Abstract
An innovative edible wrapping with potential use for designing functional foods with antimicrobial capacity was developed by complexation of ε-polylysine with peptide-loaded liposomes. Unmarketable long-term frozen cooked shrimp (Litopenaeus vannamei) muscle was used as a source of both bioactive peptides and complex liposomal suspension carrier, producing a sustainable value-added protein wrapping material with desirable sensory properties. A <10-kDa peptide fraction (SH) with antioxidant and angiotensin-converting enzyme inhibitory capacity was encapsulated in partially purified phosphatidylcholine (PC) liposomes (LSH) with an entrapment efficiency of 85 %. The average size and zeta potential of LSH were 164 ± 2 nm and –37.0 ± 1.7 mV, respectively. The LSH surface changed from electronegative to electropositive upon adsorption of ε-polylysine (PL) with an optimal concentration of 0.5 %. The average diameter and zeta potential of the resulting complex ε-polylysine-adsorbed liposomes containing the peptide hydrolysate (PL-LSH) were 216 ± 5 nm and +51.1 ± 1.1 mV, respectively. The ε-PL proved to be effective as liposome stabilizing and antimicrobial agent. The PL-LSH suspension was incorporated in the formulation of the protein wrapping to provide it with both bioactive and antimicrobial properties. The wrapping showed low water solubility (≈30 %) and low mechanical resistance (tensile strength = 0.23 ± 0.06 MPa; elongation at break = 0.91 ± 0.19 %) properties that allowed it to be very versatile for varied food design and was effective against Listeria monocytogenes, Escherichia coli, Staphylococcus aureus and Yersinia enterocolitica.
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References
A.O.A.C. (1995). Official methods of analysis. Method number 934.01.. Maryland, USA: Association of Official Analytical Chemistry.
Adler-Nissen, J. (1977). Enzymatic hydrolysis of food proteins. Process Biochemistry, 8, 18–32.
Alemán, A., Giménez, B., Pérez-Santin, E., Gómez-Guillén, M. C., & Montero, P. (2011a). Contribution of Leu and Hyp residues to antioxidant and ACE-inhibitory activities of peptide sequences isolated from squid gelatin hydrolysate. Food Chemistry, 125(2), 334–341.
Alemán, A., Giménez, B., Montero, P., & Gómez-Guillén, M. C. (2011b). Antioxidant activity of several marine skin gelatins. LWT - Food Science and Technology, 44(2), 407–413.
Amado IR, González M, Murado MA & Vázquez JA (2015). Shrimp (Penaueus vannamei) cooking wastewater as a source of astaxanthin and bioactive peptides. Journal of Chemical Technology and Biotechnology, in press.
Blanco-Pascual, N., Fernández-Martín, F., & Montero, M. P. (2013). Effect of different protein extracts from Dosidicus gigas muscle co-products on edible films development. Food Hydrocolloids, 33(1), 118–131.
Carr, W. E. S., Netherton, J. C., Gleeson, R. A., & Derby, C. D. (1996). Stimulants of feeding behavior in fish: analyses of tissues of diverse marine organisms. Biological Bulletin, 190(2), 149–160.
Cheung, I. W. Y., & Li-Chan, E. C. Y. (2010). Angiotensin-I-converting enzyme inhibitory activity and bitterness of enzymatically-produced hydrolysates of shrimp (Pandalopsis dispar) processing byproducts investigated by Taguchi design. Food Chemistry, 122(4), 1003–1012.
Cheung, L. K. Y., Cheung, I. W. Y., & Li-Chan, E. C. Y. (2012). Effects of production factors and egg-bearing period on the antioxidant activity of enzymatic hydrolysates from shrimp (Pandalopsis dispar) processing byproducts. Journal of Agricultural and Food Chemistry, 60(27), 6823–6831.
Efimova, A. A., Sybachin, A. V., & Yaroslavov, A. A. (2011). Effect of anionic-lipid-molecule geometry on the structure and properties of liposome-polycation complexes. Polymer Science - Series C, 53(1), 89–96.
FDA (2004). Food and Drug Administration. Agency Response Letter GRAS Notice No. GRN 000135.
Finogenova, O. A., Filinsky, D. V., & Ermakov, Y. A. (2008). Electrostatic effects upon adsorption and desorption of polylysines on the surface of lipid membranes of different composition. Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology, 2(2), 181–188.
Giménez, B., Gómez-Guillén, M. C., López-Caballero, M. E., Gómez-Estaca, J., & Montero, P. (2012). Role of sepiolite in the release of active compounds from gelatin-egg white films. Food Hydrocolloids, 27(2), 475–486.
Gomez-Estaca, J., Montero, P., & Gomez-Guillen, M. C. (2014). Shrimp (Litopenaeus vannamei) muscle proteins as source to develop edible films. Food Hydrocolloids, 41, 86–94.
Guerard, F., Sumaya-Martinez, M. T., Laroque, D., Chabeaud, A., & Dufossé, L. (2007). Optimization of free radical scavenging activity by response surface methodology in the hydrolysis of shrimp processing discards. Process Biochemistry, 42(11), 1486–1491.
Harrigan, P. R., Madden, T. D., & Cullis, P. R. (1990). Protection of liposomes during dehydration or freezing. Chemistry and Physics of Lipids, 52, 139–149.
He, H. L., Chen, X. L., Sun, C. Y., Zhang, Y. Z., & Zhou, B. C. (2006). Analysis of novel angiotensin-I-converting enzyme inhibitory peptides from protease-hydrolyzed marine shrimp Acetes chinensis. Journal of Peptide Science, 12(11), 726–733.
Hiraki, J., Ichikawa, T., Ninomiya, S., Seki, H., Uohama, K., Seki, H., Kimura, S., Yanagimoto, Y., & Barnett, J. W., Jr. (2003). Use of ADME studies to confirm the safety of ε-polylysine as a preservative in food. Regulatory Toxicology and Pharmacology, 37(2), 328–340.
Imran, M., Revol-Junelles, A. M., René, N., Jamshidian, M., Akhtar, M. J., Arab-Tehrany, E., Jacquot, M., & Desobry, S. (2012). Microstructure and physico-chemical evaluation of nano-emulsion-based antimicrobial peptides embedded in bioactive packaging films. Food Hydrocolloids, 29(2), 407–419.
Jiménez, A., Sánchez-González, L., Desobry, S., Chiralt, A., & Tehrany, E. A. (2014). Influence of nanoliposomes incorporation on properties of film forming dispersions and films based on corn starch and sodium caseinate. Food Hydrocolloids, 35, 159–169.
Jong, C. J., Azuma, J., & Schaffer, S. (2012). Mechanism underlying the antioxidant activity of taurine: prevention of mitochondrial oxidant production. Amino Acids, 42(6), 2223–2232.
Kim, D. S., Baek, H. H., Ahn, C. B., Byun, D. S., Jung, K. J., Lee, H. G., Cadwallader, K. R., & Kim, H. R. (2000). Development and characterization of a flavoring agent from oyster cooker effluent. Journal of Agricultural and Food Chemistry, 48(10), 4839–4843.
Li, Y.-Q., Feng, J.-L., Han, Q., Dai, Z.-Y., Liu, W., & Mo, H.-Z. (2014). Effects of ε-polylysine on physicochemical characteristics of chilled pork. Food and Bioprocess Technology, 7(9), 2507–2515.
Liñán-Cabello, M. A., Paniagua-Michel, J., & Hopkins, P. M. (2002). Bioactive roles of carotenoids and retinoids in crustaceans. Aquaculture Nutrition, 8(4), 299–309.
Malcher, M., Volodkin, D., Heurtault, B., André, P., Schaaf, P., Möhwald, H., Voegel, J. C., Sokolowski, A., Ball, V., Boulmedais, F., & Frisch, B. (2008). Embedded silver ions-containing liposomes in polyelectrolyte multilayers: cargos films for antibacterial agents. Langmuir, 24(18), 10209–10215.
Malheiros, P., Daroit, D. J., & Brandelli, A. (2010). Food applications of liposome-encapsulated antimicrobial peptides. Trends in Food Science and Technology, 21(6), 284–292.
Mandeville, S., Yaylayan, V., & Simpson, B. K. (1992). Proximate analysis, isolation and identification of amino acids and sugars from raw and cooked commercial shrimp waste. Food Biotechnology, 6(1), 51–64.
McClements, D. J. (2015). Encapsulation, protection, and release of hydrophilic active components: potential and limitations of colloidal delivery systems. Advances in Colloid and Interface Science, 219, 27–53.
Mente, E., Coutteau, P., Houlihan, D., Davidson, I., & Sorgeloos, P. (2002). Protein turnover, amino acid profile and amino acid flux in juvenile shrimp Litopenaeus vannamei: effects of dietary protein source. Journal of Experimental Biology, 205(20), 3107–3122.
Michel, M., Vautier, D., Voegel, J. C., Schaaf, P., & Ball, V. (2004). Layer by layer self-assembled polyelectrolyte multilayers with embedded phospholipid vesicles. Langmuir, 20(12), 4835–4839.
Moeller, E. H., Holst, B., Nielsen, L. H., Pedersen, P. S., & Østergaard, J. (2010). Stability, liposome interaction, and in vivo pharmacology of ghrelin in liposomal suspensions. International Journal of Pharmaceutics, 390(1), 13–18.
Mosquera, M., Giménez, B., Mallmann da Silva, I., Ferreira Boelter, J., Montero, P., Gómez-Guillén, M. C., & Brandelli, A. (2014). Nanoencapsulation of an active peptidic fraction from sea bream scales collagen. Food Chemistry, 156, 144–150.
