Nrf2, a pparγ alternative pathway to promote cd36 expression on inflammatory macrophages: Implication for malaria

PLoS Pathogens

Volumn 7, Issue 9, 2011, Pages

  Olagnier, David ^a   Lavergne, Rose Anne ^a   Meunier, Etienne ^a   Lefèvre, Lise ^a   Dardenne, Christophe ^a   Aubouy, Agnès ^a   Benoit Vical, Françoise ^b   Ryffel, Bernhard ^c   Coste, Agnès ^a   Berry, Antoine ^a   Pipy, Bernard ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b LCC LABORATOIRE DE CHIMIE DE COORDINATION   (France)

^c Laboratoire d'Immunologie et Embryologie Moleculaires Orleans   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; NFE2L2 PROTEIN, HUMAN; NFE2L2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DOWN REGULATION; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; MALARIA; MONOCYTE; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; ERYTHROCYTE; FEMALE; GENETICS; IMMUNOLOGY; MALARIA FALCIPARUM; METABOLISM; MOUSE; PARASITOLOGY; PHAGOCYTOSIS; TRANSGENIC MOUSE;

MURINAE; PLASMODIUM FALCIPARUM;

ANIMALS; ANTIGENS, CD36; DOWN-REGULATION; ERYTHROCYTES; FEMALE; HUMANS; MACROPHAGES; MALARIA, FALCIPARUM; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-E2-RELATED FACTOR 2; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PPAR GAMMA;

EID: 80053490263     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002254     Document Type: Article

References (38)

