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Angiogenesis

Erschienen in:

Open Access 04.05.2017 | Review Paper

miRNAs: micro-managers of anticancer combination therapies

verfasst von: Judy R. van Beijnum, Elisa Giovannetti, Dennis Poel, Patrycja Nowak-Sliwinska, Arjan W. Griffioen

Erschienen in: Angiogenesis | Ausgabe 2/2017

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Abstract

Angiogenesis is one of the hallmarks of cancer progression and as such has been considered a target of therapeutic interest. However, single targeted agents have not fully lived up to the initial promise of anti-angiogenic therapy. Therefore, it has been suggested that combining therapies and agents will be the way forward in the oncology field. In recent years, microRNAs (miRNAs) have received considerable attention as drivers of tumor development and progression, either acting as tumor suppressors or as oncogenes (so-called oncomiRs), as well as in the process of tumor angiogenesis (angiomiRs). Not only from a functional, but also from a therapeutic view, miRNAs are attractive tools. Thus far, several mimics and antagonists of miRNAs have entered clinical development. Here, we review the provenance and promise of miRNAs as targets as well as therapeutics to contribute to anti-angiogenesis-based (combination) treatment of cancer.

Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674. doi:10.1016/j.cell.2011.02.013 PubMedCrossRef

Griffioen AW, Molema G (2000) Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacol Rev 52:237–268PubMed

Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298–307. doi:10.1038/nature10144 PubMedPubMedCentralCrossRef

Weis SM, Cheresh DA (2011) Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med 17:1359–1370. doi:10.1038/nm.2537 PubMedCrossRef

van Beijnum JR, Nowak-Sliwinska P, Huijbers EJM et al (2015) The great escape; the hallmarks of resistance to antiangiogenic therapy. Pharmacol Rev 67:441–461. doi:10.1124/PR.114.010215 PubMedCrossRef

Huijbers EJM, van Beijnum JR, Thijssen VL et al (2016) Role of the tumor stroma in resistance to anti-angiogenic therapy. Drug Resist Updat 25:26–37. doi:10.1016/j.drup.2016.02.002 PubMedCrossRef

Gotink KJ, Broxterman HJ, Labots M et al (2011) Lysosomal sequestration of sunitinib: a novel mechanism of drug resistance. Clin Cancer Res 17:7337–7346. doi:10.1158/1078-0432.CCR-11-1667 PubMedPubMedCentralCrossRef

Sethi S, Ali S, Sethi S, Sarkar FH (2014) MicroRNAs in personalized cancer therapy. Clin Genet 86:68–73. doi:10.1111/cge.12362 PubMedCrossRef

van Beijnum JR, Griffioen AW (2005) In silico analysis of angiogenesis associated gene expression identifies angiogenic stage related profiles. Biochim Biophys Acta—Rev Cancer 1755:121–134. doi:10.1016/j.bbcan.2005.06.001 CrossRef

10.

van Beijnum JR, Dings RP, van der Linden E et al (2006) Gene expression of tumor angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood 108:2339–2348. doi:10.1182/blood-2006-02-004291 PubMedCrossRef

11.

Nanda A, St Croix B (2004) Tumor endothelial markers: new targets for cancer therapy. Curr Opin Oncol 16:44–49PubMedCrossRef

12.

Poliseno L, Tuccoli A, Mariani L et al (2006) MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108:3068–3071. doi:10.1182/blood-2006-01-012369 PubMedCrossRef

13.

Wang S, Olson EN (2009) AngiomiRs—key regulators of angiogenesis. Curr Opin Genet Dev 19:205–211. doi:10.1016/j.gde.2009.04.002 PubMedPubMedCentralCrossRef

14.

Landskroner-Eiger S, Moneke I, Sessa WC (2013) miRNAs as modulators of angiogenesis. Cold Spring Harb Perspect Med 3:a006643. doi:10.1101/cshperspect.a006643 PubMedPubMedCentralCrossRef

15.

Suarez Y, Fernandez-Hernando C, Pober JS, Sessa WC (2007) Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 100:1164–1173. doi:10.1161/01.RES.0000265065.26744.17 PubMedCrossRef

16.

Heusschen R, van Gink M, Griffioen AW, Thijssen VL (2010) MicroRNAs in the tumor endothelium: novel controls on the angioregulatory switchboard. Biochim Biophys Acta 1805:87–96. doi:10.1016/j.bbcan.2009.09.005 PubMed

17.

Kuehbacher A, Urbich C, Dimmeler S (2008) Targeting microRNA expression to regulate angiogenesis. Trends Pharmacol Sci 29:12–15. doi:10.1016/j.tips.2007.10.014 PubMedCrossRef

18.

Anand S, Cheresh DA (2011) MicroRNA-mediated regulation of the angiogenic switch. Curr Opin Hematol 18:171–176. doi:10.1097/MOH.0b013e328345a180 PubMedPubMedCentralCrossRef

19.

Gallach S, Calabuig-Fariñas S, Jantus-Lewintre E, Camps C (2014) MicroRNAs: promising new antiangiogenic targets in cancer. Biomed Res Int 2014:878450. doi:10.1155/2014/878450 PubMedPubMedCentralCrossRef

20.

Wu F, Yang Z, Li G (2009) Role of specific microRNAs for endothelial function and angiogenesis. Biochem Biophys Res Commun 386:549–553. doi:10.1016/j.bbrc.2009.06.075 PubMedPubMedCentralCrossRef

21.

