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Published in: Gut Pathogens 1/2020

01-12-2020 | Respiratory Microbiota | Research

The absence of murine cathelicidin-related antimicrobial peptide impacts host responses enhancing Salmonella enterica serovar Typhimurium infection

Authors: Danisa M. Bescucci, Sandra T. Clarke, Catherine L. J. Brown, Valerie F. Boras, Tony Montina, Richard R. E. Uwiera, G. Douglas Inglis

Published in: Gut Pathogens | Issue 1/2020

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Abstract

Background

Cathelicidins are a class of antimicrobial peptide, and the murine cathelicidin-related antimicrobial peptide (mCRAMP) has been demonstrated in vitro to impair Salmonella enterica serovar Typhimurium proliferation. However, the impact of mCRAMP on host responses and the microbiota following S. Typhimurium infection has not been determined. In this study mCRAMP−/− and mCRAMP+/+ mice (± streptomycin) were orally inoculated with S. enterica serovar Typhimurium DT104 (SA +), and impacts on the host and enteric bacterial communities were temporally evaluated.

Results

Higher densities of the pathogen were observed in cecal digesta and associated with mucosa in SA+/mCRAMP−/− mice that were pretreated (ST+) and not pretreated (ST−) with streptomycin at 24 h post-inoculation (hpi). Both SA+/ST+/mCRAMP−/− and SA+/ST−/mCRAMP−/− mice were more susceptible to infection exhibiting greater histopathologic changes (e.g. epithelial injury, leukocyte infiltration, goblet cell loss) at 48 hpi. Correspondingly, immune responses in SA+/ST+/mCRAMP–/− and SA+/ST−/mCRAMP–/− mice were affected (e.g. Ifnγ, Kc, Inos, Il1β, RegIIIγ). Systemic dissemination of the pathogen was characterized by metabolomics, and the liver metabolome was affected to a greater degree in SA+/ST+/mCRAMP–/− and SA+/ST−/mCRAMP–/− mice (e.g. taurine, cadaverine). Treatment-specific changes to the structure of the enteric microbiota were associated with infection and mCRAMP deficiency, with a higher abundance of Enterobacteriaceae and Veillonellaceae observed in infected null mice. The microbiota of mice that were administered the antibiotic and infected with Salmonella was dominated by Proteobacteria.

Conclusion

The study findings showed that the absence of mCRAMP modulated both host responses and the enteric microbiota enhancing local and systemic infection by Salmonella Typhimurium.
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Literature
1.
2.
go back to reference Mukherjee S, Vaishnava S, Hooper LV. Multi-layered regulation of intestinal antimicrobial defense. Cell Mol Life Sci. 2008;65(19):3019–27.PubMedCrossRef Mukherjee S, Vaishnava S, Hooper LV. Multi-layered regulation of intestinal antimicrobial defense. Cell Mol Life Sci. 2008;65(19):3019–27.PubMedCrossRef
3.
go back to reference Iimura M, Gallo RL, Hase K, Miyamoto Y, Eckmann L, Kagnoff MF. Cathelicidin mediates innate intestinal defense against colonization with epithelial adherent bacterial pathogens. J Immunol. 2005;174(8):4901–7.PubMedCrossRef Iimura M, Gallo RL, Hase K, Miyamoto Y, Eckmann L, Kagnoff MF. Cathelicidin mediates innate intestinal defense against colonization with epithelial adherent bacterial pathogens. J Immunol. 2005;174(8):4901–7.PubMedCrossRef
4.
go back to reference Travis SM, Anderson NN, Forsyth WR, Espiritu C, Conway BD, Greenberg EP, McCray PB Jr, Lehrer RI, Welsh MJ, Tack BF. Bactericidal activity of mammalian cathelicidin-derived peptides. Infect Immun. 2000;68(5):2748–55.PubMedPubMedCentralCrossRef Travis SM, Anderson NN, Forsyth WR, Espiritu C, Conway BD, Greenberg EP, McCray PB Jr, Lehrer RI, Welsh MJ, Tack BF. Bactericidal activity of mammalian cathelicidin-derived peptides. Infect Immun. 2000;68(5):2748–55.PubMedPubMedCentralCrossRef
5.
go back to reference Gudmundsson GH, Agerberth B, Odeberg J, Bergman T, Olsson B, Salcedo R. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur J Biochem. 1996;238(2):325–32.PubMedCrossRef Gudmundsson GH, Agerberth B, Odeberg J, Bergman T, Olsson B, Salcedo R. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur J Biochem. 1996;238(2):325–32.PubMedCrossRef
6.
go back to reference Larrick JW, Morgan JG, Palings I, Hirata M, Yen MH. Complementary DNA sequence of rabbit CAP18–a unique lipopolysaccharide binding protein. Biochem Biophys Res Commun. 1991;179(1):170–5.PubMedCrossRef Larrick JW, Morgan JG, Palings I, Hirata M, Yen MH. Complementary DNA sequence of rabbit CAP18–a unique lipopolysaccharide binding protein. Biochem Biophys Res Commun. 1991;179(1):170–5.PubMedCrossRef
7.
go back to reference Bals R, Lang C, Weiner DJ, Vogelmeier C, Welsch U, Wilson JM. Rhesus monkey (Macaca mulatta) mucosal antimicrobial peptides are close homologues of human molecules. Clin Diagn Lab Immunol. 2001;8(2):370–5.PubMedPubMedCentralCrossRef Bals R, Lang C, Weiner DJ, Vogelmeier C, Welsch U, Wilson JM. Rhesus monkey (Macaca mulatta) mucosal antimicrobial peptides are close homologues of human molecules. Clin Diagn Lab Immunol. 2001;8(2):370–5.PubMedPubMedCentralCrossRef
8.
