Profiling individual human red blood cells using common-path diffraction optical tomography

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Kim, Youngchan ^a,c   Shim, Hyoeun ^b,d   Kim, Kyoohyun ^a   Park, HyunJoo ^a   Jang, Seongsoo ^b   Park, YongKeun ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d Seegene Medical Foundation   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CELL TRACKING; ERYTHROCYTE; HOLOGRAPHY; HUMAN; OPTICAL TOMOGRAPHY; SINGLE CELL ANALYSIS; ULTRASTRUCTURE;

CELL TRACKING; ERYTHROCYTES; HOLOGRAPHY; HUMANS; SINGLE-CELL ANALYSIS; TOMOGRAPHY, OPTICAL;

EID: 84922280878     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06659     Document Type: Article

References (72)

1. Suresh, S. Mechanical response of human red blood cells in health and disease: some structure-property-function relationships. J. Mater. Res 21, 1872 (2006).
2. Park, Y. et al. Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 105, 13730-13735 (2008).
3. Byun, H. S. et al. Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient. Acta Biomater 8, 4130-4138 (2012).
4. Mills, J. P. et al. Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 104, 9213-9217 (2007).
5. Kaushansky, K. Williams hematology, (McGraw-Hill Medical New York, 2010).
6. Weatherall, D. J. Systems biology and red cells. N. Engl. J. Med 364, 376-377 (2011).
7. Hochmuth, R. M. Micropipette aspiration of living cells. J Biomech 33, 15-22 (2000).
8. Sem'yanov, K. A., Tarasov, P. A., Soini, J. T., Petrov, A. K. & Maltsev, V. P. Calibration-free method to determine the size and hemoglobin concentration of individual red blood cells from light scattering. Appl. Opt. 39, 5884-5889 (2000).
9. Dao, M., Lim, C. & Suresh, S. Mechanics of the human red blood cell deformed by optical tweezers. J. Mech. Phys. Solid 51, 2259-2280 (2003).
10. Esposito, A. et al. FRET imaging of hemoglobin concentration in Plasmodium falciparum-infected red cells. PLoS One 3, e3780 (2008).
11. Rusciano, G. Experimental analysis of Hb oxy-deoxy transition in single optically stretched red blood cells. Phys. Medica 26, 233-239 (2010).
12. DeBlois, R. & Bean, C. Counting and sizing of submicron particles by the resistive pulse technique. Rev. Sci. Instrum. 41, 909-916 (1970).
13. Mohandas, N. et al. Accurate and independent measurement of volume and hemoglobin concentration of individual red cells by laser light scattering. Blood 68, 506-513 (1986).
14. Tomaiuolo, G., Rossi, D., Caserta, S., Cesarelli, M. & Guido, S. Comparison of two flow-based imaging methods to measure individual red blood cell area and volume. Cytometry. Part A: the journal of the International Society for Analytical Cytology 81, 1040-1047 (2012).
15. Waugh, R. E. et al. Rheologic Properties of Senescent Erythrocytes - Loss of Surface-Area and Volume with Red-Blood-Cell Age. Blood 79, 1351-1358 (1992).
16. Popescu, G. Quantitative Phase Imaging of Cells and Tissues, (McGraw-Hill Professional, 2011).
17. Lee, K. et al. Quantitative phase imaging techniques for the study of cell pathophysiology: from principles to applications. Sensors 13, 4170-4191 (2013).
18. Popescu, G. et al. Imaging red blood cell dynamics by quantitative phase microscopy. Blood Cells Mol. Dis. 41, 10-16 (2008).
19. Kim, K., and Kim, K. S., Park, H., Ye, J. C. & Park, Y. Real-time visualization of 3-D dynamic microscopic objects using optical diffraction tomography. Opt Express 21, 32269-32278 (2013).
20. Popescu, G. et al. Optical imaging of cell mass and growth dynamics. Am J Physiol Cell Physiol 295, C538-544 (2008).
21. Kemper, B. & von Bally, G. Digital holographic microscopy for live cell applications and technical inspection. Appl. Opt. 47, A52-A61 (2008).
22. Rappaz, B. et al. Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer. Cytometry. Part A: the journal of the International Society for Analytical Cytology 73, 895-903 (2008).
