Abstract
The binding interaction between emerging pollutant polyvinyl chloride microplastics (PVC MPs) and bovine serum albumin (BSA) was studied by fluorescence spectroscopy, resonance scattering spectroscopy (RLS), UV-visible (UV-vis) absorption spectroscopy, circular dichroism (CD), and Fourier transform infrared (FT-IR) spectroscopy under simulative physiological conditions. Fluorescence results revealed that the fluorescence quenching of BSA induced by PVC MPs was originated from the formation of BSA-PVC complex in static quenching mode. According to Stern-Volmer equation, the binding constants (Ka) between PVC MPs and BSA at different temperatures were obtained, and the number of binding sites was 1.62. The thermodynamic parameters, enthalpy change (ΔH), entropy change (ΔS), and free energy change (ΔG) were calculated to be − 41.77 kJ mol-1, 43.17 J mol-1 K-1, and − 54.63 kJ mol-1 via Van’t Hoff equation, indicating electrostatic interaction played a key role in the formation of BSA-PVC complex spontaneously. In addition, the alterations of microenvironment and secondary structure in BSA induced by PVC MPs were further confirmed by synchronous fluorescence spectra, UV-vis, FT-IR, and CD. This work not only provides further information for better understanding the binding interaction of PVC MPs with BSA, but also elucidates the potential biological toxicity of MPs at a molecular level.
Similar content being viewed by others
Data availability
All data generated or analyzed in this study are included in this published article and its supplementary materials.
References
Avio CG, Gorbi S, Milan M, Benedetti M, Fattorini D, d’Errico G, Pauletto M, Bargelloni L, Regoli F (2015) Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ Pollut 198:211–222. https://doi.org/10.1016/j.envpol.2014.12.021
Browne M, Dissanayake A, Galloway T, Lowe D, Thompson RC (2008) Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L.). Environ Sci Technol 42:5026–5031. https://doi.org/10.1021/es800249a
Carter DC, Ho JX (1994) Structure of serum albumin. Adv Protein Chem 45:153–203. https://doi.org/10.1016/S0065-2911(08)60174-5
Cole M, Lindeque P, Fileman E, Halsband C, Galloway TS (2015) The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ Sci Technol 49:1130–1137. https://doi.org/10.1021/es504525u
Cox KD, Covernton GA, Davies HL, Dower JF, Juanes F, Dudas SE (2019) Human consumption of microplastics. Environ Sci Technol 53:7068–7074. https://doi.org/10.1021/acs.est.9b01517
Cozar A, Echevarria F, Gonzalez-Gordillo JI, Irigoien X, Ubeda B, Hernandez-Leon S, Palma AT, Navarro S, Garcia-de-Lomas J, Ruiz A, Fernandez-de-Puelles ML, Duarte CM (2014) Plastic debris in the open ocean. Proc Nat Acad Sci USA 111:10239–10244. https://doi.org/10.1073/pnas.1314705111
Curry S, Mandelkow H, Brick P, Franks N (1998) Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites. Nat Struct Mol Biol 5:827–835. https://doi.org/10.1038/1869
De Jonge HR (1973) Toxicity of tetracyclines in rat-small-intestinal epithelium and liver. Biochem Pharmacol 22:2659–2677. https://doi.org/10.1016/0006-2952(73)90127-5
Derraik JGB (2002) The pollution of the marine environment by plastic debris: a review. Mar Pollut Bull 44:842–852. https://doi.org/10.1016/S0025-326X(02)00220-5
Ding JF, Jiang FH, Li JX, Wang ZX, Sun CJ, Wang ZY, Fu L, Ding NXY, He CF (2019) Microplastics in the coral reef systems from Xisha islands of South China Sea. Environ Sci Technol 53:8036–8046. https://doi.org/10.1021/acs.est.9b01452
