Sp1-driven up-regulation of miR-19a decreases RHOB and promotes pancreatic cancer

Oncotarget

Volumn 6, Issue 19, 2015, Pages 17391-17403

  Tan, Yonggang ^a   Yin, Hongzhuan ^a   Zhang, Heying ^a   Fang, Jun ^b   Zheng, Wei ^a   Li, Dan ^a   Li, Yue ^a   Cao, Wei ^a   Sun, Cheng ^a   Liang, Yusi ^a   Zeng, Juan ^a   Zou, Huawei ^a   Fu, Weineng ^a   Yang, Xianghong ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b SOJO UNIVERSITY   (Japan)

Author keywords

miRNA; Pancreatic cancer; Target gene; Transcription factor

Indexed keywords

GEMCITABINE; MICRORNA; MICRORNA 19A; PACLITAXEL; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; RECOMBINANT ENDOSTATIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; MIRN19 MICRORNA, HUMAN; SP1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SP1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INFILTRATION; CANCER INHIBITION; CANCER PROGNOSIS; CELL CYCLE S PHASE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; FEMALE; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MOUSE; NONHUMAN; PANCREAS CANCER; PROTEIN FUNCTION; RHOB GENE; TUMOR DIFFERENTIATION; TUMOR GROWTH; TUMOR VOLUME; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CHROMATIN IMMUNOPRECIPITATION; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; MALE; METABOLISM; PANCREAS TUMOR; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICRORNAS; PANCREATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; RHOB GTP-BINDING PROTEIN; SP1 TRANSCRIPTION FACTOR; TRANSFECTION; UP-REGULATION;

EID: 84938234041     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3975     Document Type: Article

