Assembly of macromolecular complexes in bacterial and baculovirus expression systems

Current Opinion in Structural Biology

Volumn 6, Issue 2, 1996, Pages 157-161

  Roy, Polly ^a,b   Jones, Ian ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT PROTEIN;

BACTERIUM; BACULOVIRUS; COMPLEX FORMATION; ESCHERICHIA COLI; EXPRESSION VECTOR; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SHORT SURVEY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; UNIDENTIFIED BACULOVIRUS;

EID: 0029913126     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(96)80069-8     Document Type: Article

References (53)

1. Wynn RM, Davie JR, Cox RP, Chuang DT: Molecular chaperones: heat-shock proteins, foldases, and matchmakers. J Lab Clin Med 1994, 124:31-36.
2. Klikova M, Rhee SS, Hunter E, Ruml T: Efficient in vivo and in vitro assembly of retroviral capsids from Gag precursor proteins expressed in bacteria. J Virol 1995, 69:1093-1098. This paper gives details of the first demonstration of retrovirus Gag assembly in a prokaryote. The particles formed within inclusion bodies but could be isolated by differential centrifugation. They lacked membrane and so were particularly suitable for cryoelectron microscopy.
3. Duronio RJ, Jackson-Machelski E, Heuckeroth RO, Olins PO, Devine CS, Yonemoto W, Slice LW, Taylor SS, Gordon JI: Protein N-myristoylation in Escherichia coli: reconstitution of a eukaryotic protein modification in bacteria. Proc Natl Acad Sci USA 1990, 87:1506-1510.
4. Belyaev AS, Hails RS, Roy P: High-level expression of five foreign genes by a single recombinant baculovirus. Gene 1995, 156:229-233. This paper describes the construction of a novel baculovirus expression vector with the ability to express four different genes at the same time. When this vector was used to create a recombinant virus which already contained one foreign gene, a virus expressing five proteins in the same cell was isolated. Dual infections would allow 10 proteins to be expressed together, although this was not directly demonstrated in this paper.
5. Roy P: Orbivirus structure and assembly. Virology 1996, 215:1-11.
6. Hsu TA, Eiden JJ, Bourgarel P, Meo T, Betenbaugh MJ: Effects of co-expressing chaperone BiP on functional antibody production in the baculovirus system. Protein Expr Purif 1994, 5:595-603. The correct folding of proteins, especially after expression at high level, represents a grey area in the application of expression systems. In this report, chaperonins are co-expressed with antibody heavy chains and shown to be beneficial for the amount of functional protein made. The study suggests that folding pathways may be engineered to maximize the recovery of fully functional product.
7. Fraenkel-Conrat H, Williams RC: Reconstitution of active tobacco mosaic virus from its inactive protein and nucleic acid components. Proc Natl Acad Sci USA 1955, 41:690-698.
8. Popa MP, McKelvey TA, Hempel J, Hendrix RW: Bacteriophage HK97 structure: wholesale covalent cross-linking between the major head shell subunits. J Virol 1991, 65:3227-3237.
9. Duda RL, Martincic K, Hendrix RW: Genetic basis of bacteriophage HK97 prohead assembly. J Mol Biol 1995, 247:636-647. A thorough analysis of the requirements for assembly of the prohead of phage HK97. In contrast to the data in [10•], prohead formation occurs with a single gene product in the absence of a scaffold protein. Co-expression of the viral protease led to maturation of the prohead and provides a model for understanding the interaction of the protease with the prohead substrate.
10. Lee CS, Guo P: Sequential interactions of structural proteins in phage phi 29 procapsid assembly. J Virol 1995, 69:5024-5032. An elegant study demonstrating the assembly of the prohead of the Bacillus subtilis phage phi29 in E. coli. The work concludes that correct prohead assembly is inherent as long as all necessary components are present and that neither the gene order of the expression system used nor the molar ratios of protein is important as long as they reach the threshold level for assembly to occur.
11. Valegård K, Murray JB, Stockley PG, Stonehouse NJ, Liljas L: Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature 1994, 371:623-626.
12. Stockley PG, Stonehouse NJ, Valegård K: Molecular mechanism of RNA phage morphogenesis. Int J Biochem 1994, 26:1249-1260.
13. Mastico RA, Talbot SJ, Stockley PG: Multiple presentation of foreign peptides on the surface of an RNA-free spherical bacteriophage capsid. J Gen Virol 1993, 74:541-548.
