Endosialidases: Versatile tools for the study of polysialic acid

Topics in Current Chemistry

Volumn 367, Issue , 2015, Pages 29-74

  Jakobsson, Elina ^a   Schwarzer, David ^b   Jokilammi, Anne ^a   Finne, Jukka ^c  

^a UNIVERSITY OF TURKU   (Finland)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Bacteria; Bacteriophages; Cell adhesion; Endosialidase; Polysialic acid

Indexed keywords

ENDO-N-ACETYLNEURAMINIDASE; HYBRID PROTEIN; N ACETYLNEURAMINIC ACID; POLYSIALIC ACID; SIALIC ACID DERIVATIVE; SIALIDASE; VIRUS PROTEIN;

ANIMAL; BACTERIAL MENINGITIS; BACTERIOPHAGE; BACTERIUM; CELL MEMBRANE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; HUMAN; METABOLISM; PATHOLOGY; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEPSIS; VIROLOGY;

ANIMALS; BACTERIA; BACTERIOPHAGES; CATALYTIC DOMAIN; CELL MEMBRANE; HUMANS; MENINGITIS, BACTERIAL; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SEPSIS; SIALIC ACIDS; VIRAL PROTEINS;

EID: 84938320666     PISSN: 03401022     EISSN: None     Source Type: Book Series    
DOI: 10.1007/128_2012_349     Document Type: Article

References (204)

1. Barry GT (1958) Colominic acid, a polymer of N-acetylneuraminic acid. J Exp Med 107:507-521
2. Reglero A, Rodríguez-Aparicio LB, Luengo JM (1993) Polysialic acids. Int J Biochem 25:1517-1527
3. Drake PM, Nathan JK, Stock CM, Chang PV, Muench MO, Nakata D, Reader JR, Gip P, Golden KPK, Weinhold B, Gerardy-Schahn R, Troy FA, Bertozzi CR (2008) Polysialic acid, a glycan with highly restricted expression, is found on human and murine leukocytes and modulates immune responses. J Immunol 181:6850-6858
4. Finne J, Finne U, Deagostini-Bazin H, Goridis C (1983) Occurrence of alpha 2-8 linked polysialosyl units in a neural cell adhesion molecule. Biochem Biophys Res Commun 112:482-487
5. Rutishauser U (1998) Polysialic acid at the cell surface: biophysics in service of cell interactions and tissue plasticity. J Cell Biochem 70:304-312
6. Tanaka F, Otake Y, Nakagawa T, Kawano Y, Miyahara R, Li M, Yanagihara K, Nakayama J, Fujimoto I, Ikenaka K, Wada H (2000) Expression of polysialic acid and STX, a human polysialyltransferase, is correlated with tumor progression in non-small cell lung cancer. Cancer Res 60:3072-3080
7. Seidenfaden R, Krauter A, Schertzinger F, Gerardy-Schahn R, Hildebrandt H (2003) Polysialic acid directs tumor cell growth by controlling heterophilic neural cell adhesion molecule interactions. Mol Cell Biol 23:5908-5918
8. Cheung IY, Vickers A, Cheung NKV (2006) Sialyltransferase STX (ST8SiaII): a novel molecular marker of metastatic neuroblastoma. Int J Cancer 119:152-156
9. Jann K, Jann B (1987) Polysaccharide antigens of Escherichia coli. Rev Infect Dis 9 (Suppl 5):S517-S526
10. Wyle FA, Artenstein MS, Brandt BL, Tramont EC, Kasper DL, Altieri PL, Berman SL, Lowenthal JP (1972) Immunologic response of man to group B meningococcal polysaccharide vaccines. J Infect Dis 126:514-521
11. Sundar MM, Nagananda GS, Das A, Bhattacharya S, Suryan S (2009) Isolation of hostspecific bacteriophages from sewage against human pathogens. Asian J Biotechnol 1:163-170
12. Stummeyer K, Dickmanns A, Mühlenhoff M, Gerardy-Schahn R, Ficner R (2005) Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 12:90-96
13. Leiman PG, Battisti AJ, Bowman VD, Stummeyer K, Mühlenhoff M, Gerardy-Schahn R, Scholl D, Molineux IJ (2007) The structures of bacteriophages K1E and K1-5 explain processive degradation of polysaccharide capsules and evolution of new host specificities. J Mol Biol 371:836-849
14. Mühlenhoff M, Stummeyer K, Grove M, Sauerborn M, Gerardy-Schahn R (2003) Proteolytic processing and oligomerization of bacteriophage-derived endosialidases. J Biol Chem 278:12634-12644
15. Pelkonen S, Aalto J, Finne J (1992) Differential activities of bacteriophage depolymerase on bacterial polysaccharide: binding is essential but degradation is inhibitory in phage infection of K1-defective Escherichia coli. J Bacteriol 174:7757-7761
16. Twort FW (1915) An investigation on the nature of ultramicroscopic viruses. Lancet 186:1241-1243
17. d'Herelle F (1917) Sur un microbe invisible antagoniste des bacilles dysentériques. Comptes Rendus de 1' Académie des Sciences (Paris) 165:373-375
18. Bergh O, Børsheim KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340:467-468
19. Chibani-Chennoufi S, Canchaya C, Bruttin A, Brüssow H (2004) Comparative genomics of the T4-like Escherichia coli phage JS98: implications for the evolution of T4 phages. J Bacteriol 186:8276-8286
20. Brüssow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560-602
21. Ackermann HW (2007) 5500 Phages examined in the electron microscope. Arch Virol 152:227-243
22. Ackermann HW (2006) Classification of bacteriophages. In: Calendar R, Abedon ST (eds) The bacteriophages, 2nd edn. Oxford University Press, New York, pp 8-16
23. Bradley DE (1967) Ultrastructure of bacteriophage and bacteriocins. Bacteriol Rev 31:230-314
