Isolation and characterisation of acid- and pepsin-soluble collagen from the skin of Cervus korean TEMMINCK var. mantchuricus Swinhoe
Gaurav Lodhi A , Yon-Suk Kim A , Eun-Kyung Kim B , Jin-Woo Hwang A , Hyung-Sik Won A , Whangi Kim C , Sang-Ho Moon D , Byong-Tae Jeon D and Pyo-Jam Park A D E
+ Author Affiliations
- Author Affiliations
A Department of Biotechnology, Konkuk University, Chungju, 27478, Korea.
B Division of Food Bio Science, College of Biomedical and Health Sciences, Konkuk University, Chungju 27478, Korea.
C Department of Applied Chemistry, Konkuk University, Chungju, 27478, Korea.
D Nokyong Research Centre, Konkuk University, Chungju, 27478, Korea.
E Corresponding author. Email: parkpj@kku.ac.kr
Animal Production Science 58(3) 585-594 https://doi.org/10.1071/AN16143
Submitted: 7 March 2016 Accepted: 8 September 2016 Published: 20 June 2017
Abstract
Acid-soluble collagen and pepsin-soluble collagen were extracted from the skin of deer, Cervus korean TEMMINCK var. mantchuricus Swinhoe. The two types of collagen were then characterised using sodium dodecyl sulfate–polyacrylamide gel electrophoresis, amino acid composition analysis, peptide hydrolysis patterns, thermal denaturation temperature, differential scanning calorimetry, Fourier transform infrared spectroscopy, and nuclear magnetic resonance imaging. The yield of pepsin-soluble collagen (9.62%) was greater than that of acid-soluble collagen (2.24%), but both types of collagen showed similar electrophoretic patterns with each other and with calf skin collagen. The peptide hydrolysis pattern results suggested that calf skin collagen and pepsin-soluble collagen from deer skin may be similar in terms of their primary structure. The thermal denaturation temperature of acid-soluble collagen and pepsin-soluble collagen were 36.67°C and 36.44°C, respectively, and their melting temperatures were 110°C and 120°C, respectively, which suggest high thermal stability. Fourier transform infrared showed a triple helical structure and nuclear magnetic resonance confirmed the presence of ‘hydration’ water. These results provide a basis for large-scale production and further application as alternatives to other mammalian collagens.
Additional keywords: characterisation, collagen, deer skin, extraction.
References
AOAC (1995) ‘Official methods of analysis.’ 16th edn. (Association of Official Analytical Chemists: Washington, DC)Bae I, Osatomi K, Yoshida A, Osako K, Yamaguchi A, Hara K (2008) Biochemical properties of acid-soluble collagens extracted from the skins of underutilised fishes. Food Chemistry 108, 49–54.
| Biochemical properties of acid-soluble collagens extracted from the skins of underutilised fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVGksA%3D%3D&md5=93d878e2a5082520948512f6d21fb2f8CAS |
Belitz HD, Grosch W, Schieberle P (2009) ‘Food chemistry.’ 4th edn. (Springer-Verlag: Berlin)
Bundi A, Wuethrich K (1979) Proton NMR parameters of the common amino acid residues measured in aqueous solutions of the linear tetrapeptides H-Gly-Gly- X–L-Ala-OH. Biopolymers 18, 285–297.
| Proton NMR parameters of the common amino acid residues measured in aqueous solutions of the linear tetrapeptides H-Gly-Gly- X–L-Ala-OH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhvVOgsL0%3D&md5=079895dddb6690dc891a31398f5aba79CAS |
Burghagen M (1999) Collagen. In ‘Food chemistry’. (Eds HD Belitz, W Grosch) pp. 540–547. (Springer-Verlag: Berlin)
Doyle BB, Bendit EG, Blout ER (1975) Infrared spectroscopy of collagen and collagen-like polypeptides. Biopolymers 14, 937–957.
| Infrared spectroscopy of collagen and collagen-like polypeptides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXktl2jur8%3D&md5=ee08fb36617d4ec2eb2118a5e2267343CAS |
Fox MA (2008) Novel roles for collagens in wiring the vertebrate nervous system. Current Opinion in Cell Biology 20, 508–513.
| Novel roles for collagens in wiring the vertebrate nervous system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyks73P&md5=e7abdb323eb600084fb1fcf93f766ef8CAS |
Fullerton GD, Nes E, Amurao M, Rahal A, Krasnosselskaia L, Cameron I (2006) An NMR method to characterize multiple water compartments on mammalian collagen. Cell Biology International 30, 66–73.
