Schistosoma mansoni hemozoin modulates alternative activation of macrophages via specific suppression of Retnla expression and secretion

Infection and Immunity

Volumn 81, Issue 1, 2013, Pages 133-142

  Truscott, Martha ^a   Evans, D Andrew ^b   Gunn, Matt ^b   Hoffmann, Karl F ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; HEMOZOIN; INTERLEUKIN 4; RETNLA PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL CULTURE; CELLULAR IMMUNITY; CONTROLLED STUDY; DETOXIFICATION; EFFECTOR CELL; FEMALE; HOST PARASITE INTERACTION; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; TH2 CELL;

ANIMALS; CYTOKINES; FEMALE; HEMEPROTEINS; IMMUNOLOGIC FACTORS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-4; LIVER; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; OVUM; PHAGOCYTES; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; TH2 CELLS;

EID: 84871867341     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00701-12     Document Type: Article

References (60)

1. Hotez PJ, Fenwick A, Savioli L, Molyneux DH. 2009. Rescuing the bottom billion through control of neglected tropical diseases. Lancet 373: 1570-1575.
2. King CH, Dickman K, Tisch DJ. 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365:1561-1569.
3. Cheever AW, Macedonia JG, Mosimann JE, Cheever EA. 1994. Kinetics of egg production and egg excretion by Schistosoma mansoni and S. japonicum in mice infected with a single pair of worms. Am. J. Trop. Med. Hyg. 50:281-295.
4. Wynn TA, Thompson RW, Cheever AW, Mentink-Kane MM. 2004. Immunopathogenesis of schistosomiasis. Immunol. Rev. 201:156-167.
5. Fallon PG, Dunne DW. 1999. Tolerization of mice to Schistosoma mansoni egg antigens causes elevated type 1 and diminished type 2 cytokine responses and increased mortality in acute infection. J. Immunol. 162: 4122- 4132.
6. Hoffmann KF, Cheever AW, Wynn TA. 2000. IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J. Immunol. 164:6406-6416.
7. Herbert DR, Holscher C, Mohrs M, Arendse B, Schwegmann A, Radwanska M, Leeto M, Kirsch R, Hall P, Mossmann H, Claussen B, Forster I, Brombacher F. 2004. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20:623- 635.
8. Zussman RA, Bauman PM, Petruska JC. 1970. The role of ingested hemoglobin in the nutrition of Schistosoma mansoni. J. Parasitol. 56: 75-79.
9. Oliveira MF, d'Avila JC, Torres CR, Oliveira PL, Tempone AJ, Rumjanek FD, Braga CM, Silva JR, Dansa-Petretski M, Oliveira MA, de Souza W, Ferreira ST. 2000. Haemozoin in Schistosoma mansoni. Mol. Biochem. Parasitol. 111:217-221.
10. Correa Soares JB, Maya-Monteiro CM, Bittencourt-Cunha PR, Atella GC, Lara FA, D'Avila JC, Menezes D, Vannier-Santos MA, Oliveira PL, Egan TJ, Oliveira MF. 2007. Extracellular lipid droplets promote hemozoin crystallization in the gut of the blood fluke Schistosoma mansoni. FEBS Lett. 581:1742-1750.
11. Oliveira MF, Kycia SW, Gomez A, Kosar AJ, Bohle DS, Hempelmann E, Menezes D, Vannier-Santos MA, Oliveira PL, Ferreira ST. 2005. Structural and morphological characterization of hemozoin produced by Schistosoma mansoni and Rhodnius prolixus. FEBS Lett. 579:6010-6016.
12. Kloetzel K, Lewert RM. 1966. Pigment formation in Schistosoma mansoni infections in the white mouse. Am. J. Trop. Med. Hyg. 15:28 -31.
13. Riley EM, Wahl S, Perkins DJ, Schofield L. 2006. Regulating immunity to malaria. Parasite Immunol. 28:35- 49.
14. Jaramillo M, Plante I, Ouellet N, Vandal K, Tessier PA, Olivier M. 2004. Hemozoin-inducible proinflammatory events in vivo: potential role in malaria infection. J. Immunol. 172:3101-3110.
15. 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.
16. Urban BC, Todryk S. 2006. Malaria pigment paralyzes dendritic cells. J. Biol. 5:4.
17. Carter MD, Reese Harry S, Wright DW. 2007. Identification of hydroxyeicosatetraenoic acid components of schistosomal hemozoin. Biochem. Biophys. Res. Commun. 363:867- 872.
