Abstract
We examined the ability of Melanesian ovalocytes from Papua New Guinea to be deformed in order to probe the resistance of these cells to invasion by several species of malaria parasite. We found ovalocytes were refractile to drug-induced endocytosis, that they formed abnormal rouleaux, showed reduced deformability when aspirated into 0.6-micron diameter pores in polycarbonate sieves, and failed to crenate when mounted under a glass coverslip. No substantial differences were found between normocytes and ovalocytes in their initial rate of filtration through 4.5-micron pore polycarbonate sieves, their membrane fluidity as measured by the rate of depolarization of fluorescent probes or the rate of extraction of cytoskeletal proteins in low ionic strength buffers. We conclude that the resistance of ovalocytes to undergo localized deformation might be significant in explaining the resistance of these cells to invasion by malarial merozoites.
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- Aikawa M., Miller L. H., Johnson J., Rabbege J. Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J Cell Biol. 1978 Apr;77(1):72–82. doi: 10.1083/jcb.77.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bashford C. L., Morgan C. G., Radda G. K. Measurement and interpretation of fluorescence polarisations in phospholipid dispersions. Biochim Biophys Acta. 1976 Mar 5;426(2):157–172. doi: 10.1016/0005-2736(76)90329-1. [DOI] [PubMed] [Google Scholar]
- Ben-Bassat I., Bensch K. G., Schrier S. L. Drug-induced erythrocyte membrane internalization. J Clin Invest. 1972 Jul;51(7):1833–1844. doi: 10.1172/JCI106985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Booth P. B., Serjeantson S., Woodfield D. G., Amato D. Selective depression of blood group antigens associated with hereditary ovalocytosis among melanesians. Vox Sang. 1977;32(2):99–110. doi: 10.1111/j.1423-0410.1977.tb00612.x. [DOI] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
- Castelino D., Saul A., Myler P., Kidson C., Thomas H., Cooke R. Ovalocytosis in Papua New Guinea -- dominantly inherited resistance to malaria. Southeast Asian J Trop Med Public Health. 1981 Dec;12(4):549–555. [PubMed] [Google Scholar]
- Ginn F. L., Hochstein P., Trump B. F. Membrane alterations in hemolysis: Internalization of plasmalemma induced by primaquine. Science. 1969 May 16;164(3881):843–845. doi: 10.1126/science.164.3881.843. [DOI] [PubMed] [Google Scholar]
- Greenwalt T. J., Lau F. O., Swierk E. M., Williams R. E. Studies of erythrocyte membrane loss produced by amphipathic drugs and in vitro storage. Br J Haematol. 1978 Aug;39(4):551–557. doi: 10.1111/j.1365-2141.1978.tb03625.x. [DOI] [PubMed] [Google Scholar]
- Gregersen M. I., Bryant C. A., Hammerle W. E., Usami S., Chien S. Flow Characteristics of Human Erythrocytes through Polycarbonate Sieves. Science. 1967 Aug 18;157(3790):825–827. doi: 10.1126/science.157.3790.825. [DOI] [PubMed] [Google Scholar]
- Hadley T., Saul A., Lamont G., Hudson D. E., Miller L. H., Kidson C. Resistance of Melanesian elliptocytes (ovalocytes) to invasion by Plasmodium knowlesi and Plasmodium falciparum malaria parasites in vitro. J Clin Invest. 1983 Mar;71(3):780–782. doi: 10.1172/JCI110827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill J. S., Sawyer W. H., Howlett G. J., Wiley J. S. Hereditary spherocytosis of man. Altered binding of cytoskeletal components to the erythrocyte membrane. Biochem J. 1982 Feb 1;201(2):259–266. doi: 10.1042/bj2010259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holt M., Hogan P. F., Nurse G. T. The ovalocytosis polymorphism on the western border of Papua, New Guinea. Hum Biol. 1981 Feb;53(1):23–34. [PubMed] [Google Scholar]
- Howard R. J., Sawyer W. H. Changes in the membrane microviscosity of mouse red blood cells infected with Plasmodium berghei detected using n-(9-anthroyloxy) fatty acid fluorescent probes. Parasitology. 1980 Apr;80(2):331–342. doi: 10.1017/s0031182000000792. [DOI] [PubMed] [Google Scholar]
