Ethanolamine Signaling Promotes Niche Recognition and Adaptation during Infection
Chemical signaling underlies all cellular processes. Bacteria rely on chemical signaling to gain information about the local environment and precisely regulate gene expression. Ethanolamine is an abundant molecule within mammalian hosts that plays an important role in mammalian physiology and also serves as a carbon and nitrogen source for bacteria. Here we show that the foodborne pathogen Salmonella enterica exploits ethanolamine as a signal of distinct host environments to coordinate metabolism and virulence, which enhances disease progression during infection. The ability to sense ethanolamine is conserved in diverse bacteria; thus, these studies reveal that ethanolamine signaling may be important for bacterial adaptation to the mammalian host.
Vyšlo v časopise:
Ethanolamine Signaling Promotes Niche Recognition and Adaptation during Infection. PLoS Pathog 11(11): e32767. doi:10.1371/journal.ppat.1005278
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1005278
Souhrn
Chemical signaling underlies all cellular processes. Bacteria rely on chemical signaling to gain information about the local environment and precisely regulate gene expression. Ethanolamine is an abundant molecule within mammalian hosts that plays an important role in mammalian physiology and also serves as a carbon and nitrogen source for bacteria. Here we show that the foodborne pathogen Salmonella enterica exploits ethanolamine as a signal of distinct host environments to coordinate metabolism and virulence, which enhances disease progression during infection. The ability to sense ethanolamine is conserved in diverse bacteria; thus, these studies reveal that ethanolamine signaling may be important for bacterial adaptation to the mammalian host.
Zdroje
1. Hughes DT, Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and their hosts. Nature Rev Microbiol 6: 111–120.
2. Bakovic M, Fullerton MD, Michel V (2007) Metabolic and moleclar aspects of ethanolamine phospholipid biosynthesis: the role of CTP:phosphoethanolamine cytidylyl-transferase (Pcyt2). Biochem Cell Biol 85: 283–300. 17612623
3. Meijerink J, Plastina P, Vincken JP, Poland M, Attya M, et al. (2011) The ethanolamide metabolite of DHA, docosahexaenoylethanolamine, shows immunomodulating effects in mouse peritoneal and RAW264.7 macrophages: evidence for a new link between fish oil and inflammation. Br J Nutr 105: 1798–1807. doi: 10.1017/S0007114510005635 21294934
4. Sugiura T, Kobayashi Y, Oka S, Waku K (2002) Biosynthesis and degradation of anandamide and 2-arachidonoylglycerol and their possible physiological significance. Prostaglandins Leukot Essent Fatty Acids 66: 173–192. 12052034
5. Cotton PB (1972) Non-dietary lipid in the intestinal lumen. Gut 13: 675–681. 4639402
6. Garsin DA (2010) Ethanolamine utilization in bacterial pathogens: roles and regulation. Nature Rev Microbiol 8: 290–295.
7. Lipton BA, Davidson EP, Ginsberg BH, Yorek MA (1990) Ethanolamine metabolism in cultured bovine aortic endothelial cells. J Biol Chem 265: 7195–7201. 2110161
8. Lipton BA, Yorek MA, Ginsberg BH (1988) Ethanolamine and choline transport in cultured bovine aortic endothelial cells. J Cell Physiol 137: 571–576. 3192633
9. Nikawa J, Tsukagoshi Y, Yamashita S (1986) Cloning of a gene encoding choline transport in Saccharomyces cerevisiae. J Bacteriol 166: 328–330. 3514579
10. Sandra A, Cai J (1991) Plasma membrane appearance of phosphatidylethanolamine in stimulated macrophages. J Leukoc Biol 50: 19–27. 2056244
11. Cohen JI, Bartlett JA, Corey GR (1987) Extra-intestinal manifestations of salmonella infections. Medicine (Baltimore) 66: 349–388.
