GH79家族糖苷水解酶分子进化关系和蛋白结构研究

doi:10.13560/j.cnki.biotech.bull.1985.2022-0417

摘要/Abstract

摘要：

GH79家族的糖苷水解酶在碳水化合物改性、细胞免疫识别和信号传导等方面具有广泛的生理活性和重要的应用前景。然而，目前GH79家族的多样性催化机理仍不清楚，识别底物的结构基础和分子机制尚不清晰。本文总结了近几年GH79家族的研究进展，系统分析了GH79家族酶的来源与分布，通过对酶的序列特征、分子进化关系、蛋白结构解析等方面进行深入阐述，旨在为后续的GH79家族的蛋白质工程和功能催化机制的解析奠定基础。

关键词: GH79家族, 催化机理, 分子进化, 结构解析

Abstract:

The glycoside hydrolases of the GH79 family have extensive physiological activities and important application prospects in carbohydrate modification, cellular immune recognition and signal transduction. However, the diverse catalysis mechanism of GH79 family remains unclear, and the structural basis and molecular mechanism of substrate recognition are still unclear. This review summarizes the research progress of the GH79 family, systematically analyzes the origin and distribution of GH79 family enzymes, and deeply expounds their sequence features, molecular evolutionary relationships, and the crystal structures analysis, aiming to lay a foundation for protein engineering and functional metabolic mechanism of GH79 family.

Key words: GH family 79, catalytic mechanism, molecular evolution, structural analysis

陈泉冰, 曹伟洁, 李春, 吕波. GH79家族糖苷水解酶分子进化关系和蛋白结构研究[J]. 生物技术通报, 2023, 39(1): 104-114.

CHEN Quan-bing, CAO Wei-jie, LI Chun, LV Bo. Molecular Evolutionary Relationship and Protein Structure of Glycoside Hydrolases from GH79 Family[J]. Biotechnology Bulletin, 2023, 39(1): 104-114.

