Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient

Acta Biomaterialia

Volumn 8, Issue 11, 2012, Pages 4130-4138

  Byun, HeeSu ^a   Hillman, Timothy R ^b   Higgins, John M ^c,d   Diez Silva, Monica ^e   Peng, Zhangli ^e   Dao, Ming ^e   Dasari, Ramachandra R ^b   Suresh, Subra ^e   Park, YongKeun ^a  

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

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Cell biomechanics; Cell membrane; Optical measurement; Red blood cell; Sickle cell disease

Indexed keywords

BIOMECHANICS; BLOOD; CELLS; CYTOLOGY; DYNAMICS; LASER INTERFEROMETRY; MEMBRANES; OPTICAL VARIABLES MEASUREMENT; PROBES; VISCOSITY;

BIOMECHANICAL PROPERTIES; CELL BIOMECHANICS; DEOXYGENATED CONDITIONS; DYNAMIC MEMBRANES; MEASUREMENTS OF; MEMBRANE FLUCTUATIONS; OPTICAL MEASUREMENT; RED BLOOD CELL; SICKLE CELL; SICKLE CELL DISEASE;

OPTICAL DATA PROCESSING;

HEMOGLOBIN;

ARTICLE; BIOMECHANICS; CELL MEMBRANE; CYTOPLASM; ERYTHROCYTE; HUMAN; HUMAN CELL; INTERFEROMETRY; LASER; MAJOR CLINICAL STUDY; MEASUREMENT; MEMBRANE MODEL; MICROVASCULATURE; NON INVASIVE PROCEDURE; OPTICS; OXYGEN CONCENTRATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SICKLE CELL ANEMIA; VISCOSITY; BIOLOGICAL MODEL; BLOOD; CELL SHAPE; ERYTHROCYTE DISORDER; ERYTHROCYTE MEMBRANE; METABOLISM; METHODOLOGY; MICROSCOPY; PATHOLOGY; YOUNG MODULUS;

ANEMIA, SICKLE CELL; BIOMECHANICS; CELL SHAPE; ELASTIC MODULUS; ERYTHROCYTE MEMBRANE; ERYTHROCYTES, ABNORMAL; HEMOGLOBINS; HUMANS; MICROSCOPY; MODELS, BIOLOGICAL; OPTICS AND PHOTONICS; VISCOSITY;

EID: 84873966188     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2012.07.011     Document Type: Article

References (60)

