Loss of suppression of tumorigenicity 2 (ST2) gene reverses sepsis-induced inhibition of lung host defense in mice

American Journal of Respiratory and Critical Care Medicine

Volumn 183, Issue 7, 2011, Pages 932-940

  Hoogerwerf, Jacobien J ^a   Leendertse, Masja ^a   Wieland, Catharina W ^a   De Vos, Alex F ^a   De Boer, J Daan ^a   Florquin, Sandrine ^a   Van Der Poll, Tom ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

CLP; Immunosuppression; Sepsis; ST2; T lymphocytes

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GAMMA INTERFERON; INTERLEUKIN 6; SUPPRESSION OF TUMORIGENICITY 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL INFECTION; CD8+ T LYMPHOCYTE; CECUM; CONTROLLED STUDY; GENE LOSS; GENOTYPE; HOST RESISTANCE; INNATE IMMUNITY; LUNG ALVEOLUS; LUNG INFECTION; MACROPHAGE; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RESPIRATORY TRACT INFECTION; SEPSIS;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNITY, INNATE; KAPLAN-MEIER ESTIMATE; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, INBRED BALB C; PNEUMONIA, BACTERIAL; PSEUDOMONAS INFECTIONS; RANDOM ALLOCATION; RECEPTORS, INTERLEUKIN; SEPSIS; STATISTICS, NONPARAMETRIC; SURVIVAL RATE; TUMOR NECROSIS FACTORS;

EID: 79953306457     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201006-0934OC     Document Type: Article

References (58)

