Abstract
Using equilibrium dialysis, isothermal titration calorimetry (ITC) and circular dichroism (CD), the interactions of perfluorooctanoic acid (PFOA) and lysozyme were investigated under normal human physiological conditions, i.e., at pH 4.40, 6.00 and 7.40 at 37°C in 0.15 M electrolyte. A simple and rapid spectrophotometric method was developed for determining PFOA concentrations. Interactions between PFOA and lysozyme were found to result from non-specific non-covalent bonds—F/N and F/O affinity, ion-pair attraction, hydrogen bond, hydrophobic interaction and van der Waals force—and were affected by chemical adsorption to monolayers. The results indicated that binding of PFOA altered the secondary structure and activity of lysozyme. This work provides a useful experimental strategy for research into the enzyme toxicity of organic chemicals, e.g., food additives and organic contaminants, and it may help to elucidate the molecular toxicology of human health risks.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbott BD, Wolf CJ, Schmid JE et al (2007) Perfluorooctanoic acid-induced developmental toxicity in the mouse is dependent on expression of peroxisome proliferator-activated receptor-alpha. Toxicol Sci 98:571–581
Ajloo D, Behnam H, Saboury AA et al (2007) Thermodynamic and structural studies on the human serum albumin in the presence of a polyoxometalate. Bull Korean Chem Soc 28:733–736
Almogren A, Furtado PB, Sun Z et al (2006) Purification, properties and extended solution structure of the complex formed between human immunoglobulin a1 and human serum albumin by scattering and ultracentrifugation. J Mol Biol 356:413–431
Blake CCF, Koenig DF, Mair GA et al (1965) Structure of hen egg-white lysozyme, a three-dimensional Fourier synthesis at 2-A resolution. Nature 206:757–761
Brazeau BJ, Johnson BJ, Wilmot CM (2004) Copper-containing amine oxidases. Biogenesis and catalysis; a structural perspective. Arch Biochem Biophys 428:22–31
Calafat AM, Kuklenyik Z, Reidy JA et al (2007) Serum concentrations of 11 polyfluoroalkyl compounds in the US population, data from the national health and nutrition examination survey (NHANES). Environ Sci Technol 41:2237–2242
Collins MD, Hummer G, Quillin ML et al (2005) Cooperative water filling of a nonpolar protein cavity observed by high-pressure crystallography and simulation. Proc Natl Acad Sci USA 102:16668–16671
Cooper A, McAlpine A, Stockley PG (1994) Calorimetric studies of the energetics of protein–DNA interactions in the E. coli methionine repressor (MetJ) system. FEBS Lett 348:41–45
Cunningham FE, Lineweaver H (1967) Inactivation of lysozyme by native ovalbumin. Poultry Sci 46:1471–1477
Derham BK, Harding JJ (2000) The effect of the presence of globular proteins and elongated polymers on enzyme activity. Biochim Biophys Acta 1764:1000–1006
Durek T, Torbeev VY, Kent SBH (2007) Convergent chemical synthesis and high-resolution X-ray structure of human lysozyme. Proc Natl Acad Sci USA 104:4846–4851
Gao HW, Qian Y, Hu ZJ (2004) Tetraiodophenolsuphonphthalein as a spectral substitute to characterize the complexation between cationic and anionic surfactant. J Colloid Interf Sci 279:244–252
Gao HW, Zhao JF, Yang QZ et al (2006) Non-covalent interaction of 2′,4′,5′,7′-tetrabromo-4,5,6,7-tetrachlorofluorescein with proteins and its application. Proteomics 6:5140–5151
Gao HW, Liu XH, Qiu Z et al. (2008) Non-covalent binding of azo compound to peptide chain resulting in the conformational change of protein: interactions of biebrich scarlet and naphthochrome green with four model proteins. Amino Acids 35. doi: 10.1007/s00726-008-0058-1
Giaginis C, Gatzidou E, Theocharis S (2006) DNA repair systems as targets of cadmium toxicity. Toxical Appl Pharmacol 213:282–290
Housaindokht MR, Bahrololoom M, Tarighatpoor S et al (2002) An approach based on diffusion to study ligand–macromolecule interaction. Acta Biochim Polonica 49:703–707
Hu HY, Xu GJ (1999) Structural transformation of proteins. Prog Biochem Biophys 1:9–12
Hunter TM, McNae IW, Liang XY et al (2005) Protein recognition of macrocycles, binding of anti-HIV metallocyclams to lysozyme. Proc Natl Acad Sci USA 102:2288–2292
Kamiya M, Torigoe H, Shindo H (1996) Temperature dependence and sequence specificity of DNA triplex formation, an analysis using isothermal titration calorimetry. J Am Chem Soc 118:4532–4538
Karrman A, Ericson I, van BB et al (2007) Exposure of perfluorinated chemicals through lactation, Levels of matched human milk and serum and a temporal trend, 1996–2004, in Sweden. Environ Health Perspect 115:226–230
