Bacterial CMP-sialic acid synthetases: Production, properties, and applications

Applied Microbiology and Biotechnology

Volumn 80, Issue 5, 2008, Pages 757-765

  Mizanur, Rahman M ^a   Pohl, Nicola L ^b  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

CMP sialic acid synthetases; Sialic acid; Sugar nucleotide

Indexed keywords

ACIDS; ADHESION; BACTERIA; BACTERIOLOGY; BIOTECHNOLOGY; CARBOHYDRATES; CARBOXYLIC ACIDS; CATALYSTS; CELL ADHESION; CELLS; CYTOLOGY; ESCHERICHIA COLI; FOOD ADDITIVES; NANOTECHNOLOGY; PROTEINS; SUGAR (SUCROSE); SUGARS; TECHNOLOGY;

BACTERIAL SOURCES; BACTERIAL SPECIES; BIFUNCTIONAL; BIOLOGICAL FUNCTIONS; BIOTECHNOLOGICAL APPLICATIONS; CARBON SUGARS; CATALYTIC MECHANISMS; CATALYTIC PROPERTIES; CELL-CELL ADHESION; CHEMO-ENZYMATIC SYNTHESIS; CLOSTRIDIUM THERMOCELLUM; CMP-SIALIC ACID SYNTHETASES; CYTIDINE; DIVALENT CATIONS; DONOR MOLECULES; EUKARYOTIC CELLS; GLYCOCONJUGATES; GRAM-NEGATIVE BACTERIA; GROUP B STREPTOCOCCUS; INTRACELLULAR SIGNALLING; MONOPHOSPHATE; N-ACETYLNEURAMINIC ACID; NEISSERIA MENINGITIDIS; NON-PATHOGENIC BACTERIUM; SIALIC ACID; SIALIC ACIDS; SIALYL TRANSFERASES; SUGAR NUCLEOTIDE; SYNTHETASE; SYNTHETASES; VIRULENCE FACTORS;

ENZYMES;

CYTIDINE PHOSPHATE; DIVALENT CATION; HYDROLASE; NUCLEOTIDYLTRANSFERASE; SIALIC ACID;

BACTERIUM; BIOTECHNOLOGY; CYTOLOGY; ENZYME ACTIVITY; PROTEIN; SUGAR;

BIOSYNTHESIS; BIOTECHNOLOGY; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CATALYSIS; CLOSTRIDIUM THERMOCELLUM; ENZYME ACTIVITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HAEMOPHILUS DUCREYI; MANNHEIMIA HAEMOLYTICA; MOLECULAR WEIGHT; NEISSERIA MENINGITIDIS; PH; PROTEIN FUNCTION; SHORT SURVEY; TEMPERATURE;

BACTERIA; BACTERIAL PROTEINS; INDUSTRIAL MICROBIOLOGY; KINETICS; N-ACETYLNEURAMINIC ACID; N-ACYLNEURAMINATE CYTIDYLYLTRANSFERASE;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM THERMOCELLUM; ESCHERICHIA COLI; EUKARYOTA; HAEMOPHILUS DUCREYI; MANNHEIMIA HAEMOLYTICA; NEGIBACTERIA; NEISSERIA MENINGITIDIS; POSIBACTERIA; PROKARYOTA; STREPTOCOCCUS SP. 'GROUP B';

EID: 51849119565     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-008-1643-7     Document Type: Short Survey

References (78)

