Hemozoin induces hepatic inflammation in mice and is differentially associated with liver pathology depending on the Plasmodium strain

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Deroost, Katrien ^a   Lays, Natacha ^a   Pham, Thao Thy ^a   Baci, Denisa ^b,c   Van Den Eynde, Kathleen ^d   Komuta, Mina ^d   Prato, Mauro ^e   Roskams, Tania ^d   Schwarzer, Evelin ^b,e   Opdenakker, Ghislain ^a   Van Den Steen, Philippe E ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; FAS LIGAND; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GELATINASE B; HEME OXYGENASE 1; HEMOZOIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; LYMPHOTOXIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCYTE CHEMOTACTIC PROTEIN 1; PERFORIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; CYTOKINE; HEMOPROTEIN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENETIC TRANSCRIPTION; HEPATITIS; LIVER CELL DAMAGE; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PLASMODIUM; PLASMODIUM BERGHEI INFECTION; PLASMODIUM CHABAUDI INFECTION; PLASMODIUM FALCIPARUM; STRAIN DIFFERENCE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; C57BL MOUSE; CLASSIFICATION; COMPLICATION; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; GENE EXPRESSION; GENETICS; HOST PARASITE INTERACTION; LIVER; MACROPHAGE; MALARIA; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEVERITY OF ILLNESS INDEX; SPECIES DIFFERENCE;

MUS;

ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; CYTOKINES; DRUG-INDUCED LIVER INJURY; FEMALE; GENE EXPRESSION; HEMEPROTEINS; HOST-PARASITE INTERACTIONS; LIVER; MACROPHAGES; MALARIA; MALE; MICE, INBRED BALB C; MICE, INBRED C57BL; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEVERITY OF ILLNESS INDEX; SPECIES SPECIFICITY;

EID: 84913535534     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113519     Document Type: Article

References (55)