图/表 8

参考文献 56

[1]	OKUYAMA M. Function and structure studies of GH family 31 and 97 α-glycosidases[J]. Biosci Biotechnol Biochem, 2011, 75(12): 2269-2277. doi: 10.1271/bbb.110610 URL
[2]	Larrucea S, Butta N, Arias-Salgado EG, et al. Expression of podocalyxin enhances the adherence, migration, and intercellular communication of cells[J]. Exp Cell Res, 2008, 314(10): 2004-2015. doi: 10.1016/j.yexcr.2008.03.009 pmid: 18456258
[3]	Singh RS, Singh RP, Kennedy JF. Recent insights in enzymatic synthesis of fructooligosaccharides from inulin[J]. Int J Biol Macromol, 2016, 85:565-572. doi: 10.1016/j.ijbiomac.2016.01.026 pmid: 26791586
[4]	Guo LC, Katiyo W, Lu LS, et al. Glycyrrhetic acid 3-O-mono-β-d-glucuronide(GAMG):an innovative high-potency sweetener with improved biological activities[J]. Compr Rev Food Sci Food Saf, 2018, 17(4): 905-919. doi: 10.1111/1541-4337.12353 URL
[5]	Lu DQ, Zhang SM, Wang J, et al. Adsorption separation of 3 beta-D-monoglucuronyl-18 beta-glycyrrhetinic acid from directional biotransformation products of glycyrrhizin[J]. African J Biotechnol, 2008, 7(22): 3995-4003.
[6]	Tang WJ, Yang YA, Xu H, et al. Synthesis and discovery of 18α-GAMG as anticancer agent in vitro and in vivo via down expression of protein p65[J]. Sci Rep, 2014, 4:7106. doi: 10.1038/srep07106 URL
[7]	Mitsudome T, Xu J, Nagata Y, et al. Expression, purification, and characterization of endo-β-N-acetylglucosaminidase H using baculovirus-mediated silkworm protein expression system[J]. Appl Biochem Biotechnol, 2014, 172(8): 3978-3988. doi: 10.1007/s12010-014-0814-5 pmid: 24599668
[8]	Komba S, Ito Y. Β-galactosidase-catalyzed intramolecular transglycosylation[J]. Tetrahedron Lett, 2001, 42(48): 8501-8505. doi: 10.1016/S0040-4039(01)01826-3 URL
[9]	Davies GJ, Williams SJ. Carbohydrate-active enzymes:sequences, shapes, contortions and cells[J]. Biochem Soc Trans, 2016, 44(1): 79-87. doi: 10.1042/BST20150186 URL
[10]	Niers TMH, Klerk CPW, DiNisio M, et al. Mechanisms of heparin induced anti-cancer activity in experimental cancer models[J]. Crit Rev Oncol Hematol, 2007, 61(3): 195-207. doi: 10.1016/j.critrevonc.2006.07.007 URL
[11]	Hamre AG, Strømnes AGS, Gustavsen D, et al. Treatment of recalcitrant crystalline polysaccharides with lytic polysaccharide monooxygenase relieves the need for glycoside hydrolase processivity[J]. Carbohydr Res, 2019, 473:66-71. doi: 10.1016/j.carres.2019.01.001 URL
[12]	Saito A, Wakao M, Deguchi H, et al. Towards the assembly of heparin and heparan sulfate oligosaccharide libraries:efficient synthesis of uronic acid and disaccharide building blocks[J]. Tetrahedron, 2010, 66(22): 3951-3962. doi: 10.1016/j.tet.2010.03.077 URL
[13]	Michikawa M, Ichinose H, Momma M, et al. Structural and biochemical characterization of glycoside hydrolase family 79 β-glucuronidase from Acidobacterium capsulatum[J]. J Biol Chem, 2012, 287(17): 14069-14077. doi: 10.1074/jbc.M112.346288 pmid: 22367201
[14]	Bohlmann L, Tredwell GD, Yu X, et al. Functional and structural characterization of a heparanase[J]. Nat Chem Biol, 2015, 11(12): 955-957. doi: 10.1038/nchembio.1956 pmid: 26565989
[15]	Konishi T, Kotake T, Soraya D, et al. Properties of family 79 beta-glucuronidases that hydrolyze beta-glucuronosyl and 4-O-methyl-beta-glucuronosyl residues of arabinogalactan-protein[J]. Carbohydr Res, 2008, 343(7): 1191-1201. doi: 10.1016/j.carres.2008.03.004 URL
[16]	Eudes A, Mouille G, Thévenin J, et al. Purification, cloning and functional characterization of an endogenous beta-glucuronidase in Arabidopsis thaliana[J]. Plant Cell Physiol, 2008, 49(9): 1331-1341. doi: 10.1093/pcp/pcn108 URL
[17]	Hulett MD, Freeman C, Hamdorf BJ, et al. Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis[J]. Nat Med, 1999, 5(7): 803-809. doi: 10.1038/10525 pmid: 10395326
[18]	Podyma-Inoue KA, Yokote H, Sakaguchi K, et al. Characterization of heparanase from a rat parathyroid cell line[J]. J Biol Chem, 2002, 277(36): 32459-32465. doi: 10.1074/jbc.M203282200 pmid: 12077130
[19]	Toyoshima M, Nakajima M. Human heparanase. purification, characterization, cloning, and expression[J]. J Biol Chem, 1999, 274(34): 24153-24160. doi: 10.1074/jbc.274.34.24153 pmid: 10446189
