链球菌神经氨酸酶的作用机制及酶活性的测定技术
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摘要
神经氨酸酶不仅存在于流感病毒,在细菌中也有分布。细菌的神经氨酸酶可裂解宿主体内糖结合物末端的神经氨酸残基,有助于细菌实现在宿主体内的定殖、穿透和扩散,是细菌重要的毒力因子之一。链球菌是自然界广泛存在的人畜共患的病原菌,在多种链球菌中均可检测出神经氨酸酶。肺炎链球菌的神经氨酸酶研究最为透彻,该菌可产生3种神经氨酸酶(NanA,NanB,NanC),NanA不但可以发挥酶的催化作用,分解唾液酸残基,暴露细菌的黏附受体,还能不依赖酶活基团,辅助细菌感染宿主细胞;NanB催化后产物可作为细菌的碳源;NanC可辅助细菌入侵脑部。在无乳链球菌和猪链球菌中,神经氨酸酶的活性一直未得到确切的验证,可能是由于它们的荚膜均含有神经氨酸,所以其神经氨酸酶的活性逐渐在进化中丧失。另外一些链球菌,例如化脓链球菌和C、G、L群链球菌,其神经氨酸酶的底物偏好相近,均对唾液类黏蛋白的催化活性较强,利于链球菌在含唾液类黏蛋白的组织中扩散。在口腔链球菌和血链球菌中,神经氨酸酶破坏血液成分中的神经氨酸链。由此可见,神经氨酸酶的特异性催化作用与链球菌在宿主体内的定植部位密切相关。此外,随着科技的发展,对神经氨酸酶的活性检测,也由早期的硫代巴比妥法,转为现在的荧光值和吸光度的测定,更为便捷和敏感。本文旨在对链球菌的神经氨酸酶的作用机制、与毒力关系及酶活测定方法等研究进展作一综述,为从事相关研究的科学工作者提供参考。
Neuraminidase hydrolyzes the terminal neuraminic acid residue of glycoconjugations. It is used in bacteria for adhesion to host cells, plasma proteins, hemocyte and important barriers and for further colonization,penetration and spread. Thus, the enzyme is an important virulence factor for various bacteria. Streptococci are widely spread pathogens for zoonoses. The activity of neuraminidase could be detected in many Streptococci spp.Streptococcus pneumonia produces 3 neuraminidases(NanA, NanB, NanC). NanA not only catalyzes the sialic residue covering the adhesion receptor, but also accelerates the bacterial infection on host cells. NanB provides carbon source for the bacteria. NanC helps S. pneumonia invading into the brain. As for group B streptococcus and S. suis, the activity of neuraminidase has not been certified yet. Researchers tend to hold the view that the neuraminidase activity has lost through evolution as both kinds of bacteria contain sialic acid in their capsules. The preference for neuraminidase of S. pyogenes and group C, G and L streptococcus is similar with strong catalytic activity for saliva mucin which avails the proliferation in organizations containing saliva mucin. The neuraminidase in S. oralis and S. sanguis destroys the sialic chain in component of blood. In all, the functions of neuraminidase are closely related to the location of bacterial colonization. In the test of enzyme activity, thiobarbital is used in the 1960 s. Now the fluorogenic substrate and spectrophotometric method, the more convenient and sensitive methods,are the main ways measuring the neuraminidase activity. This paper summarizes the category, properties,mechanism of neuraminidase produced by Streptococci as well as the relationship between the enzyme and virulence. The assays for detection of neuraminidase activity are also reviewed.