Gao FL, Li JX, Sun CJ, Zhang LT, Jiang FH, Cao W, Zheng L (2019) Study on the capability and characteristics of heavy metals enriched on microplastics in marine environment. Mar Pollut Bull 144:61–67. https://doi.org/10.1016/j.marpolbul.2019.04.039
Garrett NL, Lalatsa A, Uchegbu I, Schätzlein A, Moger J (2012) Exploring uptake mechanisms of oral nanomedicines using multimodal nonlinear optical microscopy. J Biophotonics 5:458–468. https://doi.org/10.1002/jbio.201200006
Geyer R, Jambeck JR, Law KL (2017) Production, use, and fate of all plastics ever made. Sci Adv 3:25–29. https://doi.org/10.1126/sciadv.1700782
Graham ER, Thompson JT (2009) Deposit- and suspension-feeding sea cucumbers (Echinodermata) ingest plastic fragments. J Exp Mar Biol Ecol 368:22–29. https://doi.org/10.1016/j.jembe.2008.09.007
Hussain N, Jaitley V, Florence AT (2001) Recent advances in the understanding of uptake of microparticulates across the gastrointestinal lymphatics. Adv Drug Deliv Rev 50:107–142. https://doi.org/10.1016/S0169-409X(01)00152-1
Jhonsi MA, Renganathan R (2010) Investigations on the photoinduced interaction of water soluble thioglycolic acid (TGA) capped CdTe quantum dots with certain porphyrins. J Colloid Interf Sci 344:596–602. https://doi.org/10.1016/j.jcis.2010.01.022
Jin YX, Xia JZ, Pan ZH, Yang JJ, Wang WC, Fu ZW (2018) Polystyrene microplastics induce microbiota dysbiosis and inflammation in the gut of adult zebrafish. Environ Pollut 235:322–329. https://doi.org/10.1016/j.envpol.2017.12.088
Ju P, Fan H, Liu T, Cui L, Ai SY (2011) Probing the interaction of flower-like CdSe nanostructure particles targeted to bovine serum albumin using spectroscopic techniques. J Lumin 131:1724–1730. https://doi.org/10.1016/j.jlumin.2011.03.070
Kathiravan A, Renganathan R, Anandan S (2009) Interaction of colloidal AgTiO2 nanoparticles with bovine serum albumin. Polyhedron 28:157–161. https://doi.org/10.1016/j.poly.2008.09.023
Lakowicz JR, Weber G (1973) Quenching of fluorescence by oxygen. Probe for structural fluctuations in macromolecules. Biochemistry 12:4161–4170. https://doi.org/10.1021/bi00745a020
Law KL, Thompson RC (2014) Microplastics in the seas. Science 345:144–145. https://doi.org/10.1126/science.1254065
Lehrer SS (1971) Solute perturbation of protein fluorescence. Quenching of the tryptophyl fluorescence of model compounds and of lysozyme by iodide ion. Biochemistry 10:3254–3263. https://doi.org/10.1021/bi00793a015
Mao HB, Yang TL, Cremer PS (2002) Design and characterization of immobilized enzymes in microfluidic systems. Anal Chem 74:379–385. https://doi.org/10.1021/ac010822u
Marty A, Boiret M, Deumie M (1986) How to illustrate ligand-protein binding in a class experiment: an elementary fluorescent assay. J Chem Educ 63:365–366. https://doi.org/10.1021/ed063p365
Matyus L, Szollosi J, Jenei A (2006) Steady-state fluorescence quenching applications for studying protein structure and dynamics. J Photochem Photobiol B Bio 83:223–236. https://doi.org/10.1016/j.jphotobiol.2005.12.017
Moriyama Y, Ohta D, Hachiya K, Mitsui Y, Takeda K (1996) Fluorescence behavior of tryptophan residues of bovine and human serum albumins in ionic surfactant solutions: a comparative study of the two and one tryptophan (s) of bovine and human albumins. J Protein Chem 15:265–272. https://doi.org/10.1007/BF01887115
Nobre CR, Santana MFM, Maluf A, Cortez FS, Cesar A, Pereira CDS, Turra A (2015) Assessment of microplastic toxicity to embryonic development of the sea urchin Lytechinus variegatus (Echinodermata: Echinoidea). Mar Pollut Bull 92:99–104. https://doi.org/10.1016/j.marpolbul.2014.12.050
