Peptide Nucleic Acid-Based Biosensors for Cancer Diagnosis

The monitoring of DNA and RNA biomarkers freely circulating in the blood constitutes the basis of innovative cancer detection methods based on liquid biopsy. Such methods are expected to provide new opportunities for a better understanding of cancer disease at the molecular level, thus contributing to improved patient outcomes. Advanced biosensors can advance possibilities for cancer-related nucleic acid biomarkers detection. In this context, peptide nucleic acids (PNAs) play an important role in the fabrication of highly sensitive biosensors. This review provides an overview of recently described PNA-based biosensors for cancer biomarker detection. One of the most striking features of the described detection approaches is represented by the possibility to detect target nucleic acids at the ultra-low concentration with the capability to identify single-base mutations.

[1]  K. Pantel,et al.  Challenges in circulating tumour cell research , 2014, Nature Reviews Cancer.

[2]  M. Fabbri,et al.  MicroRNAs and other non-coding RNAs as targets for anticancer drug development , 2013, Nature Reviews Drug Discovery.

[3]  Roberto Corradini,et al.  Ultrasensitive detection of non-amplified genomic DNA by nanoparticle-enhanced surface plasmon resonance imaging. , 2010, Biosensors & bioelectronics.

[4]  Jeong-Woo Choi,et al.  Application of peptide nucleic acid towards development of nanobiosensor arrays. , 2010, Bioelectrochemistry.

[5]  Sang Woo Han,et al.  Quantitative and multiplexed microRNA sensing in living cells based on peptide nucleic acid and nano graphene oxide (PANGO). , 2013, ACS nano.

[6]  K. Miura,et al.  Quantitative assessment of DNA microarrays--comparison with Northern blot analyses. , 2001, Genomics.

[7]  Guojun Zhang,et al.  Gold nanoparticles-decorated graphene field-effect transistor biosensor for femtomolar MicroRNA detection. , 2015, Biosensors & bioelectronics.

[8]  Q. Cui,et al.  An Analysis of Human MicroRNA and Disease Associations , 2008, PloS one.

[9]  D. Beebe,et al.  The present and future role of microfluidics in biomedical research , 2014, Nature.

[10]  Pier Paolo Pompa,et al.  Nanotechnology-based strategies for the detection and quantification of microRNA. , 2014, Chemistry.

[11]  Orawon Chailapakul,et al.  Electrochemical detection of human papillomavirus DNA type 16 using a pyrrolidinyl peptide nucleic acid probe immobilized on screen-printed carbon electrodes. , 2014, Biosensors & bioelectronics.

[12]  G. Ginsburg,et al.  The path to personalized medicine. , 2002, Current opinion in chemical biology.

[13]  Poul Nielsen,et al.  LNA (locked nucleic acids): synthesis and high-affinity nucleic acid recognition , 1998 .

[14]  Ilaria Palchetti,et al.  A review on the electrochemical biosensors for determination of microRNAs. , 2013, Talanta.

[15]  Wei Wang,et al.  Fluorescence quenching of carbon nitride nanosheet through its interaction with DNA for versatile fluorescence sensing. , 2013, Analytical chemistry.

[16]  Bicai Pan,et al.  Enhanced photoresponsive ultrathin graphitic-phase C3N4 nanosheets for bioimaging. , 2013, Journal of the American Chemical Society.

[17]  A. Manicardi,et al.  Peptide nucleic acids with a structurally biased backbone. Updated review and emerging challenges. , 2011, Current topics in medicinal chemistry.

[18]  C. Croce,et al.  Clinical Applications for microRNAs in Cancer , 2013, Clinical pharmacology and therapeutics.

[19]  Tingrui Pan,et al.  From Cleanroom to Desktop: Emerging Micro-Nanofabrication Technology for Biomedical Applications , 2010, Annals of Biomedical Engineering.

[20]  A. Thierry.  A Targeted Q-PCR-Based Method for Point Mutation Testing by Analyzing Circulating DNA for Cancer Management Care. , 2016, Methods in molecular biology.

[21]  Sang Jun Sim,et al.  Nanoplasmonic biosensor: detection and amplification of dual bio-signatures of circulating tumor DNA. , 2015, Biosensors & bioelectronics.

[22]  A. Nitsche,et al.  Real-time PCR in virology. , 2002, Nucleic acids research.

