Research Progress in Chondroitinase

XIAO Mengyuan; WU Ruiyun; LI Pinglan

doi:10.13386/j.issn1002-0306.2021070372

Volume 43 Issue 15

Jul. 2022

Turn off MathJax

Article Contents

Abstract

References

Science and Technology of Food Industry > 2022 > 43(15): 409-417. > DOI: 10.13386/j.issn1002-0306.2021070372

XIAO Mengyuan, WU Ruiyun, LI Pinglan. Research Progress in Chondroitinase[J]. Science and Technology of Food Industry, 2022, 43(15): 409−417. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2021070372.

Citation:

PDF (6202 KB)

Research Progress in Chondroitinase

Key Laboratory of Precision Nutrition and Food Quality, Key Laboratory of Functional Dairy, Ministry of Education, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China

More Information

Received Date: August 01, 2021
Available Online: May 24, 2022

Graphical Abstract

Abstract

Abstract

Chondroitin sulfate (CS) is a negatively charged linear macromolecule polysaccharide interlaced with glucuronic acid and acetylgalactosamine. It has a variety of physiological activities, including repair of articular cartilage, antioxidant, lipid-lowering, anticoagulant, antithrombotic and antitumor, etc. However, the high molecular weight of CS restricts its effective use of many functions. Chondroitinase (Chase), as a type of lyase that degrades CS, can cleave CS to low-molecular-weight CS, which effectively overcomes the shortcomings of low bioavailability. Based on the author’s work, this article briefly introduces the biological activities of CS and low-molecular-weight CS, expounds on the catalytic mechanism of Chase cracking CS, systematically sorts out the types and sources of Chase, fermentation production and characterization, as well as research progress in recombinant expression and application, view intending to deeply understand the research status and development trend of low molecular weight CS and Chase, and promote the industrial production of Chase.
- low-molecular-weight chondroitin sulfate,
- chondroitinase,
- recombinant expression,
- application

FullText(HTML)

References (65)

