Environmental Science and Pollution Research

, Volume 25, Issue 31, pp 31427–31438 | Cite as

Physicochemical properties of acid- and pepsin-soluble collagens from the cartilage of Siberian sturgeon

  • Qian-Bin Luo
  • Chang-Feng ChiEmail author
  • Fan Yang
  • Yu-Qin Zhao
  • Bin WangEmail author
Research Article


To look for the collagen alternatives of mammalian cartilages from aquatics and their by-products, acid-soluble collagen (ASC-SC) and pepsin-soluble collagen (PSC-SC) were extracted from cartilages of Siberian sturgeon (Acipenser baerii) with yields of 27.13 ± 1.15 and 14.69 ± 0.85% on dry weight basis. ASC-SC and PSC-SC had glycine as the major amino acid with the contents of 326.8 and 327.5 residues 1000 residues−1, and their contents of proline and hydroxyproline were 205.9 and 208.0 residues 1000 residues−1. ASC-SC and PSC-SC comprised type I collagen ([α1(I)]2α2(I)) and type II collagen ([α1(II)]3) on the literatures and results of amino acid composition, SDS-PAGE pattern, UV, and FTIR spectra. Meanwhile, FTIR spectra data indicated that there were more hydrogen bonds in ASC-SC and more intermolecular crosslinks in PSC-SC. The maximum transition temperature (Tmax) of the ASC (28.3 °C) and PSC (30.5 °C) was lower than those of collagens from mammalian cartilages (> 37 °C). ASC-SC and PSC-SC showed high solubility in the acidic pH ranges and the solubility decreased in the presence of NaCl at concentrations above 3%. Zeta potential studies indicated that both ASC-SC and PSC-SC exhibited a net zero charge at pH 6.30 and 6.32. SEM results indicated that ASC-SC and PSC-SC presented irregular dense sheet-like film linked by random-coiled filaments. Therefore, collagens from Siberian sturgeon cartilages might be the suitable alternatives of the collagens of mammal cartilages as functional ingredient to treat some diseases.


Siberian sturgeon (Acipenser baeriiCartilage Acid-soluble collagen (ASC) Pepsin-soluble collagen (PSC) Antioxidant activity 


Funding information

This work was funded by the National Natural Science Foundation of China (NSFC) (No. 81673349), Science and Technology Program of Zhoushan (No. 2016C41016), Natural Science Foundation of Zhejiang Province, China (No. LY15C190010), and Open Foundation from Marine Sciences in the Most Important Subjects of Zhejiang (No. 20160116).

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflicts of interest.


