Combining Three-Dimensional Quantitative Phase Imaging and Fluorescence Microscopy for the Study of Cell Pathophysiology

Quantitative phase imaging (QPI) has emerged as one of the powerful imaging tools for the study of live cells in a non-invasive manner. In particular, multimodal approaches combining QPI and fluorescence microscopic techniques have been recently developed for superior spatiotemporal resolution as well as high molecular specificity. In this review, we briefly summarize recent advances in three-dimensional QPI combined with fluorescence techniques for the correlative study of cell pathophysiology. Through this review, biologists and clinicians can be provided with insights on this rapidly growing field of research and may find broader applications to investigate unrevealed nature in cell physiology and related diseases.

[1]  J. Rodrigo,et al.  Partially coherent optical diffraction tomography for label-free quantitative microscopy , 2017, 2017 16th Workshop on Information Optics (WIO).

[2]  Zhuo Wang,et al.  Measuring the scattering parameters of tissues from quantitative phase imaging of thin slices. , 2011, Optics letters.

[3]  Tan H. Nguyen,et al.  Gradient light interference microscopy for 3D imaging of unlabeled specimens , 2017, Nature Communications.

[4]  YongKeun Park,et al.  Super-resolution three-dimensional fluorescence and optical diffraction tomography of live cells using structured illumination generated by a digital micromirror device , 2018, Scientific Reports.

[5]  C. Fang-Yen,et al.  Optical diffraction tomography for high resolution live cell imaging. , 2009, Optics express.

[6]  Im,et al.  Correlative three-dimensional fluorescence and refractive index tomography : bridging the gap between molecular specificity and quantitative bioimaging , 2017 .

[7]  Yongkeun Park,et al.  Three-dimensional refractive index distributions of individual angiosperm pollen grains , 2018, bioRxiv.

[8]  Victoria J Allan,et al.  Light Microscopy Techniques for Live Cell Imaging , 2003, Science.

[9]  Gert von Bally,et al.  Contrast-enhanced digital holographic imaging of cellular structures by manipulating the intracellular refractive index. , 2010, Journal of biomedical optics.

[10]  R. Barer,et al.  Refractometry of Living Cells , 1952, Nature.

[11]  Subra Suresh,et al.  Biophysics of Malarial Parasite Exit from Infected Erythrocytes , 2011, PloS one.

[12]  Joseph M. Martel,et al.  Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel. , 2014, Physical review applied.

[13]  Natan T. Shaked,et al.  Wide-field interferometric phase microscopy with molecular specificity using plasmonic nanoparticles , 2013, Journal of biomedical optics.

[14]  Daniel Carl,et al.  Investigation of living pancreas tumor cells by digital holographic microscopy. , 2006, Journal of biomedical optics.

[15]  Kyoohyun Kim,et al.  Label-free high-resolution 3-D imaging of gold nanoparticles inside live cells using optical diffraction tomography , 2016, bioRxiv.

[16]  YongKeun Park,et al.  High-resolution three-dimensional imaging of red blood cells parasitized by Plasmodium falciparum and in situ hemozoin crystals using optical diffraction tomography , 2013, Journal of biomedical optics.

[17]  Joseph A Izatt,et al.  Structured illumination microscopy for dual-modality 3D sub-diffraction resolution fluorescence and refractive-index reconstruction. , 2017, Biomedical optics express.

[18]  Hayit Greenspan,et al.  Automated analysis of individual sperm cells using stain‐free interferometric phase microscopy and machine learning , 2017, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[19]  E. Wolf.  Three-dimensional structure determination of semi-transparent objects from holographic data , 1969 .

[20]  E. Cuche,et al.  Cell refractive index tomography by digital holographic microscopy. , 2006, Optics letters.

[21]  Bertrand Simon,et al.  High‐resolution tomographic diffractive microscopy of biological samples , 2010, Journal of biophotonics.

[22]  I. Dörr.  How Striga Parasitizes its Host: a TEM and SEM Study , 1997 .

[23]  Björn Kemper,et al.  Quantitative phase imaging for cell culture quality control , 2017, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[24]  YongKeun Park,et al.  Active illumination using a digital micromirror device for quantitative phase imaging. , 2015, Optics letters.

[25]  YongKeun Park,et al.  Hyperspectral optical diffraction tomography. , 2016, Optics express.

[26]  Michael S. Feld,et al.  Combined confocal Raman and quantitative phase microscopy system for biomedical diagnosis , 2011, Biomedical optics express.

[27]  V. Lauer.  New approach to optical diffraction tomography yielding a vector equation of diffraction tomography and a novel tomographic microscope , 2002, Journal of microscopy.

[28]  YongKeun Park,et al.  Measurements of three-dimensional refractive index tomography and membrane deformability of live erythrocytes from Pelophylax nigromaculatus , 2017, Scientific Reports.