[23]  Andrey L Rogach,et al.  Properties and Applications of Colloidal Nonspherical Noble Metal Nanoparticles , 2010, Advanced materials.

[24]  F. Nicolantonio,et al.  Liquid biopsy: monitoring cancer-genetics in the blood , 2013, Nature Reviews Clinical Oncology.

[25]  R. Marchelli,et al.  Kinetic and affinity analyses of hybridization reactions between peptide nucleic acid probes and DNA targets using surface plasmon field-enhanced fluorescence spectroscopy , 2006, Biointerphases.

[26]  Jurriaan Huskens,et al.  Reactivity mapping with electrochemical gradients for monitoring reactivity at surfaces in space and time , 2013, Nature Communications.

[27]  Yuejun Kang,et al.  Nano metal-organic framework (NMOF)-based strategies for multiplexed microRNA detection in solution and living cancer cells. , 2015, Nanoscale.

[28]  I. Oh,et al.  Peptide Nucleic Acid Clamping Versus Direct Sequencing for the Detection of EGFR Gene Mutation in Patients with Non-small Cell Lung Cancer , 2015, Cancer research and treatment : official journal of Korean Cancer Association.

[29]  T. Hudson,et al.  The Genetic Basis for Cancer Treatment Decisions , 2012, Cell.

[30]  Voravee P. Hoven,et al.  Synthesis and immobilization of thiolated pyrrolidinyl peptide nucleic acids on gold-coated piezoelectric quartz crystals for the detection of DNA hybridization , 2009 .

[31]  M. Egholm,et al.  Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide. , 1991, Science.

[32]  Construction of a novel peptide nucleic acid piezoelectric gene sensor microarray detection system. , 2005, Journal of nanoscience and nanotechnology.

[33]  E. Izaurralde,et al.  Gene silencing by microRNAs: contributions of translational repression and mRNA decay , 2011, Nature Reviews Genetics.

[34]  Takahiro Ochiya,et al.  Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis , 2010, Cancer science.

[35]  Giuseppe Spoto,et al.  Isothermal Amplification Methods for the Detection of Nucleic Acids in Microfluidic Devices , 2012, Biosensors.

[36]  H. Orum.  PCR clamping. , 2000, Current issues in molecular biology.

[37]  S. Awasthi,et al.  Cell-dependent differential cellular uptake of PNA, peptides, and PNA-peptide conjugates. , 2002, Antisense & nucleic acid drug development.

[38]  Gang Liu,et al.  High-sensitivity nanosensors for biomarker detection. , 2012, Chemical Society reviews.

[39]  Gerhard Breipohl,et al.  PNA: Synthetic Polyamide Nucleic Acids with Unusual Binding Properties. , 1998, Angewandte Chemie.

[40]  Peter E. Nielsen,et al.  LNA (Locked Nucleic Acids): Synthesis and High-Affinity Nucleic Acid Recognition. , 1998 .

[41]  Zhengchun Liu,et al.  A review: fabrications, detections and applications of peptide nucleic acids (PNAs) microarray. , 2015, Biosensors & bioelectronics.

[42]  Rajeev Ranjan,et al.  Rapid biosensing tools for cancer biomarkers. , 2017, Biosensors & bioelectronics.

[43]  Shana O Kelley,et al.  DNA Clutch Probes for Circulating Tumor DNA Analysis. , 2016, Journal of the American Chemical Society.

[44]  S. Deo,et al.  MicroRNA Detection: Challenges for the Analytical Chemist , 2007 .

[45]  Marcelo Mulato,et al.  Highly sensitive dual mode electrochemical platform for microRNA detection , 2016, Scientific Reports.

[46]  M. O'keeffe,et al.  Design and synthesis of an exceptionally stable and highly porous metal-organic framework , 1999, Nature.

[47]  K. E. Lundin,et al.  Biological activity and biotechnological aspects of peptide nucleic acid. , 2006, Advances in genetics.

[48]  R. Gambari.  Peptide nucleic acids: a review on recent patents and technology transfer , 2014, Expert opinion on therapeutic patents.

[49]  Klaus Pantel,et al.  Cell-free nucleic acids as biomarkers in cancer patients , 2011, Nature Reviews Cancer.

