A bacteriophage endolysin that eliminates intracellular streptococci

eLife

Volumn 5, Issue MARCH2016, 2016, Pages

  Shen, Yang ^a   Barros, Marilia ^b   Vennemann, Tarek ^b   Gallagher, D Travis ^a,c   Yin, Yizhou ^a   Linden, Sara B ^a   Heselpoth, Ryan D ^a   Spencer, Dennis J ^d   Donovan, David M ^e   Moult, John ^a   Fischetti, Vincent A ^d   Heinrich, Frank ^b,c   Lösche, Mathias ^b,c,f   Nelson, Daniel C ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

^f CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; ENDOLYSIN; PHOSPHATIDYLSERINE; UNCLASSIFIED DRUG; PROTEINASE;

ARTICLE; BACTERIOPHAGE; BACTERIUM MUTANT; CELL VIABILITY; CONTROLLED STUDY; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; EPIFLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INTRACELLULAR BACTERIUM; INTRACELLULAR KILLING; LUNG ALVEOLUS EPITHELIUM CELL; MOLECULAR DOCKING; PROTEIN INTERACTION; REFLECTOMETRY; SPECTROPHOTOMETRY; STREPTOCOCCUS; STREPTOCOCCUS PYOGENES; SURFACE PLASMON RESONANCE; X RAY DIFFRACTION; CELL MEMBRANE; CHEMISTRY; DNA MUTATIONAL ANALYSIS; DRUG EFFECTS; ENZYMOLOGY; EPITHELIUM CELL; GENETICS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PROTEIN TRANSPORT; SITE DIRECTED MUTAGENESIS; STREPTOCOCCUS PHAGE; X RAY CRYSTALLOGRAPHY;

CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; ENDOPEPTIDASES; EPITHELIAL CELLS; MICROBIAL VIABILITY; MOLECULAR DOCKING SIMULATION; MUTAGENESIS, SITE-DIRECTED; PHOSPHATIDYLSERINES; PROTEIN TRANSPORT; STREPTOCOCCUS PHAGES; STREPTOCOCCUS PYOGENES;

EID: 84968829634     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.13152     Document Type: Article

References (66)

