Induction of Neutrophil Extracellular Traps in Shiga Toxin-Associated Hemolytic Uremic Syndrome

Journal of Innate Immunity

Volumn 8, Issue 4, 2016, Pages 400-411

  Ramos, Maria Victoria ^a   Mejias, Maria Pilar ^a   Sabbione, Florencia ^a   Fernandez Brando, Romina Jimena ^a   Santiago, Adriana Patricia ^c   Amaral, Maria Marta ^b   Exeni, Ramon ^c   Trevani, Analia Silvina ^a   Palermo, Marina Sandra ^a  

^a ACADEMIA NACIONAL DE MEDICINA   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Hospital Municipal Del Niño   (Argentina)

Author keywords

Endothelial cells; Extracellular traps; Hemolytic uremic syndrome; Leukocyte elastase; Neutrophils; Shiga toxin

Indexed keywords

BIOLOGICAL MARKER; CD11B ANTIGEN; CD66B ANTIGEN; CIRCULATING FREE DNA; DNA; INTERLEUKIN 6; INTERLEUKIN 8; LYMPHOCYTE ANTIGEN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VEROTOXIN 2; SHIGA TOXIN;

ADULT; ANIMAL CELL; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; EX VIVO STUDY; EXTRACELLULAR TRAP; GLOMERULAR ENDOTHELIAL CELL; GLOMERULUS; HEMOLYTIC UREMIC SYNDROME; HUMAN; HUMAN CELL; INFLAMMATION; KIDNEY CELL; NETOSIS; NEUTROPHIL; NONHUMAN; NUCLEOSOME; OXIDATIVE STRESS; PLASMA; PRIORITY JOURNAL; UPREGULATION; ACUTE KIDNEY FAILURE; BACTERIAL INFECTION; CELL CULTURE; HEMOLYTIC ANEMIA; IMMUNOLOGY; KIDNEY; LEUKOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; PATHOLOGY; THROMBOCYTOPENIA;

ACUTE KIDNEY INJURY; ANEMIA, HEMOLYTIC; APOPTOSIS; BACTERIAL INFECTIONS; CELLS, CULTURED; CHILD; ENDOTHELIAL CELLS; EXTRACELLULAR TRAPS; HEMOLYTIC-UREMIC SYNDROME; HUMANS; INTERLEUKIN-6; INTERLEUKIN-8; KIDNEY; NEUTROPHIL ACTIVATION; NEUTROPHILS; REACTIVE OXYGEN SPECIES; SHIGA TOXIN; THROMBOCYTOPENIA;

EID: 84976872270     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000445770     Document Type: Article

References (42)

