Role of miRNA in the regulation of inflammatory genes in staphylococcal enterotoxin B-Induced acute inflammatory lung injury and mortality

Toxicological Sciences

Volumn 144, Issue 2, 2015, Pages 284-297

  Rao, Roshni ^a   Nagarkatti, Prakash ^a   Nagarkatti, Mitzi ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

ALI; Inflammation; microRNA; Mortality; SEB

Indexed keywords

CHEMOKINE; CYCLIN D; CYCLIN D1; CYCLIN E; CYCLIN E1; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LET 7E; MESSENGER RNA; MICRORNA; MICRORNA 132; MICRORNA 155; MICRORNA 192; MICRORNA 193; MICRORNA 20B; MICRORNA 222; MICRORNA 31; MICRORNA 34A; PROSTAGLANDIN SYNTHASE; PROSTAGLANDIN SYNTHASE 2; SMAD3 PROTEIN; SMALL UNTRANSLATED RNA; STAPHYLOCOCCUS ENTEROTOXIN B; STAT3 PROTEIN; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ENTEROTOXIN; ENTEROTOXIN B, STAPHYLOCOCCAL;

3' UNTRANSLATED REGION; ACUTE INFLAMMATORY LUNG INJURY; ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLOGICAL FUNCTIONS; CELL CYCLE PROGRESSION; CELL DEATH; CELL INFILTRATION; CELL PROLIFERATION; CELL SURVIVAL; COMPUTER MODEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LUNG FUNCTION; LUNG INFILTRATE; MONONUCLEAR CELL; MORTALITY; MOUSE; NONHUMAN; PNEUMONIA; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; C3H MOUSE; CHEMICALLY INDUCED; GENETICS; IMMUNOLOGY; PHYSIOLOGY; VALIDATION STUDY;

MUS;

ACUTE LUNG INJURY; ANIMALS; CELL PROLIFERATION; ENTEROTOXINS; FEMALE; INFLAMMATION; MICE; MICE, INBRED C3H; MICRORNAS;

EID: 84926452707     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu315     Document Type: Article

References (51)