1. Ahrén IL, Karlsson E, Forsgren A, Riesbeck K. 2002. Comparison of the antibacterial activities of ampicillin, ciprofloxacin, clarithromycin, telithromycin and quinupristin/dalfopristin against intracellular non-typeable Haemophilus influenzae. The Journal of Antimicrobial Chemotherapy 50:903–906. doi: 10.1093/jac/dkf221
2. Barer R, Joseph S. 1954. Refractometry of living cells. Part I. Basic principles. Quarterly Journal of Microscopical Science 95:399–423. doi: 10.1038/171720a0
3. Barnett TC, Liebl D, Seymour LM, Gillen CM, Lim JY, Larock CN, Davies MR, Schulz BL, Nizet V, Teasdale RD, Walker MJ. 2013. The globally disseminated M1T1 clone of group a Streptococcus evades autophagy for intracellular replication. Cell Host & Microbe 14:675–682. doi: 10.1016/j.chom.2013.11.003
4. Benesch J, Askendal A, Tengvall P. 2000. Quantification of adsorbed human serum albumin at solid interfaces: a comparison between radioimmunoassay (RIA) and simple null ellipsometry. Colloids B: Biointerfaces 18:71–81. doi: 10.1016/S0927-7765(99)00136-8
5. Borysowski J, Górski A. 2010. Fusion to cell-penetrating peptides will enable lytic enzymes to kill intracellular bacteria. Medical Hypotheses 74:164–166. doi: 10.1016/j.mehy.2009.07.006
6. Budvytyte R, Valincius G, Niaura G, Voiciuk V, Mickevicius M, Chapman H, Goh HZ, Shekhar P, Heinrich F, Shenoy S, Lösche M, Vanderah DJ. 2013. Structure and properties of tethered bilayer lipid membranes with unsaturated anchor molecules. Langmuir 29:8645–8656. doi: 10.1021/la401132c
7. Carapetis JR, Steer AC, Mulholland EK, Weber M. 2005. The global burden of group a streptococcal diseases. The Lancet. Infectious Diseases 5:685–694. doi: 10.1016/S1473-3099(05)70267-X
8. Carneiro FA, Lapido-Loureiro PA, Cordo SM, Stauffer F, Weissmüller G, Bianconi ML, Juliano MA, Juliano L, Bisch PM, Da Poian AT, Poian AT. 2006. Probing the interaction between vesicular stomatitis virus and phosphatidylserine. European Biophysics Journal: EBJ 35:145–154. doi: 10.1007/s00249-005-0012-z
9. Celia LK, Nelson D, Kerr DE. 2008. Characterization of a bacteriophage lysin (Ply700) from Streptococcus uberis. Veterinary Microbiology 130:107–117. doi: 10.1016/j.vetmic.2007.12.004
10. Couvreur P, Fattal E, Andremont A. 1991. Liposomes and nanoparticles in the treatment of intracellular bacterial infections. Pharmaceutical Research 8:1079–1086.
11. Cunningham MW. 2000. Pathogenesis of group a streptococcal infections. Clinical Microbiology Reviews 13: 470–511. doi: 10.1128/cmr.13.3.470-511.2000
12. Daniel A, Euler C, Collin M, Chahales P, Gorelick KJ, Fischetti VA. 2010. Synergism between a novel chimeric lysin and oxacillin protects against infection by methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 54:1603–1612. doi: 10.1128/AAC.01625-09
13. Davis IW, Baker D. 2009. RosettaLigand docking with full ligand and receptor flexibility. Journal of Molecular Biology 385:381–392. doi: 10.1016/j.jmb.2008.11.010
14. Di Grazia A, Luca V, Segev-Zarko LA, Shai Y, Mangoni ML. 2014. Temporins a and B stimulate migration of HaCaT keratinocytes and kill intracellular Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 58: 2520–2527. doi: 10.1128/AAC.02801-13
15. Dietz GP. 2010. Cell-penetrating peptide technology to deliver chaperones and associated factors in diseases and basic research. Current Pharmaceutical Biotechnology 11:167–174. doi: 10.2174/138920110790909731
16. Donovan DM, Foster-Frey J, Dong S, Rousseau GM, Moineau S, Pritchard DG. 2006. The cell lysis activity of the Streptococcus agalactiae bacteriophage B30 endolysin relies on the cysteine, histidine-dependent amidohydrolase/peptidase domain. Applied and Environmental Microbiology 72:5108–5112. doi: 10.1128/AEM.03065-05
