#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium


Cellular membranes organize proteins related to signal transduction, protein sorting and membrane trafficking into the so-called lipid rafts. It has been proposed that the functional diversity of lipid rafts would require a heterogeneous population of raft domains with varying compositions. However, a mechanism for such diversification is not known due in part to the complexity that entails the manipulation of eukaryotic cells. The recent discovery that bacteria organize many cellular processes in membrane microdomains (FMMs), functionally similar to the eukaryotic lipid rafts, prompted us to explore FMMs diversity in the bacterial model Bacillus subtilis. We show that diversification of FMMs occurs in cells and gives rise to functionally distinct microdomains, which compartmentalize distinct signal transduction pathways and regulate the expression of different genetic programs. We discovered that FMMs diversification does not occur randomly. Cells sequentially regulate the specialization of the FMMs during cell growth to ensure an effective and diverse activation of signaling processes.


Vyšlo v časopise: Spatio-temporal Remodeling of Functional Membrane Microdomains Organizes the Signaling Networks of a Bacterium. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005140
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005140

Souhrn

Cellular membranes organize proteins related to signal transduction, protein sorting and membrane trafficking into the so-called lipid rafts. It has been proposed that the functional diversity of lipid rafts would require a heterogeneous population of raft domains with varying compositions. However, a mechanism for such diversification is not known due in part to the complexity that entails the manipulation of eukaryotic cells. The recent discovery that bacteria organize many cellular processes in membrane microdomains (FMMs), functionally similar to the eukaryotic lipid rafts, prompted us to explore FMMs diversity in the bacterial model Bacillus subtilis. We show that diversification of FMMs occurs in cells and gives rise to functionally distinct microdomains, which compartmentalize distinct signal transduction pathways and regulate the expression of different genetic programs. We discovered that FMMs diversification does not occur randomly. Cells sequentially regulate the specialization of the FMMs during cell growth to ensure an effective and diverse activation of signaling processes.


Zdroje

1. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387: 569–572. 9177342

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

3. Neumann AK, Itano MS, Jacobson K (2010) Understanding lipid rafts and other related membrane domains. F1000 Biol Rep 2: 31. doi: 10.3410/B2-31 20606718

4. Lingwood D, Kaiser HJ, Levental I, Simons K (2009) Lipid rafts as functional heterogeneity in cell membranes. Biochem Soc Trans 37: 955–960. doi: 10.1042/BST0370955 19754431

5. Mishra S, Joshi PG (2007) Lipid raft heterogeneity: an enigma. J Neurochem 103 Suppl 1: 135–142. 17986148

6. Dermine JF, Duclos S, Garin J, St-Louis F, Rea S, et al. (2001) Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J Biol Chem 276: 18507–18512. 11279173

7. Lang DM, Lommel S, Jung M, Ankerhold R, Petrausch B, et al. (1998) Identification of reggie-1 and reggie-2 as plasmamembrane-associated proteins which cocluster with activated GPI-anchored cell adhesion molecules in non-caveolar micropatches in neurons. J Neurobiol 37: 502–523. 9858255

8. Langhorst MF, Reuter A, Stuermer CA (2005) Scaffolding microdomains and beyond: the function of reggie/flotillin proteins. Cell Mol Life Sci 62: 2228–2240. 16091845

9. Morrow IC, Parton RG (2005) Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic 6: 725–740. 16101677

10. Stuermer CA (2011) Reggie/flotillin and the targeted delivery of cargo. J Neurochem 116: 708–713. doi: 10.1111/j.1471-4159.2010.07007.x 21214550

11. Michel V, Bakovic M (2007) Lipid rafts in health and disease. Biol Cell 99: 129–140. 17064251

12. Lopez D, Kolter R (2010) Functional microdomains in bacterial membranes. Genes Dev 24: 1893–1902. doi: 10.1101/gad.1945010 20713508

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

14. Dempwolff F, Moller HM, Graumann PL (2012) Synthetic motility and cell shape defects associated with deletions of flotillin/reggie paralogs in Bacillus subtilis and interplay of these proteins with NfeD proteins. J Bacteriol 194: 4652–4661. doi: 10.1128/JB.00910-12 22753055

