Novel etoposide analogue modulates expression of angiogenesis associated microRNAs and regulates cell proliferation by targeting STAT3 in breast cancer

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Srinivas, Chatla ^a   Ramaiah, M Janaki ^a,b   Lavanya, A ^a   Yerramsetty, Suresh ^a   Kavi Kishor, P B ^c   Basha, Shaik Anver ^a   Kamal, Ahmed ^a   Bhadra, Utpal ^d   Bhadra, Manika Pal ^a  

^a INDIAN INSTITUTE OF CHEMICAL TECHNOLOGY   (India)

^b SASTRA UNIVERSITY   (India)

^c OSMANIA UNIVERSITY   (India)

^d CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; ETOPOSIDE; ETOPOSIDE DERIVATIVE; MICRORNA; MICRORNA 15; MICRORNA 16; MICRORNA 17; MICRORNA 221; PROTEIN BCL 2; QUINAZOLINO 4BETA AMIDOPODOPHYLLOTOXIN; STAT3 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; BCL2 PROTEIN, HUMAN; CASPASE 9; MIRN15 MICRORNA, HUMAN; MIRN16 MICRORNA, HUMAN; MIRN17 MICRORNA, HUMAN; MIRN221 MICRORNA, HUMAN; PODOPHYLLOTOXIN; PROTEIN BINDING; QUINAZOLINE DERIVATIVE; QUINAZOLINO-4-AMIDOPODOPHYLLOTOXIN; SMALL INTERFERING RNA; STAT3 PROTEIN, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; APOPTOSIS; ARTICLE; BREAST CANCER; CELL PROLIFERATION; CONTROLLED STUDY; DRUG PROTEIN BINDING; DRUG TARGETING; GENE EXPRESSION; HUMAN; HUMAN CELL; MOLECULAR DOCKING; TUMOR VASCULARIZATION; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; BREAST NEOPLASMS; CELL CYCLE CHECKPOINT; CELL SURVIVAL; DNA DAMAGE; DRUG EFFECTS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; MCF-7 CELL LINE; METABOLISM; MOLECULAR MODEL; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; RNA INTERFERENCE; TUMOR CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL;

APOPTOSIS; BREAST NEOPLASMS; CASPASE 9; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; ENZYME ACTIVATION; ETOPOSIDE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MCF-7 CELLS; MICRORNAS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; NEOVASCULARIZATION, PATHOLOGIC; PODOPHYLLOTOXIN; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-2; QUINAZOLINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; STAT3 TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84950256269     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142006     Document Type: Article

References (60)

1. Key TJ, Verkasalo PK, Banks E. Epidemiology of breast cancer. The Lancet Oncology. 2001; 2 (3):133-40. doi: 10.1016/S1470-2045(00)00254-0 PMID: 11902563.
2. Shi M, Liu D, Duan H, Shen B, Guo N. Metastasis-related miRNAs, active players in breast cancer invasion, and metastasis. Cancer metastasis reviews. 2010; 29(4):785-99. doi: 10.1007/s10555-010-9265-9 PMID: 20938719.
3. Jain RK, Duda DG, Clark JW, Loeffler JS. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nature clinical practice Oncology. 2006; 3(1):24-40. doi: 10.1038/ncponc0403 PMID: 16407877.
4. Takahashi Y, Tucker SL, Kitadai Y, Koura AN, Bucana CD, Cleary KR, et al. Vessel counts and expression of vascular endothelial growth factor as prognostic factors in node-negative colon cancer. Archives of surgery. 1997; 132(5):541-6. PMID: 9161399.
5. Shinkaruk S, Bayle M, Lain G, Deleris G. Vascular endothelial cell growth factor (VEGF), an emerging target for cancer chemotherapy. Current medicinal chemistry Anti-cancer agents. 2003; 3(2):95-117. PMID: 12678905.
6. Schneider BP, Sledge GW Jr. Drug insight: VEGF as a therapeutic target for breast cancer. Nature clinical practice Oncology. 2007; 4(3):181-9. doi: 10.1038/ncponc0740 PMID: 17327858.
