Macrophages engulfing apoptotic thymocytes produce retinoids to promote selection, differentiation, removal and replacement of double positive thymocytes

Immunobiology

Volumn 218, Issue 11, 2013, Pages 1354-1360

  Sarang, Zsolt ^a   Garabuczi, Éva ^a   Joós, Gergely ^a   Kiss, Beáta ^a   Tóth, Katalin ^a   Rühl, Ralph ^a   Szondy, Zsuzsa ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Apoptosis; Engulfment; Macrophages; Retinaldehyde dehydrogenase; Retinoic acid; Thymus

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CELLULAR RETINOL BINDING PROTEIN 1; CELLULAR RETINOL BINDING PROTEIN 2; LACTADHERIN; LECITHIN RETINOL ACYLTRANSFERASE; PHOSPHATIDYLSERINE; PROTEIN S; RETINOIC ACID BINDING PROTEIN; RETINOID; RETINOL ACYLTRANSFERASE; T LYMPHOCYTE RECEPTOR; THROMBOSPONDIN 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; HUMAN; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; PHAGOCYTOSIS; PRIORITY JOURNAL; T LYMPHOCYTE; THYMOCYTE; THYMUS;

9-CIS RA; 9-CIS RETINOIC ACID; ACYL-COA:RETINOL ACYLTRANSFERASE; ADH; ALCOHOL DEHYDROGENASE; ALL-TRANS RETINOIC ACID; ALL-TRANS-DIHYDRORETINOIC ACID; ALL-TRANS-DRA; APOPTOSIS; ARAT; ATRA; BAI1; BRAIN-SPECIFIC ANGIOGENESIS INHIBITOR 1; CELLULAR RETINOIC ACID-BINDING PROTEIN; CELLULAR RETINOL-BINDING PROTEIN; CRABP; CRBP; ENGULFMENT; GAS6; GROWTH ARREST-SPECIFIC-6; LECITHIN:RETINOL ACYLTRANSFERASE; LIVER X RECEPTOR; LRAT; LXR; MACROPHAGES; MAJOR HISTOCOMPATIBILITY COMPLEX; MFG-E8; MHC; MILK FAT GLOBULE EGF-FACTOR 8; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PHOSPHATIDYLSERINE; PPAR; PS; RA; RALDH; RAR; RARE; RBP; RETINALDEHYDE DEHYDROGENASE; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOIC ACID RESPONSE ELEMENT; RETINOID X RECEPTOR; RETINOL SATURASE; RETINOL-BINDING PROTEIN; RETSAT; RXR; RXR RESPONSE ELEMENT; RXRE; SCAVENGER RECEPTOR; SDR; SHORT-CHAIN DEHYDROGENASE/REDUCTASE; SR; T CELL RECEPTOR; T-CELL IMMUNOGLOBULIN- AND MUCIN-DOMAIN-CONTAINING MOLECULE; TCR; TEC; TG2; THYMIC EPITHELIAL CELL; THYMUS; TIM4; TRANSGLUTAMINASE 2;

APOPTOSIS; CELL DIFFERENTIATION; HUMANS; MACROPHAGES; PHAGOCYTOSIS; RETINOIDS; THYMOCYTES; THYMUS GLAND;

EID: 84884127640     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2013.06.009     Document Type: Article

References (82)

