Advertisement

MicroRNA sensors based on gold nanoparticles

  • Catarina Coutinho
  • Álvaro Somoza
Review
Part of the following topical collections:
  1. Nanoparticles for Bioanalysis

Abstract

MicroRNAs (miRNAs) are small regulatory RNAs, the dysregulation of which has been associated with the progression of several human diseases, including cancer. Interestingly, these molecules can be used as biomarkers for early disease diagnosis and can be found in a variety of body fluids and tissue samples. However, their specific properties and very low concentrations make their detection rather challenging. In this regard, current detection methods are complex, cost-ineffective, and of limited application in point-of-care settings or resource-limited facilities. Recently, nanotechnology-based approaches have emerged as promising alternatives to conventional miRNA detection methods and paved the way for research towards sensitive, fast, and low-cost detection systems. In particular, due to their exceptional properties, the use of gold nanoparticles (AuNPs) has significantly improved the performance of miRNA biosensors. This review discusses the application of AuNPs in different miRNA sensor modalities, commenting on recently reported examples. A practical overview of each modality is provided, highlighting their future use in clinical diagnosis.

Graphical abstract

Keywords

Disease diagnosis Nanotechnology-based sensors miRNA detection Gold nanoparticles Oligonucleotide probes Point-of-care 

Notes

Acknowledgments

IMDEA Nanociencia acknowledges support from the “Severo Ochoa” Programme for Centres of Excellence in R&D (MINECO, Grant SEV-2016-0686). Catarina Coutinho acknowledges the Erasmus+ Mobility Program for financial support (2017-1-PT01-KA103-035245).

Funding information

This work was partially supported by the Spanish Ministry of Economy and Competitiveness (SAF2017-87305-R, PCIN-2016-167), Comunidad de Madrid (IND2017/IND-7809; S2017/BMD-3867), co-financed by European Structural and Investment Fund, Asociación Española Contra el Cáncer, and IMDEA Nanociencia.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    Lytle JR, Yario TA, Steitz JA. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5’ UTR as in the 3’ UTR. Proc Natl Acad Sci U S A. 2007;104:9667–72.  https://doi.org/10.1073/pnas.0703820104.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Bartel D. MicroRNAsGenomics, biogenesis, mechanism, and function. Cell. 2004;116:281–97.  https://doi.org/10.1016/S0092-8674(04)00045-5.CrossRefPubMedGoogle Scholar
  3. 3.
    Huang Y, Shen XJ, Zou Q, Wang SP, Tang SM, Zhang GZ. Biological functions of microRNAs: a review. J Physiol Biochem. 2011;67:129–39.  https://doi.org/10.1007/s13105-010-0050-6.CrossRefPubMedGoogle Scholar
  4. 4.
    Hammond SM. An overview of microRNAs. Adv Drug Deliv Rev. 2015;87:3–14.  https://doi.org/10.1016/j.addr.2015.05.001.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Li J, Smyth P, Flavin R, Cahill S, Denning K, Aherne S, et al. Comparison of miRNA expression patterns using total RNA extracted from matched samples of formalin-fixed paraffin-embedded (FFPE) cells and snap frozen cells. BMC Biotechnol. 2007;7:36.  https://doi.org/10.1186/1472-6750-7-36.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Xi Y, Nakajima G, Gavin E, Morris CG, Kudo K, Hayashi K, et al. Systematic analysis of microRNA expression of RNA extracted from fresh frozen and formalin-fixed paraffin-embedded samples. RNA. 2007;13:1668–74.  https://doi.org/10.1261/rna.642907.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A. 2008;105:10513–8.  https://doi.org/10.1073/pnas.0804549105.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–9.  https://doi.org/10.1038/ncb1596.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A. 2011;108:5003–8.  https://doi.org/10.1073/pnas.1019055108.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13:423–33.  https://doi.org/10.1038/ncb2210.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Ferracin M, Veronese A, Negrini M. Micromarkers: miRNAs in cancer diagnosis and prognosis. Expert Rev Mol Diagn. 2010;10:297–308.  https://doi.org/10.1586/erm.10.11.CrossRefPubMedGoogle Scholar
  12. 12.
    Fiammengo R. Can nanotechnology improve cancer diagnosis through miRNA detection? Biomark Med. 2017;11:69–86.  https://doi.org/10.2217/bmm-2016-0195.CrossRefPubMedGoogle Scholar
  13. 13.
    Josefsen K, Nielsen H. Northern blotting analysis. Methods Mol Biol. 2011;703:87–105.  https://doi.org/10.1007/978-1-59745-248-9_7.Google Scholar
  14. 14.
    Flowers E, Froelicher ES, Aouizerat BE. Measurement of microRNA: a regulator of gene expression. Biol Res Nurs. 2013;15:167–78.  https://doi.org/10.1177/1099800411430380.CrossRefPubMedGoogle Scholar
  15. 15.
    Degliangeli F, Pompa PP, Fiammengo R. Nanotechnology-based strategies for the detection and quantification of microRNA. Chem Eur J. 2014;20:9476–92.  https://doi.org/10.1002/chem.201402649.CrossRefPubMedGoogle Scholar
  16. 16.
    Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: approaches and considerations. Nat Rev Genet. 2012;13:358–69.  https://doi.org/10.1038/nrg3198.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Hunt EA, Broyles D, Head T, Deo SK. MicroRNA detection: current technology and research strategies. Annu Rev Anal Chem. 2015;8:217–37.  https://doi.org/10.1146/annurev-anchem-071114-040343.CrossRefGoogle Scholar
  18. 18.
    Das S, Mitra S, Khurana SMP, Debnath N. Nanomaterials for biomedical applications. Front Life Sci. 2013;7:90–8.  https://doi.org/10.1080/21553769.2013.869510.CrossRefGoogle Scholar
  19. 19.