1. Trinchieri G, Sher A, (2007) Cooperation of Toll-like receptor signals in innate immune defence. Nat Rev Immunol 7: 179-190.
2. Greenberg ME, Sun M, Zhang R, Febbraio M, Silverstein R, et al. (2006) Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J Exp Med 203: 2613-2625.
3. Baranova IN, Kurlander R, Bocharov AV, Vishnyakova TG, Chen Z, et al. (2008) Role of human CD36 in bacterial recognition, phagocytosis, and pathogen-induced JNK-mediated signaling. J Immunol 181: 7147-7156.
4. Serghides L, Kain KC, (2001) Peroxisome proliferator-activated receptor gamma-retinoid X receptor agonists increase CD36-dependent phagocytosis of Plasmodium falciparum-parasitized erythrocytes and decrease malaria-induced TNF-alpha secretion by monocytes/macrophages. J Immunol 166: 6742-6748.
5. Patel SN, Lu Z, Ayi K, Serghides L, Gowda DC, et al. (2007) Disruption of CD36 impairs cytokine response to Plasmodium falciparum glycosylphosphatidylinositol and confers susceptibility to severe and fatal malaria in vivo. J Immunol 178: 3954-3961.
6. Nagy L, Tontonoz P, Alvarez JG, Chen H, Evans RM, (1998) Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell 93: 229-240.
7. Huang JT, Welch JS, Ricote M, Binder CJ, Willson TM, et al. (1999) Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature 400: 378-382.
8. Berry A, Balard P, Coste A, Olagnier D, Lagane C, et al. (2007) IL-13 induces expression of CD36 in human monocytes through PPARgamma activation. Eur J Immunol 37: 1642-1652.
9. Serghides L, Patel SN, Ayi K, Lu Z, Gowda DC, et al. (2009) Rosiglitazone modulates the innate immune response to Plasmodium falciparum infection and improves outcome in experimental cerebral malaria. J Infect Dis 199: 1536-1545.
10. Stevenson MM, Riley EM, (2004) Innate immunity to malaria. Nat Rev Immunol 4: 169-180.
11. Lyke KE, Burges R, Cissoko Y, Sangare L, Dao M, et al. (2004) Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect Immun 72: 5630-5637.
12. Berry A, Chene G, Benoit-Vical F, Lepert JC, Bernad J, et al. (2005) Ex vivo and in vitro impairment of CD36 expression and tumor necrosis factor-alpha production in human monocytes in response to Plasmodium falciparum-parasitized erythrocytes. J Parasitol 91: 316-322.
13. Boyer JF, Balard P, Authier H, Faucon B, Bernad J, et al. (2007) Tumor necrosis factor alpha and adalimumab differentially regulate CD36 expression in human monocytes. Arthritis Res Ther 9: R22.
14. Nakagawa T, Nozaki S, Nishida M, Yakub JM, Tomiyama Y, et al. (1998) Oxidized LDL increases and interferon-gamma decreases expression of CD36 in human monocyte-derived macrophages. Arterioscler Thromb Vasc Biol 18: 1350-1357.
15. Necela BM, Su W, Thompson EA, (2008) Toll-like receptor 4 mediates cross-talk between peroxisome proliferator-activated receptor gamma and nuclear factor-kappaB in macrophages. Immunology 125: 344-358.
16. Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Yamamoto M, et al. (2006) Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest 116: 984-995.
17. D'Archivio M, Scazzocchio B, Filesi C, Vari R, Maggiorella MT, et al. (2008) Oxidised LDL up-regulate CD36 expression by the Nrf2 pathway in 3T3-L1 preadipocytes. FEBS Lett 582: 2291-2298.
18. Ishii T, Itoh K, Ruiz E, Leake DS, Unoki H, et al. (2004) Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal. Circ Res 94: 609-616.
19. Sussan TE, Jun J, Thimmulappa R, Bedja D, Antero M, et al. (2008) Disruption of Nrf2, a key inducer of antioxidant defenses, attenuates ApoE-mediated atherosclerosis in mice. PLoS One 3: e3791.
20. Su Z, Fortin A, Gros P, Stevenson MM, (2002) Opsonin-independent phagocytosis: an effector mechanism against acute blood-stage Plasmodium chabaudi AS infection. J Infect Dis 186: 1321-1329.
21. Artavanis-Tsakonas K, Tongren JE, Riley EM, (2003) The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin Exp Immunol 133: 145-152.
22. Memon RA, Feingold KR, Moser AH, Fuller J, Grunfeld C, (1998) Regulation of fatty acid transport protein and fatty acid translocase mRNA levels by endotoxin and cytokines. Am J Physiol 274: E210-217.
23. Yesner LM, Huh HY, Pearce SF, Silverstein RL, (1996) Regulation of monocyte CD36 and thrombospondin-1 expression by soluble mediators. Arterioscler Thromb Vasc Biol 16: 1019-1025.
24. 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.
25. Chuang PC, Wu MH, Shoji Y, Tsai SJ, (2009) Downregulation of CD36 results in reduced phagocytic ability of peritoneal macrophages of women with endometriosis. J Pathol 219: 232-241.
26. Coste A, Dubourdeau M, Linas MD, Cassaing S, Lepert JC, et al. (2003) PPARgamma promotes mannose receptor gene expression in murine macrophages and contributes to the induction of this receptor by IL-13. Immunity 19: 329-339.
27. Afif H, Benderdour M, Mfuna-Endam L, Martel-Pelletier J, Pelletier JP, et al. (2007) Peroxisome proliferator-activated receptor gamma1 expression is diminished in human osteoarthritic cartilage and is downregulated by interleukin-1beta in articular chondrocytes. Arthritis Res Ther 9: R31.
28. Mracek T, Cannon B, Houstek J, (2004) IL-1 and LPS but not IL-6 inhibit differentiation and downregulate PPAR gamma in brown adipocytes. Cytokine 26: 9-15.
29. Zhou M, Wu R, Dong W, Jacob A, Wang P, (2008) Endotoxin downregulates peroxisome proliferator-activated receptor-gamma via the increase in TNF-alpha release. Am J Physiol Regul Integr Comp Physiol 294: R84-92.
30. Katayama K, Wada K, Nakajima A, Mizuguchi H, Hayakawa T, et al. (2003) A novel PPAR gamma gene therapy to control inflammation associated with inflammatory bowel disease in a murine model. Gastroenterology 124: 1315-1324.
31. Lewis JD, Lichtenstein GR, Stein RB, Deren JJ, Judge TA, et al. (2001) An open-label trial of the PPAR-gamma ligand rosiglitazone for active ulcerative colitis. Am J Gastroenterol 96: 3323-3328.
32. Dubuquoy L, Jansson EA, Deeb S, Rakotobe S, Karoui M, et al. (2003) Impaired expression of peroxisome proliferator-activated receptor gamma in ulcerative colitis. Gastroenterology 124: 1265-1276.
33. Boggild AK, Krudsood S, Patel SN, Serghides L, Tangpukdee N, et al. (2009) Use of peroxisome proliferator-activated receptor gamma agonists as adjunctive treatment for Plasmodium falciparum malaria: a randomized, double-blind, placebo-controlled trial. Clin Infect Dis 49: 841-849.
34. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, et al. (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236: 313-322.
35. Trager W, Jensen JB, (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
36. Benoit-Vical F, Lelievre J, Berry A, Deymier C, Dechy-Cabaret O, et al. (2007) Trioxaquines are new antimalarial agents active on all erythrocytic forms, including gametocytes. Antimicrob Agents Chemother 51: 1463-1472.
37. Galès A, Conduche A, Bernad J, Lefevre L, Olagnier D, et al. (2010) PPARgamma controls dectin-1 expression required for host antifungal defense against Candida albicans. PLoS Pathog 6: e1000714.
38. Lefèvre L, Galès A, Olagnier D, Bernad J, Perez L, et al. (2010) PPARgamma ligands switched high fat diet-induced macrophage M2b polarization toward M2a thereby improving intestinal Candida elimination. PLoS One 5: e12828.