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Min Oscillation in Bacteria

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Cellular Oscillatory Mechanisms

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 641))

Abstract

Oscillation of the Min proteins is a key regulator of the division plane in many bacteria including the model organism E. coli. The coupled oscillation of these proteins between the ends of the cell restricts the formation of the Zring, an essential cytoskeletal element that serves as a scaffold for the cytokinesis machinery, to a narrow region at midcell. The oscillation was discovered following the fusion of the Min proteins to green fluorescent protein. Importantly, the Min system is readily manipulated allowing rapid advances in understanding key aspects of the oscillation. In addition, details of the biochemistry of the Min proteins have pmerged that provide the basis for their dynamic interaction with the membrane. Furthermore, the in vivo description of the oscillations along with the biochemical details of the Min proteins have provided the fuel for mathematical approaches to try and understand the critical features have underlie this oscillatory system. The simplicity and ease of manipulating the Min system make it a tractable model to obtain a complete understanding of a self-organizing system.

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References

  1. Lutkenhaus J, Addinall SG Bacterial cell division and the Z ring. Annu Rev Biochem 1997; 66:93–116.

    Article  PubMed  CAS  Google Scholar 

  2. Addinall SG, Lutkenhaus J. FtsZ-spirals and-arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol Microbiol 1996; 22:231–237.

    Article  PubMed  CAS  Google Scholar 

  3. Sun Q, Yu XC, Margolin W. Assembly of the FtsZ ring at the central division site in the absence of the chromosome. Mol Microbiol 1998; 29:491–503.

    Article  PubMed  CAS  Google Scholar 

  4. Woldringh CL, Mulder E, Huls PG et al. Toporegulation of bacterial division according to the nucleoid occlusion model. Res Microbiol 1991; 142:309–320.

    Article  PubMed  CAS  Google Scholar 

  5. Wu LJ, Errington, J. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 2004; 117:915–925.

    Article  PubMed  CAS  Google Scholar 

  6. Bernhardt TG, de Boer PAJ. SlmA, a nucleoid-associated, FtsZ-binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 2005; 555–564.

    Google Scholar 

  7. Adler HI, Fisher WD, Cohen A et al. Minature Escherichia coli cells deficient in DNA. Proc Natl Acad Sci USA 1967; 57:321–326.

    Article  PubMed  CAS  Google Scholar 

  8. de Boer PA, Crossley RE, Rothfield LI. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 1989; 56:641–649.

    Article  PubMed  Google Scholar 

  9. Rothfield L, Taghbalout A, Shih YL. Spatial control of bacterial division-site placement. Nat Rev Microbiol 2005; 3:959–968.

    Article  PubMed  CAS  Google Scholar 

  10. Lutkenhaus J. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 2007.

    Google Scholar 

  11. Pichoff S, Lutkenhaus J. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 2005; 55:1722–1734.

    Article  PubMed  CAS  Google Scholar 

  12. Mukherjee A, Lutkenhaus J. Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol 1994; 176:2754–2758.

    PubMed  CAS  Google Scholar 

  13. Lowe J, Amos LA. Crystal structure of the bacterial cell-division protein FtsZ. Nature 1998; 391:203–206.

    Article  PubMed  CAS  Google Scholar 

  14. Mukherjee A, Lutkenhaus J. Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J 1998; 17:462–469.

    Article  PubMed  CAS  Google Scholar 

  15. Stricker J, Maddox P, Salmon ED et al. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci USA 2002; 99:3171–3175.

    Article  PubMed  CAS  Google Scholar 

  16. Anderson DE, Gueiros-Filho FJ, Erickson HP. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J Bacteriol 2004; 186:5775–5781.

    Article  PubMed  CAS  Google Scholar 

  17. Desai A, Mitchison TJ. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 1997; 13:83–117.

    Article  PubMed  CAS  Google Scholar 

  18. Garner EC, Campbell CS, Mullins RD. Dynamic instability in a DNA-segregating prokaryotic actin homolog. Science 2004; 306:1021–1025.

    Article  PubMed  CAS  Google Scholar 

  19. Thanedar S, Margolin W. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr Biol 2004; 14:1167–1173.

    Article  PubMed  CAS  Google Scholar 

  20. Yu XC, Margolin W. FtsZ ring clusters in min and partition mutants: Role of both the Min system and the nucleoid in regulating FtsZ ring localization. Mol Microbiol 1999; 32:315–326.

