微生物来源的唾液酸转移酶研究进展
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摘要
唾液酸转移酶属糖基转移酶家族,以唾液酸胞苷单磷酸酯(CMP-Neu5Ac)为供体底物,催化唾液酸转移至糖蛋白与糖脂末端,是合成唾液酸化寡糖途径中所必需的酶类。微生物来源的唾液酸转移酶具有较广泛的底物特异性,且容易在常见的原核生物表达系统中过量表达,对酶学特性的研究及丰富唾液酸寡糖种类具有重要意义。本文综述了唾液酸转移酶的分类与微生物来源、晶体结构、催化反应机理、酶学性质、异源表达以及在唾液酸寡糖合成中的应用,并对唾液酸转移酶的未来发展方向进行了展望,以扩展这些酶在糖化学和糖生物学中的应用。
Sialic acid transferase belongs to the family of glycosyl transferase,with cytidyl sialoside phosphate (CMP-Neu5 Ac)as the donor substrate and transferring sialic acid to the ends of glycoproteins and glycolipids.Such enzymes are essential in the synthesis pathways of sialic acid oligosaccharides.Microbial sialyltransferases have broader substrate specificities and are readily overexpressed in common prokaryotic expression systems. It is of great significance for studying enzymatic properties and producing different sialyl oligosaccharides.This review summarized the classification and microbial sources of sialyltransferases,the crystal structure,the mechanism of catalytic reaction,the enzymatic properties,the clone and expression,and their applications in the synthesis of sialylated oligosaccharides.The future study direction of sialyltransferases was also prospected,in order to expand the application of these enzymes in sugar chemistry and sugar biology.
Sialic acid transferase belongs to the family of glycosyl transferase,with cytidyl sialoside phosphate (CMP-Neu5 Ac)as the donor substrate and transferring sialic acid to the ends of glycoproteins and glycolipids.Such enzymes are essential in the synthesis pathways of sialic acid oligosaccharides.Microbial sialyltransferases have broader substrate specificities and are readily overexpressed in common prokaryotic expression systems. It is of great significance for studying enzymatic properties and producing different sialyl oligosaccharides.This review summarized the classification and microbial sources of sialyltransferases,the crystal structure,the mechanism of catalytic reaction,the enzymatic properties,the clone and expression,and their applications in the synthesis of sialylated oligosaccharides.The future study direction of sialyltransferases was also prospected,in order to expand the application of these enzymes in sugar chemistry and sugar biology.
引文
[1]Kurniyati,Supaporn.Studies of sialic acid and sialidase in the oral spirochete,Treponema denticola[D].State University of New York at Buffalo,2015:7-8.
[2]Blix F G,Gottschalk A,Klenk E.Proposed nomenclature in the field of neuraminic and sialic acids[J].Nature,1957,179(4569):1088-1088.
[3]Chen X,Varki A.Advances in the biology and chemistry of sialic acids[J].Acs Chemical Biology,2010,5(2):163-176.
[4]Mehr K,Withers S G.Mechanisms of the sialidase and transsialidase activities of bacterial sialyltransferases from glycosyltransferase family 80(GT80)[J].Glycobiology,2016,26(4):353-359.
[5]Pandey B K,Jabannavar V B,Sonoli S S,et al.Serum sialic acid and lipid levels in the offsprings of type 2 diabetic parents[J].Journal of Krishna Institute of Medical Sciences University,2015,4(3):89-92.
[6]R9hrig C H,Choi S S,Baldwin N.The nutritional role of free sialic acid,a human milk monosaccharide,and its application as a functional food ingredient[J].C R C Critical Reviews in Food Technology,2015,57(5):1017-1038.
[7]齐晓彦.唾液酸在婴幼儿配方奶粉中的应用进展[J].食品工业,2017,38(8):221-225.
[8]王亚娟,邢国文.唾液酸酶和唾液酸糖基转移酶的结构、功能与催化反应研究进展[J].有机化学,2011,31(8):1157-1168.
[9]Ortiz-Soto M E,Seibel J.Expression of functional human sialyltransferases ST3Gal1 and ST6Gal1 in Escherichia coli[J].Plos One,2016,11(5):1-23.
