The Quest for Optical Multiplexing in Bio-discoveries

Summary Optical multiplexing has significantly boosted our capacity to acquire and process information in the modern era. This review surveys new methods for coding optical information to move from the macroscopic to the nanoscale. We highlight that advances in new materials, fabrication methods, super-resolution imaging tools, and microfluidic devices are the enabling technologies for many recent breakthroughs in micro- and nanoscale biophotonics. Multidimensional optical coding has been developed to assign addressable molecular probes for multiplexed molecular and cellular sensing. While illustrating the principles of coding information in multiple dimensions, we discuss prospective opportunities in material design and technological advancement and identify the challenges for eventually integrating and translating these biophotonic tools into cellular insights.

[1]  Simone Lamon,et al.  Nanomaterials for optical data storage , 2016 .

[2]  Mark Bates,et al.  Short-range spectroscopic ruler based on a single-molecule optical switch. , 2005, Physical review letters.

[3]  Y. Li,et al.  Efficient incorporation of quantum dots into porous microspheres through a solvent-evaporation approach. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[4]  S. Hell,et al.  Simultaneous multi-lifetime multi-color STED imaging for colocalization analyses. , 2011, Optics express.

[5]  Ji-Xin Cheng,et al.  Far-field Imaging of Non-fluorescent Species with Sub-diffraction Resolution , 2013, Nature Photonics.

[6]  Bradley E. Bernstein,et al.  High-Throughput Single-Cell Labeling (Hi-SCL) for RNA-Seq Using Drop-Based Microfluidics , 2015, PloS one.

[7]  Dan Luo,et al.  Multiplexed detection of pathogen DNA with DNA-based fluorescence nanobarcodes , 2005, Nature Biotechnology.

[8]  R. Yuan,et al.  Multicolor-Encoded Reconfigurable DNA Nanostructures Enable Multiplexed Sensing of Intracellular MicroRNAs in Living Cells. , 2016, ACS Applied Materials and Interfaces.

[9]  M. A. Stott,et al.  Optofluidic wavelength division multiplexing for single-virus detection , 2015, Proceedings of the National Academy of Sciences.

[10]  Robert C. Leif,et al.  On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays , 2014, Nature Communications.

[11]  J. V. Moran,et al.  Initial sequencing and analysis of the human genome. , 2001, Nature.

[12]  D. Zhao,et al.  Rare-earth upconverting nanobarcodes for multiplexed biological detection. , 2011, Small.

[13]  Peng Yin,et al.  DNA-barcoded labeling probes for highly multiplexed Exchange-PAINT imaging† †Electronic supplementary information (ESI) available. See DOI: 10.1039/c6sc05420j Click here for additional data file. , 2017, Chemical science.

[14]  Kevin Braeckmans,et al.  Encoding microcarriers: present and future technologies , 2002, Nature Reviews Drug Discovery.

[15]  Baoping Wang,et al.  Multifunctional photonic crystal barcodes from microfluidics , 2012 .

[16]  Vito Mennella,et al.  Super-Resolution Microscopy: From Single Molecules to Supramolecular Assemblies. , 2015, Trends in cell biology.

[17]  Dhananjay Dendukuri,et al.  Stop-flow lithography in a microfluidic device. , 2007, Lab on a chip.

[18]  D. Pe’er,et al.  Highly multiplexed profiling of single-cell effector functions reveals deep functional heterogeneity in response to pathogenic ligands , 2015, Proceedings of the National Academy of Sciences.

[19]  N. Perrimon,et al.  Droplet microfluidic technology for single-cell high-throughput screening , 2009, Proceedings of the National Academy of Sciences.

[20]  Angela S. Wochnik,et al.  Narrow-band red-emitting Sr[LiAl₃N₄]:Eu²⁺ as a next-generation LED-phosphor material. , 2014, Nature materials.

[21]  D. Losic,et al.  Nanoporous hard data: optical encoding of information within nanoporous anodic alumina photonic crystals. , 2016, Nanoscale.

[22]  Wesley R. Legant,et al.  Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution , 2014, Science.

[23]  Rafael Yuste,et al.  Super-multiplex vibrational imaging , 2017, Nature.

[24]  A. Egner,et al.  Two-color far-field fluorescence nanoscopy based on photoswitchable emitters , 2007 .

