Toward biosensors for the detection of circulating microRNA as a cancer biomarker: An overview of the challenges and successes

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 7, Issue 4, 2015, Pages 580-592

  Tavallaie, Roya ^a   De Almeida, Swahnnya R M ^a   Gooding, J Justin ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMARKERS; BIOSENSORS; DIAGNOSIS; DISEASES; NONINVASIVE MEDICAL PROCEDURES; PATIENT TREATMENT;

CANCER BIOMARKERS; CIRCULATING MICRORNA; CLINICAL PRACTICES; CLINICAL UTILITY; FUTURE PROSPECTS; MIRNA DETECTIONS; POINT-OF-CARE TESTING; SAMPLE PREPARATION;

RNA;

MICRORNA; TUMOR MARKER;

ARTICLE; BIOGENESIS; BIOSENSOR; BODY FLUID; CANCER DIAGNOSIS; CANCER PATIENT; CANCER PROGNOSIS; CIRCULATING TUMOR CELL; CLINICAL PRACTICE; COMPARATIVE STUDY; DEVELOPING COUNTRY; DIAGNOSTIC TEST ACCURACY STUDY; DNA SEQUENCE; ELECTROMECHANICAL BIOSENSOR; GENE EXPRESSION; HUMAN; LIMIT OF DETECTION; MEDICAL PROCEDURES; OPTICAL BIOSENSOR; POINT OF CARE TESTING; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA SEQUENCE; BLOOD; ELECTROCHEMICAL ANALYSIS; GENETIC PROCEDURES; NEOPLASMS; PROCEDURES;

BIOMARKERS, TUMOR; BIOSENSING TECHNIQUES; ELECTROCHEMICAL TECHNIQUES; HUMANS; MICRORNAS; NEOPLASMS;

EID: 84931567968     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1324     Document Type: Article

References (90)

