Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: A peroxisome proliferator-activated receptor-γ-mediated effect

Journal of Immunology

Volumn 173, Issue 6, 2004, Pages 4066-4074

  Skorokhod, Oleksii A ^a   Alessio, Massimo ^b   Mordmüller, Benjamin ^c   Arese, Paolo ^a   Schwarzer, Evelin ^a,d  

^a UNIVERSITY OF TURIN   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

15 HYDROXYICOSATETRAENOIC ACID; B7 ANTIGEN; CD40 ANTIGEN; CD83 ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HEMOZOIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; T6 ANTIGEN;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LIPID PEROXIDATION; MALARIA FALCIPARUM; MONOCYTE; NUCLEOTIDE SEQUENCE; OPSONIZATION; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 4644220083     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.6.4066     Document Type: Article

References (55)

1. Weidanz, W. P. 1982. Malaria and alterations in immune reactivity. Br. Med. Bull. 38:167.
2. Williamson, W. A., and B. M. Greenwood. 1978. Impairment of the immune response to vaccination after acute malaria. Lancet i:1328.
3. Usen, S., P. Milligan, C. Ethevenaux, B. M. Greenwood, and K. Mulholland. 2000. Effect of fever on the serum antibody response of Gambian children to Haemophilus influenzae type b conjugate vaccine. Pediatr. Infect. Dis. J. 19:444.
4. Urban, B. C., and D. J. Roberts. 2003. Inhibition of T cell functioning during malaria: implications for immunology and vaccinology. J. Exp. Med. 197:137.
5. Riley, E. M., P. H. Jakobsen, S. J. Allen, J. G. Wheeler, S. Bennett, S. Jepsen, and B. M. Greenwood. 1991. Immune response to soluble exoantigens of Plasmodium falciparum may contribute to both pathogenesis and protection in clinical malaria: evidence from a longitudinal, prospective study of semi-immune African children. Eur. J. Immunol. 21:1019.
6. Whittle, H. C., J. Brown, K. Marsh, B. M. Greenwood, P. Seidelin, H. Tighe, and L. Wedderburn. 1984. T-cell control of Epstein-Barr virus-infected B cells is lost during P. falciparum malaria. Nature 312:449.
7. Palucka, K. A., N. Taquet, F. Danchez-Chapuis, and J. C. Gluckman. 1998. Dendritic cells as the terminal stage of monocyte differentiation. J. Immunol. 160:4587.
8. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767.
9. Lanzavecchia, A., and F. Sallusto. 2001. Regulation of T cell immunity by dendritic cells. Cell. 106:263.
10. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and down-regulated by tumor necrosis factor a. J. Exp. Med. 179:1109.
11. Phu, N. H., N. Day, P. T. Diep, D. J. P. Ferguson, and N. J. White. 1995. Intraleucocytic malaria pigment and prognosis in severe malaria. Trans. R. Soc. Trop. Med. Hyg. 89:200.
12. Clark, H. C., and W. J. Tomlinson. 1949. The pathologic anatomy of malaria. In Malariology, Vol. 2. M. F. Boyd, ed. W.B. Saunders, Philadelphia, p. 874.
13. Schwarzer, E., M. Alessio, D. Ulliers, and P. Arese. 1998. Phagocytosis of malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes Infect. Immun. 66:1601.
14. Pichyangkul, S., P. Saengkrai, and H. K. Webster. 1994. Plasmodium falciparum pigment induces monocytes to release high levels of tumor necrosis factor-α and interleukin-1β. Am. J. Trop. Med. Hyg. 51:430.
15. Mordmüller, B., F. Turrini, H. Long, P. G. Kremsner, and P. Arese. 1998. Neutrophils and monocytes from patients with the Mediterranean G6PD mutation: constitutive and Plasmodium falciparum hemozoin-induced functions. Eur. Cytokine Network 6:239.
16. Scorza, T., S. Magez, L. Brys, and P. De Baetselier. 1999. Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunol. 21:545.
17. Lechmann, M., S. Berchtold, J. Hauber, and A. Steinkasserer. 2002. CD83 on dendritic cells: more than just a marker for maturation. Trends Immunol. 23:273.
