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Listeria monocytogenes is a Gram-positive, intracellular pathogen that is highly adapted to invade and replicate in the cytosol of eukaryotic cells. Intermediate metabolites in the menaquinone biosynthesis pathway are essential for the cytosolic survival and virulence of L. monocytogenes , independent of the production of menaquinone (MK) and aerobic respiration. Determining which specific intermediate metabolite(s) are essential for cytosolic survival and virulence has been hindered by the lack of an identified 1,4-dihydroxy-2-naphthoyl-coenzyme A (DHNA-CoA) thioesterase essential for converting DHNA-CoA to DHNA in the MK synthesis pathway. Using the recently identified Escherichia coli DHNA-CoA thioesterase as a query, homology sequence analysis revealed a single homolog in L. monocytogenes , LMRG_02730 Genetic deletion of LMRG_02730 resulted in an ablated membrane potential, indicative of a nonfunctional electron transport chain (ETC) and an inability to aerobically respire. Biochemical kinetic analysis of LMRG_02730 revealed strong activity toward DHNA-CoA, similar to its E. coli homolog, further demonstrating that LMRG_02730 is a DHNA-CoA thioesterase. Functional analyses in vitro , ex vivo , and in vivo using mutants directly downstream and upstream of LMRG_02730 revealed that DHNA-CoA is sufficient to facilitate in vitro growth in minimal medium, intracellular replication, and plaque formation in fibroblasts. In contrast, protection against bacteriolysis in the cytosol of macrophages and tissue-specific virulence in vivo requires the production of 1,4-dihydroxy-2-naphthoate (DHNA). Taken together, these data implicate LMRG_02730 (renamed MenI) as a DHNA-CoA thioesterase and suggest that while DHNA, or an unknown downstream product of DHNA, protects the bacteria from killing in the macrophage cytosol, DHNA-CoA is necessary for intracellular bacterial replication.

Titel:	Listeria monocytogenes MenI Encodes a DHNA-CoA Thioesterase Necessary for Menaquinone Biosynthesis, Cytosolic Survival, and Virulence.
Autor/in / Beteiligte Person:	Smith, HB ; Li, TL ; Liao, MK ; Chen, GY ; Guo, Z ; Sauer, JD
Link:	Full Text Finder (Volltext)
Zeitschrift:	Infection and immunity, Jg. 89 (2021-04-16), Heft 5
Veröffentlichung:	Washington, DC : American Society For Microbiology ; <i>Original Publication</i>: [Bethesda, Md.] American Society for Microbiology., 2021
Medientyp:	academicJournal
ISSN:	1098-5522 (electronic)
DOI:	10.1128/IAI.00792-20
Schlagwort:	Biosynthetic Pathways Escherichia coli Proteins genetics Escherichia coli Proteins metabolism Macrophages immunology Macrophages metabolism Microbial Viability Oxo-Acid-Lyases genetics Oxo-Acid-Lyases metabolism Sequence Deletion Thiolester Hydrolases genetics Virulence Listeria monocytogenes physiology Listeriosis microbiology Thiolester Hydrolases metabolism Vitamin K 2 metabolism
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't Language: English [Infect Immun] 2021 Apr 16; Vol. 89 (5). <i>Date of Electronic Publication: </i>2021 Apr 16 (<i>Print Publication: </i>2021). MeSH Terms: Listeria monocytogenes / physiology ; Listeriosis / microbiology ; Thiolester Hydrolases / metabolism ; Vitamin K 2 / metabolism ; Biosynthetic Pathways ; Escherichia coli Proteins / genetics ; Escherichia coli Proteins / metabolism ; Macrophages / immunology ; Macrophages / metabolism ; Microbial Viability ; Oxo-Acid-Lyases / genetics ; Oxo-Acid-Lyases / metabolism ; Sequence Deletion ; Thiolester Hydrolases / genetics ; Virulence References: Appl Microbiol Biotechnol. 