Interplay of the Serine/Threonine-Kinase StkP and the Paralogs DivIVA and GpsB in Pneumococcal Cell Elongation and Division

PLoS Genetics

Volumn 10, Issue 4, 2014, Pages

  Fleurie, Aurore ^a   Manuse, Sylvie ^a   Zhao, Chao ^a,b   Campo, Nathalie ^a,c   Cluzel, Caroline ^d   Lavergne, Jean Pierre ^a   Freton, Céline ^a   Combet, Christophe ^a   Guiral, Sébastien ^a   Soufi, Boumediene ^e   Macek, Boris ^e   Kuru, Erkin ^f   VanNieuwenhze, Michael S ^f   Brun, Yves V ^f   Di Guilmi, Anne Marie ^g   Claverys, Jean Pierre ^a,c   Galinier, Anne ^h   Grangeasse, Christophe ^a  

^a CNRS   (France)

^b FUDAN UNIVERSITY   (China)

^c UPS   (France)

^d UNIVERSITÉ LYON 1   (France)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f INDIANA UNIVERSITY   (United States)

^g INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^h AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FTSZ PROTEIN; PENICILLIN BINDING PROTEIN 2B; PENICILLIN BINDING PROTEIN 2X; PEPTIDOGLYCAN; PROTEIN EZRA; PROTEIN RODA; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE STKP; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; CELL DIVISION; CELL ELONGATION; CELL SHAPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIVIVA GENE; ENZYME ACTIVITY; GENE DELETION; GPSB GENE; NONHUMAN; PHENOTYPE; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; STKP GENE; STREPTOCOCCUS PNEUMONIAE; CELL WALL; GENETICS; METABOLISM; MORPHOGENESIS; PHOSPHORYLATION; PHYSIOLOGY;

BACTERIAL PROTEINS; CELL CYCLE PROTEINS; CELL DIVISION; CELL WALL; CYTOSKELETAL PROTEINS; MORPHOGENESIS; PEPTIDOGLYCAN; PHOSPHORYLATION; PROTEIN INTERACTION MAPS; PROTEIN-SERINE-THREONINE KINASES; STREPTOCOCCUS PNEUMONIAE;

EID: 84901336227     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004275     Document Type: Article

References (54)

