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References

  1. Jorgensen KD. 1987. Comparison of the pharmacological properties of pituitary and biosynthetic human growth hormone. Demonstration of antinatriuretic/antidiuretic and barbital sleep effects of human growth hormone in rats. Acta Endocrinol. (Copenh.) 114: 124-131.
  2. Hindmarsh PC, Brook CG. 1987. Effect of growth hormone on short normal children. Br. Med. J. (Clin. Res. Ed.) 295: 573-577.
    CrossRef
  3. Hsiung HM, Cantrell A, Luirink J, Oudega B, Veros AJ, Becker GW. 1989. Use of bacteriocin release protein in E. coli for excretion of human growth hormone into the culture medium. Nat. Biotechnol. 7: 267-271.
    CrossRef
  4. Becker GW, Hsiung HM. 1986. Expression, secretion and folding of human growth hormone in Escherichia coli. Purification and characterization. FEBS Lett. 204: 145-150.
    CrossRef
  5. Mukhija R, Rupa P, Pillai D, Garg LC. 1995. High-level production and one-step purification of biologically active human growth hormone in Escherichia coli. Gene 165: 303-306.
    CrossRef
  6. Ghorpade A, Garg LC. 1993. Efficient processing and export of human growth hormone by heat labile enterotoxin chain B signal sequence. FEBS Lett. 330: 61-65.
    CrossRef
  7. Massa G, Vanderschueren-Lodeweyckx M, Bouillon R. 1993. Five-year follow-up of growth hormone antibodies in growth hormone deficient children treated with recombinant human growth hormone. Clin. Endocrinol. (Oxf.) 38: 137-142.
    CrossRef
  8. Ahangari G, Ostadali MR, Rabani A, Rashidian J, Sanati MH, Zarindast MR. 2004. Growth hormone antibodies formation in patients treated with recombinant human growth hormone. Int. J. Immunopathol. Pharmacol. 17: 33-38.
    Pubmed CrossRef
  9. Kipriyanov SM, Moldenhauer G, Little M. 1997. High level production of soluble single chain antibodies in small-scale Escherichia coli cultures. J. Immunol. Methods 200: 69-77.
    CrossRef
  10. Makrides SC. 1996. Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol. Rev. 60: 512-538.
    Pubmed PMC
  11. Nakazawa K, Takano T, Sohma A, Yamane K. 1986. Secretion activities of Bacillus subtilis alpha-amylase signal peptides of different lengths in Escherichia coli cells. Biochem. Biophys. Res. Commun. 134: 624-631.
    CrossRef
  12. Nakamura K, Fujita Y, Itoh Y, Yamane K. 1989. Modification of length, hydrophobic properties and electric charge of Bacillus subtilis alpha-amylase signal peptide and their different effects on the production of secretory proteins in B. subtilis and Escherichia coli cells. Mol. Gen. Genet. 216: 1-9.
    Pubmed CrossRef
  13. Suominen I, Meyer P, Tilgmann C, Glumoff T, Glumoff V, Kapyla J, et al. 1995. Effects of signal peptide mutations on processing of Bacillus stearothermophilus alpha-amylase in Escherichia coli. Microbiology 141: 649-654.
    Pubmed CrossRef
  14. Kiany J, Zomorodipour A, Ahmadzadeh Raji M, Sanati MH. 2003. Construction of recombinant plasmids for periplasmic expression of human growth hormone in Escherichia coli under T7 and lac promoters. J. Sci. Islam. Repub. 14: 311-316.
  15. Ghasemi F, Zomorodipour A, Shojai S, Ataei F, Khodabandeh M, Sanati MH. 2004. Using L-arabinose for production of human growth hormone in Escherichia coli, studying the processing of gIII:: hGH precursor. Iran. J. Biotechnol. 2: 250-260.
  16. Chung BH, Sohn M-J, Oh S-W, Park U-S, Poo H, Kim BS, et al. 1998. Overproduction of human granulocyte-colony stimulating factor fused to the pelB signal peptide in Escherichia coli. J. Ferment. Bioeng. 85: 443-446.
