Epigenetic modifiers reduce inflammation and modulate macrophage phenotype during endotoxemia-induced acute lung injury

Journal of Cell Science

Volumn 128, Issue 15, 2015, Pages 3094-3105

  Thangavel, Jayakumar ^a   Samanta, Saheli ^a   Rajasingh, Sheeja ^a   Barani, Bahar ^a   Xuan, Yu Ting ^a   Dawn, Buddhadeb ^a   Rajasingh, Johnson ^a,b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Acute lung injury; Epigenetic modifiers; Histone deacetylase inhibitor; Inflammation and apoptosis; Sepsis

Indexed keywords

CYTOKINE; DECITABINE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; HISTONE H3; HUR PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOPEROXIDASE; PROTEIN BCL 2; STAT3 PROTEIN; TRICHOSTATIN A; TUMOR NECROSIS FACTOR; AZACITIDINE; DRUG COMBINATION; HISTONE DEACETYLASE; HYDROXAMIC ACID; LIPOPOLYSACCHARIDE; METHYLTRANSFERASE;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; EPIGENETICS; EXPERIMENTAL INFLAMMATION; HISTONE ACETYLATION; HISTOPATHOLOGY; IMMUNOMODULATION; LIPOPOLYSACCHARIDE-INDUCED ENDOTOXEMIA; MACROPHAGE; MALE; MONOTHERAPY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; COMPLICATION; DRUG COMBINATION; DRUG EFFECTS; ENDOTOXEMIA; GENETIC EPIGENESIS; GENETICS; HUMAN; INFLAMMATION; PATHOLOGY; SEPSIS;

ACUTE LUNG INJURY; ANIMALS; AZACITIDINE; DRUG COMBINATIONS; ENDOTOXEMIA; EPIGENESIS, GENETIC; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; METHYLTRANSFERASES; MICE; SEPSIS; SIGNAL TRANSDUCTION;

EID: 84939547558     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.170258     Document Type: Article

References (52)

