Endogenous Proteases in Sea Cucumber (Apostichopus japonicas): Deterioration and Prevention during Handling, Processing, and Preservation
"> Figure 1
<p>Histological analysis by light microscopy (<b>A</b>–<b>F</b>), scanning electron microscopy (<b>G</b>–<b>L</b>), and transmission electron microscopy (<b>M</b>–<b>R</b>) of fresh and autolyzed sea cucumber (<span class="html-italic">Apostichopus japonicas</span>) body walls (SCBWs) at room temperature (20–25 °C) for 72 h [<a href="#B12-foods-13-02153" class="html-bibr">12</a>,<a href="#B37-foods-13-02153" class="html-bibr">37</a>,<a href="#B38-foods-13-02153" class="html-bibr">38</a>]. Note: AB-PAS: alcian blue-periodic acid schiff. White arrow: the location where collagen fibers fracture.</p> "> Figure 2
<p>Endogenous enzymes in the intestine and body wall causing the autolysis of the sea cucumber. Note: SCBW: sea cucumber body wall, ALP: acid phosphatase, AChE: acetylcholine esterase, SP: serine protease SEP: serine endopeptidases, GMP: gelatinolytic metalloproteinase, ACP: acid phosphatase, SOD: superoxide dismutase.</p> "> Figure 3
<p>The mechanism of apoptosis participating in the autolysis process of a sea cucumber under UV induction. Note: ROS: reactive oxygen species, MMP: matrix metalloproteinase, “<span class="html-fig-inline" id="foods-13-02153-i001"><img alt="Foods 13 02153 i001" src="/foods/foods-13-02153/article_deploy/html/images/foods-13-02153-i001.png"/></span>”: glycosaminoglycan (GAG), “<span class="html-fig-inline" id="foods-13-02153-i002"><img alt="Foods 13 02153 i002" src="/foods/foods-13-02153/article_deploy/html/images/foods-13-02153-i002.png"/></span>”: soluble collagen.</p> ">
Abstract
:1. Introduction
2. Autolysis Phenomenon in Sea Cucumber
2.1. Autolysis in Sea Cucumber during Processing and Storage
2.2. Role of UV Light in the Autolysis of Sea Cucumber
2.3. Physicochemical Changes in the SCBW Induced by Autolysis
2.3.1. Microscopic Molecular Structure
2.3.2. Mechanical Properties
2.3.3. Chemical Compositions
3. The Characteristics and Mechanism of Endogenous Enzymes in the Sea Cucumber
3.1. Endogenous Proteases: Characteristics and Mode of Action
3.2. ROS Mediated Oxidative Stress: Occurrence and Mode of Action
3.3. Degradation of the SCBW
4. Inhibitors for Sea Cucumber Endogenous Enzyme Proteases
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Pangestuti, R.; Arifin, Z. Medicinal and health benefit effects of functional sea cucumbers. J. Tradit. Complement. Med. 2018, 8, 341–351. [Google Scholar] [CrossRef] [PubMed]
- Haider, M.S.; Sultana, R.; Jamil, K.; Lakht-e-Zehra, O.M.T.; Shirin, K.G.; Afzal, W. A study on proximate composition, amino acid profile, fatty acid profile and some mineral contents in two species of sea cucumber. J. Anim. Plant Sci. 2015, 25, 168–175. [Google Scholar]
- Yin, P.P.; Jia, A.R.; Heimann, K.; Zhang, M.S.; Liu, X.; Zhang, W.; Liu, C.H. Hot water pretreatment-induced significant metabolite changes in the sea cucumber Apostichopus japonicus. Food Chem. 2020, 314, 126211. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Sun, Z.L.; Zhang, M.S.; Meng, X.M.; Xia, X.K.; Yuan, W.P.; Xue, F.; Liu, C.H. Antioxidant and antihyperlipidemic activities of polysaccharides from sea cucumber Apostichopus japonicus. Carbohydr. Polym. 2012, 90, 1664–1670. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.C.; Xue, C.H.; Zhang, T.T.; Wang, Y.M. Saponins from sea cucumber and their biological activities. J. Agric. Food Chem. 2018, 66, 7222–7237. [Google Scholar] [CrossRef]
- Xu, J.; Wang, Y.M.; Feng, T.Y.; Zhang, B.; Sugawara, T.; Xue, C.H. Isolation and anti-fatty liver activity of a novel cerebroside from the sea cucumber Acaudina molpadioides. Biosci. Biotechnol. Biochem. 2011, 75, 1466–1471. [Google Scholar] [CrossRef]
- Sánchez-Tapia, I.A.; Slater, M.; Olvera-Novoa, M.A. Evaluation of the growth and survival rate of the Caribbean Sea cucumber, Isostichopus badionotus (Selenka, 1867), early juveniles produced in captivity. J. World Aquac. Soc. 2019, 50, 763–773. [Google Scholar] [CrossRef]
- Fan, X.R.; Ma, Y.S.; Li, M.; Li, Y.; Sang, X.; Zhao, Q.C. Thermal treatments and their influence on physicochemical properties of sea cucumbers: A comprehensive review. Int. J. Food Sci. Technol. 2022, 57, 5790–5800. [Google Scholar] [CrossRef]
- FAO. The State of World Fisheries and Aquaculture: Blue Transformation in Action; FAO: Rome, Italy, 2024; p. 33. [Google Scholar]
- China Fishery Statistics Yearbook; China Agriculture Press: Beijing, China, 2023.
