Cross talk between histone deacetylase 4 and STAT6 in the transcriptional regulation of arginase 1 during mouse dendritic cell differentiation

Molecular and Cellular Biology

Volumn 35, Issue 1, 2015, Pages 63-75

  Yang, Quan ^a   Wei, Jianyang ^a   Zhong, Limei ^a   Shi, Maohua ^a   Zhou, Pan ^a   Zuo, Shengkai ^c   Wu, Kang ^a   Zhu, Mingjiang ^c   Huang, Xi ^a,b   Yu, Ying ^c   Zhang, Hui ^a,b   Yin, Huiyong ^c   Zhou, Jie ^a,b  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c Chinese Academy of Sciences   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; CD8 ANTIGEN; FLT3 LIGAND; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; STAT6 PROTEIN; ARG1 PROTEIN, MOUSE; ARGINASE; HDAC4 PROTEIN, HUMAN; HDAC5 PROTEIN, MOUSE; HISTONE; HISTONE DEACETYLASE; REPRESSOR PROTEIN; STAT6 PROTEIN, HUMAN; STAT6 PROTEIN, MOUSE;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL CULTURE; CELL DIFFERENTIATION; DENDRITIC CELL; MONOCYTE; MOUSE; MYELOID DENDRITIC CELL; NONHUMAN; OBSERVATION; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; CELL SEPARATION; CYTOLOGY; GENE EXPRESSION REGULATION; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD8; ARGINASE; BINDING SITES; CELL DIFFERENTIATION; CELL SEPARATION; DENDRITIC CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEK293 CELLS; HISTONE DEACETYLASES; HISTONES; HUMANS; MICE; MICE, TRANSGENIC; MONOCYTES; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; STAT6 TRANSCRIPTION FACTOR;

EID: 84919977101     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00805-14     Document Type: Article

References (55)

1. Banchereau J, Steinman RM. 1998. Dendritic cells and the control of immunity. Nature 392:245-252. http://dx.doi.org/10.1038/32588.
2. Mellman I, Steinman RM. 2001. Dendritic cells: specialized and regulated antigen processing machines. Cell 106:255-258. http://dx.doi.org/10.1016/S0092-8674(01)00449-4.
3. Zenke M, Hieronymus T. 2006. Towards an understanding of the transcription factor network of dendritic cell development. Trends Immunol 27:140-145. http://dx.doi.org/10.1016/j.it.2005.12.007.
4. Satpathy AT, Murphy KM, WKC. 2011. Transcription factor networks in dendritic cell development. Semin Immunol 23:388-397. http://dx.doi.org/10.1016/j.smim.2011.08.009.
5. Gabrilovich D. 2004. Mechanisms and functional significance of tumourinduced dendritic-cell defects. Nat Rev Immunol 4:941-952. http://dx.doi.org/10.1038/nri1498.
6. Fitzgerald-Bocarsly P, Jacobs ES. 2010. Plasmacytoid dendritic cells in HIV infection: striking a delicate balance. J Leukoc Biol 87:609-620. http://dx.doi.org/10.1189/jlb.0909635.
7. Moretto MM, Lawlor EM, Khan IA. 2008. Aging mice exhibit a functional defect in mucosal dendritic cell response against an intracellular pathogen. J Immunol 181:7977-7984. http://dx.doi.org/10.4049/jimmunol.181.11.7977.
8. Schmid MA, Kingston D, Boddupalli S, Manz MG. 2010. Instructive cytokine signals in dendritic cell lineage commitment. Immunol Rev 234: 32-44. http://dx.doi.org/10.1111/j.0105-2896.2009.00877.x.
9. Onai N, Manz MG. 2008. The STATs on dendritic cell development. Immunity 28:490-492. http://dx.doi.org/10.1016/j.immuni.2008.03.006.
10. Zhou J, Cheng P, Youn J I, Cotter MJ, Gabrilovich DI. 2009. Notch and wingless signaling cooperate in regulation of dendritic cell differentiation. Immunity 30:845-859. http://dx.doi.org/10.1016/j.immuni.2009.03.021.
