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Lipid peroxidation of erythrocytes during anemia of the hamsters infected withLeishmania donovani

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Abstract

Visceral leishmaniasis has been found to be associated with severe anemia and premature lysis of erythrocytes. Peroxidative damage of red cells has been noted in several hemolytic anemias. Present study shows enhanced formation of methemoglobin in hamsters infected withLeishmania donovani. Increased formation of malonyldialdehyde and diene conjugate has been noted in the erythrocytes of the infected animals with the progress of anemia. Results showed decreased activities of protective enzymes like superoxide dismutase, catalase and glutathione reductase against peroxidative attack. An increase in the membrane cholesterol/phospholipid ratio and a decrease in membrane fluidity of erythrocytes were observed under the diseased condition. Densitometric scan after SDS-PAGE of red cell membrane of the infected animals revealed significant degradation of band 3 and band 4.1 proteins. The results suggest that alteration in the membrane may lead to reduced life span of the red cells in experimental visceral leishmaniasis.

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References

  1. Knight R, Woodruff AW, Pettitt LE. The mechanism of anemia in kala-azar. Trans Royal Soc Trop Med Hyg 61: 701–705, 1967

    Google Scholar 

  2. Weed RI, Reed CF. Membrane alterations leading to red cell destruction. Am Jr Med 41: 681–698, 1966

    Google Scholar 

  3. Cartwright GE, Chung HL, Chang A. Studies on pancytopenia of kala-azar. Blood 3: 249–275, 1948

    Google Scholar 

  4. Biswas T, Chakraborty M, Naskar K, Ghosh DK, Ghosal J. Anemia in experimental visceral leishmaniasis in hamsters. J Parasitol 78: 140–142 1992

    Google Scholar 

  5. Cronkite EP. Blood and Lymph. In: J.R. Brobeck (ed.) Physiological Basis of Medical Practice, Section 4. The Williams and Wilkins Company, Baltimore, 1973, pp 1–129

    Google Scholar 

  6. Woodruff AW, Topley E, Knight R, Cambell Downie GB. The anemia of kala-azar. Brit J Hematol 22: 319–329, 1972

    Google Scholar 

  7. Fletcher KA, Maegraith BG. Erythrocyte reduced glutathione in malaria (Plasmodium berghei andPlasmodium knowlesi). Anals Trop Med Parasitol 64: 481–486, 1970

    Google Scholar 

  8. Sherman IW. Membrane structure and function of malaria parasites and infected erythrocyte. Parasitology 91: 609–645, 1985

    Google Scholar 

  9. Manson-Bahr PEC, Bell DR. Manson's Tropical Disease, 19th ed. Balliere Tindall: ELBS, 1987, pp 87–113

    Google Scholar 

  10. Rosse WF. Quantitative immunology of immune hemolytic anemia II. The relationship of cell bound antibody to hemolysis and the effect of treatment. J Clin Invest 50: 734–743, 1971

    Google Scholar 

  11. Lamola AA, Piomeilli S, Puh-Fitzpatrick MB, Yamane T, Harber LC. Erythropoietic protoporphyria and lead intoxication; the molecular basis for difference in cutaneous photosensitivity. J Clin Invest 56: 1528–1535, 1975

    Google Scholar 

  12. Lux SE, John MM, Karnovsky J. Irreversible deformation of the spectrin actin lattice in irreversibly sickled cells. J Clin Invest 58: 955–963, 1976

    Google Scholar 

  13. Etkin NL, Eaton JW. Malaria induced erythrocyte oxidant sensitivity. In: G.J. Brewer (ed.) Erythrocyte Structure and Metabolism. A Liss Inc, New York, 1975, pp 219–232

    Google Scholar 

  14. Friedman M, Roth E, Nagel R, Truger W. Plasmodium falciparum: physiological interactions with the human sickle cell. Exp Parasitol 47: 73–80, 1979

    Google Scholar 

  15. Ghosh AK, Ghosh DK. Infection pattern of leishmaniasis in hamsters produced by recent isolates from kala-azar patients in India. Indian J Med Res 86: 14–19, 1987

    Google Scholar 

  16. Varley H. In: Practical Clinical Biochemistry, 3rd ed. William Heinemann Medical Books Ltd and Interscience Books Inc, New York, 1962, p 494

    Google Scholar 

  17. Evelyn KA, Malloy IIT. Microdetermination of oxyhemoglobin, methemoglobin and sulfhemoglobin in a single sample of blood. J Biol Chem 126: 655–662, 1938

    Google Scholar 

  18. Dahle LK, Hill EG, Holman RT. The thiobarbituric acid reaction and autoxidation of polyunsaturated fatty acid methyl esters. Arch Biochem Biophys 98: 253–261, 1962

    Google Scholar 

  19. Wills ED. Evaluation of lipid peroxidation in lipids and biological membranes. In: K. Snell, B. Mullock (eds) Biochemical Toxicology a Practical Approach IRL Press, Oxford, Washington DC, 1987, pp 127–152.

