Salmonella Enterica infection stimulates macrophages to hemophagocytose

mBio

Volumn 5, Issue 6, 2014, Pages 1-14

  Pilonieta, M Carolina ^a   Moreland, Sarah M ^a,b   English, Christopher N ^a,c   Detweiler, Corrella S ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Intelligent Imaging Innovations Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; LIGAND; LIPOPOLYSACCHARIDE; POLYSTYRENE;

ARTICLE; BACTERIAL INFECTION; BRUCELLA ABORTUS; CELL CULTURE; CONTROLLED STUDY; ERYTHROCYTE; ERYTHROPHAGOCYTOSIS; HUMAN; LEUKOCYTE; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SEROTYPE; TARGET CELL; TYPE III SECRETION SYSTEM; TYPHOID FEVER; ANIMAL; ANIMAL SALMONELLOSIS; CELL LINE; IMMUNOLOGY; LIVER; METABOLISM; PATHOLOGY; PHAGOCYTOSIS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

BACTERIA (MICROORGANISMS); BRUCELLA MELITENSIS BIOVAR ABORTUS; MURINAE; MYCOBACTERIUM TUBERCULOSIS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

ANIMALS; CELL LINE; ERYTHROCYTES; LEUKOCYTES; LIVER; MACROPHAGES; MICE; PHAGOCYTOSIS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM;

EID: 84920992198     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02211-14     Document Type: Article

References (57)