    CrossRef
  17. Sockolosky JT, Szoka FC. 2013. Periplasmic production via the pET expression system of soluble, bioactive human growth hormone. Protein Expr. Purif. 87: 129-135.
    Pubmed PMC CrossRef
  18. Berges H, Joseph-Liauzun E, Fayet O. 1996. Combined effects of the signal sequence and the major chaperone proteins on the export of human cytokines in Escherichia coli. Appl. Environ. Microbiol. 62: 55-60.
    Pubmed PMC
  19. Le Calvez H, Green JM, Baty D. 1996. Increased efficiency of alkaline phosphatase production levels in Escherichia coli using a degenerate PelB signal sequence. Gene 170: 51-55.
    CrossRef
  20. Denefle P, Kovarik S, Ciora T, Gosselet N, Benichou JC, Latta M, et al. 1989. Heterologous protein export in Escherichia coli: influence of bacterial signal peptides on the export of human interleukin 1 beta. Gene 85: 499-510.
    CrossRef
  21. Cheah KC, Harrison S, King R, Crocker L, Wells JR, Robins A. 1994. Secretion of eukaryotic growth hormones in Escherichia coli is influenced by the sequence of the mature proteins. Gene 138: 9-15.
    CrossRef
  22. Jana S, Deb JK. 2005. Strategies for efficient production of heterologous proteins in Escherichia coli. Appl. Microbiol. Biotechnol. 67: 289-298.
    Pubmed CrossRef
  23. Kane JF. 1995. Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol. 6: 494-500.
    CrossRef
  24. Zhang W, Xiao W, Wei H, Zhang J, Tian Z. 2006. mRNA secondary structure at start AUG codon is a key limiting factor for human protein expression in Escherichia coli. Biochem. Biophys. Res. Commun. 349: 69-78.
    Pubmed CrossRef
  25. Duffaud G, Inouye M. 1988. Signal peptidases recognize a structural feature at the cleavage site of secretory proteins. J. Biol. Chem. 263: 10224-10228.
    Pubmed
  26. Shahhoseini M, Ziaee AA, Ghaemi N. 2003. Expression and secretion of an alpha-amylase gene from a native strain of Bacillus licheniformis in Escherichia coli by T7 promoter and putative signal peptide of the gene. J. Appl. Microbiol. 95: 1250-1254.
    Pubmed CrossRef
  27. Nilsson I, von Heijne G. 1991. A de novo designed signal peptide cleavage cassette functions in vivo. J. Biol. Chem. 266: 3408-3410.
    Pubmed
  28. Karamyshev AL, Karamysheva ZN, Kajava AV, Ksenzenko VN, Nesmeyanova MA. 1998. Processing of Escherichia coli alkaline phosphatase: role of the primary structure of the signal peptide cleavage region. J. Mol. Biol. 277: 859-870.
    Pubmed CrossRef
  29. Das S, Paul S, Chatterjee S, Dutta C. 2005. Codon and amino acid usage in two major human pathogens of genus Bartonella - optimization between replicational-transcriptional selection, translational control and cost minimization. DNA Res. 12: 91-102.
    Pubmed CrossRef
  30. Ramachandiran V, Kramer G, Hardesty B. 2000. Expression of different coding sequences in cell-free bacterial and eukaryotic systems indicates translational pausing on Escherichia coli ribosomes. FEBS Lett. 482: 185-188.
    CrossRef
  31. McNulty DE, Claffee BA, Huddleston MJ, Porter ML, Cavnar KM, Kane JF. 2003. Mistranslational errors associated with the rare arginine codon CGG in Escherichia coli. Protein Expr. Purif. 27: 365-374.
    CrossRef
  32. Mattanovich D, Kramer W, Luttich C, Weik R, Bayer K, Katinger H. 1998. Rational design of an improved induction scheme for recombinant Escherichia coli. Biotechnol. Bioeng. 58: 296-298.