[10]Schm9lzer K,Eibinger M,Nidetzky B.Active-site His85 of Pasteurella dagmatis sialyltransferase facilitates productive sialyl transfer and so prevents futile hydrolysis of CMP-Neu5Ac[J].Chembiochem,2017,18(15):1544-1550.
[11]Kaya Bork,Wenke Weidemann,et al.The expression of sialyltransferases is regulated by the bioavailability and biosynthesis of sialic acids[J].Gene Expression Patterns,2017,23-24.
[12]Lombard V,Golaconda H R,Drula E,et al.The carbohydrate-active enzymes database(CAZy)in 2013[J].Nucleic Acids Research,2014,42(Database issue):D490-D495.
[13]Thon V,Lau K,Yu H,et al.Pm ST2:a novel Pasteurella multocida glycolipidα2-3-sialyltransferase[J].Glycobiology,2011,21(9):1206-1216.
[14]Ji S,Wang F,Chen Y,et al.Developmental changes in the level of free and conjugated sialic acids,Neu5Ac,Neu5Gc and KDN in different organs of pig:a LC-MS/MS quantitative analyses[J].Glycoconjugate Journal,2016,34(1):1-10.
[15]赵玉洁,汪淑晶.唾液酰基转移酶ST6Gal-I在肿瘤中的生物学作用[J].生物学杂志,2016,(6):82-85.
[16]Andreishcheva E N,Vann W F.Gene products required for de novo synthesis of polysialic acid in Escherichia coli K1[J].Journal of Bacteriology,2006,188(5):1786-1797.
[17]Willis L M,Gilbert M,Karwaski M F,et al.Characterization of theα-2,8-polysialyltransferase from Neisseria meningitidis with synthetic acceptors,and the development of a self-priming polysialyltransferase fusion enzyme[J].Glycobiology,2008,18(2):177-186.
[18]Lindhout T,Bainbridge C R,Costain W J,et al.Biochemical characterization of a polysialyltransferase from Mannheimia haemolytica A2 and comparison to other bacterial polysialyltransferases[J].Plos One,2013,8(7):e69888.
[19]Melissa J Schur,Emilie Lameignere,Natalie CJ Strynadka,et al.Characterization ofα2,3-andα2,6-sialyltransferases from Helicobacter acinonychis[J].Glycobiology,2012,22(7):997-1006.
[20]Gilbert M,Brisson J R,Karwaski M F,et al.Biosynthesis of ganglioside mimics in Campylobacter jejuni OH4384.Identification of the glycosyltransferase genes,enzymatic synthesis of model compounds,and characterization of nanomole amounts by 600-mhz(1)h and(13)c NMR analysis[J].Journal of Biological Chemistry,2000,275(6):3896-3906.
[21]Thon V,Li Y,Yu H,et al.PmST3 from Pasteurella multocida encoded by Pm1174 gene is a monofunctionalα2-3-sialyltransferase.[J].Applied Microbiology&Biotechnology,2012,94(4):977-985.
[22]Harrison A,Dyer D W,Gillaspy A,et al.Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae:comparative study with H.influenzae serotype d,strain KW20[J].Journal of Bacteriology,2005,187(13):4627-4636.
[23]Gilbert M,Watson D C,Cunningham A M,et al.Cloning of the lipooligosaccharide alpha-2,3-sialyltransferase from the bacterial pathogens Neisseria meningitidis and Neisseria gonorrhoeae[J].Journal of Biological Chemistry,1996,271(45):28271-28276.
[24]Tsukamoto H,Takakura Y,Mine T,et al.Photobacterium sp.JT-ISH-224 produces two sialyltransferases,alpha-/betagalactoside alpha2,3-sialyltransferase and beta-galactoside alpha2,6-sialyltransferase[J].Journal of Biochemistry,2008,143(2):187-197.
[25]Li Y,Sun M,Huang S,et al.The Hd0053 gene of Haemophilus ducreyi encodes anα2,3-sialyltransferase[J].Biochemical&Biophysical Research Communications,2007,361(2):555-560.
