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Structural Properties and Biological Activities of Collagens from Four Main Processing By-Products (Skin, Fin, Cartilage, Notochord) of Sturgeon (Acipenser gueldenstaedti)

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Abstract

During the processing of sturgeon, large amounts of by-products, such as skin, fin, cartilage, and notochord, are produced. These by-products have not been effectively used, resulting in a serious waste of sturgeon resources. In this study, we aimed to obtain the collagen from these by-products and evaluate the fibril-forming characteristics of the collagen molecules and the antioxidant activity of the collagen peptides. The structural properties of pepsin-soluble collagen were analyzed by SDS-PAGE and FTIR. Collagen fibril-forming characteristics were detected by turbidity assay and SEM observation. The antioxidant activities of collagen peptides were determined by Hydroxyl and ABTS radical scavenging assays. SDS-PAGE results showed that the skin and fin collagens were characterized as type I collagen, and the cartilage and notochord collagens were characterized as type II collagen. Sturgeon type II collagens could only be self-assembled into fibrils at low phosphate ion concentration, whereas sturgeon type I collagens could be self-assembled into fibrils at long range of phosphate ion concentrations. The fibril-forming ability of sturgeon type I collagen was higher than that of porcine type I collagen. The fibril diameter of type I collagen was higher than that of type II collagen. The antioxidant activity of notochord and skin collagen peptides was higher than that of the other two collagen peptides. The results of this study will provide helpful information for the application of sturgeon collagen in the functional food and biomedical material industries. Meanwhile, it will promote the effective use of collagen from different sturgeon by-products.

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References

  1. Birstein, V.J., Bemis, W.E., Waldman, J.R.: The threatened status of acipenseriform species: a summary. Environ. Biol. Fish. 48, 427–435 (1997)

    Article  Google Scholar 

  2. Tavakoli, S., Luo, Y.K., Regenstein, J.M., Daneshvar, E., Bhatnagar, A., Tan, Y.Q., Hong, H.: Sturgeon, caviar, and caviar substitutes: from production, gastronomy, nutrition, and quality change to trade and commercial mimicry. Rev. fish. Sci. Aquac. 29, 753–768 (2021)

    Article  Google Scholar 

  3. Bronzi, P., Chebanov, M., Michaels, J.T., Wei, Q.W., Rosenthal, H., Gessner, J.: Sturgeon meat and caviar production: global update 2017. J. Appl. Ichthyol. 35, 257–266 (2019)

    Article  Google Scholar 

  4. Hurvitz, A., Jackson, K., Degani, G., Levavi-Sivan, B.: Use of endoscopy for gender and ovarian stage determinations in Russian sturgeon (Acipenser gueldenstaedtii) grown in aquaculture. Aquaculture 270, 158–166 (2007)

    Article  Google Scholar 

  5. Chen, Y.W., Cai, W.Q., Shi, Y.G., Dong, X.P., Bai, F., Shen, S.K., Jiao, R., Zhang, X.Y., Zhu, X.: Effects of different salt concentrations and vacuum packaging on the shelf stability of Russian sturgeon (Acipenser gueldenstaedti) stored at 4 °C. Food Control 109, 106865 (2020)

    Article  Google Scholar 

  6. Meng, D.W., Leng, X.Q., Zhang, Y., Luo, J., Du, H., Takagi, Y., Dai, Z.Y., Wei, Q.W.: Comparation of the structural characteristics and biological activities of chondroitin sulfates extracted from notochord and backbone of Chinese sturgeon (Acipenser sinensis). Carbohydr. Res. 522, 108685 (2022)

    Article  Google Scholar 

  7. Zhang, X., Ookawa, M., Tan, Y.K., Ura, K., Adachi, S., Takagi, Y.: Biochemical characterisation and assessment of fibril-forming ability of collagens extracted from Bester sturgeon Huso huso × Acipenser ruthenus. Food Chem. 160, 305–312 (2014)

    Article  Google Scholar 

  8. Meng, D.W., Tanaka, H., Kobayashi, T., Hatayama, H., Zhang, X., Ura, K., Yunoki, S., Takagi, Y.: The effect of alkaline pretreatment on the biochemical characteristics and fibril-forming abilities of types I and II collagen extracted from bester sturgeon by-products. Int. J. Biol. Macromol. 131, 572–580 (2019)

    Article  Google Scholar 

  9. Strueuli, C.: Extracellular matrix remodelling and cellular differentiation. Curr. Opin. Cell. Biol. 11, 634–640 (1999)

    Article  Google Scholar 

  10. Silver, F.H., Freeman, J.W., Seehra, G.P.: Collagen self-assembly and the development of tendon mechanical properties. J. Biomech. 36, 1529–1553 (2003)