  1. Abdollahi M, Rezaei M, Jafarpour A, Undeland I (2018) Sequential extraction of gel-forming proteins, collagen and collagen hydrolysate from gutted silver carp (Hypophthalmichthys molitrix), a biorefinery approach. Food Chem 242:568–578CrossRefGoogle Scholar
  2. AOAC (2003) Official methods of analysis of AOAC international (17th ed.). Association of the Official Analytical Chemists (AOAC) International, GaithersburgGoogle Scholar
  3. Asghar A, Henrickson RL (1982) Chemical, biochemical, functional and nutritional characteristics of collagen in food systems. In: Chichester CO, Marata EM, Schweigert BS (eds) Advances in food research. Academic, London, pp 237–273Google Scholar
  4. Bagi CM, Berryman ER, Teo S, Lane NE (2017) Oral administration of undenatured native chicken type II collagen (UC-II) diminished deterioration of articular cartilage in a rat model of osteoarthritis (OA). Osteoarthr Cartil 25(12):2080–2090CrossRefGoogle Scholar
  5. Benjakul S, Thiansilakul Y, Visessanguan W, Roytrakul S, Kishimura H, Prodpran T, Meesane J (2010) Extraction and characterisation of pepsin solubilised collagens from the skin of bigeye snapper (Priacanthus tayenus and Priacanthus macracanthus). J Sci Food Agric 90:132–138CrossRefGoogle Scholar
  6. Bu Y, Elango J, Zhang J, Bao B, Guo R, Palaniyandi K, Robinson JS, Geevaretnam J, Regenstein JM, Wu W (2017) Immunological effects of collagen and collagen peptide from blue shark cartilage on 6T-CEM cells. Process Biochem 57:219–227CrossRefGoogle Scholar
  7. Chen J, Li L, Yi R, Xu N, Gao R, Hong B (2016) Extraction and characterization of acid-soluble collagen from scales and skin of tilapia (Oreochromis niloticus). LWT Food Sci Technol 66:453–459CrossRefGoogle Scholar
  8. Chi CF, Wang B, Li ZR, Luo HY, Ding GF (2013) Characterization of acid-soluble collagens from the cartilages of scalloped hammerhead (Sphyrna lewini), red stingray (Dasyatis akajei), and skate (Raja porosa). Food Sci Biotechnol 22:909–916CrossRefGoogle Scholar
  9. Chi CF, Wang B, Li ZR, Luo HY, Ding GF, Wu CW (2014) Characterization of acid-soluble collagen from the skin of hammerhead shark (Sphyrna lewini). J Food Biochem 38(2):236–247CrossRefGoogle Scholar
  10. Ciarloa AS, Paredi ME, Fraga AN (1997) Isolation of soluble collagen from hake skin (Merluccius hubbsi). J Aquat Food Prod Technol 6:65–77CrossRefGoogle Scholar
  11. Cui FX, Xue CH, Li ZJ, Zhang YQ, Dong P, Fu XY, Gao X (2007) Characterization and subunit composition of collagen from the body wall of sea cucumber Stichopus japonicus. Food Chem 100(3):1120–1125CrossRefGoogle Scholar
  12. Doyle BB, Bendit EG, Blout ER (1975) Infrared spectroscopy of collagen and collagen-like polypeptides. Biopolymers 14:937–957CrossRefGoogle Scholar
  13. Elango J, Zhang J, Bao B, Palaniyandi K, Robinson JS (2016) Rheological, biocompatibility and osteogenesis assessment of fish collagen scaffold for bone tissue engineering. Int J Biol Macromol 91:51–59CrossRefGoogle Scholar
  14. Foegeding EA, Laneir TC, Hultin HO (1996) Characteristics of edible muscle tissues. In: Fennema OR (ed) Food chemistry. Marcel Dekker Inc., New York, pp 902–906Google Scholar
  15. Gelse K, Pöschl E, Aigner T (2003) Collagens-structure, function, and bio-synthesis. Adv Drug Deliv Rev 55(12):1531–1546CrossRefGoogle Scholar
  16. Gross J, Dumsha B, Glazer N (1958) Comparative biochemistry of collagen: some amino acids and carbohydrates. Biochim Biophys Acta 30:293–297CrossRefGoogle Scholar
  17. Gui M, Song J, Zhang L, Wang S, Wu R, Ma C et al (2015) Chemical characteristics and antithrombotic effect of chondroitin sulfates from sturgeon skull and sturgeon backbone. Carbohyd Polym 123:454–460CrossRefGoogle Scholar
  18. Gustavson KH (1955) The function of hydroxyproline in collagens. Nature 175:70–74CrossRefGoogle Scholar
  19. Jeevithan E, Bao B, Bu Y, Zhou Y, Zhao Q, Wu W (2014a) Type II collagen and gelatin from silvertip shark (Carcharhinus albimarginatus) cartilage: isolation, purification, physicochemical and antioxidant properties. Mar Drugs 12:3852–3873CrossRefGoogle Scholar
  20. Jeevithan E, Wu W, Nanping W, Lan H, Bao B (2014b) Isolation, purification and characterization of pepsin soluble collagen isolated from silvertip shark (Carcharhinus albimarginatus) skeletal and head bone. Process Biochem 49(10):1767–1777CrossRefGoogle Scholar
