Induction of transglutaminase 2 by a liver X receptor/retinoic acid receptor α pathway increases the clearance of apoptotic cells by human Macrophages

Circulation Research

Volumn 105, Issue 4, 2009, Pages 393-401

  Rébé, Cédric ^a,d,e   Raveneau, Magalie ^a   Chevriaux, Angélique ^a   Lakomy, Daniela ^a   Sberna, Anne Laure ^a   Costa, Annie ^a   Bessède, Ginette ^a   Athias, Anne ^a   Steinmetz, Eric ^a   Lobaccaro, Jean Marc A ^b   Alves, Georges ^b   Menicacci, Alexandre ^c   Vachenc, Sébastien ^c   Solary, Eric ^a   Gambert, Philippe ^a   Masson, David ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

^c Solvay Pharmaceuticals   (France)

^d CENTRE GEORGES FRANÇOIS LECLERC   (France)

^e Chu   (France)

Author keywords

LXR; Macrophages; Phagocytosis; RAR; Transglutaminase

Indexed keywords

4 [(5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 NAPHTHYL)CARBOXAMIDO]BENZOIC ACID; LIVER X RECEPTOR; MESSENGER RNA; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; RETINOIC ACID RECEPTOR ALPHA; CELL RECEPTOR; DNA BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RETINOIC ACID RECEPTOR;

APOPTOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; CELL ACTIVATION; GENE EXPRESSION; GENE SILENCING; HEART MUSCLE CAPILLARY; HUMAN; HUMAN CELL; MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; ATHEROSCLEROSIS; BIOSYNTHESIS; CELL LINE; DRUG POTENTIATION; ENZYME INDUCTION; ENZYMOLOGY; MACROPHAGE ACTIVATION; METABOLISM;

APOPTOSIS; ATHEROSCLEROSIS; CELL LINE; DNA-BINDING PROTEINS; ENZYME INDUCTION; GTP-BINDING PROTEINS; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES; PHAGOCYTOSIS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, RETINOIC ACID; TRANSGLUTAMINASES;

EID: 70349237816     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.201855     Document Type: Article

References (40)

