#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Fha Interaction with Phosphothreonine of TssL Activates Type VI Secretion in


The bacterial type VI secretion system (T6SS) resembles a contractile phage tail structure and functions to deliver effectors to eukaryotic or prokaryotic target cells for the survival of many pathogenic bacteria. T6SS is highly regulated by various regulatory systems at multiple levels in response to environmental cues. Post-translational regulation via threonine (Thr) phosphorylation is an emerging theme in regulating prokaryotic signaling, including T6SS; the knowledge is mainly contributed by studies of Hcp secretion island 1-encoded T6SS (H1-T6SS) of Pseudomonas aeruginosa. Here, we discover a new phosphorylated target, a T6SS core-component TssL, and demonstrate that this Thr phosphorylation event post-translationally regulates type VI secretion in a plant pathogenic bacterium, Agrobacterium tumefaciens. We provide the first demonstration that the specific binding of Fha, a forkhead-associated domain-containing protein, to the phosphorylated target is required to stimulate type VI secretion. Genetic and biochemical data strongly suggest an ordered TssL-phosphorylation–dependent assembly and secretion pathway.


Vyšlo v časopise: Fha Interaction with Phosphothreonine of TssL Activates Type VI Secretion in. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003991
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003991

Souhrn

The bacterial type VI secretion system (T6SS) resembles a contractile phage tail structure and functions to deliver effectors to eukaryotic or prokaryotic target cells for the survival of many pathogenic bacteria. T6SS is highly regulated by various regulatory systems at multiple levels in response to environmental cues. Post-translational regulation via threonine (Thr) phosphorylation is an emerging theme in regulating prokaryotic signaling, including T6SS; the knowledge is mainly contributed by studies of Hcp secretion island 1-encoded T6SS (H1-T6SS) of Pseudomonas aeruginosa. Here, we discover a new phosphorylated target, a T6SS core-component TssL, and demonstrate that this Thr phosphorylation event post-translationally regulates type VI secretion in a plant pathogenic bacterium, Agrobacterium tumefaciens. We provide the first demonstration that the specific binding of Fha, a forkhead-associated domain-containing protein, to the phosphorylated target is required to stimulate type VI secretion. Genetic and biochemical data strongly suggest an ordered TssL-phosphorylation–dependent assembly and secretion pathway.


Zdroje

1. BoyerF, FichantG, BerthodJ, VandenbrouckY, AttreeI (2009) Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10: 104.

2. PukatzkiS, MaAT, RevelAT, SturtevantD, MekalanosJJ (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A 104: 15508–15513.

3. SchwarzS, HoodRD, MougousJD (2010) What is type VI secretion doing in all those bugs? Trends Microbiol 18: 531–537.

4. HoodRD, SinghP, HsuF, GuvenerT, CarlMA, et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7: 25–37.

5. RussellAB, SinghP, BrittnacherM, BuiNK, HoodRD, et al. (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11: 538–549.

6. EnglishG, TrunkK, RaoVA, SrikannathasanV, HunterWN, et al. (2012) New secreted toxins and immunity proteins encoded within the type VI secretion system gene cluster of Serratia marcescens. Mol Microbiol 86: 921–936.

7. BaslerM, PilhoferM, HendersonGP, JensenGJ, MekalanosJJ (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483: 182–186.

8. KapiteinN, BonemannG, PietrosiukA, SeyfferF, HausserI, et al. (2013) ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol Microbiol 87: 1013–1028.

9. BonemannG, PietrosiukA, DiemandA, ZentgrafH, MogkA (2009) Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 28: 315–325.

10. SilvermanJM, BrunetYR, CascalesE, MougousJD (2012) Structure and Regulation of the Type VI Secretion System. Annu Rev Microbiol 66: 453–472.

11. LinJS, MaLS, LaiEM (2013) Systematic Dissection of the Agrobacterium Type VI secretion system reveals machinery and secreted components for subcomplex formation. PLoS One 8: e67647.