    Article  Google Scholar 

  11. Kim, S.K., Mendis, E.: Bioactive compounds from marine processing byproducts—a review. Food Res. Int. 39, 383–393 (2006)

    Article  Google Scholar 

  12. Alves, A.L., Marques, A.L.P., Martins, E., Silva, T.H., Reis, R.L.: Cosmetic potential of marine fish skin collagen. Cosmetics 4, 4040039 (2017)

    Article  Google Scholar 

  13. Meng, D.W., Li, W., Ura, K., Takagi, Y.: Effects of phosphate ion concentration on in-vitro fibrillogenesis of sturgeon type I collagen. Int. J. Biol. Macromol. 148, 182–191 (2020)

    Article  Google Scholar 

  14. Curtis, A.S.G., Clark, P.: The effects of topographic and mechanical properties of materials on cell behavior. Crit. Rev. Biocompat. 5, 343–362 (1990)

    Google Scholar 

  15. Ahmed, M., Verma, A.K., Patel, R.: Collagen extraction and recent biological activities of collagen peptides derived from sea-food waste: a review. Sustain. Chem. Pharm. 18, 100315 (2020)

    Article  Google Scholar 

  16. Taghvaei, M., Jafari, S.M., Mahoonak, A.S., Nikoo, A.M., Rahmanian, N., Hajitabar, J., Meshginfar, N.: The effect of natural antioxidants extracted from plant and animal resources on the oxidative stability of soybean oil. LWT Food Sci. Technol. 56, 124–130 (2014)

    Article  Google Scholar 

  17. Mahapatra, S., Chakraborty, S., Majumdar, S., Bag, B., Roy, S.: Eugenol protects nicotine-induced superoxide mediated oxidative damage in murine peritoneal macrophages in vitro. Eur. J. Pharmacol. 623, 132–140 (2009)

    Article  Google Scholar 

  18. Zhao, X.C., Zhang, X.J., Liu, D.Y.: Collagen peptides and the related synthetic peptides: a review on improving skin health. J. Funct. Foods. 86, 104680 (2021)

    Article  Google Scholar 

  19. Sheng, Y., Qiu, Y.T., Wang, Y.M., Chi, C.F., Wang, B.: Novel antioxidant collagen peptides of Siberian Sturgeon (Acipenser baerii) cartilages: the preparation, characterization, and cytoprotection of H2O2-damaged human umbilical vein endothelial cells (HUVECs). Mar. Drugs. 20, 325 (2022)

    Article  Google Scholar 

  20. Nikoo, M., Benjakul, S., Xu, X.M.: Antioxidant and cryoprotective effects of Amur sturgeon skin gelatin hydrolysate in unwashed fish mince. Food Chem. 181, 295–303 (2015)

    Article  Google Scholar 

  21. Clowacki, J., Mizuno, S.: Collagen scaffolds for tissue engineering. Biopolymers 89, 338–344 (2007)

    Article  Google Scholar 

  22. Nalinanon, S., Benjakul, S., Visessanguan, W., Kishimura, H.: Use of pepsin for collagen extraction from the skin of bigeye snapper (Priacanthus tayenus). Food Chem. 104, 593–601 (2007)

    Article  Google Scholar 

  23. Meng, D.W., Li, W., Leng, X.Q., Takagi, Y., Dai, Z.Y., Du, H., Wei, Q.W.: Extraction of chondroitin sulfate and type II collagen from sturgeon (Acipenser gueldenstaedti) notochord and characterization of their hybrid fibrils. Process. Biochem. 124, 180–188 (2023)

    Article  Google Scholar 

  24. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277, 680–685 (1970)

    Article  Google Scholar 

  25. Atef, M., Ojagh, S.M., Latifi, A.M., Esmaeili, M., Udenigwe, C.C.: Biochemical and structural characterization of sturgeon fish skin collagen (Huso huso). J. Food Biochem. 44, e13256 (2020)

    Article  Google Scholar 

  26. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J.: Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951)

    Article  Google Scholar 

  27. Pan, X., Zhao, Y., Hu, F., Wang, B.: Preparation and identification of antioxidant peptides from protein hydrolysate of skate (Raja porosa) cartilage. J. Funct. Foods 25, 220–230 (2016)

    Article  Google Scholar 

  28. Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., Rice-Evans, C.: Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26, 1231–1237 (1999)

    Article  Google Scholar 

  29. Nagai, T.: Characterization of collagen from Japanese sea bass caudal fin as waste material. Eur. Food Res. Technol. 218, 424–427 (2004)

    Article  Google Scholar 

  30. Liu, D.S., Liang, L., Regenstein, J.M., Zhou, P.: Extraction and characterisation of pepsin-solubilised collagen from fins, scales, skins, bones and swim bladders of bighead carp (Hypophthalmichthys nobilis). Food Chem. 133, 1441–1448 (2012)

