Lipid flippases for bacterial peptidoglycan biosynthesis

Lipid Insights

Volumn 2015, Issue , 2015, Pages 21-31

  Ruiz, Natividad ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

MATE transporter; MOP exporter; Murein; MviN; YdaH

Indexed keywords

AMJ PROTEIN; BACTERIAL PROTEIN; FTSW PROTEIN; LIPID FLIPPASE; MEMBRANE PROTEIN; MURJ PROTEIN; PEPTIDOGLYCAN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM IDENTIFICATION; BIOSYNTHESIS; ESCHERICHIA COLI; MOLECULAR DYNAMICS; NONHUMAN; PEPTIDE ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

EID: 85013483827     PISSN: None     EISSN: 11786353     Source Type: Journal    
DOI: 10.4137/Lpi.s31783     Document Type: Article

References (105)

1. Vollmer W, Bertsche U. Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta. 2008;1778(9):1714-1734.
2. Vollmer W, Blanot D, de Pedro MA. Peptidoglycan structure and architecture. FEMS Microbiol Rev. 2008;32(2):149-167.
3. Typas A, Banzhaf M, Gross CA, et al. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol. 2012;10(2): 123-136.
4. Young KD. The selective value of bacterial shape. Microbiol Mol Biol Rev. 2006; 70(3):660-703.
5. Silhavy TJ, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harb Perspect Biol. 2010;2(5):a000414.
6. Sanyal S, Menon AK. Flipping lipids: why an' what's the reason for? ACS Chem Biol. 2009;4(11):895-909.
7. Chatterjee AN, Park JT. Biosynthesis of cell wall mucopeptide by a particulate fraction from Staphylococcus aureus. Proc Natl Acad Sci U S A. 1964;51:9-16.
8. Meadow PM, Anderson JS, Strominger JL. Enzymatic polymerization of UDPacetylmuramyl. L-ala.D-glu.L-lys.D-ala.D-ala and UDP-acetylglucosamine by a particulate enzyme from Staphylococcus aureus and its inhibition by antibiotics. Biochem Biophys Res Commun. 1964;14:382-387.
9. Barreteau H, Kovac A, Boniface A, et al. Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol Rev. 2008;32(2):168-207.
10. 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(15): 4625-4636.
11. Ikeda M, Wachi M, Jung HK, et al. The Escherichia coli mraY gene encoding UDP-N-acetylmuramoyl-pentapeptide: undecaprenyl-phosphate phospho-Nacetylmuramoyl- pentapeptide transferase. J Bacteriol. 1991;173(3):1021-1026.
12. Bouhss A, Trunkfield AE, Bugg TD, et al. The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev. 2008;32(2):208-233.
13. van Heijenoort J. Lipid intermediates in the biosynthesis of bacterial peptidoglycan. Microbiol Mol Biol Rev. 2007;71(4):620-635.
14. Van Heijenoort Y, Derrien M, Van Heijenoort J. Polymerization by transglycosylation in the biosynthesis of the peptidoglycan of Escherichia coli K 12 and its inhibition by antibiotics. FEBS Lett. 1978;89(1):141-144.
15. Broome-Smith JK, Edelman A, Yousif S, et al. The nucleotide sequences of the ponA and ponB genes encoding penicillin-binding protein 1A and 1B of Escherichia coli K12. Eur J Biochem. 1985;147(2):437-446.
16. Sauvage E, Kerff F, Terrak M, et al. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev. 2008;32(2):234-258.
17. Thorne KJ, Kodicek E. The structure of bactoprenol, a lipid formed by lactobacilli from mevalonic acid. Biochem J. 1966;99(1):123-127.
18. Anderson JS, Matsuhashi M, Haskin MA, et al. Biosynthesis of the peptidoglycan of bacterial cell walls. II. Phospholipid carriers in the reaction sequence. J Biol Chem. 1967;242(13):3180-3190.
19. Higashi Y, Strominger JL, Sweeley CC. Structure of a lipid intermediate in cell wall peptidoglycan synthesis: a derivative of a C55 isoprenoid alcohol. Proc Natl Acad Sci U S A. 1967;57(6):1878-1884.
