Sickle hemoglobin confers tolerance to plasmodium infection

Cell

Volumn 145, Issue 3, 2011, Pages 398-409

  Ferreira, Ana ^a   Marguti, Ivo ^a   Bechmann, Ingo ^b,c   Jeney, Viktória ^a   Chora, Ângelo ^a   Palha, Nuno R ^a   Rebelo, Sofia ^a   Henri, Annie ^d,e,f   Beuzard, Yves ^d,e,f   Soares, Miguel P ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c GOETHE UNIVERSITY   (Germany)

^d UNIVERSITÉ PARIS DIDEROT   (France)

^e INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^f Institute of Emerging Diseases and Innovative Therapies   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; CD8 ANTIGEN; HEME OXYGENASE 1; HEMOGLOBIN S; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MALARIA; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; HEMATOPOIETIC CELL; HOST; MOUSE; NEUROPROTECTION; NONHUMAN; PARASITE LOAD; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE;

MUS;

EID: 79955528559     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2011.03.049     Document Type: Article

References (64)

1. J. Alam, D. Stewart, C. Touchard, S. Boinapally, A.M. Choi, and J.L. Cook Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene J. Biol. Chem. 274 1999 26071 26078
2. A.C. Allison Protection afforded by sickle-cell trait against subtertian malareal infection BMJ 1 1954 290 294
3. K. Ayi, F. Turrini, A. Piga, and P. Arese Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait Blood 104 2004 3364 3371 (Pubitemid 39507160)
4. S.K. Bains, R. Foresti, J. Howard, S. Atwal, C.J. Green, and R. Motterlini Human sickle cell blood modulates endothelial heme oxygenase activity: effects on vascular adhesion and reactivity Arterioscler. Thromb. Vasc. Biol. 30 2010 305 312
5. G. Balla, H.S. Jacob, J. Balla, M. Rosenberg, K. Nath, F. Apple, J.W. Eaton, and G.M. Vercellotti Ferritin: a cytoprotective antioxidant strategem of endothelium J. Biol. Chem. 267 1992 18148 18153
6. E.A. Beet Sickle cell disease in Northern Rhodesia East Afr. Med. J. 24 1947 212 222
7. J.D. Belcher, H. Mahaseth, T.E. Welch, L.E. Otterbein, R.P. Hebbel, and G.M. Vercellotti Heme oxygenase-1 is a modulator of inflammation and vaso-occlusion in transgenic sickle mice J. Clin. Invest. 116 2006 808 816 (Pubitemid 43326890)
8. E. Belnoue, M. Kayibanda, A.M. Vigario, J.C. Deschemin, N. van Rooijen, M. Viguier, G. Snounou, and L. Renia On the pathogenic role of brain-sequestered alphabeta CD8+ T cells in experimental cerebral malaria J. Immunol. 169 2002 6369 6375 (Pubitemid 36903485)
9. P.O. Berberat, M. Katori, E. Kaczmarek, D. Anselmo, C. Lassman, B. Ke, X. Shen, R.W. Busuttil, K. Yamashita, and E. Csizmadia Heavy chain ferritin acts as an antiapoptotic gene that protects livers from ischemia reperfusion injury FASEB J. 17 2003 1724 1726
10. G.S. Campanella, A.M. Tager, J.K. El Khoury, S.Y. Thomas, T.A. Abrazinski, L.A. Manice, R.A. Colvin, and A.D. Luster Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria Proc. Natl. Acad. Sci. USA 105 2008 4814 4819 (Pubitemid 351753829)
11. I.A. Clark, L.M. Alleva, A.C. Mills, and W.B. Cowden Pathogenesis of malaria and clinically similar conditions Clin. Microbiol. Rev. 17 2004 509 539 (Pubitemid 38970680)
12. P.D. Crompton, B. Traore, K. Kayentao, S. Doumbo, A. Ongoiba, S.A. Diakite, M.A. Krause, D. Doumtabe, Y. Kone, and G. Weiss Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria J. Infect. Dis. 198 2008 1265 1275
13. R.S. Eisenstein, M.D. Garcia, W. Pettingell, and H.N. Munro Regulation of ferritin and heme oxygenase synthesis in rat fibroblasts by different forms of iron Proc. Natl. Acad. Sci. USA 88 1991 688 692 (Pubitemid 21916088)
