Dysregulation in microRNA expression in peripheral blood mononuclear cells of sepsis patients is associated with immunopathology

Cytokine

Volumn 71, Issue 1, 2015, Pages 89-100

  Zhou, Juhua ^a,b   Chaudhry, Hina ^a   Zhong, Yin ^a   Ali, Mir Mustafa ^a   Perkins, Linda A ^a   Owens, William B ^a   Morales, Juan E ^a   McGuire, Franklin R ^a   Zumbrun, Elizabeth E ^a   Zhang, Jiajia ^c   Nagarkatti, Prakash S ^a   Nagarkatti, Mitzi ^a  

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

^b LUDONG UNIVERSITY   (China)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cytokine; MiR 146a; MiRNA; Monocyte; Sepsis

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; MICRORNA; MICRORNA 143; MICRORNA 145; MICRORNA 146A; MICRORNA 150; MICRORNA 155; MICRORNA 182; MONOCYTE CHEMOTACTIC PROTEIN 1; UNCLASSIFIED DRUG; CHEMOKINE; CYTOKINE; MIRN146 MICRORNA, HUMAN;

ADULT; ARTICLE; BIOINFORMATICS; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; IMMUNOREGULATION; INFLAMMATION; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; MALE; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SEPSIS; T LYMPHOCYTE; TH2 CELL; AGED; BIOLOGY; BLOOD; CELL DIFFERENTIATION; CLASSIFICATION; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; PATHOLOGY;

AGED; CELL DIFFERENTIATION; CHEMOKINES; COMPUTATIONAL BIOLOGY; CYTOKINES; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-6; LEUKOCYTES, MONONUCLEAR; MALE; METABOLIC NETWORKS AND PATHWAYS; MICRORNAS; MIDDLE AGED; MONOCYTES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEPSIS; T-LYMPHOCYTES;

EID: 84910023962     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2014.09.003     Document Type: Article

References (55)