1. Repa JJ, Mangelsdorf DJ. The role of orphan nuclear receptors in the regulation of cholesterol homeostasis. Annu Rev Cell Dev Biol. 2000;16: 459-481.
2. Janowski BA, Willy PJ, Devi TR, Falck JR, Mangelsdorf DJ. An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature. 1996;383:728-731.
3. Zelcer N, Tontonoz P. Liver X receptors as integrators of metabolic and inflammatory signaling. J Clin Invest. 2006;116:607-614.
4. Rigamonti E, Chinetti-Gbaguidi G, Staels B. Regulation of macrophage functions by PPAR-alpha, PPAR-gamma, and LXRs in mice and men. Arterioscler Thromb Vasc Biol. 2008;28:1050-1059.
5. Costet P, Luo Y, Wang N, Tall AR. Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor. J Biol Chem. 2000;275:28240-28245.
6. Kennedy MA, Venkateswaran A, Tarr PT, Xenarios I, Kudoh J, Shimizu N, Edwards PA. Characterization of the human ABCG1 gene: liver X receptor activates an internal promoter that produces a novel transcript encoding an alternative form of the protein. J Biol Chem. 2001;276: 39438-39447. (Pubitemid 37371322)
7. Mak PA, Laffitte BA, Desrumaux C, Joseph SB, Curtiss LK, Mangelsdorf DJ, Tontonoz P, Edwards PA. Regulated expression of the apolipoprotein E/C-I/C-IV/C-II gene cluster in murine and human macrophages. A critical role for nuclear liver X receptors alpha and beta. J Biol Chem. 2002;277:31900-33190
8. Joseph SB, Castrillo A, Laffitte BA, Mangelsdorf DJ, Tontonoz P. Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat Med. 2003;9:213-219.
9. Joseph SB, Bradley MN, Castrillo A, Bruhn KW, Mak PA, Pei L, Hogenesch J, O'Connell RM, Cheng G, Saez E, Miller JF, Tontonoz P. LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell. 2004;119:299-309.
10. Fontaine C, Rigamonti E, Nohara A, Gervois P, Teissier E, Fruchart JC, Staels B, Chinetti-Gbaguidi G. Liver X receptor activation potentiates the lipopolysaccharide response in human macrophages. Circ Res. 2007;101: 40-49.
11. Myhre AE, Agren J, Dahle MK, Tamburstuen MV, Lyngstadaas SP, Collins AJ, Foster SJ, Thiemermann C, Aasen AO, Wang JE. Liver X receptor is a key regulator of cytokine release in human monocytes. Shock. 2008;29:468-474.
12. Laffitte BA, Joseph SB, Walczak R, Pei L, Wilpitz DC, Collins JL, Tontonoz P. Autoregulation of the human liver X receptor alpha promoter. Mol Cell Biol. 2001;21:7558-7568.
13. Seo JB, Moon HM, Kim WS, Lee YS, Jeong HW, Yoo EJ, Ham J, Kang H, Park MG, Steffensen KR, Stulnig TM, Gustafsson JA, Park SD, Kim JB. Activated liver X receptors stimulate adipocyte differentiation through induction of peroxisome proliferator-activated receptor gamma expression. Mol Cell Biol. 2004;24:3430-3444.
14. Tangirala RK, Bischoff ED, Joseph SB, Wagner BL, Walczak R, Laffitte BA, Daige CL, Thomas D, Heyman RA, Mangelsdorf DJ, Wang X, Lusis AJ, Tontonoz P, Schulman IG. Identification of macrophage liver X receptors as inhibitors of atherosclerosis. Proc Natl Acad Sci U S A. 2002;99:11896-11901.
15. Edwards PA, Kast HR, Anisfeld AM. BAREing it all: the adoption of LXR and FXR and their roles in lipid homeostasis. J Lipid Res. 2002; 43:2-12.
16. Hjalt TA, Murray JC. Genomic structure of the human retinoic acid receptor-alpha1 gene. Mamm Genome. 1999;10:528-529.
17. Parrado A, Despouy G, Kraiba R, Le Pogam C, Dupas S, Choquette M, Robledo M, Larghero J, Bui H, Le Gall I, Rochette-Egly C, Chomienne C, Padua RA. Retinoic acid receptor alpha1 variants, RARalpha1DeltaB and RARalpha1DeltaBC, define a new class of nuclear receptor isoforms. Nucleic Acids Res. 2001;29:4901-4908.
18. Brand NJ, Petkovich M, Chambon P. Characterization of a functional promoter for the human retinoic acid receptor-alpha (hRAR-alpha). Nucleic Acids Res. 1990;18:6799-6806.
19. Frankenberger M, Hauck RW, Frankenberger B, Haussinger K, Maier KL, Heyder J, Ziegler-Heitbrock HW. All trans-retinoic acid selectively down-regulates matrix metalloproteinase-9 (MMP-9) and up-regulates tissue inhibitor of metalloproteinase-1 (TIMP-1) in human bronchoalveolar lavage cells. Mol Med. 2001;7:263-270.
20. Kubo A, Minamino N, Isumi Y, Katafuchi T, Kangawa K, Dohi K, Matsuo H. Production of adrenomedullin in macrophage cell line and peritoneal macrophage. J Biol Chem. 1998;273:16730-16738.