14. A. Ferreira, J. Balla, V. Jeney, G. Balla, and M.P. Soares A central role for free heme in the pathogenesis of severe malaria: the missing link? J. Mol. Med. 86 2008 1097 1111
15. M.J. Friedman Erythrocytic mechanism of sickle cell resistance to malaria Proc. Natl. Acad. Sci. USA 75 1978 1994 1997 (Pubitemid 8335470)
16. R. Gozzelino, V. Jeney, and M.P. Soares Mechanisms of cell protection by heme oxygenase-1 Annu. Rev. Pharmacol. Toxicol. 50 2010 323 354
17. A. Guindo, R.M. Fairhurst, O.K. Doumbo, T.E. Wellems, and D.A. Diallo X-linked G6PD deficiency protects hemizygous males but not heterozygous females against severe malaria PLoS Med. 4 2007 e66
18. R.P. Hebbel, W.T. Morgan, J.W. Eaton, and B.E. Hedlund Accelerated autoxidation and heme loss due to instability of sickle hemoglobin Proc. Natl. Acad. Sci. USA 85 1988 237 241 (Pubitemid 18055323)
19. A.T. Hood, M.E. Fabry, F. Costantini, R.L. Nagel, and H.L. Shear Protection from lethal malaria in transgenic mice expressing sickle hemoglobin Blood 87 1996 1600 1603 (Pubitemid 26056927)
20. R. Hutagalung, P. Wilairatana, S. Looareesuwan, G.M. Brittenham, M. Aikawa, and V.R. Gordeuk Influence of hemoglobin E trait on the severity of Falciparum malaria J. Infect. Dis. 179 1999 283 286 (Pubitemid 29028372)
21. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, and I. Hatayama An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322 (Pubitemid 27373291)
22. M. Jallow, Y.Y. Teo, K.S. Small, K.A. Rockett, P. Deloukas, T.G. Clark, K. Kivinen, K.A. Bojang, D.J. Conway, and M. Pinder Genome-wide and fine-resolution association analysis of malaria in West Africa 2009 Nat Genet
23. M.L. Jison, P.J. Munson, J.J. Barb, A.F. Suffredini, S. Talwar, C. Logun, N. Raghavachari, J.H. Beigel, J.H. Shelhamer, and R.L. Danner Blood mononuclear cell gene expression profiles characterize the oxidant, hemolytic, and inflammatory stress of sickle cell disease Blood 104 2004 270 280 (Pubitemid 38879868)
24. T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu. Rev. Pharmacol. Toxicol. 47 2007 89 116
25. R. Larsen, R. Gozzelino, V. Jeney, L. Tokaji, F.A. Bozza, A.M. Japiassu, D. Bonaparte, M.M. Cavalcante, A. Chora, and A. Ferreira A central role for free heme in the pathogenesis of severe sepsis Sci Transl Med 2 2010 51ra71
26. F.B. Livincstone Malaria and human polymorphisms Annu. Rev. Genet. 5 1971 33 64
27. R.J. Lundie, T.F. de Koning-Ward, G.M. Davey, C.Q. Nie, D.S. Hansen, L.S. Lau, J.D. Mintern, G.T. Belz, L. Schofield, and F.R. Carbone Blood-stage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8alpha+ dendritic cells Proc. Natl. Acad. Sci. USA 105 2008 14509 14514
28. J. May, J.A. Evans, C. Timmann, C. Ehmen, W. Busch, T. Thye, T. Agbenyega, and R.D. Horstmann Hemoglobin variants and disease manifestations in severe falciparum malaria JAMA 297 2007 2220 2226 (Pubitemid 47010879)
29. S.K. Mishra, and C.R. Newton Diagnosis and management of the neurological complications of falciparum malaria Nat Rev Neurol 5 2009 189 198
30. D. Modiano, G. Luoni, B.S. Sirima, J. Simpore, F. Verra, A. Konate, E. Rastrelli, A. Olivieri, C. Calissano, and G.M. Paganotti Haemoglobin C protects against clinical Plasmodium falciparum malaria Nature 414 2001 305 308 (Pubitemid 33097806)
31. A.G. Motulsky, J. Vandepitte, and G.R. Fraser Population genetic studies in the Congo. I. Glucose-6-phosphate dehydrogenase deficiency, hemoglobin S, and malaria Am. J. Hum. Genet. 18 1966 514 537