14. Hwang DJ, Roberts IM, Wilson TM: Expression of tobacco mosaic virus coat protein and assembly of pseudovirus particles in Escherichia coli. Proc Natl Acad Sci USA 1994, 91:9067-9071.
15. Lewis SA, Morgan DO, Grubman MJ: Expression, processing, and assembly of foot-and-mouth disease virus capsid structures in heterologous systems: induction of a neutralizing antibody response in guinea pigs. J Virol 1991, 65:6572-6580.
16. Bernstein HB, Tucker SP, Kar SR, McPherson SA, McPherson DT, Dubay JW, Lebowitz J, Compans RW, Hunter E: Oligomerization of the hydrophobic heptad repeat of gp41. J Virol 1995, 69:2745-2750. Eukaryotic glycoproteins are seldom well expressed in E. coli but the use of fragments here demonstrates that inherent properties of self assembly can be visualized in E. coli. The rapid analysis of mutants that is possible in E. coli allows an analysis of the residues involved in the oligomerization.
17. Lessard IA, Perham RN: Expression in Escherichia coli of genes encoding the E1 alpha and E1 beta subunits of the pyruvate dehydrogenase complex of Bacillus stearothermophilus and assembly of a functional E1 component (alpha 2 beta 2) in vitro. J Biol Chem 1994, 269:10378-10383.
18. Davie JR, Wynn RM, Cox RP, Chuang DT: Expression and assembly of a functional E1 component (alpha 2 beta 2) of mammalian branched-chain alpha-ketoacid dehydrogenase complex in Escherichia coli. J Biol Chem 1992, 267:16601-16606.
19. Overton HA, Fujii Y, Price I, Jones IM: The protease and Gag gene products of the human immunodeficiency virus: authentic cleavage and post-translational modification in an insect cell expression system. Virology 1989, 170:107-116.
20. Gheysen D, Jacobs E, De-Foresta F, Thiriart C, Francotte M, Thines D, De-Wilde M: Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells. Cell 1989, 59:103-112.
21. Delchambre M, Gheysen D, Thines D, Thiriart C, Jacobs E, Verdin E, Horth M, Burny A, Bex F: The Gag precursor of simian immunodeficiency virus assembles into virus like particles. EMBO J 1989, 8:2653-2660.
22. Morikawa S, Booth TF, Bishop DH: Analyses of the requirements for the synthesis of virus-like particles by feline immunodeficiency virus Gag using baculovirus vectors. Virology 1991, 183:288-297.
23. Rasmussen L, Battles JK, Ennis WH, Nagashima K, Gonda MA: Characterization of virus-like particles produced by a recombinant baculovirus containing the Gag gene of the bovine immunodeficiency-like virus. Virology 1990, 178:435-451.
24. Sommerfelt MA, Roberts CR, Hunter E: Expression of simian type D retroviral (Mason-Pfizer monkey virus) capsids in insect cells using recombinant baculovirus. Virology 1993, 192:298-306.
25. Thomsen DR, Meyer AL, Post LE: Expression of feline leukaemia virus gp85 and Gag proteins and assembly into virus-like particles using the baculovirus expression vector system. J Gen Virol 1992, 73:1819-1824.
26. Chazal N, Gay B, Carriere C, Tournier J, Boulanger P: Human immunodeficiency virus type 1 MA deletion mutants expressed in baculovirus-infected cells: cis and trans effects on the Gag precursor assembly pathway. J Virol 1995, 69:365-375. This paper describes the use of the baculovirus system to map the sites of assembly of the HIV Gag protein into virus-like particles. It also includes an analysis of trans-dominant negative phenotypes which prevent assembly of the wild-type molecule by formation of hetero-oligomeric VLP.
27. Morikawa Y, Kishi T, Zhang W-H, Nermut MV, Hockley DJ, Jones IM: A molecular determinant of HIV particle assembly located in the matrix antigen p17. J Virol 1995, 69:4519-4523. This paper constitutes the first analysis of HIV Gag VLPs that includes an interpretation of mutational data in the knowledge of protein structure and shows the clustering of mutations that affect assembly into a single α helix.
28. Chazal N, Carriere C, Gay B, Boulanger P: Phenotypic characterization of insertion mutants of the human immunodeficiency virus type 1 Gag precursor expressed in recombinant baculovirus-infected cells. J Virol 1994, 68:111-122.
29. Carriere C, Gay B, Chazal N, Morin N, Boulanger P: Sequence requirements for encapsidation of deletion mutants and chimeras of human immunodeficiency virus type 1 Gag precursor into retrovirus-like particles. J Virol 1995, 69:2366-2377.
30. Nermut MV, Hockley DJ, Jowett JBM, Jones IM, Garreau M, Thomas D: Fullerene-like organisation of HIV Gag-protein shell in virus-like particles produced by recombinant baculoviruses. Virology 1994, 198:288-296.