| An NMR method to characterize multiple water compartments on mammalian collagen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsF2ntrk%3D&md5=c01d3e0cf0cb82e7cb7ba7dca740d9d3CAS |
Gómez-Guillén MC, Giménez B, López-Caballero ME, Montero MP (2011) Functional and bioactive properties of collagen and gelatin from alternative sources: a review. Food Hydrocolloids 25, 1813–1827.
| Functional and bioactive properties of collagen and gelatin from alternative sources: a review.Crossref | GoogleScholarGoogle Scholar |
Heino J, Huhtala M, Käpylä J, Johnson MS (2009) Evolution of collagen based adhesion systems. The International Journal of Biochemistry & Cell Biology 41, 341–348.
| Evolution of collagen based adhesion systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCgsL7I&md5=e97a9473078d5073619bb68997216ebaCAS |
Ichikawa S, Morifuji M, Ohara H, Matsumoto H, Takeuchi Y, Sato K (2010) Hydroxyproline-containing dipeptides and tripeptides quantified at high concentration in human blood after oral administration of gelatin hydrolysate. International Journal of Food Sciences and Nutrition 61, 52–60.
| Hydroxyproline-containing dipeptides and tripeptides quantified at high concentration in human blood after oral administration of gelatin hydrolysate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVCnuw%3D%3D&md5=63dd08fdc9238dcc25c2fde6f3e95b91CAS |
Ikoma T, Kobayashi H, Tanaka J, Walsh D, Mann S (2003) Physical properties of type I collagen extracted from fish scales of Pagrus major and Oreochromis niloticas. International Journal of Biological Macromolecules 32, 199–204.
| Physical properties of type I collagen extracted from fish scales of Pagrus major and Oreochromis niloticas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvVygsL0%3D&md5=97eee924cd000c85a79bb8131abd1206CAS |
Jongjareonrak A, Benjakul S, Visessanguan W, Nagai T, Tanaka M (2005) Isolation and characterization of acid and pepsin-solubilized collagens from the skin of brownstripe red snapper (Lutjanus vitta). Food Chemistry 93, 475–484.
| Isolation and characterization of acid and pepsin-solubilized collagens from the skin of brownstripe red snapper (Lutjanus vitta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksV2isLk%3D&md5=5a735e84eb85c5fdaec312c5b2455757CAS |
Kimura S (1992) Wide distribution of the skin type I collagen α3 chain in bony fish. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 102, 255–260.
| Wide distribution of the skin type I collagen α3 chain in bony fish.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zhsFKhtQ%3D%3D&md5=a73b9a5f5af8a694f2236cfaab5cbc8fCAS |
Kimura S, Zhu XP, Matsui R, Shijoh M, Takamizawa S (1988) Characterization of fish muscle type I collagen. Journal of Food Science 53, 1315–1318.
| Characterization of fish muscle type I collagen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXmtV2rs7c%3D&md5=3e6efbcd085bb10b54dc09e19624c102CAS |
Kittiphattanabawon P, Benjakul S, Visessanguan W, Nagai T, Tanaka M (2005) Characterisation of acid-soluble collagen from skin and bone of bigeye snapper (Priacanthus tayenus). Food Chemistry 89, 363–372.
| Characterisation of acid-soluble collagen from skin and bone of bigeye snapper (Priacanthus tayenus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVGit7Y%3D&md5=543c2c9570c64e945e2fc2c3a069be1cCAS |
Kittiphattanabawon P, Benjakul S, Visessanguan W, Shahidi F (2010) Isolation and characterization of collagen from the cartilages of brownbanded bamboo shark (Chiloscyllium punctatum) and blacktip shark (Carcharhinus limbatus). LWT-Food Science and Technology 43, 792–800.
| Isolation and characterization of collagen from the cartilages of brownbanded bamboo shark (Chiloscyllium punctatum) and blacktip shark (Carcharhinus limbatus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1OktLY%3D&md5=bd2964a6bfc0eda3aa26f25d01b385d9CAS |
Krimm S, Bandekar J (1986) Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Advances in Protein Chemistry 38, 181–364.
| Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhsVOmsQ%3D%3D&md5=7906aecf3a9c588ef9d42c251b7a48b0CAS |
Laemmli UK (1970) Cleavage of structural proteins during assembly of head of bacteriophage T4. Nature 227, 680–685.
| Cleavage of structural proteins during assembly of head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFags7s%3D&md5=82c0146fed66f8769ce37163b9c83c1eCAS |
Lin YK, Lin TY, Su HP (2011) Extraction and characterisation of telopeptide-poor collagen from porcine lung. Food Chemistry 124, 1583–1588.
