Pro-stimulatory role of methemoglobin in inflammation through hemin oxidation and polymerization

Inflammation and Allergy - Drug Targets

Volumn 12, Issue 1, 2013, Pages 68-78

  Deshmukh, Rohitas ^a   Trivedi, Vishal ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY GUWAHATI   (India)

Author keywords

Cerebral malaria hemin; Hemozoin; Inflammation; Macrophages; Methemoglobin

Indexed keywords

HEMIN; METHEMOGLOBIN; PEROXIDASE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; INFLAMMATION; INFRARED SPECTROSCOPY; MALARIA; MICROENVIRONMENT; MOUSE; NONHUMAN; OXIDATION; PROTEIN POLYMERIZATION; SPECTROSCOPY;

CELL LINE; CELLS, CULTURED; HEMIN; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MACROPHAGES; MALARIA, CEREBRAL; METHEMOGLOBIN; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLASMODIUM FALCIPARUM; POLYMERIZATION; REACTIVE OXYGEN SPECIES;

EID: 84875932188     PISSN: 18715281     EISSN: None     Source Type: Journal    
DOI: 10.2174/1871528111312010010     Document Type: Article

References (54)

1. Weatherall, D. J.; Abdalla, S. The anaemia of Plasmodium falciparum malaria. Br. Med. Bull., 1982, 38(2), 147-151.
2. Combes, V.; Coltel, N.; Faille, D.; Wassmer, S. C.; Grau, G. E. Cerebral malaria: role of microparticles and platelets in alterations of the blood-brain barrier. Int. J. Parasitol., 2006, 36, (5), 541-546.
3. Hunt, N. H.; Grau, G. E. Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends. Immunol., 2003, 24, (9), 491-499.
4. Schofield, L.; Grau, G. E. Immunological processes in malaria pathogenesis. Nat. Rev. Immunol., 2005, 5, (9), 722-735.
5. Kim, K. S. Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat. Rev. Neurosci., 2003, 4, (5), 376-385.
6. Sarra, M.; Cupi, M. L.; Pallone, F.; Monteleone, G. Interleukin-21 in immune and allergic diseases. Inflamm. Allergy. Drug. Targets., 2012, 11, (4), 313-319.
7. Fauser, S.; Deininger, M. H.; Kremsner, P. G.; Magdolen, V.; Luther, T.; Meyermann, R.; Schluesener, H. J. Lesion associated expression of urokinase-type plasminogen activator receptor (uPAR, CD87) in human cerebral malaria. J. Neuroimmunol., 2000, 111, (1-2), 234-240.
8. Manucha, W.; Valles, P. G. Apoptosis modulated by oxidative stress and inflammation during obstructive nephropathy. Inflamm. Allergy. Drug. Targets., 2012, 11, (4), 303-312.
9. Sun, S.; Rao, N. L.; Venable, J.; Thurmond, R.; Karlsson, L. TLR7/9 antagonists as therapeutics for immune-mediated inflammatory disorders. Inflamm. Allergy. Drug. Targets., 2007, 6, (4), 223-235.
10. Nitcheu, J.; Bonduelle, O.; Combadiere, C.; Tefit, M.; Seilhean, D.; Mazier, D.; Combadiere, B. Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J. Immunol., 2003, 170, (4), 2221-2228.
11. Pais, T. F.; Chatterjee, S. Brain macrophage activation in murine cerebral malaria precedes accumulation of leukocytes and CD8+ T cell proliferation. J. Neuroimmunol., 2005, 163, (1-2), 73-83.
12. La Cava, A. Proinflammatory activities of leptin in nonautoimmune conditions. Inflamm. Allergy. Drug. Targets., 2012, 11, (4), 298-302.
13. Pamplona, A.; Hanscheid, T.; Epiphanio, S.; Mota, M. M.; Vigario, A. M. Cerebral malaria and the hemolysis/methemoglobin/heme hypothesis: shedding new light on an old disease. Int. J. Biochem. Cell. Biol., 2009, 41, (4), 711-716.
14. Shio, M. T.; Kassa, F. A.; Bellemare, M. J.; Olivier, M. Innate inflammatory response to the malarial pigment hemozoin. Microbes. Infect., 2010, 12, (12-13), 889-899.
15. Kamchonwongpaisan, S.; Samoff, E.; Meshnick, S. R. Identification of hemoglobin degradation products in Plasmodium falciparum. Mol. Biochem. Parasitol., 1997, 86, (2), 179-186.
16. Coban, C.; Ishii, K. J.; Kawai, T.; Hemmi, H.; Sato, S.; Uematsu, S.; Yamamoto, M.; Takeuchi, O.; Itagaki, S.; Kumar, N.; Horii, T.; Akira, S. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J. Exp. Med., 2005, 201, (1), 19-25.