References

[1]	MARTEL P J, FARRAN A, MONTELL E, et al. Discrepancies in composition and biological effects of different formulations of chondroitin sulfate[J]. Molecules,2015,20(3):4277−4289. doi: 10.3390/molecules20034277
[2]	XU X Q, XUE C H, CHANG Y G, et al. Conformational and physicochemical properties of fucosylated chondroitin sulfate from sea cucumber Apostichopus japonicus[J]. Carbohydrate Polymers,2016,152:26−32. doi: 10.1016/j.carbpol.2016.06.061
[3]	NOVOA C R, PEREZ M R, BLANCO M, et al. By-products of Scyliorhinus canicula, Prionace glauca and Raja clavata: A valuable source of predominantly 6S sulfated chondroitin sulfate[J]. Carbohydrate Polymers,2017,157:31−37. doi: 10.1016/j.carbpol.2016.09.050
[4]	XIAO Y L, LI P L, CHENG Y N, et al. Effect of α-linolenic acid-modified low molecular weight chondroitin sulfate on atherosclerosis in apoE-deficient mice[J]. Biochimica et Biophysica Acta,2016,1860(11):2589−2597. doi: 10.1016/j.bbagen.2016.07.032
[5]	MUIR E, DE W F, VERHAAGEN J, et al. Recent advances in the therapeutic uses of chondroitinase ABC[J]. Experimental Neurology, 2019, 321(UNSP 113032).
[6]	SMITH P D, COULSON-THOMAS V J, FOSCARIN S, et al. "GAG-ing with the neuron": The role of glycosaminoglycan patterning in the central nervous system[J]. Experimental Neurology,2015,274(B):100−114.
[7]	PAL D, SAHA S. Chondroitin: A natural biomarker with immense biomedical applications[J]. RSC Advances,2019,9(48):28061−28077. doi: 10.1039/C9RA05546K
[8]	ABDALLAH M M, FERNÁNDEZ N, MATIAS A A, et al. Hyaluronic acid and chondroitin sulfate from marine and terrestrial sources: Extraction and purification methods[J]. Carbohydrate Polymers, 2020, 243:116441.
[9]	LAN R, LI Y, SHEN R, et al. Preparation of low-molecular-weight chondroitin sulfates by complex enzyme hydrolysis and their antioxidant activities[J]. Carbohydrate Polymers,2020,241:116302.
[10]	IGARASHI N, TAKEGUCHI A, SAKAI S, et al. Effect of molecular sizes of chondroitin sulfate on interaction with L-selectin[J]. International Journal of Carbohydrate Chemistry,2013:856142−856149.
[11]	JI Y, ZHANG S L, QIAO M, et al. Synthesis of structurally defined chondroitin sulfate: Paving the way to the structure-activity relationship studies[J]. Carbohydrate Polymers,2020,248:116796−116796.
[12]	WANG H N, BETTI M. Sulfated glycosaminoglycan-derived oligosaccharides produced from chicken connective tissue promote iron uptake in a human intestinal Caco-2 cell line[J]. Food Chemistry,2017,220:460−469. doi: 10.1016/j.foodchem.2016.10.025
[13]	LI W, KOBAYASHI T, MOROI S, et al. Anti-obesity effects of chondroitin sulfate oligosaccharides from the skate Raja pulchra[J]. Carbohydrate Polymers,2019,214:303−310. doi: 10.1016/j.carbpol.2019.03.025
[14]	LINHARDT R J, AVCI F Y, TOIDA T, et al. CS lyases: Structure, activity, and applications in analysis and the treatment of diseases[M]//Volpi N. Advances in Pharmacology, 2006: 187−215.
[15]	MICHAUD P, DA COSTA A, COURTOIS B, et al. Polysaccharide lyases: Recent developments as biotechnological tools[J]. Critical Reviews in Biotechnology,2003,23(4):233−266. doi: 10.1080/07388550390447043
[16]	王文爽, 许莹莹, 石立冉, 等. 海洋来源硫酸软骨素降解酶的研究进展[J]. 生命科学,2019,31(9):894−901. [WANG W S, XU Y Y, SHI L R, et al. Research progress in chondroitinase from marine bacteria[J]. Chinese Bulletin of Life Sciences,2019,31(9):894−901. WANG W S, XU Y Y, SHI L R, et al. Research progress in chondroitinase from marine bacteria[J]. Chinese Bulletin of Life Sciences, 2019, 31(9): 894-901.