1. C Adlam JM Knight A Mugridge JM Williams JC Lindon 1987 Production of colominic acid by Pasteurella haemolytica serotype A2 organisms FEBS Microbiol Lett 42 23 25
2. MG Ambrose SJ Freese MS Reinhold TG Warner WF Vann 1992 Carbon-13 NMR investigation of the anomeric specificity of CMP-N-acetylneuraminic acid synthetase from Escherichia coli Biochemistry 31 775 780
3. T Angata A Varki 2002 Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective Chem Rev 102 439 469
4. GT Barry 1959 Detection of sialic acid in various E. coli strains and other species of bacteria Nature 183 117 118
5. Bitter-Suermann D (1993) In: Roth J, Rutishauser U, Troy FA II (eds) Polysialic acid: from microbes to man. Birkhauser, Basel, pp 11-24
6. IG Bravo S Barrallo MA Ferrero LB Rodriguez-Aparicio H Martinez-Blanco A Reglero 2001 Kinetic properties of the acylneuraminate cytidylyltransferase from Pasteurella haemolytica A2 Biochem J 358 585 598
7. IG Bravo S Garcia-Vallve A Romeu A Reglero 2004 Prokaryotic origin of cytidylyltransferases and alpha-ketoacid synthases Trends Microbiol 12 120 127
8. JL Bruses U Rutishauser 2001 Roles, regulation, and mechanism of polysialic acid function during neural development Biochimie 83 635 643
9. AA Campagnari SM Spinola AJ Lesse YA Kwaik RE Mandrell MA Apicella 1990 Lipooligosaccharide epitopes shared among Gram negative non-enteric mucosal pathogens Microb Pathog 8 353 362
10. S-K Cha B Ortega H Kurosu KP Rosenblatt M Kouro-o C-L Huang 2008 Removal of sialic acid involving Klotho causes cell-surface retention of TRPV5 channel via binding to galectin-1 Proc Natl Acad Sci 105 9805 9810
11. HA Chokhawala H Cao X Chen 2007 Enzymatic synthesis of fluorinated probes for sialidases and sialyltransferases J Am Chem Soc 129 10630 10631
12. HA Chokhawala H Yu X Chen 2007 High-throughput substrate specificity studies of sialidases by using chemoenzymatically synthesized sialoside libraries ChemBioChem 8 194 201
13. N Choudhry M Bajaj-Elliott V McDonald 2008 The terminal sialic acid of glycoconjugates on the surface of intestinal epithelial cells activates excystation of Cryptosporidium parvum Infect Immun 76 3735 3741
14. DG Comb F Shimizu S Roseman 1959 Isolation of cytidine-5′- monophosphate-N-acetylneuraminic acid J Am Chem Soc 81 5513 5514
15. DG Comb DR Watson S Roseman 1966 The sialic acids IX. Isolation of cytidine 5′-monophospho-N-acetylneuraminic acid from E. coli K-235 J Biol Chem 241 5637 5642
16. PR Crocker 2002 Siglecs: sialic-acid-binding immunoglobulin-like lectins in cell-cell interactions and signaling Curr Opin Struc Biol 12 609 615
17. L Daniel J Trouillas W Renaud P Chevallier J Gouvernet G Rougon D Figarella-Branger 2000 Polysialylated-neural cell adhesion molecule expression in rat pituitary transplantable tumors (spontaneous mammotropic transplantable tumor in wistar-furth rats) is related to growth rate and malignancy Cancer Res 60 80 85
18. U Edwards M Frosch 1992 Sequence and functional analysis of the cloned Neisseria meningitidis CMP-NeuAc synthetase FEMS Microbiol Lett 96 161 166
19. C Elkins NH Carbonetti VA Varela D Stirewalt DG Klapper PF Sparling 1992 Antibodies to N-terminal peptides of gonococcal porin are bactericidal when gonococcal lipopolysaccharide is not sialylated Mol Microbiol 6 2617 2628
20. S Ganguli G Zapata T Wallis C Reid G Boulnois WF Vann IS Roberts 1994 Molecular cloning and analysis of genes for sialic acid synthesis in Neisseria meningitidis group B and purification of the meningococcal CMP-NeuNAc synthetase enzyme J Bacteriol 176 4583 4589
21. M Gilbert DC Watson WW Wakarchuck 1997 Purification and characterization of the recombinant CMP-sialic acid synthetase from Neisseria meningitidis Biotechnol Lett 19 417 420