[50]  G. Spoto,et al.  Streptavidin-coated gold nanoparticles: critical role of oligonucleotides on stability and fractal aggregation , 2017, Beilstein journal of nanotechnology.

[51]  A. Weinhäusel,et al.  The current status of cancer biomarker research using tumour-associated antigens for minimal invasive and early cancer diagnostics. , 2012, Journal of proteomics.

[52]  Shenguang Ge,et al.  Nanomaterials-modified cellulose paper as a platform for biosensing applications. , 2017, Nanoscale.

[53]  Sebastian D. Mackowiak,et al.  Circular RNAs are a large class of animal RNAs with regulatory potency , 2013, Nature.

[54]  G. Parmigiani,et al.  Detection of Chromosomal Alterations in the Circulation of Cancer Patients with Whole-Genome Sequencing , 2012, Science Translational Medicine.

[55]  Bo Liedberg,et al.  Naked eye detection of lung cancer associated miRNA by paper based biosensing platform. , 2013, Analytical chemistry.

[56]  Giuseppe Spoto,et al.  Surface plasmon resonance imaging for nucleic acid detection , 2012, Analytical and Bioanalytical Chemistry.

[57]  J. Lyu,et al.  Graphene and graphene-like two-denominational materials based fluorescence resonance energy transfer (FRET) assays for biological applications. , 2017, Biosensors & bioelectronics.

[58]  J. Deleuze,et al.  Comprehensive evaluation of methods to isolate, quantify, and characterize circulating cell-free DNA from small volumes of plasma , 2015, Analytical and Bioanalytical Chemistry.

[59]  S. Murata,et al.  Novel Methodology for Rapid Detection of KRAS Mutation Using PNA-LNA Mediated Loop-Mediated Isothermal Amplification , 2016, PloS one.

[60]  J. Bisi,et al.  Antisense and antigene properties of peptide nucleic acids. , 1992, Science.

[61]  V. Velculescu,et al.  Blood-based analyses of cancer: circulating tumor cells and circulating tumor DNA. , 2014, Cancer discovery.

[62]  Peter E. Nielsen,et al.  Kinetics and mechanism of the DNA double helix invasion by pseudocomplementary peptide nucleic acids , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Sebo Withoff,et al.  Genetic variation in the non-coding genome: Involvement of micro-RNAs and long non-coding RNAs in disease. , 2014, Biochimica et biophysica acta.

[64]  Zhiyong Zhang,et al.  Ultrasensitive label-free detection of PNA-DNA hybridization by reduced graphene oxide field-effect transistor biosensor. , 2014, ACS nano.

[65]  Shana O Kelley,et al.  An electrochemical clamp assay for direct, rapid analysis of circulating nucleic acids in serum. , 2015, Nature chemistry.

[66]  Ryan C Bailey,et al.  Emerging Biosensing Approaches for microRNA Analysis. , 2016, Analytical chemistry.

[67]  D. Reinhoudt,et al.  Patterning of peptide nucleic acids using reactive microcontact printing. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[68]  Q. Nguyen,et al.  Molecular imaging for cancer diagnosis and surgery. , 2014, Advanced drug delivery reviews.

[69]  Adisorn Tuantranont,et al.  Electrochemical paper-based peptide nucleic acid biosensor for detecting human papillomavirus. , 2017, Analytica chimica acta.

[70]  Longhua Guo,et al.  Metal-organic framework (MOF): a novel sensing platform for biomolecules. , 2013, Chemical communications.

[71]  C. Croce,et al.  Targeting microRNAs in cancer: rationale, strategies and challenges , 2010, Nature Reviews Drug Discovery.

[72]  A. Manicardi,et al.  Building on the peptide nucleic acid (PNA) scaffold: a biomolecular engineering approach , 2017 .

[73]  Xiaoyuan Chen,et al.  Gold Nanoparticles for In Vitro Diagnostics. , 2015, Chemical reviews.

[74]  Mehmet Toner,et al.  Advancing the speed, sensitivity and accuracy of biomolecular detection using multi-length-scale engineering. , 2014, Nature nanotechnology.

[75]  Ajay Agarwal,et al.  Label-free and highly sensitive biomolecular detection using SERS and electrokinetic preconcentration. , 2009, Lab on a chip.

[76]  K. Pantel,et al.  Real-time liquid biopsy in cancer patients: fact or fiction? , 2013, Cancer research.