Neuraminidase hydrolyzes the terminal neuraminic acid residue of glycoconjugations. It is used in bacteria for adhesion to host cells, plasma proteins, hemocyte and important barriers and for further colonization,penetration and spread. Thus, the enzyme is an important virulence factor for various bacteria. Streptococci are widely spread pathogens for zoonoses. The activity of neuraminidase could be detected in many Streptococci spp.Streptococcus pneumonia produces 3 neuraminidases(NanA, NanB, NanC). NanA not only catalyzes the sialic residue covering the adhesion receptor, but also accelerates the bacterial infection on host cells. NanB provides carbon source for the bacteria. NanC helps S. pneumonia invading into the brain. As for group B streptococcus and S. suis, the activity of neuraminidase has not been certified yet. Researchers tend to hold the view that the neuraminidase activity has lost through evolution as both kinds of bacteria contain sialic acid in their capsules. The preference for neuraminidase of S. pyogenes and group C, G and L streptococcus is similar with strong catalytic activity for saliva mucin which avails the proliferation in organizations containing saliva mucin. The neuraminidase in S. oralis and S. sanguis destroys the sialic chain in component of blood. In all, the functions of neuraminidase are closely related to the location of bacterial colonization. In the test of enzyme activity, thiobarbital is used in the 1960 s. Now the fluorogenic substrate and spectrophotometric method, the more convenient and sensitive methods,are the main ways measuring the neuraminidase activity. This paper summarizes the category, properties,mechanism of neuraminidase produced by Streptococci as well as the relationship between the enzyme and virulence. The assays for detection of neuraminidase activity are also reviewed.
引文
[1]Ketterer MR,Rice PA,Gulati S,Kiel S,Byerly L,Fortenberry JD,Soper DE,Apicella MA.Desialylation of Neisseria gonorrhoeae lipooligosaccharide by cervicovaginal microbiome sialidases:the potential for enhancing infectivity in men.The Journal of Infectious Diseases,2016,214(11):1621-1628.
[2]Saito T,Taylor G,Webster RG.Steps in maturation of influenza a virus neuraminidase.Journal of Virology,1995,69(8):5011-5017.
[3]Wang QY,Qiao CL,Shen ZY.The structure and biology function of avian influenza virus neuraminidase.Progress in Veterinary Medicine,2005,26(12):40-43.(in Chinese)王全英,乔传玲,申之义.禽流感病毒神经氨酸酶的结构及其生物学功能.动物医学进展,2005,26(12):40-43.
[4]Horimoto T,Kawaoka Y.Pandemic threat posed by avian influenza a viruses.Clinical Microbiology Reviews,2001,14(1):129-149.
[5]Pettigrew MM,Fennie KP,York MP,Daniels J,Ghaffar F.Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types.Infection and Immunity,2006,74(6):3360-3365.
[6]Chen QH,Huang HC,Li ZN,Xu GG.Study on the key virulence factor neuraminidase Nan A in Streptococcus pneumoniae.China Journal of Modern Medicine,2014,24(8):22-25.(in Chinese)陈乾华,黄汉琮,李泽年,徐国纲.肺炎链球菌主要毒力蛋白神经氨酸酶Nan A的基本特性研究.中国现代医学杂志,2014,24(8):22-25.
[7]Williamson YM,Gowrisankar R,Longo DL,Facklam R,Gipson IK,Ades EP,Carlone GM,Sampson JS.Adherence of nontypeable Streptococcus pneumoniae to human conjunctival epithelial cells.Microbial Pathogenesis,2008,44(3):175-185.
[8]Kadioglu A,Weiser JN,Paton JC,Andrew PW.The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease.Nature Reviews Microbiology,2008,6(4):288-301.
[9]Wren JT,Blevins LK,Pang B,Basu Roy A,Oliver MB,Reimche JL,Wozniak JE,Alexander-Miller MA,Swords WE.Pneumococcal neuraminidase a(NanA)promotes biofilm formation and synergizes with influenza a virus in nasal colonization and middle ear infection.Infection and Immunity,2017,85(4):e01044-16.
[10]Manco S,Hernon F,Yesilkaya H,Paton JC,Andrew PW,Kadioglu A.Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis.Infection and Immunity,2006,74(7):4014-4020.
