Stat3 and C/EBPβ synergize to induce miR-21 and miR-181b expression during sepsis

Immunology and Cell Biology

Volumn 95, Issue 1, 2017, Pages 42-55

  McClure, Clara ^a   McPeak, Melissa B ^a   Youssef, Dima ^a   Yao, Zhi Q ^a   McCall, Charles E ^b   El Gazzar, Mohamed ^a  

^a East Tennessee State University   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; CD11B ANTIGEN; CD31 ANTIGEN; INTERLEUKIN 6; MICRORNA; MICRORNA 181B; MICRORNA 21; RETINOBLASTOMA PROTEIN; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG; LEUKOCYTE ANTIGEN; MIRN181 MICRORNA, MOUSE; MIRN21 MICRORNA, MOUSE; PROTEIN BINDING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; GENETIC TRANSFECTION; IN VIVO STUDY; MACROPHAGE; MALE; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; REPORTER GENE; SEPSIS; SUPPRESSOR CELL; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; BAGG ALBINO MOUSE; BINDING SITE; BIOLOGICAL MODEL; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MYELOID-DERIVED SUPPRESSOR CELL; PHOSPHORYLATION;

ANIMALS; ANTIGENS, CD; BINDING SITES; CCAAT-ENHANCER-BINDING PROTEIN-BETA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENES, REPORTER; MALE; MICE, INBRED BALB C; MICRORNAS; MODELS, BIOLOGICAL; MYELOID-DERIVED SUPPRESSOR CELLS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RETINOBLASTOMA PROTEIN; SEPSIS; STAT3 TRANSCRIPTION FACTOR;

EID: 84981263365     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2016.63     Document Type: Article

References (60)

1. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9: 162-174.
2. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009; 182: 4499-4506.
3. Bronte V. Myeloid-derived suppressor cells in inflammation: uncovering cell subsets with enhanced immunosuppressive functions. Eur J Immunol 2009; 39: 2670-2672.
4. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181: 5791-5802.
5. Condamine T, Gabrilovich DI. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol 2011; 32: 19-25.
6. Trikha P, Carson, III WE. Signaling pathways involved in MDSC regulation. Biochim Biophys Acta 2014; 1846: 55-65.
7. Vuk-Pavlovic S, Bulur PA, Lin Y, Qin R, Szumlanski CL, Zhao X et al. Immunosuppressive CD14+HLA-DRlow/-monocytes in prostate cancer. Prostate 2010; 70: 443-455.
8. Brudecki L, Ferguson DA, McCall CE, El Gazzar M. Myeloid-derived suppressor cells evolve during sepsis and can enhance or attenuate the systemic inflammatory response. Infect Immun 2012; 80: 2026-2034.
9. Cuenca AG, Delano MJ, Kelly-Scumpia KM, Moreno C, Scumpia PO, Laface DM et al. A paradoxical role for myeloid-derived suppressor cells in sepsis and trauma. Mol Med 2011; 17: 281-292.
10. Kong YY, Fuchsberger M, Xiang SD, Apostolopoulos V, Plebanski M. Myeloid derived suppressor cells and their role in diseases. Curr Med Chem 2013; 20: 1437-1444.
11. Delano MJ, Scumpia PO, Weinstein JS, Coco D, Nagaraj S, Kelly-Scumpia KM et al. MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J Exp Med 2007; 204: 1463-1474.
12. Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, Beschin A et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008; 111: 4233-4244.
13. Kusmartsev S, Gabrilovich DI. Inhibition of myeloid cell differentiation in cancer: the role of reactive oxygen species. J Leukoc Biol 2003; 74: 186-196.
14. Saleem SJ, Conrad DH. Hematopoietic cytokine-induced transcriptional regulation and Notch signaling as modulators of MDSC expansion. Int Immunopharmacol 2011; 11: 808-815.
15. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 2010; 10: 111-122.
16. Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993; 75: 855-862.
17. Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 2008; 9: 219-230.
18. Williams AE. Functional aspects of animal microRNAs. Cell Mol Life Sci 2008; 65: 545-562.
19. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9: 102-114.
20. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11: 228-234.
21. Ballarino M, Pagano F, Girardi E, Morlando M, Cacchiarelli D, Marchioni M et al. Coupled RNA processing and transcription of intergenic primary microRNAs. Mol Cell Biol 2009; 29: 5632-5638.
22. Chekulaeva M, Filipowicz W. Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr Opin Cell Biol 2009; 21: 452-460.
23. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-233.
24. Bushati N, Cohen SM. microRNA functions. Annu Rev Cell Dev Biol 2007; 23: 175-205.
25. Tsitsiou E, Lindsay MA. microRNAs and the immune response. Curr Opin Pharmacol 2009; 9: 514-520.
26. McClure C, Brudecki L, Ferguson DA, Yao ZQ, Moorman JP, McCall CE et al. MicroRNA
27. (miR-21) and miR-181b couple with NFI-A to generate myeloid-derived suppressor cells and promote immunosuppression in late sepsis. Infect Immun 2014; 82: 3816-3825.
28. Hirai H, Zhang P, Dayaram T, Hetherington CJ, Mizuno S, Imanishi J et al. C/EBPbeta is required for 'emergency' granulopoiesis. Nat Immunol 2006; 7: 732-739.
29. Zhang H, Nguyen-Jackson H, Panopoulos AD, Li HS, Murray PJ, Watowich SS. STAT3 controls myeloid progenitor growth during emergency granulopoiesis. Blood 2010; 116: 2462-2471.
30. Landschulz WH, Johnson PF, McKnight SL. The DNA binding domain of the rat liver nuclear protein C/EBP is bipartite. Science 1989; 243: 1681-1688.
31. Hu X, Zuckerman KS. Cell cycle and transcriptional control of human myeloid leukemic cells by transforming growth factor beta. Leuk Lymphoma 2000; 38: 235-246.
32. Kitagawa M, Higashi H, Jung HK, Suzuki-Takahashi I, Tamai K, Kato J et al. The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J 1996; 15: 7060-7069.
33. Riley DJ, Lee EY, Lee WH. The retinoblastoma protein: more than a tumor suppressor. Annu Rev Cell Biol 1994; 10: 1-29.
34. McClure C, Ali E, Youssef D, Yao ZQ, McCall CE, El Gazzar M. NFI-A disrupts myeloid cell differentiation and maturation in septic mice. J Leukoc Biol 2016; 99: 201-211.
35. Braun DA, Fribourg M, Sealfon SC. Cytokine response is determined by duration of receptor and signal transducers and activators of transcription 3 (STAT3) activation. J Biol Chem 2013; 288: 2986-2993.
36. Hutchins AP, Diez D, Miranda-Saavedra D. The IL-10/STAT3-mediated antiinflammatory response: recent developments and future challenges. Brief Funct Genomics 2013; 12: 489-498.
37. Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl K. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 2010; 39: 493-506.
38. Loffler D, Brocke-Heidrich K, Pfeifer G, Stocsits C, Hackermuller AK, Burger R et al. Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 2007; 110: 1330-1333.
39. Xin H, Zhang C, Herrmann A, Du Y, Figlin R, Yu H. Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res 2009; 69: 2506-2513.
40. Marigo I, Bosio E, Solito S, Mesa C, Fernandez A, Dolcetti L et al. Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity 2010; 32: 790-802.
41. Li P, Grgurevic S, Liu Z, Harris D, Rozorski U, Calin GA et al. Signal transducer and activator of transcription-3 induces microRNA-155 expression in chronic lymphocytic leukemia. PLoS ONE 2013; 8: e64678.
42. Gupta AK, Kone BC. CCAAT/enhancer binding protein-beta trans-activates murine nitric oxide synthase 2 gene in an MTAL cell line. Am J Physiol 1999; 276: F599-F605.
43. Pauleau AL, Rutschman R, Lang R, Pernis A, Watowich SS, Murray PJ. Enhancermediated control of macrophage-specific arginase I expression. J Immunol 2004; 172: 7565-7573.
44. Chen PL, Riley DJ, Chen-Kiang S, Lee WH. Retinoblastoma protein directly interacts with and activates the transcription factor NF-IL6. Proc Natl Acad Sci USA 1996; 93: 465-469.
45. Nevins JR. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 1992; 258: 424-429.
46. Chau BN, Wang JY. Coordinated regulation of life and death by RB. Nat Rev Cancer 2003; 3: 130-138.
47. Chen HZ, Tsai SY, Leone G. Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat Rev Cancer 2009; 9: 785-797.
48. Dotto GP. p21(WAF1/Cip1): more than a break to the cell cycle? Biochim Biophys Acta 2000; 1471: M43-M56.
49. Starostina NG, Kipreos ET. Multiple degradation pathways regulate versatile CIP/KIP CDK inhibitors. Trends Cell Biol 2012; 22: 33-41.
50. Hotchkiss RS, Monneret G, Payen D. Sepsis-induced immunosuppression: from cellular dysfunctions to immunotherapy. Nat Rev Immunol 2013; 13: 862-874.
51. Muenzer JT, Davis CG, Chang K, Schmidt RE, Dunne WM, Coopersmith CM et al. Characterization and modulation of the immunosuppressive phase of sepsis. Infect Immun 2010; 78: 1582-1592.
52. Hotchkiss RS, Monneret G, Payen D. Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect Dis 2013; 13: 260-268.
53. McCall CE, El Gazzar M, Liu T, Vachharajani V, Yoza B. Epigenetics, bioenergetics, and microRNA coordinate gene-specific reprogramming during acute systemic inflammation. J Leukoc Biol 2011; 90: 439-446.
54. Shubin NJ, Monaghan SF, Ayala A. Anti-inflammatory mechanisms of sepsis. Contrib Microbiol 2011; 17: 108-124.
55. Sheedy FJ. Turning 21: Induction of miR-21 as a Key Switch in the Inflammatory Response. Front Immunol 2015; 6: 19-28.
56. Belikoff B, Hatfield S, Sitkovsky M, Remick DG. Adenosine negative feedback on A2A adenosine receptors mediates hyporesponsiveness in chronically septic mice. Shock 2011; 35: 382-387.
57. Osuchowski MF, Welch K, Siddiqui J, Remick DG. Circulating cytokine/inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality. J Immunol 2006; 177: 1967-1974.
58. Brudecki L, Ferguson DA, Yin D, Lesage GD, McCall CE, El Gazzar M. Hematopoietic stem-progenitor cells restore immunoreactivity and improve survival in late sepsis. Infect Immun 2012; 80: 602-611.
59. Mazuski JE, Sawyer RG, Nathens AB, DiPiro JT, Schein M, Kudsk KA et al. The Surgical Infection Society guidelines on antimicrobial therapy for intra-abdominal infections: an executive summary. Surg Infect (Larchmt) 2002; 3: 161-173.
60. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E et al. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 2005; 309: 1573-1576.