7. Regis G, Pensa S, Boselli D, Novelli F, Poli V. Ups and downs: the STAT1:STAT3 seesaw of Interferon andgp130 receptor signalling. Seminars in cell & developmental biology. 2008; 19(4):351-9. doi: 10.1016/j.semcdb.2008.06.004 PMID: 18620071.
8. Albasanz-Puig A, Murray J, Namekata M, Wijelath ES. Opposing roles of STAT-1 and STAT-3 in regulating vascular endothelial growth factor expression in vascular smooth muscle cells. Biochemical and biophysical research communications. 2012; 428(1):179-84. doi: 10.1016/j.bbrc.2012.10.037 PMID: 23068100.
9. Fossey SL, Liao AT, McCleese JK, Bear MD, Lin J, Li PK, et al. Characterization of STAT3 activation and expression in canine and human osteosarcoma. BMC cancer. 2009; 9:81. doi: 10.1186/1471-2407-9-81 PMID: 19284568; PubMed Central PMCID: PMC2666757.
10. Bid HK, Oswald D, Li C, London CA, Lin J, Houghton PJ. Anti-angiogenic activity of a small molecule STAT3 inhibitor LLL12. PloS one. 2012; 7(4):e35513. doi: 10.1371/journal.pone.0035513 PMID: 22530037; PubMed Central PMCID: PMC3328460.
11. Zushi S, Shinomura Y, Kiyohara T, Miyazaki Y, Kondo S, Sugimachi M, et al. STAT3 mediates the survival signal in oncogenic ras-transfected intestinal epithelial cells. International journal of cancer Journal international du cancer. 1998; 78(3):326-30. doi: 10.1002/(SICI)1097-0215(19981029)78:3<326::AID-IJC12>3.0.CO;2-4 PMID: 9766567.
12. Wei D, Le X, Zheng L, Wang L, Frey JA, Gao AC, et al. Stat3 activation regulates the expression of vascular endothelial growth factor and human pancreatic cancer angiogenesis and metastasis. Oncogene. 2003; 22(3):319-29. doi: 10.1038/sj.onc.1206122 PMID: 12545153.
13. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell. 2003; 113(1):25-36. PMID: 12679032.
14. Cohen SM, Brennecke J, Stark A. Denoising feedback loops by thresholding - a new role for micro-RNAs. Genes & development. 2006; 20(20):2769-72. doi: 10.1101/gad.1484606 PMID: 17043305.
15. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nature reviews Cancer. 2006; 6(4):259-69. doi: 10.1038/nrc1840 PMID: 16557279.
16. van Schooneveld E, Wildiers H, Vergote I, Vermeulen PB, Dirix LY, Van Laere SJ. Dysregulation of microRNAs in breast cancer and their potential role as prognostic and predictive biomarkers in patient management. Breast cancer research: BCR. 2015; 17:21. doi: 10.1186/s13058-015-0526-y PMID: 25849621; PubMed Central PMCID: PMC4332424.
17. Bossung V, Harbeck N. Angiogenesis inhibitors in the management of breast cancer. Current opinion in obstetrics & gynecology. 2010; 22(1):79-86. doi: 10.1097/GCO.0b013e328334e462 PMID: 19952746.
18. Chen HX, Cleck JN. Adverse effects of anticancer agents that target the VEGF pathway. Nature reviews Clinical oncology. 2009; 6(8):465-77. doi: 10.1038/nrclinonc.2009.94 PMID: 19581909.
19. Bellou S, Karali E, Bagli E, Al-Maharik N, Morbidelli L, Ziche M, et al. The isoflavone metabolite 6-methoxyequol inhibits angiogenesis and suppresses tumor growth. Molecular cancer. 2012; 11:35. doi: 10.1186/1476-4598-11-35 PMID: 22583931; PubMed Central PMCID: PMC3406996.
20. Auyeung KK, Law PC, Ko JK. Novel anti-angiogenic effects of formononetin in human colon cancer cells and tumor xenograft. Oncology reports. 2012; 28(6):2188-94. doi: 10.3892/or.2012.2056 PMID: 23023137.
21. Porcu E, Viola G, Bortolozzi R, Persano L, Mitola S, Ronca R, et al. TR-644 a novel potent tubulin binding agent induces impairment of endothelial cells function and inhibits angiogenesis. Angiogenesis. 2013; 16(3):647-62. doi: 10.1007/s10456-013-9343-z PMID: 23456551.
