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Magnetic resonance studies of the pathophysiology of murine malaria

Published online by Cambridge University Press:  17 March 2009

Roxanne Deslauriers ,
Yves Geoffrion ,
Keith W. Butler  and
Ian C. P. Smith
Roxanne Deslauriers
Affiliation:
Division of Biological Sciences, National Research Council of Canada, Ottawa, Ontario, CanadaK1A OR6
Yves Geoffrion
Affiliation:
Division of Biological Sciences, National Research Council of Canada, Ottawa, Ontario, CanadaK1A OR6
Keith W. Butler
Affiliation:
Division of Biological Sciences, National Research Council of Canada, Ottawa, Ontario, CanadaK1A OR6
Ian C. P. Smith
Affiliation:
Division of Biological Sciences, National Research Council of Canada, Ottawa, Ontario, CanadaK1A OR6
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Extract

The non-invasive and non-destructive aspects of NMR and ESR spectroscopy have prompted a variety of research on the pathophysiological impact of murine malaria. NMR is unique in its ability to monitor intracellular pH non-invasively in a heterogeneous sample, a compartmentalized cell and in a whole organism. It has also been shown to be sensitive to unusual structures and metabolic products in free-living protozoa such as Acanthamoeba (Deslauriers et al. 1982a) and Tetrahymena (Deslauriers et al. 1982b; Jarrell et al. 1981). Using the appropriate spin probe, ESR can give valuable information on membrane structure (Schreier, Polnaszek & Smith; 1978). It is particularly useful when quantities of material are limited.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 18 , Issue 1 , February 1985 , pp. 65 - 110
Copyright
Copyright © Cambridge University Press 1985

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References

REFERENCES

Ackerman, J. J. H., Grove, T. H., Wong, G. G., Gadian, D. G. & Radda, G. K. (1980). Mapping of metabolites in whole animals by 31P NMR using surface coils. Nature 283, 167–170.Google Scholar
Allred, D. R., Sterling, C. R., & Morse, P. D. (1983). Increased fluidity of Plasmodium berghei-infected mouse red blood cell membranes detected by electron spin resonance spectroscopy. Mol. Biochem. Parasit 7, 27–39.Google Scholar
Alvares, A. P., Ueng, T-H., Scheibel, L. W. & Hollingdale, M. R. (1984). Impairment of hepatic cytochrome P-450-dependent mono-oxygenases by the malaria parasite Plasmodium berghei. Mol. Biochem. Parasit 13, 277–282.CrossRefGoogle Scholar
Assimacopoulos-Jeannet, F., Exton, J. H. & Jeanreaud, B. (1973). Control of gluconeogenesis and glyconeogenesis in perfused livers of normal mice. Am. J. Physiol. 225, 25–32.Google Scholar
Backer, J. M., Dubker, V. G., Eremenko, S. I. & Molin, Yu. N. (1977). Detection of the kinetics of biochemical reactions with oxygen using exchange broadening in the ESR spectra of nitroxide radicals. Biochim. biophys. Acta 460, 152–156.Google Scholar
Barzu, O. (1978). Spectrophotometric assay of oxygen consumption. Meth. Enzym. 485–498.Google Scholar
Berliner, J. J. (ed.) (1976). Spin Labeling. New York: Academic Press.Google Scholar
Bligh, E. G. & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917.CrossRefGoogle ScholarPubMed
Bossi, L., Alema, S., Calissano, P. & Marra, E. (1975). Interaction of different forms of haemoglobin with artificial lipid membranes. Biochim. biophys. Acta 375, 477–482.CrossRefGoogle ScholarPubMed
