Treatment in vitro with PPARα and PPARγ ligands drives M1-to-M2 polarization of macrophages from T. cruzi-infected mice

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 5, 2015, Pages 893-904

  Penas, Federico ^a   Mirkin, Gerardo A ^a   Vera, Marcela ^a   Cevey, Ágata ^a   González, Cintia D ^a   Gómez, Marisa I ^a   Sales, María Elena ^b   Goren, Nora B ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b Centre de Estudios Farmacologicos y Botanicos   (Argentina)

Author keywords

Inflammatory mediators; Macrophage polarization; PPAR; Trypanosoma cruzi

Indexed keywords

15DPGJ 2; ARGINASE 1; CD36 ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MANNOSE RECEPTOR; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIRINIXIC ACID; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; 15-DEOXYPROSTAGLANDIN J2; ARG1 PROTEIN, MOUSE; ARGINASE; AUTACOID; BETA N ACETYLHEXOSAMINIDASE; CHI3L3 PROTEIN, MOUSE; CYTOKINE; LECTIN; LIGAND; NOS2 PROTEIN, MOUSE; PROSTAGLANDIN D2; PYRIMIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL VIABILITY; CHAGAS DISEASE; CONTROLLED STUDY; CYTOKINE RELEASE; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOMODULATION; IN VITRO STUDY; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MACROPHAGE POLARIZATION; MALE; MOUSE; NONHUMAN; PARASITE LOAD; PERITONEAL EXUDATE CELL; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRYPANOSOMA CRUZI; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CLASSIFICATION; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENETICS; HOST PATHOGEN INTERACTION; MACROPHAGE; METABOLISM; PARASITOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

MUS; TRYPANOSOMA CRUZI;

ANIMALS; ARGINASE; BETA-N-ACETYLHEXOSAMINIDASES; BLOTTING, WESTERN; CELLS, CULTURED; CHAGAS DISEASE; CYTOKINES; HOST-PATHOGEN INTERACTIONS; INFLAMMATION MEDIATORS; LECTINS; LIGANDS; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MICE, INBRED BALB C; MICROSCOPY, FLUORESCENCE; NITRIC OXIDE SYNTHASE TYPE II; PHAGOCYTOSIS; PPAR ALPHA; PPAR GAMMA; PROSTAGLANDIN D2; PYRIMIDINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSFORMING GROWTH FACTOR BETA; TRYPANOSOMA CRUZI;

EID: 84922553531     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.12.019     Document Type: Article

References (42)