[26]Schm9lzer K,Ribitsch D,Czabany T,et al.Characterization of a multifunctionalα2,3-sialyltransferase from Pasteurella dagmatis[J].Glycobiology,2013,23(11):1293-1304.
[27]Yu H,Harshal Chokhawala,Rebekah Karpel,et al.Amultifunctional Pasteurella multocida sialyltransferase:a powerful tool for the synthesis of sialoside libraries[J].J.am.chem.soc,2005,127(50):17618-17619.
[28]Tsukamoto H,Takakura Y,Yamamoto T.Purification,cloning,and expression of an alpha/beta-galactoside alpha-2,3-sialyltransferase from a luminous marine bacterium,Photobacterium phosphoreum[J].Journal of Biological Chemistry,2007,282(41):29794-29802.
[29]Yamamoto T,Nakashizuka M,Terada I.Cloning and expression of a marine bacterial beta-galactoside alpha 2,6-sialyltransferase gene from Photobacterium damsela JT0160[J].Journal of Biochemistry,1998,123(1):94-100.
[30]Talafova K,Hrabarova E,Nahalka J.A semi-multifunctional sialyltransferase from Bibersteinia trehalosi and its comparison to the Pasteurella multocida ST1 mutants[J].Journal of Biotechnology,2015,216:116-124.
[31]Breton C,Mucha J,Jeanneau C.Structural and functional features of glycosyltransferases[J].Biochimie,2001,83(8):713-718.
[32]Bhide G P,Colley K J.Sialylation of N-glycans:mechanism,cellular compartmentalization and function[J].Histochemistry&Cell Biology,2017,147(2):1-26.
[33]Legaigneur P,Breton C,El B A,et al.Exploring the acceptor substrate recognition of the human beta-galactoside alpha 2,6-sialyltransferase[J].Journal of Biological Chemistry,2001,276(24):21608-21617.
[34]Albesa-JovéD,Guerin ME.The conformational plasticity of glycosyltransferases[J].Curr Opin Struc Biol,2016,40:23-32.
[35]Volkers G,Worrall L J,Kwan D H,et al.Structure of human ST8SiaIII sialyltransferase provides insight into cell-surface polysialylation[J].Nature Structural&Molecular Biology,2015,22(8):627-635.
[36]Audry M,Jeanneau C,Imberty A,et al.Current trends in the structure-activity relationships of sialyltransferases[J].Glycobiology,2011,21(6):716-726.
[37]Li Y,Chen X.Sialic acid metabolism and sialyltransferases:natural functions and applications[J].Applied Microbiology&Biotechnology,2012,94(4):887-905.
[38]Chiu C P,Watts A G,Lairson L L,et al.Structural analysis of the sialyltransferase Cst II from Campylobacter jejuni in complex with a substrate analog[J].Nature Structural&Molecular Biology,2004,11(2):163-170.
[39]Breton C,SnajdrováL,Jeanneau C,et al.Structures and mechanisms of glycosyltransferases[J].Glycobiology,2006,16(2):29R-37R.
[40]Huynh N,Li Y,Yu H,et al.Crystal structures of sialyltransferase from Photobacterium damselae[J].Febs Letters,2014,588(24):4720-4729.
[41]Rao F V,Al E.Structural insight into mammalian sialyltransferases[J].Nat.struct.mol.biol,2009,16(11):1186-1188.
[42]Alejandro Buschiazzo,Pedro M Alzari.Structural insights into sialic acid enzymology[J].Current Opinion in Chemical Biology,2008,12(5):565-572.
[43]Kakuta Y,Okino N,Kajiwara H,et al.Crystal structure of vibrionaceae Photobacterium sp.jt-ish-224α2,6-sialyltransferase in a ternary complex with donor product cmp and acceptor substrate lactose:catalytic mechanism and substrate recognition[J].Glycobiology,2008,18(1):66-73.
[44]Yoshimitsu Takakura,Hiroshi Tsukamoto,Takeshi Yamamoto.Molecular cloning,expression and properties of anα/β-galactosideα2,3-sialyltransferase from Vibrio sp.JT-FAJ-16[J].Journal of Biochemistry,2007,142(3):403-412.
