An in silico overview on the usefulness of tags and linkers in plant molecular pharming

Authors

  • Abdullah Makhzoum Department of Biology, The University of Western Ontario, London, ON N6A 5B7
  • Shifa Tahir Quaid-i-Azam University, National Center for Bioinformatics
  • Marjorie Elizabeth Osborn Locke Department of Computer Science, The University of Western Ontario, London, ON N6A 5B7
  • Jocelyne Trémouillaux-Guiller University F.Rabelais, Tours
  • Kathleen Hefferon Cornell University, Department of Cell Biology and Genetics

DOI:

https://doi.org/10.14719/pst.2014.1.4.72

Keywords:

plant molecular pharming, ADA, SBA, linkers, tags, protein fusions

Abstract

Plant molecular pharming is a promising concept based on the large-scale production of recombinant proteins encompassing antibodies, vaccines and enzymes for human or veterinary uses and treatments. This new branch of biopharmaceutical industry offers pratcical and safety advantages over other traditional production systems. In higher plants, the complex cellular machinery makes possible synthesis and posttranslational modifications of heterologous protein macromolecules. The limiting obstacle to using this plant system at industrial scale is most often the low yield of the recombinant proteins. To improve this production level, many studies have been focusing on the choice of plant species, tissues, organs and cell suspension cultures or various upstream and downstream constituents in the expression cassettes. Likewise, new engineering technologies in plant molecular pharming have emerged relying on the usefulness of using soybean agglutinin (SBA), hydrophobin, zein and elastin-like peptide tags which are employed to extract and purify recombinant proteins in some host systems and under the control, and as a part, of different expression cassettes. Known to be very useful tools in recombinant proteins linkers separate different domains or units of the heterologous gene and thereby keep the functionality of the protein of interest. Here, we compare computationally one tag SBA as a part of fusion with a pharmaceutical human protein ADA joint directly or by the specific flexible (GGGGS)3 liker. The in silico analysis focuses on the mRNAs stability and fusions of tagged and tagged-linked ADA recombinant proteins.

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References

Abdullah, M. A., Rahmah, A. U., Sinskey, A. J., & Rha, C. K. (2008). Cell engineering and molecular pharming for biopharmaceuticals. The Open Medicinal Chemistry Journal, 2, 49-61. http://dx.doi.org/10.2174/1874104500802010049

Agarwal, P., Garg, V., Gautam, T., Pillai, B., Kanoria, S., & Burma, P. K. (2014). A study on the influence of different promoter and 5'UTR (URM) cassettes from Arabidopsis thaliana on the expression level of the reporter gene beta glucuronidase in tobacco and cotton. Transgenic Research, 23(2), 351-363. http://dx.doi.org/10.1007/s11248-013-9757-9

Alvarez, M. L., Topal, E., Martin, F., & Cardineau, G. A. (2010). Higher accumulation of F1-V fusion recombinant protein in plants after induction of protein body formation. Plant Molecular Biology, 72(1-2), 75-89. http://dx.doi.org/10.1007/s11103-009-9552-4

Amani, J., Mousavi, S. L., Rafati, S., & Salmanian, A. H. (2009). In silico analysis of chimeric espA, eae and tir fragments of Escherichia coli O157:H7 for oral immunogenic applications. Theoretical Biology and Medical Modelling, 6, 28. http://dx.doi.org/10.1186/1742-4682-6-28

Amani, J., Mousavi, S. L., Rafati, S., & Salmanian, A. H. (2011). Immunogenicity of a plant-derived edible chimeric EspA, Intimin and Tir of Escherichia coli O157:H7 in mice. Plant Science, 180(4), 620-627. http://dx.doi.org/10.1016/j.plantsci.2011.01.004

Arai, R., Ueda, H., Kitayama, A., Kamiya, N., & Nagamune, T. (2001). Design of the linkers which effectively separate domains of a bifunctional fusion protein. Protein Engineering, 14(8), 529-532. http://dx.doi.org/10.1093/protein/14.8.529