- Kidson C., Lamont G., Saul A., Nurse G. T. Ovalocytic erythrocytes from Melanesians are resistant to invasion by malaria parasites in culture. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5829–5832. doi: 10.1073/pnas.78.9.5829. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koeweiden E., Ponnudurai T., Meuwissen J. H. In vitro observations on hereditary spherocytosis and malaria. Trans R Soc Trop Med Hyg. 1979;73(5):589–590. doi: 10.1016/0035-9203(79)90061-0. [DOI] [PubMed] [Google Scholar]
- Leblond P. F., Coulombe L. The measurement of erythrocyte deformability using micropore membranes. A sensitive technique with clinical applications. J Lab Clin Med. 1979 Jul;94(1):133–143. [PubMed] [Google Scholar]
- Lux S. E., Wolfe L. C. Inherited disorders of the red cell membrane skeleton. Pediatr Clin North Am. 1980 May;27(2):463–486. doi: 10.1016/s0031-3955(16)33862-7. [DOI] [PubMed] [Google Scholar]
- Mohandas N., Clark M. R., Jacobs M. S., Shohet S. B. Analysis of factors regulating erythrocyte deformability. J Clin Invest. 1980 Sep;66(3):563–573. doi: 10.1172/JCI109888. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakashima K., Beutler E. Effect of anti-spectrin antibody and ATP on deformability of resealed erythrocyte membranes. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3823–3825. doi: 10.1073/pnas.75.8.3823. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakashima K., Beutler E. Erythrocyte cellular and membrane deformability in hereditary spherocytosis. Blood. 1979 Mar;53(3):481–485. [PubMed] [Google Scholar]
- Olson J. A., Kilejian A. Involvement of spectrin and ATP in infection of resealed erythrocyte ghosts by the human malarial parasite, Plasmodium falciparum. J Cell Biol. 1982 Dec;95(3):757–762. doi: 10.1083/jcb.95.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Penniston J. T., Vaughan L., Nakamura M. Endocytosis in erythrocytes and ghosts: occurrence at 0 degrees C after ATP preincubation. Arch Biochem Biophys. 1979 Dec;198(2):339–348. doi: 10.1016/0003-9861(79)90506-x. [DOI] [PubMed] [Google Scholar]
- Schmid-Schönbein H., Gaehtgens P. What is red cell deformability? Scand J Clin Lab Invest Suppl. 1981;156:13–26. doi: 10.3109/00365518109097425. [DOI] [PubMed] [Google Scholar]
- Schrier S. L., Ben-Bassat I., Bensch K., Seeger M., Junga I. Erythrocyte membrane vacuole formation in hereditary spherocytosis. Br J Haematol. 1974 Jan;26(1):59–69. doi: 10.1111/j.1365-2141.1974.tb00449.x. [DOI] [PubMed] [Google Scholar]
- Schrier S. L., Hardy B., Bensch K. G. Endocytosis in erythrocytes and their ghosts. Prog Clin Biol Res. 1979;30:437–449. [PubMed] [Google Scholar]
- Sewchand L. S., Canham P. B. Modes of rouleaux formation of human red blood cells in polyvinylpyrrolidone and dextran solutions. Can J Physiol Pharmacol. 1979 Nov;57(11):1213–1222. doi: 10.1139/y79-183. [DOI] [PubMed] [Google Scholar]
- Sheetz M. P., Singer S. J. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4457–4461. doi: 10.1073/pnas.71.11.4457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shinitzky M., Barenholz Y. Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim Biophys Acta. 1978 Dec 15;515(4):367–394. doi: 10.1016/0304-4157(78)90010-2. [DOI] [PubMed] [Google Scholar]
- Thulborn K. R., Sawyer W. H. Properties and the locations of a set of fluorescent probes sensitive to the fluidity gradient of the lipid bilayer. Biochim Biophys Acta. 1978 Aug 4;511(2):125–140. doi: 10.1016/0005-2736(78)90308-5. [DOI] [PubMed] [Google Scholar]
- Thulborn K. R., Tilley L. M., Sawyer W. H., Treloar F. E. The use of n-(9-anthroyloxy) fatty acids to determine fluidity and polarity gradients in phospholipid bilayers. Biochim Biophys Acta. 1979 Dec 4;558(2):166–178. doi: 10.1016/0005-2736(79)90057-9. [DOI] [PubMed] [Google Scholar]