Hemozoin induces lung inflammation and correlates with malaria-associated acute respiratory distress syndrome

American Journal of Respiratory Cell and Molecular Biology

Volumn 48, Issue 5, 2013, Pages 589-600

  Deroost, Katrien ^a   Tyberghein, Ariane ^a   Lays, Natacha ^a   Noppen, Sam ^a   Schwarzer, Evelin ^c   Vanstreels, Els ^a   Komuta, Mina ^b   Prato, Mauro ^c   Lin, Jing Wen ^d   Pamplona, Ana ^e   Janse, Chris J ^d   Arese, Paolo ^c   Roskams, Tania ^b   Daelemans, Dirk ^a   Opdenakker, Ghislain ^a   Van Den Steen, Philippe E ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF TURIN   (Italy)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e INSTITUTO DE MEDICINA MOLECULAR JOÃO LOBO ANTUNES   (Portugal)

Author keywords

ARDS; Hemozoin; Malaria; Plasmodium berghei NK65; Pulmonary inflammation

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEME OXYGENASE 1; HEMOZOIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; VASCULOTROPIN; CCL2 PROTEIN, MOUSE; HEMOPROTEIN; IL10 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ADULT RESPIRATORY DISTRESS SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE ASSOCIATION; ERYTHROCYTE; GRANULOCYTE; HISTOPATHOLOGY; INFLAMMATORY CELL; LUNG ALVEOLUS CELL; LUNG EDEMA; LUNG WEIGHT; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHAGOCYTE; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PLASMODIUM CHABAUDI; PLASMODIUM CHABAUDI INFECTION; PLASMODIUM FALCIPARUM; PNEUMONIA; PROTEIN EXPRESSION; SCHIZONT; ANIMAL; C57BL MOUSE; CD4 LYMPHOCYTE COUNT; CHEMISTRY; GENE EXPRESSION; GENETICS; HOST PARASITE INTERACTION; HUMAN; IMMUNOLOGY; LUNG; LUNG LAVAGE; MACROPHAGE; MALARIA; METABOLISM; ORGAN SIZE; PARASITOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CD4 LYMPHOCYTE COUNT; CHEMOKINE CCL2; ERYTHROCYTES; GENE EXPRESSION; HEMEPROTEINS; HOST-PARASITE INTERACTIONS; HUMANS; INTERLEUKIN-10; LUNG; MACROPHAGES; MALARIA; MICE; MICE, INBRED C57BL; ORGAN SIZE; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PNEUMONIA; RESPIRATORY DISTRESS SYNDROME, ADULT; SCHIZONTS; SPECIES SPECIFICITY; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MLCS; MLOWN;

EID: 84879321328     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0450OC     Document Type: Article

References (51)