24. Ackermann HW (1998) Tailed bacteriophages: the order Caudovirales. Adv Virus Res 51:135-201
25. Leiman PG, Kanamaru S, Mesyanzhinov VV, Arisaka F, Rossmann MG (2003) Structure and morphogenesis of bacteriophage T4. Cell Mol Life Sci 60:2356-2370
26. Mesyanzhinov VV, Leiman PG, Kostyuchenko VA, Kurochkina LP, Miroshnikov KA, Sykilinda NN, Shneider MM (2004) Molecular architecture of bacteriophage T4. Biochemistry (Mosc) 69:1190-1202
27. Rossmann MG, Mesyanzhinov VV, Arisaka F, Leiman PG (2004) The bacteriophage T4 DNA injection machine. Curr Opin Struct Biol 14:171-180
28. Sayers JR (2006) Bacteriophage T5. In: Calendar R, Abedon ST (eds) The bacteriophages, 2nd edn. Oxford University Press, New York, pp 268-276
29. Molineux IJ (2006) The T7 group. In: Calendar R, Abedon ST (eds) The bacteriophages, 2nd edn. Oxford University Press, New York, pp 277-301
30. Steinbacher S, Seckler R, Miller S, Steipe B, Huber R, Reinemer P (1994) Crystal structure of P22 tailspike protein: interdigitated subunits in a thermostable trimer. Science 265:383-386
31. van Raaij MJ, Schoehn G, Burda MR, Miller S (2001) Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre. J Mol Biol 314:1137-1146
32. Kanamaru S, Leiman PG, Kostyuchenko VA, Chipman PR, Mesyanzhinov VV, Arisaka F, Rossmann MG (2002) Structure of the cell-puncturing device of bacteriophage T4. Nature 415:553-557
33. Freiberg A, Morona R, den Bosch LV, Jung C, Behlke J, Carlin N, Seckler R, Baxa U (2003) The tailspike protein of Shigella phage Sf6. A structural homolog of salmonella phage P22 tailspike protein without sequence similarity in the beta-helix domain. J Biol Chem 278:1542-1548
34. Weigele PR, Scanlon E, King J (2003) Homotrimeric, beta-stranded viral adhesins and tail proteins. J Bacteriol 185:4022-4030
35. Stirm S, Freund-Mölbert E (1971) Escherichia coli capsule bacteriophages. II. Morphology. J Virol 8:330-342
36. Lindberg AA (1977) Bacterial surface carbohydrates and bacteriophage adsorption. In: Sutherland IW (ed) Surface carbohydrates of the procaryotic cell. Academic, New York, pp 289-356
37. Sutherland IW (1977) Enzymes acting on bacterial surface carbohydrates. In: Sutherland IW (ed) Surface carbohydrates of the procaryotic cell. Academic, New York, pp 209-245
38. Scholl D, Adhya S, Merril C (2005) Escherichia coli K1's capsule is a barrier to bacteriophage T7. Appl Environ Microbiol 71:4872-4874
39. Cross AS (1990) The biologic significance of bacterial encapsulation. Curr Top Microbiol Immunol 150:87-95
40. Moxon ER, Kroll JS (1990) The role of bacterial polysaccharide capsules as virulence factors. Curr Top Microbiol Immunol 150:65-85
41. Taylor CM, Roberts IS (2005) Capsular polysaccharides and their role in virulence. Contrib Microbiol 12:55-66
42. Johnson JR (1991) Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4:80-128
43. Goller CC, Seed PC (2010) Revisiting the Escherichia coli polysaccharide capsule as a virulence factor during urinary tract infection: contribution to intracellular biofilm development. Virulence 1:333-337
44. Robbins JB, McCracken JGH, Gotschlich EC, Orskov F, Orskov I, Hanson LA (1974) Escherichia coli K1 capsular polysaccharide associated with neonatal meningitis. N Engl J Med 290:1216-1220
45. Sarff LD, McCracken GH, Schiffer MS, Glode MP, Robbins JB, Orskov I, Orskov F (1975) Epidemiology of Escherichia coli K1 in healthy and diseased newborns. Lancet 1:1099-1104
46. Varki NM, Varki A (2007) Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab Invest 87:851-857
47. Barry GT, Goebel WF (1957) Colominic acid, a substance of bacterial origin related to sialic acid. Nature 179:206
48. McGuire EJ, Binkley SB (1964) The structure and chemistry of colominic acid. Biochemistry 3:247-251
49. Bhattacharjee AK, Jennings HJ, Kenny CP, Martin A, Smith IC (1975) Structural determination of the sialic acid polysaccharide antigens of Neisseria meningitidis serogroups B and C with carbon 13 nuclear magnetic resonance. J Biol Chem 250:1926-1932
50. Devi SJN, Schneerson R, Egan W, Vann WF, Robbins JB, Shiloach J (1991) Identity between polysaccharide antigens of Moraxella nonliquefaciens, group B Neisseria meningitidis, and Escherichia coli K1 (non-O acetylated). Infect Immun 59:732-736
51. Adlam C, Knights JM, Mugridge A, Williams JM, Lindon JC (1987) Production of colominic acid by Pasteurella haemolytica serotype A2 organism. FEMS Microbiol Lett 42:23-26
52. Furowicz AJ, Ørskov F (1972) Two new Escherichia coli O antigens, O150 and O157, and one new K antigen, K92, in strains isolated from veterinary diseases. Acta Pathol Microbiol Scand B Microbiol Immunol 80:441-444
53. Zhang Y, Inoue Y, Inoue S, Lee YC (1997) Separation of oligo/polymers of 5-N-acetylneuraminic acid, 5-N-glycolylneuraminic acid, and 2-keto-3-deoxy-D-glycero- D-galacto-nononic acid by high-performance anion-exchange chromatography with pulsed amperometric detector. Anal Biochem 250:245-251
