The enterococcal cytolysin synthetase has an unanticipated lipid kinase fold

eLife

Volumn 4, Issue JULY2015, 2015, Pages

  Dong, Shi Hui ^a   Tang, Weixin ^b   Lukk, Tiit ^c   Yu, Yi ^a   Nair, Satish K ^a   van der donk, Wilfred A ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOLYSIN; ENTEROCOCCAL CYTOLYSIN; LANTHIONINE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE; SYNTHETASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; LIGASE; PERFORIN; PHOSPHOTRANSFERASE;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME SUBSTRATE; GENE EXPRESSION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MUTAGENESIS; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY; BIOSYNTHESIS; CHEMISTRY; ENTEROCOCCUS; ENZYMOLOGY; HUMAN; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION;

CRYSTALLOGRAPHY, X-RAY; ENTEROCOCCUS; HUMANS; LIGASES; MODELS, MOLECULAR; PERFORIN; PHOSPHOTRANSFERASES; PROTEIN CONFORMATION;

EID: 84940538541     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07607     Document Type: Article

References (62)

1. Abts A, Montalban-Lopez M, Kuipers OP, Smits SH, Schmitt L. 2013. NisC binds the FxLx motif of the nisin leader peptide. Biochemistry 52:5387-5395. doi: 10.1021/bi4008116.
2. Aon JC, Caimi RJ, Taylor AH, Lu Q, Oluboyede F, Dally J, Kessler MD, Kerrigan JJ, Lewis TS, Wysocki LA, Patel PS. 2008. Suppressing posttranslational gluconoylation of heterologous proteins by metabolic engineering of Escherichia coli. Applied and Environmental Microbiology 74:950-958. doi: 10.1128/AEM. 01790-07.
3. Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS, Bulaj G, Camarero JA, Campopiano DJ, Challis GL, Clardy J, Cotter PD, Craik DJ, Dawson M, Dittmann E, Donadio S, Dorrestein PC, Entian KD, Fischbach MA, Garavelli JS, Göransson U, Gruber CW, Haft DH, Hemscheidt TK, Hertweck C, Hill C, Horswill AR, Jaspars M, Kelly WL, Klinman JP, Kuipers OP, Link AJ, Liu W, Marahiel MA, Mitchell DA, Moll GN, Moore BS, Müller R, Nair SK, Nes IF, Norris GE, Olivera BM, Onaka H, Patchett ML, Piel J, Reaney MJ, Rebuffat S, Ross RP, Sahl HG, Schmidt EW, Selsted ME, Severinov K, Shen B, Sivonen K, Smith L, Stein T, Süssmuth RD, Tagg JR, Tang GL, Truman AW, Vederas JC, Walsh CT, Walton JD, Wenzel SC, Willey JM, van der Donk WA. 2013. Ribosomally synthesized and Post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Natural Product Reports 30:108-160. doi: 10.1039/c2np20085f.
4. Bao ZQ, Jacobsen DM, Young MA. 2011. Briefly bound to activate: transient binding of a second catalytic magnesium activates the structure and dynamics of CDK2 kinase for catalysis. Structure 19:675-690. doi: 10.1016/j.str.2011.02.016.
5. Bierbaum G, Sahl HG. 2009. Lantibiotics: mode of action, biosynthesis and bioengineering. Current Pharmaceutical Biotechnology 10:2-18. doi: 10.2174/138920109787048616.
6. Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM, Bricogne G. 2004. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallographica. Section D, Biological Crystallography 60:2210-2221. doi: 10.1107/S0907444904016427.
7. Booth MC, Bogie CP, Sahl HG, Siezen RJ, Hatter KL, Gilmore MS. 1996. Structural analysis and proteolytic activation of Enterococcus faecalis cytolysin, a novel lantibiotic. Molecular Microbiology 21:1175-1184. doi: 10.1046/j.1365-2958.1996.831449.x.
8. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W. 2003. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallographica. Section D, Biological Crystallography 59:2023-2030. doi: 10.1107/S0907444903017694.
9. Burkhart BJ, Hudson GA, Dunbar KL, Mitchell DA. 2015. A prevalent peptide-binding domain guides ribosomal natural product biosynthesis. Nature Chemical Biology 11:558-563. doi: 10.1038/nchembio.1856.
10. Chatterjee C, Miller LM, Leung YL, Xie L, Yi M, Kelleher NL, van der Donk WA. 2005. Lacticin 481 synthetase phosphorylates its substrate during lantibiotic production. Journal of the American Chemical Society 127: 15332-15333. doi: 10.1021/ja0543043.