    Su H, Li S, Jin Y, Xian Z, Yang D, Zhou W, et al. Nanomaterial-based biosensors for biological detections. Adv Health Care Technol. 2017;3:19–29.  https://doi.org/10.2147/AHCT.S94025.CrossRefGoogle Scholar
  20. 20.
    Saha K, Agasti SS, Kim C, Li X, Rotello VM. Gold nanoparticles in chemical and biological sensing. Chem Rev. 2012;112:2739–79.CrossRefGoogle Scholar
  21. 21.
    Abdulbari HA, Basheer EAM. Electrochemical biosensors: electrode development, materials, design, and fabrication. ChemBioEng Rev. 2017;4:92–105.  https://doi.org/10.1002/cben.201600009.CrossRefGoogle Scholar
  22. 22.
    Zeng S, Baillargeat D, Ho H-P, Yong K-T. Nanomaterials enhanced surface plasmon resonance for biological and chemical sensing applications. Chem Soc Rev. 2014;43:3426.  https://doi.org/10.1039/c3cs60479a.CrossRefPubMedGoogle Scholar
  23. 23.
    Liz-Marzán LM. Tailoring surface plasmons through the morphology and assembly of metal nanoparticles. Langmuir. 2006;22:32–41.  https://doi.org/10.1021/LA0513353.CrossRefPubMedGoogle Scholar
  24. 24.
    Rosi NL, Mirkin CA. Nanostrucutres in biodiagnostics. Chem Rev. 2005;105:1547–62.  https://doi.org/10.1021/cr030067f.CrossRefPubMedGoogle Scholar
  25. 25.
    Giljohann DA, Seferos DS, Daniel WL, Massich MD, Patel PC, Mirkin CA. Gold nanoparticles for biology and medicine. Angew Chem Int Ed. 2010;49:3280–94.  https://doi.org/10.1002/anie.200904359.CrossRefGoogle Scholar
  26. 26.
    Heuer-Jungemann A, Harimech PK, Brown T, Kanaras AG. Gold nanoparticles and fluorescently-labelled DNA as a platform for biological sensing. Nanoscale. 2013;5:9503.  https://doi.org/10.1039/c3nr03707j.CrossRefPubMedGoogle Scholar
  27. 27.
    Mieszawska AJ, Mulder WJM, Fayad ZA, Cormode DP. Multifunctional gold nanoparticles for diagnosis and therapy of disease. Mol Pharm. 2013;10:831–47.CrossRefGoogle Scholar
  28. 28.
    Johnson BN, Mutharasan R. Biosensor-based microRNA detection: techniques, design, performance, and challenges. Analyst. 2014;139:1576–88.  https://doi.org/10.1039/c3an01677c.CrossRefPubMedGoogle Scholar
  29. 29.
    Válóczi A, Hornyik C, Varga N, Burgyán J, Kauppinen S, Havelda Z. Sensitive and specific detection of microRNAs by northern blot analysis using LNA-modified oligonucleotide probes. Nucleic Acids Res. 2004;32:e175.  https://doi.org/10.1093/nar/gnh171.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Kim SW, Li Z, Moore PS, Monaghan AP, Chang Y, Nichols M, et al. A sensitive non-radioactive northern blot method to detect small RNAs. Nucleic Acids Res. 2010;38:e98.  https://doi.org/10.1093/nar/gkp1235.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Wu W, Gong P, Li J, Yang J, Zhang G, Li H, et al. Simple and nonradioactive detection of microRNAs using digoxigenin (DIG)-labeled probes with high sensitivity. RNA. 2014;20:580–4.  https://doi.org/10.1261/rna.042150.113.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Schmittgen TD, Jiang J, Liu Q, Yang L. A high-throughput method to monitor the expression of microRNA precursors. Nucleic Acids Res. 2004;32:e43.  https://doi.org/10.1093/nar/gnh040.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 2005;33:e179.  https://doi.org/10.1093/nar/gni178.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Androvic P, Valihrach L, Elling J, Sjoback R, Kubista M. Two-tailed RT-qPCR: a novel method for highly accurate miRNA quantification. Nucleic Acids Res. 2017;45:e144.  https://doi.org/10.1093/nar/gkx588.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Nelson PT, Baldwin DA, Scearce LM, Oberholtzer JC, Tobias JW, Mourelatos Z. Microarray-based, high-throughput gene expression profiling of microRNAs. Nat Methods. 2004;1:155–61.  https://doi.org/10.1038/nmeth717.CrossRefPubMedGoogle Scholar
  36. 36.
    Castoldi M, Schmidt S, Benes V, Noerholm M, Kulozik AE, Hentze MW, et al. A sensitive array for microRNA expression profiling (miChip) based on locked nucleic acids (LNA). RNA. 2006;12:913–20.  https://doi.org/10.1261/rna.2332406.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Beuvink I, Kolb FA, Budach W, Garnier A, Lange J, Natt F, et al. A novel microarray approach reveals new tissue-specific signatures of known and predicted mammalian microRNAs. Nucleic Acids Res. 2007;35:e52.  https://doi.org/10.1093/nar/gkl1118.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Shen W, Deng H, Ren Y, Gao Z. A real-time colorimetric assay for label-free detection of microRNAs down to sub-femtomolar levels. Chem Commun. 2013;49:4959.  https://doi.org/10.1039/c3cc41565a.CrossRefGoogle Scholar
  39. 39.
    Yao J, Zhang Z, Zhao Y, Jing W, Zuo G. Double-stranded probe modified AuNPs for sensitive and selective detection of microRNA 30a in solution and live cell. RSC Adv. 2016;6:38869–74.  https://doi.org/10.1039/C6RA05131F.CrossRefGoogle Scholar
  40. 40.
