High Sensitivity, High Selectivity SERS Detection of MnSOD Using Optical Nanoantennas Functionalized with Aptamers

In this paper, we present the development of a highly sensitive, specific and reproducible nanobiosensor to detect one specific liver cancer biomarker, the manganese super oxide dismutase (MnSOD). The high sensitivity and reproducibility was reached by using SERS on gold nanostructures (nanocylinders and coupled nanorods) produced by electron-beam lithography (EBL). The specificity of the detection was provided by the use of a specific aptamer with high affinity to the targeted protein as a recognition element. With such a sensor, we have been able to observe the SERS signal of the MnSOD at concentrations down to the nM level and to show with negative control that this detection is specific due to the use of the aptamer. This latter issue has allowed us to detect the MnSOD in different body fluids (serum and saliva) at concentrations in the nM range. We have then demonstrated the effectiveness of our SERS nanobiosensor using aptamer as a bioreceptor for the detection of disease biomarker at low concentrat...

[1]  D. McNaughton,et al.  Density functional theoretical (DFT) and surface-enhanced Raman spectroscopic study of guanine and its alkylated derivatives: Part 1. DFT calculations on neutral, protonated and deprotonated guanine , 2002 .

[2]  R. Lequin.  Enzyme immunoassay (EIA)/enzyme-linked immunosorbent assay (ELISA). , 2005, Clinical Chemistry.

[3]  Yiping Zhao,et al.  Novel nanostructures for SERS biosensing , 2008 .

[4]  D. S. St. Clair,et al.  Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. , 1995, Oncogene.

[5]  D. O'shea,et al.  Raman scattering and fluorescence in calcium fluoride , 1966 .

[6]  D. A. Stuart,et al.  In vivo glucose measurement by surface-enhanced Raman spectroscopy. , 2006, Analytical chemistry.

[7]  Z. Kim,et al.  Charge transfer enhancement in the SERS of a single molecule. , 2010, Nano letters.

[8]  Salil K. Das,et al.  Expression of Mn-Superoxide Dismutase Gene in Nontumorigenic and Tumorigenic Human Mammary Epithelial Cells , 2004, Journal of biomedicine & biotechnology.

[9]  N. Jang.  SERS Analysis of Self-Assembled Monolayers of DNA Strands on Gold Surfaces , 2010 .

[10]  R. Marks,et al.  A lower limit of detection for atrazine was obtained using bioluminescent reporter bacteria via a lower incubation temperature. , 2012, Ecotoxicology and environmental safety.

[11]  J. Greenberger,et al.  Radioprotection of lung and esophagus by overexpression of the human manganese superoxide dismutase transgene. , 2002, Military medicine.

[12]  Olga Lyandres,et al.  Rapid detection of an anthrax biomarker by surface-enhanced Raman spectroscopy. , 2005, Journal of the American Chemical Society.

[13]  Catalina David,et al.  Raman and IR spectroscopy of manganese superoxide dismutase, a pathology biomarker , 2012 .

[14]  K. McGlynn,et al.  A Comparison of Trends in the Incidence of Hepatocellular Carcinoma and Intrahepatic Cholangiocarcinoma in the United States , 2006, Cancer Epidemiology Biomarkers & Prevention.

[15]  Frances S. Ligler,et al.  Array biosensor for detection of toxins , 2003, Analytical and bioanalytical chemistry.

[16]  K. Suzuki,et al.  Serum-manganese-superoxide dismutase: normal values and increased levels in patients with acute myocardial infarction and several malignant diseases determined by an enzyme-linked immunosorbent assay using a monoclonal antibody. , 1990, Journal of immunological methods.

[17]  Andrea Toma,et al.  Breaking the diffusion limit with super-hydrophobic delivery of molecules to plasmonic nanofocusing SERS structures , 2011 .

[18]  R. Misselwitz,et al.  DNA structure at low pH values, in the presence of Mn2+ ions: a Raman study , 2005 .

[19]  Mauro Prasciolu,et al.  Attomole (amol) myoglobin Raman detection from plasmonic nanostructures , 2008 .

[20]  Lingwen Zeng,et al.  A lateral flow biosensor for rapid detection of DNA-binding protein c-jun. , 2011, Biosensors & bioelectronics.

[21]  M. Roukes,et al.  Comparative advantages of mechanical biosensors. , 2011, Nature nanotechnology.

[22]  R. V. Van Duyne,et al.  Toward a glucose biosensor based on surface-enhanced Raman scattering. , 2003, Journal of the American Chemical Society.