22. M Gilbert R Bayer AM Cunningham S DeFrees Y Gao DC Watson NM Young WW Wakarchuk 1998 The synthesis of sialylated oligosaccharides using a CMP-Neu5Ac synthetase/sialyltransferase fusion Nat Biotechnol 16 769 772
23. RF Haft MR Wessels 1994 Characterization of CMP-N-acetylneuraminic acid synthetase of group B streptococci J Bacteriol 176 7372 7374
24. RF Haft MR Wessels MF Mebane N Conaty CE Rubens 1996 Characterization of cpsF and its product CMP-N-acetylneuraminic acid synthetase, a group B streptococcal enzyme that can function in K1 capsular polysaccharide biosynthesis in Escherichia coli Mol Microbiol 19 555 563
25. T Hamamoto S Takeda T Noguchi 2005 Enzymatic synthesis of cytidine 5′-monophospho-N-acteylneuraminic acid Biosci Biotechnol Biochem 69 1944 1950
26. M Hedlund P Tangvoranuntakul H Takematsu JM Long GD Housley Y Kozutsumi A Suzuki A Wynshaw-Boris AF Ryan RL Gallo N Varki A Varki 2007 N-glycolylneuraminic acid deficiency in mice: implications for human biology and evolution Mol Cell Biol 27 4340 4346
27. Hidari KI, Murata T, Yoshida K, Takahashi Y, Minamijima YH, Miwa Y, Adachi S, Ogata M, Usui T, Suzuki Y, Suzuki T (2008) Chemoenzymatic synthesis, characterization, and application of glycopolymers carrying lactosamine repeats as entry inhibitors against influenza virus infection. Glycobiology. doi: 10.1093/glycob/cwn067
28. K Ishige T Hamamoto T Shiba T Noguchi 2001 Novel method for enzymatic synthesis of CMP-NeuAc Biosci Biotech Biochem 65 1736 1740
29. Jann K, Jann B (1985) Cell surface components and virulence: Escherichia coli O and K antigens in relation to virulence and pathogenicity. In: Sussman M (ed) The virulence of Escherichia coli: reviews and methods. Academic, Orlando, FL, pp 157-176
30. M-F Karwaski WW Wakarchuk M Gilbert 2002 High-level expression of recombinant Neisseria CMP-sialic acid synthetase in Escherichia coli Protein Expr Purif 25 237 240
31. EL Kean 1991 Sialic acid activation Glycobiology 1 441 447
32. JZ Kiss D Muller 2001 Contribution of the neural cell adhesion molecule to neuronal and synaptic plasticity Rev Neurosci 12 297 310
33. M Kittelmann T Klein U Kragl C Wandrey O Ghisalba 1995 CMP-N-acetyl neuraminic acid synthetase from Escherichia coli: fermentation production and application for the preparative synthesis of CMP-neuraminic acid Appl Microbiol Biotechnol 44 59 67
34. M Knorst W-D Fessner 2001 CMP-sialate synthetase from Neisseria meningitidis-overexpression and application to the synthesis of oligosaccharides containing modified sialic acids Adv Synth Catal 343 698 710
35. AL Lewis H Cao SK Patel S Diaz W Ryan AF Carlin V Thon WG Lewis A Varki X Chen V Nizet 2007 NeuA sialic acid O-acetylesterase activity modulates O-acetylation of capsular polysaccharide in group B Streptococcus J Biol Chem 282 27562 27571
36. JL-C Liu C-J Shen Y Ichikawa JF Rutan C Zapata WF Vann C-H Wong 1992 Overproduction of CMP-sialic acid synthetase for organic synthesis J Am Chem Soc 114 3901 3910
37. G Liu C Jin C Jin 2004 CMP-N-acetylneuraminic acid synthetase from Escherichia coli K1 is a bifunctional enzyme. Identification of minimal catalytic domain for the synthetase activity and novel functional domain for platelet-activating factor acetylhydrolase activity J Biol Chem 279 17738 17749
38. Louwen R, Heikema A, van Belkum A, Ott A, Gilbert M, Ang W, Endtz H, Bergman MP, Nieuwenhuis EE (2008) The sialylated lipo-oligosaccharide outer core of Campylobacter jejuni is an important determinant for epithelial cell invasion. Infect Immun. doi: 10.1128/IAI.00321-08