    Miao X, Cheng Z, Ma H, Li Z, Xue N, Wang P. Label-free platform for microRNA detection based on the fluorescence quenching of positively charged gold nanoparticles to silver nanoclusters. Anal Chem. 2018;90:1098–103.  https://doi.org/10.1021/acs.analchem.7b01991.CrossRefPubMedGoogle Scholar
  41. 41.
    Cheng F-F, He T-T, Miao H-T, Shi J-J, Jiang L-P, Zhu J-J. Electron transfer mediated electrochemical biosensor for microRNAs detection based on metal ion functionalized titanium phosphate nanospheres at attomole level. ACS Appl Mater Interfaces. 2015;7:2979–85.  https://doi.org/10.1021/am508690x.CrossRefPubMedGoogle Scholar
  42. 42.
    Miao P, Tang Y, Wang B, Jiang C, Gao L, Bo B, et al. Nuclease assisted target recycling and spherical nucleic acids gold nanoparticles recruitment for ultrasensitive detection of microRNA. Electrochim Acta. 2016;190:396–401.  https://doi.org/10.1016/J.ELECTACTA.2016.01.034.CrossRefGoogle Scholar
  43. 43.
    Liu R, Wang Q, Li Q, Yang X, Wang K, Nie W. Surface plasmon resonance biosensor for sensitive detection of microRNA and cancer cell using multiple signal amplification strategy. Biosens Bioelectron. 2017;87:433–8.  https://doi.org/10.1016/j.bios.2016.08.090.CrossRefPubMedGoogle Scholar
  44. 44.
    Hong L, Lu M, Dinel M-P, Blain P, Peng W, Gu H, et al. Hybridization conditions of oligonucleotide-capped gold nanoparticles for SPR sensing of microRNA. Biosens Bioelectron. 2018;109:230–6.  https://doi.org/10.1016/J.BIOS.2018.03.032.CrossRefPubMedGoogle Scholar
  45. 45.
    Gao X, Xu H, Baloda M, Gurung AS, Xu L-P, Wang T, et al. Visual detection of microRNA with lateral flow nucleic acid biosensor. Biosens Bioelectron. 2014;54:578–84.  https://doi.org/10.1016/j.bios.2013.10.055.CrossRefPubMedGoogle Scholar
  46. 46.
    Ying N, Ju C, Sun X, Li L, Chang H, Song G, et al. Lateral flow nucleic acid biosensor for sensitive detection of microRNAs based on the dual amplification strategy of duplex-specific nuclease and hybridization chain reaction. PLoS One. 2017;12:e0185091.  https://doi.org/10.1371/journal.pone.0185091.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Alhasan AH, Kim DY, Daniel WL, Watson E, Meeks JJ, Thaxton CS, et al. Scanometric microRNA array profiling of prostate cancer markers using spherical nucleic acid-gold nanoparticle conjugates. Anal Chem. 2012;84:4153–60.  https://doi.org/10.1021/ac3004055.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Vilela D, González MC, Escarpa A. Sensing colorimetric approaches based on gold and silver nanoparticles aggregation: chemical creativity behind the assay. A review. Anal Chim Acta. 2012;751:24–43.  https://doi.org/10.1016/J.ACA.2012.08.043.CrossRefPubMedGoogle Scholar
  49. 49.
    Piriya VSA, Joseph P, Daniel SCGK, Lakshmanan S, Kinoshita T, Muthusamy S. Colorimetric sensors for rapid detection of various analytes. Mater Sci Eng C. 2017;78:1231–45.  https://doi.org/10.1016/J.MSEC.2017.05.018.CrossRefGoogle Scholar
  50. 50.
    Elghanian R, Storhoff JJ, Mucic RC, Letsinger RL, Mirkin CA. Selective colorimetric detection of polynucleotides based on the distance-dependent optical properties of gold nanoparticles. Science. 1997;277:1078–81.  https://doi.org/10.1126/SCIENCE.277.5329.1078.CrossRefPubMedGoogle Scholar
  51. 51.
    Storhoff JJ, Elghanian R, Mucic RC, Mirkin CA, Letsinger RL. One-pot colorimetric differentiation of polynucleotides with single base imperfections using gold nanoparticle probes. J Am Chem Soc. 1998;120:1959–64.  https://doi.org/10.1021/ja972332i.CrossRefGoogle Scholar
  52. 52.
    Reynolds RA, Mirkin CA, Letsinger RL. Homogeneous, nanoparticle-based quantitative colorimetric detection of oligonucleotides. J Am Chem Soc. 2000;122:3795–6.  https://doi.org/10.1021/JA000133K.CrossRefGoogle Scholar
  53. 53.
    Sanromán-Iglesias M, Lawrie CH, Schäfer T, Grzelczak M, Liz-Marzán LM. Sensitivity limit of nanoparticle biosensors in the discrimination of single nucleotide polymorphism. ACS Sens. 2016;1:1110–6.  https://doi.org/10.1021/acssensors.6b00393.CrossRefGoogle Scholar
  54. 54.
    Sanromán-Iglesias M, Lawrie CH, Liz-Marzán LM, Grzelczak M. Nanoparticle-based discrimination of single-nucleotide polymorphism in long DNA sequences. Bioconjug Chem. 2017;28:903–6.  https://doi.org/10.1021/acs.bioconjchem.7b00028.CrossRefPubMedGoogle Scholar
  55. 55.
    Sanromán-Iglesias M, Lawrie CH, Liz-Marzán LM, Grzelczak M. The role of chemically modified DNA in discrimination of single-point mutation through plasmon-based colorimetric assays. ACS Appl Nano Mater. 2018;1:3741–6.  https://doi.org/10.1021/acsanm.8b00984.CrossRefGoogle Scholar
  56. 56.
