Estimation of membrane bending modulus of stiffness tuned human red blood cells from micropore filtration studies
Autoři:
Rekha Selvan aff001; Praveen Parthasarathi aff002; Shruthi S. Iyengar aff001; Sharath Ananthamurthy aff001; Sarbari Bhattacharya aff001
Působiště autorů:
Department of Physics, Bangalore University, Bangalore, India
aff001; Soft Condensed Matter Group, Raman Research Institute, Bangalore, India
aff002; School of Physics, University of Hyderabad, Hyderabad, Telangana, India
aff003
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226640
Souhrn
Human red blood cells (RBCs) need to deform in order to pass through capillaries in human vasculature with diameter smaller than that of the RBC. An altered RBC cell membrane stiffness (CMS), thereby, is likely to have consequences on their flow rate. RBC CMS is known to be affected by several commonly encountered disease conditions. This study was carried out to investigate whether an increase in RBC CMS, to the extent seen in such commonly encountered medical conditions, affects the RBC flow rate through channels with diameters comparable to that of the RBC. To do this, we use RBCs extracted from a healthy individual with no known medical conditions and treated with various concentrations of Bovine Serum Albumin (BSA). We study their flow through polycarbonate membranes with pores of diameter 5μm and 8μm which are smaller than and comparable to the RBC diameter respectively. The studies are carried out at constant hematocrit and volumetric flow rate. We find that when the diameter of the capillary is smaller than that of the RBC, the flow rate of the RBCs is lowered as the concentration of BSA is increased while the reverse is true when the diameter is comparable to that of the RBC. We confirm that this is a consequence of altered CMS of the RBCs from their reorientation dynamics in an Optical Tweezer. We find that a treatment with 0.50mg/ml BSA mimics the situation for RBCs extracted from a healthy individual while concentrations higher than 0.50mg/ml elevate the RBC CMS across a range expected for individuals with a condition of hyperglycemia. Using a simple theoretical model of the RBC deformation process at the entry of a narrow channel, we extract the RBC membrane bending modulus from their flow rate.
Klíčová slova:
Filter paper – Radii – Lasers – Deformation – Flow rate – Hematocrit – Drag – Bending
Zdroje
1. Jensen FB. The dual roles of red blood cells in tissue oxygen delivery: oxygen carriers and regulators of local blood flow. J Exp Biol. 2009;212:3387. doi: 10.1242/jeb.023697 19837879
2. Gompper G, Schick M. vol. 4. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim; 2008.
3. Tomaiuolo G, Simeone M, Martinelli V, Rotoli B, Guido S. Red blood cell deformation in micro—confined flow. Soft Matter. 2009;5:3736. doi: 10.1039/b904584h
4. Braunmuller S, Schmid L, Sackmann E, Franke T, et al. Hydrodynamic deformation reveals two coupled modes/time scales of red blood cell relaxation. Soft Matter. 2012;8:11240. doi: 10.1039/c2sm26513c
5. Quinn DJ, et al. Combined Simulation and experimental study of large deformation of red blood cells in microfluidic systems. Ann Biomed Eng. 2011;39(3):1041. doi: 10.1007/s10439-010-0232-y 21240637
6. Babu N, Singh M. Influence of hyperglycemia on aggregation, deformability and shape parameters of erythrocytes. Clin Hemorheol. 2004;31:273.
