A biotechnological approach for the production of new protein bioplastics.

E. coli biopolymer disulfide bridges phaseolin transplastomic plants

Journal

Biotechnology journal
ISSN: 1860-7314
Titre abrégé: Biotechnol J
Pays: Germany
ID NLM: 101265833

Informations de publication

Date de publication:
06 Oct 2023
Historique:
revised: 06 09 2023
received: 27 07 2023
accepted: 27 09 2023
pubmed: 6 10 2023
medline: 6 10 2023
entrez: 6 10 2023
Statut: aheadofprint

Résumé

The future of biomaterial production will leverage biotechnology based on the domestication of cells as biological factories. Plants, algae, and bacteria can produce low-environmental impact biopolymers. Here, two strategies were developed to produce a biopolymer derived from a bioengineered vacuolar storage protein of the common bean (phaseolin; PHSL). The cys-added PHSL* forms linear-structured biopolymers when expressed in the thylakoids of transplastomic tobacco leaves by exploiting the formation of inter-chain disulfide bridges. The same protein without signal peptide (ΔPHSL*) accumulates in Escherichia coli inclusion bodies as high-molar-mass species polymers that can subsequently be oxidized to form disulfide crosslinking bridges in order to increase the stiffness of the biomaterial, a valid alternative to the use of chemical crosslinkers. The E. coli cells produced 300 times more engineered PHSL, measured as percentage of total soluble proteins, than transplastomic tobacco plants. Moreover, the thiol groups of cysteine allow the site-specific PEGylation of ΔPHSL*, which is a desirable functionality in the design of a protein-based drug carrier. In conclusion, ΔPHSL* expressed in E. coli has the potential to become an innovative biopolymer.

Identifiants

pubmed: 37801630
doi: 10.1002/biot.202300363
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2300363

Subventions

Organisme : European Union - NextGenerationEU under the Italian Ministry of University and Research (MUR) National Innovation Ecosystem
ID : ECS00000041 - VITALITY-CUPH33C22000430006

Informations de copyright

© 2023 The Authors. Biotechnology Journal published by Wiley-VCH GmbH.