20. Umbreit JN, Strominger JL. Isolation of the lipid intermediate in peptidoglycan biosynthesis from Escherichia coli. J Bacteriol. 1972;112(3):1306-1309.
21. Bupp K, van Heijenoort J. The final step of peptidoglycan subunit assembly in Escherichia coli occurs in the cytoplasm. J Bacteriol. 1993;175(6):1841-1843.
22. 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(11):3549-3557.
23. Kramer NE, Smid EJ, Kok J, et al. Resistance of Gram-positive bacteria to nisin is not determined by lipid II levels. FEMS Microbiol Lett. 2004;239(1): 157-161.
24. Pomorski T, Menon AK. Lipid flippases and their biological functions. Cell Mol Life Sci. 2006;63(24):2908-2921.
25. Islam ST, Lam JS. Wzx flippase-mediated membrane translocation of sugar polymer precursors in bacteria. Environ Microbiol. 2013;15(4):1001-1015.
26. Islam ST, Lam JS. Synthesis of bacterial polysaccharides via the Wzx/Wzydependent pathway. Can J Microbiol. 2014;60(11):697-716.
27. Cuthbertson L, Kos V, Whitfield C. ABC transporters involved in export of cell surface glycoconjugates. Microbiol Mol Biol Rev. 2010;74(3):341-362.
28. Greenfield LK, Whitfield C. Synthesis of lipopolysaccharide O-antigens by ABC transporter-dependent pathways. Carbohydr Res. 2012;356:12-24.
29. Willis LM, Whitfield C. Structure, biosynthesis, and function of bacterial capsular polysaccharides synthesized by ABC transporter-dependent pathways. Carbohydr Res. 2013;378:35-44.
30. Young KD. Microbiology. A flipping cell wall ferry. Science. 2014;345(6193): 139-140.
31. 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 U S A. 2015; 112(20):6437-6442.
32. Ruiz N. Bioinformatics identification of MurJ (MviN) as the peptidoglycan lipid II flippase in Escherichia coli. Proc Natl Acad Sci U S A. 2008;105(40): 15553-15557.
33. Ruiz N. Streptococcus pyogenes YtgP (Spy_0390) complements Escherichia coli strains depleted of the putative peptidoglycan flippase MurJ. Antimicrob Agents Chemother. 2009;53(8):3604-3605.
34. Butler EK, Davis RM, Bari V, et al. Structure-function analysis of MurJ reveals a solvent-exposed cavity containing residues essential for peptidoglycan biogenesis in Escherichia coli. J Bacteriol. 2013;195(20):4639-4649.
35. Butler EK, Tan WB, Joseph H, et al. Charge requirements of lipid II flippase activity in Escherichia coli. J Bacteriol. 2014;196(23):4111-4119.
36. 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(6193): 220-222.
37. de Boer PA. Advances in understanding E. coli cell fission. Curr Opin Microbiol. 2010;13(6):730-737.
38. Egan AJ, Vollmer W. The physiology of bacterial cell division. Ann N Y Acad Sci. 2013;1277:8-28.
39. Miyakawa T, Matsuzawa H, Matsuhashi M, et al. Cell wall peptidoglycan mutants of Escherichia coli K-12: existence of two clusters of genes, mra and mrb, for cell wall peptidoglycan biosynthesis. J Bacteriol. 1972;112(2):950-958.
40. Ishino F, Jung HK, Ikeda M, et al. New mutations fts-36, lts-33, and ftsW clustered in the mra region of the Escherichia coli chromosome induce thermosensitive cell growth and division. J Bacteriol. 1989;171(10):5523-5530.
41. Boyle DS, Khattar MM, Addinall SG, et al. ftsW is an essential cell-division gene in Escherichia coli. Mol Microbiol. 1997;24(6):1263-1273.
42. Wang L, Khattar MK, Donachie WD, et al. FtsI and FtsW are localized to the septum in Escherichia coli. J Bacteriol. 1998;180(11):2810-2816.
43. Mercer KL, Weiss DS. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J Bacteriol. 2002;184(4):904-912.