Fish JE, Santoro MM, Morton SU et al (2008) miR-126 regulates Angiogenic signaling and vascular integrity. Dev Cell 15:272–284. doi:10.1016/j.devcel.2008.07.008 PubMedPubMedCentralCrossRef

22.

Wang S, Aurora AB, Johnson BA et al (2008) The endothelial-specific microrna miR-126 governs vascular integrity and angiogenesis. Dev Cell 15:261–271. doi:10.1016/j.devcel.2008.07.002 PubMedPubMedCentralCrossRef

23.

Kuhnert F, Mancuso MR, Hampton J et al (2008) Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development 135:3989–3993. doi:10.1242/dev.029736 PubMedCrossRef

24.

Png KJ, Halberg N, Yoshida M, Tavazoie SF (2011) A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature 481:190–194. doi:10.1038/nature10661 PubMedCrossRef

25.

Würdinger T, Tannous BA, Saydam O et al (2008) miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 14:382–393. doi:10.1016/j.ccr.2008.10.005 PubMedPubMedCentralCrossRef

26.

Liu X-Q, Song W-J, Sun T-M et al (2011) Targeted delivery of antisense inhibitor of miRNA for antiangiogenesis therapy using cRGD-functionalized nanoparticles. Mol Pharm 8:250–259. doi:10.1021/mp100315q PubMedCrossRef

27.

Feng J, Huang T, Huang Q et al (2015) Pro-angiogenic microRNA-296 upregulates vascular endothelial growth factor and downregulates notch1 following cerebral ischemic injury. Mol Med Rep 12:8141–8147. doi:10.3892/mmr.2015.4436 PubMedCrossRef

28.

Li Y, Song Y-H, Li F et al (2009) microRNA-221 regulates high glucose-induced endothelial dysfunction. Biochem Biophys Res Commun 381:81–83. doi:10.1016/j.bbrc.2009.02.013 PubMedPubMedCentralCrossRef

29.

Hua Z, Lv Q, Ye W et al (2006) MiRNA-directed regulation of vegf and other angiogenic factors under hypoxia. PLoS ONE 1:e116. doi:10.1371/journal.pone.0000116 PubMedPubMedCentralCrossRef

30.

Dai X, Tan C (2015) Combination of microRNA therapeutics with small-molecule anticancer drugs: mechanism of action and co-delivery nanocarriers. Adv Drug Deliv Rev 81:184–197. doi:10.1016/j.addr.2014.09.010 PubMedCrossRef

31.

Shi Z, Chen Q, Li C et al (2014) MiR-124 governs glioma growth and angiogenesis and enhances chemosensitivity by targeting R-Ras and N-Ras. Neuro Oncol 16:1341–1353. doi:10.1093/neuonc/nou084 PubMedPubMedCentralCrossRef

32.

Cascio S, D’Andrea A, Ferla R et al (2010) miR-20b modulates VEGF expression by targeting HIF-1 alpha and STAT3 in MCF-7 breast cancer cells. J Cell Physiol 224:242–249. doi:10.1002/jcp.22126 PubMed

33.

Kong W, He L, Richards EJ et al (2014) Upregulation of miRNA-155 promotes tumour angiogenesis by targeting VHL and is associated with poor prognosis and triple-negative breast cancer. Oncogene 33:679–689. doi:10.1038/onc.2012.636 PubMedCrossRef

34.

Liu L-Z, Li C, Chen Q et al (2011) MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression. PLoS ONE 6:e19139. doi:10.1371/journal.pone.0019139 PubMedPubMedCentralCrossRef

35.

Polytarchou C, Iliopoulos D, Hatziapostolou M et al (2011) Akt2 regulates all Akt isoforms and promotes resistance to hypoxia through induction of miR-21 upon oxygen deprivation. Cancer Res 71:4720–4731. doi:10.1158/0008-5472.CAN-11-0365 PubMedPubMedCentralCrossRef

36.

Babae N, Bourajjaj M, Liu Y et al (2014) Systemic miRNA-7 delivery inhibits tumor angiogenesis and growth in murine xenograft glioblastoma. Oncotarget 5:6687–6700. doi:10.18632/oncotarget.2235 PubMedPubMedCentralCrossRef

37.

Nowak-Sliwinska P, Segura T, Iruela-Arispe ML (2014) The chicken chorioallantoic membrane model in biology, medicine and bioengineering. Angiogenesis 17:779–804. doi:10.1007/s10456-014-9440-7 PubMedPubMedCentralCrossRef

38.

Chan YC, Khanna S, Roy S, Sen CK (2011) miR-200b targets Ets-1 and is down-regulated by hypoxia to induce angiogenic response of endothelial cells. J Biol Chem 286:2047–2056. doi:10.1074/jbc.M110.158790 PubMedCrossRef

39.

Shi L, Zhang S, Wu H et al (2013) MiR-200c Increases the radiosensitivity of non-small-cell lung cancer cell line A549 by targeting VEGF-VEGFR2 pathway. PLoS ONE 8:e78344. doi:10.1371/journal.pone.0078344 PubMedPubMedCentralCrossRef

40.

Anand S, Majeti BK, Acevedo LM et al (2010) MicroRNA-132–mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat Med 16:909–914. doi:10.1038/nm.2186 PubMedPubMedCentralCrossRef

41.

Ling H, Fabbri M, Calin GA (2013) MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat Rev Drug Discov 12:847–865. doi:10.1038/nrd4140 PubMedPubMedCentralCrossRef

42.

