HDAC inhibition upregulates PD-1 ligands in melanoma and augments immunotherapy with PD-1 blockade

Cancer Immunology Research

Volumn 3, Issue 12, 2015, Pages 1375-1385

  Woods, David M ^a   Sodré, Andressa L ^a   Villagra, Alejandro ^a   Sarnaik, Amod ^a   Sotomayor, Eduardo M ^a   Weber, Jeffrey ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BELINOSTAT; ENTINOSTAT; HISTONE; HISTONE DEACETYLASE; MOCETINOSTAT; PANOBINOSTAT; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; RICOLINOSTAT; ANTINEOPLASTIC AGENT; CD274 PROTEIN, MOUSE; HISTONE DEACETYLASE INHIBITOR; MONOCLONAL ANTIBODY; NIVOLUMAB; PDCD1 PROTEIN, MOUSE; PDCD1LG2 PROTEIN, MOUSE; PEMBROLIZUMAB; PROGRAMMED DEATH 1 RECEPTOR;

ANIMAL CELL; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFICACY; ENZYME INHIBITION; EPIGENETICS; GENE EXPRESSION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MELANOMA; MOUSE; MURINE MODEL; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; SURVIVAL RATE; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; IMMUNOLOGY; IMMUNOTHERAPY; MELANOMA, EXPERIMENTAL; METABOLISM; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD274; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; IMMUNOTHERAPY; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; PROGRAMMED CELL DEATH 1 LIGAND 2 PROTEIN; PROGRAMMED CELL DEATH 1 RECEPTOR; TUMOR MICROENVIRONMENT; UP-REGULATION;

EID: 84962189576     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-15-0077-T     Document Type: Article

References (46)

