collagen fibril; collagen fibril gel; gel property; self-assembly behavior; ultrasonic treatment; Collagen Type I; Collagen; Gels; Animals; Cattle; Extracellular Matrix/chemistry; Cytoskeleton; Collagen/chemistry; Extracellular Matrix; Analytical Chemistry; Chemistry (miscellaneous); Molecular Medicine; Pharmaceutical Science; Drug Discovery; Physical and Theoretical Chemistry; Organic Chemistry
Abstract :
[en] This study deliberated the effect of ultrasonic treatment on collagen self-assembly behavior and collagen fibril gel properties. Bovine bone collagen I which had undergone ultrasonic treatment with different power (0-400 W) and duration (0-60 min) was analyzed. SDS-PAGE and spectroscopic analysis revealed that ultrasonic treatment decreased collagen molecular order degree and the number of hydrogen bonds, stretching collagen telopeptide regions while maintaining the integrity of the collagen triple-helical structure. Ultrasonic treatment (p ≤ 200 W, t ≤ 15 min) dispersed the collagen aggregates more evenly, and accelerated collagen self-assembly rate with a decreased but more homogeneous fibril diameter (82.78 ± 16.47-115.52 ± 19.51 nm) and D-periodicity lengths (62.1 ± 2.9-66.5 ± 1.8 nm) than that of the untreated collagen (119.15 ± 27.89 nm; 66.5 ± 1.8 nm). Meanwhile, ultrasonic treatment (p ≤ 200 W, t ≤ 15 min) decreased the viscoelasticity index and gel strength, enhancing thermal stability and promoting specific surface area and porosity of collagen fibril gels than that of the untreated collagen fibril gel. These results testified that collagen self-assembly behavior and collagen fibril gel properties can be regulated by ultrasonic treatment through multi-hierarchical structural alteration. This study provided a new approach for controlling in vitro collagen fibrillogenesis process so as to manufacture novel desirable collagen-based biomaterials with propitious performances for further valorization.
Disciplines :
Food science Chemistry
Author, co-author :
Liu, Hong ; Comprehensive Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Zhang, Hongru ; Université de Liège - ULiège > TERRA Research Centre ; Comprehensive Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Wang, Kangyu; Comprehensive Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Qi, Liwei; Comprehensive Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Guo, Yujie; Comprehensive Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Zhang, Chunhui; Comprehensive Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
National Agricultural Science and Technology Innovation Project Technical Breakthrough Projects of Inner Mongolia Science and Technology Program
Funding text :
This research was funded by Technical Breakthrough Projects of Inner Mongolia Science and Technology Program (No. 2022JBGS0007), National Agricultural Science and Technology Innovation Project (No. CAAS-ASTIP-2023).
Qin L. Bi J.R. Li D.M. Dong M. Zhao Z.Y. Dong X.P. Zhou D.Y. Zhu B.W. Unfolding/refolding study on collagen from sea cucumber based on 2D fourier transform infrared spectroscopy Molecules 2016 21 1546 10.3390/molecules21111546 27854344
Gunasekaran D. Thada R. Jeyakumar G.F.S. Manimegalai N.P. Shanmugam G. Sivagnanam U.T. Physicochemical characterization and self-assembly of human amniotic membrane and umbilical cord collagen: A comparative study Int. J. Biol. Macromol. 2020 165 2920 2933 10.1016/j.ijbiomac.2020.10.107 33098903
Zou Y.E. Xu P. Li P. Cai P. Zhang M. Sun Z.L. Sun C. Xu W.M. Wang D.Y. Effect of ultrasound pre-treatment on the characterization and properties of collagen extracted from soft-shelled turtle (Pelodiscus sinensis) LWT Food Sci. Technol. 2017 82 72 81 10.1016/j.lwt.2017.04.024
Tian H.H. Ren Z.Y. Shi L.F. Hao G.X. Chen J. Weng W.Y. Self-assembly characterization of tilapia skin collagen in simulated body fluid with different salt concentrations Process Biochem. 2021 108 153 160 10.1016/j.procbio.2021.06.013
Ju H.Y. Liu X.Y. Zhang G. Liu D.Z. Yang Y.S. Comparison of the structural characteristics of native collagen fibrils derived from bovine tendons using two different methods: Modified acid-solubilized and pepsin-aided extraction Materials 2020 13 358 10.3390/ma13020358
