Progress and application of collagenase research

doi:10.11949/0438-1157.20190328

Abstract

Abstract:

Collagen is widely distributed in various tissues of living organisms and is one of the basic proteins that constitute living organisms. The structure of collagen is more complicated than that of general protein and it displays a more stable property so that normal proteases have no significant effect to deal with it. There are only two typical enzymes have ability to hydrolyze collagen in situ, one is called matrix metalloproteinase (MMP) and another is bacterial collagenase. In this review the collagen and hydrolase are introduced in briefly, then the development process and the hydrolysis mechanism to collagen between matrix metalloproteinase and collagenase are presented, then the particular aspects of the different enzyme activities will be contextualized within relevant areas of application, mainly about therapeutics, food processing, environmental protection and tissue engineering. In the end the development of the present research and guide further potential research orientation of the system of collagen & collagenase is summarized.

Key words: bioengineering, enzyme, protein, matrix metalloproteinase, bacterial collagenase

摘要：

胶原蛋白广泛存在于有机体生命各组织，是构成生命体的基础性蛋白之一。胶原蛋白结构相对复杂、稳定性良好、不易受到普通蛋白酶的降解破坏。而基质金属蛋白酶和微生物胶原酶是为数不多能原位降解胶原蛋白的两类胶原酶，能够在生理环境下保持较高酶活力从而发挥作用，因此受到研究者的广泛关注。首先简要介绍胶原蛋白及其水解酶，其次重点介绍基质金属蛋白酶和微生物胶原酶的发掘历程和水解机理，然后综述这两类酶的最新研究进展及其在医疗诊治、食品加工、环境保护及组织工程等多方面的应用，最后总结胶原酶及胶原蛋白研究现状、研究难点和未来研究方向。

关键词: 生物工程, 酶, 蛋白质, 基质金属蛋白酶, 微生物胶原酶

CLC Number:

Q 814.9

Yihang SONG, Chuhao WANG, Baishan FANG. Progress and application of collagenase research[J]. CIESC Journal, 2019, 70(9): 3213-3227.

宋易航, 王楚浩, 方柏山. 胶原酶研究进展与应用[J]. 化工学报, 2019, 70(9): 3213-3227.

