PREDICTION; PROTEIN EXPRESSION; RENAL CANCER CELL LINE; RNA INTERFERENCE; TUMOR GROWTH; TUMOR INVASION; TUMOR XENOGRAFT; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; NEOPLASM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; MICE; MICE, NUDE; NEOPLASMS; SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR; SP4 TRANSCRIPTION FACTOR;

EID: 84965050339     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7925     Document Type: Article

References (54)

1. Suske G, Bruford E and Philipsen S. Mammalian SP/KLF transcription factors: bring in the family. Genomics. 2005; 85:551-556.
2. Oh JE, Han JA and Hwang ES. Downregulation of transcription factor, Sp1, during cellular senescence. Biochemical and biophysical research communications. 2007; 353:86-91.
3. Ammendola R, Mesuraca M, Russo T and Cimino F. Sp1 DNA binding efficiency is highly reduced in nuclear extracts from aged rat tissues. The Journal of biological chemistry. 1992; 267:17944-17948.
4. Adrian GS, Seto E, Fischbach KS, Rivera EV, Adrian EK, Herbert DC, Walter CA, Weaker FJ and Bowman BH. YY1 and Sp1 transcription factors bind the human transferrin gene in an age-related manner. The journals of gerontology Series A, Biological sciences and medical sciences. 1996; 51:B66-75.
5. Jiang NY, Woda BA, Banner BF, Whalen GF, Dresser KA and Lu D. Sp1, a new biomarker that identifies a subset of aggressive pancreatic ductal adenocarcinoma. Cancer epidemiology, biomarkers & prevention. 2008; 17:1648-1652.
6. Guan H, Cai J, Zhang N, Wu J, Yuan J, Li J and Li M. Sp1 is upregulated in human glioma, promotes MMP-2-mediated cell invasion and predicts poor clinical outcome. International journal of cancer. 2012; 130:593-601.
7. Maurer GD, Leupold JH, Schewe DM, Biller T, Kates RE, Hornung HM, Lau-Werner U, Post S and Allgayer H. Analysis of specific transcriptional regulators as early predictors of independent prognostic relevance in resected colorectal cancer. Clinical cancer research. 2007; 13:1123-1132.
8. Wang F, Ma YL, Zhang P, Shen TY, Shi CZ, Yang YZ, Moyer MP, Zhang HZ, Chen HQ, Liang Y and Qin HL. SP1 mediates the link between methylation of the tumour suppressor miR-149 and outcome in colorectal cancer. The Journal of pathology. 2013; 229:12-24.
9. Wang L, Wei D, Huang S, Peng Z, Le X, Wu TT, Yao J, Ajani J and Xie K. Transcription factor Sp1 expression is a significant predictor of survival in human gastric cancer. Clinical cancer research. 2003; 9:6371-6380.
10. Essafi-Benkhadir K, Grosso S, Puissant A, Robert G, EssafiM, Deckert M, Chamorey E, Dassonville O, Milano G, Auberger P and Pages G. Dual role of Sp3 transcription factor as an inducer of apoptosis and a marker of tumour aggressiveness. PloS one. 2009; 4:e4478.
11. Bedolla RG, Gong J, Prihoda TJ, Yeh IT, Thompson IM, Ghosh R and Kumar AP. Predictive value of Sp1/Sp3/FLIP signature for prostate cancer recurrence. PloS one. 2012; 7:e44917.
12. Kong LM, Liao CG, Fei F, Guo X, Xing JL and Chen ZN. Transcription factor Sp1 regulates expression of cancerassociated molecule CD147 in human lung cancer. Cancer science. 2010; 101:1463-1470.
13. Wang XB, Peng WQ, Yi ZJ, Zhu SL and Gan QH. [Expression and prognostic value of transcriptional factor sp1 in breast cancer]. Chinese journal of cancer. 2007; 26:996-1000.
14. Safe S, Imanirad P, Sreevalsan S, Nair V and Jutooru I. Transcription factor Sp1, also known as specificity protein 1 as a therapeutic target. Expert opinion on therapeutic targets. 2014; 18:759-769.
15. Kennett SB, Udvadia AJ and Horowitz JM. Sp3 encodes multiple proteins that differ in their capacity to stimulate or repress transcription. Nucleic acids research. 1997; 25:3110-3117.
16. Li L and Davie JR. The role of Sp1 and Sp3 in normal and cancer cell biology. Ann Anat. 2010; 192:275-283.
17. Beishline K and Azizkhan-Clifford J. Sp1 and the 'hallmarks of cancer'. FEBS J. 2015; 282:224-258.
18. Jutooru I, Chadalapaka G, Lei P and Safe S. Inhibition of NFkappaB and pancreatic cancer cell and tumor growth by curcumin is dependent on specificity protein downregulation. The Journal of biological chemistry. 2010; 285:25332-25344.