31. Prasad BV, Rothnagel R, Jiang X, Estes MK: Three-dimensional structure of baculovirus-expressed Norwalk virus capsids. J Virol 1994, 68:5117-5125. The authors provide an excellent demonstration of the possibilities of combining baculovirus expression of virus capsid protein with the high-resolution observational power of cryoelectron microscopy.
32. Zeng CQ, Labbe M, Cohen J, Prasad BV, Chen D, Ramig RF, Estes MK: Characterization of rotavirus VP2 particles. Virology 1994, 201:55-65.
33. Montross L, Watkins S, Moreland RB, Mamon H, Caspar DL, Garcea RL: Nuclear assembly of polyomavirus capsids in insect cells expressing the major capsid protein VP1. J Virol 1991, 65:4991-4998.
34. Schneemann A, Dasgupta R, Johnson JE, Rueckert RR: Use of recombinant baculoviruses in synthesis of morphologically distinct viruslike particles of flock house virus, a nodavirus. J Virol 1993, 67:2756-2763.
35. Fisher AJ, McKinney BR, Schneemann A, Rueckert RR, Johnson JE: Crystallization of viruslike particles assembled from flock house virus coat protein expressed in a baculovirus system. J Virol 1993, 67:2950-2953.
36. Rose RC, Bonnez W, Reichman RC, Garcea RL: Expression of human papillomavirus type 11 L1 protein in insect cells: in vivo and in vitro assembly of viruslike particles. J Virol 1993, 67:1936-1944.
37. Kirnbauer R, Taub J, Greenstone H, Roden R, Durst M, Gissmann L, Lowy DR, Schiller JT: Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles. J Virol 1993, 67:6929-6936.
38. Volpers C, Schirmacher P, Streeck RE, Sapp M: Assembly of the major and the minor capsid protein of human papillomavirus type 33 into virus-like particles and tubular structures in insect cells. Virology 1994, 200:504-512.
39. French TJ, Roy P: Synthesis of bluetongue virus (BTV) corelike particles by a recombinant baculovirus expressing the two major structural core proteins of BTV. J Virol 1990, 64:1530-1536.
40. Prasad BV, Yamaguchi S, Roy P: Three-dimensional structure of single-shelled bluetongue virus. J Virol 1992, 66:2135-2142.
41. French TJ, Marshall JJ, Roy P: Assembly of double-shelled, viruslike particles of bluetongue virus by the simultaneous expression of four structural proteins. J Virol 1990, 64:5695-5700.
42. Hewat EA, Booth TF, Roy P: Structure of correctly self-assembled bluetongue virus-like particles. J Struct Biol 1994, 112:183-191.
43. Loudon PT, Roy P: Assembly of five bluetongue virus proteins expressed by recombinant baculoviruses: inclusion of the largest protein VP1 in the core and virus-like proteins. Virology 1991, 180:798-802.
44. Belyaev AS, Roy P: Presentation of hepatitis B virus preS2 epitope on bluetongue virus core-like particles. Virology 1992, 190:840-844.
45. Roy P, Urakawa T, Van-Dijk AA, Erasmus BJ: Recombinant virus vaccine for bluetongue disease in sheep. J Virol 1990, 64:1998-2003.
46. Takehara K, Ireland D, Bishop DH: Co-expression of the hepatitis B surface and core antigens using baculovirus multiple expression vectors. J Gen Virol 1988, 69:2763-2777.
47. Prehaud C, Nel K, Bishop DH: Baculovirus-expressed rabies virus M1 protein is not phosphorylated: it forms multiple complexes with expressed rabies N protein. Virology 1992, 189:766-770.
48. Thomsen DR, Roof LL, Homa FL: Assembly of herpes simplex virus (HSV) intermediate capsids in insect cells infected with recombinant baculoviruses expressing HSV capsid proteins. J Virol 1994, 68:2442-2457.
49. Thomsen DR, Newcomb WW, Brown JC, Homa FL: Assembly of the herpes simplex virus capsid: requirement for the carboxyl-terminal twenty-five amino acids of the proteins encoded by the UL26 and UL26.5 genes. J Virol 1995, 69:3690-3703. An excellent example of the use of the system described in [48] to dissect stages of the process, including the role of post-translational modifications.
50. Brautigam S, Snezhkov E, Bishop DH: Formation of poliovirus-like particles by recombinant baculoviruses expressing the individual VP0, VP3, and VP1 proteins by comparison to particles derived from the expressed poliovirus polyprotein. Virology 1993, 192:512-524.
51. Godeau F, Casanova JL, Luescher IF, Fairchild KD, Delarbre C, Saucier C, Gachelin G, Kourilsky P: Binding of low concentration of peptide to H-2Kd produced in insect cells requires mouse beta 2-microglobulin co-expression. Int Immunol 1992, 4:265-275.
52. DeTomaso AW, Xie ZJ, Liu G, Mercer RW: Expression, targeting, and assembly of functional Na,K-ATPase polypeptides in baculovirus-infected insect cells. J Biol Chem 1993, 268:1470-1478.
53. Atkinson AE, Bermudez I, Darlison MG, Barnard EA, Earley FG, Possee RD, Beadle DJ, King LA: Assembly of functional GABAA receptors in insect cells using baculovirus expression vectors. Neuroreport 1992, 3:597-600.