    Latorre A, Posch C, Garcimartín Y, Ortiz-Urda S, Somoza Á. Single-point mutation detection in RNA extracts using gold nanoparticles modified with hydrophobic molecular beacon-like structures. Chem Commun (Camb). 2014;50:3018–20.  https://doi.org/10.1039/c3cc47862a.CrossRefGoogle Scholar
  57. 57.
    Zhao Y, Chen F, Li Q, Wang L, Fan C. Isothermal amplification of nucleic acids. Chem Rev. 2015;115:12491–545.  https://doi.org/10.1021/acs.chemrev.5b00428.CrossRefPubMedGoogle Scholar
  58. 58.
    Li R-D, Yin B-C, Ye B-C. Ultrasensitive, colorimetric detection of microRNAs based on isothermal exponential amplification reaction-assisted gold nanoparticle amplification. Biosens Bioelectron. 2016;86:1011–6.  https://doi.org/10.1016/j.bios.2016.07.042.CrossRefPubMedGoogle Scholar
  59. 59.
    Bae HJ, Jung KH, Eun JW, Shen Q, Kim HS, Park SJ, et al. MicroRNA-221 governs tumor suppressor HDAC6 to potentiate malignant progression of liver cancer. J Hepatol. 2015;63:408–19.  https://doi.org/10.1016/j.jhep.2015.03.019.CrossRefPubMedGoogle Scholar
  60. 60.
    Garofalo M, Quintavalle C, Romano G, Croce CM, Condorelli G. miR221/222 in cancer: their role in tumor progression and response to therapy. Curr Mol Med. 2012;12:27–33.CrossRefGoogle Scholar
  61. 61.
    Wang Q, Li R-D, Yin B-C, Ye B-C. Colorimetric detection of sequence-specific microRNA based on duplex-specific nuclease-assisted nanoparticle amplification. Analyst. 2015;140:6306–12.  https://doi.org/10.1039/c5an01350j.CrossRefPubMedGoogle Scholar
  62. 62.
    Guo L, Lin Y, Chen C, Qiu B, Lin Z, Chen G. Direct visualization of sub-femtomolar circulating microRNAs in serum based on the duplex-specific nuclease-amplified oriented assembly of gold nanoparticle dimers. Chem Commun. 2016;52:11347–50.  https://doi.org/10.1039/C6CC06021H.CrossRefGoogle Scholar
  63. 63.
    Miao X, Ning X, Li Z, Cheng Z. Sensitive detection of miRNA by using hybridization chain reaction coupled with positively charged gold nanoparticles. Sci Rep. 2016;6:32358.  https://doi.org/10.1038/srep32358.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Ferhan AR, Jackman JA, Park JH, Cho N-J, Kim D-H. Nanoplasmonic sensors for detecting circulating cancer biomarkers. Adv Drug Deliv Rev.  https://doi.org/10.1016/J.ADDR.2017.12.004.CrossRefGoogle Scholar
  65. 65.
    Neupane S, Pan Y, Takalkar S, Bentz K, Farmakes J, Xu Y, et al. Probing the aggregation mechanism of gold nanoparticles triggered by a globular protein. J Phys Chem C. 2017;121:1377–86.  https://doi.org/10.1021/acs.jpcc.6b11963.CrossRefGoogle Scholar
  66. 66.
    Dubertret B, Calame M, Libchaber AJ. Single-mismatch detection using gold-quenched fluorescent oligonucleotides. Nat Biotechnol. 2001;19:365–70.  https://doi.org/10.1038/86762.CrossRefPubMedGoogle Scholar
  67. 67.
    Katz E, Willner I. Integrated nanoparticle-biomolecule hybrid systems: synthesis, properties, and applications. Angew Chem Int Ed. 2004;43:6042–108.  https://doi.org/10.1002/anie.200400651.CrossRefGoogle Scholar
  68. 68.
    Tyagi S, Kramer FR. Molecular beacons: probes that fluoresce upon hybridization. Nat Biotechnol. 1996;14:303–8.  https://doi.org/10.1038/nbt0396-303.CrossRefPubMedGoogle Scholar
  69. 69.
    Posch C, Latorre A, Crosby MB, Celli A, Latorre A, Vujic I, et al. Detection of GNAQ mutations and reduction of cell viability in uveal melanoma cells with functionalized gold nanoparticles. Biomed Microdevices. 2015;17.  https://doi.org/10.1007/s10544-014-9908-7.
  70. 70.
    Seferos DS, Giljohann DA, Hill HD, Prigodich AE, Mirkin CA. Nano-flares: probes for transfection and mRNA detection in living cells. J Am Chem Soc. 2007;129:15477–9.  https://doi.org/10.1021/ja0776529.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Prigodich AE, Seferos DS, Massich MD, Giljohann DA, Lane BC, Mirkin CA. Nano-flares for mRNA regulation and detection. ACS Nano. 2009;3:2147–52.  https://doi.org/10.1021/nn9003814.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Prigodich AE, Randeria PS, Briley WE, Kim NJ, Daniel WL, Giljohann DA, et al. Multiplexed nanoflares: mRNA detection in live cells. Anal Chem. 2012;84:2062–6.  https://doi.org/10.1021/ac202648w.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Halo TL, McMahon KM, Angeloni NL, Xu Y, Wang W, Chinen AB, et al. NanoFlares for the detection, isolation, and culture of live tumor cells from human blood. Proc Natl Acad Sci U S A. 2014;111:17104–9.  https://doi.org/10.1073/pnas.1418637111.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Zhu H, Wu H, Liu X, Li B, Chen Y, Ren X, et al. Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy. 2009;5:816–23.CrossRefGoogle Scholar
  75. 75.
    Yang X, Chen Y, Chen L. The versatile role of microRNA-30a in human cancer. Cell Physiol Biochem. 2017;41:1616–32.  https://doi.org/10.1159/000471111.CrossRefPubMedGoogle Scholar
  76. 76.