    Article  Google Scholar 

  31. Foegeding, E.A., Lanier, T.C., Hultin, H.O.: Food. Chem, Fennema, O. R. (ed.). Marcel Dekker Inc, New York, pp. 902–906 (1996)

  32. Saito, M., Takenouchi, Y., Kunisaki, N., Kimura, S.: Complete primary structure of rainbow trout type I collagen consisting of α1 (I) α2 (I) α3 (I) heterotrimers. Eur. J. Med. Chem. 268, 2817–2827 (2001)

    Google Scholar 

  33. Zhang, X., Adachi, S., Ura, K., Takagi, Y.: Properties of collagen extracted from Amur sturgeon Acipenser schrenckii and assessment of collagen fibrils in vitro. Int. J. Biol. Macromol. 137, 809–820 (2019)

    Article  Google Scholar 

  34. Liang, Q.F., Wang, L., Sun, W.H., Wang, Z.B., Xu, J.M., Ma, H.L.: Isolation and characterization of collagen from the cartilage of Amur sturgeon (Acipenser schrenckii). Process. Biochem. 49, 318–323 (2014)

    Article  Google Scholar 

  35. Li, S.W., Prockop, D.J., Helminen, H., Fassler, R., Lapvetelainen, T., Kiraly, K., Peltarri, A., Arokoski, J., Lui, H., Arita, M.: Transgenic mice with targeted inactivation of the Col2 alpha 1 gene for collagen II develop a skeleton with membranous and periosteal bone but no endochondral bone. Gene Dev. 9, 2821–2830 (1995)

    Article  Google Scholar 

  36. Medici, D., Olsen, B.R.: The role of endothelial–mesenchymal transition in heterotopic ossification. J. Bone Miner. 27, 1619–1622 (2012)

    Article  Google Scholar 

  37. Zhang, X., Shimoda, K., Ura, K., Adachi, S., Takagi, Y.: Developmental structure of the vertebral column, fins, scutes and scales in bester sturgeon, a hybrid of beluga Huso huso and sterlet Acipenser ruthenus. J. Fish. Bio. 81, 1985–2004 (2012)

    Article  Google Scholar 

  38. Leprévost, A., Azaïs, T., Trichet, A., Sire, J.Y.: Vertebral development and ossification in the siberian sturgeon (Acipenser Baerii), with new insights on bone histology and ultrastructure of vertebral elements and scutes. Anat. Rec. 300, 437–449 (2017)

    Article  Google Scholar 

  39. Viguet-Carrin, S., Garnero, P., Delmas, P.D.: The role of collagen in bone strength. Osteoporosis Int. 17, 319–336 (2006)

    Article  Google Scholar 

  40. Zhang, X., Azuma, N., Hagihara, S., Adachi, S., Ura, K., Takagi, Y.: Characterization of type I and II procollagen α1chain in Amur sturgeon (Acipenser schrenckii) and comparison of their gene expression. Gene 579, 8–16 (2016)

    Article  Google Scholar 

  41. Mizuta, S., Asano, C., Yokoyama, Y., Taniguchi, M.: Molecular species of collagen in muscular and vertebral parts of white sturgeon Acipenser transmontanus. Fish. Sci. 78, 399–406 (2012)

    Article  Google Scholar 

  42. Luo, Q.B., Chi, C.F., Yang, F., Zhao, Y.Q., Wang, B.: Physicochemical properties of acid-and pepsin-soluble collagens from the cartilage of Siberian sturgeon. Environ. Sci. Pollut. R 25, 31427–31438 (2018)

    Article  Google Scholar 

  43. Zhu, L.L., Li, J.W., Wang, Y.C., Sun, X., Li, B.F., Poungchawanwong, S., Hou, H.: Structural feature and self-assembly properties of type II collagens from the cartilages of skate and sturgeon. Food Chem. 331, 127340 (2020)

    Article  Google Scholar 

  44. Sato, K., Ohashi, C., Ohtsuki, K., Kawabata, M.: Type V collagen in trout (Salmo gairdneri) muscle and its solubility change during chilled storage of muscle. J. Agric. Food Chem. 39, 1222–1225 (1991)

    Article  Google Scholar 

  45. Plepis, A.M.D.G., Goissis, G., Gupta, D.D.: Dielectric and pyroelectric characterization of anionic and native collagen. Polym. Eng. Sci. 36, 2932–2938 (1996)

    Article  Google Scholar 

  46. Muyonga, J.H., Cole, C.G.B., Duodu, K.G.: Characterisation of acid soluble collagen from skins of young and adult Nile perch (Lates niloticus). Food Chem. 85, 81–89 (2004)