39. RE Mandrell MA Apicella 1993 Lipo-oligosaccharides (LOS) of mucosal pathogens: molecular mimicry and host-modification of LOS Immunobiology 187 382 402
40. J Martinez S Steenbergen E Vimr 1995 Derived structure of the putative sialic acid transporter from Escherichia coli predicts a novel sugar permease domain J Bacteriol 177 6005 6010
41. L Masson BE Holbein 1983 Physiology of sialic acid capsular polysaccharide synthesis in serogroup B of N. meningitidis J Bacteriol 54 728 736
42. EJ McGuire SB Binkley 1964 The structure and chemistry of colominic acid Biochemistry 3 247 251
43. W Melaugh BW Gibson AA Campagnari 1996 The lipooligosaccharides of Haemophilus ducreyi are highly sialylated J Bacteriol 178 564 570
44. W Melaugh NJ Phillips AA Campagnari MV Tullius BW Gibson 1994 Structure of the major oligosaccharide from the lipooligosaccharide of Haemophilus ducreyi strain 35000 and evidence for additional glycoforms Biochemistry 33 13070 13078
45. RM Mizanur NL Pohl 2007 Cloning and characterization of a heat-stable CMP-N-acylneuraminic acid synthetase from Clostridium thermocellum Appl Microbiol Biotechnol 76 827 834
46. SC Mosimann M Gilbert D Dombroswki R To W Wakarchuk NCJ Strynadka 2001 Structure of a sialic acid-activating synthetase, CMP-acylneuraminate synthetase in the presence and absence of CDP J Biol Chem 276 8190 8196
47. AK Munster-Kuhnel J Tiralongo S Krapp B Weinhold V Ritz-Sedlacek U Jacob R Gererdy-Schahn 2004 Structure and function of vertebrate CMP-sialic acid synthetases Glycobiology 14 43R 51R
48. S Muthana H Yu S Huang X Chen 2007 Chemoenzymatic synthesis of size-defined polysaccharides by sialyltransferase-catalyzed block transfer of oligosaccharides J Am Chem Soc 129 11918 11919
49. J Nahalka B Wu J Shao P Gemeiner PG Wang 2004 Production of cytidine 5′-monophospho-β-D-neuraminic acid (CMP-sialic acid) using enzymes or whole cells entrapped in calcium pectate-silica-gel beads Biotechnol Appl Biochem 40 101 106
50. NJ Parsons PV Patel EL Tan JR Andrade CA Nairn M Goldner JA Cole H Smith 1988 Cytidine 5′-monophospho-N-acetyl neuraminic acid and a low molecular weight factor from human blood cells induce lipopolysaccharide alteration in gonococci when conferring resistance to killing by human serum Microb Pathog 5 303 309
51. J Plumbridge E Vimr 1999 Convergent pathways for utilization of the amino sugars N-acetylglucosamine, N-acetylmannosamine, and N-acetylneuraminic acid by Escherichia coli J Bacteriol 181 47 54
52. J Rauvolfova A Venot G-J Boons 2008 Chemo-enzymatic synthesis of C-9 acetylated sialosides Carbohydr Res 343 1605 1611
53. RF Rest JV Frangipane 1992 Growth of Neisseria gonorrhoeae in CMP-N-acetylneuraminic acid inhibits non opsonic (opacity-associated outer membrane protein mediated) interactions with human neutrophils Infect Immun 60 989 997
54. MA Ringenberg SM Steenbergen ER Vimr 2003 The first committed step in the biosynthesis of sialic acid by Escherichia coli K1 does not involve a phosphorylated N-acetylmannosamine intermediate Mol Microbiol 50 961 975
55. NM Samuels BW Gibson SM Miller 1999 Investigation of the kinetic mechanism of cytidine 5′monophosphate N-acetylneuraminic acid synthetase from Haemophilus ducrey with new insights on rate limiting steps from product inhibition analysis Biochemistry 38 6195 6203
56. R Schauer 1985 Sialic acids and their role as biological masks Trends Biochem Sci 10 357 360
57. R Schauer 2000 Achievements and challenges of sialic acid research Glycoconj J 17 485 499
58. M Schwarzkopf K-P Knobeloch E Rohde S Hinderlich N Wiechens L Lucka I Horak W Reutter RD Horstkorte 2002 Sialylation is essential for early development in mice Proc Nat Acad Sci 99 5267 5270
