Bacterial stimulation of Toll-like receptor 4 drives macrophages to hemophagocytose

Infection and Immunity

Volumn 84, Issue 1, 2015, Pages 47-55

  McDonald, Erin M ^a   Carolina Pilonieta, M ^a   Nick, Heidi J ^a   Detweiler, Corrella S ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIUM LIPOPOLYSACCHARIDE; DEOXYCYTIDINE; GAMMA INTERFERON; LIPOTEICHOIC ACID; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; TEICHOIC ACID; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TLR9 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; ERYTHROPHAGOCYTOSIS; GENE DELETION; INNATE IMMUNITY; LONG TERM EXPOSURE; MACROPHAGE; MOUSE; MYCOBACTERIUM MARINUM; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; 3T3 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; C3H MOUSE; CELL LINE; ERYTHROCYTE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PHAGOCYTOSIS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

3T3 CELLS; ANIMALS; BACILLUS SUBTILIS; CELL LINE; ERYTHROCYTES; INTERFERON-GAMMA; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; MYCOBACTERIUM MARINUM; NF-KAPPA B; PHAGOCYTOSIS; SALMONELLA TYPHIMURIUM; TEICHOIC ACIDS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 9;

EID: 84957690278     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/iai.01149-15     Document Type: Article

References (60)