    Google Scholar 

  20. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47: 469–474, 1974

    Google Scholar 

  21. Beers RF, Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195: 133–140, 1952

    Google Scholar 

  22. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70: 158–169, 1967

    Google Scholar 

  23. Staal GEJ, Visser J, Veeger C. Purification and properties of glutathione reductase of human erythrocytes. Biochim Biophys Acta 185: 39–48, 1969

    Google Scholar 

  24. Marks PA, Gelhorn A, Kidson C. Lipid synthesis in human leukocytes, platelets and erythrocytes. J Biol Chem 235: 2579–2583, 1960

    Google Scholar 

  25. Dodge JT, Mitchell C, Hanahan DJ. The preparation and chemical characteristics of hemoglobin free ghosts of human erythrocytes. Arch Biochem Biophys 100: 119–130, 1963

    Google Scholar 

  26. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685, 1970

    Google Scholar 

  27. Shinitzky M, Barenholz Y. Dynamics of the hydrocarbon layer in liposomes of lecithin and sphingomyelin containing dicetylphosphate. J Biol Chem 249: 2652–2657, 1974

    Google Scholar 

  28. Shinitzky M, Inbar M. Microviscosity parameters and protein mobility in biological membranes. Biochim Biophys Acta 433: 133–149, 1976

    Google Scholar 

  29. Folch J, Less M, Stanely GHS. A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 226: 497–509, 1957

    Google Scholar 

  30. Lowry OM, Rosebrough IJ, Farr AL, Randal RJ. Protein measurement with folin phenol reagent. J Biol Chem 193: 265–275, 1951

    Google Scholar 

  31. Ames BN, Duben DL. The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid. J Biol Chem 235: 769–775, 1960

    Google Scholar 

  32. Abell LL, Levy BB, Brodie BB, Kendal FE. A simplified method for the estimation of total cholesterol in serum and demonstration of its specificity. J Biol Chem 195: 357–366, 1952

    Google Scholar 

  33. Bray RS. Leishmaniasis in the old world. Brit Med Bull 28: 39–43, 1972

    Google Scholar 

  34. Misra HL, Fridovich I. The generation of superoxide radical during the autoxidation of hemoglobin. J Biol Chem 247: 6960–6962, 1972

    Google Scholar 

  35. Weaver R, Oudega B, Van Gelder BF. Generation of superoxide radicals during the autoxidation of mammalian oxyhemoglobin. Biochim Biophys Acta 303: 475–478, 1973

    Google Scholar 

  36. Thomas MJ, Mehl KS, Pryor WA. The role of the superoxide anion in the xanthie oxidase induced autoxidation of linoleic acid. Biochem Biophys Res Commun 83: 927–932, 1978

    Google Scholar 

  37. Fridovich I. Superoxide dismutase. Ann Rev Biochem 44: 147–159, 1975

    Google Scholar 

  38. Jacob HS, Ingbar SH, Jandl JH. Oxidative hemolysis and erythrocyte metabolism in hereditary a catalasia. J Clin Invest 44: 1187–1199, 1965

    Google Scholar 

  39. Little C, O'Brien PJ. An intracellular GSH peroxidase with a lipid peroxide substrate. Biochem Biophys Res Commun 31: 145–150, 1968

    Google Scholar 

  40. Beutler E. Drug induced hemolytic anemia. Pharmacol Rev 21: 73–97, 1969

    Google Scholar 

  41. Christopherson BO. Reduction of linolenic acid hydroperoxide by a glutathione peroxidase. Biochim Biophys Acta 176: 463–470, 1969

    Google Scholar 

  42. Haest CWM, Plasa G, Kamp D, Deuticke B. Spectrin as a stabilizer of the phospholipid asymmetry in the human erythrocyte membrane. Biochim Biophys Acta 589: 21–32, 1978

    Google Scholar 

  43. Rice-Evans C, Hochstein P. Alterations in erythrocyte membrane fluidity by phenylhydrazine induced peroxidation of lipids. Biochem Biophys Res Commun 100: 1537–1542, 1981

    Google Scholar 

  44. Shinitzky M, Inbar M. Difference in microviscosity induced by different cholesterol levels in the surface membrane lipid layer of normal lymphocytes and malignant lymphoma cells. J Mol Biol 85: 603–615, 1974

    Google Scholar 

  45. Van Blitterswijk WJ, Van Hoeven RP, Vander Meer BW. Lipid structural order parameters (reciprocal of fluidity) in biomembranes derived from the state fluorescence polarization measurements. Biochim Biophys Acta 644: 323–332, 1981

    Google Scholar 

  46. Jain SK. The accumulation of malonyldialdehyde a product of fatty acid peroxidation, can disturb aminophospholipid organization in the membrane bilayer of human erythrocytes. J Biol Chem 259: 3391–3394, 1984

    Google Scholar 

  47. Gupta CM, Mishra GC. Transbilayer phospholipid assymetry inPlasmodium knowlesi infected host cell membrane. Science 212: 1047–1049, 1981

    Google Scholar 

  48. Hunt JV, Simpson JA, Dean RT. Hydroperoxide mediated fragmentation of proteins. Biochem J 250: 87–93, 1988

    Google Scholar 

  49. Fowler V, Taylor DL. Spectrin plus band 4.1 crosslink actin. J Cell Biol 85: 361–376, 1980

    Google Scholar 

  50. Ungewickel E, Gratzer WB. Self association of human spectrin. Eur J Biochem 88: 379–385, 1978

    Google Scholar 

  51. Liu SC, Palek J. Spectrin tetramer-dimer equilibrium and the stability of erythrocyte membrane skeleton. Nature 285: 586–588, 1980

    Google Scholar 

  52. Chakrabarti S, Naik AA, Reddy GR. Phenylhydrazine mediated degradation of bovine serum albumin and membrane proteins of human erythrocytes. Biochim Biophys Acta 1028: 89–94, 1990

    Google Scholar 

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Presented in part: 61st AGB Meeting of Society of Biological Chemists (India), Hyderabad, December, 1992

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Biswas, T., Pal, J.K., Naskar, K. et al. Lipid peroxidation of erythrocytes during anemia of the hamsters infected withLeishmania donovani . Mol Cell Biochem 146, 99–105 (1995). https://doi.org/10.1007/BF00944601

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