BIOCHEMICAL RESPONSES OF THE DREISSENA POLYMORPHA FROM MUNICIPAL POND TO CAFFEINE, MICROPLASTICS, AND HEATING IN SINGLE AND COMBINED EXPOSURES
DOI: http://dx.doi.org/10.30970/sbi.1702.717
Abstract
Background. Pharmaceuticals have become the aquatic pollutants of growing concern. Caffeine is one of the most widely distributed in the surface waters among them. However, the environmentally relevant models of its effect, which include combined exposures with probable confounding factors, are unknown. Microplastics are a suspected vector that influences caffeine bioavailability. The temperature dependence of response, considering the increase of temperature in surface waters, can also be anticipated. The aim of this study was to analyze the input of caffeine, microplastics and elevated temperature into their combined effect on the zebra mussel Dreissena polymorpha (Pallas, 1771).
Materials and Methods. Molluscs were exposed to caffeine (Caf, 20.0 μg·L−1), microplastics (MP, 1 mg·L−1, 2 μm in size), or elevated temperature (T, 25 °C) in the single and combined (Mix- and MixT-) exposures for 14 days. The concentrations of metallothioneins, metallothioneins-bound zinc, total Zn and Cu concentration in the tissue, total glutathione level, antioxidant (superoxide dismutase) and metabolic (citrate synthase) enzymes activities, acid phosphatase activity as the lysosomal functionality marker were determined.
Results and Discussion. The decrease in Zn/Cu concentrations ratio in the soft tissues shared the common response in all exposures, reflecting the metal imbalance as the most sensitive marker. The MP-group was distinguished by the decrease in the levels of total Zn and extra lysosomal acid phosphatase activity, proving injury of Zn transportation and Zn-related enzyme activities. All other exposures (T-, Mix-, MixT-) caused citrate synthase and superoxide dismutase activation. Caf-related groups demonstrated the elevation of the levels of phosphatase lysosomal membrane-linked latency, metallothionein total protein and its apo-form. However, glutathione level was stable in all exposures.
Conclusion. These data revealed the adverse effect of MP and shared beneficial effects in the exposures that involved caffeine, which can be explained by the antioxidant activity of this substance. Exposure to elevated temperature partially alleviated the effect of caffeine in the mixture. Thus, the results indicate the importance of multi-stress exposures modeling, which allows the evaluation of environmentally realistic responces of an organism to xenobiotics.
Keywords
zebra mussel, pharmaceuticals, zinc, copper, acid phosphatase, oxidative stress
Full Text:
PDFReferences
| Aguirre-Martínez, G. V., Del Valls, T. A., & Martín-Díaz, M. L. (2013). Identification of biomarkers responsive to chronic exposure to pharmaceuticals in target tissues of Carcinus maenas. Marine Environmental Research, 87-88, 1-11. doi:10.1016/j.marenvres.2013.02.011 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Alfaro-Núñez, A., Astorga, D., Cáceres-Farías, L., Bastidas, L., Soto Villegas, C., Macay, K., & Christensen, J. H. (2021). Microplastic pollution in seawater and marine organisms across the Tropical Eastern Pacific and Galápagos. Scientific Reports, 11(1), 6424. doi:10.1038/s41598-021-85939-3 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Alomar, C., Sureda, A., Capó, X., Guijarro, B., Tejada, S., & Deudero, S. (2017). Microplastic ingestion by Mullus surmuletus Linnaeus, 1758 fish and its potential for causing oxidative stress. Environmental Research, 159, 135-142. doi:10.1016/j.envres.2017.07.043 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Atrián-Blasco, E., Santoro, A., Pountney, D. L., Meloni, G., Hureau, C., & Faller, P. (2017). Chemistry of mammalian metallothioneins and their interaction with amyloidogenic peptides and proteins. Chemical Society Reviews, 46(24), 7683-7693. doi:10.1039/c7cs00448f Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Barcelos, R. P., Souza, M. A., Amaral, G. P., Stefanello, S. T., Bresciani, G., Fighera, M. R., Soares, F. A. A., & Barbosa, N. V. (2014). Caffeine supplementation modulates oxidative stress markers in the liver of trained rats. Life Sciences, 96(1-2), 40-45. doi:10.1016/j.lfs.2013.12.002 