References (52)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61:69-90.
2. Moshal KS, Ferri-Lagneau KF, Leung T. Zebrafish model: worth considering in defining tumor angiogenesis. Trends Cardiovasc Med. 2010; 20:114-9.
3. Brideau G, Mäkinen MJ, Elamaa H, Tu H, Nilsson G, Alitalo K, Pihlajaniemi T, Heljasvaara R. Endostatin overexpression inhibits lymphangiogenesis and lymph node metastasis in mice. Cancer Res. 2007; 67:11528-35.
4. Wang RS, Liu LX, Gu YH, Lin QF, Guo RH, Shu YQ. The effect of endostatin and gemcitabine combined with HIFU on the animal xenograft model of human pancreatic cancer. Biomed Pharmacother. 2010; 64:309-12.
5. Ambros V. microRNAs: tiny regulators with great potential. Cell. 2001; 107:823-6.
6. Srivastava SK, Arora S, Singh S, Bhardwaj A, Averett C, Singh AP. MicroRNAs in pancreatic malignancy: Progress and promises. Cancer Lett. 2014; 347:167-74.
7. O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997; 88:277-85.
8. Ling Y, Yang Y, Lu N, You QD, Wang S, Gao Y, Chen Y, Guo QL. Endostar, a novel recombinant human endostatin, exerts antiangiogenic effect via blocking VEGF-induced tyrosine phosphorylation of KDR/Flk-1 of endothelial cells. Biochem Biophys Res Commun. 2007; 361:79-84.
9. Ling Y, Lu N, Gao Y, Chen Y, Wang S, Yang Y, Guo Q. Endostar induces apoptotic effects in HUVECs through activation of caspase-3 and decrease of Bcl-2. Anticancer Res. 2009; 29:411-7.
10. Song W, Li Q, Wang L, Wang L. Modulation of FoxO1 expression by miR-21 to promote growth of pancreatic ductal adenocarcinoma. Cell Physiol Biochem. 2015; 35:184-90.
11. Sicard F, Gayral M, Lulka H, Buscail L, Cordelier P. Targeting miR-21 for the therapy of pancreatic cancer. Mol Ther. 2013; 21:986-94.
12. Wang P, Zhuang L, Zhang J, Fan J, Luo J, Chen H, Wang K, Liu L, Chen Z, Meng Z. The serum miR-21 level serves as a predictor for the chemosensitivity of advanced pancreatic cancer, and miR-21 expression confers chemoresistance by targeting FasL. Mol Oncol. 2013; 7:334-45.
13. Ali S, Ahmad A, Banerjee S, Padhye S, Dominiak K, Schaffert JM, Wang Z, Philip PA, Sarkar FH. Gemcitabine sensitivity can be induced in pancreatic cancer cells through modulation of miR-200 and miR-21 expression by curcumin or its analogue CDF. Cancer Res. 2010; 70:3606-17.
14. Tavano F, di Mola FF, Piepoli A, Panza A, Copetti M, Burbaci FP, Latiano T, Pellegrini F, Maiello E, Andriulli A, di Sebastiano P. Changes in miR-143 and miR-21 expression and clinicopathological correlations in pancreatic cancers. Pancreas. 2012; 41:1280-4.
15. Awasthi NI, Zhang C, Schwarz AM, Hinz S, Wang C, Williams NS, Schwarz MA, Schwarz RE. Comparative benefits of Nab-paclitaxel over gemcitabine or polysorbate-based docetaxel in experimental pancreatic cancer. Carcinogenesis. 2013; 34:2361-9.
16. Qin S, Ai F, Ji WF, Rao W, Zhang HC, Yao WJ. miR-19a Promotes Cell Growth and Tumorigenesis through Targeting SOCS1 in Gastric Cancer. Asian Pac J Cancer Prev. 2013; 14:835-40.
17. Xu XM, Wang XB, Chen MM, Liu T, Li YX, Jia WH, Liu M, Li X, Tang H. MicroRNA-19a and -19b regulate cervical carcinoma cell proliferation and invasion by targeting CUL5. Cancer Lett. 2012; 322:148-58.
18. Yu G, Li H, Wang X, Wu T, Zhu J, Huang S, Wan Y, Tang J. MicroRNA-19a targets tissue factor to inhibit colon cancer cells migration and invasion. Mol Cell Biochem. 2013; 380:239-47.
19. Yang J, Zhang Z, Chen C, Liu Y, Si Q, Chuang TH, Li N, Gomez-Cabrero A, Reisfeld RA, Xiang R, Luo Y. MicroRNA-19a-3p inhibits breast cancer progression and metastasis by inducing macrophage polarization through downregulated expression of Fra-1 proto-oncogene. Oncogene. 2014; 33:3014-23.
20. Lin Q, Chen T, Lin Q, Lin G, Lin J, Chen G, Guo L. Serum miR-19a expression correlates with worse prognosis of patients with non-small cell lung cancer. J Surg Oncol. 2013; 107:767-71.