Arzola, L., Chen, J., Rattanaporn, K., Maclean, J. M., & McDonald, K. A. (2011). Transient co-expression of post-transcriptional gene silencing suppressors for increased in planta expression of a recombinant anthrax receptor fusion protein. International Journal of Molecular Sciences, 12(8), 4975-4990. http://dx.doi.org/10.3390/ijms12084975

Bundo, M., Montesinos, L., Izquierdo, E., Campo, S., Mieulet, D., Guiderdoni, E., ... Coca, M. (2014). Production of cecropin A antimicrobial peptide in rice seed endosperm. BMC Plant Biology, 14(1), 102. http://dx.doi.org/10.1186/1471-2229-14-102

Buyel, J. F., Kaever, T., Buyel, J. J., & Fischer, R. (2013). Predictive models for the accumulation of a fluorescent marker protein in tobacco leaves according to the promoter/5'UTR combination. Biotechnol Bioengineering, 110(2), 471-482. http://dx.doi.org/10.1002/bit.24715

Chen, L., Dempsey, B. R., Gyenis, L., Menassa, R., Brandle, J. E., & Dhaubhadel, S. (2013). Identification of the factors that control synthesis and accumulation of a therapeutic protein, human immune-regulatory interleukin-10, in Arabidopsis thaliana. Plant Biotechnology Journal, 11(5), 546-554. http://dx.doi.org/10.1111/pbi.12042

Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: patterns of nonbonded atomic interactions. Protein Science, 2(9), 1511-1519. http://dx.doi.org/10.1002/pro.5560020916

Colquhoun, A. J., & Mellon, J. K. (2002). Epidermal growth factor receptor and bladder cancer. Postgraduate Medical Journal, 78(924), 584-589. http://dx.doi.org/10.1136/pmj.78.924.584

Conley, A. J., Joensuu, J. J., Jevnikar, A. M., Menassa, R., & Brandle, J. E. (2009). Optimization of elastin-like polypeptide fusions for expression and purification of recombinant proteins in plants. Biotechnology and Bioengineering, 103(3), 562-573. http://dx.doi.org/10.1002/bit.22278

Conley, A. J., Joensuu, J. J., Richman, A., & Menassa, R. (2011). Protein body-inducing fusions for high-level production and purification of recombinant proteins in plants. Plant Biotechnol Journal, 9(4), 419-433. http://dx.doi.org/10.1111/j.1467-7652.2011.00596.x

Crasto, C. J., & Feng, J. A. (2000). LINKER: a program to generate linker sequences for fusion proteins. Protein Engineering, 13(5), 309-312. http://dx.doi.org/10.1093/protein/13.5.309

Del, L. Y. M., Farran, I., Becher, M. L., Sander, V., Sanchez, V. R., Martin, V., ... Clemente, M. (2012). A chloroplast-derived Toxoplasma gondii GRA4 antigen used as an oral vaccine protects against toxoplasmosis in mice. Plant Biotechnol Journal, 10(9), 1136-1144. http://dx.doi.org/10.1111/pbi.12001

Floss, D. M., Sack, M., Arcalis, E., Stadlmann, J., Quendler, H., Rademacher, T., ... Conrad, U. (2009). Influence of elastin-like peptide fusions on the quantity and quality of a tobacco-derived human immunodeficiency virus-neutralizing antibody. Plant Biotechnol Journal, 7(9), 899-913. http://dx.doi.org/10.1111/j.1467-7652.2009.00452.x

Friedman, M., Orlova, A., Johansson, E., Eriksson, T. L., Hoiden-Guthenberg, I., Tolmachev, V., ... Stahl, S. (2008). Directed evolution to low nanomolar affinity of a tumor-targeting epidermal growth factor receptor-binding affibody molecule. Journal of Molecular Biology, 376(5), 1388-1402. http://dx.doi.org/10.1016/j.jmb.2007.12.060

