Staphylococcal enterotoxin B-induced MicroRNA-155 targets SOCS1 to promote acute inflammatory lung injury

Infection and Immunity

Volumn 82, Issue 7, 2014, Pages 2971-2979

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

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

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; MICRORNA; MICRORNA 155; STAPHYLOCOCCUS ENTEROTOXIN B; SUPPRESSOR OF CYTOKINE SIGNALING 1;

ACUTE INFLAMMATORY LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; HISTOPATHOLOGY; INFLAMMATION; LUNG INFILTRATE; LUNG INJURY; LUNG LAVAGE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION;

ACUTE LUNG INJURY; ANIMALS; ENTEROTOXINS; FEMALE; GENE EXPRESSION REGULATION; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84903167027     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01666-14     Document Type: Article

References (45)

1. Pinchuk IV, Beswick EJ, Reyes VE. 2010. Staphylococcal enterotoxins. Toxins 2:2177-2197. http://dx.doi.org/10.3390/toxins2082177.
2. Savransky V, Rostapshov V, Pinelis D, Polotsky Y, Korolev S, Komisar J, Fegeding K. 2003. Murine lethal toxic shock caused by intranasal administration of staphylococcal enterotoxin B. Toxicol. Pathol. 31:373-378. http://dx.doi.org/10.1080/01926230309725.
3. Ulrich RG, Sidell S, Taylor TJ, Wilhelmsen CL, Franz DR. 2001. Textbook of military medicine: medical aspects of chemical and biological warfare. Office of The Surgeon General at TMM Publications, Borden Institute, Walter Reed Army Medical Center, Washington, DC.
4. Saeed AI, Rieder SA, Price RL, Barker J, Nagarkatti P, 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. http://dx.doi.org/10.1017/S1431927612000190.
5. Neumann B, Engelhardt B, Wagner H, Holzmann B. 1997. Induction of acute inflammatory lung injury by staphylococcal enterotoxin B. J. Immunol. 158:1862-1871.
6. Bavari S, Ulrich RG. 1995. Staphylococcal enterotoxin A and toxic shock syndrome toxin compete with CD4 for human major histocompatibility complex class II binding. Infect. Immun. 63:423-429.
7. Kozono H, Parker D, White J, Marrack P, Kappler J. 1995. Multiple binding sites for bacterial superantigens on soluble class II MHC molecules. Immunity 3:187-196. http://dx.doi.org/10.1016/1074-7613(95) 90088-8.
8. Miethke T, Duschek K, Wahl C, Heeg K, Wagner H. 1993. Pathogenesis of the toxic shock syndrome: T cell mediated lethal shock caused by the superantigen TSST-1. Eur. J. Immunol. 23:1494-1500. http://dx.doi.org/10.1002/eji.1830230715.
9. Bette M, Schafer MK, van Rooijen N, Weihe E, Fleischer B. 1993. Distribution and kinetics of superantigen-induced cytokine gene expression in mouse spleen. J. Exp. Med. 178:1531-1539. http://dx.doi.org/10.1084/jem.178.5.1531.
10. Tilahun AY, Holz M, Wu TT, David CS, Rajagopalan G. 2011. Interferon gamma-dependent intestinal pathology contributes to the lethality in bacterial superantigen-induced toxic shock syndrome. PLoS One 6:e16764. http://dx.doi.org/10.1371/journal.pone.0016764.
11. Florquin S, Amraoui Z, Goldman M. 1995. T cells made deficient in interleukin-2 production by exposure to staphylococcal enterotoxin B in vivo are primed for interferon-gamma and interleukin-10 secretion. Eur. J. Immunol. 25:1148-1153. http://dx.doi.org/10.1002/eji.1830250503.
12. Fleischer B, Gerardy-Schahn R, Metzroth B, Carrel S, Gerlach D, Kohler W. 1991. An evolutionary conserved mechanism of T cell activation by microbial toxins. Evidence for different affinities of T cell receptortoxin interaction. J. Immunol. 146:11-17.
13. Herman A, Kappler JW, Marrack P, Pullen AM. 1991. Superantigens: mechanism of T-cell stimulation and role in immune responses. Annu. Rev. Immunol. 9:745-772. http://dx.doi.org/10.1146/annurev.immunol.9.1.745.
