Molecular mechanistic insights into the endothelial receptor mediated cytoadherence of Plasmodium falciparum-infected erythrocytes

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Li, Ang ^a   Lim, Tong Seng ^b   Shi, Hui ^a   Yin, Jing ^d   Tan, Swee Jin ^e   Li, Zhengjun ^f   Low, Boon Chuan ^c,f   Tan, Kevin Shyong Wei ^c,d   Lim, Chwee Teck ^c,e,f  

^a SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^b AGENCY FOR SCIENCE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; THROMBOSPONDIN; PEPTIDE;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING KINETICS; CELL ADHESION; CONTROLLED STUDY; ERYTHROCYTE; HUMAN; HUMAN CELL; LIGAND BINDING; MALARIA FALCIPARUM; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; RECEPTOR AFFINITY; CONFOCAL MICROSCOPY; CYTOLOGY; ENDOTHELIUM CELL; KINETICS; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM; SPECTROSCOPY; TEMPERATURE;

PLASMODIUM FALCIPARUM;

ANTIGENS, CD36; CELL ADHESION; ENDOTHELIAL CELLS; ERYTHROCYTES; HUMANS; KINETICS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, CONFOCAL; PEPTIDES; PLASMODIUM FALCIPARUM; SPECTRUM ANALYSIS; TEMPERATURE; THROMBOSPONDINS;

EID: 79952781332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016929     Document Type: Article

References (53)

