IFN-alpha receptor deficiency enhances host resistance to oral Salmonella enterica serovar Typhimurium infection during murine pregnancy.
Salmonella
cell death
cytokines
oral infection
pregnancy
type I interferon
Journal
American journal of reproductive immunology (New York, N.Y. : 1989)
ISSN: 1600-0897
Titre abrégé: Am J Reprod Immunol
Pays: Denmark
ID NLM: 8912860
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
09
05
2021
received:
01
03
2021
accepted:
10
05
2021
pubmed:
16
5
2021
medline:
26
2
2022
entrez:
15
5
2021
Statut:
ppublish
Résumé
Maternal tolerance during pregnancy increases the risk of infection with certain intracellular pathogens. Systemic Salmonella enterica serovar Typhimurium (S.Tm) infection during pregnancy in normally resistant 129X1/SvJ mice leads to severe placental infection, as well as fetal and maternal deaths. However, the effect of oral infection with S.Tm in pregnant mice and the roles of infection-induced inflammation and cell death pathways in contributing to susceptibility to infection are unclear. Non-pregnant and pregnant C57BL/6J wild-type (WT) and cell death pathway-altered mice (IFNAR1 Oral infection of WT mice with S.Tm on days 9-10 of gestation resulted in systemic dissemination of the bacteria, substantial placental colonization, and fetal loss 5 days post-infection. Histopathological examination of the placentas indicated that infection-induced widespread focal necrosis and neutrophil infiltration throughout the spongiotrophoblast (SpT) layer. In the non-pregnant state, IFNAR1 Oral S.Tm exposure leads to placental infection, inflammation, and resorption, whereas IFNAR1 deficiency enhances host resistance both in the non-pregnant and pregnant states.
Substances chimiques
Cytokines
0
Receptor, Interferon alpha-beta
156986-95-7
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13454Subventions
Organisme : NIH HHS
ID : 1R01AI101049-01
Pays : United States
Informations de copyright
© 2021 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Ohl ME, Miller SI. Salmonella: a model for bacterial pathogenesis. Annu Rev Med. 2001;52:259-274.
Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ. 2004;82(5):346-353.
Buckle GC, Walker CLF, Black RE. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J Glob Health. 2012;2(1):10401.
Crum-Cianflone NF. Salmonellosis and the gastrointestinal tract: more than just peanut butter. Curr Gastroenterol Rep. 2008;10(4):424-431.
Saleh S, Van Puyvelde S, Staes A, et al. Salmonella Typhi, Paratyphi A, Enteritidis and Typhimurium core proteomes reveal differentially expressed proteins linked to the cell surface and pathogenicity. PLoS Negl Trop Dis. 2019;13(5):e0007416.
Majowicz SE, Musto J, Scallan E, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010;50(6):882-889.
Stanaway JD, Parisi A, Sarkar K, et al. The global burden of non-typhoidal Salmonella invasive disease: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis. 2019;19(12):1312-1324.
Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Bäumler AJ. Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect. 2001;3(14-15):1335-1344.
Mastroeni P, Grant A, Restif O, Maskell D. A dynamic view of the spread and intracellular distribution of Salmonella enterica. Nat Rev Microbiol. 2009;7(1):73-80.
Bravo-Blas A, Utriainen L, Clay SL, Kästele V, Cerovic V, Cunningham AF, et al. Salmonella enterica Serovar Typhimurium travels to mesenteric lymph nodes both with host cells and autonomously. J Immunol. 2019;202(1):260-267.
Voedisch S, Koenecke C, David S, et al. Mesenteric lymph nodes confine dendritic cell-mediated dissemination of Salmonella enterica serovar Typhimurium and limit systemic disease in mice. Infect Immun. 2009;77(8):3170-3180.
Vazquez-Torres A, Jones-Carson J, Bäumler AJ, et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature. 1999;401(6755):804-808.
Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001;2(4):361-367.
Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 2001;204(5):572-581.
Rescigno M, Borrow P. The host-pathogen interaction: new themes from dendritic cell biology. Cell. 2001;106(3):267-270.
Alpuche-Aranda CM, Racoosin EL, Swanson JA, Miller SI. Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J Exp Med. 1994;179(2):601-608.
Miao EA, Leaf IA, Treuting PM, et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol. 2010;11(12):1136-1142.
Sansonetti PJ. War and peace at mucosal surfaces. Nat Rev Immunol. 2004;4(12):953-964.
Bohnhoff M, Drake BL, Miller CP. Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection. Proc Soc Exp Biol Med. 1954;86(1):132-137.