Figures/Tables 5

References 96

1	Shoulders M D , Raines R T . Collagen structure and stability[J]. Annual Review of Biochemistry, 2009, 78(1): 929-958.
2	Veit G , Kobbe B , Keene D R , et al . Collagen ⅩⅩⅧ, a novel von Willebrand factor a domain-containing protein with many imperfections in the collagenous domain[J]. Journal of Biological Chemistry, 2006, 281(6): 3494-3504.
3	Pauling L , Corey R B . The structure of fibrous proteins of the collagen-gelatin group[J]. Proceedings of the National Academy of Sciences, 1951, 37(5): 272-281.
4	Rich A , Crick F H C . The structure of collagen[J]. Nature, 1955, 176: 915-916.
5	Ramshaw J A M , Shah N K , Brodsky B . Gly-XY tripeptide frequencies in collagen: a context for host-guest triple-helical peptides[J]. Journal of Structural Biology, 1998, 122(1/2): 86-91.
6	Boryskina O P , Bolbukh T V , Semenov M A , et al . Energies of peptide–peptide and peptide-water hydrogen bonds in collagen: evidences from infrared spectroscopy quartz piezogravimetry and differential scanning calorimetry[J]. Journal of Molecular Structure, 2007, 827(1): 1-10.
7	Hyde T J , Bryan M A , Brodsky B , et al . Sequence dependence of renucleation after a Gly mutation in model collagen peptides[J]. Journal of Biological Chemistry, 2006, 281(48): 36937.
8	Khoshnoodi J , Cartailler J P , Alvares K , et al . Molecular recognition in the assembly of collagens: terminal noncollagenous domains are key recognition modules in the formation of triple helical protomers[J]. Journal of Biological Chemistry, 2006, 25(50): 38117-38121.
9	Raghunath M , Bruckner P , Steinmann B . Delayed triple helix formation of mutant collagen from patients with osteogenesis imperfecta[J]. Journal of Molecular Biology, 1994, 236(3): 940.
10	Cram D J . The design of molecular hosts, guests, and their complexes[J]. Journal of Inclusion Phenomena, 1988, 27(8): 1009-1020.
11	Berg R A , Prockop D J . The thermal transition of a non-hydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen[J]. Biochemical and Biophysical Research Communications, 1973, 52(1): 115-120.
12	Kim C A , Berg J M . Thermodynamic β-sheet propensities measured using a zinc-finger host peptide[J]. Nature, 1993, 362(6417): 267-270.
13	Minor D L , Kim P S . Measurement of the β-sheet-forming propensities of amino acids[J]. Nature, 1994, 367(6464): 660-663.
14	Buehler M J . Nature designs tough collagen: explaining the nanostructure of collagen fibrils [J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(33): 12285-12290.
15	Chung L , Dinakarpandian D , Yoshida N , et al . Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis[J]. The EMBO Journal, 2004, 23(15): 3020-3030.
16	Zhao W , Byrne M H , Boyce B F , et al . Bone resorption induced by parathyroid hormone is strikingly diminished in collagenase-resistant mutant mice[J]. Journal of Clinical Investigation, 1999, 103(4): 517-524.
17	Gross J , Lapiere C M . Collagenolytic activity in amphibian tissues: a tissue culture assay[J]. Proceedings of the National Academy of Sciences of the United States of America, 1962, 48(6): 1014-1022.
18	Brinckerhoff C E , Matrisian L M . Matrix metalloproteinases: a tail of a frog that became a prince[J]. Nature Reviews Molecular Cell Biology, 2002, 3(3): 207-214.
19	Visse R , Nagase H . Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry[J]. Circulation Research, 2003, 92(8): 827-839.
20	Peng W , Yan J , Wan Y , et al . Matrix metalloproteinases: a review of their structure and role in systemic sclerosis[J]. Journal of Clinical Immunology, 2012, 32(6): 1409-1414.
21	van Wart H E , Birkedal-Hansen H . The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family[J]. Proceedings of the National Academy of Sciences, 1990, 87(14): 5578-5582.
22	Itoh Y , Takamura A , Ito N , et al . Homophilic complex formation of MT1‐MMP facilitates proMMP‐2 activation on the cell surface and promotes tumor cell invasion[J]. The EMBO Journal, 2001, 20(17): 4782-4793.
23	Gomis-Rüth F X , Maskos K , Betz M , et al . Mechanism of inhibition of the human matrix metalloproteinase stromelysin-1 by TIMP-1[J]. Nature, 1997, 389(6646): 77.
24	Goldberg G I , Strongin A , Collier I E , et al . Interaction of 92-kDa type Ⅳ collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin[J]. J.Biol. Chem., 1992, 267(7): 4583-4591.
25	Fields G B , Prockop D J . Perspectives on the synthesis and application of triple‐helical, collagen‐model peptides[J]. Peptide Science, 1996, 40(4): 345-357.
