MicroRNA-155 potentiates the inflammatory response in hypothermia by suppressing IL-10 production

FASEB Journal

Volumn 28, Issue 12, 2014, Pages 5322-5336

  Billeter, Adrian T ^a   Hellmann, Jason ^a   Roberts, Henry ^a   Druen, Devin ^a   Gardner, Sarah A ^a   Sarojini, Harshini ^a   Galandiuk, Susan ^a   Chien, Sufan ^a   Bhatnagar, Aruni ^a   Spite, Matthew ^a   Polk, Hiram C ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Cold exposure; Peritonitis; Sepsis

Indexed keywords

INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MICRORNA 155; PROTEIN; SHIP1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CYTOKINE; MICRORNA; MIRN155 MICRORNA, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLD EXPOSURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; HUMAN; HUMAN CELL; INDUCED HYPOTHERMIA; INFLAMMATION; MALE; MONOCYTE; MOUSE; NONHUMAN; PERITONITIS; SIGNAL TRANSDUCTION; SURVIVAL; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; COMPLICATION; HYPOTHERMIA; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

MURINAE;

ANIMALS; CELLS, CULTURED; CYTOKINES; HUMANS; HYPOTHERMIA; INFLAMMATION; INTERLEUKIN-10; MICE; MICRORNAS; MONOCYTES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84919756065     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-258335     Document Type: Article

References (60)