22. Ren X, Dai M, Lin LP, Li PK, Ding J. Anti-angiogenic and vascular disrupting effects of C9, anew micro-tubule-depolymerizing agent. British journal of pharmacology. 2009; 156(8):1228-38. doi: 10.1111/j.1476-5381.2009.00112.x PMID: 19302593; PubMed Central PMCID: PMC2697741.
23. Nathwani SM, Hughes L, Greene LM, Carr M, O'Boyle NM, McDonnell S, et al. Novel cis-restricted beta-lactam combretastatin A-4 analogues display anti-vascular and anti-metastatic properties in vitro. Oncology reports. 2013; 29(2):585-94. doi: 10.3892/or.2012.2181 PMID: 23232969.
24. Prudent R, Vassal-Stermann E, Nguyen CH, Mollaret M, Viallet J, Desroches-Castan A, et al. Azain-dole derivatives are inhibitors of microtubule dynamics, with anti-cancer and anti-angiogenic activities. British journal of pharmacology. 2013; 168(3):673-85. doi: 10.1111/j.1476-5381.2012.02230.x PMID: 23004938; PubMed Central PMCID: PMC3579287.
25. Kamal A, Tamboli JR, Ramaiah MJ, Adil SF, Pushpavalli SN, Ganesh R, et al. Quinazolino linked 4beta-amidopodophyllotoxin conjugates regulate angiogenic pathway and control breast cancer cell proliferation. Bioorganic & medicinal chemistry. 2013; 21(21):6414-26. doi: 10.1016/j.bmc.2013.08.051 PMID: 24055291.
26. Kumar A, Bora U. Molecular docking studies on inhibition of Stat3 dimerization by curcumin natural derivatives and its conjugates with amino acids. Bioinformation. 2012; 8(20):988-93. doi: 10.6026/97320630008988 PMID: 23275693; PubMed Central PMCID: PMC3524947.
27. Huang W, Dong Z, Wang F, Peng H, Liu JY, Zhang JT. A small molecule compound targeting STAT3 DNA-binding domain inhibits cancer cell proliferation, migration, and invasion. ACS chemical biology. 2014; 9(5):1188-96. doi: 10.1021/cb500071v PMID: 24661007; PubMed Central PMCID: PMC4033648.
28. Vangala JR, Dudem S, Jain N, Kalivendi SV. Regulation of PSMB5 protein and beta subunits of mammalian proteasome by constitutively activated signal transducer and activator of transcription 3 (STAT3): potential role in bortezomib-mediated anticancer therapy. The Journal of biological chemistry. 2014; 289(18):12612-22. doi: 10.1074/jbc.M113.542829 PMID: 24627483; PubMed Central PMCID: PMC4007451.
29. Kim Y, Kim SB, You YJ, Ahn BZ. Deoxypodophyllotoxin; the cytotoxic and antiangiogenic component from Pulsatilla koreana. Planta medica. 2002; 68(3):271-4. doi: 10.1055/s-2002-23140 PMID: 11914969.
30. Panigrahy D, Kaipainen A, Butterfield CE, Chaponis DM, Laforme AM, Folkman J, et al. Inhibition of tumor angiogenesis by oral etoposide. Experimental and therapeutic medicine. 2010; 1(5):739-46. doi: 10.3892/etm.2010.127 PMID: 22993597; PubMed Central PMCID: PMC3445956.
31. Claesson-Welsh L, Welsh M. VEGFA and tumour angiogenesis. Journal of internal medicine. 2013; 273(2):114-27. doi: 10.1111/joim.12019 PMID: 23216836.
32. Ando H, Okamoto A, Yokota M, Shimizu K, Asai T, Dewa T, et al. Development of a miR-92a delivery system for anti-angiogenesis-based cancer therapy. The journal of gene medicine. 2013; 15(1):20-7. doi: 10.1002/jgm.2690 PMID: 23239404.