44. Fraipont C, Alexeeva S, Wolf B, et al. The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a subcomplex in Escherichia coli. Microbiology. 2011;157(pt 1):251-259.
45. Datta P, Dasgupta A, Singh AK, et al. Interaction between FtsW and penicillinbinding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol Microbiol. 2006;62(6):1655-1673.
46. Lara B, Ayala JA. Topological characterization of the essential Escherichia coli cell division protein FtsW. FEMS Microbiol Lett. 2002;216(1):23-32.
47. Ikeda M, Sato T, Wachi M, et al. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J Bacteriol. 1989;171(11):6375-6378.
48. Matsuzawa H, Hayakawa K, Sato T, et al. Characterization and genetic analysis of a mutant of Escherichia coli K-12 with rounded morphology. J Bacteriol. 1973;115(1):436-442.
49. Henriques AO, de Lencastre H, Piggot PJ. A Bacillus subtilis morphogene cluster that includes spoVE is homologous to the mra region of Escherichia coli. Biochimie. 1992;74(7-8):735-748.
50. Henriques AO, Glaser P, Piggot PJ, et al. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol Microbiol. 1998;28(2):235-247.
51. Holtje JV. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev. 1998;62(1):181-203.
52. Matsuhashi M. Utilization of lipid-linked precursors and the formation of peptidoglycan in the process of cell growth and division: membrane enzymes involved in the final steps of peptidoglycan synthesis and the mechanism of their regulation. In: Ghuysen J-M, Hakenbeck R, eds. Bacterial Cell Wall. Amsterdam: Elsevier Science B.V.; 1994:55-71.
53. Mohammadi T, Sijbrandi R, Lutters M, et al. Specificity of the transport of lipid II by FtsW in Escherichia coli. J Biol Chem. 2014;289(21):14707-14718.
54. Mohammadi T, van Dam V, Sijbrandi R, et al. Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. EMBO J. 2011;30(8):1425-1432.
55. Breukink E, van Heusden HE, Vollmerhaus PJ, et al. Lipid II is an intrinsic component of the pore induced by nisin in bacterial membranes. J Biol Chem. 2003;278(22):19898-19903.
56. van Dam V, Sijbrandi R, Kol M, et al. Transmembrane transport of peptidoglycan precursors across model and bacterial membranes. Mol Microbiol. 2007;64(4): 1105-1114.
57. McIntyre JC, Sleight RG. Fluorescence assay for phospholipid membrane asymmetry. Biochemistry. 1991;30(51):11819-11827.
58. Perkins HR. Specificity of combination between mucopeptide precursors and vancomycin or ristocetin. Biochem J. 1969;111(2):195-205.
59. Inoue A, Murata Y, Takahashi H, et al. Involvement of an essential gene, mviN, in murein synthesis in Escherichia coli. J Bacteriol. 2008;190(21):7298-7301.
60. Mohamed YF, Valvano MAA. Burkholderia cenocepacia MurJ (MviN) homolog is essential for cell wall peptidoglycan synthesis and bacterial viability. Glycobiology. 2014;24(6):564-576.
61. Ling JM, Moore RA, Surette MG, et al. The mviN homolog in Burkholderia pseudomallei is essential for viability and virulence. Can J Microbiol. 2006;52(9):831-842.
62. Rudnick PA, Arcondeguy T, Kennedy CK, et al. glnD and mviN are genes of an essential operon in Sinorhizobium meliloti. J Bacteriol. 2001;183(8):2682-2685.
63. Hvorup RN, Winnen B, Chang AB, et al. The multidrug/oligosaccharidyl-lipid/ polysaccharide (MOP) exporter superfamily. Eur J Biochem. 2003;270(5):799-813.
64. Long F, Rouquette-Loughlin C, Shafer WM, et al. Functional cloning and characterization of the multidrug efflux pumps NorM from Neisseria gonorrhoeae and YdhE from Escherichia coli. Antimicrob Agents Chemother. 2008;52(9):3052-3060.