1. Arrich, J., Holzer, M., Havel, C., Mullner, M., and Herkner, H. (2012) Hypothermia for neuroprotection in adults after cardiopulmonary resuscitation. Cochrane Database Syst. Rev. 9, CD004128
2. Matsui, T., Yoshida, Y., Yanagihara, M., and Suenaga, H. (2014) Hypothermia at 35 degrees C reduces the time-dependent microglial production of pro-inflammatory and anti-inflammatory factors that mediate neuronal cell death. Neurocrit. Care 20, 301-310
3. Tian, D. H., Wan, B., Bannon, P. G., Misfeld, M., Lemaire, S. A., Kazui, T., Kouchoukos, N. T., Elefteriades, J. A., Bavaria, J., Coselli, J. S., Griepp, R. B., Mohr, F. W., Oo, A., Svensson, L. G., Hughes, G. C., and Yan, T. D. (2013) A meta-analysis of deep hypothermic circulatory arrest versus moderate hypothermic circulatory arrest with selective antegrade cerebral perfusion. Ann. Cardiothorac. Surg. 2, 148-158
4. Jiang, S. Y., Zhao, Y. Y., and Zhao, X. G. (2013) Potential role of therapeutic hypothermia in the salvage of traumatic hemorrhagic shock. Crit. Care 17, 318
5. Ahmad, F. U., Wang, M. Y., and Levi, A. D. (2014) Hypothermia for acute spinal cord injury-a review. World Neurosurg. 82, 207-214
6. Geurts, M., Macleod, M. R., Kollmar, R., Kremer, P. H., and van der Worp, H. B. (2014) Therapeutic hypothermia and the risk of infection: a systematic review and meta-analysis. Crit. Care Med. 42, 231-242
7. Perbet, S., Mongardon, N., Dumas, F., Bruel, C., Lemiale, V., Mourvillier, B., Carli, P., Varenne, O., Mira, J. P., Wolff, M., and Cariou, A. (2011) Early-onset pneumonia after cardiac arrest: characteristics, risk factors and influence on prognosis. Am. J. Respir. Crit. Care Med. 184, 1048-1054
8. Mourvillier, B., Tubach, F., van de Beek, D., Garot, D., Pichon, N., Georges, H., Lefevre, L. M., Bollaert, P. E., Boulain, T., Luis, D., Cariou, A., Girardie, P., Chelha, R., Megarbane, B., Delahaye, A., Chalumeau-Lemoine, L., Legriel, S., Beuret, P., Brivet, F., Bruel, C., Camou, F., Chatellier, D., Chillet, P., Clair, B., Constantin, J. M., Duguet, A., Galliot, R., Bayle, F., Hyvernat, H., Ouchenir, K., Plantefeve, G., Quenot, J. P., Richecoeur, J., Schwebel, C., Sirodot, M., Esposito-Farese, M., Le Tulzo, Y., and Wolff, M. (2013) Induced hypothermia in severe bacterial meningitis: a randomized clinical trial. JAMA 310, 2174-2183
9. Bukur, M., Kurtovic, S., Berry, C., Tanios, M., Ley, E. J., and Salim, A. (2012) Pre-hospital hypothermia is not associated with increased survival after traumatic brain injury. J. Surg. Res. 175, 24-29
10. Kurz, A., Sessler, D. I., and Lenhardt, R. (1996) Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. Study of Wound Infection and Temperature Group. N. Engl. J. Med. 334, 1209-1215
11. Frank, S. M., Fleisher, L. A., Breslow, M. J., Higgins, M. S., Olson, K. F., Kelly, S., and Beattie, C. (1997) Perioperative maintenance of normothermia reduces the incidence of morbid cardiac events. A randomized clinical trial. JAMA 277, 1127-1134
12. Billeter, A. T., Hohmann, S. F., Druen, D., Cannon, R., and Polk, H. C., Jr. (2014) Unintentional perioperative hypothermia is associated with severe complications and high mortality in elective operations. [E-pub ahead of print] Surgery doi:10.1016/j.surg.2014.04.024
13. Akriotis, V., and Biggar, W. D. (1985) The effects of hypothermia on neutrophil function in vitro. J. Leukoc. Biol. 37, 51-61
14. Wenisch, C., Narzt, E., Sessler, D. I., Parschalk, B., Lenhardt, R., Kurz, A., and Graninger, W. (1996) Mild intraoperative hypothermia reduces production of reactive oxygen intermediates by polymorphonuclear leukocytes. Anesth. Analg. 82, 810-816
15. Fairchild, K. D., Singh, I. S., Carter, H. C., Hester, L., and Hasday, J. D. (2005) Hypothermia enhances phosphorylation of IκB kinase and prolongs nuclear localization of NF-κB in lipopolysaccharide-activated macrophages. Am. J. Physiol. Cell Physiol. 289, C1114-C1121
16. Fairchild, K. D., Singh, I. S., Patel, S., Drysdale, B. E., Viscardi, R. M., Hester, L., Lazusky, H. M., and Hasday, J. D. (2004) Hypothermia prolongs activation of NF-kappaB and augments generation of inflammatory cytokines. Am. J. Physiol. Cell Physiol. 287, C422-C431
17. Fairchild, K. D., Viscardi, R. M., Hester, L., Singh, I. S., and Hasday, J. D. (2000) Effects of hypothermia and hyperthermia on cytokine production by cultured human mononuclear phagocytes from adults and newborns. J. Interferon Cytokine Res. 20, 1049-1055
18. Hammarfjord, O., and Wallin, R. P. (2010) Dendritic cell function at low physiological temperature. J. Leukoc. Biol. 88, 747-756
19. O'Neill, L. A., Sheedy, F. J., and McCoy, C. E. (2011) MicroRNAs: the fine-tuners of Toll-like receptor signalling. Nat. Rev. Immunol. 11, 163-175