11. Chen J, Zheng XF, Brown EJ, Schreiber SL. 1995. Identification of an 11-kDa FKBP12-rapamycin-binding domain within the 289-kDa FKBP12-rapamycin-associated protein and characterization of a critical serine residue. Proceedings of the National Academy of Sciences of USA 92:4947-4951. doi: 10.1073/pnas.92.11.4947.
12. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica. Section D, Biological Crystallography 66:12-21. doi: 10.1107/S0907444909042073.
13. Choi J, Chen J, Schreiber SL, Clardy J. 1996. Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 273:239-242. doi: 10.1126/science.273.5272.239.
14. Chow JW, Thal LA, Perri MB, Vazquez JA, Donabedian SM, Clewell DB, Zervos MJ. 1993. Plasmid-associated hemolysin and aggregation substance production contribute to virulence in experimental enterococcal endocarditis. Antimicrobial Agents and Chemotherapy 37:2474-2477. doi: 10.1128/AAC.37.11.2474.
15. Chung CH, Kurien BT, Mehta P,MhatreM, Mou S, Pye QN, Stewart C,WestM, Williamson KS, Post J, Liu L, Wang R, Hensley K. 2007. Identification of lanthionine synthase C-like protein-1 as a prominent glutathione binding protein expressed in the mammalian central nervous system. Biochemistry 46:3262-3269. doi: 10.1021/bi061888s.
16. Cox CR, Coburn PS, Gilmore MS. 2005. Enterococcal cytolysin: a novel two component peptide system that serves as a bacterial defense against eukaryotic and prokaryotic cells. Current Protein & Peptide Science 6:77-84. doi: 10.2174/1389203053027557.
17. Crowther GS, Baines SD, Todhunter SL, Freeman J, Chilton CH, Wilcox MH. 2013. Evaluation of NVB302 versus vancomycin activity in an in vitro human gut model of Clostridium difficile infection. The Journal of Antimicrobial Chemotherapy 68:168-176. doi: 10.1093/jac/dks359.
18. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallographica. Section D, Biological Crystallography 66:486-501. doi: 10.1107/S0907444910007493.
19. Garg N, Salazar-Ocampo LM, van der Donk WA. 2013. In vitro activity of the nisin dehydratase NisB. Proceedings of the National Academy of Sciences of USA 110:7258-7263. doi: 10.1073/pnas.1222488110.
20. Gilmore MS, Segarra RA, Booth MC, Bogie CP, Hall LR, Clewell DB. 1994. Genetic structure of the Enterococcus faecalis plasmid pAD1-encoded cytolytic toxin system and its relationship to lantibiotic determinants. Journal of Bacteriology 176:7335-7344.
21. Goto Y, Li B, Claesen J, Shi Y, Bibb MJ, van der DonkWA. 2010. Discovery of unique lanthionine synthetases reveals new mechanistic and evolutionary insights. PLOS Biology 8:e1000339. doi: 10.1371/journal.pbio.1000339.
22. Grasemann H, Stehling F, Brunar H, Widmann R, Laliberte TW, Molina L, Doring G, Ratjen F. 2007. Inhalation of Moli1901 in patients with cystic fibrosis. Chest 131:1461-1466. doi: 10.1378/chest.06-2085.
23. Hanks SK, Hunter T. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB Journal 9:576-596.
24. Huang C, Chen M, Pang D, Bi D, Zou Y, Xia X, Yang W, Luo L, Deng R, Tan H, Zhou L, Yu S, Guo L, Du X, Cui Y, Hu J, Mao Q, Worley PF, Xiao B. 2014. Developmental and activity-dependent expression of LanCL1 confers antioxidant activity required for neuronal survival. Developmental Cell 30:479-487. doi: 10.1016/j.devcel.2014.06.011.
25. Huycke MM, Spiegel CA, Gilmore MS. 1991. Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis. Antimicrobial Agents & Chemotherapy 35:1626-1634. doi: 10.1128/AAC.35.8.1626.
26. Ike Y, Clewell DB. 1984. Genetic analysis of the pAD1 pheromone response in Streptococcus faecalis, using transposon Tn917 as an insertional mutagen. Journal of Bacteriology 158:777-783.
27. Johnson AP. 2010. New antibiotics for selective treatment of gastrointestinal infection caused by Clostridium difficile. Expert Opinion on Therapeutic Patents 20:1389-1399. doi: 10.1517/13543776.2010.511177.