Brown, F. F. & Campbell, I. D. (1980). NMR studies of red cells. Phil. Trans. R. Soc. Land. B 289, 395–406.Google Scholar
Butler, K. W., Deslauriers, R. & Smith, I. C. P. (1984). Plasmodium berghei: electron spin resonance and lipid analysis of infected mouse erythrocyte membranes. Expl. Parasit 57, 178–184.CrossRefGoogle ScholarPubMed
Cameron, D. G. & Moffatt, D. J. (1984). Deconvolution, derivation and smoothing of spectra using Fourier transforms. J. Testing Eval. 12, 78–85.Google Scholar
Chongsuphajaisiddhi, T. (1981). Pathophysiology of malaria. Southeast Asian J. trop. Med. pubi. Hlth. 12, 298–307.Google ScholarPubMed
Chupin, V. V., Ushakova, I. P., Bondarenko, S. V., Vasilenko, I. A., Serebrennikova, G. A., Evstigneeva, R. P., Rosenberg, G. Ya. & Kol'Tsova, G. N. (1983). A study of the interaction of methemoglobin with model membranes by 31P NMR spectroscopy. Bioorganicheskaya Khimiya 8, 1275–1280.Google Scholar
Cohen, S. M., Shulman, R. G. & McLaughlin, A. C. (1979). Effects of ethanol on alanine metabolism in perfused mouse liver studied by 13C NMR. Proc. Natn. Acad. Sci. U.S.A. 76, 4808–4812.CrossRefGoogle Scholar
Cohen, S. M. & Shulman, R. G. (1980). 13C NMR studies of gluconeo-genesis in rat liver suspensions and perfused mouse livers. Phil. Trans. R. Soc. Land. B 289, 407–411.Google Scholar
Coleman, R. N., Reincricca, N. J., Ritterhaus, C. W. & Brissette, W. H. (1976). Malaria: decreased survival of transfused normal erythrocytes in infected rats. J. Parasit 62, 318–340.Google Scholar
Costello, A. J. R., Marshall, W. E., Omachi, A. & Henderson, T. O. (1976). Interactions between haemoglobin and organic phosphates investigated with 31P nuclear magnetic resonance spectroscopy and ultrafiltration. Biochim. biophys. Acta 427, 481–491.CrossRefGoogle ScholarPubMed
Cullis, P. R. (1976). Hydrocarbon phase transitions, heterogeneous lipid distributions and lipid-protein interactions in erythrocyte membranes. FEBS Lett. 68, 173–176.Google Scholar
Deas, J. E., Alder, K. A. & Wilson, L. A. (1981). Effect of Plasmodium berghei on membranes of murine erythrocytes. Am. J. Trop. Med. Hyg. 30, 544–554.CrossRefGoogle ScholarPubMed
Deschênes, J., Valet, J. P. & Marceau, J. P. (1980). Hepatocytes from newborn and weanling rats in monolayer culture: isolation by perfusion, fibronectin-mediated adhesion, spreading, and functional activities. In Vitro 16, 722–730.Google Scholar
Deslauriers, R., Byrd, R. A., Jarrell, H. C. & Smith, I. C. P. (1982 a). NMR studies of differentiation in Acanthamoeba castellanii. In Non Invasive Probes of Tissue Metabolism (ed. Cohen, J. S.), pp. 49–78. New York: Wiley.Google Scholar
Deslauriers, R., Ekiel, I., Byrd, A., Jarrell, H. C., & Smith, I. C. P. (1982 b). A 31P NMR study of structural and functional aspects of phosphonate and phosphate distribution in Tetrahymena. Biochim. biophys. Acta 720, 329–7.CrossRefGoogle ScholarPubMed
Deslauriers, R., Ekiel, I., Kroft, T. & Smith, I. C. P. (1982 c). NMR studies of malaria. 31P nuclear magnetic resonance of blood from mice infected with Plasmodium berghei. Biochim. biophys. Acta 721, 449–457.CrossRefGoogle ScholarPubMed
Deslauriers, R., Ekiel, I., Kroft, T., Léveillé, L. & Smith, I. C. P. (1983). Glycolysis in red cells of mice infected with Plasmodium berghei and the effects thereon of antimalarial drugs. Tetrahedron 39, 3543–3548.Google Scholar
