1,942
Views
13
CrossRef citations to date
0
Altmetric
Special Issue: Recent advances in isoprenoid studies (REVIEW)

Undecaprenyl phosphate metabolism in Gram-negative and Gram-positive bacteria

&
Pages 940-946 | Received 10 Sep 2017, Accepted 01 Nov 2017, Published online: 04 Dec 2017

References

  • Bouhss A, Trunkfield AE, Bugg TD, et al. The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev. 2008;32:208–233.10.1111/j.1574-6976.2007.00089.x
  • Samuel G, Reeves P. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr Res. 2003;338:2503–2519.10.1016/j.carres.2003.07.009
  • Mancuso DJ, Chiu TH. Biosynthesis of glucosyl monophosphoryl undecaprenol and its role in lipoteichoic acid biosynthesis. J Bacteriol. 1982;152:616–625.
  • Manat G, Roure S, Auger R, et al. Deciphering the metabolism of undecaprenyl-phosphate: the bacterial cell-wall unit carrier at the membrane frontier. Microb Drug Resit. 2014;20:199–214.10.1089/mdr.2014.0035
  • Hartley MD, Imperiali B. At the membrane frontier: a prospectus on the remarkable evolutionary conserveation of polyprenols and polyprenyl-phosphates. Arch Bichem Biophys. 2012;517:83–97.10.1016/j.abb.2011.10.018
  • Coker OO, Palittapongarnpim P. Current understanding of de novo synthesis of bacterial lipid carrier (undecaprenyl phosphate): more enzymes to be discovered. Afr J Microbiol Res. 2011;5:2555–2565.
  • Anderson JS, Matsuhashi M, Haskin MA, et al. Lipid-phosphoacetylmuramyl-pentapetide and lipid-phosphodisaccharide-pnetapeptide: presumed membrane transport intermediate in cell wall synthesis. Proc Natl Acad Sci USA. 1965;53:881–889.10.1073/pnas.53.4.881
  • Bugg TD, Lloyd AJ, Roper DI. Phospho-MurNAc-pnetapeptide translocase (MraY) as a target for antibacterial agents and antibacterial proteins. Infect Disord Drug Target. 2006;6:85–106.10.2174/187152606784112128
  • Mengin-Lecreulx D, Texier L, Rousseau M, et al. The murG gene of Escherichia coli codes for the UDP-N-acetylglucosamine:N-acetylmuramyl-(pentapeptide) pyrophosphoryl-undecaprenol N-acetylglucosamine transferase involved in the membrane steps of peptidoglycan synthesis. J Bacteriol. 1991;173:4625–4636.10.1128/jb.173.15.4625-4636.1991
  • Ruiz N. Bioinformatics identification of MurJ (MviN) as the peptidoglycan lipid II flippase in Escherichia coli. Proc Natl Acad Sci USA. 2008;105:15553–15557.10.1073/pnas.0808352105
  • Inoue A, Murata Y, Takahashi H, et al. Involvement of an essential gene, mviN, in murein synthesis in Escherichia coli. J Bacteriol. 2008;190:7298–7301.10.1128/JB.00551-08
  • Sham LT, Butler EK, Lebar MD, et al. Bacterial cell wall. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science. 2014;345:220–222.10.1126/science.1254522
  • Suzuki H, van Heijenoort Y, Tamura T, et al. In vitro peptidoglycan polymerization catalyzed by penicillin binding protein 1b of Escherichia coli K-12. FEBS Lett. 1980;110:245–249.10.1016/0014-5793(80)80083-4
  • van Heijenoort Y, Gomez M, Derrien M, et al. Membrane intermediates in the peptidoglycan metabolism of Escherichia coli: possible roles of PBP 1b and PBP 3. J Bacteriol. 1992;174:3549–3557.10.1128/jb.174.11.3549-3557.1992
  • Shimizu N, Koyama T, Ogura K. Molecular cloning, expression, and purification of undecaprenyl diphosphate synthase. No sequence similarity between E- and Z-prenyl diphosphate synthases. J Biol Chem. 1998;273:19476–19481.10.1074/jbc.273.31.19476
  • Koyama T. Molecular analysis of prenyl chain elongating enzymes. Biosci Biotech Biochem. 1999;63:1671–1676.10.1271/bbb.63.1671
  • Apfel CM, Takacs B, Fountoulakis M, et al. Use of genomics to identify bacterial undecaprenyl pyrophosphate synthetase: cloning, expression, and characterization of the essential uppS gene. J Bacteriol. 1999;181:483–492.
