Efficient orthogonal integration of the bacteriophage φ29 DNAportal connector protein in engineered lipid bilayers

ACS Synthetic Biology

Volumn 1, Issue 9, 2012, Pages 414-424

  Moleiro, Lara H ^a   López Montero, Iván ^a   Márquez, Ileana ^b   Moreno, Sonia ^c   Vélez, Marisela ^b,d   Carrascosa, José L ^c,d   Monroy, Francisco ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b INSTITUTO DE CATÁLISIS Y PETROLEOQUÍMICA   (Spain)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^d INSTITUTO MADRILEÑO DE ESTUDIOS AVANZADOS EN NANOCIENCIA IMDEA NANOCIENCIA   (Spain)

Author keywords

Bacteriophage phi29; DNA translocation; Giant vesicles; Lipid membranes; Membrane pore; Membrane reconstitution

Indexed keywords

CELL PROTEIN; DNA PORTAL CONNECTOR PROTEIN; LIPID; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; BACTERIOPHAGE; CELL VACUOLE; CHANNEL GATING; CHEMICAL STRUCTURE; CONTROLLED STUDY; EFFICIENT ORTHOGONAL INTEGRATION; GENE DELIVERY SYSTEM; GENE TRANSLOCATION; HYDROPHILICITY; LIPID BILAYER; LIPID MEMBRANE; LIPID VESICLE; MEMBRANE BIOLOGY; NANOENGINEERING; NANOTECHNOLOGY; NUCLEAR PORE; ORTHOGONAL ROTATION; PRIORITY JOURNAL; PROTEIN ENGINEERING; SURFACE PROPERTY; TUNING CURVE;

CAPSID PROTEINS; DNA, VIRAL; GENE TRANSFER TECHNIQUES; LIPID BILAYERS; MEMBRANE PROTEINS; NANOTECHNOLOGY; TRANSLOCATION, GENETIC; VIRAL PROTEINS;

BACILLUS PHAGE PHI29;

EID: 84868252763     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/sb3000063     Document Type: Article

References (45)

