A central role for free heme in the pathogenesis of severe malaria: The missing link?

Journal of Molecular Medicine

Volumn 86, Issue 10, 2008, Pages 1097-1111

  Ferreira, Ana ^a   Balla, József ^b   Jeney, Viktória ^b   Balla, György ^b   Soares, Miguel P ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Carbon monoxide; Heme; Heme oxygenase 1; Inflammation; Malaria; Plasmodium

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; FERRITIN; FREE HEME; HEME; HEME OXYGENASE 1; HEMOGLOBIN; IRON; UNCLASSIFIED DRUG;

BINDING SITE; BRAIN MALARIA; CATABOLISM; CELL FREE SYSTEM; DEFENSE MECHANISM; ERYTHROCYTE; EXPERIMENTAL MODEL; GENE EXPRESSION; HUMAN; MALARIA; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PLASMODIUM FALCIPARUM; REVIEW; SIGNAL TRANSDUCTION; STRESS; SURVIVAL; UPREGULATION;

ANIMALS; CARBON MONOXIDE; DISEASE MODELS, ANIMAL; HEME; HEME OXYGENASE-1; HEMOGLOBINS; HUMANS; MALARIA; MALARIA, CEREBRAL; MODELS, BIOLOGICAL;

EID: 52549119182     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-008-0368-5     Document Type: Review

References (98)

