The histone deacetylase inhibitor, LBH589, promotes the systemic cytokine and effector responses of adoptively transferred CD8+ T cells

Journal for ImmunoTherapy of Cancer

Volumn 2, Issue 1, 2014, Pages

  Lisiero, Dominique N ^a   Soto, Horacio ^a   Everson, Richard G ^a   Liau, Linda M ^a   Prins, Robert M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dendritic cells; Inflammation; T cells; Tumor immunity

Indexed keywords

CYTOKINE; DENDRITIC CELL VACCINE; GLYCOPROTEIN GP 100; INTERLEUKIN 2 RECEPTOR; PANOBINOSTAT;

ADOPTIVE CELL TRANSFER THERAPY; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CANCER TRANSPLANTATION; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; DRUG EFFECT; DRUG MECHANISM; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REGULATORY T LYMPHOCYTE; TUMOR IMMUNITY; TUMOR REGRESSION;

EID: 84977134550     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/2051-1426-2-8     Document Type: Article

References (41)

1. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, Topalian SL, Sherry R, Restifo NP, Hubicki AM, Robinson MR, Raffeld M, Duray P, Seipp CA, Rogers-Freezer L, Morton KE, Mavroukakis SA, White DE, Rosenberg SA. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002, 298:850-854. 10.1126/science.1076514, 1764179, 12242449.
2. Rosenberg SA, Aebersold P, Cornetta K, Kasid A, Morgan RA, Moen R, Karson EM, Lotze MT, Yang JC, Topalian SL. Gene transfer into humans-immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. N Engl J Med 1990, 323:570-578. 10.1056/NEJM199008303230904, 2381442.
3. Hu HM, Urba WJ, Fox BA. Gene-modified tumor vaccine with therapeutic potential shifts tumor-specific T cell response from a type 2 to a type 1 cytokine profile. J Immunol 1998, 161:3033-3041.
4. Sussman JJ, Parihar R, Winstead K, Finkelman FD. Prolonged culture of vaccine-primed lymphocytes results in decreased antitumor killing and change in cytokine secretion. Cancer Res 2004, 64:9124-9130. 10.1158/0008-5472.CAN-03-0376, 15604282.
5. Tatsumi T, Kierstead LS, Ranieri E, Gesualdo L, Schena FP, Finke JH, Bukowski RM, Mueller-Berghaus J, Kirkwood JM, Kwok WW, Storkus WJ. Disease-associated bias in T helper type 1 (Th1)/Th2 CD4+ T cell responses against MAGE-6 in HLA-DRB10401+ patients with renal cell carcinoma or melanoma. J Exp Med 2002, 196:619-628. 10.1084/jem.20012142, 2193999, 12208877.
6. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ, Hwang LN, Yu Z, Wrzesinski C, Heimann DM, Surh CD, Rosenberg SA, Restifo NP. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 2005, 202:907-912. 10.1084/jem.20050732, 1397916,1397916, 16203864.
7. Klebanoff CA, Khong HT, Antony PA, Palmer DC, Restifo NP. Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends Immunol 2005, 26:111-117. 10.1016/j.it.2004.12.003, 1388277, 15668127.
8. Klebanoff CA, Gattinoni L, Palmer DC, Muranski P, Ji Y, Hinrichs CS, Borman ZA, Kerkar SP, Scott CD, Finkelstein SE, Rosenberg SA, Restifo NP. Determinants of successful CD8+ T-cell adoptive immunotherapy for large established tumors in mice. Clin Cancer Res 2011, 17:5343-5352. 10.1158/1078-0432.CCR-11-0503, 3176721, 21737507.
9. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 2006, 5:769-784. 10.1038/nrd2133, 16955068.
10. Lane AA, Chabner BA. Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 2009, 27:5459-5468. 10.1200/JCO.2009.22.1291, 19826124.
11. Kurdistani SK, Grunstein M. Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol 2003, 4:276-284. 10.1038/nrm1075, 12671650.
12. Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 2006, 6:38-51. 10.1038/nrc1779, 16397526.
