Activation of a TGF-β-specific multistep gene expression program in mature macrophages requires glucocorticoid-mediated surface expression of TGF-β receptor II

Journal of Immunology

Volumn 180, Issue 10, 2008, Pages 6553-6565

  Gratchev, Alexei ^a   Kzhyshkowska, Julia ^a   Kannookadan, Sheila ^a   Ochsenreiter, Miriam ^a   Popova, Anna ^a   Yu, Xiaolei ^a   Mamidi, Srinivas ^a   Stonehouse Usselmann, Eugenia ^a   Muller Molinet, Isabelle ^a   Gooi, LiMing ^a   Goerdt, Sergij ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; DEXAMETHASONE; GLUCOCORTICOID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INHIBITOR OF DIFFERENTIATION 3; INTERLEUKIN 13; INTERLEUKIN 4; MESSENGER RNA; SIRTUIN 1; SMAD2 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA1; IL17RB PROTEIN, HUMAN; INTERLEUKIN RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ARTICLE; ATHEROSCLEROSIS; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MACROPHAGE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; BIOSYNTHESIS; CELL MEMBRANE; CYTOLOGY; DNA MICROARRAY; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; MACROPHAGE ACTIVATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CELL DIFFERENTIATION; CELL MEMBRANE; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GLUCOCORTICOIDS; HUMANS; INTERLEUKIN-4; MACROPHAGE ACTIVATION; MACROPHAGES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, INTERLEUKIN; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA;

EID: 45549109370     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.10.6553     Document Type: Article

References (67)

1. Stein, M., S. Keshav, N. Harris, and S. Gordon. 1992. Intcrlcukin 4 potently enhances murine macrophagc mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 176: 287-292.
2. Gratchev, A., K. Schledzewski, P. Guillot, and S. Goerdt. 2001. Alternatively activated antigen-presenting cells: molecular repertoire, immune regulation, and healing. Skin Pharmacol. Appl. Skin Physiol. 14: 272-279.
3. Goerdt, S., and C. E. Orfanos. 1999. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10: 137-142.
4. Gratchev, A., J. Kzhyshkowska, J. Utikal, and S. Goerdt. 2005. Interleukin-4 and dexamcthasone counterregulate extracellular matrix remodelling and phagocytosis in type-2 macrophages. Scand. J. Immunol. 61: 10-17.
5. Stout, R. D., and J. Suttles. 2004. Functional plasticity of macrophages: reversible adaptation to changing microenvironments. J. Leukocyte Biol. 76: 509-513.
6. Gratchev, A., J. Kzhyshkowska, K. Kothe, I. Muller-Molinet, S. Kannookadan, J. Utikal, and S. Goerdt. 2006. Mphil and Mphi2 can be re-polarized by Th2 or Thl cytokincs, respectively, and respond to exogenous danger signals. Immuno-biology 211:473-486.
7. Herrero, C, X. Hu, W. P. Li, S. Samuels, M. N. Sharif, S. Kotenko, and L. B. Ivashkiv. 2003. Reprogramming of 1L-10 activity and signaling by IFN-γ. J. Immunol. 171: 5034-5041.
8. Schaer, D. J., F. S. Boretti, G. Schoedon, and A. Schaffner. 2002. Induction of the CD163-dependent haemoglobin uptake by macrophages as a novel anti-inflammatory action of glucocorticoids. Br. J. Haematol. 119: 239-243.
9. Kzhyshkowska, J., A. Gratchev, and S. Goerdt. 2006. Stabilin-l, a homeostatic scavenger receptor with multiple functions. J. Cell. Mol. Med. 10: 635-649.
10. Kzhyshkowska. J., S. Mamidi, A. Gratchev, E. Kremmer, C. Schmuttermaier, L. Krusell, G. Haus, J. Utikal, K. Schledzewski, J. Scholtze, and S. Goerdt. 2006. Novel stabilin-I interacting chitinase-like protein (SI-CLP) is up-regulated in alternatively activated macrophages and secreted via lysosomal pathway. Blood 107: 3221-3228.
11. Kzhyshkowska, J., G. Workman, M. Cardo-Vila, W. Arap, R. Pasqualini, A. Gratchev, L. Krusell, S. Goerdt, and E. H. Sage. 2006. Novel function of alternatively activated macrophages: stabilin-1-mcdiated clearance of SPARC. J. Immunol. 176: 5825-5832.
12. Politz, O., A. Gratchev, P. A. McCourt, K. Schledzewski, P. Guillot, S. Johansson, G. Svineng, P. Franke, C. Kannicht, J. Kzhyshkowska, et al. 2002. Stabilin-l and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues. Biochem. J. 362: 155-164.