1. Angus DC, Wax RS. Epidemiology of sepsis: an update. Crit Care Med 2001;29(Suppl. 7):S109-S116. (Pubitemid 32681592)
2. Hotchkiss RS, Karl IE. The pathophysiology and treatment of sepsis. N Engl J Med 2003;348:138-150. (Pubitemid 36056721)
3. Hotchkiss RS, Nicholson DW. Apoptosis and caspases regulate death and inflammation in sepsis. Nat Rev Immunol 2006;6:813-822. (Pubitemid 44631650)
4. van der Poll T, Opal SM. Host-pathogen interactions in sepsis. Lancet Infect Dis 2008;8:32-43.
5. Volk HD, Reinke P, Docke WD. Clinical aspects: from systemic inflammation to immunoparalysis. Chem Immunol 2000;74:162-177.
6. Steinhauser ML, Hogaboam CM, Kunkel SL, Lukacs NW, Strieter RM, Standiford TJ. IL-10 is a major mediator of sepsis-induced impairment in lung antibacterial host defense. J Immunol 1999;162:392-399. (Pubitemid 29018946)
7. Chen GH, Reddy RC, Newstead MW, Tateda K, Kyasapura BL, Standiford TJ. Intrapulmonary TNF gene therapy reverses sepsisinduced suppression of lung antibacterial host defense. J Immunol 2000;165:6496-6503.
8. Deng JC, Cheng G, Newstead MW, Zeng X, Kobayashi K, Flavell RA, Standiford TJ. Sepsis-induced suppression of lung innate immunity is mediated by IRAK-M. J Clin Invest 2006;116:2532-2542. (Pubitemid 44330152)
9. Muenzer JT, Davis CG, Dunne BS, Unsinger J, Dunne WM, Hotchkiss RS. Pneumonia after cecal ligation and puncture: a clinically relevant ''two-hit'' model of sepsis. Shock 2006;26:565-570.
10. Muenzer JT, Davis CG, Chang K, Schmidt RE, Dunne WM, Coopersmith CM, Hotchkiss RS. Characterization and modulation of the immunosuppressive phase of sepsis. Infect Immun 2010;78:1582-1592.
11. Pene F, Zuber B, Courtine E, Rousseau C, Ouaaz F, Toubiana J, Tazi A, Mira JP, Chiche JD. Dendritic cells modulate lung response to Pseudomonas aeruginosa in a murine model of sepsis-induced immune dysfunction. J Immunol 2008;181:8513-8520.
12. Hotchkiss RS, Tinsley KW, Swanson PE, Schmieg RE Jr, Hui JJ, Chang KC, Osborne DF, Freeman BD, Cobb JP, Buchman TG, et al. Sepsis-induced apoptosis causes progressive profound depletion of B and CD41 T lymphocytes in humans. J Immunol 2001;166:6952-6963. (Pubitemid 32467243)
13. Hotchkiss RS, Chang KC, Swanson PE, Tinsley KW, Hui JJ, Klender P, Xanthoudakis S, Roy S, Black C, Grimm E, et al. Caspase inhibitors improve survival in sepsis: a critical role of the lymphocyte. Nat Immunol 2000;1:496-501.
14. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006;124:783-801. (Pubitemid 43261452)
15. Liew FY, Xu D, Brint EK, O'Neill LA. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 2005;5:446-458. (Pubitemid 40835033)
16. Brint EK, Xu D, Liu H, Dunne A, McKenzie AN, O'Neill LA, Liew FY. ST2 is an inhibitor of interleukin 1 receptor and Toll-like receptor 4 signaling and maintains endotoxin tolerance. Nat Immunol 2004;5: 373-379. (Pubitemid 38500085)
17. Wiersinga WJ, van't Veer C, van den Pangaart PS, Dondorp AM, Day NP, Peacock SJ, van der Poll T. Immunosuppression associated with interleukin-1R-associated-kinase-M upregulation predicts mortality in gram-negative sepsis (melioidosis). Crit Care Med 2009;37:569-576.
18. Xu D, Chan WL, Leung BP, Huang F, Wheeler R, Piedrafita D, Robinson JH, Liew FY. Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells. J Exp Med 1998;187:787-794. (Pubitemid 28115194)
19. Moritz DR, Rodewald HR, Gheyselinck J, Klemenz R. The IL-1 receptor-related T1 antigen is expressed on immature and mature mast cells and on fetal blood mast cell progenitors. J Immunol 1998; 161:4866-4874. (Pubitemid 28492065)
20. Cherry WB, Yoon J, Bartemes KR, Iijima K, Kita H. A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J Allergy Clin Immunol 2008;121:1484-1490. (Pubitemid 351787349)
21. Oshikawa K, Yanagisawa K, Tominaga S, Sugiyama Y. ST2 protein induced by inflammatory stimuli can modulate acute lung inflammation. Biochem Biophys Res Commun 2002;299:18-24. (Pubitemid 35366029)