Wan Y.F. Gao Y.F. Shao J.H. Tumarbekova A. Zhang D.Q. Zhu J. Effects of ultrasound and thermal treatment on the ultrastructure of collagen fibers from bovine tendon using atomic force microscopy Food Chem. 2021 347 128985 10.1016/j.foodchem.2020.128985
Jiang Y. Wang H.B. Deng M.X. Wang Z.W. Zhang J.T. Wang H.Y. Zhang H.J. Effect of ultrasonication on the fibril-formation and gel properties of collagen from grass carp skin Mater. Sci. Eng. C 2016 59 1038 1046 10.1016/j.msec.2015.11.007
Akram A.N. Zhang C.H. Extraction of collagen-II with pepsin and ultrasound treatment from chicken sternal cartilage; physicochemical and functional properties Ultrason Sonochem. 2020 64 105053 10.1016/j.ultsonch.2020.105053 32173183
Akram A.N. Zhang C.H. Effect of ultrasonication on the yield, functional and physicochemical characteristics of collagen-II from chicken sternal cartilage Food Chem. 2020 307 125544 10.1016/j.foodchem.2019.125544
Ye Y.K. Dai S.Q. Zhang H.Y. He S.D. Hu W.W. Cao X.D. Wei Z.J. Ultrasound-Assisted Preparation of Maillard Reaction Products Derived from Hydrolyzed Soybean Meal with Meaty Flavor in an Oil-In-Water System Molecules 2022 27 7236 10.3390/molecules27217236
Ata O. Kumcuoglu S. Tavman S. Effects of sonication on the extraction of pepsin-soluble collagens from lamb feet and product characterization LWT Food Sci. Technol. 2022 159 113253 10.1016/j.lwt.2022.113253
Li G.X. Wan Y.F. Song X. Wang Y. Zan L.S. Zhu J. Effects of various processing methods on the ultrastructure of tendon collagen fibrils from Qinchuan beef cattle observed with atomic force microscopy J. Food Qual. 2018 2018 9090831 10.1155/2018/9090831
Yu X.J. Tu S.S. Li Y.H. Yagoub A.E.A. Ma H.L. Zhou C.S. Effects of single-and tri-frequency ultrasound on self-assembly and characterizations of bionic dynamic rat stomach digestion of pepsin-soluble collagen from chicken leg skin Food Res. Int. 2020 137 109710 10.1016/j.foodres.2020.109710
Liu H. Xu X. Liu J.Q. Zhang H.R. Qi L.W. Zhang C.H. Comparative assessment of bone collagen recovered from different livestock and poultry species: Microstructure, physicochemical characteristics and functional properties Int. J. Food Sci. Tech. 2023 58 1597 1610 10.1111/ijfs.15896
Thankachan S.N. Ilamaran M. Ayyadurai N. Shanmugam G. Insights into the effect of artificial sweeteners on the structure, stability, and fibrillation of type I collagen Int. J. Biol. Macromol. 2020 164 748 758 10.1016/j.ijbiomac.2020.07.152
Ran Y.Q. Su W. Ma L. Wang X.L. Li X.D. Insight into the effect of sulfonated chitosan on the structure, rheology and fibrillogenesis of collagen Int. J. Biol. Macromol. 2021 166 1480 1490 10.1016/j.ijbiomac.2020.11.027
Chandrapala J. Oliver C. Kentish S. Ashokkumar M. Ultrasonics in food processing Ultrason. Sonochem. 2012 19 975 983 10.1016/j.ultsonch.2012.01.010
Liao W. Xia G.H. Li Y.C. Shen X.R. Li C. Comparison of characteristics and fibril-forming ability of skin collagen from barramundi (Lates calcarifer) and tilapia (Oreochromis niloticus) Int. J. Biol. Macromol. 2018 107 549 559 10.1016/j.ijbiomac.2017.09.022
Li Y.P. Asadi A. Monroe M.R. Douglas E.P. pH effects on collagen fibrillogenesis in vitro: Electrostatic interactions and phosphate binding Mater. Sci. Eng. C 2009 29 1643 1649 10.1016/j.msec.2009.01.001
Tang L.L. Chen S.L. Su W.J. Weng W.Y. Osako K. Tanaka M. Physicochemical properties and film-forming ability of fish skin collagen extracted from different freshwater species Process Biochem. 2015 50 148 155 10.1016/j.procbio.2014.10.015
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. 2014 160 305 312 10.1016/j.foodchem.2014.03.075 24799243
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. 2019 131 572 580 10.1016/j.ijbiomac.2019.03.091 30880060
Ferraro V. Gaillard-Martinie B. Sayd T. Chambon C. Anton M. Santé-Lhoutellier V. Collagen type I from bovine bone. Effect of animal age, bone anatomy and drying methodology on extraction yield, self-assembly, thermal behaviour and electrokinetic potential Int. J. Biol. Macromol. 2017 97 55 66 10.1016/j.ijbiomac.2016.12.068 28038914
Yousefi M. Ariffin F. Huda N. An alternative source of type I collagen based on by-product with higher thermal stability Food Hydrocolloid 2017 63 372 382 10.1016/j.foodhyd.2016.09.029
