Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces

Molecular Microbiology

Volumn 70, Issue 4, 2008, Pages 1037-1050

  Bagchi, Sonchita ^a   Tomenius, Henrik ^a   Belova, Lyubov M ^b   Ausmees, Nora ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; CRESCENTIN; TUBULIN; UNCLASSIFIED DRUG;

ACTINOBACTERIA; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; CYTOSKELETON; INTERMEDIATE FILAMENT; MORPHOGENESIS; MYCOBACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STREPTOMYCES; STREPTOMYCES COELICOLOR;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CONSERVED SEQUENCE; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GENOME, BACTERIAL; INTERMEDIATE FILAMENT PROTEINS; INTERMEDIATE FILAMENTS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; PLASMIDS; SEQUENCE ALIGNMENT; STREPTOMYCES COELICOLOR;

ACTINOBACTERIA (CLASS); CAULOBACTER; CAULOBACTER VIBRIOIDES; METAZOA; MYCOBACTERIUM; STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 54249099195     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06473.x     Document Type: Article

References (60)

1. Aaron, M., Charbon, G., Lam, H., Schwarz, H., Vollmer, W. Jacobs-Wagner, C. (2007) The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol Microbiol 64 : 938 952.
2. Ausmees, N., Kuhn, J.R. Jacobs-Wagner, C. (2003) The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115 : 705 713.
3. Bi, E.F. Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354 : 161 164.
4. Cabeen, M.T. Jacobs-Wagner, C. (2007) Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis. J Cell Biol 179 : 381 387.
5. Carballido-Lopez, R. (2006) The bacterial actin-like cytoskeleton. Microbiol Mol Biol Rev 70 : 888 909.
6. Carballido-Lopez, R., Formstone, A., Li, Y., Ehrlich, S.D., Noirot, P. Errington, J. (2006) Actin homologue MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev Cell 11 : 399 409.
7. Chater, K.F. (2000) Developmental decisions during sporulation in the aerial mycelium in Streptomyces. In Prokaryotic Development. Brun, Y.V. Shimkets, L.J. (eds). Washington, DC : American Society for Microbiology Press, pp. 33 48.
8. Chater, K.F. Losick, R. (1997) Multicellular lifestyle of Streptomyces coelicolor A3 (2) and its relatives. In Bacteria as Multicellular Organisms. Shapiro, J.A. Dworkin, M. (eds). New York, NY : Oxford University Press, pp. 149 182.
9. Chou, Y.H., Flitney, F.W., Chang, L., Mendez, M., Grin, B. Goldman, R.D. (2007) The motility and dynamic properties of intermediate filaments and their constituent proteins. Exp Cell Res 313 : 2236 2243.
10. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16 : 10881 10890.
11. Daniel, R.A. Errington, J. (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113 : 767 776.
12. Divakaruni, A.V., Baida, C., White, C.L. Gober, J.W. (2007) The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. Mol Microbiol 66 : 174 188.
13. Domingo, A., Sarria, A.J., Evans, R.M. Klymkowsky, M.W. (1992) Studying intermediate filaments. In The Cytoskeleton; a Practical Approach. Carraway, K.L. Carraway, C.A.C. (eds). Oxford : IRL Press, pp. 223 255.
14. Dye, N.A., Pincus, Z., Theriot, J.A., Shapiro, L. Gitai, Z. (2005) Two independent spiral structures control cell shape in Caulobacter. Proc Natl Acad Sci USA 102 : 18608 18613.
15. Ebersbach, G., Galli, E., Moller-Jensen, J., Lowe, J. Gerdes, K. (2008) Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol Microbiol 68 : 720 735.
