Hemoglobin serves to protect Plasmodium parasites from nitric oxide and reactive oxygen species

Journal of Investigative Medicine

Volumn 53, Issue 5, 2005, Pages 246-252

  Sobolewski, Peter ^a   Gramaglia, Irene ^a   Frangos, John A ^a   Intaglietta, Marcos ^a   Van Der Heyde, Henri C ^a  

^a LA JOLLA BIOENGINEERING INSTITUTE   (United States)

Author keywords

Hemoglobin; Malaria; Nitric oxide; Plasmodium; Reactive oxygen species

Indexed keywords

HEMOGLOBIN; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

CHEMICAL REACTION; ERYTHROCYTE; IMMUNE RESPONSE; MALARIA; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PLASMODIUM; REVIEW;

PLASMODIUM PARASITES;

EID: 23744434278     PISSN: 17088267     EISSN: None     Source Type: Journal    
DOI: 10.2310/6650.2005.53507     Document Type: Review

References (77)

1. Breman JG, Egan A, Keusch GT. The intolerable burden of malaria: a new look at the numbers. Am J Trop Med Hyg 2001;64:iv-vii.
2. Breman JG. The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am J Trop Med Hyg 2001;64:1-11.
3. Krogstad DJ. Malaria. In: Guerrant RL, Walker DH, Weller PF, editors. Tropical infectious diseases, principles, pathogens, and practice. Philadelphia: Churchill Livingstone; 1999. p.736-66.
4. Jensen JB, Boland MT, Akood M. Induction of crisis forms in cultured Plasmodium falciparum with human immune serum from Sudan. Science 1982;216:1230-3.
5. Taylor-Robinson AW, Phillips RS, Severn A, et al. The role of TH1 and TH2 cells in a rodent malaria infection. Science 1993;260:1931-4.
6. Grisham MB, Jourd'Heuil D, Wink DA. Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites: implications in inflammation. Am J Physiol 1999;276:G315-21.
7. Bredt DS, Snyder SH. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 1990;87:682-5.
8. Green SJ, Scheller LF, Marietta MA, et al. Nitric oxide: cytokine-regulation of nitric oxide in host resistance to intracellular pathogens. Immunol Lett 1994;43:87-94.
9. Pollock JS, Forstermann U, Mitchell JA, et al. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc Natl Acad Sci U S A 1991;88:10480-4.
10. Feelisch M, Stamler JS. Methods in nitric oxide research. Chichester (UK): John Wiley and Sons; 1996.
11. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J 1992;6:3051-64.
12. Babior BM. NADPH oxidase. Curr Opin Immunol 2004;16:42-7.
13. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001;2:907-16.
14. Favre N, Ryffel B, Rudin W. Parasite killing in murine malaria does not require nitric oxide production. Parasitology 1999;118(Pt2):139-43.
15. Yoneto T, Yoshimoto T, Wang CR, et al. Gamma interferon production is critical for protective immunity to infection with blood-stage Plasmodium berghei XAT but neither NO production nor NK cell activation is critical. Infect Immun 1999;67:2349-56.
16. van der Heyde HC, Gu Y, Zhang Q, et al. Nitric oxide is neither necessary nor sufficient for resolution of Plasmodium chabaudi malaria in mice. J Immunol 2000;165:3317-23.
17. Cavacini LA, Guidotti M, Parke LA, et al. Reassessment of the role of splenic leukocyte oxidative activity and macrophage activation in expression of immunity to malaria. Infect Immun 1989;57:3677-82.
18. Sanni LA, Fu S, Dean RT, et al. Are reactive oxygen species involved in the pathogenesis of murine cerebral malaria? J Infect Dis 1999;179:217-22.
19. Winslow RM. aa-Crosslinked hemoglobin: was failure predicted by preclinical testing? Vox Sang 2000;79:1-20.
20. Alayash AI. Oxygen therapeutics: can we tame haemoglobin? Nat Rev Drug Discov 2004;3:152-9.
21. Kerger H, Saltzman DJ, Menger MD, et al. Systemic and subcutaneous microvascular Po2 dissociation during 4-h hemorrhagic shock in conscious hamsters. Am J Physiol 1996;270:H827-36.
22. Liu X, Miller MJ, Joshi MS, et al. Diffusion-limited reaction of free nitric oxide with erythrocytes. J Biol Chem 1998;273:18709-13.
23. McMahon TJ, Pawloski JR, Hess DT, et al. S-Nitrosohemoglobin is distinguished from other nitrosovasodilators by unique oxygen-dependent responses that support an allosteric mechanism of action. Blood 2003;102:410-1.
24. McMahon TJ, Moon RE, Luschinger BP, et al. Nitric oxide in the human respiratory cycle. Nat Med 2002;8:711-7.
25. Winterbourn CC. Oxidative reactions of hemoglobin. Methods Enzymol 1990;186:265-72.