    Article  PubMed  CAS  Google Scholar 

  21. Bi E, Lutkenhaus J. Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol 1993; 175:1118–1125.

    PubMed  CAS  Google Scholar 

  22. Hu Z, Mukherjee A, Pichoff S et al. The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci USA 1999; 96:14819–14824.

    Article  PubMed  CAS  Google Scholar 

  23. Hu Z, Lutkenhaus J. A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol Microbiol 2003; 47:345–355.

    Article  PubMed  CAS  Google Scholar 

  24. de Boer PA, Crossley RE, Rothfield LI. Central role for the Escherichia coli minC gene product in two different cell division-inhibition systems. Proc Natl Acad Sci USA 1990; 87:1129–1133.

    Article  PubMed  Google Scholar 

  25. de Boer PA, Crossley RE, Hand AR et al. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J 1991; 10:4371–4380.

    PubMed  Google Scholar 

  26. Lutkenhaus J, Sundaramoorthy M. MinD and role of the deviant Walker A motif, dimerization andmembrane binding in oscillation. Mol Microbiol 2003;48:295–303.

    Article  PubMed  CAS  Google Scholar 

  27. Zhou H, Schulze R, Cox S et al. Analysis of MinD mutations reveals residues required for MinE stimulation of the MinD ATPase and residues required for MinC interaction. J Bacteriol 2005; 187:629–638.

    Article  PubMed  CAS  Google Scholar 

  28. Schindelin H, Kisker C, Schlessman JL et al. Structure of ADP × AIF4(−)-stabilized nitrogenase complex and its implications for signal transduction. Nature 1997; 387:370–376.

    Article  PubMed  CAS  Google Scholar 

  29. Cordell SC, Lowe J. Crystal structure of the bacterial cell division regulator MinD. FEBS Lett 2001; 492:160–165.

    Article  PubMed  CAS  Google Scholar 

  30. Sakai N, Yao M, Itou H et al. The three-dimensional structure of septum site-determining protein MinD from Pyrococcus horikoshii OT3 in complex with Mg-ADP. Structure 2001; 9:817–826.

    Article  PubMed  CAS  Google Scholar 

  31. Hayashi I, Oyama T, Morikawa K. Structural and functional studies of MinD ATPase: Implications for the molecular recognition of the bacterial cell division apparatus. EMBO J 2001; 20:1819–1828.

    Article  PubMed  CAS  Google Scholar 

  32. Hu Z, Saez C, Lutkenhaus J. Recruitment of MinC, an inhibitor of Z-ring formation, to the membrane in Escherichia coli: Role of MinD and MinE. J Bacteriol 2003; 185:196–203.

    Article  PubMed  CAS  Google Scholar 

  33. Leonard TA, Butler PJ, Lowe J. Bacterial chromosome segregation: Structure and DNA binding of the Soj dimer—A conserved biological switch. EMBO J 2005; 24:270–282.

    Article  PubMed  CAS  Google Scholar 

  34. Lackner LL, Raskin DM, de Boer PA. ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J Bacteriol 2003; 185:735–749.

    Article  PubMed  CAS  Google Scholar 

  35. Hu Z, Gogol EP, Lutkenhaus J. Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc Natl Acad Sci USA 2002; 99:6761–6716.

    Article  PubMed  CAS  Google Scholar 

  36. King GF, Shih YL, Maciejewski MW et al. Structural basis for the topological specificity function of MinE. Nat Struct Biol 2000; 7:1013–1017.

    Article  PubMed  CAS  Google Scholar 

  37. Shih YL, Le T, Rothfield L. Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc Natl Acad Sci USA 2003; 100:7865–7870.

    Google Scholar 

  38. Zhao CR, de Boer PA, Rothfield LI. Proper placement of the Escherichia coli division site requires two functions that are associated with different domains of the MinE protein. Proc Natl Acad Sci USA 1995;92:4313–4317.

    Article  PubMed  CAS  Google Scholar 

  39. Pichoff S, Vollrath B, Touriol C et al. Deletion analysis of gene minE which encodes the topological specificity factor of cell division in Escherichia coli. Mol Microbiol 1995; 18:321–329.

    Article  PubMed  CAS  Google Scholar 

  40. Hu Z, Lutkenhaus J. Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J Bacteriol 2000; 182:3965–3971.

    Article  PubMed  CAS  Google Scholar 

  41. Cordell SC, Anderson RE, Lowe J. Crystal structure of the bacterial cell division inhibitor MinC. EMBO J 2001; 20:2454–2461.