    CrossRef
  33. Marston FA. 1986. The purification of eukaryotic polypeptides synthesized in Escherichia coli. Biochem. J. 240: 1-12.
    Pubmed PMC CrossRef
  34. Hoang TT, Ma Y, Stern RJ, McNeil MR, Schweizer HP. 1999. Construction and use of low-copy number T7 expression vectors for purification of problem proteins: purification of Mycobacterium tuberculosis RmlD and Pseudomonas aeruginosa LasI and RhlI proteins, and functional analysis of purified RhlI. Gene 237: 361-371.
    CrossRef
  35. Neubauer P, Hofmann K, Holst O, Mattiasson B, Kruschke P. 1992. Maximizing the expression of a recombinant gene in Escherichia coli by manipulation of induction time using lactose as inducer. Appl. Microbiol. Biotechnol. 36: 739-744.
    Pubmed CrossRef
  36. Gombert AK, Kilikian BV. 1998. Recombinant gene expression in Escherichia coli cultivation using lactose as inducer. J. Biotechnol. 60: 47-54.
    CrossRef
  37. Curless CE, Pope J, Loredo L, Tsai LB. 1994. Effect of preinduction specific growth rate on secretion of granulocyte macrophage colony stimulating factor by Escherichia coli. Biotechnol. Prog. 10: 467-471.
    Pubmed CrossRef
  38. Driessen AJ, Fekkes P, van der Wolk JP. 1998. The Sec system. Curr. Opin. Microbiol. 1: 216-222.
    CrossRef
  39. Martoglio B, Dobberstein B. 1998. Signal sequences: more than just greasy peptides. Trends Cell Biol. 8: 410-415.
    CrossRef
  40. Klinkert B, Elles I, Nickelsen J. 2006. Translation of chloroplast psbD mRNA in Chlamydomonas is controlled by a secondary RNA structure blocking the AUG start codon. Nucleic Acids Res. 34: 386-394.
    Pubmed PMC CrossRef
  41. Pandey JP, Gorla P, Manavathi B, Siddavattam D. 2009. mRNA secondary structure modulates the translation of organophosphate hydrolase (OPH) in E. coli. Mol. Biol. Rep. 36: 449-454.
    Pubmed CrossRef
  42. Paulus M, Haslbeck M, Watzele M. 2004. RNA stem-loop enhanced expression of previously non-expressible genes. Nucleic Acids Res. 32: e78.
    Pubmed PMC CrossRef
  43. Chang JT, Green CB, Wolf RE Jr. 1995. Inhibition of translation initiation on Escherichia coli gnd mRNA by formation of a long-range secondary structure involving the ribosome binding site and the internal complementary sequence. J. Bacteriol. 177: 6560-6567.
    Pubmed PMC CrossRef
  44. Brunel C, Romby P, Sacerdot C, de Smit M, Graffe M, Dondon J, et al. 1995. Stabilised secondary structure at a ribosomal binding site enhances translational repression in E. coli. J. Mol. Biol. 253: 277-290.
    Pubmed CrossRef
  45. Ma CK, Kolesnikow T, Rayner JC, Simons EL, Yim H, Simons RW. 1994. Control of translation by mRNA secondary structure: the importance of the kinetics of structure formation. Mol. Microbiol. 14: 1033-1047.
    Pubmed CrossRef
  46. de Smit MH, van Duin J. 1994. Control of translation by mRNA secondary structure in Escherichia coli. A quantitative analysis of literature data. J. Mol. Biol. 244: 144-150.
    Pubmed CrossRef
  47. Nielsen H, Brunak S, von Heijne G. 1999. Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng. 12: 3-9.
    Pubmed CrossRef
  48. Hiller K, Grote A, Scheer M, Munch R, Jahn D. 2004. PrediSi: prediction of signal peptides and their cleavage positions. Nucleic Acids Res. 32: W375-W379.
    Pubmed PMC CrossRef
  49. Claros MG, von Heijne G. 1994. TopPred II: an improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10: 685-686.
    CrossRef
  50. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31: 3406-3415.