26. Romero N, Radi R, Linares E, et al. Reaction of human hemoglobin with peroxynitrite. Isomerization to nitrate and secondary formation of protein radicals. J Biol Chem 2003;278:44049-57.
27. Alayash AI. Oxidative mechanisms of hemoglobin-based blood substitutes. Artif Cells Blood Substit Immobil Biotechnol 2001;29:415-25.
28. Faivre B, Menu P, Labrude P, et al. Hemoglobin autooxidation/oxidation mechanisms and methemoglobin prevention or reduction processes in the bloodstream. Literature review and outline of autooxidation reaction. Artif Cells Blood Substit Immobil Biotechnol 1998;26:17-26.
29. Nagababu E, Rifkind JM. Heme degradation during autoxidation of oxyhemoglobin. Biochem Biophys Res Commun 2000;273:839-45.
30. Alayash AI, Patel RP, Cashon RE. Redox reactions of hemoglobin and myoglobin: biological and toxicological implications. Antioxid Redox Signal 2001;3:313-27.
31. Sadrzadeh SM, Graf E, Panter SS, et al. Hemoglobin. A biologic Fenton reagent. J Biol Chem 1984;259:14354-6.
32. Van Dyke BR, Saltman P. Hemoglobin: a mechanism for the generation of hydroxyl radicals. Free Radic Biol Med 1996;20:985-9.
33. Gutteridge JM. Iron promoters of the Fenton reaction and lipid peroxidation can be released from haemoglobin by peroxides. FEBS Lett 1986;201:291-5.
34. Puppo A, Halliwell B. Formation of hydroxyl radicals from hydrogen peroxide in the presence of iron. Is haemoglobin a biological Fenton reagent? Biochem J 1988;249:185-90.
35. Cosby K, Partovi KS, Crawford JH, et al. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 2003;9:1498-505.
36. Nagababu E, Ramasamy S, Abernethy DR, et al. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J Biol Chem 2003;278:46349-56.
37. Clark IA, Chaudhri G, Cowden WB. Some roles of free radicals in malaria. Free Radic Biol Med 1989;6:315-21.
38. Balagopalakrishna C, Manoharan PT, Abugo OO, et al. Production of superoxide from hemoglobin-bound oxygen under hypoxic conditions. Biochemistry 1996;35:6393-8.
39. Fairfield AS, Meshnick SR, Eaton JW. Malaria parasites adopt host cell superoxide dismutase. Science 1983;221:764-6.
40. Fairfield AS, Abosch A, Ranz A, et al. Oxidant defense enzymes of Plasmodium falciparum. Mol Biochem Parasitol 1988;30:77-82.
41. Weiss L, Geduldig U, Weidanz W. Mechanisms of splenic control of murine malaria: reticular cell activation and the development of a blood-spleen barrier. Am J Anat 1986;176:251-85.
42. Nalwaya N, Deen WM. Analysis of the effects of nitric oxide and oxygen on nitric oxide production by macrophages. J Theor Biol 2004;226:409-19.
43. Kuchan MJ, Frangos JA. Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. Am J Physiol 1994;266:C628-36.
44. Kharitonov VG, Sundquist AR, Sharma VS. Kinetics of nitric oxide autoxidation in aqueous solution. J Biol Chem 1994;269:5881-3.
45. Bishop JJ, Nance PR, Popel AS, et al. Erythrocyte margination and sedimentation in skeletal muscle venules. Am J Physiol Heart Circ Physiol 2001;281:H951-8.
46. Vaughn MW, Kuo L, Liao JC. Estimation of nitric oxide production and reaction rates in tissue by use of a mathematical model. Am J Physiol 1998;274:H2163-76.
47. Nalwaya N, Deen WM. Peroxynitrite exposure of cells cocultured with macrophages. Ann Biomed Eng 2004;32:664-76.
48. Prada J, Graninger W, Lehman LG, et al. Upregulation of ICAM-1, IL-1 and reactive oxygen intermediates (ROI) by exogenous antigens from Plasmodium falciparum parasites in vitro, and of sICAM-1 in the acute phase of malaria. J Chemother 1995;7:424-6.
49. Chiwakata CB, Hemmer CJ, Dietrich M. High levels of inducible nitric oxide synthase mRNA are associated with increased monocyte counts in blood and have a beneficial role in Plasmodium falciparum malaria. Infect Immun 2000;68:394-9.
50. Goldring JP, Nemaorani S. Antimalarial drugs modulate the expression of monocyte receptors. Int J Immunopharmacol 1999;21:599-607.
51. Burgner D, Xu W, Rockett K, et al. Inducible nitric oxide synthase polymorphism and fatal cerebral malaria. Lancet 1998;352:1193-4.
52. Kun JF, Mordmuller B, Lell B, et al. Polymorphism in promoter region of inducible nitric oxide synthase gene and protection against malaria. Lancet 1998;351:265-6.
53. Kun JF, Mordmuller B, Perkins DJ, et al. Nitric oxide synthase 2 (Lambarene) (G-954C), increased nitric oxide production, and protection against malaria. J Infect Dis 2001;184:330-6.