- Duan, X.; Zhang, M.; Mujumdar, A.S.; Wang, S.J. Microwave freeze drying of sea cucumber (Stichopus japonicus). J. Food. Eng. 2010, 96, 491–497. [Google Scholar] [CrossRef]
- Liu, Y.X.; Zhou, D.Y.; Liu, Z.Q.; Lu, T.; Song, L.; Li, D.M.; Dong, X.P.; Qi, H.; Zhu, B.W.; Shahidi, F. Structural and biochemical changes in dermis of sea cucumber (Stichopus japonicus) during autolysis in response to cutting the body wall. Food Chem. 2018, 240, 1254–1261. [Google Scholar] [CrossRef]
- Liu, Y.X.; Liu, Z.Q.; Song, L.; Ma, Q.R.; Zhou, D.Y.; Zhu, B.W.; Shahidi, F. Effects of collagenase type I on the structural features of collagen fibres from sea cucumber (Stichopus japonicus) body wall. Food Chem. 2019, 301, 125302. [Google Scholar] [CrossRef] [PubMed]
- Zhu, B.W.; Zheng, J.; Zhang, Z.S.; Dong, X.P.; Zhao, L.L.; Mikiro, T. Autophagy plays a potential role in the process of sea cucumber body wall “Melting” Induced by UV irradiation. Wuhan Univ. J. Nat. Sci. 2008, 13, 232–238. [Google Scholar] [CrossRef]
- Yan, L.J.; Zhan, C.L.; Cai, Q.F.; Weng, L.; Du, C.H.; Liu, G.M.; Su, W.J.; Cao, M.J. Purification, characterization, cDNA cloning and in vitro expression of a serine proteinase from the intestinal tract of sea cucumber (Stichopus japonicus) with collagen degradation activity. J. Agric. Food Chem. 2014, 62, 4769–4777. [Google Scholar] [CrossRef] [PubMed]
- Yan, L.J.; Sun, L.C.; Cao, K.Y.; Chen, Y.L.; Zhang, L.J.; Liu, G.M.; Jin, T.C.; Cao, M.J. Type I collagen from sea cucumber (Stichopus japonicus) and the role of matrix metalloproteinase-2 in autolysis. Food Biosci. 2021, 41, 100959. [Google Scholar] [CrossRef]
- Dong, X.F.; He, B.Y.; Jiang, D.; Yu, C.X.; Zhu, B.W.; Qi, H. Proteome analysis reveals the important roles of protease during tenderization of sea cucumber Apostichopus japonicus using iTRAQ. Food Res. Int. 2019, 131, 108632. [Google Scholar] [CrossRef]
- Yang, J.F.; Gao, R.C.; Wu, H.T.; Li, P.F.; Hu, X.S.; Zhou, D.Y.; Zhu, B.W.; Su, Y.C. Analysis of apoptosis in ultraviolet-induced sea cucumber (Stichopus japonicus) melting using terminal deoxynucleotidyl-transferase-mediated dutp nick end-labeling assay and cleaved caspase-3 immunohistochemistry. J. Agric. Food Chem. 2015, 63, 9601–9608. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.X.; Zhou, D.Y.; Ma, D.D.; Liu, Z.Q.; Liu, Y.F.; Song, L.; Dong, X.P.; Li, D.M.; Zhu, B.W.; Konno, K.; et al. Effects of endogenous cysteine proteinases on structures of collagen fibres from dermis of sea cucumber (Stichopus japonicus). Food Chem. 2017, 232, 10–18. [Google Scholar] [CrossRef]
- Qi, H.; Fu, H.; Dong, X.f.; Feng, D.D.; Li, N.; Wen, C.R.; Nakamura, Y.; Zhu, B.W. Apoptosis induction is involved in UVA-induced autolysis in sea cucumber Stichopus japonicus. J. Photochem. Photobiol. B Biol. 2016, 158, 130–135. [Google Scholar] [CrossRef]
- Liu, Z.Q.; Zhou, D.y.; Liu, Y.X.; Liu, X.Y.; Liu, Y.; Liu, B.; Song, L.; Shahidi, F. In vivo mechanism of action of matrix metalloprotease (MMP) in the autolysis of sea cucumber (Stichopus japonicus). J. Food Process. Preserv. 2020, 44, e14383. [Google Scholar] [CrossRef]
- Tan, Z.F.; Ding, Y.T.; Tian, J.Y.; Liu, Z.Q.; Bi, J.R.; Zhou, D.Y.; Song, L.; Chen, G.B. Inhibition of ultraviolet-induced sea cucumber (Stichopus japonicus) autolysis by maintaining coelomocyte intracellular calcium homeostasis. Food Chem. 2022, 368, 130768. [Google Scholar] [CrossRef]