65. Rouquette-Loughlin C, Dunham SA, Kuhn M, et al. The NorM efflux pump of Neisseria gonorrhoeae and Neisseria meningitidis recognizes antimicrobial cationic compounds. J Bacteriol. 2003;185(3):1101-1106.
66. Huda MN, Morita Y, Kuroda T, et al. Na+-driven multidrug efflux pump VcmA from Vibrio cholerae non-O1, a non-halophilic bacterium. FEMS Microbiol Lett. 2001;203(2):235-239.
67. Stevenson G, Andrianopoulos K, Hobbs M, et al. Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J Bacteriol. 1996;178(16):4885-4893.
68. Liu D, Cole RA, Reeves PR. An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J Bacteriol. 1996;178(7):2102-2107.
69. Islam ST, Eckford PD, Jones ML, et al. Proton-dependent gating and proton uptake by Wzx support O-antigen-subunit antiport across the bacterial inner membrane. MBio. 2013;4(5):e613-e678.
70. Islam ST, Fieldhouse RJ, Anderson EM, et al. A cationic lumen in the Wzx flippase mediates anionic O-antigen subunit translocation in Pseudomonas aeruginosa PAO1. Mol Microbiol. 2012;84(6):1165-1176.
71. Frank CG, Sanyal S, Rush JS, et al. Does Rft1 flip an N-glycan lipid precursor? Nature. 2008;454(7204):E3-E4. [discussion E4-E5].
72. Helenius J, Ng DT, Marolda CL, et al. Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein. Nature. 2002;415(6870):447-450.
73. Helenius J, Ng DTW, Marolda CL, et al. Does Rft1 flip an N-glycan lipid precursor? Reply. Nature. 2008;454(7204):E4-E5.
74. Rush JS, Gao N, Lehrman MA, et al. Suppression of Rft1 expression does not impair the transbilayer movement of Man5GlcNAc2-P-P-dolichol in sealed microsomes from yeast. J Biol Chem. 2009;284(30):19835-19842.
75. Jelk J, Gao N, Serricchio M, et al. Glycoprotein biosynthesis in a eukaryote lacking the membrane protein Rft1. J Biol Chem. 2013;288(28):20616-20623.
76. Kuroda T, Tsuchiya T. Multidrug efflux transporters in the MATE family. Biochim Biophys Acta. 2009;1794(5):763-768.
77. He X, Szewczyk P, Karyakin A, et al. Structure of a cation-bound multidrug and toxic compound extrusion transporter. Nature. 2010;467(7318):991-994.
78. Lu M, Radchenko M, Symersky J, et al. Structural insights into H+-coupled multidrug extrusion by a MATE transporter. Nat Struct Mol Biol. 2013;20(11):1310-1317.
79. Lu M, Symersky J, Radchenko M, et al. Structures of a Na+-coupled, substrate-bound MATE multidrug transporter. Proc Natl Acad Sci U S A. 2013;110(6):2099-2104.
80. Tanaka Y, Hipolito CJ, Maturana AD, et al. Structural basis for the drug extrusion mechanism by a MATE multidrug transporter. Nature. 2013;496(7444):247-251.
81. Radchenko M, Symersky J, Nie R, et al. Structural basis for the blockade of MATE multidrug efflux pumps. Nat Commun. 2015;6:7995.
82. Islam ST, Taylor VL, Qi M, et al. Membrane topology mapping of the O-antigen flippase (Wzx), polymerase (Wzy), and ligase (WaaL) from Pseudomonas aeruginosa PAO1 reveals novel domain architectures. MBio. 2010;1(3)e00189-10.
83. Thanassi JA, Hartman-Neumann SL, Dougherty TJ, et al. Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic Acids Res. 2002;30(14):3152-3162.
84. Zalacain M, Biswas S, Ingraham KA, et al. A global approach to identify novel broad-spectrum antibacterial targets among proteins of unknown function. J Mol Microbiol Biotechnol. 2003;6(2):109-126.
85. Vasudevan P, McElligott J, Attkisson C, et al. Homologues of the Bacillus subtilis SpoVB protein are involved in cell wall metabolism. J Bacteriol. 2009; 191(19):6012-6019.
