Proteomic analysis of Escherichia coli detergent-resistant membranes (DRM)

English version

Autoři: José E. Guzmán-Flores ^aff001; Lidia Steinemann-Hernández ^aff001; Luis E. González de la Vara ^aff002; Marina Gavilanes-Ruiz ^aff003; Tony Romeo ^aff004; Adrián F. Alvarez ^aff001; Dimitris Georgellis ^aff001
Působiště autorů: Departamento de Genética Molecular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México City, México ^aff001; Departamento de Biotecnología y Bioquímica, Unidad Irapuato, Cinvestav-IPN, Irapuato, Gto, México ^aff002; Departamento de Bioquímica, Facultad de Química, Universidad Nacional Autónoma de México, Mexico City, México ^aff003; Department of Microbiology and Cell Science, IFAS, University of Florida, Gainesville, Florida, United States of America ^aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223794

Souhrn

Membrane microdomains or lipid rafts compartmentalize cellular processes by laterally organizing membrane components. Such sub-membrane structures were mainly described in eukaryotic cells, but, recently, also in bacteria. Here, the protein content of lipid rafts in Escherichia coli was explored by mass spectrometry analyses of Detergent Resistant Membranes (DRM). We report that at least three of the four E. coli flotillin homologous proteins were found to reside in DRM, along with 77 more proteins. Moreover, the proteomic data were validated by subcellular localization, using immunoblot assays and fluorescence microscopy of selected proteins. Our results confirm the existence of lipid raft-like microdomains in the inner membrane of E. coli and represent the first comprehensive profiling of proteins in these bacterial membrane platforms.

Klíčová slova:

Cell membranes – Lipids – Lipoproteins – Membrane proteins – Outer membrane proteins – Signal peptides – Integral membrane proteins – Transmembrane transport proteins

Zdroje

1. Astro V, de Curtis I. Plasma membrane-associated platforms: dynamic scaffolds that organize membrane-associated events. Sci Signal. 2015;8: re1. doi: 10.1126/scisignal.aaa3312 25759479

2. Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science. 2010;327: 46–50. doi: 10.1126/science.1174621 20044567

3. Browman DT, Hoegg MB, Robbins SM. The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol. 2007;17: 394–402. doi: 10.1016/j.tcb.2007.06.005 17766116

4. Langhorst MF, Reuter A, Stuermer CAO. Scaffolding microdomains and beyond: the function of reggie/flotillin proteins. Cell Mol Life Sci. 2005;62: 2228–2240. doi: 10.1007/s00018-005-5166-4 16091845

5. Morrow IC, Parton RG. Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic. 2005;6: 725–740. doi: 10.1111/j.1600-0854.2005.00318.x 16101677

6. Kato N, Nakanishi M, Hirashima N. Flotillin-1 regulates IgE receptor-mediated signaling in rat basophilic leukemia (RBL-2H3) cells. J Immunol. 2006;177: 147–154. doi: 10.4049/jimmunol.177.1.147 16785509

7. Langhorst MF, Solis GP, Hannbeck S, Plattner H, Stuermer CAO. Linking membrane microdomains to the cytoskeleton: Regulation of the lateral mobility of reggie-1/flotillin-2 by interaction with actin. FEBS Lett. 2007;581: 4697–4703. doi: 10.1016/j.febslet.2007.08.074 17854803

8. Bach JN, Bramkamp M. Flotillins functionally organize the bacterial membrane. Mol Microbiol. 2013;88: 1205–1217. doi: 10.1111/mmi.12252 23651456

9. López D, Kolter R. Functional microdomains in bacterial membranes. Genes Dev. 2010;24: 1893–1902. doi: 10.1101/gad.1945010 20713508

10. Schneider J, Mielich-Süss B, Böhme R, Lopez D. In vivo characterization of the scaffold activity of flotillin on the membrane kinase KinC of Bacillus subtilis. Microbiology. 2015;161: 1871–1887. doi: 10.1099/mic.0.000137 26297017

11. Schneider J, Klein T, Mielich-Süss B, Koch G, Franke C, Kuipers OP, et al. Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium. Casadesús J, editor. PLOS Genet. 2015;11: e1005140. doi: 10.1371/journal.pgen.1005140 25909364

12. Feng X, Hu Y, Zheng Y, Zhu W, Li K, Huang C-H, et al. Structural and functional analysis of Bacillus subtilis YisP reveals a role of its product in biofilm production. Chem Biol. 2014;21: 1557–1563. doi: 10.1016/j.chembiol.2014.08.018 25308276

13. Mielich-Süss B, Wagner RM, Mietrach N, Hertlein T, Marincola G, Ohlsen K, et al. Flotillin scaffold activity contributes to type VII secretion system assembly in Staphylococcus aureus. PLOS Pathog. 2017;13: e1006728. doi: 10.1371/journal.ppat.1006728 29166667

