Improved expression of secretory and trimeric proteins in mammalian cells via the introduction of a new trimer motif and a mutant of the tPA signal sequence

Akey DL, Malashkevich VN, Kim PS (2001) Buried polar residues in coiled-coil interfaces. Biochemistry 40(21):6352–6360 Alekseeva E, Sominskaya I, Skrastina D, Egorova I, Starodubova E, Kushners E, Mihailova M, Petrakova N, Bruvere R, Kozlovskaya T, Isaguliants M, Pumpens P (2009) Enhancement of the expression of HCV core gene does not enhance core-specific immune response in DNA immunization: advantages of the heterologous DNA prime, protein boost immunization regimen. Genet Vaccines Ther 7:7 Andrews DW, Young JC, Mirels LF, Czarnota GJ (1992) The role of the N region in signal sequence and signal-anchor function. J Biol Chem 267(11):7761–7769 Araujo NM, Vianna CO, Moraes MT, Gomes SA (2009) Expression of Hepatitis B virus surface antigen (HBsAg) from genotypes A, D and F and influence of amino acid variations related or not to genotypes on HBsAg detection. Braz J Infect Dis 13(4):266–271 Beddows S, Franti M, Dey AK, Kirschner M, Iyer SP, Fisch DC, Ketas T, Yuste E, Desrosiers RC, Klasse PJ, Maddon PJ, Olson WC, Moore JP (2007) A comparative immunogenicity study in rabbits of disulfide-stabilized, proteolytically cleaved, soluble trimeric human immunodeficiency virus type 1 gp140, trimeric cleavage-defective gp140 and monomeric gp120. Virology 360(2):329–340 Beddows S, Schulke N, Kirschner M, Barnes K, Franti M, Michael E, Ketas T, Sanders RW, Maddon PJ, Olson WC, Moore JP (2005) Evaluating the immunogenicity of a disulfide-stabilized, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J Virol 79(14):8812–8827 Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340(4):783–795 Bhardwaj A, Walker-Kopp N, Wilkens S, Cingolani G (2008) Foldon-guided self-assembly of ultra-stable protein fibers. Protein Sci 17(9):1475–1485 Chapman BS, Thayer RM, Vincent KA, Haigwood NL (1991) Effect of intron A from human cytomegalovirus (Towne) immediate-early gene on heterologous expression in mammalian cells. Nucleic Acids Res 19(14):3979–3986 Coleman J, Inukai M, Inouye M (1985) Dual functions of the signal peptide in protein transfer across the membrane. Cell 43(1):351–360 Cornelissen LA, de Vries RP, de Boer-Luijtze EA, Rigter A, Rottier PJ, de Haan CA (2010) A single immunization with soluble recombinant trimeric hemagglutinin protects chickens against highly pathogenic avian influenza virus H5N1. PLoS ONE 5(5):e10645 Costa SM, Paes MV, Barreto DF, Pinhao AT, Barth OM, Queiroz JL, Armoa GR, Freire MS, Alves AM (2006) Protection against dengue type 2 virus induced in mice immunized with a DNA plasmid encoding the non-structural 1 (NS1) gene fused to the tissue plasminogen activator signal sequence. Vaccine 24(2):195–205 Delorenzi M, Speed T (2002) An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18(4):617–625 Deml L, Bojak A, Steck S, Graf M, Wild J, Schirmbeck R, Wolf H, Wagner R (2001) Multiple effects of codon usage optimization on expression and immunogenicity of DNA candidate vaccines encoding the human immunodeficiency virus type 1 Gag protein. J Virol 75(22):10991–11001 Derby NR, Kraft Z, Kan E, Crooks ET, Barnett SW, Srivastava IK, Binley JM, Stamatatos L (2006) Antibody responses elicited in macaques immunized with human immunodeficiency virus type 1 (HIV-1) SF162-derived gp140 envelope immunogens: comparison with those elicited during homologous simian/human immunodeficiency virus SHIVSF162P4 and heterologous HIV-1 infection. J Virol 80(17):8745–8762 Du C, Wang M, Liu J, Pan M, Cai Y, Yao J (2008) Improvement of thermostability of recombinant collagen-like protein by incorporating a foldon sequence. Appl Microbiol Biotechnol 79(2):195–202 Eckert DM, Malashkevich VN, Kim PS (1998) Crystal structure of GCN4-pIQI, a trimeric coiled coil with buried polar residues. J Mol Biol 284(4):859–865 Forsell MN, Schief WR, Wyatt RT (2009) Immunogenicity of HIV-1 envelope