Abstract
Investigations of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium have demonstrated that these bacterial pathogens can respond to the presence of catecholamines including norepinephrine and/or epinephrine in their environment by modulating gene expression and exhibiting various phenotypes. For example, one of the most intensively investigated phenotypes following exposure of E. coli and S. Typhimurium to norepinephrine is enhanced bacterial growth in a serum-based medium. Host-pathogen investigations have demonstrated that the mammalian host utilizes nutritional immunity to sequester iron and prevent extraintestinal growth by bacterial pathogens. However, Salmonella and certain E. coli strains have a genetic arsenal designed for subversion and subterfuge of the host. Norepinephrine enhances bacterial growth due, in part, to increased iron availability, and transcriptional profiling indicates differential expression of genes encoding iron acquisition and transport proteins. Bacterial motility of E. coli and S. Typhimurium is also enhanced in the presence of catecholamines and increased flagellar gene expression has been described. Furthermore, epinephrine and norepinephrine are chemoattractants for E. coli O157:H7. In S. Typhimurium, norepinephrine enhances horizontal gene transfer and increases expression of genes involved in plasmid transfer. Exposure of E. coli O157:H7 to norepinephrine increases expression of the genes encoding Shiga toxin and operons within the locus of enterocyte effacement (LEE). Alterations in the transcriptional response of enteric bacteria to catecholamine exposure in vivo are predicted to enhance bacterial colonization and pathogen virulence. This chapter will review the current literature on the transcriptional response of E. coli and S. Typhimurium to catecholamines.
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References
Bansal T, Englert D, Lee J, Hegde M, Wood TK, Jayaraman A (2007) Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun 75(9):4597–4607
Bearson BL, Bearson SM (2008) The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microb Pathog 44(4):271–278
Bearson BL, Bearson SM, Uthe JJ, Dowd SE, Houghton JO, Lee I, Toscano MJ, Lay DC Jr (2008) Iron regulated genes of Salmonella enterica serovar Typhimurium in response to norepinephrine and the requirement of fepDGC for norepinephrine-enhanced growth. Microbes Infect 10(7):807–816
Bearson BL, Bearson SM, Lee IS, Brunelle BW (2010) The Salmonella enterica serovar Typhimurium QseB response regulator negatively regulates bacterial motility and swine colonization in the absence of the QseC sensor kinase. Microb Pathog 48(6):214–219. doi:10.1016/j.micpath.2010.03.005
Brodsky IE, Ernst RK, Miller SI, Falkow S (2002) mig-14 is a Salmonella gene that plays a role in bacterial resistance to antimicrobial peptides. J Bacteriol 184(12):3203–3213
Burton CL, Chhabra SR, Swift S, Baldwin TJ, Withers H, Hill SJ, Williams P (2002) The growth response of Escherichia coli to neurotransmitters and related catecholamine drugs requires a functional enterobactin biosynthesis and uptake system. Infect Immun 70(11):5913–5923
Chilcott GS, Hughes KT (2000) Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar Typhimurium and Escherichia coli. Microbiol Mol Biol Rev 64(4):694–708
Clarke MB, Hughes DT, Zhu C, Boedeker EC, Sperandio V (2006) The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci U S A 103(27):10420–10425
Detweiler CS, Monack DM, Brodsky IE, Mathew H, Falkow S (2003) virK, somA and rcsC are important for systemic Salmonella enterica serovar Typhimurium infection and cationic peptide resistance. Mol Microbiol 48(2):385–400. doi:10.1046/j.1365-2958.2003.03455.x
Dowd SE (2007) Escherichia coli O157:H7 gene expression in the presence of catecholamine norepinephrine. FEMS Microbiol Lett 273(2):214–223. doi:10.1111/j.1574-6968.2007.00800.x