18. Jiang Y, Xue X, Chen X, Zhuang W, Sun J, Shen L, Pan W. 2010. Hemozoin from Schistosoma japonicum does not affect murine myeloid dendritic cell function. Parasitol. Res. 106:653- 659.
19. Holcomb IN, Kabakoff RC, Chan B, Baker TW, Gurney A, Henzel W, Nelson C, Lowman HB, Wright BD, Skelton NJ, Frantz GD, Tumas DB, Peale FV, Jr, Shelton DL, Hebert CC. 2000. FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO J.19:4046-4055.
20. Steppan CM, Brown EJ, Wright CM, Bhat S, Banerjee RR, Dai CY, Enders GH, Silberg DG, Wen X, Wu GD, Lazar MA. 2001. A family of tissue-specific resistin-like molecules. Proc. Natl. Acad. Sci. U. S. A. 98: 502-506.
21. Cook PC, Jones LH, Jenkins SJ, Wynn TA, Allen JE, Macdonald AS. 2012. Alternatively activated dendritic cells regulate CD4+ T-cell polarization in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 109:9977-9982.
22. Nair MG, Du Y, Perrigoue JG, Zaph C, Taylor JJ, Goldschmidt M, Swain GP, Yancopoulos GD, Valenzuela DM, Murphy A, Karow M, Stevens S, Pearce EJ, Artis D. 2009. Alternatively activated macrophage-derived RELM-alpha is a negative regulator of type 2 inflammation in the lung. J. Exp. Med. 206:937-952.
23. Pesce JT, Ramalingam TR, Wilson MS, Mentink-Kane MM, Thompson RW, Cheever AW, Urban JF, Jr, Wynn TA. 2009. Retnla (relmalpha/ fizz1) suppresses helminth-induced Th2-type immunity. PLoS Pathog. 5:e1000393. doi:10.1371/journal.ppat.1000393.
24. Lewis FA. 1998. Schistosomiasis. Curr. Protoc. Immunol. 28(Suppl): 19.11.11-19.11.28.
25. Sullivan DJ, Jr, Gluzman IY, Russell DG, Goldberg DE. 1996. On the molecular mechanism of chloroquine's antimalarial action. Proc. Natl. Acad. Sci. U. S. A. 93:11865-11870.
26. Cheever AW, Deb S, Duvall RH. 1989. Granuloma formation in Schistosoma japonicum infected nude mice: the effects of reconstitution with L3T4+ or Lyt2+ splenic cells. Am. J. Trop. Med. Hyg. 40:66-71.
27. Wynn TA, Cheever AW, Jankovic D, Poindexter RW, Caspar P, Lewis FA, Sher A. 1995. An IL-12-based vaccination method for preventing fibrosis induced by schistosome infection. Nature 376:594-596.
28. Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
29. Adam O, Vercellone A, Paul F, Monsan PF, Puzo G. 1995. A nondegradative route for the removal of endotoxin from exopolysaccharides. Anal. Biochem. 225:321-327.
30. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Bohle DS, Kosar AD, Stephens PW. 2002. Phase homogeneity and crystal morphology of the malaria pigment beta-hematin. Acta Crystallogr. D Biol. Crystallogr. 58:1752-1756.
32. Hoffmann KF, Fitzpatrick JM. 2004. Gene expression studies using self-fabricated parasite cDNA microarrays. Methods Mol. Biol. 270:219-236.
33. Foss DL, Baarsch MJ, Murtaugh MP. 1998. Regulation of hypoxanthine phosphoribosyltransferase, glyceraldehyde-3-phosphate dehydrogenase and beta-actin mRNA expression in porcine immune cells and tissues. Anim. Biotechnol. 9:67-78.
34. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. doi:10.1093/nar/29.9.e45.
35. Morris SM, Jr. 2002. Regulation of enzymes of the urea cycle and arginine metabolism. Annu. Rev. Nutr. 22:87-105.
36. Brunet LR, Beall M, Dunne DW, Pearce EJ. 1999. Nitric oxide and the Th2 response combine to prevent severe hepatic damage during Schistosoma mansoni infection. J. Immunol. 163:4976-4984.
37. Menzies FM, Henriquez FL, Alexander J, Roberts CW. 2010. Sequential expression of macrophage anti-microbial/inflammatory and wound healing markers following innate, alternative and classical activation. Clin. Exp. Immunol. 160:369-379.
38. Donnelly S, O'Neill SM, Sekiya M, Mulcahy G, Dalton JP. 2005. Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect. Immun. 73:166-173.
39. Nair MG, Gallagher IJ, Taylor MD, Loke P, Coulson PS, Wilson RA, Maizels RM, Allen JE. 2005. Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infect. Immun. 73:385-394.
40. Slater AF, Swiggard WJ, Orton BR, Flitter WD, Goldberg DE, Cerami A, Henderson GB. 1991. An iron-carboxylate bond links the heme units of malaria pigment. Proc. Natl. Acad. Sci. U. S. A. 88:325-329.