7. Tsukada K, Sekizuka E, Oshio C, Minamitani H. Direct measurement of erythrocyte deformability in diabetes mellitus with a transparent microchannel capillarymodel and high- speed video camera system. Microvasc Res. 2001;61:231. doi: 10.1006/mvre.2001.2307 11336534
8. Moon JS, et al. Impaired RBC deformability is associated with diabetic retinopathy in patients with type 2 diabetes. Diabetes Metab. 2016;42(6):448. doi: 10.1016/j.diabet.2016.04.008 27209441
9. Singh M, Kumravel M. Influence of jaundice on aggregation process and deformability of erythrocytes. Clin Hemorheol Microcirc. 1995;15(3):273. doi: 10.3233/CH-1995-15301
10. Dobbe JGG, et al. Analyzing Red Blood Cell Deformability Distributions. Blood Cells Mol Dis. 2002;28(3):373. doi: 10.1006/bcmd.2002.0528 12367581
11. Glenister FK, Coppel RL, Cowman AF, Mohandas N, Cooke BM. Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. Blood. 2002;99:1060. doi: 10.1182/blood.v99.3.1060 11807013
12. Evans EA. Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests. Biophys J. 1983;43(1):27. doi: 10.1016/S0006-3495(83)84319-7 6882860
13. Chien S, Paul KL, Skalak R, Usami S, Tözeren A. Theoretical and experimental studies on viscoelastic properties of erythrocyte membrane. Biophys J. 1978;24(2):463. doi: 10.1016/S0006-3495(78)85395-8 728524
14. Parthasarathi P, et al. Orientational dynamics of human red blood cells in an optical trap. J Biomed Opt. 2013;18(2):025001. doi: 10.1117/1.JBO.18.2.025001
15. Agarwal R, et al. Assessment of red blood cell deformability in type 2 diabetes mellitus and diabetic retinopathy by dual optical tweezers stretching technique. Sci Rep. 2016;6:15873. doi: 10.1038/srep15873
16. Barnes T, Shulman A, Farone A, Farone M, Erenso D. Assessment of the elasticity of erythrocytes in different physiological fluids by laser traps. OPJ. 2013;3:211. doi: 10.4236/opj.2013.32034
17. Henon S, Lenormand G, Richert A, Gallet F. A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys J. 1999;76(2):1145. doi: 10.1016/S0006-3495(99)77279-6 9916046
18. Alster Y, Loewenstein A, Levin S, Lazar M, Korenstein R. Low-frequency submicron fluctuations of red blood cells in diabetic retinopathy. Arch Ophthalmol. 1998;116(10):1321. doi: 10.1001/archopht.116.10.1321 9790630
19. Evans J, Gratzer W, Mohandas N, Parker K, Sleep J. Fluctuations of the red blood cell membrane: relation to mechanical properties and lack of ATP dependence. Biophys J. 2008;94(10):4134. doi: 10.1529/biophysj.107.117952 18234829
20. Yang T, Bragheri F, Minzioni PA. Comprehensive review of optical stretcher for cell mechanical characterization at single-cell level. Micromachines. 2016;7(5):90. doi: 10.3390/mi7050090
21. Guck J, et al. The Optical Stretcher: A Novel Laser Tool to Micromanipulate Cells. Biophys J. 2001;81:767. doi: 10.1016/S0006-3495(01)75740-2 11463624
22. Zheng Y, Nguyen J, Wang C, Sun Y. Electrical measurement of red blood cell deformability on a microfluidic device. Lab Chip. 2013;13:3275. doi: 10.1039/c3lc50427a 23798004
23. Gosett DR, et al. Hydrodynamic stretching of single cells for large population mechanical phenotyping. PNAS. 2012;109(20):7630. doi: 10.1073/pnas.1200107109
24. Dulińska I, et al. Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy. J Biochem Biophys Meth. 2006;66:1. doi: 10.1016/j.jbbm.2005.11.003 16443279
25. Maciaszek JL, Lykotrafitis G. Sickle cell trait human erythrocytes are significantly stiffer than normal. J Biomech. 2011;44:657. doi: 10.1016/j.jbiomech.2010.11.008 21111421
26. Zhang W, Liu F. Effect of polylysine on blood clotting, and red blood cell morphology, aggregation and hemolysis. J Nanosci Nanotechnol. 2017;17(1):251. doi: 10.1166/jnn.2017.12593 29620337