    He X, Zeng T, Li Z, Wang G, Ma N. Catalytic molecular imaging of microRNA in living cells by DNA-programmed nanoparticle disassembly. Angew Chem Int Ed. 2016;55:3073–6.  https://doi.org/10.1002/anie.201509726.CrossRefGoogle Scholar
  77. 77.
    Shen Y, Li Z, Wang G, Ma N. Photocaged nanoparticle sensor for sensitive microRNA imaging in living cancer cells with temporal control. ACS Sensors. 2018;3:494–503.  https://doi.org/10.1021/acssensors.7b00922.CrossRefPubMedGoogle Scholar
  78. 78.
    Liang C-P, Ma P-Q, Liu H, Guo X, Yin B-C, Ye B-C. Rational engineering of a dynamic, entropy-driven DNA nanomachine for intracellular microRNA imaging. Angew Chem Int Ed. 2017;56:9077–81.  https://doi.org/10.1002/anie.201704147.CrossRefGoogle Scholar
  79. 79.
    Li D, Zhou W, Yuan R, Xiang Y. A DNA-fueled and catalytic molecule machine lights up trace under-expressed microRNAs in living cells. Anal Chem. 2017;89:9934–40.  https://doi.org/10.1021/acs.analchem.7b02247.CrossRefPubMedGoogle Scholar
  80. 80.
    Yang Y, Huang J, Yang X, He X, Quan K, Xie N, et al. Gold nanoparticle based hairpin-locked-DNAzyme probe for amplified miRNA imaging in living cells. Anal Chem. 2017;89:5850–6.  https://doi.org/10.1021/acs.analchem.7b00174.CrossRefPubMedGoogle Scholar
  81. 81.
    Wu Y, Huang J, Yang X, Yang Y, Quan K, Xie N, et al. Gold nanoparticle loaded split-DNAzyme probe for amplified miRNA detection in living cells. Anal Chem. 2017;89:8377–83.  https://doi.org/10.1021/acs.analchem.7b01632.CrossRefPubMedGoogle Scholar
  82. 82.
    Peng H, Li X-F, Zhang H, Le XC. A microRNA-initiated DNAzyme motor operating in living cells. Nat Commun. 2017;8:14378.  https://doi.org/10.1038/ncomms14378.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Degliangeli F, Kshirsagar P, Brunetti V, Pompa PP, Fiammengo R. Absolute and direct microRNA quantification using DNA–gold nanoparticle probes. J Am Chem Soc. 2014;136:2264–7.  https://doi.org/10.1021/ja412152x.CrossRefPubMedGoogle Scholar
  84. 84.
    Grieshaber D, MacKenzie R, Vörös J, Reimhult E. Electrochemical biosensors - sensor principles and architectures. Sensors (Basel). 2008;8:1400–58.  https://doi.org/10.3390/s80314000.CrossRefGoogle Scholar
  85. 85.
    Thévenot DR, Toth K, Durst RA, Wilson GS. Electrochemical biosensors: recommended definitions and classification. Biosens Bioelectron. 2001;16:121–31.  https://doi.org/10.1016/S0956-5663(01)00115-4.CrossRefPubMedGoogle Scholar
  86. 86.
    D’Orazio P. Biosensors in clinical chemistry. Clin Chim Acta. 2003;334:41–69.  https://doi.org/10.1016/S0009-8981(03)00241-9.CrossRefPubMedGoogle Scholar
  87. 87.
    Daniels JS, Pourmand N. Label-free impedance biosensors: opportunities and challenges. Electroanalysis. 2007;19:1239–57.  https://doi.org/10.1002/elan.200603855.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Ronkainen NJ, Halsall HB, Heineman WR. Electrochemical biosensors. Chem Soc Rev. 2010;39:1747.  https://doi.org/10.1039/b714449k.CrossRefPubMedGoogle Scholar
  89. 89.
    Hernandez-Vargas G, Sosa-Hernández J, Saldarriaga-Hernandez S, Villalba-Rodríguez A, Parra-Saldivar R, Iqbal H. Electrochemical biosensors: a solution to pollution detection with reference to environmental contaminants. Biosensors. 2018;8:29.  https://doi.org/10.3390/bios8020029.CrossRefPubMedCentralGoogle Scholar
  90. 90.
    Inzelt G. Chronocoulometry. In: Electroanalytical methods. Berlin, Heidelberg: Springer Berlin Heidelberg. p. 147–58.Google Scholar
  91. 91.
    Hamidi-Asl E, Palchetti I, Hasheminejad E, Mascini M. A review on the electrochemical biosensors for determination of microRNAs. Talanta. 2013;115:74–83.  https://doi.org/10.1016/J.TALANTA.2013.03.061.CrossRefPubMedGoogle Scholar
  92. 92.
    Feng Q-M, Shen Y-Z, Li M-X, Zhang Z-L, Zhao W, Xu J-J, et al. Dual-wavelength electrochemiluminescence ratiometry based on resonance energy transfer between Au nanoparticles functionalized g-C 3 N 4 nanosheet and Ru(bpy)32+ for microRNA detection. Anal Chem. 2016;88:937–44.  https://doi.org/10.1021/acs.analchem.5b03670.CrossRefPubMedGoogle Scholar
  93. 93.
    Yin H, Zhou Y, Li B, Li X, Yang Z, Ai S, et al. Photoelectrochemical immunosensor for microRNA detection based on gold nanoparticles-functionalized g-C3N4 and anti-DNA:RNA antibody. Sensors Actuators B Chem. 2016;222:1119–26.  https://doi.org/10.1016/J.SNB.2015.08.019.CrossRefGoogle Scholar
  94. 94.