1. Abu-Abed S.S., Beckett B.R., Chiba H., Chithalen J.V., Jones G., Metzger D., Chambon P., Petkovich M. Mouse P450RAI (CYP26) expression and retinoic acid-inducible retinoic acid metabolism in F9 cells are regulated by retinoic acid receptor gamma and retinoid X receptor alpha. J. Biol. Chem. 1998, 273:2409-24015.
2. A-Gonzalez N., Bensinger S.J., Hong C., Beceiro S., Bradley M.N., Zelcer N., Deniz J., Ramirez C., Díaz M., Gallardo G., de Galarreta C.R., Salazar J., Lopez F., Edwards P., Parks J., Andujar M., Tontonoz P., Castrillo A. Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 2009, 31:245-258.
3. Alexandropoulos K., Danzi N.M. Thymic epithelial cells: antigen presenting cells that regulate T cell repertoire and tolerance development. Immunol. Res. 2012, 54:177-190.
4. Anderson M.S., Venanzi E.S., Klein L., Chen Z., Berzins S.P., Turley S.J., von Boehmer H., Bronson R., Dierich A., Benoist C., Mathis D. Projection of an immunological self shadow within the thymus by the aire protein. Science 2002, 298:1395-1401.
5. Benoist C., Mathis D. Treg cells, life history, and diversity. Cold Spring Harb. Perspect. Biol. 2011, 4:a007021. 2012.
6. Benson M.J., Pino-Lagos K., Rosemblatt M., Noelle R.J. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 2007, 204:1765-1774.
7. Blanco J.C., Minucci S., Lu J., Yang X.J., Walker K.K., Chen H., Evans R.M., Nakatani Y., Ozato K. The histone acetylase PCAF is a nuclear receptor coactivator. Genes Dev. 1998, 12:1638-1651.
8. Bommhardt U., Beyer M., Hünig T., Reichardt H.M. Molecular andcellular mechanisms of T cell development. Cell. Mol. Life Sci. 2004, 61:263-280.
9. Calnan B.J., Szychowski S., Chan F.K., Cado D., Winoto A. A role for the orphan steroid receptor Nur77 in apoptosis accompanying antigen-induced negative selection. Immunity 1995, 3:273-282.
10. Cao X., Liu W., Lin F., Li H., Kolluri S.K., Lin B., Han Y.H., Dawson M.I., Zhang X.K. Retinoid X receptor regulates Nur77/TR3-dependent apoptosis [corrected] by modulating its nuclear export and mitochondrial targeting. Mol. Cell. Biol. 2004, 24:9705-9725.
11. Chen J., Carey K., Godowski P.J. Identification of Gas6 as a ligand for Mer, a neural cell adhesion molecule related receptor tyrosine kinase implicated in cellular transformation. Oncogene 1997, 14:2033-2039.
12. de Urquiza A.M., Liu S., Sjöberg M., Zetterström R.H., Griffiths W., Sjövall J., Perlmann T. Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science 2000, 290:2140-2144.
13. Dillehay D.L., Cornay W.J., Alia A.S., Lamon E.W. Effect of retinoids on human thymus-dependent and thymus-independent mitogenesis. Clin. Immunol. Immunopathol. 1989, 50:100-108.
14. Duester G. Families of retinoid dehydrogenases regulating vitamin A function: production of visual pigment and retinoic acid. Eur. J. Biochem. 2000, 267:4315-4324.
15. Dzhagalov I., Chambon P., He Y.W. Regulation of CD8+ T lymphocyte effector function and macrophage inflammatory cytokine production by retinoic acid receptor gamma. J. Immunol. 2007, 178:2113-2121.
16. Fassett M.S., Jiang W., D'Alise A.M., Mathis D., Benoist C. Nuclear receptor Nr4a1 modulates both regulatory T-cell (Treg) differentiation and clonal deletion. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3891-3896.
17. Fésüs L., Szondy Z. Transglutaminase 2 in the balance of cell death and survival. FEBS Lett. 2005, 579:3297-3302.
18. Fésüs L., Szondy Z., Uray I. Probing the molecular program of apoptosis by cancer chemopreventive agents. J. Cell. Biochem. Suppl. 1995, 22:151-161.
19. Fisher G.J., Talwar H.S., Lin J., Lin P., McPhillips F., Wang Z., Li X., Wan Y., Kang S., Voorhees J.J. Retinoic acid inhibits induction of c-Jun protein by ultraviolet radiation that occurs subsequent to activation of mitogen-activated protein kinase pathways in human skin in vivo. J. Clin. Invest. 1998, 101:1432-1440.
20. Garabuczi É., Kiss B., Felszeghy S., Tsay G.J., Fésüs L., Szondy Z. Retinoids produced by macrophages engulfing apoptotic cells contribute to the appearance of transglutaminase 2 in apoptotic thymocytes. Amino Acids 2013, 44:235-244.