[17]	LUNIN V V, LI Y G, LINHARDT R J, et al. High-resolution crystal structure of Arthrobacter aurescens chondroitin AC lyase: An enzyme-substrate complex defines the catalytic mechanism[J]. Journal of Molecular Biology,2004,337(2):367−386. doi: 10.1016/j.jmb.2003.12.071
[18]	PRABHAKAR V, CAPILA I, SOUNDARARAJAN V, et al. Recombinant expression, purification, and biochemical characterization of chondroitinase ABC Ⅱ from Proteus vulgaris[J]. Journal of Biological Chemistry,2009,284(2):974−982. doi: 10.1074/jbc.M806630200
[19]	YAMAGATA T, SAITO H, HABUCHI O, et al. Purification and properties of bacterial chondroitinases and chondrosulfatases[J]. Journal of Biological Chemistry,1968,243(7):1523. doi: 10.1016/S0021-9258(18)93574-X
[20]	MAKAREM E H, BERK R S. Partial purification and characterization of chondroitinase from Proteus mirabilis[J]. Journal of Infectious Diseases,1968,118(4):427. doi: 10.1093/infdis/118.4.427
[21]	LINN S, CHAN T, LIPESKI L, et al. Isolation and characterization of 2 chondroitin lyases from Bacteroides thetaiotaomicron[J]. Journal of Bacteriology,1983,156(2):859−866. doi: 10.1128/jb.156.2.859-866.1983
[22]	陶科, 王忠彦, 胡承, 等. 硫酸软骨素裂解酶ABC产生菌的筛选及酶学性质的初步研究[J]. 四川大学学报(自然科学版),2003(6):1168−1171. [TAO K, WANG Z Y, HU C, et al. Isolation and characterization of a novel chondroitinase ABC producing strain[J]. Journal of Sichuan University (Natural Science Edition),2003(6):1168−1171. TAO K, WANG Z Y, HU C, et al. Isolation and characterization of a novel chondroitinase ABC producing strain[J]. Journal of Sichuan University (Natural Science Edition), 2003(6): 1168-1171.
[23]	刘万顺, 付静芸, 常菁, 等. 硫酸软骨素酶高产菌株的筛选、鉴定和发酵培养条件的研究[J]. 中国海洋大学学报(自然科学版),2012,42(11):35−39. [LIU W S, FU J Y, CHANG J, et al. Screening ang identification of two high chondroitinase producing bacterial strains and determination of their fermenting condition[J]. Periodical of Ocean University of China (Natural Science Edition),2012,42(11):35−39. LIU W S, FU J Y, CHANG J, et al. Screening ang identification of two high chondroitinase producing bacterial strains and determination of their fermenting condition[J]. Periodical of Ocean University of China (Natural Science Edition), 2012, 42(11): 35-39.
[24]	WANG W S, CAI X J, HAN N H, et al. Sequencing of chondroitin sulfate oligosaccharides using a novel exolyase from a marine bacterium that degrades hyaluronan and chondroitin sulfate/dermatan sulfate[J]. Biochemical Journal,2017,474(22):3831−3848. doi: 10.1042/BCJ20170591
[25]	张京良, 姜言晖, 朱常亮, 等. 高产胞外硫酸软骨素酶菌株的筛选、鉴定及发酵条件优化[J]. 中国海洋药物,2018,37(3):1−8. [ZHANG J L, JIANG Y H, ZHU C L, et al. Screening, identification and optimization of fermentation conditions of the strain with high-yield extracellular chondroitinase[J]. Chinese Journal of Marine Drugs,2018,37(3):1−8. ZHANG J L, JIANG Y H, ZHU C L, et al. Screening, identification and optimization of fermentation conditions of the strain with high-yield extracellular chondroitinase[J]. Chinese Journal of Marine Drugs, 2018, 37(3): 1-8.
[26]	HUANG W J, LUNIN V V, LI Y G, et al. Crystal structure of proteus vulgaris chondroitin sulfate ABC lyase I at 1.9 Å resolution[J]. Journal of Molecular Biology,2003,328(3):623−634. doi: 10.1016/S0022-2836(03)00345-0
[27]	BENITO-ARENAS R, ZARATE S G, REVUELTA J, et al. Chondroitin sulfate-degrading enzymes as tools for the development of new pharmaceuticals[J]. Catalysts,2019,9(4):322.