    Pubmed PMC CrossRef
  51. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P. 1994. Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 125: 167-188.
    CrossRef
  52. Sambrook J, Russell D. 2001. Molecular Cloning: A Laboratory Manual, 3rd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  53. Libby RT, Braedt G, Kronheim SR, March CJ, Urdal DL, Chiaverotti TA, et al. 1987. Expression and purification of native human granulocyte-macrophage colony-stimulating factor from an Escherichia coli secretion vector. DNA 6: 221-229.
    Pubmed CrossRef
  54. Jeiranikhameneh M, Razavi MR, Irani S, Siadat SD, Oloomi M. 2017. Designing novel construction for cell surface display of protein E on Escherichia coli using non-classical pathway based on Lpp-OmpA. AMB Express 7: 53.
    Pubmed PMC CrossRef
  55. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(11): 1999-2009

Published online November 28, 2017 https://doi.org/10.4014/jmb.1703.03080

Copyright © The Korean Society for Microbiology and Biotechnology.

Designing Signal Peptides for Efficient Periplasmic Expression of Human Growth Hormone in Escherichia coli

Meisam Jeiranikhameneh 1, 2, Farzaneh Moshiri 1, Soheil Keyhan Falasafi 1 and Alireza Zomorodipour 1*

1Department of Molecular Medicine, Institute of Medical Biotechnology, National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran, Iran, 2Department of Biology, School of Basic Science, Sciences and Researches Branch, Islamic Azad University, Tehran, Iran

Received: May 2, 2017; Accepted: August 28, 2017

Abstract

The secretion efficiency of a protein in a Sec-type secretion system is mainly determined by an
N-terminal signal peptide and its combination with its cognate protein. Five signal peptides,
namely, two synthetic Sec-type and three Bacillus licheniformis alpha-amylase-derived signal
peptides, were compared for periplasmic expression of the human growth hormone (hGH) in
E. coli. Based on in silico predictions on the signal peptides’ cleavage efficiencies and their
corresponding mRNA secondary structures, a number of amino acid substitutions and silent
mutations were considered in the modified signal sequences. The two synthetic signal
peptides, specifically designed for hGH secretion in E. coli, differ in their N-terminal positively
charged residues and hydrophobic region lengths. According to the mRNA secondary
structure predictions, combinations of the protein and each of the five signal sequences could
lead to different outcomes, especially when accessibility of the initiator ATG and ribosome
binding sites were considered. In the experimental stage, the two synthetic signal peptides
displayed complete processing and resulted in efficient secretion of the mature hGH in
periplasmic regions, as was demonstrated by protein analysis. The three alpha-amylasederived
signal peptides, however, were processed partially from their precursors. Therefore,
to achieve efficient secretion of a protein in a heterologous system, designing a specific signal
peptide by using a combined approach of optimizations of the mRNA secondary structure and
the signal peptide H-domain and cleavage site is recommended.

Keywords: Signal Peptide, human growth hormone, periplasmic space, Escherichia Coli, alpha-amylase, mRNA secondary structure

References

  1. Jorgensen KD. 1987. Comparison of the pharmacological properties of pituitary and biosynthetic human growth hormone. Demonstration of antinatriuretic/antidiuretic and barbital sleep effects of human growth hormone in rats. Acta Endocrinol. (Copenh.) 114: 124-131.
  2. Hindmarsh PC, Brook CG. 1987. Effect of growth hormone on short normal children. Br. Med. J. (Clin. Res. Ed.) 295: 573-577.
    CrossRef
  3. Hsiung HM, Cantrell A, Luirink J, Oudega B, Veros AJ, Becker GW. 1989. Use of bacteriocin release protein in E. coli for excretion of human growth hormone into the culture medium. Nat. Biotechnol. 7: 267-271.
    CrossRef
  4. Becker GW, Hsiung HM. 1986. Expression, secretion and folding of human growth hormone in Escherichia coli. Purification and characterization. FEBS Lett. 204: 145-150.