2020 May;104(10):4397-4406. (PMID: 32193574) ; Infect Immun. 2003 Dec;71(12):6754-65. (PMID: 14638761) ; Elife. 2019 Jun 24;8:. (PMID: 31232690) ; Nat Rev Microbiol. 2009 Sep;7(9):623-8. (PMID: 19648949) ; Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6193-8. (PMID: 22474394) ; Mol Microbiol. 1993 Apr;8(1):143-57. (PMID: 8388529) ; Nature. 2018 Oct;562(7725):140-144. (PMID: 30209391) ; Nat Methods. 2012 Jun 28;9(7):676-82. (PMID: 22743772) ; J Bacteriol. 2013 Aug;195(15):3331-40. (PMID: 23687268) ; Infect Immun. 2004 Oct;72(10):5622-9. (PMID: 15385459) ; J Bacteriol. 2015 Feb;197(3):581-91. (PMID: 25422304) ; Infect Immun. 2019 Dec 17;88(1):. (PMID: 31685546) ; Appl Environ Microbiol. 2008 Jul;74(13):3921-34. (PMID: 18441118) ; Vitam Horm. 2001;61:173-218. (PMID: 11153266) ; Prev Nutr Food Sci. 2015 Mar;20(1):78-81. (PMID: 25866754) ; Infect Immun. 1990 Nov;58(11):3770-8. (PMID: 2172168) ; J Exp Med. 1988 Apr 1;167(4):1459-71. (PMID: 2833557) ; Metab Eng. 2002 Jul;4(3):230-7. (PMID: 12616692) ; Immunol Cell Biol. 2014 May-Jun;92(5):460-5. (PMID: 24518984) ; Gut. 2006 May;55(5):681-8. (PMID: 16299037) ; Cell Host Microbe. 2010 May 20;7(5):412-9. (PMID: 20417169) ; Biochemistry. 2008 Mar 18;47(11):3426-34. (PMID: 18284213) ; J Cell Biol. 1989 Oct;109(4 Pt 1):1597-608. (PMID: 2507553) ; Biosci Biotechnol Biochem. 2002 Mar;66(3):679-81. (PMID: 12005071) ; Appl Microbiol Biotechnol. 2004 Feb;63(5):571-7. (PMID: 12908086) ; Clin Microbiol Rev. 2001 Jul;14(3):584-640. (PMID: 11432815) ; Hepatol Commun. 2019 Apr 22;3(6):730-743. (PMID: 31168508) ; Biochemistry. 2009 Mar 3;48(8):1712-22. (PMID: 19193103) ; Microbes Infect. 2007 Aug;9(10):1236-43. (PMID: 17720602) ; J Infect Dis. 2004 Feb 1;189(3):393-401. (PMID: 14745696) ; BMC Bioinformatics. 2004 Aug 12;5:109. (PMID: 15307895) ; Front Immunol. 2018 Sep 19;9:2033. (PMID: 30283437) ; Cell Microbiol. 2017 Oct;19(10):. (PMID: 28656691) ; Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18745-50. (PMID: 17124169) ; J Exp Med. 1962 Sep 1;116:381-406. (PMID: 14467923) ; Immunity. 2015 Jan 20;42(1):145-58. (PMID: 25577440) ; Mol Microbiol. 2017 Apr;104(2):212-233. (PMID: 28097715) ; Toxicol Sci. 2017 Feb;155(2):458-473. (PMID: 27837168) ; Mol Microbiol. 2016 Oct;102(1):81-91. (PMID: 27328751) ; Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):12221-6. (PMID: 11572936) ; J Leukoc Biol. 2013 Sep;94(3):473-80. (PMID: 23801651) ; Nat Rev Microbiol. 2009 May;7(5):333-40. (PMID: 19369949) ; mBio. 2017 Mar 21;8(2):. (PMID: 28325762) ; Microbiology (Reading). 2002 Sep;148(Pt 9):2705-2715. (PMID: 12213917) ; Cell Microbiol. 2009 May;11(5):703-9. (PMID: 19191786) ; J Bacteriol. 2013 Jun;195(12):2768-75. (PMID: 23564174) Grant Information: R01 AI137070 United States AI NIAID NIH HHS; T32 GM007215 United States GM NIGMS NIH HHS Contributed Indexing: Keywords: 1,4-dihydroxy-2-naphthoate; Listeria monocytogenes; menaquinone; thioesterase Substance Nomenclature: 0 (Escherichia coli Proteins) ; 11032-49-8 (Vitamin K 2) ; EC 3.1.2.- (Thiolester Hydrolases) ; EC 4.1.3.- (1,4-dihydroxy-2-naphthoyl-CoA synthase, E coli) ; EC 4.1.3.- (Oxo-Acid-Lyases) Entry Date(s): Date Created: 20210223 Date Completed: 20210920 Latest Revision: 20211022 Update Code: 20231215 PubMed Central ID: PMC8091085

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Listeria monocytogenes MenI Encodes a DHNA-CoA Thioesterase Necessary for Menaquinone Biosynthesis, Cytosolic Survival, and Virulence.