Subpolar addition of new cell wall is directed by DivIVA in mycobacteria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 31, 2014, Pages

  Meniche, Xavier ^a   Otten, Renee ^b   Siegrist, M Sloan ^c   Baer, Christina E ^a   Murphy, Kenan C ^a   Bertozzi, Carolyn R ^a   Sassetti, Christopher M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Polarity; Tuberculosis

Indexed keywords

MYCOLIC ACID; TROPOMYOSIN; TROPOMYOSIN LIKE PROTEIN DIVIVA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL GROWTH; CELL SHAPE; MYCOBACTERIUM; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SYNTHESIS;

POLARITY; TUBERCULOSIS;

BACTERIAL PROTEINS; CELL CYCLE PROTEINS; CELL MEMBRANE; CELL POLARITY; CELL WALL; MODELS, BIOLOGICAL; MYCOBACTERIUM SMEGMATIS; MYCOLIC ACIDS; PROTEIN BINDING;

EID: 84905650444     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1402158111     Document Type: Article

References (54)

1. de Pedro MA, Quintela JC, Höltje JV, Schwarz H (1997) Murein segregation in Escherichia coli. J Bacteriol 179(9):2823-2834. (Pubitemid 27194426)
2. Daniel RA, Errington J (2003) Control of cell morphogenesis in bacteria: Two distinct ways to make a rod-shaped cell. Cell 113(6):767-776. (Pubitemid 36724940)
3. Salje J, van den Ent F, de Boer P, Löwe J (2011) Direct membrane binding by bacterial actin MreB. Mol Cell 43(3):478-487.
4. Wagner JK, Galvani CD, Brun YV (2005) Caulobacter crescentus requires RodA and MreB for stalk synthesis and prevention of ectopic pole formation. J Bacteriol 187(2):544-553. (Pubitemid 40096243)
5. Brown PJ, et al. (2012) Polar growth in the Alphaproteobacterial order Rhizobiales. Proc Natl Acad Sci USA 109(5):1697-1701.
6. Flärdh K (2003) Growth polarity and cell division in Streptomyces. Curr Opin Microbiol 6(6):564-571.
7. Thanky NR, Young DB, Robertson BD (2007) Unusual features of the cell cycle in mycobacteria: Polar-restricted growth and the snapping-model of cell division. Tuberculosis (Edinb) 87(3):231-236. (Pubitemid 46551845)
8. Aldridge BB, et al. (2012) Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science 335(6064):100-104.
9. Santi I, Dhar N, Bousbaine D, Wakamoto Y, McKinney JD (2013) Single-cell dynamics of the chromosome replication and cell division cycles in mycobacteria. Nat Commun 4:2470.
10. Hett EC, Rubin EJ (2008) Bacterial growth and cell division: A mycobacterial perspective. Microbiol Mol Biol Rev 72(1):126-156. (Pubitemid 351398058)
11. Daffe M, Brennan PJ, McNeil M (1990) Predominant structural features of the cell wall arabinogalactan of Mycobacterium tuberculosis as revealed through characterization of oligoglycosyl alditol fragments by gas chromatography/mass spectrometry and by 1H and 13C NMR analyses. J Biol Chem 265(12):6734-6743.
12. McNeil M, Daffe M, Brennan PJ (1991) Location of the mycolyl ester substituents in the cell walls of mycobacteria. J Biol Chem 266(20):13217-13223. (Pubitemid 21907331)
13. Liu J, Barry CE, 3rd, Besra GS, Nikaido H (1996) Mycolic acid structure determines the fluidity of the mycobacterial cell wall. J Biol Chem 271(47):29545-29551. (Pubitemid 26389573)
14. Liu J, Rosenberg EY, Nikaido H (1995) Fluidity of the lipid domain of cell wall from Mycobacterium chelonae. Proc Natl Acad Sci USA 92(24):11254-11258.
15. Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H (2008) Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 105(10):3963-3967. (Pubitemid 351723507)
16. Zuber B, et al. (2008) Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J Bacteriol 190(16):5672-5680.
17. Daffé M, Draper P (1998) The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 39:131-203. (Pubitemid 29077883)
18. Hempel AM, et al. (2012) The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces. Proc Natl Acad Sci USA 109(35):E2371-E2379.
19. Nguyen L, et al. (2007) Antigen 84, an effector of pleiomorphism in Mycobacterium smegmatis. J Bacteriol 189(21):7896-7910. (Pubitemid 350035098)
20. 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(Pt 3):725-735. (Pubitemid 351736287)
21. Letek M, et al. (2008) DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J Bacteriol 190(9):3283-3292. (Pubitemid 351581424)
22. Edwards DH, Errington J (1997) The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol 24(5):905-915. (Pubitemid 27286144)
23. Cha JH, Stewart GC (1997) The divIVA minicell locus of Bacillus subtilis. J Bacteriol 179(5):1671-1683.
24. Ginda K, et al. (2013) ParA of Mycobacterium smegmatis co-ordinates chromosome segregation with the cell cycle and interacts with the polar growth determinant DivIVA. Mol Microbiol 87(5):998-1012.
25. Donovan C, Sieger B, Krämer R, Bramkamp M (2012) A synthetic Escherichia coli system identifies a conserved origin tethering factor in Actinobacteria. Mol Microbiol 84(1):105-116.
