MicroRNA-125b prevents cardiac dysfunction in polymicrobial sepsis by targeting TRAF6-mediated nuclear factor κb activation and p53-mediated apoptotic signaling

Journal of Infectious Diseases

Volumn 214, Issue 11, 2016, Pages 1773-1783

  Ma, He ^a,c   Wang, Xiaohui ^a   Ha, Tuanzhu ^a   Gao, Ming ^a   Liu, Li ^c   Wang, Ruitao ^d   Yu, Kaijiang ^d   Kalbfleisch, John H ^a,b   Kao, Race L ^a   Williams, David L ^a   Li, Chuanfu ^a  

^a East Tennessee State University   (United States)

^b Department of Biometry and Medical Computing ^*  (United States)

^c THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^d HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Cardiac function; microRNA 125b; NF B; Sepsis; TRAF6

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; MICRORNA 125B; PROTEIN BAK; PROTEIN BAK1; PROTEIN BAX; PROTEIN P53; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; MICRORNA; MIRN125 MICRORNA, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ECHOCARDIOGRAPHY; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; HEART EJECTION FRACTION; HEART FAILURE; HEART FUNCTION; HEART PROTECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; LENTIVIRINAE; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SEPSIS; SIGNAL TRANSDUCTION; SURVIVAL RATE; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; COMPLICATION; DIAGNOSTIC IMAGING; DISEASE MODEL; METABOLISM; MIXED INFECTION; PATHOLOGY; SURVIVAL ANALYSIS;

ANIMALS; COINFECTION; DISEASE MODELS, ANIMAL; ECHOCARDIOGRAPHY; HEART FAILURE; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MYOCARDIUM; NF-KAPPA B; SEPSIS; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TNF RECEPTOR-ASSOCIATED FACTOR 6;

EID: 85014600075     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiw449     Document Type: Article

References (44)