26	Bertini I , Calderone V , Fragai M , et al . Snapshots of the reaction mechanism of matrix metalloproteinases[J]. Angewandte Chemie, 2006, 45(47): 7952-7955.
27	Iyer S , Visse R , Nagase H , et al . Crystal structure of an active form of human MMP-1[J]. Journal of Molecular Biology, 2006, 362(1): 78-88.
28	Manka S W , Carafoli F , Visse R , et al . Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1[J]. Proceedings of the National Academy of Sciences, 2012, 109(31): 12461-12466.
29	Bertini I , Fragai M , Luchinat C , et al . Structural basis for matrix metalloproteinase 1-catalyzed collagenolysis[J]. Journal of the American Chemical Society, 2012, 134(4): 2100-2110.
30	Maclennan J D , Mandl I , Howes E L . Bacterial digestion of collagen[J]. Journal of Clinical Investigation, 1954, 32(12): 1317-1322.
31	Shi L , Carson D . Collagenase Santyl ointment: a selective agent for wound debridement[J]. Journal of Wound Ostomy & Continence Nursing, 2009, 36(6S): S12-S16.
32	Allen F E , Larick D K . Tenderization of beef with bacterial collagenase[J]. Meat Science, 1986, 18(3): 201-214.
33	Duarte A S , Correia A , Esteves A C . Bacterial collagenases—a review[J]. Critical Reviews in Microbiology, 2016, 42(1): 106-126.
34	Weinberg M , Randin A . Proprietes physicochimiques du ferment fibrolytique d’origine microbienne[J]. Compt. Rend. Soc. Biol., 1932, 110: 352.
35	Matsushita O , Koide T , Kobayashi R , et al . Substrate recognition by the collagen-binding domain of Clostridium histolyticum Class I collagenase[J]. Journal of Biological Chemistry, 2001, 276(12): 8761-8770.
36	Matsushita O , Jung C M , Katayama S , et al . Gene duplication and multiplicity of collagenases in Clostridium histolyticum [J]. Journal of Bacteriology, 1999, 181(3): 923-933.
37	Eckhard U , Brandstetter H . Polycystic kidney disease-like domains of clostridial collagenases and their role in collagen recruitment[J]. Biological Chemistry, 2011, 392(11): 1039-1045.
38	Vaitkevicius K , Rompikuntal P K , Lindmark B , et al . The metalloprotease PrtV from Vibrio cholerae [J]. FEBS Journal, 2008, 275(12): 3167-3177.
39	Eckhard U , Schönauer E , Nüss D , et al . Structure of collagenase G reveals a chew-and-digest mechanism of bacterial collagenolysis[J]. Nature Structural & Molecular Biology, 2011, 18(10): 1109-1114.
40	Wilson J J , Matsushita O , Okabe A , et al . A bacterial collagen‐binding domain with novel calcium‐binding motif controls domain orientation[J]. The EMBO Journal, 2003, 22(8): 1743-1752.
41	Popoff M R , Bouvet P . Clostridial toxins[J]. Future Microbiology, 2009, 4(8): 1021-1064.
42	Pruteanu M , Hyland N P , Clarke D J , et al . Degradation of the extracellular matrix components by bacterial-derived metalloproteases: implications for inflammatory bowel diseases[J]. Inflammatory Bowel Diseases, 2011, 17(5): 1189-1200.
43	Choi J S , Ha Y M , Joo C U , et al . Inhibition of oral pathogens and collagenase activity by seaweed extracts[J]. Journal of Environmental Biology, 2012, 33(1): 115.
44	Maeda H , Yamamoto T . Pathogenic mechanisms induced by microbial proteases in microbial infections[J]. Biological Chemistry Hoppe-Seyler, 1996, 377(4): 217.
45	Fratzl P . Collagen: Structure and Mechanics, an Introduction[M]. US: Springer, 2008: 1-13.
46	Martin-Ferrero M . Ten-year long-term results of total joint arthroplasties with ARPE(R) implant in the treatment of trapeziometacarpal osteoarthritis[J]. Journal of Hand Surgery (European Volume), 2014, 39(8): 826-832.
47	Hupez A , Detrembleur C , van Innis F , et al . Comparative study of collagenase injection versus fasciectomy in Dupuytren’s contracture: a 1-year follow-up[J]. Louvain. Med., 2017, 136(4): 231-237.
48	Badalamente M A , Hurst L C . Development of collagenase treatment for dupuytren disease[J]. Hand Clinics, 2018, 34(3): 345-349.
49	Villegas M R , Baeza A , Usategui A , et al . Collagenase nanocapsules: an approach to fibrosis treatment[J]. Acta Biomaterialia, 2018, 74: 430-438.
50	Zhang D , Zhang Y , Wang Z , et al . Target radiofrequency combined with collagenase chemonucleolysis in the treatment of lumbar intervertebral disc herniation[J]. International Journal of Clinical and Experimental Medicine, 2015, 8(1): 526.
51	Huett E , Bartley W , Morris D , et al . Collagenase for wound debridement in the neonatal intensive care unit: a retrospective case series[J]. Pediatric Dermatology, 2017, 34(3): 277-281.
