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Effect of Glycosylation on the Physicochemical Properties, Structure and Iron Bioavailability of Ferritin Extracted from Tegillarca granosa

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Abstract

Iron deficiency anemia (IDA) is a major global health problem. Tegillarca granosa has been considered as an excellent source of iron given its high content of iron-binding protein, ferritin. The aim of the present study was to determine the physicochemical properties, protein structures, and iron uptake of ferritin extracted from T. granosa, and to evaluate the potential impacts of chitosan glycosylation on these characteristics. Based on Box-Behnken design and response surface methodology, the optimal conditions for glycosylation included a ferritin/chitosan mass ratio of 4:1, a pH of 5.5, a reaction time of 10 min, and a reaction temperature of 50 °C. Glycosylation caused decreased surface hydrophobicity and elevated water-holding capacity of ferritin due to the introduction of hydrophilic groups. Additionally, glycosylation improved antioxidant capacity of ferritin by 20.69%–189.66%, likely owing to the protons donated by saccharide moiety to terminate free radical chain reaction. The in vitro digestibility of ferritin was elevated by 22.56%–104.85% after glycosylation, which could be associated with less β-sheet content in secondary structure that made the glycosylated protein less resistant to enzymatic digestion. The results of the iron bioavailability in Caco-2 cells revealed that ferritin (78.85–231.77ng mg−1) exhibited better iron bioavailability than FeSO4 (51.48–114.37 ng mg−1) and the values were further elevated by glycosylation with chitosan (296.23–358.20 ng mg−1), which may be related to the physicochemical properties of ferritin via glycosylation modification. These results provide a basis for the development of T. granosa derived ferritin and its glycosylated products, and can promote the utilization of aquatic resources.

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References

  • Benjakul, S., Visessanguan, W., Phongkanpai, V., and Tanaka, M., 2005. Antioxidative activity of caramelisation products and their preventive effect on lipid oxidation in fish mince. Food Chemistry, 90: 231–239.

    Article  Google Scholar 

  • Bi, C., Yuan, Y., Tu, Y., Wu, J., Liang, Y., Li, Y., et al., 2020. Facile synthesis of hydrophilic magnetic graphene nanocomposites via dopamine self-polymerization and Michael addition for selective enrichment of N-linked glycopeptides. Scientific Reports, 10: 71.

    Article  Google Scholar 

  • Cancelo-Hidalgo, M. J., Castelo-Branco, C., Palacios, S., Haya-Palazuelos, J., Ciria-Recasens, M., Manasanch, J., et al., 2013. Tolerability of different oral iron supplements: A systematic review. Current Medical Research and Opinion, 29: 291–303.

    Article  Google Scholar 

  • Chelh, I., Gatellier, P., and Santé-Lhoutellier, V., 2006. Technical note: A simplified procedure for myofibril hydrophobicity determination. Meat Science, 74: 681–683.

    Article  Google Scholar 

  • Chen, C., You, L. J., Abbasi, A. M., Fu, X., and Liu, R. H., 2015. Optimization for ultrasound extraction of polysaccharides from mulberry fruits with antioxidant and hyperglycemic activity in vitro. Carbohydrate Polymers, 130: 122–132.

    Article  Google Scholar 

  • Chi, C. F., Hu, F. Y., Wang, B., Li, T., and Ding, G. F., 2015. Antioxidant and anticancer peptides from the protein hydrolysate of blood clam (Tegillarca granosa) muscle. Journal of Functional Foods, 15: 301–313.

    Article  Google Scholar 

  • Clark, S., 2008. Iron deficiency anemia. Nutrition in Clinical Practice, 23: 128–141.

    Article  Google Scholar 

  • Damron, F. H., Oglesby-Sherrouse, A. G., Wilks, A., and Barbier, M., 2016. Dual-seq transcriptomics reveals the battle for iron during Pseudomonas aeruginosa acute murine pneumonia. Scientific Reports, 6: 39172.

    Article  Google Scholar 

  • DeMaeyer, E., and Adiels-Tegman, M., 1985. The prevalence of anaemia in the world. World Health Statistics Quarterly. Rapport Trimestriel de Statistiques Sanitaires Mondiales, 38: 302–316.

    Google Scholar 

  • de Oliveira, F. C., dos Reis Coimbra, J. S., de Oliveira, E. B., Giraldo Zuñiga, A. D., and Garcia Rojas, E. E., 2016. Food protein-polysaccharide conjugates obtained via the Maillard reaction: A review. Critical Reviews in Food Science and Nutrition, 56(7): 1108–1125.

    Article  Google Scholar 

  • Etcheverry, P., Grusak, M. A., and Fleige, L. E., 2012. Application of in vitro bioaccessibility and bioavailability methods for calcium, carotenoids, folate, iron, magnesium, polyphenols, zinc, and vitamins B(6), B(12), D, and E. Frontiers in Physiology, 3: 317.