1. Paton JC, Paton AW: Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 1998; 3: 450-479.
2. Donohue-Rolfe A, Acheson DW, Keusch GT: Shiga toxin: purification, structure, and function. Rev Infect Dis 1991; 13:S293-S297.
3. Fernandez GC, Lopez MF, Gomez SA, Ramos MV, Bentancor LV, Fernandez-Brando RJ, Landoni VI, Dran GI, Meiss R, Isturiz MA, Palermo MS: Relevance of neutrophils in the murine model of haemolytic uraemic syndrome: mechanisms involved in Shiga toxin type 2-induced neutrophilia. Clin Exp Immunol 2006; 1: 76-84.
4. Milford DV, Staten J, MacGreggor I, Dawes J, Taylor CM, Hill FG: Prognostic markers in diarrhoea-associated haemolytic-uraemic syndrome: initial neutrophil count, human neutrophil elastase and von Willebrand factor antigen. Nephrol Dial Transplant 1991; 4: 232-237.
5. Fernandez GC, Gomez SA, Rubel CJ, Bentancor LV, Barrionuevo P, Alduncin M, Grimoldi I, Exeni R, Isturiz MA, Palermo MS: Impaired neutrophils in children with the typical form of hemolytic uremic syndrome. Pediatr Nephrol 2005; 9: 1306-1314.
6. Arfilli V, Carnicelli D, Rocchi L, Ricci F, Pagliaro P, Tazzari PL, Brigotti M: Shiga toxin 1 and ricin A chain bind to human polymorphonuclear leucocytes through a common receptor. Biochem J 2010; 1: 173-180.
7. Brigotti M, Carnicelli D, Arfilli V, Tamassia N, Borsetti F, Fabbri E, Tazzari PL, Ricci F, Pagliaro P, Spisni E, Cassatella MA: Identification of TLR4 as the receptor that recognizes Shiga toxins in human neutrophils. J Immunol 2013; 9: 4748-4758.
8. Brigotti M, Tazzari PL, Ravanelli E, Carnicelli D, Barbieri S, Rocchi L, Arfilli V, Scavia G, Ricci F, Bontadini A, Alfieri RR, Petronini PG, Pecoraro C, Tozzi AE, Caprioli A: Endothelial damage induced by Shiga toxins delivered by neutrophils during transmigration. J Leukoc Biol 2010; 1: 201-210.
9. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A: Neutrophil extracellular traps kill bacteria. Science 2004; 5663: 1532-1535.
10. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A: Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007; 2: 231-241.
11. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, Patel KD, Chakrabarti S, McAvoy E, Sinclair GD, Keys EM, Allen-Vercoe E, Devinney R, Doig CJ, Green FH, Kubes P: Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 4: 463-469.
12. Zawrotniak M, Rapala-Kozik M: Neutrophil extracellular traps (NETs)-formation and implications. Acta Biochim Pol 2013; 3: 277-284.
13. Kessenbrock K, Krumbholz M, Schonermarck U, Back W, Gross WL, Werb Z, Grone HJ, Brinkmann V, Jenne DE: Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009; 6: 623-625.
14. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD: Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 2010; 36: 15880-15885.
15. Margraf S, Logters T, Reipen J, Altrichter J, Scholz M, Windolf J: Neutrophil-derived circulating free DNA (cf-DNA/NETs): a potential prognostic marker for posttraumatic development of inflammatory second hit and sepsis. Shock 2008; 4: 352-358.
16. Bentancor LV, Bilen M, Brando RJ, Ramos MV, Ferreira LC, Ghiringhelli PD, Palermo MS: A DNA vaccine encoding the enterohemorragic Escherichia coli Shiga-like toxin 2 A2 and B subunits confers protective immunity to Shiga toxin challenge in the murine model. Clinical Vaccine Immunol 2009; 5: 712-718.
17. Boyum A: Separation of leukocytes from blood and bone marrow (introduction). Scand J Clin Lab Invest Suppl 1968; 97: 7.
18. McGinn S, Poronnik P, Gallery ED, Pollock CA: A method for the isolation of glomerular and tubulointerstitial endothelial cells and a comparison of characteristics with the human umbilical vein endothelial cell model. Nephrology (Carlton) 2004; 4: 229-237.
19. Amaral MM, Sacerdoti F, Jancic C, Repetto HA, Paton AW, Paton JC, Ibarra C: Action of shiga toxin type-2 and subtilase cytotoxin on human microvascular endothelial cells. PLoS One 2013; 7:e70431.
20. Brinkmann V, Goosmann C, Kuhn LI, Zychlinsky A: Automatic quantification of in vitro NET formation. Frontiers in Immunology 2013; 3: 413.
21. Balestracci A, Martin SM, Toledo I: Hyperuricemia in children with post-diarrheal hemolytic uremic syndrome. Pediatr Nephrol 2012; 8: 1421-1422.