1. Haraga A, Ohlson MB, Miller SI. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:53–66. http://dx.doi.org/10.1038/nrmicro1788.
2. 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.
3. 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.
4. Fisman DN. 2000. Hemophagocytic syndromes and infection. Emerg. Infect. Dis. 6:601–608. http://dx.doi.org/10.3201/eid0606.000608.
5. Osler SW. 1892. The principles and practice of medicine. D. Appleton and Company, New York, NY.
6. Shin BM, Paik IK, Cho HI. 1994. Bone marrow pathology of culture proven typhoid fever. J. Korean Med. Sci. 9:57-63. http://dx.doi.org/10.3346/jkms.1994.9.1.57.
7. 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.
8. 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.
9. Fame TM, Engelhard D, Riley HD. 1986. Hemophagocytosis accompanying typhoid fever. Pediatr. Infect. Dis. 5:367–369. http://dx.doi.org/10.1097/00006454-198605000-00018.
10. Pandey M, Dhingra B, Sharma S, Chandra J, Pemde H, Singh V. 2012. Enteric fever presenting as secondary hemophagocytic lymphohistiocytosis. Indian J. Pediatr. 79:1671–1672. http://dx.doi.org/10.1007/s12098-012-0728-6.
11. Singh ZN, Rakheja D, Yadav TP, Shome DK. 2005. Infection-associated haemophagocytosis: the tropical spectrum. Clin. Lab. Haematol. 27: 312–315. http://dx.doi.org/10.1111/j.1365-2257.2005.00717.x.
12. Nagy TA, Moreland SM, Detweiler CS. 2014. Salmonella acquires ferrous iron from haemophagocytic macrophages. Mol. Microbiol. 93: 1314–1326.
13. Akashi K, Hayashi S, Gondo H, Mizuno S, Harada M, Tamura K, Yamasaki K, Shibuya T, Uike N, Okamura T, et al. 1994. Involvement of interferon-gamma and macrophage colony-stimulating factor in pathogenesis of haemophagocytic lymphohistiocytosis in adults. Br. J. Haematol. 87:243–250. http://dx.doi.org/10.1111/j.1365-2141.1994.tb04905.x.
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. Behrens EM, Canna SW, Slade K, Rao S, Kreiger PA, Paessler M, Kambayashi T, Koretzky GA. 2011. Repeated TLR9 stimulation results in macrophage activation syndrome-like disease in mice. J. Clin. Invest. 121: 2264–2277. http://dx.doi.org/10.1172/JCI43157.
16. Milner JD, Orekov T, Ward JM, Cheng L, Torres-Velez F, Junttila I, Sun G, Buller M, Morris SC, Finkelman FD, Paul WE. 2010. Sustained IL-4 exposure leads to a novel pathway for hemophagocytosis, inflammation, and tissue macrophage accumulation. Blood 116:2476–2483. http://dx.doi.org/10.1182/blood-2009-11-255174.
17. 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.
18. 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.
19. Ginocchio C, Pace J, Galán JE. 1992. Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of salmonellae into cultured epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 89:5976-5980. http://dx.doi.org/10.1073/pnas.89.13.5976.
20. Mallory FB. 1898. A histological study of typhoid fever. J. Exp. Med. 3:611–638. http://dx.doi.org/10.1084/jem.3.6.611.
21. Osler W, McCrae T. 1912. The principles and practice of medicine, 8th ed. D. Appleton and Company, New York, NY.
22. Smith BP, Reina-Guerra M, Hoiseth SK, Stocker BA, Habasha F, Johnson E, Merritt F. 1984. Aromatic-dependent Salmonella typhimurium as modified live vaccines for calves. Am. J. Vet. Res. 45:59–66.
23. Diakonova M, Bokoch G, Swanson JA. 2002. Dynamics of cytoskeletal proteins during Fc_ receptor-mediated phagocytosis in macrophages. Mol. Biol. Cell 13:402–411. http://dx.doi.org/10.1091/mbc.01-05-0273.
24. Roux CM, Butler BP, Chau JY, Paixao TA, Cheung KW, Santos RL, Luckhart S, Tsolis RM. 2010. Both hemolytic anemia and malaria parasite-specific factors increase susceptibility to non-typhoidal Salmonella infection in mice. Infect. Immun. 78:1520–1527. http://dx.doi.org/10.1128/IAI.00887-09.
25. Govoni G, Vidal S, Gauthier S, Skamene E, Malo D, Gros P. 1996. TheBcg/Ity/Lsh locus: genetic transfer of resistance to infections in C57BL/6J mice transgenic for the Nramp1 Gly169 allele. Infect. Immun. 64: 2923–2929.
26. Govoni G, Canonne-Hergaux F, Pfeifer CG, Marcus SL, Mills SD, Hackam DJ, Grinstein S, Malo D, Finlay BB, Gros P. 1999. Functional expression of Nramp1 in vitro in the murine macrophage line RAW264.7. Infect. Immun. 67:2225–2232.
27. Van Zandt KE, Sow FB, Florence WC, Zwilling BS, Satoskar AR, Schlesinger LS, Lafuse WP. 2008. The iron export protein ferroportin 1 is differentially expressed in mouse macrophage populations and is present in the mycobacterial-containing phagosome. J. Leukoc. Biol. 84:689–700. http://dx.doi.org/10.1189/jlb.1107781.
28. Mosser DM. 2003. The many faces of macrophage activation. J. Leukoc. Biol. 73:209–212. http://dx.doi.org/10.1189/jlb.0602325.
29. Vazquez-Torres A, Jones-Carson J, Mastroeni P, Ischiropoulos H, Fang FC. 2000. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J. Exp. Med. 192:227–236. http://dx.doi.org/10.1084/jem.192.2.227.
30. Silva-Herzog E, Detweiler CS. 2010. Salmonella enterica replication in hemophagocytic macrophages requires two type 3 secretion systems. Infect. Immun. 78:3369–3377. http://dx.doi.org/10.1128/IAI.00292-10.
31. Malik-Kale P, Jolly CE, Lathrop S, Winfree S, Luterbach C, Steele- Mortimer O. 2011. Salmonella—at home in the host cell. Front. Microbiol. 2:125. http://dx.doi.org/10.3389/fmicb.2011.00125.
32. Brawn LC, Hayward RD, Koronakis V. 2007. Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe 1:63–75. http://dx.doi.org/10.1016/j.chom.2007.02.001.