11. Bronte V, Zanovello P. 2005. Regulation of immune responses by Larginine metabolism. Nat Rev Immunol 5:641-654. http://dx.doi.org/10.1038/nri1668.
12. Gordon S. 2003. Alternative activation of macrophages. Nat Rev Immunol 3:23-35. http://dx.doi.org/10.1038/nri978.
13. Gabrilovich DI, Nagaraj S. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9:162-174. http://dx.doi.org/10.1038/nri2506.
14. Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293: 1074-1080. http://dx.doi.org/10.1126/science.1063127.
15. Struhl K. 1998. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 12:599-606. http://dx.doi.org/10.1101/gad.12.5.599.
16. Eberharter A, Becker PB. 2002. Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep 3:224-229. http://dx.doi.org/10.1093/embo -reports/kvf053.
17. Van Lint C, Emiliani S, Verdin E. 1996. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr 5:245-253.
18. Weishaupt H, Sigvardsson M, Attema JL. 2010. Epigenetic chromatin states uniquely define the developmental plasticity of murine hematopoietic stem cells. Blood 115:247-256. http://dx.doi.org/10.1182/blood-2009-07-235176.
19. Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W, Zhao K. 2009. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4:80-93. http://dx.doi.org/10.1016/j.stem.2008.11.011.
20. Attema JL, Papathanasiou P, Forsberg EC, Xu J, Smale ST, Weissman IL. 2007. Epigenetic characterization of hematopoietic stem cell differentiation using miniChIP and bisulfite sequencing analysis. Proc Natl Acad Sci U S A 104:12371-12376. http://dx.doi.org/10.1073/pnas.0704468104.
21. Chang S, Aune TM. 2007. Dynamic changes in histone-methylation 'marks' across the locus encoding interferon-gamma during the differentiation of T helper type 2 cells. Nat Immunol 8:723-731. http://dx.doi.org/10.1038/ni1473.
22. Reddy P, Sun Y, Toubai T, Duran-Struuck R, Clouthier SG, Weisiger E, Maeda Y, Tawara I, Krijanovski O, Gatza E, Liu C, Malter C, Mascagni P, Dinarello CA, Ferrara JL. 2008. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J Clin Invest 118: 2562-2573. http://dx.doi.org/10.1172/JCI34712.
23. Sun Y, Chin YE, Weisiger E, Malter C, Tawara I, Toubai T, Gatza E, Mascagni P, Dinarello CA, Reddy P. 2009. Cutting edge: negative regulation of dendritic cells through acetylation of the nonhistone protein STAT-3. J Immunol 182:5899-58903. http://dx.doi.org/10.4049/jimmunol.0804388.
24. Nencioni A, Beck J, Werth D, Grunebach F, Patrone F, Ballestrero A, Brossart P. 2007. Histone deacetylase inhibitors affect dendritic cell differentiation and immunogenicity. Clin Cancer Res 13:3933-3941. http://dx.doi.org/10.1158/1078-0432.CCR-06-2903.
25. Licciardi PV, Karagiannis TC. 2012. Regulation of immune responses by histone deacetylase inhibitors. ISRN Hematol 2012:690-901. http://dx.doi.org/10.5402/2012/690901.
26. Rosborough BR, Castellaneta A, Natarajan S, Thomson AW, Turnquist HR. 2012. Histone deacetylase inhibition facilitates GM-CSF-mediated expansion of myeloid-derived suppressor cells in vitro and in vivo. J Leukoc Biol 91:701-709. http://dx.doi.org/10.1189/jlb.0311119.
27. Qin A, Cai W, Pan T, Wu K, Yang Q, Wang N, Liu Y, Yan D, Hu F, Guo P, Chen X, Chen L, Zhang H, Tang X, Zhou J. 2013. Expansion of monocytic myeloid-derived suppressor cells dampens T cell function in HIV-1-seropositive individuals. J Virol 87:1477-1490. http://dx.doi.org/10.1128/JVI.01759-12.
28. Sharabi AB, Aldrich M, Sosic D, Olson EN, Friedman AD, Lee SH, Chen SY. 2008. Twist-2 controls myeloid lineage development and function. PLoS Biol 6(12):e316. http://dx.doi.org/10.1371/journal.pbio.0060316.