  • Kato J, Fujisaki S, Nakajima K, et al. The Escherichia coli homologue of yeast Rer2, a key enzyme of dolichol synthesis, is essential for the carrier lipid formation in bacterial cell wall synthesis. J Bacteriol. 1999;181:2733–2738.
  • Fujisaki S, Nishino T, Katsuki H. Biosynthesis of isoprenoids in intact cells of Escherichia coli. J Biochem. 1986;99:1137–1146.10.1093/oxfordjournals.jbchem.a135577
  • Barreteau H, Magnet S, El Ghachi M, et al. Quantitative high-performance liquid chromatography analysis of the pool levels of undecaprenyl phosphate and its derivatives in bacterial membranes. J Chromatogr B Analyt Technol Biomed Life Sci. 2009;877:213–220.10.1016/j.jchromb.2008.12.010
  • Higashi Y, Strominger JL, Sweeley CC. Biosynthesis of the peptidoglycan of bacterial cell walls. XXI. Isolation of free C55-isoprenoid alcohol of lipid in peptidoglycan synthesis from Staphylococcus aureus. J Biol Chem. 1970;245:3697–3702.
  • Gough DP, Kirby AL, Richards JB, et al. The characterization of undecaprenol of Lactobacillus plantarum. Biochem J. 1970;118:167–170.10.1042/bj1180167
  • Thorne KJ. Identification of prenol intermediates of wall biosynthesis in growing cells of Lactobacillus plantarum. J Bacteriol. 1973;116:235–244.
  • Lis M, Kuramitsu HK. The stress-responsive dgk gene from Streptococcus mutans encodes a putative undecaprenol kinase activity. Infect Immun. 2003;71:1938–1943.10.1128/IAI.71.4.1938-1943.2003
  • Jerga A, Lu YJ, Schujman GE, et al. Identification of a soluble diacylglycerol kinase required for lipoteichoic acid production in Bacillus subtilis. J Biol Chem. 2007;282:21738–21745.10.1074/jbc.M703536200
  • El Ghachi M, Bouhss A, Blanot D, et al. The bacA gene of Escherichia coli encodes an undecaprenyl pyrophosphate phosphatase activity. J Biol Chem. 2004;279:30106–30113.10.1074/jbc.M401701200
  • Chang HY, Chou CC, Hsu MF, et al. Proposed carrier lipid-binding site of undecaprenyl pyrophosphate phosphatase from Escherichia coli. J Biol Chem. 2014;289:18719–18735.10.1074/jbc.M114.575076
  • Manat G, El Ghachi M, Auger R, et al. Membrane topology and biochemical characterization of the Escherichia coli BacA undecaprenyl-pyrophosphate phosphatase. PLoS One. 2015;10:e0142870.10.1371/journal.pone.0142870
  • Bickford JS, Nick HS. Conservation of the PTEN catalytic motif in the bacterial undecaprenyl pyrophosphate phosphatase, BacA/UppP. Microbiology. 2013;159:2444–2455.10.1099/mic.0.070474-0
  • Chang HY, Chou CC, Wu ML, et al. Expression, purification and enzymatic characterization of undecaprenyl pyrophosphate phosphatase from Vibrio vulnificus. Protein Expr Purif. 2017;133:121–131.10.1016/j.pep.2017.01.015
  • El Ghachi M, Derbise A, Bouhss A, et al. Identification of multiple genes encoding membrane proteins with undecaprenyl pyrophosphate phosphatase (UppP) activity in Escherichia coli. J Biol Chem. 2005;280:18689–18695.10.1074/jbc.M412277200
  • Zhao H, Sun Y, Peters JM, et al. Depletion of undecaprenyl pyrophosphate phosphatases disrupts cell envelope biogenesis in Bacillus subtilis. J Bacteriol. 2016;198:2925–2935.10.1128/JB.00507-16
  • Lu YH, Guan Z, Zhao J, et al. Three phosphatidylglycerol-phosphate phosphatases in the inner membrane of Escherichia coli. J Biol Chem. 2011;286:5506–5518.10.1074/jbc.M110.199265
  • Icho T, Raetz CR. Multiple genes for membrane-bound phosphatases in Escherichia coli and their action on phospholipid precursors. J Bacteriol. 1983;153:722–730.