32. U. Muller-Eberhard, J. Javid, H.H. Liem, A. Hanstein, and M. Hanna Plasma concentrations of hemopexin, haptoglobin and heme in patients with various hemolytic diseases Blood 32 1968 811 815
33. K.A. Nath, G. Balla, G.M. Vercellotti, J. Balla, H.S. Jacob, M.D. Levitt, and M.E. Rosenberg Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat J. Clin. Invest. 90 1992 267 270
34. K.A. Nath, J.P. Grande, J.J. Haggard, A.J. Croatt, Z.S. Katusic, A. Solovey, and R.P. Hebbel Oxidative stress and induction of heme oxygenase-1 in the kidney in sickle cell disease Am. J. Pathol. 158 2001 893 903 (Pubitemid 32221782)
35. K. Ogawa, J. Sun, S. Taketani, O. Nakajima, C. Nishitani, S. Sassa, N. Hayashi, M. Yamamoto, S. Shibahara, and H. Fujita Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1 EMBO J. 20 2001 2835 2843 (Pubitemid 32938566)
36. A. Pamplona, A. Ferreira, J. Balla, V. Jeney, G. Balla, S. Epiphanio, A. Chora, C.D. Rodrigues, I.P. Gregoire, and M. Cunha-Rodrigues Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria Nat. Med. 13 2007 703 710 (Pubitemid 46889755)
37. G. Pasvol, D.J. Weatherall, and R.J. Wilson Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria Nature 274 1978 701 703 (Pubitemid 8405068)
38. L. Raberg, D. Sim, and A.F. Read Disentangling genetic variation for resistance and tolerance to infectious diseases in animals Science 318 2007 812 814 (Pubitemid 351411775)
39. C.D. Reiter, X. Wang, J.E. Tanus-Santos, N. Hogg, R.O. Cannon 3rd, A.N. Schechter, and M.T. Gladwin Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease Nat. Med. 8 2002 1383 1389 (Pubitemid 36019423)
40. N. Sabaa, L. de Franceschi, P. Bonnin, Y. Castier, G. Malpeli, H. Debbabi, A. Galaup, M. Maier-Redelsperger, S. Vandermeersch, and A. Scarpa Endothelin receptor antagonism prevents hypoxia-induced mortality and morbidity in a mouse model of sickle-cell disease J. Clin. Invest. 118 2008 1924 1933 (Pubitemid 351632394)
41. K. Sato, J. Balla, L. Otterbein, N.R. Snith, S. Brouard, Y. Lin, E. Czismadia, J. Sevigny, S.C. Robson, and G. Vercellotti Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse to rat cardiac transplants J. Immunol. 166 2001 4185 4194 (Pubitemid 32224952)
42. D.S. Schneider, and J.S. Ayres Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases Nat. Rev. Immunol. 8 2008 889 895
43. L. Schofield, and G.E. Grau Immunological processes in malaria pathogenesis Nat. Rev. Immunol. 5 2005 722 735 (Pubitemid 43086173)
44. D.A. Sears, M.M. Udden, and L.J. Thomas Carboxyhemoglobin levels in patients with sickle-cell anemia: relationship to hemolytic and vasoocclusive severity Am. J. Med. Sci. 322 2001 345 348 (Pubitemid 33139188)
45. E. Seixas, R. Gozzelino, A. Chora, A. Ferreira, G. Silva, R. Larsen, S. Rebelo, C. Penido, N.R. Smith, and A. Coutinho Heme oxygenase-1 affords protection against noncerebral forms of severe malaria Proc. Natl. Acad. Sci. USA 106 2009 15837 15842
46. H.L. Shear, E.F. Roth Jr., M.E. Fabry, F.D. Costantini, A. Pachnis, A. Hood, and R.L. Nagel Transgenic mice expressing human sickle hemoglobin are partially resistant to rodent malaria Blood 81 1993 222 226 (Pubitemid 23013698)
47. M.P. Soares, and F.H. Bach Heme oxygenase-1: from biology to therapeutic potential Trends Mol. Med. 15 2009 50 58
48. R. Tenhunen, H.S. Marver, and R. Schmid The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase Proc. Natl. Acad. Sci. USA 61 1968 748 755
49. M. Trudel, M.E. De Paepe, N. Chretien, N. Saadane, J. Jacmain, M. Sorette, T. Hoang, and Y. Beuzard Sickle cell disease of transgenic SAD mice Blood 84 1994 3189 3197 (Pubitemid 24328114)