Kraut DA, Carroll KS, Herschlag D (2003) Challenges in enzyme mechanism and energetics. Rev Biochem 72:517–571
Lau C, Butenhoff JL, Rogers JM (2004) The developmental toxicity of perfluoroalkyl acids and their derivatives. Toxicol Appl Pharmacol 15:231–241
Liu ST, Sugimoto T, Azakami H et al (2000) Lipophilization of lysozyme by short and middle chain fatty acids. J Agric Food Chem 48:265–269
Luque I, Todd MJ, Gomez J (1998) Molecular basis of resistance to HIV-1 protease inhibition, a plausible hypothesis. Biochemistry 37:5791–5797
Maestri L, Negri S, Ferrari M et al (2006) Determination of perfluorooctanoic acid and perfluorooctanesulfonate in human tissues by liquid chromatography/single quadrupole mass spectrometry. Mass Spectrom 20:2728–2734
Maras M, Vanparys C, Muylle F et al (2006) Estrogen-like properties of fluorotelomer alcohols as revealed by MCF-7 breast cancer cell proliferation. Environ Health Perspect 114:100–105
Marolia KZ, D’Souza SF (1999) Enhancement in the lysozyme activity of the hen egg white foam matrix by cross-linking in the presence of N-acetyl glucosamine. J Biochem Biophys Methods 39:115–117
Martin MT, Brennan RJ, Hu WY et al (2007) Toxicogenomic study of triazole fungicides and perfluoroalkyl acids in rat livers predicts toxicity and categorizes chemicals based on mechanisms of toxicity. Toxicol Sci 97:595–613
Miller CM, Szegedi SS, Garrow TA (2005) Conformation-dependent inactivation of human betaine–homocysteine S-methyltransferase by hydrogen peroxide in vitro. Biochem J 392:443–448
Mulkiewicz E, Jastorff B, Składanowski AC et al (2007) Evaluation of the acute toxicity of perfluorinated carboxylic acids using eukaryotic cell lines, bacteria and enzymatic assays. Environ Toxicol Pharmacol 23:279–285
Park T, Struck DK, Deaton JF et al (2006) Topological dynamics of holins in programmed bacterial lysis. Proc Natl Acad Sci USA 103:19713–19718
Petitpas I, Petersen CE, Ha CE (2003) Structural basis of albumin–thyroxine interactions and familial dysalbuminemic hyperthyroxinemia. Proc Natl Acad Sci USA 100:6440–6445
Piekarska B, Skowronek M, Rybarska J et al (1996) Congo red-stabilized intermediates in the lambda light chain transition from native to molten state. Biochimie 78:183–189
Service RF (2005) American Chemical Society meeting. Safer alternative could replace widespread contaminant. Science 309:1810
Tsai SY, Lin SC, Suen SY et al (2006) Effect of number of poly (His) tags on the adsorption of engineered proteins on immobilized metal affinity chromatography adsorbents. Process Biochem 41:2058–2067
Waehneldt TV (1975) Sodium dodecyl sulfate in protein chemistry. Biosystems 6:176–187
Wania FA (2007) Global mass balance analysis of the source of perfluorocarboxylic acids in the Arctic ocean. Environ Sci Technol 41:4529–4535
Washburn ST, Bingman TS, Braithwaite SK et al (2005) Exposure assessment and risk characterization for perfluorooctanoate in selected consumer articles. Environ Sci Technol 39:3904–3910
Wu LL, Chen L, Chen FF et al. (2008) Binding of perfluorooctanoic acid to human serum albumin: insights into the molecular toxicity of perfluorochemical. BMC Struct Biol (submitted)
Xie MX, Xu XY, Wang YD (2005) Interaction between hesperetin and human serum albumin revealed by spectroscopic methods. Biochim Biophys Acta 1724:215–224
Yang M (1998) Molecular recognition of DNA targeting small molecule drugs. J Beijing Med Univ 30:97–99
Acknowledgment
We sincerely thank the State Key Laboratory Foundation of China Science and Technology Ministry (Grant No. PCRRK08003) and the National Major Project of Science and Technology Ministry of China (Grant No.2008ZX07421-002) for financially supporting this work.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
726_2008_217_MOESM1_ESM.pdf
(A) Cartoon illustrating the color reaction between ECR and CPC and then the substitution reaction with PFOA. (B) Absorption spectra (from 1 to 7) of solutions containing 0.050 mM ECR and 0.030 mM CPC in the presence of various PFOA concentrations from 0 to 0.050 mM at pH 3.81. (C) Standard curve for PFOA assay at 522 nm
Rights and permissions
About this article
Cite this article
Wu, LL., Chen, L., Song, C. et al. Potential enzyme toxicity of perfluorooctanoic acid. Amino Acids 38, 113–120 (2010). https://doi.org/10.1007/s00726-008-0217-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-008-0217-4