19. Kim K, Chadalapaka G, Pathi SS, Jin UH, Lee JS, Park YY, Cho SG, Chintharlapalli S and Safe S. Induction of the transcriptional repressor ZBTB4 in prostate cancer cells by drug-induced targeting of microRNA-17-92/106b-25 clusters. Molecular cancer therapeutics. 2012; 11:1852-1862.
20. Chadalapaka G, Jutooru I, Sreevalsan S, Pathi S, Kim K, Chen C, Crose L, Linardic C and Safe S. Inhibition of rhabdomyosarcoma cell and tumor growth by targeting specificity protein (Sp) transcription factors. International journal of cancer. 2013; 132:795-806.
21. Jutooru I, Guthrie AS, Chadalapaka G, Pathi S, Kim K, Burghardt R, Jin UH and Safe S. Mechanism of action of phenethylisothiocyanate and other reactive oxygen speciesinducing anticancer agents. Molecular and cellular biology. 2014; 34:2382-2395.
22. Nair V, Sreevalsan S, Basha R, Abdelrahim M, Abudayyeh A, Rodrigues Hoffman A and Safe S. Mechanism of metformin-dependent inhibition of mammalian target of rapamycin (mTOR) and Ras activity in pancreatic cancer: role of specificity protein (Sp) transcription factors. The Journal of biological chemistry. 2014; 289:27692-27701.
23. Pathi S, Jutooru I, Chadalapaka G, Nair V, Lee SO and Safe S. Aspirin inhibits colon cancer cell and tumor growth and downregulates specificity protein (Sp) transcription factors. PloS one. 2012; 7:e48208.
24. Chadalapaka G, Jutooru I, Burghardt R and Safe S. Drugs that target specificity proteins downregulate epidermal growth factor receptor in bladder cancer cells. Molecular cancer research. 2010; 8:739-750.
25. Luo J, Solimini NL and Elledge SJ. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell. 2009; 136:823-837.
26. Nicolas M, Noe V, Jensen KB and Ciudad CJ. Cloning and characterization of the 5'-flanking region of the human transcription factor Sp1 gene. The Journal of biological chemistry. 2001; 276:22126-22132.
27. Song J, Mangold M, Suske G, Geltinger C, Kanazawa I, Sun K and Yokoyama KK. Characterization and promoter analysis of the mouse gene for transcription factor Sp4. Gene. 2001; 264:19-27.
28. Lou Z, Maher VM and McCormick JJ. Identification of the promoter of human transcription factor Sp3 and evidence of the role of factors Sp1 and Sp3 in the expression of Sp3 protein. Gene. 2005; 351:51-59.
29. Sapetschnig A, Koch F, Rischitor G, Mennenga T and Suske G. Complexity of translationally controlled transcription factor Sp3 isoform expression. The Journal of biological chemistry. 2004; 279:42095-42105.
30. Kim K, Jutooru I, Chadalapaka G, Johnson G, Frank J, Burghardt R, Kim S and Safe S. HOTAIR is a negative prognostic factor and exhibits pro-oncogenic activity in pancreatic cancer. Oncogene. 2013; 32:1616-1625.
31. Cheng Y, Jutooru I, Chadalapaka G, Corton JC and Safe S. The long non-coding RNA HOTTIP enhances pancreatic cancer cell proliferation, survival and migration. Oncotarget. 2015; 6:10840-10852. doi:10.18632/oncotarget.3450.
32. Duxbury MS and Whang EE. RRM2 induces NF-kappaBdependent MMP-9 activation and enhances cellular invasiveness. Biochemical and biophysical research communications. 2007; 354:190-196.
33. Hata T, Furukawa T, Sunamura M, Egawa S, Motoi F, Ohmura N, Marumoto T, Saya H and Horii A. RNA interference targeting aurora kinase a suppresses tumor growth and enhances the taxane chemosensitivity in human pancreatic cancer cells. Cancer research. 2005; 65:2899-2905.
34. Baker AF, Koh MY, Williams RR, James B, Wang H, Tate WR, Gallegos A, Von HoffDD, Han H and Powis G. Identification of thioredoxin-interacting protein 1 as a hypoxia-inducible factor 1alpha-induced gene in pancreatic cancer. Pancreas. 2008; 36:178-186.
35. Karamitopoulou E, Pallante P, Zlobec I, Tornillo L, Carafa V, Schaffner T, Borner M, Diamantis I, Esposito F, Brunner T, Zimmermann A, Federico A, Terracciano L and Fusco A. Loss of the CBX7 protein expression correlates with a more aggressive phenotype in pancreatic cancer. Eur J Cancer. 2010; 46:1438-1444.
36. Chen Z, Yang Y, Liu B, Wang B, Sun M, Zhang L, Chen B, You H and Zhou M. Promotion of metastasis-associated gene expression in survived PANC-1 cells following trichostatin A treatment. Anticancer Agents Med Chem. 2015; 15:1317-1325.