  • Touzé T, Blanot D, Mengin-Lecreulx D. Substrate specificity and membrane topology of Escherichia coli PgpB, an undecaprenyl pyrophosphate phosphatase. J Biol Chem. 2008;283:16573–16583.10.1074/jbc.M800394200
  • Touzé T, Tran AX, Hankins JV, et al. Periplasmic phosphorylation of lipid A is linked to the synthesis of undecaprenyl phosphate. Mol Microbiol. 2008;67:264–277.
  • Ghachi EM, Howe N, Auger R, et al. Crystal structure and biochemical characterization of the transmembrane PAP2 type phosphatidylglycerol phosphate phosphatase from Bacillus subtilis. Cell Mol Life Sci. 2017;74:2319–2332.10.1007/s00018-017-2464-6
  • Tatar LD, Marolda CL, Polischuk AN, et al. An Escherichia coli undecaprenyl- pyrophosphate phosphatase implicated in undecaprenyl phosphate recycling. Microbiology. 2007;153:2518–2529.10.1099/mic.0.2007/006312-0
  • Fan J, Jiang D, Zhao Y, et al. Crystal structure of lipid phosphatase Escherichia coli phosphatidylglycerophosphate phosphatase B. Proc Natl Acad Sci USA. 2014;111:7636–7640.10.1073/pnas.1403097111
  • Stukey J, Carman GM. Identification of a novel phosphatase sequence motif. Protein Sci. 1997;6:469–472.
  • Neuwald AF. An unexpected structural relationship between integral membrane phosphatases and soluble haloperoxidases. Protein Sci. 1997;6:1764–1767.10.1002/pro.v6:8
  • Cain BD, Norton PJ, Eubanks W, et al. Amplification of the bacA gene confers bacitracin resistance to Escherichia coli. J Bacteriol. 1993;175:3784–3789.10.1128/jb.175.12.3784-3789.1993
  • Bernard R, El Ghachi M, Mengin-Lecreulx D, et al. BcrC from Bacillus subtilis acts as an undecaprenyl pyrophosphate phosphatase in bacitracin resistance. J Biol Chem. 2005;280:28852–28857.10.1074/jbc.M413750200
  • Inaoka T, Ochi K. Undecaprenyl pyrophosphate involvement in susceptibility of Bacillus subtilis to rare earth elements. J Bacteriol. 2012;194:5632–5637.10.1128/JB.01147-12
  • Meeske AJ, Rodrigues CD, Brady J, et al. High-throughput genetic screens identify a large and diverse collection of new sporulation genes in Bacillus subtilis. PLoS Biol. 2016;14:e1002341.10.1371/journal.pbio.1002341
  • Chalker AF, Ingraham KA, Lunsford RD, et al. The bacA gene, which determines bacitracin susceptibility in Streptococcus pneumoniae and Staphylococcus aureus, is also required for virulence. Microbiology. 2000;146:1547–1553.10.1099/00221287-146-7-1547
  • Jalal N, Tian XL, Dong G, et al. Identification and characterization of SMU.244 encoding a putative undecaprenyl pyrophosphate phosphatase protein required for cell wall biosynthesis and bacitracin resistance in Streptococcus mutans. Microbiology. 2015;161:1857–1870.10.1099/mic.0.000142
  • Shaaly A, Kalamorz F, Gebhard S, et al. Undecaprenyl pyrophosphate phosphatase confers low-level resistance to bacitracin in Enterococcus faecalis. J Antimicrob Chemother. 2013;68:1583–1593.10.1093/jac/dkt048
  • Saito Y, Ishikawa T, Murakami M, et al. Mutant deletions in Escherichia coli affect the cellular levels of undecaprenyl phosphate and undecaprenyl diphosphate. J Biol Macromol. 2013;13:86–91.
  • Sandermann H Jr, Strominger JL. Purification and properties of C55-isoprenoid alcohol phosphokinase from Staphylococcus aureus. J Biol Chem. 1972;247:5123–5131.
  • Higashi Y, Siewert G, Strominger JL. Biosynthesis of the peptidoglycan of bacterial cell walls. XIX. Isoprenoid alcohol phosphokinase. J Biol Chem. 1970;245:3683–3690.
  • Higashi Y, Strominger JL. Biosynthesis of the peptidoglycan of bacterial cell walls. XX. Identification of phosphatidylglycerol and cardiolipin as cofactors for isoprenoid alcohol phosphokinase. J Biol Chem. 1970;245:3691–3696.
