Class IIa HDAC inhibition reduces breast tumours and metastases through anti-tumour macrophages

Nature

Volumn 543, Issue 7645, 2017, Pages 428-432

  Guerriero, Jennifer L ^a   Sotayo, Alaba ^a   Ponichtera, Holly E ^a   Castrillon, Jessica A ^a   Pourzia, Alexandra L ^a   Schad, Sara ^a   Johnson, Shawn F ^a   Carrasco, Ruben D ^b   Lazo, Suzan ^a   Bronson, Roderick T ^c   Davis, Scott P ^d   Lobera, Mercedes ^d   Nolan, Michael A ^d   Letai, Anthony ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CARBOPLATIN; CASPASE 3; CD11B ANTIGEN; CD34 ANTIGEN; CD40 ANTIGEN; CD45 ANTIGEN; EPITHELIAL CELL ADHESION MOLECULE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANZYME B; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITOR; INTERLEUKIN 4; PACLITAXEL; TMP 195; UNCLASSIFIED DRUG; VIRUS MIDDLE T ANTIGEN; VORINOSTAT; BENZAMIDE DERIVATIVE; OXADIAZOLE DERIVATIVE; TMP195;

CANCER; HOMEOSTASIS; IMMUNE SYSTEM; INHIBITION; INHIBITOR; PHENOTYPE; PROTEIN; RODENT; TUMOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; MONOCYTE; MONOTHERAPY; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; ANIMAL; BREAST NEOPLASMS; CELL DIFFERENTIATION; CLASSIFICATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; DRUG POTENTIATION; ENZYMOLOGY; FEMALE; IMMUNOLOGY; LUNG NEOPLASMS; MACROPHAGE; MACROPHAGE ACTIVATION; SECONDARY; TUMOR CELL LINE; TUMOR VOLUME; VASCULARIZATION;

ANIMALS; BENZAMIDES; BREAST NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; FEMALE; HISTONE DEACETYLASE INHIBITORS; HUMANS; LUNG NEOPLASMS; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; OXADIAZOLES; PHAGOCYTOSIS; TUMOR BURDEN;

EID: 85015368931     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature21409     Document Type: Article

References (35)

1. Pollard, J. W. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4, 71-78 (2004).
2. DeNardo, D. G. et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 1, 54-67 (2011).
3. Pyonteck, S. M. et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat. Med. 19, 1264-1272 (2013).
4. Beatty, G. L. et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 331, 1612-1616 (2011).
5. Willingham, S. B. et al. The CD47-signal regulatory protein alpha (SIRP? ) interaction is a therapeutic target for human solid tumors. Proc. Natl Acad. Sci. USA 109, 6662-6667 (2012).
6. Lobera, M. et al. Selective class IIa histone deacetylase inhibition via a nonchelating zinc-binding group. Nat. Chem. Biol. 9, 319-325 (2013).
7. Fischle, W. et al. Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol. Cell 9, 45-57 (2002).
8. Lahm, A. et al. Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc. Natl Acad. Sci. USA 104, 17335-17340 (2007).
9. Di Giorgio, E., Gagliostro, E. & Brancolini, C. Selective class IIa HDAC inhibitors: myth or reality. Cell. Mol. Life Sci. 72, 73-86 (2015).
10. Lin, E. Y., Nguyen, A. V., Russell, R. G. & Pollard, J. W. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 193, 727-740 (2001).
11. Malhotra, D. et al. Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks. Nat. Immunol. 13, 499-510 (2012).
12. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).
13. Franklin, R. A. et al. The cellular and molecular origin of tumor-associated macrophages. Science 344, 921-925 (2014).
14. Hanahan, D. & Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364 (1996).
15. Qian, B. Z. & Pollard, J. W. Macrophage diversity enhances tumor progression and metastasis. Cell 141, 39-51 (2010).
16. Heldin, C. H., Rubin, K., Pietras, K. & Ostman, A. High interstitial fluid pressure-an obstacle in cancer therapy. Nat. Rev. Cancer 4, 806-813 (2004).
17. Trédan, O., Galmarini, C. M., Patel, K. & Tannock, I. F. Drug resistance and the solid tumor microenvironment. J. Natl. Cancer Inst. 99, 1441-1454 (2007).
18. Jain, R. K. Antiangiogenesis strategies revisited: from starving tumors to alleviating hypoxia. Cancer Cell 26, 605-622 (2014).
19. Garber, K. Targeting vessel abnormalization in cancer. J. Natl. Cancer Inst. 99, 991-995 (2007).
20. Heng, T. S. & Painter, M. W. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9, 1091-1094 (2008).
21. Bos, P. D., Plitas, G., Rudra, D., Lee, S. Y. & Rudensky, A. Y. Transient regulatory T cell ablation deters oncogene-driven breast cancer and enhances radiotherapy. J. Exp. Med. 210, 2435-2466 (2013).
22. Simpson, T. R. et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J. Exp. Med. 210, 1695-1710 (2013).
23. Dahan, R. et al. Fc? Rs modulate the anti-tumor activity of antibodies targeting the PD-1/PD-L1 axis. Cancer Cell 28, 285-295 (2015).
24. Zhang, M. et al. Anti-CD47 treatment stimulates phagocytosis of glioblastoma by M1 and M2 polarized macrophages and promotes M1 polarized macrophages in vivo. PLoS One 11, e0153550 (2016).
25. van der Sluis, T. C. et al. Therapeutic peptide vaccine-induced CD8 T cells strongly modulate intratumoral macrophages required for tumor regression. Cancer Immunol. Res. 3, 1042-1051 (2015).
26. Gül, N. et al. Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J. Clin. Invest. 124, 812-823 (2014).
27. Burgos, E. S. et al. Histone H2A and H4 N-terminal tails are positioned by the MEP50 WD repeat protein for efficient methylation by the PRMT5 arginine methyltransferase. J. Biol. Chem. 290, 9674-9689 (2015).
28. Theodoulou, N. H. et al. Discovery of I-BRD9, a selective cell active chemical probe for bromodomain containing protein 9 inhibition. J. Med. Chem. 59, 1425-1439 (2016).
29. Ullman-Culleré, M. H. & Foltz, C. J. Body condition scoring: a rapid and accurate method for assessing health status in mice. Lab. Anim. Sci. 49, 319-323 (1999).
30. Ruffell, B. et al. Macrophage IL-10 blocks CD8+ T cell-dependent responses to chemotherapy by suppressing IL-12 expression in intratumoral dendritic cells. Cancer Cell 26, 623-637 (2014).
31. Ahn, G. O. et al. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc. Natl Acad. Sci. USA 107, 8363-8368 (2010).
32. Qian, B. Z. et al. CCL2 recruits inflammatory monocytes to facilitate breasttumour metastasis. Nature 475, 222-225 (2011).
33. Lohela, M. et al. Intravital imaging reveals distinct responses of depleting dynamic tumor-associated macrophage and dendritic cell subpopulations. Proc. Natl Acad. Sci. USA 111, E5086-E5095 (2014).
34. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
35. Huang, F. J. et al. Pericyte deficiencies lead to aberrant tumor vascularizaton in the brain of the NG2 null mouse. Dev. Biol. 344, 1035-1046 (2010).