1. Whitten R, Milner DA Jr., Yeh MM, Kamiza S, Molyneux ME, et al. (2011) Liver pathology in Malawian children with fatal encephalopathy. Hum Pathol 42: 1230-1239.
2. Anand AC, Puri P (2005) Jaundice in malaria. J Gastroenterol Hepatol 20: 1322-1332.
3. Deroost K, Lays N, Noppen S, Martens E, Opdenakker G, et al. (2012) Improved methods for haemozoin quantification in tissues yield organ- and parasite-specific information in malaria-infected mice. Malar J 11: 166.
4. Levesque MA, Sullivan AD, Meshnick SR (1999) Splenic and hepatic hemozoin in mice after malaria parasite clearance. J Parasitol 85: 570-573.
5. Frita R, Carapau D, Mota MM, Hanscheid T (2012) In vivo hemozoin kinetics after clearance of Plasmodium berghei infection in mice. Malar Res Treat 2012: 373086.
6. Murthy GL, Sahay RK, Sreenivas DV, Sundaram C, Shantaram V (1998) Hepatitis in falciparum malaria. Trop Gastroenterol 19: 152-154.
7. Nacher M, Treeprasertsuk S, Singhasivanon P, Silachamroon U, Vannaphan S, et al. (2001) Association of hepatomegaly and jaundice with acute renal failure but not with cerebral malaria in severe falciparum malaria in Thailand. Am J Trop Med Hyg 65: 828-833.
8. Singh RP, Kashiwamura S, Rao P, Okamura H, Mukherjee A, et al. (2002) The role of IL-18 in blood-stage immunity against murine malaria Plasmodium yoelii 265 and Plasmodium berghei ANKA. J Immunol 168: 4674-4681.
9. Niikura M, Kamiya S, Kita K, Kobayashi F (2008) Coinfection with nonlethal murine malaria parasites suppresses pathogenesis caused by Plasmodium berghei NK65. J Immunol 180: 6877-6884.
10. Mastelic B, do Rosario AP, Veldhoen M, Renauld JC, Jarra W, et al. (2012) IL-22 Protects Against Liver Pathology and Lethality of an Experimental Blood-Stage Malaria Infection. Front Immunol 3: 85.
11. Findlay EG, Greig R, Stumhofer JS, Hafalla JC, De Souza JB, et al. (2010) Essential role for IL-27 receptor signaling in prevention of Th1-mediated immunopathology during malaria infection. J Immunol 185: 2482-2492.
12. Jacobs T, Plate T, Gaworski I, Fleischer B (2004) CTLA-4-dependent mechanisms prevent T cell induced-liver pathology during the erythrocyte stage of Plasmodium berghei malaria. Eur J Immunol 34: 972-980.
13. Seixas E, Gozzelino R, Chora A, Ferreira A, Silva G, et al. (2009) Heme oxygenase-1 affords protection against noncerebral forms of severe malaria. Proc Natl Acad Sci U S A 106: 15837-15842.
14. Van den Steen PE, Geurts N, Deroost K, Van Aelst I, Verhenne S, et al. (2010) Immunopathology and dexamethasone therapy in a new model for malaria-associated acute respiratory distress syndrome. Am J Respir Crit Care Med 181: 957-968.
15. de Kossodo S, Grau GE (1993) Profiles of cytokine production in relation with susceptibility to cerebral malaria. J Immunol 151: 4811-4820.
16. Van den Steen PE, Deroost K, Van Aelst I, Geurts N, Martens E, et al. (2008) CXCR3 determines strain susceptibility to murine cerebral malaria by mediating T lymphocyte migration toward IFN-gamma-induced chemokines. Eur J Immunol 38: 1082-1095.
17. Geurts N, Martens E, Verhenne S, Lays N, Thijs G, et al. (2011) Insufficiently defined genetic background confounds phenotypes in transgenic studies as exemplified by malaria infection in Tlr9 knockout mice. PLoS ONE 6: e27131.
18. Stevenson MM, Lyanga JJ, Skamene E (1982) Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infect Immun 38: 80-88.
19. Deroost K, Tyberghein A, Lays N, Noppen S, Schwarzer E, et al. (2013) Hemozoin induces lung inflammation and correlates with malaria-associated acute respiratory distress syndrome. Am J Respir Cell Mol Biol 48: 589-600.
20. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
21. Rodriguez-Acosta A, Finol HJ, Pulido-Mendez M, Marquez A, Andrade G, et al. (1998) Liver ultrastructural pathology in mice infected with Plasmodium berghei. J Submicrosc Cytol Pathol 30: 299-307.
22. Crispe IN (2009) The liver as a lymphoid organ. Annu Rev Immunol 27: 147-163.
23. Brugat T, Cunningham D, Sodenkamp J, Coomes S, Wilson M, et al. (2014) Sequestration and histopathology in Plasmodium chabaudi malaria are influenced by the immune response in an organ-specific manner. Cell Microbiol 16: 687-700.
24. Jaramillo M, Plante I, Ouellet N, Vandal K, Tessier PA, et al. (2004) Hemozoin-inducible proinflammatory events in vivo: potential role in malaria infection. J Immunol 172: 3101-3110.
25. Jaramillo M, Bellemare MJ, Martel C, Shio MT, Contreras AP, et al. (2009) Synthetic Plasmodium-like hemozoin activates the immune response: a morphology - function study. PLoS ONE 4: e6957.
26. Tyberghein A, Deroost K, Schwarzer E, Arese P, Van den Steen PE (2013) Immunopathological effects of malaria pigment or hemozoin and other crystals. Biofactors In Press.