[28]	SHAYA D, HAHN B, BJERKAN T M, et al. Composite active site of chondroitin lyase ABC accepting both epimers of uronic acid[J]. Glycobiology,2008,18(3):270−277. doi: 10.1093/glycob/cwn002
[29]	GU K N, LINHARDT R J, LALIBERTE M, et al. Purification, characterization and specificity of chondroitin lyases and glycuronidase from Flavobacterium heparinum[J]. Biochemical Journal,1995,312(2):569−577. doi: 10.1042/bj3120569
[30]	HIYAMA K, OKADA S. Crystallization and some properties of chondroitinase from Arthrobacter aurescens[J]. Journal of Biological Chemistry,1975,250(5):1824−1828. doi: 10.1016/S0021-9258(19)41768-7
[31]	YIN F X, WANG F S, SHENG J Z. Uncovering the catalytic direction of chondroitin AC exolyase from the reducing end towards the non-reducing end[J]. Journal of Biological Chemistry,2016,291(9):4399−4406. doi: 10.1074/jbc.C115.708396
[32]	KITAMIKADO M, LEE Y Z. Chondroitinase-producing bacteria in natural habitats[J]. Applied Microbiology,1975,29(3):414−421. doi: 10.1128/am.29.3.414-421.1975
[33]	HONG S W, KIM B T, SHIN H Y, et al. Purification and characterization of novel chondroitin ABC and AC lyases from Bacteroides stercoris HJ-15, a human intestinal anaerobic bacterium[J]. European Journal of Biochemistry,2002,269(12):2934−2940. doi: 10.1046/j.1432-1033.2002.02967.x
[34]	阎浩林, 何汉洲, 蔡苏兰, 等. 硫酸软骨素酶产生菌的筛选及酶的分离纯化[J]. 微生物学报,2004(1):79−82. [YAN H L, HE H Z, CAI S L, et al. Screening and purification of chondroitinase from chondroitinase-producing strains[J]. Acta Microbiologica Sinica,2004(1):79−82. doi: 10.3321/j.issn:0001-6209.2004.01.017 YAN H L, HE H Z, CAI S L, et al. Screening and purification of chondroitinase from chondroitinase-producing strains[J]. Acta Microbiologica Sinica, 2004(1): 79-82. doi: 10.3321/j.issn:0001-6209.2004.01.017
[35]	TAO K, LONG Z F, GAO Q, et al. Isolation of Serratia marcescens as a chondroitinase-producing bacterium and purification of a novel chondroitinase AC[J]. Biotechnology Letters,2005,27(7):489−493. doi: 10.1007/s10529-005-2538-7
[36]	KALE V, FRIDJONSSON O, JONSSON J O, et al. Chondroitin lyase from a marine Arthrobacter sp. MAT3885 for the production of chondroitin sulfate disaccharides[J]. Marine Biotechnology,2015,17(4):479−492. doi: 10.1007/s10126-015-9629-9
[37]	FANG Y T, YANG S X, FU X D, et al. Expression, purification and characterization of chondroitinase AC Ⅱ from marine bacterium Arthrobacter sp. CS01[J]. Marine Drugs,2019,17(3):185.
[38]	HUANG W J, BOJU L, TKALEC L, et al. Active site of chondroitin AC lyase revealed by the structure of enzyme-oligosaccharide complexes and mutagenesis[J]. Biochemistry,2001,40(8):2359−2372. doi: 10.1021/bi0024254
[39]	蔡苏兰, 阎浩林, 何汉洲. 微生物硫酸软骨素裂解酶的研究进展[J]. 沈阳药科大学学报,2004(1):76−80. [CAI S L, HAN H L, HE H Z, et al. Advances of the study on chondroitinases produced by microorganisms[J]. Journal of Shenyang Pharmaceutical University,2004(1):76−80. doi: 10.3969/j.issn.1006-2858.2004.01.022 CAI S L, HAN H L, HE H Z, et al. Advances of the study on chondroitinases produced by microorganisms[J]. Journal of Shenyang Pharmaceutical University, 2004(1): 76-80. doi: 10.3969/j.issn.1006-2858.2004.01.022
[40]	MICHEL G, POJASEK K, LI Y G, et al. The structure of chondroitin B lyase complexed with glycosaminoglycan oligosaccharides unravels a calcium-dependent catalytic machinery[J]. Journal of Biological Chemistry,2004,279(31):32882−32896. doi: 10.1074/jbc.M403421200