M Mk, Goyal R (2016) LncRNA as a therapeutic target for angiogenesis. Curr Top Med Chem. https://www.ncbi.nlm.nih.gov/pubmed/27848894

43.

Jia P, Cai H, Liu X et al (2016) Long non-coding RNA H19 regulates glioma angiogenesis and the biological behavior of glioma-associated endothelial cells by inhibiting microRNA-29a. Cancer Lett 381:359–369. doi:10.1016/j.canlet.2016.08.009 PubMedCrossRef

44.

Gandhi NS, Tekade RK, Chougule MB (2014) Nanocarrier mediated delivery of siRNA/miRNA in combination with chemotherapeutic agents for cancer therapy: current progress and advances. J Control Releas 194:238–256. doi:10.1016/j.jconrel.2014.09.001 CrossRef

45.

Williams M, Cheng YY, Blenkiron C, Reid G (2016) Exploring mechanisms of microRNA downregulation in cancer. MicroRNA (Shariqah, United Arab Emirates). https://www.ncbi.nlm.nih.gov/pubmed/27928946

46.

Bader AG, Brown D, Winkler M (2010) The promise of microRNA replacement therapy. Cancer Res 70:7027–7030. doi:10.1158/0008-5472.CAN-10-2010 PubMedPubMedCentralCrossRef

47.

Li Z, Rana TM (2014) Therapeutic targeting of microRNAs: current status and future challenges. Nat Rev Drug Discov 13:622–638. doi:10.1038/nrd4359 PubMedCrossRef

48.

Rupaimoole R, Slack FJ (2017) MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov 16:203–222. doi:10.1038/nrd.2016.246 PubMedCrossRef

49.

van Rooij E, Kauppinen S (2014) Development of microRNA therapeutics is coming of age. EMBO Mol Med 6:851–864. doi:10.15252/emmm.201100899 PubMedPubMedCentralCrossRef

50.

Soriano A, París-Coderch L, Jubierre L et al (2016) MicroRNA-497 impairs the growth of chemoresistant neuroblastoma cells by targeting cell cycle, survival and vascular permeability genes. Oncotarget 7:9271–9287. doi:10.18632/oncotarget.7005 PubMedPubMedCentralCrossRef

51.

Cheng CJ, Bahal R, Babar IA et al (2014) MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature 518:107–110. doi:10.1038/nature13905 PubMedPubMedCentralCrossRef

52.

Würdinger T, Tannous BA (2009) Glioma angiogenesis: towards novel RNA therapeutics. Cell Adhes Migr 3:230–235. doi:10.4161/cam.3.2.7910 CrossRef

53.

Simonson B, Das S (2015) MicroRNA therapeutics: the next magic bullet? Mini Rev Med Chem 15:467–474PubMedPubMedCentralCrossRef

54.

Chen L, Zhang K, Shi Z et al (2014) A lentivirus-mediated miR-23b sponge diminishes the malignant phenotype of glioma cells in vitro and in vivo. Oncol Rep 31:1573–1580. doi:10.3892/or.2014.3012 PubMedCrossRef

55.

Li X, Su Y, Sun B et al (2016) An artificially designed interfering lncRNA expressed by oncolytic adenovirus competitively consumes oncomiRs to exert antitumor efficacy in hepatocellular carcinoma. Mol Cancer Ther 15:1436–1451. doi:10.1158/1535-7163.MCT-16-0096 PubMedCrossRef

56.

Su Y, Sun B, Lin X et al (2014) Therapeutic strategy with artificially-designed i-lncRNA targeting multiple oncogenic microRNAs exhibits effective antitumor activity in diffuse large B-cell lymphoma. Oncotarget 7:49143–49155. doi:10.18632/oncotarget.9237 CrossRef

57.

Xiao Z, Chen Y (2017) Identification of small molecule modulators of microRNA by library screening. Method Mol Biol. https://www.ncbi.nlm.nih.gov/pubmed/27924482

58.

Gumireddy K, Young DD, Xiong X et al (2008) Small-molecule inhibitors of microRNA miR-21 function. Angew Chemie Int Ed 47:7482–7484. doi:10.1002/anie.200801555 CrossRef

59.

Velagapudi SP, Cameron MD, Haga CL et al (2016) Design of a small molecule against an oncogenic noncoding RNA. Proc Natl Acad Sci USA 113:5898–5903. doi:10.1073/pnas.1523975113 PubMedPubMedCentralCrossRef

60.

Xiao Z, Li CH, Chan SL et al (2014) A small-molecule modulator of the tumor-suppressor miR34a inhibits the growth of hepatocellular carcinoma. Cancer Res 74:6236–6247. doi:10.1158/0008-5472.CAN-14-0855 PubMedCrossRef

61.

Lee S-Y, Lee S, Choi E et al (2016) Small molecule-mediated up-regulation of microRNA targeting a key cell death modulator BNIP3 improves cardiac function following ischemic injury. Sci Rep 6:23472. doi:10.1038/srep23472 PubMedPubMedCentralCrossRef

62.

Dowdy SF (2017) Overcoming cellular barriers for RNA therapeutics. Nat Biotechnol. doi:10.1038/nbt.3802 PubMed

63.

Nair JK, Willoughby JLS, Chan A et al (2014) Multivalent N-acetylgalactosamine-conjugated siRNA localizes in hepatocytes and elicits robust RNAi-mediated gene silencing. J Am Chem Soc 136:16958–16961. doi:10.1021/ja505986a PubMedCrossRef

64.

