Exploring the potential of two Pseudomonas species to produce vincristine from vinblastine via biotransformation.
Pseudomonas spp
Antiangiogenic
Biotransformation
CAM assay
Vinblastine
Vincristine
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
23 Aug 2024
23 Aug 2024
Historique:
received:
26
03
2024
accepted:
19
08
2024
medline:
24
8
2024
pubmed:
24
8
2024
entrez:
23
8
2024
Statut:
epublish
Résumé
A biotransformation pair consisting of vinblastine: vincristine present in the Catharanthus roseus plant is of immense pharmacological significance. In this study, we successfully transformed vinblastine into vincristine outside the plant using Pseudomonas aeruginosa 8485 and Pseudomonas fluorescens 2421 and evaluated the antiangiogenic potential of thus produced vincristine through the CAM assay. The toxicity assay showed that both Pseudomonas spp. can tolerate varying concentrations (25-100 µl of 1 mg/ml) of vinblastine. The biotransformation was performed in a liquid nutrient broth medium containing vinblastine (25-100 µl), and Pseudomonas spp. inoculums (50-150 µl) by incubating at 30 °C and 37 °C, respectively for 8 days. The process was optimized for substrate and culture concentrations, pH, temperature, and rotation speed (rpm) for the highest conversion. Analysis using LC-MS/MS confirmed the presence of vincristine as a product of the vinblastine biotransformation by two Pseudomonas spp. P. fluorescens 2421 showed a faster conversion rate with 95% of vinblastine transformed within 24 h than P. aeruginosa 8485, which demonstrated a conversion rate of 92% on the 8
Identifiants
pubmed: 39179785
doi: 10.1038/s41598-024-70571-8
pii: 10.1038/s41598-024-70571-8
doi:
Substances chimiques
Vincristine
5J49Q6B70F
Vinblastine
5V9KLZ54CY
Angiogenesis Inhibitors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
19652Informations de copyright
© 2024. The Author(s).
Références
Keglevich, P., Hazai, L., Kalaus, G. & Szantay, C. Modifications on the basic skeletons of vinblastine and vincristine. Molecules 17, 5893–5914 (2012).
doi: 10.3390/molecules17055893
pubmed: 22609781
pmcid: 6268133
Field, J. J., Waight, A. B. & Senter, P. D. A previously undescribed tubulin binder. Proc. Natl. Acad. Sci. USA 111, 13684–13685 (2014).
doi: 10.1073/pnas.1414572111
pubmed: 25187564
pmcid: 4183339
Skubník, J., Pavlíčková, V. S., Ruml, T. & Rimpelová, S. Vincristine in combination therapy of cancer: Emerging trends in clinics. Biology 10, 849. https://doi.org/10.3390/biology10090849 (2021).
doi: 10.3390/biology10090849
pubmed: 34571726
pmcid: 8468923
Almagro, L., Fernández-Perez, F. & Pedreno, M. A. Indole alkaloids from Catharanthus roseus: Bioproduction and their effect on human health. Molecules 20, 2973–3000 (2015).
doi: 10.3390/molecules20022973
pubmed: 25685907
pmcid: 6272713
Gajalakshmi, S., Vijayalakshmi, S. & Devi, R. V. Pharmacological activities of Catharanthus roseus: A perspective review. Int. J. Pharm. Biol. Sci. 4, 431–439 (2013).
Dhyani, P. et al. Anticancer potential of alkaloids: A key emphasis to colchicine, vinblastine, vincristine, vindesine, vinorelbine and vincamine. Cancer Cell Int. 22, 1–20 (2022).
doi: 10.1186/s12935-022-02624-9
Prasad, V. & Mailankody, S. Research and development spending to bring a single cancer drug to market and revenues after approvall. JAMA Intern. Med. 177, 1569–1575 (2017).
doi: 10.1001/jamainternmed.2017.3601
pubmed: 28892524
pmcid: 5710275
Qu, Y., Safonova, O. & De Luca, V. Completion of the canonical pathway for assembly of anticancer drugs vincristine/vinblastine in Catharanthus roseus. Plant J. 97, 257–266 (2019).
doi: 10.1111/tpj.14111
pubmed: 30256480
Zhu, X., Zeng, X., Sun, C. & Chen, S. Biosynthetic pathway of terpenoid indole alkaloids in Catharanthus roseus. Front. Med. 8, 285–293 (2014).
doi: 10.1007/s11684-014-0350-2
pubmed: 25159992
Sharma, A., Verma, P., Mathur, A. & Mathur, A. K. Genetic engineering approach using early vinca alkaloid biosynthesis genes led to increased tryptamine and terpenoid indole alkaloids biosynthesis in differentiating cultures of Catharanthus roseus. Protoplasma 255, 425–435 (2018).