Figueira R, Holden DW (2012) Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology 158(Pt 5):1147–1161. doi:10.1099/mic.0.058115-0
Fischbach MA, Lin H, Liu DR, Walsh CT (2005) In vitro characterization of IroB, a pathogen-associated C-glycosyltransferase. Proc Natl Acad Sci U S A 102(3):571–576. doi:10.1073/pnas.0408463102
Fischbach MA, Lin H, Zhou L, Yu Y, Abergel RJ, Liu DR, Raymond KN, Wanner BL, Strong RK, Walsh CT, Aderem A, Smith KD (2006) The pathogen-associated iroA gene cluster mediates bacterial evasion of lipocalin 2. Proc Natl Acad Sci U S A 103(44):16502–16507
Freestone PP, Haigh RD, Williams PH, Lyte M (1999) Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers. FEMS Microbiol Lett 172(1):53–60
Freestone PP, Lyte M, Neal CP, Maggs AF, Haigh RD, Williams PH (2000) The mammalian neuroendocrine hormone norepinephrine supplies iron for bacterial growth in the presence of transferrin or lactoferrin. J Bacteriol 182(21):6091–6098
Freestone PP, Haigh RD, Williams PH, Lyte M (2003) Involvement of enterobactin in norepinephrine-mediated iron supply from transferrin to enterohaemorrhagic Escherichia coli. FEMS Microbiol Lett 222(1):39–43. doi:S037810970300243X
Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, Strong RK (2002) The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 10(5):1033–1043
Guckes KR, Kostakioti M, Breland EJ, Gu AP, Shaffer CL, Martinez CR 3rd, Hultgren SJ, Hadjifrangiskou M (2013) Strong cross-system interactions drive the activation of the QseB response regulator in the absence of its cognate sensor. Proc Natl Acad Sci U S A 110(41):16592–16597. doi:10.1073/pnas.1315320110
Gunn JS (2008) The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more. Trends Microbiol 16(6):284–290. doi:10.1016/j.tim.2008.03.007
Hadjifrangiskou M, Kostakioti M, Chen SL, Henderson JP, Greene SE, Hultgren SJ (2011) A central metabolic circuit controlled by QseC in pathogenic Escherichia coli. Mol Microbiol 80(6):1516–1529. doi:10.1111/j.1365-2958.2011.07660.x
Hantke K, Nicholson G, Rabsch W, Winkelmann G (2003) Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci U S A 100(7):3677–3682
Hood MI, Skaar EP (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10(8):525–537. doi:10.1038/nrmicro2836
Hughes DT, Clarke MB, Yamamoto K, Rasko DA, Sperandio V (2009) The QseC adrenergic signaling cascade in Enterohemorrhagic E. coli (EHEC). PLoS Pathog 5(8), e1000553. doi:10.1371/journal.ppat.1000553
Karavolos MH, Spencer H, Bulmer DM, Thompson A, Winzer K, Williams P, Hinton JC, Khan CM (2008) Adrenaline modulates the global transcriptional profile of Salmonella revealing a role in the antimicrobial peptide and oxidative stress resistance responses. BMC Genomics 9:458. doi:10.1186/1471-2164-9-458
Karavolos MH, Winzer K, Williams P, Khan CM (2013) Pathogen espionage: multiple bacterial adrenergic sensors eavesdrop on host communication systems. Mol Microbiol 87(3):455–465. doi:10.1111/mmi.12110
Kostakioti M, Hadjifrangiskou M, Pinkner JS, Hultgren SJ (2009) QseC-mediated dephosphorylation of QseB is required for expression of genes associated with virulence in uropathogenic Escherichia coli. Mol Microbiol 73(6):1020–1031. doi:10.1111/j.1365-2958.2009.06826.x
Luo M, Lin H, Fischbach MA, Liu DR, Walsh CT, Groves JT (2006) Enzymatic tailoring of enterobactin alters membrane partitioning and iron acquisition. ACS Chem Biol 1(1):29–32. doi:10.1021/cb0500034
Merighi M, Septer AN, Carroll-Portillo A, Bhatiya A, Porwollik S, McClelland M, Gunn JS (2009) Genome-wide analysis of the PreA/PreB (QseB/QseC) regulon of Salmonella enterica serovar Typhimurium. BMC Microbiol 9:42. doi:10.1186/1471-2180-9-42
Moreira CG, Sperandio V (2012) Interplay between the QseC and QseE bacterial adrenergic sensor kinases in Salmonella enterica serovar Typhimurium pathogenesis. Infect Immun 80(12):4344–4353. doi:10.1128/IAI.00803-12
Moreira CG, Weinshenker D, Sperandio V (2010) QseC mediates Salmonella enterica serovar typhimurium virulence in vitro and in vivo. Infect Immun 78(3):914–926. doi:10.1128/IAI.01038-09