13. Sutheesophon K, Nishimura N, Kobayashi Y, Furukawa Y, Kawano M, Itoh K, Kano Y, Ishii H, Furukawa Y. Involvement of the tumor necrosis factor (TNF)/TNF receptor system in leukemic cell apoptosis induced by histone deacetylase inhibitor depsipeptide (FK228). J Cell Physiol 2005, 203:387-397. 10.1002/jcp.20235, 15515013.
14. Magner WJ, Kazim AL, Stewart C, Romano MA, Catalano G, Grande C, Keiser N, Santaniello F, Tomasi TB. Activation of MHC class I, II, and CD40 gene expression by histone deacetylase inhibitors. J Immunol 2000, 165:7017-7024. 10.4049/jimmunol.165.12.7017, 11120829.
15. Maeda T, Towatari M, Kosugi H, Saito H. Up-regulation of costimulatory/adhesion molecules by histone deacetylase inhibitors in acute myeloid leukemia cells. Blood 2000, 96:3847-3856.
16. Inoue S, MacFarlane M, Harper N, Wheat LMC, Dyer MJS, Cohen GM. Histone deacetylase inhibitors potentiate TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in lymphoid malignancies. Cell Death Differ 2004, 11(Suppl 2):S193-S206.
17. Murakami T, Sato A, Chun NAL, Hara M, Naito Y, Kobayashi Y, Kano Y, Ohtsuki M, Furukawa Y, Kobayashi E. Transcriptional modulation using HDACi depsipeptide promotes immune cell-mediated tumor destruction of murine B16 melanoma. J Invest Dermatol 2008, 128:1506-1516. 10.1038/sj.jid.5701216, 18185535.
18. Li B, Samanta A, Song X, Iacono KT, Bembas K, Tao R, Basu S, Riley JL, Hancock WW, Shen Y, Saouaf SJ, Greene MI. FOXP3 interactions with histone acetyltransferase and class II histone deacetylases are required for repression. Proc Natl Acad Sci U S A 2007, 104:4571-4576. 10.1073/pnas.0700298104, 1838642, 17360565.
19. 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 JLM. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J Clin Invest 2008, 118:2562-2573. 2430497, 18568076.
20. Tao R, de Zoeten EF, Ozkaynak E, Chen C, Wang L, Porrett PM, Li B, Turka LA, Olson EN, Greene MI, Wells AD, Hancock WW. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 2007, 13:1299-1307. 10.1038/nm1652, 17922010.
21. Atadja P. Development of the pan-DAC inhibitor panobinostat (LBH589): successes and challenges. Cancer Lett 2009, 280:233-241. 10.1016/j.canlet.2009.02.019, 19344997.
22. Younes A, Sureda A, Ben-Yehuda D, Zinzani PL, Ong T-C, Prince HM, Harrison SJ, Kirschbaum M, Johnston P, Gallagher J, Le Corre C, Shen A, Engert A. Panobinostat in patients with relapsed/refractory Hodgkin's lymphoma after autologous stem-cell transplantation: results of a phase II study. J Clin Oncol 2012, 30:2197-2203. 10.1200/JCO.2011.38.1350, 22547596.
23. Ellis L, Bots M, Lindemann RK, Bolden JE, Newbold A, Cluse LA, Scott CL, Strasser A, Atadja P, Lowe SW, Johnstone RW. The histone deacetylase inhibitors LAQ824 and LBH589 do not require death receptor signaling or a functional apoptosome to mediate tumor cell death or therapeutic efficacy. Blood 2009, 114:380-393. 10.1182/blood-2008-10-182758, 19383971.
24. Vo DD, Prins RM, Begley JL, Donahue TR, Morris LF, Bruhn KW, de la Rocha P, Yang M-Y, Mok S, Garban HJ, Craft N, Economou JS, Marincola FM, Wang E, Ribas A. Enhanced antitumor activity induced by adoptive T-cell transfer and adjunctive use of the histone deacetylase inhibitor LAQ824. Cancer Res 2009, 69:8693-8699. 10.1158/0008-5472.CAN-09-1456, 2779578, 19861533.
25. Leoni F, Zaliani A, Bertolini G, Porro G, Pagani P, Pozzi P, Donà G, Fossati G, Sozzani S, Azam T, Bufler P, Fantuzzi G, Goncharov I, Kim S-H, Pomerantz BJ, Reznikov LL, Siegmund B, Dinarello CA, Mascagni P. The antitumor histone deacetylase inhibitor suberoylanilide hydroxamic acid exhibits antiinflammatory properties via suppression of cytokines. Proc Natl Acad Sci U S A 2002, 99:2995-3000. 10.1073/pnas.052702999, 122461, 11867742.
26. Beutler BA, Milsark IW, Cerami A. Cachectin/tumor necrosis factor: production, distribution, and metabolic fate in vivo. J Immunol 1985, 135:3972-3977.
