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Extraction and Characterisation of Pepsin-Solubilised Collagen from Fins, Scales, Skins, Bones and Swim Bladders of Bighead Carp

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Extraction and Characterisation of Pepsin-Solubilised Collagen from Fins, Scales, Skins, Bones and Swim Bladders of Bighead Carp Food Chemistry xxx (2012) xxx–xxx Contents lists available at SciVerse ScienceDirect Food Chemistry journal homepage: www.elsevier.com/locate/foodchem Extraction and characterisation of pepsin-solubilised collagen from fins, scales, skins, bones and swim bladders of bighead carp (Hypophthalmichthys nobilis) ⇑ Dasong Liu a, Li Liang a, Joe M. Regenstein b, Peng Zhou a, a State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu Province 214122, China b Department of Food Science, Cornell University, Ithaca, NY 14853-7201, USA article info abstract Article history: The objective of this study was to extract and characterise pepsin-solubilised collagens (PSC) from the Received 26 September 2011 fins, scales, skins, bones and swim bladders of bighead carp and to provide a simultaneous comparison Received in revised form 15 December 2011 of five different sources from one species. The PSC were mainly characterised as type I collagen, contain- Accepted 7 February 2012 ing two a-chains, and each maintained their triple helical structure well. The thermostability of PSC from Available online xxxx the internal tissues (swim bladders and bones) was slightly higher than that of PSC from the external tissues (fins, scales and skins). The peptide hydrolysis patterns of all PSC digests using the V8 protease Keywords: were similar. All PSC were soluble at acidic pH (1–6) and lost their solubility at NaCl concentrations above Collagen 30 g/l. The resulting PSC from the five tissues would all be potentially useful commercially. Pepsin Bighead carp Ó 2012 Elsevier Ltd. All rights reserved. Fins Scales Skins Bones Swim bladders V8 protease 1. Introduction nicity (Liu, Li, Miao, & Wu, 2009). However, the outbreaks of bovine sponge encephalopathy (BSE), transmissible spongiform encepha- Collagen is the major structural proteins in vertebrates and con- lopathy (TSE), foot-and-mouth disease (FMD) and avian influenza stitutes about 30% of the total animal’s protein (Muyonga, Cole, & have raised anxiety among some consumers of collagen and Duodu, 2004). It is unique in its ability to form insoluble fibres with collagen-derived products from these land-based animals. Further- high tensile strength and stability, and also in its right-handed tri- more, porcine collagen and other collagens from animals that were ple superhelical structure consisting of three similarly sized left- not religiously slaughtered are unacceptable to some religious and handed helical polypeptide chains with a Gly-X–Y repeating motif, ethnic groups, such as Jews and Muslims (Regenstein & Zhou, 2007). in which the X and Y positions are often occupied by proline and Therefore, the global demand for collagen from alternative sources hydroxyproline, respectively (Gelse, Pöschl, & Aigner, 2003). At such as aquatic animals has been increasing over the years. With the present, at least 29 collagen types have been identified, and each rapid development of the fish processing industry in China, large differs considerably in their sequence, structure and function quantities of by-products are generated, accounting for 50–70% (McCormick, 2009). They are widely distributed in the skins, bones, of the original raw material (Kittiphattanabawon, Benjakul, tendons, vascular system and intramuscular connective tissue, Visessanguan, Nagai, & Tanaka, 2005). Consequently, optimal use where they contribute to the stability and structural integrity of of these by-products is a promising way to protect the environment, these tissues and organs (Gelse et al., 2003). Particularly, type I col- to produce value-added products to increase the revenue to the fish lagen is found in all vertebrae connective tissues (Nagai, Suzuki, & processors, and to create new job/business opportunities. Nagashima, 2008). Research on the extraction and characterisation of collagen from Commonly isolated from by-products of land-based animals, by-products of marine animals has been reported (Ahmad & such as cows, pigs and poultry, collagen has been widely used in Benjakul, 2010; Jongjareonrak, Benjakul, Visessanguan, Nagai, & the food, pharmaceutical, and cosmetic industries because of its Tanaka, 2005; Kittiphattanabawon et al., 2005; Liu, Oliveira, & Su, excellent biocompatibility and biodegradability, and weak antige- 2010; Saito, Kunisaki, Urano, & Kimura, 2002). However, informa- tion regarding the preparation of collagen from freshwater fish is limited (Wang, Yang, Wang, & Du, 2008), and none of the work ⇑ Corresponding author. Tel./fax: +86 510 85912123. has characterised the collagen from different tissues of bighead E-mail address: [email protected] (P. Zhou). carp. 0308-8146/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodchem.2012.02.032 Please cite this article