    CrossRef
  5. Mukhija R, Rupa P, Pillai D, Garg LC. 1995. High-level production and one-step purification of biologically active human growth hormone in Escherichia coli. Gene 165: 303-306.
    CrossRef
  6. Ghorpade A, Garg LC. 1993. Efficient processing and export of human growth hormone by heat labile enterotoxin chain B signal sequence. FEBS Lett. 330: 61-65.
    CrossRef
  7. Massa G, Vanderschueren-Lodeweyckx M, Bouillon R. 1993. Five-year follow-up of growth hormone antibodies in growth hormone deficient children treated with recombinant human growth hormone. Clin. Endocrinol. (Oxf.) 38: 137-142.
    CrossRef
  8. Ahangari G, Ostadali MR, Rabani A, Rashidian J, Sanati MH, Zarindast MR. 2004. Growth hormone antibodies formation in patients treated with recombinant human growth hormone. Int. J. Immunopathol. Pharmacol. 17: 33-38.
    Pubmed CrossRef
  9. Kipriyanov SM, Moldenhauer G, Little M. 1997. High level production of soluble single chain antibodies in small-scale Escherichia coli cultures. J. Immunol. Methods 200: 69-77.
    CrossRef
  10. Makrides SC. 1996. Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol. Rev. 60: 512-538.
    Pubmed KoreaMed
  11. Nakazawa K, Takano T, Sohma A, Yamane K. 1986. Secretion activities of Bacillus subtilis alpha-amylase signal peptides of different lengths in Escherichia coli cells. Biochem. Biophys. Res. Commun. 134: 624-631.
    CrossRef
  12. Nakamura K, Fujita Y, Itoh Y, Yamane K. 1989. Modification of length, hydrophobic properties and electric charge of Bacillus subtilis alpha-amylase signal peptide and their different effects on the production of secretory proteins in B. subtilis and Escherichia coli cells. Mol. Gen. Genet. 216: 1-9.
    Pubmed CrossRef
  13. Suominen I, Meyer P, Tilgmann C, Glumoff T, Glumoff V, Kapyla J, et al. 1995. Effects of signal peptide mutations on processing of Bacillus stearothermophilus alpha-amylase in Escherichia coli. Microbiology 141: 649-654.
    Pubmed CrossRef
  14. Kiany J, Zomorodipour A, Ahmadzadeh Raji M, Sanati MH. 2003. Construction of recombinant plasmids for periplasmic expression of human growth hormone in Escherichia coli under T7 and lac promoters. J. Sci. Islam. Repub. 14: 311-316.
  15. Ghasemi F, Zomorodipour A, Shojai S, Ataei F, Khodabandeh M, Sanati MH. 2004. Using L-arabinose for production of human growth hormone in Escherichia coli, studying the processing of gIII:: hGH precursor. Iran. J. Biotechnol. 2: 250-260.
  16. Chung BH, Sohn M-J, Oh S-W, Park U-S, Poo H, Kim BS, et al. 1998. Overproduction of human granulocyte-colony stimulating factor fused to the pelB signal peptide in Escherichia coli. J. Ferment. Bioeng. 85: 443-446.
    CrossRef
  17. Sockolosky JT, Szoka FC. 2013. Periplasmic production via the pET expression system of soluble, bioactive human growth hormone. Protein Expr. Purif. 87: 129-135.
    Pubmed KoreaMed CrossRef
  18. Berges H, Joseph-Liauzun E, Fayet O. 1996. Combined effects of the signal sequence and the major chaperone proteins on the export of human cytokines in Escherichia coli. Appl. Environ. Microbiol. 62: 55-60.
    Pubmed KoreaMed
  19. Le Calvez H, Green JM, Baty D. 1996. Increased efficiency of alkaline phosphatase production levels in Escherichia coli using a degenerate PelB signal sequence. Gene 170: 51-55.
    CrossRef
  20. Denefle P, Kovarik S, Ciora T, Gosselet N, Benichou JC, Latta M, et al. 1989. Heterologous protein export in Escherichia coli: influence of bacterial signal peptides on the export of human interleukin 1 beta. Gene 85: 499-510.