Reid G, Kao SC, Pavlakis N et al (2016) Clinical development of TargomiRs, a miRNA mimic-based treatment for patients with recurrent thoracic cancer. Epigenomics 8:1079–1085. doi:10.2217/epi-2016-0035 PubMedCrossRef

65.

Yousefi A, Bourajjaj M, Babae N et al (2014) Anginex lipoplexes for delivery of anti-angiogenic siRNA. Int J Pharm 472:175–184. doi:10.1016/j.ijpharm.2014.06.028 PubMedCrossRef

66.

Beg MS, Brenner AJ, Sachdev J et al (2016) Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Invest New Drugs. doi:10.1007/s10637-016-0407-y PubMed

67.

Arunachalam G, Lakshmanan AP, Samuel SM et al (2016) Molecular interplay between microRNA-34a and Sirtuin1 in hyperglycemia-mediated impaired angiogenesis in endothelial cells: effects of metformin. J Pharmacol Exp Ther 356:314–323. doi:10.1124/jpet.115.226894 PubMedCrossRef

68.

Zhao Y, Tu M-J, Yu Y-F et al (2015) Combination therapy with bioengineered miR-34a prodrug and doxorubicin synergistically suppresses osteosarcoma growth. Biochem Pharmacol 98:602–613. doi:10.1016/j.bcp.2015.10.015 PubMedPubMedCentralCrossRef

69.

Yu G, Yao W, Xiao W et al (2014) MicroRNA-34a functions as an anti-metastatic microRNA and suppresses angiogenesis in bladder cancer by directly targeting CD44. J Exp Clin Cancer Res 33:779. doi:10.1186/s13046-014-0115-4 PubMedPubMedCentralCrossRef

70.

Yang F, Li Q, Gong Z et al (2013) MicroRNA-34a targets Bcl-2 and sensitizes human hepatocellular carcinoma cells to sorafenib treatment. Technol Cancer Res Treat 13:77–86. doi:10.7785/tcrt.2012.500364 PubMedCrossRef

71.

Costa PM, Cardoso AL, Custódia C et al (2015) MiRNA-21 silencing mediated by tumor-targeted nanoparticles combined with sunitinib: a new multimodal gene therapy approach for glioblastoma. J Control Release 207:31–39. doi:10.1016/j.jconrel.2015.04.002 PubMedCrossRef

72.

Costa PM, Cardoso AL, Nóbrega C et al (2013) MicroRNA-21 silencing enhances the cytotoxic effect of the antiangiogenic drug sunitinib in glioblastoma. Hum Mol Genet 22:904–918. doi:10.1093/hmg/dds496 PubMedCrossRef

73.

Passadouro M, Pedroso de Lima MC, Faneca H (2014) MicroRNA modulation combined with sunitinib as a novel therapeutic strategy for pancreatic cancer. Int J Nanomedicine 9:3203–3217. doi:10.2147/IJN.S64456 PubMedPubMedCentral

74.

Liu H, Liu Z, Jiang B et al (2015) Synthetic miR-145 mimic enhances the cytotoxic effect of the antiangiogenic drug sunitinib in glioblastoma. Cell Biochem Biophys 72:551–557. doi:10.1007/s12013-014-0501-8 PubMedCrossRef

75.

Gotink KJ, Verheul HMW (2010) Anti-angiogenic tyrosine kinase inhibitors: what is their mechanism of action? Angiogenesis 13:1–14. doi:10.1007/s10456-009-9160-6 PubMedCrossRef

76.

Thijssen V, Postel R, Brandwijk R (2006) Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci USA. https://www.ncbi.nlm.nih.gov/pubmed/17043243

77.

Wu SY, Rupaimoole R, Shen F et al (2016) A miR-192-EGR1-HOXB9 regulatory network controls the angiogenic switch in cancer. Nat Commun 7:11169. doi:10.1038/ncomms11169 PubMedPubMedCentralCrossRef

78.

Lee SH, Jung YD, Choi YS, Lee YM (2015) Targeting of RUNX3 by miR-130a and miR-495 cooperatively increases cell proliferation and tumor angiogenesis in gastric cancer cells. Oncotarget 6:33269–33278. doi:10.18632/oncotarget.5037 PubMedPubMedCentralCrossRef

79.

Pihlmann M, Askou AL, Aagaard L et al (2012) Adeno-associated virus-delivered polycistronic microRNA-clusters for knockdown of vascular endothelial growth factor in vivo. J Gene Med 14:328–338. doi:10.1002/jgm.2623 PubMedCrossRef

80.

Askou AL, Aagaard L, Kostic C et al (2015) Multigenic lentiviral vectors for combined and tissue-specific expression of miRNA—and protein-based antiangiogenic factors. Mol Ther Methods Clin Dev 2:14064. doi:10.1038/mtm.2014.64 PubMedPubMedCentralCrossRef

81.

Khella HWZ, Butz H, Ding Q et al (2015) miR-221/222 are involved in response to sunitinib treatment in metastatic renal cell carcinoma. Mol Ther 23:1748–1758. doi:10.1038/mt.2015.129 PubMedPubMedCentralCrossRef

82.

García-Donas J, Beuselinck B, Inglada-Pérez L et al (2016) Deep sequencing reveals microRNAs predictive of antiangiogenic drug response. JCI Insight 1:e86051. doi:10.1172/jci.insight.86051 PubMedPubMedCentralCrossRef

83.