14. Somani VK, Aggarwal S, Singh D, Prasad T, Bhatnagar R. Identification of novel raft marker protein, FlotP in Bacillus anthracis. Front Microbiol. 2016;7: 169. doi: 10.3389/fmicb.2016.00169 26925042

15. LaRocca TJ, Pathak P, Chiantia S, Toledo A, Silvius JR, Benach JL, et al. Proving lipid rafts exist: membrane domains in the prokaryote Borrelia burgdorferi have the same properties as eukaryotic lipid rafts. PLOS Pathog. 2013;9: e1003353. doi: 10.1371/journal.ppat.1003353 23696733

16. Hutton ML, D’Costa K, Rossiter AE, Wang L, Turner L, Steer DL, et al. A Helicobacter pylori homolog of eukaryotic flotillin is involved in cholesterol accumulation, epithelial cell responses and host colonization. Front Cell Infect Microbiol. 2017;7: 219. doi: 10.3389/fcimb.2017.00219 28634572

17. Guzmán-Flores JE, Alvarez AF, Poggio S, Gavilanes-Ruiz M, Georgellis D. Isolation of detergent-resistant membranes (DRMs) from Escherichia coli. Anal Biochem. 2017;518: 1–8. doi: 10.1016/j.ab.2016.10.025 27984012

18. Staneva G, Seigneuret M, Koumanov K, Trugnan G, Angelova MI. Detergents induce raft-like domains budding and fission from giant unilamellar heterogeneous vesicles: A direct microscopy observation. Chem Phys Lipids. 2005;136: 55–66. doi: 10.1016/j.chemphyslip.2005.03.007 15927174

19. Brown DA. Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda). 2006;21: 430–439. doi: 10.1152/physiol.00032.2006 17119156

20. Yepes A, Schneider J, Mielich B, Koch G, García-Betancur J-C, Ramamurthi KS, et al. The biofilm formation defect of a Bacillus subtilis flotillin-defective mutant involves the protease FtsH. Mol Microbiol. 2012;86: 457–471. doi: 10.1111/j.1365-2958.2012.08205.x 22882210

21. Toledo A, Pérez A, Coleman JL, Benach JL. The lipid raft proteome of Borrelia burgdorferi. Proteomics. 2015;15: 3662–3675. doi: 10.1002/pmic.201500093 26256460

22. García-Fernández E, Koch G, Wagner RM, Fekete A, Stengel ST, Schneider J, et al. Membrane Microdomain Disassembly Inhibits MRSA Antibiotic Resistance. Cell. 2017; doi: 10.1016/j.cell.2017.10.012 29103614

23. Toledo A, Huang Z, Coleman JL, London E, Benach JL. Lipid rafts can form in the inner and outer membranes of Borrelia burgdorferi and have different properties and associated proteins. Mol Microbiol. 2018;108: 63–76. doi: 10.1111/mmi.13914 29377398

24. Zhang N, Chen R, Young N, Wishart D, Winter P, Weiner JH, et al. Comparison of SDS- and methanol-assisted protein solubilization and digestion methods for Escherichia coli membrane proteome analysis by 2-D LC-MS/MS. Proteomics. 2007;7: 484–493. doi: 10.1002/pmic.200600518 17309111

25. Bernsel A, Daley DO. Exploring the inner membrane proteome of Escherichia coli: which proteins are eluding detection and why? Trends Microbiol. 2009;17: 444–449. doi: 10.1016/j.tim.2009.07.005 19766000

26. Masuda T, Saito N, Tomita M, Ishihama Y. Unbiased quantitation of Escherichia coli membrane proteome using phase transfer surfactants. Mol Cell Proteomics. 2009;8: 2770–7. doi: 10.1074/mcp.M900240-MCP200 19767571

27. Papanastasiou M, Orfanoudaki G, Koukaki M, Kountourakis N, Sardis MF, Aivaliotis M, et al. The Escherichia coli peripheral inner membrane proteome. Mol Cell Proteomics. 2013;12: 599–610. doi: 10.1074/mcp.M112.024711 23230279

28. Lee H-L, Chiang I-C, Liang S-Y, Lee D-Y, Chang G-D, Wang K-Y, et al. Quantitative Proteomics Analysis Reveals the Min System of Escherichia coli Modulates Reversible Protein Association with the Inner Membrane. Mol Cell Proteomics. 2016;15: 1572–83. doi: 10.1074/mcp.M115.053603 26889046

29. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000;97: 6640–6645. doi: 10.1073/pnas.120163297 10829079

30. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L. Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A. 2001;98: 15264–15269. doi: 10.1073/pnas.261348198 11742086