28. Jones AM, Helm JM. 2009. Emerging treatments in cystic fibrosis. Drugs 69:1903-1910. doi: 10.2165/11318500-000000000-00000.
29. Jungmann NA, Krawczyk B, Tietzmann M, Ensle P, Süssmuth RD. 2014. Dissecting reactions of nonlinear precursor peptide processing of the class III lanthipeptide curvopeptin. Journal of the American Chemical Society 136: 15222-15228. doi: 10.1021/ja5062054.
30. Kabsch W. 2014. Processing of X-ray snapshots from crystals in random orientations. Acta Crystallographica. Section D, Biological Crystallography 70:2204-2216. doi: 10.1107/S1399004714013534.
31. Knerr PJ, van der Donk WA. 2012. Discovery, biosynthesis, and engineering of lantipeptides. Annual Review of Biochemistry 81:479-505. doi: 10.1146/annurev-biochem-060110-113521.
32. Koehnke J, Bent AF, Zollman D, Smith K, HoussenWE, Zhu X,Mann G, Lebl T, Scharff R, Shirran S, Botting CH, Jaspars M, Schwarz-Linek U, Naismith JH. 2013. The cyanobactin heterocyclase enzyme: a processive adenylase that operates with a defined order of reaction. Angewandte Chemie International Edition 52:13991-13996. doi: 10.1002/anie.201306302.
33. Koehnke J, Mann G, Bent AF, Ludewig H, Shirran S, Botting C, Lebl T, Houssen WE, Jaspars M, Naismith JH. 2015. Structural analysis of leader peptide binding enables leader-free cyanobactin processing. Nature Chemical Biology 11:558-563. doi: 10.1038/nchembio.1841.
34. Li B, Yu JP, Brunzelle JS, Moll GN, van der Donk WA, Nair SK. 2006. Structure and mechanism of the lantibiotic cyclase involved in nisin biosynthesis. Science 311:1464-1467. doi: 10.1126/science.1121422.
35. Li H, Xu H, Zhou Y, Zhang J, Long C, Li S, Chen S, Zhou JM, Shao F. 2007. The phosphothreonine lyase activity of a bacterial type III effector family. Science 315:1000-1003. doi: 10.1126/science.1138960.
36. Ma H, Gao Y, Zhao F, Wang J, Teng K, Zhang J, Zhong J. 2014. Dissecting the catalytic and substrate binding activity of a class II lanthipeptide synthetase BovM. Biochemical and Biophysical Research Communications 450: 1126-1132. doi: 10.1016/j.bbrc.2014.06.129.
37. Ma H, Gao Y, Zhao F, Zhong J. 2015. Individual catalytic activity of two functional domains of bovicin HJ50 synthase BovM. Wei sheng wu xue bao 55:50-58.
38. Miller S, Tavshanjian B, Oleksy A, Perisic O, Houseman BT, Shokat KM, Williams RL. 2010. Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34. Science 327:1638-1642. doi: 10.1126/science.1184429.
39. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallographica. Section D, Biological Crystallography 67:355-367. doi: 10.1107/S0907444911001314.
40. Oliynyk I, Varelogianni G, Roomans GM, Johannesson M. 2010. Effect of duramycin on chloride transport and intracellular calcium concentration in cystic fibrosis and non-cystic fibrosis epithelia. APMIS 118:982-990. doi: 10.1111/j.1600-0463.2010.02680.x.
41. Oman TJ, van der Donk WA. 2010. Follow the leader: the use of leader peptides to guide natural product biosynthesis. Nature Chemical Biology 6:9-18. doi: 10.1038/nchembio.286.
42. Ortega MA, Hao Y, Zhang Q, Walker MC, van der Donk WA, Nair SK. 2015. Structure and mechanism of the tRNAdependent lantibiotic dehydratase NisB. Nature 517:509-512. doi: 10.1038/nature13888.
43. Otwinowski Z, Borek D, Majewski W, Minor W. 2003. Multiparametric scaling of diffraction intensities. Acta Crystallographica. Section A 59:228-234. doi: 10.1107/S0108767303005488.
44. Sheldrick GM. 2010. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallographica. Section D, Biological Crystallography 66:479-485. doi: 10.1107/S0907444909038360.
45. Shimafuji C, Noguchi M, Nishie M, Nagao JI, Shioya K, Zendo T, Nakayama J, Sonomoto K. 2015. In vitro catalytic activity of N-terminal and C-terminal domains in NukM, the post-translational modification enzyme of nukacin ISK-1. Journal of Bioscience and Bioengineering S1389-S1723. doi: 10.1016/j.jbiosc.2015.03.020.