29. Teerlink T, Nijveldt RJ, de Jong S, van Leeuwen PA. 2002. Determination of arginine, asymmetric dimethylarginine, and symmetric dimethylarginine in human plasma and other biological samples by highperformance liquid chromatography. Anal Biochem 303:131-137. http://dx.doi.org/10.1006/abio.2001.5575.
30. Kutner RH, Zhang XY, Reiser J. 2009. Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat Protoc 4:495-505. http://dx.doi.org/10.1038/nprot.2009.22.
31. Shen L, Evel-Kabler K, Strube R, Chen SY. 2004. Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific antitumor immunity. Nat Biotechnol 22:1546-1553. http://dx.doi.org/10.1038/nbt1035.
32. Haviernik P, Zhang Y, Bunting KD. 2008. Retroviral transduction of murine hematopoietic stem cells. Methods Mol Biol 430:229-241. http://dx.doi.org/10.1007/978-1-59745-182-6_16.
33. Kamphorst AO, Guermonprez P, Dudziak D, Nussenzweig MC. 2010. Route of antigen uptake differentially impacts presentation by dendritic cells and activated monocytes. J Immunol 185:3426-3435. http://dx.doi.org/10.4049/jimmunol.1001205.
34. Luskey BD, Rosenblatt M, Zsebo K, Williams DA. 1992. Stem cell factor, interleukin-3, and interleukin-6 promote retroviral-mediated gene transfer into murine hematopoietic stem cells. Blood 80:396-402.
35. Naik SH, Proietto AI, Wilson NS, Dakic A, Schnorrer P, Fuchsberger M, Lahoud MH, O'Keeffe M, Shao Q X, Chen WF, Villadangos J A, Shortman K, Wu L. 2005. Cutting edge: generation of splenic CD8 and CD8 dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J Immunol 174:6592-6597. http://dx.doi.org/10.4049/jimmunol.174.11.6592.
36. Zhou W, Zhu P, Wang J, Pascual G, Ohgi KA, Lozach J, Glass CK, Rosenfeld MG. 2008. Histone H2A monoubiquitination represses transcription by inhibitingRNApolymerase II transcriptional elongation. Mol Cell 29:69-80. http://dx.doi.org/10.1016/j.molcel.2007.11.002.
37. Pauleau AL, Rutschman R, Lang R, Pernis A, Watowich SS, Murray PJ. 2004. Enhancer-mediated control of macrophage-specific arginase I expression. J Immunol 172:7565-7573. http://dx.doi.org/10.4049/jimmunol.172.12.7565.
38. Kramer OH, Knauer SK, Greiner G, Jandt E, Reichardt S, Guhrs KH, Stauber RH, Bohmer FD, Heinzel T. 2009. A phosphorylation-acetylation switch regulates STAT1 signaling. Genes Dev 23:223-235. http://dx.doi.org/10.1101/gad.479209.
39. Naik SH, Metcalf D, van Nieuwenhuijze A, Wicks I, Wu L, O'Keeffe M, Shortman K. 2006. Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol 7:663-671. http://dx.doi.org/10.1038/ni1340.
40. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128:693-705. http://dx.doi.org/10.1016/j.cell.2007.02.005.
41. Singh SK, Williams CA, Klarmann K, Burkett SS, Keller J R, Oberdoerffer P. 2013. Sirt1 ablation promotes stress-induced loss of epigenetic and genomic hematopoietic stem and progenitor cell maintenance. J Exp Med 210:987-1001. http://dx.doi.org/10.1084/jem.20121608.
42. Mann GE, Yudilevich DL, Sobrevia L. 2003. Regulation of amino acid and glucose transporters in endothelial and smooth muscle cells. Physiol Rev 83:183-252.
43. Rodriguez PC, Zea AH, DeSalvo J, Culotta KS, Zabaleta J, Quiceno DG, Ochoa J B, Ochoa AC. 2003. L-Arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J Immunol 171:1232-1239. http://dx.doi.org/10.4049/jimmunol.171.3.1232.
