Stretching and relaxation of malaria-infected red blood cells.

The invasion of red blood cells (RBCs) by malaria parasites is a complex dynamic process, in which the infected RBCs gradually lose their deformability and their ability to recover their original shape is greatly reduced with the maturation of the parasites. In this work, we developed two types of cell model, one with an included parasite, and the other without an included parasite. The former is a representation of real malaria-infected RBCs, in which the parasite is treated as a rigid body. In the latter, where the parasite is absent, the membrane modulus and viscosity are elevated so as to produce the same features present in the parasite model. In both cases, the cell membrane is modeled as a viscoelastic triangular network connected by wormlike chains. We studied the transient behaviors of stretching deformation and shape relaxation of malaria-infected RBCs based on these two models and found that both models can generate results in agreement with those of previously published studies. With the parasite maturation, the shape deformation becomes smaller and smaller due to increasing cell rigidity, whereas the shape relaxation time becomes longer and longer due to the cell's reduced ability to recover its original shape.

[1]  Y. C. Fung,et al.  Improved measurements of the erythrocyte geometry. , 1972, Microvascular research.

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

[3]  Huixin Shi,et al.  The Malaria Parasite Progressively Dismantles the Host Erythrocyte Cytoskeleton for Efficient Egress* , 2011, Molecular & Cellular Proteomics.

[4]  Yang Liu,et al.  Experimental study on the deformation of erythrocytes under optically trapping and stretching , 2006 .

[5]  P. Español,et al.  Statistical Mechanics of Dissipative Particle Dynamics. , 1995 .

[6]  Petia M. Vlahovska,et al.  Vesicles and red blood cells in flow: From individual dynamics to rheology , 2009 .

[7]  R. Hochmuth,et al.  Red cell extensional recovery and the determination of membrane viscosity. , 1979, Biophysical journal.

[8]  R M Hochmuth,et al.  Erythrocyte membrane elasticity and viscosity. , 1987, Annual review of physiology.

[9]  George Em Karniadakis,et al.  A multiscale red blood cell model with accurate mechanics, rheology, and dynamics. , 2010, Biophysical journal.

[10]  P. B. Warren,et al.  DISSIPATIVE PARTICLE DYNAMICS : BRIDGING THE GAP BETWEEN ATOMISTIC AND MESOSCOPIC SIMULATION , 1997 .

[11]  Prosenjit Bagchi,et al.  Phase diagram and breathing dynamics of a single red blood cell and a biconcave capsule in dilute shear flow. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[12]  Clemens F Kaminski,et al.  Quantitative imaging of human red blood cells infected with Plasmodium falciparum. , 2010, Biophysical journal.

[13]  A. Cowman,et al.  Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. , 2002, Blood.

[14]  Daniel T Chiu,et al.  A microfluidic model for single-cell capillary obstruction by Plasmodium falciparum-infected erythrocytes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Clemens F Kaminski,et al.  Detection of Plasmodium falciparum-infected red blood cells by optical stretching. , 2010, Journal of biomedical optics.

[16]  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.

[17]  F. John,et al.  Stretching DNA , 2022 .

[18]  R M Hochmuth,et al.  Measurement of the elastic modulus for red cell membrane using a fluid mechanical technique. , 1973, Biophysical journal.

[19]  J. Koelman,et al.  Simulating microscopic hydrodynamic phenomena with dissipative particle dynamics , 1992 .

[20]  Chwee Teck Lim,et al.  Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. , 2005, Acta biomaterialia.

[21]  J. Rowe,et al.  Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications , 2009, Expert Reviews in Molecular Medicine.

[22]  C. Pozrikidis,et al.  Modeling and Simulation of Capsules and Biological Cells , 2003 .

[23]  J. Dormandy,et al.  Abnormalities in the mechanical properties of red blood cells caused by Plasmodium falciparum , 1989 .

[24]  Yulia M. Serebrennikova,et al.  Quantitative analysis of morphological alterations in Plasmodium falciparum infected red blood cells through theoretical interpretation of spectral measurements. , 2010, Journal of theoretical biology.

[25]  I. Gluzman,et al.  Plasmodium falciparum maturation abolishes physiologic red cell deformability. , 1984, Science.

[26]  Bruce Russell,et al.  High deformability of Plasmodium vivax-infected red blood cells under microfluidic conditions. , 2009, The Journal of infectious diseases.

[27]  G. Karniadakis,et al.  Systematic coarse-graining of spectrin-level red blood cell models. , 2010, Computer Methods in Applied Mechanics and Engineering.

[28]  James J. Feng,et al.  How malaria parasites reduce the deformability of infected red blood cells. , 2012, Biophysical journal.

[29]  G. Nash,et al.  Membrane rigidity of red blood cells parasitized by different strains of Plasmodium falciparum. , 1993, The Journal of laboratory and clinical medicine.

[30]  C. Lim,et al.  Host cell deformability is linked to transmission in the human malaria parasite Plasmodium falciparum , 2012, Cellular microbiology.

[31]  Kasturi Haldar,et al.  Erythrocyte remodeling by malaria parasites , 2007, Current opinion in hematology.

[32]  P. Español,et al.  FLUID PARTICLE MODEL , 1998 .

[33]  Leann Tilley,et al.  The Plasmodium falciparum-infected red blood cell. , 2011, The international journal of biochemistry & cell biology.

[34]  G E Karniadakis,et al.  Quantifying the biophysical characteristics of Plasmodium-falciparum-parasitized red blood cells in microcirculation , 2010, Proceedings of the National Academy of Sciences.

[35]  C. Lim,et al.  Observations on the internal and surface morphology of malaria infected blood cells using optical and atomic force microscopy. , 2006, Journal of microbiological methods.

[36]  Leann Tilley,et al.  Malaria parasite proteins that remodel the host erythrocyte , 2009, Nature Reviews Microbiology.

[37]  Leann Tilley,et al.  Cellular architecture of Plasmodium falciparum-infected erythrocytes. , 2010, International journal for parasitology.