Dodge, J. T., Mitchell, C. & Hannahan, D. J. (1963). The preparation and chemical characteristics of haemoglobin-free ghosts of human erythrocytes. Archs Biochem. Biophys. 100, 119–130.Google Scholar
Exton, J. H. & Park, C. R. (1967). Control of gluconeogenesis in liver. J. biol. Chem. 242, 2622–2636.Google Scholar
Fabry, M. E. (1980). Detection of haemoglobin S polymerization in intact red cells by 31P- NMR Biochim. biophys. Res. Commun. 97, 1399–1406.Google Scholar
Fabry, M. E. & San George, R. C.(1983). Effect of magnetic susceptibility on nuclear magnetic resonance signals arising from red cells: a warning. Biochemistry 22, 4119–425.CrossRefGoogle ScholarPubMed
Folch, J., Lees, M. & Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipides from animal tissue. J. biol. Chem. 226, 497–509.Google Scholar
Fossel, E. T. & Solomon, A. K. (1976). Modulation of 2,3 diphospho-glycerate 31P-NMR resonance position by red cell membrane shape. Biochim. biophys. Acta 436, 5005–511.Google Scholar
Friedan, M. J., Roth, E. F., Nagel, R. L. & Trager, W. (1979). Plasmodium falciparium: physiological interactions with the human sickle cell. Expl. Parasit. 47, 73–80.CrossRefGoogle Scholar
Gadian, D. G. (1982). Nuclear Magnetic Resonance and Its Applications to Living Systems. Oxford: Clarendon Press.Google Scholar
Garnham, P. C. C. (1966). Rodent species of malarial parasites. In Malarial Parasites and Other Haemosporidia, pp. 431–459. Oxford: Blackwell.Google Scholar
Geoffrion, Y., Butler, K., Pass, M., Smith, I. C. P. & Deslauriers, R. (1985 b). Plasmodium berghei: gluconeogenesis in the infected mouse liver studied by 13C nuclear magnetic resonance. Expl. Parasit. 59, 369–374.Google Scholar
Geoffrion, Y., Lareau, S., Deslauriers, R., Butler, K., Pass, M. & Smith, I. C. P. (1985 a). A versatile perfusion technique for metabolic studies by NMR. Mag. Res. Med. 2, 65–72.Google Scholar
Gupta, R. K., Benovic, J. & Rose, Z. B. (1978).The determination of the free magnesium level in the human red blood cell by 31P NMR. J. biol. Chem. 253, 6172–6176.CrossRefGoogle Scholar
Gonzales-Mendez, R., Wemmer, D., Hahn, G., Wade-Jardetzky, N. & Jardetzky, O. (1982). Continuous-flow NMR culture system for mammalian cells. Biochim. biophys. Acta 720, 274–280.CrossRefGoogle Scholar
Harris, R. K. & Mann, B. E. (ed.). (1978). NMR and the Periodic Table. New York: Academic Press.Google Scholar
Hems, R., Ross, B. D., Berry, M. N. & Krebs, H. A. (1966). Gluconeogenesis in perfused rat liver. Biochem. J. 101, 284–292.Google Scholar
Herlitz, H. & Hultborn, R. (1974). A microspectrophotometric technique for determination of respiration in comparison to the Cartesian diver method – respiratory activity of rat corpus luteum cells with reference to substrate. Acta physiol. scand. 90, 594–601.Google Scholar
Homewood, C. A. & Neame, K. D. (1980). Biochemistry of malarial parasites. In Malaria vol. 1, (ed.). Kreier, J. P., pp. 345–405. New York: Academic Press.Google Scholar
Hubbell, W. L. & McConnell, H. M. (1971). Molecular motion in spin-labelled phospholipids and membranes. J. Am. chem. Soc. 93, 314–326.Google Scholar
Hultborn, R. (1972). A sensitive method for measuring oxygen consumption. Analyt. Biochemistry 47, 442–450.Google Scholar
Hultborn, R. & Hyden, H. (1974). Microspectrophotometric determination of nerve cell respiration at high potassium concentration. Expl. Cell. Res. 87, 346–350.Google Scholar