12. Galan JE, Curtis R III (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci 86: 6383–6387. 2548211
13. Cirillo DM, Valdivia RH, Monack DM, Falkow S (1998) Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30: 175–188. 9786194
14. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, et al. (1998) Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30: 163–174. 9786193
15. Ochman H, Soncini FC, Solomon F, Groisman EA (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci 93: 7800–7804. 8755556
16. Joseph B, Przybilla K, Stuhler C, Schauer K, Slaghis J, et al. (2006) Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J Bacteriol 188: 556–568. 16385046
17. Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, et al. (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci 108: 17480–17485. doi: 10.1073/pnas.1107857108 21969563
18. Roof DM, Roth JR (1988) Ethanolamine utilization in Salmonella typhimurium. J Bacteriol 170: 3855–3863. 3045078
19. Luzader DH, Clark DE, Gonyar LA, Kendall MM (2013) EutR is a direct regulator of genes that contribute to metabolism and virulence in enterohemorrhagic Escherichia coli O157:H7. J Bacteriol 195: 4947–4953. doi: 10.1128/JB.00937-13 23995630
20. Roof DM, Roth JR (1992) Autogenous regulation of ethanolamine utilization by a transcriptional activator of the eut operon in Salmonella typhimurium. J Bacteriol 174: 6634–6643. 1328159
21. Gonyar LA, Kendall MM (2014) Ethanolamine and choline promote expression of putative and characterized fimbriae in enterohemorrhagic Escherichia coli O157:H7. Infect Immun 82: 193–201. doi: 10.1128/IAI.00980-13 24126525
22. Kendall MM, Gruber CC, Parker CT, Sperandio V (2012) Ethanolamine controls expression of genes encoding components involved in interkingdom signaling and virulence in enterohemorrhagic Escherichia coli O157:H7. mBio 3: e00050–00012. doi: 10.1128/mBio.00050-12 22589288
23. Steeb B, Claudi B, Burton NA, Tienz P, Schmidt A, et al. (2013) Parallel exploitation of diverse host nutrients enhances Salmonella virulence. PLoS Pathog 9: e1003301. doi: 10.1371/journal.ppat.1003301 23633950
24. Stojiljkovic I, Bäumler AJ, Heffron F (1995) Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J Bacteriol 177: 1357–1366. 7868611
25. Hapfelmeier S, Hardt W-D (2005) A mouse model for S. typhimurium-induced enterocolits. Trends Microbiol 13: 497–503. 16140013
26. Lara-Tejero M, Galán JE (2009) Salmonella enterica serovar typhimurium pathogenicity island 1-encoded type III secretion system translocases mediate intimate attachment to nonphagocytic cells. Infect Immun 77: 2635–2642. doi: 10.1128/IAI.00077-09 19364837
27. Lee CA, Falkow S (1990) The ability of Salmonella to enter mammalian cells is affected by growth state. Proc Natl Acad Sci 87: 4303–4308.
28. Brown NF, Rogers LD, Sanderson KL, Gouw JW, Hartland EL, et al. (2014) A horizontally acquired transcription factor coordinates Salmonella adaptations to host microenvironments. mBio 5: e01727–01714. doi: 10.1128/mBio.01727-14 25249283
29. Feng X, Walthers D, Oropeza R, Kenney LJ (2004) The response regulator SsrB activates transcription and binds to a region overlapping OmpR binding sites at Salmonella pathogenicity island 2. Mol Microbiol 54: 823–835. 15491370
30. Walthers D, Carroll RK, Navarre WW, Libby SJ, Fang FC, et al. (2007) The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS. MolMicrobiol 65: 477–493.
31. Worley MJ, Ching KH, Heffron F (2000) Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol Microbiol 36: 749–761. 10844662
32. Deiwick J, Nikolaus T, Erdogan S, Hensel M (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759–1773. 10209748
33. Bertin Y, Girardeau JP, Chaucheyras-Durand F, Lyan B, Pujos-Guillot E, et al. (2011) Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ Microbiol 13: 365–377. doi: 10.1111/j.1462-2920.2010.02334.x 20849446
34. Coombes BK, Brown NF, Valdez Y, Brumell JH, Finlay BB (2004) Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J Biol Chem 279: 49804–49815. 15383528
35. Vazquez-Torres A, Fang FC (2001) Salmonella evasion of the NADPH phagocyte oxidase. Microbes Infect 3: 1313–1320. 11755420
36. Jeter RM, Olivera B, Roth JR (1984) Salmonella typhimurium synthesizes cobalamin vitamin B12 de novo under anaerobic growth conditions. J Bacteriol 159: 206–213. 6376471
37. Chakravortty D, Hansen-Wester I, Hensel M (2002) Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med 195: 1155–1166. 11994420
38. Vazquez-Torres A, Xu Y, Jones-Carson J, Holden DW, Lucia SM, et al. (2000) Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287: 1655–1658. 10698741
39. Miao EA, Freeman JA, Miller SI (2002) Transcription of the SsrAB regulon is repressed by alkaline pH and is independent of PhoPQ and magnesium concentration. J Bacteriol 184: 1493–1497. 11844786
40. Mulder DT, McPhee JB, Savchenko A, Coombes BK (2015) Multiple histidines in the periplasmic domain of the Salmonella enterica sensor kinase SsrA enhance signaling in response to extracellular acidification. Mol Microbiol 95: 678–691. doi: 10.1111/mmi.12895 25442048
41. Feng X, Oropeza R, Kenney LJ (2003) Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2. Mol Microbiol 48: 1131–1143. 12753201
42. Bijlsma JJE, Groisman EA (2005) The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Mol Microbiol 57: 85–96. 15948951
43. Chaudhuri RR, Morgan E, Peters SE, Pleasance SJ, Hudson DL, et al. (2013) Comprehensive assignment of roles for Salmonella typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet 9: e1003456. doi: 10.1371/journal.pgen.1003456 23637626
44. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, et al. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467: 426–429. doi: 10.1038/nature09415 20864996
45. Garsin DA (2012) Ethanolamine: a signal to commence a host-associated lifestyle? mBio 3: e00172–00112. doi: 10.1128/mBio.00172-12 22761393
46. Alteri CJ, Mobley HLT (2012) Escherichia coli physiology and metabolism dictates adaptation to diverse host microenvironments. Curr Opin Microbiol 15: 3–9. doi: 10.1016/j.mib.2011.12.004 22204808
47. Hoiseth SK, Stocker BA (1982) Aromatic-dependent Salmonella typhimurium are non-virulenct and effective as live vaccines. Nature 291: 238–239.