    Article  Google Scholar 

  • Farhat, I. A., Orset, S., Moreau, P., and Blanshard, J. M. V., 1998. FTIR study of hydration phenomena in protein-sugar systems. Journal of Colloid and Interface Science, 207: 200–208.

    Article  Google Scholar 

  • Feng, K., Lu, X., Luo, J., and Tang, F., 2020. SMRT sequencing of the full-length transcriptome of Odontotermes formosanus (Shiraki) under Serratia marcescens treatment. Scientific Reports, 10: 15909.

    Article  Google Scholar 

  • Ford, G. C., Harrison, P. M., Rice, D. W., Smith, J. M., Treffry, A., White, J. L., et al., 1984. Ferritin: Design and formation of an iron-storage molecule. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 304: 551–565.

    Article  Google Scholar 

  • Glahn, R. P., Lee, O. A., Yeung, A., Goldman, M. I., and Miller, D. D., 1998. Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion/Caco-2 cell culture model. Journal of Nutrition, 128: 1555–1561.

    Article  Google Scholar 

  • Greenfield, N. J., 2006. Using circular dichroism spectra to estimate protein secondary structure. Nature Protocols, 1(6): 2876–2890.

    Article  Google Scholar 

  • Gu, F. L., Kim, J., Abbas, S., Zhang, X. M., **a, S. Q., and Chen, Z. X., 2010. Structure and antioxidant activity of high molecular weight Maillard reaction products from casein-glucose. Food Chemistry, 120: 505–511.

    Article  Google Scholar 

  • Guan, J. J., Qiu, A. Y., Liu, X. Y., Hua, Y. F., and Ma, Y. H., 2006. Microwave improvement of soy protein isolate–saccharide graft reactions. Food Chemistry, 97: 577–585.

    Article  Google Scholar 

  • Guo, W., Zhao, Y., Yao, Y., Wu, N., Xu, M., Du, H., et al, 2019. Relationship between protein structure changes and in vitro digestion of preserved egg white during pickling. International Journal of Biological Macromolecules, 138: 116–124.

    Article  Google Scholar 

  • Haskard, C., and Li-Chan, E., 1998. Hydrophobicity of bovine serum albumin and ovalbumin determined using uncharged (PRODAN) and anionic (ANS-) fluorescent probes. Journal of Agricultural and Food Chemistry, 46: 2671–2677.

    Article  Google Scholar 

  • Huang, X., Tu, Z., **ao, H., Wang, H., Zhang, L., Hu, Y., et al., 2012. Characteristics and antioxidant activities of ovalbumin glycated with different saccharides under heat moisture treatment. Food Research International, 48: 866–872.

    Article  Google Scholar 

  • Jimtaisong, A., and Saewan, N., 2014. Utilization of carboxymethyl chitosan in cosmetics. International Journal of Cosmetic Science, 36: 12–21.

    Article  Google Scholar 

  • Kumar, M. N. V. R., Muzzarelli, R. A. A., Muzzarelli, C., Sashiwa, H., and Domb, A. J., 2004. Chitosan chemistry and pharmaceutical perspectives. Chemical Reviews, 104: 6017–6084.

    Article  Google Scholar 

  • Kurukji, D., Norton, I., and Spyropoulos, F., 2016. Fabrication of sub-micron protein-chitosan electrostatic complexes for encapsulation and pH-Modulated delivery of model hydrophilic active compounds. Food Hydrocolloids, 53: 249–260.

    Article  Google Scholar 

  • Latunde-Dada, G. O., Yang, W., and Vera Aviles, M., 2016. In vitro iron availability from insects and sirloin beef. Journal of Agricultural and Food Chemistry, 64: 8420–8424.

    Article  Google Scholar 

  • Le, N. T., and Richardson, D. R., 2002. The role of iron in cell cycle progression and the proliferation of neoplastic cells. Biochimica et Biophysica Acta, 1603: 31–46.

    Google Scholar 

  • Li, G., Zhan, J., Xu, A., Tan, B., Sun, N., Wang, C., et al., 2021. Determination of the iron bioavailability, conformation, and rheology of iron-binding proteins from Tegillarca granosa. Journal of Food Biochemistry, 45: e13517.

    Article  Google Scholar 

  • Li, Y., Jiang, H., and Huang, G., 2017. Protein hydrolysates as promoters of non-haem iron absorption. Nutrients, 9: 609.

    Article  Google Scholar 

  • Liu, J., Ru, Q., and Ding, Y., 2012. Glycation a promising method for food protein modification: Physicochemical properties and structure, a review. Food Research International, 49: 170–183.