[25]  Patrick S Doyle,et al.  Universal process-inert encoding architecture for polymer microparticles. , 2014, Nature materials.

[26]  Kevin Braeckmans,et al.  Encoding microcarriers by spatial selective photobleaching , 2003, Nature materials.

[27]  Long Cai,et al.  Single cell systems biology by super-resolution imaging and combinatorial labeling , 2012, Nature Methods.

[28]  John P Nolan,et al.  Suspension array technology: evolution of the flat-array paradigm. , 2002, Trends in biotechnology.

[29]  Shawn M. Douglas,et al.  Self-assembly of DNA into nanoscale three-dimensional shapes , 2009, Nature.

[30]  Darryn Bryant,et al.  Toward larger chemical libraries: Encoding with fluorescent colloids in combinatorial chemistry , 2000 .

[31]  Soong Ho Um,et al.  Dendrimer-like DNA-based fluorescence nanobarcodes , 2006, Nature Protocols.

[32]  Gwendolyn A. Lawrie,et al.  Optical encoding of microbeads for gene screening: alternatives to microarrays , 2001 .

[33]  Hao Zhang,et al.  Controlled fabrication of fluorescent barcode nanorods. , 2010, ACS nano.

[34]  D. Weitz,et al.  Fabrication of tunable spherical colloidal crystals immobilized in soft hydrogels. , 2010, Small.

[35]  Seung-Man Yang,et al.  Microfluidic multicolor encoding of microspheres with nanoscopic surface complexity for multiplex immunoassays. , 2011, Angewandte Chemie.

[36]  H. Stone,et al.  Formation of dispersions using “flow focusing” in microchannels , 2003 .

[37]  Bing Yan,et al.  SERS tags: novel optical nanoprobes for bioanalysis. , 2013, Chemical reviews.

[38]  Zhongze Gu,et al.  Microfluidic generation of magnetoresponsive Janus photonic crystal particles. , 2013, Nanoscale.

[39]  Michael J Sailor,et al.  Biomolecular screening with encoded porous-silicon photonic crystals , 2002, Nature Materials.

[40]  Dylan T Burnette,et al.  Bleaching/blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules , 2011, Proceedings of the National Academy of Sciences.

[41]  Johannes B. Woehrstein,et al.  Multiplexed 3D Cellular Super-Resolution Imaging with DNA-PAINT and Exchange-PAINT , 2014, Nature Methods.

[42]  A. Gad,et al.  Multicolor fluorescence nanoscopy by photobleaching: concept, verification, and its application to resolve selective storage of proteins in platelets. , 2014, ACS nano.

[43]  Igor Nabiev,et al.  Functionalized nanocrystal-tagged fluorescent polymer beads: synthesis, physicochemical characterization, and immunolabeling application. , 2004, Analytical biochemistry.

[44]  Hywel Morgan,et al.  Microparticle encoding technologies for high-throughput multiplexed suspension assays , 2009, Integrative biology : quantitative biosciences from nano to macro.

[45]  L. Shui,et al.  Multiplexed optical coding nanobeads and their application in single-molecule counting analysis for multiple gene expression analysis. , 2015, Analytica chimica acta.

[46]  David M. Rissin,et al.  Single-Molecule enzyme-linked immunosorbent assay detects serum proteins at subfemtomolar concentrations , 2010, Nature Biotechnology.

[47]  A. Diaspro,et al.  Live-cell 3D super-resolution imaging in thick biological samples , 2011, Nature Methods.

[48]  Peter G. Schultz,et al.  Identification of small-molecule inducers of pancreatic β-cell expansion , 2009, Proceedings of the National Academy of Sciences.

[49]  Wei Huang,et al.  Temporal full-colour tuning through non-steady-state upconversion. , 2015, Nature nanotechnology.

[50]  Didier Gigmes,et al.  Chemoselective Synthesis of Uniform Sequence-Coded Polyurethanes and Their Use as Molecular Tags , 2016 .

[51]  Bai Yang,et al.  Highly photoluminescent carbon dots for multicolor patterning, sensors, and bioimaging. , 2013, Angewandte Chemie.

[52]  Dhananjay Dendukuri,et al.  Synthesis and self-assembly of amphiphilic polymeric microparticles. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[53]  Alf Honigmann,et al.  Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution. , 2013, Biophysical journal.

