Terminal glycosylation in cystic fibrosis (CF): A review emphasizing the airway epithelial cell

Glycoconjugate Journal

Volumn 18, Issue 9, 2001, Pages 649-659

  Rhim, Andrew D ^a   Stoykova, Lydia ^a   Glick, Mary Catherine ^a   Scanlin, Thomas F ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Airway epithelial cells; CFTR; CFTR transfection; Cystic fibrosis; Fucose; Glycosylation; Sialic acid

Indexed keywords

GLYCOCONJUGATE; GLYCOPROTEIN; LIGAND; OLIGOSACCHARIDE; SELECTIN; TRANSMEMBRANE CONDUCTANCE REGULATOR; CFTR PROTEIN, HUMAN; FUCOSE; FUCOSYLTRANSFERASE; SIALYLTRANSFERASE;

AMINO ACID SEQUENCE; BACTERIAL INFECTION; CELL SURFACE; CYSTIC FIBROSIS; DNA MODIFICATION; EPITHELIUM CELL; FUCOSYLATION; GENE THERAPY; GLYCOSYLATION; HAEMOPHILUS INFLUENZAE; HUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA; RESPIRATORY EPITHELIUM; REVIEW; SIALYLATION; ANIMAL; CARBOHYDRATE ANALYSIS; GENETICS; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; RESPIRATORY SYSTEM; TRANS GOLGI NETWORK;

ANIMALS; CARBOHYDRATE SEQUENCE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; FUCOSE; FUCOSYLTRANSFERASES; GLYCOSYLATION; HAEMOPHILUS INFLUENZAE; HUMANS; MOLECULAR SEQUENCE DATA; PHENOTYPE; PSEUDOMONAS AERUGINOSA; RESPIRATORY SYSTEM; SIALYLTRANSFERASES; TRANS-GOLGI NETWORK;

EID: 0035470158     PISSN: 02820080     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1020815205022     Document Type: Review

References (97)