    Article  Google Scholar 

  • Marciniak-Darmochwal, K., and Kostyra, H., 2009. Influence of nonenzymatic glycosylation (glycation) of pea proteins (Pisum sativum) on their susceptibility to enzymatic hydrolysis. Journal of Food Biochemistry, 33: 506–521.

    Article  Google Scholar 

  • Martins da Costa, J. C., Lima Miki, K. S., da Silva Ramos, A., and Teixeira-Costa, B. E., 2020. Development of biodegradable films based on purple yam starch/chitosan for food application. Heliyon, 6: e03718.

    Article  Google Scholar 

  • Martins, S. I. F. S., Jongen, W. M. F., and van Boekel, M. A. J. S., 2000. A review of maillard reaction in food and implications to kinetic modelling. Trends in Food Science & Technology, 11(9): 364–373.

    Article  Google Scholar 

  • Matemu, A., Kayahara, H., Murasawa, H., and Nakamura, S., 2009. Importance of size and charge of carbohydrate chains in the preparation of functional glycoproteins with excellent emulsifying properties from tofu whey. Food Chemistry, 114: 1328–1334.

    Article  Google Scholar 

  • Miller, A. G., and Gerrard, J., 2005. The Maillard reaction and food protein crosslinking. Progress in Food Biopolymer Research, 1: 69–86.

    Google Scholar 

  • Mimura, E. C., Breganó, J. W., Dichi, J. B., Gregório, E. P., and Dichi, I., 2008. Comparison of ferrous sulfate and ferrous glycinate chelate for the treatment of iron deficiency anemia in gastrectomized patients. Nutrition, 24: 663–668.

    Article  Google Scholar 

  • Oliver, C. M., 2011. Insight into the glycation of milk proteins: An ESI- and MALDI-MS perspective (review). Critical Reviews in Food Science and Nutrition, 51: 410–431.

    Article  Google Scholar 

  • Pirestani, S., Nasirpour, A., Keramat, J., and Desobry, S., 2017. Preparation of chemically modified canola protein isolate with gum Arabic by means of Maillard reaction under wet-heating conditions. Carbohydrate Polymers, 155: 201–207.

    Article  Google Scholar 

  • Qu, W., Zhang, X., Han, X., Wang, Z., He, R., and Ma, H., 2018. Structure and functional characteristics of rapeseed protein isolate-dextran conjugates. Food Hydrocolloids, 82: 329–337.

    Article  Google Scholar 

  • Sheng, L., Su, P., Han, K., Chen, J., Cao, A., Zhang, Z., et al., 2017. Synthesis and structural characterization of lysozyme-pullulan conjugates obtained by the Maillard reaction. Food Hydrocolloids, 71: 1–7.

    Article  Google Scholar 

  • Solá, R. J., and Griebenow, K., 2009. Effects of glycosylation on the stability of protein pharmaceuticals. Journal of Pharmaceutical Sciences, 98: 1223–1245.

    Article  Google Scholar 

  • Song, C. L., and Zhao, X. H., 2013. The preparation of an oligochitosan-glycosylated and cross-linked caseinate obtained by a microbial transglutaminase and its functional properties. International Journal of Dairy Technology, 67: 110–116.

    Article  Google Scholar 

  • Song, C. L., and Zhao, X. H., 2014. Structure and property modification of an oligochitosan-glycosylated and crosslinked soybean protein generated by microbial transglutaminase. Food Chemistry, 163: 114–119.

    Article  Google Scholar 

  • Spiro, T., Pape, L., and Saltman, P., 1967. The hydrolytic polymerization of ferric citrate. I. The chemistry of the polymer. Journal of the American Chemical Society, 89: 5555–5559.

    Article  Google Scholar 

  • Storz, G., and Imlay, J. A., 1999. Oxidative stress. Current Opinion in Microbiology, 2: 188–194.

    Article  Google Scholar 

  • Sun, X., Yin, S. W., and Ma, C. Y., 2008. Transglutaminase-in-duced cross-linking of vicilin-rich kidney protein isolate: Influence on the functional properties and in vitro digestibility. Food Research International, 41: 941–947.

    Article  Google Scholar 

  • Tan, B., Sun, B., Sun, N., Li, C., Zhang, J., and Yang, W., 2021. Structure, functional properties and iron bioavailability of Pneumatophorus japonicus myoglobin and its glycosylation products. International Journal of Biological Macromolecules, 173: 524–531.

    Article  Google Scholar 

  • Taniguchi, C., Dobbs, J., and Dunn, M., 2016. Heme iron, non-heme iron, and mineral content of blood clams (Anadara spp.) compared to Manila clams (V. philippinarum), Pacific oysters (C. gigas), and beef liver (B. taurus). Journal of Food Composition and Analysis, 57: 49–55.

    Article  Google Scholar 

  • Tian, S., Chen, J. I. E., and Small, D., 2010. Enhancement of solubility and emulsifying properties of soy protein isolates by glucose conjugation. Journal of Food Processing and Preservation, 35: 80–95.