54. Egan W, Liu TY, Dorow D, Cohen JS, Robbins JD, Gotschlich EC, Robbins JB (1977) Structural studies on the sialic acid polysaccharide antigen of Escherichia coli strain Bos-12. Biochemistry 16:3687-3692
55. Steenbergen SM, Lee YC, Vann WF, Vionnet J, Wright LF, Vimr ER (2006) Separate pathways for O acetylation of polymeric and monomeric sialic acids and identification of sialyl O-acetyl esterase in Escherichia coli K1. J Bacteriol 188:6195-6206
56. Bergfeld AK, Claus H, Vogel U, Mühlenhoff M (2007) Biochemical characterization of the polysialic acid-specific O-acetyltransferase NeuO of Escherichia coli K1. J Biol Chem 282:22217-22227
57. Bergfeld AK, Claus H, Lorenzen NK, Spielmann F, Vogel U, Mühlenhoff M (2009) The polysialic acid-specific O-acetyltransferase OatC from Neisseria meningitidis serogroup C evolved apart from other bacterial sialate O-acetyltransferases. J Biol Chem 284:6-16
58. Finne J (1982) Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J Biol Chem 257:11966-11970
59. Zuber C, Lackie PM, Catterall WA, Roth J (1992) Polysialic acid is associated with sodium channels and the neural cell adhesion molecule N-CAM in adult rat brain. J Biol Chem 267:9965-9971
60. Yabe U, Sato C, Matsuda T, Kitajima K (2003) Polysialic acid in human milk. CD36 is a new member of mammalian polysialic acid-containing glycoprotein. J Biol Chem 278:13875-13880
61. Moebius JM, Widera D, Schmitz J, Kaltschmidt C, Piechaczek C (2007) Impact of polysialylated CD56 on natural killer cell cytotoxicity. BMC Immunol 8:13
62. Curreli S, Arany Z, Gerardy-Schahn R, Mann D, Stamatos NM (2007) Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. J Biol Chem 282:30346-30356
63. Galuska SP, Rollenhagen M, Kaup M, Eggers K, Oltmann-Norden I, Schiff M, Hartmann M, Weinhold B, Hildebrandt H, Geyer R, Mühlenhoff M, Geyer H (2010) Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proc Natl Acad Sci USA 107:10250-10255
64. Finne J, Leinonen M, Mäkelä PH (1983) Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet 322:355-357
65. Frosch M, Roberts I, Görgen I, Metzger S, Boulnois GJ, Bitter-Suermann D (1987) Serotyping and genotyping of encapsulated Escherichia coli K1 sepsis isolates with a monoclonal IgG anti K1 antibody and K1 gene probes. Microb Pathog 2:319-326
66. Prasadarao NV, Wass CA, Weiser JN, Stins MF, Huang SH, Kim KS (1996) Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 64:146-153
67. Jódar L, Feavers IM, Salisbury D, Granoff DM (2002) Development of vaccines against meningococcal disease. Lancet 359:1499-1508
68. Gross RJ, Cheasty T, Rowe B (1977) Isolation of bacteriophages specific for the K1 polysaccharide antigen of Escherichia coli. J Clin Microbiol 6:548-550
69. Jakobsson E, Jokilammi A, Aalto J, Ollikka P, Lehtonen JV, Hirvonen H, Finne J (2007) Identification of amino acid residues at the active site of endosialidase that dissociate the polysialic acid binding and cleaving activities in Escherichia coli K1 bacteriophages. Biochem J 405:465-472
70. Long GS, Bryant JM, Taylor PW, Luzio JP (1995) Complete nucleotide sequence of the gene encoding bacteriophage E endosialidase: implication for K1E endosialidase structure and function. Biochem J 309:543-550
71. Gerardy-Schahn R, Bethe A, Brennecke T,Mühlenhoff M, Eckhardt M, Ziesing S, Lottspeich F, Frosch M (1995) Molecular cloning and functional expression of bacteriophage PK1E-encoded endoneuraminidase Endo NE. Mol Microbiol 16:441-450
72. Kwiatkowski B, Boschek B, Thiele H, Stirm S (1982) Endo-N-acetylneuraminidase associated with bacteriophage particles. J Virol 43:697-704
73. Smith HW, Huggins MB (1982) Successful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics. J Gen Microbiol 128:307-318
74. Kwiatkowski B, Boschek B, Thiele H, Stirm S (1983) Substrate specificity of two bacteriophage-associated endo-N-acetylneuraminidases. J Virol 45:367-374
75. Vimr ER, McCoy RD, Vollger HF, Wilkison NC, Troy FA (1984) Use of prokaryotic-derived probes to identify poly(sialic acid) in neonatal neuronal membranes. Proc Natl Acad Sci USA 81:1971-1975
76. Petter JG, Vimr ER (1993) Complete nucleotide sequence of the bacteriophage K1F tail gene encoding endo-N-acylneuraminidase (endo-N) and comparison to an endo-N homolog in bacteriophage PK1E. J Bacteriol 175:4354-4363
77. Miyake K, Muraki T, Hattori K, Machida Y, Watanabe M, Kawase M, Yoshida Y, Iijima S (1997) Screening of bacteriophages producing endo-N-acetylneuraminidase. J Ferment Bioeng 84:90-93
78. Machida Y, Hattori K, Miyake K, Kawase Y, Kawase M, Iijima S (2000) Molecular cloning and characterization of a novel bacteriophage-associated sialidase. J Biosci Bioeng 90:62-68
79. Scholl D, Rogers S, Adhya S, Merril CR (2001) Bacteriophage K1-5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. J Virol 75:2509-2515