[77]  M. Moreno,et al.  Applications of peptide nucleic acids (PNAs) and locked nucleic acids (LNAs) in biosensor development , 2012, Analytical and Bioanalytical Chemistry.

[78]  J. Mattick,et al.  Structure and function of long noncoding RNAs in epigenetic regulation , 2013, Nature Structural &Molecular Biology.

[79]  Zhiqiang Gao,et al.  A highly sensitive microRNA biosensor based on hybridized microRNA-guided deposition of polyaniline. , 2014, Biosensors & bioelectronics.

[80]  S. Awasthi,et al.  Versatility of peptide nucleic acids (PNAs): role in chemical biology, drug discovery, and origins of life , 2017, Chemical biology & drug design.

[81]  Ç. Gerçel-Taylor,et al.  Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments , 2011, Seminars in Immunopathology.

[82]  Roberto Corradini,et al.  Detection of Non-Amplified Genomic DNA , 2012 .

[83]  M. Egholm,et al.  An introduction to peptide nucleic acid. , 1999, Current issues in molecular biology.

[84]  Jin-Wu Nam,et al.  Incredible RNA: Dual Functions of Coding and Noncoding , 2016, Molecules and cells.

[85]  X. Su,et al.  SPR study of DNA hybridization with DNA and PNA probes under stringent conditions. , 2009, Biosensors & bioelectronics.

[86]  T. Mok,et al.  Single-Molecule Detection of Epidermal Growth Factor Receptor Mutations in Plasma by Microfluidics Digital PCR in Non–Small Cell Lung Cancer Patients , 2009, Clinical Cancer Research.

[87]  G. Spoto,et al.  Artificial DNA and surface plasmon resonance , 2012, Artificial DNA, PNA & XNA.

[88]  J. Homola.  Surface plasmon resonance sensors for detection of chemical and biological species. , 2008, Chemical reviews.

[89]  Giuseppe Spoto,et al.  Functionalized gold nanoparticles for ultrasensitive DNA detection , 2012, Analytical and Bioanalytical Chemistry.

[90]  Peter E. Nielsen.  Peptide Nucleic Acids (PNA) in Chemical Biology and Drug Discovery , 2010, Chemistry & biodiversity.

[91]  Roberto Corradini,et al.  Ultrasensitive Detection of DNA by PNA and Nanoparticle‐Enhanced Surface Plasmon Resonance Imaging , 2008, Chembiochem : a European journal of chemical biology.

[92]  Y. Zhao,et al.  Rapid microRNA (miRNA) detection and classification via surface-enhanced Raman spectroscopy (SERS). , 2008, Biosensors & bioelectronics.

[93]  R. Gambari,et al.  Direct detection of point mutations in nonamplified human genomic DNA. , 2011, Analytical chemistry.

[94]  M. Pagliai,et al.  SERS and Computational studies on microRNA chains adsorbed on silver surfaces , 2010 .

[95]  Jianzhong Xi,et al.  Real-time polymerase chain reaction microRNA detection based on enzymatic stem-loop probes ligation. , 2009, Analytical chemistry.

[96]  K. Hanazawa,et al.  Detecting KRAS mutations in peripheral blood of colorectal cancer patients by peptide nucleic acid clamp PCR , 2012, Experimental and therapeutic medicine.

[97]  Jing Kong,et al.  Electrophoretic and field-effect graphene for all-electrical DNA array technology , 2014, Nature Communications.

[98]  A. Bardelli,et al.  Integrating liquid biopsies into the management of cancer , 2017, Nature Reviews Clinical Oncology.

[99]  Manuel Mayr,et al.  MicroRNAs in vascular and metabolic disease. , 2012, Circulation research.

[100]  B. Liedberg,et al.  Polythiophene derivative on quartz resonators for miRNA capture and assay. , 2015, The Analyst.

[101]  Yongqiang Cheng,et al.  Ultrasensitive detection of microRNAs by exponential isothermal amplification. , 2010, Angewandte Chemie.

[102]  Bert Vogelstein,et al.  DETECTION OF CIRCULATING TUMOR DNA IN EARLY AND LATE STAGE HUMAN MALIGNANCIES , 2014 .

[103]  S. Kelley.  Advancing Ultrasensitive Molecular and Cellular Analysis Methods to Speed and Simplify the Diagnosis of Disease. , 2017, Accounts of chemical research.