1. Schafer JF. 1971. Tolerance to plant disease. Annu Rev Phytopathol 9:235-252.
2. Caldwell RM, Schafer JF, Compton LE, Patterson FL. 1958. Tolerance to cereal leaf rusts. Science 128:714-715. http://dx.doi.org/10.1126/science.128.3326.714.
3. Ayres JS, Schneider DS. 2012. Tolerance of infections. Annu Rev Immunol 30:271-294. http://dx.doi.org/10.1146/annurev-immunol-020711-075030.
4. Koh TJ, Di Pietro LA. 2011. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med 13:e23. http://dx.doi.org/10.1017/S1462399411001943.
5. Cohen HB, Briggs KT, Marino JP, Ravid K, Robson SC, Mosser DM. 2013 TLR stimulation initiates a CD39-based autoregulatory mechanism that limits macrophage inflammatory responses. Blood 122:1935-1945. http://dx.doi.org/10.1182/blood-2013-04-496216.
6. Liu G, Friggeri A, Yang Y, Park Y-J, Tsuruta Y, Abraham E. 2009. miR-147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc Natl Acad Sci U S A 106: 15819-15824. http://dx.doi.org/10.1073/pnas.0901216106.
7. Brisse E, Wouters CH, Matthys P. 2014. Hemophagocytic lymphohistiocytosis (HLH): a heterogeneous spectrum of cytokine-driven immune disorders. Cytokine Growth Factor Rev 26:263-280. http://dx.doi.org/10.1016/j.cytogfr.2014.10.001.
8. Castillo L, Carcillo J. 2009. Secondary hemophagocytic lymphohistiocytosis and severe sepsis/systemic inflammatory response syndrome/multiorgan dysfunction syndrome/macrophage activation syndrome share common intermediate phenotypes on a spectrum of inflammation. Pediatr Crit Care Med 10:387-392. http://dx.doi.org/10.1097/PCC.0b013e3181a1ae08.
9. Mallory FB. 1898. A histological study of typhoid fever. J Exp Med 3:611-638.
10. Osler SW. 1892. The principles and practice of medicine. D. Appleton and Company, New York, NY.
11. Henter J-I, Horne A, Aricó M, Egeler RM, Filipovich AH, Imashuku S, Ladisch S, McClain K, Webb D, Winiarski J, Janka G. 2007. HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 48:124-131. http://dx.doi.org/10.1002/pbc.21039.
12. Jordan MB, Hildeman D, Kappler J, Marrack P. 2004. An animal model of hemophagocytic lymphohistiocytosis (HLH): CD8+ T cells and interferon gamma are essential for the disorder. Blood 104:735-743. http://dx.doi.org/10.1182/blood-2003-10-3413.
13. Pachlopnik Schmid J, Ho C-H, Chrétien F, Lefebvre JM, Pivert G, Kosco-Vilbois M, Ferlin W, Geissmann F, Fischer A, de Saint Basile G. 2009 Neutralization of IFNγ defeats haemophagocytosis in LCMVinfected perforin-and Rab27a-deficient mice. EMBO Mol Med 1:112-124 http://dx.doi.org/10.1002/emmm.200900009.
14. Zoller EE, Lykens JE, Terrell CE, Aliberti J, Filipovich AH, Henson PM, Jordan MB. 2011. Hemophagocytosis causes a consumptive anemia of inflammation. J Exp Med 208:1203-1214. http://dx.doi.org/10.1084/jem.20102538.
15. Canna SW, Behrens EM. 2012. Not all hemophagocytes are created equally: appreciating the heterogeneity of the hemophagocytic syndromes. Curr Opin Rheumatol 24:113-118. http://dx.doi.org/10.1097/BOR.0b013e32834dd37e.
16. Brown GC, Neher JJ. 2012. Eaten alive! Cell death by primary phagocytosis: "phagoptosis." Trends Biochem Sci 37:325-332. http://dx.doi.org/10.1016/j.tibs.2012.05.002.
17. Cnops J, De Trez C, Stijlemans B, Keirsse J, Kauffmann F, Barkhuizen M, Keeton R, Boon L, Brombacher F, Magez S. 2015. NK-, NKT-, and CD8-derived IFN-γ drives myeloid cell activation and erythrophagocytosis, resulting in trypanosomosis-associated acute anemia. PLoS Pathog 11:e1004964. http://dx.doi.org/10.1371/journal.ppat.1004964.
18. Brown DE, McCoy MW, Pilonieta MC, Nix RN, Detweiler CS. 2010. Chronic murine typhoid fever is a natural model of secondary hemophagocytic lymphohistiocytosis. PLoS One 5:e9441. http://dx.doi.org/10.1371/journal.pone.0009441.
19. Tsolis RM, Xavier MN, Santos RL, Bäumler AJ. 2011. How to become a top model: impact of animal experimentation on human Salmonella disease research. Infect Immun 79:1806-1814. http://dx.doi.org/10.1128/IAI.01369-10.
20. Nix RN, Altschuler SE, Henson PM, Detweiler CS. 2007. Hemophagocytic macrophages harbor Salmonella enterica during persistent infection. PLoS Pathog 3:e193. http://dx.doi.org/10.1371/journal.ppat.0030193.
21. McCoy MW, Moreland SM, Detweiler CS. 2012. Hemophagocytic macrophages in murine typhoid fever have an anti-inflammatory phenotype. Infect Immun 80:3642-3649. http://dx.doi.org/10.1128/IAI.00656-12.