glycoprotein oligomers. Curr Opin HIV AIDS 4(5):380–387 Garmory HS, Brown KA, Titball RW (2003) DNA vaccines: improving expression of antigens. Genet Vaccines Ther 1(1):2 Golden JW, Josleyn MD, Hooper JW (2008) Targeting the vaccinia virus L1 protein to the cell surface enhances production of neutralizing antibodies. Vaccine 26(27–28):3507–3515 Gonzalez L Jr, Woolfson DN, Alber T (1996) Buried polar residues and structural specificity in the GCN4 leucine zipper. Nat Struct Biol 3(12):1011–1018 Gratkowski H, Lear JD, DeGrado WF (2001) Polar side chains drive the association of model transmembrane peptides. Proc Natl Acad Sci USA 98(3):880–885 Haas J, Park EC, Seed B (1996) Codon usage limitation in the expression of HIV-1 envelope glycoprotein. Curr Biol 6(3):315–324 Harbury PB, Zhang T, Kim PS, Alber T (1993) A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262(5138):1401–1407 Hattori T, Sagawa K, Matsushita S, Koito A, Suto H, Matsuoka M, Yokoyama M, Takatsuki K (1987) Characterization of three monoclonal antibodies (VAK3-5) that identify p24, core protein of human immunodeficiency virus, and its precursors. Jpn J Cancer Res 78(3):235–241 Hernandez Alvarez B, Hartmann MD, Albrecht R, Lupas AN, Zeth K, Linke D (2008) A new expression system for protein crystallization using trimeric coiled-coil adaptors. Protein Eng Des Sel 21(1):11–18 Jalah R, Rosati M, Kulkarni V, Patel V, Bergamaschi C, Valentin A, Zhang GM, Sidhu MK, Eldridge JH, Weiner DB, Pavlakis GN, Felber BK (2007) Efficient systemic expression of bioactive IL-15 in mice upon delivery of optimized DNA expression plasmids. DNA Cell Biol 26(12):827–840 Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292(2):195–202 Kaur M, Rai A, Bhatnagar R (2009) Rabies DNA vaccine: no impact of MHC class I and class II targeting sequences on immune response and protection against lethal challenge. Vaccine 27(15):2128–2137 Kim M, Qiao ZS, Montefiori DC, Haynes BF, Reinherz EL, Liao HX (2005) Comparison of HIV Type 1 ADA gp120 monomers versus gp140 trimers as immunogens for the induction of neutralizing antibodies. AIDS Res Hum Retroviruses 21(1):58–67 Knappenberger JA, Smith JE, Thorpe SH, Zitzewitz JA, Matthews CR (2002) A buried polar residue in the hydrophobic interface of the coiled-coil peptide, GCN4-p1, plays a thermodynamic, not a kinetic role in folding. J Mol Biol 321(1):1–6 Kutzler MA, Weiner DB (2008) DNA vaccines: ready for prime time? Nat Rev Genet 9(10):776–788 Kwong PD, Wyatt R, Sattentau QJ, Sodroski J, Hendrickson WA (2000) Oligomeric modeling and electrostatic analysis of the gp120 envelope glycoprotein of human immunodeficiency virus. J Virol 74(4):1961–1972 Li Z, Howard A, Kelley C, Delogu G, Collins F, Morris S (1999) Immunogenicity of DNA vaccines expressing tuberculosis proteins fused to tissue plasminogen activator signal sequences. Infect Immun 67(9):4780–4786 Liu Y, Xu Y, Lou Z, Zhu J, Hu X, Gao GF, Qiu B, Rao Z, Tien P (2006) Structural characterization of mumps virus fusion protein core. Biochem Biophys Res Commun 348(3):916–922 Luo M, Tao P, Li J, Zhou S, Guo D, Pan Z (2008) Immunization with plasmid DNA encoding influenza A virus nucleoprotein fused to a tissue plasminogen activator signal sequence elicits strong immune responses and protection against H5N1 challenge in mice. J Virol Methods 154(1–2):121–127 Mason JM, Arndt KM (2004) Coiled coil domains: stability, specificity, and biological implications. Chembiochem 5(2):170–176 McGuffin LJ, Bryson K, Jones DT (2000) The PSIPRED protein structure prediction server. Bioinformatics 16(4):404–405 Midha S, Bhatnagar R (2009) Anthrax protective antigen administered by DNA vaccination to distinct subcellular locations potentiates humoral and cellular immune responses. Eur J Immunol 39(1):159–177 Navaratnarajah CK, Leonard VH, Cattaneo R (2009) Measles virus glycoprotein complex assembly, receptor attachment, and cell entry. Curr Top Microbiol Immunol 329:59–76 Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int J Neural Syst 8(5–6):581–599 Papanikolopoulou K, Forge V, Goeltz P, Mitraki A (2004) Formation of highly stable chimeric trimers by fusion of an adenovirus fiber shaft fragment with the foldon domain of bacteriophage t4 fibritin. J Biol Chem 279(10):8991–8998 Pfeffer SR, Rothman JE (1987) Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu Rev Biochem 56:829–852 Qiu JT, Liu B, Tian C, Pavlakis GN, Yu XF (2000) Enhancement of primary and secondary cellular immune responses against human immunodeficiency virus type 1 gag by using DNA expression vectors that target Gag antigen to the secretory pathway. J Virol 74(13):5997–6005 Qiu JT, Song R, Dettenhofer M, Tian C, August T, Felber BK, Pavlakis GN, Yu XF (1999) Evaluation of novel human immunodeficiency virus type 1 Gag DNA vaccines for protein expression in mammalian cells and induction of immune responses. J Virol 73(11):9145–9152 Sammalkorpi M, Lazaridis T (2007) Configuration of influenza hemagglutinin fusion peptide monomers and oligomers in membranes. Biochim Biophys Acta 1768(1):30–38 Schulke N, Vesanen MS, Sanders RW, Zhu P, Lu M, Anselma DJ, Villa AR, Parren PW, Binley JM, Roux KH, Maddon PJ, Moore JP, Olson WC (2002) Oligomeric and conformational properties of a proteolytically mature, disulfide-stabilized human immunodeficiency virus type 1 gp140 envelope glycoprotein. J Virol 76(15):7760–7776 Seo SH, Jin HT, Park SH, Youn JI, Sung YC (2009) Optimal induction of HPV DNA vaccine-induced CD8+ T cell responses and therapeutic antitumor effect by antigen engineering and electroporation. Vaccine 27(42):5906–5912 von Heijne G (1983) Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem 133(1):17–21 Wagschal K, Tripet B, Lavigne P, Mant C, Hodges RS (1999) The role of position a in determining the stability and oligomerization state of alpha-helical coiled coils: 20 amino acid stability coefficients in the hydrophobic core of proteins. Protein Sci 8(11):2312–2329 Wang S, Farfan-Arribas DJ, Shen S, Chou TH, Hirsch A, He F, Lu S (2006) Relative contributions of codon usage, promoter efficiency and leader sequence to the antigen expression and immunogenicity of HIV-1 Env DNA vaccine. Vaccine 24(21):4531–4540 Wei CJ, Xu L, Kong WP, Shi W, Canis K, Stevens J, Yang ZY, Dell A, Haslam SM, Wilson IA, Nabel GJ (2008) Comparative efficacy of neutralizing antibodies elicited by recombinant hemagglutinin proteins from avian H5N1 influenza virus. J Virol 82(13):6200–6208 Woolfson DN (2005) The design of coiled-coil structures and assemblies. Adv Protein Chem 70:79–112 Yan Z, Holmes KV, Hodges RS (2009) Expression and characterization of recombinant S2 subunit of SARS-coronavirus S fusion protein. Adv Exp Med Biol 611:153–154 Yang X, Farzan M, Wyatt R, Sodroski J (2000a) Characterization of stable, soluble trimers containing complete ectodomains of human immunodeficiency virus type 1 envelope glycoproteins. J Virol 74(12):5716–5725 Yang X, Florin L, Farzan M, Kolchinsky P, Kwong PD, Sodroski J, Wyatt R (2000b) Modifications that stabilize human immunodeficiency virus envelope glycoprotein trimers in solution. J Virol 74(10):4746–4754 Yang X, Lee J, Mahony EM, Kwong PD, Wyatt R, Sodroski J (2002) Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J Virol 76(9):4634–4642 Yang X, Wyatt R, Sodroski J (2001) Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers. J Virol 75(3):1165–1171 Zhang W, Zhou HZ, Wang KL, Cheng DC, Zhang FM, Ling H (2007) Analyzing of the genetic characteristics of HIV-1 CHLJBF06044 envelope. J Harbin Med Univ 41(6):537–540 Zhou HZ, Li Y, Zhou H, Liu YC, Du HT, Wang KL, Wang FX, Ling H (2008) A new CRF01_AE/B recombinant structure of HIV type 1 found in Heilongjiang province, China. AIDS 22(13):1690–1693 zur Megede J, Chen MC, Doe B, Schaefer M, Greer CE, Selby M, Otten GR, Barnett SW (2000) Increased expression and immunogenicity of sequence-modified human immunodeficiency virus type 1 gag gene. J Virol 74(6):2628–2635