Functional Improvement of Human Cardiotrophin 1 Produced in Tobacco Chloroplasts by Co-Expression with Plastid Thioredoxin m
Human cardiotrophin 1 (CT1), a cytokine with excellent therapeutic potential, was previously expressed in tobacco chloroplasts. However, the growth conditions required to reach the highest expression levels resulted in an impairment of its bioactivity. In the present study, we have examined new stra...
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| Published in | Plants (Basel) Vol. 9; no. 2; p. 183 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
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MDPI
02.02.2020
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| Online Access | Get full text |
| ISSN | 2223-7747 2223-7747 |
| DOI | 10.3390/plants9020183 |
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| Abstract | Human cardiotrophin 1 (CT1), a cytokine with excellent therapeutic potential, was previously expressed in tobacco chloroplasts. However, the growth conditions required to reach the highest expression levels resulted in an impairment of its bioactivity. In the present study, we have examined new strategies to modulate the expression of this recombinant protein in chloroplasts so as to enhance its production and bioactivity. In particular, we assessed the effect of both the fusion and co-expression of Trx m with CT1 on the production of a functional CT1 by using plastid transformation. Our data revealed that the Trx m fusion strategy was useful to increase the expression levels of CT1 inside the chloroplasts, although CT1 bioactivity was significantly impaired, and this was likely due to steric hindrance between both proteins. By contrast, the expression of functional CT1 was increased when co-expressed with Trx m, because we demonstrated that recombinant CT1 was functionally active during an in vitro signaling assay. While Trx m/CT1 co-expression did not increase the amount of CT1 in young leaves, our results revealed an increase in CT1 protein stability as the leaves aged in this genotype, which also improved the recombinant protein’s overall production. This strategy might be useful to produce other functional biopharmaceuticals in chloroplasts. |
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| AbstractList | Human cardiotrophin 1 (CT1), a cytokine with excellent therapeutic potential, was previously expressed in tobacco chloroplasts. However, the growth conditions required to reach the highest expression levels resulted in an impairment of its bioactivity. In the present study, we have examined new strategies to modulate the expression of this recombinant protein in chloroplasts so as to enhance its production and bioactivity. In particular, we assessed the effect of both the fusion and co-expression of Trx m with CT1 on the production of a functional CT1 by using plastid transformation. Our data revealed that the Trx m fusion strategy was useful to increase the expression levels of CT1 inside the chloroplasts, although CT1 bioactivity was significantly impaired, and this was likely due to steric hindrance between both proteins. By contrast, the expression of functional CT1 was increased when co-expressed with Trx m, because we demonstrated that recombinant CT1 was functionally active during an in vitro signaling assay. While Trx m/CT1 co-expression did not increase the amount of CT1 in young leaves, our results revealed an increase in CT1 protein stability as the leaves aged in this genotype, which also improved the recombinant protein's overall