22. Ruby T, McLaughlin L, Gopinath S, Monack D. 2012. Salmonella's long-term relationship with its host. FEMS Microbiol Rev 36:600-615. http://dx.doi.org/10.1111/j.1574-6976.2012.00332.x.
23. Nagy TA, Moreland SM, Detweiler CS. 2014. Salmonella acquires ferrous iron from haemophagocytic macrophages. Mol Microbiol 93:1314-1326 http://dx.doi.org/10.1111/mmi.12739.
24. Canna SW, Costa-Reis P, Bernal WE, Chu N, Sullivan KE, Paessler ME, Behrens EM. 2014. Brief report: alternative activation of laser-captured murine hemophagocytes. Arthritis Rheumatol 66:1666-1671. http://dx.doi.org/10.1002/art.38379.
25. Benoit M, Desnues B, Mege J-L. 2008. Macrophage polarization in bacterial infections. J Immunol 181:3733-3739.
26. Pilonieta MC, Moreland SM, English CN, Detweiler CS. 2014. Salmonella enterica infection stimulates macrophages to hemophagocytose. mBio 5:e02211. http://dx.doi.org/10.1128/mBio.02211-14.
27. Barat S, Willer Y, Rizos K, Claudi B, Mazé A, Schemmer AK, Kirchhoff D, Schmidt A, Burton N, Bumann D. 2012. Immunity to intracellular Salmonella depends on surface-associated antigens. PLoS Pathog 8:e1002966. http://dx.doi.org/10.1371/journal.ppat.1002966.
28. Grabenstein JP, Marceau M, Pujol C, Simonet M, Bliska JB. 2004. The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect Immun 72:4973-4984 http://dx.doi.org/10.1128/IAI.72.9.4973-4984.2004.
29. Silva-Herzog E, Detweiler CS. 2010. Salmonella enterica replication in hemophagocytic macrophages requires two type three secretion systems. Infect Immun 78:3369-3377. http://dx.doi.org/10.1128/IAI.00292-10.
30. Fisman DN. 2000. Hemophagocytic syndromes and infection. Emerg Infect Dis 6:601-608. http://dx.doi.org/10.3201/eid0606.000608.
31. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. 1999. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162:3749-3752.
32. Arpaia N, Godec J, Lau L, Sivick KE, McLaughlin LM, Jones MB, Dracheva T, Peterson SN, Monack DM, Barton GM. 2011. TLR signaling is required for Salmonella typhimurium virulence. Cell 144:675-688. http://dx.doi.org/10.1016/j.cell.2011.01.031.
33. Józefowski S, Sulahian TH, Arredouani M, Kobzik L. 2006. Role of scavenger receptor MARCO in macrophage responses to CpG oligodeoxynucleotides. J Leukoc Biol 80:870-879. http://dx.doi.org/10.1189/jlb.0705357.
34. Hong SW, Baik JE, Kang S-S, Yun C-H, Seo D-G, Han SH. 2014. Lipoteichoic acid of Streptococcus mutans interacts with Toll-like receptor 2 through the lipid moiety for induction of inflammatory mediators in murine macrophages. Mol Immunol 57:284-291. http://dx.doi.org/10.1016/j.molimm.2013.10.004.
35. Sheikh F, Dickensheets H, Gamero AM, Vogel SN, Donnelly RP. 2014. An essential role for IFN-β in the induction of IFN-stimulated gene expression by LPS in macrophages. J Leukoc Biol 96:591-600. http://dx.doi.org/10.1189/jlb.2A0414-191R.
36. Yang H-T, Papoutsopoulou S, Belich M, Brender C, Janzen J, Gantke T, Handley M, Ley SC. 2012. Coordinate regulation of TPL-2 and NF-κB signaling in macrophages by NF-κB1 p105. Mol Cell Biol 32:3438-3451. http://dx.doi.org/10.1128/MCB.00564-12.
37. Feuillet V, Medjane S, Mondor I, Demaria O, Pagni PP, Galán JE, Flavell RA, Alexopoulou L. 2006. Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc Natl Acad Sci U S A 103: 12487-12492. http://dx.doi.org/10.1073/pnas.0605200103.
38. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. 2001. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413:732-738. http://dx.doi.org/10.1038/35099560.
39. Spiller S, Elson G, Ferstl R, Dreher S, Mueller T, Freudenberg M, Daubeuf B, Wagner H, Kirschning CJ. 2008. TLR4-induced IFNgamma production increases TLR2 sensitivity and drives Gramnegative sepsis in mice. J Exp Med 205:1747-1754. http://dx.doi.org/10.1084/jem.20071990.
40. Matsunaga N, Tsuchimori N, Matsumoto T, Ii M. 2011. TAK-242 (resatorvid), a small-molecule inhibitor of Toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules. Mol Pharmacol 79:34-41. http://dx.doi.org/10.1124/mol.110.068064.
41. Burke JR, Pattoli MA, Gregor KR, Brassil PJ, MacMaster JF, McIntyre KW, Yang X, Iotzova VS, Clarke W, Strnad J, Qiu Y, Zusi FC. 2003 BMS-345541 is a highly selective inhibitor of IκB kinase that binds at an allosteric site of the enzyme and blocks NF-κB-dependent transcription in mice. J Biol Chem 278:1450-1456. http://dx.doi.org/10.1074/jbc.M209677200.
42. Schroder K, Hertzog PJ, Ravasi T, Hume DA. 2004. Interferongamma: an overview of signals, mechanisms, and functions. J Leukoc Biol 75:163-189.
