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Published in: Journal of Translational Medicine 1/2012

Open Access 01-12-2012 | Research

The association of blood angioregulatory microRNA levels with circulating endothelial cells and angiogenic proteins in patients receiving dacarbazine and interferon

Authors: Pierre L Triozzi, Susan Achberger, Wayne Aldrich, Arun D Singh, Ronald Grane, Ernest C Borden

Published in: Journal of Translational Medicine | Issue 1/2012

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Abstract

Background

Blood biomarkers are needed to monitor anti-angiogenic treatments for cancer. The association of blood levels of microRNAs (miRs) implicated in angiogenesis with circulating endothelial cells (CEC) and with angiogenic proteins was examined in patients administered drugs with anti-angiogenic activity.

Methods

Blood was collected from patients with uveal melanoma enrolled on an adjuvant therapy trial in which they were treated sequentially with dacarbazine and interferon-alfa-2b. Plasma levels of nine angioregulatory miRs, miR-16, 20a, 106a, 125b, 126, 146a, 155, 199a, and 221, were determined by quantitative real time polymerase chain reaction; CEC, by semi-automated immunomagnetic; and plasma angiogenic proteins, by enzyme linked immunosorbent assays.

Results

Levels of miR-199a were positively correlated and miR-106a negatively correlated with CEC pre-therapy. Decreases in miR-126 and miR-199a and increases in miR-16 and miR-106a were observed after interferon-alfa-2b, but not after dacarbazine. CEC also increased after treatment with interferon but not after treatment with dacarbazine. Levels of miRs did not correlate with levels of vascular endothelial growth factor, basic fibroblast growth factor, and interleukin-8. Angiogenic proteins also did not change significantly with treatment.

Conclusions

Blood levels of specific angioregulatory miRs are associated with CEC, and changes in specific angioregulatory miRs parallel increases in CEC after treatment with interferon-alfa-2b. Blood levels of specific angioregulatory miRs are not associated with levels of angiogenic proteins. miRs warrant further evaluation as blood biomarkers of angiogenesis.
Appendix
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Literature
1.
go back to reference Bertolini F, Marighetti P, Shaked Y: Cellular and soluble markers of tumor angiogenesis: from patient selection to the identification of the most appropriate postresistance therapy. Biochim Biophys Acta. 2010, 1806: 131-137.PubMed Bertolini F, Marighetti P, Shaked Y: Cellular and soluble markers of tumor angiogenesis: from patient selection to the identification of the most appropriate postresistance therapy. Biochim Biophys Acta. 2010, 1806: 131-137.PubMed
2.
go back to reference Gruenwald V, Beutel G, Schuch-Jantsch S, Reuter C, Ivanyi P, Ganser A, Haubitz M: Circulating endothelial cells are an early predictor in renal cell carcinoma for tumor response to sunitinib. BMC Cancer. 2010, 10: 695-10.1186/1471-2407-10-695.CrossRefPubMedPubMedCentral Gruenwald V, Beutel G, Schuch-Jantsch S, Reuter C, Ivanyi P, Ganser A, Haubitz M: Circulating endothelial cells are an early predictor in renal cell carcinoma for tumor response to sunitinib. BMC Cancer. 2010, 10: 695-10.1186/1471-2407-10-695.CrossRefPubMedPubMedCentral
3.
go back to reference Starlinger P, Brugger P, Reiter C, Schauer D, Sommerfeldt S, Tamandl D, Kuehrer I, Schoppmann SF, Gnant M, Brostjan C: Discrimination between circulating endothelial cells and blood cell populations with overlapping phenotype reveals distinct regulation and predictive potential in cancer therapy. Neoplasia. 2011, 13: 980-990.CrossRefPubMedPubMedCentral Starlinger P, Brugger P, Reiter C, Schauer D, Sommerfeldt S, Tamandl D, Kuehrer I, Schoppmann SF, Gnant M, Brostjan C: Discrimination between circulating endothelial cells and blood cell populations with overlapping phenotype reveals distinct regulation and predictive potential in cancer therapy. Neoplasia. 2011, 13: 980-990.CrossRefPubMedPubMedCentral
4.