production. This strategy might be useful to produce other functional biopharmaceuticals in chloroplasts. Human cardiotrophin 1 (CT1), a cytokine with excellent therapeutic potential, was previously expressed in tobacco chloroplasts. However, the growth conditions required to reach the highest expression levels resulted in an impairment of its bioactivity. In the present study, we have examined new strategies to modulate the expression of this recombinant protein in chloroplasts so as to enhance its production and bioactivity. In particular, we assessed the effect of both the fusion and co-expression of Trx m with CT1 on the production of a functional CT1 by using plastid transformation. Our data revealed that the Trx m fusion strategy was useful to increase the expression levels of CT1 inside the chloroplasts, although CT1 bioactivity was significantly impaired, and this was likely due to steric hindrance between both proteins. By contrast, the expression of functional CT1 was increased when co-expressed with Trx m, because we demonstrated that recombinant CT1 was functionally active during an in vitro signaling assay. While Trx m/CT1 co-expression did not increase the amount of CT1 in young leaves, our results revealed an increase in CT1 protein stability as the leaves aged in this genotype, which also improved the recombinant protein's overall production. This strategy might be useful to produce other functional biopharmaceuticals in chloroplasts.Human cardiotrophin 1 (CT1), a cytokine with excellent therapeutic potential, was previously expressed in tobacco chloroplasts. However, the growth conditions required to reach the highest expression levels resulted in an impairment of its bioactivity. In the present study, we have examined new strategies to modulate the expression of this recombinant protein in chloroplasts so as to enhance its production and bioactivity. In particular, we assessed the effect of both the fusion and co-expression of Trx m with CT1 on the production of a functional CT1 by using plastid transformation. Our data revealed that the Trx m fusion strategy was useful to increase the expression levels of CT1 inside the chloroplasts, although CT1 bioactivity was significantly impaired, and this was likely due to steric hindrance between both proteins. By contrast, the expression of functional CT1 was increased when co-expressed with Trx m, because we demonstrated that recombinant CT1 was functionally active during an in vitro signaling assay. While Trx m/CT1 co-expression did not increase the amount of CT1 in young leaves, our results revealed an increase in CT1 protein stability as the leaves aged in this genotype, which also improved the recombinant protein's overall production. This strategy might be useful to produce other functional biopharmaceuticals in chloroplasts. |
| Author | Farran, Inmaculada Fernández-San Millán, Alicia Santamaría, Eva Sanz-Barrio, Ruth Veramendi, Jon Ancín, María Larraya, Luis |
| AuthorAffiliation | 4 CIBERehd, Instituto de Salud Carlos III, 28220 Majadahonda, Madrid, Spain 1 Institute for Multidisciplinary Research in Applied Biology, UPNA, 31006 Pamplona, Spain; maria.ancin@unavarra.es (M.A.); alicia.fernandez@unavarra.es (A.F.-S.M.); luis.larraya@unavarra.es (L.L.); jon@unavarra.es (J.V.) 3 Hepatology Program, University of Navarra, CIMA, E-31008 Pamplona, Spain; evasmaria@unav.es 2 National Centre for Biotechnology, Plant Molecular Genetics Department, CSIC, 28049 Madrid, Spain |
