Synergistic inflammation is induced by blood degradation products with microbial Toll-like receptor agonists and is blocked by hemopexin

Journal of Infectious Diseases

Volumn 202, Issue 4, 2010, Pages 624-632

  Lin, Tian ^a   Kwak, Young Ho ^a   Sammy, Fatima ^a   He, Ping ^a   Thundivalappil, Sujatha ^a   Sun, Guangjie ^a   Chao, Wei ^a   Warren, H Shaw ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEME; HEMOGLOBIN; HEMOPEXIN; INTERLEUKIN 6; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR;

ARTICLE; BLOOD; BLOOD SAMPLING; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRADATION; ERYTHROCYTE; ESCHERICHIA COLI; HUMAN; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIAL TOXINS; BLOOD; CELLS, CULTURED; CYTOKINES; ESCHERICHIA COLI; HEME; HEMOGLOBINS; HEMOPEXIN; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; STAPHYLOCOCCUS AUREUS; TOLL-LIKE RECEPTORS;

EID: 77954699484     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/654929     Document Type: Article

References (49)

1. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001; 2:675-680 (Pubitemid 32747155)
2. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124:783-801.
3. Bone RC, Balk RA, Cerra FB, et al. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 1992; 101: 1644-1655
4. Rittirsch D, Flierl MA, Ward PA. Harmful molecular mechanisms in sepsis. Nat Rev Immunol 2008; 8:776-787
5. Lombardi V, Van Overtvelt L, Horiot S, Moingeon P. Human dendritic cells stimulated via TLR7 and/or TLR8 induce the sequential production of Il-10, IFN-g, and IL-17A by naive CD4+ T cells. J Immunol 2009; 182:3372-3379
6. Strandskog G, Skjaeveland I, Ellingsen T, Jorgensen JB. Double-stranded RNA-and CpG DNA-induced immune responses in Atlantic salmon: comparison and synergies. Vaccine 2008; 26:4704-4715
7. Vanhoutte F, Paget C, Breuilh L, et al. Toll-like receptor (TLR)2 and TLR3 synergy and cross-inhibition in murine myeloid dendritic cells. Immunol Lett 2008; 116:86-94.
8. He H, Genovese KJ, Nisbet DJ, Kogut MH. Synergy of CpG oligodeoxynucleotide and double-stranded RNA (poly I:C) on nitric oxide induction in chicken peripheral blood monocytes. Mol Immunol 2007; 44:3234-3242
9. Roelofs MF, Joosten LA, Abdollahi-Roodsaz S, et al. The expression of toll-like receptors 3 and 7 in rheumatoid arthritis synovium is increased and costimulation of Toll-like receptors 3, 4, and 7/8 results in synergistic cytokine production by dendritic cells. Arthritis Rheum 2005; 52:2313-2322
10. Napolitani G, Rinaldi A, Bertoni F, Sallusto F, Lanzavecchia A. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 2005; 6: 769-776
11. Bagchi A, Herrup EA,Warren HS et al. MyD88-dependent andMyD88-independent pathways in synergy, priming, and tolerance between TLR agonists. J Immunol 2007; 178:1164-1171
12. Paul-Clark MJ, Sorrentino R, Bailey LK, Sriskandan S, Mitchell JA. Gram-positive and gram-negative bacteria synergize with oxidants to release CXCL8 from innate immune cells. Mol Med 2008; 14:238-246
13. Tsujimoto H, Ono S, Efron PA, Scumpia PO, Moldawer LL,Mochizuki H. Role of Toll-like receptors in the development of sepsis. Shock 2008; 29:315-321
14. Bornside GH, Bouis PJ Jr, Cohn I Jr. Hemoglobin and Escherichia coli, a lethal intraperitoneal combination. J Bacteriol 1968; 95:1567-1571
15. Roth RI, Levin FC, Levin J. Distribution of bacterial endotoxin in human and rabbit blood and effects of stroma-free hemoglobin. Infect Immun 1993; 61:3209-3215
16. Su D, Roth RI, Yoshida M, Levin J. Hemoglobin increases mortality from bacterial endotoxin. Infect Immun 1997; 65:1258-1266
17. Su D, Roth RI, Levin J. Hemoglobin infusion augments the tumor necrosis factor response to bacterial endotoxin (lipopolysaccharide) in mice. Crit Care Med 1999; 27:771-778
18. Bodet C, Chandad F, Grenier D. Hemoglobin and LPS act in synergy to amplify the inflammatory response. J Dent Res 2007; 86:878-882
19. Kaca W, Roth RI, Levin J. Hemoglobin, a newly recognized lipopolysaccharide (LPS)-binding protein that enhances LPS biological activity. J Biol Chem 1994; 269:25078-25084
20. Brandenburg K, Garidel P, Andra J, et al. Cross-linked hemoglobin converts endotoxically inactive pentaacyl endotoxins into a physiologically active conformation. J Biol Chem 2003; 278:47660-47669
21. Bornside GH, Bouis PJ Jr, Cohn I Jr. Enhancement of Escherichia coli infection and endotoxic activity by hemoglobin and ferric ammonium citrate. Surgery 1970; 68:350-355