1. Day N, Dondorp AM. The management of patients with severe malaria. Am J Trop Med Hyg 2007;77: 29-35.
2. Matthay MA, Zemans RL. The acute respiratory distress syndrome: pathogenesis and treatment. Annu Rev Pathol 2011;6: 147-163.
3. Mohan A, Sharma SK, Bollineni S. Acute lung injury and acute respiratory distress syndrome in malaria. J Vector Borne Dis 2008;45: 179-193.
4. Taylor WR, Hanson J, Turner GD, White NJ, Dondorp AM. Respiratory manifestations of malaria. Chest 2012;142: 492-505.
5. Daneshvar C, Davis TM, Cox-Singh J, Rafa'ee MZ, Zakaria SK, Divis PC, Singh B. Clinical and laboratory features of human Plasmodium knowlesi infection. Clin Infect Dis 2009;49: 852-860.
6. William T, Menon J, Rajahram G, Chan L, Ma G, Donaldson S, Khoo S, Frederick C, Jelip J, Anstey NM, et al. Severe Plasmodium knowlesi malaria in a tertiary care hospital, Sabah, Malaysia. Emerg Infect Dis 2011;17: 1248-1255.
7. Tan LK, Yacoub S, Scott S, Bhagani S, Jacobs M. Acute lung injury and other serious complications of Plasmodium vivax malaria. Lancet Infect Dis 2008;8: 449-454.
8. Anstey NM, Russell B, Yeo TW, Price RN. The pathophysiology of vivax malaria. Trends Parasitol 2009;25: 220-227.
9. Van den Steen PE, Geurts N, Deroost K, Van Aelst I, Verhenne S, Heremans H, Van Damme J, Opdenakker G. Immunopathology and dexamethasone therapy in a new model for malaria-associated acute respiratory distress syndrome. Am J Respir Crit Care Med 2010;181: 957-968.
10. Valecha N, Pinto RG, Turner GD, Kumar A, Rodrigues S, Dubhashi NG, Rodrigues E, Banaulikar SS, Singh R, Dash AP, et al. Histopathology of fatal respiratory distress caused by Plasmodium vivax malaria. Am J Trop Med Hyg 2009;81: 758-762.
11. Duarte MI, Corbett CE, Boulos M, Amato NV. Ultrastructure of the lung in Falciparum malaria. Am J Trop Med Hyg 1985;34: 31-35.
12. Egan TJ. Haemozoin formation. Mol Biochem Parasitol 2008;157: 127-136.
13. Amodu OK, Adeyemo AA, Olumese PE, Gbadegesin RA. Intraleucocytic malaria pigment and clinical severity of malaria in children. Trans R Soc Trop Med Hyg 1998;92: 54-56.
14. Nguyen PH, Day N, Pram TD, Ferguson DJ, White NJ. Intraleucocytic malaria pigment and prognosis in severe malaria. Trans R Soc Trop Med Hyg 1995;89: 200-204.
15. Hanscheid T, Egan TJ, Grobusch MP. Haemozoin: from melatonin pigment to drug target, diagnostic tool, and immune modulator. Lancet Infect Dis 2007;7: 675-685.
16. Shio MT, Kassa FA, Bellemare MJ, Olivier M. Innate inflammatory response to the malarial pigment hemozoin. Microbes Infect 2010;12: 889-899.
17. Arese P, Schwarzer E. Malarial pigment (haemozoin): a very active "inert" substance. Ann Trop Med Parasitol 1997;91: 501-516.
18. Jaramillo M, Plante I, Ouellet N, Vandal K, Tessier PA, Olivier M. Hemozoin-inducible proinflammatory events in vivo: potential role in malaria infection. J Immunol 2004;172: 3101-3110.
19. Deroost K, Lays N, Noppen S, Martens E, Opdenakker G, Van den Steen PE. Improved methods for haemozoin quantification in tissues yield organ- and parasite-specific information in malaria-infected mice. Malar J 2012;11:166.
20. Janse CJ, Ramesar J, Waters AP. High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 2006;1: 346-356.
21. Spence PJ, Cunningham D, Jarra W, Lawton J, Langhorne J, Thompson J. Transformation of the rodent malaria parasite Plasmodium chabaudi. Nat Protoc 2011;6: 553-561.
22. Levesque MA, Sullivan AD, Meshnick SR. Splenic and hepatic hemozoin in mice after malaria parasite clearance. J Parasitol 1999; 85: 570-573.
23. Frita R, Carapau D, Mota MM, Hanscheid T. In vivo hemozoin kinetics after clearance of Plasmodium berghei infection in mice. Malar Res Treat 2012;2012:373086.
24. Lawrence C, Olson JA. Birefringent hemozoin identifies malaria. Am J Clin Pathol 1986;86: 360-363.
25. Epiphanio S, Campos MG, Pamplona A, Carapau D, Pena AC, Ataide R, Monteiro CA, Felix N, Costa-Silva A, Marinho CR, et al. VEGF promotes malaria-associated acute lung injury in mice. PLoS Pathog 2010;6:e1000916.
26. Mura M, dos Santos CC, Stewart D, Liu M. Vascular endothelial growth factor and related molecules in acute lung injury. J Appl Physiol 2004; 97: 1605-1617.
27. Strieter RM, Lynch JP III, Basha MA, Standiford TJ, Kasahara K, Kunkel SL. Host responses in mediating sepsis and adult respiratory distress syndrome. Semin Respir Infect 1990;5: 233-247.
28. Taylor TE, Fu WJ, Carr RA, Whitten RO, Mueller JS, Fosiko NG, Lewallen S, Liomba NG, Molyneux ME. Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat Med 2004;10: 143-145.
29. Craig A, Grau G, Janse C, Kazura J, Milner D, Barnwell J, Turner G, Langhorne J. The role of animal models for research on severe malaria. PLoS Pathog 2012;8:e1002401.
