Advertisement

Molecular Neurobiology

, Volume 50, Issue 2, pp 545–558 | Cite as

Circulating MicroRNA Biomarkers for Glioma and Predicting Response to Therapy

  • Charlotte A. Tumilson
  • Robert W. Lea
  • Jane E. Alder
  • Lisa ShawEmail author
Article

Abstract

The need for glioma biomarkers with improved sensitivity and specificity has sparked research into short non-coding RNA known as microRNA (miRNA). Altered miRNA biogenesis and expression in glioma plays a vital role in important signaling pathways associated with a range of tumor characteristics including gliomagenesis, invasion, and malignancy. This review will discuss current research into the role of miRNA in glioma and altered miRNA expression in biofluids as candidate biomarkers with a particular focus on glioblastoma, the most malignant form of glioma. The isolation and characterization of miRNA using cellular and molecular biology techniques from the circulation of glioma patients could potentially be used for improved diagnosis, prognosis, and treatment decisions. We aim to highlight the links between research into miRNA function, their use as biomarkers, and how these biomarkers can be used to predict response to therapy. Furthermore, increased understanding of miRNA in glioma biology through biomarker research has led to the development of miRNA therapeutics which could restore normal miRNA expression and function and improve the prognosis of glioma patients. A panel of important miRNA biomarkers for glioma in various biofluids discovered to date has been summarized here. There is still a need, however, to standardize techniques for biomarker characterization to bring us closer to clinically relevant miRNA-based diagnostic and therapeutic signatures. A clinically validated biomarker panel has potential to improve time to diagnosis, predicting response to treatment and ultimately the prognosis of glioma patients.

Keywords

MicroRNA Glioma Biomarker Serum Cerebrospinal fluid 

Notes

Acknowledgments

The authors would like to acknowledge Katherine Ashton and Mohit Arora at Royal Preston Hospital for provision of patient samples and Brain Tumour North West and the University of Central Lancashire for funding.