1. Skrupky L.P., Kerby P.W., Hotchkiss R.S. Advances in the management of sepsis and the understanding of key immunologic defects. Anesthesiology 2011, 115:1349-1362.
2. Stearns-Kurosawa D.J., Osuchowski M.F., Valentine C., Kurosawa S., Remick D.G. The pathogenesis of sepsis. Annu Rev Pathol 2011, 6:19-48.
3. Mera S., Tatulescu D., Cismaru C., Bondor C., Slavcovici A., Zanc V., et al. Multiplex cytokine profiling in patients with sepsis. Apmis 2011, 119:155-163.
4. van Dissel J.T., van Langevelde P., Westendorp R.G., Kwappenberg K., Frolich M. Anti-inflammatory cytokine profile and mortality in febrile patients. Lancet 1998, 351:950-953.
5. Tsitsiou E., Lindsay M.A. MicroRNAs and the immune response. Curr Opin Pharmacol 2009, 9:514-520.
6. O'Connell R.M., Kahn D., Gibson W.S., Round J.L., Scholz R.L., Chaudhuri A.A., et al. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 2010, 33:607-619.
7. Xiao C., Rajewsky K. MicroRNA control in the immune system: basic principles. Cell 2009, 136:26-36.
8. Giza D.E., Vasilescu C. [MicroRNA's role in sepsis and endotoxin tolerance. More players on the stage]. Chirurgia (Bucur) 2010, 105:625-630.
9. Vasilescu C., Rossi S., Shimizu M., Tudor S., Veronese A., Ferracin M., et al. MicroRNA fingerprints identify miR-150 as a plasma prognostic marker in patients with sepsis. PLoS ONE 2009, 4:e7405.
10. Wang J.F., Yu M.L., Yu G., Bian J.J., Deng X.M., Wan X.J., et al. Serum miR-146a and miR-223 as potential new biomarkers for sepsis. Biochem Biophys Res Commun 2010, 394:184-188.
11. Bhaumik D., Scott G.K., Schokrpur S., Patil C.K., Orjalo A.V., Rodier F., et al. MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8. Aging (Albany NY) 2009, 1:402-411.
12. Vincent J.L., Moreno R., Takala J., Willatts S., De Mendonca A., Bruining H., et al. The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. On behalf of the Working Group on Sepsis-Related Problems of the European Society of Intensive Care Medicine. Intensive Care Med 1996, 22:707-710.
13. Hegde V.L., Tomar S., Jackson A., Rao R., Yang X., Singh U.P., et al. Distinct microRNA expression profile and targeted biological pathways in functional myeloid-derived suppressor cells induced by Delta9-tetrahydrocannabinol in vivo: regulation of CCAAT/enhancer-binding protein alpha by microRNA-690. J Biol Chem 2013, 288:36810-36826.
14. Zhou J., Nagarkatti P., Zhong Y., Nagarkatti M. Immune modulation by chondroitin sulfate and its degraded disaccharide product in the development of an experimental model of multiple sclerosis. J Neuroimmunol 2010, 223:55-64.
15. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2013. <>. http://www.R-project.org.
16. Hotchkiss R.S., Karl I.E. The pathophysiology and treatment of sepsis. New England J Med 2003, 348:138-150.
17. Dai R., Ahmed S.A. MicroRNA, a new paradigm for understanding immunoregulation, inflammation, and autoimmune diseases. Trans Res 2011, 157:163-179.
18. Wang H.J., Lo W.Y., Lin L.J. Angiotensin-(1-7) decreases glycated albumin-induced endothelial interleukin-6 expression via modulation of miR-146a. Biochem Biophys Res Commun 2013, 430:1157-1163.
19. Song Z., Yao C., Yin J., Tong C., Zhu D., Sun Z., et al. Genetic variation in the TNF receptor-associated factor 6 gene is associated with susceptibility to sepsis-induced acute lung injury. J Trans Med 2012, 10:166.
20. Bennett S., Por S.B., Stanley E.R., Breit S.N. Monocyte proliferation in a cytokine-free, serum-free system. J Immunol Methods 1992, 153:201-212.
21. Yu H., Maurer F., Medcalf R.L. Plasminogen activator inhibitor type 2: a regulator of monocyte proliferation and differentiation. Blood 2002, 99:2810-2818.
22. McDevitt T.M., Tchao R., Harrison E.H., Morel D.W. Carotenoids normally present in serum inhibit proliferation and induce differentiation of a human monocyte/macrophage cell line (U937). J Nutr 2005, 135:160-164.
23. Saito R., Smoot M.E., Ono K., Ruscheinski J., Wang P.L., Lotia S., et al. A travel guide to Cytoscape plugins. Nat Methods 2012, 9:1069-1076.
24. Hotchkiss R.S., 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.
25. Jiang L.N., Yao Y.M., Sheng Z.Y. The role of regulatory T cells in the pathogenesis of sepsis and its clinical implication. J Interferon Cytokine Res: Official J Int Soc Interferon Cytokine Res 2012, 32:341-349.
26. Wang H., Zhang P., Chen W., Feng D., Jia Y., Xie L. Serum microRNA signatures identified by Solexa sequencing predict sepsis patients' mortality: a prospective observational study. PLoS ONE 2012, 7:e38885.
27. Ma Y., Vilanova D., Atalar K., Delfour O., Edgeworth J., Ostermann M., et al. Genome-wide sequencing of cellular microRNAs identifies a combinatorial expression signature diagnostic of sepsis. PLoS ONE 2013, 8:e75918.
28. Wang L., Wang H.C., Chen C., Zeng J., Wang Q., Zheng L., et al. Differential expression of plasma miR-146a in sepsis patients compared with non-sepsis-SIRS patients. Exp Ther Med 2013, 5:1101-1104.