1. Bala, S., Marcos, M., Kodys, K., Csak, T., Catalano, D., Mandrekar, P., and Szabo, G. (2011). Up-regulation of microRNA-155 in macrophages contributes to increased tumor necrosis factor a (TNFa) production via increased mRNA half-life in alcoholic liver disease. J. Biol. Chem. 286, 1436-1444.
2. Baltimore,D., Boldin,M. P., O'Connell, R. M.,Rao,D. S., andTaganov, K. D. (2008).MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9, 839-845.
3. Busbee, P. B., Nagarkatti, M., and Nagarkatti, P. S. (2014). Natural indoles, indole-3-carbinol and 3,30-diindolymethane, inhibit T cell activation by staphylococcal enterotoxin B through epigenetic regulation involving HDAC expression. Toxicol. Appl. Pharmacol. 274, 7-16.
4. Calin, G. A., Dumitru, C. D., Shimizu, M., Bichi, R., Zupo, S., Noch, E., Aldler, H., Rattan, S., Keating, M., Rai, K., et al. (2002). Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. U.S.A. 99, 15524-15529.
5. Chen, J., Feilotter, H. E., Pare, G. C., Zhang, X., Pemberton, J. G., Garady, C., Lai, D., Yang, X., and Tron, V. A. (2010). MicroRNA-193b represses cell proliferation and regulates cyclin D1 in melanoma. Am. J. Pathol. 176, 2520-2529.
6. Dai, R., and Ahmed, S. A. (2011). MicroRNA, a new paradigm for understanding immunoregulation, inflammation, and autoimmune diseases. Transl. Res. 157, 163-179.
7. Davidson-Moncada, J., Papavasiliou, F. N., and Tam, W. (2010). MicroRNAs of the immune system: roles in inflammation and cancer. Ann. N. Y. Acad. Sci. 1183, 183-194.
8. Delisle, J. S., Giroux, M., Boucher, G., Landry, J. R., Hardy, M. P., Lemieux, S., Jones, R. G., Wilhelm, B. T., and Perreault, C. (2013). The TGF-beta-Smad3 pathway inhibits CD28-dependent cell growth and proliferation of CD4 T cells. Genes Immun. 14, 115-126.
9. Faulkner, L., Cooper, A., Fantino, C., Altmann, D. M., and Sriskandan, S. (2005). The mechanism of superantigen-mediated toxic shock: not a simple Th1 cytokine storm. J. Immunol. 175, 6870-6877.
10. Foster, T. J. (2004). The Staphylococcus aureus "superbug". J. Clin. Invest. 114, 1693-1696.
11. Green, J. M., Turka, L. A., June, C. H., and Thompson, C. B. (1992). CD28 and staphylococcal enterotoxins synergize to induce MHC-independent T-cell proliferation. Cell Immunol. 145, 11-20.
12. Hanieh, H., and Alzahrani, A. (2013). A microRNA-132 suppresses autoimmune encephalomyelitis by inducing cholinergic anti-inflammation: a new Ahr-based exploration. Eur. J. Immunol. 43, 2771-2782.
13. Hedrick, S. M., Hess Michelini, R., Doedens, A. L., Goldrath, A. W., and Stone, E. L. (2012). FOXO transcription factors throughout T cell biology. Nat. Rev. Immunol. 12, 649-661.
14. Huzella, L. M., Buckley, M. J., Alves, D. A., Stiles, B. G., and Krakauer, T. (2009). Central roles for IL-2 and MCP-1 following intranasal exposure to SEB: a new mouse model. Res. Vet. Sci. 86, 241-247.
15. Kissner, T. L., Ruthel, G., Alam, S., Ulrich, R. G., Fernandez, S., and Saikh, K. U. (2011). Activation of MyD88 signaling upon staphylococcal enterotoxin binding to MHC class II molecules. PLoS One 6, e15985.
16. Kozono, H., Parker, D., White, J., Marrack, P., and Kappler, J. (1995). Multiple binding sites for bacterial superantigens on soluble class II MHC molecules. Immunity 3, 187-196.
17. Krakauer, T. (2013). Update on staphylococcal superantigeninduced signaling pathways and therapeutic interventions. Toxins (Basel) 5, 1629-1654.
18. Krakauer, T., Buckley, M., and Fisher, D. (2010). Murine models of staphylococcal enterotoxin B-induced toxic shock. Mil. Med. 175, 917-922.
19. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20.
20. Li, J., Wan, Y., Guo, Q., Zou, L., Zhang, J., Fang, Y., Zhang, J., Zhang, J., Fu, X., Liu, H., Lu, L., and Wu, Y. (2010). Altered microRNA expression profile with miR-146a upregulation in CD4{thorn} T cells from patients with rheumatoid arthritis. Arthritis Res. Ther. 12, R81.
21. Lin, L., Hron, J. D., and Peng, S. L. (2004). Regulation of NFkappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 21, 203-213.
22. Liu, D., Zienkiewicz, J., DiGiandomenico, A., and Hawiger, J. (2009). Suppression of acute lung inflammation by intracellular peptide delivery of a nuclear import inhibitor. Mol. Ther. 17, 796-802.
23. Lowy, F. D. (1998). Staphylococcus aureus infections. N. Engl. J. Med. 339, 520-532.
24. Lungu, G., Stoica, G., and Ambrus, A. (2013). MicroRNA profiling and the role of microRNA-132 in neurodegeneration using a rat model. Neurosci. Lett. 553, 153-158.
25. Mattes, J., Collison, A., Plank, M., Phipps, S., and Foster, P. S. (2009). Antagonism of microRNA-126 suppresses the effector function of TH2 cells and the development of allergic airways disease. Proc. Natl. Acad. Sci. U.S.A. 106, 18704-18709.
26. Miethke, T., Wahl, C., Heeg, K., Echtenacher, B., Krammer, P. H., and Wagner, H. (1992). T cell-mediated lethal shock triggered in mice by the superantigen staphylococcal enterotoxin B: critical role of tumor necrosis factor. J. Exp. Med. 175, 91-98.
27. Miethke, T., Wahl, C., Regele, D., Gaus, H., Heeg, K., and Wagner, H. (1993). Superantigen mediated shock: a cytokine release syndrome. Immunobiology 189, 270-284.
