Osmolyte-mediated encapsulation of proteins inside MS2 viral capsids

ACS Nano

Volumn 6, Issue 10, 2012, Pages 8658-8664

  Glasgow, Jeff E ^a   Capehart, Stacy L ^a   Francis, Matthew B ^a   Tullman Ercek, Danielle ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

compartmentalization; encapsulation; enzyme catalysis; nanoscience; virus

Indexed keywords

ALKALINE PHOSPHATASE; AMINO ACID PEPTIDES; BACTERIOPHAGE MS2; COAT PROTEINS; COMPARTMENTALIZATION; COMPLEX EFFECTS; DNA OLIGOMERS; EFFECT OF ENCAPSULATION; ENCAPSULATED ENZYME; ENCAPSULATION OF PROTEINS; ENZYMATIC ACTIVITIES; ENZYME CATALYSIS; FREE ENZYME; HIGH YIELD; IN-VITRO; IN-VIVO; MINIMAL EFFECTS; OSMOLYTES; PEPTIDE TAGS; QUANTITATIVE DATA; REASSEMBLY; VIRAL CAPSIDS;

AMINO ACIDS; ENCAPSULATION; ENZYME KINETICS; NANOSCIENCE; OLIGOMERS; PEPTIDES; PHOSPHATASES; VIRUSES;

MOLECULES;

NANOCAPSULE; PROTEIN;

ARTICLE; CHEMISTRY; COLIPHAGE; CONFORMATION; MACROMOLECULE; MATERIALS TESTING; OSMOLARITY; SURFACE PROPERTY; ULTRASTRUCTURE; VIRUS CAPSID;

CAPSID; LEVIVIRUS; MACROMOLECULAR SUBSTANCES; MATERIALS TESTING; MOLECULAR CONFORMATION; NANOCAPSULES; OSMOLAR CONCENTRATION; PROTEINS; SURFACE PROPERTIES;

EID: 84867817800     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn302183h     Document Type: Article

References (48)