59. SL Shames ES Simon CW Christopher W Schmid GM Whitesides LL Yang 1991 CMP-N-acetylneuraminic acid synthetase of Escherichia coli: high level expression, purification and use in the enzymatic synthesis of CMP-N-acetylneuraminic acid and CMP-neuraminic acid derivatives Glycobiology 1 187 191
60. DM Stoughton G Zapata R Picone WF Vann 1999 Identification of Arg-12 in the active site of Escherichia coli K1 CMP-sialic acid synthetase Biochem J 343 397 402
61. KN Timmis GJ Boulnois D Bitter-Suermann FC Cabello 1985 Surface components of Escherichia coli that mediate resistance to the bactericidal activities of serum and phagocytes Curr Top Microbiol Immunol 118 197 218
62. C Traving R Schauer 1998 Structure, function and metabolism of sialic acids Cell Mol Life Sci 54 330 1349
63. MV Tullius RS Munson Jr J Wang BW Gibson 1996 Purification, cloning, and expression of a cytidine 5′-monophosphate N-acetylneuraminic acid synthetase from Haemophilus ducreyi J Biol Chem 271 15373 15380
64. MV Tullius WF Vann BW Gibson 1999 Covalent modification of Lys19 in the CTP binding site of cytidine 5′-monophosphate N-acetylneuraminic acid synthetase Prot Sci 8 666 675
65. WF Vann RP Silver C Abeijon K Chang W Aaronson A Sutton CW Finn W Lindner M Kotsatos 1987 Purification, properties, and genetic location of Escherichia coli cytidine 5′-monophosphate N-acetylneuraminic acid synthetase J Biol Chem 262 17556 17562
66. A Varki 1993 Biological roles of oligosaccharides: all of the theories are correct Glycobiology 3 97 130
67. A Varki 2007 Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins Nature 446 1023 1029
68. E Vimr L Lichtensteiger 2002 To sialylate, or not to sialylate: that is the question Trends Microbiol 10 254 257
69. ER Vimr FA Troy 1985 Identification of an inducible catabolic system for sialic acids (Nan) in Escherichia coli J Bacteriol 164 845 853
70. E Vimr C Lichtensteiger S Steenbergen 2000 Sialic acid metabolism's dual function in Haemophilus influenzae Mol Microbiol 36 1113 1123
71. L Warren RS Blacklow 1962 The biosynthesis of cytidine 5′-monophospho-N-acetylneuraminic acid by an enzyme from Neisseria meningitidis J Biol Chem 237 3527 3534
72. G Xia X Han H Ding S Yang S Zhang C Jin 2000 Cloning and over expression of a cytidine 5′-monophosphate N-acetylneuraminic acid synthetase from Escherichia coli J Mol Catal B Enzym 10 199 206
73. H Yu H Yu R Karpel X Chen 2004 Chemoenzymatic synthesis of CMP-sialic acid derivatives by a one-pot two-enzyme system: comparison of substrate flexibility of three microbial CMP-sialic acid synthetases Bioorg Med Chem 12 6427 6435
74. H Yu H Chokhawala R Karpel H Yu B Wu J Zhang Y Zhang Q Jia X Chen 2005 A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries J Am Chem Soc 127 17618 17619
75. H Yu HA Chokhawala S Huang X Chen 2006 One-pot three-enzyme chemoenzymatic approach to the synthesis of sialosides containing natural and non-natural functionalities Nat Protoc 5 2485 2492
76. H Yu S Huang H Chokhawala M Sun H Zheng X Chen 2006 Highly efficient chemoenzymatic synthesis of naturally occurring and non-natural a-2,6-linked sialosides: a P. damsella a-2,6-sialyltransferase with extremely flexible donor-substrate specificity Angew Chem Int Ed 45 3938 3944
77. H Yu W Ryan H Yu X Chen 2006 Characterization of a bifunctional cytidine 5′-monophosphate N-acetylneuraminic acid synthetase cloned from Streptococcus agalactiae Biotechnol Lett 28 107 113
78. Yu C-C, Lin P-C, Lin C-C (2008) Site-specific immobilization of CMP-sialic acid synthetase on magnetic nanoparticles and its use in the synthesis of CMP-sialic acid. Chem Commun (11):1308-1310