Frontline science: HMGB1 induces neutrophil dysfunction in experimental sepsis and in patients who survive septic shock

Journal of Leukocyte Biology

Volumn 101, Issue 6, 2017, Pages 1281-1287

  Grégoire, Murielle ^a,b,c,d   Tadié, Jean Marc ^a,b,c,d,e   Uhel, Fabrice ^a,b,c,d,e   Gacouin, Arnaud ^d,e   Piau, Caroline ^d   Bone, Nathaniel ^f   Le Tulzo, Yves ^a,b,c,d,e   Abraham, Edward ^g   Tarte, Karin ^a,b,c,d   Zmijewski, Jaroslaw W ^f  

^a INSERM   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c ETABLISSEMENT FRANÇAIS DU SANG   (France)

^d RENNES UNIVERSITY HOSPITAL   (France)

^e UNIVERSITÉ DE RENNES 1   (France)

^f University of Alabama at Birmingham   (United States)

^g WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

HMGB1; Immunosuppression; NADPH oxidase; Neutrophils; Sepsis

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; HYPERTENSIVE FACTOR; IMIPENEM; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TOLL LIKE RECEPTOR 4; LIPOPOLYSACCHARIDE;

ABDOMINAL INFECTION; ADULT; ADULT RESPIRATORY DISTRESS SYNDROME; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL CLEARANCE; BACTERIAL ENDOCARDITIS; BACTERICIDAL ACTIVITY; CARDIOGENIC SHOCK; CECAL LIGATION AND PUNCTURE-INDUCED SEPSIS; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; EPILEPTIC STATE; EXTRACELLULAR MATRIX; HEART ARREST; HUMAN; HUMAN CELL; HYPOTENSION; IMMUNE DEFICIENCY; IN VITRO STUDY; INFECTION SENSITIVITY; LENGTH OF STAY; MALE; MENINGITIS; MOUSE; NEUTROPHIL; NONHUMAN; PNEUMONIA; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RESPIRATORY BURST; SECONDARY INFECTION; SEPTIC SHOCK; URINARY TRACT INFECTION; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; COMPARATIVE STUDY; FEMALE; IMMUNOLOGY; LEUKOCYTE DISORDER; METABOLISM; MIDDLE AGED; PATHOLOGY; PERITONITIS; SEPSIS; SIGNAL TRANSDUCTION;

AGED; ANIMALS; CASE-CONTROL STUDIES; FEMALE; HMGB1 PROTEIN; HUMANS; LEUKOCYTE DISORDERS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; NADPH OXIDASE; NEUTROPHILS; PERITONITIS; SEPSIS; SIGNAL TRANSDUCTION;

EID: 85020177470     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.5HI0316-128RR     Document Type: Article

References (49)