1. Kim, K. T.; Meeuwissen, S. A.; Nolte, R. J. M.; van Hest, J. C. M. Smart Nanocontainers and Nanoreactors Nanoscale 2010, 2, 844-858
2. Vriezema, D.; Comellas-Aragonès, M.; Elemans, J.; Cornelissen, J. J. L. M.; Rowan, A. E.; Nolte, R. J. M. Self-Assembled Nanoreactors Chem. Rev. 2005, 105, 1445-1490
3. Huang, X.; Holden, H. M.; Raushel, F. M. Channeling of Substrates and Intermediates in Enzyme-Catalyzed Reactions Annu. Rev. Biochem. 2001, 70, 149-180 (Pubitemid 32662208)
4. Yeates, T.; Kerfeld, C.; Heinhorst, S.; Cannon, G.; Shively, J. Protein-Based Organelles in Bacteria: Carboxysomes and Related Microcompartments Nat. Rev. 2008, 6, 681-691
5. Kinney, J. N.; Axen, S. D.; Kerfeld, C. A. Comparative Analysis of Carboxysome Shell Proteins Photosynth. Res. 2011, 109, 21-32
6. de la Escosura, A.; Nolte, R. J. M.; Cornelissen, J. J. L. M. Viruses and Protein Cages as Nanocontainers and Nanoreactors J. Mat. Chem. 2009, 19, 2274-2278
7. Conrado, R. J.; Varner, J. D.; DeLisa, M. P. Engineering the Spatial Organization of Metabolic Enzymes: Mimicking Nature's Synergy Curr. Opin. Biotechnol. 2008, 19, 492-499
8. Aniagyei, S. E.; DuFort, C.; Kao, C. C.; Dragnea, B. Self-Assembly Approaches to Nanomaterial Encapsulation in Viral Protein Cages J. Mater. Chem. 2008, 18, 3763-3774
9. Conrado, R. J.; Mansell, T. J.; Varner, J. D.; DeLisa, M. P. Stochastic Reaction-Diffusion Simulation of Enzyme Compartmentalization Reveals Improved Catalytic Efficiency for a Synthetic Metabolic Pathway Metab. Eng. 2007, 9, 355-363 (Pubitemid 47102687)
10. Renggli, K.; Baumann, P.; Langowska, K.; Onaca, O.; Bruns, N.; Meier, W. Selective and Responsive Nanoreactors Adv. Func. Mater. 2011, 21, 1241-1259
11. Comellas-Aragonès, M.; Engelkamp, H.; Claessen, V. I.; Sommerdijk, N. A. J. M.; Rowan, A. E.; Christianen, P. C. M.; Maan, J. C.; Verduin, B. J. M.; Cornelissen, J. J. L. M.; Nolte, R. J. M. A Virus-Based Single-Enzyme Nanoreactor Nat. Nanotechnol. 2007, 2, 635-639 (Pubitemid 47527123)
12. Minten, I. J.; Wilke, K. D. M.; Hendriks, L. J. A.; van Hest, J. C. M.; Nolte, R. J. M.; Cornelissen, J. J. L. M. Metal-Ion-Induced Formation and Stabilization of Protein Cages Based on the Cowpea Chlorotic Mottle Virus Small 2011, 7, 911-919
13. Minten, I. J.; Claessen, V. I.; Blank, K.; Rowan, A. E.; Nolte, R. J. M.; Cornelissen, J. J. L. M. Catalytic Capsids: The Art of Confinement Chem. Sci. 2011, 2, 358-362
14. Lee, K. W.; Tan, W. S. Recombinant Hepatitis B Virus Core Particles: Association, Dissociation and Encapsidation of Green Fluorescent Protein J. Virol. Meth. 2008, 151, 172-180
15. O'Neil, A.; Reichhardt, C.; Johnson, B.; Prevelige, P.; Douglas, T. Genetically Programmed in Vivo Packaging of Protein Cargo and Its Controlled Release from Bacteriophage P22 Angew. Chem., Int. Ed. 2011, 50, 7425-7428
16. Patterson, D. P.; Prevelige, P. E.; Douglas, T. Nanoreactors by Programmed Enzyme Encapsulation Inside the Capsid of the Bacteriophage P22 ACS Nano 2012, 6, 5000-5009
17. Inoue, T.; Kawano, M.; Takahashi, R.; Tsukamoto, H.; Enomoto, T.; Imai, T.; Kataoka, K.; Handa, H. Engineering of SV40-Based Nano-capsules for Delivery of Heterologous Proteins As Fusions with the Minor Capsid Proteins VP2/3 J. Biotechnol. 2008, 134, 181-192
18. Fiedler, J. D.; Brown, S. D.; Lau, J. L.; Finn, M. G. RNA-Directed Packaging of Enzymes within Virus-Like Particles Angew. Chem., Int. Ed. 2010, 49, 9648-9651
19. Wörsdörfer, B.; Woycechowsky, K. J.; Hilvert, D. Directed Evolution of a Protein Container Science 2011, 331, 589-592
20. Wörsdörfer, B.; Pianowski, Z.; Hilvert, D. Efficient in Vitro Encapsulation of Protein Cargo by an Engineered Protein Container J. Am. Chem. Soc. 2012, 3, 9-11
21. Wu, W.; Hsiao, S. C.; Carrico, Z. M.; Francis, M. B. Genome-Free Viral Capsids as Multivalent Carriers for Taxol Delivery Angew. Chem., Int. Ed. 2009, 48, 9493-9497
22. Stephanopoulos, N.; Carrico, Z. Nanoscale Integration of Sensitizing Chromophores and Porphyrins with Bacteriophage MS2 Angew. Chem., Int. Ed. 2009, 9498-9502
23. Stephanopoulos, N.; Tong, G. J.; Hsiao, S. C.; Francis, M. B. Dual-Surface Modified Virus Capsids for Targeted Delivery of Photodynamic Agents to Cancer Cells ACS Nano 2010, 4, 6014-6020
24. Anderson, E. A.; Isaacman, S.; Peabody, D. S.; Wang, E. Y.; Canary, J. W.; Kirshenbaum, K. Viral Nanoparticles Donning a Paramagnetic Coat: Conjugation of MRI Contrast Agents to the MS2 Capsid Nano Lett. 2006, 6, 1160-1164 (Pubitemid 44013476)