Griffioen AW, Mans LA, de Graaf AMA et al (2012) Rapid angiogenesis onset after discontinuation of sunitinib treatment of renal cell carcinoma patients. Clin Cancer Res 18:3961–3971. doi:10.1158/1078-0432.CCR-12-0002 PubMedPubMedCentralCrossRef

84.

Goto Y, Kurozumi A, Nohata N et al (2016) The microRNA signature of patients with sunitinib failure: regulation of UHRF1 pathways by microRNA-101 in renal cell carcinoma. Oncotarget 7:59070–59086. doi:10.18632/oncotarget.10887 PubMedPubMedCentralCrossRef

85.

Merhautova J, Hezova R, Poprach A et al (2015) MiR-155 and miR-484 are associated with time to progression in metastatic renal cell carcinoma treated with sunitinib. Biomed Res Int 2015:941980. doi:10.1155/2015/941980 PubMedPubMedCentralCrossRef

86.

Prior C, Perez-Gracia JL, Garcia-Donas J et al (2014) Identification of tissue microRNAs predictive of sunitinib activity in patients with metastatic renal cell carcinoma. PLoS ONE 9:e86263. doi:10.1371/journal.pone.0086263 PubMedPubMedCentralCrossRef

87.

Berkers J, Govaere O, Wolter P et al (2013) A possible role for microRNA-141 down-regulation in sunitinib resistant metastatic clear cell renal cell carcinoma through induction of epithelial-to-mesenchymal transition and hypoxia resistance. J Urol 189:1930–1938. doi:10.1016/j.juro.2012.11.133 PubMedCrossRef

88.

Gámez-Pozo A, Antón-Aparicio LM, Bayona C et al (2012) MicroRNA expression profiling of peripheral blood samples predicts resistance to first-line sunitinib in advanced renal cell carcinoma patients. Neoplasia 14:1144–1152PubMedPubMedCentralCrossRef

89.

Shivapurkar N, Mikhail S, Navarro R et al (2013) Decrease in blood miR-296 predicts chemotherapy resistance and poor clinical outcome in patients receiving systemic chemotherapy for metastatic colon cancer. Int J Colorectal Dis 28:887. doi:10.1007/s00384-012-1560-1 PubMedCrossRef

90.

Fojo T (2007) Multiple paths to a drug resistance phenotype: mutations, translocations, deletions and amplification of coding genes or promoter regions, epigenetic changes and microRNAs. Drug Resist Updat 10:59–67. doi:10.1016/j.drup.2007.02.002 PubMedCrossRef

91.

Blower PE, Chung J-H, Verducci JS et al (2008) MicroRNAs modulate the chemosensitivity of tumor cells. Mol Cancer Ther 7:1–9. doi:10.1158/1535-7163.MCT-07-0573 PubMedCrossRef

92.

Shi L, Chen J, Yang J et al (2010) MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax/Bcl-2 ratio and caspase-3 activity. Brain Res 1352:255–264. doi:10.1016/j.brainres.2010.07.009 PubMedCrossRef

93.

Li W-Q, Yu H-Y, Li Y-M et al (2014) Higher LRRFIP1 expression in glioblastoma multiforme is associated with better response to teniposide, a type II topoisomerase inhibitor. Biochem Biophys Res Commun 446:1261–1267. doi:10.1016/j.bbrc.2014.03.105 PubMedCrossRef

94.

Si M-L, Zhu S, Wu H et al (2007) miR-21-mediated tumor growth. Oncogene 26:2799–2803. doi:10.1038/sj.onc.1210083 PubMedCrossRef

95.

De Mattos-Arruda L, Bottai G, Nuciforo PG et al (2015) MicroRNA-21 links epithelial-to-mesenchymal transition and inflammatory signals to confer resistance to neoadjuvant trastuzumab and chemotherapy in HER2-positive breast cancer patients. Oncotarget 6:37269–37280. doi:10.18632/oncotarget.5495 PubMedPubMedCentralCrossRef

96.

Hwang J-H, Voortman J, Giovannetti E et al (2010) Identification of microRNA-21 as a biomarker for chemoresistance and clinical outcome following adjuvant therapy in resectable pancreatic cancer. PLoS ONE 5:e10630. doi:10.1371/journal.pone.0010630 PubMedPubMedCentralCrossRef

97.

Jamieson NB, Morran DC, Morton JP et al (2012) MicroRNA molecular profiles associated with diagnosis, clinicopathologic criteria, and overall survival in patients with resectable pancreatic ductal adenocarcinoma. Clin Cancer Res 18:534–545. doi:10.1158/1078-0432.CCR-11-0679 PubMedCrossRef

98.

Frampton AE, Castellano L, Colombo T et al (2014) MicroRNAs cooperatively inhibit a network of tumor suppressor genes to promote pancreatic tumor growth and progression. Gastroenterology 146(268–77):e18. doi:10.1053/j.gastro.2013.10.010

99.

Mei Y, Gao C, Wang K et al (2014) Effect of microRNA-210 on prognosis and response to chemotherapeutic drugs in pediatric acute lymphoblastic leukemia. Cancer Sci 105:463–472. doi:10.1111/cas.12370 PubMedPubMedCentralCrossRef

100.

Lee D, Sun S, Zhang XQ et al (2015) MicroRNA-210 and endoplasmic reticulum chaperones in the regulation of chemoresistance in glioblastoma. J Cancer 6:227–232. doi:10.7150/jca.10765 PubMedPubMedCentralCrossRef

101.

Nicoli S, Standley C, Walker P et al (2010) MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature 464:1196–1200. doi:10.1038/nature08889 PubMedPubMedCentralCrossRef

102.