17. Fischetti VA. 2005. Bacteriophage lytic enzymes: novel anti-infectives. Trends in Microbiology 13:491–496. doi: 10.1016/j.tim.2005.08.007
18. Gump JM, Dowdy SF. 2007. TAT transduction: the molecular mechanism and therapeutic prospects. Trends in Molecular Medicine 13:443–448. doi: 10.1016/j.molmed.2007.08.002
19. Heinrich F, Ng T, Vanderah DJ, Shekhar P, Mihailescu M, Nanda H, Lösche M. 2009. A new lipid anchor for sparsely tethered bilayer lipid membranes. Langmuir: The ACS Journal of Surfaces and Colloids 25:4219–4229. doi: 10.1021/la8033275
20. Heinrich F, Lösche M. 2014. Zooming in on disordered systems: neutron reflection studies of proteins associated with fluid membranes. Biochimica Et Biophysica Acta 1838:2341–2349. doi: 10.1016/j.bbamem.2014.03.007
21. Helaine S, Cheverton AM, Watson KG, Faure LM, Matthews SA, Holden DW. 2014. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 343:204–208. doi: 10.1126/science.1244705
22. Hing E, Hall MJ, Xu J. 2008. National Hospital Ambulatory Medical Care Survey: 2006 outpatient department summary. National Health Statistics Reports 4:1–31.
23. Iovino F, Gradstedt H, Bijlsma JJ. 2014. The proteasome-ubiquitin system is required for efficient killing of intracellular Streptococcus pneumoniae by brain endothelial cells. mBio 5:14:e00984. doi: 10.1128/mBio.00984-14
24. Kenis H, van Genderen H, Bennaghmouch A, Rinia HA, Frederik P, Narula J, Hofstra L, Reutelingsperger CP. 2004. Cell surface-expressed phosphatidylserine and annexin A5 open a novel portal of cell entry. The Journal of Biological Chemistry 279:52623–52629. doi: 10.1074/jbc.M409009200
25. Kienzle PA, Doucet M, McGillivray DJ, O’Donovan KV, Berk NF, Majkrzak CF. 2000-2010. Reflpak software. http://www.ncnr.nist.gov/reflpak/.
26. Kirby BJ, Kienzle PA, Maranville BB, Berk NF, Krycka J, Heinrich F, Majkrzak CF. 2012. Phase-sensitive specular neutron reflectometry for imaging the nanometer scale composition depth profile of thin-film materials. Current Opinion in Colloid Interface SciScience 17:44–53. doi: 10.1016/j.cocis.2011.11.001
27. Kugelberg E, Norström T, Petersen TK, Duvold T, Andersson DI, Hughes D. 2005. Establishment of a superficial skin infection model in mice by using Staphylococcus aureus and Streptococcus pyogenes. Antimicrobial Agents and Chemotherapy 49:3435–3441. doi: 10.1128/AAC.49.8.3435-3441.2005
28. LaPenta D, Rubens C, Chi E, Cleary PP. 1994. Group a streptococci efficiently invade human respiratory epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 91:12115–12119. doi: 10.1073/pnas.91.25.12115
29. Latif R, Ando T, Daniel S, Davies TF. 2003. Localization and regulation of thyrotropin receptors within lipid rafts. Endocrinology 144:4725–4728. doi: 10.1210/en.2003-0932
30. Lee CJ, Lin HR, Liao CL, Lin YL. 2008. Cholesterol effectively blocks entry of flavivirus. Journal of Virology 82: 6470–6480. doi: 10.1128/JVI.00117-08
31. Loessner MJ. 2005. Bacteriophage endolysins–current state of research and applications. Current Opinion in Microbiology 8:480–487. doi: 10.1016/j.mib.2005.06.002
32. Mandell GL, Coleman EJ. 2000. Activities of antimicrobial agents against intracellular pneumococci. Antimicrobial Agents and Chemotherapy 44:2561–2563. doi: 10.1128/aac.44.9.2561-2563.2000
33. Marouni MJ, Sela S. 2004. Fate of Streptococcus pyogenes and epithelial cells following internalization. Journal of Medical Microbiology 53:1–7. doi: 10.1099/jmm.0.05263-0
34. McGillivray DJ, Valincius G, Vanderah DJ, Febo-Ayala W, Woodward JT, Heinrich F, Kasianowicz JJ, Lösche M. 2007. Molecular-scale structural and functional characterization of sparsely tethered bilayer lipid membranes. Biointerphases 2:21–33. doi: 10.1116/1.2709308