doi: 10.1007/s00709-017-1151-7
pubmed: 28808798
Mistry, V., Darji, S., Tiwari, P. & Sharma, A. Engineering Catharanthus roseus monoterpenoid indole alkaloid pathway in yeast. Appl. Microbiol. Biotechnol. 106, 2337–2347 (2022).
doi: 10.1007/s00253-022-11883-5
pubmed: 35333954
Sottomayor, M. & Ros Barceló, A. Peroxidase from Catharanthus roseus (L.) G. Don and the biosynthesis of alpha-3’,4’-anhydrovinblastine: A specific role for a multifunctional enzyme. Protoplasma 222, 97–105. https://doi.org/10.1007/s00709-003-0003-9 (2003).
doi: 10.1007/s00709-003-0003-9
pubmed: 14513315
Zhu, J., Wang, M., Wen, W. & Yu, R. Biosynthesis and regulation of terpenoid indole alkaloids in Catharanthus roseus. Pharmacogn. Rev. 9, 24–28. https://doi.org/10.4103/0973-7847 (2015).
doi: 10.4103/0973-7847
pubmed: 26009689
pmcid: 4441158
Caputi, L. et al. Missing enzymes in the biosynthesis of the anticancer drug vinblastine in Madagascar periwinkle. Science 360, 1235–1239. https://doi.org/10.1126/science.aat4100 (2018).
doi: 10.1126/science.aat4100
pubmed: 29724909
Ferreres, F. et al. Simple and reproducible HPLC-DAD-ESI-MS/MS analysis of alkaloids in Catharanthus roseus roots. J. Pharm. Biomed. Anal. 51, 65–69. https://doi.org/10.1016/j.jpba.2009.08.005 (2010).
doi: 10.1016/j.jpba.2009.08.005
pubmed: 19720492
Hamada, H. & Nakazawa, K. Biotransformation of vinblastine to vincristine by cell suspension cultures of Catharanthus roseus. Biotechnol. Lett. 13, 805–806 (1991).
doi: 10.1007/BF01026763
Kumar, A. & Ahmad, A. Biotransformation of vinblastine to vincristine by the endophytic fungus Fusarium oxysporum isolated from Catharanthus roseus. Biocatal. Biotransform. 31, 89–93 (2013).
doi: 10.3109/10242422.2013.776544
Tonk, D. et al. Fungal elicitation enhances vincristine and vinblastine yield in the embryogenic tissues of Catharanthus roseus. Plants 12, 3373 (2023).
doi: 10.3390/plants12193373
pubmed: 37836112
pmcid: 10574240
Zhang, J. et al. A microbial supply chain for production of the anti-cancer drug vinblastine. Nature 609, 341–347. https://doi.org/10.1038/s41586-022-05157-3 (2022).
doi: 10.1038/s41586-022-05157-3
pubmed: 36045295
pmcid: 9452304
Borges, K. B. et al. Stereoselective biotransformations using fungi as biocatalysts. Tetrahedron 20, 385–397 (2009).
doi: 10.1016/j.tetasy.2009.02.009
Hegazy, M. E. F. et al. Microbial biotransformation as a tool for drug development based on natural products from mevalonic acid pathway: A review. J. Adv. Res. 6, 17–33 (2015).
doi: 10.1016/j.jare.2014.11.009
pubmed: 25685541
Naik, S. B. Potential roles for endophytic fungi in biotechnological processes: A review. In Plant and Human Health Volume 2: Phytochemistry and Molecular Aspect 327–344 (Springer, 2019).
doi: 10.1007/978-3-030-03344-6_14
Mishra, S., Sahu, P. K., Agarwal, V. & Singh, N. Exploiting endophytic microbes as micro-factories for plant secondary metabolite production. Appl. Microbiol. Biotechnol. 105, 6579–6596 (2021).
doi: 10.1007/s00253-021-11527-0
pubmed: 34463800
Rathbone, D. A. & Bruce, N. C. Microbial transformation of alkaloids. Curr. Opin. Microbiol. 5, 274–281 (2002).
doi: 10.1016/S1369-5274(02)00317-X
pubmed: 12057681
Chen, T. S., Li, X., Bollag, D., Liu, Y. & Chang, C. Biotransformation of taxol. Tetrahedron Lett. 42, 3787–3789 (2001).
doi: 10.1016/S0040-4039(01)00557-3
Asano, Y. Development of new microbial enzymes and their application to organic synthesis. J. Synth. Organ. Chem. 57, 1064–1072 (1999).
doi: 10.5059/yukigoseikyokaishi.57.1064
Neuss, N. et al. Vinca alkaloids XXXIII [1]. Microbiological conversions of vinca leukoblastine (VLB, vinblastine), an antitumor alkaloid from Vinca rosea. Linn. Helv. Chim. Acta 57, 1886–1890 (1974).