80. Deszo EL, Steenbergen SM, Freedberg DI, Vimr ER (2005) Escherichia coli K1 polysialic acid O-acetyltransferase gene, neuO, and the mechanism of capsule form variation involving a mobile contingency locus. Proc Natl Acad Sci USA 102:5564-5569
81. Stummeyer K, Schwarzer D, Claus H, Vogel U, Gerardy-Schahn R, Mühlenhoff M (2006) Evolution of bacteriophages infecting encapsulated bacteria: lessons from Escherichia coli K1-specific phages. Mol Microbiol 60:1123-1135
82. Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V, Sabo A, Blasiar D, Bieri T, Meyer RR, Ozersky P, Armstrong JR, Fulton RS, Latreille JP, Spieth J, Hooton TM, Mardis ER, Hultgren SJ, Gordon JI (2006) Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci USA 103:5977-5982
83. Johnson TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, Doetkott C, Skyberg JA, Lynne AM, Johnson JR, Nolan LK (2007) The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol 189:3228-3236
84. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, Karoui ME, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Bouguénec CL, Lescat M, Mangenot S, Martinez-Jéhanne V, Matic I, Nassif X, Oztas S, Petit MA, Pichon C, Rouy Z, Ruf CS, Schneider D, Tourret J, Vacherie B, Vallenet D, Médigue C, Rocha EPC, Denamur E (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5:e1000344
85. Moriel DG, Bertoldi I, Spagnuolo A, Marchi S, Rosini R, Nesta B, Pastorello I, Corea VAM, Torricelli G, Cartocci E, Savino S, Scarselli M, Dobrindt U, Hacker J, Tettelin H, Tallon LJ, Sullivan S, Wieler LH, Ewers C, Pickard D, Dougan G, Fontana MR, Rappuoli R, Pizza M, Serino L (2010) Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli. Proc Natl Acad Sci USA 107:9072-9077
86. Bull JJ, Vimr ER, Molineux IJ (2010) A tale of tails: sialidase is key to success in a model of phage therapy against K1-capsulated Escherichia coli. Virology 398:79-86
87. Krause DO, Little AC, Dowd SE, Bernstein CN (2011) Complete genome sequence of adherent invasive Escherichia coli UM146 isolated from ileal Crohn's disease biopsy tissue. J Bacteriol 193:583
88. Steinbacher S, Baxa U, Miller S, Weintraub A, Seckler R, Huber R (1996) Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors. Proc Natl Acad Sci USA 93:10584-10588
89. Müller JJ, Barbirz S, Heinle K, Freiberg A, Seckler R, Heinemann U (2008) An intersubunit active site between supercoiled parallel beta helices in the trimeric tailspike endorhamnosidase of Shigella flexneri Phage Sf6. Structure 16:766-775
90. Barbirz S, Müller JJ, Uetrecht C, Clark AJ, Heinemann U, Seckler R (2008) Crystal structure of Escherichia coli phage HK620 tailspike: podoviral tailspike endoglycosidase modules are evolutionarily related. Mol Microbiol 69:303-316
91. Li YT, Nakagawa H, Ross SA, Hansson GC, Li SC (1990) A novel sialidase which releases 2,7-anhydro-alpha-N-acetylneuraminic acid from sialoglycoconjugates. J Biol Chem 265:21629-21633
92. Hirst GK (1942) Adsorption of influenza hemagglutinins and virus by red blood cells. J Exp Med 76:195-209
93. Stirm S (1968) Escherichia coli K bacteriophages. I. Isolation and introductory characterization of five Escherichia coli K bacteriophages. J Virol 2:1107-1114
94. Stirm S, Bessler W, Fehmel F, Freund-Mölbert E (1971) Bacteriophage particles with endoglycosidase activity. J Virol 8:343-346
95. Cabezas JA (1991) Some questions and suggestions on the type references of the official nomenclature (IUB) for sialidase (s) and endosialidase. Biochem J 278(Pt 1):311-312
96. Kitajima K, Inoue S, Inoue Y, Troy FA (1988) Use of a bacteriophage-derived endo-Nacetylneuraminidase and an equine antipolysialyl antibody to characterize the polysialyl residues in salmonid fish egg polysialoglycoproteins. Substrate and immunospecificity studies. J Biol Chem 263:18269-18276
97. Uchida Y, Tsukada Y, Sugimori T (1979) Enzymatic properties of neuraminidases from Arthrobacter ureafaciens. J Biochem 86:1573-1585
98. Cheng MC, Lin CH, Lin HJ, Yu YP, Wu SH (2004) Hydrolysis, lactonization, and identification of alpha(2 ->8)/alpha(2 ->9) alternatively linked tri-, tetra-, and polysialic acids. Glycobiology 14:147-155
99. Kwiatkowski B, Stirm S (1987) Polysialic acid depolymerase. Methods Enzymol 138:786-792
100. Orskov F, Orskov I, Sutton A, Schneerson R, Lin W, Egan W, Hoff GE, Robbins JB (1979) Form variation in Escherichia coli K1: determined by O-acetylation of the capsular polysaccharide. J Exp Med 149:669-685
101. Tomlinson S, Taylor PW (1985) Neuraminidase associated with coliphage E that specifically depolymerizes the Escherichia coli K1 capsular polysaccharide. J Virol 55:374-378
102. Finne J, Mäkelä PH (1985) Cleavage of the polysialosyl units of brain glycoproteins by a bacteriophage endosialidase. Involvement of a long oligosaccharide segment in molecular interactions of polysialic acid. J Biol Chem 260:1265-1270
103. Pelkonen S, Pelkonen J, Finne J (1989) Common cleavage pattern of polysialic acid by bacteriophage endosialidases of different properties and origins. J Virol 63:4409-4416