[54]  R. G. Freeman,et al.  Submicrometer metallic barcodes. , 2001, Science.

[55]  M. Gerstein,et al.  RNA-Seq: a revolutionary tool for transcriptomics , 2009, Nature Reviews Genetics.

[56]  Mark Bates,et al.  Multicolor Super-Resolution Imaging with Photo-Switchable Fluorescent Probes , 2007, Science.

[57]  David R. Liu,et al.  Sequence-Controlled Polymers , 2013, Science.

[58]  Peng Yin,et al.  Submicrometre geometrically encoded fluorescent barcodes self-assembled from DNA. , 2012, Nature chemistry.

[59]  R. Hochstrasser,et al.  Wide-field subdiffraction imaging by accumulated binding of diffusing probes , 2006, Proceedings of the National Academy of Sciences.

[60]  X. Zhuang,et al.  Spatially resolved, highly multiplexed RNA profiling in single cells , 2015, Science.

[61]  Y. K. Kim,et al.  Synthesis, microstructure, and physical properties of metallic barcode nanowires , 2017, Metals and Materials International.

[62]  P. Rothemund.  Folding DNA to create nanoscale shapes and patterns , 2006, Nature.

[63]  David G Spiller,et al.  Encoded microcarriers for high-throughput multiplexed detection. , 2006, Angewandte Chemie.

[64]  Ho Cheung Shum,et al.  Microfluidic generation of multifunctional quantum dot barcode particles. , 2011, Journal of the American Chemical Society.

[65]  E. Peterman,et al.  Fluorescence and absorption spectroscopy of the weakly fluorescent chlorophyll a in cytochrome b6f of Synechocystis PCC6803. , 1998, Biophysical journal.

[66]  R J Fulton,et al.  Advanced multiplexed analysis with the FlowMetrix system. , 1997, Clinical chemistry.

[67]  Howon Lee,et al.  Colour-barcoded magnetic microparticles for multiplexed bioassays. , 2010, Nature materials.

[68]  V. T. Liveri,et al.  Controlled Synthesis of Nanoparticles in Microheterogeneous Systems , 2006 .

[69]  Mehmet Toner,et al.  Multifunctional Encoded Particles for High-Throughput Biomolecule Analysis , 2007, Science.

[70]  A. Griffiths,et al.  High-resolution dose–response screening using droplet-based microfluidics , 2011, Proceedings of the National Academy of Sciences of the United States of America.

[71]  S. Hell,et al.  Two-color far-field fluorescence nanoscopy. , 2007, Biophysical journal.

[72]  H. Ågren,et al.  Phase angle encoded upconversion luminescent nanocrystals for multiplexing applications. , 2017, Nanoscale.

[73]  A. Wu,et al.  Red, green, and blue luminescence by carbon dots: full-color emission tuning and multicolor cellular imaging. , 2015, Angewandte Chemie.

[74]  Wook Park,et al.  Three-dimensional fabrication of heterogeneous microstructures using soft membrane deformation and optofluidic maskless lithography. , 2009, Lab on a chip.

[75]  S. Achilefu,et al.  Fluorescence lifetime measurements and biological imaging. , 2010, Chemical reviews.

[76]  George C Schatz,et al.  Silver-based nanodisk codes. , 2010, ACS nano.

[77]  D. Vignali.  Multiplexed particle-based flow cytometric assays. , 2000, Journal of immunological methods.

[78]  T. Nisisako,et al.  High-volume production of single and compound emulsions in a microfluidic parallelization arrangement coupled with coaxial annular world-to-chip interfaces. , 2012, Lab on a chip.

[79]  Linan Song,et al.  Multiplexed single molecule immunoassays. , 2013, Lab on a chip.

[80]  S. Nie,et al.  Quantum-dot-tagged microbeads for multiplexed optical coding of biomolecules , 2001, Nature Biotechnology.

[81]  Mark Bates,et al.  Multicolor Super-Resolution Fluorescence Imaging via Multi-Parameter Fluorophore Detection , 2011, Chemphyschem : a European journal of chemical physics and physical chemistry.

[82]  Shuming Nie,et al.  Multicolor quantum dots for molecular diagnostics of cancer , 2006, Expert review of molecular diagnostics.