23. Park, Y. K. et al. Measurement of red blood cell mechanics during morphological changes. Proc. Natl. Acad. Sci. USA 107, 6731 (2010).
24. Popescu, G., and Park, Y. K., Dasari, R. R., Badizadegan, K. & Feld, M. S. Coherence properties of red blood cell membrane motions. Phys Rev E 76, 31902 (2007).
25. Rappaz, B. et al. Spatial analysis of erythrocyte membrane fluctuations by digital holographic microscopy. Blood Cells Mol. Dis. 42, 228-232 (2009).
26. Kim, Y. et al. Common-path diffraction optical tomography for investigation of three-dimensional structures and dynamics of biological cells. Opt Express 22, 10398-10407 (2014).
27. Debnath, S. K. & Park, Y. Real-time quantitative phase imaging with a spatial phase-shifting algorithm. Opt Lett 36, 4677-4679 (2011).
28. Popescu, G., Ikeda, T., Dasari, R. R. & Feld, M. S. Diffraction phase microscopy for quantifying cell structure and dynamics. Opt. Lett. 31, 775-777 (2006).
29. Park, Y., Popescu, G., Badizadegan, K., Dasari, R. R. & Feld, M. S. Diffraction phase and fluorescence microscopy. Opt Express 14, 8263-8268 (2006).
30. Kim, K. et al. High-resolution three-dimensional imaging of red blood cells parasitized by Plasmodium falciparum and in situ hemozoin crystals using optical diffraction tomography. J. Biomed. Opt. 19, 011005 (2013).
31. Wolf, E. Three-dimensional structure determination of semi-transparent objects from holographic data. Opt Commun 1, 4 (1969).
32. Pham, H. V., Bhaduri, B., Tangella, K., Best-Popescu, C. & Popescu, G. Real time blood testing using quantitative phase imaging. PLoS One 8, e55676 (2013).
33. Clark, M. R., Mohandas, N. & Shohet, S. B. Osmotic gradient ektacytometry: comprehensive characterization of red cell volume and surface maintenance. Blood 61, 899-910 (1983).
34. Canham, P. & Burton, A. C. Distribution of size and shape in populations of normal human red cells. Circ Res 22, 405-422 (1968).
35. Canham, P. B. The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. J. Therm. Biol. 26, 61-81 (1970).
36. Yip, R. et al. Red cell membrane stiffness in iron deficiency. Blood 62, 99-106 (1983).
37. Ntaios, G. et al. Discrimination indices as screening tests for β-thalassemic trait. Ann. Hematol. 86, 487-491 (2007).
38. Brandão, M. M. et al. Impaired red cell deformability in iron deficient subjects. Clin. Hemorheol. Microcirc. 43, 217-221 (2009).
39. d'Onofrio, G. et al. Simultaneous measurement of reticulocyte and red blood cell indices in healthy subjects and patients with microcytic and macrocytic anemia. Blood 85, 818-823 (1995).
40. Da Costa, L., Galimand, J., Fenneteau, O. & Mohandas, N. Hereditary spherocytosis, elliptocytosis, and other red cell membrane disorders. Blood Rev 27, 167-178 (2013).
41. Cynober, T., Mohandas, N. & Tchernia, G. Red cell abnormalities in hereditary spherocytosis: relevance to diagnosis and understanding of the variable expression of clinical severity. J. Lab. Clin. Med. 128, 259-269 (1996).
42. Da Costa, L. et al. Temporal differences in membrane loss lead to distinct reticulocyte features in hereditary spherocytosis and in immune hemolytic anemia. Blood 98, 2894-2899 (2001).
43. Chasis, J., Agre, P. & Mohandas, N. Decreased membrane mechanical stability and in vivo loss of surface area reflect spectrin deficiencies in hereditary spherocytosis. J. Clin. Invest. 82, 617 (1988).
44. Waugh, R. E. & Agre, P. Reductions of erythrocyte membrane viscoelastic coefficients reflect spectrin deficiencies in hereditary spherocytosis. J. Clin. Invest. 81, 133 (1988).
45. Bolton-Maggs, P. et al. Guidelines for the diagnosis and management of hereditary spherocytosis. Brit J Haematol 126, 455-474 (2004).
46. Tycko, D., Metz, M., Epstein, E. & Grinbaum, A. Flow-cytometric light scattering measurement of red blood cell volume and hemoglobin concentration. Applied optics 24, 1355-1365 (1985).
47. Schonbrun, E., Malka, R., Caprio, G., Schaak, D. & Higgins, J. M. Quantitative absorption cytometry for measuring red blood cell hemoglobin mass and volume. Cytometry Part A 85, 338 (2014).