[20]	Masola V, Bellin G, Gambaro G, et al. Heparanase:a multitasking protein involved in extracellular matrix(ECM)remodeling and intracellular events[J]. Cells, 2018, 7(12): 236. doi: 10.3390/cells7120236 URL
[21]	Kondo T, Kichijo M, Nakaya M, et al. Biochemical and structural characterization of a novel 4-O-α-l-rhamnosyl-β-d-glucuronidase from Fusarium oxysporum[J]. FEBS J, 2021, 288(16): 4918-4938. doi: 10.1111/febs.15795 URL
[22]	Wei KH, Liu IH. Heparan sulfate glycosaminoglycans modulate migration and survival in zebrafish primordial germ cells[J]. Theriogenology, 2014, 81(9): 1275-1285. e1-2. doi: 10.1016/j.theriogenology.2014.02.009 URL
[23]	Goldshmidt O, Zcharia E, Aingorn H, et al. Expression pattern and secretion of human and chicken heparanase are determined by their signal peptide sequence[J]. J Biol Chem, 2001, 276(31): 29178-29187. doi: 10.1074/jbc.M102462200 pmid: 11387326
[24]	Strausberg RL, Feingold EA, Grouse LH, et al. Generation and initial analysis of more than 15, 000 full-length human and mouse cDNA sequences[J]. Proc Natl Acad Sci USA, 2002, 99(26): 16899-16903. doi: 10.1073/pnas.242603899 pmid: 12477932
[25]	Miles JR, Vallet JL, Freking BA, et al. Molecular cloning and characterisation of heparanase mRNA in the porcine placenta throughout gestation[J]. Reprod Fertil Dev, 2009, 21(6): 757-772. doi: 10.1071/RD09041 URL
[26]	Jin P, Kang Z, Zhang N, et al. High-yield novel leech hyaluronidase to expedite the preparation of specific hyaluronan oligomers[J]. Sci Rep, 2014, 4:4471. doi: 10.1038/srep04471 pmid: 24667183
[27]	Huang H, Hou XD, Xu RR, et al. Structure and cleavage pattern of a hyaluronate 3-glycanohydrolase in the glycoside hydrolase 79 family[J]. Carbohydr Polym, 2022, 277:118838.
[28]	Sasaki K, Taura F, Shoyama Y, et al. Molecular characterization of a novel beta-glucuronidase from Scutellaria baicalensis Georgi[J]. J Biol Chem, 2000, 275(35): 27466-27472. doi: 10.1074/jbc.M004674200 pmid: 10858442
[29]	Xu YH, Feng XD, Jia JT, et al. A novel β-glucuronidase from Talaromyces pinophilus Li-93 precisely hydrolyzes glycyrrhizin into glycyrrhetinic acid 3- O-mono-β- d-glucuronide[J]. Appl Environ Microbiol, 2018, 84(19): e00755-18.
[30]	Sánchez-Pérez R, Pavan S, Mazzeo R, et al. Mutation of a bHLH transcription factor allowed almond domestication[J]. Science, 2019, 364(6445): 1095-1098. doi: 10.1126/science.aav8197 pmid: 31197015
[31]	Hambruch N, Kumstel S, Haeger JD, et al. Bovine placentomal heparanase and syndecan expression is related to placental maturation[J]. Placenta, 2017, 57:42-51. doi: S0143-4004(17)30290-4 pmid: 28864018
[32]	Li WC, Lin TC, Chen CL, et al. Complete genome sequences and genome-wide characterization of Trichoderma biocontrol agents provide new insights into their evolution and variation in genome organization, sexual development, and fungal-plant interactions[J]. Microbiol Spectr, 2021, 9(3): e0066321.
[33]	Wu L, Jiang JB, Jin Y, et al. Activity-based probes for functional interrogation of retaining β-glucuronidases[J]. Nat Chem Biol, 2017, 13(8): 867-873. doi: 10.1038/nchembio.2395 pmid: 28581485
[34]	Li QF, Jiang T, Liu R, et al. Tuning the pH profile of β-glucuronidase by rational site-directed mutagenesis for efficient transformation of glycyrrhizin[J]. Appl Microbiol Biotechnol, 2019, 103(12): 4813-4823. doi: 10.1007/s00253-019-09790-3 pmid: 31055652
[35]	Vlodavsky I, Ilan N, Naggi A, et al. Heparanase:structure, biological functions, and inhibition by heparin-derived mimetics of heparan sulfate[J]. Curr Pharm Des, 2007, 13(20): 2057-2073. doi: 10.2174/138161207781039742 URL
[36]	Wang F, Wan A, Rodrigues B. The function of heparanase in diabetes and its complications[J]. Can J Diabetes, 2013, 37(5): 332-338. doi: 10.1016/j.jcjd.2013.05.008 pmid: 24500561
[37]	Kuroyama H, Tsutsui N, Hashimoto Y, et al. Purification and characterization of a beta-glucuronidase from Aspergillus niger[J]. Carbohydr Res, 2001, 333(1): 27-39. doi: 10.1016/S0008-6215(01)00114-8 URL