27. Vire B, de Walque S, Restouin A, Olive D, Van Lint C, Collette Y. Anti-leukemia activity of MS-275 histone deacetylase inhibitor implicates 4-1BBL/4-1BB immunomodulatory functions. PLoS One 2009, 4:e7085. 10.1371/journal.pone.0007085, 2738963, 19759901.
28. Reddy RM, Yeow W-S, Chua A, Nguyen DM, Baras A, Ziauddin MF, Shamimi-Noori SM, Maxhimer JB, Schrump DS, Nguyen DM. Rapid and profound potentiation of Apo2L/TRAIL-mediated cytotoxicity and apoptosis in thoracic cancer cells by the histone deacetylase inhibitor Trichostatin A: the essential role of the mitochondria-mediated caspase activation cascade. Apoptosis 2007, 12:55-71. 10.1007/s10495-006-0484-z, 17136498.
29. Buglio D, Khaskhely NM, Voo KS, Martinez-Valdez H, Liu Y-J, Younes A. HDAC11 plays an essential role in regulating OX40 ligand expression in Hodgkin lymphoma. Blood 2011, 117:2910-2917. 10.1182/blood-2010-08-303701, 3062301, 21239696.
30. Lisiero DN, Soto H, Liau LM, Prins RM. Enhanced sensitivity to IL-2 signaling regulates the clinical responsiveness of IL-12-primed CD8(+) T cells in a melanoma model. J Immunol 2011, 186:5068-5077. 10.4049/jimmunol.1003317, 3532507, 21430221.
31. Quezada SA, Peggs KS, Curran MA, Allison JP. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J Clin Invest 2006, 116:1935-1945. 10.1172/JCI27745, 1479425, 16778987.
32. Quezada SA, Peggs KS, Simpson TR, Shen Y, Littman DR, Allison JP. Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. J Exp Med 2008, 205:2125-2138. 10.1084/jem.20080099, 2526206, 18725522.
33. Yao X, Ahmadzadeh M, Lu Y-C, Liewehr DJ, Dudley ME, Liu F, Schrump DS, Steinberg SM, Rosenberg SA, Robbins PF. Levels of peripheral CD4 + FoxP3+ regulatory T cells are negatively associated with clinical response to adoptive immunotherapy of human cancer. Blood 2012, 119:5688-5696. 10.1182/blood-2011-10-386482, 3382928, 22555974.
34. Song W, Tai Y-T, Tian Z, Hideshima T, Chauhan D, Nanjappa P, Exley MA, Anderson KC, Munshi NC. HDAC inhibition by LBH589 affects the phenotype and function of human myeloid dendritic cells. Leukemia 2011, 25:161-168. 10.1038/leu.2010.244, 3839585, 21102427.
35. Croft M. The role of TNF superfamily members in T-cell function and diseases. Nat Rev Immunol 2009, 9:271-285. 10.1038/nri2526, 2737409, 19319144.
36. Calzascia T, Pellegrini M, Hall H, Sabbagh L, Ono N, Elford AR, Mak TW, Ohashi PS. TNF-alpha is critical for antitumor but not antiviral T cell immunity in mice. J Clin Invest 2007, 117:3833-3845. 2066188, 17992258.
37. Bansal-Pakala P, Halteman BS, Cheng MH-Y, Croft M. Costimulation of CD8 T cell responses by OX40. J Immunol 2004, 172:4821-4825. 10.4049/jimmunol.172.8.4821, 15067059.
38. Gough MJ, Ruby CE, Redmond WL, Dhungel B, Brown A, Weinberg AD. OX40 agonist therapy enhances CD8 infiltration and decreases immune suppression in the tumor. Cancer Res 2008, 68:5206-5215. 10.1158/0008-5472.CAN-07-6484, 18593921.
39. Redmond WL, Gough MJ, Charbonneau B, Ratliff TL, Weinberg AD. Defects in the acquisition of CD8 T cell effector function after priming with tumor or soluble antigen can be overcome by the addition of an OX40 agonist. J Immunol 2007, 179:7244-7253. 10.4049/jimmunol.179.11.7244, 18025166.
40. Ruby CE, Redmond WL, Haley D, Weinberg AD. Anti-OX40 stimulation in vivo enhances CD8+ memory T cell survival and significantly increases recall responses. Eur J Immunol 2007, 37:157-166. 10.1002/eji.200636428, 17183611.
41. Prins RM, Shu CJ, Radu CG, Vo DD, Khan-Farooqi H, Soto H, Yang M-Y, Lin M-S, Shelly S, Witte ON, Ribas A, Liau LM. Anti-tumor activity and trafficking of self, tumor-specific T cells against tumors located in the brain. Cancer Immunol Immunother 2008, 57:1279-1289. 10.1007/s00262-008-0461-1, 2614264, 18253732.