15. Donovan C, Bramkamp M (2009) Characterization and subcellular localization of a bacterial flotillin homologue. Microbiology 155: 1786–1799. doi: 10.1099/mic.0.025312-0 19383680

16. Mielich-Suss B, Schneider J, Lopez D (2013) Overproduction of flotillin influences cell differentiation and shape in Bacillus subtilis. MBio 4: e00719–00713. doi: 10.1128/mBio.00719-13 24222488

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

18. Babuke T, Ruonala M, Meister M, Amaddii M, Genzler C, et al. (2009) Hetero-oligomerization of reggie-1/flotillin-2 and reggie-2/flotillin-1 is required for their endocytosis. Cell Signal 21: 1287–1297. doi: 10.1016/j.cellsig.2009.03.012 19318123

19. Banning A, Tomasovic A, Tikkanen R (2011) Functional aspects of membrane association of reggie/flotillin proteins. Curr Protein Pept Sci 12: 725–735. 22329548

20. Amaddii M, Meister M, Banning A, Tomasovic A, Mooz J, et al. (2012) Flotillin-1/reggie-2 protein plays dual role in activation of receptor-tyrosine kinase/mitogen-activated protein kinase signaling. J Biol Chem 287: 7265–7278. doi: 10.1074/jbc.M111.287599 22232557

21. Nicolas P, Mader U, Dervyn E, Rochat T, Leduc A, et al. (2012) Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335: 1103–1106. doi: 10.1126/science.1206848 22383849

22. Buescher JM, Liebermeister W, Jules M, Uhr M, Muntel J, et al. (2012) Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science 335: 1099–1103. doi: 10.1126/science.1206871 22383848

23. Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A 98: 11621–11626. 11572999

24. Lopez D, Gontang EA, Kolter R (2010) Potassium sensing histidine kinase in Bacillus subtilis. Methods Enzymol 471: 229–251. doi: 10.1016/S0076-6879(10)71013-2 20946851

25. Hamon MA, Lazazzera BA (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42: 1199–1209. 11886552

26. Hahn J, Roggiani M, Dubnau D (1995) The major role of Spo0A in genetic competence is to downregulate abrB, an essential competence gene. J Bacteriol 177: 3601–3605. 7768874

27. Fujita M, Gonzalez-Pastor JE, Losick R (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187: 1357–1368. 15687200

28. Jiang M, Shao W, Perego M, Hoch JA (2000) Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol 38: 535–542. 11069677

29. LeDeaux JR, Yu N, Grossman AD (1995) Different roles for KinA, KinB, and KinC in the initiation of sporulation in Bacillus subtilis. J Bacteriol 177: 861–863. 7836330

30. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J (2012) Segregation of molecules at cell division reveals native protein localization. Nat Methods 9: 480–482. doi: 10.1038/nmeth.1955 22484850

31. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642–1645. 16902090

32. Lando D, Endesfelder U, Berger H, Subramanian L, Dunne PD, et al. (2012) Quantitative single-molecule microscopy reveals that CENP-A(Cnp1) deposition occurs during G2 in fission yeast. Open biology 2: 120078. doi: 10.1098/rsob.120078 22870388

33. Karimova G, Pidoux J, Ullmann A, Ladant D (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95: 5752–5756. 9576956

34. Tavernarakis N, Driscoll M, Kyrpides NC (1999) The SPFH domain: implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins. Trends Biochem Sci 24: 425–427. 10542406

35. Rivera-Milla E, Stuermer CA, Malaga-Trillo E (2006) Ancient origin of reggie (flotillin), reggie-like, and other lipid-raft proteins: convergent evolution of the SPFH domain. Cell Mol Life Sci 63: 343–357. 16389450

36. Neumann-Giesen C, Falkenbach B, Beicht P, Claasen S, Luers G, et al. (2004) Membrane and raft association of reggie-1/flotillin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem J 378: 509–518. 14599293

37. Wittig I, Braun HP, Schagger H (2006) Blue native PAGE. Nat Protoc 1: 418–428. 17406264

38. Scheffers DJ, Pinho MG (2005) Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69: 585–607. 16339737

39. Muller JP, An Z, Merad T, Hancock IC, Harwood CR (1997) Influence of Bacillus subtilis phoR on cell wall anionic polymers. Microbiology 143 (Pt 3): 947–956.