1. Mayr FB, Yende S, Angus DC. Epidemiology of severe sepsis. Virulence 2014; 5:4-11.
2. Sepsis Alliance website. http://www.sepsisalliance.org. Accessed 10 September 2016.
3. Fernandes CJ Jr, de Assuncao MSC. Myocardial dysfunction in sepsis: a large, un-solved puzzle. Crit Care Res Pract 2012; 2012:896430.
4. Gao M, Ha T, Zhang X, et al. Toll-like receptor 3 plays a central role in cardiac dysfunction during polymicrobial sepsis. Crit Care Med 2012; 40:2390-9.
5. Feng Y, Zou L, Zhang M, Li Y, Chen C, Chao W. MyD88 and Trif signaling play distinct roles in cardiac dysfunction and mortality during endotoxin shock and polymicrobial sepsis. Anesthesiology 2011; 115:555-67.
6. Zou L, Feng Y, Chen YJ, et al. Toll-like receptor 2 plays a critical role in cardiac dysfunction during polymicrobial sepsis. Crit Care Med 2010; 38:1335-42.
7. Medzhitov R, Preston-Hurlburt P, Janeway CA Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 1997; 388:394-7.
8. Williams DL, Ha T, Li C, et al. Modulation of tissue toll-like receptor 2 and 4 during the early phases of polymicrobial sepsis correlates with mortality. Crit Care Med 2003; 31:1808-18.
9. Quinn SR, O'Neill LA. A trio of microRNAs that control Toll-like receptor signalling. Int Immunol 2011; 23:421-5.
10. O'Neill LA, Sheedy FJ, McCoy CE. MicroRNAs: the fine-tuners of Toll-like receptor signalling. Nat Rev Immunol 2011; 11:163-75.
11. Essandoh K, Fan G-C. Role of extracellular and intracellular microRNAs in sepsis. Biochim Biophys Acta 2014; 1842:2155-62.
12. Sun X, Icli B, Wara AK, et al. MicroRNA-181b regulates NF-κB-mediated vascular inflammation. J Clin Invest 2012; 122:1973-90.
13. Gao M, Wang X, Zhang X, et al. Attenuation of cardiac dysfunction in polymicro-bial sepsis by microRNA-146a is mediated via targeting of IRAK1 and TRAF6 expression. J Immunol 2015; 195:672-82.
14. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75:843-54.
15. Tili E, Michaille JJ, Cimino A, et al. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol 2007; 179:5082-9.
16. Androulidaki A, Iliopoulos D, Arranz A, et al. The kinase Akt1 controls macro-phage response to lipopolysaccharide by regulating microRNAs. Immunity 2009; 31:220-31.
17. Cheng NL, Chen X, Kim J, et al. MicroRNA-125b modulates inflammatory che-mokine CCL4 expression in immune cells and its reduciton causes CCl4 increase with age. Aging Cell 2015; 14:200-8.
18. Wang X, Ha T, Zou J, et al. MicroRNA-125b protects against myocardial ischae-mia/reperfusion injury via targeting p53-mediated apoptotic signalling and TRAF6. Cardiovasc Res 2014; 102:385-95.
19. Le MTN, Teh C, Shyh-Chang N, et al. MicroRNA-125b is a novel negative regulator of p53. Genes Dev 2009; 23:862-76.
20. Oberholzer C, Oberholzer A, Clare-Salzler M, Moldawer LL. Apoptosis in sepsis: a new target for therapeutic exploration. FASEB J 2001; 15:879-92.
21. Hotchkiss RS, Swanson PE, Freeman BD, et al. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 1999; 27:1230-51.
22. Hotchkiss RS, Swanson PE, Cobb JP, Jacobson A, Buchman TG, Karl IE. Apopto-sis in lymphoid and parenchymal cells during sepsis: findings in normal and T-and B-cell-deficient mice. Crit Care Med 1997; 25:1298-307.
23. Neviere R, Fauvel H, Chopin C, Formstecher P, Marchetti P. Caspase inhibition prevents cardiac dysfunction and heart apoptosis in a rat model of sepsis. Am J Respir Crit Care Med 2001; 163:218-25.
24. Zheng D, Yu Y, Li M, et al. Inhibition of microRNA 195 prevents apoptosis and multiple-organ injury in mouse models of sepsis. J Infect Dis 2016; 213:1661-70.
25. Ha T, Hua F, Grant D, et al. Glucan phosphate attenuates cardiac dysfunction and inhibits cardiac MIF expression and apoptosis in septic mice. Am J Physiol Heart Circ Physiol 2006; 291:H1910-8.
26. National Research Council Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the care and use of laboratory animals. 8th ed.Washington, DC: National Academies Press, 2011.
27. Ha T, Lu C, Liu L, et al. TLR2 ligands attenuate cardiac dysfunction in polymicro-bial sepsis via a phosphoinositide-3-kinase dependent mechanism. Am J Physiol Heart Circ Physiol 2010; 298:H984-91.
28. Gao M, Ha T, Zhang X, et al. The Toll-like receptor 9 ligand, CpG oligodeoxynu-cleotide, attenuates cardiac dysfunction in polymicrobial sepsis, involving activation of both phosphoinositide 3 kinase/AKT and extracellular-signal-related kinase signaling. J Infect Dis 2013; 207:1471-9.
29. Wang X, Ha T, Liu L, et al. Increased expression of microRNA-164a decreases myocardial ischemia/reperfusion injury. Cardiovasc Res 2013; 97:432-42.
30. Lu C, Wang X, Ha T, et al. Attenuation of cardiac dysfunction and remodeling of myocardial infarction by microRNA-130a are mediated by suppression of PTEN and activation of PI3K dependent signaling. J Mol Cell Cardiol 2015; 89(Pt A):87-97.
31. Lu C, Hua F, Liu L, et al. Scavenger receptor class-A has a central role in cerebral ischemia/reperfusion injury. J Cereb Blood Flow Metab 2010; 30:1972-81.
32. Alves-Filho JC, de Freitas A, Spiller F, Souto FO, Cunha CQ. The role of neutro-phils in severe sepsis. Shock 2008; 30(suppl 1):3-9.
33. Cavaillon J-M, Adib-Conquy M. Monocytes/macrophages and sepsis. Crit Care Med 2005; 33(12 suppl):S506-9.
34. Peters K, Unger RE, Brunner J, Kirkpatrick CJ. Molecular basis of endothelial dysfunction in sepsis. Cardiovasc Res 2003; 60:49-57.
35. Ma X, Buscaglia LEB, Barker JR, Li Y. MicroRNAs in NF-κB signaling. J Mol Cell Biol 2011; 3:159-66.
36. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschi T. Identification of tissue-specific microRNAs from mouse. Curr Biol 2002; 12:735-9.
37. Murphy AJ, Guyre PM, Pioli PA. Estradiol suppresses NF-kappa B activation through coordinated regulation of let-7a and miR-125b in primary human mac-rophages. J Immunol 2010; 184:5029-37.
38. Rajaram MV, Ni B, Morris JD, et al. Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein ki-nase 2 (MK2) and microRNA miR-125b. Proc Natl Acad Sci USA 2011; 108:17408-13.
39. Tsujimoto H, Ono S, Efron PA, Scumpia PO, Moldawer LL, Mochizuki H. Role of Toll-like receptors in the development of sepsis. Shock 2008; 29:315-21.
40. Aird WC. The role of the endothelium in severe sepsis and multiple organ dys-function syndrome. Blood 2003; 101:3765-77.
41. Rao RM, Yang L, Garcia-Cardena G, Lusinskas FW. Endotheliel-dependent mechanisms of leukocyte recruitment to the vascular wall. Circ Res 2007; 101:234-47.
42. Lockyer JM, Colladay JS, Alperin-Lea WL, Hammond T, Buda AJ. Inhibition of nuclear factor-κB-mediated adhesion molecule expression in human endothelial cells. Circ Res 1998; 82:314-20.
43. Vaseva AV, Moll UM. The mitochondrial p53 pathway. Biochim Biophys Acta 2009; 1787:414-20.
44. Zhou M, Liu Z, Zhao Y, et al. MicroRNA-125b confers the resistance of breast cancer cells to paclitaxel through suppression of pro-apoptotic Bcl-2 antagonist kiler 1 (BAK1) expression. J Biol Chem 2010; 285:21496-507.