go back to reference Mancuso P, Colleoni M, Calleri A, Orlando L, Maisonneuve P, Pruneri G, Agliano A, Goldhirsch A, Shaked Y, Kerbel RS, Bertolini F: Circulating endothelial-cell kinetics and viability predict survival in breast cancer patients receiving metronomic chemotherapy. Blood. 2006, 108: 452-459. 10.1182/blood-2005-11-4570.CrossRefPubMedPubMedCentral Mancuso P, Colleoni M, Calleri A, Orlando L, Maisonneuve P, Pruneri G, Agliano A, Goldhirsch A, Shaked Y, Kerbel RS, Bertolini F: Circulating endothelial-cell kinetics and viability predict survival in breast cancer patients receiving metronomic chemotherapy. Blood. 2006, 108: 452-459. 10.1182/blood-2005-11-4570.CrossRefPubMedPubMedCentral
5.
go back to reference Norden-Zfoni A, Desai J, Manola J, Beaudry P, Force J, Maki R, Folkman J, Bello C, Baum C, DePrimo SE, Shalinsky DR, Demetri GD, Heymach JV: Blood-based biomarkers of SU11248 activity and clinical outcome in patients with metastatic imatinib-resistant gastrointestinal stromal tumor. Clin Cancer Res. 2007, 13: 2643-2650. 10.1158/1078-0432.CCR-06-0919.CrossRefPubMed Norden-Zfoni A, Desai J, Manola J, Beaudry P, Force J, Maki R, Folkman J, Bello C, Baum C, DePrimo SE, Shalinsky DR, Demetri GD, Heymach JV: Blood-based biomarkers of SU11248 activity and clinical outcome in patients with metastatic imatinib-resistant gastrointestinal stromal tumor. Clin Cancer Res. 2007, 13: 2643-2650. 10.1158/1078-0432.CCR-06-0919.CrossRefPubMed
6.
go back to reference Noberasco C, Spitaleri G, Mancuso P, Zorzino L, Radice D, Milani A, Rocca A, Bertolini F, Sandri MT, Curigliano G, de Pas T, Jemos C, Omodeo Salè E, Boselli S, de Braud F: Safety, tolerability and biological effects of long-term metronomic administration of non-cytotoxic anti-angiogenic agents. Oncology. 2009, 77: 358-365. 10.1159/000275830.CrossRefPubMed Noberasco C, Spitaleri G, Mancuso P, Zorzino L, Radice D, Milani A, Rocca A, Bertolini F, Sandri MT, Curigliano G, de Pas T, Jemos C, Omodeo Salè E, Boselli S, de Braud F: Safety, tolerability and biological effects of long-term metronomic administration of non-cytotoxic anti-angiogenic agents. Oncology. 2009, 77: 358-365. 10.1159/000275830.CrossRefPubMed
7.
go back to reference Willett CG, Duda DG, di Tomaso E, Boucher Y, Ancukiewicz M, Sahani DV, Lahdenranta J, Chung DC, Fischman AJ, Lauwers GY, Shellito P, Czito BG, Wong TZ, Paulson E, Poleski M, Vujaskovic Z, Bentley R, Chen HX, Clark JW, Jain RK: Efficacy, safety, and biomarkers of neoadjuvant bevacizumab, radiation therapy, and fluorouracil in rectal cancer: a multidisciplinary phase II study. J Clin Oncol. 2009, 27: 3020-3026. 10.1200/JCO.2008.21.1771.CrossRefPubMedPubMedCentral Willett CG, Duda DG, di Tomaso E, Boucher Y, Ancukiewicz M, Sahani DV, Lahdenranta J, Chung DC, Fischman AJ, Lauwers GY, Shellito P, Czito BG, Wong TZ, Paulson E, Poleski M, Vujaskovic Z, Bentley R, Chen HX, Clark JW, Jain RK: Efficacy, safety, and biomarkers of neoadjuvant bevacizumab, radiation therapy, and fluorouracil in rectal cancer: a multidisciplinary phase II study. J Clin Oncol. 2009, 27: 3020-3026. 10.1200/JCO.2008.21.1771.CrossRefPubMedPubMedCentral
8.