29. Boldin M.P., Taganov K.D., Rao D.S., Yang L., Zhao J.L., Kalwani M., et al. MiR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med 2011, 208:1189-1201.
30. He Y., Sun X., Huang C., Long X.R., Lin X., Zhang L., et al. MiR-146a regulates IL-6 production in lipopolysaccharide-induced RAW264.7 macrophage cells by inhibiting notch1. Inflammation 2013.
31. Li S., Yue Y., Xu W., Xiong S. MicroRNA-146a represses mycobacteria-induced inflammatory response and facilitates bacterial replication via targeting IRAK-1 and TRAF-6. PLoS ONE 2013, 8:e81438.
32. Zeng Z., Gong H., Li Y., Jie K., Ding C., Shao Q., et al. Upregulation of miR-146a contributes to the suppression of inflammatory responses in LPS-induced acute lung injury. Exp Lung Res 2013, 39:275-282.
33. Nahid M.A., Pauley K.M., Satoh M., Chan E.K. MiR-146a is critical for endotoxin-induced tolerance: implication in innate immunity. J Biol Chem 2009, 284:34590-34599.
34. Taganov K.D., Boldin M.P., Chang K.J., Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 2006, 103:12481-12486.
35. Ikeda T., Kumagai E., Iwata S., Yamakawa A. Soluble CD26/dipeptidyl peptidase IV enhances the transcription of IL-6 and TNF-alpha in THP-1 cells and monocytes. PLoS ONE 2013, 8:e66520.
36. Yang K., He Y.S., Wang X.Q., Lu L., Chen Q.J., Liu J., et al. MiR-146a inhibits oxidized low-density lipoprotein-induced lipid accumulation and inflammatory response via targeting toll-like receptor 4. FEBS Lett 2011, 585:854-860.
37. Quinn S.R., O'Neill L.A. A trio of microRNAs that control toll-like receptor signalling. Int Immunol 2011, 23:421-425.
38. Lu L.F., Boldin M.P., Chaudhry A., Lin L.L., Taganov K.D., Hanada T., et al. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 2010, 142:914-929.
39. Chen T., Li Z., Jing T., Zhu W., Ge J., Zheng X., et al. MicroRNA-146a regulates the maturation process and pro-inflammatory cytokine secretion by targeting CD40L in oxLDL-stimulated dendritic cells. FEBS Lett 2011, 585:567-573.
40. Roderburg C., Luedde M., Vargas Cardenas D., Vucur M., Scholten D., Frey N., et al. Circulating microRNA-150 serum levels predict survival in patients with critical illness and sepsis. PLoS ONE 2013, 8:e54612.
41. Stanley E.R., Berg K.L., Einstein D.B., Lee P.S., Pixley F.J., Wang Y., et al. Biology and action of colony-stimulating factor-1. Mol Reprod Dev 1997, 46:4-10.
42. Rouas R., Fayyad-Kazan H., El Zein N., Lewalle P., Rothe F., Simion A., et al. Human natural Treg microRNA signature: role of microRNA-31 and microRNA-21 in FOXP3 expression. Eur J Immunol 2009, 39:1608-1618.
43. Liu J., Zhang Z., Bando M., Itoh T., Deardorff M.A., Clark D., et al. Transcriptional dysregulation in NIPBL and cohesin mutant human cells. PLoS Biol 2009, 7:e1000119.
44. Garrett-Sinha L.A. Review of Ets1 structure, function, and roles in immunity. Cell Mol Life Sci: CMLS 2013, 70:3375-3390.
45. Terme M., Pernot S., Marcheteau E., Sandoval F., Benhamouda N., Colussi O., et al. VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res 2013, 73:539-549.
46. Luo C.T., Li M.O. Transcriptional control of regulatory T cell development and function. Trends Immunol 2013.
47. Ji F., Chen R., Liu B., Zhang X., Han J., Wang H., et al. BAFF induces spleen CD4+ T cell proliferation by down-regulating phosphorylation of FOXO3A and activates cyclin D2 and D3 expression. Biochem Biophys Res Commun 2012, 425:854-858.
48. Salomone T., Tosi P., Di Battista N., Binetti N., Raiti C., Tomassetti P., et al. Impaired alveolar gas exchange in acute pancreatitis. Dig Dis Sci 2002, 47:2025-2028.
49. Lim E.M., Cembrowski G., Cembrowski M., Clarke G. Race-specific WBC and neutrophil count reference intervals. Int J Lab Hematol 2010, 32:590-597.
50. Horn P.L., Pyne D.B., Hopkins W.G., Barnes C.J. Lower white blood cell counts in elite athletes training for highly aerobic sports. Eur J Appl Phys 2010, 110:925-932.
51. Ardron M.J., Westengard J.C., Dutcher T.F. Band neutrophil counts are unnecessary for the diagnosis of infection in patients with normal total leukocyte counts. Am J Clin Pathol 1994, 102:646-649.
52. Dragomirescu T., Siara C., Ghitescu M., Antonescu M., Baglagian M., Flavian L., et al. [Normal values of the neutrophil granulocyte adhesion test in the peripheral blood of adults]. Rev Ig Bacteriol Virusol Parazitol Epidemiol Pneumoftiziol Bacteriol Virusol Parazitol Epidemiol 1978, 23:221-230.
53. Ferrarini M., Ferrero E., Fortis C., Poggi A., Zocchi M.R. LAK1 antigen defines two distinct subsets among human tumour infiltrating lymphocytes. Br J Cancer 1990, 62:754-757.
54. Sato H., Shiobara S., Yasue S., Chuhjo T., Nakao S. Lymphocyte collection for donor leucocyte infusion from normal donors: estimation of the minimum processed blood volume and safety of the procedure. Vox Sang 2001, 81:124-127.
55. Okamoto H., Mizuno K., Horio T. Circulating CD14+ CD16+ monocytes are expanded in sarcoidosis patients. J Dermatol 2003, 30:503-509.