Zhu X, Li H, Long L et al (2012) miR-126 enhances the sensitivity of non-small cell lung cancer cells to anticancer agents by targeting vascular endothelial growth factor A. Acta Biochim Biophys Sin (Shanghai) 44:519–526. doi:10.1093/abbs/gms026 CrossRef

103.

Saito Y, Friedman JM, Chihara Y et al (2009) Epigenetic therapy upregulates the tumor suppressor microRNA-126 and its host gene EGFL7 in human cancer cells. Biochem Biophys Res Commun 379:726–731. doi:10.1016/j.bbrc.2008.12.098 PubMedCrossRef

104.

Berndsen RH, Abdul UK, Weiss A et al (2017) Epigenetic approach for angiostatic therapy: promising combinations for cancer treatment. Angiogenesis. doi:10.1007/s10456-017-9551-z PubMed

105.

Wang S, Zhu L, Zuo W et al (2016) MicroRNA-mediated epigenetic targeting of Survivin significantly enhances the antitumor activity of paclitaxel against non-small cell lung cancer. Oncotarget 7:37693–37713. doi:10.18632/oncotarget.9264 PubMedPubMedCentralCrossRef

106.

Bi C, Chung T-H, Huang G et al (2015) Genome-wide pharmacologic unmasking identifies tumor suppressive microRNAs in multiple myeloma. Oncotarget 6:26508–26518. doi:10.18632/oncotarget.4769 PubMedPubMedCentralCrossRef

107.

Zhao J, Fu W, Liao H et al (2015) The regulatory and predictive functions of miR-17 and miR-92 families on cisplatin resistance of non-small cell lung cancer. BMC Cancer 15:731. doi:10.1186/s12885-015-1713-z PubMedPubMedCentralCrossRef

108.

Zhao H-Y, Ooyama A, Yamamoto M et al (2008) Down regulation of c-Myc and induction of an angiogenesis inhibitor, thrombospondin-1, by 5-FU in human colon cancer KM12C cells. Cancer Lett 270:156–163. doi:10.1016/j.canlet.2008.04.045 PubMedCrossRef

109.

Pineau P, Volinia S, McJunkin K et al (2010) miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci USA 107:264–269. doi:10.1073/pnas.0907904107 PubMedCrossRef

110.

Chen L, Zhang J, Han L et al (2012) Downregulation of miR-221/222 sensitizes glioma cells to temozolomide by regulating apoptosis independently of p53 status. Oncol Rep 27:854–860. doi:10.3892/or.2011.1535 PubMedCrossRef

111.

Ye Z, Hao R, Cai Y et al (2016) Knockdown of miR-221 promotes the cisplatin-inducing apoptosis by targeting the BIM-Bax/Bak axis in breast cancer. Tumour Biol 37:4509–4515. doi:10.1007/s13277-015-4267-4 PubMedCrossRef

112.

Park J-K, Lee EJ, Esau C, Schmittgen TD (2009) Antisense inhibition of microRNA-21 or -221 arrests cell cycle, induces apoptosis, and sensitizes the effects of gemcitabine in pancreatic adenocarcinoma. Pancreas 38:e190–e199. doi:10.1097/MPA.0b013e3181ba82e1 PubMedCrossRef

113.

Gan R, Yang Y, Yang X et al (2014) Downregulation of miR-221/222 enhances sensitivity of breast cancer cells to tamoxifen through upregulation of TIMP3. Cancer Gene Ther 21:290–296. doi:10.1038/cgt.2014.29 PubMedCrossRef

114.

Chen D, Yan W, Liu Z et al (2016) Downregulation of miR-221 enhances the sensitivity of human oral squamous cell carcinoma cells to Adriamycin through upregulation of TIMP3 expression. Biomed Pharmacother 77:72–78. doi:10.1016/j.biopha.2015.12.002 PubMedCrossRef

115.

Qi JH, Anand-Apte B (2015) Tissue inhibitor of metalloproteinase-3 (TIMP3) promotes endothelial apoptosis via a caspase-independent mechanism. Apoptosis 20:523–534. doi:10.1007/s10495-014-1076-y PubMedPubMedCentralCrossRef

116.

Schaake-Koning C, van den Bogaert W, Dalesio O et al (1992) Effects of concomitant cisplatin and radiotherapy on inoperable non-small-cell lung cancer. N Engl J Med 326:524–530. doi:10.1056/NEJM199202203260805 PubMedCrossRef

117.

Chinot OL, Wick W, Mason W et al (2014) Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 370:709–722. doi:10.1056/NEJMoa1308345 PubMedCrossRef

118.

Forastiere AA, Goepfert H, Maor M et al (2003) Concurrent chemotherapy and radiotherapy for organ preservation in advanced laryngeal cancer. N Engl J Med 349:2091–2098. doi:10.1056/NEJMoa031317 PubMedCrossRef

119.

Overgaard J (2007) Hypoxic radiosensitization: adored and ignored. J Clin Oncol 25:4066–4074. doi:10.1200/JCO.2007.12.7878 PubMedCrossRef

120.

Curtin NJ (2012) DNA repair dysregulation from cancer driver to therapeutic target. Nat Rev Cancer 12:801–817. doi:10.1038/nrc3399 PubMedCrossRef

121.

West C, Davidson S, Roberts S, Hunter R (1993) Intrinsic radiosensitivity and prediction of patient response to radiotherapy for carcinoma of the cervix. Br J Cancer 68:819–823. doi:10.1038/bjc.1993.434 PubMedPubMedCentralCrossRef

122.