References

  1. 1.
    Preusser M (2012) Clinically useful biomarkers in neurooncology. memo—Magazine of. Eur Med Oncol 5(3):201–204. doi: 10.1007/s12254-012-0030-3 Google Scholar
  2. 2.
    Manne U, Srivastava R-G, Srivastava S (2005) Keynote review: recent advances in biomarkers for cancer diagnosis and treatment. Drug Discov Today 10(14):965–976. doi: 10.1016/S1359-6446(05)03487-2 PubMedCrossRefGoogle Scholar
  3. 3.
    Lenos K, Grawenda AM, Lodder K, Kuijjer ML, Teunisse AFAS, Repapi E, Grochola LF, Bartel F, Hogendoorn PCW, Wuerl P, Taubert H, Cleton-Jansen A-M, Bond GL, Jochemsen AG (2012) Alternate splicing of the p53 inhibitor HDMX offers a superior prognostic biomarker than p53 mutation in human cancer. Cancer Res 72(16):4074–4084. doi: 10.1158/0008-5472.can-12-0215 PubMedCrossRefGoogle Scholar
  4. 4.
    Zougman A, Hutchins GG, Cairns DA, Verghese E, Perry SL, Jayne DG, Selby PJ, Banks RE (2013) Retinoic acid-induced protein 3: identification and characterisation of a novel prognostic colon cancer biomarker. Eur J Cancer 49(2):531–539. doi: 10.1016/j.ejca.2012.07.031 PubMedCrossRefGoogle Scholar
  5. 5.
    Bauer TM, El-Rayes BF, Li X, Hammad N, Philip PA, Shields AF, Zalupski MM, Bekaii-Saab T (2013) Carbohydrate antigen 19-9 is a prognostic and predictive biomarker in patients with advanced pancreatic cancer who receive gemcitabine-containing chemotherapy. Cancer 119(2):285–292. doi: 10.1002/cncr.27734 PubMedCrossRefGoogle Scholar
  6. 6.
    Qian X, Li C, Pang B, Xue M, Wang J, Zhou J (2012) Spondin-2 (SPON2), a more prostate-cancer-specific diagnostic biomarker. PLoS ONE 7(5):e37225. doi: 10.1371/journal.pone.0037225 PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Morrison DH, Rahardja D, King E, Peng Y, Sarode VR (2012) Tumour biomarker expression relative to age and molecular subtypes of invasive breast cancer. Br J Cancer 107(2):382–387PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Diamandis (2010) Cancer biomarkers: can we turn recent failures into success? J Natl Cancer Inst 102(19):1462–1467. doi: 10.1093/jnci/djq306 PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Abu-Asab MS, Chaouchi M, Alesci S, Galli S, Laassri M, Cheema AK, Atouf F, VanMeter J, Amri H (2011) Biomarkers in the age of omics: time for a systems biology approach. OMICS J Integr Biol 15(3):105–112CrossRefGoogle Scholar
  10. 10.
    Chauhan S, Kumar D, Jaggi M (2009) Mucins in ovarian cancer diagnosis and therapy. J Ovarian Res 2(1):21PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Favilla V, Cimino S, Madonia M, Morgia G (2010) New advances in clinical biomarkers in testis cancer. Front Biosci (Elite edition) 2:456–477CrossRefGoogle Scholar
  12. 12.
    Lam L, Czerniecki BJ, Fitzpatrick E, Xu S, Schuchter L, Xu X, Zhang H (2013) Interference-free HER2 ECD as a serum biomarker in breast cancer. J Mol Biomark Diagn 4(151)Google Scholar
  13. 13.
    Wang, Yuan X, Zhou Z, Hu J, Zhang T, Hu S, Luo J, Li X (2011) MicroRNAs might be promising biomarkers of human gliomas. Asian Pac J Cancer Prev 12:833–835PubMedGoogle Scholar
  14. 14.
    Baraniskin A, Kuhnhenn J, Schlegel U, Maghnouj A, Zöllner H, Schmiegel W, Hahn S, Schroers R (2012) Identification of microRNAs in the cerebrospinal fluid as biomarker for the diagnosis of glioma. Neuro-Oncology 14(1):29–33. doi: 10.1093/neuonc/nor169 PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Kuratsu J-i, Yoshizato K, Yoshimura T, Leonard EJ, Takeshima H, Ushio Y (1993) Quantitative study of monocyte chemoattractant protein-1 (MCP-1) in cerebrospinal fluid and cyst fluid from patients with malignant glioma. J Natl Cancer Inst 85(22):1836–1839. doi: 10.1093/jnci/85.22.1836 PubMedCrossRefGoogle Scholar