- Wang, J.; Lin, L.; Sun, X.; Hou, H. Mechanism of sea cucumbers (Apostichopus japonicus) body wall changes under different thermal treatment at micro-scale. LWT-Food Sci. Technol. 2020, 130, 109461. [Google Scholar] [CrossRef]
- Dong, X.F.; Qi, H.; Feng, D.D.; He, B.Y.; Zhu, B.W. Oxidative stress involved in textural changes of sea cucumber Stichopus japonicus body wall during low-temperature treatment. Int. J. Food Prop. 2018, 21, 2646–2659. [Google Scholar] [CrossRef]
- Wu, H.T.; Li, D.M.; Zhu, B.W.; Du, Y.; Chai, X.Q.; Murata, Y. Characterization of acetylcholinesterase from the gut of sea cucumber Stichopus japonicus. Fish. Sci. 2013, 79, 303–311. [Google Scholar] [CrossRef]
- Sun, L.M.; Wang, T.T.; Zhu, B.W.; Niu, H.L.; Zhang, R.; Hou, H.M.; Zhang, G.L.; Murata, Y. Effect of matrix metalloproteinase on autolysis of sea cucumber Stichopus japonicus. Food Sci. Biotechnol. 2013, 22, 1–3. [Google Scholar] [CrossRef]
- Zhou, D.Y.; Chang, X.N.; Bao, S.S.; Song, L.; Zhu, B.W.; Dong, X.P.; Zong, Y.; Li, D.M.; Zhang, M.M.; Liu, Y.X.; et al. Purification and partial characterisation of a cathepsin L-like proteinase from sea cucumber (Stichopus japonicus) and its tissue distribution in body wall. Food Chem. 2014, 158, 192–199. [Google Scholar] [CrossRef] [PubMed]
- Zhu, B.W.; Zhao, L.L.; Sun, L.M.; Li, D.M.; Murata, Y.; Yu, L.; Zhang, L. Purification and characterization of a cathepsin L-like enzyme from the body wall of the sea cucumber Stichopus japonicus. Biosci. Biotechnol. Biochem. 2008, 72, 1430–1437. [Google Scholar] [CrossRef] [PubMed]
- Xiong, X.; He, B.Y.; Jiang, D.; Dong, X.F.; Yu, C.X.; Hang, Q. Postmortem biochemical and textural changes in the sea cucumber Stichopus japonicus body wall (SJBW) during iced storage. LWT-Food Sci. Technol. 2020, 118, 108705. [Google Scholar] [CrossRef]
- Fu, X.Y.; Xue, C.H.; Miao, B.C.; Li, Z.J.; Yang, W.G.; Wang, D.F. Study of a highly alkaline protease extracted from digestive tract of sea cucumber (Stichopus japonicus). Food Res. Int. 2005, 38, 323–329. [Google Scholar] [CrossRef]
- Su, L.; Yang, J.F.; Fu, X.; Dong, L.; Zhou, D.Y.; Sun, L.M.; Gong, Z.W. Ultraviolet-ray-induced sea cucumber (Stichopus japonicus) melting is mediated by the caspase-dependent mitochondrial apoptotic pathway. J. Agric. Food Chem. 2018, 66, 45–52. [Google Scholar] [CrossRef]
- Sun, J.H.; Zheng, J.; Wang, Y.N.; Yang, S.L.; Yang, J.F. The exogenous autophagy inducement alleviated the sea cucumber (Stichopus japonicus) autolysis with exposure to stress stimuli of ultraviolet light. J. Sci. Food Agric. 2022, 102, 3416–3424. [Google Scholar] [CrossRef]
- Scott, J.E. Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. FASEB J. 1992, 6, 2639–2645. [Google Scholar] [CrossRef]
- Scott, J.E.; Orford, C.R.; Hughes, E.W. Proteoglycan-collagen arrangements in developing rat tail tendon. An electron microscopical and biochemical investigation. Biochem. J. 2019, 195, 573–581. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.X.; Zhou, D.Y.; Ma, D.D.; Liu, Y.F.; Li, D.M.; Dong, X.P.; Tan, M.Q.; Du, M.; Zhu, B.W. Changes in collagenous tissue microstructures and distributions of cathepsin L in body wall of autolytic sea cucumber (Stichopus japonicus). Food Chem. 2016, 212, 341–348. [Google Scholar] [CrossRef]