go back to reference Holani R, Shah C, Haji Q, Inglis GD, Uwiera RRE, Cobo ER. Proline-arginine rich (PR-39) cathelicidin: structure, expression and functional implication in intestinal health. Comp Immunol Microbiol Infect Dis. 2016;49:95–101.PubMedCrossRef Holani R, Shah C, Haji Q, Inglis GD, Uwiera RRE, Cobo ER. Proline-arginine rich (PR-39) cathelicidin: structure, expression and functional implication in intestinal health. Comp Immunol Microbiol Infect Dis. 2016;49:95–101.PubMedCrossRef
9.
go back to reference Zanetti M, Del Sal G, Storici P, Schneider C, Romeo D. The cDNA of the neutrophil antibiotic Bac5 predicts a pro-sequence homologous to a cysteine proteinase inhibitor that is common to other neutrophil antibiotics. J Biol Chem. 1993;268(1):522–6.PubMed Zanetti M, Del Sal G, Storici P, Schneider C, Romeo D. The cDNA of the neutrophil antibiotic Bac5 predicts a pro-sequence homologous to a cysteine proteinase inhibitor that is common to other neutrophil antibiotics. J Biol Chem. 1993;268(1):522–6.PubMed
10.
go back to reference Gallo RL, Kim KJ, Bernfield M, Kozak CA, Zanetti M, Merluzzi L, Gennaro R. Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse. J Biol Chem. 1997;272(20):13088–93.PubMedCrossRef Gallo RL, Kim KJ, Bernfield M, Kozak CA, Zanetti M, Merluzzi L, Gennaro R. Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse. J Biol Chem. 1997;272(20):13088–93.PubMedCrossRef
11.
go back to reference Pestonjamasp VK, Huttner KH, Gallo RL. Processing site and gene structure for the murine antimicrobial peptide CRAMP. Peptides. 2001;22(10):1643–50.PubMedCrossRef Pestonjamasp VK, Huttner KH, Gallo RL. Processing site and gene structure for the murine antimicrobial peptide CRAMP. Peptides. 2001;22(10):1643–50.PubMedCrossRef
12.
go back to reference Brogden KA. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol. 2005;3(3):238–50.PubMedCrossRef Brogden KA. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol. 2005;3(3):238–50.PubMedCrossRef
13.
go back to reference Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, Dorschner RA, Pestonjamasp V, Piraino J, Huttner K, Gallo RL. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature. 2001;414(6862):454–7.PubMedCrossRef Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, Dorschner RA, Pestonjamasp V, Piraino J, Huttner K, Gallo RL. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature. 2001;414(6862):454–7.PubMedCrossRef
14.
go back to reference Chromek M, Slamova Z, Bergman P, Kovacs L, Podracka L, Ehren I, Hokfelt T, Gudmundsson GH, Gallo RL, Agerberth B, et al. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med. 2006;12(6):636–41.PubMedCrossRef Chromek M, Slamova Z, Bergman P, Kovacs L, Podracka L, Ehren I, Hokfelt T, Gudmundsson GH, Gallo RL, Agerberth B, et al. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med. 2006;12(6):636–41.PubMedCrossRef
15.
go back to reference Fan D, Coughlin LA, Neubauer MM, Kim J, Kim MS, Zhan X, Simms-Waldrip TR, Xie Y, Hooper LV, Koh AY. Activation of HIF-1alpha and LL-37 by commensal bacteria inhibits Candida albicans colonization. Nat Med. 2015;21(7):808–14.PubMedPubMedCentralCrossRef Fan D, Coughlin LA, Neubauer MM, Kim J, Kim MS, Zhan X, Simms-Waldrip TR, Xie Y, Hooper LV, Koh AY. Activation of HIF-1alpha and LL-37 by commensal bacteria inhibits Candida albicans colonization. Nat Med. 2015;21(7):808–14.PubMedPubMedCentralCrossRef
16.
go back to reference Koon HW, Shih DQ, Chen J, Bakirtzi K, Hing TC, Law I, Ho S, Ichikawa R, Zhao D, Xu H, et al. Cathelicidin signaling via the Toll-like receptor protects against colitis in mice. Gastroenterology. 2011;141(5):1852–63.PubMedCrossRef Koon HW, Shih DQ, Chen J, Bakirtzi K, Hing TC, Law I, Ho S, Ichikawa R, Zhao D, Xu H, et al. Cathelicidin signaling via the Toll-like receptor protects against colitis in mice. Gastroenterology. 2011;141(5):1852–63.PubMedCrossRef
17.
go back to reference Kurosaka K, Chen Q, Yarovinsky F, Oppenheim JJ, Yang D. Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J Immunol. 2005;174(10):6257–65.PubMedCrossRef Kurosaka K, Chen Q, Yarovinsky F, Oppenheim JJ, Yang D. Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J Immunol. 2005;174(10):6257–65.PubMedCrossRef
18.
go back to reference van Harten RM, van Woudenbergh E, van Dijk A, Haagsman HP. Cathelicidins: immunomodulatory antimicrobials. Vaccines. 2018;6(3):63.PubMedCentralCrossRef van Harten RM, van Woudenbergh E, van Dijk A, Haagsman HP. Cathelicidins: immunomodulatory antimicrobials. Vaccines. 2018;6(3):63.PubMedCentralCrossRef
19.