1. WHO (2000) Expert Committee on Malaria: 20th Report. http://www.rbm.who. int/docs/ecr20.pdf
2. M Prudencio A Rodriguez MM Mota 2006 The silent path to thousands of merozoites: the Plasmodium liver stage Nat Rev Microbiol 4 849 856
3. L Schofield GE Grau 2005 Immunological processes in malaria pathogenesis Nat Rev Immunol 5 722 735
4. K Haldar SC Murphy DA Milner TE Taylor 2007 Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease Annu Rev Pathol 2 217 249
5. R Idro NE Jenkins CR Newton 2005 Pathogenesis, clinical features, and neurological outcome of cerebral malaria Lancet Neurol 4 827 840
6. LH Miller DI Baruch K Marsh OK Doumbo 2002 The pathogenic basis of malaria Nature 415 673 679
7. K Marsh D Forster C Waruiru 1995 Indicators of life-threatening malaria in African children N Engl J Med 332 1399 1404
8. A Pamplona A Ferreira J Balla 2007 Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria Nat Med 13 703 710
9. I Gramaglia P Sobolewski D Meays 2006 Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria Nat Med 12 1417 1422
10. RT Gazzinelli EY Denkers 2006 Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism Nat Rev Immunol 6 895 906
11. G Krishnegowda AM Hajjar J Zhu 2005 Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity J Biol Chem 280 8606 8616
12. P Parroche FN Lauw N Goutagny 2007 Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9 Proc Natl Acad Sci U S A 104 1919 1924
13. C Coban KJ Ishii S Uematsu 2007 Pathological role of Toll-like receptor signaling in cerebral malaria Int Immunol 19 67 79
14. FP Mockenhaupt JP Cramer L Hamann 2006 Toll-like receptor (TLR) polymorphisms in African children: common TLR-4 variants predispose to severe malaria Proc Natl Acad Sci U S A 103 177 182
15. FP Mockenhaupt L Hamann C von Gaertner 2006 Common polymorphisms of toll-like receptors 4 and 9 are associated with the clinical manifestation of malaria during pregnancy J Infect Dis 194 184 188
16. CC Khor SJ Chapman FO Vannberg 2007 A Mal functional variant is associated with protection against invasive pneumococcal disease, bacteremia, malaria and tuberculosis Nat Genet 39 523 528
17. D Togbe L Schofield GE Grau 2007 Murine cerebral malaria development is independent of toll-like receptor signaling Am J Pathol 170 1640 1648
18. B Lepenies JP Cramer GD Burchard H Wagner CJ Kirschning T Jacobs 2008 Induction of experimental cerebral malaria is independent of TLR2/4/9 Med Microbiol Immunol 197 39 44
19. MF Good H Xu M Wykes CR Engwerda 2005 Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research Annu Rev Immunol 23 69 99
20. L Raberg D Sim AF Read 2007 Disentangling genetic variation for resistance and tolerance to infectious diseases in animals Science 318 812 814
21. SE Francis DJ Sullivan Jr DE Goldberg 1997 Hemoglobin metabolism in the malaria parasite Plasmodium falciparum Annu Rev Microbiol 51 97 123
22. AU Orjih HS Banyal R Chevli CD Fitch 1981 Hemin lyses malaria parasites Science 214 667 669
23. RP Rother L Bell P Hillmen MT Gladwin 2005 The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease JAMA 293 1653 1662
24. V Jeney J Balla A Yachie 2002 Pro-oxidant and cytotoxic effects of circulating heme Blood 100 879 887
25. J Balla G Balla V Jeney G Kakuk HS Jacob GM Vercellotti 2000 Ferriporphyrins and endothelium: a 2-edged sword-promotion of oxidation and induction of cytoprotectants Blood 95 3442 3450
26. J Balla HS Jacob G Balla K Nath JW Eaton GM Vercellotti 1993 Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage Proc Natl Acad Sci U S A 90 9285 9289
27. J Balla GM Vercellotti V Jeney 2005 Heme, heme oxygenase and ferritin in vascular endothelial cell injury Mol Nutr Food Res 49 1030 1043
28. R Tenhunen HS Marver R Schmid 1968 The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase Proc Natl Acad Sci U S A 61 748 755
29. S-Y Seong P Matzinger 2004 Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses Nat Rev Immunol 4 469 478
30. RT Figueiredo PL Fernandez DS Mourao-Sa 2007 Characterization of heme as activator of Toll-like receptor 4 J Biol Chem 282 20221 20229
31. BN Porto LS Alves PL Fernandez 2007 Heme induces neutrophil migration and reactive oxygen species generation through signaling pathways characteristic of chemotactic receptors J Biol Chem 282 24430 24436
32. AV Graca-Souza MA Arruda MS de Freitas C Barja-Fidalgo PL Oliveira 2002 Neutrophil activation by heme: implications for inflammatory processes Blood 99 4160 4165
33. MA Arruda AG Rossi MS de Freitas C Barja-Fidalgo AV Graca-Souza 2004 Heme inhibits human neutrophil apoptosis: involvement of phosphoinositide 3-kinase, MAPK, and NF-kappaB J Immunol 173 2023 2030
34. GE Grau LF Fajardo PF Piguet B Allet PH Lambert P Vassalli 1987 Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria Science 237 1210 1212
