Inward cholesterol gradient of the membrane system in P. falciparum-infected erythrocytes involves a dilution effect from parasite-produced lipids

Biology Open

Volumn 3, Issue 6, 2014, Pages 529-541

  Tokumasu, Fuyuki ^a,c   Crivat, Georgeta ^a,b   Ackerman, Hans ^a   Hwang, Jeeseong ^b   Wellems, Thomas E ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Detergent resistant membrane domain; Fluorescence lifetime imaging microscopy; Malaria; Maurer's cleft; Membrane rafts; Parasitophorous vacuole membrane; Plasmodium falciparum

Indexed keywords

EID: 84979071572     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20147732     Document Type: Article

References (101)

1. Aikawa, M. (1988). Morphological changes in erythrocytes induced by malarial parasites. Biol. Cell 64, 173-181.
2. Aikawa, M., Hepler, P. K., Huff, C. G. and Sprinz, H. (1966). The feeding mechanism of avian malarial parasites. J. Cell Biol. 28, 355-373.
3. Aikawa, M., Miller, L. H., Johnson, J. and Rabbege, J. (1978). Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J. Cell Biol. 77, 72-82.
4. Aikawa, M., Miller, L. H., Rabbege, J. R. and Epstein, N. (1981). Freeze-fracture study on the erythrocyte membrane during malarial parasite invasion. J. Cell Biol. 91, 55-62.
5. Aikawa, M., Uni, Y., Andrutis, A. T. and Howard, R. J. (1986). Membraneassociated electron-dense material of the asexual stages of Plasmodium falciparum: evidence for movement from the intracellular parasite to the erythrocyte membrane. Am. J. Trop. Med. Hyg. 35, 30-36.
6. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. and Walter, P. (2002). olecular Biology of the Cell. New York, NY: Garland Science. Allison, A. C. (1954). Protection afforded by sickle-cell trait against subtertian malareal infection. BMJ 1, 290-294.
7. Atkinson, C. T. and Aikawa, M. (1990). Ultrastructure of malaria-infected erythrocytes. Blood Cells 16, 351-368.
8. Besteiro, S., Vo Duy, S., Perigaud, C., Lefebvre-Tournier, I. and Vial, H. J. (2010). Exploring metabolomic approaches to analyse phospholipid biosynthetic pathways in Plasmodium. Parasitology 137, 1343-1356.
9. Bhattacharjee, S., van Ooij, C., Balu, B., Adams, J. H. and Haldar, K. (2008). aurer's clefts of Plasmodium falciparum are secretory organelles that concentrate virulence protein reporters for delivery to the host erythrocyte. Blood 111, 2418-2426.
10. Blackman, M. J. (2008). Malarial proteases and host cell egress: an 'emerging' cascade. Cell. Microbiol. 10, 1925-1934.
11. Brown, D. A. and London, E. (1998). Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol. 164, 103-114.
12. Chang, C. W., Sud, D. and Mycek, M. A. (2007). Fluorescence lifetime imaging microscopy. Methods Cell Biol. 81, 495-524.
13. Chen, Z. and Rand, R. P. (1997). The influence of cholesterol on phospholipid membrane curvature and bending elasticity. Biophys. J. 73, 267-276.
14. Chia, T. H., Williamson, A., Spencer, D. D. and Levene, M. J. (2008). ultiphoton fluorescence lifetime imaging of intrinsic fluorescence in human and rat brain tissue reveals spatially distinct NADH binding. Opt. Express 16, 4237-4249.
15. Cholera, R., Brittain, N. J., Gillrie, M. R., Lopera-Mesa, T. M., Diakité, S. A., Arie, T., Krause, M. A., Guindo, A., Tubman, A., Fujioka, H. et al. (2008). mpaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Proc. Natl. Acad. Sci. USA 105, 991-996.
16. Cowman, A. F., Berry, D. and Baum, J. (2012). The cellular and molecular basis for malaria parasite invasion of the human red blood cell. J. Cell Biol. 198, 961-971.