52	Eikenes L , Tari M , Tufto I , et al . Hyaluronidase induces a transcapillary pressure gradient and improves the distribution and uptake of liposomal doxorubicin (Caelyx™) in human osteosarcoma xenografts[J]. British Journal of Cancer, 2005, 93(1): 81-88.
53	Eikenes L , Tufto I , Schnell E A , et al . Effect of collagenase and hyaluronidase on free and anomalous diffusion in multicellular spheroids and xenografts[J]. Anticancer Research, 2010, 30(2): 359-368.
54	Gómez-Guillén M C , Ihl M , Bifani V , et al . Edible films made from tuna-fish gelatin with antioxidant extracts of two different murta ecotypes leaves (Ugni molinae Turcz)[J]. Food HydroColloids, 2007, 21(7): 1133-1143.
55	Karim A A . Fish gelatin: properties, challenge and prospects as an alternative to mammalian gelatins[J]. Food HydroColloids, 2009, 23(3): 563-576.
56	Rawdkuen S , Saiut S , Benjakul S . Properties of gelatin films from giant catfish skin and bovine bone: a comparative study[J]. European Food Research & Technology, 2010, 231(6): 907-916.
57	Zhang Y , Kouguchi T , Shimizu K , et al . Chicken collagen hydrolysate reduces proinflammatory cytokine production in C57BL/6.KOR-ApoEshl mice[J]. Journal of Nutritional Science & Vitaminology, 2010, 56(3): 208.
58	Saito M , Kiyose C , Higuchi T , et al . Effect of collagen hydrolysates from salmon and trout skins on the lipid profile in rats[J]. Journal of Agricultural & Food Chemistry, 2009, 57(21): 10477.
59	Hu H , Li B , Xue Z , et al . The effect of pacific cod (Gadus macrocephalus) skin gelatin polypeptides on UV radiation-induced skin photoaging in ICR mice[J]. Food Chemistry, 2012, 115(3): 945-950.
60	Giménez B , Alemán A , Montero P , et al . Antioxidant and functional properties of gelatin hydrolysates obtained from skin of sole and squid [J]. Food Chemistry, 2009, 114(3): 976-983.
61	Patrzykat A , Douglas S E . Antimicrobial peptides: cooperative approaches to protection[J]. Protein and Peptide Letters, 2005, 12(1): 19-25.
62	Ranathunga S , Rajapakse N , Kim S , et al . Purification and characterization of antioxidative peptide derived from muscle of conger eel (Conger myriaster)[J]. European Food Research and Technology, 2006: 310-315.
63	Ichimura T , Yamanaka A , Otsuka T , et al . Antihypertensive effect of enzymatic hydrolysate of collagen and Gly-Pro in spontaneously hypertensive rats[J]. Journal of the Agricultural Chemical Society of Japan, 2009, 73(10): 2317-2319.
64	Fu Y , Young J F , Løkke M M , et al . Revalorisation of bovine collagen as a potential precursor of angiotensin I-converting enzyme (ACE) inhibitory peptides based on in silico and in vitro protein digestions[J]. Journal of Functional Foods, 2016, 24: 196-206.
65	Lin L , Li B F . Radical scavenging properties of protein hydrolysates from jumbo flying squid (Dosidicus eschrichitii Steenstrup) skin gelatin[J]. Journal of the Science of Food & Agriculture, 2010, 86(14): 2290-2295.
66	Cheng F Y , Wan T C , Liu Y T , et al . Determination of angiotensin-I converting enzyme inhibitory peptides in chicken leg bone protein hydrolysate with alcalase[J]. Animal Science Journal, 2010, 80(1): 91-97.
67	Cheng F Y , Liu Y T , Wan T C , et al . The development of angiotensin I-converting enzyme inhibitor derived from chicken bone protein[J]. Animal Science Journal, 2010, 79(1): 122-128.
68	Gómez-Guillén M C , Giménez B , López-Caballero M E , et al . Functional and bioactive properties of collagen and gelatin from alternative sources: a review[J]. Food HydroColloids, 2011, 25(8): 1813-1827.
69	Fernandes P . Enzymes in food processing: a condensed overview on strategies for better biocatalysts[J]. Enzyme Research, 2010, 2010: 1-19.
70	Kemp C M , Sensky P L , Bardsley R G , et al . Tenderness—an enzymatic view[J]. Meat Science, 2010, 84(2): 248-256.
71	Zhao G Y , Zhou M Y , Zhao H L , et al . Tenderization effect of cold-adapted collagenolytic protease MCP-01 on beef meat at low temperature and its mechanism[J]. Food Chemistry, 2012, 134(4): 1738-1744.
72	Pal G K , Suresh P V . Microbial collagenases: challenges and prospects in production and potential applications in food and nutrition[J]. RSC Advances, 2016, 6(40): 33763-33780.
73	Plaza M , Cifuentes A , Ibáñez E . In the search of new functional food ingredients from algae[J]. Trends in Food Science & Technology, 2008, 19(1): 31-39.
74	Pangestuti R , Kim S K . Bioactive materials derived from seafood and seafood processing by-products[M]// Functional Foods and Dietary Supplements: Processing Effects and Health Benefits. New Jersey: John Wiley & Sons, Ltd., 2014: 139-158.