21. Becker PS, Li Z, Potselueva T, Madri JA, Newburger PE, Berliner N. Laminin promotes differentiation of NB4 promyelocytic leukemia cells with all-trans retinoic acid. Blood. 1996;88:261-267.
22. Kutty RK, Kutty G, Samuel W, Duncan T, Bridges CC, El-Sherbeeny A, Nagineni CN, Smith SB, Wiggert B. Molecular characterization and developmental expression of NORPEG, a novel gene induced by retinoic acid. J Biol Chem. 2001;276:2831-2840.
23. Nagy L, Saydak M, Shipley N, Lu S, Basilion JP, Yan ZH, Syka P, Chandraratna RA, Stein JP, Heyman RA, Davies PJ. Identification and characterization of a versatile retinoid response element (retinoic acid receptor response element-retinoid X receptor response element) in the mouse tissue transglutaminase gene promoter. J Biol Chem. 1996;271: 4355-4365.
24. Szondy Z, Sarang Z, Molnar P, Nemeth T, Piacentini M, Mastroberardino PG, Falasca L, Aeschlimann D, Kovacs J, Kiss I, Szegezdi E, Lakos G, Rajnavolgyi E, Birckbichler PJ, Melino G, Fesus L. Transglutaminase 2-/- mice reveal a phagocytosis-associated crosstalk between macrophages and apoptotic cells. Proc Natl Acad Sci U S A. 2003;100: 7812-7817.
25. Falasca L, Iadevaia V, Ciccosanti F, Melino G, Serafino A, Piacentini M. Transglutaminase type II is a key element in the regulation of the antiinflammatory response elicited by apoptotic cell engulfment. J Immunol. 2005;174:7330-7340.
26. Fontaine C, Rigamonti E, Pourcet B, Duez H, Duhem C, Fruchart JC, Chinetti-Gbaguidi G, Staels B. The nuclear receptor Rev-erbalpha is a liver X receptor (LXR) target gene driving a negative feedback loop on select LXR-induced pathways in human macrophages. Mol Endocrinol. 2008;22:1797-1811.
27. Chawla A, Boisvert WA, Lee CH, Laffitte BA, Barak Y, Joseph SB, Liao D, Nagy L, Edwards PA, Curtiss LK, Evans RM, Tontonoz P. A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol Cell. 2001;7:161-171.
28. Mark M, Ghyselinck NB, Chambon P. Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu Rev Pharmacol Toxicol. 2006;46:451-480.
29. Fesus L, Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci. 2002;27:534-539.
30. Zhang LX, Mills KJ, Dawson MI, Collins SJ, Jetten AM. Evidence for the involvement of retinoic acid receptor RAR alpha-dependent signaling pathway in the induction of tissue transglutaminase and apoptosis by retinoids. J Biol Chem. 1995;270:6022-6029.
31. Murtaugh MP, Arend WP, Davies PJ. Induction of tissue transglutaminase in human peripheral blood monocytes. J Exp Med. 1984;159: 114-125.
32. Hamon Y, Broccardo C, Chambenoit O, Luciani MF, Toti F, Chaslin S, Freyssinet JM, Devaux PF, McNeish J, Marguet D, Chimini G. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol. 2000;2:399-406.
33. Huq MD, Tsai NP, Gupta P, Wei LN. Regulation of retinal dehydrogenases and retinoic acid synthesis by cholesterol metabolites. EMBO J. 2006;25:3203-3213.
34. Szatmari I, Pap A, Ruhl R, Ma JX, Illarionov PA, Besra GS, Rajnavolgyi E, Dezso B, Nagy L. PPARgamma controls CD1d expression by turning on retinoic acid synthesis in developing human dendritic cells. J Exp Med. 2006;203:2351-2362.
35. Szanto A, Benko S, Szatmari I, Balint BL, Furtos I, Ruhl R, Molnar S, Csiba L, Garuti R, Calandra S, Larsson H, Diczfalusy U, Nagy L. Transcriptional regulation of human CYP27 integrates retinoid, peroxisome proliferator-activated receptor, and liver X receptor signaling in macrophages. Mol Cell Biol. 2004;24:8154-8166.
36. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler Thromb Vasc Biol. 2005;25:2255-2264.
37. Boisvert WA, Rose DM, Boullier A, Quehenberger O, Sydlaske A, Johnson KA, Curtiss LK, Terkeltaub R. Leukocyte transglutaminase 2 expression limits atherosclerotic lesion size. Arterioscler Thromb Vasc Biol. 2006;26:563-569.
38. Wuttge DM, Romert A, Eriksson U, Torma H, Hansson GK, Sirsjo A. Induction of CD36 by all-trans retinoic acid: retinoic acid receptor signaling in the pathogenesis of atherosclerosis. FASEB J. 2001;15: 1221-1223.
39. Garcia-Cruset S, Carpenter KL, Guardiola F, Stein BK, Mitchinson MJ. Oxysterol profiles of normal human arteries, fatty streaks and advanced lesions. Free Radic Res. 2001;35:31-41.
40. Tanaka M, Miyake Y. Apoptotic cell clearance and autoimmune disorder. Curr Med Chem. 2007;14:2892-2897.