22. Mitroulis I, Kambas K, Chrysanthopoulou A, Skendros P, Apostolidou E, Kourtzelis I, Drosos GI, Boumpas DT, Ritis K: Neutrophil extracellular trap formation is associated with IL-1beta and autophagy-related signaling in gout. PLoS One 2011; 12:e29318.
23. Kongmuang U, Honda T, Miwatani T: Isolation of Shiga toxin-resistant Vero cells and their use for easy identification of the toxin. Infect Immun 1988; 9: 2491-2494.
24. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, Herrmann M, Voll RE, Zychlinsky A: Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA 2010; 21: 9813-9818.
25. Meng W, Paunel-Gorgulu A, Flohe S, Witte I, Schadel-Hopfner M, Windolf J, Logters TT: Deoxyribonuclease is a potential counter regulator of aberrant neutrophil extracellular traps formation after major trauma. Mediators Inflamm 2012; 2012: 149560.
26. Fuchs TA, Kremer Hovinga JA, Schatzberg D, Wagner DD, Lammle B: Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood 2012; 6: 1157-1164.
27. Coad NA, Marshall T, Rowe B, Taylor CM: Changes in the postenteropathic form of the hemolytic uremic syndrome in children. Clin Nephrol 1991; 1: 10-16.
28. Walters MD, Matthei IU, Kay R, Dillon MJ, Barratt TM: The polymorphonuclear leucocyte count in childhood haemolytic uraemic syndrome. Pediatr Nephrol 1989; 2: 130-134.
29. Fernandez GC, Gomez SA, Ramos MV, Bentancor LV, Fernandez-Brando RJ, Landoni VI, Lopez L, Ramirez F, Diaz M, Alduncin M, Grimoldi I, Exeni R, Isturiz MA, Palermo MS: The functional state of neutrophils correlates with the severity of renal dysfunction in children with hemolytic uremic syndrome. Pediatr Res 2007; 1: 123-128.
30. Gomez SA, Abrey-Recalde MJ, Panek CA, Ferrarotti NF, Repetto MG, Mejias MP, Fernandez GC, Vanzulli S, Isturiz MA, Palermo MS: The oxidative stress induced in vivo by Shiga toxin-2 contributes to the pathogenicity of haemolytic uraemic syndrome. Clin Exp Immunol 2013; 3: 463-472.
31. King AJ, Sundaram S, Cendoroglo M, Acheson DW, Keusch GT: Shiga toxin induces superoxide production in polymorphonuclear cells with subsequent impairment of phagocytosis and responsiveness to phorbol esters. J Infect Dis 1999; 2: 503-507.
32. Fitzpatrick MM, Shah V, Filler G, Dillon MJ, Barratt TM: Neutrophil activation in the haemolytic uraemic syndrome: free and complexed elastase in plasma. Pediatr Nephrol 1992; 1: 50-53.
33. Griener TP, Mulvey GL, Marcato P, Armstrong GD: Differential binding of Shiga toxin
34. to human and murine neutrophils. J Med Microbiol 2007; 11: 1423-1430.
35. Brigotti M, Carnicelli D, Ravanelli E, Barbieri S, Ricci F, Bontadini A, Tozzi AE, Scavia G, Caprioli A, Tazzari PL: Interactions between Shiga toxins and human polymorphonuclear leukocytes. J Leukoc Biol 2008; 4: 1019-1027.
36. Brigotti M: The interactions of human neutrophils with shiga toxins and related plant toxins: danger or safety? Toxins 2012; 3: 157-190.
37. Geelen JM, van der Velden TJ, Te Loo DM, Boerman OC, van den Heuvel LP, Monnens LA: Lack of specific binding of Shiga-like toxin (verocytotoxin) and non-specific interaction of Shiga-like toxin 2 antibody with human polymorphonuclear leucocytes. Nephrol Dial Transplant 2007; 3: 749-755.
38. Holle JU, Williams JM, Harper L, Savage CO, Taylor CM: Effect of verocytotoxins (Shigalike toxins) on human neutrophils in vitro. Pediatr Nephrol 2005; 9: 1237-1244.
39. Flagler MJ, Strasser JE, Chalk CL, Weiss AA: Comparative analysis of the abilities of Shiga toxins 1 and 2 to bind to and influence neutrophil apoptosis. Infect Immun 2007; 2: 760-765.
40. Kannemeier C, Shibamiya A, Nakazawa F, Trusheim H, Ruppert C, Markart P, Song Y, Tzima E, Kennerknecht E, Niepmann M, von Bruehl ML, Sedding D, Massberg S, Gunther A, Engelmann B, Preissner KT: Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci USA 2007; 15: 6388-6393.
41. Arai Y, Yamashita K, Mizugishi K, Watanabe T, Sakamoto S, Kitano T, Kondo T, Kawabata H, Kadowaki N, Takaori-Kondo A: Serum neutrophil extracellular trap levels predict thrombotic microangiopathy after allogeneic stem cell transplantation. Biol Blood Marrow Transplant 2013; 12: 1683-1689.
42. Ma AC, Kubes P: Platelets, neutrophils, and neutrophil extracellular traps (NETs) in sepsis. J Thromb Haemost 2008; 3: 415-420.