[23]  M. Mahmoud,et al.  Effect of silver nanowires on the surface-enhanced Raman spectra (SERS) of the RNA bases. , 2006, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[24]  Luke P. Lee,et al.  Aptamer-based SERRS sensor for thrombin detection. , 2008, Nano letters.

[25]  Nicolas Guillot,et al.  The electromagnetic effect in surface enhanced Raman scattering: Enhancement optimization using precisely controlled nanostructures , 2012 .

[26]  N. Halas,et al.  Surface-enhanced Raman spectroscopy of DNA. , 2008, Journal of the American Chemical Society.

[27]  W. Smith,et al.  Immunoassay for P38 MAPK using surface enhanced resonance Raman spectroscopy (SERRS). , 2008, The Analyst.

[28]  Clive G. Wilson,et al.  Surface-Enhanced Raman Scattering Spectroscopy as a Sensitive and Selective Technique for the Detection of Folic Acid in Water and Human Serum , 2008, Applied spectroscopy.

[29]  Kelsey R. Beavers,et al.  Limitations of surface enhanced Raman scattering in sensing DNA hybridization demonstrated by label-free DNA oligos as molecular rulers of distance-dependent enhancement. , 2013, Analytical chemistry.

[30]  Jeffrey N. Anker,et al.  Biosensing with plasmonic nanosensors. , 2008, Nature materials.

[31]  Honghui Shen,et al.  Optimized plasmonic nanostructures for improved sensing activities. , 2012, Optics express.

[32]  J. Duguid,et al.  Raman spectroscopy of DNA-metal complexes. I. Interactions and conformational effects of the divalent cations: Mg, Ca, Sr, Ba, Mn, Co, Ni, Cu, Pd, and Cd. , 1993, Biophysical journal.

[33]  Jeremy J. Baumberg,et al.  Understanding the Surface-Enhanced Raman Spectroscopy 'Background' , 2010 .

[34]  J. Homola.  Present and future of surface plasmon resonance biosensors , 2003, Analytical and bioanalytical chemistry.

[35]  D. Schadendorf,et al.  Serum manganese superoxide dismutase is a new tumour marker for malignant melanoma , 1995, Melanoma research.

[36]  L. Oberley,et al.  Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase , 1997, Oncogene.

[37]  Nak Han Jang,et al.  The Coordination Chemistry of DNA Nucleosides on Gold Nanoparticles as a Probe by SERS , 2002 .

[38]  H. Jeong,et al.  QCM DNA biosensor for the diagnosis of a fish pathogenic virus VHSV. , 2010, Talanta.

[39]  Catherine J. Murphy,et al.  Oligonucleotide Adsorption to Gold Nanoparticles: A Surface-Enhanced Raman Spectroscopy Study of Intrinsically Bent DNA , 2001 .

[40]  Pablo G. Etchegoin,et al.  Surface Enhanced Raman Scattering Enhancement Factors: A Comprehensive Study , 2007 .

[41]  A. Ido,et al.  Serum manganese superoxide dismutase and thioredoxin are potential prognostic markers for hepatitis C virus-related hepatocellular carcinoma. , 2011, World journal of gastroenterology.

[42]  Dor Ben-Amotz,et al.  Raman detection of proteomic analytes. , 2003, Analytical chemistry.

[43]  David Erickson,et al.  Aptamer based surface enhanced Raman scattering detection of vasopressin using multilayer nanotube arrays. , 2010, Biosensors & bioelectronics.

[44]  Lisa C Shriver-Lake,et al.  The Array Biosensor: Portable, Automated Systems , 2007, Analytical sciences : the international journal of the Japan Society for Analytical Chemistry.

[45]  W. Wilson,et al.  Inhibition of high-mobility-group A2 protein binding to DNA by netropsin: a biosensor-surface plasmon resonance assay. , 2008, Analytical biochemistry.

[46]  Mengsu Yang,et al.  Effects of small molecular inhibitors on the binding between HIV-1 reverse transcriptase and DNA as revealed by SPR biosensor , 2007 .

[47]  G. Schatz,et al.  Electromagnetic fields around silver nanoparticles and dimers. , 2004, The Journal of chemical physics.

[48]  Andrea Toma,et al.  Gold Dimer Nanoantenna with Slanted Gap for Tunable LSPR and Improved SERS , 2014 .

[49]  Nianqiang Wu,et al.  Detection of adenosine triphosphate with an aptamer biosensor based on surface-enhanced Raman scattering. , 2012, Analytical chemistry.