1. Dong H, Lei J, Ding L, Wen Y, Ju H, Zhang X. MicroRNA: function, detection, and bioanalysis. Chem Rev 2013, 113:6207-6233.
2. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008, 105:10513-10518.
3. Ma RM, Jiang T, Kang XX. Circulating microRNAs in cancer: origin, function and application. J Exp Clin Cancer Res 2012, 31:38.
4. Mo MH, Chen L, Fu YB, Wang W, Fu SW. Cell-free circulating miRNA biomarkers in cancer. J. Cancer 2012, 3:432-448.
5. Tezcan G, Tunca B, Bekar A, Preusser M, Berghoff AS, Egeli U, Cecener G, Ricken G, Budak F, Taskapilioglu MO, et al. microRNA expression pattern modulates temozolomide response in GBM tumors with cancer stem cells. Cell Mol Neurobiol 2014, 34:679-692.
6. Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, Tait JF, Tewari M. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res (Phila) 2012, 5:492-497.
7. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res 2011, 39:7223-7233.
8. Williams Z, Ben-Dov IZ, Elias R, Mihailovic A, Brown M, Rosenwaks Z, Tuschl T. Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations. Proc Natl Acad Sci USA 2013, 110:4255-4260.
9. Madhavan D, Cuk K, Burwinkel B, Yang R. Cancer diagnosis and prognosis decoded by blood-based circulating microRNA signatures. Front Genet 2013, 4:116.
10. Blondal T, Jensby Nielsen S, Baker A, Andreasen D, Mouritzen P, Wrang Teilum M, Dahlsveen IK. Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods 2013, 59:S1-S6.
11. Kroh EM, Parkin RK, Mitchell PS, Tewari M. Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR) (vol 50, pg 298, 2010). Methods 2010, 52:268.
12. De Guire V, Robitaille R, Tetreault N, Guerin R, Menard C, Bambace N, Sapieha P. Circulating miRNAs as sensitive and specific biomarkers for the diagnosis and monitoring of human diseases: promises and challenges. Clin Biochem 2013, 46:846-860.
13. 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.
14. Turchinovich A, Weiz L, Burwinkel B. Extracellular miRNAs: the mystery of their origin and function. Trends Biochem Sci 2012, 37:460-465.
15. de Planell-Saguer M, Rodicio MC. Detection methods for microRNAs in clinic practice. Clin Biochem 2013, 46:869-878.
16. Wang Y, Zheng DL, Tan QL, Wang MX, Gu LQ. Nanopore-based detection of circulating microRNAs in lung cancer patients. Nat Nanotechnol 2011, 6:668-674.
17. Labib M, Khan N, Ghobadloo SM, Cheng J, Pezacki JP, Berezovski MV. Three-mode electrochemical sensing of ultralow microRNA levels. J Am Chem Soc 2013, 135:3027-3038.
18. Johnson BN, Mutharasan R. Sample preparation-free, real-time detection of microRNA in human serum using piezoelectric cantilever biosensors at attomole level. Anal Chem 2012, 84:10426-10436.
19. Tran HV, Piro B, Reisberg S, Tran LD, Duc HT, Pham MC. Label-free and reagentless electrochemical detection of microRNAs using a conducting polymer nanostructured by carbon nanotubes: application to prostate cancer biomarker miR-141. Biosens Bioelectron 2013, 49:164-169.
20. Sandhu S, Garzon R. Potential applications of microRNAs in cancer diagnosis, prognosis, and treatment. Semin Oncol 2011, 38:781-787.
21. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
22. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010, 11:597-610.
23. Neilsen CT, Goodall GJ, Bracken CP. IsomiRs-the overlooked repertoire in the dynamic microRNAome. Trends Genet 2012, 28:544-549.
24. Berezikov E. Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 2011, 12:846-860.
25. Garzon R, Marcucci G, Croce CM. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov 2010, 9:775-789.
26. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, Negrini M, Bullrich F, Croce CM. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002, 99:15524-15529.
27. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838.
28. Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med 2009, 60:167-179.
29. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ. A microRNA polycistron as a potential human oncogene. Nature 2005, 435:828-833.
30. Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2011, 39:D152-D157.
31. Lu M, Zhang Q, Deng M, Miao J, Guo Y, Gao W, Cui Q. An analysis of human microRNA and disease associations. PLoS One 2008, 3:e3420.
32. Lawrie CH, Gal S, Dunlop HM, Pushkaran B, Liggins AP, Pulford K, Banham AH, Pezzella F, Boultwood J, Wainscoat JS, et al. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008, 141:672-675.