17. Cyrklaff, M., Sanchez, C. P., Kilian, N., Bisseye, C., Simpore, J., Frischknecht, F. and Lanzer, M. (2011). Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes. Science 334, 1283-1286.
18. de Jong, K., Larkin, S. K., Styles, L. A., Bookchin, R. M. and Kuypers, F. A. (2001). Characterization of the phosphatidylserine-exposing subpopulation of sickle cells. Blood 98, 860-867.
19. de Koning-Ward, T. F., Gilson, P. R., Boddey, J. A., Rug, M., Smith, B. J., Papenfuss, A. T., Sanders, P. R., Lundie, R. J., Maier, A. G., Cowman, A. F. et al. (2009). A newly discovered protein export machine in malaria parasites. Nature 459, 945-949.
20. Di Girolamo, F., Raggi, C., Birago, C., Pizzi, E., Lalle, M., Picci, L., Pace, T., Bachi, A., de Jong, J., Janse, C. J. et al. (2008). Plasmodium lipid rafts contain proteins implicated in vesicular trafficking and signalling as well as members of the PIR superfamily, potentially implicated in host immune system interactions. Proteomics 8, 2500-2513.
21. Diggs, C. L., Aikawa, M. and Haynes, J. D. (1977). Ultrastructure and viability of cryopreserved Plasmodium falciparum. Bull. World Health Organ. 55, 299-304.
22. Dluzewski, A. R., Zicha, D., Dunn, G. A. and Gratzer, W. B. (1995). Origins of the parasitophorous vacuole membrane of the malaria parasite: surface area of the parasitized red cell. Eur. J. Cell Biol. 68, 446-449.
23. Evans, E. A. and Mohandas, N. (1987). Membrane-associated sickle hemoglobin: a major determinant of sickle erythrocyte rigidity. Blood 70, 1443-1449.
24. Frankland, S., Adisa, A., Horrocks, P., Taraschi, T. F., Schneider, T., Elliott, S. R., Rogerson, S. J., Knuepfer, E., Cowman, A. F., Newbold, C. I. et al. (2006). Delivery of the malaria virulence protein PfEMP1 to the erythrocyte surface requires cholesterol-rich domains. Eukaryot. Cell 5, 849-860.
25. Grellier, P., Rigomier, D., Clavey, V., Fruchart, J. C. and Schrevel, J. (1991). Lipid traffic between high density lipoproteins and Plasmodium falciparuminfected red blood cells. J. Cell Biol. 112, 267-277.
26. Haldar, K. and Uyetake, L. (1992). The movement of fluorescent endocytic tracers in Plasmodium falciparum infected erythrocytes. Mol. Biochem. Parasitol. 50, 161-177.
27. Haldar, K., Samuel, B. U., Mohandas, N., Harrison, T. and Hiller, N. L. (2001). Transport mechanisms in Plasmodium-infected erythrocytes: lipid rafts and a tubovesicular network. Int. J. Parasitol. 31, 1393-1401.
28. Haldar, K., Mohandas, N., Samuel, B. U., Harrison, T., Hiller, N. L., Akompong, T. and Cheresh, P. (2002). Protein and lipid trafficking induced in erythrocytes infected by malaria parasites. Cell. Microbiol. 4, 383-395.
29. Ham, T. H., Sayre, R. W., Dunn, R. F. and Murphy, J. R. (1968). Physical properties of red cells as related to effects in vivo. II. Effect of thermal treatment on rigidity of red cells, stroma and the sickle cell. Blood 32, 862-871.
30. Hanssen, E., Sougrat, R., Frankland, S., Deed, S., Klonis, N., Lippincott-Schwartz, J. and Tilley, L. (2008). Electron tomography of the Maurer's cleft organelles of Plasmodium falciparum-infected erythrocytes reveals novel structural features. Mol. Microbiol. 67, 703-718.
31. Hanssen, E., Carlton, P., Deed, S., Klonis, N., Sedat, J., DeRisi, J. and Tilley, L. (2010). Whole cell imaging reveals novel modular features of the exomembrane system of the malaria parasite, Plasmodium falciparum. Int. J. Parasitol. 40, 123-134.