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Baykan, U., Atli, G., & Canli, M. (2007). The effects of temperature and metal exposures on the profiles of metallothionein-like proteins in Oreochromis niloticus. Environmental Toxicology and Pharmacology, 23(1), 33-38. doi:10.1016/j.etap.2006.06.002 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Buico, A., Cassino, C., Dondero, F., Vergani, L., & Osella, D. (2008). Radical scavenging abilities of fish MT-A and mussel MT-10 metallothionein isoforms: an ESR study. Journal of Inorganic Biochemistry, 102(4), 921-927. doi:10.1016/j.jinorgbio.2007.12.012 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Cruz, D., Almeida, Â., Calisto, V., Esteves, V. I., Schneider, R. J., Wrona, F. J., Soares, A. M. V. M., Figueira, E., & Freitas, R. (2016). Caffeine impacts in the clam Ruditapes philippinarum: alterations on energy reserves, metabolic activity and oxidative stress biomarkers. Chemosphere, 160, 95-103. doi:10.1016/j.chemosphere.2016.06.068 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| De Marchi, L., Vieira, L. R., Intorre, L., Meucci, V., Battaglia, F., Pretti, C., Soares, A. M. V. M., & Freitas, R. (2022). Will extreme weather events influence the toxic impacts of caffeine in coastal systems? Comparison between two widely used bioindicator species. Chemosphere, 297, 134069. doi:10.1016/j.chemosphere.2022.134069 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| de Souza, D. M., Martins, Á. C., Jensen, L., Wasielesky, W., Monserrat, J. M., & Garcia, L. de O. (2013). Effect of temperature on antioxidant enzymatic activity in the Pacific white shrimp Litopenaeus vannameiin a BFT (Biofloc technology) system. Marine and Freshwater Behaviour and Physiology, 47(1), 1-10. doi:10.1080/10236244.2013.857476 Crossref ● Google Scholar | ||||
| ||||
| Farkas, A., Ács, A., Vehovszky, Á., Falfusynska, H., Stoliar, O., Specziár, A., & Győri, J. (2017). Interspecies comparison of selected pollution biomarkers in dreissenid spp. inhabiting pristine and moderately polluted sites. Science of The Total Environment, 599-600, 760-770. doi:10.1016/j.scitotenv.2017.05.033 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Flynn, E. E., Bjelde, B. E., Miller, N. A., & Todgham, A. E. (2015). Ocean acidification exerts negative effects during warming conditions in a developing Antarctic fish. Conservation Physiology, 3(1), cov033. doi:10.1093/conphys/cov033 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Fried, R. (1975). Enzymatic and non-enzymatic assay of superoxide dismutase. Biochimie, 57(5), 657-660. doi:10.1016/s0300-9084(75)80147-7 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Gaikwad, Y. B., Gaikwad, S. M., & Bhawane, G. P. (2010). Effect of induced oxidative stress and herbal extracts on acid phosphatase activity in lysosomal and microsomal fractions of midgut tissue of the silkworm, Bombyx mori. Journal of Insect Science, 10(1), 113. doi:10.1673/031.010.11301 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Giráldez-Costas, V., Del Coso, J., Mañas, A., & Salinero, J. J. (2023). The long way to establish the ergogenic effect of caffeine on strength performance: an overview review. Nutrients, 15(5), 1178. doi:10.3390/nu15051178 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Griffith, O. W. (1980). Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry, 106, 207-212. doi:10.1016/0003-2697(80)90139-6 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Hamm, T., & Lenz, M. (2021). Negative impacts of realistic doses of spherical and irregular microplastics emerged late during a 42 weeks-long exposure experiment with blue mussels. Science of The Total Environment, 778(15), 146088. doi:10.1016/j.scitotenv.2021.146088 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Intergovernmental Panel for Global Climate Change (IPCC). (2013). Retrieved from http://www.ipcc.ch | ||||
| ||||