go back to reference Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, Kozak KR, Cahill DP, Chen PJ, Zhu M, Ancukiewicz M, Mrugala MM, Plotkin S, Drappatz J, Louis DN, Ivy P, Scadden DT, Benner T, Loeffler JS, Wen PY, Jain RK: AD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell. 2007, 11: 83-95. 10.1016/j.ccr.2006.11.021.CrossRefPubMedPubMedCentral Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, Kozak KR, Cahill DP, Chen PJ, Zhu M, Ancukiewicz M, Mrugala MM, Plotkin S, Drappatz J, Louis DN, Ivy P, Scadden DT, Benner T, Loeffler JS, Wen PY, Jain RK: AD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell. 2007, 11: 83-95. 10.1016/j.ccr.2006.11.021.CrossRefPubMedPubMedCentral
9.
go back to reference Rugo HS, Jo Chien A, Franco SX, Stopeck AT, Glencer A, Lahiri S, Arbushites MC, Scott J, Park JW, Hudis C, Nulsen B, Dickler MN: A phase II study of lapatinib and bevacizumab as treatment for HER2-overexpressing metastatic breast cancer. Breast Cancer Res Treat. 2012, 134: 13-20. 10.1007/s10549-011-1918-z.CrossRefPubMedPubMedCentral Rugo HS, Jo Chien A, Franco SX, Stopeck AT, Glencer A, Lahiri S, Arbushites MC, Scott J, Park JW, Hudis C, Nulsen B, Dickler MN: A phase II study of lapatinib and bevacizumab as treatment for HER2-overexpressing metastatic breast cancer. Breast Cancer Res Treat. 2012, 134: 13-20. 10.1007/s10549-011-1918-z.CrossRefPubMedPubMedCentral
10.
go back to reference Simkens LH, Tol J, Terstappen LW, Teerenstra S, Punt CJ, Nagtegaal ID: The predictive and prognostic value of circulating endothelial cells in advanced colorectal cancer patients receiving first-line chemotherapy and bevacizumab. Ann Oncol. 2010, 21: 2447-2448. 10.1093/annonc/mdq640.CrossRefPubMed Simkens LH, Tol J, Terstappen LW, Teerenstra S, Punt CJ, Nagtegaal ID: The predictive and prognostic value of circulating endothelial cells in advanced colorectal cancer patients receiving first-line chemotherapy and bevacizumab. Ann Oncol. 2010, 21: 2447-2448. 10.1093/annonc/mdq640.CrossRefPubMed
11.
go back to reference Farace F, Gross-Goupil M, Tournay E, Taylor M, Vimond N, Jacques N, Billiot F, Mauguen A, Hill C, Escudier B: Levels of circulating CD45[dim]CD34[+]VEGFR2[+] progenitor cells correlate with outcome in metastatic renal cell carcinoma patients treated with tyrosine kinase inhibitors. Br J Cancer. 2011, 104: 1144-1150. 10.1038/bjc.2011.72.CrossRefPubMedPubMedCentral Farace F, Gross-Goupil M, Tournay E, Taylor M, Vimond N, Jacques N, Billiot F, Mauguen A, Hill C, Escudier B: Levels of circulating CD45[dim]CD34[+]VEGFR2[+] progenitor cells correlate with outcome in metastatic renal cell carcinoma patients treated with tyrosine kinase inhibitors. Br J Cancer. 2011, 104: 1144-1150. 10.1038/bjc.2011.72.CrossRefPubMedPubMedCentral
12.