27. Shio MT, Kassa FA, Bellemare MJ, Olivier M (2010) Innate inflammatory response to the malarial pigment hemozoin. Microbes Infect 12: 889-899.
28. Boura M, Frita R, Gois A, Carvalho T, Hanscheid T (2013) The hemozoin conundrum: is malaria pigment immune-activating, inhibiting, or simply a bystander? Trends Parasitol 29: 469-476.
29. Noland GS, Briones N, Sullivan DJ Jr. (2003) The shape and size of hemozoin crystals distinguishes diverse Plasmodium species. Mol Biochem Parasitol 130: 91-99.
30. Barrera V, Skorokhod OA, Baci D, Gremo G, Arese P, et al. (2011) Host fibrinogen stably bound to hemozoin rapidly activates monocytes via TLR-4 and CD11b/CD18-integrin: a new paradigm of hemozoin action. Blood 117: 5674-5682.
31. Kassa FA, Shio MT, Bellemare MJ, Faye B, Ndao M, et al. (2011) New inflammation-related biomarkers during malaria infection. PLoS ONE 6: e26495.
32. Dasari P, Reiss K, Lingelbach K, Baumeister S, Lucius R, et al. (2011) Digestive vacuoles of Plasmodium falciparum are selectively phagocytosed by and impair killing function of polymorphonuclear leukocytes. Blood 118: 4946-4956.
33. Dostert C, Guarda G, Romero JF, Menu P, Gross O, et al. (2009) Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS ONE 4: e6510.
34. Griffith JW, Sun T, McIntosh MT, Bucala R (2009) Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol 183: 5208-5220.
35. Shio MT, Eisenbarth SC, Savaria M, Vinet AF, Bellemare MJ, et al. (2009) Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog 5: e1000559.
36. Coban C, Ishii KJ, Kawai T, Hemmi H, Sato S, et al. (2005) Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 201: 19-25.
37. Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, et al. (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.
38. Wu X, Gowda NM, Kumar S, Gowda DC (2010) Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J Immunol 184: 4338-4348.
39. Coban C, Igari Y, Yagi M, Reimer T, Koyama S, et al. (2010) Immunogenicity of whole-parasite vaccines against Plasmodium falciparum involves malarial hemozoin and host TLR9. Cell Host Microbe 7: 50-61.
40. Khadjavi A, Valente E, Giribaldi G, Prato M (2014) Involvement of p38 MAPK in haemozoin-dependent MMP-9 enhancement in human monocytes. Cell Biochem Funct 32: 5-15.
41. Polimeni M, Valente E, Aldieri E, Khadjavi A, Giribaldi G, et al. (2012) Haemozoin induces early cytokine-mediated lysozyme release from human monocytes through p38 MAPK- and NF-kappaB-dependent mechanisms. PLoS ONE 7: e39497.
42. Jaramillo M, Gowda DC, Radzioch D, Olivier M (2003) Hemozoin increases IFN-gamma-inducible macrophage nitric oxide generation through extracellular signal-regulated kinase- and NF-kappa B-dependent pathways. J Immunol 171: 4243-4253.
43. Jaramillo M, Godbout M, Olivier M (2005) Hemozoin induces macrophage chemokine expression through oxidative stress-dependent and -independent mechanisms. J Immunol 174: 475-484.
44. Prato M, Gallo V, Giribaldi G, Aldieri E, Arese P (2010) 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 12: 1780-1791.
45. Punsawad C, Krudsood S, Maneerat Y, Chaisri U, Tangpukdee N, et al. (2012) Activation of nuclear factor kappa B in peripheral blood mononuclear cells from malaria patients. Malar J 11: 191.
46. Krishnegowda G, Hajjar AM, Zhu J, Douglass EJ, Uematsu S, et al. (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.
47. Schofield L, Hackett F (1993) Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J Exp Med 177: 145-153.
48. Skorokhod OA, Alessio M, Mordmuller B, Arese P, Schwarzer E (2004) Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect. J Immunol 173: 4066-4074.
49. Perkins DJ, Moore JM, Otieno J, Shi YP, Nahlen BL, et al. (2003) In vivo acquisition of hemozoin by placental blood mononuclear cells suppresses PGE2, TNF-alpha, and IL-10. Biochem Biophys Res Commun 311: 839-846.
50. Millington OR, Di Lorenzo C, Phillips RS, Garside P, Brewer JM (2006) Suppression of adaptive immunity to heterologous antigens during Plasmodium infection through hemozoin-induced failure of dendritic cell function. J Biol 5: 5.
51. Scorza T, Magez S, Brys L, De Baetselier P (1999) Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunol 21: 545-554.
52. Urban BC, Todryk S (2006) Malaria pigment paralyzes dendritic cells. J Biol 5: 4.
53. Schwarzer E, Alessio M, Ulliers D, Arese P (1998) Phagocytosis of the malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes. Infect Immun 66: 1601-1606.
54. Good MF, Reiman JM, Rodriguez IB, Ito K, Yanow SK, El-Deeb IM, et al. (2013) Cross-species malaria immunity induced by chemically attenuated parasites. J Clin Invest 123:3353-3362.
55. Playfair JH, de Souza JB, Dockrell HM, Agomo PU, Taverne J (1979) Cell-mediated immunity in the liver of mice vaccinated against malaria. Nature 282:731-734.