Real-Time In Situ Secondary Structure Analysis of Protein Monolayer with Mid-Infrared Plasmonic Nanoantennas

Dynamic detection of protein conformational changes at physiological conditions on a minute amount of samples is immensely important for understanding the structural determinants of protein function in health and disease and to develop assays and diagnostics for protein misfolding and protein aggregation diseases. Herein, we experimentally demonstrate the capabilities of a mid-infrared plasmonic biosensor for real-time and in situ protein secondary structure analysis in aqueous environment at nanoscale. We present label-free ultrasensitive dynamic monitoring of β-sheet to disordered conformational transitions in a monolayer of the disease-related α-synuclein protein under varying stimulus conditions. Our experiments show that the extracted secondary structure signals from plasmonically enhanced amide I signatures in the protein monolayer can be reliably and reproducibly acquired with second derivative analysis for dynamic monitoring. Furthermore, by using a polymer layer we show that our nanoplasmonic approach of extracting the frequency components of vibrational signatures matches with the results attained from gold-standard infrared transmission measurements. By facilitating conformational analysis on small quantities of immobilized proteins in response to external stimuli such as drugs, our plasmonic biosensor could be used to introduce platforms for screening small molecule modulators of protein misfolding and aggregation.

[1]  Ad Bax,et al.  Multiple tight phospholipid-binding modes of alpha-synuclein revealed by solution NMR spectroscopy. , 2009, Journal of molecular biology.

[2]  Valerio Pruneri,et al.  Mid-infrared plasmonic biosensing with graphene , 2015, Science.

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

[4]  Claudio Soto,et al.  Amyloids, prions and the inherent infectious nature of misfolded protein aggregates. , 2006, Trends in biochemical sciences.

[5]  J. Kong,et al.  Obtaining information about protein secondary structures in aqueous solution using Fourier transform IR spectroscopy , 2015, Nature Protocols.

[6]  Aydogan Ozcan,et al.  Unconventional methods of imaging: computational microscopy and compact implementations , 2016, Reports on progress in physics. Physical Society.

[7]  D. Naumann,et al.  Protein folding and misfolding : shining light by infrared spectroscopy , 2012 .

[8]  N. Greenfield Using circular dichroism spectra to estimate protein secondary structure , 2007, Nature Protocols.

[9]  J. Justin Gooding,et al.  Single Nanoparticle Plasmonic Sensors , 2015, Sensors.

[10]  Hatice Altug,et al.  Infrared Plasmonic Biosensor for Real-Time and Label-Free Monitoring of Lipid Membranes. , 2016, Nano letters.

[11]  J. Wiltfang,et al.  An infrared sensor analysing label‐free the secondary structure of the Abeta peptide in presence of complex fluids , 2016, Journal of biophotonics.

[12]  E. Masliah,et al.  The many faces of α-synuclein: from structure and toxicity to therapeutic target , 2012, Nature Reviews Neuroscience.

[13]  Annemarie Pucci,et al.  Resonant plasmonic and vibrational coupling in a tailored nanoantenna for infrared detection. , 2008, Physical review letters.

[14]  Cristina Tarin,et al.  Adaptive Method for Quantitative Estimation of Glucose and Fructose Concentrations in Aqueous Solutions Based on Infrared Nanoantenna Optics , 2019, Sensors.

[15]  Alp Artar,et al.  High-throughput nanofabrication of infrared plasmonic nanoantenna arrays for vibrational nanospectroscopy. , 2010, Nano letters.

[16]  P. Nordlander,et al.  Plasmons in strongly coupled metallic nanostructures. , 2011, Chemical reviews.

[17]  C. Dobson,et al.  Differential Phospholipid Binding of α-Synuclein Variants Implicated in Parkinson’s Disease Revealed by Solution NMR Spectroscopy† , 2009, Biochemistry.

[18]  Giovanni Dietler,et al.  Nanoplasmonic mid-infrared biosensor for in vitro protein secondary structure detection , 2017, Light: Science & Applications.

[19]  C. Dobson,et al.  The amyloid state and its association with protein misfolding diseases , 2014, Nature Reviews Molecular Cell Biology.

[20]  T. Taubner,et al.  Low-Cost Infrared Resonant Structures for Surface-Enhanced Infrared Absorption Spectroscopy in the Fingerprint Region from 3 to 13 μm , 2013 .

[21]  C. Kendall,et al.  Vibrational spectroscopy: a clinical tool for cancer diagnostics. , 2009, The Analyst.

[22]  Xiaoxia Yang,et al.  Far-field nanoscale infrared spectroscopy of vibrational fingerprints of molecules with graphene plasmons , 2016, Nature Communications.

[23]  Kai Chen,et al.  Tunable Nanoantennas for Surface Enhanced Infrared Absorption Spectroscopy by Colloidal Lithography and Post-Fabrication Etching , 2017, Scientific Reports.

[24]  J. Heberle,et al.  Thinner, smaller, faster: IR techniques to probe the functionality of biological and biomimetic systems. , 2010, Angewandte Chemie.

[25]  L. Lechuga,et al.  Recent advances in nanoplasmonic biosensors: applications and lab-on-a-chip integration , 2017 .

[26]  R. T. Hill,et al.  Plasmonic biosensors. , 2015, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[27]  R. Poppi,et al.  Determination of aqueous antibiotic solutions using SERS nanogratings. , 2017, Analytica chimica acta.

[28]  I. Amenabar,et al.  Nanoscale-resolved chemical identification of thin organic films using infrared near-field spectroscopy and standard Fourier transform infrared references , 2015 .

[29]  V. Uversky,et al.  Conformational behavior and aggregation of alpha-synuclein in organic solvents: modeling the effects of membranes. , 2003, Biochemistry.

[30]  Cyril Petibois,et al.  FT-IR spectral imaging of blood vessels reveals protein secondary structure deviations induced by tumor growth , 2008, Analytical and bioanalytical chemistry.

[31]  W. Caughey,et al.  Protein secondary structures in water from second-derivative amide I infrared spectra. , 1990, Biochemistry.

[32]  Bernhard Lendl,et al.  External cavity-quantum cascade laser infrared spectroscopy for secondary structure analysis of proteins at low concentrations , 2016, Scientific Reports.

[33]  David L. Kaplan,et al.  Ultra-sensitive vibrational spectroscopy of protein monolayers with plasmonic nanoantenna arrays , 2009, Proceedings of the National Academy of Sciences.

[34]  Harald Giessen,et al.  Surface-Enhanced Infrared Spectroscopy Using Resonant Nanoantennas. , 2017, Chemical reviews.

[35]  Chao Zhang,et al.  Nanogapped Au Antennas for Ultrasensitive Surface-Enhanced Infrared Absorption Spectroscopy. , 2017, Nano letters.

[36]  D. Naumann,et al.  Protein Folding and Misfolding , 2012 .

[37]  Wei Li,et al.  Dual-band moiré metasurface patches for multifunctional biomedical applications. , 2016, Nanoscale.

[38]  H. Ishida,et al.  Optical theory applied to infrared spectroscopy , 1994 .

[39]  Ronen Adato,et al.  In-situ ultra-sensitive infrared absorption spectroscopy of biomolecule interactions in real time with plasmonic nanoantennas , 2013, Nature Communications.

[40]  H. Altug,et al.  Quantifying the Limits of Detection of Surface-Enhanced Infrared Spectroscopy with Grating Order-Coupled Nanogap Antennas , 2018, ACS photonics.