18. Scholler, N., M. Hayden-Ledbetter, A. Dahlin, I. Hellstrom, K. E. Hellstrom, and J. A. Ledbetter. 2002. Cutting edge: CD83 regulates the development of cellular immunity. J. Immunol. 168:2599.
19. Ricote, M., J. T. Huang, J. S. Welch, and C. K. Glass. 1999. The peroxisome proliferator-activated receptor (PPARγ) as a regulator of monocyte/macrophage function. J. Leukocyte Biol. 66:733.
20. Clark, R. B. 2002. The role of PPARs in inflammation and immunity. J. Leukocyte Biol. 71:388.
21. Ammon, C., R. Mondal, R. Andreesen, and S. W. Krause. 2000. Differential expression of the transcription factor NF-κB during human mononuclear phagocyte differentiation to macrophages and dendritic cells. Biochem. Biophys. Res. Commun. 268:99.
22. Ardeshna, K. M., A. R. Pizzey, S. Devereux, and A. Khwaja. 2000. The PI3 kinase, p38 SAP kinase, and NF-κB signal transduction pathways are involved in the survival and maturation of lipopolysaccharide-stimulated human monocyte-derived dendritic cells. Blood 96:1039.
23. Shankaranarayanan, P., and S. Nigam. 2003. IL-4 induces apoptosis in A549 lung adenocarcinoma cells: evidence for the pivotal role of 15-hydroxyeicosatetraenoic acid binding to activated peroxisome proliferator-activated receptor γ transcription factor. J. Immunol. 170:887.
24. Schwarzer, E., E. Kühn, E. Valente, and P. Arese. 2003. Malaria-parasitized erythrocytes and hemozoin nonenzymatically generate large amounts of hydroxy-fatty acids that inhibit monocyte functions. Blood 101:722.
25. Schwarzer, E., F. Turrini, D. Ulliers, G. Giribaldi, H. Ginsburg, and P. Arese. 1992. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J. Exp. Med. 176:1033.
26. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911.
27. Davitz, M. A., D. Hereld, S. Shak, J. Krakow, P. T. Englund, and V. Nussenzweig. 1987. A glycan-phosphatidylinositol-specific phospholipase D in human serum. Science 238:81.
28. Schwarzer, E., F. Turrini, and P. Arese. 1994. A luminescence method for the quantitative determination of phagocytosis of erythrocytes, of malaria-parasitized erythrocytes and of malarial pigment. Br. J. Haematol. 88:740.
29. Hertz, C., S. Kiertscher, P. Godowski, D. Bouis, M. Norgard, M. Roth, and R. Modlin. 2001. Microbial lipopeptides stimulate dendritic cell maturation via Toll-like receptor 2. J. Immunol. 166:2444.
30. Corte, G., F. Calabi, G. Damiani, A. Bargellesi, R. Tosi, and R. Sorrentino. 1981. Human Ia molecules carrying DC1 determinants differ in both α- and β-subunits from Ia molecules carrying DR determinants. Nature 292:357.
31. Kruse, M., O. Rosorius, F. Kratzer, D. Bevec, C. Kuhnt, A. Steinkasserer, G. Schuler, and J. Hauber. 2000. Inhibition of CD83 cell surface expression during dendritic cell maturation by interference with nuclear export of CD83 mRNA. J. Exp. Med. 191:1581.
32. Jowsey, I. R., P. R. Murdock, G. B. Moore, G. J. Murphy, S. A. Smith, and J. D. Hayes. 2003. Prostaglandin D2 synthase enzymes and PPARγ are coexpressed in mouse 3T3-L1 adipocytes and human tissues. Prostaglandins Lipid Med. 70:267.
33. Daynes, R. A., and D. C. Jones. 2002. Emerging roles of PPARS in inflammation and immunity. Nature Rev. Immunol. 2:748.
34. Hirano, F., M. Chung, H. Tanaka, N. Maruyama, I. Makino, D. D. Moore, and C. Scheidereit. 1998. Alternative splicing variants of IκBβ establish differential NF-κB signal responsiveness in human cells. Mol. Cell Biol. 18:2596.
35. Schwarzer, E., G. Bellomo, G. Giribaldi, D. Ulliers, and P. Arese. 2001. Phagocytosis of malarial pigment haemozoin by human monocytes: a confocal microscopy study. Parasitology 117:125.
36. Schwarzer, E., F. De Matteis, G. Giribaldi, D. Ulliers, E. Valente, and P. Arese. 1999. Hemozoin stability and dormant induction of heme oxygenase in hemozoin-fed human monocytes. Mol. Biochem. Parasitol. 100:61.
37. Angeli, V., H. Hammad, B. Staels, M. Capron, B. N. Lambrecht, and F. Trottein. 2003. Peroxisome proliferator-activated receptor γ inhibits the migration of dendritic cells: consequences for the immune response. J. Immunol. 170:5295.