Bohnhoff M, Miller CP. Enhanced susceptibility to Salmonella infection in streptomycin-treated mice. J Infect Dis. 1962;111:117-127.
Barthel M, Hapfelmeier S, Quintanilla-Martínez L, et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun. 2003;71(5):2839-2858.
Miller CP, Bohnhoff M, Rifkind D. The effect of an antibiotic on the susceptibility of the mouse’s intestinal tract to Salmonella infection. Trans Am Clin Climatol Assoc. 1957;68:51-58.
Grassl GA, Valdez Y, Bergstrom KSB, Vallance BA, Finlay BB. Chronic enteric Salmonella infection in mice leads to severe and persistent intestinal fibrosis. Gastroenterology. 2008;134(3):768-780.
Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity. 2006;25(3):373-381.
Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat Immunol. 2012;13(10):954-962.
Fuchs Y, Steller H. Live to die another way: modes of programmed cell death and the signals emanating from dying cells. Nat Rev Mol Cell Biol. 2015;16(6):329-344.
Blander JM. A long-awaited merger of the pathways mediating host defence and programmed cell death. Nat Rev Immunol. 2014;14(9):601-618.
Lamkanfi M, Dixit VM. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe. 2010;8(1):44-54.
Lara-Tejero M, Sutterwala FS, Ogura Y, et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med. 2006;203(6):1407-1412.
Agbayani G, Wachholz K, Chattopadhyay A, Gurnani K, Murphy SP, Krishnan L. Modulation of Th17 and regulatory T-cell responses during murine pregnancy contributes to increased maternal susceptibility to Salmonella Typhimurium infection. Am J Reprod Immunol. 2017;78(6): e12742.
Nguyen T, Robinson N, Allison SE, Coombes BK, Sad S, Krishnan L. IL-10 produced by trophoblast cells inhibits phagosome maturation leading to profound intracellular proliferation of Salmonella enterica Typhimurium. Placenta. 2013;34(9):765-774.
Pejcic-Karapetrovic B, Gurnani K, Russell MS, Finlay BB, Sad S, Krishnan L. Pregnancy impairs the innate immune resistance to Salmonella typhimurium leading to rapid fatal infection. J Immunol. 2007;179(9):6088-6096.
Newton K, Sun X, Dixit VM. Kinase RIP3 is dispensable for normal NF-kappa Bs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol Cell Biol. 2004;24(4):1464-1469.
Müller U, Steinhoff U, Reis LF, et al. Functional role of type I and type II interferons in antiviral defense. Science. 1994;264(5167):1918-1921.
Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med. 2005;202(5):637-650.
Kuida K, Lippke JA, Ku G, et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science. 1995;267(5206):2000-2003.
Chattopadhyay A, Robinson N, Sandhu JK, Finlay BB, Sad S, Krishnan L. Salmonella enterica serovar Typhimurium-induced placental inflammation and not bacterial burden correlates with pathology and fatal maternal disease. Infect Immun. 2010;78(5):2292-2301.
Wu S, Lu R, Zhang Y, Sun J. Chronic Salmonella infected mouse model. J Vis Exp JoVE. 2010;39:1947.
Que JU, Hentges DJ. Effect of streptomycin administration on colonization resistance to Salmonella typhimurium in mice. Infect Immun. 1985;48(1):169-174.
Miller CP, Bohnhoff M. Changes IN the mouse’s enteric microflora associated with enhanced susceptibility to Salmonella infection following streptomycin treatmeNT. J Infect Dis. 1963;113:59-66.
Hallstrom K, McCormick BA. Salmonella interaction with and passage through the intestinal mucosa: through the lens of the organism. Front Microbiol. 2011;2:88.
Stecher B, Robbiani R, Walker AW, et al. Salmonella enterica Serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLOS Biol. 2007;5(10):e244.
Nilsson OR, Kari L, Steele-Mortimer O. Foodborne infection of mice with Salmonella Typhimurium. PLoS One. 2019;14(8):e0215190.
Mathur R, Oh H, Zhang D, et al. A mouse model of Salmonella typhi infection. Cell. 2012;151(3):590-602.
Fontes KN, Reginatto MW, Silva NL, et al. Dysregulation of placental ABC transporters in a murine model of malaria-induced preterm labor. Sci Rep. 2019;9(1):11488.