    Article  Google Scholar 

  47. Veeruraj, A., Arumugam, M., Balasubramanian, T.: Isolation and characterization of thermostable collagen from the marine eel-fish (Evenchelys macrura). Process. Biochem. 48, 1592–1602 (2013)

    Article  Google Scholar 

  48. Li, Y.P., Douglas, E.P.: Effects of various salts on structural polymorphism of reconstituted type I collagen fibrils. Colloids. Surf. B 112, 42–50 (2013)

    Article  Google Scholar 

  49. Patrickios, C.S.: Polypeptide amino acid composition and isoelectric point: 1. A closed-form approximation. J. Colloid Interface Sci. 175, 256–260 (1995)

    Article  Google Scholar 

  50. Kalbitzer, L., Pompe, T.: Fibril growth kinetics link buffer conditions and topology of 3D collagen I networks. Acta. Biomater. 67, 206–214 (2018)

    Article  Google Scholar 

  51. Shi, L.F., Tian, H.H., Wang, Y.X., Hao, G.X., Chen, J., Weng, W.Y.: Effect of pH on properties of golden pompano skin collagen-based fibril gels by self-assembly in vitro. J. Sci. Food Agric. 100, 4801–4807 (2020)

    Article  Google Scholar 

  52. Birk, D.E., Silver, F.H.: Collagen fibrillogenesis in vitro: comparison of types I, II, and III. Arch. Biochem. Biophys. 235, 178–185 (1984)

    Article  Google Scholar 

  53. Kemp, N.E.: Banding pattern and fibrillogenesis of ceratotrichia in shark fins. J. Morphol. 154, 187–204 (1977)

    Article  Google Scholar 

  54. Weiss, C., Rosenberg, L., Helfet, A.J.: An ultrastructural study of normal young adult human articular cartilage. J. Bone Joint Surg. Am. 50, 663–674 (1968)

    Article  Google Scholar 

  55. Lapiere, C.M., Nusgens, B., Pierard, G.E.: Interaction between collagen type I and type III in conditioning bundles organization. Connect. Tissue Res. 5, 21–29 (1977)

    Article  Google Scholar 

  56. Adachi, E., Hayashi, T.: In vitro formation of hybrid fibrils of type V collagen and type I collagen limited growth of type I collagen into thick fibrils by type V collagen. Connect. Tissue Res. 14, 257–266 (1986)

    Article  Google Scholar 

  57. Li, W., Kobayashi, T., Meng, D.W., Miyamoto, N., Tsutsumi, N., Ura, K., Takagi, Y.: Free radical scavenging activity of type II collagen peptides and chondroitin sulfate oligosaccharides from by-products of mottled skate processing. Food Biosci. 41, 100991 (2021)

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Key Lab of Freshwater Biodiversity Conservation, Yangtze River Fisheries Research Institute; Zhejiang Province Joint Key Laboratory of Aquatic Products Processing, Zhejiang Gongshang University, for their financial and instrumentation support in the development of this study. Thanks for Prof. Yasuaki Takagi of Faculty of Fisheries Sciences, Hokkaido University supply to technical support and article modification.

Funding

This work was partially supported by key laboratory research fund open topics (LFBC1002) from Key Lab of Freshwater Biodiversity Conservation, Ministry of Agriculture and Rural Affairs of China; Fundamental Research Funds for the Provincial Universities of Zhejiang (3090JYN9920001G-307).

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Authors and Affiliations

  1. Zhejiang Province Joint Key Laboratory of Aquatic Products Processing, Institute of Seafood, Zhejiang Gongshang University, 149 JiaoGong Road, Hangzhou, 310012, China

    Dawei Meng & Zhiyuan Dai

  2. Key Laboratory of Freshwater Biodiversity Conservation, Ministry of Agriculture and Rural Affairs, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, 430223, China

    Qiwei Wei

  3. Faculty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido, 041-8611, Japan

    Yasuaki Takagi

  4. Liangzhu Laboratory, Zhejiang University Medical Center, Hangzhou, 310058, Zhejiang, China

    Yan Zhang

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  1. Dawei Meng
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All authors had read and agreed with the published version of the manuscript. DM: Conceptualization, Methodology, Data curation, Investigation, Writing-original draft. Prof. QW: Supervision. Prof. YT: Methodology, Writing-review & Editing. Prof. ZD: Resources. YZ: Methodology. All authors read and approved the final manuscript.

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Correspondence to Dawei Meng.

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Meng, D., Wei, Q., Takagi, Y. et al. Structural Properties and Biological Activities of Collagens from Four Main Processing By-Products (Skin, Fin, Cartilage, Notochord) of Sturgeon (Acipenser gueldenstaedti). Waste Biomass Valor 14, 3987–4002 (2023). https://doi.org/10.1007/s12649-023-02107-6

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