13. Gratchev, A., P. Guillot, N. Hakiy, O. Politz, C. E. Orfanos, K. Schledzewski, and S. Goerdt. 2001. Alternatively activated macrophages differentially express fi-bronectin and its splice variants and the extracellular matrix protein βIG-H3. Scand. J. Immunol. 53: 386-392.
14. Gratchev, A., J. Kzhyshkowska, K. Duperrier, J. Utikal, F. W. Velten, and S. Goerdt. 2004. The receptor for interleukin-I7E is induced by Th2 cytokines in antigen-presenting cells. Scand. J. Immunol. 60: 233-237.
15. Lee, Y. W., and A. A. Hirani. 2006. Role of interleukin-4 in atherosclerosis. Arch. Pharm. Res. 29: 1-15.
16. Bobik, A. 2006. Transforming growth factor-βs and vascular disorders. Arerio-scler. Thromb. Vase. Biol. 26: 1712-1720.
17. Ramji, D. P., N. N. Singh, P. Foka, S. A. Irvine, and K. Arnaoutakis. 2006. Transforming growth factor-β-regulatcd expression of genes in macrophages implicated in the control of cholesterol homoeostasis. Biochem. Soc. Trans. 34: 1141-1144.
18. Hazelbag, S., G. J. Fleuren, J. J. Baelde, E. Schuuring, G. G. Kenter, and A. Gorter. 2001. Cytokine profile of cervical cancer cells. Gynecol. Oncol. 83: 235-243.
19. Ortegel, J. W., E. D. Staren, L. P. Faber, W. H. Warren, and D. P. Braun. 2002. Modulation of tumor-infiltrating lymphocyte cytolytic activity against human non-small cell lung cancer. Lung Cancer 36: 17-25.
20. De Caestecker, M. 2004. The transforming growth factor-β superfamily of receptors. Cytokine Growth Factor Rev. 15: 1-11.
21. Brandes, M. E., L. M. Wakefield, and S. M. Wahl. 1991. Modulation of monocyte type I transforming growth factor-β receptors by inflammatory stimuli. J. Biol. Chem. 266: 19697-19703.
22. Ashcroft, G. S. 1999. Bidirectional regulation of macrophage function by TGF-β. Microbes Infect. 1: 1275-1282.
23. Dai, M., P. Wang, A. D. Boyd, G. Kostov, B. Athey, E. G. Jones, W. E. Bunney, R. M. Myers, T. P. Speed, H. Akil, et al. 2005. Evolving gene/transcript definitions significantly alter the interpretation of GcncChip data. Nucleic Acids Res. 33: el75.
24. Chu, T. M., B. Weir, and R. Wolfinger. 2002. A systematic statistical linear modeling approach to oligonucleotide array experiments. Math. Biosci. 176: 35-51.
25. Schmierer, B., and C. S. Hill. 2005. Kinetic analysis of Smad nucleocytoplasmic shuttling reveals a mechanism for transforming growth factor β-dependent nuclear accumulation of Smads. Mol. Cell. Biol. 25: 9845-9858.
26. Li, M. O., Y. Y. Wan, S. Sanjabi, A. K. Robertson, and R. A. Flavell. 2006. Transforming growth factor-β regulation of immune responses. Annu. Rev. Immunol. 24: 99-146.
27. Li, A. G., S. L. Lu, M. X. Zhang, C. Deng, and X. J. Wang. 2004. Smad3 knockout mice exhibit a resistance to skin chemical carcinogenesis. Cancer Res. 64: 7836-7845.
28. Pick, E., C. H. Heldin, and P. Ten Dijke. 1999. Specificity, diversity, and regulation in TGF-β superfamily signaling. FASEB J. 13: 2105-2124.
29. Draude, G., and R. L. Lorenz. 2000. TGF-β1 downrcgulates CD36 and scavenger receptor A but upregulates LOX-1 in human macrophaces. Am. J. Physiol. 278: H1042-111048.
30. Li, G., S. Wang, and T. D. Gelehrter. 2003. Identification of glucocorticoid receptor domains involved in transrepression of transforming growth factor-β action. J. Biol. Chem. 278: 41779-41788.
31. Pioli, P. A., K. E. Goonan, K. Wardwell, and P. M. Guyre. 2004. TGF-β regulation of human macrophage scavenger receptor CD163 is Smad3-dependent. J. Leukocyte Biol. 76: 500-508.
32. Peltier, J., J. Perez, A. Bellocq, B. Escoubet, B. Fouqueray, and L. Baud. 2003. Transforming growth factor-β1 increases glucocorticoid binding and signaling in macrophages through a Smad- and activated protein-1-mediated process. Kidney Int. 63: 2028-2036.