33. Reid G, Kirschner MB, van Zandwijk N. Circulating microRNAs: association with disease and potential use as biomarkers. Crit Rev Oncol Hematol 2011, 80:193-208.
34. Catuogno S, Esposito CL, Quintavalle C, Cerchia L, Condorelli G, de Franciscis V. Recent advance in biosensors for microRNAs detection in cancer. Cancers 2011, 3:1877-1898.
35. Yaman AF, Kovancilar M, Dizdar Y, Darendeliler E, Holdenrieder S, Dalay N, Gezer U. Investigation of miR-21, miR-141, and miR-221 in blood circulation of patients with prostate cancer. Tumor Biol 2011, 32:583-588.
36. Shen J, Liu Z, Todd NW, Zhang H, Liao J, Yu L, Guarnera MA, Li R, Cai L, Zhan M, et al. Diagnosis of lung cancer in individuals with solitary pulmonary nodules by plasma microRNA biomarkers. BMC Cancer 2011, 11:374.
37. Keller A, Leidinger P, Bauer A, ElSharawy A, Haas J, Backes C, Wendschlag A, Giese N, Tjaden C, Ott K. Toward the blood-borne miRNome of human diseases. Nat Methods 2011, 8:841-843.
38. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 2008, 18:997-1006.
39. Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer 2009, 10:42-46.
40. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011, 108:5003-5008.
41. Zampetaki A, Willeit P, Drozdov I, Kiechl S, Mayr M. Profiling of circulating microRNAs: from single biomarkers to re-wired networks. Cardiovasc Res 2012, 93:555-562.
42. Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 2010, 101:2087-2092.
43. Etheridge A, Lee I, Hood L, Galas D, Wang K. Extracellular microRNA: a new source of biomarkers. Mutat Res 2011, 717:85-90.
44. Wang K, Yuan Y, Cho J-H, McClarty S, Baxter D, Galas DJ. Comparing the MicroRNA spectrum between serum and plasma. PLoS One 2012, 7:e41561.
45. McDonald JS, Milosevic D, Reddi HV, Grebe SK, Algeciras-Schimnich A. Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem 2011, 57:833-840.
46. Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One 2012, 7:e30679.
47. Zen K, Zhang C-Y. Circulating MicroRNAs: a novel class of biomarkers to diagnose and monitor human cancers. Med Res Rev 2012, 32:326-348.
48. Kim Y-K, Yeo J, Kim B, Ha M, Kim VN. Short structured RNAs with low GC content are selectively lost during extraction from a small number of cells. Mol Cell 2012, 46:893-895.
49. Kroh EM, Parkin RK, Mitchell PS, Tewari M. Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 2010, 50:298-301.
50. Campuzano S, Kuralay F, Lobo-Castañón MJ, Bartošík M, Vyavahare K, Paleček E, Haake DA, Wang J. Ternary monolayers as DNA recognition interfaces for direct and sensitive electrochemical detection in untreated clinical samples. Biosensors and Bioelectronics 2011, 26:3577-3583.
51. Kaur H, Arora A, Wengel J, Maiti S. Thermodynamic, counterion, and hydration effects for the incorporation of locked nucleic acid nucleotides into DNA duplexes. Biochemistry 2006, 45:7347-7355.
52. Lee LW, Zhang S, Etheridge A, Ma L, Martin D, Galas D, Wang K. Complexity of the microRNA repertoire revealed by next-generation sequencing. RNA 2010, 16:2170-2180.
53. Chen C, Ridzon DA, Broomer AJ, Zhou ZH, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005, 33:e179.
54. Ell B, Mercatali L, Ibrahim T, Campbell N, Schwarzenbach H, Pantel K, Amadori D, Kang YB. Tumor-induced osteoclast miRNA changes as regulators and biomarkers of osteolytic bone metastasis. Cancer Cell 2013, 24:542-556.
55. Castoldi M, Schmidt S, Benes V, Noerholm M, Kulozik AE, Hentze MW, Muckenthaler MU. A sensitive array for microRNA expression profiling (miChip) based on locked nucleic acids (LNA). RNA 2006, 12:913-920.
56. Shendure J, Ji HL. Next-generation DNA sequencing. Nat Biotechnol 2008, 26:1135-1145.
57. Ryan BM, Robles AI, Harris CC. Genetic variation in microRNA networks: the implications for cancer research. Nat Rev Cancer 2010, 10:389.
58. Chang HT, Li SC, Ho MR, Pan HW, Ger LP, Hu LY, Yu SY, Li WH, Tsai KW. Comprehensive analysis of microRNAs in breast cancer. BMC Genomics 2012, 13:S18.
59. Jiang L, Duan DM, Shen Y, Li J. Direct microRNA detection with universal tagged probe and time-resolved fluorescence technology. Biosens Bioelectron 2012, 34:291-295.
60. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, Baek D, Johnston WK, Russ C, Luo SJ, Babiarz JE, et al. Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev 2010, 24:992-1009.
61. Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: approaches and considerations. Nat Rev Genet 2012, 13:358-369.