16. Elliot, M.A., Buttner, M.J. Nodwell, J.R. (2007) Multicellular development in Streptomyces. In Multicellularity and Differentiation Among the Myxobacteria and Their Neighbors. Kaplan, H.B. Whitworth, D.E. (eds). Washington, DC : American Society for Microbiology Press.
17. Figge, R.M., Divakaruni, A.V. Gober, J.W. (2004) MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol Microbiol 51 : 1321 1332.
18. Flärdh, K. (2003a) Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3 (2). Mol Microbiol 49 : 1523 1536.
19. Flärdh, K. (2003b) Growth polarity and cell division in Streptomyces. Curr Opin Microbiol 6 : 564 571.
20. Geisler, N., Schunemann, J., Weber, K., Haner, M. Aebi, U. (1998) Assembly and architecture of invertebrate cytoplasmic intermediate filaments reconcile features of vertebrate cytoplasmic and nuclear lamin-type intermediate filaments. J Mol Biol 282 : 601 617.
21. Goulielmos, G., Gounari, F., Remington, S., Muller, S., Haner, M., Aebi, U. Georgatos, S.D. (1996) Filensin and phakinin form a novel type of beaded intermediate filaments and coassemble de novo in cultured cells. J Cell Biol 132 : 643 655.
22. Graumann, P.L. (2007) Cytoskeletal elements in bacteria. Annu Rev Microbiol 61 : 589 618.
23. Gust, B., Challis, G.L., Fowler, K., Kieser, T. Chater, K.F. (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100 : 1541 1546.
24. Harold, F.M. (2002) Force and compliance: rethinking morphogenesis in walled cells. Fungal Genet Biol 37 : 271 282.
25. Harold, F.M. (2007) Bacterial morphogenesis: learning how cells make cells. Curr Opin Microbiol 10 : 591 595.
26. Herrmann, H. Aebi, U. (2004) Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds. Annu Rev Biochem 73 : 749 789.
27. Herrmann, H., Bar, H., Kreplak, L., Strelkov, S.V. Aebi, U. (2007) Intermediate filaments: from cell architecture to nanomechanics. Nat Rev Mol Cell Biol 8 : 562 573.
28. Hurme, R., Namork, E., Nurmiaho-Lassila, E.L. Rhen, M. (1994) Intermediate filament-like network formed in vitro by a bacterial coiled coil protein. J Biol Chem 269 : 10675 10682.
29. Jones, L.J., Carballido-Lopez, R. Errington, J. (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104 : 913 922.
30. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F. Hopwood, D. (2000) Practical Streptomyces Genetics. Norwich : The John Innes Foundation.
31. Kim, S. Coulombe, P.A. (2007) Intermediate filament scaffolds fulfill mechanical, organizational, and signalling functions in the cytoplasm. Genes Dev 21 : 1581 1597.
32. Koch, A.L. (1985) How bacteria grow and divide in spite of internal hydrostatic pressure. Can J Microbiol 31 : 1071 1084.
33. Kruse, T., Moller-Jensen, J., Lobner-Olesen, A. Gerdes, K. (2003) Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J 22 : 5283 5292.
34. Letek, M., Ordonez, E., Vaquera, J., Margolin, W., Flärdh, K., Mateos, L.M. Gil, J.A. (2008) DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J Bacteriol 190 : 3283 3292.
35. Lupas, A. (1997) Predicting coiled-coil regions in proteins. Curr Opin Struct Biol 7 : 388 393.
36. Margolin, W. (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6 : 862 871.
37. Martin, K., Schumann, P., Rainey, F.A., Schuetze, B. Groth, I. (1997) Janibacter limosus gen nov., sp. nov., a new actinomycete with meso-diaminopimelic acid in the cell wall. Int J Syst Bacteriol 47 : 529 534.
38. Mazouni, K., Pehau-Arnaudet, G., England, P., Bourhy, P., Saint Girons, I. Picardeau, M. (2006) The scc spirochetal coiled-coil protein forms helix-like filaments and binds to nucleic acids generating nucleoprotein structures. J Bacteriol 188 : 469 476.