30. Bonilla JA, Bonilla TD, Yowell CA, Fujioka H, Dame JB. Critical roles for the digestive vacuole plasmepsins of Plasmodium falciparum in vacuolar function. Mol Microbiol 2007;65: 64-75.
31. Spaccapelo R, Janse CJ, Caterbi S, Franke-Fayard B, Bonilla JA, Syphard LM, Di CristinaM, Dottorini T, Savarino A, Cassone A, et al. Plasmepsin 4-deficient Plasmodium berghei are virulence attenuated and induce protective immunity against experimental malaria. Am J Pathol 2010; 176: 205-217.
32. Giribaldi G, Prato M, Ulliers D, Gallo V, Schwarzer E, Akide-Ndunge OB, Valente E, Saviozzi S, Calogero RA, Arese P. Involvement of inflammatory chemokines in survival of human monocytes fed with malarial pigment. Infect Immun 2010;78: 4912-4921.
33. Hashimoto S, Kobayashi A, Kooguchi K, Kitamura Y, Onodera H, Nakajima H. Upregulation of two death pathways of perforin/granzyme and FasL/Fas in septic acute respiratory distress syndrome. Am J Respir Crit Care Med 2000;161: 237-243.
34. Schwarzer E, Kuhn H, Valente E, Arese P. Malaria-parasitized erythrocytes and hemozoin nonenzymatically generate large amounts of hydroxy fatty acids that inhibit monocyte functions. Blood 2003;101: 722-728.
35. Schwarzer E, Skorokhod OA, Barrera V, Arese P. Hemozoin and the human monocyte: a brief review of their interactions. Parassitologia 2008;50: 143-145.
36. Barrera V, Skorokhod OA, Baci D, Gremo G, Arese P, Schwarzer E. Host fibrinogen stably bound to hemozoin rapidly activates monocytes via TLR-4 and CD11b/CD18-integrin: a new paradigm of hemozoin action. Blood 2011;117: 5674-5682.
37. Shio MT, Eisenbarth SC, Savaria M, Vinet AF, Bellemare MJ, Harder KW, Sutterwala FS, Bohle DS, Descoteaux A, Flavell RA, et al. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog 2009;5:e1000559.
38. Dostert C, Guarda G, Romero JF, Menu P, Gross O, Tardivel A, SuvaML, Stehle JC, Kopf M, Stamenkovic I, et al. Malarial hemozoin is a NALP3 inflammasome activating danger signal. PLoS ONE 2009;4:e6510.
39. Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, Visintin A, Halmen KA, Lamphier M, Olivier M, Bartholomeu DC, et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci USA 2007;104: 1919-1924.
40. Coban C, Ishii KJ, Kawai T, Hemmi H, Sato S, Uematsu S, Yamamoto M, Takeuchi O, Itagaki S, Kumar N, et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J ExpMed 2005;201: 19-25.
41. Wu X, Gowda NM, Kumar S, Gowda DC. Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J Immunol 2010;184: 4338-4348.
42. Geurts N, Martens E, Verhenne S, Lays N, Thijs G, Magez S, Cauwe B, Li S, Heremans H, Opdenakker G, et al. Insufficiently defined genetic background confounds phenotypes in transgenic studies as exemplified by malaria infection in Tlr9 knockout mice. PLoS ONE 2011;6: e27131.
43. Schwarzer E, Muller O, Arese P, Siems WG, Grune T. Increased levels of 4-hydroxynonenal in human monocytes fed with malarial pigment hemozoin: a possible clue for hemozoin toxicity. FEBS Lett 1996;388: 119-122.
44. Schwarzer E, Turrini F, Ulliers D, Giribaldi G, Ginsburg H, Arese P. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med 1992;176: 1033-1041.
45. Prato M, Gallo V, Giribaldi G, Aldieri E, Arese P. Role of the NF-kappaB transcription pathway in the haemozoin- and 15-HETE-mediated activation of matrix metalloproteinase-9 in human adherent monocytes. Cell Microbiol 2010;12: 1780-1791.
46. Dell'Agli M, Galli GV, Bulgari M, Basilico N, Romeo S, Bhattacharya D, Taramelli D, Bosisio E. Ellagitannins of the fruit rind of pomegranate (Punica granatum) antagonize in vitro the host inflammatory response mechanisms involved in the onset of malaria. Malar J 2010; 9:208.
47. Polimeni M, Valente E, Aldieri E, Khadjavi A, Giribaldi G, Prato M. Haemozoin induces early cytokine-mediated lysozyme release from human monocytes through p38. PLoS ONE 2012;7:e39497.
48. Ekekezie II, Thibeault DW, Rezaiekhaligh MH, Norberg M, Mabry S, Zhang X, Truog WE. Endostatin and vascular endothelial cell growth factor (VEGF) in piglet lungs: effect of inhaled nitric oxide and hyperoxia. Pediatr Res 2003;53: 440-446.
49. Karmpaliotis D, Kosmidou I, Ingenito EP, Hong K, Malhotra A, Sunday ME, Haley KJ. Angiogenic growth factors in the pathophysiology of a murine model of acute lung injury. Am J Physiol Lung Cell Mol Physiol 2002;283:L585-L595.
50. Hee L, Dinudom A, Mitchell AJ, Grau GE, Cook DI, Hunt NH, Ball HJ. Reduced activity of the epithelial sodium channel in malariainduced pulmonary oedema in mice. Int J Parasitol 2011;41: 81-88.
51. GillrieMR, KrishnegowdaG, Lee K, BuretAG, Robbins SM, Looareesuwan S, Gowda DC, Ho M. Src-family kinase dependent disruption of endothelial barrier function by Plasmodium falciparum merozoite proteins. Blood 2007;110: 3426-3435.