33. Spinetti G, Fortunato O, Caporali A, Shantikumar S, Marchetti M, Meloni M, et al. MicroRNA-15aand microRNA-16 impair human circulating proangiogenic cell functions and are increased in the proangiogenic cells and serum of patients with critical limb ischemia. Circulation research. 2013; 112(2):335-46. doi: 10.1161/CIRCRESAHA.111.300418 PMID: 23233752; PubMed Central PMCID: PMC3616367.
34. Sun CY, She XM, Qin Y, Chu ZB, Chen L, Ai LS, et al. miR-15a and miR-16 affect the angiogenesis of multiple myeloma by targeting VEGF. Carcinogenesis. 2013; 34(2):426-35. doi: 10.1093/carcin/bgs333 PMID: 23104180.
35. Li H, Gupta S, Du WW, Yang BB. MicroRNA-17 inhibits tumor growth by stimulating T-cell mediated host immune response. Oncoscience. 2014; 1(7):531-9. PMID: 25594054; PubMed Central PMCID: PMC4278315.
36. Nicoli S, Knyphausen CP, Zhu LJ, Lakshmanan A, Lawson ND. miR-221 is required for endothelial tip cell behaviors during vascular development. Developmental cell. 2012; 22(2):418-29. doi: 10.1016/j.devcel.2012.01.008 PMID: 22340502; PubMed Central PMCID: PMC3285411.
37. Nahar S, Bose D, Kumar Panja S, Saha S, Maiti S. Anti-cancer therapeutic potential of quinazoline based small molecules via global upregulation of miRNAs. Chemical communications. 2014; 50 (35):4639-42. doi: 10.1039/c3cc49337g PMID: 24671295.
38. Shan G, Li Y, Zhang J, Li W, Szulwach KE, Duan R, et al. A small molecule enhances RNA interference and promotes microRNA processing. Nature biotechnology. 2008; 26(8):933-40. doi: 10.1038/nbt.1481 PMID: 18641635; PubMed Central PMCID: PMC2831467.
39. Melo S, Villanueva A, Moutinho C, Davalos V, Spizzo R, Ivan C, et al. Small molecule enoxacin is a cancer-specific growth inhibitor that acts by enhancing TAR RNA-binding protein 2-mediated microRNA processing. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(11):4394-9. doi: 10.1073/pnas.1014720108 PMID: 21368194; PubMed Central PMCID: PMC3060242.
40. Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, et al. MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PloS one. 2006; 1:e116. doi: 10.1371/journal.pone.0000116 PMID: 17205120; PubMed Central PMCID: PMC1762435.
41. Bhattacharya R, Nicoloso M, Arvizo R, Wang E, Cortez A, Rossi S, et al. MiR-15a and MiR-16 control Bmi-1 expression in ovarian cancer. Cancer research. 2009; 69(23):9090-5. doi: 10.1158/0008-5472.CAN-09-2552 PMID: 19903841; PubMed Central PMCID: PMC2859686.
42. Aggarwal BB, Kunnumakkara AB, Harikumar KB, Gupta SR, Tharakan ST, Koca C, et al. Signal Transducer and Activator of Transcription-3, Inflammation, and Cancer How Intimate Is the Relationship? Ann NyAcad Sci. 2009; 1171:59-76. doi: 10.1111/j.1749-6632.2009.04911.x PMID: WOS:000269657300008.
43. Pidgeon GP, Barr MP, Harmey JH, Foley DA, Bouchier-Hayes DJ. Vascular endothelial growth factor (VEGF) upregulates BCL-2 and inhibits apoptosis in human and murine mammary adenocarcinoma cells. Brit J Cancer. 2001; 85(2):273-8. doi: 10.1054/bjoc.2001.1876 PMID: WOS:000170152500023.
44. Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. Journal of Biological Chemistry. 1998; 273 (21):13313-6. doi: 10.1074/jbc.273.21.13313 PMID: WOS:000073768500088.
45. Kaneko T, Zhang ZC, Mantellini MG, Karl E, Zeitlin B, Verhaegen M, et al. Bcl-2 orchestrates a crosstalk between endothelial and tumor cells that promotes tumor growth. Cancer research. 2007; 67 (20):9685-93. doi: 10.1158/0008-5472.CAN-07-1497 PMID: WOS:000250286300012.