[11]Walther E,Richter M,Xu Z,Kramer C,von Grafenstein S,Kirchmair J,Grienke U,Rollinger JM,Liedl KR,Slevogt H,Sauerbrei A,Saluz HP,Pfister W,Schmidtke M.Antipneumococcal activity of neuraminidase inhibiting artocarpin.International Journal of Medical Microbiology,2015,305(3):289-297.
[12]Banerjee A,van Sorge NM,Sheen TR,Uchiyama S,Mitchell TJ,Doran KS.Activation of brain endothelium by pneumococcal neuraminidase NanA promotes bacterial internalization.Cellular Microbiology,2010,12(11):1576-1588.
[13]Yesilkaya H,Manco S,Kadioglu A,Terra VS,Andrew PW.The ability to utilize mucin affects the regulation of virulence gene expression in Streptococcus pneumoniae.FEMSMicrobiology Letters,2008,278(2):231-235.
[14]Li MJ,Cao J,Min X,Cai YY,Yin YB,Zhang XM,Wang H.Prokaryotic expression,purification and protective effects of nanA protein of Streptococcus pneumonia.Chinese Journal of Biologicals,2015,28(7):688-692.(in Chinese)黎美君,曹炬,闵讯,蔡莺莺,尹一兵,张雪梅,王虹.肺炎链球菌神经氨酸酶nanA蛋白的原核表达、纯化及其免疫保护效果.中国生物制品学杂志,2015,28(7):688-692.
[15]Xu GG,Kiefel MJ,Wilson JC,Andrew PW,Oggioni MR,Taylor GL.Three Streptococcus pneumoniae sialidases:three different products.Journal of the American Chemical Society,2011,133(6):1718-1721.
[16]Xu H,Sullivan TJ,Sekiguchi JI,Kirikae T,Ojima I,Stratton CF,Mao WM,Rock FL,Alley MRK,Johnson F,Walker SG,Tonge PJ.Mechanism and inhibition of saFabI,the enoyl reductase from Staphylococcus aureus.Biochemistry,2008,47(14):4228-4236.
[17]Marion C,Burnaugh AM,Woodiga SA,King SJ.Sialic acid transport contributes to pneumococcal colonization.Infection and Immunity,2011,79(3):1262-1269.
[18]Owen CD,Lukacik P,Potter JA,Sleator O,Taylor GL,Walsh MA.Streptococcus Pneumoniae NanC:structural insights into the specificity and mechanism of a sialidase that produces a sialidase inhibitor.The Journal of Biological Chemistry,2015,290(46):27736-27748.
[19]Chang YC,Uchiyama S,Varki A,Nizet V.Leukocyte inflammatory responses provoked by pneumococcal sialidase.mBio,2012,3(1):e00220-11.
[20]Gualdi L,Hayre JK,Gerlini A,Bidossi A,Colomba L,Trappetti C,Pozzi G,Docquier JD,Andrew P,Ricci S,Oggioni MR.Regulation of neuraminidase expression in Streptococcus pneumoniae.BMC Microbiology,2012,12:200.
[21]Milligan TW,Straus DC,Mattingly SJ.Extracellular neuraminidase production by group B Streptococci.Infection and Immunity,1977,18(1):189-195.
[22]Ekin IH,Gurturk K,Ilhan Z,Ekin S,Borum AE,Arabaci C,Yesilova A.Detection and comparison of neuraminidase activities in human and bovine group B Streptococci.APMIS,2016,124(12):1093-1098.
[23]Varki A.Multiple changes in sialic acid biology during human evolution.Glycoconjugate Journal,2009,26(3):231-245.
[24]Chang YC,Nizet V.The interplay between Siglecs and sialylated pathogens.Glycobiology,2014,24(9):818-825.
[25]Yamaguchi M,Hirose Y,Nakata M,Uchiyama S,Yamaguchi Y,Goto K,Sumitomo T,Lewis AL,Kawabata S,Nizet V.Evolutionary inactivation of a sialidase in group BStreptococcus.Scientific Reports,2016,6:28852.