35. McGillivray DJ, Valincius G, Heinrich F, Robertson JW, Vanderah DJ, Febo-Ayala W, Ignatjev I, Lösche M, Kasianowicz JJ. 2009. Structure of functional Staphylococcus aureus alpha-hemolysin channels in tethered bilayer lipid membranes. Biophysical Journal 96:1547–1553. doi: 10.1016/j.bpj.2008.11.020
36. McGowan S, Buckle AM, Mitchell MS, Hoopes JT, Gallagher DT, Heselpoth RD, Shen Y, Reboul CF, Law RH, Fischetti VA, Whisstock JC, Nelson DC. 2012. X-ray crystal structure of the streptococcal specific phage lysine PlyC. Proceedings of the National Academy of Sciences of the United States of America 109:12752–12757. doi: 10.1073/pnas.1208424109
37. Meiler J, Baker D. 2006. ROSETTALIGAND: protein-small molecule docking with full side-chain flexibility. Proteins 65:538–548. doi: 10.1002/prot.21086
38. Miteva MA, Guyon F, Tuffery P. 2010. Frog2: Efficient 3D conformation ensemble generator for small compounds. Nucleic Acids Research 38:W622–627. doi: 10.1093/nar/gkq325
39. Nanda H, Datta SA, Heinrich F, Lösche M, Rein A, Krueger S, Curtis JE. 2010. Electrostatic interactions and binding orientation of HIV-1 matrix studied by neutron reflectivity. Biophysical Journal 99:2516–2524. doi: 10.1016/j.bpj.2010.07.062
40. Nelson D, Loomis L, Fischetti VA. 2001. Prevention and elimination of upper respiratory colonization of mice by group a streptococci by using a bacteriophage lytic enzyme. Proceedings of the National Academy of Sciences of the United States of America 98:4107–4112. doi: 10.1073/pnas.061038398
41. Nelson D, Schuch R, Chahales P, Zhu S, Fischetti VA. 2006. PlyC: a multimeric bacteriophage lysin. Proceedings of the National Academy of Sciences of the United States of America 103:10765–10770. doi: 10.1073/pnas.0604521103
42. Nobbs AH, Lamont RJ, Jenkinson HF. 2009. Streptococcus adherence and colonization. Microbiology and Molecular Biology Reviews 73:407–450. doi: 10.1128/MMBR.00014-09
43. O’Seaghdha M, Wessels MR. 2013. Streptolysin O and its co-toxin NAD-glycohydrolase protect group a Streptococcus from Xenophagic killing. PLoS Pathogens 9:e1003394. doi: 10.1371/journal.ppat.1003394
44. Ogawa T, Terao Y, Okuni H, Ninomiya K, Sakata H, Ikebe K, Maeda Y, Kawabata S. 2011. Biofilm formation or internalization into epithelial cells enable Streptococcus pyogenes to evade antibiotic eradication in patients with pharyngitis. Microbial Pathogenesis 51:58–68. doi: 10.1016/j.micpath.2011.03.009
45. Osterlund A, Popa R, Nikkilä T, Scheynius A, Engstrand L. 1997. Intracellular reservoir of Streptococcus pyogenes in vivo: a possible explanation for recurrent pharyngotonsillitis. The Laryngoscope 107:640–647. doi: 10.1097/00005537-199705000-00016
46. Pastagia M, Schuch R, Fischetti VA, Huang DB. 2013. Lysins: the arrival of pathogen-directed anti-infectives. Journal of Medical Microbiology 62:1506–1516. doi: 10.1099/jmm.0.061028-0
47. Pentecost M, Kumaran J, Ghosh P, Amieva MR. 2010. Listeria monocytogenes Internalin B Activates junctionalJunctional endocytosis to accelerate intestinal invasion. PLoS 6:e1000900. doi: 10.1371/journal.ppat.1000900
48. Pfoh E, Wessels MR, Goldmann D, Lee GM. 2008. Burden and economic cost of group a streptococcal pharyngitis. Pediatrics 121:229–234. doi: 10.1542/peds.2007-0484
49. Rohde M, Cleary PP. 2016. Adhesion and invasion of Streptococcus pyogenes into host cells and clinical relevance of intracellular streptococci. In: Ferretti J. J, Stevens D. L, Fischetti V. A eds Streptococcus Pyogenes: Basic Biology to Clinical Manifestations. Oklahoma City OK.
50. Ryan PA, Pancholi V, Fischetti VA. 2001. Group a streptococci bind to mucin and human pharyngeal cells through sialic acid-containing receptors. Infection and Immunity 69:7402–7412. doi: 10.1128/IAI.69.12.7402-7412.2001