[41]	HUANG W J, MATTE A, LI Y G, et al. Crystal structure of chondroitinase B from Flavobacterium heparinum and its complex with a disaccharide product at 1.7 angstrom resolution[J]. Journal of Molecular Biology,1999,294(5):1257−1269. doi: 10.1006/jmbi.1999.3292
[42]	FU J Y, JIANG Z W, CHANG J, et al. Purification, characterization of chondroitinase ABC from Sphingomonas paucimobilis and in vitro cardiocytoprotection of the enzymatically degraded CS-A[J]. International Journal of Biological Macromolecules,2018,115:737−745. doi: 10.1016/j.ijbiomac.2018.04.117
[43]	ZHU C L, ZHANG J L, ZHANG J, et al. Purification and characterization of chondroitinase ABC from Acinetobacter sp C26[J]. International Journal of Biological Macromolecules,2017,95:80−86. doi: 10.1016/j.ijbiomac.2016.10.044
[44]	郭云瑕. 硫酸软骨素酶的发酵生产、性质研究及高活性酶解产物的制备[D]. 青岛: 青岛农业大学, 2017: 22−26 GUO Y X. Fermentation production, characterization of chondroitin sulfate and preparation of highly active enzymatic hydrolysate[D]. Qingdao: Qingdao Agricultural University, 2017: 22−26.
[45]	ABDUL-GANI M N, LAFTAAH B A. Purification and characterization of chondroitinase ABC from Proteus vulgaris, an iraqi clinically isolate[J]. Current Science,2017,113(11):2134−2140. doi: 10.18520/cs/v113/i11/2134-2140
[46]	POJASEK K, SHRIVER Z, KILEY P, et al. Recombinant expression, purification, and kinetic characterization of chondroitinase AC and chondroitinase B from Flavobacterium heparinum[J]. Biochemical and Biophysical Research Communications,2001,286(2):343−351. doi: 10.1006/bbrc.2001.5380
[47]	黄浩, 王阳, 堵国成, 等. 重组蛋白微生物表达系统的研究进展[J]. 生物产业技术,2019(3):36−43. [HUANG H, WANG Y, ZHU G C, et al. Research progress in microbial expression systems for recombinant protein production[J]. Biotechnology & Business,2019(3):36−43. HUANG H, WANG Y, ZHU G C, et al. Research progress in microbial expression systems for recombinant protein production[J]. Biotechnology & Business, 2019(3): 36-43.
[48]	曹蕾, 唐晓峰. 提高大肠杆菌表达外源蛋白胞外含量的策略[J]. 生物资源,2020,42(4):375−381. [CAO L, TANG X F. Strategies for increasing extracellular content of heterologous protein in Escherichia coli[J]. Biotic Resources,2020,42(4):375−381. CAO L, TANG X F. Strategies for increasing extracellular content of heterologous protein in Escherichia coli[J]. Biotic Resources, 2020, 42(4): 375-381.
[49]	LU X Y, ZHONG Q, LIU J, et al. Efficient expression of chondroitinase ABC I for specific disaccharides detection of chondroitin sulfate[J]. International Journal of Biological Macromolecules,2020,143:41−48. doi: 10.1016/j.ijbiomac.2019.11.215
[50]	WANG H, ZHANG L, ZHANG W J, et al. Secretory expression of biologically active chondroitinase ABC I for production of chondroitin sulfate oligosaccharides[J]. Carbohydrate Polymers, 2019, 224(UNSP 115135).
[51]	FANG Y T, FU X D, XIE W C, et al. Expression, purification and characterisation of chondroitinase AC II with glyceraldehyde-3-phosphate dehydrogenase tag and chaperone (GroEs-GroEL) from Arthrobacter sp. CS01[J]. International Journal of Biological Macromolecules,2019,129:471−476. doi: 10.1016/j.ijbiomac.2019.02.056
[52]	LI Y, ZHOU Z, CHEN Z Y. High-level production of ChSase ABC I by co-expressing molecular chaperones in Escherichia coli[J]. International Journal of Biological Macromolecules,2018,119:779−784. doi: 10.1016/j.ijbiomac.2018.08.009
[53]	CHEN Z Y, LI Y, YUAN Q P. Expression, purification and thermostability of MBP-chondroitinase ABC I from Proteus vulgaris[J]. International Journal of Biological Macromolecules,2015,72:6−10. doi: 10.1016/j.ijbiomac.2014.07.040