Iles, R. A. & Griffiths, J. R. (1982). Hepatic metabolism by 31P NMR. Biosci. Rep. 2, 735–742.CrossRefGoogle Scholar
Iles, R. A., Griffiths, J. R., Stevens, A. N., Gadian, D. G., Porteous, R. (1980). Effects of fructose on the energy metabolism and acid-base status of the perfused starved-rat liver. Biochem. J. 192, 191–202.Google Scholar
Iles, R. A., Stevens, A. N., & Griffiths, J. R. (1982). NMR studies of metabolites in living tissues. Prog. nucl. magn. Reson. Spectrosc. 15, 49–200.CrossRefGoogle Scholar
Jarrell, H. C., Byrd, R. A., Deslauriers, R., Ekiel, I. & Smith, I. C. P. (1981). Characterization of the phase behaviour of phosphonplipids in model and biological membranes by 31P-NMR. Biochim. biophys. Acta 648, 80–86.CrossRefGoogle Scholar
Jones, A. W.(1967).Introduction to Parasitology, p. 458. Reading: Addison-Wesley, 458.Google Scholar
Van Kampen, E. J. & Zijlstra, W. G. (1965). Determination of haemoglobin and its derivatives. Adv. Clin. Chem. 8, 141–187.Google Scholar
Kauppinen, J. K., Moffatt, D. J., Mantsch, H. H., & Cameron, D. G. (1981 a). Fourier self-deconvolution: a method for resolving intrinsically overlapped bands. Appl. Spectrosc. 35, 271–276.Google Scholar
Kauppinen, J. K., Moffat, D. J., Mantsch, H. H. & Cameron, D. G. (1981 b). Fourier transforms in the computation of self-deconvoluted and first order derivative spectra of overlapped band contours. Analyt. Chem. 53, 1454–1457.Google Scholar
Kauppinen, J. K., Moffatt, D. J., Mantsch, H. H. & Cameron, D. G. (1982). Smoothing of spectral data in the Fourier domain. Appl. Opt. 21, 1866–1872.Google Scholar
Krebs, H. A. & Henseleit, K. (19832). Untersuchungen über die Harn-stoffbildung im Tierkörper. Hoppe-Seyler's Z. physiol. Chem. 210, 33–66.CrossRefGoogle Scholar
Krishna, S., Shoubridge, E. A., White, N. J., Weatherall, D. J. & Radda, G. K. (1983). Plasmodium yoelii: blood oxygenation and brain function in the infected mouse. Expl. Parasit. 56, 391–396.Google Scholar
Kruckeberg, W. C., Sander, B. J. & Sullivan, D. C. (1981). Plasmodium berghei: glycolytic enzymes of the infected mouse erythrocyte. Expl. Parasitol. 54, 438–443.Google Scholar
Labotka, R. J., & Honig, G. R. (1980). 31P-NMR spectroscopy of erythrocytes in congenital hemolytic anemias: detection of heterogeneous erythrocyte populations and quantification of intracellular 2,3-diphosphoglycerate. Am. J. Hematol. 9, 55–65.Google Scholar
Lai, C. S., Hopewood, L. E., Hyde, J. S. & Lukiewicz, S. (1982). ESR studies of O2 uptake by Chinese hamster ovary cells during the cell cycle. Proc. Natn. Acad. Sci. U.S.A. 79, 1166–1170.Google Scholar
Lam, Y. F., Lin, A. K. L. & Ho, C. (1979). A phosphorus-31 nuclear magnetic resonance investigation of intracellular environment in human normal and sickle cell blood. Blood 54, 196–209.Google Scholar
McLaughlin, A. C., Takeda, H. & Chance, B. (1978). In Frontiers of Biological Energetics, (ed. Dutton, P. L., Leigh, J. S. and Scarpa, A.), vol. II, pp. 1351–1356. New York: Academic Press.Google Scholar
McLaughlin, A. C., Takeda, H. & Chance, B. (1979). Rapid ATP assays in perfused mouse liver by 31P NMR. Proc. Natn. Acad. Set. U.S.A. 76, 5445–5449.Google Scholar
Maegraith, B. G. (1981). Aspects of the pathogenesis of malaria. Southeast Asian J. trop. Med. publ, Hlth. 12, 251–261.Google Scholar