    CrossRef
  21. Cheah KC, Harrison S, King R, Crocker L, Wells JR, Robins A. 1994. Secretion of eukaryotic growth hormones in Escherichia coli is influenced by the sequence of the mature proteins. Gene 138: 9-15.
    CrossRef
  22. Jana S, Deb JK. 2005. Strategies for efficient production of heterologous proteins in Escherichia coli. Appl. Microbiol. Biotechnol. 67: 289-298.
    Pubmed CrossRef
  23. Kane JF. 1995. Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol. 6: 494-500.
    CrossRef
  24. Zhang W, Xiao W, Wei H, Zhang J, Tian Z. 2006. mRNA secondary structure at start AUG codon is a key limiting factor for human protein expression in Escherichia coli. Biochem. Biophys. Res. Commun. 349: 69-78.
    Pubmed CrossRef
  25. Duffaud G, Inouye M. 1988. Signal peptidases recognize a structural feature at the cleavage site of secretory proteins. J. Biol. Chem. 263: 10224-10228.
    Pubmed
  26. Shahhoseini M, Ziaee AA, Ghaemi N. 2003. Expression and secretion of an alpha-amylase gene from a native strain of Bacillus licheniformis in Escherichia coli by T7 promoter and putative signal peptide of the gene. J. Appl. Microbiol. 95: 1250-1254.
    Pubmed CrossRef
  27. Nilsson I, von Heijne G. 1991. A de novo designed signal peptide cleavage cassette functions in vivo. J. Biol. Chem. 266: 3408-3410.
    Pubmed
  28. Karamyshev AL, Karamysheva ZN, Kajava AV, Ksenzenko VN, Nesmeyanova MA. 1998. Processing of Escherichia coli alkaline phosphatase: role of the primary structure of the signal peptide cleavage region. J. Mol. Biol. 277: 859-870.
    Pubmed CrossRef
  29. Das S, Paul S, Chatterjee S, Dutta C. 2005. Codon and amino acid usage in two major human pathogens of genus Bartonella - optimization between replicational-transcriptional selection, translational control and cost minimization. DNA Res. 12: 91-102.
    Pubmed CrossRef
  30. Ramachandiran V, Kramer G, Hardesty B. 2000. Expression of different coding sequences in cell-free bacterial and eukaryotic systems indicates translational pausing on Escherichia coli ribosomes. FEBS Lett. 482: 185-188.
    CrossRef
  31. McNulty DE, Claffee BA, Huddleston MJ, Porter ML, Cavnar KM, Kane JF. 2003. Mistranslational errors associated with the rare arginine codon CGG in Escherichia coli. Protein Expr. Purif. 27: 365-374.
    CrossRef
  32. Mattanovich D, Kramer W, Luttich C, Weik R, Bayer K, Katinger H. 1998. Rational design of an improved induction scheme for recombinant Escherichia coli. Biotechnol. Bioeng. 58: 296-298.
    CrossRef
  33. Marston FA. 1986. The purification of eukaryotic polypeptides synthesized in Escherichia coli. Biochem. J. 240: 1-12.
    Pubmed KoreaMed CrossRef
  34. Hoang TT, Ma Y, Stern RJ, McNeil MR, Schweizer HP. 1999. Construction and use of low-copy number T7 expression vectors for purification of problem proteins: purification of Mycobacterium tuberculosis RmlD and Pseudomonas aeruginosa LasI and RhlI proteins, and functional analysis of purified RhlI. Gene 237: 361-371.
    CrossRef
  35. Neubauer P, Hofmann K, Holst O, Mattiasson B, Kruschke P. 1992. Maximizing the expression of a recombinant gene in Escherichia coli by manipulation of induction time using lactose as inducer. Appl. Microbiol. Biotechnol. 36: 739-744.