go back to reference Shao YY, Lin ZZ, Chen TJ, Hsu C, Shen YC, Hsu CH, Cheng AL: High circulating endothelial progenitor levels associated with poor survival of advanced hepatocellular carcinoma patients receiving sorafenib combined with metronomic chemotherapy. Oncology. 2011, 81: 98-103. 10.1159/000331684.CrossRefPubMed Shao YY, Lin ZZ, Chen TJ, Hsu C, Shen YC, Hsu CH, Cheng AL: High circulating endothelial progenitor levels associated with poor survival of advanced hepatocellular carcinoma patients receiving sorafenib combined with metronomic chemotherapy. Oncology. 2011, 81: 98-103. 10.1159/000331684.CrossRefPubMed
13.
go back to reference Strijbos MH, Gratama JW, Kraan J, Lamers CH, den Bakker MA, Sleijfer S: Circulating endothelial cells in oncology: pitfalls and promises. Br J Cancer. 2008, 98: 1731-1735. 10.1038/sj.bjc.6604383.CrossRefPubMedPubMedCentral Strijbos MH, Gratama JW, Kraan J, Lamers CH, den Bakker MA, Sleijfer S: Circulating endothelial cells in oncology: pitfalls and promises. Br J Cancer. 2008, 98: 1731-1735. 10.1038/sj.bjc.6604383.CrossRefPubMedPubMedCentral
14.
go back to reference Yang W, Lee DY, Ben-David Y: The roles of microRNAs in tumorigenesis and angiogenesis. Int J Physiol Pathophysiol Pharmacol. 2011, 3: 140-155.PubMedPubMedCentral Yang W, Lee DY, Ben-David Y: The roles of microRNAs in tumorigenesis and angiogenesis. Int J Physiol Pathophysiol Pharmacol. 2011, 3: 140-155.PubMedPubMedCentral
15.
go back to reference Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA: MicroRNAs in body fluids–the mix of hormones and biomarkers. Nat Rev Clin Oncol. 2011, 8: 467-477. 10.1038/nrclinonc.2011.76.CrossRefPubMedPubMedCentral Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA: MicroRNAs in body fluids–the mix of hormones and biomarkers. Nat Rev Clin Oncol. 2011, 8: 467-477. 10.1038/nrclinonc.2011.76.CrossRefPubMedPubMedCentral
16.
go back to reference von Marschall Z, Scholz A, Cramer T, Schäfer G, Schirner M, Oberg K, Wiedenmann B, Höcker M, Rosewicz S: Effects of interferon alpha on vascular endothelial growth factor gene transcription and tumor angiogenesis. J Natl Cancer Inst. 2003, 95: 437-448. 10.1093/jnci/95.6.437.CrossRefPubMed von Marschall Z, Scholz A, Cramer T, Schäfer G, Schirner M, Oberg K, Wiedenmann B, Höcker M, Rosewicz S: Effects of interferon alpha on vascular endothelial growth factor gene transcription and tumor angiogenesis. J Natl Cancer Inst. 2003, 95: 437-448. 10.1093/jnci/95.6.437.CrossRefPubMed
17.
go back to reference Kurzen H, Schmitt S, Näher H, Möhler T: Inhibition of angiogenesis by non-toxic doses of temozolomide. Anticancer Drugs. 2003, 14: 515-522. 10.1097/00001813-200308000-00003.CrossRefPubMed Kurzen H, Schmitt S, Näher H, Möhler T: Inhibition of angiogenesis by non-toxic doses of temozolomide. Anticancer Drugs. 2003, 14: 515-522. 10.1097/00001813-200308000-00003.CrossRefPubMed
18.
go back to reference Reynes G, Martinez-Sales V, Vila V, Fleitas T, Martin M, Reganon E: Circulating endothelial cells, microparticles, and markers of inflammation and coagulation in glioblastoma patients before and after protracted temozolomide and radiotherapy [abstract]. J Clin Oncol. 2010, 28 (15s): 2086- Reynes G, Martinez-Sales V, Vila V, Fleitas T, Martin M, Reganon E: Circulating endothelial cells, microparticles, and markers of inflammation and coagulation in glioblastoma patients before and after protracted temozolomide and radiotherapy [abstract]. J Clin Oncol. 2010, 28 (15s): 2086-
19.