[29]  Yongkeun Park,et al.  3D label-free imaging and analysis of Pinus pollen grains using optical diffraction tomography , 2017, bioRxiv.

[30]  N. Streibl.  Three-dimensional imaging by a microscope , 1985 .

[31]  Bahram Javidi,et al.  Recognition and classification of red blood cells using digital holographic microscopy and data clustering with discriminant analysis. , 2011, Journal of the Optical Society of America. A, Optics, image science, and vision.

[32]  P. Marquet,et al.  Marker-free phase nanoscopy , 2013, Nature Photonics.

[33]  Yongjin Sung,et al.  Stain-Free Quantification of Chromosomes in Live Cells Using Regularized Tomographic Phase Microscopy , 2012, PloS one.

[34]  K. Nugent,et al.  Refractive index measurement in viable cells using quantitative phase‐amplitude microscopy and confocal microscopy , 2005, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[35]  Myung K. Kim,et al.  Wavelength-scanning digital interference holography for tomographic three-dimensional imaging by use of the angular spectrum method. , 2005, Optics letters.

[36]  Kyoohyun Kim,et al.  Label-free characterization of white blood cells by measuring 3D refractive index maps. , 2015, Biomedical optics express.

[37]  Christian Depeursinge,et al.  Determination of Transmembrane Water Fluxes in Neurons Elicited by Glutamate Ionotropic Receptors and by the Cotransporters KCC2 and NKCC1: A Digital Holographic Microscopy Study , 2011, The Journal of Neuroscience.

[38]  YongKeun Park,et al.  Correlative three-dimensional fluorescence and refractive index tomography: bridging the gap between molecular specificity and quantitative bioimaging. , 2017, Biomedical optics express.

[39]  Gabriel Popescu,et al.  Diffraction phase and fluorescence microscopy. , 2006, Optics express.

[40]  Jeeyeon Lee,et al.  Mitochondria-targeting indolizino[3,2-c]quinolines as novel class of photosensitizers for photodynamic anticancer activity. , 2018, European journal of medicinal chemistry.

[41]  YongKeun Park,et al.  Optical characterization of red blood cells from individuals with sickle cell trait and disease in Tanzania using quantitative phase imaging , 2016, Scientific Reports.

[42]  R. Barer.  Determination of Dry Mass, Thickness, Solid and Water Concentration in Living Cells , 1953, Nature.

[43]  I. Yamaguchi,et al.  Image formation in phase-shifting digital holography and applications to microscopy. , 2001, Applied optics.

[44]  Steffi Ketelhut,et al.  Quantitative phase microscopy for evaluation of intestinal inflammation and wound healing utilizing label-free biophysical markers. , 2018, Histology and histopathology.

[45]  Kyoohyun Kim,et al.  Optical diffraction tomography techniques for the study of cell pathophysiology , 2016, 1603.00592.

[46]  YoungJu Jo,et al.  Quantitative Phase Imaging Techniques for the Study of Cell Pathophysiology: From Principles to Applications , 2013, Sensors.

[47]  Yongkeun Park,et al.  Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum , 2008, Proceedings of the National Academy of Sciences.

[48]  Jonghee Yoon,et al.  Optical diffraction tomography using a digital micromirror device for stable measurements of 4D refractive index tomography of cells , 2016, SPIE BiOS.

[49]  Jonghee Yoon,et al.  A Bacteria‐Based Remotely Tunable Photonic Device , 2017 .

[50]  E. Cuche,et al.  Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy. , 2005, Optics letters.

[51]  Gabriel Popescu,et al.  Quantitative Phase Imaging , 2012 .

[52]  Nicolas Pavillon,et al.  Noninvasive detection of macrophage activation with single-cell resolution through machine learning , 2018, Proceedings of the National Academy of Sciences.

[53]  Jochen Guck,et al.  Bacterial infection of macrophages induces decrease in refractive index , 2013, Journal of biophotonics.

[54]  Joseph A Izatt,et al.  Structured illumination multimodal 3D-resolved quantitative phase and fluorescence sub-diffraction microscopy. , 2017, Biomedical optics express.

[55]  Ji-Ho Park,et al.  Label-free high-resolution 3-D imaging of gold nanoparticles inside live cells using optical diffraction tomography , 2016, bioRxiv.

[56]  Gabriel Popescu,et al.  Solving inverse scattering problems in biological samples by quantitative phase imaging , 2016 .

[57]  Hyunjoo Park,et al.  Label-free identification of individual bacteria using Fourier transform light scattering. , 2015, Optics express.

[58]  Nir S. Gov,et al.  Metabolic remodeling of the human red blood cell membrane , 2010, Proceedings of the National Academy of Sciences.

[59]  Christian Depeursinge,et al.  Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy. , 2009, Journal of biomedical optics.

[60]  YongKeun Park,et al.  Real-time quantitative phase imaging with a spatial phase-shifting algorithm. , 2011, Optics letters.