Fu, K., Cheng, Q., Liu, Z., Chen, Z., Wang, Y., Ruan, H., ... Yang, D. (2014). Immunotoxicity assessment of rice-derived recombinant human serum albumin using human peripheral blood mononuclear cells. PLoS One, 9(8), e104426. http://dx.doi.org/10.1371/journal.pone.0104426

Gallie, D. R. (2002). The 5'-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Research, 30(15), 3401-3411. http://dx.doi.org/10.1093/nar/gkf457

Gasteiger, E., Hoogland, C., Gattiker, A., Wilkins, M. R., Appel, R. D., & Bairoch, A. (2005 ). Protein identification and analysis tools on the ExPASy server. In The proteomics protocols handbook (pp. 571-607). Humana Press. http://dx.doi.org/10.1385/1-59259-890-0:571

Geourjon, C., & Deleage, G. (1995). SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Computational Applied Bioscience, 11(6), 681-684.

Gostring, L., Chew, M. T., Orlova, A., Hoiden-Guthenberg, I., Wennborg, A., Carlsson, J., & Frejd, F. Y. (2010). Quantification of internalization of EGFR-binding Affibody molecules: Methodological aspects. International Journal of Oncology, 36(4), 757-763. http://dx.doi.org/10.3892/ijo_00000551

Grunberg, R., Ferrar, T. S., van der Sloot, A. M., Constante, M., & Serrano, L. (2010). Building blocks for protein interaction devices. Nucleic Acids Research, 38(8), 2645-2662. http://dx.doi.org/10.1093/nar/gkq152

Guo, J. Q., Li, Q. M., Zhou, J. Y., Zhang, G. P., Yang, Y. Y., Xing, G. X., ... Zhang, C. Y. (2006). Efficient recovery of the functional IP10-scFv fusion protein from inclusion bodies with an on-column refolding system. Protein Expression and Purification, 45(1), 168-174. http://dx.doi.org/10.1016/j.pep.2005.05.016

Hakkinen, S. T., Raven, N., Henquet, M., Laukkanen, M. L., Anderlei, T., Pitkanen, J. P., ... Ritala, A. (2013). Molecular farming in tobacco hairy roots by triggering the secretion of a pharmaceutical antibody. Biotechnology and Bioengineering, 111(2), 336–346. http://dx.doi.org/10.1002/bit.25113

He, Y., Ning, T., Xie, T., Qiu, Q., Zhang, L., Sun, Y., ... Yang, D. (2011). Large-scale production of functional human serum albumin from transgenic rice seeds. Proceedings of the National Academy of Sciences USA, 108(47), 19078-19083. http://dx.doi.org/10.1073/pnas.1109736108

Hefferon, K. (2014). Plant virus expression vector development: new perspectives. Biomedical Research International, 2014, 785382. http://dx.doi.org/10.1155/2014/785382

Hefferon, K. L. (2012). Plant virus expression vectors set the stage as production platforms for biopharmaceutical proteins. Virology, 433(1), 1-6. http://dx.doi.org/10.1016/j.virol.2012.06.012

Hefferon, K. L. (2014). Broadly neutralizing antibodies and the promise of universal vaccines: where are we now? Immunotherapy, 6(1), 51-57. http://dx.doi.org/10.2217/imt.13.150

Hirsch, F. R., Varella-Garcia, M., Bunn, P. A., Jr., Di Maria, M. V., Veve, R., Bremmes, R. M., ... Franklin, W. A. (2003). Epidermal growth factor receptor in non-small-cell lung carcinomas: correlation between gene copy number and protein expression and impact on prognosis. Journal of Clinical Oncology, 21(20), 3798-3807. http://dx.doi.org/10.1200/jco.2003.11.069

Hefferon, K. L. (2012). Plant virus expression vectors set the stage as production platforms for biopharmaceutical proteins. Virology, 433(1), 1-6. http://dx.doi.org/10.1016/j.virol.2012.06.012