- Liang, X.W. Changes of Collagenous Tissue in Body Wall of Autolytic Sea Cucumber Sitcgopus japonicus. Master’s thesis, Dalian Polytechnic University, Dalian, China, 2016. (In Chinese). [Google Scholar]
- Liu, Z.Q.; Tuo, F.Y.; Song, L.; Liu, Y.X.; Dong, X.P.; Li, D.M.; Zhou, D.Y.; Shahidi, F. Action of trypsin on structural changes of collagen fibres from sea cucumber (Stichopus japonicus). Food Chem. 2018, 256, 113–118. [Google Scholar] [CrossRef] [PubMed]
- Liu, Z.Q.; Zhou, D.Y.; Liu, Y.X.; Yu, M.M.; Liu, B.; Song, L.; Dong, X.P.; Qi, H.; Shahidi, F. Inhibitory effect of natural metal ion chelators on the autolysis of sea cucumber (Stichopus japonicus) and its mechanism. Food Res. Int. 2020, 133, 109205. [Google Scholar] [CrossRef]
- Bi, J.R.; Yong, L.; Cheng, S.S.; Dong, X.P.; Kamal, T.; Zhou, D.Y.; Li, D.M.; Jiang, P.F.; Zhu, B.W.; Tan, M. Changes in body wall of sea cucumber (Stichopus japonicus) during a two-step heating process assessed by rheology, LF-NMR, and texture profile analysis. Food Biophys. 2016, 11, 257–265. [Google Scholar] [CrossRef]
- Liu, Z.Q.; Li, D.Y.; Song, L.; Liu, Y.X.; Yu, M.M.; Zhang, M.; Rakariyatham, K.; Zhou, D.Y.; Shahidi, F. Effects of proteolysis and oxidation on mechanical properties of sea cucumber (Stichopus japonicus) during thermal processing and storage and their control. Food Chem. 2020, 330, 127248. [Google Scholar] [CrossRef]
- Liu, Z.Q.; Liu, Y.X.; Zhou, D.Y.; Liu, Y.X.; Dong, X.P.; Li, D.M.; Shahidi, F. The role of matrix metalloprotease (MMP) to the autolysis of sea cucumber (Stichopus japonicus). J. Sci. Food Agric. 2019, 99, 5752–5759. [Google Scholar] [CrossRef]
- Wu, H.T.; Li, D.M.; Zhu, B.W.; Sun, J.J.; Zheng, J.; Wang, F.L.; Konno, K.; Xi, J. Proteolysis of noncollagenous proteins in sea cucumber, Stichopus japonicus, body wall: Characterisation and the effects of cysteine protease inhibitors. Food Chem. 2013, 141, 1287–1294. [Google Scholar] [CrossRef] [PubMed]
- Gu, P.; Qi, S.Z.; Zhai, Z.Y.; Liu, J.; Liu, Z.Y.; Jin, Y.; Qi, Y.X.; Zhao, Q.C.; Wang, F.J. Comprehensive proteomic analysis of sea cucumbers (Stichopus japonicus) in thermal processing by HPLC-MS/MS. Food. Chem. 2022, 373, 131368. [Google Scholar] [CrossRef]
- Dong, X.F.; Shen, P.; Yu, M.Q.; Yu, C.X.; Zhu, B.W.; Hang, Q. (-)-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. [Google Scholar] [CrossRef]
- Xiong, X.; Xie, W.C.; Xie, J.W.; Qi, H.; Yang, X.H.; Chen, H.X.; Song, L.; Dong, X.F. Protein oxidation results in textural changes in sea cucumber (Apostichopus japonicus) during tenderization. LWT-Food Sci. Technol. 2021, 144, 111231. [Google Scholar] [CrossRef]
- Sun, L.M.; Zhu, B.W.; Wu, H.T.; Yu, L.; Zhou, D.Y.; Dong, X.P.; Yang, J.F.; Li, D.M.; Ye, W.X.; Murata, Y. Purification and characterization of cathepsin B from the gut of the sea cucumber (Stichopus japonicas). Food Sci. Biotechnol. 2011, 20, 919–925. [Google Scholar] [CrossRef]
- Guo, X.K.; Li, A.T.; Han, J.R.; Du, Y.N.; Guo, T.M.; Yu, C.P.; Tang, Y.; Wu, H.T. Extraction and characterization of cathepsin D from sea cucumber (Stichopus japonicus) guts. Sci. Technol. Food Ind. 2017, 18, 135–139. (In Chinese) [Google Scholar] [CrossRef]
- Zhu, B.W.; Zhao, J.G.; Yang, J.F.; Mikiro, T.; Zhang, Z.S.; Zhou, D.Y. Purification and partial characterization of a novel β-1,3-glucanase from the gut of sea cucumber Stichopus japonicus. Process. Biochem. 2008, 43, 1102–1106. [Google Scholar] [CrossRef]