62. Git A, Dvinge H, Salmon-Divon M, Osborne M, Kutter C, Hadfield J, Bertone P, Caldas C. Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression. RNA 2010, 16:991-1006.
63. Liu CG, Calin GA, Volinia S, Croce CM. MicroRNA expression profiling using microarrays. Nat Protoc 2008, 3:563-578.
64. Hydbring P, Badalian-Very G. Clinical applications of microRNAs. F1000Res 2013, 2:136.
65. Hou SY, Hsiao YL, Lin MS, Yen CC, Chang CS. MicroRNA detection using lateral flow nucleic acid strips with gold nanoparticles. Talanta 2012, 99:375-379.
66. Homola J. Surface plasmon resonance sensors for detection of chemical and biological species. Chem Rev 2008, 108:462-493.
67. Blackie EJ, Le Ru EC, Etchegoin PG. Single-molecule surface-enhanced Raman spectroscopy of nonresonant molecules. J Am Chem Soc 2009, 131:14466-14472.
68. Muniz-Miranda M, Gellini C, Pagliai M, Innocenti M, Salvi PR, Schettino V. SERS and computational studies on microRNA chains adsorbed on silver surfaces. J Phys Chem C 2010, 114:13730-13735.
69. Batchelor-McAuley C, Wildgoose GG, Compton RG. The physicochemical aspects of DNA sensing using electrochemical methods. Biosens Bioelectron 2009, 24:3183-3190.
70. Odenthal KJ, Gooding JJ. An introduction to electrochemical DNA biosensors. Analyst 2007, 132:603-610.
71. Lusi EA, Passamano M, Guarascio P, Scarpa A, Schiavo L. Innovative electrochemical approach for an early detection of microRNAs. Anal Chem 2009, 81:2819-2822.
72. Hong CY, Chen X, Liu T, Li J, Yang HH, Chen JH, Chen GN. Ultrasensitive electrochemical detection of cancer-associated circulating microRNA in serum samples based on DNA concatamers. Biosens Bioelectron 2013, 50:132-136.
73. Kilic T, Topkaya SN, Ozsoz M. A new insight into electrochemical microRNA detection: a molecular caliper, p19 protein. Biosens Bioelectron 2013, 48:165-171.
74. Khan N, Cheng J, Pezacki JP, Berezovski MV. Quantitative analysis of MicroRNA in blood serum with protein-facilitated affinity capillary electrophoresis. Anal Chem 2011, 83:6196-6201.
75. Bayley H, Jayasinghe L. Functional engineered channels and pores-(review). Mol Membr Biol 2004, 21:209-220.
76. Gyurcsanyi RE. Chemically-modified nanopores for sensing. Trac Trends Anal. Chem. 2008, 27:627-639.
77. Wanunu M, Morrison W, Rabin Y, Grosberg AY, Meller A. Electrostatic focusing of unlabelled DNA into nanoscale pores using a salt gradient. Nat Nanotechnol 2010, 5:160-165.
78. Hofler L, Gyurcsanyi RE. Nanosensors lost in space. A random walk study of single molecule detection with single-nanopore sensors. Anal Chim Acta 2012, 722:119-126.
79. Branton D, Deamer DW, Marziali A, Bayley H, Benner SA, Butler T, Di Ventra M, Garaj S, Hibbs A, Huang XH, et al. The potential and challenges of nanopore sequencing. Nat Biotechnol 2008, 26:1146-1153.
80. Bayley H. Sequencing single molecules of DNA. Curr Opin Chem Biol 2006, 10:628-637.
81. Movileanu L. Interrogating single proteins through nanopores: challenges and opportunities. Trends Biotechnol 2009, 27:333-341.
82. Ma L, Cockroft SL. Biological nanopores for single-molecule biophysics. Chembiochem 2010, 11:25-34.
83. Kasianowicz JJ, Brandin E, Branton D, Deamer DW. Characterization of individual polynucleotide molecules using a membrane channel. Proc Natl Acad Sci USA 1996, 93:13770-13773.
84. Meller A, Nivon L, Branton D. Voltage-driven DNA translocations through a nanopore. Phys Rev Lett 2001, 86:3435-3438.
85. Song LZ, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 1996, 274:1859-1866.
86. Rijal K, Mutharasan R. PEMC-based method of measuring DNA hybridization at femtomolar concentration directly in human serum and in the presence of copious noncomplementary strands. Anal Chem 2007, 79:7392-7400.
87. Fang SP, Lee HJ, Wark AW, Corn RM. Attomole microarray detection of MicroRNAs by nanoparticle-amplified SPR imaging measurements of surface polyadenylation reactions. J Am Chem Soc 2006, 128:14044-14046.
88. Yang WJ, Li XB, Li YY, Zhao LF, He WL, Gao YQ, Wan YJ, Xia W, Chen T, Zheng H, et al. Quantification of microRNA by gold nanoparticle probes. Anal Biochem 2008, 376:183-188.
89. Qavi AJ, Bailey RC. Multiplexed detection and label-free quantitation of microRNAs using arrays of silicon photonic microring resonators. Angew Chem Int Ed 2010, 49:4608-4611.
90. Li JS, Schachermeyer S, Wang Y, Yin YD, Zhong WW. Detection of microRNA by fluorescence amplification based on cation-exchange in nanocrystals. Anal Chem 2009, 81:9723-9729.