Kleibeuker EA, Fokas E, Allen PD et al (2016) Low dose angiostatic treatment counteracts radiotherapy-induced tumor perfusion and enhances the anti-tumor effect. Oncotarget 7:76613–76627. doi:10.18632/oncotarget.12814 PubMedPubMedCentral

123.

Kleibeuker EA, Griffioen AW, Verheul HM et al (2012) Combining angiogenesis inhibition and radiotherapy: a double-edged sword. Drug Resist Updat 15:173–182. doi:10.1016/j.drup.2012.04.002 PubMedCrossRef

124.

Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58–62. doi:10.1126/science.1104819 PubMedCrossRef

125.

Dings RPM, Loren M, Heun H et al (2007) Scheduling of radiation with angiogenesis inhibitors anginex and avastin improves therapeutic outcome via vessel normalization. Clin Cancer Res 13:3395–3402. doi:10.1158/1078-0432.CCR-06-2441 PubMedPubMedCentralCrossRef

126.

Hamming LC, Slotman BJ, Verheul HMW, Thijssen VL (2017) The clinical application of angiostatic therapy in combination with radiotherapy: past, present, future. Angiogenesis. doi:10.1007/s10456-017-9546-9 PubMedPubMedCentral

127.

Begg AC, Stewart FA, Vens C (2011) Strategies to improve radiotherapy with targeted drugs. Nat Rev Cancer 11:239–253. doi:10.1038/nrc3007 PubMedCrossRef

128.

Kulshreshtha R, Ferracin M, Wojcik SE et al (2007) A microRNA signature of hypoxia. Mol Cell Biol 27:1859–1867. doi:10.1128/MCB.01395-06 PubMedPubMedCentralCrossRef

129.

Fasanaro P, D’Alessandra Y, Di Stefano V et al (2008) MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 283:15878–15883. doi:10.1074/jbc.M800731200 PubMedPubMedCentralCrossRef

130.

Camps C, Buffa FM, Colella S et al (2008) hsa-miR-210 Is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res 14:1340–1348. doi:10.1158/1078-0432.CCR-07-1755 PubMedCrossRef

131.

Grosso S, Doyen J, Parks SK et al (2013) MiR-210 promotes a hypoxic phenotype and increases radioresistance in human lung cancer cell lines. Cell Death Dis 4:e544. doi:10.1038/cddis.2013.71 PubMedPubMedCentralCrossRef

132.

Yang W, Sun T, Cao J et al (2012) Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp Cell Res 318:944–954. doi:10.1016/j.yexcr.2012.02.010 PubMedCrossRef

133.

Lou Y-L, Guo F, Liu F et al (2012) miR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia. Mol Cell Biochem 370:45–51. doi:10.1007/s11010-012-1396-6 PubMedCrossRef

134.

Yang W, Wei J, Sun T, Liu F (2013) Effects of knockdown of miR-210 in combination with ionizing radiation on human hepatoma xenograft in nude mice. Radiat Oncol 8:102. doi:10.1186/1748-717X-8-102 PubMedPubMedCentralCrossRef

135.

Yang W, Wei J, Guo T et al (2014) Knockdown of miR-210 decreases hypoxic glioma stem cells stemness and radioresistance. Exp Cell Res 326:22–35. doi:10.1016/j.yexcr.2014.05.022 PubMedCrossRef

136.

Yang D, Wang J, Xiao M et al (2016) Role of Mir-155 in controlling HIF-1α level and promoting endothelial cell maturation. Sci Rep 6:35316. doi:10.1038/srep35316 PubMedPubMedCentralCrossRef

137.

Robertson ED, Wasylyk C, Ye T et al (2014) The oncogenic microRNA Hsa-miR-155-5p targets the transcription factor ELK3 and links it to the hypoxia response. PLoS ONE 9:e113050. doi:10.1371/journal.pone.0113050 PubMedPubMedCentralCrossRef

138.

Babar IA, Czochor J, Steinmetz A et al (2011) Inhibition of hypoxia-induced miR-155 radiosensitizes hypoxic lung cancer cells. Cancer Biol Ther 12:908–914. doi:10.4161/cbt.12.10.17681 PubMedPubMedCentralCrossRef

139.

Wang Y, Sun L (2016) Knockdown of LMP1-induced miR-155 sensitizes nasopharyngeal carcinoma cells to radiotherapy in vitro. Oncol Lett 11:3451–3456. doi:10.3892/ol.2016.4400 PubMedPubMedCentral

140.

Gasparini P, Lovat F, Fassan M et al (2014) Protective role of miR-155 in breast cancer through RAD51 targeting impairs homologous recombination after irradiation. Proc Natl Acad Sci 111:4536–4541. doi:10.1073/pnas.1402604111 PubMedPubMedCentralCrossRef

141.

Cortez MA, Valdecanas D, Zhang X et al (2014) Therapeutic delivery of miR-200c enhances radiosensitivity in lung cancer. Mol Ther 22:1494–1503. doi:10.1038/mt.2014.79 PubMedPubMedCentralCrossRef

142.

Cortez MA, Valdecanas D, Niknam S et al (2015) In vivo delivery of miR-34a sensitizes lung tumors to radiation through RAD51 regulation. Mol Ther Nucleic Acids 4:e270. doi:10.1038/mtna.2015.47 PubMedPubMedCentralCrossRef

143.