Pan XR, Qin PF, Liu RT, Wang J (2011) Characterizing the interaction between tartrazine and two serum albumins by a hybrid spectroscopic approach. J Agric Food Chem 59:6650–6656. https://doi.org/10.1021/jf200907x
Papadopoulou A, Green RJ, Frazier RA (2005) Interaction of flavonoids with bovine serum albumin: a fluorescence quenching study. J Agric Food Chem 53:158–163. https://doi.org/10.1007/s00216-003-2017-8
Pawar S, Joshi R, Ottoor D (2018) Spectroscopic and molecular docking study to understand the binding interaction of rosiglitazone with bovine serum albumin in presence of valsartan. J Lumin 197:200–210. https://doi.org/10.1016/j.jlumin.2018.01.017
Poureshghi F, Ghandforoushan P, Safarnejad A, Soltani S (2017) Interaction of an antiepileptic drug, lamotrigine with human serum albumin (HSA): application of spectroscopic techniques and molecular modeling methods. J Photochem Photobiol B Bio 166:87–192. https://doi.org/10.1016/j.jphotobiol.2016.09.046
Ross PD, Subramanian S (1981) Thermodynamics of protein association reactions: forces contributing to stability. Biochemistry 20:3096–3102. https://doi.org/10.1021/bi00514a017
Roy S, Nandi RK, Ganai S, Majumdar KC, Das TK (2017) Binding interaction of phosphorus heterocycles with bovine serum albumin: a biochemical study. J Pharm Anal 7:9–26. https://doi.org/10.1016/j.jpha.2016.05.009
Siddiqui GA, Siddiqi MK, Khan RH, Naeem A (2018) Probing the binding of phenolic aldehyde vanillin with bovine serum albumin: evidence from spectroscopic and docking approach. Spectrochim Acta A Mol Biomol Spectrosc 203:40–47. https://doi.org/10.1016/j.saa.2018.05.023
Sighicelli M, Pietrelli L, Lecce F, Iannilli V, Falconieri M, Coscia L, Di Vito S, Nuglio S, Zampetti G (2018) Microplastic pollution in the surface waters of Italian Subalpine Lakes. Environ Pollut 236:645–651. https://doi.org/10.1016/j.envpol.2018.02.008
Sussarellu R, Suquet M, Thomas Y, Lambert C, Fabioux C, Pernet MEJ, Goïc NL, Quillien V, Mingant C, Epelboin Y, Corporeau C, Guyomarch J, Robbens J, Paul-Pont I, Soudant P, Huvet A (2016) Oyster reproduction is affected by exposure to polystyrene microplastics. Proc Nat Acad Sci USA 113:2430–2435. https://doi.org/10.1073/pnas.1519019113
Tedesco AC, Oliveira DM, Lacava ZGM, Azevedo RB, Lima ECD, Gansau C, Buske N, Morais PC (2003) Determination of binding constant Kb of biocompatible, ferrite-based magnetic fluids to serum albumin. J Appl Phys 93:6704–6706. https://doi.org/10.1063/1.1555154
Teng Y, Liu RT, Li C, Xia Q, Zhang PJ (2011) The interaction between 4-aminoantipyrine and bovine serum albumin: multiple spectroscopic and molecular docking investigations. J Hazard Mater 190:574–581. https://doi.org/10.1016/j.jhazmat.2011.03.084
Van Cauwenberghe L, Janssen CR (2014) Microplastics in bivalves cultured for human consumption. Environ Pollut 193:65–70. https://doi.org/10.1016/j.envpol.2014.06.010
Volkheimer G (1975) Hematogenous dissemination of ingested polyvinyl chloride particles. Ann N Y Acad Sci 246:164–171. https://doi.org/10.1111/j.1749-6632.1975.tb51092.x
von Moos N, Burkhardt-Holm P, Koehler A (2012) Uptake and effects of microplastics on cells and tissues of the blue mussel Mytilus edulis L. after experimental exposure. Environ Sci Technol 46:11327–11335. https://doi.org/10.1021/es302332w
Walkinshaw C, Lindeque PK, Thompson R, Tolhurst T, Cole M (2020) Microplastics and seafood: lower trophic organisms at highest risk of contamination. Ecotox Environ Safe 190:110066. https://doi.org/10.1016/j.ecoenv.2019.110066