  16. 16.
    Su X, Chakravarti D, Cho MS, Liu L, Gi YJ, Lin Y-L, Leung ML, El-Naggar A, Creighton CJ, Suraokar MB, Wistuba I, Flores ER (2010) TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 467(7318):986–990. doi: 10.1038/nature09459 PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Louis D, Ohgaki H, Wiestler O, Cavenee W, Burger P, Jouvet A, Scheithauer B, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97–109. doi: 10.1007/s00401-007-0243-4 PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Yoon DJ, Kwan BH, Chao FC, Nicolaides TP, Phillips JJ, Lam GY, Mason AB, Weiss WA, Kamei DT (2010) Intratumoral therapy of glioblastoma multiforme using genetically engineered transferrin for drug delivery. Cancer Res 70(11):4520–4527. doi: 10.1158/0008-5472.can-09-4311 PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Tainsky MA (2009) Genomic and proteomic biomarkers for cancer: a multitude of opportunities. Biochim Biophys Acta 1796(2):176–193. doi: 10.1016/j.bbcan.2009.04.004 PubMedPubMedCentralGoogle Scholar
  20. 20.
    Garcia-Bilbao A, Armananzas R, Ispizua Z, Calvo B, Alonso-Varona A, Inza I, Larranaga P, Lopez-Vivanco G, Suarez-Merino B, Betanzos M (2012) Identification of a biomarker panel for colorectal cancer diagnosis. BMC Cancer 12(1):43PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Urquidi V, Goodison S, Cai Y, Sun Y, Rosser CJ (2012) A candidate molecular biomarker panel for the detection of bladder cancer. Cancer Epidemiol Biomark Prev 21(12):2149–2158. doi: 10.1158/1055-9965.epi-12-0428 CrossRefGoogle Scholar
  22. 22.
    Barderas R, Babel I, Díaz-Uriarte R, Moreno V, Suárez A, Bonilla F, Villar-Vázquez R, Capellá G, Casal JI (2012) An optimized predictor panel for colorectal cancer diagnosis based on the combination of tumor-associated antigens obtained from protein and phage microarrays. J Proteome 75(15):4647–4655. doi: 10.1016/j.jprot.2012.03.004 CrossRefGoogle Scholar
  23. 23.
    Gabriely G, Yi M, Narayan RS, Niers JM, Wurdinger T, Imitola J, Ligon KL, Kesari S, Esau C, Stephens RM, Tannous BA, Krichevsky AM (2011) Human glioma growth is controlled by microRNA-10b. Cancer Res 71(10):3563–3572. doi: 10.1158/0008-5472.can-10-3568 PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR (2005) MicroRNA expression profiles classify human cancers. Nature 435(7043):834–838. doi: 10.1038/nature03702 PubMedCrossRefGoogle Scholar
  25. 25.
    Rosenfeld N, Aharonov R, Meiri E, Rosenwald S, Spector Y, Zepeniuk M, Benjamin H, Shabes N, Tabak S, Levy A, Lebanony D, Goren Y, Silberschein E, Targan N, Ben-Ari A, Gilad S, Sion-Vardy N, Tobar A, Feinmesser M, Kharenko O, Nativ O, Nass D, Perelman M, Yosepovich A, Shalmon B, Polak-Charcon S, Fridman E, Avniel A, Bentwich I, Bentwich Z, Cohen D, Chajut A, Barshack I (2008) MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 26(4):462–469. doi: 10.1038/nbt1392 PubMedCrossRefGoogle Scholar
  26. 26.
    Duffy MJ, O’Donovan N, Crown J (2011) Use of molecular markers for predicting therapy response in cancer patients. Cancer Treat Rev 37(2):151–159. doi: 10.1016/j.ctrv.2010.07.004 PubMedCrossRefGoogle Scholar
  27. 27.
    Hua D, Mo F, Ding D, Li L, Han X, Zhao N, Foltz G, Lin B, Lan Q, Huang Q (2012) A catalogue of glioblastoma and brain microRNAs identified by deep sequencing. OMICS J Integr Biol 16(12):690–699CrossRefGoogle Scholar
  28. 28.