48. Criss AK, Ahlgren DM, Jou TS, McCormick BA, Casanova JE (2001) The GTPase Rac1 selectively regulates Salmonella invasion at the apical plasma membrane of polarized epithelial cells. J Cell Sci 114: 1331–1341. 11256999
49. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci 97: 6640–6645. 10829079
50. Lane MC, Alteri CJ, Smith SN, Mobley HLT (2007) Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci 104: 16669–16674. 17925449
51. Uzzau S, Figuerosa-Bossi N, Rubino S, Bossi L (2001) Epitope tagging of chromosomal genes in Salmonella. PNAS 98: 15264–15269. 11742086
52. Curtis MM, Hu Z, Klimko C, Narayanan S, Deberardinis R, et al. (2014) The gut commensal Bacteroides thetaiotaomicron exacerbates enteric enfection through modification of the metabolic landscape. Cell Host Microbe 16: 759–769. doi: 10.1016/j.chom.2014.11.005 25498343
53. Kendall MM, Gruber CC, Rasko D, A., Hughes DT, Sperandio V (2011) Hfq virulence regulation in enterohemorrhagic Escherichia coli O157:H7 strain 86–24. J Bacteriol.
54. Lee E-J, Groisman EA (2012) Control of a Salmonella virulence locus by an ATP-sensing leader messenger RNA. Nature 486: 271–275. doi: 10.1038/nature11090 22699622
55. Shin D, Lee E-J, Huang H, Groisman EA (2006) A positive feedback loop promotes transcription surge that jump-starts Salmonella virulence circui. Science 314: 1607–1609. 17158330
56. Zhang X, Goncalves R, Mosser DM (2008) The isolation and characterization of murine macrophages. In: Coligan JE, editor. Curr Prot Immunol.
57. Chen LM, Kaniga K, Galan JE (1996) Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101–1115. 8885278
58. Laughlin RC, Knodler LA, Barhoumi R, Payne HR, Wu J, et al. (2014) Spatial segregation of virulence gene expression during acute enteric infection with Salmonella enterica serovar Typhimurium. mBio 5: e00946–00913. doi: 10.1128/mBio.00946-13 24496791
59. Buchmeier NA, Heffron F (1989) Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages. Infect Immun 57: 1–7. 2642463
60. Owen K, Meyer CB, Bouton AH, Casanova JE (2014) Activation of focal adhesion kinase by Salmonella suppresses autophagy via an Akt/mTOR signaling pathway and promotes bacterial survival in macrophages. PLoS Pathog 10: e1004159. doi: 10.1371/journal.ppat.1004159 24901456
61. Barthel M, Hapfelmeier S, Quintanilla-Martínez L, Kremer M, Rohde M, et al. (2003) Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71: 2839–2858. 12704158
62. Edwards RA, Schifferli DM, Maloy SR (2000) A role for Salmonella fimbriae in intraperitoneal infections. Proc Natl Acad Sci 97: 1258–1262. 10655518
63. Kendall MM, Rasko D, A., Sperandio V (2010) The LysR-type regulator QseA regulates both characterized and putative virulence genes in enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 76: 1306–1321. doi: 10.1111/j.1365-2958.2010.07174.x 20444105
64. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
65. Rhodius VA, Wade JT (2009) Technical considerations in using DNA microarrays to define regulons. Methods 47: 63–72. doi: 10.1016/j.ymeth.2008.10.017 18955146
66. Kuras L, Struhl K (1999) Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature 399: 609–613. 10376605
67. Shin D, Groisman EA (2005) Signal-dependent binding of the response regulators PhoP and PmrA to their target promoters in vivo. J Biol Chem 280: 4089–4094. 15569664
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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