75	Wang B , Wang Y M , Chi C F , et al . Isolation and characterization of collagen and antioxidant collagen peptides from scales of croceine croaker (Pseudosciaena crocea)[J]. Marine Drugs, 2013, 11(11): 4641-4661.
76	Guo L , Harnedy P A , O’Keeffe M B , et al . Fractionation and identification of Alaska pollock skin collagen-derived mineral chelating peptides[J]. Food Chemistry, 2015, 173: 536-542.
77	Zhuang Y , Sun L , Li B . Production of the angiotensin-I-converting enzyme (ACE)-inhibitory peptide from hydrolysates of jellyfish (Rhopilema esculentum) collagen[J]. Food and Bioprocess Technology, 2012, 5(5): 1622-1629.
78	Gu Y , Liang Y , Bai J , et al . Spent hen-derived ACE inhibitory peptide IWHHT shows antioxidative and anti-inflammatory activities in endothelial cells[J]. Journal of Functional Foods, 2019, 53: 85-92.
79	O’Keeffe M B , Norris R , Alashi M A , et al . Peptide identification in a porcine gelatin prolyl endoproteinase hydrolysate with angiotensin converting enzyme (ACE) inhibitory and hypotensive activity[J]. Journal of Functional Foods, 2017, 34: 77-88.
80	Felician F F , Xia C , Qi W , et al . Collagen from marine biological sources and medical applications[J]. Chemistry & Biodiversity, 2018, 15(5): e1700557.
81	Saran S , Mahajan R V , Kaushik R , et al . Enzyme mediated beam house operations of leather industry: a needed step towards greener technology[J]. Journal of Cleaner Production, 2013, 54(9): 315-322.
82	Khandelwal H B , More S V , Kalal K M , et al . Eco-friendly enzymatic dehairing of skins and hides by C. brefeldianus protease[J]. Clean Technologies and Environmental Policy, 2015, 17(2): 393-405.
83	Thanikaivelan P , Rao J R , Nair B U , et al . Recent trends in leather making: processes, problems, and pathways[J]. Critical Reviews in Environmental Science and Technology, 2005, 35(1): 37-79.
84	Song J , Tao W , Chen W . Kinetics of enzymatic unhairing by protease in leather industry[J]. Journal of Cleaner Production, 2011, 19(4): 325-331.
85	Smail A M S , Housseiny M M , Abo-Elmagd H I , et al . Novel keratinase from Trichoderma harzianum MH-20 exhibiting remarkable dehairing capabilities[J]. International Biodeterioration & Biodegradation, 2012, 70: 14-19.
86	靳鸿蔚 .胶原酶产生菌的筛选、胶原酶的纯化及其酶学性质的研究[D].泉州: 华侨大学, 2007.
	Jin H W . Purification and partial characterization of a collagenase from a newly isolated strain of Bacillus megaterium [D]. Quanzhou: Huaqiao University, 2007.
87	Corso C R , Almeida E J R , Santos G C , et al . Bioremediation of direct dyes in simulated textile effluents by a paramorphogenic form of Aspergillus oryzae [J]. Water Science and Technology, 2012, 65(8): 1490-1495.
88	Kanth S V , Venba R , Madhan B , et al . Studies on the influence of bacterial collagenase in leather dyeing[J]. Dyes and Pigments, 2008, 76(2): 338-347.
89	王耿 .碱性脱毛蛋白酶菌株的选育及酶的提纯研究[D]. 泉州: 华侨大学, 2007.
	Wang G . Breeding of a strain producing alkaline protease for dehairing and studies on the purification of the enzyme[D]. Quanzhou: Huaqiao University, 2007.
90	Duarte A S , Rosa N , Duarte E P , et al . Cardosins: a new and efficient plant enzymatic tool to dissociate neuronal cells for the establishment of cell cultures[J]. Biotechnology & Bioengineering, 2010, 97(4): 991-996.
91	Isyar M , Yilmaz I , Sirin D Y , et al . A practical way to prepare primer human chondrocyte culture[J]. Journal of Orthopaedics, 2016, 13(3): 162-167.
92	Olsen J V , Ong S E , Mann M . Trypsin cleaves exclusively C-terminal to arginine and lysine residues[J]. Molecular & Cellular Proteomics, 2004, 3(6): 608-614.
93	Song Y , Tian K , Mi W , et al . Combinatorial enzymatic digestion with thermolysin and collagenase type Ⅰ improved the isolation and culture effects of hair cell progenitors from rat cochleae[J]. In Vitro Cellular & Developmental Biology-Animal, 2016, 52(5): 537-544.
94	Kin T , Johnson P R V , Shapiro A M J , et al . Factors influencing the collagenase digestion phase of human islet isolation[J]. Transplantation, 2007, 83(1): 7-12.
95	Loganathan G , Subhashree V , Narayanan S , et al . Improved recovery of human islets from young donor pancreases utilizing increased protease dose to collagenase for digesting peri‐islet extracellular matrix[J]. American Journal of Transplantation, 2019, 19: 831-843.
96	Berková Z , Saudek F , Leontovyč I , et al . Testing of a new collagenase blend for pancreatic islet isolation produced by Clostridium histolyticum [J]. Advances in Bioscience and Biotechnology, 2018, 9(1): 26.