  21. Jeevithan E, Zhang J, Wang N, He L, Wu W (2015) Physico-chemical, antioxidant and intestinal absorption properties of whale shark type-II collagen based on its solubility with acid and pepsin. Process Biochem 50(3):463–472CrossRefGoogle Scholar
  22. Jongjareonrak A, Benjakul S, Visessanguan W, Nagai T, Tanaka M (2005) Isolation and characterisation of acid and pepsin-solubilised collagens from the skin of Brownstripe red snapper (Lutjanus vitta). Food Chem 93:475–484CrossRefGoogle Scholar
  23. Kaewdang O, Benjakul S, Kaewmanee T, Kishimura H (2014) Characteristics of collagens from the swim bladders of yellowfin tuna (Thunnus albacares). Food Chem 155:264–270CrossRefGoogle Scholar
  24. 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 Chem 89(3):363–372CrossRefGoogle Scholar
  25. 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 Sci Technol 43(5):792–800CrossRefGoogle Scholar
  26. Krishnamoorthi J, Ramasamy P, Shanmugam V, Shanmugam A (2017) Isolation and partial characterization of collagen from outer skin of Sepia pharaonis (Ehrenberg, 1831) from Puducherry coast. Biochem Biophys Rep 10:39–45Google Scholar
  27. Kumar B, Rani S (2017) Technical note on the isolation and characterization of collagen from fish waste material. J Food Sci Technol 54(1):276–278CrossRefGoogle Scholar
  28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefGoogle Scholar
  29. Li ZR, Wang B, Chi CF, Zhang QH, Gong YD, Tang JJ, Luo HY, Ding GF (2013) Isolation and characterization of acid soluble collagens and pepsin soluble collagens from the skin and bone of Spanish mackerel (Scomberomorous niphonius). Food Hydrocoll 31:103–113CrossRefGoogle Scholar
  30. Liang Q, Wang L, Sun W, Wang Z, Xu J, Ma H (2014) Isolation and characterization of collagen from the cartilage of Amur sturgeon (Acipenser schrenckii). Process Biochem 49(2):318–323CrossRefGoogle Scholar
  31. Liu HY, Li D, Guo SD (2007) Studies on collagen from the skin of channel catfish (Ictalurus punctaus). Food Chem 101(2):621–625CrossRefGoogle Scholar
  32. Liu D, Zhang X, Li T, Yang H, Zhang H, Regenstein JM, Zhou P (2015) Extraction and characterization of acid- and pepsin-soluble collagens from the scales, skins and swim-bladders of grass carp (Ctenopharyngodon idella). Food Biosci 9:68–74CrossRefGoogle Scholar
  33. Liu A, Zhang Z, Hou H, Zhao X, Li B, Zhao T et al (2018) Characterization of acid- and pepsin-soluble collagens from the cuticle of Perinereis nuntia (Savigny). Food Biophys 13:274–283CrossRefGoogle Scholar
  34. Lugo JP, Saiyed ZM, Lau FC, Melina JPL, Pakdaman MN, Shamie AN et al (2013) Undenatured type II collagen (UC-II®) for joint support: a randomized, double-blind, placebo-controlled study in healthy volunteers. J Int Soc Sports Nutr 10:48–60CrossRefGoogle Scholar
  35. Lugo JP, Saiyed ZM, Lane NE (2016) Efficacy and tolerability of an undenaturated type II collagen (UC-II) supplement in modulating knee joint function: a multicenter randomized, double blind, placebo controlled clinical study in osteoarthritic subjects. Nutr J 15:14CrossRefGoogle Scholar
  36. Matmaroh K, Benjakul S, Prodpran T, Encarnacion AB, Kishimura H (2011) Characteristics of acid soluble collagen and pepsin soluble collagen from scale of spotted golden goatfish (Parupeneus heptacanthus). Food Chem 129:1179–1186CrossRefGoogle Scholar
  37. Montero P, Jiménez-Colmenero F, Borderias J (1991) Effect of pH and the presence of NaCl on some hydration properties of collagenous material from trout (Salmo irideus Gibb) muscle and skin. J Sci Food Agric 54:137–146CrossRefGoogle Scholar
  38. Muyonga JH, Cole CGB, Duodu KG (2004) Characterisation of acid soluble collagen from skins of young and adult Nile perch (Lates niloticus). Food Chem 85:81–89CrossRefGoogle Scholar
  39. Pal GK, Suresh PV (2016) Sustainable valorisation of seafood by-products: recovery of collagen and development of collagen-based novel functional food ingredients. Innovative Food Sci Emerg Technol 37:201–215CrossRefGoogle Scholar
  40. Pal GK, Suresh PV (2017a) Comparative assessment of physico-chemical characteristics and fibril formation capacity of thermostable carp scales collagen. Mater Sci Eng C 70:32–40CrossRefGoogle Scholar