[54]	李晔, 陈振娅, 袁其朋. 硫酸软骨素裂解酶 ABC 的研究进展[J]. 生物工程学报,2015,31(5):621−633. [LI Y, CHEN Z Y, YUAN Q P. Research progress in chondroitinase ABC[J]. Chinese Journal of Biotechnology,2015,31(5):621−633. LI Y, CHEN Z Y, YUAN Q P. Research progress in chondroitinase ABC[J]. Chinese Journal of Biotechnology, 2015, 31(5): 621-633.
[55]	VALCARCEL J, GARCIA M R, SAMPAYO L F, et al. Marine chondroitin sulfate of defined molecular weight by enzymatic depolymerization[J]. Carbohydrate Polymers,2020,229:115450. doi: 10.1016/j.carbpol.2019.115450
[56]	鲍伦军, 杨建成, 何振华, 等. 鱼翅中硫酸软骨素的酶解-高效液相色谱法测定[J]. 分析测试学报,2002,21(5):59−61. [BAO L J, YANG J C, HE Z H, et al. Determination of chondroitin sulfate in shark’s fins by enzymolysis-HPLC[J]. Journal of Instrumental Analysis,2002,21(5):59−61. doi: 10.3969/j.issn.1004-4957.2002.05.018 BAO L J, YANG J C, HE Z H, et al. Determination of chondroitin sulfate in shark’s fins by enzymolysis-HPLC[J]. Journal of Instrumental Analysis, 2002, 21(5): 59-61. doi: 10.3969/j.issn.1004-4957.2002.05.018
[57]	KASINATHAN N, VOLETY S M, JOSYULA V R. Chondroitinase: A promising therapeutic enzyme[J]. Critical Reviews in Microbiology,2016,42(3):474−484.
[58]	ROSENZWEIG E S, SALEGIO E A, LIANG J J, et al. Chondroitinase improves anatomical and functional outcomes after primate spinal cord injury[J]. Nature Neuroscience,2019,22(8):1269. doi: 10.1038/s41593-019-0424-1
[59]	中华医学会放射学分会介入学组. 腰椎间盘突出症的介入和微创治疗操作规范的专家共识[J]. 中华放射学杂志,2014,48(1):10−12. [Intervention Group of Chinese Medical Association Radiology Branch. Expert consensus on interventional and minimally invasive treatment of lumbar disc herniation[J]. Chinese Journal of Radiology,2014,48(1):10−12. doi: 10.3760/cma.j.issn.1005-1201.2014.01.004 Intervention Group of Chinese Medical Association Radiology Branch. Expert consensus on interventional and minimally invasive treatment of lumbar disc herniation[J]. Chinese Journal of Radiology, 2014, 48(1): 10-12. doi: 10.3760/cma.j.issn.1005-1201.2014.01.004
[60]	郑历明, 刘增品, 汪国石, 等. 化学髓核溶解术的新进展[J]. 实用放射学杂志,2001,17(4):303−304. [ZHENG L M, LIU Z P, WANG G S, et al. Development of the chemonucleolysis[J]. Journal of Practical Radiology,2001,17(4):303−304. doi: 10.3969/j.issn.1002-1671.2001.04.024 ZHENG L M, LIU Z P, WANG G S, et al. Development of the chemonucleolysis[J]. Journal of Practical Radiology, 2001, 17(4): 303-304. doi: 10.3969/j.issn.1002-1671.2001.04.024
[61]	ISHIKO T, NAITOH M, KUBOTA H, et al. Chondroitinase injection improves keloid pathology by reorganizing the extracellular matrix with regenerated elastic fibers[J]. Journal of Dermatology,2013,40(5):380−383. doi: 10.1111/1346-8138.12116
[62]	JAIME R A, BOLYARD C, MEISEN W, et al. Impact of humanized chondroitinase ABC on OV therapy for intracranial tumors[J]. Neuro-Oncology,2014:165.
[63]	PIZZORUSSO T, MEDINI P, BERARDI N, et al. Reactivation of ocular dominance plasticity in the adult visual cortex[J]. Science,2002,298(5596):1248−1251. doi: 10.1126/science.1072699
[64]	PIZZORUSSO T, MEDINI P, LANDI S, et al. Structural and functional recovery from early monocular deprivation in adult rats[J]. Proceedings of the National Academy of Sciences of the United States of America,2006,103(22):8517−8522. doi: 10.1073/pnas.0602657103
[65]	付静芸. 产硫酸软骨素酶菌株的筛选、发酵、酶的分离纯化及性质的研究[D]. 青岛: 中国海洋大学, 2012 FU J Y. Study on the screening, fermentation of ChSase-producing strains, and purification and properties of the ChSase abstract[D]. Qingdao: Ocean University of China, 2012.