| AuthorAffiliation_xml | – name: 1 Institute for Multidisciplinary Research in Applied Biology, UPNA, 31006 Pamplona, Spain; maria.ancin@unavarra.es (M.A.); alicia.fernandez@unavarra.es (A.F.-S.M.); luis.larraya@unavarra.es (L.L.); jon@unavarra.es (J.V.) – name: 2 National Centre for Biotechnology, Plant Molecular Genetics Department, CSIC, 28049 Madrid, Spain – name: 3 Hepatology Program, University of Navarra, CIMA, E-31008 Pamplona, Spain; evasmaria@unav.es – name: 4 CIBERehd, Instituto de Salud Carlos III, 28220 Majadahonda, Madrid, Spain |
| Author_xml | – sequence: 1 givenname: María surname: Ancín fullname: Ancín, María – sequence: 2 givenname: Ruth surname: Sanz-Barrio fullname: Sanz-Barrio, Ruth – sequence: 3 givenname: Eva surname: Santamaría fullname: Santamaría, Eva – sequence: 4 givenname: Alicia surname: Fernández-San Millán fullname: Fernández-San Millán, Alicia – sequence: 5 givenname: Luis orcidid: 0000-0002-3385-2432 surname: Larraya fullname: Larraya, Luis – sequence: 6 givenname: Jon surname: Veramendi fullname: Veramendi, Jon – sequence: 7 givenname: Inmaculada surname: Farran fullname: Farran, Inmaculada |
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| CitedBy_id | crossref_primary_10_3390_plants10010026 crossref_primary_10_1016_j_pep_2020_105636 crossref_primary_10_1007_s11248_022_00305_x |
| Cites_doi | 10.1089/ars.2011.4327 10.1104/pp.104.052233 10.1038/81161 10.1016/j.bbamcr.2008.02.003 10.1038/nprot.2007.522 10.1146/annurev.arplant.57.032905.105401 10.1089/ars.2007.1931 10.1093/jxb/erw360 10.1016/j.jmb.2005.12.058 10.1016/S0021-9258(19)83562-7 10.1038/73796 10.1146/annurev.pp.31.060180.002013 10.1111/j.1467-7652.2008.00365.x 10.3389/fpls.2013.00390 10.1186/s13007-017-0179-1 10.1111/j.1467-7652.2010.00538.x 10.1007/s00425-010-1102-4 10.1111/j.1467-7652.2004.00072.x 10.1016/0022-2836(90)90313-B 10.1042/bj20030093 10.1074/jbc.M302077200 10.1016/j.cytogfr.2015.07.009 10.1104/pp.112.203778 10.1007/s00425-009-1058-4 10.4161/hv.8247 10.1002/1097-0134(20001115)41:3<334::AID-PROT60>3.0.CO;2-M 10.1111/j.1467-7652.2008.00334.x 10.1111/j.1365-313X.2007.03278.x 10.1111/j.1467-7652.2008.00356.x 10.1104/pp.109.135426 10.1023/A:1022114427971 10.1016/j.febslet.2007.07.081 10.1016/S0021-9258(19)49464-7 10.1006/prep.1997.0767 10.1046/j.1365-313x.2001.00958.x 10.1016/j.vaccine.2011.06.039 10.1002/pro.157 10.1006/abio.1994.1060 10.1186/s13068-016-0569-z 10.1073/pnas.232703799 10.18388/abp.1999_4131 10.1007/s00294-007-0128-z 10.1104/pp.105.063040 10.1016/S0076-6879(00)26063-1 10.1073/pnas.92.4.1142 10.1007/s11248-008-9186-3 10.1093/jxb/err282 10.1105/tpc.109.071001 10.1111/j.1467-7652.2011.00608.x 10.1111/j.1365-313X.2008.03702.x 10.1016/j.vaccine.2004.11.004 10.1016/j.pep.2008.04.013 10.1046/j.1467-7652.2004.00057.x 10.1002/biot.201100155 10.1104/pp.125.1.430 10.1007/s00253-002-1158-6 10.1104/pp.110.170969 10.1074/jbc.270.43.25328 10.1016/j.pep.2004.08.004 10.1038/nbt1098-934 10.3389/fpls.2018.01893 10.1016/j.jprot.2008.12.002 10.1146/annurev-genet-102108-134201 10.1021/bi011186x 10.1007/s00425-009-0898-2 |
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| Keywords | cardiotrophin-1, thioredoxin, plastid transformation, bioactivity, tobacco |