Maegraith, B., & Fletcher, A. (1972). The pathogenesis of mammalian malaria. Adv. Parasit. 10, 49–57.Google Scholar
Marshall, W. E., Costello, A. J. R., Henderson, T. O. & Omachi, A. (1977). Organic phosphate binding to haemoglobin in intact human erythrocytes determined by 31P nuclear magnetic resonance spectro-scopy. Biochim. biophys. Acta 490, 290–300.CrossRefGoogle Scholar
Moon, R. B. & Richards, J. H. (1973). Determination of intracellular pH by 31P magnetic resonance. J. biol. Chem. 248, 7276–7278.CrossRefGoogle ScholarPubMed
Nair, C. R., Gupta, P. H., Chauhan, D. P., Bhatia, A. & Vinayak, V. K. (1981). A study on the mechanism of impared oxidative drug metabolism in experimental malaria in mice. Indian J. med. Res. 74, 829–835.Google Scholar
Navon, G., Ogawa, S., Shulman, R. G. & Yamane, T. (1977). 31P nuclear magnetic resonance studies of Erlich ascites tumor cells. Proc. Natn. Acad. Sci. U.S.A. 74, 87–91.CrossRefGoogle Scholar
Neame, K. D. & Homewood, C. A. (1975). Alterations in the permeability of mouse erythrocytes infected with the malaria parasite, Plasmodium berghei. Int. J. Parasit. 5, 537–540.Google Scholar
Nickell, S. P., Scheibel, L. W. & Cole, G. A. (1982). Inhibition by cyclosporin A of rodent malaria in vivo and human malaria in vitro. Infect. and Immun. 37, 1093–1100.Google Scholar
Oelshlegel, F. H. & Sullivan, D. C. (1978). Glycerol kinase and glycerol metabolism in Plasmodium berghei. Fed Proc. 37, 1847.Google Scholar
Oelshlegel, F. J., & Brewer, G. J. (1975). The Red Blood Cell, vol. 2 (ed. Surgenor, D. MacN.), pp. 1263–1302. New York: Academic Press.Google Scholar
Owen, J. A., Tasker, R. A. R. & Nakatsu, K. (1984). A simple, less stressful rat restrainer. Experientia 40, 306–308.Google Scholar
Pass, M., Geoffrion, Y., Deslauriers, R., Butler, K. & Smith, I. C. P. (1984). Use of 13C NMR spectroscopy for the evaluation of hepatic drug-metabolizing enzyme activity in perfused mouse livers. J. Biochem. biophys. Methods 10, 135–142.Google Scholar
Pryor, W. A. (ed.) (1976). Free Radicals in Biology. New York: Academic Press.Google Scholar
Range, M. & Byrd, R. A. (1983). Obtaining high-fidelity spin-1/2 powder spectra in anisotropic media: phase-cycled Hahn echo spectrosopy. J. Magn. Reson. 522, 221–240.Google Scholar
Refsum, H. E. & Sveinsson, S. L. (1956). Spectrophotometric determination of haemoglobin oxygen saturation in haemolyzed whole blood. Scand. J. Clinical Lab. Invest. 8, 67–70.Google Scholar
Rigdon, R. H. (1942). A consideration of the mechanism of death in acute Plasmodium falciparum infection; report of a case. Am. J. Hyg. 36, 269–275.Google Scholar
Riley, M. V. & Deegan, T. (1960). The effect of Plasmodium berghei malaria on mouse-liver mitochondria. Biochem. J. 76, 41–44.Google Scholar
Riley, M. V. & Maegraith, B. G. (1961). A factor in the serum of malaria-infected animals capable of inhibiting the in vitro oxidative metabolism of normal liver mitochondria. Ann. trop. Med. Parasit. 55, 489–497.Google Scholar
Riley, M. V. & Maegraith, B. G. (1962). Changes in the metabolism of liver mitochondria of mice infected with rapid acute Plasmodium berghei malaria. Ann. trop. Med. Parasit. 56, 473–482.Google Scholar
Ross, B. D. (1972). Perfusion Techniques in Biochemistry. Oxford: Clarendon Press.Google Scholar
Sander, B. J. & Kruckeberg, W. C. (1981). Plasmodium berghei: glycolytic intermediate concentrations of the infected mouse erythrocyte. Expl. Parasitol. 52, 1–8.Google Scholar