31. Thanbichler M, Iniesta AA, Shapiro L. A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus. Nucleic Acids Res. 2007;35: e137. doi: 10.1093/nar/gkm818 17959646

32. Peña-Sandoval GR, Kwon O, Georgellis D. Requirement of the receiver and phosphotransfer domains of ArcB for efficient dephosphorylation of phosphorylated ArcA in vivo. J Bacteriol. 2005;187: 3267–3272. doi: 10.1128/JB.187.9.3267-3272.2005 15838055

33. Dykxhoorn DM, St Pierre R, Linn T. A set of compatible tac promoter expression vectors. Gene. 1996;177: 133–136. Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=8921858 8921858

34. He L, Diedrich J, Chu YY, Yates JR. Extracting Accurate Precursor Information for Tandem Mass Spectra by RawConverter. Anal Chem. 2015;87: 11361–11367. doi: 10.1021/acs.analchem.5b02721 26499134

35. Deutsch EW, Mendoza L, Shteynberg D, Farrah T, Lam H, Tasman N, et al. A guided tour of the Trans-Proteomic Pipeline [Internet]. Proteomics. WILEY-VCH Verlag; 2010. pp. 1150–1159.

36. Tsirigos KD, Peters C, Shu N, All L, Elofsson A. The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Res. 2015;43. doi: 10.1093/nar/gkv485 25969446

37. Juncker AS, Willenbrock H, von Heijne G, Brunak S, Nielsen H, Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 2003;12: 1652–1662. doi: 10.1110/ps.0303703 12876315

38. Combet C, Blanchet C, Geourjon C, Deléage G. NPS@: Network protein sequence analysis. Trends Biochem Sci. 2000;25: 147–150. doi: 10.1016/s0968-0004(99)01540-6 10694887

39. Sambrook J, Russell DW. Molecular cloning: a Laboratory Manual. 3rd ed. NY: Cold Spring Harbor Laboratory: Cold Spring Harbor; 2001.

40. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9: 671–675. doi: 10.1038/nmeth.2089 22930834

41. Lopez D, Koch G. Exploring functional membrane microdomains in bacteria: an overview. Curr Opin Microbiol. 2017;36: 76–84. doi: 10.1016/j.mib.2017.02.001 28237903

42. Thein M, Sauer G, Paramasivam N, Grin I, Linke D. Efficient subfractionation of gram-negative bacteria for proteomics studies. J Proteome Res. 2010;9: 6135–6147. doi: 10.1021/pr1002438 20932056

43. Emiola A, Andrews SS, Heller C, George J. Crosstalk between the lipopolysaccharide and phospholipid pathways during outer membrane biogenesis in Escherichia coli. Proc Natl Acad Sci. 2016;113: 3108–3113. doi: 10.1073/pnas.1521168113 26929331

44. Lai EC. Lipid rafts make for slippery platforms. J Cell Biol. 2003;162: 365–370. doi: 10.1083/jcb.200307087 12885764

45. Kenworthy AK, Nichols BJ, Remmert CL, Hendrix GM, Kumar M, Zimmerberg J, et al. Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol. 2004;165: 735–746. doi: 10.1083/jcb.200312170 15173190

46. Klappe K, Hummel I, Hoekstra D, Kok JW. Lipid dependence of ABC transporter localization and function. Chem Phys Lipids. 2009;161: 57–64. doi: 10.1016/j.chemphyslip.2009.07.004 19651114

47. Zhou Z, White KA, Polissi A, Georgopoulos C, Raetz CRH. Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem. 1998;273: 12466–12475. doi: 10.1074/jbc.273.20.12466 9575204

48. Karow M, Georgopoulos C. The essential Escherichia coli msbA gene, a multicopy suppressor of null mutations in the htrB gene, is related to the universally conserved family of ATP-dependent translocators. Mol Microbiol. 1993;7: 69–79. doi: 10.1111/j.1365-2958.1993.tb01098.x 8094880

49. Yun UJ, Lee JH, Koo KH, Ye SK, Kim SY, Lee CH, et al. Lipid raft modulation by Rp1 reverses multidrug resistance via inactivating MDR-1 and Src inhibition. Biochem Pharmacol. 2013;85: 1441–1453. doi: 10.1016/j.bcp.2013.02.025 23473805

50. Allen JA, Halverson-Tamboli RA, Rasenick MM. Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci. 2007;8: 128–140. doi: 10.1038/nrn2059 17195035

51. Sáenz JP, Grosser D, Bradley AS, Lagny TJ, Lavrynenko O, Broda M, et al. Hopanoids as functional analogues of cholesterol in bacterial membranes. Proc Natl Acad Sci U S A. 2015;112: 11971–6. doi: 10.1073/pnas.1515607112 26351677

Proteomic analysis of Escherichia coli detergent-resistant membranes (DRM)

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