    Srinivasan S, Patric IRP, Somasundaram K (2011) A ten-microRNA expression signature predicts survival in glioblastoma. PLoS ONE 6(3):e17438. doi: 10.1371/journal.pone.0017438 PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Delfino KR, Serão NVL, Southey BR, Rodriguez-Zas SL (2011) Therapy-, gender- and race-specific microRNA markers, target genes and networks related to glioblastoma recurrence and survival. Cancer Genomics Proteomics 8(4):173–183PubMedPubMedCentralGoogle Scholar
  30. 30.
    Kim T-M, Huang W, Park R, Park PJ, Johnson MD (2011) A developmental taxonomy of glioblastoma defined and maintained by microRNAs. Cancer Res 71(9):3387–3399. doi: 10.1158/0008-5472.can-10-4117 PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Li R, Gao K, Luo H, Wang X, Shi Y, Dong Q, Luan W, You Y (2014) Identification of intrinsic subtype-specific prognostic microRNAs in primary glioblastoma. J Exp Clin Cancer Res 33(9)Google Scholar
  32. 32.
    Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843–854. doi: 10.1016/0092-8674(93)90529-Y PubMedCrossRefGoogle Scholar
  33. 33.
    Graves P, Zeng Y (2012) Biogenesis of mammalian microRNAs: a global view. Genomics Proteomics Bioinforma 10(5):239–245. doi: 10.1016/j.gpb.2012.06.004 CrossRefGoogle Scholar
  34. 34.
    Kawahara Y, Megraw M, Kreider E, Iizasa H, Valente L, Hatzigeorgiou AG, Nishikura K (2008) Frequency and fate of microRNA editing in human brain. Nucleic Acids Res 36(16):5270–5280. doi: 10.1093/nar/gkn479 PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Yang W, Chendrimada TP, Wang Q, Higuchi M, Seeburg PH, Shiekhattar R, Nishikura K (2006) Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nat Struct Mol Biol 13(1):13–21. doi: 10.1038/nsmb1041 PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Galeano F, Tomaselli S, Locatelli F, Gallo A (2012) A-to-I RNA editing: the “ADAR” side of human cancer. Semin Cell Dev Biol 23(3):244–250. doi: 10.1016/j.semcdb.2011.09.003 PubMedCrossRefGoogle Scholar
  37. 37.
    Choudhury Y, Tay FC, Lam DH, Sandanaraj E, Tang C, Ang B-T, Wang S (2012) Attenuated adenosine-to-inosine editing of microRNA-376a* promotes invasiveness of glioblastoma cells. J Clin Invest 122(11):4059–4076. doi: 10.1172/jci62925 PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Yang J-S, Phillips MD, Betel D, Mu P, Ventura A, Siepel AC, Chen KC, Lai EC (2011) Widespread regulatory activity of vertebrate microRNA* species. RNA 17(2):312–326. doi: 10.1261/rna.2537911 PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Chen L, Chen X-R, Zhang R, Li P, Liu Y, Yan K, Jiang X-D (2013) MicroRNA-107 inhibits glioma cell migration and invasion by modulating Notch2 expression. J Neurooncol 112(1):59–66. doi: 10.1007/s11060-012-1037-7 PubMedCrossRefGoogle Scholar
  40. 40.
    Loftus JC, Ross JT, Paquette KM, Paulino VM, Nasser S, Yang Z, Kloss J, Kim S, Berens ME, Tran NL (2012) miRNA expression profiling in migrating glioblastoma cells: regulation of cell migration and invasion by miR-23b via targeting of Pyk2. PLoS ONE 7(6):e39818–e39818. doi: 10.1371/journal.pone.0039818 PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Tan X, Wang S, Zhu L, Wu C, Yin B, Zhao J, Yuan J, Qiang B, Peng X (2012) cAMP response element-binding protein promotes gliomagenesis by modulating the expression of oncogenic microRNA-23a. Proc Natl Acad Sci 109(39):15805–15810. doi: 10.1073/pnas.1207787109 PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Song L, Liu L, Wu Z, Li Y, Ying Z, Lin C, Wu J, Hu B, Cheng S-Y, Li M, Li J (2012) TGF-β induces miR-182 to sustain NF-κB activation in glioma subsets. J Clin Invest 122(10):3563–3578. doi: 10.1172/jci62339 PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Karin M, Cao Y, Greten FR, Li Z-W (2002) NF-[kappa]B in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2(4):301–310PubMedCrossRefGoogle Scholar