[83]  S. Nie,et al.  Quantum dot bioconjugates for ultrasensitive nonisotopic detection. , 1998, Science.

[84]  Meghana Kulkarni.  Digital multiplexed gene expression analysis using the NanoString nCounter system. , 2011, Current protocols in molecular biology.

[85]  F. Jiang,et al.  Manipulating energy transfer in lanthanide-doped single nanoparticles for highly enhanced upconverting luminescence† †Electronic supplementary information (ESI) available: Supplementary experimental details, Fig. S1–22 and Table S1. See DOI: 10.1039/c7sc01393k , 2017, Chemical science.

[86]  Dayong Jin,et al.  Multicolor barcoding in a single upconversion crystal. , 2014, Journal of the American Chemical Society.

[87]  S. Nie,et al.  Luminescent quantum dots for multiplexed biological detection and imaging. , 2002, Current opinion in biotechnology.

[88]  Dhananjay Dendukuri,et al.  Continuous-flow lithography for high-throughput microparticle synthesis , 2006, Nature materials.

[89]  D. Ingber,et al.  Microfluidic organs-on-chips , 2014, Nature Biotechnology.

[90]  A. Vaziri,et al.  Entanglement of the orbital angular momentum states of photons , 2001, Nature.

[91]  J. Paul Robinson,et al.  Tunable lifetime multiplexing using luminescent nanocrystals , 2013, Nature Photonics.

[92]  Baoping Wang,et al.  Bioinspired multifunctional Janus particles for droplet manipulation. , 2013, Journal of the American Chemical Society.

[93]  Hans H Gorris,et al.  Photon-upconverting nanoparticles for optical encoding and multiplexing of cells, biomolecules, and microspheres. , 2013, Angewandte Chemie.

[94]  Xiaohu Gao,et al.  Quantum dot nanobarcodes: epitaxial assembly of nanoparticle-polymer complexes in homogeneous solution. , 2008, Journal of the American Chemical Society.

[95]  Matt Trau,et al.  Novel Colloidal Materials for High‐Throughput Screening Applications in Drug Discovery and Genomics , 2001 .

[96]  Kang Sun,et al.  Suspension arrays based on nanoparticle-encoded microspheres for high-throughput multiplexed detection. , 2015, Chemical Society reviews.

[97]  Michael W. Davidson,et al.  Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes , 2007, Proceedings of the National Academy of Sciences.

[98]  Jie Wang,et al.  Microfluidic synthesis of barcode particles for multiplex assays. , 2015, Small.

[99]  Xiaoqun Gong,et al.  Self-healing encapsulation strategy for preparing highly stable, functionalized quantum-dot barcodes. , 2014, ACS applied materials & interfaces.

[100]  A. Willner,et al.  Terabit-Scale Orbital Angular Momentum Mode Division Multiplexing in Fibers , 2013, Science.

[101]  D. Shen,et al.  Full‐Color Inorganic Carbon Dot Phosphors for White‐Light‐Emitting Diodes , 2017 .

[102]  Patrick S Doyle,et al.  Bar-coded hydrogel microparticles for protein detection: synthesis, assay and scanning , 2011, Nature Protocols.

[103]  Hicham Fenniri,et al.  Nanomaterial-based barcodes. , 2015, Nanoscale.

[104]  Y. Lo,et al.  Lab-on-a-chip flow cytometer employing color-space-time coding. , 2010, Applied physics letters.

[105]  Kai Huang,et al.  Engineering of Lanthanide-Doped Upconversion Nanoparticles for Optical Encoding. , 2016, Small.

[106]  S. Quake,et al.  Dynamic pattern formation in a vesicle-generating microfluidic device. , 2001, Physical review letters.

[107]  Jennifer L. Osborn,et al.  Direct multiplexed measurement of gene expression with color-coded probe pairs , 2008, Nature Biotechnology.

[108]  Fan Zhang,et al.  Single-band upconversion nanoprobes for multiplexed simultaneous in situ molecular mapping of cancer biomarkers , 2015, Nature Communications.

[109]  David R. Smith,et al.  Composite Plasmon Resonant Nanowires , 2002 .

[110]  F. Simmel,et al.  Single-molecule kinetics and super-resolution microscopy by fluorescence imaging of transient binding on DNA origami. , 2010, Nano letters.