    Shuai H-L, Huang K-J, Zhang W-J, Cao X, Jia M-P. Sandwich-type microRNA biosensor based on magnesium oxide nanoflower and graphene oxide–gold nanoparticles hybrids coupling with enzyme signal amplification. Sensors Actuators B Chem. 2017;243:403–11.  https://doi.org/10.1016/J.SNB.2016.12.001.CrossRefGoogle Scholar
  95. 95.
    Su S, Cao W, Liu W, Lu Z, Zhu D, Chao J, et al. Dual-mode electrochemical analysis of microRNA-21 using gold nanoparticle-decorated MoS2 nanosheet. Biosens Bioelectron. 2017;94:552–9.  https://doi.org/10.1016/J.BIOS.2017.03.040.CrossRefPubMedGoogle Scholar
  96. 96.
    Zhu D, Liu W, Zhao D, Hao Q, Li J, Huang J, et al. Label-free electrochemical sensing platform for microRNA-21 detection using thionine and gold nanoparticles co-functionalized MoS 2 nanosheet. ACS Appl Mater Interfaces. 2017;9:35597–603.  https://doi.org/10.1021/acsami.7b11385.CrossRefPubMedGoogle Scholar
  97. 97.
    Yin H, Wang M, Zhou Y, Zhang X, Sun B, Wang G, et al. Photoelectrochemical biosensing platform for microRNA detection based on in situ producing electron donor from apoferritin-encapsulated ascorbic acid. Biosens Bioelectron. 2014;53:175–81.  https://doi.org/10.1016/j.bios.2013.09.053.CrossRefPubMedGoogle Scholar
  98. 98.
    Liu S, Su W, Li Z, Ding X. Electrochemical detection of lung cancer specific microRNAs using 3D DNA origami nanostructures. Biosens Bioelectron. 2015;71:57–61.  https://doi.org/10.1016/j.bios.2015.04.006.CrossRefPubMedGoogle Scholar
  99. 99.
    Zouari M, Campuzano S, Pingarrón JM, Raouafi N. Competitive RNA-RNA hybridization-based integrated nanostructured-disposable electrode for highly sensitive determination of miRNAs in cancer cells. Biosens Bioelectron. 2017;91:40–5.  https://doi.org/10.1016/J.BIOS.2016.12.033.CrossRefPubMedGoogle Scholar
  100. 100.
    Xia N, Zhang L, Wang G, Feng Q, Liu L. Label-free and sensitive strategy for microRNAs detection based on the formation of boronate ester bonds and the dual-amplification of gold nanoparticles. Biosens Bioelectron. 2013;47:461–6.  https://doi.org/10.1016/j.bios.2013.03.074.CrossRefPubMedGoogle Scholar
  101. 101.
    Liu L, Xia N, Liu H, Kang X, Liu X, Xue C, et al. Highly sensitive and label-free electrochemical detection of microRNAs based on triple signal amplification of multifunctional gold nanoparticles, enzymes and redox-cycling reaction. Biosens Bioelectron. 2014;53:399–405.  https://doi.org/10.1016/j.bios.2013.10.026.CrossRefPubMedGoogle Scholar
  102. 102.
    Miao X, Wang W, Kang T, Liu J, Shiu K-K, Leung C-H, et al. Ultrasensitive electrochemical detection of miRNA-21 by using an iridium(III) complex as catalyst. Biosens Bioelectron. 2016;86:454–8.  https://doi.org/10.1016/J.BIOS.2016.07.001.CrossRefPubMedGoogle Scholar
  103. 103.
    Huo X-L, Yang H, Zhao W, Xu J-J, Chen H-Y. Nanopore-based electrochemiluminescence for detection of microRNAs via duplex-specific nuclease-assisted target recycling. ACS Appl Mater Interfaces. 2017;9:33360–7.  https://doi.org/10.1021/acsami.7b11524.CrossRefPubMedGoogle Scholar
  104. 104.
    Tao Y, Yin D, Jin M, Fang J, Dai T, Li Y, et al. Double-loop hairpin probe and doxorubicin-loaded gold nanoparticles for the ultrasensitive electrochemical sensing of microRNA. Biosens Bioelectron. 2017;96:99–105.  https://doi.org/10.1016/j.bios.2017.04.040.CrossRefPubMedGoogle Scholar
  105. 105.
    Wang B, Dong Y-X, Wang Y-L, Cao J-T, Ma S-H, Liu Y-M. Quenching effect of exciton energy transfer from CdS:Mn to Au nanoparticles: a highly efficient photoelectrochemical strategy for microRNA-21 detection. Sensors Actuators B Chem. 2018;254:159–65.  https://doi.org/10.1016/J.SNB.2017.07.078.CrossRefGoogle Scholar
  106. 106.
    Tambyah PA, Sepramaniam S, Mohamed Ali J, Chai SC, Swaminathan P, Armugam A, et al. microRNAs in circulation are altered in response to influenza A virus infection in humans. PLoS One. 2013;8:e76811.  https://doi.org/10.1371/journal.pone.0076811.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Peng F, He J, Loo JFC, Yao J, Shi L, Liu C, et al. Identification of microRNAs in throat swab as the biomarkers for diagnosis of influenza. Int J Med Sci. 2016;13:77–84.  https://doi.org/10.7150/ijms.13301.CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Homola J, Yee SS, Gauglitz G. Surface plasmon resonance sensors: review. Sensors Actuators B Chem. 1999;54:3–15.  https://doi.org/10.1016/S0925-4005(98)00321-9.CrossRefGoogle Scholar
  109. 109.
    Daghestani HN, Day BW. Theory and applications of surface plasmon resonance, resonant mirror, resonant waveguide grating, and dual polarization interferometry biosensors. Sensors. 2010;10:9630–46.  https://doi.org/10.3390/s101109630.CrossRefPubMedGoogle Scholar
  110. 110.
    Homola J. Present and future of surface plasmon resonance biosensors. Anal Bioanal Chem. 2003;377:528–39.  https://doi.org/10.1007/s00216-003-2101-0.CrossRefPubMedGoogle Scholar
  111. 111.