1. Bignami A, Bastianelli A, (1889) Observation of estivo-autumnal malaria. Riforma Medica 6: 1334-1335.
2. Miller LH, (1969) Distribution of mature trophozoites and schizonts of Plasmodium falciparum in the organs of Aotus trivirgatus, the night monkey. Am J Trop Med Hyg 18: 860-865.
3. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA, (1985) Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol 119: 385-401.
4. Aikawa M, Pongponratn E, Tegoshi T, Nakamura K, Nagatake T, et al. (1992) A study on the pathogenesis of human cerebral malaria and cerebral babesiosis. Mem Inst Oswaldo Cruz 87 (Suppl 3): 297-301.
5. Pongponratn E, Turner GD, Day NP, Phu NH, Simpson JA, et al. (2003) An ultrastructural study of the brain in fatal Plasmodium falciparum malaria. Am J Trop Med Hyg 69: 345-359.
6. Dondorp AM, Pongponratn E, White NJ, (2004) Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. Acta Tropica 89: 309-317.
7. O'Connell D, (2007) Malaria: Fatal attraction. Nat Rev Micro 5: 655-655.
8. Luse SA, Miller LH, (1971) Plasmodium falciparum malaria. Ultrastructure of parasitized erythrocytes in cardiac vessels. Am J Trop Med Hyg 20: 655-660.
9. Udeinya IJ, Schmidt JA, Aikawa M, Miller LH, Green I, (1981) Falciparum malaria-infected erythrocytes specifically bind to cultured human endothelial cells. Science 213: 555-557.
10. Li A, Mansoor AH, Tan KS, Lim CT, (2006) Observations on the internal and surface morphology of malaria infected blood cells using optical and atomic force microscopy. J Microbiol Methods 66: 434-439.
11. Nagao E, Kaneko O, Dvorak JA, (2000) Plasmodium falciparum-Infected Erythrocytes: Qualitative and Quantitative Analyses of Parasite-Induced Knobs by Atomic Force Microscopy. Journal of Structural Biology 130: 34-44.
12. Korn C, Schwarz US, (2006) Efficiency of initiating cell adhesion in hydrodynamic flow. Phys Rev Lett 97: 138103.
13. Cooke BM, Mohandas N, Coppel RL, (2001) The malaria-infected red blood cell: structural and functional changes. Adv Parasitol 50: 1-86.
14. Cooke BM, Berendt AR, Craig AG, MacGregor J, Newbold CI, et al. (1994) Rolling and stationary cytoadhesion of red blood cells parasitized by Plasmodium falciparum: separate roles for ICAM-1, CD36 and thrombospondin. Br J Haematol 87: 162-170.
15. Roberts DD, Sherwood JA, Spitalnik SL, Panton LJ, Howard RJ, et al. (1985) Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature 318: 64-66.
16. Barnwell JW, Asch AS, Nachman RL, Yamaya M, Aikawa M, et al. (1989) A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes. J Clin Invest 84: 765-772.
17. Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD, (1989) Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science 243: 1469-1471.
18. Berendt AR, Simmons DL, Tansey J, Newbold CI, Marsh K, (1989) Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature 341: 57-59.
19. Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV, (1995) Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes. J Exp Med 182: 15-20.
20. Dobrowsky TM, Zhou Y, Sun SX, Siliciano RF, Wirtz D, (2008) Monitoring early fusion dynamics of human immunodeficiency virus type 1 at single-molecule resolution. J Virol 82: 7022-7033.
21. Hinterdorfer P, Dufrene YF, (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat Meth 3: 347-355.
22. Bell GI, (1978) Models for the specific adhesion of cells to cells. Science 200: 618-627.
23. Evans E, Ritchie K, (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72: 1541-1555.
24. Riener CK, Stroh CM, Ebner A, Klampfl C, Gall AA, et al. (2003) Simple test system for single molecule recognition force microscopy. Analytica Chimica Acta 479: 59-75.
25. Bell GI, (1978) Models for the specific adhesion of cells to cells. Science 200: 618-627.
26. Benoit M, Gabriel D, Gerisch G, Gaub HE, (2000) Discrete interactions in cell adhesion measured by single-molecule force spectroscopy. Nat Cell Biol 2: 313-317.
27. Chen S, Springer TA, (1999) An automatic braking system that stabilizes leukocyte rolling by an increase in selectin bond number with shear. J Cell Biol 144: 185-200.
28. Merkel R, Nassoy P, Leung A, Ritchie K, Evans E, (1999) Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397: 50-53.
29. Evans E, (2001) Probing the relation between force-lifetime-and chemistry in single molecular bonds. Annu Rev Biophys Biomol Struct 30: 105-128.
30. Evans EA, Calderwood DA, (2007) Forces and bond dynamics in cell adhesion. Science 316: 1148-1153.
31. Perret E, Leung A, Feracci H, Evans E, (2004) Trans-bonded pairs of E-cadherin exhibit a remarkable hierarchy of mechanical strengths. Proc Natl Acad Sci U S A 101: 16472-16477.
32. Bayas MV, Leung A, Evans E, Leckband D, (2006) Lifetime measurements reveal kinetic differences between homophilic cadherin bonds. Biophys J 90: 1385-1395.
33. Ho M, White NJ, (1999) Molecular mechanisms of cytoadherence in malaria. Am J Physiol 276: C1231-1242.
34. Yipp BG, Hickey MJ, Andonegui G, Murray AG, Looareesuwan S, et al. (2007) Differential roles of CD36, ICAM-1, and P-selectin in Plasmodium falciparum cytoadherence in vivo. Microcirculation 14: 593-602.
35. Baruch DI, Ma XC, Singh HB, Bi X, Pasloske BL, et al. (1997) Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence. Blood 90: 3766-3775.
36. Cooke BM, Nash GB, (1995) Plasmodium falciparum: characterization of adhesion of flowing parasitized red blood cells to platelets. Exp Parasitol 80: 116-123.
37. Cooke BM, Nicoll CL, Baruch DI, Coppel RL, (1998) A recombinant peptide based on PfEMP-1 blocks and reverses adhesion of malaria-infected red blood cells to CD36 under flow. Mol Microbiol 30: 83-90.
38. Ockenhouse CF, Tandon NN, Jamieson GA, Greenwalt DE, (1993) Antigenic and functional differences in adhesion of Plasmodium falciparum-infected erythrocytes to human and bovine CD36. Infect Immun 61: 2229-2232.
39. Asch AS, Liu I, Briccetti FM, Barnwell JW, Kwakye-Berko F, et al. (1993) Analysis of CD36 binding domains: ligand specificity controlled by dephosphorylation of an ectodomain. Science 262: 1436-1440.
40. Daviet L, Buckland R, Puente Navazo MD, McGregor JL, (1995) Identification of an immunodominant functional domain on human CD36 antigen using human-mouse chimaeric proteins and homologue-replacement mutagenesis. Biochem J 305 (Pt 1): 221-224.
41. Baruch DI, Ma XC, Pasloske B, Howard RJ, Miller LH, (1999) CD36 peptides that block cytoadherence define the CD36 binding region for Plasmodium falciparum-infected erythrocytes. Blood 94: 2121-2127.
42. Eda S, Sherman IW, (2002) Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine. Cell Physiol Biochem 12: 373-384.
43. Winograd E, Eda S, Sherman IW, (2004) Chemical modifications of band 3 protein affect the adhesion of Plasmodium falciparum-infected erythrocytes to CD36. Mol Biochem Parasitol 136: 243-248.
44. Trager W, Jensen JB, (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
45. Lambros C, Vanderberg JP, (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
46. Baenziger NL, Majerus PW, (1974) Isolation of human platelets and platelet surface membranes. Methods Enzymol 31: 149-155.
47. Ribaut C, Berry A, Chevalley S, Reybier K, Morlais I, et al. (2008) Concentration and purification by magnetic separation of the erythrocytic stages of all human Plasmodium species. Malar J 7: 45.
48. Liu F, Burgess J, Mizukami H, Ostafin A, (2003) Sample preparation and imaging of erythrocyte cytoskeleton with the atomic force microscopy. Cell Biochemistry and Biophysics 38: 251-270.
49. Ebner A, Hinterdorfer P, Gruber HJ, (2007) Comparison of different aminofunctionalization strategies for attachment of single antibodies to AFM cantilevers. Ultramicroscopy 107: 922-927.
50. Hanley W, McCarty O, Jadhav S, Tseng Y, Wirtz D, et al. (2003) Single molecule characterization of P-selectin/ligand binding. J Biol Chem 278: 10556-10561.
51. Baumgartner W, Hinterdorfer P, Schindler H, (2000) Data analysis of interaction forces measured with the atomic force microscope. Ultramicroscopy 82: 85-95.
52. Hanley WD, Wirtz D, Konstantopoulos K, (2004) Distinct kinetic and mechanical properties govern selectin-leukocyte interactions. J Cell Sci 117: 2503-2511.
53. Panorchan P, Thompson MS, Davis KJ, Tseng Y, Konstantopoulos K, et al. (2006) Single-molecule analysis of cadherin-mediated cell-cell adhesion. J Cell Sci 119: 66-74.