Sander, B. J., Lowery, M. S. & Kruckeberg, W. C. (1981). Glycolytic metabolism in malaria infected red cells. In The Red Cell: Fifth Ann. Arbor. Conference, pp. 469–483. New York: Alan R. Liss.Google Scholar
Sarna, T., Duleba, A., Korytowski, W. & Swartz, H. (1980). Interaction of melanin with oxygen. Archs. Biochem. Biophys. 200, 140–148.Google Scholar
Scheibel, L. W. (1984). In vitro inhibition of the human malarial parasite by selected lipophilic chelators in the red cell. In The Red Cell: Sixth Ann. Arbor. Conference, pp. 377–394. New York: A. R. Liss.Google Scholar
Schreier, S., Polnaszek, C. F. & Smith, I. C. P. (1978). Spin labels in membranes: problems in practice. Biochem. biophys. Acta 515, 375–436.Google Scholar
Seed, T. M., Brindley, D., Aikawa, M. & Rabbege, J. (1976). Plasmodium berghei: osmotic fragility of malarial parasites and mouse host eryth-rocytes. Expl. Parasit. 40, 380–390.Google Scholar
Sherrat, H. S. A. (1981). Short-term Regulation of Liver Metabolism, (ed. Hue, L. and van de Werve, G.), pp. 199–227. New York: Elsevier North-Holland.Google Scholar
Smith, I. C. P. & Ekiel, I. H. (1984). Phosphorus-31 NMR of phospho-lipids in membranes. Phosphorus-31 NMR Principles and Applications (ed. Gorenstein, D.), pp. 447–475. New York: Academic Press.Google Scholar
Srivastava, S. K., Lal, A. K. & Ansari, N. H. (1980). Defence system of red cells against oxidative damage. Red Blood Cells and Lens Metabolism (ed. Srivastava, S. K.), ed. 123–137. New York: Elsevier/North Holland.Google Scholar
Styles, P., Grathwohl, C. & Brown, F. F. (1979). Simultaneous multinuclear NMR by alternate scan recording of 31P and 13C spectra. J. Magn. Reson. 35, 329–336.Google Scholar
Tehrani, A. Y., Lam, Y. F., Lin, A. K. L. C., Dosch, S. F. & Ho, C. (1982). Phosphorous-31 nuclear magnetic resonance studies of human red blood cells. Blood Cells 8, 245–261.Google Scholar
Thommen-Scott, K. (1981). The antimalarial activity of cyclosporin A. Agents and Actions 11, 770–773.Google Scholar
Thulborn, K. R. & Radda, G. C. (1981). Correlation of oxygen consumption with energy metabolism by in vivo nuclear magnetic resonance (NMR). J. Cereb. Flow Metab. 1, 582–583.Google Scholar
Thulborn, K. R., Soffe, N. F. & Radda, G. K. (1981). Simultaneous in vivo measurement of oxygen utilization and high-energy phosphate metabolism in rabbit skeletal muscle by multinuclear 1H and 31P NMR. J. Magn. Reson. 45, 362–366.Google Scholar
Vincke, I. H. & Lips, M. (1948). Un nouveau Plasmodium d'un rongeur sauvage du Congo. Annls. Soc. belg, Méd. trop. 28, 97–104.Google Scholar
Waddell, W. J. & Bates, R. J. (1969). Intracellular pH. Physiol. Rev. 49, 285–329.Google Scholar
Williams, C. A. & Chase, M. W. (1967). Methods in Immunology and Immunochemistry, vol. 1, New York: Academic Press.Google Scholar
Zijlstra, W. G. & Mullar, C. J. (1957). Spectrophotometry of solutions containing three components with special reference to the simultaneous determination of carboxyhaemoglobin and methaemoglobin in human blood. Clinica chim. Acta 2, 237–245.Google Scholar
Zukerman, A. (1957). Blood loss and replacement in plasmodial infections, I. Plasmodium berghei in untreated rats of varying age and in adult rats with erythropoietic mechanisms manipulated before innoculation. J. infect. Dis. 10, 172–206.Google Scholar