[45]Schur MJ,Lameignere E,Strynadka N C,et al.Characterization ofα2,3-andα2,6-sialyltransferases from Helicobacter acinonychis[J].Glycobiology,2012,22(7):997-1006.
[46]Okino N,Kakuta Y,Kajiwara H,et al.Purification,crystallization and preliminary crystallographic characterization of the alpha 2,6-sialyltransferase from Photobacterium sp.JT-ISH-224[J].Acta Crystallographica,2007,63(8):662-664.
[47]Crespo N,Sánchez-Murcia P A,Gago F,et al.2'-Deoxyribosyltransferase from Leishmania mexicana,an efficient biocatalyst for one-pot,one-step synthesis of nucleosides from poorly soluble purine bases[J].Applied Microbiology&Biotechnology,2017,101(19):7187-7200.
[48]Yu H,Chokhawala H A,Huang S,et al.One-pot threeenzyme chemoenzymatic approach to the synthesis of sialosides containing natural and non-natural functionalities[J].Nature Protocols,2006,1(5):2485-2492.
[49]Cheng J,Yu H,Lau K,et al.Multifunctionality of Campylobacter jejuni sialyltransferase Cst II:Characterization of GD3/GT3 oligosaccharide synthase,GD3 oligosaccharide sialidase,and trans-sialidase activities[J].Glycobiology,2008,18(9):686-697.
[2]Blix F G,Gottschalk A,Klenk E.Proposed nomenclature in the field of neuraminic and sialic acids[J].Nature,1957,179(4569):1088-1088.
[3]Chen X,Varki A.Advances in the biology and chemistry of sialic acids[J].Acs Chemical Biology,2010,5(2):163-176.
[4]Mehr K,Withers S G.Mechanisms of the sialidase and transsialidase activities of bacterial sialyltransferases from glycosyltransferase family 80(GT80)[J].Glycobiology,2016,26(4):353-359.
[5]Pandey B K,Jabannavar V B,Sonoli S S,et al.Serum sialic acid and lipid levels in the offsprings of type 2 diabetic parents[J].Journal of Krishna Institute of Medical Sciences University,2015,4(3):89-92.
[6]R9hrig C H,Choi S S,Baldwin N.The nutritional role of free sialic acid,a human milk monosaccharide,and its application as a functional food ingredient[J].C R C Critical Reviews in Food Technology,2015,57(5):1017-1038.
[7]齐晓彦.唾液酸在婴幼儿配方奶粉中的应用进展[J].食品工业,2017,38(8):221-225.
[8]王亚娟,邢国文.唾液酸酶和唾液酸糖基转移酶的结构、功能与催化反应研究进展[J].有机化学,2011,31(8):1157-1168.
[9]Ortiz-Soto M E,Seibel J.Expression of functional human sialyltransferases ST3Gal1 and ST6Gal1 in Escherichia coli[J].Plos One,2016,11(5):1-23.
[10]Schm9lzer K,Eibinger M,Nidetzky B.Active-site His85 of Pasteurella dagmatis sialyltransferase facilitates productive sialyl transfer and so prevents futile hydrolysis of CMP-Neu5Ac[J].Chembiochem,2017,18(15):1544-1550.
[11]Kaya Bork,Wenke Weidemann,et al.The expression of sialyltransferases is regulated by the bioavailability and biosynthesis of sialic acids[J].Gene Expression Patterns,2017,23-24.
[12]Lombard V,Golaconda H R,Drula E,et al.The carbohydrate-active enzymes database(CAZy)in 2013[J].Nucleic Acids Research,2014,42(Database issue):D490-D495.
[13]Thon V,Lau K,Yu H,et al.Pm ST2:a novel Pasteurella multocida glycolipidα2-3-sialyltransferase[J].Glycobiology,2011,21(9):1206-1216.
[14]Ji S,Wang F,Chen Y,et al.Developmental changes in the level of free and conjugated sialic acids,Neu5Ac,Neu5Gc and KDN in different organs of pig:a LC-MS/MS quantitative analyses[J].Glycoconjugate Journal,2016,34(1):1-10.
[15]赵玉洁,汪淑晶.唾液酰基转移酶ST6Gal-I在肿瘤中的生物学作用[J].生物学杂志,2016,(6):82-85.