    Kretschmann E. The determination of the optical constants of metals by excitation of surface plasmons. Z Physik. 1971;241:313–24.  https://doi.org/10.1007/BF01395428.CrossRefGoogle Scholar
  112. 112.
    Kretschmann E. Decay of non radiative surface plasmons into light on rough silver films. Comparison of experimental and theoretical results. Opt Commun. 1972;6:185–7.  https://doi.org/10.1016/0030-4018(72)90224-6.CrossRefGoogle Scholar
  113. 113.
    Tang Y, Zeng X, Liang J. Surface plasmon resonance: an introduction to a surface spectroscopy technique. J Chem Educ. 2010;87:742–6.  https://doi.org/10.1021/ed100186y.CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Lakayana D, Tuppurainen J, Albers M, van Linte MJ, van Iperen DJ, Weda JJA, et al. Angular scanning and variable wavelength surface plasmon resonance allowing free sensor surface selection for optimum material- and bio-sensing. Sensors Actuators B Chem. 2018;259:972–9.  https://doi.org/10.1016/J.SNB.2017.12.131.CrossRefGoogle Scholar
  115. 115.
    Olaru A, Bala C, Jaffrezic-Renault N, Aboul-Enein HY. Surface plasmon resonance (SPR) biosensors in pharmaceutical analysis. Crit Rev Anal Chem. 2015;45:97–105.  https://doi.org/10.1080/10408347.2014.881250.CrossRefPubMedGoogle Scholar
  116. 116.
    Petryayeva E, Krull UJ. Localized surface plasmon resonance: nanostructures, bioassays and biosensing - a review. Anal Chim Acta. 2011;706:8–24.  https://doi.org/10.1016/J.ACA.2011.08.020.CrossRefPubMedGoogle Scholar
  117. 117.
    Willets KA, Van Duyne RP. Localized surface plasmon resonance spectroscopy and sensing. Annu Rev Phys Chem. 2007;58:267–97.  https://doi.org/10.1146/annurev.physchem.58.032806.104607.CrossRefPubMedGoogle Scholar
  118. 118.
    Wang Q, Liu R, Yang X, Wang K, Zhu J, He L, et al. Surface plasmon resonance biosensor for enzyme-free amplified microRNA detection based on gold nanoparticles and DNA supersandwich. Sensors Actuators B Chem. 2016;223:613–20.  https://doi.org/10.1016/J.SNB.2015.09.152.CrossRefGoogle Scholar
  119. 119.
    Lu Z, Liu M, Stribinskis V, Klinge CM, Ramos KS, Colburn NH, et al. MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene. 2008;27:4373–9.  https://doi.org/10.1038/onc.2008.72.CrossRefPubMedGoogle Scholar
  120. 120.
    Medina PP, Slack FJ. MicroRNAs and cancer: an overview. Cell Cycle. 2008;7:2485–92.  https://doi.org/10.4161/cc.7.16.6453.CrossRefPubMedGoogle Scholar
  121. 121.
    Nie W, Wang Q, Yang X, Zhang H, Li Z, Gao L, et al. High sensitivity surface plasmon resonance biosensor for detection of microRNA based on gold nanoparticles-decorated molybdenum sulfide. Anal Chim Acta. 2017;993:55–62.  https://doi.org/10.1016/j.aca.2017.09.015.CrossRefPubMedGoogle Scholar
  122. 122.
    Wang Q, Li Q, Yang X, Wang K, Du S, Zhang H, et al. Graphene oxide-gold nanoparticles hybrids-based surface plasmon resonance for sensitive detection of microRNA. Biosens Bioelectron. 2016;77:1001–7.  https://doi.org/10.1016/j.bios.2015.10.091.CrossRefPubMedGoogle Scholar
  123. 123.
    Li Q, Wang Q, Yang X, Wang K, Zhang H, Nie W. High sensitivity surface plasmon resonance biosensor for detection of microRNA and small molecule based on graphene oxide-gold nanoparticles composites. Talanta. 2017;174:521–6.  https://doi.org/10.1016/j.talanta.2017.06.048.CrossRefPubMedGoogle Scholar
  124. 124.
    Mariani S, Minunni M. Surface plasmon resonance applications in clinical analysis. Anal Bioanal Chem. 2014;406:2303–23.  https://doi.org/10.1007/s00216-014-7647-5.CrossRefPubMedGoogle Scholar
  125. 125.
    Nguyen HH, Park J, Kang S, Kim M. Surface plasmon resonance: a versatile technique for biosensor applications. Sensors (Basel). 2015;15:10481–510.  https://doi.org/10.3390/s150510481.CrossRefGoogle Scholar
  126. 126.
    Scarano S, Mascini M, Turner APF, Minunni M. Surface plasmon resonance imaging for affinity-based biosensors. Biosens Bioelectron. 2010;25:957–66.  https://doi.org/10.1016/J.BIOS.2009.08.039.CrossRefPubMedGoogle Scholar
  127. 127.
    Šípová H, Homola J. Surface plasmon resonance sensing of nucleic acids: a review. Anal Chim Acta. 2013;773:9–23.  https://doi.org/10.1016/J.ACA.2012.12.040.CrossRefPubMedGoogle Scholar
  128. 128.
    Zhang GP, Wang XN, Yang JF, Yang YY, Xing GX, Li QM, et al. Development of an immunochromatographic lateral flow test strip for detection of β-adrenergic agonist Clenbuterol residues. J Immunol Methods. 2006;312:27–33.  https://doi.org/10.1016/J.JIM.2006.02.017.CrossRefPubMedGoogle Scholar
  129. 129.