104. Hallenbeck PC, Vimr ER, Yu F, Bassler B, Troy FA (1987) Purification and properties of a bacteriophage-induced endo-N-acetylneuraminidase specific for poly-alpha-2,8-sialosyl carbohydrate units. J Biol Chem 262:3553-3561
105. Schwarzer D, Stummeyer K, Haselhorst T, Freiberger F, Rode B, Grove M, Scheper T, von Itzstein M, Mühlenhoff M, Gerardy-Schahn R (2009) Proteolytic release of the intramolecular chaperone domain confers processivity to endosialidase F. J Biol Chem 284:9465-9474
106. Schulz EC, Schwarzer D, Frank M, Stummeyer K, Mühlenhoff M, Dickmanns A, Gerardy- Schahn R, Ficner R (2010) Structural basis for the recognition and cleavage of polysialic acid by the bacteriophage K1F tailspike protein EndoNF. J Mol Biol 397:341-351
107. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132
108. Vimr ER, Aaronson W, Silver RP (1989) Genetic analysis of chromosomal mutations in the polysialic acid gene cluster of Escherichia coli K1. J Bacteriol 171:1106-1117
109. Schulz EC, Dickmanns A, Urlaub H, Schmitt A,Mühlenhoff M, Stummeyer K, Schwarzer D, Gerardy-Schahn R, Ficner R (2010) Crystal structure of an intramolecular chaperone mediating triple-beta-helix folding. Nat Struct Mol Biol 17:210-215
110. Schwarzer D (2008) Characterisation of bacteriophage-derived tailspike and tail fibre proteins. Ph.D. thesis. Leibniz University Hannover. Hannover. (http://edok01.tib.unihannover. de/edoks/e01dh08/564826944.pdf)
111. Pajunen M, Kiljunen S, Skurnik M (2000) Bacteriophage phiYeO3-12, specific for Yersinia enterocolitica serotype O:3, is related to coliphages T3 and T7. J Bacteriol 182:5114-5120
112. Schwarzer D, Stummeyer K, Gerardy-Schahn R, Mühlenhoff M (2007) Characterization of a novel intramolecular chaperone domain conserved in endosialidases and other bacteriophage tail spike and fiber proteins. J Biol Chem 282:2821-2831
113. Schulz EC, Neumann P, Gerardy-Schahn R, Sheldrick GM, Ficner R (2010) Structure analysis of endosialidase NF at 0.98 A resolution. Acta Crystallogr D Biol Crystallogr 66:176-180
114. Crennell SJ, Garman EF, Laver WG, Vimr ER, Taylor GL (1993) Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase. Proc Natl Acad Sci USA 90:9852-9856
115. Newstead SL, Potter JA, Wilson JC, Xu G, Chien CH, Watts AG, Withers SG, Taylor GL (2008) The structure of Clostridium perfringens NanI sialidase and its catalytic intermediates. J Biol Chem 283:9080-9088
116. Gaskell A, Crennell S, Taylor G (1995) The three domains of a bacterial sialidase: a betapropeller, an immunoglobulin module and a galactose-binding jelly-roll. Structure 3:1197-1205
117. Luo Y, Li SC, Chou MY, Li YT, Luo M (1998) The crystal structure of an intramolecular trans-sialidase with a NeuAc alpha2->3 Gal specificity. Structure 6:521-530
118. Moustafa I, Connaris H, Taylor M, Zaitsev V, Wilson JC, Kiefel MJ, von Itzstein M, Taylor G (2004) Sialic acid recognition by Vibrio cholerae neuraminidase. J Biol Chem 279:40819-40826
119. Buschiazzo A, Tavares GA, Campetella O, Spinelli S, Cremona ML, Paris G, Amaya MF, Frasch AC, Alzari PM (2000) Structural basis of sialyltransferase activity in trypanosomal sialidases. EMBO J 19:16-24
120. Buschiazzo A, Amaya MF, Cremona ML, Frasch AC, Alzari PM (2002) The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Mol Cell 10:757-768
121. Thobhani S, Ember B, Siriwardena A, Boons GJ (2003) Multivalency and the mode of action of bacterial sialidases. J Am Chem Soc 125:7154-7155
122. Olia AS, Casjens S, Cingolani G (2007) Structure of phage P22 cell envelope-penetrating needle. Nat Struct Mol Biol 14:1221-1226
123. Manning M, ColónW(2004) Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward beta-sheet structure. Biochemistry 43:11248-11254
124. Weigele PR, Haase-Pettingell C, Campbell PG, Gossard DC, King J (2005) Stalled folding mutants in the triple beta-helix domain of the phage P22 tailspike adhesion. J Mol Biol 354:1103-1117
125. Botstein D (1980) A theory of modular evolution for bacteriophages. Ann N Y Acad Sci 354:484-490
126. Casjens SR (2005) Comparative genomics and evolution of the tailed-bacteriophages. Curr Opin Microbiol 8:451-458
127. Morley TJ, Willis LM, Whitfield C, Wakarchuk WW, Withers SG (2009) A new sialidase mechanism: bacteriophage K1F endo-sialidase is an inverting glycosidase. J Biol Chem 284:17404-17410
128. Friebolin H, Brossmer R, Keilich G, Ziegler D, Supp M (1980) 1H-NMR-Spectroscopic evidence for the release of N-acetyl-alpha-D-neuraminic acid as the first product of neuraminidase action (author's transl). Hoppe Seylers Z Physiol Chem 361:697-702
129. Todeschini AR, Mendonça-Previato L, Previato JO, Varki A, van Halbeek H (2000) Trans-sialidase from Trypanosoma cruzi catalyzes sialoside hydrolysis with retention of configuration. Glycobiology 10:213-221