| Jonsson, C. M., Paraiba, L. C., & Aoyama, H. (2009). Metals and linear alkylbenzene sulphonate as inhibitors of the algae Pseudokirchneriella subcapitata acid phosphatase activity. Ecotoxicology, 18(5), 610-619. doi:10.1007/s10646-009-0319-0 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Kazi Tani, L. S., Gourlan, A. T., Dennouni-Medjati, N., Telouk, P., Dali-Sahi, M., Harek, Y., Sun, Q., Hackler, J., Belhadj, M., Schomburg, L., & Charlet, L. (2021). Copper isotopes and copper to zinc ratio as possible biomarkers for thyroid cancer. Frontiers in Medicine, 8, 698167. doi:10.3389/fmed.2021.698167 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Khoma, V. V., Gnatyshyna, L. L., Martinyuk, V. V., Mackiv, T. R., Mishchuk, N. Y., & Stoliar, O. B. (2020). Metallothioneins contribution to the response of bivalve mollusk to xenobiotics. The Ukrainian Biochemical Journal, 92(5), 87-96. doi:10.15407/ubj92.05.087 Crossref ● Google Scholar | ||||
| ||||
| Khoma, V., Gnatyshyna, L., Martyniuk, V., Mackiv, T., Mishchenko, L., Manusadzianas, L., & Stoliar, O. (2021). Common and particular biochemical responses of Unio tumidus to herbicide, pharmaceuticals and their combined exposure with heating. Ecotoxicology and Environmental Safety, 208(9), 111695. doi:10.1016/j.ecoenv.2020.111695 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Kim, K. R., Park, S. E., Hong, J. Y., Koh, J. Y., Cho, D. H., Hwang, J. J., & Kim, Y. H. (2022). Zinc enhances autophagic flux and lysosomal function through transcription factor EB activation and V-ATPase assembly. Frontiers in cellular neuroscience, 16, 895750. doi:10.3389/fncel.2022.895750 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Lacoue-Labarthe, T., Le Bihan, E., Borg, D., Koueta, N., & Bustamante, P. (2010). Acid phosphatase and cathepsin activity in cuttlefish (Sepia officinalis) eggs: the effects of Ag, Cd, and Cu exposure. ICES Journal of Marine Science, 67, 1517-1523. doi:10.1093/icesjms/fsq044 Crossref ● Google Scholar | ||||
| ||||
| Lasee, S., Mauricio, J., Thompson, W. A., Karnjanapiboonwong, A., Kasumba, J., Subbiah, S., Morse, A. N., & Anderson, T. A. (2017). Microplastics in a freshwater environment receiving treated wastewater effluent. Integrated Environmental Assessment and Management, 13, 528-532. doi:10.1002/ieam.1915 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Lesser, M. P., & Kruse, V. A. (2004). Seasonal temperature compensation in the horse mussel, Modiolus modiolus: metabolic enzymes, oxidative stress and heat shock proteins. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 137(3), 495-504. doi:10.1016/j.cbpb.2003.10.022 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Li, J., Lusher, A. L., Rotchell, J. M., Deudero, S., Turra, A., Bråte, I. L. N., Sun, C., Shahadat Hossain, M., Li, Q., Kolandhasamy, P., & Shi, H. (2019). Using mussel as a global bioindicator of coastal microplastic pollution. Environmental Pollution, 244, 522-533. doi:10.1016/j.envpol.2018.10.032 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Li, S., Wen, J., He, B., Wang, J., Hu, X., & Liu, J. (2020). Occurrence of caffeine in the freshwater environment: implications for ecopharmacovigilance. Environmental Pollution, 263, 114371. doi:10.1016/j.envpol.2020.114371 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Lia, S., Heb, B., Liua, J. W. J., & Hu, X. (2020). Risks of caffeine residues in the environment: necessity for a targeted ecopharmacovigilance program. Chemosphere, 243, 125343. doi:10.1016/j.chemosphere.2019.125343 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Lin, S., & Steichen Jr, D. J. (1994). A method for determining the stability of lysosomal membranes in the digestive cells of Mytilus edulis. Marine Ecology Progress Series, 115, 237-241. doi:10.3354/meps115237 Crossref ● Google Scholar | ||||
| ||||
| Lowry, O. H., Rosebroungh, H. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193(1), 265-275. doi:10.1016/S0021-9258(19)52451-6 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Magni, S., Gagné, F., André, C., Della Torre, C., Auclair, J., Hanana, H., Parenti, C. C., Bonasoro, F., & Binelli, A. (2018). Evaluation of uptake and chronic toxicity of virgin polystyrene microbeads in freshwater zebra mussel Dreissena polymorpha (Mollusca: Bivalvia). Science of The Total Environment, 631-632, 778-788. doi:10.1016/j.scitotenv.2018.03.075 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Marczenko, Z., & Balcerzak, M. (2000). Copper. In E. Kloczko (Ed.). Separation, preconcentration and spectrophotometry in inorganic analysis (pp. 182-183). Elsevier. doi:10.1016/s0926-4345(00)80083-8 Crossref ● Google Scholar | ||||