33. Wenting-Van Wijk, M. J., M. A. Blankenstein, F. P. Lafeber, and J. W. Bijlsma. 1999. Relation of plasma dexamethasone to clinical response. Clim. Exp. Rheu-matol. 17:305-312.
34. Ten Dijke, P., and C. S. Hill. 2004. New insights into TGF-β-Smad signalling. Trends Biochem. Sci. 29: 265-273.
35. Kume, S., M. Haneda, K. Kanasaki, T. Sugimoto, S. Araki, K. Isshiki, M. Isono, T. Uzu, L. Guarente, A. Kashiwagi, and D. Koya. 2007. SIRT1 inhibits transforming growth factor β-induced apoptosis in glomerular mesangial cells via Smad7 deacetylation. J. Biol. Chem. 282: 151-158.
36. McCartney-Francis, N. L., and S. M. Wahl. 1994. Transforming growth factor β: a matter of life and death. J. Leukocyte Biol. 55: 401-409.
37. Wong, H. L., G. R. Welch, M. E. Brandes, and S. M. Wahl. 1991. IL-4 antagonizes induction of FcγRIII (CD16) expression by transforming growth factor-β on human monocytes. J. Immunol. 147: 1843-1848.
38. John, N. J., D. A. Bravo, O. K. Haffar, and G. L. Firestone. 1988. Glucocorticoid-dependent complementation of a hepatoma cell variant defective in viral glyco-protein sorting. Proc. Natl. Acad. Sci. USA 85: 797-801.
39. Guan, Y., N. M. Rubenstein, K. L. Failor, P. L. Woo, and G. L. Firestone. 2004. Glucocorticoids control β-catenin protein expression and localization through distinct pathways that can be uncoupled by disruption of signaling events required for tight junction formation in rat mammary epithelial tumor cells. Mol. Endocrinol. 18: 214-227.
40. Buse, P., P. L. Woo, D. B. Alexander, A. Reza, and G. L. Firestone. 1995. Glucocorticoid-induced functional polarity of growth factor responsiveness regulates tight junction dynamics in transformed mammary epithelial tumor cells. J. Biol. Chem. 270: 28223-28227.
41. Itoh, S., and P. Ten Dijke. 2007. Negative regulation of TGF-β receptor/Smad signal transduction. Curr. Opin. Cell Biol. 19: 176-184.
42. Zebedee, Z., and E. Hara. 2001. Id proteins in cell cycle control and cellular senescence. Oncogene 20: 8317-8325.
43. + stem cells into predendritic cell (pre-DC)2 but not into pre-DCl: evidence for a lymphoid origin of pre-DC2. J. Exp. Med. 192: 1775-1784.
44. Sugai, M., H. Gonda, Y. Nambu, Y. Yokota, and A. Shimizu. 2004. Role of Id proteins in B lymphocyte activation: new insights from knockout mouse studies. J. Mol. Med. 82: 592-599.
45. Reif, K., and J. G. Cyster. 2000. RGS molecule expression in murine B lymphocytes and ability to down-regulate chemotaxis to lymphoid chemokines. J. Immunol. 164: 4720-4729.
46. Chen, Y. H., M. D. Layne, S. W. Chung, K. Ejima, R. M. Baron, S. F. Yet, and M. A. Perrella. 2003. Elk-3 is a transcriptional rcpressor of nitric-oxide synthase 2. J. Biol. Chem. 278: 39572-39577.
47. Brenner, O., D. Levanon, V. Kegreanu, O. Golubkov, O. Fainaru, E. Woolf, and Y. Groner. 2004. Loss of Runx3 function in leukocytes is associated with spontaneously developed colitis and gastric mucosal hyperplasia. Proc. Natl. Acad. Sci. USA 101: 16016-16021.
48. Yanagi, Y., M. Suzawa, M. Kawabata, K. Miyazono, J. Yanagisawa, and S. Kato. 1999. Positive and negative modulation of vitamin D receptor function by transforming growth factor-β signaling through smad proteins. J. Biol. Chem. 274: 12971-12974.
49. Shilatifard, A., D. R. Duan, D. Haque, C. Florence, W. H. Schubach, J. W. Conaway, and R. C. Conaway. 1997. ELL2, a new member of an ELL family of RNA polymerase II elonaation factors. Proc. Natl. Acad. Sci. USA 94: 3639-3643.
50. Liu, Y., G. Dehni, K. J. Purcell, J. Sokolow, M. L. Carcangiu, S. Artavanis-Tsakonas, and S. Stifani. 1996. Epithelial expression and chromosomal location of human TLE genes: implications for notch signaling and nco-plasia. Genomics 31: 58-64.