22. Lohning M, Grogan JL, Coyle AJ, Yazdanbakhsh M, Meisel C, Gutierrez-Ramos JC, Radbruch A, Kamradt T. T1/ST2 expression is enhanced on CD4+ T cells from schistosome egg-induced granulomas: analysis of Th cell cytokine coexpression ex vivo. J Immunol 1999;162:3882-3889. (Pubitemid 29314766)
23. Lohning M, Stroehmann A, Coyle AJ, Grogan JL, Lin S, Gutierrez- Ramos JC, Levinson D, Radbruch A, Kamradt T. T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc Natl Acad Sci USA 1998;95:6930-6935. (Pubitemid 28278084)
24. Townsend MJ, Fallon PG, Matthews DJ, Jolin HE, McKenzie AN. T1/ ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J Exp Med 2000;191:1069-1076.
25. Coyle AJ, Lloyd C, Tian J, Nguyen T, Erikkson C, Wang L, Ottoson P, Persson P, Delaney T, Lehar S, et al. Crucial role of the interleukin 1 receptor family member T1/ST2 in T helper cell type 2-mediated lung mucosal immune responses. J Exp Med 1999;190:895-902. (Pubitemid 29480818)
26. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, et al. IL-33, an interleukin-1- like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005;23:479-490. (Pubitemid 41587888)
27. Hoogerwerf J, van der Poll T. Sepsis-induced suppression of lung host defense is mediated by ST2. Presented at Toll 2008. September 24-27, 2008, Lisbon, Portugal.
28. Leendertse M, Willems RJ, Giebelen IA, Florquin S, van den Pangaart PS, Bonten MJ, van der Poll T. Cecal ligation and puncture induced sepsis impairs host defense against Enterococcus faecium peritonitis. Intensive Care Med 2009;35:924-932.
29. Leendertse M, Willems RJ, Oei GA, Florquin S, Bonten MJ, van der Poll T. Intestinal Enterococcus faecium colonization improves host defense during polymicrobial peritonitis. J Infect Dis 2009;200:735-744.
30. Renckens R, van Westerloo DJ, Roelofs JJ, Pater JM, Schultz MJ, Florquin S, van der Poll T. Acute phase response impairs host defense against Pseudomonas aeruginosa pneumonia in mice. Crit Care Med 2008;36:580-587. (Pubitemid 351158636)
31. van Zoelen MA, Florquin S, Meijers JC, de Beer R, de Vos AF, de Boer OJ, van der Poll T. Platelet-activating factor receptor contributes to host defense against Pseudomonas aeruginosa pneumonia but is not essential for the accompanying inflammatory and procoagulant response. J Immunol 2008;180:3357-3365.
32. Knapp S, Wieland CW, van 't Veer C, Takeuchi O, Akira S, Florquin S, van der Poll T. Toll-like receptor 2 plays a role in the early inflammatory response to murine pneumococcal pneumonia but does not contribute to antibacterial defense. J Immunol 2004;172:3132-3138. (Pubitemid 38263703)
33. Leemans JC, Florquin S, Heikens M, Pals ST, van der Neut R, Van Der Poll T. CD44 is a macrophage binding site for Mycobacterium tuberculosis that mediates macrophage recruitment and protective immunity against tuberculosis. J Clin Invest 2003;111:681-689. (Pubitemid 36278586)
34. Ramphal R, Balloy V, Huerre M, Si-Tahar M, Chignard M. TLRs 2 and 4 are not involved in hypersusceptibility to acute Pseudomonas aeruginosa lung infections. J Immunol 2005;175:3927-3934. (Pubitemid 41292053)
35. Skerrett SJ, Wilson CB, Liggitt HD, Hajjar AM. Redundant Toll-like receptor signaling in the pulmonary host response to Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol 2007;292: L312-L322. (Pubitemid 46103456)
36. Liew FY, Pitman NI, McInnes IB. Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol 2010;10:103-110.
37. Carriere V, Roussel L, Ortega N, Lacorre DA, Americh L, Aguilar L, Bouche G, Girard JP. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc Natl Acad Sci USA 2007;104:282-287. (Pubitemid 46068023)
38. Fitting C, Dhawan S, Cavaillon JM. Compartmentalization of tolerance to endotoxin. J Infect Dis 2004;189:1295-1303. (Pubitemid 38457256)
39. Smith PD, Suffredini AF, Allen JB, Wahl LM, Parrillo JE, Wahl SM. Endotoxin administration to humans primes alveolar macrophages for increased production of inflammatory mediators. J Clin Immunol 1994;14:141-148. (Pubitemid 24108801)