21. Germain P., Iyer J., Zechel C., Gronemeyer H. Co-regulator recruitment and the mechanism of retinoic acid receptor synergy. Nature 2002, 415:187-192.
22. Hall M.O., Obin M.S., Heeb M.J., Burgess B.L., Abrams T.A. Both protein S and Gas6 stimulate outer segment phagocytosis by cultured rat retinal pigment epithelial cells. Exp. Eye Res. 2005, 81:581-591.
23. Hanayama R., Tanaka M., Miwa K., Shinohara A., Iwamatsu A., Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002, 417:182-187.
24. Hernandez J.B., Newton R.H., Walsh C.M. Life and death in the thymus - cell death signaling during T cell development. Curr. Opin. Cell Biol. 2010, 22:865-871.
25. Heyman R.A., Mangelsdorf D.J., Dyck J.A., Stein R.B., Eichele G., Evans R.M., Thaller C. 9-Cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 1992, 68:397-406.
26. Hoffmann B., Lehmann J.M., Zhang X.K., Hermann T., Husmann M., Graupner G., Pfahl M. A retinoic acid receptor-specific element controls the retinoic acid receptor-beta promoter. Mol. Endocrinol. 1990, 4:1727-1736.
27. Iwata M., Mukai M., Nakai Y., Iseki R. Retinoic acids inhibit activation-induced apoptosis in T cell hybridomas and thymocytes. J. Immunol. 1992, 149:3302-3308.
28. Jaffe H.L. The influence of the supradrenal gland on the thymus: I. Regeneration of the thymus following double supradrenalectomy in the rat. J. Exp. Med. 1924, 40:753-759.
29. Kang H.J., Song M.R., Lee S.K., Shin E.C., Choi Y.H., Kim S.J., Lee J.W., Lee M.O. Retinoic acid and its receptors repress the expression and transactivation functions of Nur77: a possible mechanism for the inhibition of apoptosis by retinoic acid. Exp. Cell Res. 2000, 256:545-554.
30. Kisielow P., von Boehmer H. Development and selection of T cells: facts and puzzles. Adv. Immunol. 1995, 58:87-209.
31. Kiss I., Rühl R., Szegezdi E., Fritzsche B., Tóth B., Pongrácz J., Perlmann T., Fésüs L., Szondy Z. Retinoid receptor-activating ligands are produced within the mouse thymus during postnatal development. Eur. J. Immunol. 2008, 38:147-155.
32. Kliewer S.A., Umesono K., Noonan D.J., Heyman R.A., Evans R.M. Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature 1992, 358:771-774.
33. Kojo H., Tajima K., Fukagawa M., Isogai T., Nishimura S. Molecular cloning and characterization of two novel human RXR alpha splice variants. J. Steroid Biochem. Mol. Biol. 2004, 92:19-28.
34. Kurlandsky S.B., Gamble M.V., Ramakrishnan R., Blaner W.S. Plasma delivery of retinoic acid to tissues in the rat. J. Biol. Chem. 1995, 270:17850-17857.
35. Kurokawa R., Söderström M., Hörlein A., Halachmi S., Brown M., Rosenfeld M.G., Glass C.K. Polarity-specific activities of retinoic acid receptors determined by a co-repressor. Nature 1995, 377:451-454.
36. Lammi J., Perlmann T., Aarnisalo P. Corepressor interaction differentiates the permissive and non-permissive retinoid X receptor heterodimers. Arch. Biochem. Biophys. 2008, 472:105-114.
37. Lehmann J.M., Hoffmann B., Pfahl M. Genomic organization of the retinoic acid receptor gamma gene. Nucleic Acids Res. 1991, 19:573-578.
38. Lemotte P.K., Keidel S., Apfel C.M. Phytanic acid is a retinoid X receptor ligand. Eur. J. Biochem. 1996, 236:328-333.
39. Ling L., Templeton D., Kung H.J. Identification of the major autophosphorylation sites of Nyk/Mer, an NCAM-related receptor tyrosine kinase. J. Biol. Chem. 1996, 271:18355-18362.
40. Liu Q., Linney E. The mouse retinoid-X receptor-gamma gene: genomic organization and evidence for functional isoforms. Mol. Endocrinol. 1993, 7:651-658.
41. Malkovský M., Medawar P.B., Thatcher D.R., Toy J., Hunt R., Rayfield L.S., Doré C. Acquired immunological tolerance of foreign cells is impaired by recombinant interleukin 2 or vitamin A acetate. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:536-538.
42. Mangelsdorf D.J., Umesono K., Kliewer S.A., Borgmeyer U., Ong E.S., Evans R.M. A direct repeat in the cellular retinol-binding protein type II gene confers differential regulation by RXR and RAR. Cell 1991, 66:555-561.