- Wu, H.T.; Li, D.M.; Zhu, B.W.; Cheng, J.H.; Sun, J.J.; Wang, F.L.; Yang, Y.L.; Song, Y.K.; Yu, C.X. Purification and characterization of alkaline phosphatase from the gut of sea cucumber Stichopus japonicus. Fish. Sci. 2013, 79, 477–485. [Google Scholar] [CrossRef]
- Xu, S.Q.; Zhang, Z.Y.; Nie, B.; Du, Y.N.; Tang, Y.; Wu, H.T. Characteristics of the intestine extracts and their effect on the crude collagen fibers of the body wall from sea cucumber Apostichopus japonicus. Biology 2023, 12, 705. [Google Scholar] [CrossRef] [PubMed]
- Fu, H.; Zhang, J.Y.; Zhao, X.T.; Liu, Q.; Xu, Z.; Feng, D.D.; Wei, J.Y.; Hang, Q. Extraction and characterization of superoxide dismutase from the body wall of sea cucumber Stichopus japonicus. Food Sci. Technol. 2015, 40, 150–154. (In Chinese) [Google Scholar] [CrossRef]
- Wang, L.; Nian, Y.Y.; Xu, P.; Ji, X.T.; Cui, Y.T.; Zhang, G.L.; Hou, H.M.; Sun, L.M. Two aspartic proteases in sea cucumber (Stichopus japonicus): Enzymatic properties and effect on autolysis. Food Sci. 2018, 39, 99–105. (In Chinese) [Google Scholar] [CrossRef]
- Ji, X.T.; Wang, L.; Xue, P.; Nian, Y.Y.; Zhou, W.R.; Zhang, Y.F.; Zhang, G.L.; Hou, H.M.; Sun, L.M. Characteristics of cathepsin K of sea cucumber Stichopus japonicus and its effects on autolysis. J. China Agric. Univ. 2017, 22, 72–77. (In Chinese) [Google Scholar]
- Zhu, B.W.; Yu, J.W.; Zhang, Z.S.; Zhou, D.Y.; Yang, J.F.; Li, D.M.; Murata, Y. Purification and partial characterization of an acid phosphatase from the body wall of sea cucumber Stichopus japonicus. Process. Biochem. 2009, 44, 875–879. [Google Scholar] [CrossRef]
- Wu, H.L.; Hu, Y.Q.; Shen, J.D.; Cai, Q.F.; Liu, G.M.; Su, W.J.; Cao, M.J. Identification of a novel gelatinolytic metalloproteinase (GMP) in the body wall of sea cucumber (Stichopus japonicus) and its involvement in collagen degradation. Process. Biochem. 2013, 48, 871–877. [Google Scholar] [CrossRef]
- Qi, H.; Dong, X.P.; Gao, Y.; Liu, L.; Mikiro, T.; Zhu, B.W. Purification and characterization of a cysteine-like protease from the body wall of the sea cucumber Stichopus japonicus. Fish Physiol. Biochem. 2007, 33, 181–188. [Google Scholar] [CrossRef]
- Zhong, M.; Hu, C.Q.; Ren, C.H.; Luo, X.; Cai, Y.M. Characterization of a main extracellular matrix autoenzyme from the dermis of sea cucumber Stichopus monotuberculatus: Collagenase. Int. J. Food Prop. 2016, 19, 2495–2509. [Google Scholar] [CrossRef]
- Zhang, J.; Zhang, Y.Q.; Luo, C.H.; Liu, Z.D.; Cheng, Y.F.; Lu, F.F.; Zhang, T. Purifi cation and characterization of α-1,4-amylase in body wall of sea cucumber. Food Sci. 2015, 36, 137–141. (In Chinese) [Google Scholar] [CrossRef]
- Li, Y.N.; Chen, Z.F.; Zhang, P.; Gao, F.; Wang, J.F.; Lin, L.; Zhang, H.B. Characterization of a novel superoxide dismutase from a deep-sea sea cucumber (Psychoropotes verruciaudatus). Antioxidants 2023, 12, 1227. [Google Scholar] [CrossRef]
- Yan, J.N.; Guo, X.K.; Tang, Y.; Li, A.T.; Zhu, Z.M.; Chai, X.Q.; Duan, X.H.; Wu, H.T. Contribution of cathepsin L to autolysis of sea cucumber Stichopus japonicus intestines. J. Aquat. Food Prod. Technol. 2019, 28, 233–240. [Google Scholar] [CrossRef]