44. Highfill SL, Rodriguez PC, Zhou Q, Goetz CA, Koehn BH, Veenstra R, Taylor PA, Panoskaltsis-Mortari A, Serody J S, Munn DH, Tolar J, Ochoa AC, Blazar BR. 2010. Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graft-versus-host disease (GVHD) via an arginase- 1-dependent mechanism that is up-regulated by interleukin-13. Blood 116:5738-5747. http://dx.doi.org/10.1182/blood-2010-06-287839.
45. Gray MJ, Poljakovic M, Kepka-Lenhart D, Morris SJ. 2005. Induction of arginase I transcription by IL-4 requires a composite DNA response element for STAT6 and C/EBPbeta. Gene 353:98-106. http://dx.doi.org/10.1016/j.gene.2005.04.004.
46. Osorio EY, Travi BL, Da CA, Saldarriaga OA, Medina AA, Melby PC. 2014. Growth factor and Th2 cytokine signaling pathways converge at STAT6 to promote arginase expression in progressive experimental visceral leishmaniasis. PLoS Pathog 10(6):e1004165. http://dx.doi.org/10.1371/journal.ppat.1004165.
47. Sheldon KE, Shandilya H, Kepka-Lenhart D, Poljakovic M, Ghosh A, Morris SJ. 2013. Shaping the murine macrophage phenotype: IL-4 and cyclic AMP synergistically activate the arginase I promoter. J Immunol 191:2290-2298.
48. Icardi L, De Bosscher K, Tavernier J. 2012. The HAT/HDAC interplay: multilevel control of STAT signaling. Cytokine Growth Factor Rev 23: 283-291. http://dx.doi.org/10.1016/j.cytogfr.2012.08.002.
49. Zhuang S. 2013. Regulation of STAT signaling by acetylation. Cell Signal 25:1924-1931. http://dx.doi.org/10.1016/j.cellsig.2013.05.007.
50. Pang M, Ma L, Liu N, Ponnusamy M, Zhao TC, Yan H, Zhuang S. 2011. Histone deacetylase 1/2 mediates proliferation of renal interstitial fibroblasts and expression of cell cycle proteins. J Cell Biochem 112:2138-2148. http://dx.doi.org/10.1002/jcb.23135.
51. Shankaranarayanan P, Chaitidis P, Kuhn H, Nigam S. 2001. Acetylation by histone acetyltransferase CREB-binding protein/p300 of STAT6 is required for transcriptional activation of the 15-lipoxygenase-1 gene. J Biol Chem 276:42753-42760. http://dx.doi.org/10.1074/jbc. M102626200.
52. Tussiwand R, Lee WL, Murphy TL, Mashayekhi MWKC, Albring JC, Satpathy AT, Rotondo J A, Edelson BT, Kretzer NM, Wu X, Weiss LA, Glasmacher E, Li P, Liao W, Behnke M, Lam SS, Aurthur CT, Leonard WJ, Singh H, Stallings CL, Sibley LD, Schreiber RD, Murphy KM. 2012. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature 490:502-507. http://dx.doi.org/10.1038/nature11531.
53. Edelson BT, KC W, Juang R, Kohyama M, Benoit LA, Klekotka PA, Moon C, Albring J C, Ise W, Michael DG, Bhattacharya D, Stappenbeck TS, Holtzman MJ, Sung SS, Murphy TL, Hildner K, Murphy KM. 2010. Peripheral CD103 dendritic cells form a unified subset developmentally related to CD8alpha conventional dendritic cells. J Exp Med 207:823-836. http://dx.doi.org/10.1084/jem.20091627.
54. Kashiwada M, Pham NL, Pewe LL, Harty J T, Rothman PB. 2011. NFIL3/E4BP4 is a key transcription factor for CD8alpha(+) dendritic cell development. Blood 117:6193-6197. http://dx.doi.org/10.1182/blood-2010-07-295873.
55. Prince HM, Bishton MJ, Harrison SJ. 2009. Clinical studies of histone deacetylase inhibitors. Clin Cancer Res 15:3958-3969. http://dx.doi.org/10.1158/1078-0432.CCR-08-2785.