  44. 44.
    Jiang L, Lin C, Song L, Wu J, Chen B, Ying Z, Fang L, Yan X, He M, Li J, Li M (2012) MicroRNA-30e* promotes human glioma cell invasiveness in an orthotopic xenotransplantation model by disrupting the NF-κB/IκBα negative feedback loop. J Clin Invest 122(1):33–47. doi: 10.1172/jci58849 PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Godlewski J, Nowicki MO, Bronisz A, Nuovo G, Palatini J, De Lay M, Van Brocklyn J, Ostrowski MC, Chiocca EA, Lawler SE (2010) MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells. Mol Cell 37(5):620–632. doi: 10.1016/j.molcel.2010.02.018 PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Yang, Wang C, Chen X, Chen S, Zhang Y, Zhi F, Wang J, Li L, Zhou X, Li N, Pan H, Zhang J, Zen K, Zhang C-Y, Zhang C (2013) Identification of seven serum microRNAs from a genome-wide serum microRNA expression profile as potential noninvasive biomarkers for malignant astrocytomas. Int J Cancer 132(1):116–127. doi: 10.1002/ijc.27657 PubMedCrossRefGoogle Scholar
  47. 47.
    Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brügger B, Simons M (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319(5867):1244–1247. doi: 10.1126/science.1153124 PubMedCrossRefGoogle Scholar
  48. 48.
    Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12(1):19–30. doi: 10.1038/ncb2000 PubMedCrossRefGoogle Scholar
  49. 49.
    Bobrie A, Krumeich S, Reyal F, Recchi C, Moita LF, Seabra MC, Ostrowski M, Théry C (2012) Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res 72(19):4920–4930. doi: 10.1158/0008-5472.can-12-0925 PubMedCrossRefGoogle Scholar
  50. 50.
    Chen X, Liang H, Zhang J, Zen K, Zhang C-Y (2012) Secreted microRNAs: a new form of intercellular communication. Trends Cell Biol 22(3):125–132. doi: 10.1016/j.tcb.2011.12.001 PubMedCrossRefGoogle Scholar
  51. 51.
    Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Curry WT, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10(12):1470–1476. doi: 10.1038/ncb1800 PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Li CCY, Eaton SA, Young PE, Lee M, Shuttleworth R, Humphreys DT, Grau GE, Combes V, Bebawy M, Gong J, Brammah S, Buckland ME, Suter CM (2013) Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol 10(8):1333–1344PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33(20):e179. doi: 10.1093/nar/gni178 PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Sheinerman KS, Umansky SR (2013) Circulating cell-free microRNA as biomarkers for screening, diagnosis and monitoring of neurodegenerative diseases and other neurologic pathologies. Front Cell Neurosci 7:150. doi: 10.3389/fncel.2013.00150 PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Wang Q, Li P, Li A, Jiang W, Wang H, Wang J, Xie K (2012) Plasma specific miRNAs as predictive biomarkers for diagnosis and prognosis of glioma. J Exp Clin Cancer Res 31(97):1–10PubMedPubMedCentralGoogle Scholar
  56. 56.
    de Bont JM, den Boer ML, Reddingius RE, Jansen J, Passier M, van Schaik RH, Kros JM, Sillevis Smitt PA, Luider TH, Pieters R (2006) Identification of apolipoprotein A-II in cerebrospinal fluid of pediatric brain tumor patients by protein expression profiling. Clin Chem 52(8):1501–1509. doi: 10.1373/clinchem.2006.069294 PubMedCrossRefGoogle Scholar
  57. 57.
    Niclou SP, Fack F, Rajcevic U (2010) Glioma proteomics: status and perspectives. J Proteome 73(10):1823–1838. doi: 10.1016/j.jprot.2010.03.007 CrossRefGoogle Scholar
  58. 58.
    Baraniskin A, Kuhnhenn J, Schlegel U, Maghnouj A, Zollner H, Schmiegel W, Hahn S, Schroers R (2011) Identification of microRNAs in the cerebrospinal fluid as biomarker for the diagnosis of glioma. Neuro-Oncology 117(11):3140–3146. doi: 10.1093/neuonc/nor169 Google Scholar