1. Young KD, (2010) Bacterial shape: two-dimensional questions and possibilities. Annual review of microbiology 64: 223-240.
2. Egan AJ, Vollmer W, (2012) The physiology of bacterial cell division. Annals of the New York Academy of Sciences 1277: 8-28.
3. Typas A, Banzhaf M, Gross CA, Vollmer W, (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nature reviews Microbiology 10: 123-136.
4. Cabeen MT, Jacobs-Wagner C, (2010) The bacterial cytoskeleton. Annual review of genetics 44: 365-392.
5. Flardh K, (2010) Cell polarity and the control of apical growth in Streptomyces. Current opinion in microbiology 13: 758-765.
6. Fadda D, Santona A, D'Ulisse V, Ghelardini P, Ennas MG, et al. (2007) Streptococcus pneumoniae DivIVA: localization and interactions in a MinCD-free context. Journal of bacteriology 189: 1288-1298.
7. Lara B, Rico AI, Petruzzelli S, Santona A, Dumas J, et al. (2005) Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Molecular microbiology 55: 699-711.
8. Le Gouellec A, Roux L, Fadda D, Massidda O, Vernet T, et al. (2008) Roles of pneumococcal DivIB in cell division. Journal of bacteriology 190: 4501-4511.
9. Land AD, Winkler ME, (2011) The requirement for pneumococcal MreC and MreD is relieved by inactivation of the gene encoding PBP1a. Journal of bacteriology 193: 4166-4179.
10. Pinho MG, Kjos M, Veening JW, (2013) How to get (a)round: mechanisms controlling growth and division of coccoid bacteria. Nature reviews Microbiology 11: 601-614.
11. Higgins ML, Shockman GD, (1976) Study of cycle of cell wall assembly in Streptococcus faecalis by three-dimensional reconstructions of thin sections of cells. Journal of bacteriology 127: 1346-1358.
12. Sham LT, Tsui HC, Land AD, Barendt SM, Winkler ME, (2012) Recent advances in pneumococcal peptidoglycan biosynthesis suggest new vaccine and antimicrobial targets. Current opinion in microbiology 15: 194-203.
13. Claessen D, Emmins R, Hamoen LW, Daniel RA, Errington J, et al. (2008) Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Molecular microbiology 68: 1029-1046.
14. Fleurie A, Cluzel C, Guiral S, Freton C, Galisson F, et al. (2012) Mutational dissection of the S/T-kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae. Molecular microbiology 83: 746-758.
15. Beilharz K, Novakova L, Fadda D, Branny P, Massidda O, et al. (2012) Control of cell division in Streptococcus pneumoniae by the conserved Ser/Thr protein kinase StkP. Proc Natl Acad Sci U S A 109: E905-913.
16. Morlot C, Bayle L, Jacq M, Fleurie A, Tourcier G, et al. (2013) Interaction of Penicillin-Binding Protein 2x and Ser/Thr protein kinase StkP, two key players in Streptococcus pneumoniae R6 morphogenesis. Molecular microbiology 90: 88-102.
17. Novakova L, Bezouskova S, Pompach P, Spidlova P, Saskova L, et al. (2010) Identification of multiple substrates of the StkP Ser/Thr protein kinase in Streptococcus pneumoniae. Journal of bacteriology 192: 3629-3638.
18. Falk SP, Weisblum B, (2012) Phosphorylation of the Streptococcus pneumoniae Cell Wall Biosynthesis Enzyme MurC by a Eukaryotic-like Ser/Thr Kinase. FEMS microbiology letters 340 (1) (): 19-23.
19. Tavares JR, de Souza RF, Meira GL, Gueiros-Filho FJ, (2008) Cytological characterization of YpsB, a novel component of the Bacillus subtilis divisome. Journal of bacteriology 190: 7096-7107.
20. Macek B, Mijakovic I, Olsen JV, Gnad F, Kumar C, et al. (2007) The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 4: 697-707.
21. Burnside K, Lembo A, Harrell MI, Gurney M, Xue L, et al. (2011) Serine/threonine phosphatase Stp1 mediates post-transcriptional regulation of hemolysin, autolysis, and virulence of group B Streptococcus. The Journal of biological chemistry 286: 44197-44210.
22. Fadda D, Pischedda C, Caldara F, Whalen MB, Anderluzzi D, et al. (2003) Characterization of divIVA and other genes located in the chromosomal region downstream of the dcw cluster in Streptococcus pneumoniae. Journal of bacteriology 185: 6209-6214.
23. Kuru E, Hughes HV, Brown PJ, Hall E, Tekkam S, et al. (2012) In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angewandte Chemie 51: 12519-12523.
24. Pilhofer M, Aistleitner K, Biboy J, Gray J, Kuru E, et al. (2013) Discovery of chlamydial peptidoglycan reveals bacteria with murein sacculi but without FtsZ. Nature communications 4: 2856.
25. Land AD, Tsui HC, Kocaoglu O, Vella SA, Shaw SL, et al. (2013) Requirement of essential Pbp2x and GpsB for septal ring closure in Streptococcus pneumoniae D39. Molecular microbiology 90: 939-955.
26. 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.
27. Kaval KG, Halbedel S, (2012) Architecturally the same, but playing a different game: the diverse species-specific roles of DivIVA proteins. Virulence 3: 406-407.