21. Wu TY, Zhang TH, Qu LM, Feng JP, Tian LL, Zhang BH, Li DD, Sun YN, Liu M. MiR-19a is correlated with prognosis and apoptosis of laryngeal squamous cell carcinoma by regulating TIMP-2 expression. Int J Clin Exp Pathol. 2013; 7:56-63.
22. Wang F, Li T, Zhang B, Li H, Wu Q, Yang L, Nie Y, Wu K, Shi Y, Fan D. MicroRNA-19a/b regulates multidrug resistance in human gastric cancer cells by targeting PTEN. Biochem Biophys Res Commun. 2013; 434:688-94.
23. Chen Q, Xia HW, Ge XJ, Zhang YC, Tang QL, Bi F. Serum miR-19a predicts resistance to FOLFOX chemotherapy in advanced colorectal cancer cases. Asian Pac J Cancer Prev. 2013; 14:7421-6.
24. Liu M, Wang Z, Yang S, Zhang W, He S, Hu C, Zhu H, Quan L, Bai J, Xu N. TNF-α is a novel target of miR-19a. Int J Oncol. 2011; 38:1013-22.
25. Wu TY, Zhang TH, Qu LM, Feng JP, Tian LL, Zhang BH, Li DD, Sun YN, Liu M. MiR-19a is correlated with prognosis and apoptosis of laryngeal squamous cell carcinoma by regulating TIMP-2 expression. Int J Clin Exp Pathol. 2013; 7:56-63.
26. Hill R, Calvopina JH, Kim C, Wang Y, Dawson DW, Donahue TR, Dry S, Wu H. PTEN loss accelerates KrasG12D-induced pancreatic cancer development. Cancer Res. 2010; 70:7114-24.
27. Ying H, Elpek KG, Vinjamoori A, Zimmerman SM, Chu GC, Yan H, Fletcher-Sananikone E, Zhang H, Liu Y, Wang W, Ren X, Zheng H, Kimmelman AC, Paik JH, Lim C, Perry SR, Jiang S, Malinn B, Protopopov A, Colla S, Xiao Y, Hezel AF, Bardeesy N, Turley SJ, Wang YA, Chin L, Thayer SP, DePinho RA. PTEN is a major tumor suppressor in pancreatic ductal adenocarcinoma and regulates an NF-κB-cytokine network. Cancer Discov. 2011; 1:158-69.
28. Sarkar S, Dubaybo H, Ali S, Goncalves P, Kollepara SL, Sethi S, Philip PA, Li Y. Down-regulation of miR-221 inhibits proliferation of pancreatic cancer cells through up-regulation of PTEN, p27(kip1), p57(kip2), and PUMA. Am J Cancer Res. 2013; 3:465-77.
29. Soubani O, Ali AS, Logna F, Ali S, Philip PA, Sarkar FH. Re-expression of miR-200 by novel approaches regulates the expression of PTEN and MT1-MMP in pancreatic cancer. Carcinogenesis. 2012; 33:1563-71.
30. Zhou J, Zhu Y, Zhang G, Liu N, Sun L, Liu M, Qiu M, Luo D, Tang Q, Liao Z, Zheng Y, Bi F. A distinct role of RhoB in gastric cancer suppression. Int J Cancer. 2011; 128:1057-68.
31. Kim DM, Chung KS, Choi SJ, Jung YJ, Park SK, Han GH, Ha JS, Song KB, Choi NS, Kim HM, Won M, Seo YS. RhoB induces apoptosis via direct interaction with TNFAIP1 in HeLa cells. Int J Cancer. 2009; 125:2520-7.
32. Marlow LA, Reynolds LA, Cleland AS, Cooper SJ, Gumz ML, Kurakata S, Fujiwara K, Zhang Y, Sebo T, Grant C, McIver B, Wadsworth JT, Radisky DC, Smallridge RC, Copland JA. Reactivation of suppressed RhoB is a critical step for the inhibition of anaplastic thyroid cancer growth. Cancer Res. 2009; 69:1536-44.
33. Couderc B, Pradines A, Rafii A, Golzio M, Deviers A, Allal C, Berg D, Penary M, Teissie J, Favre G. In vivo restoration of RhoB expression leads to ovarian tumor regression. Cancer Gene Ther. 2008; 15:456-64.
34. Kim BK, Kim HM, Chung KS, Kim DM, Park SK, Song A, Won KJ, Lee K, Oh YK, Lee K, Song KB, Simon JA, Han G, Won M. Upregulation of RhoB via c-Jun N-terminal kinase signaling induces apoptosis of the human gastric carcinoma NUGC-3 cells treated with NSC12618. Carcinogenesis. 2011; 32:254-61.
35. Luis-Ravelo D, Antón I, Zandueta C, Valencia K, Pajares MJ, Agorreta J, Montuenga L, Vicent S, Wistuba II, De Las Rivas J, Lecanda F. RHOB influences lung adenocarcinoma metastasis and resistance in a host-sensitive manner. Mol Oncol. 2014; 8:196-206.
36. Liu Y, Song N, Ren K, Meng S, Xie Y, Long Q, Chen X, Zhao X. Expression loss and revivification of RhoB gene in ovary carcinoma carcinogenesis and development. PLoS One. 2013; 8:e78417.
37. Kazerounian S, Gerald D, Huang M, Chin YR, Udayakumar D, Zheng N, O'Donnell RK, Perruzzi C, Mangiante L, Pourat J, Phung TL, Bravo-Nuevo A, Shechter S, McNamara S, Duhadaway JB, Kocher ON, Brown LF, Toker A, Prendergast GC, Benjamin LE. RhoB differentially controls Akt function in tumor cells and stromal endothelial cells during breast tumorigenesis. Cancer Res. 2013; 73:50-61.