[16]Andreishcheva E N,Vann W F.Gene products required for de novo synthesis of polysialic acid in Escherichia coli K1[J].Journal of Bacteriology,2006,188(5):1786-1797.
[17]Willis L M,Gilbert M,Karwaski M F,et al.Characterization of theα-2,8-polysialyltransferase from Neisseria meningitidis with synthetic acceptors,and the development of a self-priming polysialyltransferase fusion enzyme[J].Glycobiology,2008,18(2):177-186.
[18]Lindhout T,Bainbridge C R,Costain W J,et al.Biochemical characterization of a polysialyltransferase from Mannheimia haemolytica A2 and comparison to other bacterial polysialyltransferases[J].Plos One,2013,8(7):e69888.
[19]Melissa J Schur,Emilie Lameignere,Natalie CJ Strynadka,et al.Characterization ofα2,3-andα2,6-sialyltransferases from Helicobacter acinonychis[J].Glycobiology,2012,22(7):997-1006.
[20]Gilbert M,Brisson J R,Karwaski M F,et al.Biosynthesis of ganglioside mimics in Campylobacter jejuni OH4384.Identification of the glycosyltransferase genes,enzymatic synthesis of model compounds,and characterization of nanomole amounts by 600-mhz(1)h and(13)c NMR analysis[J].Journal of Biological Chemistry,2000,275(6):3896-3906.
[21]Thon V,Li Y,Yu H,et al.PmST3 from Pasteurella multocida encoded by Pm1174 gene is a monofunctionalα2-3-sialyltransferase.[J].Applied Microbiology&Biotechnology,2012,94(4):977-985.
[22]Harrison A,Dyer D W,Gillaspy A,et al.Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae:comparative study with H.influenzae serotype d,strain KW20[J].Journal of Bacteriology,2005,187(13):4627-4636.
[23]Gilbert M,Watson D C,Cunningham A M,et al.Cloning of the lipooligosaccharide alpha-2,3-sialyltransferase from the bacterial pathogens Neisseria meningitidis and Neisseria gonorrhoeae[J].Journal of Biological Chemistry,1996,271(45):28271-28276.
[24]Tsukamoto H,Takakura Y,Mine T,et al.Photobacterium sp.JT-ISH-224 produces two sialyltransferases,alpha-/betagalactoside alpha2,3-sialyltransferase and beta-galactoside alpha2,6-sialyltransferase[J].Journal of Biochemistry,2008,143(2):187-197.
[25]Li Y,Sun M,Huang S,et al.The Hd0053 gene of Haemophilus ducreyi encodes anα2,3-sialyltransferase[J].Biochemical&Biophysical Research Communications,2007,361(2):555-560.
[26]Schm9lzer K,Ribitsch D,Czabany T,et al.Characterization of a multifunctionalα2,3-sialyltransferase from Pasteurella dagmatis[J].Glycobiology,2013,23(11):1293-1304.
[27]Yu H,Harshal Chokhawala,Rebekah Karpel,et al.Amultifunctional Pasteurella multocida sialyltransferase:a powerful tool for the synthesis of sialoside libraries[J].J.am.chem.soc,2005,127(50):17618-17619.
[28]Tsukamoto H,Takakura Y,Yamamoto T.Purification,cloning,and expression of an alpha/beta-galactoside alpha-2,3-sialyltransferase from a luminous marine bacterium,Photobacterium phosphoreum[J].Journal of Biological Chemistry,2007,282(41):29794-29802.
[29]Yamamoto T,Nakashizuka M,Terada I.Cloning and expression of a marine bacterial beta-galactoside alpha 2,6-sialyltransferase gene from Photobacterium damsela JT0160[J].Journal of Biochemistry,1998,123(1):94-100.
[30]Talafova K,Hrabarova E,Nahalka J.A semi-multifunctional sialyltransferase from Bibersteinia trehalosi and its comparison to the Pasteurella multocida ST1 mutants[J].Journal of Biotechnology,2015,216:116-124.
[31]Breton C,Mucha J,Jeanneau C.Structural and functional features of glycosyltransferases[J].Biochimie,2001,83(8):713-718.