[50]  Evanthia Papadopoulou,et al.  Label-Free Detection of Single-Base Mismatches in DNA by Surface-Enhanced Raman Spectroscopy , 2011, Angewandte Chemie.

[51]  Anthony D. Keefe,et al.  Aptamers as therapeutics , 2010, Nature Reviews Drug Discovery.

[52]  M. Allegrini,et al.  Re-radiation enhancement in polarized surface-enhanced resonant Raman scattering of randomly oriented molecules on self-organized gold nanowires. , 2011, ACS nano.

[53]  Cristiano D'Andrea,et al.  Optical nanoantennas for multiband surface-enhanced infrared and Raman spectroscopy. , 2013, ACS nano.

[54]  M. Calleja,et al.  Biosensors based on nanomechanical systems. , 2013, Chemical Society reviews.

[55]  V. Pavlov,et al.  Label free and amplified detection of cancer marker EBNA-1 by DNA probe based biosensors. , 2011, Biosensors & bioelectronics.

[56]  Jan Greve,et al.  Surface-enhanced Raman spectroscopy of DNA bases , 1986 .

[57]  Yuze Sun,et al.  Sensitive optical biosensors for unlabeled targets: a review. , 2008, Analytica chimica acta.

[58]  S. Lane,et al.  Raman and surface‐enhanced Raman spectroscopic studies of the 15‐mer DNA thrombin‐binding aptamer , 2009 .

[59]  F. Buonaguro,et al.  The Functional Role of MnSOD as a Biomarker of Human Diseases and Therapeutic Potential of a New Isoform of a Human Recombinant MnSOD , 2014, BioMed research international.

[60]  George G. Guilbault,et al.  Commercial quartz crystal microbalances-Theory and applications , 1999 .

[61]  M. Porter,et al.  Femtomolar detection of prostate-specific antigen: an immunoassay based on surface-enhanced Raman scattering and immunogold labels. , 2003, Analytical chemistry.

[62]  Frances S Ligler,et al.  Perspective on optical biosensors and integrated sensor systems. , 2009, Analytical chemistry.

[63]  P. Meltzer,et al.  Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Hyungsoon Im,et al.  Recent progress in SERS biosensing. , 2011, Physical chemistry chemical physics : PCCP.

[65]  Eric C Le Ru,et al.  Single-molecule surface-enhanced Raman spectroscopy. , 2012, Annual review of physical chemistry.

[66]  N. Taniguchi,et al.  Reactivity of a monoclonal antibody to manganese superoxide dismutase with human ovarian carcinoma. , 1990, Cancer research.

[67]  Nicolas Guillot,et al.  Lithographied nanostructures as nanosensors , 2012 .

[68]  Emmanuel Rinnert,et al.  Surface enhanced Raman scattering optimization of gold nanocylinder arrays: Influence of the localized surface plasmon resonance and excitation wavelength , 2010 .

[69]  R. V. Van Duyne,et al.  Wavelength-scanned surface-enhanced Raman excitation spectroscopy. , 2005, The journal of physical chemistry. B.

[70]  Hiromi Okamoto,et al.  Properties of photoluminescence from single gold nanorods induced by near-field two-photon excitation , 2009 .

[71]  Yanying Rao,et al.  Fabrication of large-scale gold nanoplate films as highly active SERS substrates for label-free DNA detection. , 2013, Biosensors & bioelectronics.

[72]  Catalina David,et al.  SERS detection of biomolecules using lithographed nanoparticles towards a reproducible SERS biosensor , 2010, Nanotechnology.

[73]  P. Etchegoin,et al.  Proof of single-molecule sensitivity in surface enhanced Raman scattering (SERS) by means of a two-analyte technique. , 2006, The journal of physical chemistry. B.

[74]  Bruno Guelorget,et al.  New Gold Nanoparticles Adhesion Process Opening the Way of Improved and Highly Sensitive Plasmonics Technologies , 2013, Plasmonics.

[75]  Volker Deckert,et al.  Surface- and tip-enhanced Raman scattering of DNA components† , 2006 .

[76]  M. Mascini,et al.  Analytical applications of aptamers. , 2005, Biosensors & bioelectronics.

[77]  F. Ligler,et al.  Evanescent wave fluorescence biosensors. , 2005, Biosensors & bioelectronics.

[78]  Y. Ozaki,et al.  Surface-enhanced Raman scattering for protein detection , 2009, Analytical and bioanalytical chemistry.