Références

Andrady, A. L., & Neal, M. A. (2009). Applications and societal benefits of plastics. Philosophical Transactions: Biological Sciences, 364(1526), 1977-1984. https://doi.org/10.1098/rstb.2008.0304
Ryan, P. G., Moore, C. J., van Franeker, J. A., & Moloney, C. L. (2009). Monitoring the abundance of plastic debris in the marine environment. Philosophical Transactions of the Royal Society B: Biological Sciences, 364(1526), 1999-2012. https://doi.org/10.1098/rstb.2008.0207
Moslehi, Z., Nafchi, A. M., Moslehi, M., & Jafarzadeh, S. (2021). Aflatoxin, microbial contamination, sensory attributes, and morphological analysis of pistachio nut coated with methylcellulose. Food Science & Nutrition, 9(5), 2576-2584. https://doi.org/10.1002/fsn3.2212
Varanko, A., Saha, S., & Chilkoti, A. (2020). Recent trends in protein and peptide-based biomaterials for advanced drug delivery. Advanced Drug Delivery Reviews, 156, 133-187. https://doi.org/10.1016/j.addr.2020.08.008
Song, F., & Zhang, L.-M. (2009). Gelation modification of soy protein isolate by a naturally occurring cross-linking agent and its potential biomedical application. Industrial & Engineering Chemistry Research, 48(15), 7077-7083. https://doi.org/10.1021/ie801372f
Li, H., Wang, M., Williams, G. R., Wu, J., Sun, X., Lv, Y., & Zhu, L.-M. (2016). Electrospun gelatin nanofibers loaded with vitamins A and E as antibacterial wound dressing materials. RSC Advances, 6(55), 50267-50277. https://doi.org/10.1039/C6RA05092A
Sharma, A. K., & Sharma, M. K. (2009). Plants as bioreactors: Recent developments and emerging opportunities. Biotechnology Advances, 27(6), 811-832. https://doi.org/10.1016/J.BIOTECHADV.2009.06.004
Lössl, A., Eibl, C., Harloff, H. J., Jung, C., & Koop, H. U. (2003). Polyester synthesis in transplastomic tobacco (Nicotiana tabacum L.): Significant contents of polyhydroxybutyrate are associated with growth reduction. Plant Cell Reports, 21(9), 891-899. https://doi.org/10.1007/S00299-003-0610-0
Bally, J., Paget, E., Droux, M., Job, C., Job, D., & Dubald, M. (2008). Both the stroma and thylakoid lumen of tobacco chloroplasts are competent for the formation of disulphide bonds in recombinant proteins. Plant Biotechnology Journal, 6(1), 46-61. https://doi.org/10.1111/J.1467-7652.2007.00298.X
De Marchis, F., Pompa, A., & Bellucci, M. (2012). Plastid proteostasis and heterologous protein accumulation in transplastomic plants. Plant Physiology, 160(2), 571-581. https://doi.org/10.1104/pp.112.203778
Pompa, A., De Marchis, F., Vitale, A., Arcioni, S., & Bellucci, M. (2010). An engineered C-terminal disulfide bond can partially replace the phaseolin vacuolar sorting signal. The Plant Journal, 61(5), 782-791. https://doi.org/10.1111/j.1365-313X.2009.04113.x
Marassi, V., De Marchis, F., Roda, B., Bellucci, M., Capecchi, A., Reschiglian, P., Pompa, A., & Zattoni, A. (2021). Perspectives on protein biopolymers: Miniaturized flow field-flow fractionation-assisted characterization of a single-cysteine mutated phaseolin expressed in transplastomic tobacco plants. Journal of Chromatography A, 1637, 461806. https://doi.org/10.1016/J.CHROMA.2020.461806
De Marchis, F., Pompa, A., Mannucci, R., Morosinotto, T., & Bellucci, M. (2011). A plant secretory signal peptide targets plastome-encoded recombinant proteins to the thylakoid membrane. Plant Molecular Biology, 76(3-5), 427-441. https://doi.org/10.1007/s11103-010-9676-6
De Marchis, F., Bellucci, M., & Pompa, A. (2016). Phaseolin expression in tobacco chloroplast reveals an autoregulatory mechanism in heterologous protein translation. Plant Biotechnology Journal, 14(2), 603-614. https://doi.org/10.1111/PBI.12405
Freudl, R. (2018). Signal peptides for recombinant protein secretion in bacterial expression systems. Microbial Cell Factories, 17(1), 52. https://doi.org/10.1186/s12934-018-0901-3
Pedrazzini, E., Giovinazzo, G., Bielli, A., De Virgilio, M., Frigerio, L., Pesca, M., Faoro, F., Bollini, R., Ceriotti, A., & Vitale, A. (1997). Protein quality control along the route to the plant vacuole. The Plant Cell, 9(10), 1869-1880. https://doi.org/10.1105/TPC.9.10.1869
Watson, J., Koya, V., Leppla, S. H., & Daniell, H. (2004). Expression of Bacillus anthracis protective antigen in transgenic chloroplasts of tobacco, a non-food/feed crop, a non-food/feed crop. Vaccine, 22(31-32), 4374-4384. https://doi.org/10.1016/j.vaccine.2004.01.069
Dhingra, A., Portis Jr, A. R., & Daniell, H. (2004). Enhanced translation of a chloroplast-expressed RbcS gene restores small subunit levels and photosynthesis in nuclear RbcS antisense plants. Proceedings of the National Academy of Sciences of USA, 101(16), 6315-6320. https://doi.org/10.1073/pnas.0400981101