51. Huynh, K. D., W. Fischle, E. Verdin, and V. J. Bardwell. 2000. BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev. 14: 1810-1823.
52. Briggs, R. C, J. B. Atkinson, and R. N. Miranda. 2005. Variable expression of human myeloid specific nuclear antigen MNDA in monocyte lineage cells in atherosclerosis. J. Cell. Biochem. 95: 293-301.
53. Briggs, R. C., K. E. Shults, L. A. Flye, S. A. McClintock-Treep, M. H. Jagasia, S. A. Goodman, F. I. Boulos, J. W. Jacobberger, G. T. Stelzer, and D. R. Head. 2006. Dysregulated human myeloid nuclear differentiation antigen expression in myelodysplastic syndromes: evidence for a role in apoptosis. Cancer Res. 66: 4645-4651.
54. Kawano, M., K. Kodama, H. Inadera, Y. Saito, M. Saito, T. Yaginuma, Y. Kanazawa, and M. Kawakami. 2002. A case of apolipoprotein C-II deficiency with coronary artery disease. Clin. Exp. Med. 2: 29-31.
55. Carter, C. J. 2007. Convergence of genes implicated in Alzheimer's disease on the cerebral cholesterol shuttle: APP, cholesterol, lipoproteins, and atherosclerosis. Neurochem. Int. 50: 12-38.
56. Rosenfeld, M. E., S. Butler, V. A. Ord, B. A. Lipton, C. A. Dyer, L. K. Curtiss, W. Palinski, and J. L. Witztum. 1993. Abundant expression of apoprotein E by macrophages in human and rabbit atherosclerotic lesions. Arterioscler. Thromb. 13: 1382-1389.
57. Kataoka, H., N. Kume, S. Miyamoto, M. Minami, H. Moriwaki, T. Murase, T. Sawamura, T. Masaki, N. Hashimoto, and T. Kita. 1999. Expression of lect-inlike oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation 99: 3110-3117.
58. Klucken, J., C. Buchler, E. Orso, W. E. Kaminski, M. Porsch-Ozcurumez, G. Liebisch, M. Kapinsky, W. Diederich, W. Drobnik, M. Dean, et al. 2000. ABCGI (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport. Proc. Natl. Acad. Sci. USA 97: 817-822.
59. Ganz, T. 2006. Hepcidin: a peptide hormone at the interface of innate immunity and iron metabolism. Curr. Top. Microbiol. Immunol. 306: 183-198.
60. Back, M., and G. K. Hansson. 2006. Leukotriene receptors in atherosclerosis. Ann. Med. 38: 493-502.
61. Helgadottir, A., A. Manolescu, G. Thorleifsson, S. Gretarsdottir, H. Jonsdottir, U. Thorsteinsdottir, N. J. Samani, G. Gudmundsson, S. F. Grant, G. Thorgeirsson, et al. 2004. The gene encoding 5-lipoxygenase activating protein confers risk of myocardial infarction and stroke. Nat. Genet. 36: 233-239.
62. Colonna, M., and F. Facchetti. 2003. TREM-1 (triggering receptor expressed on myeloid cells): a new player in acute inflammatory responses. J. Infect. Dis. 187 (Suppl. 2): S397-S40I.
63. Hansson, G. K. 2005. Inflammation, atherosclerosis, and coronary artery disease. N. Engl. J. Med. 352: 1685-1695.
64. Melchionna, R., D. Porcelli, A. Mangoni, D. Carlini, G. Liuzzo, G. Spinetti, A. Antonini, M. C. Capogrossi, and M. Napolitano. 2005. Laminar shear stress inhibits CXCR4 expression on endothelial cells: functional consequences for atherogenesis. FASEB J. 19:629-631.
65. Tiret, L., T. Godefroy, E. Lubos, V. Nicaud, D. A. Tregouct, S. Barbaux, R. Schnabel, C. Bickel, C. Espinola-Klein, O. Poirier, et al. 2005. Genetic analysis of the interleukin-18 system highlights the role of the interleukin-18 gene in cardiovascular disease. Circulation 112: 643-650.
66. Mallat, Z., and A. Tedgui. 2002. The role of transforming growth factor β in atherosclerosis: novel insights and future perspectives. Curr. Opin. Lipidol. 13: 523-529.
67. Grainger, D. J. 2004. Transforming growth factor β and atherosclerosis: so far, so good for the protective cytokine hypothesis. Arterioscler. Thromb. Vasc. Biol. 24: 399-404.