go back to reference Kress E, Merres J, Albrecht LJ, Hammerschmidt S, Pufe T, Tauber SC, Brandenburg LO. CRAMP deficiency leads to a pro-inflammatory phenotype and impaired phagocytosis after exposure to bacterial meningitis pathogens. Cell Commun Signal. 2017;15(1):32.PubMedPubMedCentralCrossRef Kress E, Merres J, Albrecht LJ, Hammerschmidt S, Pufe T, Tauber SC, Brandenburg LO. CRAMP deficiency leads to a pro-inflammatory phenotype and impaired phagocytosis after exposure to bacterial meningitis pathogens. Cell Commun Signal. 2017;15(1):32.PubMedPubMedCentralCrossRef
20.
go back to reference Koczulla R, von Degenfeld G, Kupatt C, Krotz F, Zahler S, Gloe T, Issbrucker K, Unterberger P, Zaiou M, Lebherz C, et al. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Investig. 2003;111(11):1665–72.PubMedCrossRefPubMedCentral Koczulla R, von Degenfeld G, Kupatt C, Krotz F, Zahler S, Gloe T, Issbrucker K, Unterberger P, Zaiou M, Lebherz C, et al. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Investig. 2003;111(11):1665–72.PubMedCrossRefPubMedCentral
21.
go back to reference Yoshimura T, McLean MH, Dzutsev AK, Yao X, Chen K, Huang J, Gong W, Zhou J, Xiang Y, et al. The antimicrobial peptide CRAMP is essential for colon homeostasis by maintaining microbiota balance. J Immunol. 2018;200(6):2174–85.PubMedCrossRef Yoshimura T, McLean MH, Dzutsev AK, Yao X, Chen K, Huang J, Gong W, Zhou J, Xiang Y, et al. The antimicrobial peptide CRAMP is essential for colon homeostasis by maintaining microbiota balance. J Immunol. 2018;200(6):2174–85.PubMedCrossRef
22.
23.
go back to reference Momose Y, Hirayama K, Itoh K. Competition for proline between indigenous Escherichia coli and E coli O157:H7 in gnotobiotic mice associated with infant intestinal microbiota and its contribution to the colonization resistance against E coli O157:H7. Anton Leeuw Int J G. 2008;94(2):165–71.CrossRef Momose Y, Hirayama K, Itoh K. Competition for proline between indigenous Escherichia coli and E coli O157:H7 in gnotobiotic mice associated with infant intestinal microbiota and its contribution to the colonization resistance against E coli O157:H7. Anton Leeuw Int J G. 2008;94(2):165–71.CrossRef
24.
go back to reference Freter R, Brickner H, Botney M, Cleven D, Aranki A. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun. 1983;39(2):676–85.PubMedPubMedCentralCrossRef Freter R, Brickner H, Botney M, Cleven D, Aranki A. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun. 1983;39(2):676–85.PubMedPubMedCentralCrossRef
25.
go back to reference Jana B, Salomon D. Type VI secretion system: a modular toolkit for bacterial dominance. Future Microbiol. 2019;14:1451–63.PubMedCrossRef Jana B, Salomon D. Type VI secretion system: a modular toolkit for bacterial dominance. Future Microbiol. 2019;14:1451–63.PubMedCrossRef
26.
go back to reference Martinez FA, Balciunas EM, Converti A, Cotter PD, de Souza Oliveira RP. Bacteriocin production by Bifidobacterium spp. A review. Biotechnol Adv. 2013;31(4):482–8.PubMedCrossRef Martinez FA, Balciunas EM, Converti A, Cotter PD, de Souza Oliveira RP. Bacteriocin production by Bifidobacterium spp. A review. Biotechnol Adv. 2013;31(4):482–8.PubMedCrossRef
27.
go back to reference Rios-Covian D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los Reyes-Gavilan CG, Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol. 2016;7:185.PubMedPubMedCentralCrossRef Rios-Covian D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los Reyes-Gavilan CG, Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol. 2016;7:185.PubMedPubMedCentralCrossRef
28.
go back to reference Hasegawa M, Kamada N, Jiao Y, Liu MZ, Nunez G, Inohara N. Protective role of commensals against Clostridium difficile infection via an IL-1beta-mediated positive-feedback loop. J Immunol. 2012;189(6):3085–91.PubMedCrossRef Hasegawa M, Kamada N, Jiao Y, Liu MZ, Nunez G, Inohara N. Protective role of commensals against Clostridium difficile infection via an IL-1beta-mediated positive-feedback loop. J Immunol. 2012;189(6):3085–91.PubMedCrossRef
29.
go back to reference Gu S, Chen D, Zhang JN, Lv X, Wang K, Duan LP, Nie Y, Wu XL. Bacterial community mapping of the mouse gastrointestinal tract. PLoS One. 2013;8(10):e74957.PubMedPubMedCentralCrossRef Gu S, Chen D, Zhang JN, Lv X, Wang K, Duan LP, Nie Y, Wu XL. Bacterial community mapping of the mouse gastrointestinal tract. PLoS One. 2013;8(10):e74957.PubMedPubMedCentralCrossRef
30.
go back to reference Coburn B, Grassl GA, Finlay BB. Salmonella, the host and disease: a brief review. Immunol Cell Biol. 2007;85(2):112–8.PubMedCrossRef Coburn B, Grassl GA, Finlay BB. Salmonella, the host and disease: a brief review. Immunol Cell Biol. 2007;85(2):112–8.PubMedCrossRef
31.