Welden NAC, Cowie PR (2016) Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus. Environ Pollut 218:895–900. https://doi.org/10.1016/j.envpol.2016.08.020
Wright SL, Thompson RC, Galloway TS (2013) The physical impacts of microplastics on marine organisms: a review. Environ Pollut 178:483–492. https://doi.org/10.1016/j.envpol.2013.02.031
Yang QQ, Liang JG, Han HY (2009) Probing the interaction of magnetic iron oxide nanoparticles with bovine serum albumin by spectroscopic techniques. J Phys Chem B 113:10454–10458. https://doi.org/10.1021/jp904004w
Yu MY, Ding ZS, Jiang FS, Ding XH, Sun JY, Chen SH, Lv GY (2011) Analysis of binding interaction between pegylated puerarin and bovine serum albumin by spectroscopic methods and dynamic light scattering. Spectrochim Acta A Mol Biomol Spectrosc 83:453–460. https://doi.org/10.1016/j.saa.2011.08.065
Yuan T, Weljie AM, Vogel HJ (1998) Tryptophan fluorescence quenching by methionine and selenomethionine residues of calmodulin: orientation of peptide and protein binding. Biochemistry 37:3187–3195. https://doi.org/10.1021/bi9716579
Zhang YZ, Zhou B, Zhang XP, Huang P, Li CH, Liu Y (2009) Interaction of malachite green with bovine serum albumin: determination of the binding mechanism and binding site by spectroscopic methods. J Hazard Mater 163:1345–1352. https://doi.org/10.1016/j.jhazmat.2008.07.132
Zhao XC, Liu RT, Chi ZX, Teng Y, Qin PF (2010) New insights into the behavior of bovine serum albumin adsorbed onto carbon nanotubes: comprehensive spectroscopic studies. J Phys Chem B 114:5625–5631. https://doi.org/10.1021/jp100903x
Zhu LX, Zhao SY, Bittarc TB, Stubbinsd A, Li DJ (2020) Photochemical dissolution of buoyant microplastics to dissolved organic carbon: rates and microbial impacts. J Hazard Mater 383:121065. https://doi.org/10.1016/j.jhazmat.2019.121065
Funding
This work was supported by the Basic Scientific Fund for National Public Research Institutes of China (2020S02, 2019Y03, and 2017Q09), Open Fund of Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao) (LMEES201802), National Natural Science Foundation of China (41806201), the Aoshan Scientific and Technological Innovation Project Financially Supported by Pilot National Laboratory for Marine Science and Technology (Qingdao) (2016ASKJ14), and Construction and Operation of Test and Technical Support System for Natural Resources Investigation and Evaluation.
Author information
Authors and Affiliations
Contributions
Peng Ju: Conceptualization, methodology, validation, formal analysis, data curation, writing-original draft, writing—review & editing, visualization, supervision, project administration, funding acquisition; Yu Zhang: Methodology, software, formal analysis, investigation, writing—original draft; Jinfeng Ding: Methodology, formal analysis, investigation; Yifan Zheng: Formal analysis, investigation; Shuai Wang: Resources, funding acquisition; Fenghua Jiang: Resources, data curation, writing—review & editing; Chengjun Sun: Validation, data curation, writing—review & editing, supervision, project administration, funding acquisition.
Corresponding authors
Ethics declarations
Competing interests
The authors declare that they have no conflict of interest.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 669 kb)
Rights and permissions
About this article
Cite this article
Ju, P., Zhang, Y., Ding, J. et al. New insights into the toxic interactions of polyvinyl chloride microplastics with bovine serum albumin. Environ Sci Pollut Res 28, 5520–5531 (2021). https://doi.org/10.1007/s11356-020-10707-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-10707-1