Andonegi M. Las Heras K. Santos-Vizcaíno E. Igartua M. Hernandez R.M. de la Caba K. Guerrero P. Structure-properties relationship of chitosan/collagen films with potential for biomedical applications Carbohyd. Polym. 2020 237 116159 10.1016/j.carbpol.2020.116159
Valencia-Llano C.H. López-Tenorio D. Saavedra M. Zapata P.A. Grande-Tovar C.D. Comparison of Two Bovine Commercial Xenografts in the Regeneration of Critical Cranial Defects Molecules 2022 27 5745 10.3390/molecules27185745
Ion A. Andronescu E. Rădulescu D. Rădulescu M. Iordache F. Vasile B.Ș. Surdu A.V. Albu M.G. Maniu H. Chifiriuc M.C. et al. Biocompatible 3d matrix with antimicrobial properties Molecules 2016 21 115 10.3390/molecules21010115
Du X. Li H.J. Nuerjiang M. Shi S. Kong B.H. Liu Q. Xia X.F. Application of ultrasound treatment in chicken gizzards tenderization: Effects on muscle fiber and connective tissue Ultrason. Sonochem. 2021 79 105786 10.1016/j.ultsonch.2021.105786 34634549
Liu D.S. Zhou P. Li T.C. Regenstein J.M. Comparison of acid-soluble collagens from the skins and scales of four carp species Food Hydrocolloid 2014 41 290 297 10.1016/j.foodhyd.2014.04.030
Pal G.K. Suresh P.V. Comparative assessment of physico-chemical characteristics and fibril formation capacity of thermostable carp scales collagen Mater. Sci. Eng. C 2017 70 32 40 10.1016/j.msec.2016.08.047 27770898
Dong X.F. Shen P. Yu M.Q. Yu C.X. Zhu B.W. Qi H. (−)-Epigallocatechin gallate protected molecular structure of collagen fibers in sea cucumber Apostichopus japonicus body wall during thermal treatment LWT Food Sci. Technol. 2020 123 109076 10.1016/j.lwt.2020.109076
Adamiak K. Lewandowska K. Sionkowska A. The infuence of salicin on rheological and film-forming properties of collagen Molecules 2021 26 1661 10.3390/molecules26061661
Li Y.S. Yang L.H. Wu S.J. Chen J.D. Lin H.W. Structural, functional, rheological, and biological properties of the swim bladder collagen extracted from grass carp (Ctenopharyngodon idella) LWT Food Sci. Technol. 2022 153 112518 10.1016/j.lwt.2021.112518
Song X. Si L.L. Sun X. Zhu X. Li Z.X. Li Y.Y. Wang Y.F. Hou H. Rheological properties, thermal stability and conformational changes of collagen from sea cucumber (Apostichopus japonicas) Food Chem. 2022 389 133033 10.1016/j.foodchem.2022.133033 35490516
Duan L. Li J.H. Li C.H. Li G.Y. Effects of NaCl on the rheological behavior of collagen solution Korea-Aust. Rheol. J. 2013 25 137 144 10.1007/s13367-013-0014-9
Lai G.L. Li Y. Li G.Y. Effect of concentration and temperature on the rheological behavior of collagen solution Int. J. Biol. Macromol. 2008 42 285 291 10.1016/j.ijbiomac.2007.12.010
Pudło A. Juchniewicz S. Kopeć W. Characteristics of Reconstituted Collagen Fibers from Chicken Keel Cartilage Depends on Salt Type for Removal of Proteoglycans Molecules 2021 26 3538 10.3390/molecules26123538
Kang D.C. Wang A.R. Zhou G.H. Zhang W.G. Xu S.M. Guo G.P. Power ultrasonic on mass transport of beef: Effects of ultrasound intensity and NaCl concentration Innov. Food Sci. Emerg. 2016 35 36 44 10.1016/j.ifset.2016.03.009
Thuy L.T.M. Okazaki E. Osako K. Isolation and characterization of acid-soluble collagen from the scales of marine fishes from Japan and Vietnam Food Chem. 2014 149 264 270 10.1016/j.foodchem.2013.10.094
Kang D.C. Zou Y.H. Cheng Y.P. Xing L.J. Zhou G.H. Zhang W.G. Effects of power ultrasound on oxidation and structure of beef proteins during curing processing Ultrason. Sonochem. 2016 33 47 53 10.1016/j.ultsonch.2016.04.024
Pezeshk S. Rezaei M. Abdollahi M. Impact of ultrasound on extractability of native collagen from tuna by-product and its ultrastructure and physicochemical attributes Ultrason. Sonochem. 2022 89 106129 10.1016/j.ultsonch.2022.106129 36007329
Monago-Maraña O. Wold J.P. Rødbotten R. Dankel K.R. Afseth N.K. Raman, near-infrared and fluorescence spectroscopy for determination of collagen content in ground meat and poultry by-products LWT-Food Sci. Technol. 2021 140 110592 10.1016/j.lwt.2020.110592
Qu W.J. Guo T.T. Zhang X.X. Jin Y.T. Wang B. Wahia H. Ma H.L. Preparation of tuna skin collagen-chitosan composite film improved by sweep frequency pulsed ultrasound technology Ultrason. Sonochem. 2022 82 105880 10.1016/j.ultsonch.2021.105880 34952341