Hirsch, F. R., Varella-Garcia, M., Bunn, P. A., Jr., Di Maria, M. V., Veve, R., Bremmes, R. M., ... Franklin, W. A. (2003). Epidermal growth factor receptor in non-small-cell lung carcinomas: correlation between gene copy number and protein expression and impact on prognosis. Journal of Clinical Oncology, 21(20), 3798-3807. http://dx.doi.org/10.1200/jco.2003.11.069

Hu, C. D., Chinenov, Y., & Kerppola, T. K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Molecular Cell, 9(4), 789-798. http://dx.doi.org/10.1016/S1097-2765(02)00496-3

Hu, C. D., & Kerppola, T. K. (2003). Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nature Biotechnology, 21(5), 539-545. http://dx.doi.org/10.1038/nbt816

Jiang, Z., & Zhou, Y. (2005). Using bioinformatics for drug target identification from the genome. American Journal of Pharmacogenomics, 5(6), 387-396. http://dx.doi.org/10.2165/00129785-200505060-00005

Joensuu, J. J., Conley, A. J., Lienemann, M., Brandle, J. E., Linder, M. B., & Menassa, R. (2010). Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana benthamiana. Plant Physiology, 152(2), 622-633. http://dx.doi.org/10.1104/pp.109.149021

Joensuu, J. J., Conley, A. J., Linder, M. B., & Menassa, R. (2012). Bioseparation of recombinant proteins from plant extract with hydrophobin fusion technology. Methods in Molecular Biology, 824, 527-534. http://dx.doi.org/10.1007/978-1-61779-433-9_28

Jung, S. K., & McDonald, K. (2011). Visual gene developer: a fully programmable bioinformatics software for synthetic gene optimization. BMC Bioinformatics, 12, 340. http://dx.doi.org/10.1186/1471-2105-12-340

Kamphausen, S., Holtge, N., Wirsching, F., Morys-Wortmann, C., Riester, D., Goetz, R., ... Schwienhorst, A. (2002). Genetic algorithm for the design of molecules with desired properties. Journal of Computer-Aided Molecular Design, 16(8-9), 551-567. http://dx.doi.org/10.1023/A:1021928016359

Kanoria, S., & Burma, P. K. (2012). A 28 nt long synthetic 5'UTR (synJ) as an enhancer of transgene expression in dicotyledonous plants. BMC Biotechnology, 12, 85. http://dx.doi.org/10.1186/1472-6750-12-85

Kapust, R. B., & Waugh, D. S. (2000). Controlled intracellular processing of fusion proteins by TEV protease. Protein Expression and Purification, 19(2), 312-318. http://dx.doi.org/10.1006/prep.2000.1251

Kerppola, T. K. (2006). Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nature Protocols, 1(3), 1278-1286. http://dx.doi.org/10.1038/nprot.2006.201

Kingsbury, N. J., & McDonald, K. A. (2014). Quantitative Evaluation of E1 Endoglucanase Recovery from Tobacco Leaves Using the Vacuum Infiltration-Centrifugation Method. BioMedical Research International, 2014, 10. http://dx.doi.org/10.1155/2014/483596

Kuo, Y. C., Tan, C. C., Ku, J. T., Hsu, W. C., Su, S. C., Lu, C. A., & Huang, L. F. (2013). Improving Pharmaceutical Protein Production in Oryza sativa. International Journal of Molecular Science, 14(5), 8719-8739. http://dx.doi.org/10.3390/ijms14058719

Laguia-Becher, M., Martin, V., Kraemer, M., Corigliano, M., Yacono, M. L., Goldman, A., & Clemente, M. (2010). Effect of codon optimization and subcellular targeting on Toxoplasma gondii antigen SAG1 expression in tobacco leaves to use in subcutaneous and oral immunization in mice. BMC Biotechnol,ogy 10, 52. http://dx.doi.org/10.1186/1472-6750-10-52

Laskowski, R. A., Watson, J. D., & Thornton, J. M. (2005). ProFunc: a server for predicting protein function from 3D structure. Nucleic Acids Research, 33(Web Server issue), W89-93. http://dx.doi.org/10.1093/nar/gki414