20. Ceppi, M., Pereira, P. M., Dunand-Sauthier, I., Barras, E., Reith, W., Santos, M. A., and Pierre, P. (2009) MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 106, 2735-2740
21. Hou, J., Wang, P., Lin, L., Liu, X., Ma, F., An, H., Wang, Z., and Cao, X. (2009) MicroRNA-146a feedback inhibits RIG-I-dependent Type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J. Immunol. 183, 2150-2158
22. Kurowska-Stolarska, M., Alivernini, S., Ballantine, L. E., Asquith, D. L., Millar, N. L., Gilchrist, D. S., Reilly, J., Ierna, M., Fraser, A. R., Stolarski, B., McSharry, C., Hueber, A. J., Baxter, D., Hunter, J., Gay, S., Liew, F. Y., and McInnes, I. B. (2011) MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc. Natl. Acad. Sci. U. S. A. 108, 11193-11198
23. O'Connell, R. M., Taganov, K. D., Boldin, M. P., Cheng, G., and Baltimore, D. (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. U. S. A. 104, 1604-1609
24. Tili, E., Michaille, J. J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., Fabbri, M., Alder, H., Liu, C. G., Calin, G. A., and Croce, C. M. (2007) 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. 179, 5082-5089
25. Zhu, Q. Y., Liu, Q., Chen, J. X., Lan, K., and Ge, B. X. (2010) MicroRNA-101 targets MAPK phosphatase-1 to regulate the activation of MAPKs in macrophages. J. Immunol. 185, 7435-7442
26. Cremer, T. J., Ravneberg, D. H., Clay, C. D., Piper-Hunter, M. G., Marsh, C. B., Elton, T. S., Gunn, J. S., Amer, A., Kanneganti, T. D., Schlesinger, L. S., Butchar, J. P., and Tridandapani, S. (2009) MiR-155 induction by F. novicida but not the virulent F. tularensis results in SHIP down-regulation and enhanced pro-inflammatory cytokine response. PLoS One 4, e8508
27. McCoy, C. E., Sheedy, F. J., Qualls, J. E., Doyle, S. L., Quinn, S. R., Murray, P. J., and O'Neill, L. A. (2010) IL-10 inhibits miR-155 induction by toll-like receptors. J. Biol. Chem. 285, 20492-20498
28. Sheedy, F. J., Palsson-McDermott, E., Hennessy, E. J., Martin, C., O'Leary, J. J., Ruan, Q., Johnson, D. S., Chen, Y., and O'Neill, L. A. (2010) Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat. Immunol. 11, 141-147
29. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25, 402-408
30. Ghosn, E. E., Cassado, A. A., Govoni, G. R., Fukuhara, T., Yang, Y., Monack, D. M., Bortoluci, K. R., Almeida, S. R., and Herzenberg, L. A. (2010) Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc. Natl. Acad. Sci. U. S. A. 107, 2568-2573
31. O'Connell, R. M., Chaudhuri, A. A., Rao, D. S., and Baltimore, D. (2009) Inositol phosphatase SHIP1 is a primary target of miR-155. Proc. Natl. Acad. Sci. U. S. A. 106, 7113-7118
32. Trotta, R., Chen, L., Ciarlariello, D., Josyula, S., Mao, C., Costinean, S., Yu, L., Butchar, J. P., Tridandapani, S., Croce, C. M., and Caligiuri, M. A. (2012) miR-155 regulates IFN-gamma production in natural killer cells. Blood 119, 3478-3485
33. Wang, P., Hou, J., Lin, L., Wang, C., Liu, X., Li, D., Ma, F., Wang, Z., and 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
34. Billeter, A. T., Druen, D., Kanaan, Z. M., and Polk, H. C., Jr. (2012) MicroRNAs: new helpers for surgeons? Surgery 151, 1-5
35. Inaba, K., Berg, R., Barmparas, G., Rhee, P., Jurkovich, G. J., Recinos, G., Teixeira, P. G., and Demetriades, D. (2012) Prospective evaluation of ambient operating room temperature on the core temperature of injured patients undergoing emergent surgery. J. Trauma Acute Care Surg. 73, 1478-1483
36. Ajuebor, M. N., Das, A. M., Virag, L., Flower, R. J., Szabo, C., and Perretti, M. (1999) Role of resident peritoneal macrophages and mast cells in chemokine production and neutrophil migration in acute inflammation: evidence for an inhibitory loop involving endogenous IL-10. J. Immunol. 162, 1685-1691
37. Goldszmid, R. S., Caspar, P., Rivollier, A., White, S., Dzutsev, A., Hieny, S., Kelsall, B., Trinchieri, G., and Sher, A. (2012) NK cell-derived interferon-gamma orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity 36, 1047-1059
38. Jenkins, S. J., Ruckerl, D., Cook, P. C., Jones, L. H., Finkelman, F. D., van Rooijen, N., MacDonald, A. S., and Allen, J. E. (2011) Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332, 1284-1288
39. Bannenberg, G. L., Chiang, N., Ariel, A., Arita, M., Tjonahen, E., Gotlinger, K. H., Hong, S., and Serhan, C. N. (2005) Molecular circuits of resolution: formation and actions of resolvins and protectins. J. Immunol. 174, 4345-4355
40. Schif-Zuck, S., Gross, N., Assi, S., Rostoker, R., Serhan, C. N., and Ariel, A. (2011) Saturated-efferocytosis generates pro-resolving CD11b low macrophages: modulation by resolvins and glucocorticoids. Eur. J. Immunol. 41, 366-379
41. Ariel, A., and Serhan, C. N. (2012) New lives given by cell death: macrophage differentiation following their encounter with apoptotic leukocytes during the resolution of inflammation. Front. Immunol. 3, 4