Ma W, Ma C, Zhou N et al (2016) Up- regulation of miR-328-3p sensitizes non-small cell lung cancer to radiotherapy. Sci Rep 6:31651. doi:10.1038/srep31651 PubMedPubMedCentralCrossRef

144.

Agostinis P, Berg K, Cengel KA et al (2011) Photodynamic therapy of cancer: an update. CA Cancer J Clin 61:250–281. doi:10.3322/caac.20114 PubMedPubMedCentralCrossRef

145.

Lim SH, Nowak-Sliwinska P, Kamarulzaman FA et al (2010) The neovessel occlusion efficacy of 15-hydroxypurpurin-7-lactone dimethyl ester induced with photodynamic therapy. Photochem Photobiol 86:397–402. doi:10.1111/j.1751-1097.2009.00684.x PubMedCrossRef

146.

Babilas P, Schreml S, Landthaler M, Szeimies R-M (2010) Photodynamic therapy in dermatology: state-of-the-art. Photodermatol Photoimmunol Photomed 26:118–132. doi:10.1111/j.1600-0781.2010.00507.x PubMedCrossRef

147.

Allison RR, Downie GH, Cuenca R et al (2004) Photosensitizers in clinical PDT. Photodiagnosis Photodyn Ther 1:27–42. doi:10.1016/S1572-1000(04)00007-9 PubMedCrossRef

148.

Rumie Vittar NB, Lamberti MJ, Pansa MF et al (2013) Ecological photodynamic therapy: new trend to disrupt the intricate networks within tumor ecosystem. Biochim Biophys Acta 1835:86–99. doi:10.1016/j.bbcan.2012.10.004 PubMed

149.

Nowak-Sliwinska P, van Beijnum JR, van Berkel M et al (2010) Vascular regrowth following photodynamic therapy in the chicken embryo chorioallantoic membrane. Angiogenesis 13:281–292. doi:10.1007/s10456-010-9185-x PubMedPubMedCentralCrossRef

150.

Weiss A, Ding X, van Beijnum JR et al (2015) Rapid optimization of drug combinations for the optimal angiostatic treatment of cancer. Angiogenesis 18:233–244. doi:10.1007/s10456-015-9462-9 PubMedPubMedCentralCrossRef

151.

Griffioen AW, Weiss A, Berndsen RH et al (2014) The emerging quest for the optimal angiostatic combination therapy. Biochem Soc Trans 42:1608–1615. doi:10.1042/BST20140193 PubMedCrossRef

152.

Weiss A, Den Bergh H, van Griffioen AW, Nowak-Sliwinska P (2012) Angiogenesis inhibition for the improvement of photodynamic therapy: the revival of a promising idea. Biochim Biophys Acta Rev Cancer 1826:53–70. doi:10.1016/j.bbcan.2012.03.003 CrossRef

153.

Casas A, Di Venosa G, Hasan T, Batlle Al (2011) Mechanisms of resistance to photodynamic therapy. Curr Med Chem 18:2486–2515PubMedPubMedCentralCrossRef

154.

Bach D, Fuereder J, Karbiener M et al (2013) Comprehensive analysis of alterations in the miRNome in response to photodynamic treatment. J Photochem Photobiol B 120:74–81. doi:10.1016/j.jphotobiol.2013.01.012 PubMedCrossRef

155.

Kushibiki T (2010) Photodynamic therapy induces microRNA-210 and -296 expression in HeLa cells. J Biophotonics 3:368–372. doi:10.1002/jbio.200900082 PubMedCrossRef

156.

Nowak-Sliwinska P, Weiss A, van Beijnum JR et al (2012) Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion. J Cell Mol Med 16:1553–1562. doi:10.1111/j.1582-4934.2011.01440.x PubMedPubMedCentralCrossRef

157.

Chakrabarti M, Banik NL, Ray SK (2013) Photofrin based photodynamic therapy and miR-99a transfection inhibited FGFR3 and PI3 K/Akt signaling mechanisms to control growth of human glioblastoma In vitro and in vivo. PLoS ONE 8:e55652. doi:10.1371/journal.pone.0055652 PubMedPubMedCentralCrossRef

158.

Kuusk T, Albiges L, Escudier B et al (2017) Antiangiogenic therapy combined with immune checkpoint blockade in renal cancer. Angiogenesis. doi:10.1007/s10456-017-9550-0 PubMed

159.

Ramjiawan RR, Griffioen AW, Duda DG (2017) Anti-angiogenesis for cancer revisited: is there a role for combinations with immunotherapy? Angiogenesis. doi:10.1007/s10456-017-9552-y PubMed

160.

Nowak-Sliwinska P, Weiss A, Ding X et al (2016) Optimization of drug combinations using feedback system control. Nat Protoc 11:302–315. doi:10.1038/nprot.2016.017 PubMedCrossRef

161.

Weiss A, Nowak-Sliwinska P (2016) Current trends in multidrug optimization. J Lab Autom. doi:10.1177/2472630316682338 PubMed

Titel: miRNAs: micro-managers of anticancer combination therapies
verfasst von: Judy R. van Beijnum
Elisa Giovannetti
Dennis Poel
Patrycja Nowak-Sliwinska
Arjan W. Griffioen
Publikationsdatum: 04.05.2017
Verlag: Springer Netherlands
Erschienen in: Angiogenesis / Ausgabe 2/2017
Print ISSN: 0969-6970
Elektronische ISSN: 1573-7209
DOI: https://doi.org/10.1007/s10456-017-9545-x

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