    Pubmed CrossRef
  36. Gombert AK, Kilikian BV. 1998. Recombinant gene expression in Escherichia coli cultivation using lactose as inducer. J. Biotechnol. 60: 47-54.
    CrossRef
  37. Curless CE, Pope J, Loredo L, Tsai LB. 1994. Effect of preinduction specific growth rate on secretion of granulocyte macrophage colony stimulating factor by Escherichia coli. Biotechnol. Prog. 10: 467-471.
    Pubmed CrossRef
  38. Driessen AJ, Fekkes P, van der Wolk JP. 1998. The Sec system. Curr. Opin. Microbiol. 1: 216-222.
    CrossRef
  39. Martoglio B, Dobberstein B. 1998. Signal sequences: more than just greasy peptides. Trends Cell Biol. 8: 410-415.
    CrossRef
  40. Klinkert B, Elles I, Nickelsen J. 2006. Translation of chloroplast psbD mRNA in Chlamydomonas is controlled by a secondary RNA structure blocking the AUG start codon. Nucleic Acids Res. 34: 386-394.
    Pubmed KoreaMed CrossRef
  41. Pandey JP, Gorla P, Manavathi B, Siddavattam D. 2009. mRNA secondary structure modulates the translation of organophosphate hydrolase (OPH) in E. coli. Mol. Biol. Rep. 36: 449-454.
    Pubmed CrossRef
  42. Paulus M, Haslbeck M, Watzele M. 2004. RNA stem-loop enhanced expression of previously non-expressible genes. Nucleic Acids Res. 32: e78.
    Pubmed KoreaMed CrossRef
  43. Chang JT, Green CB, Wolf RE Jr. 1995. Inhibition of translation initiation on Escherichia coli gnd mRNA by formation of a long-range secondary structure involving the ribosome binding site and the internal complementary sequence. J. Bacteriol. 177: 6560-6567.
    Pubmed KoreaMed CrossRef
  44. Brunel C, Romby P, Sacerdot C, de Smit M, Graffe M, Dondon J, et al. 1995. Stabilised secondary structure at a ribosomal binding site enhances translational repression in E. coli. J. Mol. Biol. 253: 277-290.
    Pubmed CrossRef
  45. Ma CK, Kolesnikow T, Rayner JC, Simons EL, Yim H, Simons RW. 1994. Control of translation by mRNA secondary structure: the importance of the kinetics of structure formation. Mol. Microbiol. 14: 1033-1047.
    Pubmed CrossRef
  46. de Smit MH, van Duin J. 1994. Control of translation by mRNA secondary structure in Escherichia coli. A quantitative analysis of literature data. J. Mol. Biol. 244: 144-150.
    Pubmed CrossRef
  47. Nielsen H, Brunak S, von Heijne G. 1999. Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng. 12: 3-9.
    Pubmed CrossRef
  48. Hiller K, Grote A, Scheer M, Munch R, Jahn D. 2004. PrediSi: prediction of signal peptides and their cleavage positions. Nucleic Acids Res. 32: W375-W379.
    Pubmed KoreaMed CrossRef
  49. Claros MG, von Heijne G. 1994. TopPred II: an improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10: 685-686.
    CrossRef
  50. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31: 3406-3415.
    Pubmed KoreaMed CrossRef
  51. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P. 1994. Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 125: 167-188.
    CrossRef
  52. Sambrook J, Russell D. 2001. Molecular Cloning: A Laboratory Manual, 3rd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  53. Libby RT, Braedt G, Kronheim SR, March CJ, Urdal DL, Chiaverotti TA, et al. 1987. Expression and purification of native human granulocyte-macrophage colony-stimulating factor from an Escherichia coli secretion vector. DNA 6: 221-229.
    Pubmed CrossRef
  54. Jeiranikhameneh M, Razavi MR, Irani S, Siadat SD, Oloomi M. 2017. Designing novel construction for cell surface display of protein E on Escherichia coli using non-classical pathway based on Lpp-OmpA. AMB Express 7: 53.
    Pubmed KoreaMed CrossRef
  55. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
    Pubmed CrossRef