- Martin, S.L.; Moffitt, K.L.; McDowell, A.; Greenan, C.; Bright-Thomas, R.J.; Jones, A.M.; Webb, A.K.; Elborn, J.S. Association of airway cathepsin B and S with inflammation in cystic fibrosis. Pediatr. Pulmonol. 2010, 45, 860–868. [Google Scholar] [CrossRef]
- Jiang, P.Z.; Gao, S.; Chen, Z.F.; Sun, H.J.; Li, P.P.; Yue, D.M.; Pan, Y.J.; Wang, X.D.; Mi, R.; Dong, Y.; et al. Cloning and characterization of a phosphomevalonate kinase gene that is involved in saponin biosynthesis in the sea cucumber Apostichopus japonicus. Fish Shellfish Immunol. 2022, 128, 67–73. [Google Scholar] [CrossRef]
- Benes, P.; Vetvicka, V.; Fusek, M. Cathepsin D-Many functions of one aspartic protease. Crit. Rev. Oncol./Hematol. 2008, 68, 12–28. [Google Scholar] [CrossRef]
- Yu, C.P.; Cha, Y.; Wu, F.; Xu, X.B.; Qin, L.; Du, M. Molecular cloning and functional characterization of cathepsin D from sea cucumber Apostichopus japonicus. Fish Shellfish Immunol. 2017, 70, 553–559. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.; Nelson-Moon, Z.L.; Thomas, G.J.; Hunt, N.P.; Lewis, M.P. Identification of matrix metalloproteinases and their tissue inhibitors type 1 and 2 in human masseter muscle. Arch. Oral Biol. 2000, 45, 431–440. [Google Scholar] [CrossRef] [PubMed]
- Tipper, J.P.; Lyons-Levy, G.; Atkinson, M.A.L.; Trotter, J.A. Purification, characterization and cloning of tensilin, the collagen-fibril binding and tissue-stiffening factor from Cucumaria frondosa dermis. Matrix Biol. 2002, 21, 625–635. [Google Scholar] [CrossRef] [PubMed]
- Coriicchiato, O.; Cajot, J.-F.; Abrahamson, M.; Chan, S.J.; Keppler, D.; Sordat, B. Cystatin C and cathepsin B in human colon carcinoma: Expression by cell lines and matrix degradation. Int. J. Cancer 1992, 52, 645–652. [Google Scholar] [CrossRef] [PubMed]
- Garnero, P.; Borel, O.; Byrjalsen, I.; Ferreras, M.; Drake, F.H.; McQueney, M.S.; Foged, N.T.; Delmas, P.D.; Delaissé, J.-M. The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J. Biol. Chem. 1998, 273, 32347–32352. [Google Scholar] [CrossRef] [PubMed]
- Helske, S.; Syväranta, S.; Lindstedt, K.A.; Lappalainen, J.; Öörni, K.; Lommi, J.; Turto, H.; Werkkala, K.; Kupari, M.; Kovanen, P. Increased expression of elastolytic cathepsins S, K, and V, and their inhibitor cystatin C in stenotic aortic valves. Arterioscler. Thromb. Vasc. Biol. 2006, 7, 242–243. [Google Scholar] [CrossRef] [PubMed]
- Davies, D.R. The structure and function of the aspartic proteinases. Annu. Rev. Biophys. Biophys. Chem. 1990, 19, 189–215. [Google Scholar] [CrossRef]
- Takashi, S.; Hideaki, S.; Yasuaki, S.; Yuzo, K.; Kenji, Y. An immunocytochemical study on distinct intracellular localization of Cathepsin E and Cathepsin D in human gastric cells and various rat cells. J. Biochem. 1991, 110, 956–964. [Google Scholar] [CrossRef]
- Laronha, H.; Caldelra, J. Structure and function of human matrixmetalloproteinases. Cell 2020, 9, 1076. [Google Scholar] [CrossRef]
- Trotter, J.A.; Lyons-Levy, G.; Chino, K.; Koob, T.J.; Keene, D.R.; Atkinson, M.A.L. Collagen fibril aggregation-inhibitor from sea cucumber dermis. Matrix Biol. 1999, 18, 569–578. [Google Scholar] [CrossRef]
- Zhang, Y.T.; Zhao, B.L. Green tea polyphenols enhance sodium nitroprusside-induced neurotoxicity in human neuroblastoma SH-SY5Y cells. J. Neurochem. 2003, 86, 1189–1200. [Google Scholar] [CrossRef] [PubMed]