  41. Pal GK, Suresh PV (2017b) Physico-chemical characteristics and fibril-forming capacity of carp swim bladder collagens and exploration of their potential bioactive peptides by in silico approaches. Int J Biol Macromol 101:304–313CrossRefGoogle Scholar
  42. Piez KA, Gross J (1960) The amino acid composition of some fish collagens: the relation between composition and structure. J Biol Chem 235(4):995–998Google Scholar
  43. Prockop DJ, Kivirikko KI (1995) Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 64:12–14CrossRefGoogle Scholar
  44. Rama S, Chandrakasan G (1984) Distribution of different molecular species of collagen in the vertebral cartilage of shark (Carcharius acutus). Connect Tissue Res 12:111–118CrossRefGoogle Scholar
  45. Ramachandran GN (1988) Stereochemistry of collagen. Int J Pept Protein Res 31:1–16CrossRefGoogle Scholar
  46. Ramachandran GN, Kartha G (1955) Structure of collagen. Nature 176:593–595CrossRefGoogle Scholar
  47. Ramachandran GN, Bansal M, Bhatnagar RS (1973) A hypothesis on the role of hydroxyproline in stabilizing the collagen structure. Biochim Biophys Acta 322:166–171CrossRefGoogle Scholar
  48. Rich A, Crick FHC (1961) The molecular structure of collagen. J Mol Biol 3:483–506CrossRefGoogle Scholar
  49. Sadowska M, Kolodziejska I, Niecikowska C (2003) Isolation of collagen from the skins of Baltic cod (Gadus morhua). Food Chem 81(2):257–262CrossRefGoogle Scholar
  50. Shoulders MD, Raines RT (2009) Collagen structure and stability. Annu Rev Biochem 78:929–958CrossRefGoogle Scholar
  51. Sinthusamran S, Benjakul S, Kishimura H (2013) Comparative study on molecular characteristics of acid soluble collagens from skin and swim bladder of seabass (Lates calcarifer). Food Chem 138:2435–2441CrossRefGoogle Scholar
  52. Subhan F, Ikram M, Shehzad A, Ghafoor A (2015) Marine collagen: an emerging player in biomedical applications. J Food Sci Technol 52(8):4703–4707CrossRefGoogle Scholar
  53. Tziveleka L, Ioannou E, Tsiourvas D, Berillis P, Foufa E, Roussis V (2017) Collagen from the marine sponges Axinella cannabina and Suberites carnosus: isolation and morphological, biochemical, and biophysical characterization. Mar Drugs 15:152CrossRefGoogle Scholar
  54. Venkatesan J, Anil S, Kim S-K, Shim MS (2017) Marine fish proteins and peptides for cosmeceuticals: a review. Mar Drugs 15:143CrossRefGoogle Scholar
  55. Wang L, An X, Xin Z, Zhao L, Hu Q (2007) Isolation and characterization of collagen from the skin of deep-sea redfish (Sebastes mentella). J Food Sci 72(8):E450–E455CrossRefGoogle Scholar
  56. Wang L, Liang Q, Chen T, Wang Z, Xu J, Ma H (2014) Characterization of collagen from the skin of Amur sturgeon (Acipenser schrenckii). Food Hydrocoll 38:104–109CrossRefGoogle Scholar
  57. Wang J, Pei X, Liu H, Zhou D (2018) Extraction and characterization of acid-soluble and pepsin-soluble collagen from skin of loach (Misgurnus anguillicaudatus). Int J Biol Macromol 106:544–550CrossRefGoogle Scholar
  58. Wong DWS (1989) Mechanism and theory in food chemistry. Van Nostrand Reinhold Company Inc., New YorkGoogle Scholar
  59. Wu QQ, Li T, Wang B, Ding GF (2015) Preparation and characterization of acid and pepsin-soluble collagens from scales of croceine and redlip croakers. Food Sci Biotechnol 24(6):2003–2010CrossRefGoogle Scholar
  60. Yu D, Chi CF, Wang B, Ding GF, Li Z (2014) Characterization of acid and pepsin soluble collagens from spine and skull of skipjack tuna (Katsuwonus pelamis). Chin J Nat Med 12(9):712–720Google Scholar
  61. Zhang J, Duan R (2017) Characterisation of acid-soluble and pepsin-solubilised collagen from frog (Rana nigromaculata) skin. Int J Biol Macromol 101:638–642CrossRefGoogle Scholar
  62. Zhao WH, Chi CF, Zhao YQ, Wang B (2018) Preparation, physicochemical and antioxidant properties of acid- and pepsin-soluble collagens from the swim bladders of miiuy croaker (Miichthys miiuy). Mar Drugs 16:161CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.National and Provincial Joint Laboratory of Exploration and Utilization of Marine Aquatic Genetic Resources, National Engineering Research Center of Marine Facilities Aquaculture, School of Marine Science and TechnologyZhejiang Ocean UniversityZhoushanChina
  2. 2.Zhejiang Provincial Engineering Technology Research Center of Marine Biomedical Products, School of Food and PharmacyZhejiang Ocean UniversityZhoushanChina

Personalised recommendations