[26]Liu GJ,Zhang W,Lu CP.Comparative genomics analysis of Streptococcus agalactiae reveals that isolates from cultured tilapia in China are closely related to the human strain A909.BMC Genomics,2013,14:775.
[27]Wang Y.The neuraminidase B in group B streptococcus is actually a hyaluronidase.Foreign Medicine(Microbiology Section),1994,17(3):137.(in Chinese)王云.B群链球菌神经氨酸酶实际上是一种透明质酸酶.国外医学(微生物学分册),1994,17(3):137.
[28]Wang ZF,Guo CM,Xu YN,Liu GJ,Lu CP,Liu YJ.Two novel functions of hyaluronidase from Streptococcus agalactiae are enhanced intracellular survival and inhibition of proinflammatory cytokine expression.Infection and Immunity,2014,82(6):2615-2625.
[29]Wang ZF.Construction and characterization of hylb and MPdeleted mutant srain in piscine streptococcus agalactiae.Master Dissertation of Nanjing Agricultural University,2014.(in Chinese)王兆飞.鱼源无乳链球菌透明质酸酶和金属蛋白酶基因缺失株构建及特性分析.南京农业大学硕士学位论文,2014.
[30]Hayano S,Tanaka A,Okuyama Y.Distribution and serological specificity of sialidase produced by various groups of streptococci.Journal of Bacteriology,1969,100(1):354-357.
[31]Davis L,Baig MM,Ayoub EM.Properties of extracellular neuraminidase produced by group A Streptococcus.Infection and Immunity,1979,24(3):780-786.
[32]Hayano S,Tanaka A.Sialidase-like enzymes produced by group A,B,C,G,and L streptococci and by Streptococcus sanguis.Journal of Bacteriology,1969,97(3):1328-1333.
[33]Griswold WR,McIntosh JR,Weil III R,McIntosh RM.Neuraminidase treated homologous IgG and immune deposit renal disease in inbred rats.Experimental Biology and Medicine,1975,148(4):1018-1024.
[34]Dong RP.Studies on the pathogenic roles of sialic acid in streptococcus suis serotype 2.Master Dissertation of Nanjing Medical University,2009.(in Chinese)董瑞萍.唾液酸与2型猪链球菌致病性关系的研究.南京医科大学硕士学位论文,2009.
[35]Segura M,Gottschalk M.Streptococcus suis interactions with the murine macrophage cell line J774:adhesion and cytotoxicity.Infection and Immunity,2002,70(8):4312-4322.
[36]Gottschalk M,Segura M.The pathogenesis of the meningitis caused by Streptococcus suis:the unresolved questions.Veterinary Microbiology,2000,76(3):259-272.
[37]Hayano S,Tanaka A.Streptococcal sialidase I.isolation and properties of sialidase produced by group K Streptococcus.Journal of Bacteriology,1967,93(6):1753-1757.
[38]Hayano S,Tanaka A.Streptococcal sialidase II.Kinetic and immunological studies of sialidase produced by group Kstreptococcus.Journal of Bacteriology,1968,95(5):1551-1554.
[39]Reichmann P,Nuhn M,Denapaite D,Brückner R,Henrich B,Maurer P,Rieger M,Klages S,Reinhard R,Hakenbeck R.Genome of Streptococcus oralis strain Uo5.Journal of Bacteriology,2011,193(11):2888-2889.
[40]Beighton D,Whiley RA.Sialidase activity of the“Streptococcus milleri group”and other viridans group streptococci.Journal of Clinical Microbiology,1990,28(6):1431-1433.
[41]Singh AK,Woodiga SA,Grau MA,King SJ.Streptococcus oralis neuraminidase modulates adherence to multiple carbohydrates on platelets.Infection and Immunity,2017,85(3):e00774-16.
[42]Muller HE.Neuraminidase activity in Streptococcus sanguis and in the viridans group,and occurrence of acylneuraminate lyase in viridans organisms isolated from patients with septicemia.Infection and Immunity,1974,9(2):323-328.