86. Vasudevan P, Weaver A, Reichert ED, et al. Spore cortex formation in Bacillus subtilis is regulated by accumulation of peptidoglycan precursors under the control of sigma K. Mol Microbiol. 2007;65(6):1582-1594.
87. Fay A, Dworkin J. Bacillus subtilis homologs of MviN (MurJ), the putative Escherichia coli lipid II flippase, are not essential for growth. J Bacteriol. 2009; 191(19):6020-6028.
88. El Ghachi M, Bouhss A, Barreteau H, et al. Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. J Biol Chem. 2006;281(32):22761-22772.
89. Touze T, Barreteau H, El Ghachi M, et al. Colicin M, a peptidoglycan lipid- II-degrading enzyme: potential use for antibacterial means? Biochem Soc Trans. 2012;40(6):1522-1527.
90. Perez C, Gerber S, Boilevin J, et al. Structure and mechanism of an active lipidlinked oligosaccharide flippase. Nature. 2015;524(7566):433-438.
91. Eiamphungporn W, Helmann JD. The Bacillus subtilis sigma(M) regulon and its contribution to cell envelope stress responses. Mol Microbiol. 2008;67(4):830-848.
92. Jervis AJ, Thackray PD, Houston CW, et al. SigM-responsive genes of Bacillus subtilis and their promoters. J Bacteriol. 2007;189(12):4534-4538.
93. Cao M, Kobel PA, Morshedi MM, et al. Defining the Bacillus subtilis sigma(W) regulon: a comparative analysis of promoter consensus search, run-off transcription/ macroarray analysis (ROMA), and transcriptional profiling approaches. J Mol Biol. 2002;316(3):443-457.
94. Alaimo C, Catrein I, Morf L, et al. Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J. 2006;25(5):967-976.
95. Feldman MF, Marolda CL, Monteiro MA, et al. The activity of a putative polyisoprenol-linked sugar translocase (Wzx) involved in Escherichia coli O antigen assembly is independent of the chemical structure of the O repeat. J Biol Chem. 1999;274(49):35129-35138.
96. Hug I, Couturier MR, Rooker MM, et al. Helicobacter pylori lipopolysaccharide is synthesized via a novel pathway with an evolutionary connection to protein N-glycosylation. PLoS Pathog. 2010;6(3):e1000819.
97. Marolda CL, Vicarioli J, Valvano MA. Wzx proteins involved in biosynthesis of O antigen function in association with the first sugar of the O-specific lipopolysaccharide subunit. Microbiology. 2004;150(pt 12):4095-4105.
98. Hong Y, Reeves PR. Diversity of o-antigen repeat unit structures can account for the substantial sequence variation of wzx translocases. J Bacteriol. 2014; 196(9):1713-1722.
99. Hong Y, Cunneen MM, Reeves PR. The Wzx translocases for Salmonella enterica O-antigen processing have unexpected serotype specificity. Mol Microbiol. 2012; 84(4):620-630.
100. Liu MA, Stent TL, Hong Y, et al. Inefficient translocation of a truncated O unit by a Salmonella Wzx affects both O-antigen production and cell growth. FEMS Microbiol Lett. 2015;362(9):fnv053.
101. Yan A, Guan Z, Raetz CR. An undecaprenyl phosphate-aminoarabinose flippase required for polymyxin resistance in Escherichia coli. J Biol Chem. 2007;282(49): 36077-36089.
102. Jack DL, Yang NM, Saier MH Jr. The drug/metabolite transporter superfamily. Eur J Biochem. 2001;268(13):3620-3639.
103. Moreno MJ, Estronca LM, Vaz WL. Translocation of phospholipids and dithionite permeability in liquid-ordered and liquid-disordered membranes. Biophys J. 2006;91(3):873-881.
104. Grabowicz M, Andres D, Lebar MD, et al. A mutant Escherichia coli that attaches peptidoglycan to lipopolysaccharide and displays cell wall on its surface. Elife. 2014;3:e05334.
105. Raetz CR, Whitfield C. Lipopolysaccharide endotoxins. Annu Rev Biochem. 2002;71:635-700.