130. Manzi AE, Higa HH, Diaz S, Varki A (1994) Intramolecular self-cleavage of polysialic acid. J Biol Chem 269:23617-23624
131. Yamasaki R, Bacon B (1991) Three-dimensional structural analysis of the group B polysaccharide of Neisseria meningitides 6275 by two-dimensional NMR: the polysaccharide is suggested to exist in helical conformations in solution. Biochemistry 30:851-857
132. Brisson JR, Baumann H, Imberty A, Pérez S, Jennings HJ (1992) Helical epitope of the group B meningococcal alpha(2-8)-linked sialic acid polysaccharide. Biochemistry 31:4996-5004
133. Azurmendi HF, Vionnet J, Wrightson L, Trinh LB, Shiloach J, Freedberg DI (2007) Extracellular structure of polysialic acid explored by on cell solution NMR. Proc Natl Acad Sci USA 104:11557-11561
134. Michon F, Brisson JR, Jennings HJ (1987) Conformational differences between linear alpha (2-8)-linked homosialooligosaccharides and the epitope of the group B meningococcal polysaccharide. Biochemistry 26:8399-8405
135. Haselhorst T, Stummeyer K, Mühlenhoff M, Schaper W, Gerardy-Schahn R, von Itzstein M (2006) Endosialidase NF appears to bind polySia DP5 in a helical conformation. Chembiochem 7:1875-1877
136. Schulz EC, Ficner R (2011) Knitting and snipping: chaperones in b-helix folding. Curr Opin Struct Biol 21:232-239
137. Xiang Y, Leiman PG, Li L, Grimes S, Anderson DL, Rossmann MG (2009) Crystallographic insights into the autocatalytic assembly mechanism of a bacteriophage tail spike. Mol Cell 34:375-386
138. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
139. Marvik OJ, Jacobsen E, Dokland T, Lindqvist BH (1994) Bacteriophage P2 and P4 morphogenesis: assembly precedes proteolytic processing of the capsid proteins. Virology 205:51-65
140. Conway JF, Duda RL, Cheng N, Hendrix RW, Steven AC (1995) Proteolytic and conformational control of virus capsid maturation: the bacteriophage HK97 system. J Mol Biol 253:86-99
141. Wang S, Chandramouli P, Butcher S, Dokland T (2003) Cleavage leads to expansion of bacteriophage P4 procapsids in vitro. Virology 314:1-8
142. Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Rüger W (2003) Bacteriophage T4 genome. Microbiol Mol Biol Rev 67:86-156, table of contents
143. Cunningham EL, Jaswal SS, Sohl JL, Agard DA (1999) Kinetic stability as a mechanism for protease longevity. Proc Natl Acad Sci USA 96:11008-11014
144. Bayer ME, Thurow H, Bayer MH (1979) Penetration of the polysaccharide capsule of Escherichia coli (Bi161/42) by bacteriophage K29. Virology 94:95-118
145. Leiman PG, Molineux IJ (2008) Evolution of a new enzyme activity from the same motif fold. Mol Microbiol 69:287-290
146. Koivula A, Kinnari T, Harjunpää V, Ruohonen L, Teleman A, Drakenberg T, Rouvinen J, Jones TA, Teeri TT (1998) Tryptophan 272: an essential determinant of crystalline cellulose degradation by Trichoderma reesei cellobiohydrolase Cel6A. FEBS Lett 429:341-346
147. Zhang S, Irwin DC, Wilson DB (2000) Site-directed mutation of noncatalytic residues of Thermobifida fusca exocellulase Ce16B. Eur J Biochem 267:3101-3115
148. Watanabe T, Ariga Y, Sato U, Toratani T, Hashimoto M, Nikaidou N, Kezuka Y, Nonaka T, Sugiyama J (2003) Aromatic residues within the substrate-binding cleft of Bacillus circulans chitinase A1 are essential for hydrolysis of crystalline chitin. Biochem J 376:237-244
149. Katouno F, Taguchi M, Sakurai K, Uchiyama T, Nikaidou N, Nonaka T, Sugiyama J, Watanabe T (2004) Importance of exposed aromatic residues in chitinase B from Serratia marcescens 2170 for crystalline chitin hydrolysis. J Biochem 136:163-168
150. Eijsink VGH, Vaaje-Kolstad G, Vårum KM, Horn SJ (2008) Towards new enzymes for biofuels: lessons from chitinase research. Trends Biotechnol 26:228-235
151. Horn SJ, Sikorski P, Cederkvist JB, Vaaje-Kolstad G, Sørlie M, Synstad B, Vriend G, Vårum KM, Eijsink VGH (2006) Costs and benefits of processivity in enzymatic degradation of recalcitrant polysaccharides. Proc Natl Acad Sci USA 103:18089-18094
152. Nimmich W, Zingler G (1984) Biochemical characteristics, phage patterns, and O1 factor analysis of Escherichia coli O1:K1:H7:F11 and O1:K1:H-:F9 strains isolated from patients with urinary tract infections. Med Microbiol Immunol 173:75-85
153. Rutishauser U, Watanabe M, Silver J, Troy FA, Vimr ER (1985) Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J Cell Biol 101:1842-1849
154. Leggate DR, Bryant JM, Redpath MB, Head D, Taylor PW, Luzio JP (2002) Expression, mutagenesis and kinetic analysis of recombinant K1E endosialidase to define the site of proteolytic processing and requirements for catalysis. Mol Microbiol 44:749-760
155. Pelkonen S, Häyrinen J, Finne J (1988) Polyacrylamide gel electrophoresis of the capsular polysaccharides of Escherichia coli K1 and other bacteria. J Bacteriol 170:2646-2653
156. Sato C, Inoue S, Matsuda T, Kitajima K (1998) Development of a highly sensitive chemical method for detecting alpha2->8-linked oligo/polysialic acid residues in glycoproteins blotted on the membrane. Anal Biochem 261:191-197