    Posthuma-Trumpie GA, Korf J, van Amerongen A. Lateral flow (immuno)assay: its strengths, weaknesses, opportunities and threats. A literature survey. Anal Bioanal Chem. 2009;393:569–82.  https://doi.org/10.1007/s00216-008-2287-2.CrossRefPubMedGoogle Scholar
  130. 130.
    Ngom B, Guo Y, Wang X, Bi D. Development and application of lateral flow test strip technology for detection of infectious agents and chemical contaminants: a review. Anal Bioanal Chem. 2010;397:1113–35.  https://doi.org/10.1007/s00216-010-3661-4.CrossRefPubMedGoogle Scholar
  131. 131.
    Xu H, Chen J, Birrenkott J, Zhao JX, Takalkar S, Baryeh K, et al. Gold-nanoparticle-decorated silica nanorods for sensitive visual detection of proteins. Anal Chem. 2014;86:7351–9.  https://doi.org/10.1021/ac502249f.CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    Parolo C, Merkoçi A. Paper-based nanobiosensors for diagnostics. Chem Soc Rev. 2013;42:450–7.  https://doi.org/10.1039/C2CS35255A.CrossRefPubMedGoogle Scholar
  133. 133.
    Georges SA, Biery MC, Kim S -y, Schelter JM, Guo J, Chang AN, et al. Coordinated regulation of cell cycle transcripts by p53-inducible microRNAs, miR-192 and miR-215. Cancer Res. 2008;68:10105–12.  https://doi.org/10.1158/0008-5472.CAN-08-1846.CrossRefPubMedGoogle Scholar
  134. 134.
    Cai X, Peng D, Wei H, Yang X, Huang Q, Lin Z, et al. miR-215 suppresses proliferation and migration of non-small cell lung cancer cells. Oncol Lett. 2017;13:2349–53.  https://doi.org/10.3892/ol.2017.5692.CrossRefPubMedPubMedCentralGoogle Scholar
  135. 135.
    Yao Y, Shen H, Zhou Y, Yang Z, Hu T. MicroRNA-215 suppresses the proliferation, migration and invasion of non-small cell lung carcinoma cells through the downregulation of matrix metalloproteinase-16 expression. Exp Ther Med. 2018;15:3239–46.  https://doi.org/10.3892/etm.2018.5869.CrossRefPubMedPubMedCentralGoogle Scholar
  136. 136.
    Hou S-Y, Hsiao Y-L, Lin M-S, Yen C-C, Chang C-S. MicroRNA detection using lateral flow nucleic acid strips with gold nanoparticles. Talanta. 2012;99:375–9.  https://doi.org/10.1016/j.talanta.2012.05.067.CrossRefPubMedGoogle Scholar
  137. 137.
    Gao X, Xu L-P, Wu T, Wen Y, Ma X, Zhang X. An enzyme-amplified lateral flow strip biosensor for visual detection of microRNA-224. Talanta. 2016;146:648–54.  https://doi.org/10.1016/J.TALANTA.2015.06.060.CrossRefPubMedGoogle Scholar
  138. 138.
    Huang Y, Wang W, Wu T, Xu L-P, Wen Y, Zhang X. A three-line lateral flow biosensor for logic detection of microRNA based on Y-shaped junction DNA and target recycling amplification. Anal Bioanal Chem. 2016;408:8195–202.  https://doi.org/10.1007/s00216-016-9925-x.CrossRefPubMedGoogle Scholar
  139. 139.
    Li W, Ruan K. MicroRNA detection by microarray. Anal Bioanal Chem. 2009;394:1117–24.  https://doi.org/10.1007/s00216-008-2570-2.CrossRefPubMedGoogle Scholar
  140. 140.
    Roy S, Soh JH, Ying JY. A microarray platform for detecting disease-specific circulating miRNA in human serum. Biosens Bioelectron. 2016;75:238–46.  https://doi.org/10.1016/j.bios.2015.08.039.CrossRefPubMedGoogle Scholar
  141. 141.
    Taton TA, Mirkin CA, Letsinger RL. Scanometric DNA array detection with nanoparticle probes. Science. 2000;289:1757–60.CrossRefGoogle Scholar
  142. 142.
    Alhasan AH, Scott AW, Wu JJ, Feng G, Meeks JJ, Thaxton CS, et al. Circulating microRNA signature for the diagnosis of very high-risk prostate cancer. Proc Natl Acad Sci U S A. 2016;113:10655–60.  https://doi.org/10.1073/pnas.1611596113.CrossRefPubMedPubMedCentralGoogle Scholar
  143. 143.
    Park J, Yeo J-S. Colorimetric detection of microRNA miR-21 based on nanoplasmonic core–satellite assembly. Chem Commun. 2014;50:1366–8.  https://doi.org/10.1039/C3CC48154A.CrossRefGoogle Scholar
  144. 144.
    Wang Y, MacLachlan E, Nguyen BK, Fu G, Peng C, Chen JIL. Direct detection of microRNA based on plasmon hybridization of nanoparticle dimers. Analyst. 2015;140:1140–8.  https://doi.org/10.1039/c4an02189d.CrossRefPubMedGoogle Scholar
  145. 145.
    Yin JQ, Zhao RC, Morris KV. Profiling microRNA expression with microarrays. Trends Biotechnol. 2008;26:70–6.  https://doi.org/10.1016/J.TIBTECH.2007.11.007.CrossRefPubMedGoogle Scholar
  146. 146.
    Dong H, Lei J, Ding L, Wen Y, Ju H, Zhang X. MicroRNA: function, detection, and bioanalysis. Chem Rev. 2013;113:6207–33.  https://doi.org/10.1021/cr300362f.CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto Madrileño de Estudios Avanzados en Nanociencia (IMDEA Nanociencia) & Nanobiotecnología (IMDEA Nanociencia)Unidad Asociada al Centro Nacional de Biotecnología (CSIC)MadridSpain

Personalised recommendations