38. Marlow LA, D'Innocenzi J, Zhang Y, Rohl SD, Cooper SJ, Sebo T, Grant C, McIver B, Kasperbauer JL, Wadsworth JT, Casler JD, Kennedy PW, Highsmith WE, Clark O, Milosevic D, Netzel B, Cradic K, Arora S, Beaudry C, Grebe SK, Silverberg ML, Azorsa DO, Smallridge RC, Copland JA. Detailed molecular fingerprinting of four new anaplastic thyroid carcinoma cell lines and their use for verification of RhoB as a molecular therapeutic target. J Clin Endocrinol Metab. 2010; 95:5338-47.
39. Vishnu P, Colon-Otero G, Kennedy GT, Marlow LA, Kennedy WP, Wu KJ, Santoso JT, Copland JA. RhoB mediates antitumor synergy of combined ixabepilone and sunitinib in human ovarian serous cancer. Gynecol Oncol. 2012; 124:589-97.
40. Eisermann K, Broderick CJ, Bazarov A, Moazam MM, Fraizer GC. Androgen up-regulates vascular endothelial growth factor expression in prostate cancer cells via an Sp1 binding site. Mol Cancer. 2013; 12:7.
41. Kim MK, Jeon BN, Koh DI, Kim KS, Park SY, Yun CO, Hur MW. Regulation of the cyclin-dependent kinase inhibitor 1A gene (CDKN1A) by the repressor BOZF1 through inhibition of p53 acetylation and transcription factor Sp1 binding. J Biol Chem. 2013; 288:7053-64.
42. Koizume S, Ito S, Miyagi E, Hirahara F, Nakamura Y, Sakuma Y, Osaka H, Takano Y, Ruf W, Miyagi Y. HIF2α-Sp1 interaction mediates a deacetylation-dependent FVII-gene activation under hypoxic conditions in ovarian cancer cells. Nucleic Acids Res. 2012; 40:5389-401.
43. Li F, Jiang Z, Wang K, Guo J, Hu G, Sun L, Wang T, Tang X, He L, Yao J, Wen D, Qin X, Zhang L. Transactivation of the human NME5 gene by Sp1 in pancreatic cancer cells. Gene. 2012; 503:200-7.
44. Kong LM, Liao CG, Zhang Y, Xu J, Li Y, Huang W, Zhang Y, Bian H, Chen ZN. A regulatory loop involving miR-22, Sp1 and c-Myc modulates CD147 expression in breast cancer invasion and metastasis. Cancer Res. 2014; 74:3764-78.
45. 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; 17:1648-52.
46. 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.
47. Safe S, Imanirad P, Sreevalsan S, Nair V, Jutooru I. Transcription factor Sp1, also known as specificity protein 1 as a therapeutic target. Expert Opin Ther Targets. 2014; 18:759-69.
48. Eder JP Jr, Supko JG, Clark JW, Puchalski TA, Garcia-Carbonero R, Ryan DP, Shulman LN, Proper J, Kirvan M, Rattner B, Connors S, Keogan MT, Janicek MJ, Fogler WE, Schnipper L, Kinchla N, Sidor C, Phillips E, Folkman J, Kufe DW. Phase I clinical trial of recombinant human endostatin administered as a short intravenous infusion repeated daily. J Clin Oncol. 2002; 20:3772-84.
49. Herbst RS, Hess KR, Tran HT, Tseng JE, Mullani NA, Charnsangavej C, Madden T, Davis DW, McConkey DJ, O'Reilly MS, Ellis LM, Pluda J, Hong WK, Abbruzzese JL. Phase I study of recombinant human endostatin in patients with advanced solid tumors. J Clin Oncol. 2002; 20:3792-803.
50. Thomas JP, Arzoomanian RZ, Alberti D, Marnocha R, Lee F, Friedl A, Tutsch K, Dresen A, Geiger P, Pluda J, Fogler W, Schiller JH, Wilding G. Phase I pharmacokinetic and pharmacodynamic study of recombinant human endostatin in patients with advanced solid tumors. J Clin Oncol. 2003; 21:223-31.
51. Hansma AH, Broxterman HJ, van der Horst I, Yuana Y, Boven E, Giaccone G, Pinedo HM, Hoekman K. Recombinant human endostatin administered as a 28-day continuous intravenous infusion, followed by daily subcutaneous injections: a phase I and pharmacokinetic study in patients with advanced cancer. Ann Oncol. 2005; 16:1695-701.
52. Chen Z, Guo W, Cao J, Lv F, Zhang W, Qiu L, Li W, Ji D, Zhang S, Xia Z, Wang J, Li J. Endostar in combination with modified FOLFOX6 as an initial therapy in advanced colorectal cancer patients: a phase I clinical trial. Cancer Chemother Pharmacol. 2015; 75:547-57.