[104]  Wentao Xu,et al.  Specific and relative detection of urinary microRNA signatures in bladder cancer for point-of-care diagnostics. , 2017, Chemical communications.

[105]  Kathryn A. O’Donnell,et al.  c-Myc-regulated microRNAs modulate E2F1 expression , 2005, Nature.

[106]  M. Ferrari.  Cancer nanotechnology: opportunities and challenges , 2005, Nature Reviews Cancer.

[107]  Ł. Górski,et al.  Application of nucleic acid analogues as receptor layers for biosensors , 2016 .

[108]  R. Gambari,et al.  miRNA therapeutics: delivery and biological activity of peptide nucleic acids targeting miRNAs. , 2011, Epigenomics.

[109]  H. Horvitz,et al.  MicroRNA expression profiles classify human cancers , 2005, Nature.

[110]  G. Spoto,et al.  Biosensors for liquid biopsy: circulating nucleic acids to diagnose and treat cancer , 2016, Analytical and Bioanalytical Chemistry.

[111]  Franck Molina,et al.  Clinical validation of the detection of KRAS and BRAF mutations from circulating tumor DNA , 2014, Nature Medicine.

[112]  Maria Chiara Giuffrida,et al.  Integration of isothermal amplification methods in microfluidic devices: Recent advances. , 2017, Biosensors & bioelectronics.

[113]  George M Yousef,et al.  Personalized Medicine: Marking a New Epoch in Cancer Patient Management , 2010, Molecular Cancer Research.

[114]  M. Doble,et al.  Nanomaterials for early detection of cancer biomarker with special emphasis on gold nanoparticles in immunoassays/sensors. , 2015, Biosensors & bioelectronics.

[115]  H. Ju,et al.  A peptide nucleic acid-functionalized carbon nitride nanosheet as a probe for in situ monitoring of intracellular microRNA. , 2015, The Analyst.

[116]  Yang Li,et al.  An oligonucleotide microarray for microRNA expression analysis based on labeling RNA with quantum dot and nanogold probe , 2005, Nucleic acids research.

[117]  R. Turner,et al.  Peptide nucleic acid clamp PCR: A novel K‐ras mutation detection assay for colorectal cancer micrometastases in lymph nodes , 2004, International journal of cancer.

[118]  Roberto Gambari,et al.  Isothermal circular-strand-displacement polymerization of DNA and microRNA in digital microfluidic devices , 2015, Analytical and Bioanalytical Chemistry.

[119]  P. Nielsen,et al.  Pyrrolidine PNA: a novel conformationally restricted PNA analogue. , 2000, Organic letters.

[120]  R. Juliano,et al.  The delivery of therapeutic oligonucleotides , 2016, Nucleic acids research.

[121]  Kyung-A Hyun,et al.  Isolation and enrichment of circulating biomarkers for cancer screening, detection, and diagnostics. , 2016, The Analyst.

[122]  N. Rosenfeld,et al.  Noninvasive Identification and Monitoring of Cancer Mutations by Targeted Deep Sequencing of Plasma DNA , 2012, Science Translational Medicine.

[123]  Vladimir Benes,et al.  A sensitive array for microRNA expression profiling (miChip) based on locked nucleic acids (LNA). , 2006, RNA.

[124]  Nianqiang Wu,et al.  Plasmon-enhanced optical sensors: a review. , 2015, The Analyst.

[125]  Shana O Kelley,et al.  Beyond the Capture of Circulating Tumor Cells: Next-Generation Devices and Materials. , 2016, Angewandte Chemie.

[126]  E. Lianidou.  Circulating tumor cells--new challenges ahead. , 2012, Clinical chemistry.

[127]  B. Nordén,et al.  Thermodynamics of sequence-specific binding of PNA to DNA. , 2000, Biochemistry.

[128]  C. Lawrie,et al.  The circulating transcriptome as a source of non-invasive cancer biomarkers: concepts and controversies of non-coding and coding RNA in body fluids , 2015, Journal of cellular and molecular medicine.

[129]  Paola Guglielmelli,et al.  Effect of mutation order on myeloproliferative neoplasms. , 2015, The New England journal of medicine.

[130]  J. Hafner,et al.  Localized surface plasmon resonance sensors. , 2011, Chemical reviews.