43. Jiang Z, Mak TW, Sen G, Li X. 2004. Toll-like receptor 3-mediated activation of NF-κB and IRF3 diverges at Toll-IL-1 receptor domaincontaining adapter inducing IFN-β. Proc Natl Acad Sci U S A 101:3533-3538 http://dx.doi.org/10.1073/pnas.0308496101.
44. Gardella S, Andrei C, Ferrera D, Lotti LV, Torrisi MR, Bianchi ME, Rubartelli A. 2002. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 3:995-1001. http://dx.doi.org/10.1093/embo-reports/kvf198.
45. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ. 1999. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285:248-251. http://dx.doi.org/10.1126/science.285.5425.248.
46. Youn JH, Kwak MS, Wu J, Kim ES, Ji Y, Min HJ, Yoo J-H, Choi JE, Cho H-S, Shin J-S. 2011. Identification of lipopolysaccharide-binding peptide regions within HMGB1 and their effects on subclinical endotoxemia in a mouse model. Eur J Immunol 41:2753-2762. http://dx.doi.org/10.1002/eji.201141391.
47. Bode KA, Schmitz F, Vargas L, Heeg K, Dalpke AH. 2009. Kinetic of RelA activation controls magnitude of TLR-mediated IL-12p40 induction. J Immunol 182:2176-2184.
48. Zhou R, Hu G, Liu J, Gong A-Y, Drescher KM, Chen X-M. 2009. NF-κB p65-dependent transactivation of miRNA genes following Cryptosporidium parvum infection stimulates epithelial cell immune responses. PLoS Pathog 5:e1000681. http://dx.doi.org/10.1371/journal.ppat.1000681.
49. Ohyagi H, Onai N, Sato T, Yotsumoto S, Liu J, Akiba H, Yagita H, Atarashi K, Honda K, Roers A, Müller W, Kurabayashi K, Hosoi-Amaike M, Takahashi N, Hirokawa M, Matsushima K, Sawada K, Ohteki T. 2013. Monocyte-derived dendritic cells perform hemophagocytosis to fine-tune excessive immune responses. Immunity 39:584-598. http://dx.doi.org/10.1016/j.immuni.2013.06.019.
50. Gardenghi S, Renaud TM, Meloni A, Casu C, Crielaard BJ, Bystrom LM, Greenberg-Kushnir N, Sasu BJ, Cooke KS, Rivella S. 2014. Distinct roles for hepcidin and interleukin-6 in the recovery from anemia in mice injected with heat-killed Brucella abortus. Blood 123:1137-1145. http://dx.doi.org/10.1182/blood-2013-08-521625.
51. Canna SW, Wrobel J, Chu N, Kreiger PA, Paessler M, Behrens EM. 2013 Interferon-γ mediates anemia but is dispensable for fulminant Tolllike receptor 9-induced macrophage activation syndrome and hemophagocytosis. Arthritis Rheum 65:1764-1775. http://dx.doi.org/10.1002/art.37958.
52. Costelloe EO, Stacey KJ, Antalis TM, Hume DA. 1999. Regulation of the plasminogen activator inhibitor-2 (PAI-2) gene in murine macrophages: demonstration of a novel pattern of responsiveness to bacterial endotoxin. J Leukoc Biol 66:172-182.
53. Schroder K, Sweet MJ, Hume DA. 2006. Signal integration between IFNγ and TLR signaling pathways in macrophages. Immunobiology 211:511-524 http://dx.doi.org/10.1016/j.imbio.2006.05.007.
54. Ellis TN, Beaman BL. 2004. Interferon-gamma activation of polymorphonuclear neutrophil function. Immunology 112:2-12. http://dx.doi.org/10.1111/j.1365-2567.2004.01849.x.
55. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. 2012. Neutrophil function: from mechanisms to disease. Annu Rev Immunol 30:459-489. http://dx.doi.org/10.1146/annurev-immunol-020711-074942.
56. Schaefer L. 2014. Complexity of danger: the diverse nature of damageassociated molecular patterns. J Biol Chem 289:35237-35245. http://dx.doi.org/10.1074/jbc.R114.619304.
57. MacWilliams C, Johnson G, Groman D, Kibenge FSB. 2007. Morphologic description of infectious salmon anaemia virus (ISAV)-induced lesions in rainbow trout Oncorhynchus mykiss compared to Atlantic salmon Salmo salar. Dis Aquat Organ 78:1-12. http://dx.doi.org/10.3354/dao01866.
58. Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958-969. http://dx.doi.org/10.1038/nri2448.
59. Bessede A, Gargaro M, Pallotta MT, Matino D, Servillo G, Brunacci C, Bicciato S, Mazza EMC, Macchiarulo A, Vacca C, Iannitti R, Tissi L, Volpi C, Belladonna ML, Orabona C, Bianchi R, Lanz TV, Platten M, Fazia Della MA, Piobbico D, Zelante T, Funakoshi H, Nakamura T, Gilot D, Denison MS, Guillemin GJ, Du Hadaway JB, Prendergast GC, Metz R, Geffard M, Boon L, Pirro M, Iorio A, Veyret B, Romani L, Grohmann U, Fallarino F, Puccetti P. 2014. Aryl hydrocarbon receptor control of a disease tolerance defence pathway. Nature 511: 184-190. http://dx.doi.org/10.1038/nature13323.
60. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6:422-428. http://dx.doi.org/10.1038/74680.