[38]	Harty DWS, Mayo JA, Cook SL, et al. Environmental regulation of glycosidase and peptidase production by Streptococcus gordonii FSS2[J]. Microbiology(Reading), 2000, 146(Pt 8): 1923-1931.
[39]	Imaki H, Tomoyasu T, Yamamoto N, et al. Identification and characterization of a novel secreted glycosidase with multiple glycosidase activities in Streptococcus intermedius[J]. J Bacteriol, 2014, 196(15): 2817-2826. doi: 10.1128/JB.01727-14 URL
[40]	Tomoyasu T, Yamasaki T, Chiba S, et al. Positive- and negative-control pathways by blood components for intermedilysin production in Streptococcus intermedius[J]. Infect Immun, 2017, 85(9): e00379-e00317.
[41]	Fratianni F, Ombra MN, D'Acierno A, et al. Polyphenols content and in vitro α-glycosidase activity of different Italian monofloral honeys, and their effect on selected pathogenic and probiotic bacteria[J]. Microorganisms, 2021, 9(8): 1694. doi: 10.3390/microorganisms9081694 URL
[42]	Weber BA, Klein JR, Henrich B. Expression of the phospho-beta-glycosidase ArbZ from Lactobacillus delbrueckii subsp. lactis in Lactobacillus helveticus:substrate induction and catabolite repression[J]. Microbiology(Reading), 2000, 146(Pt 8): 1941-1948.
[43]	Chang CF, Ho CW, Wu CY, et al. Discovery of picomolar slow tight-binding inhibitors of alpha-fucosidase[J]. Chem Biol, 2004, 11(9): 1301-1306. doi: 10.1016/j.chembiol.2004.07.009 URL
[44]	Liu L, Tharmalingam T, Maischberger E, et al. A HPLC-based glycoanalytical protocol allows the use of natural O-glycans derived from glycoproteins as substrates for glycosidase discovery from microbial culture[J]. Glycoconj J, 2013, 30(8): 791-800. doi: 10.1007/s10719-013-9483-9 URL
[45]	Zhang LW, Qiu HL, Yuan S, et al. Revelation of mechanism for aqueous saponins content decrease during storage of Dioscorea zingiberensis C. H. Wright tubers:an essential prerequisite to ensure clean production of diosgenin[J]. Ind Crops Prod, 2018, 125:178-185. doi: 10.1016/j.indcrop.2018.09.003 URL
[46]	Brooks JF II, Gyllborg MC, Cronin DC, et al. Global discovery of colonization determinants in the squid symbiont Vibrio fischeri[J]. PNAS, 2014, 111(48): 17284-17289. doi: 10.1073/pnas.1415957111 pmid: 25404340
[47]	Zhang BQ, Zhang N, Zhang QQ, et al. Transcriptome profiles of Sporisorium reilianum during the early infection of resistant and susceptible maize isogenic lines[J]. J Fungi(Basel), 2021, 7(2): 150.
[48]	Novakazi F, Göransson M, Stefánsson TS, et al. Virulence of Icelandic Pyrenophora teres f. teres populations and resistance of Icelandic spring barley lines[J]. J Plant Pathol, 2022, 104(1): 205-213. doi: 10.1007/s42161-021-00972-5 URL
[49]	Hall BG. Building phylogenetic trees from molecular data with MEGA[J]. Mol Biol Evol, 2013, 30(5): 1229-1235. doi: 10.1093/molbev/mst012 pmid: 23486614
[50]	Newman L, Duffus ALJ, Lee C. Using the free program MEGA to build phylogenetic trees from molecular data[J]. Am Biol Teach, 2016, 78(7): 608-612. doi: 10.1525/abt.2016.78.7.608 URL
[51]	Vinader V, Haji-Abdullahi MH, Patterson LH, et al. Synthesis of a pseudo-disaccharide library and its application to the characterisation of the heparanase catalytic site[J]. PLoS One, 2013, 8(11): e82111. doi: 10.1371/journal.pone.0082111 URL
[52]	Okuyama M, Yoshida T, Hondoh H, et al. Catalytic role of the calcium ion in GH97 inverting glycoside hydrolase[J]. FEBS Lett, 2014, 588(17): 3213-3217. doi: 10.1016/j.febslet.2014.07.002 pmid: 25017438
[53]	Qin Z, Yang SQ, Zhao LM, et al. Catalytic mechanism of a novel glycoside hydrolase family 16 “elongating” β-transglycosylase[J]. J Biol Chem, 2017, 292(5): 1666-1678. doi: 10.1074/jbc.M116.762419 URL
[54]	Vuong TV, Wilson DB. Glycoside hydrolases:catalytic base/nucleophile diversity[J]. Biotechnol Bioeng, 2010, 107(2): 195-205. doi: 10.1002/bit.22838 pmid: 20552664
[55]	Davies G, Henrissat B. Structures and mechanisms of glycosyl hydrolases[J]. Structure, 1995, 3(9): 853-859. doi: 10.1016/S0969-2126(01)00220-9 pmid: 8535779
[56]	Wu L, Viola CM, Brzozowski AM, et al. Structural characterization of human heparanase reveals insights into substrate recognition[J]. Nat Struct Mol Biol, 2015, 22(12): 1016-1022. doi: 10.1038/nsmb.3136 pmid: 26575439