- Fomina, M.; Hillier, S.; Charnock, J.M.; Melville, K.; Alexander, L.J.; Gadd, G.M. Role of oxalic acid overexcretion in transformations of toxic metal minerals by Beauveria caledonica. Appl. Environ. Microbiol. 2005, 71, 371–381. [Google Scholar] [CrossRef] [PubMed]
- Ming, Y.; Wang, Y.Z.; Xie, Y.Q.Q.; Sun, C.H.; Dong, X.F.; Nakamura, Y.; Chen, X.; Dong, X.P.; Qi, H. Phlorotannin extracts from Ascophyllum nodosum inhibited proteases activities and structural changes from Apostichopus japonicus. ACS Food Sci. Technol. 2022, 2, 1586–1596. [Google Scholar] [CrossRef]
- Ming, Y.; Wang, Y.Z.; Xie, Y.Q.Q.; Dong, X.F.; Nakamura, Y.; Chen, X.; Qi, H. Polyphenol extracts from Ascophyllum nodosum protected sea cucumber (Apostichopus japonicas) body wall against thermal degradation during tenderization. Food Res. Int. 2023, 164, 112419. [Google Scholar] [CrossRef] [PubMed]
- Guo, Y.C.; Ming, Y.; Li, X.; Sun, C.H.; Dong, X.P.; Qi, H. Effect of phlorotannin extracts from Ascophyllum nodosum on the textural properties and structural changes of Apostichopus japonicus. Food Chem. 2024, 437, 137918. [Google Scholar] [CrossRef] [PubMed]
- Guo, Y.C.; Ming, Y.; Sun, K.L.; Dong, X.F.; Nakamura, Y.; Dong, X.P.; Qi, H. Polyphenol oxidase mediates (−)-epigallocatechin gallate to inhibit endogenous cathepsin activity in Apostichopus japonicus. Food Chem. 2024, 449, 139166. [Google Scholar] [CrossRef]
- Du, Y.N.; Li, A.T.; Yan, J.N.; Jiang, X.Y.; Wu, H.T. Inhibitory effect of coelomic fluid isolates on autolysis of minced muscle tissue from sea cucumber Stichopus japonicus. J. Food Meas. Charact. 2021, 15, 4575–4581. [Google Scholar] [CrossRef]
Enzymes Species | Endogenous Enzymes | Heating/Storage Condition | Target Protein | Inhibitors | Metal ions (Activation (↑)/Inactivation (↓)) | Molecule Weight | Textural Properties Decrease (↓) | References |
---|---|---|---|---|---|---|---|---|
Metalloprotease (MMP) | Matrix metalloproteinase-2 (MMP-2) | 25 °C for 72 h | Type I collagen | NaN3 (0.03%), PMSF (5 mM), E-64 (0.1 mM) and CaCl2 (5 mM) | - | - | - | [16] |
Gelatinolytic metalloproteinase (GMP) | 37 °C for 18 h | Collagen bands (α1 and β) | EDTA (10 mM); EGTA (10 mM); 1,10-phenanthroline (10 mM) | Ca2+ (↑) | 45 kDa | - | [25] | |
Collagenase type I | 30 °C for 72 h | Collagen fibers | - | - | - | - | [13] | |
Matrix metalloproteinase (MMP) | Boiled (10 min) sea cucumber stored at 4 °C for 60 d | Extracellular matrix in the dermis; Interfibrillar proteoglycan bridges | EDTA Na2 (10 mM); 1,10-phenanthroline (10 mM) | Ca2+ (↑) | - | Shear force (↓); hardness (↓); elasticity (↓); cohesiveness (↓); chewiness (↓); coverability (↓) | [21,26] | |
Cysteine protease (CP) | Cysteine proteinases | 37 °C for 2~72 h | Collagen fibers | PMSF (1 mM), 1,10-phenanthroline (1 mM), and E-64 (0.5 mM) | - | - | - | [19] |
Cathepsin L-like proteinase | 20~70 °C for 30 min | The epidermis of the body wall | E-64 (0.1 mM); Indoacetic acid (1 mM); Antipain (1 mM) | Zn2+ (↓); Cu2+ (↓); Fe2+ (↓) | 30.9 kDa | - | [27,28] | |
Cathepsin L and Cathepsin B | 4 °C for 8 days | Body wall | - | - | - | Hardness (↓); chewiness (↓); springiness (↓); adhesiveness (↓) | [29] | |
Serine proteinase (SP) | High alkaline protease (serine protease-like) | 4~65 °C for 1 h | - | EDTA (10 mM); PMSF (5 mM) | Ca2+ (↑); Mg2+ (↑); Cu2+ (↑); Zn2+ (↓); Hg2+ (↓); | 20.6 kDa; 39.1 kDa; 114.1 kDa; | - | [30] |