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| References | Azhagiri (ref_7) 2007; 52 Collin (ref_27) 2004; 136 Carballeda (ref_19) 2012; 63 Park (ref_18) 2009; 150 Samson (ref_8) 2009; 5 Bustos (ref_13) 2015; 26 Katti (ref_32) 1990; 212 Sul (ref_70) 1996; 2 Adem (ref_3) 2017; 13 Young (ref_23) 2012; 7 Oey (ref_5) 2009; 57 Ye (ref_48) 2001; 25 Jurado (ref_22) 2006; 357 Lee (ref_54) 2011; 9 Kern (ref_17) 2003; 371 Meyer (ref_26) 2012; 17 (ref_41) 2009; 8 Meyer (ref_15) 2009; 43 Maliga (ref_39) 2011; 155 Buyel (ref_2) 2019; 9 Farran (ref_14) 2008; 6 Buchanan (ref_29) 1980; 31 LaVallie (ref_68) 1993; 268 Pennica (ref_12) 1995; 92 Staub (ref_47) 2000; 18 Ahmad (ref_4) 2016; 67 LaVallie (ref_24) 2000; 326 Balmer (ref_60) 2003; 100 Yasukawa (ref_20) 1995; 270 Nilsson (ref_25) 1997; 11 Lemaire (ref_53) 2007; 51 Parks (ref_69) 1994; 216 Kuroda (ref_35) 2001; 125 Zhou (ref_49) 2008; 6 Montrichard (ref_61) 2009; 72 Rey (ref_59) 2013; 4 Garcia (ref_64) 2008; 9 Collin (ref_57) 2003; 278 Daniell (ref_11) 2005; 23 Iamtham (ref_36) 2000; 18 Lentz (ref_55) 2010; 231 Yuan (ref_42) 2004; 38 Leelavathi (ref_44) 2003; 11 Castiglia (ref_6) 2016; 9 Pompa (ref_40) 2012; 160 Newell (ref_50) 2004; 2 Terpe (ref_62) 2003; 60 Lancelin (ref_31) 2000; 41 Farran (ref_33) 2011; 9 Lenzi (ref_45) 2008; 17 Arakawa (ref_67) 1998; 16 Berndt (ref_16) 2008; 1783 Zhao (ref_66) 2008; 61 Sakamoto (ref_52) 2006; 57 Verma (ref_10) 2008; 3 Arsova (ref_28) 2010; 22 Christensen (ref_65) 2009; 18 McCabe (ref_51) 2008; 6 Buchanan (ref_56) 2008; 10 ref_1 Neira (ref_30) 2001; 40 Molina (ref_34) 2004; 2 Holmgren (ref_38) 1979; 254 Yu (ref_21) 2011; 29 Wu (ref_63) 1999; 46 Daniell (ref_37) 1997; 62 Farran (ref_43) 2010; 231 Laugier (ref_58) 2007; 581 Ruiz (ref_9) 2005; 138 Scotti (ref_46) 2009; 229 |
| References_xml | – volume: 17 start-page: 1124 year: 2012 ident: ref_26 article-title: Thioredoxin and glutaredoxin systems in plants: Molecular mechanisms, crosstalks, and functional significance publication-title: Antioxid. Redox Signal. doi: 10.1089/ars.2011.4327 – volume: 136 start-page: 4088 year: 2004 ident: ref_27 article-title: Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type publication-title: Plant Physiol. doi: 10.1104/pp.104.052233 – volume: 18 start-page: 1172 year: 2000 ident: ref_36 article-title: Removal of antibiotic resistance genes from transgenic tobacco plastids publication-title: Nat. Biotechnol. doi: 10.1038/81161 – volume: 1783 start-page: 641 year: 2008 ident: ref_16 article-title: Thioredoxins and glutaredoxins as facilitators of protein folding publication-title: Biochim. Biophys. Acta Mol. Cell Res. doi: 10.1016/j.bbamcr.2008.02.003 – volume: 3 start-page: 739 year: 2008 ident: ref_10 article-title: A protocol for expression of foreign genes in chloroplasts publication-title: Nat. Protoc. doi: 10.1038/nprot.2007.522 – volume: 57 start-page: 599 year: 2006 ident: ref_52 article-title: Protein Degradation Machineries in Plastids publication-title: Annu. Rev. Plant Biol. doi: 10.1146/annurev.arplant.57.032905.105401 – volume: 10 start-page: 1235 year: 2008 ident: ref_56 article-title: The ferredoxin/thioredoxin system of oxygenic photosynthesis publication-title: Antioxid. Redox Signal. doi: 10.1089/ars.2007.1931 – volume: 67 start-page: 5945 year: 2016 ident: ref_4 article-title: Challenges and perspectives in commercializing plastid transformation technology publication-title: J. Exp. Bot. doi: 10.1093/jxb/erw360 – volume: 357 start-page: 49 year: 2006 ident: ref_22 article-title: Thioredoxin Fusions Increase Folding of Single Chain Fv Antibodies in the Cytoplasm of Escherichia coli: Evidence that Chaperone Activity is the Prime Effect of Thioredoxin publication-title: J. Mol. Biol. doi: 10.1016/j.jmb.2005.12.058 – volume: 254 start-page: 9627 year: 1979 ident: ref_38 article-title: Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide publication-title: J. Biol. Chem. doi: 10.1016/S0021-9258(19)83562-7 – volume: 18 start-page: 333 year: 2000 