Le Gall, F., Reusch, U., Little, M., & Kipriyanov, S. M. (2004). Effect of linker sequences between the antibody variable domains on the formation, stability and biological activity of a bispecific tandem diabody. Protein Engineering, Design and Selection, 17(4), 357-366. http://dx.doi.org/10.1093/protein/gzh039

Ma, J. K., Christou, P., Chikwamba, R., Haydon, H., Paul, M., Ferrer, M. P., ... Thangaraj, H. (2013). Realising the value of plant molecular pharming to benefit the poor in developing countries and emerging economies. Plant Biotechnology Journal, 11(9), 1029-1033. http://dx.doi.org/10.1111/pbi.12127

Makhzoum, A., Benyammi, R., Moustafa, K., & Tremouillaux-Guiller, J. (2013). Recent advances on host plants and expression cassettes' structure and function in plant molecular pharming. BioDrugs, 28, 145-159 http://dx.doi.org/10.1007/s40259-013-0062-1

Makhzoum, A., Petit-Paly, G., St Pierre, B., & Bernards, M. A. (2011). Functional analysis of the DAT gene promoter using transient Catharanthus roseus and stable Nicotiana tabacum transformation systems. Plant Cell Reporter, 30(7), 1173-1182. http://dx.doi.org/10.1007/s00299-011-1025-y

Makhzoum, A. B., Sharma, P., Bernards, M. A., & Trémouillaux-Guiller, J. (2013). Hairy Roots: An Ideal Platform for Transgenic Plant Production and Other Promising Applications. Recent Advances in Phytochemistry, Volume 42, Phytochemicals, Plant Growth, and the Environment, pp. 95-142.

Matic, S., Masenga, V., Poli, A., Rinaldi, R., Milne, R. G., Vecchiati, M., & Noris, E. (2012). Comparative analysis of recombinant Human Papillomavirus 8 L1 production in plants by a variety of expression systems and purification methods. Plant Biotechnology Journal, 10(4), 410-421. http://dx.doi.org/10.1111/j.1467-7652.2011.00671.x

Merutka, G., Shalongo, W., & Stellwagen, E. (1991). A model peptide with enhanced helicity. Biochemistry, 30(17), 4245-4248. http://dx.doi.org/10.1021/bi00231a020

Moeller, L., Gan, Q., & Wang, K. (2009). A bacterial signal peptide is functional in plants and directs proteins to the secretory pathway. Journal of Experimental Botany, 60(12), 3337-3352. http://dx.doi.org/10.1093/jxb/erp167

Orlova, A., Tolmachev, V., Pehrson, R., Lindborg, M., Tran, T., Sandstrom, M., ... Feldwisch, J. (2007). Synthetic affibody molecules: a novel class of affinity ligands for molecular imaging of HER2-expressing malignant tumors. Cancer Research, 67(5), 2178-2186. http://dx.doi.org/10.1158/0008-5472.can-06-2887

Ou, J., Guo, Z., Shi, J., Wang, X., Liu, J., Shi, B., ... Yang, D. (2014). Transgenic rice endosperm as a bioreactor for molecular pharming. Plant Cell Reporter, 33(4), 585-594. http://dx.doi.org/10.1007/s00299-013-1559-2

Paul, M. J., Teh, A. Y., Twyman, R. M., & Ma, J. K. (2013). Target product selection - where can Molecular Pharming make the difference? Current Pharmaceutical Design, 19(31), 5478-5485. http://dx.doi.org/10.2174/1381612811319310003

Rademacher, T., Sack, M., Arcalis, E., Stadlmann, J., Balzer, S., Altmann, F., ... Stoger, E. (2008). Recombinant antibody 2G12 produced in maize endosperm efficiently neutralizes HIV-1 and contains predominantly single-GlcNAc N-glycans. Plant Biotechnology Journal, 6(2), 189-201. http://dx.doi.org/10.1111/j.1467-7652.2007.00306.x

