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Citations to this article

Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase–dependent DC functions and regulates experimental graft-versus-host disease in mice
Pavan Reddy, … , Charles A. Dinarello, James L.M. Ferrara
Pavan Reddy, … , Charles A. Dinarello, James L.M. Ferrara
Published June 20, 2008
Citation Information: J Clin Invest. 2008;118(7):2562-2573. https://doi.org/10.1172/JCI34712.
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Research Article Immunology

Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase–dependent DC functions and regulates experimental graft-versus-host disease in mice

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Abstract

Histone deacetylase (HDAC) inhibitors are antitumor agents that also have antiinflammatory properties. However, the mechanisms of their immunomodulatory functions are not known. We investigated the mechanisms of action of 2 HDAC inhibitors, suberoylanilide hydroxamic acid (SAHA) and ITF 2357, on mouse DC responses. Pretreatment of DCs with HDAC inhibitors significantly reduced TLR-induced secretion of proinflammatory cytokines, suppressed the expression of CD40 and CD80, and reduced the in vitro and in vivo allostimulatory responses induced by the DCs. In addition, injection of DCs treated ex vivo with HDAC inhibitors reduced experimental graft-versus-host disease (GVHD) in a murine allogeneic BM transplantation model. Exposure of DCs to HDAC inhibitors increased expression of indoleamine 2,3-dioxygenase (IDO), a suppressor of DC function. Blockade of IDO in WT DCs with siRNA and with DCs from IDO-deficient animals caused substantial reversal of HDAC inhibition–induced in vitro suppression of DC-stimulated responses. Direct injection of HDAC inhibitors early after allogeneic BM transplantation to chimeric animals whose BM-derived cells lacked IDO failed to protect from GVHD, demonstrating an in vivo functional role for IDO. Together, these data show that HDAC inhibitors regulate multiple DC functions through the induction of IDO and suggest that they may represent a novel class of agents to treat immune-mediated diseases.

Authors

Pavan Reddy, Yaping Sun, Tomomi Toubai, Raimon Duran-Struuck, Shawn G. Clouthier, Elizabeth Weisiger, Yoshinobu Maeda, Isao Tawara, Oleg Krijanovski, Erin Gatza, Chen Liu, Chelsea Malter, Paolo Mascagni, Charles A. Dinarello, James L.M. Ferrara