17. Dostert, C.; Guarda, G.; Romero, J. F.; Menu, P.; Gross, O.; Tardivel, A.; Suva, M. L.; Stehle, J. C.; Kopf, M.; Stamenkovic, I.; Corradin, G.; Tschopp, J. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS. One., 2009, 4, (8), e6510.
18. Francis, S. E.; Gluzman, I. Y.; Oksman, A.; Knickerbocker, A.; Mueller, R.; Bryant, M. L.; Sherman, D. R.; Russell, D. G.; Goldberg, D. E. Molecular characterization and inhibition of a Plasmodium falciparum aspartic hemoglobinase. EMBO. J., 1994, 13, (2), 306-317.
19. Griffith, J. W.; Sun, T.; McIntosh, M. T.; Bucala, R. Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J. Immunol., 2009, 183, (8), 5208-5220.
20. Jaramillo, M.; Gowda, D. C.; Radzioch, D.; Olivier, M. Hemozoin increases IFN-gamma-inducible macrophage nitric oxide generation through extracellular signal-regulated kinase-and NFkappa B-dependent pathways. J. Immunol., 2003, 171, (8), 4243-4253.
21. Parroche, P.; Lauw, F. N.; Goutagny, N.; Latz, E.; Monks, B. G.; Visintin, A.; Halmen, K. A.; Lamphier, M.; Olivier, M.; Bartholomeu, D. C.; Gazzinelli, R. T.; Golenbock, D. T. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc. Natl. Acad. Sci. U SA., 2007, 104, (6), 1919-1924.
22. Pichyangkul, S.; Saengkrai, P.; Webster, H. K. Plasmodium falciparum pigment induces monocytes to release high levels of tumor necrosis factor-alpha and interleukin-1 beta. Am. J. Trop. Med. Hyg., 1994, 51, (4), 430-435.
23. Reimer, T.; Shaw, M. H.; Franchi, L.; Coban, C.; Ishii, K. J.; Akira, S.; Horii, T.; Rodriguez, A.; Nunez, G. Experimental cerebral malaria progresses independently of the Nlrp3 inflammasome. Eur. J. Immunol., 2010, 40, (3), 764-769.
24. Shio, M. T.; Eisenbarth, S. C.; Savaria, M.; Vinet, A. F.; Bellemare, M. J.; Harder, K. W.; Sutterwala, F. S.; Bohle, D. S.; Descoteaux, A.; Flavell, R. A.; Olivier, M. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS. Pathog., 2009, 5, (8), e1000559.
25. Sakamoto, M.; Takaki, E.; Yamashita, K.; Watanabe, K.; Tabuchi, S.; Watanabe, T.; Satoh, K. Nonenzymatic derived lipid peroxide, 8-iso-PGF2 alpha, participates in the pathogenesis of delayed cerebral vasospasm in a canine SAH model. Neurol. Res., 2002, 24, (3), 301-306.
26. Krishnegowda, G.; Hajjar, A. M.; Zhu, J.; Douglass, E. J.; Uematsu, S.; Akira, S.; Woods, A. S.; Gowda, D. C. 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., 2005, 280, (9), 8606-8616.
27. Ekdahl, C. T.; Claasen, J. H.; Bonde, S.; Kokaia, Z.; Lindvall, O. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. U S A., 2003, 100, (23), 13632-13637.
28. Moore, K. J.; El Khoury, J.; Medeiros, L. A.; Terada, K.; Geula, C.; Luster, A. D.; Freeman, M. W. A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid. J. Biol. Chem., 2002, 277, (49), 47373-47379.
29. Kiefer, C. R.; Snyder, L. M. Oxidation and erythrocyte senescence. Curr. Opin. Hematol., 2000, 7, (2), 113-116.
30. Balaji, S., Trivedi, V. Extracellular methemoglobin mediated ROS spike extracellular methemoglobin mediated early ROS spike triggers osmotic fragility and RBC destruction: An insight into the enhanced hemolysis during malaria. Indian J. Clin. Biochem., 2012, 27, (2), 178-185.
31. Balla, J.; Jacob, H. S.; Balla, G.; Nath, K.; Eaton, J. W.; Vercellotti, G. M. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc. Natl. Acad. Sci. U S A., 1993, 90, (20), 9285-9.
32. Boretti, F. S.; Buehler, P. W.; D'Agnillo, F.; Kluge, K.; Glaus, T.; Butt, O. I.; Jia, Y.; Goede, J.; Pereira, C. P.; Maggiorini, M.; Schoedon, G.; Alayash, A. I.; Schaer, D. J. Sequestration of extracellular hemoglobin within a haptoglobin complex decreases its hypertensive and oxidative effects in dogs and guinea pigs. J. Clin. Invest., 2009, 119, (8), 2271-2280.
33. Anstey, N. M.; Hassanali, M. Y.; Mlalasi, J.; Manyenga, D.; Mwaikambo, E. D. Elevated levels of methaemoglobin in Tanzanian children with severe and uncomplicated malaria. Trans R Soc Trop Med Hyg 1996, 90, (2), 147-151.