  59. 59.
    Teplyuk NM, Mollenhauer B, Gabriely G, Giese A, Kim E, Smolsky M, Kim RY, Saria MG, Pastorino S, Kesari S, Krichevsky AM (2012) MicroRNAs in cerebrospinal fluid identify glioblastoma and metastatic brain cancers and reflect disease activity. Neuro-Oncology 14(6):689–700. doi: 10.1093/neuonc/nos074 PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, Krichevsky AM (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28(17):5369–5380. doi: 10.1128/mcb.00479-08 PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Xia H, Qi Y, Ng SS, Chen X, Chen S, Fang M, Li D, Zhao Y, Ge R, Li G, Chen Y, He M-L, H-f K, Lai L, Lin MC (2009) MicroRNA-15b regulates cell cycle progression by targeting cyclins in glioma cells. Biochem Biophys Res Commun 380(2):205–210. doi: 10.1016/j.bbrc.2008.12.169 PubMedCrossRefGoogle Scholar
  62. 62.
    Peng B, Hu S, Jun Q, Luo D, Zhang X, Zhao H, Li D (2013) MicroRNA-200b targets CREB1 and suppresses cell growth in human malignant glioma. Mol Cell Biochem 379(1–2):51–58. doi: 10.1007/s11010-013-1626-6 PubMedCrossRefGoogle Scholar
  63. 63.
    Carden CP, Sarker D, Postel-Vinay S, Yap TA, Attard G, Banerji U, Garrett MD, Thomas GV, Workman P, Kaye SB, de Bono JS (2010) Can molecular biomarker-based patient selection in phase I trials accelerate anticancer drug development? Drug Discov Today 15(3–4):88–97. doi: 10.1016/j.drudis.2009.11.006 PubMedCrossRefGoogle Scholar
  64. 64.
    Zhang W, Zhang J, Hoadley K, Kushwaha D, Ramakrishnan V, Li S, Kang C, You Y, Jiang C, Song SW, Jiang T, Chen CC (2012) miR-181d: a predictive glioblastoma biomarker that downregulates MGMT expression. Neuro-Oncology 14(6):712–719. doi: 10.1093/neuonc/nos089 PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Shi L, Chen J, Yang J, Pan T, Zhang S, Wang Z (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 PubMedCrossRefGoogle Scholar
  66. 66.
    WONG STS, X-Q ZHANG, ZHUANG JT-F, H-L CHAN, C-H LI, LEUNG GKK (2012) MicroRNA-21 inhibition enhances in vitro chemosensitivity of temozolomide-resistant glioblastoma cells. Anticancer Res 32(7):2835–2841PubMedGoogle Scholar
  67. 67.
    Gwak H-S, Kim TH, Jo GH, Kim Y-J, Kwak H-J, Kim JH, Yin J, Yoo H, Lee SH, Park JB (2012) Silencing of microRNA-21 confers radio-sensitivity through inhibition of the PI3K/AKT pathway and enhancing autophagy in malignant glioma cell lines. PLoS ONE 7(10):e47449. doi: 10.1371/journal.pone.0047449 PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Quintavalle C, Donnarumma E, Iaboni M, Roscigno G, Garofalo M, Romano G, Fiore D, De Marinis P, Croce CM, Condorelli G (2012) Effect of miR-21 and miR-30b/c on TRAIL-induced apoptosis in glioma cells. Oncogene. doi: 10.1038/onc.2012.410 Google Scholar
  69. 69.
    Chan LW, Moses MA, Goley E, Sproull M, Muanza T, Coleman CN, Figg WD, Albert PS, Ménard C, Camphausen K (2004) Urinary VEGF and MMP levels as predictive markers of 1-year progression-free survival in cancer patients treated with radiation therapy: a longitudinal study of protein kinetics throughout tumor progression and therapy. J Clin Oncol 22(3):499–506. doi: 10.1200/jco.2004.07.022 PubMedCrossRefGoogle Scholar
  70. 70.
    Vinther J, Rukov J, Shomron N (2012) MicroRNAs and their antagonists as novel therapeutics. In: Erdmann VA, Barciszewski J (eds) From nucleic acids sequences to molecular medicine. RNA technologies. Springer, Berlin, pp 503–523. doi: 10.1007/978-3-642-27426-8_20 CrossRefGoogle Scholar
  71. 71.
    Nana-Sinkam SP, Croce CM (2013) Clinical applications for microRNAs in cancer. Clin Pharmacol Ther 93(1):98–104PubMedCrossRefGoogle Scholar