42. Truettner, J. S., Alonso, O. F., Bramlett, H. M., and Dietrich, W. D. (2011) Therapeutic hypothermia alters microRNA responses to traumatic brain injury in rats. J. Cereb. Blood Flow Metab. 31, 1897-1907
43. Truettner, J. S., Motti, D., and Dietrich, W. D. (2013) MicroRNA overexpression increases cortical neuronal vulnerability to injury. Brain Res. 1533, 122-130
44. Meybohm, P., Gruenewald, M., Zacharowski, K. D., Albrecht, M., Lucius, R., Fosel, N., Hensler, J., Zitta, K., and Bein, B. (2010) Mild hypothermia alone or in combination with anesthetic post-conditioning reduces expression of inflammatory cytokines in the cerebral cortex of pigs after cardiopulmonary resuscitation. Crit. Care 14, R21
45. Beilman, G. J., Blondet, J. J., Nelson, T. R., Nathens, A. B., Moore, F. A., Rhee, P., Puyana, J. C., Moore, E. E., and Cohn, S. M. (2009) Early hypothermia in severely injured trauma patients is a significant risk factor for multiple organ dysfunction syndrome but not mortality. Ann. Surg. 249, 845-850
46. Flores-Maldonado, A., Medina-Escobedo, C. E., Rios-Rodriguez, H. M., and Fernandez-Dominguez, R. (2001) Mild perioperative hypothermia and the risk of wound infection. Arch. Med. Res. 32, 227-231
47. Seamon, M. J., Wobb, J., Gaughan, J. P., Kulp, H., Kamel, I., and Dempsey, D. T. (2012) The effects of intraoperative hypothermia on surgical site infection: an analysis of 524 trauma laparotomies. Ann. Surg. 255, 789-795
48. Xiao, H., and Remick, D. G. (2005) Correction of perioperative hypothermia decreases experimental sepsis mortality by modulating the inflammatory response. Crit. Care Med. 33, 161-167
49. Arons, M. M., Wheeler, A. P., Bernard, G. R., Christman, B. W., Russell, J. A., Schein, R., Summer, W. R., Steinberg, K. P., Fulkerson, W., Wright, P., Dupont, W. D., and Swindell, B. B. (1999) Effects of ibuprofen on the physiology and survival of hypothermic sepsis. Ibuprofen in Sepsis Study Group. Crit. Care Med. 27, 699-707
50. Fries, M., Stoppe, C., Brucken, D., Rossaint, R., and Kuhlen, R. (2009) Influence of mild therapeutic hypothermia on the inflammatory response after successful resuscitation from cardiac arrest. J. Crit. Care 24, 453-457
51. Monk, C. E., Hutvagner, G., and Arthur, J. S. (2010) Regulation of miRNA transcription in macrophages in response to Candida albicans. PLoS One 5, e13669
52. Van Der Poll, T., Marchant, A., and van Deventer, S. J. (1997) The role of interleukin-10 in the pathogenesis of bacterial infection. Clin. Microbiol. Infect. 3, 605-607
53. Pu, J., Bai, D., Yang, X., Lu, X., Xu, L., and Lu, J. (2012) Adrenaline promotes cell proliferation and increases chemoresistance in colon cancer HT29 cells through induction of miR-155. Biochem. Biophys. Res. Commun. 428, 210-215
54. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., and Julius, D. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824
55. Clark, N., Keeble, J., Fernandes, E. S., Starr, A., Liang, L., Sugden, D., de Winter, P., and Brain, S. D. (2007) The transient receptor potential vanilloid 1 (TRPV1) receptor protects against the onset of sepsis after endotoxin. FASEB J. 21, 3747-3755
56. Fernandes, E. S., Liang, L., Smillie, S. J., Kaiser, F., Purcell, R., Rivett, D. W., Alam, S., Howat, S., Collins, H., Thompson, S. J., Keeble, J. E., Riffo-Vasquez, Y., Bruce, K. D., and Brain, S. D. (2012) TRPV1 deletion enhances local inflammation and accelerates the onset of systemic inflammatory response syndrome. J. Immunol. 188, 5741-5751
57. Brock, M., Samillan, V. J., Trenkmann, M., Schwarzwald, C., Ulrich, S., Gay, R. E., Gassmann, M., Ostergaard, L., Gay, S., Speich, R., and Huber, L. C. (2012) AntagomiR directed against miR-20a restores functional BMPR2 signalling and prevents vascular remodelling in hypoxia-induced pulmonary hypertension. [Epub ahead of print] Eur. Heart J. doi:10.1093/eurheartj/ehs060
58. Li, R. C., Tao, J., Guo, Y. B., Wu, H. D., Liu, R. F., Bai, Y., Lv, Z. Z., Luo, G. Z., Li, L. L., Wang, M., Yang, H. Q., Gao, W., Han, Q. D., Zhang, Y. Y., Wang, X. J., Xu, M., and Wang, S. Q. (2013) In vivo suppression of microRNA-24 prevents the transition toward decompensated hypertrophy in aortic-constricted mice. Circ. Res. 112, 601-605
59. Care, A., Catalucci, D., Felicetti, F., Bonci, D., Addario, A., Gallo, P., Bang, M. L., Segnalini, P., Gu, Y., Dalton, N. D., Elia, L., Latronico, M. V., Hoydal, M., Autore, C., Russo, M. A., Dorn, G. W., 2nd, Ellingsen, O., Ruiz-Lozano, P., Peterson, K. L., Croce, C. M., Peschle, C., and Condorelli, G. (2007) MicroRNA-133 controls cardiac hypertrophy. Nat. Med. 13, 613-618
60. Krutzfeldt, J., Rajewsky, N., Braich, R., Rajeev, K. G., Tuschl, T., Manoharan, M., and Stoffel, M. (2005) Silencing of microRNAs in vivo with "antagomirs." Nature 438, 685-689