1. In: Howlader N NA, Krapcho M, Garshell J, Miller D, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (editors). SEER Cancer Statistics Review, 1975-2011. 2014; Available from: Http: //seer.cancer.gov/csr/1975-2011/.
2. Costanza ME, Nathanson L, Costello WG, Wolter J, Brunk SF, Colsky J, et al. Results of a randomized study comparing DTIC with TIC mustard in malignant melanoma. Cancer 1976; 37: 1654-9.
3. Patel PM, Suciu S, Mortier L, Kruit WH, Robert C, Schadendorf D, et al. Extended schedule, escalated dose temozolomide versus dacarbazine in stage IV melanoma: Final results of a randomised phase III study (EORTC 18032). Eur J Cancer 2011; 47: 1476-83.
4. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survivalwith ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363: 711-23.
5. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013; 369: 134-44.
6. Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci U S A 2002; 99: 12293-7.
7. Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, et al. PD-L2 is a second ligand for PD-1 and inhibits T-cell activation. Nat Immunol 2001; 2: 261-8.
8. Sheppard KA, Fitz LJ, Lee JM, Benander C, George JA, Wooters J, et al. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett 2004; 574: 37-41.
9. Parry RV, Chemnitz JM, Frauwirth KA, Lanfranco AR, Braunstein I, Kobayashi SV, et al. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol 2005; 25: 9543-53.
10. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat Med 2002; 8: 793-800.
11. Chemnitz JM, Parry RV, Nichols KE, June CH, Riley JL. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T-cell activation. J Immunol 2004; 173: 945-54.
12. Latchman YE, Liang SC, Wu Y, Chernova T, Sobel RA, Klemm M, et al. PDL1- deficientmice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc Natl Acad Sci U S A 2004; 101: 10691-6.
13. Keir ME, Liang SC, Guleria I, Latchman YE, Qipo A, Albacker LA, et al. Tissue expression of PD-L1 mediates peripheral T-cell tolerance. J Exp Med 2006; 203: 883-95.
14. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med 2012; 4: 127ra37.
15. Saunders PA, Hendrycks VR, Lidinsky WA, Woods ML. PD-L2: PD-1 involvement in T-cell proliferation, cytokine production, and integrinmediated adhesion. Eur J Immunol 2005; 35: 3561-9.
16. Yamazaki T, Akiba H, Iwai H, Matsuda H, Aoki M, Tanno Y, et al. Expression of programmed death 1 ligands by murine T cells and APC. J Immunol 2002; 169: 5538-45.
17. Topalian SL, Drake CG, Pardoll DM. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol 2012; 24: 207-12.
18. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014; 32: 1020-30.
19. Brahmer JR, Tykodi SS, ChowLQ,HwuWJ, Topalian SL,HwuP, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366: 2455-65.
20. Taube JM, Klein A, Brahmer JR, Xu H, Pan X, Kim JH, et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res 2014; 20: 5064-74.
21. Weber JS, Kudchadkar RR, Yu B, Gallenstein D, Horak CE, Inzunza HD, et al. Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanoma. J Clin Oncol 2013; 31: 4311-8.
22. Delcuve GP, Khan DH, Davie JR. Roles of histone deacetylases in epigenetic regulation: Emerging paradigms from studies with inhibitors. Clin Epigenetics 2012; 4: 5.
23. Woods DM, Woan K, Cheng F, Wang H, Perez-Villarroel P, Lee C, et al. The antimelanoma activity of the histone deacetylase inhibitor panobinostat (LBH589) is mediated by direct tumor cytotoxicity and increased tumor immunogenicity. Melanoma Res 2013; 23: 341-8.
24. Khan AN, Tomasi TB. Histone deacetylase regulation of immune gene expression in tumor cells. Immunol Res 2008; 40: 164-78.
25. Magner WJ, Kazim AL, Stewart C, Romano MA, Catalano G, Grande C, et al. Activation of MHC class I, II, and CD40 gene expression by histone deacetylase inhibitors. J Immunol 2000; 165: 7017-24.
26. Vo DD PR, Begley JL, Donahue TR, Morris LF, Bruhn KW, de la Rocha P, et al. Enhanced antitumor activity induced by adoptive T-cell transfer and adjunctive use of the histone deacetylase inhibitor LAQ824. Cancer Res 2009; 69: 8693-9.
27. Kim K, Skora AD, Li Z, Liu Q, Tam AJ, Blosser RL, et al. Eradication of metastatic mouse cancers resistant to immune checkpoint blockade by suppression of myeloid-derived cells. Proc Natl Acad Sci U S A 2014; 111: 11774-9.
28. Desai S, Bolick SC, Maurin M, Wright KL. PU.1 regulates positive regulatory domain I-binding factor 1/Blimp-1 transcription in lymphoma cells. J Immunol 2009; 183: 5778-87.
29. Dokmanovic M, Clarke C, Marks PA. Histone deacetylase inhibitors: Overview and perspectives. Mol Cancer Res 2007; 5: 981-9.
30. Tsao H, Goel V, Wu H, Yang G, Haluska FG. Genetic interaction between NRAS and BRAF mutations and PTEN/MMAC1 inactivation in melanoma. J Invest Dermatol 2004; 122: 337-41.
31. Tanami H, Imoto I, Hirasawa A, Yuki Y, Sonoda I, Inoue J, et al. Involvement of overexpressed wild-type BRAF in the growth of malignant melanoma cell lines. Oncogene 2004; 23: 8796-804.
32. Herlyn M. Melanoma cell lines grouped for BRAF/-N-ras/PTEN/CDk4 mutations. The Wistar Institute 2015.
33. Herlyn M, Thurin J, Balaban G, Bennicelli JL, Herlyn D, Elder DE, et al. Characteristics of cultured human melanocytes isolated from different stages of tumor progression. Cancer Res 1985; 45: 5670-6.
34. Rivoltini L, Barracchini KC, Viggiano V, Kawakami Y, Smith A, Mixon A, et al. Quantitative correlation between HLA class I allele expression and recognition ofmelanoma cells by antigen-specific cytotoxic T lymphocytes. Cancer Res 1995; 55: 3149-57.
35. Shidham VB, Qi DY, Acker S, Kampalath B, Chang CC, George V, et al. Evaluation of micrometastases in sentinel lymph nodes of cutaneous melanoma: Higher diagnostic accuracy with Melan-A and MART-1 compared with S-100 protein and HMB-45. Am J Surg Pathol 2001; 25: 1039-46.
36. Santo L, Hideshima T, Kung AL, Tseng JC, Tamang D, Yang M, et al. Preclinical activity, pharmacodynamic, and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215, in combination with bortezomib in multiple myeloma. Blood 2012; 119: 2579-89.
37. Balasubramanian S, Ramos J, Luo W, Sirisawad M, Verner E, Buggy JJ. A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas. Leukemia 2008; 22: 1026-34.
38. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998; 19: 187-91.
39. Xiong Y, Dowdy SC, Podratz KC, Jin F, Attewell JR, Eberhardt NL, et al. Histone deacetylase inhibitors decrease DNA methyltransferase-3B messenger RNA stability and down-regulate de novo DNA methyltransferase activity in human endometrial cells. Cancer Res 2005; 65: 2684-9.
40. Chiang EY, Henson M, Stroynowski I. Correction of defects responsible for impaired Qa-2 class Ib MHC expression on melanoma cells protects mice from tumor growth. J Immunol 2003; 170: 4515-23.
41. Arts J, King P, Marien A, Floren W, Belien A, Janssen L, et al. JNJ-26481585, a novel "second-generation" oral histone deacetylase inhibitor, shows broad-spectrum preclinical antitumoral activity. Clin Cancer Res 2009; 15: 6841-51.
42. Beckers T, Burkhardt C, Wieland H, Gimmnich P, Ciossek T, Maier T, et al. Distinct pharmacological properties of second generation HDAC inhibitors with the benzamide or hydroxamate head group. Int J Cancer 2007; 121: 1138-48.
43. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC,McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366: 2443-54.
44. Rodig N, Ryan T, Allen JA, Pang H, Grabie N, Chernova T, et al. Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+T cell activation and cytolysis. Eur J Immunol 2003; 33: 3117-26.
45. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A 2010; 107: 4275-80.
46. van Elsas A, Hurwitz AA, Allison JP. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GMCSF)- producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J Exp Med 1999; 190: 355-66.