43. Meco D., Scarpa S., Napolitano M., Maroder M., Bellavia D., De Maria R., Ragano-Caracciolo M., Frati L., Modesti A., Gulino A. Modulation of fibronectin and thymic stromal cell-dependent thymocyte maturation by retinoic acid. J Immunol. 1994, 153:73-83.
44. Moise A.R., Alvarez S., Domínguez M., Alvarez R., Golczak M., Lobo G.P., von Lintig J., de Lera A.R., Palczewski K. Activation of retinoic acid receptors by dihydroretinoids. Mol. Pharmacol. 2009, 76:1228-1237.
45. Moise A.R., Kuksa V., Imanishi Y., Palczewski K. Identification of all-trans-retinol: all-trans-13,14-dihydroretinol saturase. J. Biol. Chem. 2004, 279:50230-50242.
46. Mora J.R., Iwata M., Andriam U.H. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat. Rev. Immunol. 2008, 8:685-698.
47. Moran A.E., Holzapfel K.L., Xing Y., Cunningham R.L., Maltzman J.S., Punt J., Hogquist K.A. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 2011, 208:1279-1289.
48. Mukundan L., Odegaard J.I., Morel C.R., Heredia J.E., Mwangi J.W., Ricardo-Gonzalez R.R., Goh Y.P., Eagle A.R., Dunn S.E., Awakuni J.U., Nguyen K.D., Steinman L., Michie S.A., Chawla A. PPAR-delta senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat. Med. 2009, 15:1266-1272.
49. Nagy L., Saydak M., Shipley N., Lu S., Basilion J.P., Yan Z.H., Syka P., Chandraratna R.A., Stein J.P., Heyman R.A., Davies P.J. 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.
50. Parrado A., Despouy G., Kraïba R., Le Pogam C., Dupas S., Choquette M., Robledo M., Larghero J., Bui H., Le Gall I., Rochette-Egly C., Chomienne C., Padua R.A. Retinoic acid receptor alpha1 variants, RARalpha1 DeltaB and RARalpha1 DeltaBC, define a new class of nuclear receptor isoforms. Nucleic Acids Res. 2001, 29:4901-4908.
51. Petrie H.T., Zuniga-Pflucker J.C. Zoned out: functional mapping of stromal signaling microenvironments in the thymus. Annu. Rev. Immunol. 2007, 25:649-679.
52. Pohl J., LeFace D., Sands J.F. Transcription of retinoic acid receptor genes in transgenic mice increases CD8 T-cell subset. Mol. Biol. Rep. 1993, 17:135-142.
53. Rébé C., Raveneau M., Chevriaux A., Lakomy D., Sberna A.L., Costa A., Bessède G., Athias A., Steinmetz E., Lobaccaro.J.M., Alves G., Menicacci A., Vachenc S., Solary E., Gambert P., Masson D. Induction of transglutaminase 2 by a liver X receptor/retinoic acid receptor alpha pathway increases the clearance of apoptotic cells by human macrophages. Circ. Res. 2009, 105:393-401.
54. Rajpal A., Cho Y.A., Yelent B., Koza-Taylor P.H., Li D., Chen E., Whang M., Kang C., Turi T.G., Winoto A. Transcriptional activation of known and novel apoptotic pathways by Nur77 orphan steroid receptor. EMBO J. 2003, 22:6526-6536.
55. Rezzani R., Bonomini F., Rodella L.F. Histochemical and molecular overview of the thymus as site for T-cells development. Prog. Histochem. Cytochem. 2008, 43:73-120.
56. Ross A.C. Vitamin A status: relationship to immunity and the antibody response. Proc. Soc. Exp. Biol. Med. 1992, 200:303-320.
57. Roszer T., Menéndez-Gutiérrez M.P., Lefterova M.I., Alameda D., Núñez V., Lazar M.A., Fischer T., Ricote M. Autoimmune kidney disease and impaired engulfment of apoptotic cells in mice with macrophage peroxisome proliferator-activated receptor gamma or retinoid X receptor alpha deficiency. J. Immunol. 2011, 186:621-631.
58. Savill J.S., Hogg N., Ren Y., Haslett C. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 1992, 90:1513-1522.
59. Schreiber L., Sharabi Y., Schwartz D., Goldfinger N., Brodie C., Rotter V., Shoham J. Induction of apoptosis and p53 expression in immature thymocytes by direct interaction with thymic epithelial cells. Scand. J. Immunol. 1996, 44:314-322.
60. Sitnik K.M., Kotarsky K., White A.J., Jenkinson W.E., Anderson G., Agace W.W. Mesenchymal cells regulate retinoic acid receptor-dependent cortical thymic epithelial cell homeostasis. J. Immunol. 2012, 188:4801-4809.
61. Sitnik K.M. Phenotypic and functional analysis of the mesenchymal stromal cell compartment in the thymus 2013, Lund University, (Ph.D. Thesis).