Rigano, M. M., De Guzman, G., Walmsley, A. M., Frusciante, L., & Barone, A. (2013). Production of pharmaceutical proteins in solanaceae food crops. International Journal of Molecular Science, 14(2), 2753-2773. http://dx.doi.org/10.3390/ijms14022753

Roy, S., Maheshwari, N., Chauhan, R., Sen, N. K., & Sharma, A. (2011). Structure prediction and functional characterization of secondary metabolite proteins of Ocimum. Bioinformation, 6(8), 315-319. http://dx.doi.org/10.6026/97320630006315

Sabalza, M., Vamvaka, E., Christou, P., & Capell, T. (2013). Seeds as a production system for molecular pharming applications: status and prospects. Current Pharmaceutical Design, 19(31), 5543-5552. http://dx.doi.org/10.2174/1381612811319310009

Satoh, J., Kato, K., & Shinmyo, A. (2004). The 5'-untranslated region of the tobacco alcohol dehydrogenase gene functions as an effective translational enhancer in plant. Journal of Bioscience and Bioengineering, 98(1), 1-8. http://dx.doi.org/10.1016/s1389-1723(04)70234-0

Shah, K., Almaghrabi, B., & Bohlmann, H. (2013). Comparison of Expression Vectors for Transient Expression of Recombinant Proteins in Plants. Plant Molecular Biology Reporter, 31(6), 1529-1538. http://dx.doi.org/10.1007/s11105-013-0614-z

Singhabahu, S., George, J., & Bringloe, D. (2013). Expression of a functional human adenosine deaminase in transgenic tobacco plants. Transgenic Research, 22(3), 643-649. http://dx.doi.org/10.1007/s11248-012-9676-1

Singhabahu, S., George, J., & Bringloe, D. (2014). High yield production of apoplast-directed human adenosine deaminase in transgenic tobacco BY-2 cell suspensions. Biotechnology and Applied Biochemistry. Article first published online: 14 JUL 2014 http://dx.doi.org/10.1002/bab.1240

Skarjinskaia, M., Ruby, K., Araujo, A., Taylor, K., Gopalasamy-Raju, V., Musiychuk, K., ... Yusibov, V. (2013). Hairy roots as a vaccine production and delivery system. Advances in Biochemical Engineering/Biotechnology, 134, 115-134. http://dx.doi.org/10.1007/10_2013_184

Sommese, R. F., Sivaramakrishnan, S., Baldwin, R. L., & Spudich, J. A. (2010). Helicity of short E-R/K peptides. Protein Science, 19(10), 2001-2005. http://dx.doi.org/10.1002/pro.469

Soria-Guerra, R. E., Moreno-Fierros, L., & Rosales-Mendoza, S. (2011). Two decades of plant-based candidate vaccines: a review of the chimeric protein approaches. Plant Cell Reporter, 30(8), 1367-1382. http://dx.doi.org/10.1007/s00299-011-1065-3

Specht, E. A., & Mayfield, S. P. (2014). Algae-based oral recombinant vaccines. Frontiers in Microbiology, 5, 60. http://dx.doi.org/10.3389/fmicb.2014.00060

Stoger, E., Fischer, R., Moloney, M., & Ma, J. K. (2014). Plant molecular pharming for the treatment of chronic and infectious diseases. Annual Review of Plant Biology, 65, 743-768. http://dx.doi.org/10.1146/annurev-arplant-050213-035850

Tremblay, R., Diao, H., Huner, N., Jevnikar, A. M., & Ma, S. (2011). The development of a high-yield recombinant protein bioreactor through RNAi induced knockdown of ATP/ADP transporter in Solanum tuberosum. Journal of Biotechnology, 156(1), 59-66. http://dx.doi.org/10.1016/j.jbiotec.2011.08.005