14. Saeed AI, Rieder SA, Price RL, Barker J, Nagarkatti P, Nagarkatti M. 2012. AcutelunginjuryinducedbystaphylococcalenterotoxinB:disruptionofterminal vessels as amechanismof induction of vascular leak. Microsc. Microanal. 18:445-452. http://dx.doi.org/10.1017/S1431927612000190.
15. Cai Y, Yu X, Hu S, Yu J. 2009. A brief review on the mechanisms of miRNA regulation. Genomics Proteomics Bioinformatics 7:147-154. http://dx.doi.org/10.1016/S1672-0229(08)60044-3.
16. O'Connell RM, Rao DS, Baltimore D. 2012. microRNA regulation of inflammatory responses. Annu. Rev. Immunol. 30:295-312. http://dx.doi.org/10.1146/annurev-immunol-020711-075013.
17. Rossi RL, Rossetti G, Wenandy L, Curti S, Ripamonti A, Bonnal RJ, Birolo RS, Moro M, Crosti MC, Gruarin P, Maglie S, Marabita F, Mascheroni D, Parente V, Comelli M, Trabucchi E, De Francesco R, Geginat J, Abrignani S, Pagani M. 2011. Distinct microRNA signatures in human lymphocyte subsets and enforcement of the naive state in CD4+ T cells by the microRNA miR-125b. Nat. Immunol. 12:796-803. http://dx.doi.org/10.1038/ni.2057.
18. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J, Henderson JM, Kutok JL, Rajewsky K. 2008. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat. Immunol. 9:405-414. http://dx.doi.org/10.1038/ni1575.
19. O'Connell RM, Kahn D, Gibson WS, Round JL, Scholz RL, Chaudhuri AA, Kahn ME, Rao DS, Baltimore D. 2010. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33:607-619. http://dx.doi.org/10.1016/j.immuni.2010.09.009.
20. Committee for the Update of the Guide for the Care and Use of Laboratory Animals. 2011. Guide for the care and use of laboratory animals, 8th ed. The National Academies Press, Washington, DC.
21. Rieder SA, Nagarkatti P, Nagarkatti M. 2012. Multiple antiinflammatory pathways triggered by resveratrol lead to amelioration of staphylococcal enterotoxin B-induced lung injury. Br. J. Pharmacol. 167: 1244-1258. http://dx.doi.org/10.1111/j.1476-5381.2012.02063.x.
22. Rieder SA, Nagarkatti P, Nagarkatti M. 2011. CD1d-independent activation of invariant natural killer T cells by staphylococcal enterotoxin B through major histocompatibility complex class II/T cell receptor interaction results in acute lung injury. Infect. Immun. 79:3141-3148. http://dx.doi.org/10.1128/IAI.00177-11.
23. Wheeler AP, Bernard GR. 2007. Acute lung injury and the acute respiratory distress syndrome: a clinical review. Lancet 369:1553-1564. http://dx.doi.org/10.1016/S0140-6736(07)60604-7.
24. Miyata A, Natsuaki M, Yamanishi K. 2008. Staphylococcal enterotoxin B enhances a flare-up reaction of murine contact hypersensitivity through up-regulation of interferon-gamma. Exp. Dermatol. 17:843-848. http://dx.doi.org/10.1111/j.1600-0625.2008.00714.x.
25. Plaza R, Rodriguez-Sanchez JL, Juarez C. 2007. Staphylococcal enterotoxin B in vivo modulates both gamma interferon receptor expression and ligand-induced activation of signal transducer and activator of transcription 1 in T cells. Infect. Immun. 75:306-313. http://dx.doi.org/10.1128/IAI.01220-06.
26. Sonkoly E, Pivarcsi A. 2009. microRNAs in inflammation. Int. Rev. Immunol. 28:535-561. http://dx.doi.org/10.3109/08830180903208303.
27. Lindsay MA. 2008. microRNAs and the immune response. Trends Immunol. 29:343-351. http://dx.doi.org/10.1016/j.it.2008.04.004.
28. Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, Murphy A, Frendewey D, Valenzuela D, Kutok JL, Schmidt-Supprian M, Rajewsky N, Yancopoulos G, Rao A, Rajewsky K. 2007. Regulation of the germinal center response by microRNA-155. Science 316:604-608. http://dx.doi.org/10.1126/science.1141229.
29. Stahl HF, Fauti T, Ullrich N, Bopp T, Kubach J, Rust W, Labhart P, Alexiadis V, Becker C, Hafner M, Weith A, Lenter MC, Jonuleit H, Schmitt E, Mennerich D. 2009. miR-155 inhibition sensitizes CD4+ Th cells for TREG mediated suppression. PLoS One 4:e7158. http://dx.doi.org/10.1371/journal.pone.0007158.