25. Meldrum, T.; Seim, K. L.; Bajaj, V. S.; Palaniappan, K. K.; Wu, W.; Francis, M. B.; Wemmer, D. E.; Pines, A. A Xenon-Based Molecular Sensor Assembled on an MS2 Viral Capsid Scaffold J. Am. Chem. Soc. 2010, 132, 5936-5937
26. Garimella, P. D.; Datta, A.; Romanini, D. W.; Raymond, K. N.; Francis, M. B. Multivalent, High-Relaxivity MRI Contrast Agents Using Rigid Cysteine-Reactive Gadolinium Complexes J. Am. Chem. Soc. 2011, 133, 14704-14709
27. Wu, M.; Brown, W.; Stockley, P. Cell-Specific Delivery of Bacteriophage-Encapsidated Ricin A Chain Bioconjugate Chem. 1995, 587-595
28. Ashley, C. E.; Carnes, E. C.; Phillips, G. K.; Durfee, P. N.; Buley, M. D.; Lino, C. A.; Padilla, D. P.; Phillips, B.; Carter, M. B.; Willman, C. L. et al. Cell-Specific Delivery of Diverse Cargos by Bacteriophage MS2 Virus-Like Particles ACS Nano 2011, 5, 5729-5745
29. Stonehouse, N.; Stockley, P. Effects of Amino Acid Substitution on the Thermal Stability of MS2 Capsids Lacking Genomic RNA FEBS Lett. 1993, 334, 355-359 (Pubitemid 23341748)
30. Beckett, D.; Uhlenbeck, O. C. Ribonucleoprotein Complexes of R17 Coat Protein and a Translational Operator Analog J. Mol. Biol. 1988, 204, 927-938 (Pubitemid 19050660)
31. Kumar, R. Role of Naturally Occurring Osmolytes in Protein Folding and Stability Arch. Biochem. Biophys. 2009, 491, 1-6
32. Bolen, D. W. Effects of Naturally Occurring Osmolytes on Protein Stability and Solubility: Issues Important in Protein Crystallization Methods 2004, 34, 312-322 (Pubitemid 39119815)
33. Yancey, P. H.; Clark, M. E.; Hand, S. C.; Bowlus, R. D.; Somero, G. N. Living With Water Stress: Evolution of Osmolyte Systems Science 1982, 217, 1214-1222 (Pubitemid 13283134)
34. Wang, A.; Bolen, D. A Naturally Occurring Protective System in Urea-Rich Cells: Mechanism of Osmolyte Protection of Proteins Against Urea Denaturation Biochemistry 1997, 36, 9101-9108 (Pubitemid 27329494)
35. Street, T. O.; Bolen, D. W.; Rose, G. D. A Molecular Mechanism for Osmolyte-Induced Protein Stability Proc. Nat. Acad. Sci. 2006, 103, 13997-14002 (Pubitemid 44488414)
36. Zhang, Y.; Cremer, P. S. Chemistry of Hofmeister Anions and Osmolytes Annu. Rev. Phys. Chem. 2010, 61, 63-83
37. ElSawy, K.; Caves, L.; Twarock, R. The Impact of Viral RNA on the Association Rates of Capsid Protein Assembly: Bacteriophage MS2 as a Case Study J. Mol. Biol. 2010, 400, 935-947
38. Rolfsson, O.; Toropova, K.; Ranson, N. A; Stockley, P. G. Mutually-Induced Conformational Switching of RNA and Coat Protein Underpins Efficient Assembly of a Viral Capsid J. Mol. Biol. 2010, 401, 309-322
39. Valegård, K.; Murray, J. B.; Stockley, P. G.; Stonehouse, N. J.; Liljas, L. Crystal Structure of an RNA Phage Coat Protein-Operator Complex Nature 1994, 371, 623-626 (Pubitemid 24315746)
40. Douglas, T.; Young, M. Host-Guest Encapsulation of Materials by AssembledVirus Protein Cages Nature 1998, 393, 1996-1999
41. Hu, Y.; Zandi, R.; Anavitarte, A.; Knobler, C. M.; Gelbart, W. M. Packaging of a Polymer by a Viral Capsid: The Interplay Between Polymer Length and Capsid Size Biophys. J. 2008, 94, 1428-1436
42. Hohn, T. Role of RNA in the Assembly Process of Bacteriophage fr J. Mol. Biol. 1969, 43, 191-200
43. Zacharias, D. A.; Violin, J. D.; Newton, A. C.; Tsien, R. Y. Partitioning of Lipid-Modified Monomeric GFPs Into Membrane Microdomains of Live Cells Science 2002, 296, 913-916 (Pubitemid 34464897)
44. Hooker, J. M.; Esser-Kahn, A. P.; Francis, M. B. Modification of Aniline Containing Proteins Using an Oxidative Coupling Strategy J. Am. Chem. Soc. 2006, 128, 15558-15559 (Pubitemid 44894074)
45. Karamyshev, A. L.; Karamysheva, Z. N.; Kajava, A. V.; Ksenzenko, V. N.; Nesmeyanova, M. A. Processing of Escherichia coli Alkaline Phosphatase: Role of the Primary Structure of the Signal Peptide Cleavage Region J. Mol. Biol. 1998, 277, 859-870 (Pubitemid 28195986)
46. Simopoulos, T. T.; Jencks, W. P. Alkaline Phosphatase is an Almost Perfect Enzyme Biochemistry 1994, 33, 10375-10380 (Pubitemid 24281803)
47. Peters, R.; Louzao, I.; van Hest, J. C. M. From Polymeric Nanoreactors to Artificial Organelles Chem. Sci. 2011, 3, 335-342
48. Jesorka, A.; Orwar, O. Liposomes: Technologies and Analytical Applications Ann. Rev. Anal. Chem. 2008, 1, 801-832