[43]Aminoff D.Methods for the quantitative estimation of N-acetylneuraminic acid and their application to hydrolysates of sialomucoids.Biochemical Journal,1961,81(2):384-392.
[44]Xu GG,Potter JA,Russell RJM,Oggioni MR,Andrew PW,Taylor GL.Crystal structure of the NanB sialidase from Streptococcus pneumoniae.Journal of Molecular Biology,2008,384(2):436-449.
[45]Hayre JK,Xu GG,Borgianni L,Taylor GL,Andrew PW,Docquier JD,Oggioni MR.Optimization of a direct spectrophotometric method to investigate the kinetics and inhibition of sialidases.BMC Biochemistry,2012,13:19.
[46]Xu G,Li X,Andrew PW,Taylor GL.Structure of the catalytic domain of Streptococcus pneumoniae sialidase NanA.Acta Crystallographica Section F:Structural Biology Communications,2008,64(9):772-775.
[2]Saito T,Taylor G,Webster RG.Steps in maturation of influenza a virus neuraminidase.Journal of Virology,1995,69(8):5011-5017.
[3]Wang QY,Qiao CL,Shen ZY.The structure and biology function of avian influenza virus neuraminidase.Progress in Veterinary Medicine,2005,26(12):40-43.(in Chinese)王全英,乔传玲,申之义.禽流感病毒神经氨酸酶的结构及其生物学功能.动物医学进展,2005,26(12):40-43.
[4]Horimoto T,Kawaoka Y.Pandemic threat posed by avian influenza a viruses.Clinical Microbiology Reviews,2001,14(1):129-149.
[5]Pettigrew MM,Fennie KP,York MP,Daniels J,Ghaffar F.Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types.Infection and Immunity,2006,74(6):3360-3365.
[6]Chen QH,Huang HC,Li ZN,Xu GG.Study on the key virulence factor neuraminidase Nan A in Streptococcus pneumoniae.China Journal of Modern Medicine,2014,24(8):22-25.(in Chinese)陈乾华,黄汉琮,李泽年,徐国纲.肺炎链球菌主要毒力蛋白神经氨酸酶Nan A的基本特性研究.中国现代医学杂志,2014,24(8):22-25.
[7]Williamson YM,Gowrisankar R,Longo DL,Facklam R,Gipson IK,Ades EP,Carlone GM,Sampson JS.Adherence of nontypeable Streptococcus pneumoniae to human conjunctival epithelial cells.Microbial Pathogenesis,2008,44(3):175-185.
[8]Kadioglu A,Weiser JN,Paton JC,Andrew PW.The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease.Nature Reviews Microbiology,2008,6(4):288-301.
[9]Wren JT,Blevins LK,Pang B,Basu Roy A,Oliver MB,Reimche JL,Wozniak JE,Alexander-Miller MA,Swords WE.Pneumococcal neuraminidase a(NanA)promotes biofilm formation and synergizes with influenza a virus in nasal colonization and middle ear infection.Infection and Immunity,2017,85(4):e01044-16.
[10]Manco S,Hernon F,Yesilkaya H,Paton JC,Andrew PW,Kadioglu A.Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis.Infection and Immunity,2006,74(7):4014-4020.
[11]Walther E,Richter M,Xu Z,Kramer C,von Grafenstein S,Kirchmair J,Grienke U,Rollinger JM,Liedl KR,Slevogt H,Sauerbrei A,Saluz HP,Pfister W,Schmidtke M.Antipneumococcal activity of neuraminidase inhibiting artocarpin.International Journal of Medical Microbiology,2015,305(3):289-297.
[12]Banerjee A,van Sorge NM,Sheen TR,Uchiyama S,Mitchell TJ,Doran KS.Activation of brain endothelium by pneumococcal neuraminidase NanA promotes bacterial internalization.Cellular Microbiology,2010,12(11):1576-1588.