1. Angus, D. C., van der Poll, T. (2013) Severe sepsis and septic shock. N. Engl. J. Med. 369, 840–851.
2. Boomer, J. S., To, K., Chang, K. C., Takasu, O., Osborne, D. F., Walton, A. H., Bricker, T. L., Jarman II S. D., Kreisel, D., Krupnick, A. S., Srivastava, A., Swanson, P. E., Green, J. M., Hotchkiss, R. S. (2011) Immunosuppression in patients who die of sepsis and multiple organ failure. JAMA 306, 2594–2605.
3. Hotchkiss, R. S., Monneret, G., Payen, D. (2013) Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect. Dis. 13, 260–268.
4. Benjamim, C. F., Hogaboam, C. M., Kunkel, S. L. (2004) The chronic consequences of severe sepsis. J. Leukoc. Biol. 75, 408–412.
5. Hotchkiss, R. S., Coopersmith, C. M., McDunn, J. E., Ferguson, T. A. (2009) The sepsis seesaw: tilting toward immunosuppression. Nat. Med. 15, 496–497.
6. Le Tulzo, Y., Pangault, C., Amiot, L., Guilloux, V., Tribut, O., Arvieux, C., Camus, C., Fauchet, R., Thomas, R., Drénou, B. (2004) Monocyte human leukocyte antigen-DR transcriptional downregulation by cortisol during septic shock. Am. J. Respir. Crit. Care Med. 169, 1144–1151.
7. Ward, P. A. (2011) Immunosuppression in sepsis. JAMA 306, 2618–2619.
8. Cohen, J., Opal, S., Calandra, T. (2012) Sepsis studies need new direction. Lancet Infect. Dis. 12, 503–505.
9. Vincent, J. L., Opal, S. M., Marshall, J. C., Tracey, K. J. (2013) Sepsis definitions: time for change. Lancet 381, 774–775.
10. Leentjens, J., Kox, M., Koch, R. M., Preijers, F., Joosten, L. A., van der Hoeven, J. G., Netea, M. G., Pickkers, P. (2012) Reversal of immunoparalysis in humans in vivo: a double-blind, placebo-controlled, randomized pilot study. Am. J. Respir. Crit. Care Med. 186, 838–845.
11. Dellinger, R. P., Levy, M. M., Rhodes, A., Annane, D., Gerlach, H., Opal, S. M., Sevransky, J. E., Sprung, C. L., Douglas, I. S., Jaeschke, R., Osborn, T. M., Nunnally, M. E., Townsend, S. R., Reinhart, K., Kleinpell, R. M., Angus, D. C., Deutschman, C. S., Machado, F. R., Rubenfeld, G. D., Webb, S. A., Beale, R. J., Vincent, J. L., Moreno, R.; Surviving Sepsis Campaign Guidelines Committee including the Pediatric Subgroup. (2013) Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2012. Crit. Care Med. 41, 580–637.
12. Stephan, F., Yang, K., Tankovic, J., Soussy, C. J., Dhonneur, G., Duvaldestin, P., Brochard, L., Brun-Buisson, C., Harf, A., Delclaux, C. (2002) Impairment of polymorphonuclear neutrophil functions precedes nosocomial infections in critically ill patients. Crit. Care Med. 30, 315–322.
13. Kolaczkowska, E., Kubes, P. (2013) Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159–175.
14. Grailer, J. J., Kalbitz, M., Zetoune, F. S., Ward, P. A. (2014) Persistent neutrophil dysfunction and suppression of acute lung injury in mice following cecal ligation and puncture sepsis. J. Innate Immun. 6, 695–705.
15. Mantovani, A., Cassatella, M. A., Costantini, C., Jaillon, S. (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519–531.
16. Segal, A. W. (2005) How neutrophils kill microbes. Annu. Rev. Immunol. 23, 197–223.
17. Tadié, J. M., Bae, H. B., Banerjee, S., Zmijewski, J. W., Abraham, E. (2012) Differential activation of RAGE by HMGB1 modulates neutrophilassociated NADPH oxidase activity and bacterial killing. Am. J. Physiol. Cell Physiol. 302, C249–C256.
18. Panday, A., Sahoo, M. K., Osorio, D., Batra, S. (2015) NADPH oxidases: an overview from structure to innate immunity-associated pathologies. Cell. Mol. Immunol. 12, 5–23.