30. Murugaiyan G, Beynon V, Mittal A, Joller N, Weiner HL. 2011. Silencing microRNA-155 ameliorates experimental autoimmune encephalomyelitis. J. Immunol. 187:2213-2221. http://dx.doi.org/10.4049/jimmunol.1003952.
31. Oertli M, Engler DB, Kohler E, Koch M, Meyer TF, Muller A. 2011. MicroRNA-155 is essential for the T cell-mediated control of Helicobacter pylori infection and for the induction of chronic gastritis and colitis. J. Immunol. 187:3578-3586. http://dx.doi.org/10.4049/jimmunol.1101772.
32. Muhie S, Hammamieh R, Cummings C, Yang D, Jett M. 2013. Transcriptome characterization of immune suppression from battlefield-like stress. Genes Immun. 14:19-34. http://dx.doi.org/10.1038/gene.2012.49.
33. Schoenborn JR, Wilson CB. 2007. Regulation of interferon-gamma during innate and adaptive immune responses. Adv. Immunol. 96:41-101. http://dx.doi.org/10.1016/S0065-2776(07)96002-2.
34. Krakauer T. 2013. Update on staphylococcal superantigen-induced signaling pathways and therapeutic interventions. Toxins 5:1629-1654. http://dx.doi.org/10.3390/toxins5091629.
35. Lee CL, Lee SH, Jay FT, Rozee KR. 1990. Immunobiological study of interferon-gamma-producing cells after staphylococcal enterotoxin B stimulation. Immunology 70:94-99.
36. Assenmacher M, Lohning M, Scheffold A, Manz RA, Schmitz J, Radbruch A. 1998. Sequential production of IL-2, IFN-gamma and IL-10 by individual staphylococcal enterotoxin B-activated T helper lymphocytes. Eur. J. Immunol. 28:1534-1543. http://dx.doi.org/10.1002/(SICI)1521-4141(199805)28:05<1534::AID-IMMU1534>3.0.CO;2-R.
37. Huang W, Koller LD. 1998. Superantigen activation and kinetics of cytokines in the Long-Evans rat. Immunology 95:331-338. http://dx.doi.org/10.1046/j.1365-2567.1998.00613.x.
38. Trotta R, Chen L, Ciarlariello D, Josyula S, Mao C, Costinean S, Yu L, Butchar JP, Tridandapani S, Croce CM, Caligiuri MA. 2012. miR-155 regulates IFN-gamma production in natural killer cells. Blood 119:3478-3485. http://dx.doi.org/10.1182/blood-2011-12-398099.
39. Kurowska-Stolarska M, Alivernini S, Ballantine LE, Asquith DL, Millar NL, Gilchrist DS, Reilly J, Ierna M, Fraser AR, Stolarski B, McSharry C, Hueber AJ, Baxter D, Hunter J, Gay S, Liew FY, McInnes IB. 2011. MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc. Natl. Acad. Sci. U. S. A. 108:11193-11198. http://dx.doi.org/10.1073/pnas.1019536108.
40. Krebs DL, Hilton DJ. 2001. SOCS proteins: negative regulators of cytokine signaling. Stem Cells 19:378-387. http://dx.doi.org/10.1634/stemcells.19-5-378.
41. Tamiya T, Kashiwagi I, Takahashi R, Yasukawa H, Yoshimura A. 2011. Suppressors of cytokine signaling (SOCS) proteins and JAK/STAT pathways: regulation of T-cell inflammation by SOCS1 and SOCS3. Arterioscler. Thromb. Vasc. Biol. 31:980-985. http://dx.doi.org/10.1161/ATVBAHA.110.207464.
42. Cardoso AL, Guedes JR, Pereira de Almeida L, Pedroso de Lima MC. 2012. miR-155 modulates microglia-mediated immune response by down-regulating SOCS-1 and promoting cytokine and nitric oxide production. Immunology 135:73-88. http://dx.doi.org/10.1111/j.1365-2567.2011.03514.x.
43. Zhang M, Zhang Q, Liu F, Yin L, Yu B, Wu J. 2011. MicroRNA-155 may affect allograft survival by regulating the expression of suppressor of cytokine signaling 1. Med. Hypotheses 77:682-684. http://dx.doi.org/10.1016/j.mehy.2011.07.016.
44. Jiang S, Zhang HW, Lu MH, He XH, Li Y, Gu H, Liu MF, Wang ED. 2010. MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res. 70:3119-3127. http://dx.doi.org/10.1158/0008-5472.CAN-09-4250.
45. Wang P, Hou J, Lin L, Wang C, Liu X, Li D, Ma F, Wang Z, Cao X. 2010. Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J. Immunol. 185:6226-6233. http://dx.doi.org/10.4049/jimmunol.1000491.