ident: ref_47 article-title: High-yield production of a human therapeutic protein in tobacco chloroplasts publication-title: Nat. Biotechnol. doi: 10.1038/73796 – volume: 31 start-page: 341 year: 1980 ident: ref_29 article-title: Role of Light in the Regulation of Chloroplast Enzymes publication-title: Annu. Rev. Plant Physiol. doi: 10.1146/annurev.pp.31.060180.002013 – volume: 6 start-page: 914 year: 2008 ident: ref_51 article-title: Plastid transformation of high-biomass tobacco variety Maryland Mammoth for production of human immunodeficiency virus type 1 (HIV-1) p24 antigen publication-title: Plant Biotechnol. J. doi: 10.1111/j.1467-7652.2008.00365.x – volume: 4 start-page: 390 year: 2013 ident: ref_59 article-title: Overexpression of plastidial thioredoxins f and m differentially alters photosynthetic activity and response to oxidative stress in tobacco plants publication-title: Front. Plant Sci. doi: 10.3389/fpls.2013.00390 – volume: 13 start-page: 1 year: 2017 ident: ref_3 article-title: Recent achievements obtained by chloroplast transformation publication-title: Plant Methods doi: 10.1186/s13007-017-0179-1 – volume: 9 start-page: 100 year: 2011 ident: ref_54 article-title: Expression and characterization of antimicrobial peptides Retrocyclin-101 and Protegrin-1 in chloroplasts to control viral and bacterial infections publication-title: Plant Biotechnol. J. doi: 10.1111/j.1467-7652.2010.00538.x – volume: 231 start-page: 977 year: 2010 ident: ref_43 article-title: The vaccine adjuvant extra domain A from fibronectin retains its proinflammatory properties when expressed in tobacco chloroplasts publication-title: Planta doi: 10.1007/s00425-010-1102-4 – volume: 2 start-page: 261 year: 2004 ident: ref_50 article-title: Accumulation of rotavirus VP6 protein in chloroplasts of transplastomic tobacco is limited by protein stability publication-title: Plant Biotechnol. J. doi: 10.1111/j.1467-7652.2004.00072.x – volume: 212 start-page: 167 year: 1990 ident: ref_32 article-title: Crystal structure of thioredoxin from Escherichia coli at 1.68 Å resolution publication-title: J. Mol. Biol. doi: 10.1016/0022-2836(90)90313-B – ident: ref_1 – volume: 371 start-page: 965 year: 2003 ident: ref_17 article-title: Chaperone properties of Escherichia coli thioredoxin and thioredoxin reductase publication-title: Biochem. J. doi: 10.1042/bj20030093 – volume: 278 start-page: 23747 year: 2003 ident: ref_57 article-title: The Arabidopsis plastidial thioredoxins publication-title: J. Biol. Chem. doi: 10.1074/jbc.M302077200 – volume: 8 start-page: 1 year: 2009 ident: ref_41 article-title: Strategies for successful recombinant expression of disulfide bond-dependent proteins in Escherichia coli publication-title: Microb. Cell Fact. – volume: 26 start-page: 523 year: 2015 ident: ref_13 article-title: Cardiotrophin-1: A multifaceted cytokine publication-title: Cytokine Growth Factor Rev. doi: 10.1016/j.cytogfr.2015.07.009 – volume: 9 start-page: 1 year: 2008 ident: ref_64 article-title: Rapid regulation of protein activity in fission yeast publication-title: BMC Cell Biol. – volume: 160 start-page: 571 year: 2012 ident: ref_40 article-title: Plastid proteostasis and heterologous protein accumulation in transplastomic plants publication-title: Plant Physiol. doi: 10.1104/pp.112.203778 – volume: 231 start-page: 387 year: 2010 ident: ref_55 article-title: High expression level of a foot and mouth disease virus epitope in tobacco transplastomic plants publication-title: Planta doi: 10.1007/s00425-009-1058-4 – volume: 5 start-page: 488 year: 