1. Stuart MJ, Nagel RL. Sickle-cell disease. The Lancet 2004;364(9442):1343- 60. (Pubitemid 39335827)
2. Platt OS, Brambilla DJ, Rosse WF, Milner PF, Castro O, Steinberg MH, et al. Mortality in sickle cell disease-life expectancy and risk factors for early death. N Engl J Med 1994;330(23):1639-44.
3. Diez-Silva M, Dao M, Han J, Lim C, Suresh S. Shape and biomechanical characteristics of human red blood cells in health and disease. MRS Bull: Mater Res Soc 2010;35(5):382.
4. Bao G, Suresh S. Cell and molecular mechanics of biological materials. Nat Mater 2003;2:715-25.
5. Suresh S, Spatz J, Mills JP, Micoulet A, Dao M, Lim CT, et al. Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. Acta Biomater 2005;1(1):15-30. (Pubitemid 43348807)
6. Barabino G, Platt M, Kaul D. Sickle cell biomechanics. Annu Rev Biomed Eng 2010;12:345-67.
7. Chien S, Usami S, Bertles JF. Abnormal rheology of oxygenated blood in sickle cell anemia. J Clin Invest 1970;49(4):623.
8. Sorette MP, Lavenant MG, Clark MR. Ektacytometric measurement of sickle cell deformability as a continuous function of oxygen tension. Blood 1987;69(1):316 [published erratum appears in 1987;69(4):1272].
9. Evans E, Mohandas N, Leung A. Static and dynamic rigidities of normal and sickle erythrocytes. Major influence of cell hemoglobin concentration. J Clin Invest 1984;73(2):477.
10. Nash GB, Johnson CS, Meiselman HJ. Mechanical properties of oxygenated red blood cells in sickle cell (HbSS) disease. Blood 1984;63(1):73-82. (Pubitemid 14224523)
11. Barabino GA, McIntire L, Eskin SG, Sears DA, Udden M. Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow. Blood 1987;70(1):152.
12. Maciaszek JL, Andemariam B, Lykotrafitis G. Microelasticity of red blood cells in sickle cell disease. J Strain Anal Eng Des [accepted].
13. Park Y, Best C, Badizadegan K, Dasari R, Feld M, Kuriabova T, et al. Measurement of red blood cell mechanics during morphological changes. Proc Natl Acad Sci 2010;107(15):6731.
14. Park YK, Best CA, Auth T, Gov N, Safran SA, Popescu G, et al. Metabolic remodeling of the human red blood cell membran. Proc Natl Acad Sci 2010;107:1289.
15. Park YK, Diez-Silva M, Popescu G, Lykotrafitis G, Choi W, Feld MS, et al. Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum. Proc Natl Acad Sci 2008;105(37):13730.
16. Kuriabova T, Levine AJ. Nanorheology of viscoelastic shells: Applications to viral capsids. Phys Rev E 2008;77(3):031921.
17. Park YK, Best CA, Kuriabova T, Henle ML, Feld MS, Levine AJ, et al. Measurement of the nonlinear elasticity of red blood cell membranes. Phys Rev E 2011;83(5):051925.
18. Discher DE, Carl P. New insights into red cell network structure, elasticity, and spectrin unfolding-A current review. Cell Mol Biol Lett 2001;6(3):593-606. (Pubitemid 33678434)
19. Hochmuth RM, Buxbaum KL, Evans EA. Temperature dependence of the viscoelastic recovery of red cell membrane. Biophys J 1980;29(1):177-82. (Pubitemid 10207715)
20. Wells R, Schmid-Schonbein H. Red cell deformation and fluidity of concentrated cell suspensions. J Appl Physiol 1969;27(2):213-7.
21. Evans E. New membrane concept applied to the analysis of fluid shear-And micropipette-deformed red blood cells. Biophys J 1973;13(9):941-54.
22. Betz T, Lenz M, Joanny J, Sykes C. ATP-dependent mechanics of red blood cells. Proc Natl Acad Sci USA 2009;106(36):15312-7.
23. Gov N, Zilman AG, Safran S. Cytoskeleton confinement and tension of red blood cell membranes. Phys Rev Lett 2003;90(22):228101.
24. Hochmuth RM, Waugh RE. Erythrocyte membrane elasticity and viscocity. Ann Rev Physiol 1987;49:209-19.
25. Lelièvre J, Bucherer C, Geiger S, Lacombe C, Vereycken V. Blood cell biomechanics evaluated by the single-cell micromanipulation. J Phys III France 1995;5:1689-706.
26. Rawicz W, Olbrich K, McIntosh T, Needham D, Evans E. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 2000;79(1):328-39. (Pubitemid 30436749)
27. Lenormand G, Hénon S, Richert A, Siméon J, Gallet F. Direct measurement of the area expansion and shear moduli of the human red blood cell membrane skeleton. Biophys J 2001;81(1):43-56. (Pubitemid 32605950)
28. Dao M, Li J, Suresh S. Molecularly based analysis of deformation of spectrin network and human erythrocyte. Mater Sci Eng C 2006;26(8):1232-44. (Pubitemid 44163188)
29. Evans EA, Waugh R. Osmotic correction to elastic area compressibility measurements on red-cell membrane. Biophys J 1977;20(3):307-13. (Pubitemid 8242211)
30. Evans EA, Waugh R, Melnik L. Elastic area compressibility modulus of red-cell membrane. Biophys J 1976;16(6):585-95.
31. Peng ZL, Asaro RJ, Zhu Q. Multiscale simulation of erythrocyte membranes. Phys Rev E 2010;81(3):031904.