Raupach B, Peuschel S-K, Monack DM, Zychlinsky A. Caspase-1-mediated activation of interleukin-1β (IL-1β) and IL-18 contributes to innate immune defenses against Salmonella enterica Serovar Typhimurium infection. Infect Immun. 2006;74(8):4922-4926.
Broz P, Ruby T, Belhocine K, et al. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature. 2012;490(7419):288-291.
McComb S, Cessford E, Alturki NA, et al. Type-I interferon signaling through ISGF3 complex is required for sustained Rip3 activation and necroptosis in macrophages. Proc Natl Acad Sci USA. 2014;111(31):E3206-E3213.
Agbayani G, Wachholz K, Murphy SP, Sad S, Krishnan L. Type I interferons differentially modulate maternal host immunity to infection by Listeria monocytogenes and Salmonella enterica serovar Typhimurium during pregnancy. Am J Reprod Immunol. 2019;81(1):e13068.
Reis AS, Barboza R, Murillo O, et al. Inflammasome activation and IL-1 signaling during placental malaria induce poor pregnancy outcomes. Sci Adv. 2020;6(10):eaax6346.
Broz P, Ohlson MB, Monack DM. Innate immune response to Salmonella typhimurium, a model enteric pathogen. Gut Microbes. 2012;3(2):62-70.
Bao S, Beagley KW, France MP, Shen J, Husband AJ. Interferon-gamma plays a critical role in intestinal immunity against Salmonella typhimurium infection. Immunology. 2000;99(3):464-472.
Cousens LP, Orange JS, Su HC, Biron CA. Interferon-α/β inhibition of interleukin 12 and interferon-γ production in vitro and endogenously during viral infection. Proc Natl Acad Sci USA. 1997;94(2):634-639.
Gutierrez KD, Davis MA, Daniels BP, et al. MLKL activation triggers NLRP3-mediated processing and release of IL-1β independently of gasdermin-D. J Immunol. 2017;198(5):2156-2164.
Malireddi RKS, Kanneganti T-D. Role of type I interferons in inflammasome activation, cell death, and disease during microbial infection. Front Cell Infect Microbiol. 2013;3:77.
Gurung P, Malireddi RKS, Anand PK, et al. Toll or interleukin-1 receptor (TIR) domain-containing adaptor inducing interferon-β (TRIF)-mediated caspase-11 protease production integrates Toll-like receptor 4 (TLR4) protein- and Nlrp3 inflammasome-mediated host defense against enteropathogens. J Biol Chem. 2012;287(41):34474-34483.
Kayagaki N, Warming S, Lamkanfi M, et al. Non-canonical inflammasome activation targets caspase-11. Nature. 2011;479(7371):117-121.
Rathinam VAK, Vanaja SK, Waggoner L, et al. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell. 2012;150(3):606-619.
Zhou F, Li C, Zhang S-Y. NLRP3 inflammasome: a new therapeutic target for high-risk reproductive disorders? Chin Med J (Engl). 2021;134(1):20-27.
Gomez-Lopez N, Romero R, Panaitescu B, et al. Inflammasome activation during spontaneous preterm labor with intra-amniotic infection or sterile intra-amniotic inflammation. Am J Reprod Immunol. 2018;80(5):e13049.
Megli C, Morosky S, Rajasundaram D, Coyne CB. Inflammasome signaling in human placental trophoblasts regulates immune defense against Listeria monocytogenes infection. J Exp Med. 2021;218(1):e20200649.
Vidal S, Tremblay ML, Govoni G, et al. The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J Exp Med. 1995;182(3):655-666.
Forbes JR, Gros P. Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol. 2001;9(8):397-403.
Valdez Y, Diehl GE, Vallance BA, et al. Nramp1 expression by dendritic cells modulates inflammatory responses during Salmonella Typhimurium infection. Cell Microbiol. 2008;10(8):1646-1661.
Yockey LJ, Jurado KA, Arora N, et al. Type I interferons instigate fetal demise after Zika virus infection. Sci Immunol. 2018;3(19):eaao1680.
Cappelletti M, Presicce P, Lawson MJ, et al. Type I interferons regulate susceptibility to inflammation-induced preterm birth. JCI Insight. 2017;2(5):e91288.
Cardenas I, Mor G, Aldo P, et al. Placental viral infection sensitizes to endotoxin-induced pre-term labor: a double hit hypothesis. Am J Reprod Immunol. 2011;65(2):110-117.
Racicot K, Cardenas I, Wünsche V, et al. Viral infection of the pregnant cervix predisposes to ascending bacterial infection. J Immunol. 2013;191(2):934-941.