19. Groemping, Y., Rittinger, K. (2005) Activation and assembly of the NADPH oxidase: a structural perspective. Biochem. J. 386, 401–416.
20. Geiszt, M., Kapus, A., Ligeti, E. (2001) Chronic granulomatous disease: more than the lack of superoxide? J. Leukoc. Biol. 69, 191–196.
21. Demaret, J., Venet, F., Friggeri, A., Cazalis, M. A., Plassais, J., Jallades, L., Malcus, C., Poitevin-Later, F., Textoris, J., Lepape, A., Monneret, G. (2015) Marked alterations of neutrophil functions during sepsis-induced immunosuppression. J. Leukoc. Biol. 98, 1081–1090.
22. Bianchi, M. E. (2009) HMGB1 loves company. J. Leukoc. Biol. 86, 573–576.
23. Andersson, U., Tracey, K. J. (2011) HMGB1 is a therapeutic target for sterile inflammation and infection. Annu. Rev. Immunol. 29, 139–162.
24. Yang, H., Antoine, D. J., Andersson, U., Tracey, K. J. (2013) The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis. J. Leukoc. Biol. 93, 865–873.
25. Wang, H., Ward, M. F., Sama, A. E. (2009) Novel HMGB1-inhibiting therapeutic agents for experimental sepsis. Shock 32, 348–357.
26. Manganelli, V., Signore, M., Pacini, I., Misasi, R., Tellan, G., Garofalo, T., Lococo, E., Chirletti, P., Sorice, M., Delogu, G. (2010) Increased HMGB1 expression and release by mononuclear cells following surgical/ anesthesia trauma. Crit. Care 14, R197.
27. Gibot, S., Massin, F., Cravoisy, A., Barraud, D., Nace, L., Levy, B., Bollaert, P. E. (2007) High-mobility group box 1 protein plasma concentrations during septic shock. Intensive Care Med. 33, 1347–1353.
28. Karlsson, S., Pettilä, V., Tenhunen, J., Laru-Sompa, R., Hynninen, M., Ruokonen, E. (2008) HMGB1 as a predictor of organ dysfunction and outcome in patients with severe sepsis. Intensive Care Med. 34, 1046–1053.
29. Tadié, J. M., Trinquart, L., Jannière-Nartey, C., Guerot, E., Louis, B., Fagon, J. Y., Diehl, J. L., Delclaux, C. (2010) Prediction of nosocomial infection acquisition in ventilated patients by nasal nitric oxide: proof-ofconcept study. Shock 34, 217–221.
30. Otto, G. P., Sossdorf, M., Claus, R. A., Rödel, J., Menge, K., Reinhart, K., Bauer, M., Riedemann, N. C. (2011) The late phase of sepsis is characterized by an increased microbiological burden and death rate. Crit. Care 15, R183.
31. Santos, S. S., Brunialti, M. K., Rigato, O., Machado, F. R., Silva, E., Salomao, R. (2012) Generation of nitric oxide and reactive oxygen species by neutrophils and monocytes from septic patients and association with outcomes. Shock 38, 18–23.
32. Grégoire, M., Guilloton, F., Pangault, C., Mourcin, F., Sok, P., Latour, M., Amé-Thomas, P., Flecher, E., Fest, T., Tarte, K. (2015) Neutrophils trigger a NF-kB dependent polarization of tumor-supportive stromal cells in germinal center B-cell lymphomas. Oncotarget 6, 16471–16487.
33. Tadie, J. M., Bae, H. B., Deshane, J. S., Bell, C. P., Lazarowski, E. R., Chaplin, D. D., Thannickal, V. J., Abraham, E., Zmijewski, J. W. (2012) Toll-like receptor 4 engagement inhibits adenosine 59-monophosphateactivated protein kinase activation through a high mobility group box 1 protein-dependent mechanism. Mol. Med. 18, 659–668.
34. Rittirsch, D., Huber-Lang, M. S., Flierl, M. A., Ward, P. A. (2009) Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 4, 31–36.
35. Lotze, M. T., Tracey, K. J. (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 5, 331–342.