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Histone deacetylase inhibitors for purging HIV-1 from the latent reservoir
S Matalon, TA Rasmussen, CA Dinarello
Molecular Medicine 2011
The oral histone deacetylase inhibitor ITF2357 reduces cytokines and protects islet β cells in vivo and in vitro
EC Lewis, L Blaabjerg, J Størling, SG Ronn, P Mascagni, CA Dinarello, T Mandrup-Poulsen
Molecular Medicine 2011
HDAC inhibition in lupus models
CM Reilly, N Regna, N Mishra
Molecular Medicine 2011
Histone Deacetylase Inhibitors for Treating a Spectrum of Diseases Not Related to Cancer
CA Dinarello, G Fossati, P Mascagni
Molecular Medicine 2011
Clinical perspectives for regulatory T cells in transplantation tolerance
KL Hippen, JL Riley, CH June, BR Blazar
Seminars in Immunology 2011
Histone deacetylase inhibition alters dendritic cells to assume a tolerogenic phenotype and ameliorates arthritis in SKG mice
K Misaki, A Morinobu, J Saegusa, S Kasagi, M Fujita, Y Miyamoto, F Matsuki, S Kumagai
Arthritis Research & Therapy 2011
Trichostatin Differentially Regulates Th1 and Th2 Responses and Alleviates Rheumatoid Arthritis in Mice
X Zhou, X Hua, X Ding, Y Bian, X Wang
Journal of Clinical Immunology 2011
Inhibition of histone deacetylases in inflammatory bowel diseases
R Glauben, B Siegmund
Molecular Medicine 2011
Histone deacetylase inhibitor LAQ824 augments inflammatory responses in macrophages through transcriptional regulation of IL-10
H Wang, F Cheng, K Woan, E Sahakian, O Merino, J Rock-Klotz, I Vicente-Suarez, J Pinilla-Ibarz, KL Wright, E Seto, K Bhalla, A Villagra, EM Sotomayor
Journal of immunology (Baltimore, Md. : 1950) 2011
The therapeutic potential of HDAC inhibitors in the treatment of multiple sclerosis
G Faraco, L Cavone, A Chiarugi
Molecular Medicine 2011
HDAC inhibition in rheumatoid arthritis and juvenile idiopathic arthritis
J Vojinovic, N Damjanov
Molecular Medicine 2011
Tolerance in clinical transplantation: progress, challenge or just a dream?
F Fändrich
Langenbeck's Archives of Surgery 2011
Modulation of antigen-presenting cells by HDAC inhibitors: implications in autoimmunity and cancer
KV Woan, E Sahakian, EM Sotomayor, E Seto, A Villagra
Immunology and Cell Biology 2011
IFN-γ and indoleamine 2,3-dioxygenase signaling between donor dendritic cells and T cells regulates graft versus host and graft versus leukemia activity
Y Lu, CR Giver, A Sharma, JM Li, KA Darlak, LM Owens, JD Roback, J Galipeau, EK Waller
Blood 2011
IDO in human gut graft-versus-host disease
P Ratajczak, A Janin, RP de Larour, L Koch, B Roche, D Munn, BR Blazar, G Socié
Biology of Blood and Marrow Transplantation 2011
The Histone Deacetylase Inhibitor ITF2357 Decreases Surface CXCR4 and CCR5 Expression on CD4+ T-Cells and Monocytes and is Superior to Valproic Acid for Latent HIV-1 Expression in Vitro
S Matalon, BE Palmer, MF Nold, A Furlan, A Kassu, G Fossati, P Mascagni, CA Dinarello
Journal of acquired immune deficiency syndromes (1999) 2010
Histone deacetylase inhibitors: potential targets responsible for their anti-cancer effect
M Dickinson, RW Johnstone, HM Prince
Investigational New Drugs 2010
Concise review: hitting the right spot with mesenchymal stromal cells
J Tolar, KL Blanc, A Keating, BR Blazar
Stem Cells 2010
A Crucial Role for Host APCs in the Induction of Donor CD4 + CD25 + Regulatory T Cell-Mediated Suppression of Experimental Graft-versus-Host Disease
I Tawara, WD Shlomchik, A Jones, W Zou, E Nieves, C Liu, T Toubai, R Duran-Struuck, Y Sun, SG Clouthier, R Evers, KP Lowler, RB Levy, P Reddy
Journal of immunology (Baltimore, Md. : 1950) 2010
Immunization with host-type CD8{alpha}+ dendritic cells reduces experimental acute GVHD in an IL-10-dependent manner
T Toubai, C Malter, I Tawara, C Liu, E Nieves, KP Lowler, Y Sun, P Reddy
Blood 2010
Dendritic Cells, Indoleamine 2,3 Dioxygenase and Acquired Immune Privilege
L Huang, B Baban, BA Johnson, AL Mellor
International Reviews of Immunology 2010
B-lymphoid cells with attributes of dendritic cells regulate T cells via indoleamine 2,3-dioxygenase
BA 3rd, DJ Kahler, B Baban, PR Chandler, B Kang, M Shimoda, PA Koni, J Pihkala, B Vilagos, M Busslinger, DH Munn, AL Mellor
Proceedings of the National Academy of Sciences 2010
Interleukin-6 modulates graft-versus-host responses after experimental allogeneic bone marrow transplantation
I Tawara, M Koyama, C Liu, T Toubai, D Thomas, R Evers, P Chockley, E Nieves, Y Sun, KP Lowler, C Malter, N Nishimoto, GR Hill, P Reddy
Clinical cancer research 2010
p21(Cip1) up-regulated during histone deacetylase inhibitor-induced CD4(+) T-cell anergy selectively associates with mitogen-activated protein kinases
AS Dagtas, KM Gilbert
Immunology 2010
Transcriptome analysis revealed unique genes as targets for the anti-inflammatory action of activated protein C in human macrophages
CP Pereira, EB Bachli, DJ Schaer, G Schoedon
PloS one 2010
HDAC inhibition by LBH589 affects the phenotype and function of human myeloid dendritic cells
W Song, YT Tai, Z Tian, T Hideshima, D Chauhan, P Nanjappa, MA Exley, KC Anderson, NC Munshi
Leukemia 2010
Pancreatic Islet Transplants and IDO: When Starving the Enemy Does You Good
L Crisa
Diabetes 2010
Indoleamine 2,3-dioxygenase in human hematopoietic stem cell transplantation.
Jürgens B, Raberger J, Fuchs D, Heitger A
International journal of tryptophan research : IJTR 2010
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009
Acute graft-versus-host disease: from the bench to the bedside
G Socié, BR Blazar
Blood 2009
New perspectives on the biology of acute GVHD
S Paczesny, D Hanauer, Y Sun, P Reddy
Bone Marrow Transplantation 2009
The many roles of histone deacetylases in development and physiology: implications for disease and therapy
M Haberland, RL Montgomery, EN Olson
Nature reviews. Genetics 2009
Immunomodulatory effects of deacetylase inhibitors: therapeutic targeting of FOXP3+ regulatory T cells
L Wang, EF de Zoeten, MI Greene, WW Hancock
Nature Reviews Drug Discovery 2009
Cutting Edge: Negative Regulation of Dendritic Cells through Acetylation of the Nonhistone Protein STAT-3
Y Sun, YE Chin, E Weisiger, C Malter, I Tawara, T Toubai, E Gatza, P Mascagni, CA Dinarello, P Reddy
Journal of immunology (Baltimore, Md. : 1950) 2009
Targeting the immunoregulatory indoleamine 2,3 dioxygenase pathway in immunotherapy
BA rd, B Baban, AL Mellor
Immunotherapy 2009
Acute graft-versus-host disease: new treatment strategies:
S Paczesny, SW Choi, JL Ferrara
Current Opinion in Hematology 2009
Inducing the tryptophan catabolic pathway, indoleamine 2,3-dioxygenase (IDO), for suppression of graft-versus-host disease (GVHD) lethality
LK Jasperson, C Bucher, A Panoskaltsis-Mortari, AL Mellor, DH Munn, BR Blazar
Blood 2009
Granulocyte colony-stimulating factor-induced immature myeloid cells inhibit acute graft-versus-host disease lethality through an indoleamine dioxygenase-independent mechanism
YD Joo, SM Lee, SW Lee, WS Lee, SM Lee, JK Park, IW Choi, SG Park, I Choi, SK Seo
Immunology 2009
The Importance of NAD in Multiple Sclerosis
Penberthy WT, Tsunoda I
Current pharmaceutical design 2009
IDO: a double-edged sword for T(H)1/T(H)2 regulation
H Xu, GX Zhang, B Ciric, A Rostami
Immunology Letters 2008
Gene microarray analysis of human renal cell carcinoma: The effects of HDAC inhibition and retinoid treatment
Tavares TS, Nanus D, Yang XJ, Gudas LJ
Cancer biology & therapy 2008

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