32. Harrison, T., Samuel, B. U., Akompong, T., Hamm, H., Mohandas, N., Lomasney, J. W. and Haldar, K. (2003). Erythrocyte G protein-coupled receptor signaling in malarial infection. Science 301, 1734-1736.
33. Hebbel, R. P. (1984). Erythrocyte autoxidation and the membrane abnormalities of sickle red cells. Prog. Clin. Biol. Res. 159, 219-225.
34. Hölttä-Vuori, M., Uronen, R. L., Repakova, J., Salonen, E., Vattulainen, I., Panula, P., Li, Z., Bittman, R. and Ikonen, E. (2008). BODIPY-cholesterol: a new tool to visualize sterol trafficking in living cells and organisms. Traffic 9, 1839-1849.
35. Holz, G. G., Jr. (1977). Lipids and the malarial parasite. Bull. World Health Organ. 55, 237-248.
36. Hsiao, L. L., Howard, R. J., Aikawa, M. and Taraschi, T. F. (1991). Modification of host cell membrane lipid composition by the intra-erythrocytic human malaria parasite Plasmodium falciparum. Biochem. J. 274, 121-132.
37. Hu, J., Shibata, Y., Zhu, P. P., Voss, C., Rismanchi, N., Prinz, W. A., Rapoport, T. A. and Blackstone, C. (2009). A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 138, 549-561.
38. Jackson, K. E., Klonis, N., Ferguson, D. J., Adisa, A., Dogovski, C. and Tilley, L. (2004). Food vacuole-associated lipid bodies and heterogeneous lipid environments in the malaria parasite, Plasmodium falciparum. Mol. Microbiol. 54, 109-122.
39. Jin, L., Millard, A. C., Wuskell, J. P., Clark, H. A. and Loew, L. M. (2005). Cholesterol-enriched lipid domains can be visualized by di-4-ANEPPDHQ with linear and nonlinear optics. Biophys. J. 89, L04-L06.
40. Keller, P. and Simons, K. (1998). Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140, 1357-1367.
41. Kilian, N., Dittmer, M., Cyrklaff, M., Ouermi, D., Bisseye, C., Simpore, J., Frischknecht, F., Sanchez, C. P. and Lanzer, M. (2013). Haemoglobin S and C affect the motion of Maurer's clefts in Plasmodium falciparum-infected erythrocytes. Cell. Microbiol. 15, 1111-1126.
42. Kriek, N., Tilley, L., Horrocks, P., Pinches, R., Elford, B. C., Ferguson, D. J., Lingelbach, K. and Newbold, C. I. (2003). Characterization of the pathway for transport of the cytoadherence-mediating protein, PfEMP1, to the host cell surface in malaria parasite-infected erythrocytes. Mol. Microbiol. 50, 1215-1227.
43. Kuypers, F. A. (2008). Red cell membrane lipids in hemoglobinopathies. Curr. Mol. Med. 8, 633-638.
44. Langreth, S. G. (1977). Electron microscope cytochemistry of host-parasite membrane interactions in malaria. Bull. World Health Organ. 55, 171-178.
45. Lauer, S., VanWye, J., Harrison, T., McManus, H., Samuel, B. U., Hiller, N. L., Mohandas, N. and Haldar, K. (2000). Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J. 19, 3556-3564.
46. Lauer, S. A., Chatterjee, S. and Haldar, K. (2001). Uptake and hydrolysis of sphingomyelin analogues in Plasmodium falciparum-infected red cells. Mol. Biochem. Parasitol. 115, 275-281.
47. Ledesma, M. D., Simons, K. and Dotti, C. G. (1998). Neuronal polarity: essential role of protein-lipid complexes in axonal sorting. Proc. Natl. Acad. Sci. USA 95, 3966-3971.
48. Li, Z. and Bittman, R. (2007). Synthesis and spectral properties of cholesterol- and FTY720-containing boron dipyrromethene dyes. J. Org. Chem. 72, 8376-8382.
49. Li, Z., Mintzer, E. and Bittman, R. (2006). First synthesis of free cholesterol-BODIPY conjugates. J. Org. Chem. 71, 1718-1721.