go back to reference Moschos SJ, Odoux C, Land SR, Agarwala S, Friedland D, Volker KM, Sidor C, Wong M, Kirkwood JM: Endostatin plus interferon-alpha2b therapy for metastatic melanoma: a novel combination of antiangiogenic and immunomodulatory agents. Melanoma Res. 2007, 17: 193-200. 10.1097/CMR.0b013e3281ad91a3.CrossRefPubMed Moschos SJ, Odoux C, Land SR, Agarwala S, Friedland D, Volker KM, Sidor C, Wong M, Kirkwood JM: Endostatin plus interferon-alpha2b therapy for metastatic melanoma: a novel combination of antiangiogenic and immunomodulatory agents. Melanoma Res. 2007, 17: 193-200. 10.1097/CMR.0b013e3281ad91a3.CrossRefPubMed
20.
go back to reference Stadler R, Luger T, Bieber T, Köhler U, Linse R, Technau K, Schubert R, Schroth K, Vakilzadeh F, Volkenandt M, Gollnick H, Von Eick H, Thoren F, Strannegård O: Long-term survival benefit after adjuvant treatment of cutaneous melanoma with dacarbazine and low dose natural interferon alpha: A controlled, randomised multicentre trial. Acta Oncol. 2006, 45: 389-399. 10.1080/02841860600630954.CrossRefPubMed Stadler R, Luger T, Bieber T, Köhler U, Linse R, Technau K, Schubert R, Schroth K, Vakilzadeh F, Volkenandt M, Gollnick H, Von Eick H, Thoren F, Strannegård O: Long-term survival benefit after adjuvant treatment of cutaneous melanoma with dacarbazine and low dose natural interferon alpha: A controlled, randomised multicentre trial. Acta Oncol. 2006, 45: 389-399. 10.1080/02841860600630954.CrossRefPubMed
21.
go back to reference Woywodt A, Blann AD, Kirsch T, Erdbruegger U, Banzet N, Haubitz M, Dignat-George F: Isolation and enumeration of circulating endothelial cells by immunomagnetic isolation: proposal of a definition and a consensus protocol. J Thromb Haemost. 2006, 4: 671-677. 10.1111/j.1538-7836.2006.01794.x.CrossRefPubMed Woywodt A, Blann AD, Kirsch T, Erdbruegger U, Banzet N, Haubitz M, Dignat-George F: Isolation and enumeration of circulating endothelial cells by immunomagnetic isolation: proposal of a definition and a consensus protocol. J Thromb Haemost. 2006, 4: 671-677. 10.1111/j.1538-7836.2006.01794.x.CrossRefPubMed
22.
go back to reference Rowand JL, Martin G, Doyle GV, Miller MC, Pierce MS, Connelly MC, Rao C, Terstappen LW: Endothelial cells in peripheral blood of healthy subjects and patients with metastatic carcinomas. Cytometry A. 2007, 71: 105-113.CrossRefPubMed Rowand JL, Martin G, Doyle GV, Miller MC, Pierce MS, Connelly MC, Rao C, Terstappen LW: Endothelial cells in peripheral blood of healthy subjects and patients with metastatic carcinomas. Cytometry A. 2007, 71: 105-113.CrossRefPubMed
23.
go back to reference Shatseva T, Lee DY, Deng Z, Yang BB: MicroRNA miR-199a-3p regulates cell proliferation and survival by targeting caveolin-2. J Cell Sci. 2011, 124: 2826-2836. 10.1242/jcs.077529.CrossRefPubMed Shatseva T, Lee DY, Deng Z, Yang BB: MicroRNA miR-199a-3p regulates cell proliferation and survival by targeting caveolin-2. J Cell Sci. 2011, 124: 2826-2836. 10.1242/jcs.077529.CrossRefPubMed
24.
go back to reference Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, Calin GA, Ivan M: A microRNA signature of hypoxia. Mol Cell Biol. 2007, 27: 1859-1867. 10.1128/MCB.01395-06.CrossRefPubMedPubMedCentral Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, Calin GA, Ivan M: A microRNA signature of hypoxia. Mol Cell Biol. 2007, 27: 1859-1867. 10.1128/MCB.01395-06.CrossRefPubMedPubMedCentral
25.