34. Carmona-Fonseca, J.; Alvarez, G.; Maestre, A. Methemoglobinemia and adverse events in Plasmodium vivax malaria patients associated with high doses of primaquine treatment. Am. J. Trop. Med. Hyg., 2009, 80, (2), 188-193.
35. Rizvi, I.; Zaman, S.; Zaidi, N.; Asif, M. S.; Abdali, N. Acute lifethreatening methaemoglobinaemia following ingestion of chloroquine. BMJ. Case. Rep., 2012, 2012.
36. Sankar, J.; Gupta, A.; Pathak, S.; Dubey, N. K. Death in an adolescent girl with methemoglobinemia and malaria. J. Trop. Pediatr., 2012, 58, (2), 154-156.
37. Uko, E. K.; Udoh, A. E.; Etukudoh, M. H. Methaemoglobin profile in malaria infected children in Calabar. Niger. J. Med., 2003, 12, (2), 94-97.
38. van der Heyde, H. C.; Nolan, J.; Combes, V.; Gramaglia, I.; Grau, G. E. A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction. Trends. Parasitol., 2006, 22, (11), 503-508.
39. Trivedi, V.; Chand, P.; Maulik, P. R.; Bandyopadhyay, U. Mechanism of horseradish peroxidase-catalyzed heme oxidation and polymerization (beta-hematin formation). Biochim. Biophys. Acta., 2005, 1723, (1-3), 221-228.
40. Trivedi, V.; Chand, P.; Srivastava, K.; Puri, S. K.; Maulik, P. R.; Bandyopadhyay, U. Clotrimazole inhibits hemoperoxidase of Plasmodium falciparum and induces oxidative stress. Proposed antimalarial mechanism of clotrimazole. J. Biol. Chem., 2005, 280, (50), 41129-41136.
41. Trivedi, V.; Srivastava, K.; Puri, S. K.; Maulik, P. R.; Bandyopadhyay, U. Purification and biochemical characterization of a heme containing peroxidase from the human parasite P. falciparum. Protein. Expr. Purif., 2005, 41, (1), 154-161.
42. Reeder, B. J. The redox activity of hemoglobins: from physiologic functions to pathologic mechanisms. Antioxid. Redox. Signal., 2010, 13, (7), 1087-1123.
43. Orjih, A. U.; Fitch, C. D. Hemozoin production by Plasmodium falciparum: variation with strain and exposure to chloroquine. Biochem. Biophys. Acta., 1993, 1157, (3), 270-274.
44. Cambos, M.; Scorza, T. Robust erythrophagocytosis leads to macrophage apoptosis via a hemin-mediated redox imbalance: role in hemolytic disorders. J. Leukoc. Biol., 2010, 89, (1), 159-171.
45. Anstey, A.; Marks, R.; Long, C.; Navabi, H.; Pearse, A.; Wynford-Thomas, D.; Jasani, B. In vivo photoinduction of metallothionein in human skin by ultraviolet irradiation. J. Pathol., 1996, 178, (1), 84-88.
46. Wagener, F. A.; Volk, H. D.; Willis, D.; Abraham, N. G.; Soares, M. P.; Adema, G. J.; Figdor, C. G. Different faces of the hemeheme oxygenase system in inflammation. Pharmacol. Rev., 2003, 55, (3), 551-571.
47. Shiga, T.; Imaizumi, K. Generation of phenoxy radicals by methemoglobin-hydrogen peroxide studies by electron paramagnetic resonance. Arch. Biochem. Biophys., 1973, 154, (2), 540-547.
48. Shiga, T.; Imaizumi, K. Electron spin resonance study on peroxidase-and oxidase-reactions of horse radish peroxidase and methemoglobin. Arch. Biochem. Biophys., 1975, 167, (2), 469-479.
49. Sullivan, D. J., Jr.; Gluzman, I. Y.; Goldberg, D. E. Plasmodium hemozoin formation mediated by histidine-rich proteins. Science., 1996, 271, (5246), 219-222.
50. Deshmukh, R.; Trivedi, V. Methemoglobin exposure produces toxicological effects in macrophages due to multiple ROS spike induced apoptosis. Toxicol. In Vitro, 2013, 27, 16-23.
51. Roach, J. P.; Moore, E. E.; Partrick, D. A.; Damle, S. S.; Silliman, C. C.; McIntyre, R. C., Jr.; Banerjee, A. Heme oxygenase-1 induction in macrophages by a hemoglobin-based oxygen carrier reduces endotoxin-stimulated cytokine secretion. Shock., 2009, 31, (3), 251-257.
52. Chen-Roetling, J.; Regan, R. F. Effect of heme oxygenase-1 on the vulnerability of astrocytes and neurons to hemoglobin. Biochem. Biophys. Res. Commun., 2006, 350, (1), 233-237.
53. Wang, J.; Dore, S. Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain., 2007, 130, (Pt 6), 1643-1652.
54. Buehler, P. W.; D'Agnillo, F. Toxicological consequences of extracellular hemoglobin: biochemical and physiological perspectives. Antioxid. Redox. Signal., 2010, 12, (2), 275-291.