50. Lingwood, D. and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
51. Lucero, H. A. and Robbins, P. W. (2004). Lipid rafts-protein association and the regulation of protein activity. Arch. Biochem. Biophys. 426, 208-224.
52. Maier, A. G., Cooke, B. M., Cowman, A. F. and Tilley, L. (2009). Malaria parasite proteins that remodel the host erythrocyte. Nat. Rev. Microbiol. 7, 341-354.
53. Mantel, P. Y., Hoang, A. N., Goldowitz, I., Potashnikova, D., Hamza, B., Vorobjev, I., Ghiran, I., Toner, M., Irimia, D., Ivanov, A. R. et al. (2013). Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe 13, 521-534.
54. Marsh, D. (2009). Cholesterol-induced fluid membrane domains: a compendium of lipid-raft ternary phase diagrams. Biochim. Biophys. Acta 1788, 2114-2123.
55. Marsh, D. and Smith, I. C. (1973). An interacting spin label study of the fluidizing and condensing effects of cholesterol on lecithin bilayers. Biochim. Biophys. Acta 298, 133-144.
56. Marti, M., Good, R. T., Rug, M., Knuepfer, E. and Cowman, A. F. (2004). Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306, 1930-1933.
57. Mayor, S. and Maxfield, F. R. (1995). Insolubility and redistribution of GPIanchored proteins at the cell surface after detergent treatment. Mol. Biol. Cell 6, 929-944.
58. Mayor, S., Sabharanjak, S. and Maxfield, F. R. (1998). Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J. 17, 4626-4638.
59. McLaren, D. J., Bannister, L. H., Trigg, P. I. and Butcher, G. A. (1979). Freeze fracture studies on the interaction between the malaria parasite and the host erythrocyte in Plasmodium knowlesi infections. Parasitology 79, 125-139.
60. Mikkelsen, R. B., Kamber, M., Wadwa, K. S., Lin, P. S. and Schmidt-Ullrich, R. (1988). The role of lipids in Plasmodium falciparum invasion of erythrocytes: a coordinated biochemical and microscopic analysis. Proc. Natl. Acad. Sci. USA 85, 5956-5960.
61. Miller, L. H., Aikawa, M., Johnson, J. G. and Shiroishi, T. (1979). Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J. Exp. Med. 149, 172-184.
62. Mishra, S. and Joshi, P. G. (2007). Lipid raft heterogeneity: an enigma. J. Neurochem. 103 Suppl. 1:, 135-142.
63. Mitchell, G. H. and Bannister, L. H. (1988). Malaria parasite invasion: interactions with the red cell membrane. Crit. Rev. Oncol. Hematol. 8, 255-310.
64. Murphy, S. C., Samuel, B. U., Harrison, T., Speicher, K. D., Speicher, D. W., Reid, M. E., Prohaska, R., Low, P. S., Tanner, M. J., Mohandas, N. et al. (2004). Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection. Blood 103, 1920-1928.
65. Murphy, S. C., Hiller, N. L., Harrison, T., Lomasney, J. W., Mohandas, N. and Haldar, K. (2006). Lipid rafts and malaria parasite infection of erythrocytes. Mol. Membr. Biol. 23, 81-88.
66. Murphy, S. C., Fernandez-Pol, S., Chung, P. H., Prasanna Murthy, S. N., Milne, S. B., Salomao, M., Brown, H. A., Lomasney, J. W., Mohandas, N. and Haldar, K. (2007). Cytoplasmic remodeling of erythrocyte raft lipids during infection by the human malaria parasite Plasmodium falciparum. Blood 110, 2132-2139.
67. Nyasae, L. K., Hubbard, A. L. and Tuma, P. L. (2003). Transcytotic efflux from early endosomes is dependent on cholesterol and glycosphingolipids in polarized hepatic cells. Mol. Biol. Cell 14, 2689-2705.
68. Obaid, A. L., Loew, L. M., Wuskell, J. P. and Salzberg, B. M. (2004). Novel naphthylstyryl-pyridium potentiometric dyes offer advantages for neural network analysis. J. Neurosci. Methods 134, 179-190.
