Characterizations of individual mouse red blood cells parasitized by Babesia microti using 3-D holographic microscopy

Babesia microti causes “emergency” human babesiosis. However, little is known about the alterations in B. microti invaded red blood cells (Bm-RBCs) at the individual cell level. Through quantitative phase imaging techniques based on laser interferometry, we present the simultaneous measurements of structural, chemical, and mechanical modifications in individual mouse Bm-RBCs. 3-D refractive index maps of individual RBCs and in situ parasite vacuoles are imaged, from which total contents and concentration of dry mass are also precisely quantified. In addition, we examine the dynamic membrane fluctuation of Bm-RBCs, which provide information on cell membrane deformability.

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

[2]  P. So,et al.  Diffraction optical tomography using a quantitative phase imaging unit. , 2014, Optics letters.

[3]  S. Suresh,et al.  Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum , 2007, Proceedings of the National Academy of Sciences.

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

[5]  A. Spielman,et al.  Babesia microti Primarily Invades Mature Erythrocytes in Mice , 2006, Infection and Immunity.

[6]  H. G. Davies,et al.  Interference Microscopy and Mass Determination , 1952, Nature.

[7]  W. Trager,et al.  An electron microscopic study of Babesia microti invading erythrocytes , 1976, Cell and Tissue Research.

[8]  R. Pollack,et al.  Concurrent Lyme disease and babesiosis. Evidence for increased severity and duration of illness. , 1996, JAMA.

[9]  K. Kirk,et al.  Membrane transport in the malaria-infected erythrocyte , 2000 .

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

[11]  Mario Cesarelli,et al.  Comparison of two flow‐based imaging methods to measure individual red blood cell area and volume , 2012, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[12]  T Suzuki,et al.  Rheologic properties of senescent erythrocytes: loss of surface area and volume with red blood cell age. , 1992, Blood.

[13]  R. Barer,et al.  Refractive Index of Concentrated Protein Solutions , 1954, Nature.

[14]  K. Lewandrowski,et al.  Clinical Laboratory Medicine: Self-Assessment and Review , 1997 .

[15]  S. Telford,et al.  What is Babesia microti? , 2003, Parasitology.

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

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

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

[19]  Nicholas J White,et al.  Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. , 2004, Acta tropica.

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

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

[22]  F. Schuster.  Cultivation of Babesia and Babesia-Like Blood Parasites: Agents of an Emerging Zoonotic Disease , 2002, Clinical Microbiology Reviews.

[23]  Gabriel Popescu,et al.  Imaging red blood cell dynamics by quantitative phase microscopy. , 2008, Blood cells, molecules & diseases.

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

[25]  N. Kapel,et al.  In Vitro Evaluation of Drug Susceptibilities of Babesia divergens Isolates , 1998, Antimicrobial Agents and Chemotherapy.

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

[27]  Subra Suresh,et al.  Pf155/RESA protein influences the dynamic microcirculatory behavior of ring-stage Plasmodium falciparum infected red blood cells , 2012, Scientific Reports.

[28]  YongKeun Park,et al.  Quantitative phase imaging unit. , 2014, Optics letters.

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

[30]  S. Suresha,et al.  Mechanical response of human red blood cells in health and disease : Some structure-property-function relationships , 2006 .

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

[32]  J. Gray,et al.  Babesiosis: recent insights into an ancient disease. , 2008, International journal for parasitology.

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

[34]  R. Johnson,et al.  Shape and volume changes in erythrocyte ghosts and spectrin-actin networks , 1980, The Journal of cell biology.

[35]  CLINICAL MICROBIOLOGY REVIEWS , 2011, Clinical Microbiology Reviews.

[36]  R. Weed,et al.  Is hemoglobin an essential structural component of human erythrocyte membranes? , 1963, The Journal of clinical investigation.

[37]  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.

[38]  Bojana Gligorijevic,et al.  Spinning disk confocal microscopy of live, intraerythrocytic malarial parasites. 2. Altered vacuolar volume regulation in drug resistant malaria. , 2006, Biochemistry.

[39]  L. Kats,et al.  Recent insights into alteration of red blood cells by Babesia bovis: moovin' forward. , 2010, Trends in parasitology.

[40]  YongKeun Park,et al.  Spectroscopic phase microscopy for quantifying hemoglobin concentrations in intact red blood cells , 2009, BiOS.

[41]  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.

[42]  P. Conrad,et al.  Human babesiosis: an emerging tick-borne disease. , 2000, International journal for parasitology.

[43]  Miwa Takahashi,et al.  High susceptibility of Djungarian hamsters (Phodopus sungorus) to the infection with Babesia microti supported by hemodynamics. , 2005, The Journal of veterinary medical science.

[44]  D. Barto,et al.  Babesiosis , 2014 .

[45]  C. Lim,et al.  New insights into the altered adhesive and mechanical properties of red blood cells parasitized by Babesia bovis , 2007, Molecular microbiology.

[46]  S. Kahn,et al.  Red blood cell metabolism in AKR mice in the prelymphomatous phase. , 1976, Cancer research.

[47]  S J Singer,et al.  On the mechanism of ATP-induced shape changes in human erythrocyte membranes. I. The role of the spectrin complex , 1977, The Journal of cell biology.

[48]  F. Cox.  Human babesiosis , 1980, Nature.