32. Chien S, Sung K, Skalak R, Usami S, Tözeren A. Theoretical and experimental studies on viscoelastic properties of erythrocyte membrane. Biophys J 1978;24(2):463-87. (Pubitemid 9053114)
33. Helfrich W. Elastic properties of lipid bilayers: Theory and possible experiments. Z naturforsch C 1973;28(11-12):693-703.
34. Jones C, Jhonson Jr C, Penniston J. Photon correlation spectroscopy of hemoglobin: diffusion of Oxy HbA and Oxy HbS. Biopolymers 1978;17(6):1581-93. (Pubitemid 8345357)
35. Phillies G. Translational diffusion coefficient of macroparticles in solvents of high viscosity. J Phys Chem 1981;85(19):2838-43.
36. Popescu G, Ikeda T, Dasari RR, Feld MS. Diffraction phase microscopy for quantifying cell structure and dynamics. Opt Lett 2006;31(6):775-7.
37. Park YK, Popescu G, Badizadegan K, Dasari RR, Feld MS. Diffraction phase and fluorescence microscopy. Opt Exp 2006;14(18):8263-8. (Pubitemid 44331043)
38. Popescu G, Park Y, Choi W, Dasari R, Feld M, Badizadegan K. Imaging red blood cell dynamics by quantitative phase microscopy. Blood Cells, Molecules, and Diseases 2008;41(1):10-6.
39. Debnath SK, Park Y. Real-time quantitative phase imaging by spatial phase shifting algorithm. Opt Lett 2011;36(23):4677-9.
40. Harris N, Kunicka J, Kratz A. The ADVIA 2120 hematology system: Flow cytometry-based analysis of blood and body fluids in the routine hematology laboratory. Lab Hematol 2005;11(1):47-61. (Pubitemid 40444033)
41. Popescu G, Park Y, Lue N, Best-Popescu C, Deflores L, Dasari R, et al. Optical imaging of cell mass and growth dynamics. Am J Physiol: Cell Physiol 2008;295(2):C538.
42. Ferster A, Vermylen C, Cornu G, Buyse M, Corazza F, Devalck C, et al. Hydroxyurea for treatment of severe sickle cell anemia: A pediatric clinical trial. Blood 1996;88(6):1960-4. (Pubitemid 26307897)
43. Kaul D, Fabry M, Windisch P, Baez S, Nagel R. Erythrocytes in sickle cell anemia are heterogeneous in their rheological and hemodynamic characteristics. J Clin Invest 1983;72(1):22.
44. Barer R. Determination of dry mass, thickness, solid and water concentration in living cells. Nature 1953;172(4389):1097-8.
45. Rodgers GP, Dover GJ, Noguchi CT, Schechter AN, Nienhuis AW. Hematologic responses of patients with sickle cell disease to treatment with hydroxyurea. N Engl J Med 1990;322(15):1037-45. (Pubitemid 20146662)
46. Fedosov DA, Lei H, Caswell B, Suresh S, Karniadakis GE. Multiscale modeling of red blood cell mechanics and blood flow in malaria. PLoS Comput Biol 2011;7(12):e1002270.
47. Shaked NT, Satterwhite LL, Telen MJ, Truskey GA, Wax A. Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry. J Biomed Opt 2011;16:030506.
48. Hiruma H, Noguchi CT, Uyesaka N, Hasegawa S, Blanchette Mackie EJ, Schechter AN, Rodgers GP. Sickle cell rheology is determined by polymer fraction-not cell morphology. Am J Hematol 1995;48(1):19-28.
49. Clark M, Mohandas N, Shohet S. Hydration of sickle cells using the sodium ionophore monensin. A model for therapy. J Clin Invest 1982;70(5):1074.
50. Gulley ML, Ross DW, Feo C, Orringer EP. The effect of cell hydration on the deformability of normal and sickle erythrocytes. Am J Hematol 1982;13(4):283-91. (Pubitemid 13208192)
51. Clark M, Mohandas N, Embury SH, Lubin BH. A simple laboratory alternative to irreversibly sickled cell (ISC) counts. Blood 1982;60:659.
52. Messer M, Harris J. Filtration characteristics of sickle cells: rates of alteration of filterability after deoxygenation and reoxygenation, and correlations with sickling and unsickling. J Lab Clin Med 1970;76(4):537.
53. Frenette PS, Atweh GF. Sickle cell disease: old discoveries, new concepts, and future promise. J Clin Invest 2007;117(4):850.
54. Franck P, Bevers E, Lubin B, Comfurius P, Chiu D, den Kamp JAO, et al. Uncoupling of the membrane skeleton from the lipid bilayer. The cause of accelerated phospholipid flip-flop leading to an enhanced procoagulant activity of sickled cells. J Clin Invest 1985;75(1):183.
55. Hebbel R. Beyond hemoglobin polymerization: The red blood cell membrane and sickle disease pathophysiology. Blood 1991;77(2):214-37.
56. Higgins J, Eddington D, Bhatia S, Mahadevan L. Sickle cell vasoocclusion and rescue in a microfluidic device. Proc Natl Acad Sci 2007;104(51):20496.
57. Hebbel RP. Perspectives series: cell adhesion in vascular biology. Adhesive interactions of sickle erythrocytes with endothelium. J Clin Invest 1997;99(11):2561.
58. Ben-Isaac E, Park YK, Popescu G, Brown FLH, Gov NS, Shokef Y. Effective temperature of red-blood-cell membrane fluctuations. Phys Rev Lett 2011;106(23):238103.
59. Nash GB, Johnson CS, Meiselman HJ. Rheologic impairment of sickle RBCs induced by repetitive cycles of deoxygenation-reoxygenation. Blood 1988;72(2):539.
60. Cho S, Kim S, Kim Y, Park YK. Optical imaging techniques for the study of malaria. Trends Biotechnol 2011;30(2):71-9.