Multiple stiffening effects of nanoscale knobs on human red blood cells infected with Plasmodium falciparum malaria parasite

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 19, 2015, Pages 6068-6073

  Zhang, Yao ^a   Huang, Changjin ^a   Kim, Sangtae ^b   Golkaram, Mahdi ^a   Dixon, Matthew W A ^b   Tilley, Leann ^b   Li, Ju ^b,c   Zhang, Sulin ^a   Suresh, Subra ^d,e  

^a The Pennsylvania State University   (United States)

^b Massachusetts Institute of Technology   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d CARNEGIE MELLON UNIVERSITY   (United States)

^e Department of Materials Science and Engineering Carnegie Mellon University ^*  (United States)

Author keywords

Coarse grained simulations; Malaria; Red blood cells; Shear modulus; Stiffening

Indexed keywords

SPECTRIN; LIPID BILAYER;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CELL DENSITY; CELL INVASION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ERYTHROCYTE; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE STRUCTURE; HUMAN; HUMAN CELL; LIPID BILAYER; MALARIA FALCIPARUM; MICROVASCULATURE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN STRUCTURE; SCHIZONT; TROPHOZOITE; CHEMISTRY; COMPUTER SIMULATION; CYTOSKELETON; ERYTHROCYTE COUNT; ERYTHROCYTE MEMBRANE; MECHANICAL STRESS; PARASITOLOGY; PLASMODIUM FALCIPARUM; SHEAR STRENGTH;

PLASMODIUM FALCIPARUM;

COMPUTER SIMULATION; CYTOSKELETON; ERYTHROCYTE COUNT; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HUMANS; LIPID BILAYERS; MALARIA, FALCIPARUM; MOLECULAR DYNAMICS SIMULATION; PLASMODIUM FALCIPARUM; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 84929192715     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505584112     Document Type: Article

References (55)