| Extraction and characterisation of telopeptide-poor collagen from porcine lung.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Sns7vK&md5=aa95df56088a81eec0191bbad69079a7CAS |
Liu D, Liang L, Regenstein JM, Zhou P (2012) Extraction and characterisation of pepsin-solubilized collagen from fins, scales, skins, bones and swim bladders of bighead carp (Hypophthalmichthys nobilis). Food Chemistry 133, 1441–1448.
| Extraction and characterisation of pepsin-solubilized collagen from fins, scales, skins, bones and swim bladders of bighead carp (Hypophthalmichthys nobilis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1egtrk%3D&md5=e1d20563f596b27cf53ab33fa2abdf06CAS |
Muyonga JH, Cole CGB, Duodu KG (2004) Characterization of acid soluble collagen from skin of young and adult Nile perch (Lates nilotics). Food Chemistry 85, 81–89.
| Characterization of acid soluble collagen from skin of young and adult Nile perch (Lates nilotics).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFGjtLw%3D&md5=a60f7a8d1698cb5b803cabb78eaa6197CAS |
Nagai T, Suzuki N (2002) Preparation and partial characterization of collagen from paper nautilus (Argonauta argo, Linnaeus) outer skin. Food Chemistry 76, 149–153.
| Preparation and partial characterization of collagen from paper nautilus (Argonauta argo, Linnaeus) outer skin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptlajt7k%3D&md5=40c4dc59ecc18b3380e46493097965dbCAS |
Nagai T, Araki Y, Suzuki N (2002) Collagen of the skin of ocellate puffer fish (Takifugu rubripes). Food Chemistry 78, 173–177.
| Collagen of the skin of ocellate puffer fish (Takifugu rubripes).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlslyltro%3D&md5=ba4828fcd1ee9008888c714ef4d4ff75CAS |
Nagai T, Suzuki N, Nagashima T (2008) Collagen from common minke whale (Balaenoptera acutorostrata) unesu. Food Chemistry 111, 296–301.
| Collagen from common minke whale (Balaenoptera acutorostrata) unesu.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsFehtLs%3D&md5=e817929ec0b9b8a80f960abda8aedeb8CAS |
Ogawa M, Portier RJ, Moody MW, Bell J, Schexnayder MA, Losso JN (2004) Biochemical properties of bone and scale collagens isolated from the subtropical fish black drum (Pogonia cromis) and sheepshead seabream (Archosargus probatocephalus). Food Chemistry 88, 495–501.
| Biochemical properties of bone and scale collagens isolated from the subtropical fish black drum (Pogonia cromis) and sheepshead seabream (Archosargus probatocephalus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFarsLk%3D&md5=cd460c7ae8ad50861f4bb558ca6685f8CAS |
Payne KJ, Veis A (1988) Fourier transform IR spectroscopy of collagen and gelatin solutions: deconvolution of the amide I band for conformational studies. Biopolymers 27, 1749–1760.
| Fourier transform IR spectroscopy of collagen and gelatin solutions: deconvolution of the amide I band for conformational studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXjs1eguw%3D%3D&md5=dafe1fb2262abe0bb39baf7ad3d2dc41CAS |
Piez KA (1965) Characterization of a collagen from codfish skin containing three chromatographically different α chains. Biochemistry 4, 2590–2596.
| Characterization of a collagen from codfish skin containing three chromatographically different α chains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28XitVyitA%3D%3D&md5=3ceee555587834fd581665566b15c453CAS |
Rault I, Frei V, Herbage D, Abdul-Malak N, Huc A (1996) Evaluation of different chemical methods for cross-linking collagen gel, films and sponges. Journal of Materials Science. Materials in Medicine 7, 215–221.
| Evaluation of different chemical methods for cross-linking collagen gel, films and sponges.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisVWjt74%3D&md5=e4ebaa0f5d271354f87f9c96c4cff32dCAS |
Regenstein JM, Zhou P (2007) Collagen and gelatin from marine by-product. In ‘Maximising the value of marine by-products’. (Ed. F Shahidi) pp. 279–303. (CRC Press: Boca Raton, FL)
Safandowska M, Pietrucha K (2013) Effect of fish collagen modification on its thermal and rheological properties. International Journal of Biological Macromolecules 53, 32–37.
| Effect of fish collagen modification on its thermal and rheological properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2kurnM&md5=b8436c9420dc5ef4924f8f23204e3fa6CAS |
Saito M, Kunisaki N, Urano N, Kimura S (2002) Collagen as the major edible component of sea cucumber (Stichopus japonicus). Journal of Food Science 67, 1319–1322.