go back to reference Gal-Mor O, Boyle EC, Grassl GA. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front Microbiol. 2014;5:391.PubMedPubMedCentralCrossRef Gal-Mor O, Boyle EC, Grassl GA. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front Microbiol. 2014;5:391.PubMedPubMedCentralCrossRef
32.
go back to reference Kaiser P, Diard M, Stecher B, Hardt WD. The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen’s virulence factors, and the host’s mucosal immune response. Immunol Rev. 2012;245(1):56–83.PubMedCrossRef Kaiser P, Diard M, Stecher B, Hardt WD. The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen’s virulence factors, and the host’s mucosal immune response. Immunol Rev. 2012;245(1):56–83.PubMedCrossRef
33.
go back to reference Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Russmann H, Hardt WD. 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):2839–58.PubMedPubMedCentralCrossRef Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Russmann H, Hardt WD. 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):2839–58.PubMedPubMedCentralCrossRef
34.
go back to reference Zachar Z, Savage DC. Microbial interference and colonization of the murine gastrointestinal tract by Listeria monocytogenes. Infect Immun. 1979;23(1):168–74.PubMedPubMedCentralCrossRef Zachar Z, Savage DC. Microbial interference and colonization of the murine gastrointestinal tract by Listeria monocytogenes. Infect Immun. 1979;23(1):168–74.PubMedPubMedCentralCrossRef
35.
go back to reference Wadolkowski EA, Laux DC, Cohen PS. Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of growth in mucus. Infect Immun. 1988;56(5):1030–5.PubMedPubMedCentralCrossRef Wadolkowski EA, Laux DC, Cohen PS. Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of growth in mucus. Infect Immun. 1988;56(5):1030–5.PubMedPubMedCentralCrossRef
36.
go back to reference Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229–41.PubMedCrossRef Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229–41.PubMedCrossRef
37.
go back to reference Salzman NH, Underwood MA, Bevins CL. Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin Immunol. 2007;19(2):70–83.PubMedCrossRef Salzman NH, Underwood MA, Bevins CL. Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin Immunol. 2007;19(2):70–83.PubMedCrossRef
38.
go back to reference Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M, Kremer M, Chaffron S, Macpherson AJ, Buer J, Parkhill J, et al. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 2007;5(10):2177–89.PubMedCrossRef Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M, Kremer M, Chaffron S, Macpherson AJ, Buer J, Parkhill J, et al. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 2007;5(10):2177–89.PubMedCrossRef
40.
go back to reference Rosenberger CM, Gallo RL. Interplay between antibacterial effectors: a macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proc Natl Acad Sci USA. 2004;101(8):2422–7.PubMedCrossRefPubMedCentral Rosenberger CM, Gallo RL. Interplay between antibacterial effectors: a macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proc Natl Acad Sci USA. 2004;101(8):2422–7.PubMedCrossRefPubMedCentral
41.
go back to reference Yin F, Farzan A, Wang QC, Yu H, Yin Y, Hou Y, Friendship R, Gong J. Reduction of Salmonella enterica serovar Typhimurium DT104 infection in experimentally challenged weaned pigs fed a Lactobacillus-fermented feed. Foodborne Pathog Dis. 2014;11(8):628–34.PubMedCrossRef Yin F, Farzan A, Wang QC, Yu H, Yin Y, Hou Y, Friendship R, Gong J. Reduction of Salmonella enterica serovar Typhimurium DT104 infection in experimentally challenged weaned pigs fed a Lactobacillus-fermented feed. Foodborne Pathog Dis. 2014;11(8):628–34.PubMedCrossRef
42.
go back to reference Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesús J, Platt DJ, Olsen JE. Host adapted serotypes of Salmonella enterica. Epidemiol Infect. 2000;125(02):229–55.PubMedPubMedCentralCrossRef Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesús J, Platt DJ, Olsen JE. Host adapted serotypes of Salmonella enterica. Epidemiol Infect. 2000;125(02):229–55.PubMedPubMedCentralCrossRef
43.
go back to reference Stecher B, Macpherson AJ, Hapfelmeier S, Kremer M, Stallmach T, Hardt WD. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect Immun. 2005;73(6):3228–41.PubMedPubMedCentralCrossRef Stecher B, Macpherson AJ, Hapfelmeier S, Kremer M, Stallmach T, Hardt WD. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect Immun. 2005;73(6):3228–41.PubMedPubMedCentralCrossRef
45.
go back to reference Arpaia N, Godec J, Lau L, Sivick KE, McLaughlin LM, Jones MB, Dracheva T, Peterson SN, Monack DM, Barton GM. TLR signaling is required for Salmonella Typhimurium virulence. Cell. 2011;144(5):675–88.PubMedPubMedCentralCrossRef Arpaia N, Godec J, Lau L, Sivick KE, McLaughlin LM, Jones MB, Dracheva T, Peterson SN, Monack DM, Barton GM. TLR signaling is required for Salmonella Typhimurium virulence. Cell. 2011;144(5):675–88.PubMedPubMedCentralCrossRef
46.
go back to reference Raupach B, Peuschel SK, Monack DM, Zychlinsky A. Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect Immun. 2006;74(8):4922–6.PubMedPubMedCentralCrossRef Raupach B, Peuschel SK, Monack DM, Zychlinsky A. Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect Immun. 2006;74(8):4922–6.PubMedPubMedCentralCrossRef
47.