Bellucci, M., De Marchis, F., Nicoletti, I., & Arcioni, S. (2007). Zeolin is a recombinant storage protein with different solubility and stability properties according to its localization in the endoplasmic reticulum or in the chloroplast. Journal of Biotechnology, 131(2), 97-105. https://doi.org/10.1016/j.jbiotec.2007.06.004
De Marchis, F., Pompa, A., & Bellucci, M. (2016). Chemical secretory pathway modulation in plant protoplasts. Methods in Molecular Biology, 1459, 67-79. https://doi.org/10.1007/978-1-4939-3804-9_4
Marassi, V., Marangon, M., Zattoni, A., Vincenzi, S., Versari, A., Reschiglian, P., Roda, B., & Curioni, A. (2021). Characterization of red wine native colloids by asymmetrical flow field-flow fractionation with online multidetection. Food Hydrocolloids, 110, 106204. https://doi.org/10.1016/j.foodhyd.2020.106204
Marassi, V., Giordani, S., Reschiglian, P., Roda, B., & Zattoni, A. (2022). Tracking heme-protein interactions in healthy and pathological human serum in native conditions by miniaturized FFF-multidetection. Applied Sciences, 12(13), 6762. https://doi.org/10.3390/app12136762
Frigerio, L., De Virgilio, M., Prada, A., Faoro, F., & Vitale, A. (1998). Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide. The Plant Cell, 10(6), 1031-1042. https://doi.org/10.1105/tpc.10.6.1031
Singh, P., Sharma, L., Kulothungan, S. R., Adkar, B. V., Prajapati, R. S., Ali, P. S. S., Krishnan, B., & Varadarajan, R. (2013). Effect of signal peptide on stability and folding of Escherichia coli thioredoxin. PLoS One, 8(5), e63442. https://doi.org/10.1371/JOURNAL.PONE.0063442
Pilipchuk, S. P., Vaicik, M. K., Larson, J. C., Gazyakan, E., Cheng, M. H., & Brey, E. M. (2013). Influence of crosslinking on the stiffness and degradation of dermis-derived hydrogels. Journal of Biomedical Materials Research, Part A, 101(10), 2883-2895. https://doi.org/10.1002/JBM.A.34602
Francius, G., Hemmerlé, J., Ohayon, J., Schaaf, P., Voegel, J.-C., Picart, C., & Senger, B. (2006). Effect of crosslinking on the elasticity of polyelectrolyte multilayer films measured by colloidal probe AFM. Microscopy Research and Technique, 69(2), 84-92. https://doi.org/10.1002/jemt.20275
Abe, M. M., Martins, J. R., Sanvezzo, P. B., Macedo, J. V., Branciforti, M. C., Halley, P., Botaro, V. R., & Brienzo, M. (2021). Advantages and disadvantages of bioplastics production from starch and lignocellulosic components. Polymers, 13(15), 2484. https://doi.org/10.3390/POLYM13152484
Ruf, S., Hermann, M., Berger, I. J., Carrer, H., & Bock, R. (2001). Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nature Biotechnology, 19(9), 870-875. https://doi.org/10.1038/nbt0901-870
Oey, M., Lohse, M., Kreikemeyer, B., & Bock, R. (2008). Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. The Plant Journal, 57(3), 436-445. https://doi.org/10.1111/j.1365-313X.2008.03702.x
Dozier, J., & Distefano, M. (2015). Site-specific PEGylation of therapeutic proteins. International Journal of Molecular Sciences, 16(10), 25831-25864. https://doi.org/10.3390/ijms161025831
Krishnakumar, G. S., Sampath, S., Muthusamy, S., & John, M. A. (2019). Importance of crosslinking strategies in designing smart biomaterials for bone tissue engineering: A systematic review. Materials Science and Engineering, C, 96, 941-954. https://doi.org/10.1016/j.msec.2018.11.081

Auteurs

Francesca De Marchis (F)

Institute of Biosciences and Bioresources, Division of Perugia, National Research Council, Perugia, Italy.

Tania Vanzolini (T)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Urbino (PU), Italy.

Elisa Maricchiolo (E)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Urbino (PU), Italy.

Michele Bellucci (M)

Institute of Biosciences and Bioresources, Division of Perugia, National Research Council, Perugia, Italy.

Michele Menotta (M)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Urbino (PU), Italy.

Tomas Di Mambro (T)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Urbino (PU), Italy.

Annalisa Aluigi (A)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Urbino (PU), Italy.

Andrea Zattoni (A)

Department of Chemistry G. Ciamician, University of Bologna, Bologna (BO), Italy.

Barbara Roda (B)

Department of Chemistry G. Ciamician, University of Bologna, Bologna (BO), Italy.

Valentina Marassi (V)

Department of Chemistry G. Ciamician, University of Bologna, Bologna (BO), Italy.

Rita Crinelli (R)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Urbino (PU), Italy.

Andrea Pompa (A)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Urbino (PU), Italy.

Classifications MeSH