水解方式 Hydrolysis method	名称 Name	切割位点 Cleavage site
外切型 Exo-type	唾液酸酶	α-2,6糖苷键连接的唾液酸残基
	β-半乳糖苷酶	β-1,4糖苷键连接的半乳糖残基
	α-甘露糖苷酶	α-1,2糖苷键，α-1,3糖苷键，α-1,6糖苷键连接的甘露糖型
	β-甘露糖苷酶	β-1,4糖苷键连接的甘露糖型
	β-淀粉酶	自非还原末端依次切割麦芽糖单位，不切也不逾越α-1,6糖苷键
内切型 Endo-type	α-淀粉酶	在分子内部随机切割α-1,4糖苷键，不切α-1,6糖苷键
	异淀粉酶	水解支链淀粉或糖原中的α-1,6糖苷键
	Endo F	β-1,4糖苷键连接的高甘露糖型杂合糖型
	Endo H	β-1,4糖苷键连接的高甘露糖型杂合糖型
	O-糖苷酶	水解蛋白核心1（Galβ1-3 GalNAC-Thr/Ser）和核心3（GlcNACβ1-3 GalNAC-Thr/Ser）之间的O-连接二糖单位

水解方式 Hydrolysis method	名称 Name	切割位点 Cleavage site
外切型 Exo-type	唾液酸酶	α-2,6糖苷键连接的唾液酸残基
	β-半乳糖苷酶	β-1,4糖苷键连接的半乳糖残基
	α-甘露糖苷酶	α-1,2糖苷键，α-1,3糖苷键，α-1,6糖苷键连接的甘露糖型
	β-甘露糖苷酶	β-1,4糖苷键连接的甘露糖型
	β-淀粉酶	自非还原末端依次切割麦芽糖单位，不切也不逾越α-1,6糖苷键
内切型 Endo-type	α-淀粉酶	在分子内部随机切割α-1,4糖苷键，不切α-1,6糖苷键
	异淀粉酶	水解支链淀粉或糖原中的α-1,6糖苷键
	Endo F	β-1,4糖苷键连接的高甘露糖型杂合糖型
	Endo H	β-1,4糖苷键连接的高甘露糖型杂合糖型
	O-糖苷酶	水解蛋白核心1（Galβ1-3 GalNAC-Thr/Ser）和核心3（GlcNACβ1-3 GalNAC-Thr/Ser）之间的O-连接二糖单位