22. Su D, Roth RI, Levin J. Hemoglobin infusion augments the tumor necrosis factor response to bacterial endotoxin (lipopolysaccharide) in mice. Crit Care Med 1999; 27:771-778
23. Warren HS, Fitting C, Hoff E, et al. Resilience to bacterial infection: difference between species could be due to proteins in serum. J Infect Dis 2010; 201:223-232
24. Figueiredo RT, Fernandez PL, Mourao-Sa DS, et al. Characterization of heme as activator of Toll-like receptor 4. J Biol Chem 2007; 282:20221-20229
25. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 1999; 11:115-122
26. Andrade CT, Barros LA, Lima MC, Azero EG. Purification and characterization of human hemoglobin: effect of the hemolysis conditions. Int J Biol Macromol 2004; 34:233-240
27. Liang X, Lin T, Sun G, Beasley-Topliffe L, Cavaillon JM, Warren HS. Hemopexin down-regulates LPS-induced proinflammatory cytokines from macrophages. J Leukoc Biol 2009; 86:229-235
28. Novitsky TJ, Roslansky PF, Siber GR, Warren HS. Turbidometric method for quantifying serum inhibition of limulus amoebocyte lysate response. J Clin Micro 1985; 20:211-216
29. Schilling D, Thomas K, Nixdorff K, Vogel SN, Fenton MJ. Toll-like receptor 4 and Toll-IL-1 receptor domain-containing adapter protein (TIRAP)/myeloid differentiation protein 88 adapter-like (Mal) contribute to maximal IL-6 expression in macrophages. J Immunol 2002; 169: 5874-5880
30. Liang MD, Bagchi A, Warren HS et al. Bacterial peptidoglycan-associated lipoprotein: a naturally occurring Toll-like receptor 2 agonist that is shed into serum and has synergy with lipopolysaccharide. J Infect Dis 2005; 191:939-948
31. Yang H, Wang H, Bernik TR, et al. Globin attenuates the innate immune response to endotoxin. Shock 2002; 17:485-490
32. Tolosano E, Altruda F. Hemopexin: structure, function, and regulation. DNA Cell Biol 2002; 21:297-306.
33. Paoli M, Anderson BF, Baker HM, Morgan WT, Smith A, Baker EN. Crystal structure of hemopexin reveals a novel high-affinity heme site formed between two beta-propeller domains. Nat Struct Biol 1999; 6: 926-931
34. Watanabe J, Grijalva V, Hama S, et al. Hemoglobin and its scavenger protein haptoglobin associate with ApoA-1-containing particles and influence the inflammatory properties and function of high density lipoprotein. J Biol Chem 2009; 284:18292-18301
35. Wilson BMG, Severn A, Rapson NT, Chana J, Hopkins P. A convenient human whole blood culture system for studying the regulation of tumour necrosis factor release by bacterial lipopolysaccharide. J Immunol Methods 1991; 139:233-240
36. Cox KH, Ofek I, and Hasty DL. Enhancement of macrophage stimulation by lipoteichoic acid and the costimulant hemoglobin is dependent on Toll-like receptors 2 and 4. Infect Immun 2007; 75:2638-2641
37. Tanabe S, Gottschalk M, Grenier D. Hemoglobin and Streptococcus suis cell wall act in synergy to potentiate the inflammatory response of monocyte-derived macrophages. Innate Immun 2008; 14:357-363
38. Takeda K, Akira S. Toll-like receptors (chapter 14). In: Coligan JE, et al. (eds). Current Protocols in Immunology 2007:unit 14.12.
39. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol 2005; 17:1-14.
40. Crowley JP, Metzger J, Gray A, Pivacek LE, Cassidy G, Valeri CR. Infusion of stroma-free cross-linked hemoglobin during acute gramnegative bacteremia. Circ Shock 1993; 41:144-149
41. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001; 2:907-916
42. Schaer DJ, Alayash AI, Buehler PW. Gating the radical hemoglobin to macrophages: the anti-inflammatory role of CD163, a scavenger receptor. Antioxid Redox Signal 2007; 9:991-999
43. Polticelli F, Bocedi A, Minervini G, Ascenzi P. Human haptoglobin structure and function-a molecular modelling study. FEBS J 2008; 275:5648-5656
44. Hrkal Z, Vodrazka Z, Kalousek I. Transfer of heme from ferrihemoglobin and ferrihemoglobin isolated chains to hemopexin. Eur J Biochem 1974; 43:73-78
45. Chung SW, Liu X, Macias AA, Baron RM, Perrella MA. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. J Clin Invest 2008; 118:239-247
46. Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 2003; 24:449-455
47. Pamplona A, Ferreira A, Balla J, et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 2007; 13:703-710
48. Warren HS. Editorial: Mouse models to study sepsis syndrome in humans. J Leukoc Biol 2009; 86:199-201.
49. Perez-Padilla R, Rosa-Zamboni D, Ponce dL, et al. Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. N Engl J Med 2009; 361:680-689