1. Tanowitz H.B., Kirchhoff L.V., Simon D., Morris S.A., Weiss L.M., Wittner M. Chagas' disease. Clin. Microbiol. Rev. 1992, 5:400-419.
2. Van Ginderachter J.A., Movahedi K., Hassanzadeh Ghassabeh G., Meerschaut S., Beschin A., Raes G., De Baetselier P. Classical and alternative activation of mononuclear phagocytes: picking the best of both worlds for tumor promotion. Immunobiology 2006, 211:487-501.
3. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
4. Porcheray F., Viaud S., Rimaniol A.C., Leone C., Samah B., Dereuddre-Bosquet N., Dormont D., Gras G. Macrophage activation switching: an asset for the resolution of inflammation. Clin. Exp. Immunol. 2005, 142:481-489.
5. Mantovani A., Biswas S.K., Galdiero M.R., Sica A., Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 2013, 229:176-185.
6. Olefsky J.M., Glass C.K. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 2010, 72:219-246.
7. Straus D.S., Pascual G., Li M., Welch J.S., Ricote M., Hsiang C.H., Sengchanthalangsy L.L., Ghosh G., Glass C.K. 15-Deoxy-delta 12, 14-prostaglandin J2 inhibits multiple steps in the NF-kappa B signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4844-4849.
8. Hovsepian E., Penas F., Goren N. 15-Deoxy-delta12,14 PGJ2 but not rosiglitazone regulates MMP-9, NOS-2 and COX-2 expression and function by PPARgamma-dependent and independent mechanisms in cardiac cells. Shock 2010, 34:60-67.
9. Gardner O.S., Dewar B.J., Graves L.M. Activation of mitogen-activated protein kinases by peroxisome proliferator-activated receptor ligands: an example of nongenomic signaling. Mol. Pharmacol. 2005, 68:933-941.
10. Issemann I., Green S. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature 1990, 347:645-650.
11. Castrillo A., Tontonoz P. Nuclear receptors in macrophage biology: at the crossroads of lipid metabolism and inflammation. Annu. Rev. Cell Dev. Biol. 2004, 20:455-480.
12. Straus D.S., Glass C.K. Anti-inflammatory actions of PPAR ligands: new insights on cellular and molecular mechanisms. Trends Immunol. 2007, 28:551-558.
13. Delerive P., De Bosscher K., Besnard S., Vanden Berghe W., Peters J.M., Gonzalez F.J., Fruchart J.C., Tedgui A., Haegeman G., Staels B. Peroxisome proliferator-activated receptor α negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-κB and AP-1. J. Biol. Chem. 1999, 274:32048-32054.
14. Hourton D., Delerive P., Stankova J., Staels B., Chapman M.J., Ninio E. Oxidized low-density lipoprotein and peroxisome-proliferator-activated receptor α downregulate platelet-activating-factor receptor expression in human macrophages. Biochem. J. 2001, 354:225-232.
15. Bouhlel M.A., Derudas B., Rigamonti E., Dievart R., Brozek J., Haulon S., Zawadzki C., Jude B., Torpier G., Marx N., Staels B., Chinetti-Gbaguidi G. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab. 2007, 6:137-143.
16. Odegaard J.I., Ricardo-Gonzalez R.R., Goforth M.H., Morel C.R., Subramanian V., Mukundan L., Red Eagle A., Vats D., Brombacher F., Ferrante A.W., Chawla A. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 2007, 447:1116-1120.
17. Gallardo-Soler A., Gómez-Nieto C., Campo M.L., Marathe C., Tontonoz P., Castrillo A., Corraliza I. Arginase I induction by modified lipoproteins in macrophages: a peroxisome proliferator-activated receptor-gamma/delta-mediated effect that links lipid metabolism and immunity. Mol. Endocrinol. 2008, 22:1394-1402.
18. Fruchart J.C. Peroxisome proliferator-activated receptor-alpha (PPAR-alpha): at the crossroads of obesity, diabetes and cardiovascular disease. Atherosclerosis 2009, 205:1-8.
19. Mirkin G.A., Jones M., Sanz O.P., Rey R., Sica R.E., González Cappa S.M. Experimental Chagas' disease: electrophysiology and cell composition of the neuromyopathic inflammatory lesions in mice infected with a myotropic and a pantropic strain of Trypanosoma cruzi. Clin. Immunol. Immunopathol. 1994, 73:69-79.
20. de la Torre E., Hovsepian E., Penas F., Dmytrenko G., Castro M.E., Goren N., Sales M.E. Macrophages derived from septic mice modulate nitric oxide synthase and angiogenic mediators in the heart. J. Cell. Physiol. 2013, 228:1584-1593.
21. Hovsepian E., Mirkin G.A., Penas F., Manzano A., Bartrons R., Goren N.B. Modulation of inflammatory response and parasitism by 15-deoxy-δ12,14 prostaglandin J2 in Trypanosoma cruzi-infected cardiomyocytes. Int. J. Parasitol. 2011, 41:553-562.
22. Goren N., Cuenca J., Martin-Sanz P., Bosca L. Attenuation of NF-kappaB signalling in rat cardiomyocytes at birth restricts the induction of inflammatory genes. Cardiovasc. Res. 2004, 64:289-297.