[13]Yesilkaya H,Manco S,Kadioglu A,Terra VS,Andrew PW.The ability to utilize mucin affects the regulation of virulence gene expression in Streptococcus pneumoniae.FEMSMicrobiology Letters,2008,278(2):231-235.
[14]Li MJ,Cao J,Min X,Cai YY,Yin YB,Zhang XM,Wang H.Prokaryotic expression,purification and protective effects of nanA protein of Streptococcus pneumonia.Chinese Journal of Biologicals,2015,28(7):688-692.(in Chinese)黎美君,曹炬,闵讯,蔡莺莺,尹一兵,张雪梅,王虹.肺炎链球菌神经氨酸酶nanA蛋白的原核表达、纯化及其免疫保护效果.中国生物制品学杂志,2015,28(7):688-692.
[15]Xu GG,Kiefel MJ,Wilson JC,Andrew PW,Oggioni MR,Taylor GL.Three Streptococcus pneumoniae sialidases:three different products.Journal of the American Chemical Society,2011,133(6):1718-1721.
[16]Xu H,Sullivan TJ,Sekiguchi JI,Kirikae T,Ojima I,Stratton CF,Mao WM,Rock FL,Alley MRK,Johnson F,Walker SG,Tonge PJ.Mechanism and inhibition of saFabI,the enoyl reductase from Staphylococcus aureus.Biochemistry,2008,47(14):4228-4236.
[17]Marion C,Burnaugh AM,Woodiga SA,King SJ.Sialic acid transport contributes to pneumococcal colonization.Infection and Immunity,2011,79(3):1262-1269.
[18]Owen CD,Lukacik P,Potter JA,Sleator O,Taylor GL,Walsh MA.Streptococcus Pneumoniae NanC:structural insights into the specificity and mechanism of a sialidase that produces a sialidase inhibitor.The Journal of Biological Chemistry,2015,290(46):27736-27748.
[19]Chang YC,Uchiyama S,Varki A,Nizet V.Leukocyte inflammatory responses provoked by pneumococcal sialidase.mBio,2012,3(1):e00220-11.
[20]Gualdi L,Hayre JK,Gerlini A,Bidossi A,Colomba L,Trappetti C,Pozzi G,Docquier JD,Andrew P,Ricci S,Oggioni MR.Regulation of neuraminidase expression in Streptococcus pneumoniae.BMC Microbiology,2012,12:200.
[21]Milligan TW,Straus DC,Mattingly SJ.Extracellular neuraminidase production by group B Streptococci.Infection and Immunity,1977,18(1):189-195.
[22]Ekin IH,Gurturk K,Ilhan Z,Ekin S,Borum AE,Arabaci C,Yesilova A.Detection and comparison of neuraminidase activities in human and bovine group B Streptococci.APMIS,2016,124(12):1093-1098.
[23]Varki A.Multiple changes in sialic acid biology during human evolution.Glycoconjugate Journal,2009,26(3):231-245.
[24]Chang YC,Nizet V.The interplay between Siglecs and sialylated pathogens.Glycobiology,2014,24(9):818-825.
[25]Yamaguchi M,Hirose Y,Nakata M,Uchiyama S,Yamaguchi Y,Goto K,Sumitomo T,Lewis AL,Kawabata S,Nizet V.Evolutionary inactivation of a sialidase in group BStreptococcus.Scientific Reports,2016,6:28852.
[26]Liu GJ,Zhang W,Lu CP.Comparative genomics analysis of Streptococcus agalactiae reveals that isolates from cultured tilapia in China are closely related to the human strain A909.BMC Genomics,2013,14:775.
[27]Wang Y.The neuraminidase B in group B streptococcus is actually a hyaluronidase.Foreign Medicine(Microbiology Section),1994,17(3):137.(in Chinese)王云.B群链球菌神经氨酸酶实际上是一种透明质酸酶.国外医学(微生物学分册),1994,17(3):137.