12. SilvermanJM, AgnelloDM, ZhengH, AndrewsBT, LiM, et al. (2013) Haemolysin coregulated protein Is an exported receptor and chaperone of type VI secretion substrates. Mol Cell 51: 584–593.

13. ZhengJ, LeungKY (2007) Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66: 1192–1206.

14. BaslerM, MekalanosJJ (2012) Type 6 secretion dynamics within and between bacterial cells. Science 337: 815.

15. BrunetYR, EspinosaL, HarchouniS, MignotT, CascalesE (2013) Imaging type VI secretion-mediated bacterial killing. Cell Rep 3: 1–6.

16. LerouxM, De LeonJA, KuwadaNJ, RussellAB, Pinto-SantiniD, et al. (2012) Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword. Proc Natl Acad Sci U S A 109: 19804–19809.

17. BaslerM, HoBT, MekalanosJJ (2013) Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152: 884–894.

18. ShalomG, ShawJG, ThomasMS (2007) In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. Microbiology 153: 2689–2699.

19. ZhengJ, HoB, MekalanosJJ (2011) Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS One 6: e23876.

20. MaLS, LinJS, LaiEM (2009) An IcmF family protein, ImpLM, is an integral inner membrane protein interacting with ImpKL, and its walker a motif is required for type VI secretion system-mediated Hcp secretion in Agrobacterium tumefaciens. J Bacteriol 191: 4316–4329.

21. Felisberto-RodriguesC, DurandE, AschtgenMS, BlangyS, Ortiz-LombardiaM, et al. (2011) Towards a structural comprehension of bacterial type VI secretion systems: characterization of the TssJ-TssM complex of an Escherichia coli pathovar. PLoS Pathog 7: e1002386.

22. MaLS, NarberhausF, LaiEM (2012) IcmF family protein TssM exhibits ATPase activity and energizes type VI secretion. J Biol Chem 287: 15610–15621.

23. DurandE, ZouedA, SpinelliS, WatsonPJ, AschtgenMS, et al. (2012) Structural characterization and oligomerization of the TssL protein, a component shared by bacterial type VI and type IVb secretion systems. J Biol Chem 287: 14157–14168.

24. RobbCS, NanoFE, BorastonAB (2012) The structure of the conserved type six secretion protein TssL (DotU) from Francisella novicida. J Mol Biol 419: 277–283.

25. CascalesE, CambillauC (2012) Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci 367: 1102–1111.

26. CascalesE (2008) The type VI secretion toolkit. EMBO Rep 9: 735–741.

27. SilvermanJM, AustinLS, HsuF, HicksKG, HoodRD, et al. (2011) Separate inputs modulate phosphorylation-dependent and -independent type VI secretion activation. Mol Microbiol 82: 1277–1290.

28. FritschMJ, TrunkK, Alcoforado DinizJ, GuoM, TrostM, et al. (2013) Proteomic identification of novel secreted anti-bacterial toxins of the Serratia marcescens type VI secretion system. Mol Cell Proteomics 12: 2739–2749.

29. MougousJD, GiffordCA, RamsdellTL, MekalanosJJ (2007) Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 9: 797–803.

30. HsuF, SchwarzS, MougousJD (2009) TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol Microbiol 72: 1111–1125.

31. CasabonaMG, SilvermanJM, SallKM, BoyerF, CouteY, et al. (2013) An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa. Environ Microbiol 15: 471–486.

32. PallenM, ChaudhuriR, KhanA (2002) Bacterial FHA domains: neglected players in the phospho-threonine signalling game? Trends Microbiol 10: 556–563.

33. DurocherD, JacksonSP (2002) The FHA domain. FEBS Lett 513: 58–66.

34. DurocherD, TaylorIA, SarbassovaD, HaireLF, WestcottSL, et al. (2000) The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol Cell 6: 1169–1182.

35. MahajanA, YuanC, LeeH, ChenES, WuPY, et al. (2008) Structure and function of the phosphothreonine-specific FHA domain. Sci Signal 1: re12.