23. Hovsepian E., Penas F., Siffo S., Mirkin G.A., Goren N. IL-10 inhibits the NF-κB and ERK/MAPK-mediated production of pro-inflammatory mediators by up-regulation of SOCS-3 in Trypanosoma cruzi-infected cardiomyocytes. PLoS One 2013, 8:e79445. (18).
24. Lefèvre L., Galès A., Olagnier D., Bernad J., Perez L., Burcelin R., Valentin A., Auwerx J., Pipy B., Coste A. PPARγ ligands switched high fat diet-induced macrophage M2b polarization toward M2a thereby improving intestinal Candida elimination. PLoS One 2010, 5:e12828.
25. Coste A., Dubourdeau M., Linas M.D., Cassaing S., Lepert J.C., Balard P., Chalmeton S., Bernad J., Orfila C., Séguéla J.P., Pipy B. PPARgamma promotes mannose receptor gene expression in murine macrophages and contributes to the induction of this receptor by IL-13. Immunity 2003, 19:329-339.
26. Gales A., Conduche A., Bernad J., Lefevre L., Olagnier D., Béraud M., Martin-Blondel G., Linas M.D., Auwerx J., Coste A., Pipy B. PPARgamma controls dectin-1 expression required for host antifungal defense against Candida albicans. PLoS Pathog. 2010, 6:e1000714.
27. Berry A., Balard P., Coste A., Olagnier D., Lagane C., Authier H., Benoit-Vical F., Lepert J.C., Séguéla J.P., Magnaval J.F., Chambon P., Metzger D., Desvergne B., Wahli W., Auwerx J., Pipy B. IL-13 induces expression of CD36 in human monocytes through PPARgamma activation. Eur. J. Immunol. 2007, 37:1642-1652.
28. Penas F., Mirkin G.A., Hovsepian E., Cevey A., Caccuri R., Sales M.E., Goren N.B. PPARγ ligand treatment inhibits cardiac inflammatory mediators induced by infection with different lethality strains of Trypanosoma cruzi. Biochim. Biophys. Acta 2013, 1832:239-248.
29. Adapala N., Chan M.M. Long-term use of an antiinflammatory, curcumin, suppressed type 1 immunity and exacerbated visceral leishmaniasis in a chronic experimental model. Lab. Investig. 2008, 88:1329-1339.
30. Nagajyothi F., Desruisseaux M.S., Machado F.S., Upadhya R., Zhao D., Schwartz G.J., Teixeira M.M., Albanese C., Lisanti M.P., Chua S.C., Weiss L.M., Scherer P.E., Tanowitz H.B. Response of adipose tissue to early infection with Trypanosoma cruzi (Brazil strain). J. Infect. Dis. 2012, 205:830-840.
31. Freire-de-Lima C.G., Nascimento D.O., Soares M.B., Bozza P.T., Castro-Faria-Neto H.C., de Mello F.G., DosReis G.A., Lopes M.F. Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 2000, 403:199-203.
32. Stempin C.C., Tanos T.B., Coso O.A., Cerbán F.M. Arginase induction promotes Trypanosoma cruzi intracellular replication in Cruzipain-treated J774 cells through the activation of multiple signaling pathways. Eur. J. Immunol. 2004, 34:200-209.
33. Garrido V.V., Dulgerian L.R., Stempin C.C., Cerbán F.M. The increase in mannose receptor recycling favors arginase induction and Trypanosoma cruzi survival in macrophages. Int. J. Biol. Sci. 2011, 7:1257-1272.
34. Huang J.T., Welch J.S., Ricote M., Binder C.J., Willson T.M., Kelly C., Witztum J.L., Funk C.D., Conrad D., Glass C.K. Interleukin-4-dependent production of PPAR-γ ligands in macrophages by 12/15-lipoxygenase. Nature 1999, 400:378-382.
35. Corraliza I.M., Soler G., Eichmann K., Modolell M. Arginase induction by suppressors of nitric oxide synthesis (IL-4, IL-10 and PGE2) in murine bone-marrow-derived macrophages. Biochem. Biophys. Res. Commun. 1995, 206:667-673.
36. Sorenson A.L., Poczobutt J., Amin J., Joyal T., Sullivan T., Crossno J.T., Weiser-Evans M.C., Nemenoff R.A. Activation of PPARγ in myeloid cells promotes lung cancer progression and metastasis. PLoS One 2011, 6:e28133.
37. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008, 13:453-461.
38. Bouhlel M.A., Brozek J., Derudas B., Zawadzki C., Jude B., Staels B., Chinetti-Gbaguidi G. Unlike PPARgamma, PPARalpha or PPARbeta/delta activation does not promote human monocyte differentiation toward alternative macrophages. Biochem. Biophys. Res. Commun. 2009, 386:459-462.
39. Lovren F., Pan Y., Quan A., Szmitko P.E., Singh K.K., Shukla P.C., Gupta M., Chan L., Al-Omran M., Teoh H., Verma S. Adiponectin primes human monocytes into alternative anti-inflammatory M2 macrophages. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:656-663.
40. Buroker N.E., Barboza J., Huang J.Y. The IkappaBalpha gene is a peroxisome proliferator activated receptor cardiac target gene. FEBS J. 2009, 276:3247-3255.
41. Fernandez-Boyanapalli R.F., Frasch S.C., McPhillips K., Vandivier R.W., Harry B.L., Riches D.W., Henson P.M., Bratton D.L. Impaired apoptotic cell clearance in CGD due to altered macrophage programming is reversed by phosphatidylserine-dependent production of IL-4. Blood 2009, 113:2047-2055.
42. Zhao X., Grotta J., Gonzales N., Aronowski J. Hematoma resolution as a therapeutic target: the role of microglia/macrophages. Stroke 2009, 40:92-94.