40. Lauw FN, ten Hove T, Dekkers PE, de Jonge E, van Deventer SJ, van Der Poll T. Reduced Th1, but not Th2, cytokine production by lymphocytes after in vivo exposure of healthy subjects to endotoxin. Infect Immun 2000;68:1014-1018.
41. Hensler T, Hecker H, Heeg K, Heidecke CD, Bartels H, Barthlen W, Wagner H, Siewert JR, Holzmann B. Distinct mechanisms of immunosuppression as a consequence of major surgery. Infect Immun 1997;65:2283-2291. (Pubitemid 27237311)
42. Meisel C, Bonhagen K, Lohning M, Coyle AJ, Gutierrez-Ramos JC, Radbruch A, Kamradt T. Regulation and function of T1/ST2 expression on CD4+ T cells: induction of type 2 cytokine production by T1/ ST2 cross-linking. J Immunol 2001;166:3143-3150. (Pubitemid 33117311)
43. Brun-Buisson C, Doyon F, Carlet J, Dellamonica P, Gouin F, Lepoutre A, Mercier JC, Offenstadt G, Regnier B. Incidence, risk factors, and outcome of severe sepsis and septic shock in adults. A multicenter prospective study in intensive care units. French ICU Group for Severe Sepsis. JAMA 1995;274:968-974.
44. Seidenfeld JJ, Pohl DF, Bell RC, Harris GD, Johanson WG Jr. Incidence, site, and outcome of infections in patients with the adult respiratory distress syndrome. Am Rev Respir Dis 1986;134:12-16. (Pubitemid 16057452)
45. Niederman MS, Fein AM. Sepsis syndrome, the adult respiratory distress syndrome, and nosocomial pneumonia: a common clinical sequence. Clin Chest Med 1990;11:633-656.
46. Wichterman KA, Baue AE, Chaudry IH. Sepsis and septic shock: a review of laboratory models and a proposal. J Surg Res 1980;29:189-201. (Pubitemid 10039498)
47. Schultz MJ, Knapp S, Florquin S, Pater J, Takeda K, Akira S, van der Poll T. Interleukin-18 impairs the pulmonary host response to Pseudomonas aeruginosa. Infect Immun 2003;71:1630-1634. (Pubitemid 36368690)
48. Granowitz EV, Porat R, Mier JW, Orencole SF, Kaplanski G, Lynch EA, Ye K, Vannier E, Wolff SM, Dinarello CA. Intravenous endotoxin suppresses the cytokine response of peripheral blood mononuclear cells of healthy humans. J Immunol 1993;151:1637-1645. (Pubitemid 23219302)
49. van der Poll T, Coyle SM, Moldawer LL, Lowry SF. Changes in endotoxin-induced cytokine production by whole blood after in vivo exposure of normal humans to endotoxin. J Infect Dis 1996;174:1356-1360. (Pubitemid 26393922)
50. van 't Veer C, van den Pangaart PS, van Zoelen MA, de Kruif M, Birjmohun RS, Stroes ES, de Vos AF, van der Poll T. Induction of IRAK-M is associated with lipopolysaccharide tolerance in a human endotoxemia model. J Immunol 2007;179:7110-7120.
51. Schultz MJ, Rijneveld AW, Speelman P, van Deventer SJ, van der Poll T. Endogenous interferon-gamma impairs bacterial clearance from lungs during Pseudomonas aeruginosa pneumonia. Eur Cytokine Netw 2001;12:39-44. (Pubitemid 32281187)
52. Ostendorf U, Ewig S, Torres A. Nosocomial pneumonia. Curr Opin Infect Dis 2006;19:327-338. (Pubitemid 43982504)
53. Chackerian AA, Oldham ER, Murphy EE, Schmitz J, Pflanz S, Kastelein RA. IL-1 receptor accessory protein and ST2 comprise the IL-33 receptor complex. J Immunol 2007;179:2551-2555.
54. Moussion C, Ortega N, Girard JP. The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel 'alarmin'? PLoS ONE 2008;3:e3331.
55. Alves-Filho JC, Sonego F, Souto FO, Freitas A, Verri WA Jr, Auxiliadora-Martins M, Basile-Filho A, McKenzie AN, Xu D, Cunha FQ, et al. Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat Med 2010;16:708-712.
56. Tominaga S, Kuroiwa K, Tago K, Iwahana H, Yanagisawa K, Komatsu N. Presence and expression of a novel variant form of ST2 gene product in human leukemic cell line UT-7/GM. Biochem Biophys Res Commun 1999;264:14-18. (Pubitemid 29500455)
57. Hayakawa H, Hayakawa M, Kume A, Tominaga S. Soluble ST2 blocks interleukin-33 signaling in allergic airway inflammation. J Biol Chem 2007;282:26369-26380. (Pubitemid 47443815)
58. Tago K, Noda T, Hayakawa M, Iwahana H, Yanagisawa K, Yashiro T, Tominaga S. Tissue distribution and subcellular localization of a variant form of the human ST2 gene product, ST2V. Biochem Biophys Res Commun 2001;285:1377-1383. (Pubitemid 32912936)