36. Wrona, M., Patel, K., Wardman, P. (2005) Reactivity of 29,79- dichlorodihydrofluorescein and dihydrorhodamine 123 and their oxidized forms toward carbonate, nitrogen dioxide, and hydroxyl radicals. Free Radic. Biol. Med. 38, 262–270.
37. Zmijewski, J. W., Banerjee, S., Bae, H., Friggeri, A., Lazarowski, E. R., Abraham, E. (2010) Exposure to hydrogen peroxide induces oxidation and activation of AMP-activated protein kinase. J. Biol. Chem. 285, 33154–33164.
38. Stevenson, E. K., Rubenstein, A. R., Radin, G. T., Wiener, R. S., Walkey, A. J. (2014) Two decades of mortality trends among patients with severe sepsis: a comparative meta-analysis. Crit. Care Med. 42, 625–631.
39. Luyt, C. E., Combes, A., Deback, C., Aubriot-Lorton, M. H., Nieszkowska, A., Trouillet, J. L., Capron, F., Agut, H., Gibert, C., Chastre, J. (2007) Herpes simplex virus lung infection in patients undergoing prolonged mechanical ventilation. Am. J. Respir. Crit. Care Med. 175, 935–942.
40. Limaye, A. P., Kirby, K. A., Rubenfeld, G. D., Leisenring, W. M., Bulger, E. M., Neff, M. J., Gibran, N. S., Huang, M. L., Santo Hayes, T. K., Corey, L., Boeckh, M. (2008) Cytomegalovirus reactivation in critically ill immunocompetent patients. JAMA 300, 413–422.
41. Liu, Z., Bone, N., Jiang, S., Park, D. W., Tadie, J. M., Deshane, J., Rodriguez, C. A., Pittet, J. F., Abraham, E., Zmijewski, J. W. (2015) AMPactivated protein kinase and glycogen synthase kinase 3b modulate the severity of sepsis-induced lung injury [E-pub ahead of print]. Mol. Med. 10.2119/molmed.2015.00198.
42. Achouiti, A., de Vos, A. F., van’t Veer, C., Florquin, S., Tanck, M. W., Nawroth, P. P., Bierhaus, A., van der Poll, T., van Zoelen, M. A. (2016) Receptor for advanced glycation end products (RAGE) serves a Protective Role during Klebsiella pneumoniae - Induced Pneumonia. PLoS One 11, e0141000.
43. Fossati, G., Moulding, D. A., Spiller, D. G., Moots, R. J., White, M. R., Edwards, S. W. (2003) The mitochondrial network of human neutrophils: role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. J. Immunol. 170, 1964–1972.
44. Jiang, S., Park, D. W., Stigler, W. S., Creighton, J., Ravi, S., Darley-Usmar, V., Zmijewski, J. W. (2013) Mitochondria and AMP-activated protein kinase-dependent mechanism of efferocytosis. J. Biol. Chem. 288, 26013–26026.
45. Yang, L., Xie, M., Yang, M., Yu, Y., Zhu, S., Hou, W., Kang, R., Lotze, M. T., Billiar, T. R., Wang, H., Cao, L., Tang, D. (2014) PKM2 regulates the Warburg effect and promotes HMGB1 release in sepsis. Nat. Commun. 5, 4436.
46. Entezari, M., Weiss, D. J., Sitapara, R., Whittaker, L., Wargo, M. J., Li, J., Wang, H., Yang, H., Sharma, L., Phan, B. D., Javdan, M., Chavan, S. S., Miller, E. J., Tracey, K. J., Mantell, L. L. (2012) Inhibition of high-mobility group box 1 protein (HMGB1) enhances bacterial clearance and protects against Pseudomonas Aeruginosa pneumonia in cystic fibrosis. Mol. Med. 18, 477–485.
47. Barnay-Verdier, S., Fattoum, L., Borde, C., Kaveri, S., Gibot, S., Maréchal, V. (2011) Emergence of autoantibodies to HMGB1 is associated with survival in patients with septic shock. Intensive Care Med. 37, 957–962.
48. Sims, G. P., Rowe, D. C., Rietdijk, S. T., Herbst, R., Coyle, A. J. (2010) HMGB1 and RAGE in inflammation and cancer. Annu. Rev. Immunol. 28, 367–388.
49. LeBlanc, P. M., Doggett, T. A., Choi, J., Hancock, M. A., Durocher, Y., Frank, F., Nagar, B., Ferguson, T. A., Saleh, M. (2014) An immunogenic peptide in the A-box of HMGB1 protein reverses apoptosis-induced tolerance through RAGE receptor. J. Biol. Chem. 289, 7777–7786.