2009 ident: ref_8 article-title: The green vaccine: A global strategy to combat infectious and autoimmune diseases publication-title: Hum. Vaccin. doi: 10.4161/hv.8247 – volume: 41 start-page: 334 year: 2000 ident: ref_31 article-title: NMR structures of thioredoxin m from the green alga Chlamydomonas reinhardtii publication-title: Proteins Struct. Funct. Genet. doi: 10.1002/1097-0134(20001115)41:3<334::AID-PROT60>3.0.CO;2-M – volume: 6 start-page: 516 year: 2008 ident: ref_14 article-title: High-density seedling expression system for the production of bioactive human cardiotrophin-1, a potential therapeutic cytokine, in transgenic tobacco chloroplasts publication-title: Plant Biotechnol. J. doi: 10.1111/j.1467-7652.2008.00334.x – volume: 52 start-page: 817 year: 2007 ident: ref_7 article-title: Exceptional paternal inheritance of plastids in Arabidopsis suggests that low-frequency leakage of plastids via pollen may be universal in plants publication-title: Plant J. doi: 10.1111/j.1365-313X.2007.03278.x – volume: 6 start-page: 897 year: 2008 ident: ref_49 article-title: High-level expression of human immunodeficiency virus antigens from the tobacco and tomato plastid genomes publication-title: Plant Biotechnol. J. doi: 10.1111/j.1467-7652.2008.00356.x – volume: 150 start-page: 552 year: 2009 ident: ref_18 article-title: Heat-shock and redox-dependent functional switching of an h-type Arabidopsis thioredoxin from a disulfide reductase to a molecular chaperone publication-title: Plant Physiol. doi: 10.1104/pp.109.135426 – volume: 11 start-page: 49 year: 2003 ident: ref_44 article-title: Chloroplast expression of His-tagged GUS-fusions: A general strategy to overproduce and purify foreign proteins using transplastomic plants as bioreactors publication-title: Mol. Breed. doi: 10.1023/A:1022114427971 – volume: 581 start-page: 4371 year: 2007 ident: ref_58 article-title: Specificity of thioredoxins and glutaredoxins as electron donors to two distinct classes of Arabidopsis plastidial methionine sulfoxide reductases B publication-title: FEBS Lett. doi: 10.1016/j.febslet.2007.07.081 – volume: 268 start-page: 23311 year: 1993 ident: ref_68 article-title: Cloning and functional expression of a cDNA encoding the catalytic subunit of bovine enterokinase publication-title: J. Biol. Chem. doi: 10.1016/S0021-9258(19)49464-7 – volume: 11 start-page: 1 year: 1997 ident: ref_25 article-title: Affinity Fusion Strategies for Detection, Purification, and Immobilization of Recombinant Proteins publication-title: Protein Expr. Purif. doi: 10.1006/prep.1997.0767 – volume: 25 start-page: 261 year: 2001 ident: ref_48 article-title: Plastid-expressed 5-enolpyruvylshikimate-3-phosphate synthase genes provide high level glyphosate tolerance in tobacco publication-title: Plant J. doi: 10.1046/j.1365-313x.2001.00958.x – volume: 29 start-page: 5978 year: 2011 ident: ref_21 article-title: Co-expression of tetanus toxin fragment C in Escherichia coli with thioredoxin and its evaluation as an effective subunit vaccine candidate publication-title: Vaccine doi: 10.1016/j.vaccine.2011.06.039 – volume: 18 start-page: 1377 year: 2009 ident: ref_65 article-title: Fusion order controls expression level and activity of elastin-like polypeptide fusion proteins publication-title: Protein Sci. doi: 10.1002/pro.157 – volume: 216 start-page: 413 year: 1994 ident: ref_69 article-title: Release of Proteins and Peptides from Fusion Proteins Using a Recombinant Plant Virus Proteinase publication-title: Anal. Biochem. doi: 10.1006/abio.1994.1060 – volume: 9 