doi: 10.1002/hlca.19740570643
pubmed: 4465345
Bouaziz, A. et al. Antibacterial and antioxidant activities of Hammada scoparia extracts and its major purified alkaloids. South Afr. J. Bot. 105, 89–96 (2016).
doi: 10.1016/j.sajb.2016.03.012
Zheng, Y. G., Zhang, X. F. & Shen, Y. C. Microbial transformation of validamycin A to valienamine by immobilized cells. Biocatal. Biotransform. 23, 71–77 (2005).
doi: 10.1080/10242420500090128
Volkov, S. K. & Grodnitskaya, E. I. Methods for raising the efficiency of chromatographic purification of vinblastine preparations. Pharm. Chem. J. 29, 801–803 (1995).
doi: 10.1007/BF02331869
Tayal, N., Srivastava, P. & Srivastava, N. Anti angiogenic activity of Carica papaya leaf extract. J. Pure Appl. Microbiol. 13, 567–571 (2019).
doi: 10.22207/JPAM.13.1.64
Molina, G., Pimentel, M. R. & Pastore, G. M. Pseudomonas: A promising biocatalyst for the bioconversion of terpenes. Appl. Microbiol. Biotechnol. 97, 1851–1864. https://doi.org/10.1007/s00253-013-4701-8 (2013).
doi: 10.1007/s00253-013-4701-8
pubmed: 23358998
Żur, J., Wojcieszyńska, D. & Guzik, U. Metabolic responses of bacterial cells to immobilization. Molecules 21, 958 (2016).
doi: 10.3390/molecules21070958
pubmed: 27455220
pmcid: 6273605
Cardillo, A. B. et al. Production of tropane alkaloids by biotransformation using recombinant Escherichia coli whole cells. Biochem. Eng. J. 125, 180–189 (2017).
doi: 10.1016/j.bej.2017.06.013
Dhiman, S., Mukherjee, G. & Singh, A. K. Recent trends and advancements in microbial tannase-catalyzed biotransformation of tannins: A review. Int. Microbiol. 21, 175–195 (2018).
doi: 10.1007/s10123-018-0027-9
pubmed: 30810902
Singh, N. R., Rath, S. K., Behera, S. & Naik, S. K. In vitro secondary metabolite production through fungal elicitation: An approach for sustainability. In Fungal Nanobionics: Principles and Applications 215–242 (Springer Singapore, 2018).
Satheesan, J. & Sabu, K. K. Endophytic fungi for a sustainable production of major plant bioactive compounds. In Plant Derived Bioactives: Production, Properties and Therapeutic Applications 195–207 (Springer Singapore, 2020).
doi: 10.1007/978-981-15-1761-7_8
Mujib, A., Tonk, D., Gulzar, B., Maqsood, M. & Ali, M. Quantification of taxol by high performance thin layer chromatography (HPTLC) in Taxus wallichiana callus cultivated in vitro. BioTechnologia 101, 337–347 (2020).
doi: 10.5114/bta.2020.100425
Fischer, I., Gagner, J. P., Law, M., Newcomb, E. W. & Zagzag, D. Angiogenesis in gliomas: Biology and molecular pathophysiology. Brain Pathol. 15, 297–310 (2005).
doi: 10.1111/j.1750-3639.2005.tb00115.x
pubmed: 16389942
Irie, N., Matsuo, T. & Nagata, I. Protocol of radiotherapy for glioblastoma according to the expression of HIF-1. Brain Tumor Pathol. 21, 1–6 (2004).
doi: 10.1007/BF02482169
pubmed: 15696961
Jung, Y. J., Isaacs, J. S., Lee, S., Trepel, J. & Neckers, L. Microtubule disruption utilizes an NFkappa B-dependent pathway to stabilize HIF-1alpha protein. J. Biol. Chem. 278, 7445–7452 (2003).
doi: 10.1074/jbc.M209804200
pubmed: 12488445
Nowak-Sliwinska, P., Segura, T. & Iruela-Arispe, M. L. The chicken chorioallantoic membrane model in biology, medicine and bioengineering. Angiogenesis 17, 779–804 (2014).
doi: 10.1007/s10456-014-9440-7
pubmed: 25138280
pmcid: 4583126
Tayal, N. et al. Anti-angiogenic activity of columbin: A diterpenoid from Tinospora cordifolia. Int. J. Biol. Pharm. Allied Sci. 9, 540–552 (2020).
Kaur, A. et al. Novel biogenic silver nanoconjugates of Abrus precatorius seed extracts and their antiproliferative and antiangiogenic efficacies. Sci. Rep. 13, 13514 (2023).
doi: 10.1038/s41598-023-40079-8
pubmed: 37598190
pmcid: 10439965