go back to reference Godinez I, Haneda T, Raffatellu M, George MD, Paixao TA, Rolan HG, Santos RL, Dandekar S, Tsolis RM, Baumler AJ. T cells help to amplify inflammatory responses induced by Salmonella enterica serotype Typhimurium in the intestinal mucosa. Infect Immun. 2008;76(5):2008–17.PubMedPubMedCentralCrossRef Godinez I, Haneda T, Raffatellu M, George MD, Paixao TA, Rolan HG, Santos RL, Dandekar S, Tsolis RM, Baumler AJ. T cells help to amplify inflammatory responses induced by Salmonella enterica serotype Typhimurium in the intestinal mucosa. Infect Immun. 2008;76(5):2008–17.PubMedPubMedCentralCrossRef
48.
go back to reference Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, Winter SE, Godinez I, Sankaran S, Paixao TA, Gordon MA, et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med. 2008;14(4):421–8.PubMedPubMedCentralCrossRef Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, Winter SE, Godinez I, Sankaran S, Paixao TA, Gordon MA, et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med. 2008;14(4):421–8.PubMedPubMedCentralCrossRef
49.
go back to reference Dubin PJ, Kolls JK. IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am J Physiol Lung Cell Mol Physiol. 2007;292(2):L519–28.PubMedCrossRef Dubin PJ, Kolls JK. IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am J Physiol Lung Cell Mol Physiol. 2007;292(2):L519–28.PubMedCrossRef
50.
go back to reference Godinez I, Raffatellu M, Chu H, Paixao TA, Haneda T, Santos RL, Bevins CL, Tsolis RM, Baumler AJ. Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype Typhimurium in the intestine. Infect Immun. 2009;77(1):387–98.PubMedCrossRef Godinez I, Raffatellu M, Chu H, Paixao TA, Haneda T, Santos RL, Bevins CL, Tsolis RM, Baumler AJ. Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype Typhimurium in the intestine. Infect Immun. 2009;77(1):387–98.PubMedCrossRef
51.
go back to reference Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol. 2008;8(6):411–20.PubMedCrossRef Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol. 2008;8(6):411–20.PubMedCrossRef
52.
go back to reference Trivedi RN, Agarwal P, Kumawat M, Pesingi PK, Gupta VK, Goswami TK, Mahawar M. Methionine sulfoxide reductase A (MsrA) contributes to Salmonella Typhimurium survival against oxidative attack of neutrophils. Immunobiology. 2015;220(12):1322–7.PubMedCrossRef Trivedi RN, Agarwal P, Kumawat M, Pesingi PK, Gupta VK, Goswami TK, Mahawar M. Methionine sulfoxide reductase A (MsrA) contributes to Salmonella Typhimurium survival against oxidative attack of neutrophils. Immunobiology. 2015;220(12):1322–7.PubMedCrossRef
55.
go back to reference Nunes JS, Lawhon SD, Rossetti CA, Khare S, Figueiredo JF, Gull T, Burghardt RC, Baumler AJ, Tsolis RM, Andrews-Polymenis HL, et al. Morphologic and cytokine profile characterization of Salmonella enterica serovar Typhimurium infection in calves with bovine leukocyte adhesion deficiency. Vet Pathol. 2010;47(2):322–33.PubMedCrossRef Nunes JS, Lawhon SD, Rossetti CA, Khare S, Figueiredo JF, Gull T, Burghardt RC, Baumler AJ, Tsolis RM, Andrews-Polymenis HL, et al. Morphologic and cytokine profile characterization of Salmonella enterica serovar Typhimurium infection in calves with bovine leukocyte adhesion deficiency. Vet Pathol. 2010;47(2):322–33.PubMedCrossRef
56.
go back to reference Spees AM, Kingsbury DD, Wangdi T, Xavier MN, Tsolis RM, Baumler AJ. Neutrophils are a source of gamma interferon during acute Salmonella enterica serovar Typhimurium colitis. Infect Immun. 2014;82(4):1692–7.PubMedPubMedCentralCrossRef Spees AM, Kingsbury DD, Wangdi T, Xavier MN, Tsolis RM, Baumler AJ. Neutrophils are a source of gamma interferon during acute Salmonella enterica serovar Typhimurium colitis. Infect Immun. 2014;82(4):1692–7.PubMedPubMedCentralCrossRef
57.
go back to reference Que JU, Hentges DJ. Effect of streptomycin administration on colonization resistance to Salmonella Typhimurium in mice. Infect Immun. 1985;48(1):169–74.PubMedPubMedCentralCrossRef Que JU, Hentges DJ. Effect of streptomycin administration on colonization resistance to Salmonella Typhimurium in mice. Infect Immun. 1985;48(1):169–74.PubMedPubMedCentralCrossRef
58.
go back to reference Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Baumler AJ. Animal models of Salmonella infections: enteritis versus typhoid fever. Microb Infect. 2001;3(14):1335–44.CrossRef Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Baumler AJ. Animal models of Salmonella infections: enteritis versus typhoid fever. Microb Infect. 2001;3(14):1335–44.CrossRef
59.
go back to reference Nakoneczna I, Hsu HS. The comparative histopathology of primary and secondary lesions in murine salmonellosis. Br J Exp Pathol. 1980;61(1):76.PubMedPubMedCentral Nakoneczna I, Hsu HS. The comparative histopathology of primary and secondary lesions in murine salmonellosis. Br J Exp Pathol. 1980;61(1):76.PubMedPubMedCentral
60.
go back to reference Vente JP, von Meyenfeldt MF, van Eijk HM, van Berlo CL, Gouma DJ, van der Linden CJ, Soeters PB. Plasma-amino acid profiles in sepsis and stress. Ann Surg. 1989;209(1):57–62.PubMedPubMedCentralCrossRef Vente JP, von Meyenfeldt MF, van Eijk HM, van Berlo CL, Gouma DJ, van der Linden CJ, Soeters PB. Plasma-amino acid profiles in sepsis and stress. Ann Surg. 1989;209(1):57–62.PubMedPubMedCentralCrossRef
61.