蛋白名称 Protein name	来源 Organism	底物 Substrate	EC编号 EC#	参考文献 Reference
GlcA79A	Acidobacterium capsulatum	β-D-glucuronicacid	3.2.1.31	[13]
AtGUS2	Arabidopsis thaliana	pNPGlcA	3.2.1.31	[16]
Nc6GAL	Neurospora crassa	Arabinogalactan-proteins	3.2.1.31	[15]
FobglcA	Fusarium oxysporum	Gum arabic	3.2.1.31	[21]
BpHep	Burkholderia pseudomallei	Heparan sulfate	3.2.1.166	[14]
HpsE	Rattus norvegicus	Heparan sulfate	3.2.1.166	[18]
Hpse1	Danio rerio	Heparan sulfate glycosaminoglycans	3.2.1.166	[22]
Hpa1	Homo sapiens	Heparan sulfate	3.2.1.166	[19]
Heparanase	Gallus gallus	Heparan sulfate	3.2.1.166	[23]
Heparanase	Homo sapiens	Heparan sulfate	3.2.1.166	[24]
Heparanase	Sus scrofa	Heparan sulfate	3.2.1.166	[25]
Hpa	Mus musculus	Heparan sulfate	3.2.1.166	[17]
Hyaluronidase	Hirudo nipponia	Hyaluronan	3.2.1.36	[26]
LHyal	Hirudo nipponia	Hyaluronan	3.2.1.36	[27]
SguS	Scutellaria baicalensis	Baicalein-7-O-β-D-glucuronide-conjugated	3.2.1.167	[28]
AnGlcAase	Aspergillus niger	Arabinogalactan-proteins	3.2.1.-	[15]
TpGUS79A	Talaromyces pinophilus Li-93	Glycyrrhizinate	3.2.1.-	[29]
Glucuronidase 1	Prunus dulcis	Almond	3.2.1.-	[30]
Heparanase precursor	Bos taurus	Heparan sulfate	3.2.1.-	[31]
Hypothetical protein TrVGV298_008121	Trichoderma virens	-	3.2.1.-	[32]

蛋白名称 Protein name	来源 Organism	底物 Substrate	EC编号 EC#	参考文献 Reference
GlcA79A	Acidobacterium capsulatum	β-D-glucuronicacid	3.2.1.31	[13]
AtGUS2	Arabidopsis thaliana	pNPGlcA	3.2.1.31	[16]
Nc6GAL	Neurospora crassa	Arabinogalactan-proteins	3.2.1.31	[15]
FobglcA	Fusarium oxysporum	Gum arabic	3.2.1.31	[21]
BpHep	Burkholderia pseudomallei	Heparan sulfate	3.2.1.166	[14]
HpsE	Rattus norvegicus	Heparan sulfate	3.2.1.166	[18]
Hpse1	Danio rerio	Heparan sulfate glycosaminoglycans	3.2.1.166	[22]
Hpa1	Homo sapiens	Heparan sulfate	3.2.1.166	[19]
Heparanase	Gallus gallus	Heparan sulfate	3.2.1.166	[23]
Heparanase	Homo sapiens	Heparan sulfate	3.2.1.166	[24]
Heparanase	Sus scrofa	Heparan sulfate	3.2.1.166	[25]
Hpa	Mus musculus	Heparan sulfate	3.2.1.166	[17]
Hyaluronidase	Hirudo nipponia	Hyaluronan	3.2.1.36	[26]
LHyal	Hirudo nipponia	Hyaluronan	3.2.1.36	[27]
SguS	Scutellaria baicalensis	Baicalein-7-O-β-D-glucuronide-conjugated	3.2.1.167	[28]
AnGlcAase	Aspergillus niger	Arabinogalactan-proteins	3.2.1.-	[15]
TpGUS79A	Talaromyces pinophilus Li-93	Glycyrrhizinate	3.2.1.-	[29]
Glucuronidase 1	Prunus dulcis	Almond	3.2.1.-	[30]
Heparanase precursor	Bos taurus	Heparan sulfate	3.2.1.-	[31]
Hypothetical protein TrVGV298_008121	Trichoderma virens	-	3.2.1.-	[32]