| ||||
| Martinho, S. D., Fernandes, V. C., Figueiredo, S. A., & Delerue-Matos, C. (2022). Microplastic pollution focused on sources, distribution, contaminant interactions, analytical methods, and wastewater removal strategies: a review. International Journal of Environmental Research and Public Health, 19(9), 5610. doi:10.3390/ijerph19095610 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Martyniuk, V. V. (2022). Accumulation of microplastics in the bivalve mollusc Unio tumidus under experimental and field exposures. Studia Biologica, 16(4), 33-44. doi:10.30970/sbi.1604.694 Crossref ● Google Scholar | ||||
| ||||
| Martyniuk, V., Khoma, V., Matskiv, T., Baranovsky, V., Orlova-Hudim, K., Gylytė, B., Symchak, R., Matciuk, O., Gnatyshyna, L., Manusadžianas, L., & Stoliar, O. (2022a). Indication of the impact of environmental stress on the responses of the bivalve mollusk Unio tumidus to ibuprofen and microplastics based on biomarkers of reductive stress and apoptosis. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 261, 109425. doi:10.1016/j.cbpc.2022.109425 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Martyniuk, V., Gylytė, B., Matskiv, T., Khoma, V., Tulaidan, H., Gnatyshyna, L., Orlova-Hudim, K., Manusadžianas, L., & Stoliar, O. (2022b). Stress responses of bivalve mollusc Unio tumidus from two areas to ibuprofen, microplastic and their mixture. Ecotoxicology, 31(9), 1369-1381. doi:10.1007/s10646-022-02594-8 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Martyniuk, V., Khoma, V., Matskiv, T., Yunko, K., Gnatyshyna, L., Stoliar, O., & Faggio, C. (2023). Combined effect of microplastic, salinomycin and heating on Unio tumidus. Environmental Toxicology and Pharmacology, 98, 104068. doi:10.1016/j.etap.2023.104068 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Matskiv, T. R., Lytkin, D. V., Shebeko, S. K., Khoma, V. V., Martyniuk, V. V., Gnatyshyna, L. L., & Stoliar, O. B. (2021). Metallothioneins involment in the pathogenesis of synovial tissue inflammation in rats with acute gonarthritis. The Ukrainian Biochemical Journal, 93(5), 63-71. doi:10.15407/ubj93.05.063 Crossref | ||||
| ||||
| McConell, G. K., Ng, G. P. Y., Phillips, M., Ruan, Z., Macaulay, S. L., & Wadley, G. D. (2010). Central role of nitric oxide synthase in AICAR and caffeine-induced mitochondrial biogenesis in L6 myocytes. Journal of Applied Physiology, 108(3), 589-595. doi:10.1152/japplphysiol.00377.2009 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Patel, S., & Patel, B. (1985). Effect of environmental parameters on lysosomal marker enzymes in the tropical blood clam Anadara granosa. Marine Biology, 85, 245-252. doi:10.1007/bf00393244 Crossref ● Google Scholar | ||||
| ||||
| Peterson, R. E., & Bollier, M. E. (1955). Spectrophotometric determination of serum copper with biscyclohexanoneoxalyldihydrazone. Analytical Chemistry, 27(7), 1195-1197. doi:10.1021/ac60103a054 Crossref ● Google Scholar | ||||
| ||||
| Prinz, N., & Korez, Š. (2020). Understanding how microplastics affect marine biota on the cellular level is important for assessing ecosystem function: a review. In S. Jungblut, V. Liebich, & M. Bode-Dalby (Eds.), YOUMARES 9 - the oceans: our research, our future: proceedings of the 2018 conference for YOUng MArine RESearcher in Oldenburg, Germany (pp. 101-120). Springer International Publishing. doi:10.1007/978-3-030-20389-4_6 Crossref ● Google Scholar | ||||
| ||||
| Rahman, M. S., & Rahman, M. S. (2021). Effects of elevated temperature on prooxidant-antioxidant homeostasis and redox status in the American oyster: signaling pathways of cellular apoptosis during heat stress. Environmental Research, 196, 110428. doi:10.1016/j.envres.2020.110428 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Revel, M., Yakovenko, N., Caley, T., Guillet, C., Châtel, A., & Mouneyrac, C. (2018). Accumulation and immunotoxicity of microplastics in the estuarine worm Hediste diversicolor in environmentally relevant conditions of exposure. Environmental Science and Pollution Research, 27(4), 3574-3583. doi:10.1007/s11356-018-3497-6 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Saad, A. A., El-Sikaily, A., & Kassem, H. (2016). Metallothionein and glutathione content as biomarkers of metal pollution in mussels and local