1. Avila,A.M.,Burnett,B.G., Taye,A.A., Gabanella, F., Knight,M.A.,Hartenstein, P., Cizman, Z., Di Prospero, N. A., Pellizzoni, L., Fischbeck, K. H. et al. (2007). Trichostatin A increases SMN expression and survival in a mouse model of spinal muscular atrophy. J. Clin. Invest. 117, 659-671.
2. Beardmore, V. A., Hinton, H. J., Eftychi, C., Apostolaki, M., Armaka, M., Darragh, J., McIlrath, J., Carr, J. M., Armit, L. J., Clacher, C. et al. (2005). Generation and characterization of p38beta (MAPK11) gene-targeted mice. Mol. Cell. Biol. 25, 10454-10464.
3. Blanchard, F. and Chipoy, C. (2005). Histone deacetylase inhibitors: new drugs for the treatment of inflammatory diseases? Drug Discov. Today 10, 197-204.
4. Blander, J. M. and Medzhitov, R. (2004). Regulation of phagosome maturation by signals from toll-like receptors. Science 304, 1014-1018.
5. Chang, L. and Karin, M. (2001). Mammalian MAP kinase signalling cascades. Nature 410, 37-40.
6. Choi, Y., Park, S.-K., Kim, H. M., Kang, J. S., Yoon, Y. D., Han, S. B., Han, J. W., Yang, J. S. and Han, G. (2008). Histone deacetylase inhibitor KBH-A42 inhibits cytokine production in RAW 264.7 macrophage cells and in vivo endotoxemia model. Exp. Mol. Med. 40, 574-581.
7. Christman, J. K. (2002). 5-Azacytidine and 5-aza-2'-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 21, 5483-5495.
8. Davis, R. J. (2000). Signal transduction by the JNK group of MAP kinases. Cell 103, 239-252.
9. Dellinger, R. P., Levy, M. M., Carlet, J. M., Bion, J., Parker, M. M., Jaeschke, R., Reinhart, K., Angus, D. C., Brun-Buisson, C., Beale, R. et al. (2008). Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit. Care Med. 36, 296-327.
10. Di,A.,Gao,X.-P.,Qian, F.,Kawamura, T.,Han, J.,Hecquet,C.,Ye, R. D.,Vogel,S.M. and Malik, A. B. (2012). The redox-sensitive cation channel TRPM2 modulates phagocyte ROS production and inflammation. Nat. Immunol. 13, 29-34.
11. Diaz, J. V., Brower, R., Calfee, C. S. and Matthay, M. A. (2010). Therapeutic strategies for severe acute lung injury. Crit. Care Med. 38, 1644-1650.
12. Dong, C., Davis, R. J. and Flavell, R. A. (2001). Signaling by the JNK group of MAP kinases. J. Clin. Immunol. 21, 253-257.
13. Dong, C., Davis, R. J. and Flavell, R. A. (2002). MAP kinases in the immune response. Annu. Rev. Immunol. 20, 55-72.
14. Furumai, R., Ito, A., Ogawa, K., Maeda, S., Saito, A., Nishino, N., Horinouchi, S. and Yoshida, M. (2011). Histone deacetylase inhibitors block nuclear factor-kappaB-dependent transcription by interfering with RNA polymerase II recruitment. Cancer Sci. 102, 1081-1087.
15. Hashimshony, T., Zhang, J., Keshet, I., Bustin, M. and Cedar, H. (2003). The role of DNA methylation in setting up chromatin structure during development. Nat. Genet. 34, 187-192.
16. Hsing, C.-H., Lin, C.-F., So, E., Sun, D.-P., Chen, T.-C., Li, C.-F. and Yeh, C.-H. (2012). alpha2-Adrenoceptor agonist dexmedetomidine protects septic acute kidney injury through increasing BMP-7 and inhibiting HDAC2 and HDAC5. Am. J. Physiol. Renal Physiol. 303, F1443-F1453.
17. Ishii, M., Wen, H., Corsa, C. A. S., Liu, T., Coelho, A. L., Allen, R. M., Carson, W. F., Cavassani, K. A., Li, X., Lukacs, N.W. et al. (2009). Epigenetic regulation of the alternatively activated macrophage phenotype. Blood 114, 3244-3254.
18. Iwata, K., Tomita, K., Sano, H., Fujii, Y., Yamasaki, A. and Shimizu, E. (2002). Trichostatin A, a histone deacetylase inhibitor, down-regulates interleukin-12 transcription in SV-40-transformed lung epithelial cells. Cell Immunol. 218, 26-33.
19. Iwata, A., Stevenson, V. M., Minard, A., Tasch, M., Tupper, J., Lagasse, E., Weissman, I., Harlan, J. M. and Winn, R. K. (2003). Over-expression of Bcl-2 provides protection in septic mice by a trans effect. J. Immunol. 171, 3136-3141.