[32]Bhide G P,Colley K J.Sialylation of N-glycans:mechanism,cellular compartmentalization and function[J].Histochemistry&Cell Biology,2017,147(2):1-26.
[33]Legaigneur P,Breton C,El B A,et al.Exploring the acceptor substrate recognition of the human beta-galactoside alpha 2,6-sialyltransferase[J].Journal of Biological Chemistry,2001,276(24):21608-21617.
[34]Albesa-JovéD,Guerin ME.The conformational plasticity of glycosyltransferases[J].Curr Opin Struc Biol,2016,40:23-32.
[35]Volkers G,Worrall L J,Kwan D H,et al.Structure of human ST8SiaIII sialyltransferase provides insight into cell-surface polysialylation[J].Nature Structural&Molecular Biology,2015,22(8):627-635.
[36]Audry M,Jeanneau C,Imberty A,et al.Current trends in the structure-activity relationships of sialyltransferases[J].Glycobiology,2011,21(6):716-726.
[37]Li Y,Chen X.Sialic acid metabolism and sialyltransferases:natural functions and applications[J].Applied Microbiology&Biotechnology,2012,94(4):887-905.
[38]Chiu C P,Watts A G,Lairson L L,et al.Structural analysis of the sialyltransferase Cst II from Campylobacter jejuni in complex with a substrate analog[J].Nature Structural&Molecular Biology,2004,11(2):163-170.
[39]Breton C,SnajdrováL,Jeanneau C,et al.Structures and mechanisms of glycosyltransferases[J].Glycobiology,2006,16(2):29R-37R.
[40]Huynh N,Li Y,Yu H,et al.Crystal structures of sialyltransferase from Photobacterium damselae[J].Febs Letters,2014,588(24):4720-4729.
[41]Rao F V,Al E.Structural insight into mammalian sialyltransferases[J].Nat.struct.mol.biol,2009,16(11):1186-1188.
[42]Alejandro Buschiazzo,Pedro M Alzari.Structural insights into sialic acid enzymology[J].Current Opinion in Chemical Biology,2008,12(5):565-572.
[43]Kakuta Y,Okino N,Kajiwara H,et al.Crystal structure of vibrionaceae Photobacterium sp.jt-ish-224α2,6-sialyltransferase in a ternary complex with donor product cmp and acceptor substrate lactose:catalytic mechanism and substrate recognition[J].Glycobiology,2008,18(1):66-73.
[44]Yoshimitsu Takakura,Hiroshi Tsukamoto,Takeshi Yamamoto.Molecular cloning,expression and properties of anα/β-galactosideα2,3-sialyltransferase from Vibrio sp.JT-FAJ-16[J].Journal of Biochemistry,2007,142(3):403-412.
[45]Schur MJ,Lameignere E,Strynadka N C,et al.Characterization ofα2,3-andα2,6-sialyltransferases from Helicobacter acinonychis[J].Glycobiology,2012,22(7):997-1006.
[46]Okino N,Kakuta Y,Kajiwara H,et al.Purification,crystallization and preliminary crystallographic characterization of the alpha 2,6-sialyltransferase from Photobacterium sp.JT-ISH-224[J].Acta Crystallographica,2007,63(8):662-664.
[47]Crespo N,Sánchez-Murcia P A,Gago F,et al.2'-Deoxyribosyltransferase from Leishmania mexicana,an efficient biocatalyst for one-pot,one-step synthesis of nucleosides from poorly soluble purine bases[J].Applied Microbiology&Biotechnology,2017,101(19):7187-7200.
[48]Yu H,Chokhawala H A,Huang S,et al.One-pot threeenzyme chemoenzymatic approach to the synthesis of sialosides containing natural and non-natural functionalities[J].Nature Protocols,2006,1(5):2485-2492.
[49]Cheng J,Yu H,Lau K,et al.Multifunctionality of Campylobacter jejuni sialyltransferase Cst II:Characterization of GD3/GT3 oligosaccharide synthase,GD3 oligosaccharide sialidase,and trans-sialidase activities[J].Glycobiology,2008,18(9):686-697.