40. Moore CM, Helmann JD (2005) Metal ion homeostasis in Bacillus subtilis. Current Opinion in Microbiology 8: 188–195. 15802251

41. Nakano MM, Zuber P, Glaser P, Danchin A, Hulett FM (1996) Two-component regulatory proteins ResD-ResE are required for transcriptional activation of fnr upon oxygen limitation in Bacillus subtilis. J Bacteriol 178: 3796–3802. 8682783

42. Le AT, Schumann W (2009) The Spo0E phosphatase of Bacillus subtilis is a substrate of the FtsH metalloprotease. Microbiology 155: 1122–1132. doi: 10.1099/mic.0.024182-0 19332814

43. Perego M, Higgins CF, Pearce SR, Gallagher MP, Hoch JA (1991) The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol 5: 173–185. 1901616

44. Good MC, Zalatan JG, Lim WA (2011) Scaffold proteins: hubs for controlling the flow of cellular information. Science 332: 680–686. doi: 10.1126/science.1198701 21551057

45. Silva-Rocha R, Martinez-Garcia E, Calles B, Chavarria M, Arce-Rodriguez A, et al. (2013) The Standard European Vector Architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes. Nucleic Acids Res 41: D666–675. doi: 10.1093/nar/gks1119 23180763

46. Levchenko A, Bruck J, Sternberg PW (2000) Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc Natl Acad Sci U S A 97: 5818–5823. 10823939

47. Chapman SA, Asthagiri AR (2009) Quantitative effect of scaffold abundance on signal propagation. Mol Syst Biol 5: 313. doi: 10.1038/msb.2009.73 19888208

48. Dickens M, Rogers JS, Cavanagh J, Raitano A, Xia Z, et al. (1997) A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 277: 693–696. 9235893

49. Botella E, Hubner S, Hokamp K, Hansen A, Bisicchia P, et al. (2011) Cell envelope gene expression in phosphate-limited Bacillus subtilis cells. Microbiology 157: 2470–2484. doi: 10.1099/mic.0.049205-0 21636651

50. Lahooti M, Harwood CR (1999) Transcriptional analysis of the Bacillus subtilis teichuronic acid operon. Microbiology 145 (Pt 12): 3409–3417. 10627039

51. Nakano MM, Zheng G, Zuber P (2000) Dual control of sbo-alb operon expression by the Spo0 and ResDE systems of signal transduction under anaerobic conditions in Bacillus subtilis. J Bacteriol 182: 3274–3277. 10809710

52. Hartig E, Geng H, Hartmann A, Hubacek A, Munch R, et al. (2004) Bacillus subtilis ResD induces expression of the potential regulatory genes yclJK upon oxygen limitation. J Bacteriol 186: 6477–6484. 15375128

53. Eiamphungporn W, Helmann JD (2008) The Bacillus subtilis sigma(M) regulon and its contribution to cell envelope stress responses. Mol Microbiol 67: 830–848. doi: 10.1111/j.1365-2958.2007.06090.x 18179421

54. Reents H, Munch R, Dammeyer T, Jahn D, Hartig E (2006) The Fnr regulon of Bacillus subtilis. J Bacteriol 188: 1103–1112. 16428414

55. May JJ, Wendrich TM, Marahiel MA (2001) The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276: 7209–7217. 11112781

56. Uffen RL, Canale-Parola E (1972) Synthesis of pulcherriminic acid by Bacillus subtilis. J Bacteriol 111: 86–93. 4204912

57. von Dohren H (2009) Charged tRNAs charge into secondary metabolism. Nat Chem Biol 5: 374–375. doi: 10.1038/nchembio0609-374 19448602