157. Liedtke S, Geyer H, Wuhrer M, Geyer R, Frank G, Gerardy-Schahn R, Zähringer U, Schachner M (2001) Characterization of N-glycans from mouse brain neural cell adhesion molecule. Glycobiology 11:373-384
158. Calandreau L, Márquez C, Bisaz R, Fantin M, Sandi C (2010) Differential impact of polysialyltransferase ST8SiaII and ST8SiaIV knockout on social interaction and aggression. Genes Brain Behav 9:958-967
159. Galuska SP, Geyer R, Gerardy-Schahn R, Mühlenhoff M, Geyer H (2008) Enzymedependent variations in the polysialylation of the neural cell adhesion molecule (NCAM) in vivo. J Biol Chem 283:17-28
160. Frosch M, Görgen I, Boulnois GJ, Timmis KN, Bitter-Suermann D (1985) NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc Natl Acad Sci USA 82:1194-1198
161. Brusés JL, Rutishauser U (2000) Polysialic acid in neural cell development: roles, regulation and mechanism. In: Fukuda M, Hindsgaul O (eds) Molecular and cellular glycobiology. Oxford University Press, New York, pp 116-132
162. Daston MM, Bastmeyer M, Rutishauser U, O'Leary DD (1996) Spatially restricted increase in polysialic acid enhances corticospinal axon branching related to target recognition and innervation. J Neurosci 16:5488-5497
163. Seki T, Rutishauser U (1998) Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J Neurosci 18:3757-3766
164. Becker CG, Artola A, Gerardy-Schahn R, Becker T, Welzl H, Schachner M (1996) The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation. J Neurosci Res 45:143-152
165. Dityatev A, Dityateva G, Schachner M (2000) Synaptic strength as a function of post- versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron 26:207-217
166. Aalto J, Pelkonen S, Kalimo H, Finne J (2001) Mutant bacteriophage with non-catalytic endosialidase binds to both bacterial and eukaryotic polysialic acid and can be used as probe for its detection. Glycoconj J 18:751-758
167. Durbec P, Cremer H (2001) Revisiting the function of PSA-NCAM in the nervous system. Mol Neurobiol 24:53-64
168. Jokilammi A, Ollikka P, Korja M, Jakobsson E, Loimaranta V, Haataja S, Hirvonen H, Finne J (2004) Construction of antibody mimics from a noncatalytic enzyme-detection of polysialic acid. J Immunol Methods 295:149-160
169. Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, Nikonenko I, Muller D, SchachnerM (2004) Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci 24:9372-9382
170. Weinhold B, Seidenfaden R, Röckle I, Mühlenhoff M, Schertzinger F, Conzelmann S, Marth JD, Gerardy-Schahn R, Hildebrandt H (2005) Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem 280:42971-42977
171. Burgess A, Weng YQ, Ypsilanti AR, Cui X, Caines G, Aubert I (2007) Polysialic acid limits septal neurite outgrowth on laminin. Brain Res 1144:52-58
172. Freiberger F, Claus H, Günzel A, Oltmann-Norden I, Vionnet J, Mühlenhoff M, Vogel U, Vann WF, Gerardy-Schahn R, Stummeyer K (2007) Bio-chemical characterization of a Neisseria meningitidis polysialyltransferase reveals novel functional motifs in bacterial sialyltransferases. Mol Microbiol 65:1258-1275
173. Oltmann-Norden I, Galuska SP, Hildebrandt H, Geyer R, Gerardy-Schahn R, Geyer H, Mühlenhoff M (2008) Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J Biol Chem 283:1463-1471
174. Hildebrandt H, Mühlenhoff M, Gerardy-Schahn R (2010) Polysialylation of NCAM. Adv Exp Med Biol 663:95-109
175. Kiss JZ, Wang C, Olive S, Rougon G, Lang J, Baetens D, Harry D, Pralong WF (1994) Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells. EMBO J 13:5284-5292
176. Garcia-Segura LM, Cañas B, Parducz A, Rougon G, Theodosis D, Naftolin F, Torres-Aleman I (1995) Estradiol promotion of changes in the morphology of astroglia growing in culture depends on the expression of polysialic acid of neural membranes. Glia 13:209-216
177. Wang C, Rougon G, Kiss JZ (1994) Requirement of polysialic acid for the migration of the O-2A glial progenitor cell from neurohypophyseal explants. J Neurosci 14:4446-4457
178. Meyer-Franke A, Shen S, Barres BA (1999) Astrocytes induce oligodendrocyte processes to align with and adhere to axons. Mol Cell Neurosci 14:385-397
179. Berski S, van Bergeijk J, Schwarzer D, Stark Y, Kasper C, Scheper T, Grothe C, Gerardy- Schahn R, Kirschning A, Dräger G (2008) Synthesis and biological evaluation of a polysialic acid-based hydrogel as enzymatically degradable scaffold material for tissue engineering. Biomacromolecules 9:2353-2359
180. Haile Y, Berski S, Dräger G, Nobre A, Stummeyer K, Gerardy-Schahn R, Grothe C (2008) The effect of modified polysialic acid based hydrogels on the adhesion and viability of primary neurons and glial cells. Biomaterials 29:1880-1891
181. Haastert-Talini K, Schaper-Rinkel J, Schmitte R, Bastian R, Mühlenhoff M, Schwarzer D, Draeger G, Su Y, Scheper T, Gerardy-Schahn R, Grothe C (2010) In vivo evaluation of polysialic acid as part of tissue-engineered nerve transplants. Tissue Eng Part A 16:3085-3098