| Collagen as the major edible component of sea cucumber (Stichopus japonicus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVyqsLc%3D&md5=ac66fc6b10e150ba496494ccb9f9784fCAS |
Senaratne LS, Park PJ, Kim SK (2006) Isolation and characterization of collagen from brown backed toadfish (Lagocephalus gloveri) skin. Bioresource Technology 97, 191–197.
| Isolation and characterization of collagen from brown backed toadfish (Lagocephalus gloveri) skin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVanurnJ&md5=535ee94324f7e17ab8ac9fca03918b1bCAS |
Su XR, Sun B, Li YY, Hua QH (2009) Characterization of acid-soluble collagen from the coelomic wall of Sipunculida. Food Hydrocolloids 23, 2190–2194.
| Characterization of acid-soluble collagen from the coelomic wall of Sipunculida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFCktr3P&md5=f641c4492a4da82c45625797b82b8772CAS |
Surewicz WK, Mantsch HH (1988) New insight into protein secondary structure from resolution enhanced infrared spectra. Biochimica et Biophysica Acta 952, 115–130.
| New insight into protein secondary structure from resolution enhanced infrared spectra.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhtVyqtLY%3D&md5=c6dbf038d049e63fee72f75ebdf46c43CAS |
Swatschek D, Schatton W, Kellermann J, Muller WEG, Kreuter J (2002) Marine sponge collagen: isolation, characterization and effects on the skin parameters surface-pH, moisture and sebum. European Journal of Pharmaceutics and Biopharmaceutics 53, 107–113.
| Marine sponge collagen: isolation, characterization and effects on the skin parameters surface-pH, moisture and sebum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltFGg&md5=87b4d82703c68a7fea8aac9b029568e0CAS |
Thuy LTM, Okazaki E, Osako K (2014) Isolation and characterization of acid-soluble collagen from the scales of marine fishes from Japan and Vietnam. Food Chemistry 149, 264–270.
| Isolation and characterization of acid-soluble collagen from the scales of marine fishes from Japan and Vietnam.Crossref | GoogleScholarGoogle Scholar |
Uriarte-Montoya MH, Arias-Moscoso JL, Plascencia-Jatomea M, Santacruz-Ortega H, Rouzaud-Sández O, Cardenas-Lopez JL, Marquez-Rios E, Ezquerra-Brauer JM (2010) Jumbo squid (Dosidicus gigas) mantle collagen: extraction, characterization, and potential application in the preparation of chitosan-collagen biofilms. Bioresource Technology 101, 4212–4219.
| Jumbo squid (Dosidicus gigas) mantle collagen: extraction, characterization, and potential application in the preparation of chitosan-collagen biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlWrtro%3D&md5=6e0e03ebf42fb962de6a13a8c71799a9CAS |
Usha R, Ramasami T (2004) The effects of urea and n-propanol on collagen denaturation: using DSC, circular dichroism and viscosity. Thermochimica Acta 409, 201–206.
| The effects of urea and n-propanol on collagen denaturation: using DSC, circular dichroism and viscosity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvFGhtr8%3D&md5=11c6610e43fc73fa1bdcb53bc2b6143bCAS |
Zeng S, Yin J, Yang S, Zhang C, Yang P, Wu W (2012) Structure and characteristics of acid and pepsin-solubilized collagens from the skin of cobia (Rachycentron canadum). Food Chemistry 135, 1975–1984.
| Structure and characteristics of acid and pepsin-solubilized collagens from the skin of cobia (Rachycentron canadum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlSlsrnF&md5=8aa615593f1a13cf03d6bab1d5c55f03CAS |
Zhang Y, Liu WT, Li GY, Shi B, Miao YQ, Wu XH (2007) Isolation and characterization of pepsin soluble collagen from the skin of grass carp (Ctenopharyngodon idella). Food Chemistry 103, 906–912.
| Isolation and characterization of pepsin soluble collagen from the skin of grass carp (Ctenopharyngodon idella).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitFSksbo%3D&md5=2776ab1148153f2b1e182784d3c7f6cfCAS |
Zhang J, Duan R, Huang L, Song Y, Regenstein JM (2014) Characterisation of acid-soluble and pepsin-solubilized collagen from jellyfish (Cyanea nozakii Kishinouye). Food Chemistry 150, 22–26.
| Characterisation of acid-soluble and pepsin-solubilized collagen from jellyfish (Cyanea nozakii Kishinouye).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOltb3J&md5=8e4471b2923a0b57da6984e06abe4caaCAS |