37. Berberat PO, Dambrauskas Z, Gulbinas A, Giese T, Giese N, Kunzli B, Autschbach F, Meuer S, Buchler MW and Friess H. Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clinical cancer research. 2005; 11:3790-3798.
38. Sainz B, Jr., Martin B, Tatari M, Heeschen C and Guerra S. ISG15 is a critical microenvironmental factor for pancreatic cancer stem cells. Cancer research. 2014; 74:7309-7320.
39. Ma Y, Yu S, Zhao W, Lu Z and Chen J. miR-27a regulates the growth, colony formation and migration of pancreatic cancer cells by targeting Sprouty2. Cancer letters. 2010; 298:150-158.
40. Kramer A, Green J, Pollard J, Jr. and Tugendreich S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics. 2014; 30:523-530.
41. Torti D and Trusolino L. Oncogene addiction as a foundational rationale for targeted anti-cancer therapy: promises and perils. EMBO molecular medicine. 2011; 3:623-636.
42. Lou Z, O'Reilly S, Liang H, Maher VM, Sleight SD and McCormick JJ. Down-regulation of overexpressed sp1 protein in human fibrosarcoma cell lines inhibits tumor formation. Cancer research. 2005; 65:1007-1017.
43. Li L, Gao P, Li Y, Shen Y, Xie J, Sun D, Xue A, Zhao Z, Xu Z, Zhang M, Li B and Jiang J. JMJD2A-dependent silencing of Sp1 in advanced breast cancer promotes metastasis by downregulation of DIRAS3. Breast cancer research and treatment. 2014; 147:487-500.
44. Kong LM, Liao CG, Zhang Y, Xu J, Li Y, Huang W, Zhang Y, Bian H and Chen ZN. A regulatory loop involving miR-22, Sp1, and c-Myc modulates CD147 expression in breast cancer invasion and metastasis. Cancer research. 2014; 74:3764-3778.
45. Jia Z, Gao S, M'Rabet N, De Geyter C and Zhang H. Sp1 is necessary for gene activation of Adamts17 by estrogen. Journal of cellular biochemistry. 2014; 115:1829-1839.
46. Wang H, Gutierrez-Uzquiza A, Garg R, Barrio-Real L, Abera MB, Lopez-Haber C, Rosemblit C, Lu H, Abba M and Kazanietz MG. Transcriptional regulation of oncogenic protein kinase C (PKC) by STAT1 and Sp1 proteins. The Journal of biological chemistry. 2014; 289:19823-19838.
47. Hsu TI, Wang MC, Chen SY, Yeh YM, Su WC, Chang WC and Hung JJ. Sp1 expression regulates lung tumor progression. Oncogene. 2012; 31:3973-3988.
48. Chuang JY, Wu CH, Lai MD, Chang WC and Hung JJ. Overexpression of Sp1 leads to p53-dependent apoptosis in cancer cells. International journal of cancer. 2009; 125:2066-2076.
49. Li H, Zhang Y, Strose A, Tedesco D, Gurova K and Selivanova G. Integrated high-throughput analysis identifies Sp1 as a crucial determinant of p53-mediated apoptosis. Cell death and differentiation. 2014; 21:1493-1502.
50. Deniaud E, Baguet J, Mathieu AL, Pages G, Marvel J and Leverrier Y. Overexpression of Sp1 transcription factor induces apoptosis. Oncogene. 2006; 25:7096-7105.
51. Deniaud E, Baguet J, Chalard R, Blanquier B, Brinza L, Meunier J, Michallet MC, Laugraud A, Ah-Soon C, Wierinckx A, Castellazzi M, Lachuer J, Gautier C, Marvel J and Leverrier Y. Overexpression of transcription factor Sp1 leads to gene expression perturbations and cell cycle inhibition. PloS one. 2009; 4:e7035.
52. Ma Y, Chapman J, Levine M, Polireddy K, Drisko J and Chen Q. High-dose parenteral ascorbate enhanced chemosensitivity of ovarian cancer and reduced toxicity of chemotherapy. Science translational medicine. 2014; 6:222ra218.
53. Jia Z, Gao Y, Wang L, Li Q, Zhang J, Le X, Wei D, Yao JC, Chang DZ, Huang S and Xie K. Combined treatment of pancreatic cancer with mithramycin A and tolfenamic acid promotes Sp1 degradation and synergistic antitumor activity. Cancer research. 2010; 70:1111-1119.
54. Gao Y, Jia Z, Kong X, Li Q, Chang DZ, Wei D, Le X, Suyun H, Huang S, Wang L and Xie K. Combining betulinic acid and mithramycin a effectively suppresses pancreatic cancer by inhibiting proliferation, invasion, and angiogenesis. Cancer research. 2011; 71:5182-5193.