Njoroge J, Sperandio V (2012) Enterohemorrhagic Escherichia coli virulence regulation by two bacterial adrenergic kinases, QseC and QseE. Infect Immun 80(2):688–703. doi:10.1128/IAI.05921-11
Peterson G, Kumar A, Gart E, Narayanan S (2011) Catecholamines increase conjugative gene transfer between enteric bacteria. Microb Pathog 51(1–2):1–8. doi:10.1016/j.micpath.2011.03.002
Pullinger GD, Carnell SC, Sharaff FF, van Diemen PM, Dziva F, Morgan E, Lyte M, Freestone PP, Stevens MP (2010a) Norepinephrine augments Salmonella enterica-induced enteritis in a manner associated with increased net replication but independent of the putative adrenergic sensor kinases QseC and QseE. Infect Immun 78(1):372–380. doi:10.1128/IAI.01203-09
Pullinger GD, van Diemen PM, Carnell SC, Davies H, Lyte M, Stevens MP (2010b) 6-Hydroxydopamine-mediated release of norepinephrine increases faecal excretion of Salmonella enterica serovar Typhimurium in pigs. Vet Res 41(5):68. doi:10.1051/vetres/2010040
Rasko DA, Moreira CG, de Li R, Reading NC, Ritchie JM, Waldor MK, Williams N, Taussig R, Wei S, Roth M, Hughes DT, Huntley JF, Fina MW, Falck JR, Sperandio V (2008) Targeting QseC signaling and virulence for antibiotic development. Science 321(5892):1078–1080. doi:10.1126/science.1160354
Sharma VK, Casey TA (2014a) Determining the relative contribution and hierarchy of hha and qseBC in the regulation of flagellar motility of Escherichia coli O157:H7. PLoS One 9(1), e85866. doi:10.1371/journal.pone.0085866
Sharma VK, Casey TA (2014b) Escherichia coli O157:H7 lacking the qseBC-encoded quorum-sensing system outcompetes the parental strain in colonization of cattle intestines. Appl Environ Microbiol 80(6):1882–1892. doi:10.1128/AEM.03198-13
Smith KD (2007) Iron metabolism at the host pathogen interface: Lipocalin 2 and the pathogen-associated iroA gene cluster. Int J Biochem Cell Biol 39(10):1776–1780
Spencer H, Karavolos MH, Bulmer DM, Aldridge P, Chhabra SR, Winzer K, Williams P, Khan CM (2010) Genome-wide transposon mutagenesis identifies a role for host neuroendocrine stress hormones in regulating the expression of virulence genes in Salmonella. J Bacteriol 192(3):714–724. doi:10.1128/JB.01329-09
Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB (2003) Bacteria-host communication: the language of hormones. Proc Natl Acad Sci U S A 100(15):8951–8956
Touati D, Jacques M, Tardat B, Bouchard L, Despied S (1995) Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol 177(9):2305–2314
Verbrugghe E, Boyen F, Van Parys A, Van Deun K, Croubels S, Thompson A, Shearer N, Leyman B, Haesebrouck F, Pasmans F (2011) Stress induced Salmonella Typhimurium recrudescence in pigs coincides with cortisol induced increased intracellular proliferation in macrophages. Vet Res 42:118. doi:10.1186/1297-9716-42-118
Williams LP Jr, Newell KW (1970) Salmonella excretion in joy-riding pigs. Am J Public Health Nations Health 60(5):926–929
Williams PH, Rabsch W, Methner U, Voigt W, Tschape H, Reissbrodt R (2006) Catecholate receptor proteins in Salmonella enterica: role in virulence and implications for vaccine development. Vaccine 24(18):3840–3844
Wosten MM, Kox LF, Chamnongpol S, Soncini FC, Groisman EA (2000) A signal transduction system that responds to extracellular iron. Cell 103(1):113–125. doi:S0092-8674(00)00092-1
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Bearson, B.L. (2016). Molecular Profiling: Catecholamine Modulation of Gene Expression in Escherichia coli O157:H7 and Salmonella enterica Serovar Typhimurium. In: Lyte, M. (eds) Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health. Advances in Experimental Medicine and Biology(), vol 874. Springer, Cham. https://doi.org/10.1007/978-3-319-20215-0_7
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DOI: https://doi.org/10.1007/978-3-319-20215-0_7
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