1. Bustamante, C., Bryant, Z., and Smith, S. B. (2003) Ten years of tension: Single-molecule DNA mechanics. Nature 421 (6921), 423-427. (Pubitemid 36157948)
2. Smith, D. E., Tans, S. J., Smith, S. B., Grimes, S., Anderson, D. L., and Bustamante, C. (2001) The bacteriophage [phis]29 portal motor can package DNA against a large internal force. Nature 413 (6857), 748-752. (Pubitemid 33009954)
3. Sun, S., Rao, V. B., and Rossmann, M. G. (2010) Genome packaging in viruses. Curr. Opin. Struct. Biol. 20 (1), 114-120.
4. Carrascosa, J. L. (1986) Electron Microscopy of Proteins, Vol. 5, p 37-70, Academic Press, New York.
5. Johnson, J. E. (2010) Virus particle maturation: Insights into elegantly programmed nanomachines. Curr. Opin. Struct. Biol. 20 (2), 210-216.
6. Steven, A. C., Heymann, J. B., Cheng, N., Trus, B. L., and Conway, J. F. (2005) Virus maturation: Dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Curr. Opin. Struct. Biol. 15 (2), 227-236.
7. Valpuesta, J. M., and Carrascosa, J. L. (1994) Structure of viral connectors and their function in bacteriophage assembly and DNA packaging. Q. Rev. Biophys. 27 (02), 107-155. (Pubitemid 24246113)
8. Cuervo, A.; Carrascosa, J. L., Viral connectors for DNA encapsulation. Curr. Opin. Biotechnol. 2011, (0).
9. Wikoff, W. R., and Johnson, J. E. (1999) Virus assembly: Imaging a molecular machine. Curr. Biol. 9 (8), R296-R300. (Pubitemid 29205779)
10. Agirrezabala, X., Martin-Benito, J., Caston, J. R., Miranda, R., Valpuesta, J. M., and Carrascosa, J. L. (2005) Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J. 24 (21), 3820-3829. (Pubitemid 41581697)
11. Valpuesta, J. L. C. a. J. M. (1999) Bacteriophage connectors: Structural features of a DNA translocating motor. Recent Res. Dev. Virol. 1, 449-465.
12. Johnson, J. E., and Chiu, W. (2007) DNA packaging and delivery machines in tailed bacteriophages. Curr. Opin. Struct. Biol. 17 (2), 237-243. (Pubitemid 46575256)
13. Orlova, E. V., Gowen, B., Droge, A., Stiege, A., Weise, F., Lurz, R., van Heel, M., and Tavares, P. (2003) Structure of a viral DNA gatekeeper at 10 A resolution by cryo-electron microscopy. EMBO J. 22 (6), 1255-1262. (Pubitemid 36362689)
14. Newcomb, W. W., Juhas, R. M., Thomsen, D. R., Homa, F. L., Burch, A. D., Weller, S. K., and Brown, J. C. (2001) The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J. Virol. 75 (22), 10923-32. (Pubitemid 33031559)
15. Trus, B. L., Cheng, N., Newcomb, W. W., Homa, F. L., Brown, J. C., and Steven, A. C. (2004) Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J. Virol. 78 (22), 12668-71. (Pubitemid 39458785)
16. Chang, J., Weigele, P., King, J., Chiu, W., and Jiang, W. (2006) Cryo-EM asymmetric reconstruction of bacteriophage p22 reveals organization of its dna packaging and infecting machinery. Structure 14 (6), 1073-1082. (Pubitemid 43831665)
17. Jiang, W., Chang, J., Jakana, J., Weigele, P., King, J., and Chiu, W. (2006) Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439 (7076), 612-616. (Pubitemid 43185387)
18. Wendell, D., Jing, P., Geng, J., Subramaniam, V., Lee, T. J., Montemagno, C., and Guo, P. (2009) Translocation of doublestranded DNA through membrane-adapted phi29 motor protein nanopores. Nat. Nano 4 (11), 765-772.
19. Jing, P., Haque, F., Vonderheide, A. P., Montemagno, C., and Guo, P. (2010) Robust properties of membrane-embedded connector channel of bacterial virus phi29 DNA packaging motor. Mol. BioSyst. 6 (10), 1844-1852.
20. Jing, P., Haque, F., Shu, D., Montemagno, C., and Guo, P. (2010) One-way traffic of a viral motor channel for double-stranded DNA translocation. Nano Lett. 10 (9), 3620-3627.
21. Geng, J., Fang, H., Haque, F., Zhang, L., and Guo, P. (2011) Three reversible and controllable discrete steps of channel gating of a viral DNA packaging motor. Biomaterials 32 (32), 8234-8242.
22. Fang, H., Jing, P., Haque, F., and Guo, P. (2012) Role of channel lysines and the "push through a one-way valve" mechanism of the viral DNA packaging motor. Biophys. J. 102 (1), 127-135.
23. Guasch, A., Pous, J., Ibarra, B., Gomis-Rüth, F. X., Valpuesta, J. M., Sousa, N., Carrascosa, J. L., and Coll, M. (2002) Detailed architecture of a DNA translocating machine: The high-resolution structure of the bacteriophage [phi]29 connector particle. J. Mol. Biol. 315 (4), 663-676. (Pubitemid 34729317)