28. Hempel AM, Wang SB, Letek M, Gil JA, Flardh K, (2008) Assemblies of DivIVA mark sites for hyphal branching and can establish new zones of cell wall growth in Streptomyces coelicolor. Journal of bacteriology 190: 7579-7583.
29. Kang CM, Nyayapathy S, Lee JY, Suh JW, Husson RN, (2008) Wag31, a homologue of the cell division protein DivIVA, regulates growth, morphology and polar cell wall synthesis in mycobacteria. Microbiology 154: 725-735.
30. Letek M, Ordonez E, Vaquera J, Margolin W, Flardh K, et al. (2008) DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. Journal of bacteriology 190: 3283-3292.
31. Vicente M, Garcia-Ovalle M, (2007) Making a point: the role of DivIVA in streptococcal polar anatomy. Journal of bacteriology 189: 1185-1188.
32. Giefing-Kroll C, Jelencsics KE, Reipert S, Nagy E, (2011) Absence of pneumococcal PcsB is associated with overexpression of LysM domain-containing proteins. Microbiology 157: 1897-1909.
33. Halbedel S, Hahn B, Daniel RA, Flieger A, (2012) DivIVA affects secretion of virulence-related autolysins in Listeria monocytogenes. Molecular microbiology 83: 821-839.
34. van Opijnen T, Bodi KL, Camilli A, (2009) Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nature methods 6: 767-772.
35. Thanassi JA, Hartman-Neumann SL, Dougherty TJ, Dougherty BA, Pucci MJ, (2002) Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic acids research 30: 3152-3162.
36. Song JH, Ko KS, Lee JY, Baek JY, Oh WS, et al. (2005) Identification of essential genes in Streptococcus pneumoniae by allelic replacement mutagenesis. Molecules and cells 19: 365-374.
37. Hoskins J, Matsushima P, Mullen DL, Tang J, Zhao G, et al. (1999) Gene disruption studies of penicillin-binding proteins 1a, 1b, and 2a in Streptococcus pneumoniae. Journal of bacteriology 181: 6552-6555.
38. Paik J, Kern I, Lurz R, Hakenbeck R, (1999) Mutational analysis of the Streptococcus pneumoniae bimodular class A penicillin-binding proteins. Journal of bacteriology 181: 3852-3856.
39. Wheeler R, Mesnage S, Boneca IG, Hobbs JK, Foster SJ, (2011) Super-resolution microscopy reveals cell wall dynamics and peptidoglycan architecture in ovococcal bacteria. Molecular microbiology 82: 1096-1109.
40. Berg KH, Stamsas GA, Straume D, Havarstein LS, (2013) Effects of Low PBP2b Levels on Cell Morphology and Peptidoglycan Composition in Streptococcus pneumoniae R6. Journal of bacteriology 195: 4342-4354.
41. Kang CM, Abbott DW, Park ST, Dascher CC, Cantley LC, et al. (2005) The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes & development 19: 1692-1704.
42. Hempel AM, Cantlay S, Molle V, Wang SB, Naldrett MJ, et al. (2012) The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces. Proc Natl Acad Sci U S A 109: E2371-2379.
43. Pearlman SM, Serber Z, Ferrell JE Jr, (2011) A mechanism for the evolution of phosphorylation sites. Cell 147: 934-946.
44. Martin B, Prudhomme M, Alloing G, Granadel C, Claverys JP, (2000) Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Molecular microbiology 38: 867-878.
45. Canova MJ, Kremer L, Molle V, (2008) pETPhos: a customized expression vector designed for further characterization of Ser/Thr/Tyr protein kinases and their substrates. Plasmid 60: 149-153.
46. Martin B, Granadel C, Campo N, Henard V, Prudhomme M, et al. (2010) Expression and maintenance of ComD-ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae. Molecular microbiology 75: 1513-1528.
47. Eberhardt A, Wu LJ, Errington J, Vollmer W, Veening JW, (2009) Cellular localization of choline-utilization proteins in Streptococcus pneumoniae using novel fluorescent reporter systems. Molecular microbiology 74: 395-408.
48. Sung CK, Li H, Claverys JP, Morrison DA, (2001) An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Applied and environmental microbiology 67: 5190-5196.
49. Morlot C, Zapun A, Dideberg O, Vernet T, (2003) Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. Molecular microbiology 50: 845-855.
50. de Jong IG, Beilharz K, Kuipers OP, Veening JW, (2011) Live Cell Imaging of Bacillus subtilis and Streptococcus pneumoniae using Automated Time-lapse Microscopy. Journal of visualized experiments: JoVE ((53)) pp. 3145.
51. Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, et al. (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 7: 299-307.
52. Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, et al. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Molecular & cellular proteomics: Mol Cell Proteomics 4: 2010-2021.
53. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, et al. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nature protocols 4: 698-705.
54. Gouet P, Robert X, Courcelle E, (2003) ESPript/ENDscript: Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic acids research 31: 3320-3323.