start-page: 154 year: 2016 ident: ref_6 article-title: High-level expression of thermostable cellulolytic enzymes in tobacco transplastomic plants and their use in hydrolysis of an industrially pretreated Arundo donax L. biomass publication-title: Biotechnol. Biofuels doi: 10.1186/s13068-016-0569-z – volume: 100 start-page: 370 year: 2003 ident: ref_60 article-title: Proteomics gives insight into the regulatory function of chloroplast thioredoxins publication-title: Proc. Natl. Acad. Sci. USA doi: 10.1073/pnas.232703799 – volume: 46 start-page: 591 year: 1999 ident: ref_63 article-title: Hexahistidine (His6)-tag dependent protein dimerization: A cautionary tale publication-title: Acta Biochim. Pol. doi: 10.18388/abp.1999_4131 – volume: 2 start-page: 113 year: 1996 ident: ref_70 article-title: A highly efficient method for isolating genomic DNA from plant tissues publication-title: Plant Tissue Cult. Biotechnol. – volume: 51 start-page: 343 year: 2007 ident: ref_53 article-title: Thioredoxins in chloroplasts publication-title: Curr. Genet. doi: 10.1007/s00294-007-0128-z – volume: 138 start-page: 1746 year: 2005 ident: ref_9 article-title: Characterization of heterologous multigene operons in transgenic chloroplasts. Transcription, processing, and translation publication-title: Plant Physiol. doi: 10.1104/pp.105.063040 – volume: 326 start-page: 322 year: 2000 ident: ref_24 article-title: Thioredoxin as a fusion partner for production of soluble recombinant proteins in Escherichia coli publication-title: Methods Enzymol. doi: 10.1016/S0076-6879(00)26063-1 – volume: 62 start-page: 463 year: 1997 ident: ref_37 article-title: Transformation and Foreign Gene Expression in Plants Mediated by Microprojectile Bombardment publication-title: Methods Mol. Biol. – volume: 92 start-page: 1142 year: 1995 ident: ref_12 article-title: Expression cloning of cardiotrophin 1, a cytokine that induces cardiac myocyte hypertrophy publication-title: Proc. Natl. Acad. Sci. USA doi: 10.1073/pnas.92.4.1142 – volume: 17 start-page: 1091 year: 2008 ident: ref_45 article-title: Translational fusion of chloroplast-expressed human papillomavirus type 16 L1 capsid protein enhances antigen accumulation in transplastomic tobacco publication-title: Transgenic Res. doi: 10.1007/s11248-008-9186-3 – volume: 63 start-page: 365 year: 2012 ident: ref_19 article-title: Chaperone-like properties of tobacco plastid thioredoxins f and m publication-title: J. Exp. Bot. doi: 10.1093/jxb/err282 – volume: 22 start-page: 1498 year: 2010 ident: ref_28 article-title: Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: Evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana publication-title: Plant Cell Online doi: 10.1105/tpc.109.071001 – volume: 9 start-page: 639 year: 2011 ident: ref_33 article-title: Tobacco plastidial thioredoxins as modulators of recombinant protein production in transgenic chloroplasts publication-title: Plant Biotechnol. J. doi: 10.1111/j.1467-7652.2011.00608.x – volume: 57 start-page: 436 year: 2009 ident: ref_5 article-title: Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic publication-title: Plant J. doi: 10.1111/j.1365-313X.2008.03702.x – volume: 23 start-page: 1779 year: 2005 ident: ref_11 article-title: Chloroplast-derived vaccine antigens and other therapeutic proteins publication-title: Vaccine doi: 10.1016/j.vaccine.2004.11.004 – volume: 61 start-page: 73 year: 2008 ident: ref_66 article-title: Increasing the homogeneity, stability and activity of human serum albumin and interferon-α2b fusion protein by linker engineering