62. Shih T.W., Lin T.H., Shealy Y.F., Hill D.L. Nonenzymatic isomerization of 9-cis-retinoic acid catalyzed by sulfhydryl compounds. Drug Metab. Dispos. 1997, 25:27-32.
63. Strasser A., Puthalakath H., Bouilllet P. What do we know about the mechanisms of elimination of autoreactive T and B cells and what challenges remain. Immunol. Cell Biol. 2008, 86:57-66.
64. Sun H., Kawaguchi R. The membrane receptor for plasma retinol-binding protein, a new type of cell-surface receptor. Int. Rev. Cell. Mol. Biol. 2011, 288:1-41.
65. Surh C.D., Sprent J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 1994, 372:100-103.
66. Szegezdi E., Kiss I., Simon A., Blaskó B., Reichert U., Michel S., Sándor M., Fésüs L., Szondy Z. Ligation of retinoic acid receptor alpha regulates negative selection of thymocytes by inhibiting both DNA binding of nur77 and synthesis of bim. J. Immunol. 2003, 170:3577-3584.
67. Szondy Z., Reichert U., Bernardon J.M., Michel S., Tóth R., Ancian P., Fésüs L. Induction of apoptosis by retinoids and RAR gamma selective compounds in mouse thymocytes through a novel apoptosis pathway. Mol. Pharmacol. 1997, 51:972-982.
68. Szondy Z., Reichert U., Bernardon J.M., Michel S., Tóth R., Karászi E., Fésüs L. Inhibition of activation-induced apoptosis of thymocytes by all-trans and 9-cis retinoic acids is mediated via retinoic acid receptor alpha. Biochem. J. 1998, 331:767-774.
69. Thompson J., Winoto A. During negative selection, Nur77 family proteins translocate to mitochondria where they associate with Bcl-2 and expose its proapoptotic BH3 domain. J. Exp. Med. 2008, 205:1029-10236.
70. Tóth B., Garabuczi E., Sarang Z., Vereb G., Vámosi G., Aeschlimann D., Blaskó B., Bécsi B., Erdõdi F., Lacy-Hulbert A., Zhang A., Falasca L., Birge R.B., Balajthy Z., Melino G., Fésüs L., Szondy Z. Transglutaminase 2 is needed for the formation of an efficient phagocyte portal in macrophages engulfing apoptotic cells. J. Immunol. 2009, 182:2084-2092.
71. Tóth K., Sarang Z., Scholtz B., Brázda P., Ghyselinck N., Chambon P., Fésüs L., Szondy Z. Retinoids enhance glucocorticoid-induced apoptosis of T cells by facilitating glucocorticoid receptor-mediated transcription. Cell Death Differ. 2011, 18:783-792.
72. Trentham D.E., Brinckerhoff C.E. Augmentation of collagen arthritis by synthetic analogues of retinoic acid. J. Immunol. 1982, 129:2668-2672.
73. Vacchio M.S., Ashwell J.D. Glucocorticoids and thymocyte development. Semin. Immunol. 2000, 12:475-485.
74. Vacchio M.S., Papadopoulos V., Ashwell J.D. Steroid production in the thymus: implications for thymocyte selection. J. Exp. Med. 1994, 179:1835-1846.
75. Vacchio M.S., Lee J.Y., Ashwell J.D. Thymus-derived glucocorticoids set the thresholds for thymocyte selection by inhibiting TCR-mediated thymocyte activation. J. Immunol. 1999, 163:1327-1333.
76. Vogel S., Gamble M.V., Blaner W.S. Biosynthesis, absorption, metabolism and transport of retinoids. Retinoids: The Biochemical and Molecular Basis of Vitamin A and Retinoid Action 13 1999, 31-96. Springer-Verlag, Berlin, Heidelberg.
77. West K.P., Howard G.R., Sommer A. Vitamin A and infection: public health implications. Annu. Rev. Nutr. 1989, 9:63-86.
78. Willy P.J., Umesono K., Ong E.S., Evans R.M., Heyman R.A., Mangelsdorf D.J. LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 1995, 9:1033-1045.
79. Xue Y., Chomez P., Castanos-Velez E., Biberfeld P., Perlmann T., Jondal M. Positive and negative thymic selection in T cell receptor-transgenic mice correlate with Nur77 mRNA expression. Eur. J. Immunol. 1997, 27:2048-2056.
80. Yagi J., Uchida T., Kuroda K., Uchiyama T. Influence of retinoic acid on the differentiation pathway of T cells in the thymus. Cell. Immunol. 1997, 181:153-162.
81. Zacharchuk C.M., Mercep M., Chakraborti P.K., Simons S.S., Ashwell D.J. Programmed T lymphocyte death, cell activation- and steroid-induced pathways are mutually antagonistic. J. Immunol. 1990, 145:4037-4045.
82. Zhao Z., Ross A.C. Retinoic acid addition restores the number of leukocytes and their subsets and stimulates natural cytotoxicity in vitamin A deficient rats. J. Nutr. 1995, 125:2064-2073.