1. Murray CJL, et al. (2012) Global malaria mortality between 1980 and 2010: A systematic analysis. Lancet 379(9814):413-431.
2. Hay SI, et al. (2009) A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med 6(3):e1000048.
3. Maier AG, Cooke BM, Cowman AF, Tilley L (2009) Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol 7(5):341-354.
4. Bannister LH, Hopkins JM, Fowler RE, Krishna S, Mitchell GH (2000) A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitol Today 16(10):427-433.
5. Haldar K, Mohandas N (2007) Erythrocyte remodeling by malaria parasites. Curr Opin Hematol 14(3):203-209.
6. Pei X, et al. (2005) Structural and functional studies of interaction between Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and erythrocyte spectrin. J Biol Chem 280(35):31166-31171.
7. Magowan C, et al. (2000) Plasmodium falciparum histidine-rich protein 1 associates with the band 3 binding domain of ankyrin in the infected red cell membrane. Biochim Biophys Acta 1502(3):461-470.
8. Waller KL, Cooke BM, Nunomura W, Mohandas N, Coppel RL (1999) Mapping the binding domains involved in the interaction between the Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and the cytoadherence ligand P. falciparum erythrocytemembraneprotein1(PfEMP1).J Biol Chem 274(34):23808-23813.
9. Oh SS, et al. (2000) Plasmodium falciparum erythrocyte membrane protein 1 is anchored to the actin-spectrin junction and knob-associated histidine-rich protein in the erythrocyte skeleton. Mol Biochem Parasitol 108(2):237-247.
10. Cyrklaff M, et al. (2011) Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes. Science 334(6060):1283-1286.
11. Suresh S (2006) Mechanical response of human red blood cells in health and disease: Some structure-property-function relationships. J Mater Res 21(08):1871-1877.
12. Suresh S, et al. (2005) Connections between single-cell biomechanics and human disease states: Gastrointestinal cancer and malaria. Acta Biomater 1(1):15-30.
13. Park Y, et al. (2008) Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum. Proc Natl Acad Sci USA 105(37):13730-13735.
14. Maier AG, et al. (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134(1):48-61.
15. Rug M, Prescott SW, Fernandez KM, Cooke BM, Cowman AF (2006) The role of KAHRP domains in knob formation and cytoadherence of P. falciparum-infected human erythrocytes. Blood 108(1):370-378.
16. Mills JP, et al. (2007) Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum. Proc Natl Acad Sci USA 104(22):9213-9217.
17. Diez-Silva M, et al. (2012) Pf155/RESA protein influences the dynamic microcirculatory behavior of ring-stage Plasmodium falciparum infected red blood cells. Sci Rep 2:614.
18. Pei X, Guo X, Coppel R, Mohandas N, An X (2007) Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) destabilizes erythrocyte membrane skeleton. J Biol Chem 282(37):26754-26758.
19. Pei X, et al. (2007) The ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Blood 110(3):1036-1042.
20. Hodder AN, et al. (2009) Analysis of structure and function of the giant protein Pf332 in Plasmodium falciparum. Mol Microbiol 71(1):48-65.
21. Orjih AU, Cherian PT (2013) Possible relationship between Plasmodium falciparum ring-infected erythrocyte surface antigen (RESA) and host cell resistance to destruction by chemicals. Parasitol Res 112(12):4043-4051.
22. Glenister FK, et al. (2009) Functional alteration of red blood cells by a megadalton protein of Plasmodium falciparum. Blood 113(4):919-928.
23. An X, Mohandas N (2008) Disorders of red cell membrane. Br J Haematol 141(3): 367-375.
24. Boal DH (1994) Computer simulation of a model network for the erythrocyte cytoskeleton. Biophys J 67(2):521-529.
25. Boey SK, Boal DH, Discher DE (1998) Simulations of the erythrocyte cytoskeleton at large deformation. I. Microscopic models. Biophys J 75(3):1573-1583.
26. Discher DE, Boal DH, Boey SK (1998) Simulations of the erythrocyte cytoskeleton at large deformation. II. Micropipette aspiration. Biophys J 75(3):1584-1597.
27. Li J, Dao M, Lim CT, Suresh S (2005) Spectrin-level modeling of the cytoskeleton and optical tweezers stretching of the erythrocyte. Biophys J 88(5):3707-3719.
28. Gov NS (2007) Active elastic network: Cytoskeleton of the red blood cell. Phys Rev E Stat Nonlin Soft Matter Phys 75(1 Pt 1):011921.
29. Noguchi H, Gompper G (2005) Shape transitions of fluid vesicles and red blood cells in capillary flows. Proc Natl Acad Sci USA 102(40):14159-14164.
30. McWhirter JL, Noguchi H, Gompper G (2009) Flow-induced clustering and alignment of vesicles and red blood cells in microcapillaries. Proc Natl Acad Sci USA 106(15): 6039-6043.
31. Pivkin IV, Karniadakis GE (2008) Accurate coarse-grained modeling of red blood cells. Phys Rev Lett 101(11):118105.
32. Fedosov DA, Caswell B, Suresh S, Karniadakis GE (2011) Quantifying the biophysical characteristics of Plasmodium-falciparum-parasitized red blood cells in microcirculation. Proc Natl Acad Sci USA 108(1):35-39.
33. Fedosov DA, Caswell B, Karniadakis GE (2010) A multiscale red blood cell model with accurate mechanics, rheology, and dynamics. Biophys J 98(10):2215-2225.
34. Li H, Lykotrafitis G (2014) Erythrocyte membrane model with explicit description of the lipid bilayer and the spectrin network. Biophys J 107(3):642-653.
35. Peng Z, et al. (2013) Lipid bilayer and cytoskeletal interactions in a red blood cell. Proc Natl Acad Sci USA 110(33):13356-13361.
36. Sikder MKU, Stone KA, Kumar PBS, Laradji M (2014) Combined effect of cortical cytoskeleton and transmembrane proteins on domain formation in biomembranes. J Chem Phys 141(5):054902.
37. Spangler EJ, Harvey CW, Revalee JD, Kumar PBS, Laradji M (2011) Computer simulation of cytoskeleton-induced blebbing in lipid membranes. Phys Rev E Stat Nonlin Soft Matter Phys 84(5 Pt 1):051906.
38. Yuan H, Huang C, Li J, Lykotrafitis G, Zhang S (2010) One-particle-thick, solvent-free, coarse-grained model for biological and biomimetic fluid membranes. Phys Rev E Stat Nonlin Soft Matter Phys 82(1 Pt 1):011905.
39. Liu SC, Derick LH, Palek J (1987) Visualization of the hexagonal lattice in the erythrocyte membrane skeleton. J Cell Biol 104(3):527-536.
40. Li J, Lykotrafitis G, Dao M, Suresh S (2007) Cytoskeletal dynamics of human erythrocyte. Proc Natl Acad Sci USA 104(12):4937-4942.
41. Bennett V, Baines AJ (2001) Spectrin and ankyrin-based pathways: Metazoan inventions for integrating cells into tissues. Physiol Rev 81(3):1353-1392.
42. Dixon MWA, et al. (2011) Genetic ablation of a Maurer's cleft protein prevents assembly of the Plasmodium falciparum virulence complex. Mol Microbiol 81(4):982-993.
43. Shi H, et al. (2013) Life cycle-dependent cytoskeletal modifications in Plasmodium falciparum infected erythrocytes. PLoS One 8(4):e61170.
44. Gruenberg J, Allred DR, Sherman IW (1983) Scanning electron microscope-analysis of the protrusions (knobs) present on the surface of Plasmodium falciparum-infected erythrocytes. J Cell Biol 97(3):795-802.
45. Quadt KA, et al. (2012) The density of knobs on Plasmodium falciparum-infected erythrocytes depends on developmental age and varies among isolates. PLoS One 7(9):e45658.
46. Mills JP, Qie L, Dao M, Lim CT, Suresh S (2004) Nonlinear elastic and viscoelastic deformation of the human red blood cell with optical tweezers. Mech Chem Biosyst 1(3): 169-180.
47. Dao M, Li J, Suresh S (2006) Molecularly based analysis of deformation of spectrin network and human erythrocyte. Mater Sci Eng C 26(8):1232-1244.
48. Chandramohanadas R, et al. (2009) Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells. Science 324(5928):794-797.
49. Chandramohanadas R, et al. (2011) Biophysics of malarial parasite exit from infected erythrocytes. PLoS One 6(6):e20869.
50. Glenister FK, Coppel RL, Cowman AF, Mohandas N, Cooke BM (2002) Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. Blood 99(3):1060-1063.
51. Waller KL, et al. (2003) Mature parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum binds to the 30-kDa domain of protein 4.1 in malariainfected red blood cells. Blood 102(5):1911-1914.
52. Sanyal S, et al. (2012) Plasmodium falciparum STEVOR proteins impact erythrocyte mechanical properties. Blood 119(2):e1-e8.
53. Ho M, White NJ (1999) Molecular mechanisms of cytoadherence in malaria. Am J Physiol 276(6 Pt 1):C1231-C1242.
54. Carvalho PA, Diez-Silva M, Chen H, Dao M, Suresh S (2013) Cytoadherence of erythrocytes invaded by Plasmodium falciparum: Quantitative contact-probing of a human malaria receptor. Acta Biomater 9(5):6349-6359.
55. Beeson JG, Chan JA, Fowkes FJI (2013) PfEMP1 as a target of human immunity and a vaccine candidate against malaria. Expert Rev Vaccines 12(2):105-108.