38. Nencioni, A., F. Grünebach, A. Zobywlaski, C. Denzlinger, W. Brugger, and P. Brossart. 2002. Dendritic cell immunogenicity is regulated by peroxisome proliferator-activated receptor γ. J. Immunol. 169:1228.
39. Gosset, P., A.-S. Charbonnier, P. Delerive, J. Fontaine, B. Staels, J. Pestel, A.-B. Tonnel, and F. Trotteln. 2001. Peroxisome proliferator-activated receptor γ activators affect the maturation of human monocyte-derived dendritic cells. Eur. J. Immunol. 31:2857.
40. Nagy, L., P. Tontonoz, J. G. Alvarez, H. Chen, and R. M. Evans. 1998. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARγ. Cell. 93:229.
41. Shappell, S. B., R. A. Gupta, S. Manning, R. Whitehead, W. E. Boeglin, C. Schneider, T. Case, J. Price, G. S. Jack, T. M. Wheeler, et al. 2001. 15S-hydroxyeicosatetraenoic acid activates peroxisome proliferator-activated receptor γ and inhibits proliferation in PC3 prostate carcinoma cells. Cancer Res. 61:497.
42. Schild, R. L., W. T. Schaiff, M. G. Carlson, E. J. Cronbach, D. M. Nelson, and Y. Sadovsky. 2002. The activity of PPARγ in primary human trophoblasts is enhanced by oxidized lipids. J. Clin. Endocrinol. Metab. 87:1105.
43. Pizzimenti, S., S. Laurora, F. Briatore, C. Ferretti, M. U. Dianzani, and G. Barrera. 2002. Synergistic effect of 4-hydroxynonenal and PPAR ligands in controlling human leukemic cell growth and differentiation. Free Radical Biol. Med. 32:233.
44. Schwarzer, E., O. Müller, P. Arese, W. G. Siems, and T. Grune. 1996. Increased levels of 4-hydroxynonenal in human monocytes fed with malarial pigment hemozoin. FEBS Lett. 388:119.
45. Tachado, S., P. Gerold, R. Schwarz, S. Novakovic, M. McConville, and L. Schofield. 1997. Signal transduction in macrophages by glycosylphosphatidylinositols of Plasmodium, Trypanosoma, and Leishmania: activation of protein tyrosine kinases and protein kinase C by inositolglycan and diacylglycerol moieties. Proc. Natl. Acad. Sci. USA 94:4022.
46. Naik, R. S., O. H. Branch, A. S. Woods, M. Vijaykumar, D. J. Perkins, B. L. Nahlen, R. J. Lal, C. E. Costello, C. F. Ockenhouse, E. A. Davidson, and D. C. Gowda. 2000. Glycosylphosphatidylinositol anchors of Plasmodium falciparum: molecular characterization and naturally elicited antibody response that may provide immunity to malaria pathogenesis. J. Exp. Med. 192:1563.
47. + DCs. Proc. Natl. Acad. Sci. USA 93:2588.
48. Underhill, D. M., and A. Ozinsky. 2002. Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14:103.
49. Zhang, X., and H. A. Young. 2002. PPAR and immune system: what do we know? Intern. Immunopharmacol. 2:1029.
50. Suzawa, M., I. Takada, J. Yanagisawa, F. Ohtake, S. Ogawa, T. Yamauchi, T. Kadowaki, Y. Takeuchi, H. Shibuya, Y. Gotoh, et al. 2003. Cytokines suppress adipogenesis and PPAR-γ function through the TAK1/TAB1/NIK cascade. Nature Cell Biol. 5:224.
51. O'Sullivan, B., and R. Thomas. 2003. CD40 and dendritic cell function. Crit. Rev. Immunol. 23:83.
52. Moodycliffe, A. M., V. Shreedhar, S. E. Ullrich, J. Walterscheid, C. Bucana, M. L. Kripke, and L. Flores-Romo. 2000. CD40-CD40 ligand interactions in vivo regulate migration of antigen-bearing dendritic cells from the skin to draining lymph nodes. J. Exp. Med. 91:2011.
53. Celia, M., F. Sallusto, and A. Lanzavecchia. 1997. Origin, maturation and antigen presenting function of dendritic cells. Curr. Opin. Immunol. 9:10.
54. Urban, B. C., D. J. Ferguson, A. Pain, N. Willcox, M. Plebanski, J. M. Austyn, and D. I. Roberts. 1999. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400:73.
55. Coban, C., K. J. Ishii, D. J. Sullivan, and N. Kumar. 2002. Purified malaria pigment (hemozoin) enhances dendritic cell maturation and modulates the isotype of antibodies induced by a DNA vaccine. Infect. Immun. 70:3939.