28. Nakahama, T., Hanieh, H., Nguyen, N. T., Chinen, I., Ripley, B., Millrine,D., Lee, S.,Nyati,K.K., Dubey, P. K.,Chowdhury,K., et al. (2013). Aryl hydrocarbon receptor-mediated induction of the microRNA-132/212 cluster promotes interleukin-17-producing T-helper cell differentiation. Proc. Natl. Acad. Sci. U.S.A. 110, 11964-11969.
29. O'Connell, R. M., Rao, D. S., and Baltimore, D. (2012). microRNA regulation of inflammatory responses. Annu. Rev. Immunol. 30, 295-312.
30. Pauley, K. M., Satoh, M., Chan, A. L., Bubb, M. R., Reeves, W. H., and Chan, E. K. (2008). Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res. Ther. 10, R101.
31. Plaza, R., Vidal, S., Rodriguez-Sanchez, J. L., and Juarez, C. (2004). Implication of STAT1 and STAT3 transcription factors in the response to superantigens. Cytokine 25, 1-10.
32. Rajagopalan, G., Sen, M. M., Singh, M., Murali, N. S., Nath, K. A., Iijima, K., Kita, H., Leontovich, A. A., Gopinathan, U., Patel, R., and David, C. S. (2006). Intranasal exposure to staphylococcal enterotoxin B elicits an acute systemic inflammatory response. Shock 25, 647-656.
33. Rao, R., Nagarkatti, P., and Nagarkatti, M. (2014). Staphylococcal enterotoxin B (SEB)-induced microRNA-155 targets suppressor of cytokine signaling-1 (SOCS1) to promote acute inflammatory lung injury. Infect. Immun. 82, 2971-2979.
34. Rieder, S. A., Nagarkatti, P., and Nagarkatti, M. (2012). Multiple anti-inflammatory pathways triggered by resveratrol lead to amelioration of staphylococcal enterotoxin B-induced lung injury. Br. J. Pharmacol. 167, 1244-1258.
35. Rossi, R. L., Rossetti, G., Wenandy, L., Curti, S., Ripamonti, A., Bonnal, R. J., Birolo, R. S., Moro, M., Crosti, M. C., Gruarin, P., et al. (2011). Distinct microRNA signatures in human lymphocyte subsets and enforcement of the naive state in CD4{thorn} T cells by the microRNA miR-125b. Nat. Immunol. 12, 796-803.
36. Saeed, A. I., Rieder, S. A., Price, R. L., Barker, J., Nagarkatti, P., and Nagarkatti, M. (2012). Acute lung injury induced by Staphylococcal enterotoxin B: disruption of terminal vessels as a mechanism of induction of vascular leak. Microsc. Microanal. 18, 445-452.
37. Savransky, V., Rostapshov, V., Pinelis, D., Polotsky, Y., Korolev, S., Komisar, J., and Fegeding, K. (2003). Murine lethal toxic shock caused by intranasal administration of staphylococcal enterotoxin B. Toxicol. Pathol. 31, 373-378.
38. Scott, H. L., Tamagnini, F., Narduzzo, K. E., Howarth, J. L., Lee, Y. B., Wong, L. F., Brown, M. W., Warburton, E. C., Bashir, Z. I., and Uney, J. B. (2012). MicroRNA-132 regulates recognition memory and synaptic plasticity in the perirhinal cortex. Eur. J. Neurosci. 36, 2941-2948.
39. Sonkoly, E., Stahle, M., and Pivarcsi, A. (2008). MicroRNAs and immunity: novel players in the regulation of normal immune function and inflammation. Semin. Cancer Biol. 18, 131-140.
40. Strandberg, K. L., Rotschafer, J. H., Vetter, S. M., Buonpane, R. A., Kranz, D. M., and Schlievert, P. M. (2010). Staphylococcal superantigens cause lethal pulmonary disease in rabbits. J. Infect. Dis. 202, 1690-1697.
41. Sun, F., Fu, H., Liu, Q., Tie, Y., Zhu, J., Xing, R., Sun, Z., and Zheng, X. (2008). Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett. 582, 1564-1568.
42. Taganov, K. D., Boldin, M. P., Chang, K. J., and Baltimore, D. (2006). NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U.S.A. 103, 12481-12486.
43. Ten Dijke, P., Goumans, M. J., Itoh, F., and Itoh, S. (2002). Regulation of cell proliferation by Smad proteins. J. Cell Physiol. 191, 1-16.
44. Uchakina, O. N., Castillejo, C. M., Bridges, C. C., and McKallip, R. J. (2013). The role of hyaluronic acid in SEB-induced acute lung inflammation. Clin. Immunol. 146, 56-69.
45. Ulrich, R. G., Sidell, S., Taylor, T. J., Wilhelmsen, C. L., and Franz, D. R. (2001). Textbook of Military Medicine: Medical Aspects of Chemical and Biological Warfare. Office of the Surgeon General, Department of the Army, USA.
46. Wong, W. F., Kohu, K., Chiba, T., Sato, T., and Satake, M. (2012a). Interplay of transcription factors in T-cell differentiation and function: the role of Runx. Immunology 132, 157-164.
47. Wong, W. F., Kohu, K., Nakamura, A., Ebina, M., Kikuchi, T., Tazawa, R., Tanaka, K., Kon, S., Funaki, T., Sugahara-Tobinai, A., et al. (2012b). Runx1 deficiency in CD4{thorn} T cells causes fatal autoimmune inflammatory lung disease due to spontaneous hyperactivation of cells. J. Immunol. 188, 5408-5420.
48. Xiao, B., Liu, Z., Li, B. S., Tang, B., Li, W., Guo, G., Shi, Y., Wang, F., Wu, Y., Tong, W. D., et al. (2009). Induction of microRNA-155 during Helicobacter pylori infection and its negative regulatory role in the inflammatory response. J. Infect. Dis. 200, 916-925.
49. Xu, N., Meisgen, F., Butler, L. M., Han, G., Wang, X. J., Soderberg-Naucler, C., Stahle, M., Pivarcsi, A., and Sonkoly, E. (2013). MicroRNA-31 is overexpressed in psoriasis and modulates inflammatory cytokine and chemokine production in keratinocytes via targeting serine/threonine kinase 40. J. Immunol. 190, 678-688.
50. Yu, H., Pardoll, D., and Jove, R. (2009). STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 9, 798-809.
51. Zhang, X., Hu, S., Zhang, X., Wang, L., Zhang, X., Yan, B., Zhao, J., Yang, A., and Zhang, R. (2014). MicroRNA-7 arrests cell cycle in G1 phase by directly targeting CCNE1 in human hepatocellular carcinoma cells. Biochem. Biophys. Res. Commun. 443, 1078-1084.