69. Orädd, G., Lindblom, G. and Westerman, P. W. (2002). Lateral diffusion of cholesterol and dimyristoylphosphatidylcholine in a lipid bilayer measured by pulsed field gradient NMR spectroscopy. Biophys. J. 83, 2702-2704.
70. Owen, D. M., Lanigan, P. M., Dunsby, C., Munro, I., Grant, D., Neil, M. A., French, P. M. and Magee, A. I. (2006). Fluorescence lifetime imaging provides enhanced contrast when imaging the phase-sensitive dye di-4-ANEPPDHQ in model membranes and live cells. Biophys. J. 90, L80-L82.
71. Palacpac, N. M., Hiramine, Y., Mi-ichi, F., Torii, M., Kita, K., Hiramatsu, R., Horii, T. and Mitamura, T. (2004). Developmental-stage-specific triacylglycerol biosynthesis, degradation and trafficking as lipid bodies in Plasmodium falciparum-infected erythrocytes. J. Cell Sci. 117, 1469-1480.
72. Pan, J., Tristram-Nagle, S. and Nagle, J. F. (2009). Effect of cholesterol on structural and mechanical properties of membranes depends on lipid chain saturation. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 80, 021931.
73. Park, S. H. and Blackstone, C. (2010). Further assembly required: construction and dynamics of the endoplasmic reticulum network. EMBO Rep. 11, 515-521.
74. Pouvelle, B., Spiegel, R., Hsiao, L., Howard, R. J., Morris, R. L., Thomas, A. P. and Taraschi, T. F. (1991). Direct access to serum macromolecules by intraerythrocytic malaria parasites. Nature 353, 73-75.
75. Presti, F. (1985). The role of cholesterol in regulating membrane fluidity. In Cellular Aspects (ed. J. Boggs and R. Aloia), pp. 97-146. New York, NY: Academic Press.
76. Procino, G., Barbieri, C., Carmosino, M., Rizzo, F., Valenti, G. and Svelto, M. (2010). Lovastatin-induced cholesterol depletion affects both apical sorting and endocytosis of aquaporin-2 in renal cells. Am. J. Physiol. 298, F266-F278.
77. Regev-Rudzki, N., Wilson, D. W., Carvalho, T. G., Sisquella, X., Coleman, B. M., Rug, M., Bursac, D., Angrisano, F., Gee, M., Hill, A. F. et al. (2013). Cell-cell communication between malaria-infected red blood cells via exosomelike vesicles. Cell 153, 1120-1133.
78. Samuel, B. U., Mohandas, N., Harrison, T., McManus, H., Rosse, W., Reid, M. and Haldar, K. (2001). The role of cholesterol and glycosylphosphatidylinositolanchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J. Biol. Chem. 276, 29319-29329.
79. Schreier-Muccillo, S., Marsh, D., Dugas, H., Schneider, H. and Smith, C. P. (1973). A spin probe study of the influence of cholesterol on motion and orientation of phospholipids in oriented multibilayers and vesicles. Chem. Phys. Lipids 10, 11-27.
80. Setty, B. N., Kulkarni, S. and Stuart, M. J. (2002). Role of erythrocyte phosphatidylserine in sickle red cell-endothelial adhesion. Blood 99, 1564-1571.
81. Shaw, J. E., Epand, R. F., Epand, R. M., Li, Z., Bittman, R. and Yip, C. M. (2006). Correlated fluorescence-atomic force microscopy of membrane domains: structure of fluorescence probes determines lipid localization. Biophys. J. 90, 2170-2178.
82. Sherman, I. W. (1979). Biochemistry of Plasmodium (malarial parasites). Microbiol. Rev. 43, 453-495.
83. Simons, K. and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
84. Song, J. and Waugh, R. E. (1993). Bending rigidity of SOPC membranes containing cholesterol. Biophys. J. 64, 1967-1970.