[28]Wang ZF,Guo CM,Xu YN,Liu GJ,Lu CP,Liu YJ.Two novel functions of hyaluronidase from Streptococcus agalactiae are enhanced intracellular survival and inhibition of proinflammatory cytokine expression.Infection and Immunity,2014,82(6):2615-2625.
[29]Wang ZF.Construction and characterization of hylb and MPdeleted mutant srain in piscine streptococcus agalactiae.Master Dissertation of Nanjing Agricultural University,2014.(in Chinese)王兆飞.鱼源无乳链球菌透明质酸酶和金属蛋白酶基因缺失株构建及特性分析.南京农业大学硕士学位论文,2014.
[30]Hayano S,Tanaka A,Okuyama Y.Distribution and serological specificity of sialidase produced by various groups of streptococci.Journal of Bacteriology,1969,100(1):354-357.
[31]Davis L,Baig MM,Ayoub EM.Properties of extracellular neuraminidase produced by group A Streptococcus.Infection and Immunity,1979,24(3):780-786.
[32]Hayano S,Tanaka A.Sialidase-like enzymes produced by group A,B,C,G,and L streptococci and by Streptococcus sanguis.Journal of Bacteriology,1969,97(3):1328-1333.
[33]Griswold WR,McIntosh JR,Weil III R,McIntosh RM.Neuraminidase treated homologous IgG and immune deposit renal disease in inbred rats.Experimental Biology and Medicine,1975,148(4):1018-1024.
[34]Dong RP.Studies on the pathogenic roles of sialic acid in streptococcus suis serotype 2.Master Dissertation of Nanjing Medical University,2009.(in Chinese)董瑞萍.唾液酸与2型猪链球菌致病性关系的研究.南京医科大学硕士学位论文,2009.
[35]Segura M,Gottschalk M.Streptococcus suis interactions with the murine macrophage cell line J774:adhesion and cytotoxicity.Infection and Immunity,2002,70(8):4312-4322.
[36]Gottschalk M,Segura M.The pathogenesis of the meningitis caused by Streptococcus suis:the unresolved questions.Veterinary Microbiology,2000,76(3):259-272.
[37]Hayano S,Tanaka A.Streptococcal sialidase I.isolation and properties of sialidase produced by group K Streptococcus.Journal of Bacteriology,1967,93(6):1753-1757.
[38]Hayano S,Tanaka A.Streptococcal sialidase II.Kinetic and immunological studies of sialidase produced by group Kstreptococcus.Journal of Bacteriology,1968,95(5):1551-1554.
[39]Reichmann P,Nuhn M,Denapaite D,Brückner R,Henrich B,Maurer P,Rieger M,Klages S,Reinhard R,Hakenbeck R.Genome of Streptococcus oralis strain Uo5.Journal of Bacteriology,2011,193(11):2888-2889.
[40]Beighton D,Whiley RA.Sialidase activity of the“Streptococcus milleri group”and other viridans group streptococci.Journal of Clinical Microbiology,1990,28(6):1431-1433.
[41]Singh AK,Woodiga SA,Grau MA,King SJ.Streptococcus oralis neuraminidase modulates adherence to multiple carbohydrates on platelets.Infection and Immunity,2017,85(3):e00774-16.
[42]Muller HE.Neuraminidase activity in Streptococcus sanguis and in the viridans group,and occurrence of acylneuraminate lyase in viridans organisms isolated from patients with septicemia.Infection and Immunity,1974,9(2):323-328.
[43]Aminoff D.Methods for the quantitative estimation of N-acetylneuraminic acid and their application to hydrolysates of sialomucoids.Biochemical Journal,1961,81(2):384-392.
[44]Xu GG,Potter JA,Russell RJM,Oggioni MR,Andrew PW,Taylor GL.Crystal structure of the NanB sialidase from Streptococcus pneumoniae.Journal of Molecular Biology,2008,384(2):436-449.
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