39. Michie, K.A. Lowe, J. (2006) Dynamic filaments of the bacterial cytoskeleton. Annu Rev Biochem 75 : 467 492.
40. Mohammadi, T., Karczmarek, A., Crouvoisier, M., Bouhss, A., Mengin-Lecreulx, D. den Blaauwen, T. (2007) The essential peptidoglycan glycosyltransferase MurG forms a complex with proteins involved in lateral envelope growth as well as with proteins involved in cell division in Escherichia coli. Mol Microbiol 65 : 1106 1121.
41. Nguyen, L., Scherr, N., Gatfield, J., Walburger, A., Pieters, J. Thompson, C.J. (2007) Antigen 84, an effector of pleiomorphism in Mycobacterium smegmatis. J Bacteriol 189 : 7896 7910.
42. Ojha, A.K., Mukherjee, T.K. Chatterji, D. (2000) High intracellular level of guanosine tetraphosphate in Mycobacterium smegmatis changes the morphology of the bacterium. Infect Immun 68 : 4084 4091.
43. Omary, M.B., Coulombe, P.A. McLean, W.H. (2004) Intermediate filament proteins and their associated diseases. N Engl J Med 351 : 2087 2100.
44. Parry, D.A., Strelkov, S.V., Burkhard, P., Aebi, U. Herrmann, H. (2007) Towards a molecular description of intermediate filament structure and assembly. Exp Cell Res 313 : 2204 2216.
45. Pekny, M. Lane, E.B. (2007) Intermediate filaments and stress. Exp Cell Res 313 : 2244 2254.
46. Pichoff, S. Lutkenhaus, J. (2007) Overview of cell shape: cytoskeletons shape bacterial cells. Curr Opin Microbiol 10 : 601 605.
47. Pinho, M.G. Errington, J. (2003) Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol Microbiol 50 : 871 881.
48. Ramos, A., Honrubia, M.P., Valbuena, N., Vaquera, J., Mateos, L.M. Gil, J.A. (2003) Involvement of DivIVA in the morphology of the rod-shaped actinomycete Brevibacterium lactofermentum. Microbiology 149 : 3531 3542.
49. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
50. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E. Tsien, R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22 : 1567 1572.
51. Steinert, P.M., Idler, W.W. Zimmerman, S.B. (1976) Self-assembly of bovine epidermal keratin filaments in vitro. J Mol Biol 108 : 547 567.
52. Stuurman, N., Heins, S. Aebi, U. (1998) Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 122 : 42 66.
53. Takeuchi, S., DiLuzio, W.R., Weibel, D.B. Whitesides, G.M. (2005) Controlling the shape of filamentous cells of Escherichia coli. Nano Lett 5 : 1819 1823.
54. Thanbichler, M. Shapiro, L. (2008) Getting organized - how bacterial cells move proteins and DNA. Nat Rev Microbiol 6 : 28 40.
55. Varma, A. Young, K.D. (2004) FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J Bacteriol 186 : 6768 6774.
56. Ventura, M., Canchaya, C., Tauch, A., Chandra, G., Fitzgerald, G.F., Chater, K.F. van Sinderen, D. (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71 : 495 548.
57. Walter, S. Schrempf, H. (2003) Oligomerization, membrane anchoring, and cellulose-binding characteristics of AbpS, a receptor-like Streptomyces protein. J Biol Chem 278 : 26639 26647.
58. Walter, S., Wellmann, E. Schrempf, H. (1998) The Cell Wall-Anchored Streptomyces reticuli Avicel-Binding Protein (AbpS) and Its Gene. J Bacteriol 180 : 1647 1654.
59. Xu, H., Chater, K.F., Deng, Z. Tao, M. (2008) A cellulose synthase-like protein involved in hyphal tip growth and morphological differentiation in Streptomyces. J Bacteriol 190 : 4971 4978.
60. Yang, R., Bartle, S., Otto, R., Stassinopoulos, A., Rogers, M., Plamann, L. Hartzell, P. (2004) AglZ is a filament-forming coiled-coil protein required for adventurous gliding motility of Myxococcus xanthus. J Bacteriol 186 : 6168 6178.