fishermen in Abu Qir Bay, Egypt. Journal of Health and Pollution, 6(12), 50-60. doi:10.5696/2156-9614-6-12.50 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Scherer, C., Weber, A., Stock, F., Vurusic, S., Egerci, H., Kochleus, C., Arendt, N., Foeldi, C., Dierkes, G., Wagner, M., Brennholt, N., & Reifferscheid, G. (2020). Comparative assessment of microplastics in water and sediment of a large European river. Science of The Total Environment, 738, 139866. doi:10.1016/j.scitotenv.2020.139866 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Schlater, A., Jowlowsly, S., Zupetz, J., Mayola, N., & Butterfield, K. (2022). The impact of varying caffeine-induced contractile activity on metabolic enzyme activity. The FASEB Journal, 36(S1). doi:10.1096/fasebj.2022.36.S1.R4554 Crossref ● Google Scholar | ||||
| ||||
| Schneider, T., Caviezel, D., Ayata, C. K., Kiss, C., Niess, J. H., & Hruz, P. (2020). The copper/zinc ratio correlates with markers of disease activity in patients with inflammatory bowel disease. Crohn's & Colitis 360, 2(1), otaa001. doi:10.1093/crocol/otaa001 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Serafim, M. A., Company, R. M., Bebianno, M. J., & Langston, W. J. (2002). Effect of temperature and size on metallothionein synthesis in the gill of Mytilus galloprovincialis exposed to cadmium. Marine Environmental Research, 54, 361-365. doi:10.1016/s0141-1136(02)00121-6 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Serra, R., Isani, G., Tramontano, G., & Carpene, E. (1999). Seasonal dependence of cadmium accumulation and Cd-binding proteins in Mytilus galloprovincialis exposed to cadmium. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 123, 165-174. doi:10.1016/s0742-8413(99)00024-9 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Sewwandi, M., Wijesekara, H., Rajapaksha, A. U., Soysa, H. S. M., & Vithanage, M. (2022). Adsorption of caffeine to microplastics in organic matter-rich aqueous media. International Symposium on Sustainable Urban Environments (ISSUE). University of Petroleum and Energy Studies. Retrieved from https://www.researchgate.net/publication/365231691_Adsorption_of_caffeine_to_microplastics_in_organic_matter-rich_aqueous_media | ||||
| ||||
| Vaughan, R. A., Garcia-Smith, R., Bisoffi, M., Trujillo, K. A., & Conn, C. A. (2012). Effects of caffeine on metabolism and mitochondria biogenesis in rhabdomyosarcoma cells compared with 2,4-dinitrophenol. Nutrition and Metabolic Insights, 5, 59-70. doi:10.4137/nmi.s10233 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Viarengo, A., Ponzano, E., Dondero, F., & Fabbri, R. (1997). A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Marine Environmental Research, 44(1), 69-84. doi:10.1016/s0141-1136(96)00103-1 Crossref ● Google Scholar | ||||
| ||||
| Wang, J., Niu, Y., Zhang, C., & Chen, Y. (2018). A micro-plate colorimetric assay for rapid determination of trace zinc in animal feed, pet food and drinking water by ion masking and statistical partitioning correction. Food Chemistry, 245, 337-345. doi:10.1016/j.foodchem.2017.10.054 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Wang, W., Zhang, J., Qiu, Z., Cui, Z., Li, N., Li, X., Wang, Y., Zhang, H., & Zhao, C. (2022). Effects of polyethylene microplastics on cell membranes: a combined study of experiments and molecular dynamics simulations. Journal of Hazardous Materials, 429(5), 128323. doi:10.1016/j.jhazmat.2022.128323 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Wilkinson, J. L., Boxall, A. B. A., Kolpin, D. W., Leung, K. M. Y., Lai, R. W. S., Galbán-Malagón, C., … Teta, C. (2022). Pharmaceutical pollution of the world's rivers. Proceedings of the National Academy of Sciences, 119(8). doi:10.1073/pnas.2113947119 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Zhang, Z. Y., Clemens, J. C., Schubert, H. L., Stuckey, J. A., Fischer, M. W., Hume, D. M., Saper, M. A., & Dixon, J. E. (1992). Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. Journal of Biological Chemistry, 267(33), 23759-23766. doi:10.1016/s0021-9258(18)35903-9 Crossref ● PubMed ● Google Scholar | ||||
Refbacks
- There are currently no refbacks.
Copyright (c) 2023 Tetyana Matskiv, Oksana Stoliar
This work is licensed under a Creative Commons Attribution 4.0 International License.