33. Galán JE, Ginocchio C, Costeas P. 1992. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J. Bacteriol. 174:4338–4349.
34. Murray RA, Lee CA. 2000. Invasion genes are not required for Salmonella enterica serovar. Typhimurium to breach the intestinal epithelium: evidence that Salmonella pathogenicity island 1 has alternative functions during infection. Infect. Immun. 68:5050-5055. http://dx.doi.org/10.1128/IAI.68.9.5050-5055.2000.
35. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden DW. 1995. Simultaneous identification of bacterial virulence genes by negative selection. Science 269:400–403. http://dx.doi.org/10.1126/science.7618105.
36. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, Leaf IA, Aderem A. 2010. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. U. S. A. 107:3076–3080. http://dx.doi.org/10.1073/pnas.0913087107.
37. Agbor TA, McCormick BA. 2011. Salmonella effectors: important players modulating host cell function during infection. Cell. Microbiol. 13: 1858–1869. http://dx.doi.org/10.1111/j.1462-5822.2011.01701.x.
38. Monack DM, Bouley DM, Falkow S. 2004. Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1_/_ mice and can be reactivated by IFNgamma neutralization. J. Exp. Med. 199:231–241. http://dx.doi.org/10.1084/jem.20031319.
39. Richter-Dahlfors A, Buchan AM, Finlay BB. 1997. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186:569-580. http://dx.doi.org/10.1084/jem.186.4.569.
40. Sheppard M, Webb C, Heath F, Mallows V, Emilianus R, Maskell D, Mastroeni P. 2003. Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell. Microbiol. 5:593–600. http://dx.doi.org/10.1046/j.1462-5822.2003.00296.x.
41. Ibarra JA, Steele-Mortimer O. 2009. Salmonella—the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell. Microbiol. 11:1579-1586. http://dx.doi.org/10.1111/j.1462-5822.2009.01368.x.
42. Zuckerman SH, Evans GF, Snyder YM, Roeder WD. 1989. Endotoxinmacrophage interaction: post-translational regulation of tumor necrosis factor expression. J. Immunol. 143:1223–1227.
43. Brown DE, Libby SJ, Moreland SM, McCoy MW, Brabb T, Stepanek A, Fang FC, Detweiler CS. 2013. Salmonella enterica causes more severe inflammatory disease in C57/BL6 Nramp1G169 mice than Sv129S6 mice. Vet. Pathol. 50:867–876. http://dx.doi.org/10.1177/0300985813478213.
44. Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ. 2002. Typhoid fever. N. Engl. J. Med. 347:1770-1782. http://dx.doi.org/10.1056/NEJMra020201.
45. Moldawer LL, Sherry B, Lowry SF, Cerami A. 1989. Endogenous cachectin/tumour necrosis factor-alpha production contributes to experimental cancer-associated cachexia. Cancer Surv. 8:853–859.
46. Libregts SF, Gutiérrez L, de Bruin AM, Wensveen FM, Papadopoulos P, van Ijcken W, Ozgür Z, Philipsen S, Nolte MA. 2011. Chronic IFN-_ production in mice induces anemia by reducing erythrocyte life span and inhibiting erythropoiesis through an IRF-1/PU.1 axis. Blood 118: 2578–2588. http://dx.doi.org/10.1182/blood-2010-10-315218.
47. Cunnington AJ, de Souza JB, Walther M, Riley EM. 2012. Malaria impairs resistance to Salmonella through heme- and heme oxygenasedependent dysfunctional granulocyte mobilization. Nat. Med. 18: 120–127. http://dx.doi.org/10.1038/nm.260.1.
48. Canna SW, Wrobel J, Chu N, Kreiger PA, Paessler M, Behrens EM. 2013. Interferon-_ 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.
49. Eisele NA, Ruby T, Jacobson A, Manzanillo PS, Cox JS, Lam L, Mukundan L, Chawla A, Monack DM. 2013. Salmonella require the fatty acid regulator PPAR_ for the establishment of a metabolic environment essential for long-term persistence. Cell Host Microbe 14:171–182. http://dx.doi.org/10.1016/j.chom.2013.07.010.
50. Mehta A, Brewington R, Chatterji M, Zoubine M, Kinasewitz GT, Peer GT, Chang AC, Taylor FB, Shnyra A. 2004. Infection-induced modulation of m1 and m2 phenotypes in circulating monocytes: role in immune monitoring and early prognosis of sepsis. Shock 22:423-430. http://dx.doi.org/10.1097/01.shk.0000142184.49976.0c.
51. Pilonieta MC, Erickson KD, Ernst RK, Detweiler CS. 2009. A protein important for antimicrobial peptide resistance, YdeI/OmdA, is in the periplasm and interacts with OmpD/NmpC. J. Bacteriol. 191:7243–7252. http://dx.doi.org/10.1128/JB.00688-09.
52. Schechter LM, Damrauer SM, Lee CA. 1999. Two AraC/XylS family members can independently counteract the effect of repressing sequences upstream of the hilA promoter. Mol. Microbiol. 32:629-642. http://dx.doi.org/10.1046/j.1365-2958.1999.01381.x.
53. Lee CA, Falkow S. 1990. The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc. Natl. Acad. Sci. U. S. A. 87:4304–4308. http://dx.doi.org/10.1073/pnas.87.11.4304.
54. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS. 2012. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11:469–480. http://dx.doi.org/10.1016/j.chom.2012.03.007.
55. Neidhardt FC, Ingraham JL, Schaechter M. 1990. Physiology of the bacterial cell: a molecular approach. Sinauer Associates, Sunderland, MA.
56. Gmeiner J, Schlecht S. 1979. Molecular organization of the outer membrane of Salmonella typhimurium. Eur. J. Biochem. 93:609–620. http://dx.doi.org/10.1111/j.1432-1033.1979.tb12861.x.
57. Bossuyt X, Marti GE, Fleisher TA. 1997. Comparative analysis of whole blood lysis methods for flow cytometry. Cytometry 30:124–133. http://dx.doi.org/10.1002/(SICI)1097-0320(19970615)30:3_124::AID-CYTO3_30CO;2-L.