36. HofmannK, BucherP (1995) The FHA domain: a putative nuclear signalling domain found in protein kinases and transcription factors. Trends Biochem Sci 20: 347–349.

37. ColeST, BroschR, ParkhillJ, GarnierT, ChurcherC, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537–544.

38. GuptaM, SajidA, AroraG, TandonV, SinghY (2009) Forkhead-associated domain-containing protein Rv0019c and polyketide-associated protein PapA5, from substrates of serine/threonine protein kinase PknB to interacting proteins of Mycobacterium tuberculosis. J Biol Chem 284: 34723–34734.

39. GeeCL, PapavinasasundaramKG, BlairSR, BaerCE, FalickAM, et al. (2012) A phosphorylated pseudokinase complex controls cell wall synthesis in mycobacteria. Sci Signal 5: ra7.

40. WuCF, LinJS, ShawGC, LaiEM (2012) Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog 8: e1002938.

41. WuHY, ChungPC, ShihHW, WenSR, LaiEM (2008) Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J Bacteriol 190: 2841–2850.

42. HanksSK, HunterT (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9: 576–596.

43. WuHH, WuPY, HuangKF, KaoYY, TsaiMD (2012) Structural delineation of MDC1-FHA domain binding with CHK2-pThr68. Biochemistry 51: 575–577.

44. AndersonLB, HertzelAV, DasA (1996) Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc Natl Acad Sci U S A 93: 8889–8894.

45. LiuAC, ShihHW, HsuT, LaiEM (2008) A citrate-inducible gene, encoding a putative tricarboxylate transporter, is downregulated by the organic solvent DMSO in Agrobacterium tumefaciens. J Appl Microbiol 105: 1372–1383.

46. JiaYH, LiLP, HouQM, PanSQ (2002) An Agrobacterium gene involved in tumorigenesis encodes an outer membrane protein exposed on the bacterial cell surface. Gene 284: 113–124.

47. ChangBY, ChenKY, WenYD, LiaoCT (1994) The response of a Bacillus subtilis temperature-sensitive sigA mutant to heat stress. J Bacteriol 176: 3102–3110.

48. YuanZC, LiuP, SaenkhamP, KerrK, NesterEW (2008) Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a complex acid-mediated signaling involved in Agrobacterium-plant interactions. J Bacteriol 190: 494–507.

49. LiL, JiaY, HouQ, CharlesTC, NesterEW, et al. (2002) A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. Proc Natl Acad Sci U S A 99: 12369–12374.

50. LiuP, WoodD, NesterEW (2005) Phosphoenolpyruvate carboxykinase is an acid-induced, chromosomally encoded virulence factor in Agrobacterium tumefaciens. J Bacteriol 187: 6039–6045.

51. LeeH, YuanC, HammetA, MahajanA, ChenES, et al. (2008) Diphosphothreonine-specific interaction between an SQ/TQ cluster and an FHA domain in the Rad53-Dun1 kinase cascade. Mol Cell 30: 767–778.

52. PalmbosPL, WuD, DaleyJM, WilsonTE (2008) Recruitment of Saccharomyces cerevisiae Dnl4-Lif1 complex to a double-strand break requires interactions with Yku80 and the Xrs2 FHA domain. Genetics 180: 1809–1819.

53. MougousJD, CuffME, RaunserS, ShenA, ZhouM, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312: 1526–1530.

54. KadoCI, HeskettMG (1970) Selective media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas, and Xanthomonas. Phytopathology 60: 969–976.

55. BertaniG (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62: 293–300.

56. LaiEM, KadoCI (1998) Processed VirB2 is the major subunit of the promiscuous pilus of Agrobacterium tumefaciens. J Bacteriol 180: 2711–2717.

57. QuandtJ, HynesMF (1993) Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127: 15–21.

58. RosenfeldJ, CapdevielleJ, GuillemotJC, FerraraP (1992) In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal Biochem 203: 173–179.

59. HellmanU, WernstedtC, GonezJ, HeldinCH (1995) Improvement of an “In-Gel” digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal Biochem 224: 451–455.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 3
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#