    Article  PubMed  CAS  Google Scholar 

  42. Shiomi D, Margolin W. The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J Bacteriol 2007; 189:236–243.

    Article  PubMed  CAS  Google Scholar 

  43. Hu Z, Lutkenhaus J. Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol Microbiol 1999; 34:82–90.

    Article  PubMed  CAS  Google Scholar 

  44. Johnson JE, Lackner LL, de Boer PA. Targeting of (D)MinC/MinD and (D)MinC/DicB complexes to septal rings in Escherichia coli suggests a multistep mechanism for MinC-mediated destruction of nascent FtsZ rings. J Bacteriol 2002; 184:2951–2962.

    Article  PubMed  CAS  Google Scholar 

  45. Raskin DM, de Boer PA. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 1999; 181:6419–6424.

    PubMed  CAS  Google Scholar 

  46. Raskin DM, de Boer PA. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA 1999; 96:4971–4976.

    Article  PubMed  CAS  Google Scholar 

  47. Touhami A, Jericho M, Rutenberg AD. Temperature dependence of MinD oscillation in Escherichia coli: Running hot and fast. J Bacteriol 2006; 188:7661–7667.

    Article  PubMed  CAS  Google Scholar 

  48. Hale CA, Meinhardt H, de Boer PA. Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J 2001; 20:1563–1572.

    Article  PubMed  CAS  Google Scholar 

  49. Fu X, Shih YL, Zhang Y et al. The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia coli division cycle. Proc Natl Acad Sci USA 2001; 98:980–985.

    Article  PubMed  CAS  Google Scholar 

  50. Corbin BD, Yu XC, Margolin W. Exploring intracellular space: Function of the Min system in round-shaped Escherichia coli. EMBO J 2002; 21:1998–2008.

    Article  PubMed  CAS  Google Scholar 

  51. Shih YL, Kawagishi I, Rothfield L. The MreB and Min cytoskeletal-like systems play independent roles in prokaryotic polar differentiation. Mol Microbiol 2005; 58:917–928.

    Article  PubMed  CAS  Google Scholar 

  52. Szeto J, Eng NF, Acharya S et al. A conserved polar region in the cell division site determinant MinD is required for responding to MinE-induced oscillation but not for localization within coiled arrays. Res Microbiol 2005; 156:17–29.

    Article  PubMed  CAS  Google Scholar 

  53. Zhang Y, Rowland S, King G et al. The relationship between hetero-oligomer formation and function of the topological specificity domain of the Escherichia coli MinE protein. Mol Microbiol 1998; 30:265–273.

    Article  PubMed  CAS  Google Scholar 

  54. Szeto TH, Rowland SL, Rothfield LI et al. Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc Natl Acad Sci USA 2002; 99:15693–15698.

    Article  PubMed  CAS  Google Scholar 

  55. Mileykovskaya E, Fishov I, Fu X et al. Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J Biol Chem 2003; 278:22193–22198.

    Article  PubMed  CAS  Google Scholar 

  56. Mileykovskaya E, Dowhan W. Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange J Bacteriol 2000; 182:1172–1175.

    Article  PubMed  CAS  Google Scholar 

  57. Szeto TH, Rowland SL, Habrukowich CL et al. The MinD membrane targeting sequence is a transplantable lipid-binding helix. J Biol Chem 2003; 278:40050–40056.

    Article  PubMed  CAS  Google Scholar 

  58. Marston AL, Errington J. Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol Cell 1999; 4:673–682.

    Article  PubMed  CAS  Google Scholar 

  59. Ebersbach G, Gerdes K. Bacterial mitosis: Partitioning protein ParA oscillates in spiral-shaped structures and positions plasmids at mid-cell. Mol Microbiol 2004; 52:385–398.

    Article  PubMed  CAS  Google Scholar 

  60. Hu Z, Lutkenhaus J. Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol Cell 2001; 7:1337–1343.

    Article  PubMed  CAS  Google Scholar 

  61. Ma LY, King G, Rothfield L. Mapping the MinE site involved in interaction with the MinD division site selection protein of Escherichia coli. J Bacteriol 2003; 185:4948–4955.

    Article  PubMed  CAS  Google Scholar 

  62. Ma L, King GF, Rothfield L. Positioning of the MinE binding site on the MinD surface suggests a plausible mechanism for activation of the Escherichia coli MinD ATPase during division site selection. Mol Microbiol 2004; 54:99–108.