Mosquera, M., Giménez, B., Montero, P., & Gómez-Guillén, M. C. (2015). Incorporation of liposomes containing squid tunic ACE-inhibitory peptides into fish gelatin. Journal of the Science of Food and Agriculture. doi:10.1002/jsfa.7145.
Mozafari, M. R., Johnson, C., Hatziantoniou, S., & Demetzos, C. (2008). Nanoliposomes and their applications in food nanotechnology. Journal of Liposome Research, 18(4), 309–327.
Müller, R. H., Jacobs, C., & Kayser, O. (2001). Nanosuspensions as particulate drug formulations in therapy: rationale for development and what we can expect for the future. Advanced Drug Delivery Reviews, 47, 3–19.
Pérez-Santín, E., Calvo, M. M., López-Caballero, M. E., Montero, P., & Gómez-Guillén, M. C. (2013). Compositional properties and bioactive potential of waste material from shrimp cooking juice. LWT - Food Science and Technology, 54(1), 87–94.
Rao, D. R., Chawan, C. B., & Veeramachaneni, R. (1995). Liposomal encapsulation of beta-galactosidase—comparison of two methods of encapsulation and in vitro lactose digestibility. Journal of Food Biochemistry, 18, 239–251.
Sasaki, H., Karasawa, K., Hironaka, K., Tahara, K., Tozuka, Y., & Takeuchi, H. (2013). Retinal drug delivery using eyedrop preparations of poly-l-lysine-modified liposomes. European Journal of Pharmaceutics and Biopharmaceutics, 83(3), 364–369.
Sharma, A., & Sharma, U. S. (1997). Liposomes in drug delivery: progress and limitations. International Journal of Pharmaceutics, 154(2), 123–140.
Shih, I.-L., Shen, M.-H., & Van, Y.-T. (2006). Microbial synthesis of poly(ε-lysine) and its various applications. Bioresource Technology, 97(9), 1148–1159.
Sobral, P. J. D. A., Dos Santos, J. S., & García, F. T. (2005). Effect of protein and plasticizer concentrations in film forming solutions on physical properties of edible films based on muscle proteins of a Thai Tilapia. Journal of Food Engineering, 70(1), 93–100.
Taylor, T. M., Davidson, P. M., Bruce, B. D., & Weiss, J. (2005). Liposomal nanocapsules in food science and agriculture. Critical Reviews in Food Science and Nutrition, 45(7-8), 587–605.
Volodkin, D., Ball, V., Schaaf, P., Voegel, J. C., & Mohwald, H. (2007a). Complexation of phosphocholine liposomes with polylysine. Stabilization by surface coverage versus aggregation. Biochimica et Biophysica Acta - Biomembranes, 1768(2), 280–290.
Volodkin, D., Mohwald, H., Voegel, J. C., & Ball, V. (2007b). Coating of negatively charged liposomes by polylysine: drug release study. Journal of Controlled Release, 117(1), 111–120.
Weng, W. Y., Tao, Z., Liu, G. M., Su, W. J., Osako, K., Tanaka, M., & Cao, M. J. (2014). Mechanical, barrier, optical properties and antimicrobial activity of edible films prepared from silver carp surimi incorporated with ε-polylysine. Packaging Technology and Science, 27(1), 37–47.
Were, L. M., Bruce, B. D., Davidson, P. M., & Weiss, J. (2003). Size, stability, and entrapment efficiency of phospholipid nanocapsules containing polypeptide antimicrobials. Journal of Agricultural and Food Chemistry, 51, 8073–8079.
Wu, J., Liu, H., Ge, S., Wang, S., Qin, Z., Chen, L., Zheng, Q., Liu, Q., & Zhang, Q. (2015). The preparation, characterization, antimicrobial stability and in vitro release evaluation of fish gelatin films incorporated with cinnamon essential oil nanoliposomes. Food Hydrocolloids, 43, 427–435.
Yoshida, T., & Nagasawa, T. (2003). Epsilon-poly-L-lysine: microbial production, biodegradation and application potential. Applied Microbiology and Biotechnology, 62(1), 21–26.
Zhang, L., Li, R., Dong, F., Tian, A., Li, Z., & Dai, Y. (2015). Physical, mechanical and antimicrobial properties of starch films incorporated with ε-poly-l-lysine. Food Chemistry, 166, 107–114.
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This research was financed by the Spanish Ministry of Economy and Competitiveness through projects AGL2011-27607, 201370E036 and AGL2014-52825.
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Alemán, A., Mastrogiacomo, I., López-Caballero, M.E. et al. A Novel Functional Wrapping Design by Complexation of ε-Polylysine with Liposomes Entrapping Bioactive Peptides. Food Bioprocess Technol 9, 1113–1124 (2016). https://doi.org/10.1007/s11947-016-1703-4
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DOI: https://doi.org/10.1007/s11947-016-1703-4