Trinh, R., Gurbaxani, B., Morrison, S. L., & Seyfzadeh, M. (2004). Optimization of codon pair use within the (GGGGS)3 linker sequence results in enhanced protein expression. Molecular Immunology, 40(10), 717-722. http://dx.doi.org/10.1016/j.molimm.2003.08.006

Tropea, J. E., Cherry, S., & Waugh, D. S. (2009). Expression and purification of soluble His(6)-tagged TEV protease. Methods in Molecular Biology, 498, 297-307. http://dx.doi.org/10.1007/978-1-59745-196-3_19

Twyman, R. M., Schillberg, S., & Fischer, R. (2013). Optimizing the yield of recombinant pharmaceutical proteins in plants. Current Pharmaceutical Design, 19(31), 5486-5494. http://dx.doi.org/10.2174/1381612811319310004

Vaseeharan, B., & Valli, S. J. (2011 ). In silico homology modeling of prophenoloxidase activating factor Serine Proteinase gene from the haemocytes of Fenneropenaeus indicus. Journal of Proteomics and Bioinformatics, 4, 053-057.

Walker, R. A., & Dearing, S. J. (1999). Expression of epidermal growth factor receptor mRNA and protein in primary breast carcinomas. Breast Cancer Research and Treatment, 53(2), 167-176. http://dx.doi.org/10.1023/A:1006194700667

Warzecha, H. (2008). Biopharmaceuticals from plants: a multitude of options for posttranslational modifications. Biotechnology & Genetic Engineering Reviews, 25, 315-330. http://dx.doi.org/10.5661/bger-25-315

Waugh, D. S. (2005). Making the most of affinity tags. Trends in Biotechnology, 23(6), 316-320. http://dx.doi.org/10.1016/j.tibtech.2005.03.012

Waugh, D. S. (2011). An overview of enzymatic reagents for the removal of affinity tags. Protein Expression and Purification, 80(2), 283-293. http://dx.doi.org/10.1016/j.pep.2011.08.005

Wilkins, M. R., Gasteiger, E., Bairoch, A., Sanchez, J. C., Williams, K. L., Appel, R. D., & Hochstrasser, D. F. (1999). Protein identification and analysis tools in the ExPASy server. Methods in Molecular Biology, 112, 531-552.

Yan, W., Imanishi, M., Futaki, S., & Sugiura, Y. (2007). Alpha-helical linker of an artificial 6-zinc finger peptide contributes to selective DNA binding to a discontinuous recognition sequence. Biochemistry, 46(29), 8517-8524. http://dx.doi.org/10.1021/bi7006417

Yang, L., Wakasa, Y., & Takaiwa, F. (2008). Biopharming to increase bioactive peptides in rice seed. Journal of AOAC International, 91(4), 957-964.

Zhang, J., Yun, J., Shang, Z., Zhang, X., & Pan, B. (2009). Design and optimization of a linker for fusion protein construction. Progress in Natural Science, 19(10), 1197-1200. http://dx.doi.org/http://dx.doi.org/10.1016/j.pnsc.2008.12.007

Zhang, L., Shi, J., Jiang, D., Stupak, J., Ou, J., Qiu, Q., ... Yang, D. (2012). Expression and characterization of recombinant human alpha-antitrypsin in transgenic rice seed. Journal of Biotechnology, 164(2), 300-308. http://dx.doi.org/10.1016/j.jbiotec.2013.01.008

Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40. http://dx.doi.org/10.1186/1471-2105-9-40

Zhao, X., Li, G., & Liang, S. (2013). Several Affinity Tags Commonly Used in Chromatographic Purification. Journal of Analytical Methods in Chemistry, 2013, 581093. http://dx.doi.org/10.1155/2013/581093

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04-10-2014

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Makhzoum A, Tahir S, Osborn Locke ME, Trémouillaux-Guiller J, Hefferon K. An in silico overview on the usefulness of tags and linkers in plant molecular pharming. Plant Sci. Today [Internet]. 2014 Oct. 4 [cited 2024 Nov. 24];1(4):201-12. Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/72

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