20. Jacoby, J. J., Kalinowski, A., Liu, M.-G., Zhang, S. S.-M., Gao, Q., Chai, G.-X., Ji, L., Iwamoto, Y., Li, E., Schneider, M. et al. (2003). Cardiomyocyte-restricted knockout of STAT3 results in higher sensitivity to inflammation, cardiac fibrosis, and heart failure with advanced age. Proc. Natl. Acad. Sci. USA 100, 12929-12934.
21. Jenuwein, T. and Allis, C. D. (2001). Translating the histone code. Science 293, 1074-1080.
22. Kambara, K.,Ohashi,W.,Tomita, K., Takashina,M.,Fujisaka,S.,Hayashi, R.,Mori, H., Tobe, K. and Hattori, Y. (2015). In vivo depletion of CD206(+)M2macrophages exaggerates lung injury in endotoxemic mice. Am. J. Pathol. 185, 162-171.
23. Kaminskas, E., Farrell, A. T., Wang, Y.-C., Sridhara, R. and Pazdur, R. (2005). FDA drug approval summary: azacitidine (5-azacytidine, Vidaza™) for injectable suspension. Oncologist 10, 176-182.
24. Karahashi, H., Nagata, K., Ishii, K. and Amano, F. (2000). A selective inhibitor of p38 MAP kinase, SB202190, induced apoptotic cell death of a lipopolysaccharide-treated macrophage-like cell line, J774.1. Biochim. Biophys. Acta 1502, 207-223.
25. Kigerl, K. A., Gensel, J. C., Ankeny, D. P., Alexander, J. K., Donnelly, D. J. and Popovich, P. G. (2009). Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 29, 13435-13444.
26. Kochanek, A. R., Fukudome, E. Y., Li, Y., Smith, E. J., Liu, B., Velmahos, G. C., deMoya, M., King, D. and Alam, H. B. (2012). Histone deacetylase inhibitor treatment attenuates MAP kinase pathway activation and pulmonary inflammation following hemorrhagic shock in a rodent model. J. Surg. Res. 176, 185-194.
27. Krishnamurthy, P., Rajasingh, J., Lambers, E., Qin, G., Losordo, D. W. and Kishore, R. (2009). IL-10 inhibits inflammation and attenuates left ventricular remodeling after myocardial infarction via activation of STAT3 and suppression of HuR. Circ. Res. 104, e9-e18.
28. Lin, T., Chen, H., Koustova, E., Sailhamer, E. A., Li, Y., Shults, C., Liu, B., Rhee, P., Kirkpatrick, J. and Alam, H. B. (2007). Histone deacetylase as therapeutic target in a rodent model of hemorrhagic shock: effect of different resuscitation strategies on lung and liver. Surgery 141, 784-794.
29. Lin, K. L., Suzuki, Y., Nakano, H., Ramsburg, E. and Gunn, M. D. (2008). CCR2+ monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J. Immunol. 180, 2562-2572.
30. Neininger, A., Kontoyiannis, D., Kotlyarov, A.,Winzen, R., Eckert, R., Volk, H.-D., Holtmann, H., Kollias, G. and Gaestel, M. (2002). MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factorand interleukin-6 independently at different post-transcriptional levels. J. Biol. Chem. 277, 3065-3068.
31. Nemeth, K., Mayer, B. and Mezey, E. (2010). Modulation of bone marrow stromal cell functions in infectious diseases by toll-like receptor ligands. J. Mol. Med. 88, 5-10.
32. Nicodeme, E., Jeffrey, K. L., Schaefer, U., Beinke, S., Dewell, S., Chung, C.-W., Chandwani, R., Marazzi, I., Wilson, P., Coste, H. et al. (2010). Suppression of inflammation by a synthetic histone mimic. Nature 468, 1119-1123.
33. O'Dea, K. P., Wilson, M. R., Dokpesi, J. O., Wakabayashi, K., Tatton, L., van Rooijen, N. and Takata, M. (2009). Mobilization and margination of bone marrow Gr-1high monocytes during subclinical endotoxemia predisposes the lungs toward acute injury. J. Immunol. 182, 1155-1166.
34. Pal, D., Dasgupta, S., Kundu, R., Maitra, S., Das, G., Mukhopadhyay, S., Ray, S., Majumdar, S. S. and Bhattacharya, S. (2012). Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat. Med. 18, 1279-1285.
35. Rahman, I. (2002). Oxidative stress, transcription factors and chromatin remodelling in lung inflammation. Biochem. Pharmacol. 64, 935-942.