[61]  Hongying Zhu,et al.  Optofluidic Tomography on a Chip. , 2011, Applied physics letters.

[62]  YongKeun Park,et al.  Label-free non-invasive quantitative measurement of lipid contents in individual microalgal cells using refractive index tomography , 2017, Scientific Reports.

[63]  Steffi Ketelhut,et al.  Influence of sample preparation and identification of subcelluar structures in quantitative holographic phase contrast microscopy , 2010, Photonics Europe.

[64]  S. D. Babacan,et al.  White-light diffraction tomography of unlabelled live cells , 2014, Nature Photonics.

[65]  H. Greenspan,et al.  Quantitative phase microscopy spatial signatures of cancer cells , 2017, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[66]  YongKeun Park,et al.  Refractive index tomograms and dynamic membrane fluctuations of red blood cells from patients with diabetes mellitus , 2016, Scientific Reports.

[67]  Gabriel Popescu,et al.  Live cell refractometry using Hilbert phase microscopy and confocal reflectance microscopy. , 2009, The journal of physical chemistry. A.

[68]  Jonghee Yoon,et al.  Holographic deep learning for rapid optical screening of anthrax spores , 2017, Science Advances.

[69]  W. Carter,et al.  Detection of Extracellular Forms of Babesia in the Blood by Electron Microscopy: A Diagnostic Method for Differentiation from Plasmodium falciparum , 2003, Ultrastructural pathology.

[70]  Björn Kemper,et al.  Tomographic phase microscopy of living three-dimensional cell cultures , 2014, Journal of biomedical optics.

[71]  Jong Chul Ye,et al.  Comparative study of iterative reconstruction algorithms for missing cone problems in optical diffraction tomography. , 2015, Optics express.

[72]  Thomas Neumann,et al.  Three-dimensional imaging of single isolated cell nuclei using optical projection tomography. , 2005, Optics express.

[73]  M. Iglarz,et al.  Selexipag Active Metabolite ACT-333679 Displays Strong Anticontractile and Antiremodeling Effects but Low β-Arrestin Recruitment and Desensitization Potential , 2017, The Journal of Pharmacology and Experimental Therapeutics.

[74]  R. Dasari,et al.  Diffraction phase microscopy for quantifying cell structure and dynamics. , 2006, Optics letters.

[75]  T. Horii,et al.  Molecular Camouflage of Plasmodium falciparum Merozoites by Binding of Host Vitronectin to P47 Fragment of SERA5 , 2018, Scientific Reports.

[76]  K. Nugent,et al.  Quantitative phase tomography , 2000 .

[77]  Valery V. Tuchin,et al.  Biophotonics: Photonic Solutions for Better Health Care II , 2008 .

[78]  Christian Depeursinge,et al.  Submicrometer tomography of cells by multiple-wavelength digital holographic microscopy in reflection. , 2009, Optics letters.

[79]  Mor Habaza,et al.  Tomographic phase microscopy with 180° rotation of live cells in suspension by holographic optical tweezers. , 2015, Optics letters.

[80]  YongKeun Park,et al.  Label-free optical quantification of structural alterations in Alzheimer’s disease , 2016, Scientific reports.

[81]  C. Fang-Yen,et al.  Tomographic phase microscopy , 2008, Nature Methods.

[82]  T. Lukes,et al.  Combined multi-plane phase retrieval and super-resolution optical fluctuation imaging for 4D cell microscopy , 2018 .

[83]  Sung-Hee Hong,et al.  Characterizations of individual mouse red blood cells parasitized by Babesia microti using 3-D holographic microscopy , 2015, Scientific Reports.

[84]  Tomasz Kozacki,et al.  Holographic tomography with scanning of illumination: space-domain reconstruction for spatially invariant accuracy. , 2016, Biomedical optics express.

[85]  P. So,et al.  Label-free characterization of ultra violet-radiation-induced changes in skin fibroblasts with Raman spectroscopy and quantitative phase microscopy , 2017, Scientific Reports.

[86]  Jaeduck Jang,et al.  Spectro-refractometry of individual microscopic objects using swept-source quantitative phase imaging. , 2013, Analytical chemistry.

[87]  Pasquale Memmolo,et al.  3D morphometry of red blood cells by digital holography , 2014, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[88]  YongKeun Park,et al.  Profiling individual human red blood cells using common-path diffraction optical tomography , 2014, Scientific Reports.

[89]  Youngchan Kim,et al.  Common-path diffraction optical tomography for investigation of three-dimensional structures and dynamics of biological cells. , 2014, Optics express.

[90]  Cornelia Denz,et al.  Three-dimensional exploration and mechano-biophysical analysis of the inner structure of living cells. , 2013, Small.

[91]  Jochen Guck,et al.  Three‐dimensional correlative single‐cell imaging utilizing fluorescence and refractive index tomography , 2017, Journal of biophotonics.