41. Egan TJ, Chen JY, de Villiers KA, Mabotha TE, Naidoo KJ, Ncokazi KK, Langford SJ, McNaughton D, Pandiancherri S, Wood BR. 2006. Haemozoin (beta-haematin) biomineralization occurs by self-assembly near the lipid/water interface. FEBS Lett. 580:5105-5110.
42. Wood BR, Langford SJ, Cooke BM, Glenister FK, Lim J, McNaughton D. 2003. Raman imaging of hemozoin within the food vacuole of Plasmodium falciparum trophozoites. FEBS Lett. 554:247-252.
43. Abe M, Kitagawa T, Kyogoku Y. 1978. Resonance Raman spectra of octaethylporphyrinato-Ni(II) and meso-deuterated and 15N substituted derivatives. II. A normal coordinate analysis. J. Chem. Phys. 69:4526-4534.
44. Webster GT, Tilley L, Deed S, McNaughton D, Wood BR. 2008. Resonance Raman spectroscopy can detect structural changes in haemozoin (malaria pigment) following incubation with chloroquine in infected erythrocytes. FEBS Lett. 582:1087-1092.
45. Frosch T, Koncarevic S, Becker K, Popp J. 2009. Morphology-sensitive Raman modes of the malaria pigment hemozoin. Analyst 134:1126-1132.
46. Pagola S, Stephens PW, Bohle DS, Kosar AD, Madsen SK. 2000. The structure of malaria pigment beta-haematin. Nature 404:307-310.
47. Lancisi GM. 1717. De noxiis paludum effluviis, eorumque remediis. Libri duo. Typis Jo, Mariae Salvioni, Romae.
48. Deshpande P, Shastry P. 2004. Modulation of cytokine profiles by malaria pigment-hemozoin: role of IL-10 in suppression of proliferative responses of mitogen stimulated human PBMC. Cytokine 28:205-213.
49. 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.
50. Pearce EJ, Caspar P, Grzych JM, Lewis FA, Sher A. 1991. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J. Exp. Med. 173:159 -166.
51. Sher A, Fiorentino D, Caspar P, Pearce E, Mosmann T. 1991. Production of IL-10 by CD4+ T lymphocytes correlates with down-regulation of Th1 cytokine synthesis in helminth infection. J. Immunol. 147:2713- 2716.
52. Stadecker MJ, Hernandez HJ. 1998. The immune response and immunopathology in infection with Schistosoma mansoni: a key role of major egg antigen Sm-p40. Parasite Immunol. 20:217-221.
53. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, MacDonald AS, Allen JE. 2011. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332:1284-1288.
54. Cook PC, Aynsley SA, Turner JD, Jenkins GR, Van Rooijen N, Leeto M, Brombacher F, Mountford AP. 2011. Multiple helminth infection of the skin causes lymphocyte hypo-responsiveness mediated by Th2 conditioning of dermal myeloid cells. PLoS Pathog. 7:e1001323. doi:10.1371/ journal.ppat.1001323.
55. Stefanic S, Dvorak J, Horn M, Braschi S, Sojka D, Ruelas DS, Suzuki B, Lim KC, Hopkins SD, McKerrow JH, Caffrey CR. 2010. RNA interference in Schistosoma mansoni schistosomula: selectivity, sensitivity and operation for larger-scale screening. PLoS Negl. Trop. Dis. 4:e850.
56. Gray MJ, Poljakovic M, Kepka-Lenhart D, Morris SM, Jr. 2005. Induction of arginase I transcription by IL-4 requires a composite DNA response element for STAT6 and C/EBPbeta. Gene 353:98 -106.
57. Stutz AM, Pickart LA, Trifilieff A, Baumruker T, Prieschl-Strassmayr E, Woisetschlager M. 2003. The Th2 cell cytokines IL-4 and IL-13 regulate found in inflammatory zone 1/resistin-like molecule alpha gene expression by a STAT6 and CCAAT/enhancer-binding protein-dependent mechanism. J. Immunol. 170:1789-1796.
58. Welch JS, Escoubet-Lozach L, Sykes DB, Liddiard K, Greaves DR, Glass CK. 2002. TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J. Biol. Chem. 277: 42821- 42829.
59. Pauleau AL, Rutschman R, Lang R, Pernis A, Watowich SS, Murray PJ. 2004. Enhancer-mediated control of macrophage-specific arginase I expression. J. Immunol. 172:7565-7573.
60. Jaramillo M, Bellemare MJ, Martel C, Shio MT, Contreras AP, Godbout M, Roger M, Gaudreault E, Gosselin J, Bohle DS, Olivier M. 2009. Synthetic Plasmodium-like hemozoin activates the immune response: a morphology-function study. PLoS One 4:e6957. doi:10.1371/ journal.pone.0006