24. Valpuesta, J. M., Fernandez, J. J., Carazo, J. M., and Carrascosa, J. L. (1999) The three-dimensional structure of a DNA translocating machine at 10 Å resolution. Structure 7 (3), 289-296. (Pubitemid 29159688)
25. Ibanez, C., Garcia, J. A., Carrascosa, J. L., and Salas, M. (1984) Overproduction and purification of the connector protein of Bacillus subtilis phage phi 29. Nucleic Acids Res. 12 (5), 2351-2365.
26. Davies, S. S., Pontsler, A. V., Marathe, G. K., Harrison, K. A., Murphy, R. C., Hinshaw, J. C., Prestwich, G. D., Hilaire, A. S., Prescott, S. M., Zimmerman, G. A., and McIntyre, T. M. (2001) Oxidized alkyl phospholipids are specific, high affinity peroxisome proliferatoractivated receptor gamma ligands and agonists. J. Biol. Chem. 276, 16015-16023.
27. Fruhwirth, G. O., Loidl, A., and Hermetter, A. (2007) Oxidized phospholipids: From molecular properties to disease. Biochim. Biophys. Acta 1772, 718-736. (Pubitemid 46891216)
28. Mattila, J. P., and Kinnunen PK, S. K. (2008) Oxidized phospholipids as potential molecular targets for antimicrobial peptides. Biochim. Biophys. Acta 1778 (10), 2041-50.
29. Khandelia, H., and Mouritsen, O. G. (2009) Lipid gymnastics: Evidence of complete acyl chain reversal in oxidized phospholipids from molecular simulations. Biophys. J. 96 (7), 2734-2743.
30. Karlsson, O., Rytömaa, M., Dahlqvist, A., Kinnunen, P. K. J.,, A° ., and Wieslander (1996) Correlation between bilayer lipid dynamics and activity of the diglucosyldiacylglycerol synthase from Acholeplasma laidlawii membranes. Biochemistry 35, 10094-10102. (Pubitemid 26269925)
31. Prenner, E., Sommer, A., Maurer, N., Glatter, O., Gorges, R., Paltauf, F., and Hermetter, A. (2000) Lateral microheterogeneity of diphenylhexatriene- labeled choline phospholipids in the erythrocyte ghost membrane as determined by time-resolved fluorescence spectroscopy. J. Membr. Biol. 174, 237-243. (Pubitemid 30202431)
32. Sabatini, K., Mattila, J.-P., Megli, F. M., and Kinnunen, P. K. J. (2006) Characterization of two oxidatively modified phospholipids in mixed monolayers with DPPC. Biophys. J. 90, 4488-4499. (Pubitemid 43830894)
33. Boal, D. H. (2005) Mechanics of the Cell, 3rd ed., p xiv, Cambridge University Press, New York.
34. Phillips, R., Ursell, T., Wiggins, P., and Sens, P. (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459 (7245), 379-385.
35. Nagle, J. F., and Tristam-Nagle, S. (2000) Structure of lipid bilayers. Biochim. Biophys. Acta 1469, 159-195.
36. Z. V. Leonenko, E. F., Ma, H., Dahms, T. E. S., and Cramb, D. T. (2004) Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopy. Biophys. J. 86, 3783-3793. (Pubitemid 38780255)
37. Richter, R., Mukhopadhyay, A., and Brisson, A. (2003) Pathways of lipid vesicle deposition on solid surfaces: A combined QCM-D and AFM study. Biophys. J. 85 (5), 3035-3047. (Pubitemid 37345791)
38. Moreno-Herrero, F., de Pablo, P. J., Fernandez-Sanchez, R., Colchero, J., Gomez-Herrero, J., and Baro, A. M. (2002) Scanning force microscopy jumping and tapping modes in liquids. Appl. Phys. Lett. 81 (14), 2620-2622.
39. Horcas, I., Fernandez, R., Gomez-Rodriguez, J. M., Colchero, J., Gomez-Herrero, J., and Baro, A. M. (2007) WSXM: A software for scanning probe microscopy and a tool for nanotechnology. Rev. Sci. Instrum. 78 (1), 013705-8.
40. Alberts, B. (2002) Cell Biology Interactive, 4th ed., Garland Science, New York.
41. Tamba, Y., Ohba, S., Kubota, M., Yoshioka, H., Yoshioka, H., and Yamazaki, M. (2007) Single GUV method reveals interaction of tea catechin ()-epigallocatechin gallate with lipid membranes. Biophys. J. 92 (9), 3178-3194. (Pubitemid 46684578)
42. Betz, W. J., Mao, F., and Smith, C. B. (1996) Imaging exocytosis and endocytosis. Curr. Opin. Neurobiol. 6, 365-371. (Pubitemid 26235686)
43. Abramoff, M. D., Magalhaes, P. J., and Ram, S. J. (2004) Image processing with ImageJ. Biophotonics Int. 11 (7), 36-42.
44. Brian, A. A., and McConnell, H. M (1984) Allogeneic stimulation of cytotoxic T cells by supported planar membranes. Proc. Natl. Acad. Sci. U.S.A. 81, 6159-6163. (Pubitemid 15220799)
45. Lopez-Montero, I., Arriaga, L. R., Monroy, F., Rivas, G., Tarazona, P., and Velez, M. (2008) High fluidity and soft elasticity of the inner membrane of Escherichia coli revealed by the surface rheology of model langmuir monolayers. Langmuir 24 (8), 4065-4076. (Pubitemid 351569012)