26. Salmond GP, Lutkenhaus JF, Donachie WD (1980) Identification of new genes in a cell envelope-cell division gene cluster of Escherichia coli: Cell envelope gene murG. J Bacteriol 144(1):438-440. (Pubitemid 11211069)
27. Kremer L, et al. (2001) Galactan biosynthesis in Mycobacterium tuberculosis. Identification of a bifunctional UDP-galactofuranosyltransferase. J Biol Chem 276(28): 26430-26440.
28. Portevin D, et al. (2004) A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci USA 101(1):314-319. (Pubitemid 38084247)
29. Lea-Smith DJ, et al. (2007) The reductase that catalyzes mycolic motif synthesis is required for efficient attachment of mycolic acids to arabinogalactan. J Biol Chem 282(15):11000-11008. (Pubitemid 47100777)
30. Wei JR, et al. (2011) Depletion of antibiotic targets has widely varying effects on growth. Proc Natl Acad Sci USA 108(10):4176-4181.
31. Joyce G, et al. (2012) Cell division site placement and asymmetric growth in mycobacteria. PLoS ONE 7(9):e44582.
32. Gee CL, et al. (2012) A phosphorylated pseudokinase complex controls cell wall synthesis in mycobacteria. Sci Signal 5(208):ra7.
33. Siegrist MS, et al. (2013) (D)-amino acid chemical reporters reveal peptidoglycan dynamics of an intracellular pathogen. ACS Chem Biol 8(3):500-505.
34. Lenarcic R, et al. (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28(15):2272-2282.
35. Ramamurthi KS, Losick R (2009) Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proc Natl Acad Sci USA 106(32):13541-13545.
36. Oliva MA, et al. (2010) Features critical for membrane binding revealed by DivIVA crystal structure. EMBO J 29(12):1988-2001.
37. Pogliano J, Pogliano N, Silverman JA (2012) Daptomycin-mediated reorganization of membrane architecture causes mislocalization of essential cell division proteins. J Bacteriol 194(17):4494-4504.
38. Gande R, et al. (2007) The two carboxylases of Corynebacterium glutamicum essential for fatty acid and mycolic acid synthesis. J Bacteriol 189(14):5257-5264. (Pubitemid 47076071)
39. Portevin D, et al. (2005) The acyl-AMP ligase FadD32 and AccD4-containing acyl-CoA carboxylase are required for the synthesis of mycolic acids and essential for mycobacterial growth: Identification of the carboxylation product and determination of the acyl-CoA carboxylase components. J Biol Chem 280(10):8862-8874. (Pubitemid 40409576)
40. Trivedi OA, et al. (2004) Enzymic activation and transfer of fatty acids as acyladenylates in mycobacteria. Nature 428(6981):441-445. (Pubitemid 38419691)
41. Wakamoto Y, et al. (2013) Dynamic persistence of antibiotic-stressed mycobacteria. Science 339(6115):91-95, 10.1126/science.1229858.
42. Walters SB, et al. (2006) The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol 60(2):312-330.
43. Gonzalo Asensio J, et al. (2006) The virulence-associated two-component PhoP-PhoR system controls the biosynthesis of polyketide-derived lipids in Mycobacterium tuberculosis. J Biol Chem 281(3):1313-1316.
44. Chauhan A, et al. (2006) Mycobacterium tuberculosis cells growing in macrophages are filamentous and deficient in FtsZ rings. J Bacteriol 188(5):1856-1865. (Pubitemid 43346864)
45. Kang CM, et al. (2005) The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: Substrate identification and regulation of cell shape. Genes Dev 19(14): 1692-1704.
46. Jani C, et al. (2010) Regulation of polar peptidoglycan biosynthesis by Wag31 phosphorylation in mycobacteria. BMC Microbiol 10:327.
47. Holmes NA, et al. (2013) Coiled-coil protein Scy is a key component of a multiprotein assembly controlling polarized growth in Streptomyces. Proc Natl Acad Sci USA 110(5):E397-E406.
48. Hempel AM, Wang SB, Letek M, Gil JA, Flärdh K (2008) Assemblies of DivIVA mark sites for hyphal branching and can establish new zones of cell wall growth in Streptomyces coelicolor. J Bacteriol 190(22):7579-7583.
49. Léger M, et al. (2009) The dual function of the Mycobacterium tuberculosis FadD32 required for mycolic acid biosynthesis. Chem Biol 16(5):510-519.
50. Gavalda S, et al. (2009) The Pks13/FadD32 crosstalk for the biosynthesis of mycolic acids in Mycobacterium tuberculosis. J Biol Chem 284(29):19255-19264.
51. Fuchino K, et al. (2013) Dynamic gradients of an intermediate filament-like cytoskeleton are recruited by a polarity landmark during apical growth. Proc Natl Acad Sci USA 110(21):E1889-E1897.
52. Sampson SL, et al. (2004) Protection elicited by a double leucine and pantothenate auxotroph of Mycobacterium tuberculosis in guinea pigs. Infect Immun 72(5):3031-3037. (Pubitemid 38542434)
53. van Kessel JC, Hatfull GF (2007) Recombineering in Mycobacterium tuberculosis. Nat Methods 4(2):147-152. (Pubitemid 46454684)
54. Lamprecht MR, Sabatini DM, Carpenter AE (2007) CellProfiler: Free, versatile software for automated biological image analysis. Biotechniques 42(1):71-75.