46. Choi HJ, Han JS. Overexpression of phospholipase D enhances Bcl-2 expression by activating STAT3 through independent activation of ERK and p38MAPK in HeLa cells. Biochimica et biophysica acta. 2012; 1823(6):1082-91. doi: 10.1016/j.bbamcr.2012.03.015 PMID: 22504301.
47. Niu GL, Wright KL, Huang M, Song LX, Haura E, Turkson J, et al. Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene. 2002; 21(13):2000-8. doi: 10.1038/sj/onc/1205260 PMID: WOS:000174827000006.
48. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao YX, Pestell RG, Albanese C, et al. Stat3 as an oncogene. Cell. 1999; 98(3):295-303. doi: 10.1016/S0092-8674(00)81959-5 PMID: WOS:000081950300005.
49. Guo CJ, Pan Q, Li DG, Sun H, Liu BW. miR-15band miR-16 are implicated in activation of the rat hepatic stellate cell: An essential role for apoptosis. Journal of hepatology. 2009; 50(4):766-78. doi: 10.1016/j.jhep.2008.11.025 PMID: 19232449.
50. Shen J, Wan R, Hu G, Yang L, Xiong J, Wang F, et al. miR-15band miR-16 induce the apoptosis of rat activated pancreatic stellate cells by targeting Bcl-2 in vitro. Pancreatology: official journal of the International Association of Pancreatology. 2012; 12(2):91-9. doi: 10.1016/j.pan.2012.02.008 PMID: 22487517.
51. Xia L, Zhang D, Du R, Pan Y, Zhao L, Sun S, et al. miR-15band miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. International journal of cancer Journal international du cancer. 2008; 123(2):372-9. doi: 10.1002/ijc.23501 PMID: 18449891.
52. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(39):13944-9. doi: 10.1073/pnas.0506654102 PMID: 16166262; PubMed Central PMCID: PMC1236577.
53. Scherr M, Elder A, Battmer K, Barzan D, Bomken S, Ricke-Hoch M, et al. Differential expression of miR-17-92 identifies BCL2 as a therapeutic target in BCR-ABL-positive B-lineage acute lymphoblastic leukemia. Leukemia. 2014; 28(3):554-65. doi: 10.1038/leu.2013.361 PMID: 24280866; PubMed Central PMCID: PMC3948162.
54. Ihle MA, Trautmann M, Kuenstlinger H, Huss S, Heydt C, Fassunke J, et al. miRNA-221 and miRNA-222 induce apoptosis via the KIT/AKT signalling pathway in gastrointestinal stromal tumours. Molecular oncology. 2015. doi: 10.1016/j.molonc.2015.03.013 PMID: 25898773.
55. Becker S, Groner B, Muller CW. Three-dimensional structure of the Stat3beta homodimer bound to DNA. Nature. 1998; 394(6689):145-51. doi: 10.1038/28101 PMID: 9671298.
56. Mueller MD, Vigne JL, Minchenko A, Lebovic DI, Leitman DC, Taylor RN. Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proceedings of the National Academy of Sciences of the United States of America. 2000; 97(20):10972-7. doi: 10.1073/pnas.200377097 PMID: 10995484; PubMed Central PMCID: PMC27133.
57. Tischer E, Mitchell R, Hartman T, Silva M, Gospodarowicz D, Fiddes JC, et al. The human geneforvascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. The Journal of biological chemistry. 1991; 266(18):11947-54. PMID: 1711045.
58. Repovic P, Fears CY, Gladson CL, Benveniste EN. Oncostatin-M induction of vascular endothelial growth factor expression in astroglioma cells. Oncogene. 2003; 22(50):8117-24. doi: 10.1038/sj.onc.1206922 PMID: 14603252.
59. Shi Q, Le X, Abbruzzese JL, Peng Z, Qian CN, Tang H, et al. Constitutive Sp1 activity is essential for differential constitutive expression of vascular endothelial growth factor in human pancreatic adenocarcinoma. Cancer research. 2001; 61(10):4143-54. PMID: 11358838.
60. Bowman T, Garcia R, Turkson J, Jove R. STATs in oncogenesis. Oncogene. 2000; 19(21):2474-88. doi: 10.1038/sj.onc.1203527 PMID: 10851046.