Melittin-induced alterations in morphology and deformability of human red blood cells using quantitative phase imaging techniques

Here, the actions of melittin, the active molecule of apitoxin or bee venom, were investigated on human red blood cells (RBCs) using quantitative phase imaging techniques. High-resolution real-time 3-D refractive index (RI) measurements and dynamic 2-D phase images of individual melittin-bound RBCs enabled in-depth examination of melittin-induced biophysical alterations of the cells. From the measurements, morphological, intracellular, and mechanical alterations of the RBCs were analyzed quantitatively. Furthermore, leakage of haemoglobin (Hb) inside the RBCs at high melittin concentration was also investigated.

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

[2]  Gabriel Popescu,et al.  Measurement of red blood cell mechanics during morphological changes , 2010, Proceedings of the National Academy of Sciences.

[3]  B. Deuticke.  Transformation and restoration of biconcave shape of human erythrocytes induced by amphiphilic agents and changes of ionic environment. , 1968, Biochimica et biophysica acta.

[4]  Aqeel Ahmad,et al.  Cell-selective lysis by novel analogues of melittin against human red blood cells and Escherichia coli. , 2010, Biochemistry.

[5]  T. Souto-Padrón,et al.  Melittin peptide kills Trypanosoma cruzi parasites by inducing different cell death pathways. , 2013, Toxicon : official journal of the International Society on Toxinology.

[6]  Huey W. Huang,et al.  Process of inducing pores in membranes by melittin , 2013, Proceedings of the National Academy of Sciences.

[7]  D. Tosteson,et al.  Melittin lysis of red cells , 2005, The Journal of Membrane Biology.

[8]  A. Zilman,et al.  Cytoskeleton confinement and tension of red blood cell membranes. , 2003, Physical review letters.

[9]  Gabriel Popescu,et al.  Real Time Blood Testing Using Quantitative Phase Imaging , 2013, PloS one.

[10]  T. Katsu,et al.  Mechanism of membrane damage induced by the amphipathic peptides gramicidin S and melittin. , 1989, Biochimica et biophysica acta.

[11]  L. Grandison,et al.  Stimulation of anterior pituitary prolactin release by melittin, an activator of phospholipase A2. , 1984, Endocrinology.

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

[13]  M. Friebel,et al.  Model function to calculate the refractive index of native hemoglobin in the wavelength range of 250-1100 nm dependent on concentration. , 2006, Applied optics.

[14]  J. Gouaux,et al.  Structure of Staphylococcal α-Hemolysin, a Heptameric Transmembrane Pore , 1996, Science.

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

[16]  P. Sens,et al.  Force balance and membrane shedding at the red-blood-cell surface. , 2006, Physical review letters.

[17]  Felix Campelo,et al.  Crystal Structure of HIV-1 gp41 Including Both Fusion Peptide and Membrane Proximal External Regions , 2010, PLoS pathogens.

[18]  H. Erickson.  Size and Shape of Protein Molecules at the Nanometer Level Determined by Sedimentation, Gel Filtration, and Electron Microscopy , 2009, Biological Procedures Online.

[19]  Zelda R. Wasserman,et al.  Synthetic peptides as models for ion channel proteins , 1993 .

[20]  P. Canham.  The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. , 1970, Journal of theoretical biology.

[21]  Sang Yun Lee,et al.  The Effects of Ethanol on the Morphological and Biochemical Properties of Individual Human Red Blood Cells , 2015, PloS one.

[22]  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.

[23]  Gabriel Popescu,et al.  Optical imaging of cell mass and growth dynamics. , 2008, American journal of physiology. Cell physiology.

[24]  K. Wüthrich,et al.  High-resolution 1H-NMR studies of self-aggregation of melittin in aqueous solution. , 1980, Biochimica et biophysica acta.

[25]  R. Raison,et al.  Cell membrane changes induced by the cytolytic peptide, melittin, are detectable by 90° laser scatter , 1994 .

[26]  C. R. Dawson,et al.  The interaction of bee melittin with lipid bilayer membranes. , 1978, Biochimica et biophysica acta.

[27]  Oscar Murillo,et al.  Synthetic Organic Chemical Models for Transmembrane Channels , 1996 .