go back to reference Wannemacher RW Jr. Key role of various individual amino acids in host response to infection. Am J Clin Nutr. 1977;30(8):1269–80.PubMedCrossRef Wannemacher RW Jr. Key role of various individual amino acids in host response to infection. Am J Clin Nutr. 1977;30(8):1269–80.PubMedCrossRef
62.
go back to reference Wannemacher RW Jr, Powanda MC, Pekarek RS, Beisel WR. Tissue amino acid flux after exposure of rats to Diplococcus pneumoniae. Infect Immun. 1971;4(5):556–62.PubMedPubMedCentralCrossRef Wannemacher RW Jr, Powanda MC, Pekarek RS, Beisel WR. Tissue amino acid flux after exposure of rats to Diplococcus pneumoniae. Infect Immun. 1971;4(5):556–62.PubMedPubMedCentralCrossRef
63.
go back to reference Zhang S, Zeng X, Ren M, Mao X, Qiao S. Novel metabolic and physiological functions of branched chain amino acids: a review. J Anim Sci Biotechnol. 2017;8:10.PubMedPubMedCentralCrossRef Zhang S, Zeng X, Ren M, Mao X, Qiao S. Novel metabolic and physiological functions of branched chain amino acids: a review. J Anim Sci Biotechnol. 2017;8:10.PubMedPubMedCentralCrossRef
64.
go back to reference Mochizuki T, Satsu H, Nakano T, Shimizu M. Regulation of the human taurine transporter by TNF-alpha and an anti-inflammatory function of taurine in human intestinal Caco-2 cells. BioFactors. 2004;21(1–4):141–4.PubMedCrossRef Mochizuki T, Satsu H, Nakano T, Shimizu M. Regulation of the human taurine transporter by TNF-alpha and an anti-inflammatory function of taurine in human intestinal Caco-2 cells. BioFactors. 2004;21(1–4):141–4.PubMedCrossRef
65.
go back to reference Schuller-Levis GB, Park E. Taurine and its chloramine: modulators of immunity. Neurochem Res. 2004;29(1):117–26.PubMedCrossRef Schuller-Levis GB, Park E. Taurine and its chloramine: modulators of immunity. Neurochem Res. 2004;29(1):117–26.PubMedCrossRef
66.
go back to reference Sukhotnik I, Aranovich I, Ben Shahar Y, Bitterman N, Pollak Y, Berkowitz D, Chepurov D, Coran AG, Bitterman A. Effect of taurine on intestinal recovery following intestinal ischemia-reperfusion injury in a rat. Pediatr Surg Int. 2016;32(2):161–8.PubMedCrossRef Sukhotnik I, Aranovich I, Ben Shahar Y, Bitterman N, Pollak Y, Berkowitz D, Chepurov D, Coran AG, Bitterman A. Effect of taurine on intestinal recovery following intestinal ischemia-reperfusion injury in a rat. Pediatr Surg Int. 2016;32(2):161–8.PubMedCrossRef
67.
go back to reference Fernandez IM, Silva M, Schuch R, Walker WA, Siber AM, Maurelli AT, McCormick BA. Cadaverine prevents the escape of Shigella flexneri from the phagolysosome: a connection between bacterial dissemination and neutrophil transepithelial signaling. J Infect Dis. 2001;184(6):743–53.PubMedCrossRef Fernandez IM, Silva M, Schuch R, Walker WA, Siber AM, Maurelli AT, McCormick BA. Cadaverine prevents the escape of Shigella flexneri from the phagolysosome: a connection between bacterial dissemination and neutrophil transepithelial signaling. J Infect Dis. 2001;184(6):743–53.PubMedCrossRef
68.
go back to reference Wannemacher RW Jr, Klainer AS, Dinterman RE, Beisel WR. The significance and mechanism of an increased serum phenylalanine-tyrosine ratio during infection. Am J Clin Nutr. 1976;29(9):997–1006.PubMedCrossRef Wannemacher RW Jr, Klainer AS, Dinterman RE, Beisel WR. The significance and mechanism of an increased serum phenylalanine-tyrosine ratio during infection. Am J Clin Nutr. 1976;29(9):997–1006.PubMedCrossRef
69.
go back to reference Barnes DM, Song Z, Klasing KC, Bottje W. Protein metabolism during an acute phase response in chickens. Amino Acids. 2002;22(1):15–26.PubMedCrossRef Barnes DM, Song Z, Klasing KC, Bottje W. Protein metabolism during an acute phase response in chickens. Amino Acids. 2002;22(1):15–26.PubMedCrossRef
70.
go back to reference Reuter SE, Evans AM. Carnitine and acylcarnitines: pharmacokinetic, pharmacological and clinical aspects. Clin Pharmacokinet. 2012;51(9):553–72.PubMedCrossRef Reuter SE, Evans AM. Carnitine and acylcarnitines: pharmacokinetic, pharmacological and clinical aspects. Clin Pharmacokinet. 2012;51(9):553–72.PubMedCrossRef
71.
go back to reference Fattorossi A, Biselli R, Casciaro A, Tzantzoglou S, de Simone C. Regulation of normal human polyrnorphonuclear leucocytes by carnitine. Mediators Inflamm. 1993;2(7):S37–41.PubMedPubMedCentralCrossRef Fattorossi A, Biselli R, Casciaro A, Tzantzoglou S, de Simone C. Regulation of normal human polyrnorphonuclear leucocytes by carnitine. Mediators Inflamm. 1993;2(7):S37–41.PubMedPubMedCentralCrossRef
72.