51. Sakurai A, Maruyama F, Funao J, Nozawa T, Aikawa C, Okahashi N, Shintani S, Hamada S, Ooshima T, Nakagawa I. 2010. Specific behavior of intracellular Streptococcus pyogenes that has undergone autophagic degradation is associated with bacterial streptolysin O and host small G proteins Rab5 and Rab7. The Journal of Biological Chemistry 285:22666–22675. doi: 10.1074/jbc.M109.100131
52. Schasfooort RBM, Tudos AJ. 2008. Handbook of Surface Plasmon Resonance. Cambridge: Royal Society of Chemistry.
53. Schuch R, Lee HM, Schneider BC, Sauve KL, Law C, Khan BK, Rotolo JA, Horiuchi Y, Couto DE, Raz A, Fischetti VA, Huang DB, Nowinski RC, Wittekind M. 2014. Combination therapy with lysin CF-301 and antibiotic is superior to antibiotic alone for treating methicillin-resistant Staphylococcus aureus-induced murine bacteremia. The Journal of Infectious Diseases 209:1469–1478. doi: 10.1093/infdis/jit637
54. Segawa K, Suzuki J, Nagata S. 2011. Constitutive exposure of phosphatidylserine on viable cells. Proceedings of the National Academy of Sciences of the United States of America 108:19246–19251. doi: 10.1073/pnas.1114799108
55. Sharma O, O’Seaghdha M, Velarde JJ, Wessels MR. 2016. NAD+-Glycohydrolase Promotes Intracellular Survival of Group a Streptococcus. PLoS Pathogens 12:e1005468. doi: 10.1371/journal.ppat.1005468
56. Shekhar P, Nanda H, Lösche M, Heinrich F. 2011. Continuous distribution model for the investigation of complex molecular architectures near interfaces with scattering techniques. Journal of Applied Physics 110:102216–10221612. doi: 10.1063/1.3661986
57. Shen Y, Koller T, Kreikemeyer B, Nelson DC. 2013. Rapid degradation of Streptococcus pyogenes biofilms by PlyC, a bacteriophage-encoded endolysin. Journal of Chemother 68:1818–1824. doi: 10.1093/jac/dkt104
58. Shenoy SS, Nanda H, Lösche M. 2012a. Membrane association of the PTEN tumor suppressor: electrostatic interaction with phosphatidylserine-containing bilayers and regulatory role of the C-terminal tail. Journal of Structural Biology 180:394–408. doi: 10.1016/j.jsb.2012.10.003
59. Shenoy S, Shekhar P, Heinrich F, Daou M-C, Gericke A, Ross AH, Lösche M. 2012b. Membrane association of the PTEN tumor suppressor: Molecular details of the protein-membrane complex from SPR binding studies and neutron reflection. PLoS ONE 7:e32591. doi: 10.1371/journal.pone.0032591
60. Su Y, Waring AJ, Ruchala P, Hong M. 2010. Membrane-bound dynamic structure of an arginine-rich cell-penetrating peptide, the protein transduction domain of HIV TAT, from solid-state NMR. Biochemistry 49: 6009–6020. doi: 10.1021/bi100642n
61. Tyagi M, Rusnati M, Presta M, Giacca M. 2001. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. The Journal of Biological Chemistry 276:3254–3261. doi: 10.1074/jbc.M006701200
62. Valincius G, McGillivray DJ, Febo-Ayala W, Vanderah DJ, Kasianowicz JJ, Lösche M. 2006. Enzyme activity to augment the characterization of tethered bilayer membranes. The Journal of Physical Chemistry B 110:10213–10216. doi: 10.1021/jp0616516
63. Wakatsuki T, Schwab B, Thompson NC, Elson EL. 2001. Effects of cytochalasin D and latrunculin B on mechanical properties of cells. Journal of Cell Science 114:1025–1036.
64. Woods AS, Ferré S. 2005. Amazing stability of the arginine-phosphate electrostatic interaction. Journal of Proteome Research 4:1397–1402. doi: 10.1021/pr050077s
65. van Genderen HO, Kenis H, Hofstra L, Narula J, Reutelingsperger CP. 2008. Extracellular annexin A5: functions of phosphatidylserine-binding and two-dimensional crystallization. Biochimica Et Biophysica Acta 1783:953–963. doi: 10.1016/j.bbamcr.2008.01.030
66. van den Eijnde SM, van den Hoff MJ, Reutelingsperger CP, van Heerde WL, Henfling ME, Vermeij-Keers C, Schutte B, Borgers M, Ramaekers FC. 2001. Transient expression of phosphatidylserine at cell-cell contact areas is required for myotube formation. Journal of Cell Science 114:3631–3642.