Serine proteinase | 37 °C for 12 h | Collagen bands (α, β and γ) | Pefabloc SC (2 mM); Benzamidine (5 mM) | - | 34 kDa | - | [15] | |
Mixed protease system | Cysteine (cathepsins, calpains, caspases and proteasomes), serine protease and MMP | 37 °C for 1~36 h | Body wall | E-64 (0.1 mM); PMSF (1 mM); 1,10-phenanthroline (1 mM) | - | - | Hardness (↓); chewiness (↓) | [17,24] |
Sea Cucumber Species | Enzyme Types | Extracted Position | Molecule Weight (kDa) | Optimum Temperature (°C) | Optimum pH | Activator | Inhibitors | References |
---|---|---|---|---|---|---|---|---|
Janpanese sea cucumber (Apostichopus japonicus) | Cathepsin B | Intestine | 49 | 45 | 5.5 | DTT, L-Cys, EGTA, EDTA | E-64, IAA, Antipain, Cu2+, Ni2+, Zn2+ | [46] |
Cathepsin L | Intestine | - | 48 | 4.4 | - | E-64, IAA, Antipain | [60] | |
Cathepsin D | Intestine | - | 50 | 3.0 | Cd2+ | E-64, IAA, Pepstatin A, Fe3+, Fe2+ | [47] | |
Body wall | 60 | 5.0 | DTT | Pepstatin A, PMSF, Zn2+,Cu2+, Fe2+,Fe3+, Mn2+ | [51] | |||
β-1,3-glucanase | Intestine | 37.5 | 40 | 5.5 | Mn2+ | Cu2+, Ag+, Zn2+, Fe2+, Ca2+ | [48] | |
ACP | Body wall | 148 | 40 | 4.0 | Mg2+ | Zn2+, Cu2+, Fe2+, Fe3+ | [54] | |
ALP | Intestine | 166 ± 9 | 40 | 11.0 | Mg2+ | Zn2+, Ca2+, EDAT | [49] | |
AChE | Intestine | 68 | 35 | 7.5 | - | Eserine, BW284C51 | [25] | |
SP | Intestine | 34 | 35-40 | 6.0–9.0 | EDTA | Leupeptin, Cu2+, Zn2+, Mg2+, Mn2+, Ca2+, Fe2+ | [15] | |
SEP | Intestine | - | 40 | 9.0 | - | PMSF | [50] | |
Cathepsin L-like proteinase | Body wall | 30.9 | 50 | 5.0–5.5 | DTT, L-Cys, EDTA | E-64, IAA, Antipain, Zn2+, Fe2+, Cu2+ | [27] | |
Cathepsin E | Body wall | - | 40 | 4.0 | DTT | Pepstatin A, PMSF, Fe3+, Fe2+, Cu2+ | [52] | |
Cathepsin K | Body wall | - | 50 | 5.0 | Mg2+, DTT, L-Cys, | E-64, IAA, Antipain, PMSF, EDTA, Zn2+, Fe2+, Fe3+, Cu2+ | [53] | |
Cysteine-like protease | Body wall | 35.5 | 50 | 7.0 | L-cysteine hydrochloride | Antipain, leupeptin, Cu2+, Mg2+, Fe2+, Fe3+ | [56] | |
GMP | Body wall | 45 | 40-45 | 8.0–9.0 | Ca2+, Ba2+ | EDTA, EGTA, 1,10- phenanthroline | [55] | |
α-1,4-amylase | Body wall | 420 | 80 | 9.0 | Cu2+, Mg2+ | Mn2+, K+, Fe3+ | [58] | |
Collagenase | Body wall | 45 | 40 | 8.0 | Mn2+ | EDTA, 1,10-phenanthroline | [57] | |
SOD | Body wall | - | 30-60 | 4.0 | Ca2+, Zn2+ | H2O2, Fe2+ | [51] | |
Deep-sea sea cucumber (Psychoropotes verruciaudatus) | PVCuZnSOD | - | 15 | 20 | 4–11 | Mg2+, Ni2+ | Mn2+, Cu2+, Zn2+, Co2+ | [59] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Fan, X.; Wu, K.; Tian, X.; Benjakul, S.; Li, Y.; Sang, X.; Zhao, Q.; Zhang, J. Endogenous Proteases in Sea Cucumber (Apostichopus japonicas): Deterioration and Prevention during Handling, Processing, and Preservation. Foods 2024, 13, 2153. https://doi.org/10.3390/foods13132153
Fan X, Wu K, Tian X, Benjakul S, Li Y, Sang X, Zhao Q, Zhang J. Endogenous Proteases in Sea Cucumber (Apostichopus japonicas): Deterioration and Prevention during Handling, Processing, and Preservation. Foods. 2024; 13(13):2153. https://doi.org/10.3390/foods13132153
Chicago/Turabian StyleFan, Xinru, Ke Wu, Xiuhui Tian, Soottawat Benjakul, Ying Li, Xue Sang, Qiancheng Zhao, and Jian Zhang. 2024. "Endogenous Proteases in Sea Cucumber (Apostichopus japonicas): Deterioration and Prevention during Handling, Processing, and Preservation" Foods 13, no. 13: 2153. https://doi.org/10.3390/foods13132153