go back to reference Litvak Y, Byndloss MX, Tsolis RM, Baumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017;39:1–6.PubMedCrossRef Litvak Y, Byndloss MX, Tsolis RM, Baumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017;39:1–6.PubMedCrossRef
74.
go back to reference Winterbourn CC, Kettle AJ, Hampton MB. Reactive oxygen species and neutrophil function. Annu Rev Biochem. 2016;85:765–92.PubMedCrossRef Winterbourn CC, Kettle AJ, Hampton MB. Reactive oxygen species and neutrophil function. Annu Rev Biochem. 2016;85:765–92.PubMedCrossRef
75.
go back to reference Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 2010;467(7314):426–9.PubMedPubMedCentralCrossRef Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 2010;467(7314):426–9.PubMedPubMedCentralCrossRef
76.
go back to reference Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, Finlay BB. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007;2(2):119–29.PubMedCrossRef Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, Finlay BB. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007;2(2):119–29.PubMedCrossRef
77.
go back to reference Sassone-Corsi M, Raffatellu M. No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J Immunol. 2015;194(9):4081–7.PubMedCrossRef Sassone-Corsi M, Raffatellu M. No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J Immunol. 2015;194(9):4081–7.PubMedCrossRef
78.
go back to reference den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–40.CrossRef den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–40.CrossRef
79.
go back to reference Brugiroux S, Beutler M, Pfann C, Garzetti D, Ruscheweyh HJ, Ring D, Diehl M, Herp S, Lotscher Y, Hussain S, et al. Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium. Nat Microbiol. 2016;2:16215.PubMedCrossRef Brugiroux S, Beutler M, Pfann C, Garzetti D, Ruscheweyh HJ, Ring D, Diehl M, Herp S, Lotscher Y, Hussain S, et al. Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium. Nat Microbiol. 2016;2:16215.PubMedCrossRef
80.
go back to reference Ganesh BP, Klopfleisch R, Loh G, Blaut M. Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice. PLoS One. 2013;8(9):e74963.PubMedPubMedCentralCrossRef Ganesh BP, Klopfleisch R, Loh G, Blaut M. Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice. PLoS One. 2013;8(9):e74963.PubMedPubMedCentralCrossRef
81.
go back to reference Wu WK, Wong CC, Li ZJ, Zhang L, Ren SX, Cho CH. Cathelicidins in inflammation and tissue repair: potential therapeutic applications for gastrointestinal disorders. Acta Pharmacol Sin. 2010;31(9):1118–22.PubMedPubMedCentralCrossRef Wu WK, Wong CC, Li ZJ, Zhang L, Ren SX, Cho CH. Cathelicidins in inflammation and tissue repair: potential therapeutic applications for gastrointestinal disorders. Acta Pharmacol Sin. 2010;31(9):1118–22.PubMedPubMedCentralCrossRef
82.
go back to reference Zhang Y, Jiang Y, Sun C, Wang Q, Yang Z, Pan X, Zhu M, Xiao W. The human cathelicidin LL-37 enhances airway mucus production in chronic obstructive pulmonary disease. Biochem Biophys Res Commun. 2014;443(1):103–9.PubMedCrossRef Zhang Y, Jiang Y, Sun C, Wang Q, Yang Z, Pan X, Zhu M, Xiao W. The human cathelicidin LL-37 enhances airway mucus production in chronic obstructive pulmonary disease. Biochem Biophys Res Commun. 2014;443(1):103–9.PubMedCrossRef
83.
go back to reference Boyer PE, D’Costa S, Edwards LL, Milloway M, Susick E, Borst LB, Thakur S, Campbell JM, Crenshaw JD, Polo J, et al. Early-life dietary spray-dried plasma influences immunological and intestinal injury responses to later-life Salmonella Typhimurium challenge. Br J Nutr. 2015;113(5):783–93.PubMedPubMedCentralCrossRef Boyer PE, D’Costa S, Edwards LL, Milloway M, Susick E, Borst LB, Thakur S, Campbell JM, Crenshaw JD, Polo J, et al. Early-life dietary spray-dried plasma influences immunological and intestinal injury responses to later-life Salmonella Typhimurium challenge. Br J Nutr. 2015;113(5):783–93.PubMedPubMedCentralCrossRef
84.
go back to reference Garner CD, Antonopoulos DA, Wagner B, Duhamel GE, Keresztes I, Ross DA, Young VB, Altier C. Perturbation of the small intestine microbial ecology by streptomycin alters pathology in a Salmonella enterica serovar Typhimurium murine model of infection. Infect Immun. 2009;77(7):2691–702.PubMedPubMedCentralCrossRef Garner CD, Antonopoulos DA, Wagner B, Duhamel GE, Keresztes I, Ross DA, Young VB, Altier C. Perturbation of the small intestine microbial ecology by streptomycin alters pathology in a Salmonella enterica serovar Typhimurium murine model of infection. Infect Immun. 2009;77(7):2691–702.PubMedPubMedCentralCrossRef
85.
go back to reference Koelink PJ, Wildenberg ME, Stitt LW, Feagan BG, Koldijk M, Wout AB, Atreya R, Vieth M, Brandse JF, Duijst S, et al. Development of reliable, valid and responsive scoring systems for endoscopy and histology in animal models for inflammatory bowel disease. J Crohns Colitis. 2018;12(7):794–803.PubMedPubMedCentralCrossRef Koelink PJ, Wildenberg ME, Stitt LW, Feagan BG, Koldijk M, Wout AB, Atreya R, Vieth M, Brandse JF, Duijst S, et al. Development of reliable, valid and responsive scoring systems for endoscopy and histology in animal models for inflammatory bowel disease. J Crohns Colitis. 2018;12(7):794–803.PubMedPubMedCentralCrossRef
86.