58. Cryle MJ, Bell SG, Schlichting I (2010) Structural and biochemical characterization of the cytochrome P450 CypX (CYP134A1) from Bacillus subtilis: a cyclo-L-leucyl-L-leucyl dipeptide oxidase. Biochemistry 49: 7282–7296. doi: 10.1021/bi100910y 20690619

59. Gondry M, Sauguet L, Belin P, Thai R, Amouroux R, et al. (2009) Cyclodipeptide synthases are a family of tRNA-dependent peptide bond-forming enzymes. Nat Chem Biol 5: 414–420. doi: 10.1038/nchembio.175 19430487

60. Daum RS, Gupta S, Sabbagh R, Milewski WM (1992) Characterization of Staphylococcus aureus isolates with decreased susceptibility to vancomycin and teicoplanin: isolation and purification of a constitutively produced protein associated with decreased susceptibility. J Infect Dis 166: 1066–1072. 1402017

61. Reipert A, Ehlert K, Kast T, Bierbaum G (2003) Morphological and genetic differences in two isogenic Staphylococcus aureus strains with decreased susceptibilities to vancomycin. Antimicrob Agents Chemother 47: 568–576. 12543661

62. Sieradzki K, Tomasz A (2003) Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J Bacteriol 185: 7103–7110. 14645269

63. Lambert PA (2002) Cellular impermeability and uptake of biocides and antibiotics in Gram-positive bacteria and mycobacteria. J Appl Microbiol 92 Suppl: 46S–54S. 12000612

64. Sakoulas G, Bayer AS, Pogliano J, Tsuji BT, Yang SJ, et al. (2012) Ampicillin enhances daptomycin- and cationic host defense peptide-mediated killing of ampicillin- and vancomycin-resistant Enterococcus faecium. Antimicrob Agents Chemother 56: 838–844. doi: 10.1128/AAC.05551-11 22123698

65. Wolf D, Dominguez-Cuevas P, Daniel RA, Mascher T (2012) Cell envelope stress response in cell wall-deficient L-forms of Bacillus subtilis. Antimicrob Agents Chemother 56: 5907–5915. doi: 10.1128/AAC.00770-12 22964256

66. Kouwen TR, Trip EN, Denham EL, Sibbald MJ, Dubois JY, et al. (2009) The large mechanosensitive channel MscL determines bacterial susceptibility to the bacteriocin sublancin 168. Antimicrob Agents Chemother 53: 4702–4711. doi: 10.1128/AAC.00439-09 19738010

67. Butcher BG, Helmann JD (2006) Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol Microbiol 60: 765–782. 16629676

68. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11: 688–699. doi: 10.1038/nrm2977 20861879

69. Govindarajan S, Nevo-Dinur K, Amster-Choder O (2012) Compartmentalization and spatiotemporal organization of macromolecules in bacteria. FEMS Microbiol Rev 36: 1005–1022. doi: 10.1111/j.1574-6976.2012.00348.x 22775310

70. Rudner DZ, Losick R (2010) Protein subcellular localization in bacteria. Cold Spring Harb Perspect Biol 2: a000307. doi: 10.1101/cshperspect.a000307 20452938

71. Zhao F, Zhang J, Liu YS, Li L, He YL (2011) Research advances on flotillins. Virol J 8: 479. doi: 10.1186/1743-422X-8-479 22023811

72. Mishra S, Joshi PG (2007) Lipid raft heterogeneity: an enigma. Journal of neurochemistry 103 Suppl 1: 135–142. 17986148

73. Munro S (2003) Lipid rafts: elusive or illusive? Cell 115: 377–388. 14622593

74. Shaw AS (2006) Lipid rafts: now you see them, now you don't. Nat Immunol 7: 1139–1142. 17053798

75. Wach A (1996) PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12: 259–265. 8904338

76. Arnaud M, Chastanet A, Debarbouille M (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887–6891. 15528558

77. Britton RA, Eichenberger P, Gonzalez-Pastor JE, Fawcett P, Monson R, et al. (2002) Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J Bacteriol 184: 4881–4890. 12169614

78. Erwin KN, Nakano S, Zuber P (2005) Sulfate-dependent repression of genes that function in organosulfur metabolism in Bacillus subtilis requires Spx. J Bacteriol 187: 4042–4049. 15937167