[1]	Lingding MENG, Ruqing CHONG, Feixue SUN, Zihui MENG, Wenfang LIU. Immobilization of carbonic anhydrase on modified polyethylene membrane and silica [J]. CIESC Journal, 2023, 74(8): 3472-3484.
[2]	Yan GAO, Peng WU, Chao SHANG, Zejun HU, Xiaodong CHEN. Preparation of magnetic agarose microspheres based on a two-fluid nozzle and their protein adsorption properties [J]. CIESC Journal, 2023, 74(8): 3457-3471.
[3]	Yaxin CHEN, Hang YUAN, Guanzhang LIU, Lei MAO, Chun YANG, Ruifang ZHANG, Guangya ZHANG. Advances in enzyme self-immobilization mediated by protein nanocages [J]. CIESC Journal, 2023, 74(7): 2773-2782.
[4]	Xiaoling TANG, Jiarui WANG, Xuanye ZHU, Renchao ZHENG. Biosynthesis of chiral epichlorohydrin by halohydrin dehalogenase based on Pickering emulsion system [J]. CIESC Journal, 2023, 74(7): 2926-2934.
[5]	Lei MAO, Guanzhang LIU, Hang YUAN, Guangya ZHANG. Efficient preparation of carbon anhydrase nanoparticles capable of capturing CO₂ and their characteristics [J]. CIESC Journal, 2023, 74(6): 2589-2598.
[6]	Wenqi HOU, Yan SUN, Xiaoyan DONG. Basification modification of transthyretin significantly enhances inhibitory effect on amyloid-β protein aggregation [J]. CIESC Journal, 2023, 74(5): 2100-2110.
[7]	Lanhe ZHANG, Qingyi LAI, Tiezheng WANG, Xiaozhuo GUAN, Mingshuang ZHANG, Xin CHENG, Xiaohui XU, Yanping JIA. Effect of H₂O₂ on nitrogen removal and sludge properties in SBR [J]. CIESC Journal, 2023, 74(5): 2186-2196.
[8]	Lufan JIA, Yiying WANG, Yuman DONG, Qinyuan LI, Xin XIE, Hao YUAN, Tao MENG. Aqueous two-phase system based adherent droplet microfluidics for enhanced enzymatic reaction [J]. CIESC Journal, 2023, 74(3): 1239-1246.
[9]	Qiuhua ZHANG, Manlu LIU, Zheng WANG, Yiming ZHANG, Haijia SU. Biosynthesis of vitamin K2 and functional analysis of the biosynthetic enzymes involved in its menadione moiety [J]. CIESC Journal, 2023, 74(1): 342-354.
[10]	Yang HU, Yan SUN. Self-propulsion of enzyme and enzyme-induced micro-/nanomotor [J]. CIESC Journal, 2023, 74(1): 116-132.
[11]	Zhuotao TAN, Siyu QI, Mengjiao XU, Jie DAI, Chenjie ZHU, Hanjie YING. Application of the redox cascade systems with coenzyme self-cycling in biocatalytic processes: opportunities and challenges [J]. CIESC Journal, 2023, 74(1): 45-59.
[12]	Shaojie AN, Hongfeng XU, Si LI, Yuanhang XU, Jiaxi LI. Construction of pH sensitive artificial glutathione peroxidase based on the formation and dissociation of molecular machine [J]. CIESC Journal, 2022, 73(8): 3669-3678.
[13]	Xinzhe ZHANG, Wentao SUN, Bo LYU, Chun LI. Oxidative modification of plant natural products and microbial manufacturing [J]. CIESC Journal, 2022, 73(7): 2790-2805.
[14]	Wei LIU, Yan SUN. Research progress on amyloid β-protein aggregation and its regulation [J]. CIESC Journal, 2022, 73(6): 2381-2396.
[15]	Yinlong XU, Wenchieh CHENG, Lin WANG, Zhongfei XUE, Yixin XIE. Implication and enhancement mechanism of chitosan-assisted enzyme- induced carbonate precipitation for copper wastewater treatment [J]. CIESC Journal, 2022, 73(5): 2222-2232.