54. Hobbs MR, Udhayakumar V, Levesque MC, et al. A new NOS2 promoter polymorphism associated with increased nitric oxide production and protection from severe malaria in Tanzanian and Kenyan children. Lancet 2002;360:1468-75.
55. Ohashi J, Naka I, Patarapotikul J, et al. Significant association of longer forms of CCTTT microsatellite repeat in the inducible nitric oxide synthase promoter with severe malaria in Thailand. J Infect Dis 2002;186:578-81.
56. Levesque MC, Hobbs MR, Anstey NM, et al. Nitric oxide synthase type 2 promoter polymorphisms, nitric oxide production, and disease severity in Tanzanian children with malaria. J Infect Dis 1999;180:1994-2002.
57. Mombo LE, Ntoumi F, Bisseye C, et al. Human genetic polymorphisms and asymptomatic Plasmodium falciparum malaria in Gabonese schoolchildren. Am J Trop Med Hyg 2003;68:186-90.
58. Boutlis CS, Tjitra E, Maniboey H, et al. Nitric oxide production and mononuclear cell nitric oxide synthase activity in malaria-tolerant Papuan adults. Infect Immun 2003;71:3682-9.
59. Serirom S, Raharjo WH, Chotivanich K, et al. Anti-adhesive effect of nitric oxide on Plasmodium falciparum cytoadherence under flow. Am J Pathol 2003;162:1651-60.
60. Reiter CD, Wang X, Tanus-Santos JE, et al. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat Med 2002;8:1383-9.
61. Gyan B. Troye-Blomberg M, Perlmann P, et al. Human monocytes cultured with and without interferon-gamma inhibit Plasmodium falciparum parasite growth in vitro via secretion of reactive nitrogen intermediates. Parasite Immunol 1994;16:371-5.
62. Rockett KA, Awburn MM, Cowden WB, et al. Killing of Plasmodium falciparum in vitro by nitric oxide derivatives. Infect Immun 1991;59:3280-3.
63. Ockenhouse CF, Schulman S, Shear HL. Oxidative killing of malaria parasites by mononuclear phagocytes. Prog Clin Biol Res 1984;155:93-108.
64. Ockenhouse CF, Schulman S, Shear HL. Induction of crisis forms in the human malaria parasite Plasmodium falciparum by gamma-interferon-activated, monocyte-derived macrophages. J Immunol 1984;133:1601-8.
65. Pritsche G, Larcher C, Schennach H, et al. Regulatory interactions between iron and nitric oxide metabolism for immune defense against Plasmodium falciparum infection. J Infect Dis 2001;183:1388-94.
66. van der Heyde HC, Elloso MM, vande WJ, et al. Use of hydroethidine and flow cytometry to assess the effects of leukocytes on the malarial parasite Plasmodium falciparum. Clin Diagn Lab Immunol 1995;2:417-25.
67. Gillman BM, Batchelder J, Flaherty P, et al. Suppression of Plasmodium chabaudi parasitemia is independent of the action of reactive oxygen intermediates and/or nitric oxide. Infect Immun 2004;72:6359-66.
68. Jacobs P, Radzioch D, Stevenson MM. Nitric oxide expression in the spleen, but not in the liver, correlates with resistance to blood-stage malaria in mice. J Immunol 1995;155:5306-13.
69. Schofield L, Hackett F. Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J Exp Med 1993;177:145-53.
70. Krishnegowda G, Hajjar AM, Zhu J, et al. Induction of proinflammatory responses in macrophages by the glycosylphos phatidylinositols (GPIs) of Plasmodium falciparum: cell signaling receptors, GPI structural requirement, and regulation of GPI activity. J Biol Chem 2005;289:8606-16.
71. Jaramillo M, Plante I, Quellet N, et al. Hemozoin-inducible proinflammatory events in vivo: potential role in malaria infection. J Immunol 2004;172:3101-10.
72. Postma NS, Mommers EC, Eling WM, et al. Oxidative stress in malaria; implications for prevention and therapy. Pharm World Sci 1996;18:121-9.
73. Erel O, Vural H, Aksoy N, et al. Oxidative stress of platelets and thrombocytopenia in patients with vivax malaria. Clin Biochem 2001;34:341-4.
74. Sobolewski P, Gramaglia I, Frangos JA, et al. Plasmodium berghei resist reactive oxygen species killing and exhibit intrinsic defense mechanisms. Infect Immun 2005;in review.
75. Troye-Blomberg M, Weidanz WP, van der Heyde HC. Immunity to malaria. In: Wahlgren M, Perlmann P, editors. Malaria: molecular and clinical aspects. Chur (Switzerland): Charwood Academic Publishers; 1999. p. 403-38.
76. McDevitt MA, Xie J, Gordeuk V, et al. The anemia of malaria infection: role of inflammatory cytokines. Curr Hematol Rep 2004;3:97-106.
77. Wink DA, Miranda KM, Espey MG, et al. Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox Signal 2001;3:203-13.