182. Steinhaus S, Stark Y, Bruns S, Haile Y, Scheper T, Grothe C, Behrens P (2010) Polysialic acid immobilized on silanized glass surfaces: a test case for its use as a biomaterial for nerve regeneration. J Mater Sci Mater Med 21:1371-1378
183. Franz CK, Rutishauser U, Rafuse VF (2008) Intrinsic neuronal properties control selective targeting of regenerating motoneurons. Brain 131:1492-1505
184. James WM, Agnew WS (1987) Multiple oligosaccharide chains in the voltage-sensitive Na channel from electrophorus electricus: evidence for alpha-2,8-linked polysialic acid. Biochem Biophys Res Commun 148:817-826
185. Lanier LL, Testi R, Bindl J, Phillips JH (1989) Identity of Leu-19 (CD56) leukocyte differentiation antigen and neural cell adhesion molecule. J Exp Med 169:2233-2238
186. Avril T, North SJ, Haslam SM, Willison HJ, Crocker PR (2006) Probing the cis interactions of the inhibitory receptor Siglec-7 with alpha2,8-disialyated ligands on natural killer cells and other leukocytes using glycan-specific antibodies and by analysis of alpha2,8-sialytransferase gene expression. J Leukoc Biol 80:787-796
187. Rey-Gallardo A, Delgado-Martí C, Gerardy-Schahn R, Rodríguez-Fernández JL, Vega MA (2011) Polysialic acid is required for neuropilin2a/b-mediated control of CCL21-driven chemotaxis of mature dendritic cells and for their migration in vivo. Glycobiology 21:655-662
188. Rey-Gallardo A, Escribano C, Delgado-Martín C, Rodriguez-Fernández JL, Gerardy-Schahn R, Rutishauser U, Corbi AL, Vega MA (2010) Polysialylated neuropilin-2 enhances human dendritic cell migration through the basic C-terminal region of CCL21. Glycobiology 20:1139-1146
189. Hildebrandt H, Becker C, Mürau M, Gerardy-Schahn R, Rahmann H (1998) Heterogeneous expression of the polysialytransferases ST8Sia II and ST8Sia IV during postnatal rat brain development. J Neurochem 71:2339-2348
190. Lantuejoul S, Moro D, Michalides RJ, Brambilla C, Brambilla E (1998) Neural cell adhesion molecues (NCAM) and NCAM-PSA expression in neuroendocrine lung tumors. Am J Surg Pathol 22:1267-1276
191. Roth J, Zuber C, Wagner P, Taatjes DJ, Weisgerber C, Heitz PU, Goridis C, Bitter-Suermann D (1988) Reexpression of poly(sialic acid) units of the neural cell adhesion molecule in Wilms tumor. Proc Natl Acad Sci USA 85:2999-3003
192. Roesler J, Srivatsan E, Moetamed F, Peters J, Livingston EH (1997) Tumor suppressor activity of neural cell adhension molecule in colon carcinoma. Am J Surg 174:251-257
193. Tezel E, Kawase Y, Takeda S, Oshima K, Nakao A (2001) Expression of neural cell adhesion molecule in pancreatic cancer. Pancreas 22:122-125
194. Daniel L, Durbec P, Gautherot E, Rouvier E, Rougon G, Figarella-Branger D (2001) A nude mice model of human rhabdomyosarcoma lung metastases for evaluating the role of polysialic acids in the metastatic process. Oncogene 20:997-1004
195. Mushtaq N, Redpath MB, Luzio JP, Taylor PW (2005) Treatment of experimental Escherichia coli infection with recombinant bacteriophage-derived capsule depolymerase. J Antimicrob Chemother 56:160-165
196. Mushtaq N, Redpath MB, Jp L, Taylor PW (2004) Prevention and cure of systemic Escherichia coli K1 infection by modification of the bacterial phenotype. Antimicrob Agents Chemother 48:1503-1508
197. Pelkonen S (1990) Capsular sialyl chains of Escherichia coli K1 mutants resistant to K1 phage. Curr Microbiol 21:23-28
198. Colman PM, Hoyne PA, Lawrence MC (1993) Sequence and structure alignment of paramyxovirus hemagglutinin-neuraminidase with influenza virus neuraminidase. J Virol 67:2972-2980
199. Hoiczyk E, Roggenkamp A, Reichenbecher M, Lupas A, Heesemann J (2000) Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19:5989-5999
200. Pellequer JL, Van Regenmortel MH (1993) Affinity of monoclonal antibodies to large multivalent antigens: influence of steric hindrance on antibody affinity constants calculated from Scatchard plots. Mol Immunol 30:955-958
201. Häyrinen J, Haseley S, Talaga P, Mühlenhoff M, Finne J, Vliegenthart JFG (2002) High affinity binding of long-chain polysialic acid to antibody, and modulation by divalent cations and polyamines. Mol Immunol 39:399-411
202. Romano P, Manniello A, Aresu O, Armento M, Cesaro M, Parodi B (2009) Cell Line Data Base: structure and recent improvements towards molecular authentication of human cell lines. Nucleic Acids Res 37:D925-D932
203. Korja M, Jokilammi A, Salmi TT, Kalimo H, Pelliniemi TT, Isola J, Rantala I, Haapasalo H, Finne J (2009) Absence of polysialylated NCAM is an unfavorable prognostic phenotype for advanced stage neuroblastoma. BMC Cancer 9:57
204. Zelmer A, Bowen M, Jokilammi A, Finne J, Luzio JP, Taylor PW (2008) Differential expression of the polysialyl capsule during blood-to-brain transit of neuropathogenic Escherichia coli K1. Microbiology 154:2522-2532