48. Higgins, J. M. & Mahadevan, L. Physiological and pathological population dynamics of circulating human red blood cells. Proc. Natl. Acad. Sci. USA 107, 20587-20592 (2010).
49. Waugh, R. E. et al. Rheologic properties of senescent erythrocytes: loss of surface area and volume with red blood cell age. Blood 79, 1351-1358 (1992).
50. Nakashima, K. & Beutler, E. Erythrocyte cellular and membrane deformability in hereditary spherocytosis. Blood 53, 481-485 (1979).
51. Perrotta, S., Gallagher, P. G. & Mohandas, N. Hereditary spherocytosis. Lancet 372, 1411-1426 (2008).
52. Park, Y. K., Best, C. A. & Popescu, G. Optical sensing of red blood cell dynamics. in Mechanobiology of Cell-cell and Cell-matrix Interactions 279 (Springer, 2011).
53. Kim, Y., Kim, K. & Park, Y. Measurement Techniques for Red Blood Cell Deformability: Recent Advances. in Blood Cell - An Overview of Studies in Hematology (ed. Moschandreou, T.E.) 167-194 (INTECH, 2012).
54. Park, Y. et al. Measurement of the nonlinear elasticity of red blood cell membranes. Phys Rev E 83(2011).
55. Diez-Silva, M., Dao, M., Han, J., Lim, C. T. & Suresh, S. Shape and biomechanical characteristics of human red blood cells in health and disease. MRS bulletin 35, 382-388 (2010).
56. Park, Y. K. et al. Metabolic remodeling of the human red blood cell membrane. Proc. Natl. Acad. Sci. USA 107, 1289 (2010).
57. Boss, D. et al. Spatially-resolved eigenmode decomposition of red blood cells membrane fluctuations questions the role of ATP in flickering. PLoS One 7, e40667 (2012).
58. Betz, T., Lenz, M., Joanny, J. & Sykes, C. ATP-dependent mechanics of red blood cells. Proc. Natl. Acad. Sci. USA 106, 15312-15317 (2009).
59. Chandramohanadas, R. et al. Biophysics of malarial parasite exit from infected erythrocytes. PLoS One 6, e20869 (2011).
60. Diez-Silva, M. et al. Pf155/RESA protein influences the dynamic microcirculatory behavior of ring-stage Plasmodium falciparum infected red blood cells. Sci. Rep. (2012).
61. Park, Y. et al. Static and dynamic light scattering of healthy and malaria-parasite invaded red blood cells. J. Biomed. Opt. 15, 020506 (2010).
62. Shaked, N. T., Satter332white, L. L., Telen, M. J., Truskey, G. A. & Wax, A. Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry. J. Biomed. Opt. 16, 030506-030506-030503 (2011).
63. Kim, Y., and Higgins, J. M., Dasari, R. R., Suresh, S. & Park, Y. K. Anisotropic light scattering of individual sickle red blood cells. J. Biomed. Opt. 17, 040501-040501 (2012).
64. Jang, Y., Jang, J. & Park, Y. Dynamic spectroscopic phase microscopy for quantifying hemoglobin concentration and dynamic membrane fluctuation in red blood cells. Opt Express 20 (2012).
65. Jung, J. & Park, Y. Spectro-angular light scattering measurements of individual microscopic objects. Opt Express 22, 4108-4114 (2014).
66. Jung, J., Jang, J. & Park, Y. Spectro-refractometry of individual microscopic objects using swept-source quantitative phase imaging. Anal. Chem (2013).
67. Park, Y., Yamauchi, T., Choi, W., Dasari, R. & Feld, M. S. Spectroscopic phase microscopy for quantifying hemoglobin concentrations in intact red blood cells. Opt. Lett. 34, 3668-3670 (2009).
68. Wang, Z., and Millet, L. J., Gillette, M. U. & Popescu, G. Jones phase microscopy of transparent and anisotropic samples. Opt. Lett. 33, 1270-1272 (2008).
69. Kim, Y., Jeong, J., Jang, J., Kim, M. W. & Park, Y. Polarization holographic microscopy for extracting spatio-temporally resolved Jones matrix. Opt Express 20 (2012).
70. Lee, K. & Park, Y. Quantitative phase imaging unit. Opt Lett 39, 3630-3633 (2014).
71. Garay, J. et al. Crosstalk between PKA and Epac regulates the phenotypic maturation and function of human dendritic cells. J Immunol 185, 3227-3238 (2010).
72. Jo, Y. et al. Angle-resolved light scattering of individual rod-shaped bacteria based on Fourier transform light scattering. Sci. Rep. 4 (2014).