85. Spycher, C., Rug, M., Klonis, N., Ferguson, D. J., Cowman, A. F., Beck, H. P. and Tilley, L. (2006). Genesis of and trafficking to the Maurer's clefts of Plasmodium falciparum-infected erythrocytes. Mol. Cell. Biol. 26, 4074-4085.
86. Stewart, M. J., Schulman, S. and Vanderberg, J. P. (1986). Rhoptry secretion of membranous whorls by Plasmodium falciparum merozoites. Am. J. Trop. Med. Hyg. 35, 37-44.
87. Suss-Toby, E., Zimmerberg, J. and Ward, G. E. (1996). Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc. Natl. Acad. Sci. USA 93, 8413-8418.
88. Taraschi, T. F., O'Donnell, M., Martinez, S., Schneider, T., Trelka, D., Fowler, V. M., Tilley, L. and Moriyama, Y. (2003). Generation of an erythrocyte vesicle transport system by Plasmodium falciparum malaria parasites. Blood 102, 3420-3426.
89. Tarun, A. S., Vaughan, A. M. and Kappe, S. H. (2009). Redefining the role of de novo fatty acid synthesis in Plasmodium parasites. Trends Parasitol. 25, 545-550.
90. Tilley, L., Sougrat, R., Lithgow, T. and Hanssen, E. (2008). The twists and turns of Maurer's cleft trafficking in P. falciparum-infected erythrocytes. Traffic 9, 187-197.
91. Tokumasu, F., Jin, A. J., Feigenson, G. W. and Dvorak, J. A. (2003). Nanoscopic lipid domain dynamics revealed by atomic force microscopy. Biophys. J. 84, 2609-2618.
92. Tokumasu, F., Nardone, G. A., Ostera, G. R., Fairhurst, R. M., Beaudry, S. D., Hayakawa, E. and Dvorak, J. A. (2009). Altered membrane structure and surface potential in homozygous hemoglobin C erythrocytes. PLoS ONE 4, e5828.
93. Trelka, D. P., Schneider, T. G., Reeder, J. C. and Taraschi, T. F. (2000). Evidence for vesicle-mediated trafficking of parasite proteins to the host cell cytosol and erythrocyte surface membrane in Plasmodium falciparum infected erythrocytes. Mol. Biochem. Parasitol. 106, 131-145.
94. van Munster, E. B. and Gadella, T. W. (2005). Fluorescence lifetime imaging microscopy (FLIM). Adv. Biochem. Eng. Biotechnol. 95, 143-175.
95. van Ooij, C., Withers-Martinez, C., Ringel, A., Cockcroft, S., Haldar, K. and Blackman, M. J. (2013). Identification of a Plasmodium falciparum phospholipid transfer protein. J. Biol. Chem. 288, 31971-31983.
96. Vial, H. J., Ancelin, M. L., Philippot, J. R. and Thuet, M. J. (1990). Biosynthesis and dynamics of lipids in Plasmodium-infected mature mammalian erythrocytes. Blood Cells 16, 531-555, discussion 556-561.
97. Vial, H. J., Mamoun, C. and Sherman, I. W. (2005). Plasmodium lipids: metabolism and function. In Molecular Approaches to Malaria, pp. 327-352. Washington, DC: ASM Press.
98. Wang, W. Q. and Gustafson, A. (1994). Erythrocyte lipid extraction in alcohol-chloroform systems: a comparative study. Acta Chem. Scand. 48, 753-758.
99. Ward, G. E., Miller, L. H. and Dvorak, J. A. (1993). The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes. J. Cell Sci. 106, 237-248.
100. Weber, P., Wagner, M. and Schneckenburger, H. (2010). Fluorescence imaging of membrane dynamics in living cells. J. Biomed. Opt. 15, 046017.
101. Yam, X. Y., Birago, C., Fratini, F., Di Girolamo, F., Raggi, C., Sargiacomo, M., Bachi, A., Berry, L., Fall, G., Currà, C. et al. (2013). Proteomic analysis of detergent-resistant membrane microdomains in trophozoite blood stage of the human malaria parasite Plasmodium falciparum. Mol. Cell. Proteomics 12, 3948-3961.