in press as: Liu, D., et al. Extraction and characterisation of pepsin-solubilised collagen from fins, scales, skins, bones and swim bladders of bighead carp (Hypophthalmichthys nobilis). Food Chemistry (2012), doi:10.1016/j.foodchem.2012.02.032 2 D. Liu et al. / Food Chemistry xxx (2012) xxx–xxx Bighead carp, native to Asia, is one of the ‘‘four major cultured modifications. All procedures were performed in a walk-in chill fish species’’ along with black carp, grass carp and silver carp room at a temperature no higher than 4 °C. grown in China (Wang, Yang et al., 2008), and it has been intro- duced into more than 70 other countries in Europe, South America, 2.3.1. Fin, bone and scale collagen and North America. In the United States, it is regarded as a highly To remove the non-collagenous proteins and pigments, the fins destructive invasive species. and bones (0.5 kg) were soaked in 0.1 M NaOH at a sample/alkaline Pepsin is able to cleave the cross-linked regions at the telopep- solution ratio of 1:10 (w/v). The mixture was stirred for 36 h using tide without damaging the integrity of the triple-helix and hence the C-MAG HS7 magnetic stirrer (IKA Werke GmbH & Co. KG, the extraction of collagen with limited pepsin digestion contrib- Staufen, Germany), changing the alkaline solution every 12 h. Sub- utes to a higher yield (Heu et al., 2010). To make better use of this sequently, the treated samples were decalcified with 0.5 M EDTA fish, the present study was conducted to extract and characterise (pH 7.5) at a sample/EDTA solution ratio of 1:10 (w/v) for 5 days, pepsin-solubilised collagens (PSC) from bighead carp fins, scales, with the EDTA solution being changed every day. Then the residues skins, bones and swim bladders and to provide a simultaneous were suspended in 10% (v/v) butyl alcohol to remove fat at a comparison of five different sources from one species at one time. sample/solution ratio of 1:10 (w/v) for 36 h with a change of solu- tion every 12 h. After being fully washed with cold distilled water, 2. Materials and methods the residues were extracted with 0.5 M acetic acid containing 0.1% (w/v) pepsin at a sample/solution ratio of 1:10 (w/v) for 3 days. The 2.1. Chemicals and enzymes suspension was then centrifuged at 12,500g for 40 min at 4 °C using an Avanti J-E centrifuge (Beckman Coulter, Inc., Indianapolis, All chemicals used were of analytical grade. Pepsin from porcine IN, USA), and the supernatant was salted-out by adding NaCl to a gastric mucosa (EC 3.4.23.1; 2 Â crystallised and lyophilised; final concentration of 2.0 M. The resultant precipitate was 2800 U/mg dry matter based on haemoglobin hydrolysis; Sigma– collected by centrifugation at 12,500g for 40 min at 4 °C and then Aldrich Co., St. Louis, MO, USA); Staphylococcus aureus V8 protease dissolved in 0.5 M acetic acid at a sample/solution ratio of 1:10 (EC 3.4.21.19; lyophilised; 500–1000 U/mg based on the hydrolysis (w/v). The resulting solution was salted-out again with NaCl at a of N-t-Boc-L-glutamic acid a-phenyl ester; Sigma–Aldrich Co.); final concentration of 2.0 M, and the precipitate was collected bovine serum albumin (Sigma–Aldrich Co.); high molecular weight and redissolved in 0.5 M acetic acid under the same conditions (MW) markers (manufacturer’s specified MW: myosin, 220 kDa; employed above. The final solution was dialysed against cold dis- a2-macroglobulin, 170 kDa; b-galactosidase, 116 kDa; transferrin, tilled water using a dialysis bag with a nominal manufacturer’s 76 kDa; glutamic dehydrogenase, 53 kDa) were obtained from GE specified MW cut-off of 7 kDa (Shanghai Green Bird Science and Healthcare UK Ltd. (Amersham, Buckinghamshire, UK); Precision Technology Development Co., Shanghai, China) and then lyophi- Plus Protein All Blue Standards (Bio-Rad Laboratories, Inc., Hercules, lised using the Labconco freeze dryer (Labconco Corp., Kansas, CA, USA) consisted of a cocktail of pre-stained proteins with the MO, USA). The yield was calculated on the basis of the wet weight manufacturer’s specified MW of 10, 15, 20, 25, 37, 50, 75, 100, of the fins and bones, respectively. 150, and 250 kDa; sodium dodecyl sulphate (SDS), N,N,N0,N0-tetra- The procedures for extraction of PSC from the scales (0.5 kg) methyl ethylene diamine (TEMED), tris(hydroxymethyl)amino- were slightly different in that the times for decalcification was methane, acrylamide and bisacrylamide were purchased from shorten to 3 days, and the step for removing fat was omitted. Sangon Biotech Co., Ltd. (Shanghai, China). 2.3.2. Skin and swim bladder collagen 2.2. Preparation of fish fins, scales, skins, bones and swim bladders The skins and swim bladders (0.125 kg) were soaked in 0.1 M NaOH for 36 h, with the alkaline solution being changed every Live farmed bighead carps (Hypophthalmichthys nobilis), with 12 h. During alkaline treatment, the skins and swim bladders weights ranging from 2 to 3 kg, were obtained in the spring from would swell, and a sample/alkaline solution ratio of 1:30 (w/v) a local market in Wuxi, Jiangsu Province, China.
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