go back to reference Erben U, Loddenkemper C, Doerfel K, Spieckermann S, Haller D, Heimesaat MM, Zeitz M, Siegmund B, Kühl AA. A guide to histomorphological evaluation of intestinal inflammation in mouse models. Int J Clin Exp Pathol. 2014;7(8):4557.PubMedPubMedCentral Erben U, Loddenkemper C, Doerfel K, Spieckermann S, Haller D, Heimesaat MM, Zeitz M, Siegmund B, Kühl AA. A guide to histomorphological evaluation of intestinal inflammation in mouse models. Int J Clin Exp Pathol. 2014;7(8):4557.PubMedPubMedCentral
87.
go back to reference Kumar R, Surendran PK, Thampuran N. Rapid quantification of Salmonella in seafood by real-time PCR assay. J Microbiol Biotechnol. 2010;20(3):569–73.PubMed Kumar R, Surendran PK, Thampuran N. Rapid quantification of Salmonella in seafood by real-time PCR assay. J Microbiol Biotechnol. 2010;20(3):569–73.PubMed
88.
go back to reference Burgos-Ramos E, Chowen JA, Arilla-Ferreiro E, Canelles S, Argente J, Barrios V. Chronic central leptin infusion modifies the response to acute central insulin injection by reducing the interaction of the insulin receptor with IRS2 and increasing its association with SOCS3. J Neurochem. 2011;117(1):175–85.PubMedCrossRef Burgos-Ramos E, Chowen JA, Arilla-Ferreiro E, Canelles S, Argente J, Barrios V. Chronic central leptin infusion modifies the response to acute central insulin injection by reducing the interaction of the insulin receptor with IRS2 and increasing its association with SOCS3. J Neurochem. 2011;117(1):175–85.PubMedCrossRef
89.
go back to reference Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–7.PubMedPubMedCentralCrossRef Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–7.PubMedPubMedCentralCrossRef
90.
go back to reference Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3.PubMedPubMedCentralCrossRef Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3.PubMedPubMedCentralCrossRef
91.
go back to reference Morton JT, Sanders J, Quinn RA, McDonald D, Gonzalez A, Vazquez-Baeza Y, Navas-Molina JA, Song SJ, Metcalf JL, Hyde ER, et al. Balance trees reveal microbial niche differentiation. mSystems. 2017;2(1):e00162.PubMedPubMedCentral Morton JT, Sanders J, Quinn RA, McDonald D, Gonzalez A, Vazquez-Baeza Y, Navas-Molina JA, Song SJ, Metcalf JL, Hyde ER, et al. Balance trees reveal microbial niche differentiation. mSystems. 2017;2(1):e00162.PubMedPubMedCentral
92.
go back to reference Paxman EJ, Boora NS, Kiss D, Laplante DP, King S, Montina T, Metz GAS. Prenatal maternal stress from a natural disaster alters urinary metabolomic profiles in project ice storm participants. Sci Rep. 2018;8(1):12932.PubMedPubMedCentralCrossRef Paxman EJ, Boora NS, Kiss D, Laplante DP, King S, Montina T, Metz GAS. Prenatal maternal stress from a natural disaster alters urinary metabolomic profiles in project ice storm participants. Sci Rep. 2018;8(1):12932.PubMedPubMedCentralCrossRef
93.
go back to reference Veselkov KA, Lindon JC, Ebbels TM, Crockford D, Volynkin VV, Holmes E, Davies DB, Nicholson JK. Recursive segment-wise peak alignment of biological 1H NMR spectra for improved metabolic biomarker recovery. Anal Chem. 2009;1:56–66.CrossRef Veselkov KA, Lindon JC, Ebbels TM, Crockford D, Volynkin VV, Holmes E, Davies DB, Nicholson JK. Recursive segment-wise peak alignment of biological 1H NMR spectra for improved metabolic biomarker recovery. Anal Chem. 2009;1:56–66.CrossRef
94.
go back to reference Anderson PE, Mahle DA, Doom TE, Reo NV, DelRaso NJ, Raymer ML. Dynamic adaptive binning: an improved quantification technique for NMR spectroscopic data. Metabolomics. 2010;7(2):179–90.CrossRef Anderson PE, Mahle DA, Doom TE, Reo NV, DelRaso NJ, Raymer ML. Dynamic adaptive binning: an improved quantification technique for NMR spectroscopic data. Metabolomics. 2010;7(2):179–90.CrossRef
95.
96.
go back to reference Goodpaster AM, Romick-Rosendale LE, Kennedy MA. Statistical significance analysis of nuclear magnetic resonance-based metabonomics data. Anal Biochem. 2010;401(1):134–43.PubMedCrossRef Goodpaster AM, Romick-Rosendale LE, Kennedy MA. Statistical significance analysis of nuclear magnetic resonance-based metabonomics data. Anal Biochem. 2010;401(1):134–43.PubMedCrossRef
Metadata
Title
The absence of murine cathelicidin-related antimicrobial peptide impacts host responses enhancing Salmonella enterica serovar Typhimurium infection
Authors
Danisa M. Bescucci
Sandra T. Clarke
Catherine L. J. Brown
Valerie F. Boras
Tony Montina
Richard R. E. Uwiera
G. Douglas Inglis
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2020
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-020-00386-1

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