[28]  Melittin-induced membrane permeability: A nonosmotic mechanism of cell death , 2005, In Vitro Cellular & Developmental Biology - Animal.

[29]  M. Bessis,et al.  Present status of spiculed red cells and their relationship to the discocyte-echinocyte transformation: a critical review. , 1972, Blood.

[30]  L. Yang,et al.  Barrel-stave model or toroidal model? A case study on melittin pores. , 2001, Biophysical journal.

[31]  R. Barer.  Interference Microscopy and Mass Determination , 1952, Nature.

[32]  D. Tosteson,et al.  The sting. Melittin forms channels in lipid bilayers. , 1981, Biophysical journal.

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

[34]  D. Nicoli,et al.  Diffusion coefficients of hemoglobin by intensity fluctuation spectroscopy: effects of varying pH and ionic strength. , 1981, Biophysical journal.

[35]  Kyoohyun Kim,et al.  Three-dimensional label-free imaging and quantification of lipid droplets in live hepatocytes , 2016, Scientific Reports.

[36]  K. Wüthrich,et al.  Physicochemical studies of the protein-lipid interactions in melittin-containing micelles. , 1979, Biochimica et biophysica acta.

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

[38]  N. Mohandas,et al.  Osmotic gradient ektacytometry: comprehensive characterization of red cell volume and surface maintenance. , 1983, Blood.

[39]  Ji-Ho Park,et al.  Angle-resolved light scattering of individual rod-shaped bacteria based on Fourier transform light scattering , 2014, Scientific Reports.

[40]  Gabriel Popescu,et al.  Measurement of the nonlinear elasticity of red blood cell membranes. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  G. Gokel,et al.  Synthetic Organic Chemical Models for Transmembrane Channels , 1996 .

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

[43]  M. Lafleur,et al.  Study of vesicle leakage induced by melittin. , 1995, Biochimica et biophysica acta.

[44]  J. Avery.  Critical review. , 2006, The Journal of the Arkansas Medical Society.

[45]  M. J. Clague,et al.  Comparison of p25 presequence peptide and melittin. Red blood cell haemolysis and band 3 aggregation. , 1988, The Biochemical journal.

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

[47]  Jong Chul Ye,et al.  Real-time Visualization of 3-d Dynamic Microscopic Objects Using Optical Diffraction Tomography References and Links , 2022 .

[48]  J. Arbeit,et al.  Molecularly targeted nanocarriers deliver the cytolytic peptide melittin specifically to tumor cells in mice, reducing tumor growth. , 2009, The Journal of clinical investigation.

[49]  Kyoohyun Kim,et al.  High-Resolution 3-D Refractive Index Tomography and 2-D Synthetic Aperture Imaging of Live Phytoplankton , 2014 .

[50]  R M Hochmuth,et al.  Mechanical measurement of red cell membrane thickness. , 1983, Science.

[51]  Ulrich Koert,et al.  Synthetic ion channels. , 2004, Bioorganic & medicinal chemistry.

[52]  A. C. Burton,et al.  Distribution of Size and Shape in Populations of Normal Human Red Cells , 1968, Circulation research.

[53]  C. C. Condie,et al.  Conformational studies of aqueous melittin: thermodynamic parameters of the monomer-tetramer self-association reaction. , 1983, Biochemistry.

[54]  Barry R. Masters,et al.  Quantitative Phase Imaging of Cells and Tissues , 2012 .

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

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

[57]  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.

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

[59]  I. Campbell,et al.  The structure of melittin. A 1H-NMR study in methanol. , 1988, European journal of biochemistry.

[60]  Suliana Manley,et al.  Optical measurement of cell membrane tension. , 2006, Physical review letters.

[61]  YongKeun Park,et al.  Measuring cell surface area and deformability of individual human red blood cells over blood storage using quantitative phase imaging , 2016, Scientific Reports.

[62]  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.

[63]  Mary S. Gin,et al.  Signal-Triggered Transmembrane Ion Transport through Synthetic Channels , 2005 .

[64]  D. Hamar,et al.  Mechanisms of Echinocytosis Induced by Crotalus atrox Venom , 1997, Veterinary pathology.

[65]  R. B. Merrifield,et al.  Antibacterial and antimalarial properties of peptides that are cecropin‐melittin hybrids , 1989, FEBS letters.