27. Kim J, Lee H, Shin S. Advances in the measurement of red blood cell deformability: A brief review Article. J Cell Biotechnol. 2015;1:63. doi: 10.3233/JCB-15007
28. Brown CD, Ghali HS, Zhao Z, Thomas LL, Friedman EA. Association of reduced red blood cell deformability and diabetic nephropathy. Kidney Int. 2005;67:295. doi: 10.1111/j.1523-1755.2005.00082.x 15610255
29. Moia M, Tripodi A, Mozzi E, Mari D, Mannucci PM. An improved method for measuring red blood cell filterability. Ric Clin Lab. 1985;15(2):127. doi: 10.1007/bf03029829 4059793
30. Kirkpatrick UJ, Adams RA, Lardi A, McCollum CN. Rheological properties and function of blood cells in stored bank blood and salvaged blood. Br J Haematol. 1998;101:364. doi: 10.1046/j.1365-2141.1998.00689.x 9609536
31. Shin S, Ku Y, Babu N, Singh M. Erythrocyte deformability and its variation in diabetes mellitus. Indian J Exp Biol. 2007;45:121. 17249336
32. Yoon YZ, Kotar J, Brown A, Cicuta P. Red blood cell dynamics: from spontaneous fluctuations to non-linear response. Soft Matter. 2011;7:2042. doi: 10.1039/C0SM01117G
33. Jay A. Geometry of the human erythrocyte -I. Effect of albumin on cell geometry. Biophys J. 1975;15:205. doi: 10.1016/S0006-3495(75)85812-7 1122337
34. Williams A. The effect of bovine and human serum albumins on the mechanical properties of human erythrocyte membranes. Biochim Biophys Acta. 1973;307:58. doi: 10.1016/0005-2736(73)90024-2 4736380
35. Starosta W. Applications of ionizing radiation in materials processing. vol. 2. Institute of Nuclear Chemistry and Technology Warszawa; 2017.
36. Jeong JH, Sugii Y, Minamiyama M, Okamoto K. Measurement of RBC deformation and velocity in capillaries in vivo. Microvasc Res. 2006;71:212. doi: 10.1016/j.mvr.2006.02.006 16624342
37. Stucker M, et al. Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: Measured by a new Doppler laser anemometer. Microvasc Res. 1996;52:188. doi: 10.1006/mvre.1996.0054 8901447
38. Omori T, Ishikawa T, Barthès-Biesel D, et al. Tension of red blood cell membrane in simple shear flow. PRE. 2012;86:056321. doi: 10.1103/PhysRevE.86.056321 23214889
39. Chen TC, Skalak R. Stokes flow in a cylindrical tube containing a line of spheroidal particles. Appl Sci Res. 1970;22:403. doi: 10.1007/BF00400546
40. Yawata Y. Cell Membrane: The Red Blood Cell as a Model. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim; 2003.
41. Fedosov DA, Peltomäki M, Gompper G. Deformation and dynamics of red blood cells in flow through cylindrical microchannels. Soft Matter. 2014;10:4258. doi: 10.1039/c4sm00248b 24752231
42. Munoz S, Sebastián JL, Sancho M, et al. Elastic energy of the discocyte– stomatocyte transformation. BBA. 2014;1838(3):950. doi: 10.1016/j.bbamem.2013.10.020 24192054
43. Tanford C, Buzell JG. The viscosity of aqueous solutions of bovine serum albumin between pH 4.3 and 10.5. J Phys Chem. 1956;60(2):225. doi: 10.1021/j150536a020
44. Tan CY, Huang YX. Dependence of refractive index on concentration and temperature in electrolyte solution, polar solution, nonpolar solution, and protein solution. J Chem Eng. 2015;60:2827.
45. Zhang J, Johnson PC, Popel AS. Effects of erythrocyte deformability and aggregation on the cell free layer and apparent viscosity of microscopic blood flows. Microvasc Res. 2009;77(3):265. doi: 10.1016/j.mvr.2009.01.010 19323969
46. Xia Y, Callaghan PT, Jeffrey KR. Imaging velocity profiles: flow through an abrupt contraction and expansion. AlChE J. 1992;38(9):1408. doi: 10.1002/aic.690380912
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts