Effect of Collagen Hydrolysates from Clown Featherback (Chitala ornata) Skin on Angiotensin I - Converting Enzyme Inhibitory and Antioxidant Activities
Abstract
The objective of this study was to investigate effect of degree of hydrolysis and molecular weight of collagen hydrolysates from clown featherback (Chitala ornata) skin on angiotensin I-converting enzyme (ACE) inhibitory and antioxidant activities. Yield of collagen from clown featherback was 35-67% of dried skin. Based on SDS-PAGE, the collagen was classified as Type I. The collagen was hydrolyzed by various proteinases including trypsin, pepsin and alcalase at different hydrolysis time (0, 2, 4, 6 และ 8 h). The highest degree of hydrolysis was found in hydrolysates prepared from alcalase (35.09%), followed by pepsin (26.73%) and trypsin (22.03%), respectively at 8 h hydrolysis. Alcalase-induced hydrolysates (at 8 h) exhibited the highest ACE inhibitory and antioxidant activities based on 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging and ferric reducing antioxidant power (FRAP). The hydrolysates prepared from alcalase (at 8 h) were fractionated into 4 fractions: crude hydrolysates, >30 kDa, 10-30 kDa and <10 kDa using ultrafiltration membranes. The fraction with MW <10 kDa showed the highest ACE inhibitory activity (50.35%) and antioxidant activity based on DPPH radical scavenging (59.06%) and FRAP (304.56 mM FeSO4 equivalent). Keywords : clown featherback, collagen hydrolysates, angiotensin I-converting enzyme, antioxidantReferences
Adler-Nissen, J. (1979). Determination of the degree of hydrolysis of food protein hydrolysates by trinitrobenzensulfonic acid. Journal of Agricultural and Food Chemistry, 27, 1256-1262.
Adler-Nissen, J. (1986). Enzymic hydrolysis of food proteins. London: Elsevier Applied Science Publishers.
Aleman, A., Gimenez, B., Montero, P., & Gomez-Guillen, M.C. (2011). Antioxidant activity of several marine skin gelatins. LWT - Food Science and Technology, 44, 407-413.
AOAC. (2000). Official Methods of Analysis. 17th ed. Association of official analytical chemists. Gaithersburg: Md.
Atkinson, A.B., & Rovertson, J. (1979). Captopril in the treatment of clinical hypertension and cardiac failure. Lancet, 2, 836-839.
Baehaki, A., Nopianti, R., & Anggraeni, S. (2015). Antioxidant activity of skin and bone collagen hydrolyzed from striped catfish (Pangasius pangasius) with papain enzyme. Journal of Chemical and Pharmaceutical
Research, 7, 131-135.
Balti, R., Bougatef, A., El-Hadj Ali, N., Zekri, D., Barkia, A., & Nasri, M. (2010). Influence of degree of hydrolysis on functional properties and angiotensin I-converting enzyme-inhibitory activity of protein hydrolysates from cuttlefish (Sepia officinalis) by-products. Journal of the Science of Food and Agriculture, 90, 2006-2014.
Barzideh, Z., Latiff, A.A., Gan, C., Abedin, M.Z., & Alias, A.K. (2014). ACE inhibitory and antioxidant activities of collagen hydrolysates from the ribbon jellyfish (Chrysaora sp.). Food Technology and Biotechnology, 52, 495-504.
Benzie, I.F.F., & Strain, J.J. (1996). Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: The FRAP assay. Analytical Biochemistry, 239, 70-76.
Chen, H.M., Muramoto, K., Yamauchi, F., Fujimoto, K., & Nokihara, K. (1998). Antioxidative properties of histidine-containing peptides designed from peptide fragments found in the digests of a soybean protein. Journal of Agricultural and Food Chemistry, 46, 49-53.
Doucet, D., Otter, D.E., Gauthier, S.F., & Foegeding, E.A. (2003). Enzyme-induced gelation of extensively hydrolyzed whey proteins by alcalase: peptide identification and determination of enzyme specificity. Journal of Agricultural and Food Chemistry, 50, 6300-6308.
Ghanbari, R., Zarei, M., Ebrahimpour, A., Abdul-Hamid, A., Ismail, A., & Saari, N. (2015). Angiotensin-I converting enzyme (ACE) inhibitory and anti-oxidant activities of sea cucumber (Actinopyga lecanora) hydrolysates. International Journal of Molecular Sciences, 16, 28870-28885.
Giraud-Guille, M.M., Besseau, L., Chopin, C., Durand, P., & Herbage, D. (2000). Structural aspects of fish skin collagen which forms ordered arrays via liquid crystalline states. Biomaterial, 21, 899-906.
Gómez-Ruiz, J.A., Ramos, M., & Recio, I. (2007). Identification of novel angiotensin-converting enzyme-inhibitory peptides from ovine milk proteins by CE-MS and chromatographic techniques. Electrophoresis, 28, 4202-4211.
He, H.L., Chen, X.L., Wu, H., Sun, C.Y., Zhang, Y.Z., & Zhou, B.C. (2007). High throughput and rapid screening of marine protein hydrolysates enriched in peptides with angiotensin-I-converting enzyme inhibitory activity by capillary electrophoresis. Bioresource Technology, 98, 3499-3505.
Himaya, S.W.A., Ngo, D.H., Ryu, B., & Kim, S.K. (2012). An active peptide purified from gastrointestinal enzyme hydrolysate of Pacific cod skin gelatine attenuates angiotensin-1 converting enzyme (ACE) activity and cellular oxidative stress. Food Chemistry, 132, 1872-1882.
Je, J.Y., Park, P.J., & Kim, S.K. (2005). Antioxidant activity of a peptide isolated from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. Food Research International, 38, 45-50.
Jia, J., Zhou, Y., Lu, J., Chen, A., Li, Y., & Zheng, G. (2010). Enzymatic hydrolysis of Alaska Pollack (Theragra chalcogramma) skin and antioxidant activity of the resulting hydrolysates. Journal of the Science of Food and Agriculture, 90, 635-640.
Kimura, S. (1992). Wide distribution of the skin type I collagen α3 chain in bony fish. Comparative Biochemistry and Physiology Part B, 102, 255-260.
Kittiphattanabawon, P., Benjukul, S., Sinthusamran, S., & Kishimura, Hideki. (2015). Characteristics of collagen from the skin of clown featherback (Chitala ornata). International Journal of Food Science and Technology, 50, 1972-1978.
Kittiphattanabawon, P., Benjukul, S., Visessanguan, W., Nagai, T., & Tanaka, M. (2005). Characterisation of acid- soluble collagen from skin and bone of bigeye snaper (Priacanthus tayenus). Food Chemistry, 89, 363-372.
Kuo, P.L., & Pu, C. (2011). The contribution of depression to mortality among elderly with self-reported hypertension: Analysis using a national representative longitudinal survey. Journal of Hypertension, 29, 2084-2090.
Laemmli, U.K. (1970). Cleavage of structural proteins during assembly head of bacteriophage T4. Nature, 277, 680-685.
Lee, J.K., Hong, S., Jeon, J.K., Kim, S.K., & Byun, H.G. (2009). Purification and characterization of angiotensin I converting enzyme inhibitory peptides from the rotifer, Brachionus rotundiformis. Bioresource Technology, 100, 5255-5259.
Lee, S.H., Qian, Z.J., & Kim, S.K. (2010). A novel angiotensin I converting enzyme inhibitory peptide from tuna frame protein hydrolysates and its antihypertensive effect in spontaneously hypertensive rats. Food Chemistry, 118, 96-102.
Liu, Q., Kong, B., Xiong, Y.L., & Xia, X. (2010). Antioxidant activity and functional properties of porcine plasma protein hydrolysates influenced by the degree of hydrolysis. Food Chemistry, 118, 403-410.
Nagai, T., & Suzuki, N. (2000a). Isolation of collagen from fish waste material-skin, bone and fins. Food Chemistry, 68, 277-281.
Nagai, T., & Suzuki, N. (2000b). Preparation and characterization of several fish bone collagens. Journal of Food Biochemistry, 24, 427-436.
Ngo, D.H., Qian, Z.J., Ryu, B., Park, J.W., & Kim, S.K. (2010). In vitro antioxidant activity of a peptide isolated from Nile tilapia (Oreochromis niloticus) scale gelatin in free radical-mediated oxidative systems. Journal of Functional Foods, 2, 107-117.
Park, P.J., Je, J.Y., & Kim, S.K. (2003). Angiotensin I converting enzyme (ACE) inhibitory activity of hetero-chitooligosaccharides prepared from partially different deacetylated chitosans. Journal of Agriculture and Food Chemistry, 51, 4930-4934.
Pazinatto, C., Malta, L.G., Pastore, G.M., & Netto, F.M. (2013). Antioxidant capacity of amaranth products: effects of thermal and enzymatic treatments. Food Science and Technology, 33, 485-493.
Philanto, L. (2000). Bioactive peptides derived from bovine whey proteins: Opioid and ace-inhibitory. Trends in Food Science and Technology, 11, 347-356.
Piyadhammaviboon, P., Wongngam, W., Benjakul, S., & Yongsawatdigul, J. (2012). Antioxidant and angiotensin-converting enzyme inhibitory activities of protein hydrolysates prepared from threadfin bream (Nemipterus spp.) surimi byproducts. Journal of aquatic food product technology, 21, 265-278.
Rajapakse, N., Mendis, E., Byun, H.G., & Kim, S.K. (2005). Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems. The Journal of Nutritional Biochemistry, 16, 562-569.
Ranathunga, S., Rajapakse, N., & Kim, S.K. (2006). Purification and characterization of antioxidative peptide derived from muscle of conger eel (Conger myriaster). European Food Research and Technology, 222, 310-315.
Saiga, A., Iwai, K., Hayakawa, T., Takahata, Y., Kitamura, S., Nishimura, T., & Morimatsu, F. (2008). Angiotensin I-converting enzyme-inhibitory peptides obtained from chicken collagen hydrolysate. Journal of Agricultural and Food Chemistry, 56, 9586-9591.
Shimada, K., Fujikawa, K., Yahara, K., & Nakamura, T. (1992). Antioxidative properties of xanthan on the antioxidation of soybean oil in cyclodextrin emulsion. Journal of Agricultural and Food Chemistry, 40, 945-948.
Sica, M.D., & Domenic, A. (2003). Combination angiotensin-converting enzyme inhibitor and angiotensin receptor blocker therapy: its role in clinical practice. Journal of Clinical Hyperttension, 5, 414-420.
Siepen, J.A., Keevil, E.J., Knight, D., & Hubbard, S.J. (2007). Prediction of missed cleavage sites in tryptic peptides aids protein identification in proteomics. Journal of Proteome Research, 6, 399-408.
Simpson, B.K. (2000). Digestive proteinases from marine animals. In N.M. Haard, & B.K. Simpson. (Eds.), Seafood enzymes: Utilization and influence on postharvest seafood quality. (pp. 531-540). New York: Marcel Dekker.
Singh, P., Benjakul, S., Maqsood, S., & Kishimura, H. (2011). Isolation and characterisation of collagen extracted from the skin of striped catfish (Pangasianodon hypophthalmus). Food Chemistry, 124,
97-105.
Thahom, N., & Sompongse, W. (2015). Characterisation of acid-soluble collagen from skin of grey featherback (Notopterus notopterus). Thai Journal of Science and Technology, 23, 257-267. (in Thai)
Umayaparvathi, S., Meenakshi, S., Vimalraj, V., Arumugama, M., Sivagami, G., & Balasubramaniana, T. (2014). Antioxidant activity and anticancer effect of bioactive peptide from enzymatic hydrolysate of oyster (Saccostrea cucullata). Biomedicine and Preventive Nutrition, 4, 343–353.
Venskutonis, P.R. (2014). Natural antioxidants in food systems. In G. Bartosz. (Eds.), Food oxidants and antioxidants: chemical, biological, and functional properties. (pp. 235-301). New York: CRC Press.
Wang, B., Wang, Y.M., Chi, C.F., Luo, H.Y., Deng, S.G., & Ma, J.Y. (2013). Isolation and characterization of collagen and antioxidant collagen peptides from scales of croceine croaker (Pseudosciaena crocea). Marine Drugs, 11, 4641-4661.
Wiriyaphan, C., Chitsomboon, B., & Yongsawadigul, J. (2012). Antioxidant activity of protein hydrolysates derived from threadfin bream surimi byproducts. Food Chemistry, 132, 104-111.
You, L., Zhao, M., Regenstein, J.M., & Ren, J. (2010). Changes in the antioxidant activity of loach (Misgurnus anguillicaudatus) protein hydrolysates during a simulated gastrointestinal digestion. Food Chemistry, 120, 810-816.
Zambrowicz, A., Pokora, M., Eckert, E., Szoltysik, M., Dbrowska, A., Chrzanowska, J., & Trziszka, T. (2012). Antioxidant and antimicrobial activity of lecithin free egg yolk protein preparation hydrolysates obtained with digestive enzymes. Functional Foods in Health and Disease, 2, 487-500.
Zeng, S.K., Zhang, C.H., Lin, H., Yang, P., Hong, P.Z., & Jiang, Z. (2009). Isolation and characterisation of acid-solubilised collagen from the skin of Nile tilapia (Oreochromis niloticus). Food Chemistry, 116,
879-
Adler-Nissen, J. (1986). Enzymic hydrolysis of food proteins. London: Elsevier Applied Science Publishers.
Aleman, A., Gimenez, B., Montero, P., & Gomez-Guillen, M.C. (2011). Antioxidant activity of several marine skin gelatins. LWT - Food Science and Technology, 44, 407-413.
AOAC. (2000). Official Methods of Analysis. 17th ed. Association of official analytical chemists. Gaithersburg: Md.
Atkinson, A.B., & Rovertson, J. (1979). Captopril in the treatment of clinical hypertension and cardiac failure. Lancet, 2, 836-839.
Baehaki, A., Nopianti, R., & Anggraeni, S. (2015). Antioxidant activity of skin and bone collagen hydrolyzed from striped catfish (Pangasius pangasius) with papain enzyme. Journal of Chemical and Pharmaceutical
Research, 7, 131-135.
Balti, R., Bougatef, A., El-Hadj Ali, N., Zekri, D., Barkia, A., & Nasri, M. (2010). Influence of degree of hydrolysis on functional properties and angiotensin I-converting enzyme-inhibitory activity of protein hydrolysates from cuttlefish (Sepia officinalis) by-products. Journal of the Science of Food and Agriculture, 90, 2006-2014.
Barzideh, Z., Latiff, A.A., Gan, C., Abedin, M.Z., & Alias, A.K. (2014). ACE inhibitory and antioxidant activities of collagen hydrolysates from the ribbon jellyfish (Chrysaora sp.). Food Technology and Biotechnology, 52, 495-504.
Benzie, I.F.F., & Strain, J.J. (1996). Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: The FRAP assay. Analytical Biochemistry, 239, 70-76.
Chen, H.M., Muramoto, K., Yamauchi, F., Fujimoto, K., & Nokihara, K. (1998). Antioxidative properties of histidine-containing peptides designed from peptide fragments found in the digests of a soybean protein. Journal of Agricultural and Food Chemistry, 46, 49-53.
Doucet, D., Otter, D.E., Gauthier, S.F., & Foegeding, E.A. (2003). Enzyme-induced gelation of extensively hydrolyzed whey proteins by alcalase: peptide identification and determination of enzyme specificity. Journal of Agricultural and Food Chemistry, 50, 6300-6308.
Ghanbari, R., Zarei, M., Ebrahimpour, A., Abdul-Hamid, A., Ismail, A., & Saari, N. (2015). Angiotensin-I converting enzyme (ACE) inhibitory and anti-oxidant activities of sea cucumber (Actinopyga lecanora) hydrolysates. International Journal of Molecular Sciences, 16, 28870-28885.
Giraud-Guille, M.M., Besseau, L., Chopin, C., Durand, P., & Herbage, D. (2000). Structural aspects of fish skin collagen which forms ordered arrays via liquid crystalline states. Biomaterial, 21, 899-906.
Gómez-Ruiz, J.A., Ramos, M., & Recio, I. (2007). Identification of novel angiotensin-converting enzyme-inhibitory peptides from ovine milk proteins by CE-MS and chromatographic techniques. Electrophoresis, 28, 4202-4211.
He, H.L., Chen, X.L., Wu, H., Sun, C.Y., Zhang, Y.Z., & Zhou, B.C. (2007). High throughput and rapid screening of marine protein hydrolysates enriched in peptides with angiotensin-I-converting enzyme inhibitory activity by capillary electrophoresis. Bioresource Technology, 98, 3499-3505.
Himaya, S.W.A., Ngo, D.H., Ryu, B., & Kim, S.K. (2012). An active peptide purified from gastrointestinal enzyme hydrolysate of Pacific cod skin gelatine attenuates angiotensin-1 converting enzyme (ACE) activity and cellular oxidative stress. Food Chemistry, 132, 1872-1882.
Je, J.Y., Park, P.J., & Kim, S.K. (2005). Antioxidant activity of a peptide isolated from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. Food Research International, 38, 45-50.
Jia, J., Zhou, Y., Lu, J., Chen, A., Li, Y., & Zheng, G. (2010). Enzymatic hydrolysis of Alaska Pollack (Theragra chalcogramma) skin and antioxidant activity of the resulting hydrolysates. Journal of the Science of Food and Agriculture, 90, 635-640.
Kimura, S. (1992). Wide distribution of the skin type I collagen α3 chain in bony fish. Comparative Biochemistry and Physiology Part B, 102, 255-260.
Kittiphattanabawon, P., Benjukul, S., Sinthusamran, S., & Kishimura, Hideki. (2015). Characteristics of collagen from the skin of clown featherback (Chitala ornata). International Journal of Food Science and Technology, 50, 1972-1978.
Kittiphattanabawon, P., Benjukul, S., Visessanguan, W., Nagai, T., & Tanaka, M. (2005). Characterisation of acid- soluble collagen from skin and bone of bigeye snaper (Priacanthus tayenus). Food Chemistry, 89, 363-372.
Kuo, P.L., & Pu, C. (2011). The contribution of depression to mortality among elderly with self-reported hypertension: Analysis using a national representative longitudinal survey. Journal of Hypertension, 29, 2084-2090.
Laemmli, U.K. (1970). Cleavage of structural proteins during assembly head of bacteriophage T4. Nature, 277, 680-685.
Lee, J.K., Hong, S., Jeon, J.K., Kim, S.K., & Byun, H.G. (2009). Purification and characterization of angiotensin I converting enzyme inhibitory peptides from the rotifer, Brachionus rotundiformis. Bioresource Technology, 100, 5255-5259.
Lee, S.H., Qian, Z.J., & Kim, S.K. (2010). A novel angiotensin I converting enzyme inhibitory peptide from tuna frame protein hydrolysates and its antihypertensive effect in spontaneously hypertensive rats. Food Chemistry, 118, 96-102.
Liu, Q., Kong, B., Xiong, Y.L., & Xia, X. (2010). Antioxidant activity and functional properties of porcine plasma protein hydrolysates influenced by the degree of hydrolysis. Food Chemistry, 118, 403-410.
Nagai, T., & Suzuki, N. (2000a). Isolation of collagen from fish waste material-skin, bone and fins. Food Chemistry, 68, 277-281.
Nagai, T., & Suzuki, N. (2000b). Preparation and characterization of several fish bone collagens. Journal of Food Biochemistry, 24, 427-436.
Ngo, D.H., Qian, Z.J., Ryu, B., Park, J.W., & Kim, S.K. (2010). In vitro antioxidant activity of a peptide isolated from Nile tilapia (Oreochromis niloticus) scale gelatin in free radical-mediated oxidative systems. Journal of Functional Foods, 2, 107-117.
Park, P.J., Je, J.Y., & Kim, S.K. (2003). Angiotensin I converting enzyme (ACE) inhibitory activity of hetero-chitooligosaccharides prepared from partially different deacetylated chitosans. Journal of Agriculture and Food Chemistry, 51, 4930-4934.
Pazinatto, C., Malta, L.G., Pastore, G.M., & Netto, F.M. (2013). Antioxidant capacity of amaranth products: effects of thermal and enzymatic treatments. Food Science and Technology, 33, 485-493.
Philanto, L. (2000). Bioactive peptides derived from bovine whey proteins: Opioid and ace-inhibitory. Trends in Food Science and Technology, 11, 347-356.
Piyadhammaviboon, P., Wongngam, W., Benjakul, S., & Yongsawatdigul, J. (2012). Antioxidant and angiotensin-converting enzyme inhibitory activities of protein hydrolysates prepared from threadfin bream (Nemipterus spp.) surimi byproducts. Journal of aquatic food product technology, 21, 265-278.