46. Sibanda BL, Chirgadze DY, Blundell TL. 2010. Crystal structure of DNA-PKcs reveals a large open-ring cradle comprised of HEAT repeats. Nature 463:118-121. doi: 10.1038/nature08648.
47. Steiner I, Errhalt P, Kubesch K, Hubner M, Holy M, Bauer M, Müller M, Hinterberger S, Widmann R, Mascher D, Freissmuth M, Kneussl M. 2008. Pulmonary pharmacokinetics and safety of nebulized duramycin in healthy male volunteers. Naunyn-schmiedeberg's Archives of Pharmacology 378:323-333. doi: 10.1007/s00210-008-0293-8.
48. Sturla L, Fresia C, Guida L, Bruzzone S, Scarfì S, Usai C, Fruscione F, Magnone M, Millo E, Basile G, Grozio A, Jacchetti E, Allegretti M, De Flora A, Zocchi E. 2009. LANCL2 is necessary for abscisic acid binding and signaling in human granulocytes and in rat insulinoma cells. The Journal of Biological Chemistry 284:28045-28057. doi: 10. 1074/jbc.M109.035329.
49. Tang W, van der Donk WA. 2013. The sequence of the enterococcal cytolysin imparts unusual lanthionine stereochemistry. Nature Chemical Biology 9:157-159. doi: 10.1038/nchembio.1162.
50. Tao Z, Barker J, Shi SD, Gehring M, Sun S. 2010. Steady-state kinetic and inhibition studies of the mammalian target of rapamycin (mTOR) kinase domain and mTOR complexes. Biochemistry 49:8488-8498. doi: 10.1021/bi100673c.
51. Thibodeaux CJ, Ha T, van der Donk WA. 2014. A price to pay for relaxed substrate specificity: a comparative kinetic analysis of the class II lanthipeptide synthetases ProcM and HalM2. Journal of the American Chemical Society 136:17513-17529. doi: 10.1021/ja5089452.
52. Thibodeaux GN, McClerren AL, Ma Y, Gancayco MR, van der Donk WA. 2015. Synergistic binding of the leader and core peptides by the lantibiotic synthetase HalM2. ACS Chemical Biology 10:970-977. doi: 10.1021/cb5009876.
53. Van Tyne D, Martin MJ, Gilmore MS. 2013. Structure, function, and biology of the Enterococcus faecalis cytolysin. Toxins 5:895-911. doi: 10.3390/toxins5050895.
54. Walker EH, Perisic O, Ried C, Stephens L, Williams RL. 1999. Structural insights into phosphoinositide 3-kinase catalysis and signalling. Nature 402:313-320. doi: 10.1038/46319.
55. Williams R, Berndt A, Miller S, Hon WC, Zhang X. 2009. Form and flexibility in phosphoinositide 3-kinases. Biochemical Society Transactions 37:615-626. doi: 10.1042/BST0370615.
56. Yang H, Rudge DG, Koos JD, Vaidialingam B, Yang HJ, Pavletich NP. 2013. mTOR kinase structure, mechanism and regulation. Nature 497:217-223. doi: 10.1038/nature12122.
57. You YO, van der Donk WA. 2007. Mechanistic investigations of the dehydration reaction of lacticin 481 synthetase using site-directed mutagenesis. Biochemistry 46:5991-6000. doi: 10.1021/bi602663x.
58. Yu Y, Mukherjee S, van der Donk WA. 2015. Product formation by the promiscuous lanthipeptide synthetase ProcM is under kinetic control. Journal of the American Chemical Society 137:5140-5148. doi: 10.1021/jacs.5b01409.
59. Zeng M, van der Donk WA, Chen J. 2014. Lanthionine synthetase C-like protein 2 (LanCL2) is a novel regulator of Akt. Molecular Biology of the Cell 25:3954-3961. doi: 10.1091/mbc.E14-01-0004.
60. Zhang Q, Yu Y, Velásquez JE, van der Donk WA. 2012. Evolution of lanthipeptide synthetases. Proceedings of the National Academy of Sciences of USA 109:18361-18366. doi: 10.1073/pnas.1210393109.
61. ZhangW, Wang L, Liu Y, Xu J, Zhu G, Cang H, Li X, Bartlam M, Hensley K, Li G, Rao Z, Zhang XC. 2009. Structure of human lanthionine synthetase C-like protein 1 and its interaction with Eps8 and glutathione. Genes & Development 23:1387-1392. doi: 10.1101/gad.1789209.
62. Zhong WX, Wang YB, Peng L, Ge XZ, Zhang J, Liu SS, Zhang XN, Xu ZH, Chen Z, Luo JH. 2012. Lanthionine synthetase C-like protein 1 interacts with and inhibits cystathionine beta-synthase: a target for neuronal antioxidant defense. The Journal of Biological Chemistry 287:34189-34201. doi: 10.1074/jbc.M112.383646.