go back to reference Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, Ji Y, Zhao C, Wang J, Yang BB, Zhang Y: MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One. 2006, 1: e116-10.1371/journal.pone.0000116.CrossRefPubMedPubMedCentral Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, Ji Y, Zhao C, Wang J, Yang BB, Zhang Y: MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One. 2006, 1: e116-10.1371/journal.pone.0000116.CrossRefPubMedPubMedCentral
26.
go back to reference Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN: The endothelial specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008, 15: 261-271. 10.1016/j.devcel.2008.07.002.CrossRefPubMedPubMedCentral Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN: The endothelial specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008, 15: 261-271. 10.1016/j.devcel.2008.07.002.CrossRefPubMedPubMedCentral
27.
go back to reference Chamorro-Jorganes A, Araldi E, Penalva LO, Sandhu D, Fernández-Hernando C, Suárez Y: MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler Thromb Vasc Biol. 2011, 31: 2595-2606. 10.1161/ATVBAHA.111.236521.CrossRefPubMedPubMedCentral Chamorro-Jorganes A, Araldi E, Penalva LO, Sandhu D, Fernández-Hernando C, Suárez Y: MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler Thromb Vasc Biol. 2011, 31: 2595-2606. 10.1161/ATVBAHA.111.236521.CrossRefPubMedPubMedCentral
28.
go back to reference Heusschen R, van Gink M, Griffioen AW, Thijssen VL: MicroRNAs in the tumor endothelium: novel controls on the angioregulatory switchboard. Biochim Biophys Acta. 2010, 1805: 87-96.PubMed Heusschen R, van Gink M, Griffioen AW, Thijssen VL: MicroRNAs in the tumor endothelium: novel controls on the angioregulatory switchboard. Biochim Biophys Acta. 2010, 1805: 87-96.PubMed
29.
go back to reference Shen J, Yang X, Xie B, Chen Y, Swaim M, Hackett SF, Campochiaro PA: MicroRNAs regulate ocular neovascularization. Mol Ther. 2008, 16: 1208-1216. 10.1038/mt.2008.104.CrossRefPubMedPubMedCentral Shen J, Yang X, Xie B, Chen Y, Swaim M, Hackett SF, Campochiaro PA: MicroRNAs regulate ocular neovascularization. Mol Ther. 2008, 16: 1208-1216. 10.1038/mt.2008.104.CrossRefPubMedPubMedCentral
30.
go back to reference Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A: Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet. 2006, 38: 1060-1065. 10.1038/ng1855.CrossRefPubMedPubMedCentral Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A: Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet. 2006, 38: 1060-1065. 10.1038/ng1855.CrossRefPubMedPubMedCentral
31.
go back to reference Martin MM, Buckenberger JA, Jiang J, Malana GE, Nuovo GJ, Chotani M, Feldman DS, Schmittgen TD, Elton TS: The human angiotensin II type 1 receptor +1166 A/C polymorphism attenuates microrna-155 binding. J Biol Chem. 2007, 282: 24262-24269. 10.1074/jbc.M701050200.CrossRefPubMedPubMedCentral Martin MM, Buckenberger JA, Jiang J, Malana GE, Nuovo GJ, Chotani M, Feldman DS, Schmittgen TD, Elton TS: The human angiotensin II type 1 receptor +1166 A/C polymorphism attenuates microrna-155 binding. J Biol Chem. 2007, 282: 24262-24269. 10.1074/jbc.M701050200.CrossRefPubMedPubMedCentral
32.