Rajapakse, N., Mendis, E., Byun, H.G., & Kim, S.K. (2005). Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems. The Journal of Nutritional Biochemistry, 16, 562-569.
Ranathunga, S., Rajapakse, N., & Kim, S.K. (2006). Purification and characterization of antioxidative peptide derived from muscle of conger eel (Conger myriaster). European Food Research and Technology, 222, 310-315.
Saiga, A., Iwai, K., Hayakawa, T., Takahata, Y., Kitamura, S., Nishimura, T., & Morimatsu, F. (2008). Angiotensin I-converting enzyme-inhibitory peptides obtained from chicken collagen hydrolysate. Journal of Agricultural and Food Chemistry, 56, 9586-9591.
Shimada, K., Fujikawa, K., Yahara, K., & Nakamura, T. (1992). Antioxidative properties of xanthan on the antioxidation of soybean oil in cyclodextrin emulsion. Journal of Agricultural and Food Chemistry, 40, 945-948.
Sica, M.D., & Domenic, A. (2003). Combination angiotensin-converting enzyme inhibitor and angiotensin receptor blocker therapy: its role in clinical practice. Journal of Clinical Hyperttension, 5, 414-420.
Siepen, J.A., Keevil, E.J., Knight, D., & Hubbard, S.J. (2007). Prediction of missed cleavage sites in tryptic peptides aids protein identification in proteomics. Journal of Proteome Research, 6, 399-408.
Simpson, B.K. (2000). Digestive proteinases from marine animals. In N.M. Haard, & B.K. Simpson. (Eds.), Seafood enzymes: Utilization and influence on postharvest seafood quality. (pp. 531-540). New York: Marcel Dekker.
Singh, P., Benjakul, S., Maqsood, S., & Kishimura, H. (2011). Isolation and characterisation of collagen extracted from the skin of striped catfish (Pangasianodon hypophthalmus). Food Chemistry, 124,
97-105.
Thahom, N., & Sompongse, W. (2015). Characterisation of acid-soluble collagen from skin of grey featherback (Notopterus notopterus). Thai Journal of Science and Technology, 23, 257-267. (in Thai)
Umayaparvathi, S., Meenakshi, S., Vimalraj, V., Arumugama, M., Sivagami, G., & Balasubramaniana, T. (2014). Antioxidant activity and anticancer effect of bioactive peptide from enzymatic hydrolysate of oyster (Saccostrea cucullata). Biomedicine and Preventive Nutrition, 4, 343–353.
Venskutonis, P.R. (2014). Natural antioxidants in food systems. In G. Bartosz. (Eds.), Food oxidants and antioxidants: chemical, biological, and functional properties. (pp. 235-301). New York: CRC Press.
Wang, B., Wang, Y.M., Chi, C.F., Luo, H.Y., Deng, S.G., & Ma, J.Y. (2013). Isolation and characterization of collagen and antioxidant collagen peptides from scales of croceine croaker (Pseudosciaena crocea). Marine Drugs, 11, 4641-4661.
Wiriyaphan, C., Chitsomboon, B., & Yongsawadigul, J. (2012). Antioxidant activity of protein hydrolysates derived from threadfin bream surimi byproducts. Food Chemistry, 132, 104-111.
You, L., Zhao, M., Regenstein, J.M., & Ren, J. (2010). Changes in the antioxidant activity of loach (Misgurnus anguillicaudatus) protein hydrolysates during a simulated gastrointestinal digestion. Food Chemistry, 120, 810-816.
Zambrowicz, A., Pokora, M., Eckert, E., Szoltysik, M., Dbrowska, A., Chrzanowska, J., & Trziszka, T. (2012). Antioxidant and antimicrobial activity of lecithin free egg yolk protein preparation hydrolysates obtained with digestive enzymes. Functional Foods in Health and Disease, 2, 487-500.
Zeng, S.K., Zhang, C.H., Lin, H., Yang, P., Hong, P.Z., & Jiang, Z. (2009). Isolation and characterisation of acid-solubilised collagen from the skin of Nile tilapia (Oreochromis niloticus). Food Chemistry, 116,
879-
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2018-02-09
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