35. AF Slater A Cerami 1992 Inhibition by chloroquine of a novel haem polymerase enzyme activity in malaria trophozoites Nature 355 167 169
36. N Jiang NS Tan B Ho JL Ding 2007 Respiratory protein-generated reactive oxygen species as an antimicrobial strategy Nat Immunol 8 1114 1122
37. M Kristiansen JH Graversen C Jacobsen 2001 Identification of the haemoglobin scavenger receptor Nature 409 198 201
38. N Maeda F Yang DR Barnett BH Bowman O Smithies 1984 Duplication within the haptoglobin Hp2 gene Nature 309 131 135
39. SH Atkinson TW Mwangi SM Uyoga 2007 The haptoglobin 2-2 genotype is associated with a reduced incidence of Plasmodium falciparum malaria in children on the coast of Kenya Clin Infect Dis 44 802 809
40. JF Trape A Fribourg-Blanc MF Bosseno M Lallemant R Engler J Mouchet 1985 Malaria, cause of ahaptoglobinaemia in Africans Trans R Soc Trop Med Hyg 79 430 434
41. EK Uko AE Udoh MH Etukudoh 2003 Methaemoglobin profile in malaria infected children in Calabar Niger J Med 12 94 97
42. NM Anstey MY Hassanali J Mlalasi D Manyenga ED Mwaikambo 1996 Elevated levels of methaemoglobin in Tanzanian children with severe and uncomplicated malaria Trans R Soc Trop Med Hyg 90 147 151
43. V Hvidberg MB Maniecki C Jacobsen P Hojrup HJ Moller SK Moestrup 2005 Identification of the receptor scavenging hemopexin-heme complexes Blood 106 2572 2579
44. R Stocker Y Yamamoto AF McDonagh AN Glazer BN Ames 1987 Bilirubin is an antioxidant of possible physiological importance Science 235 1043 1046
45. MD Maines 2005 New insights into biliverdin reductase functions: linking heme metabolism to cell signaling Physiology (Bethesda) 20 382 389
46. G Balla HS Jacob J Balla 1992 Ferritin: a cytoprotective antioxidant strategem of endothelium J Biol Chem 267 18148 18153
47. A Cozzi B Corsi S Levi P Santambrogio A Albertini P Arosio 2000 Overexpression of wild type and mutated human ferritin H-chain in HeLa cells-in vivo role of ferritin ferroxidase activity J Biol Chem 275 25122 25129
48. PO Berberat M Katori E Kaczmarek 2003 Heavy chain ferritin acts as an antiapoptotic gene that protects livers from ischemia reperfusion injury FASEB J 17 1724 1726
49. PM Harrison P Arosio 1996 Ferritins-molecular properties, iron storage function and cellular regulation Biochimica et Biophysica Acta-Bioenergetics 1275 161 203
50. CG Pham C Bubici F Zazzeroni 2004 Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species Cell 119 529 542
51. LE Otterbein MP Soares K Yamashita FH Bach 2003 Heme oxygenase-1: unleashing the protective properties of heme Trends Immunol 24 449 455
52. HJ Schluesener PG Kremsner R Meyermann 2001 Heme oxygenase-1 in lesions of human cerebral malaria Acta Neuropathol (Berl) 101 65 68
53. IM Medana NT Mai NP Day 2001 Cellular stress and injury responses in the brains of adult Vietnamese patients with fatal Plasmodium falciparum malaria Neuropathol Appl Neurobiol 27 421 433
54. IA Clark MM Awburn CG Harper NG Liomba ME Molyneux 2003 Induction of HO-1 in tissue macrophages and monocytes in fatal falciparum malaria and sepsis Malar J 2 41
55. ML Jison PJ Munson JJ Barb 2004 Blood mononuclear cell gene expression profiles characterize the oxidant, hemolytic, and inflammatory stress of sickle cell disease Blood 104 270 280
56. A Yachie Y Niida T Wada 1999 Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency J Clin Invest 103 129 135
57. M Exner E Minar O Wagner M Schillinger 2004 The role of heme oxygenase-1 promoter polymorphisms in human disease Free Radic Biol Med 37 1097 1104
58. M Takeda M Kikuchi R Ubalee 2005 Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to cerebral malaria in Myanmar Jpn J Infect Dis 58 268 271
59. Epiphanio S, Mikolajczak SA, Goncalves et al (2008) Heme oxygenase-1 is an anti-inflammatory host factor that promotes murine plasmodium liver infection. Cell Host Microbe 3, 331-338
60. K Sato J Balla L Otterbein 2001 Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse to rat cardiac transplants J Immunol 166 4185 4194
61. LE Otterbein FH Bach J Alam 2000 Carbon monoxide mediates anti-inflammatory effects via the mitogen activated protein kinase pathway Nat Med 6 422 428
62. LE Otterbein BS Zuckerbraun M Haga 2003 Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury Nat Med 9 183 190
63. AA Chora P Fontoura A Cunha 2007 Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation J Clin Invest 117 438 447
64. R Ollinger M Bilban A Erat 2005 Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation Circulation 112 1030 1039
65. S Brouard LE Otterbein J Anrather 2000 Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis J Exp Med 192 1015 1026
66. M Bilban A Haschemi B Wegiel BY Chin O Wagner LE Otterbein 2008 Heme oxygenase and carbon monoxide initiate homeostatic signaling J Mol Med 86 267 279