go back to reference Alpini G, Glaser SS, Zhang JP, Francis H, Han Y, Gong J, Stokes A, Francis T, Hughart N, Hubble L, Zhuang SM, Meng F: Regulation of placenta growth factor by microRNA-125b in hepatocellular cancer. J Hepatol. 2011, 55: 1339-1345. 10.1016/j.jhep.2011.04.015.CrossRefPubMedPubMedCentral Alpini G, Glaser SS, Zhang JP, Francis H, Han Y, Gong J, Stokes A, Francis T, Hughart N, Hubble L, Zhuang SM, Meng F: Regulation of placenta growth factor by microRNA-125b in hepatocellular cancer. J Hepatol. 2011, 55: 1339-1345. 10.1016/j.jhep.2011.04.015.CrossRefPubMedPubMedCentral
33.
go back to reference Xu B, Wang N, Wang X, Tong N, Shao N, Tao J, Li P, Niu X, Feng N, Zhang L, Hua L, Wang Z, Chen M: MiR-146a suppresses tumor growth and progression by targeting EGFR pathway and in a p-ERK-dependent manner in castration-resistant prostate cancer. Prostate. 2012, 72: 1171-1178. 10.1002/pros.22466.CrossRefPubMed Xu B, Wang N, Wang X, Tong N, Shao N, Tao J, Li P, Niu X, Feng N, Zhang L, Hua L, Wang Z, Chen M: MiR-146a suppresses tumor growth and progression by targeting EGFR pathway and in a p-ERK-dependent manner in castration-resistant prostate cancer. Prostate. 2012, 72: 1171-1178. 10.1002/pros.22466.CrossRefPubMed
34.
go back to reference Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G: MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 2006, 108: 3068-3071. 10.1182/blood-2006-01-012369.CrossRefPubMed Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G: MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 2006, 108: 3068-3071. 10.1182/blood-2006-01-012369.CrossRefPubMed
35.
go back to reference Kang SG, Lee WH, Lee YH, Lee YS, Kim SG: Hypoxia inducible factor-1α inhibition by a pyrrolopyrazine metabolite of oltipraz as a consequence of microRNAs 199a-5p and 20a induction. Carcinogenesis. 2012, 33: 661-669. 10.1093/carcin/bgr320.CrossRefPubMed Kang SG, Lee WH, Lee YH, Lee YS, Kim SG: Hypoxia inducible factor-1α inhibition by a pyrrolopyrazine metabolite of oltipraz as a consequence of microRNAs 199a-5p and 20a induction. Carcinogenesis. 2012, 33: 661-669. 10.1093/carcin/bgr320.CrossRefPubMed
36.
go back to reference Yang C, Wei W: The miRNA expression profile of the uveal melanoma. Sci China Life Sci. 2011, 54: 351-358. 10.1007/s11427-011-4149-y.CrossRefPubMed Yang C, Wei W: The miRNA expression profile of the uveal melanoma. Sci China Life Sci. 2011, 54: 351-358. 10.1007/s11427-011-4149-y.CrossRefPubMed
37.
go back to reference Ijland SA, Jager MJ, Heijdra BM, Westphal JR, Peek R: Expression of angiogenic and immunosuppressive factors by uveal melanoma cell lines. Melanoma Res. 1999, 9: 445-450. 10.1097/00008390-199910000-00003.CrossRefPubMed Ijland SA, Jager MJ, Heijdra BM, Westphal JR, Peek R: Expression of angiogenic and immunosuppressive factors by uveal melanoma cell lines. Melanoma Res. 1999, 9: 445-450. 10.1097/00008390-199910000-00003.CrossRefPubMed
38.
go back to reference Martin MM, Buckenberger JA, Jiang J, Malana GE, Nuovo GJ, Chotani M, Feldman DS, Schmittgen TD, Elton TS: The human angiotensin II type 1 receptor +1166 A/C polymorphism attenuates microrna-155 binding. J Biol Chem. 2007, 282: 24262-24269. 10.1074/jbc.M701050200.CrossRefPubMedPubMedCentral Martin MM, Buckenberger JA, Jiang J, Malana GE, Nuovo GJ, Chotani M, Feldman DS, Schmittgen TD, Elton TS: The human angiotensin II type 1 receptor +1166 A/C polymorphism attenuates microrna-155 binding. J Biol Chem. 2007, 282: 24262-24269. 10.1074/jbc.M701050200.CrossRefPubMedPubMedCentral
39.