50. M. Trudel, N. Saadane, M.C. Garel, J. Bardakdjian-Michau, Y. Blouquit, J.L. Guerquin-Kern, P. Rouyer-Fessard, D. Vidaud, A. Pachnis, and P.H. Romeo Towards a transgenic mouse model of sickle cell disease: hemoglobin SAD EMBO J. 10 1991 3157 3165 (Pubitemid 21905338)
51. T.N. Williams Human red blood cell polymorphisms and malaria Curr. Opin. Microbiol. 9 2006 388 394 (Pubitemid 44108720)
52. T.N. Williams, T.W. Mwangi, D.J. Roberts, N.D. Alexander, D.J. Weatherall, S. Wambua, M. Kortok, R.W. Snow, and K. Marsh An immune basis for malaria protection by the sickle cell trait PLoS Med. 2 2005 e128
53. T.N. Williams, T.W. Mwangi, S. Wambua, N.D. Alexander, M. Kortok, R.W. Snow, and K. Marsh Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases J. Infect. Dis. 192 2005 178 186 (Pubitemid 40863872)
54. L.C. Wu, C.W. Sun, T.M. Ryan, K.M. Pawlik, J. Ren, and T.M. Townes Correction of sickle cell disease by homologous recombination in embryonic stem cells Blood 108 2006 1183 1188 (Pubitemid 44232013)
55. S.F. Yet, M.A. Perrella, M.D. Layne, C.M. Hsieh, K. Maemura, L. Kobzik, P. Wiesel, H. Christou, S. Kourembanas, and M.E. Lee Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice Journal of Clinical Investigation 103 1999 R23 R29
56. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., et al. (1997). An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236, 313-322. (Pubitemid 27373291)
57. Lundie, R.J., de Koning-Ward, T.F., Davey, G.M., Nie, C.Q., Hansen, D.S., Lau, L.S., Mintern, J.D., Belz, G.T., Schofield, L., Carbone, F.R., et al. (2008). Blood-stage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8alpha+ dendritic cells. Proc. Natl. Acad. Sci. USA 105, 14509-14514.
58. Pamplona, A., Ferreira, A., Balla, J., Jeney, V., Balla, G., Epiphanio, S., Chora, A., Rodrigues, C.D., Gregoire, I.P., Cunha-Rodrigues, M., et al. (2007). Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat. Med. 13, 703-710. (Pubitemid 46889755)
59. Sato, K., Balla, J., Otterbein, L., Snith, N.R., Brouard, S., Lin, Y., Czismadia, E., Sevigny, J., Robson, S.C., Vercellotti, G., et al. (2001). Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse to rat cardiac transplants. J. Immunol. 166, 4185-4194. (Pubitemid 32224952)
60. Seixas, E., Gozzelino, R., Chora, A., Ferreira, A., Silva, G., Larsen, R., Rebelo, S., Penido, C., Smith, N.R., Coutinho, A., et al. (2009). Heme oxygenase-1 affords protection against noncerebral forms of severe malaria. Proc. Natl. Acad. Sci. USA 106, 15837-15842.
61. Trudel, M., De Paepe, M.E., Chretien, N., Saadane, N., Jacmain, J., Sorette, M., Hoang, T., and Beuzard, Y. (1994). Sickle cell disease of transgenic SAD mice. Blood 84, 3189-3197. (Pubitemid 24328114)
62. Trudel, M., Saadane, N., Garel, M.C., Bardakdjian-Michau, J., Blouquit, Y., Guerquin-Kern, J.L., Rouyer-Fessard, P., Vidaud, D., Pachnis, A., Romeo, P.H., et al. (1991). Towards a transgenic mouse model of sickle cell disease: hemoglobin SAD. EMBO J. 10, 3157-3165. (Pubitemid 21905338)
63. Wu, L.C., Sun, C.W., Ryan, T.M., Pawlik, K.M., Ren, J., and Townes, T.M. (2006). Correction of sickle cell disease by homologous recombination in embryonic stem cells. Blood 108, 1183-1188. (Pubitemid 44232013)
64. Yet, S.F., Perrella, M.A., Layne, M.D., Hsieh, C.M., Maemura, K., Kobzik, L., Wiesel, P., Christou, H., Kourembanas, S., and Lee, M.E. (1999). Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J. Clin. Invest. 103, R23-R29. (Pubitemid 29207256)