    Article  Google Scholar 

  • Turner, J. A., Sivasundaram, L. R., Ottenhof, M. A., Farhat, I. A., Linforth, R. S., and Taylor, A. J., 2002. Monitoring chemical and physical changes during thermal flavor generation. Journal of Agricultural and Food Chemistry, 50: 5406–5411.

    Article  Google Scholar 

  • van Boekel, M. A., 2001. Kinetic aspects of the Maillard reaction: A critical review. Nahrung, 45: 150–159.

    Article  Google Scholar 

  • Wang, M., Gruissem, W., and Bhullar, N. K., 2013. Nicotianamine synthase overexpression positively modulates iron homeostasis-related genes in high iron rice. Frontiers in Plant Science, 4: 156–156.

    Article  Google Scholar 

  • Wang, Q., and Ismail, B., 2012. Effect of Maillard-induced glycosylation on the nutritional quality, solubility, thermal stability and molecular configuration of whey protein. International Dairy Journal, 25: 112–122.

    Article  Google Scholar 

  • Wang, W. D., Li, C., Bin, Z., Huang, Q., You, L. J., Chen, C., et al., 2020. Physicochemical properties and bioactivity of whey protein isolate-inulin conjugates obtained by Maillard reaction. International Journal of Biological Macromolecules, 150: 326–335.

    Article  Google Scholar 

  • Wang, X. J., Zheng, X. Q., Liu, X. L., Kopparapu, N. K., Cong, W. S., and Deng, Y. P., 2017. Preparation of glycosylated zein and retarding effect on lipid oxidation of ground pork. Food Chemistry, 227: 335–341.

    Article  Google Scholar 

  • Wang, Y. J., Zeng, Q. G., and Xu, L. N., 2013. Population structure of the blood clam (Tegillarca granosa) in China based on microsatellite markers. GMR, Genetics and Molecular Research, 12: 892–900.

    Article  Google Scholar 

  • Xu, W., and Zhao, X. H., 2019. Structure and property changes of the soy protein isolate glycated with maltose in an ionic liquid through the Maillard reaction. Food & Function, 10: 1948–1957.

    Article  Google Scholar 

  • Yang, J. T., Wu, C. S., and Martinez, H. M., 1986. Calculation of protein conformation from circular dichroism. Methods in Enzymology, 130: 208–269.

    Article  Google Scholar 

  • Yang, R., Liu, Y., Gao, Y., Wang, Y., Blanchard, C., and Zhou, Z., 2017. Ferritin glycosylated by chitosan as a novel EGCG nano-carrier: Structure, stability, and absorption analysis. International Journal of Biological Macromolecules, 105: 252–261.

    Article  Google Scholar 

  • Zhan, J., Li, G., and Tan, B., 2021. Optimization of hemoglobin chitosan glycosylation conditions and structural characteristics and functions of glycosylated hemoglobin after an in vitro digestion. Journal of Aquatic Food Product Technology, 30: 794–805.

    Article  Google Scholar 

  • Zhang, Q., Li, L., Lan, Q., Li, M., Wu, D., Chen, H., et al., 2019. Protein glycosylation: A promising way to modify the functional properties and extend the application in food system. Critical Reviews in Food Science and Nutrition, 59(15): 2506–2533.

    Article  Google Scholar 

  • Zhao, H., Kang, X., Zhou, X., Tong, L., Yu, W., Zhang, J., et al., 2021. Glycosylation fish gelatin with gum Arabic: Functional and structural properties. LWT-Food Science and Technology, 139: 110634.

    Article  Google Scholar 

  • Zheng, K., Wu, L., He, Z., Yang, B., and Yang, Y., 2017. Measurement of the total protein in serum by biuret method with uncertainty evaluation. Measurement, 112: 16–21.

    Article  Google Scholar 

  • Zhou, H., Watts, J. D., and Aebersold, R., 2001. A systematic approach to the analysis of protein phosphorylation. Nature Biotechnology, 19: 375–378.

    Article  Google Scholar 

  • Zhu, C. Y., Wang, X. P., and Zhao, X. H., 2015. Property modification of caseinate responsible to transglutaminase-induced glycosylation and crosslinking in the presence of a degraded chitosan. Food Science and Biotechnology, 24: 843–850.

    Article  Google Scholar 

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Acknowledgement

This work was supported by the National Key R&D Program of China (No. 2018YFD0901105).

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Correspondence to Chao Li or Wenge Yang.

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Sun, B., Tan, B., Li, G. et al. Effect of Glycosylation on the Physicochemical Properties, Structure and Iron Bioavailability of Ferritin Extracted from Tegillarca granosa. J. Ocean Univ. China 22, 1068–1078 (2023). https://doi.org/10.1007/s11802-023-5464-1

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