79. Nakano S, Kuster-Schock E, Grossman AD, Zuber P (2003) Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc Natl Acad Sci U S A 100: 13603–13608. 14597697

80. Yasbin RE, Young FE (1974) Transduction in Bacillus subtilis by bacteriophage SPP1. J Virol 14: 1343–1348. 4214946

81. Weickert MJ, Chambliss GH (1990) Site-directed mutagenesis of a catabolite repression operator sequence in Bacillus subtilis. Proc Natl Acad Sci U S A 87: 6238–6242. 2117276

82. van de Linde S, Loschberger A, Klein T, Heidbreder M, Wolter S, et al. (2011) Direct stochastic optical reconstruction microscopy with standard fluorescent probes. Nat Protoc 6: 991–1009. doi: 10.1038/nprot.2011.336 21720313

83. Wolter S, Endesfelder U, van de Linde S, Heilemann M, Sauer M (2011) Measuring localization performance of super-resolution algorithms on very active samples. Opt Express 19: 7020–7033. doi: 10.1364/OE.19.007020 21503016

84. Wolter S, Loschberger A, Holm T, Aufmkolk S, Dabauvalle MC, et al. (2012) rapidSTORM: accurate, fast open-source software for localization microscopy. Nat Methods 9: 1040–1041. doi: 10.1038/nmeth.2224 23132113

85. Kovacs AT, Kuipers OP (2011) Rok regulates yuaB expression during architecturally complex colony development of Bacillus subtilis 168. J Bacteriol 193: 998–1002. doi: 10.1128/JB.01170-10 21097620

86. van Hijum SA, de Jong A, Baerends RJ, Karsens HA, Kramer NE, et al. (2005) A generally applicable validation scheme for the assessment of factors involved in reproducibility and quality of DNA-microarray data. BMC Genomics 6: 77. 15907200

87. van Hijum SA, de Jong A, Buist G, Kok J, Kuipers OP (2003) UniFrag and GenomePrimer: selection of primers for genome-wide production of unique amplicons. Bioinformatics 19: 1580–1582. 12912842

88. Kuipers OP, de Jong A, Baerends RJ, van Hijum SA, Zomer AL, et al. (2002) Transcriptome analysis and related databases of Lactococcus lactis. Antonie Van Leeuwenhoek 82: 113–122. 12369183

89. van Hijum SA, Garcia de la Nava J, Trelles O, Kok J, Kuipers OP (2003) MicroPreP: a cDNA microarray data pre-processing framework. Appl Bioinformatics 2: 241–244. 15130795

90. Baldi P, Long AD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17: 509–519. 11395427

91. Mironczuk AM, Manu A, Kuipers OP, Kovacs AT (2011) Distinct roles of ComK1 and ComK2 in gene regulation in Bacillus cereus. PLoS One 6: e21859. doi: 10.1371/journal.pone.0021859 21747963

92. Mader U, Schmeisky AG, Florez LA, Stulke J (2012) SubtiWiki—a comprehensive community resource for the model organism Bacillus subtilis. Nucleic Acids Res 40: D1278–1287. doi: 10.1093/nar/gkr923 22096228

93. Moszer I, Glaser P, Danchin A (1995) SubtiList: a relational database for the Bacillus subtilis genome. Microbiology 141 (Pt 2): 261–268.

94. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. 11846609

95. Campo N, Marquis KA, Rudner DZ (2008) SpoIIQ anchors membrane proteins on both sides of the sporulation septum in Bacillus subtilis. J Biol Chem 283: 4975–4982. 18077456

96. Miller JH (1972) Experiments in Molecular Genetics. Cold Spring Harbor: Cold Spring Harbor Laboratories.

97. Uffen RL, Canale-Parola E (1969) Isolation of pulcherriminic acid from cultures of Bacillus cereus var. alesti. Z Allg Mikrobiol 9: 231–233. 4985560

98. Lopez D, Vlamakis H, Losick R, Kolter R (2009) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74: 609–618. doi: 10.1111/j.1365-2958.2009.06882.x 19775247

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#