  • Kalin JR, Allen CM Jr. Characterization of undecaprenol kinase from Lactobacillus plantarum. Biochim Biophys Acta. 1979;574:112–122.10.1016/0005-2760(79)90090-0
  • Kalin JR, Allen CM. Lipid activation of undecaprenol kinase from Lactobacillus plantarum. Biochim Biophys Acta. 1980;619:76–89.10.1016/0005-2760(80)90244-1
  • Huang LY, Huang SH, Chang YC, et al. Enzymatic synthesis of lipid II and analogues. Angew Chem Int Ed Engl. 2014;53:8060–8065.10.1002/anie.201402313
  • Van Horn WD, Sanders CR. Prokaryotic Diacylglycerol kinase and undecaprenol kinase. Annu Rev Biophys. 2012;41:81–101.10.1146/annurev-biophys-050511-102330
  • Li D, Stansfeld PJ, Sansom MS, et al. Ternary structure reveals mechanism of a membrane diacylglycerol kinase. Nat Commun. 2015;6:10140.10.1038/ncomms10140
  • Wen J, Chen X, Bowie JU. Exploring the allowed sequence space of a membrane protein. Nat Struct Biol. 1996;3:141–148.10.1038/nsb0296-141
  • Van Horn WD, Kim HJ, Ellis CD, et al. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science. 2009;324:1726–1729.10.1126/science.1171716
  • Shibata Y, van der Ploeg JR, Kozuki T, et al. Kinase activity of the dgk gene product is involved in the virulence of Streptococcus mutans. Microbiology. 2009;155:557–565.10.1099/mic.0.023812-0
  • Lis M, Kuramitsu HK. Characterization of a suppressor mutation complementing an acid-sensitive mutation in Streptococcus mutans. FEMS Microbiol. Lett. 2003;229:179–182.10.1016/S0378-1097(03)00818-8
  • Chen P, Novak J, Qi F, et al. Diacylglycerol kinase is involved in regulation of expression of the lantibiotic mutacin II of Streptococcus mutans. J Bacteriol. 1998;180:167–170.
  • Amiteye S, Kobayashi K, Imamura D, et al. Bacillus subtilis diacylglycerol kinase (DgkA) enhances efficient sporulation. J Bacteriol. 2003;185:5306–5309.10.1128/JB.185.17.5306-5309.2003
  • Nishibori A, Kusaka J, Hara H, et al. Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes. J Bacteriol. 2005;187:2163–2174.10.1128/JB.187.6.2163-2174.2005
  • Matsumoto K, Kusaka J, Nishibori A, et al. Lipid domains in bacterial membranes. Mol Microbiol. 2006;61:1110–1117.10.1111/mmi.2006.61.issue-5
  • Huang LY, Wang SC, Cheng TJR, et al. The undecaprenyl phosphate phosphatase activety of undecaprenol kinase regulates the lipid pool in Gram positive bacteria. Biochemistry. 2017;56:5417–5427.10.1021/acs.biochem.7b00603
  • Mengin-Lecreulx D, van Heijenoort J. Effect of growth conditions on peptidoglycan content and cytoplasmic steps of its biosynthesis in Escherichia coli. J Bacteriol. 1985;163:208–212.
  • Meeske AJ, Sham LT, Kimsey H, et al. MurJ and a novel lipid II flippase are required for cell wall biogenesis in Bacillus subtilis. Proc Natl Acad Sci USA. 2015;112:6437–6442.10.1073/pnas.1504967112
  • Rick PD, Barr K, Sankaran K, et al. Evidence that the wzxE gene of Escherichia coli K-12 encodes a protein involved in the transbilayer movement of a trisaccharide-lipid intermediate in the assembly of enterobacterial common antigen. J Biol Chem. 2003;278:16534–16542.10.1074/jbc.M301750200
  • Bohnenberger E, Sandermann H. Dephosphoryltion of C55-isoprenyl-monophosphate by non-specific phosphatases. FEBS Lett. 1976;67:85–89.10.1016/0014-5793(76)80875-7
  • Bramkamp M, Lopez D. Exploring the existence of lipid raft in bacteria. Microbiol Mol Biol Rev. 2015;79:81–100.10.1128/MMBR.00036-14
  • Lopéz D, Kolter R. Functional microdomains in bacterial membranes. Genes Dev. 2010;24:1893–1902.10.1101/gad.1945010
  • Diep BA, Gill SR, Chang RF, et al. Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. Lancet. 2006;367:731–739.10.1016/S0140-6736(06)68231-7

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.