  72. 72.
    Bouchie A (2013) First microRNA mimic enters clinic. Nat Biotechnol 31(7):577–577. doi: 10.1038/nbt0713-577 PubMedCrossRefGoogle Scholar
  73. 73.
    Melo S, Villanueva A, Moutinho C, Davalos V, Spizzo R, Ivan C, Rossi S, Setien F, Casanovas O, Simo-Riudalbas L, Carmona J, Carrere J, Vidal A, Aytes A, Puertas S, Ropero S, Kalluri R, Croce CM, Calin GA, Esteller M (2011) Small molecule enoxacin is a cancer-specific growth inhibitor that acts by enhancing TAR RNA-binding protein 2-mediated microRNA processing. Proc Natl Acad Sci 108(11):4394–4399. doi: 10.1073/pnas.1014720108 PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Git A, Dvinge H, Salmon-Divon M, Osborne M, Kutter C, Hadfield J, Bertone P, Caldas C (2010) Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression. RNA 16(5):991–1006. doi: 10.1261/rna.1947110 PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    McDonald JS, Milosevic D, Reddi HV, Grebe SK, Algeciras-Schimnich A (2011) Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem 57(6):833–840. doi: 10.1373/clinchem.2010.157198 PubMedCrossRefGoogle Scholar
  76. 76.
    Qureshi R, Sacan A (2013) A novel method for the normalization of microRNA RT-PCR data. BMC Med Genet 6(1):14–17Google Scholar
  77. 77.
    Duttagupta R, Jiang R, Gollub J, Getts RC, Jones KW (2011) Impact of cellular miRNAs on circulating miRNA biomarker signatures. PLoS ONE 6(6):e20769. doi: 10.1371/journal.pone.0020769 PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Zampetaki A, Mayr M (2012) Analytical challenges and technical limitations in assessing circulating MiRNAs. Thromb Haemost 108(10):592–598. doi: 10.1160/th12-02-0097 PubMedCrossRefGoogle Scholar
  79. 79.
    Noerholm M, Balaj L, Limperg T, Salehi A, Zhu L, Hochberg F, Breakefield X, Carter B, Skog J (2012) RNA expression patterns in serum microvesicles from patients with glioblastoma multiforme and controls. BMC Cancer 12(22):2–11Google Scholar
  80. 80.
    Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, Tait JF, Tewari M (2012) Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res 5(3):492–497. doi: 10.1158/1940-6207.capr-11-0370 CrossRefGoogle Scholar
  81. 81.
    Mathers JC, Strathdee G, Relton CL (2010) Induction of epigenetic alterations by dietary and other environmental factors. Adv Genet 71:3–39PubMedCrossRefGoogle Scholar
  82. 82.
    Whitney AR, Diehn M, Popper SJ, Alizadeh AA, Boldrick JC, Relman DA, Brown PO (2003) Individuality and variation in gene expression patterns in human blood. Proc Natl Acad Sci 100(4):1896–1901. doi: 10.1073/pnas.252784499 PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Summerer I, Niyazi M, Unger K, Pitea A, Zangen V, Hess J, Atkinson MJ, Belka C, Moertl S, Zitzelsberger H (2013) Changes in circulating microRNAs after radiochemotherapy in head and neck cancer patients. Radiat Oncol 8(296)Google Scholar
  84. 84.
    Podolska A, Kaczkowski B, Litman T, Fredholm M, Cirera S (2011) How the RNA isolation method can affect microRNA microarray results. Acta Biochim Pol 58(4):535–540PubMedGoogle Scholar
  85. 85.
    Peltier HJ, Latham GJ (2008) Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 14(5):844–852. doi: 10.1261/rna.939908 PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci 105(30):10513–10518. doi: 10.1073/pnas.0804549105 PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Charlotte A. Tumilson
    • 1
  • Robert W. Lea
    • 1
  • Jane E. Alder
    • 1
  • Lisa Shaw
    • 1
    Email author
  1. 1.School of Pharmacy and Biomedical SciencesUniversity of Central LancashirePrestonUK

Personalised recommendations