go back to reference Donnem T, Lonvik K, Eklo K, Berg T, Sorbye SW, Al-Shibli K, Al-Saad S, Andersen S, Stenvold H, Bremnes RM, Busund LT: Independent and tissue-specific prognostic impact of miR-126 in nonsmall cell lung cancer: Coexpression with vascular endothelial growth factor-A predicts poor survival. Cancer. 2011, 15: 3193-3200.CrossRef Donnem T, Lonvik K, Eklo K, Berg T, Sorbye SW, Al-Shibli K, Al-Saad S, Andersen S, Stenvold H, Bremnes RM, Busund LT: Independent and tissue-specific prognostic impact of miR-126 in nonsmall cell lung cancer: Coexpression with vascular endothelial growth factor-A predicts poor survival. Cancer. 2011, 15: 3193-3200.CrossRef
40.
go back to reference Ugurel S, Rappl G, Tilgen W, Reinhold U: Increased serum concentration of angiogenic factors in malignant melanoma patients correlates with tumor progression and survival. J Clin Oncol. 2001, 19: 577-583.PubMed Ugurel S, Rappl G, Tilgen W, Reinhold U: Increased serum concentration of angiogenic factors in malignant melanoma patients correlates with tumor progression and survival. J Clin Oncol. 2001, 19: 577-583.PubMed
41.
go back to reference Yurkovetsky ZR, Kirkwood JM, Edington HD, Marrangoni AM, Velikokhatnaya L, Winans MT, Gorelik E, Lokshin AE: Multiplex analysis of serum cytokines in melanoma patients treated with interferon-alpha2b. Clin Cancer Res. 2007, 13: 2422-2428. 10.1158/1078-0432.CCR-06-1805.CrossRefPubMed Yurkovetsky ZR, Kirkwood JM, Edington HD, Marrangoni AM, Velikokhatnaya L, Winans MT, Gorelik E, Lokshin AE: Multiplex analysis of serum cytokines in melanoma patients treated with interferon-alpha2b. Clin Cancer Res. 2007, 13: 2422-2428. 10.1158/1078-0432.CCR-06-1805.CrossRefPubMed
42.
go back to reference Siegrist F, Singer T, Certa U: MicroRNA Expression Profiling by Bead Array Technology in Human Tumor Cell Lines Treated with Interferon-Alpha-2a. Biol Proced Online. 2009, 11: 113-129. 10.1007/s12575-009-9012-1.CrossRefPubMedPubMedCentral Siegrist F, Singer T, Certa U: MicroRNA Expression Profiling by Bead Array Technology in Human Tumor Cell Lines Treated with Interferon-Alpha-2a. Biol Proced Online. 2009, 11: 113-129. 10.1007/s12575-009-9012-1.CrossRefPubMedPubMedCentral
43.
go back to reference Scagnolari C, Zingariello P, Vecchiet J, Selvaggi C, Racciatti D, Taliani G, Riva E, Pizzigallo E, Antonelli G: Differential expression of interferon-induced microRNAs in patients with chronic hepatitis C virus infection treated with pegylated interferon alpha. Virol J. 2010, 7: 311-10.1186/1743-422X-7-311.CrossRefPubMedPubMedCentral Scagnolari C, Zingariello P, Vecchiet J, Selvaggi C, Racciatti D, Taliani G, Riva E, Pizzigallo E, Antonelli G: Differential expression of interferon-induced microRNAs in patients with chronic hepatitis C virus infection treated with pegylated interferon alpha. Virol J. 2010, 7: 311-10.1186/1743-422X-7-311.CrossRefPubMedPubMedCentral
Metadata
Title
The association of blood angioregulatory microRNA levels with circulating endothelial cells and angiogenic proteins in patients receiving dacarbazine and interferon
Authors
Pierre L Triozzi
Susan Achberger
Wayne Aldrich
Arun D Singh
Ronald Grane
Ernest C Borden
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2012
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/1479-5876-10-241

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