67. JR Stone RH Sands WR Dunham MA Marletta 1996 Spectral and ligand-binding properties of an unusual hemoprotein, the ferric form of soluble guanylate cyclase Biochemistry 35 3258 3262
68. MF Perutz 1990 Mechanisms regulating the reactions of human hemoglobin with oxygen and carbon monoxide Annu Rev Physiol 52 1 25
69. VG Kharitonov VS Sharma RB Pilz D Magde D Koesling 1995 Basis of guanylate cyclase activation by carbon monoxide Proc Natl Acad Sci U S A 92 2568 2571
70. VS Sharma D Magde 1999 Activation of soluble guanylate cyclase by carbon monoxide and nitric oxide: a mechanistic model Methods 19 494 505
71. HP Kim SW Ryter AM Choi 2005 CO as a cellular signaling molecule Annu Rev Pharmacol Toxicol 46 411 449
72. QH Gibson G Palmer DC Wharton 1965 The binding of carbon monoxide by cytochrome c oxidase and the ratio of the cytochromes a and A3 J Biol Chem 240 915 920
73. S Moncada JD Erusalimsky 2002 Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev Mol Cell Biol 3 214 220
74. BS Zuckerbraun BY Chin M Bilban 2007 Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species FASEB J 21 1099 1106
75. M Bilban FH Bach SL Otterbein 2006 Carbon monoxide orchestrates a protective response through PPARgamma Immunity 24 601 610
76. BY Chin G Jiang B Wegiel 2007 Hypoxia-inducible factor 1 alpha stabilization by carbon monoxide results in cytoprotective preconditioning Proc Natl Acad Sci U S A 104 5109 5114
77. K Ono J Han 2000 The p38 signal transduction pathway: activation and function Cell Signal 12 1 13
78. G Silva A Cunha IP Gregoire MP Seldon MP Soares 2006 The antiapoptotic effect of heme oxygenase-1 in endothelial cells involves the degradation of p38{alpha} MAPK isoform J Immunol 177 1894 1903
79. HP Kim X Wang J Zhang 2005 Heat shock protein-70 mediates the cytoprotective effect of carbon monoxide: involvement of p38 beta MAPK and heat shock factor-1 J Immunol 175 2622 2629
80. HP Kim X Wang A Nakao 2005 Caveolin-1 expression by means of p38beta mitogen-activated protein kinase mediates the antiproliferative effect of carbon monoxide Proc Natl Acad Sci U S A 102 11319 11324
81. JS Welch M Ricote TE Akiyama FJ Gonzalez CK Glass 2003 PPARgamma and PPARdelta negatively regulate specific subsets of lipopolysaccharide and IFN-gamma target genes in macrophages Proc Natl Acad Sci U S A 100 6712 6717
82. EM Dioum J Rutter JR Tuckerman G Gonzalez MA Gilles-Gonzalez SL McKnight 2002 NPAS2: a gas-responsive transcription factor Science 298 2385 2387
83. F Hawking MJ Worms K Gammage 1968 Host temperature and control of 24-hour and 48-hour cycles in malaria parasites Lancet 1 506 509
84. AJ Cunnington SF Kendrick B Wamola B Lowe CR Newton 2004 Carboxyhemoglobin levels in Kenyan children with Plasmodium falciparum malaria Am J Trop Med Hyg 71 43 47
85. HC Brown TT Chau NT Mai 2000 Blood-brain barrier function in cerebral malaria and CNS infections in Vietnam Neurology 55 104 111
86. SM Potter AJ Mitchell WB Cowden 2005 Phagocyte-derived reactive oxygen species do not influence the progression of murine blood-stage malaria infections Infect Immun 73 4941 4947
87. IA Clark KA Rockett 1994 The cytokine theory of human cerebral malaria Parasitol Today 10 410 412
88. K Nakahira HP Kim XH Geng 2006 Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts J Exp Med 203 2377 2389
89. KH Stenzel AL Rubin A Novogrodsky 1981 Mitogenic and co-mitogenic properties of hemin J Immunol 127 2469 2473
90. A Novogrodsky M Suthanthiran KH Stenzel 1989 Immune stimulatory properties of metalloporphyrins J Immunol 143 3981 3987
91. TW Yeo DA Lampah R Gitawati 2007 Impaired nitric oxide bioavailability and l-arginine reversible endothelial dysfunction in adults with falciparum malaria J Exp Med 204 2693 2704
92. CD Reiter X Wang JE Tanus-Santos 2002 Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease Nat Med 8 1383 1389
93. KR Maples CH Kennedy SJ Jordan RP Mason 1990 In vivo thiyl free radical formation from hemoglobin following administration of hydroperoxides Arch Biochem Biophys 277 402 409
94. DJ McCormick MZ Atassi 1990 Hemoglobin binding with haptoglobin: delineation of the haptoglobin binding site on the alpha-chain of human hemoglobin J Protein Chem 9 735 742
95. HF Bunn JH Jandl 1968 Exchange of heme among hemoglobins and between hemoglobin and albumin J Biol Chem 243 465 475
96. M Paoli BF Anderson HM Baker WT Morgan A Smith EN Baker 1999 Crystal structure of hemopexin reveals a novel high-affinity heme site formed between two beta-propeller domains Nat Struct Biol 6 926 931
97. HN Little JB Neilands 1960 Binding of haematin by human serum albumin Nature 188 913 915
98. M Fasano G Fanali L Leboffe P Ascenzi 2007 Heme binding to albuminoid proteins is the result of recent evolution IUBMB Life 59 436 440