    Article  PubMed  CAS  Google Scholar 

  63. Taghbalout A, Ma L, Rothfield L. Role of MinD-membrane association in Min protein interactions. J Bacteriol 2006; 188:2993–3001.

    Article  PubMed  CAS  Google Scholar 

  64. Kruse K, Howard M, Margolin W. An experimentalist’s guide to computational modeling of the Min system. Mol Microbiol 2007; 63:1279–1284.

    Article  PubMed  CAS  Google Scholar 

  65. Howard M, Kruse K. Cellular organization by self-organization: Mechanisms and models for Min protein dynamics. J Cell Biol 2005; 168:533–536.

    Article  PubMed  CAS  Google Scholar 

  66. Meinhardt H, de Boer PA. Pattern formation in Escherichia coli: A model for the pole-to-pole oscillations of Min proteins and the localization of the division site. Proc Natl Acad Sci USA 2001; 98:14202–14207.

    Article  PubMed  CAS  Google Scholar 

  67. Kruse K. A dynamic model for determining the middle of Escherichia coli. Biophys J 2002; 82:618–627.

    Article  PubMed  CAS  Google Scholar 

  68. Howard M, Rutenberg AD, de Vet S. Dynamic compartmentalization of bacteria: Accurate division in E. coli. Phys Rev Lett 2001; 87:278102.

    Article  PubMed  CAS  Google Scholar 

  69. Huang KC, Meir Y, Wingreen NS. Dynamic structures in Escherichia coli: Spontaneous formation of MinE rings and MinD polar zones. Proc Natl Acad Sci USA 2003; 100:12724–12728.

    Article  PubMed  CAS  Google Scholar 

  70. Kruse K, Julicher F. Self-organization and mechanical properties of active filament bundles. Phys Rev E Stat Nonlin Soft Matter Phys 2003; 67:051913.

    PubMed  Google Scholar 

  71. Drew DA, Osborn MJ, Rothfield LI. A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement. Proc Natl Acad Sci USA 2005; 102:6114–6118.

    Article  PubMed  CAS  Google Scholar 

  72. Pavin N, Paljetak HC, Krstic V. Min-protein oscillations in Escherichia coli with spontaneous formation of two-stranded filaments in a three-dimensional stochastic reaction-diffusion model. Phys Rev E Stat Nonlin Soft Matter Phys 2006; 73:021904.

    PubMed  Google Scholar 

  73. Tostevin F, Howard M. A stochastic model of Min oscillations in, Escherichia coli and Min protein segregation during cell division. Phys Biol 2006; 3:1–12.

    Article  CAS  Google Scholar 

  74. Taghbalout A, Rothfield L. RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton. Proc Natl Acad Sci USA 2007; 104:1667–1672.

    Article  PubMed  CAS  Google Scholar 

  75. Shiomi D, Yoshimoto M, Homma M et al. helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery. Mol Microbiol 2006; 60:894–906.

    Article  PubMed  CAS  Google Scholar 

  76. Meacci G, Ries J, Fischer-Friedrich E et al. Mobility of Min-proteins in Escherichia coli measured by fluorescence correlation spectroscopy. Phys Biol 2006; 3:255–263.

    Article  PubMed  CAS  Google Scholar 

  77. Kulkarni RV, Huang KC, Kloster M et al. Pattern formation within Escherichia coli: Diffusion, membrane attachment, and self-interaction of MinD molecules. Phys Rev Lett 2004; 93:228103.

    Article  PubMed  CAS  Google Scholar 

  78. Huang KC, Wingreen NS. Min-protein oscillations in round bacteria. Phys Biol 2004; 1:229–35.

    Article  PubMed  CAS  Google Scholar 

  79. Shih YL, Fu X, King GF et al. Division site placement in E. coli: Mutations that prevent formation of the MinE ring lead to loss of the normal midcell arrest of growth of polar MinD membrane domains. EMBO J 2002; 21:3347–3357.

    Article  PubMed  CAS  Google Scholar 

  80. Cytrynbaum EN, Marshall BDL. A Multi-stranded polymer model explains MinDE dynamics in E. coli cell division. Biophys J 2007; 93:1134–1150.

    Article  PubMed  CAS  Google Scholar 

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Lutkenhaus, J. (2008). Min Oscillation in Bacteria. In: Maroto, M., Monk, N.A.M. (eds) Cellular Oscillatory Mechanisms. Advances in Experimental Medicine and Biology, vol 641. Springer, New York, NY. https://doi.org/10.1007/978-0-387-09794-7_4

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