36. Rajasingh, J., Bord, E., Luedemann, C., Asai, J., Hamada, H., Thorne, T., Qin, G., Goukassian, D., Zhu, Y., Losordo, D. W. et al. (2006). IL-10-induced TNF-alpha mRNA destabilization is mediated via IL-10 suppression of p38 MAP kinase activation and inhibition of HuR expression. FASEB J. 20, 2112-2114.
37. Rajasingh, J., Lambers, E., Hamada, H., Bord, E., Thorne, T., Goukassian, I., Krishnamurthy, P., Rosen, K. M., Ahluwalia, D., Zhu, Y. et al. (2008). Cell-free embryonic stem cell extract-mediated derivation of multipotent stem cells from NIH3T3 fibroblasts for functional and anatomical ischemic tissue repair. Circ. Res. 102, e107-e117.
38. Rajasingh, J., Thangavel, J., Siddiqui, M. R., Gomes, I., Gao, X.-P., Kishore, R. and Malik, A. B. (2011). Improvement of cardiac function in mouse myocardial infarction after transplantation of epigenetically-modified bone marrow progenitor cells. PLoS ONE 6, e22550.
39. Sander, L. E., Sackett, S. D., Dierssen, U., Beraza, N., Linke, R. P., Muller, M., Blander, J. M., Tacke, F. and Trautwein, C. (2010). Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J. Exp. Med. 207, 1453-1464.
40. Sassi, F. d. A., Caesar, L., Jaeger, M., Nör, C., Abujamra, A. L., Schwartsmann,G., de Farias, C. B., Brunetto, A. L., Lopez, P. L. d. C. and Roesler, R. (2014). Inhibitory activities of trichostatin A in U87 glioblastoma cells and tumorsphere-derived cells. J. Mol. Neurosci. 54, 27-40.
41. Schneider, C., Nobs, S. P., Kurrer, M., Rehrauer, H., Thiele, C. and Kopf, M. (2014). Induction of the nuclear receptor PPAR-gamma by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat. Immunol. 15, 1026-1037.
42. Song, Y., Ao, L., Raeburn, C. D., Calkins, C. M., Abraham, E., Harken, A. H. and Meng, X. (2001). A low level of TNF-alpha mediates hemorrhage-induced acute lung injury via p55 TNF receptor. Am. J. Physiol. Lung Cell Mol. Physiol. 281, L677-L684.
43. Suzuki, T. and Miyata, N. (2005). Non-hydroxamate histone deacetylase inhibitors. Curr. Med. Chem. 12, 2867-2880.
44. Takeda, K., Kaisho, T. and Akira, S. (2003). Toll-like receptors. Annu. Rev. Immunol. 21, 335-376.
45. Thangavel, J., Malik, A. B., Elias, H. K., Rajasingh, S., Simpson, A. D., Sundivakkam, P. K., Vogel, S. M., Xuan, Y.-T., Dawn, B. and Rajasingh, J. (2014). Combinatorial therapy with acetylation and methylation modifiers attenuates lung vascular hyperpermeability in endotoxemia-induced mouse inflammatory lung injury. Am. J. Pathol. 184, 2237-2249.
46. Trojer, P. and Reinberg, D. (2006). Histone lysine demethylases and their impact on epigenetics. Cell 125, 213-217.
47. Wang, Y. Y.,Myhre,A.E., Pettersen, S. J.,Dahle,M. K., Foster, S. J., Thiemermann, C., Bjornland, K., Aasen, A. O. and Wang, J. E. (2005). Peptidoglycan of Staphylococcus aureus induces enhanced levels of matrix metalloproteinase-9 in human blood originating from neutrophils. Shock 24, 214-218.
48. Wang, Y.-L.,Malik,A.B., Sun,Y.,Hu, S.,Reynolds, A. B.,Minshall, R. D. andHu, G. (2011). Innate immune function of the adherens junction protein p120-catenin in endothelial response to endotoxin. J. Immunol. 186, 3180-3187.
49. Wheeler, A. P. and Bernard, G. R. (2007). Acute lung injury and the acute respiratory distress syndrome: a clinical review. Lancet 369, 1553-1564.
50. Winzen,R.,Kracht,M., Ritter,B.,Wilhelm, A.,Chen,C.-Y.A.,Shyu,A.-B.,Muller,M., Gaestel, M., Resch, K. and Holtmann, H. (1999). The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18, 4969-4980.
51. Wynn, T. A. (2004). Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat. Rev. Immunol. 4, 583-594.
52. Zhang, L., Jin, S., Wang, C., Jiang, R. and Wan, J. (2010). Histone deacetylase inhibitors attenuate acute lung injury during cecal ligation and puncture-induced polymicrobial sepsis. World J. Surg. 34, 1676-1683.