publication-title: Protein Expr. Purif. doi: 10.1016/j.pep.2008.04.013 – volume: 2 start-page: 141 year: 2004 ident: ref_34 article-title: High-yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts publication-title: Plant Biotechnol. J. doi: 10.1046/j.1467-7652.2004.00057.x – volume: 7 start-page: 620 year: 2012 ident: ref_23 article-title: Recombinant protein expression and purification: A comprehensive review of affinity tags and microbial applications publication-title: Biotechnol. J. doi: 10.1002/biot.201100155 – volume: 125 start-page: 430 year: 2001 ident: ref_35 article-title: Sequences downstream of the translation initiation codon are important determinants of translation efficiency in chloroplasts publication-title: Plant Physiol. doi: 10.1104/pp.125.1.430 – volume: 60 start-page: 523 year: 2003 ident: ref_62 article-title: Overview of tag protein fusions: From molecular and biochemical fundamentals to commercial systems publication-title: Appl. Microbiol. Biotechnol. doi: 10.1007/s00253-002-1158-6 – volume: 155 start-page: 1501 year: 2011 ident: ref_39 article-title: Plastid biotechnology: Food, fuel, and medicine for the 21st century publication-title: Plant Physiol. doi: 10.1104/pp.110.170969 – volume: 270 start-page: 25328 year: 1995 ident: ref_20 article-title: Increase of solubility of foreign proteins in Escherichia coli by coproduction of the bacterial thioredoxin publication-title: J. Biol. Chem. doi: 10.1074/jbc.270.43.25328 – volume: 38 start-page: 51 year: 2004 ident: ref_42 article-title: The role of thioredoxin and disulfide isomerase in the expression of the snake venom thrombin-like enzyme calobin in Escherichia coli BL21 (DE3) publication-title: Protein Expr. Purif. doi: 10.1016/j.pep.2004.08.004 – volume: 16 start-page: 934 year: 1998 ident: ref_67 article-title: A plant-based cholera toxin B subunit–insulin fusion protein protects against the development of autoimmune diabetes publication-title: Nat. Biotechnol. doi: 10.1038/nbt1098-934 – volume: 9 start-page: 1893 year: 2019 ident: ref_2 article-title: Plant molecular farming—Integration and exploitation of side streams to achieve sustainable biomanufacturing publication-title: Front. Plant Sci. doi: 10.3389/fpls.2018.01893 – volume: 72 start-page: 452 year: 2009 ident: ref_61 article-title: Thioredoxin targets in plants: The first 30 years publication-title: J. Proteomics doi: 10.1016/j.jprot.2008.12.002 – volume: 43 start-page: 335 year: 2009 ident: ref_15 article-title: Thioredoxins and glutaredoxins: Unifying elements in redox biology publication-title: Annu. Rev. Genet. doi: 10.1146/annurev-genet-102108-134201 – volume: 40 start-page: 15246 year: 2001 ident: ref_30 article-title: Three-dimensional solution structure and stability of thioredoxin m from spinach publication-title: Biochemistry doi: 10.1021/bi011186x – volume: 229 start-page: 1109 year: 2009 ident: ref_46 article-title: High-level expression of the HIV-1 Pr55gag polyprotein in transgenic tobacco chloroplasts publication-title: Planta doi: 10.1007/s00425-009-0898-2 |
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| SubjectTerms | bioactive properties bioactivity biopharmaceuticals cardiotrophin-1 chloroplasts cytokines genotype humans leaves plastid transformation recombinant proteins thioredoxin thioredoxins tobacco |
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| Title | Functional Improvement of Human Cardiotrophin 1 Produced in Tobacco Chloroplasts by Co-Expression with Plastid Thioredoxin m |
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