1. Riordan JR, Rommens JM, Kerem B, Alon M, Rozmahel R, Grzelczak Z, Zielinski J, Lok S, Plavsic N, Chou JL, Drumm ML, Iannuzzi MC, Collins FS, Tsui LC, Identification of cystic fibrosis gene: Cloning and characterization of the complementary DNA, Science 245, 1066-73 (1989).
2. Robinson C, Scanlin TF, Cystic fibrosis. In Pulmonary Diseases and Disorders, edited by Fishman AP (McGraw-Hill, New York, 1997), pp. 1273-94.
3. Scanlin TF, Glick MC, Terminal glycosylation in cystic fibrosis, Biochim Biophys Acta 1455, 241-53 (1999).
4. Rhim AD, Kothari VA, Park PJ, Mulberg AE, Glick MC, Scanlin TF, Terminal glycosylation of cystic fibrosis airway epithelial cells, Glycoconjugate J 17, 385-91 (2000).
5. Dische Z, di Sant'Agnese P, Pallavicini C, Youlos J, Composition of mucoprotein fractions from duodenal fluid of patients with cystic fibrosis of the pancreas and from controls, Pediatrics 24, 74-91 (1959).
6. Lamblin G, et al., Human airway mucin glycosylation: A combinatory of carbohydrate determinates which vary in cystic fibrosis, Glycoconjugate J 18, 661-84 (2001).
7. Delmotte P, Degroote S, Lafitte JJ, Lamblin G, Perini JM, Roussel P, Tumor necrosis factor alpha increases the expression of glycosyltransferases and sulfotransferases responsible for the biosynthesis of sialylated and/or sulfated Lewis x epitopes in the human bronchial mucosa, J Biol Chem 277, 424-31 (2002).
8. Scanlin TF, Cystic fibrosis: Current trends in research, Clin Chest Med 1, 423-7 (1980).
9. Scanlin TF, Voynow JA, Thomas EJ, Glick MC, Glycoproteins in culture medium: A comparison from cystic fibrosis and control skin fibroblasts, Biochemistry 21, 491-7 (1982).
10. Scanlin TF, Wang MY, Glick MC, Altered fucosylation of membrane glycoproteins from cystic fibrosis fibroblasts, Pediatr Res 19, 368-74 (1985).
11. Wang YM, Hare TR, Won B, Stowell CP, Scanlin TF, Glick MC, Hard K, Van Kuik JA, Vliegenthart JFG, Additional fucosyl residues on membrane glycoproteins but not a secreted glycoprotein from cystic fibrosis fibroblasts, Clin Chim Acta 188, 193-210 (1990).
12. Jetten AM, Yankaskas JR, Stutts MJ, Willumsen NJ, Boucher RC, Persistance of abnormal chloride conductance regulation in transformed cystic fibrosis epithelia, Science 244, 1472-5 (1989).
13. Olsen JC, Johnson LG, Stutts MJ, Sarkadi B, Yankaskas JR, Swanstron R, Boucher RC, Correction of the apical membrane chloride permeability defect in polarized cystic fibrosis airway epithelia following retroviral-mediated gene transfer, Hum Gene Ther 3, 253-66 (1992).
14. Zeitlin PL, Lu L, Rhim J, Cutting G, Stetten G, Kieffer KA, Craig R, Guggino WB, A cystic fibrosis bronchial epithelial cell line: Immortalization by adeno-12-SV40 infection, Am J Respir Cell Mol Biol 4, 313-9 (1991).
15. Reddell RR, Ke Y, Gerwin BL, McMenamin MG, Lechner JF, Su RT, Brash DE, Park J-B, Rhim JS, Harris CC, Transformation of human bronchial epithelial cells by infection with SV-40 or adenovirus-12 SV40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes, Cancer Res 48, 1904-9 (1988).
16. Lazatin JO, Glick MC, Scanlin TF, Fucosylation in cystic fibrosis airway epithelial cells, Glycosylation Dis 1, 263-70 (1994).
17. Glick MC, Kothari VA, Liu A, Stoykova LI, Scanlin TF, Activity of fucosyltransferases and altered glycosylation in cystic fibrosis airway epithelial cells, Biochimie 83, 743-7 (2001).
18. Barasch J, Kiss B, Prince A, Saiman L, Gruenert D, Al-Awqati Q, Defective acidification of intracellular organelles in cystic fibrosis, Nature 352, 70-3 (1991).
19. Saiman L, Prince A, Pseudomonas aeruginosa pill bind to asialoGM1 which is increased on the surface of cystic fibrosis epithelial cells, J Clin Invest 92, 1875-80 (1993).
20. Hazen-Martin DJ, Sens DA, Spicer SS, Glycoconjugates in sweat glands and other structures of skin from normal and cystic fibrosis subjects, Am J Dermatopathol 8, 478-91 (1986).
21. Hassid S, Choufani G, Decaestecker C, Delbrouck C, Dawance S, Pelc P, Nagy N, Kaltner H, Salmon I, Danguy A, Gabius HJ, Kiss R, Glycohistochemical characteristics of nasal polyps from patients with and without cystic fibrosis, Arch Otolaryngol Head Neck Surg 126, 769-76 (2000).
22. Sharon N, Lis H, Lectins (Chapman and Hall, New York, 1989), pp. 1-5.
23. Warren L, The thiobarbituric acid assay of sialic acids, J Biol Chem 234, 1971-5 (1959).
24. Klink DT, Glick MC, Scanlin TF, Gene therapy of cystic fibrosis (CF) airways: A review emphasizing targeting with lactose, Glycoconjugate J 18, 731-40 (2001).
25. Dosanjh A, Lencer W, Brown D, Ausiello DA, Stow JL, Heterologous expression of ΔF508 CFTR results in decreased sialylation of membrane glycoconjugates, Am J Physiol 266, C360-6 (1994).
26. Kube D, Adams L, Perez A, Davis PB, Terminal sialylation is altered in airway cells with impaired CFTR-mediated chloride transport, Am J Physiol Lung Cell Mol Physiol 280, L482-92 (2001).
27. Imundo L, Barasch J, Prince A, Al-Awqati Q, Cystic fibrosis epithelial cells have a receptor for pathogenic bacteria on their apical surface, Proc Natl Acad Sci USA 92, 3019-23 (1995).
28. Jiang X, Hill WG, Pilewski JM, Weisz OA, Glycosylation differences between a cystic fibrosis and rescued airway cell line are not CFTR dependent, Am J Physiol Lung Cell Mol Physiol 273, L913-20 (1997).
29. Poschet JF, Boucher JC, Tatterson L, Skidmore J, Van Dyke RW, Deretic V, Molecular basis for defective glycosylation and pseudomonas pathogenesis in cystic fibrosis lung, Proc Natl Acad Sci USA 98, 13972-7 (2001).
30. Schwiebert EM, Egan ME, Hwang TH, Fulmer SB, Allen SS, Cutting GR, Guggino WB, CFTR regulates outwardly rectifying chloride channels through an autocrine mechanism involving ATP, Cell 81, 1063-73 (1995).
31. Kunzelmann K, CFTR: Interacting with everything?, News Physiol Sci 16, 167-70 (2001).
32. Guggino WB, Cystic fibrosis salt/fluid controversy: In the thick of it, Nature Medicine 7, 888-90 (2001).
33. Bradbury NA, Intracellular CFTR: Localization function, Physiol Rev 79, S175-91 (1999).
34. Pasyk EA, Foskett JK, Mutant (ΔF508) cystic fibrosis transmembrane regulator CI- channel is functional when retained in endoplasmic reticulum of mammalian cells, J Biol Chem 270, 12347-50 (1995).
35. Bradbury NA, Cohn JA, Venglarik CJ, Bridges RJ, Biochemical and biophysical identification of cystic fibrosis transmembrane regulator chloride channels as components of endocytic clathrincoated vesicles, J Biol Chem 269, 8296-302 (1994).
36. Scanlin TF, Glick MC, Terminal glycosylation and disease: Influence on cancer and cystic fibrosis, Glycoconjugate J 17, 617-26 (2000).
37. Welsh MJ, Smith AE, Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis, Cell 73, 1251-4 (1993).
38. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, White GA, O'Riordan CR, Smith AE, Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis, Cell 63, 827-34 (1990).
39. Bannykh SI, Bannykh GI, Fish KN, Moyer BD, Riordan JR, Balch WE, Traffic pattern of cystic fibrosis transmembrane regulator through the early exocytic pathway, Traffic 1, 852-70 (2000).
40. Cheng SH, Fang SL, Zabner J, Marshall J, Piraino S, Schiavi SC, Jefferson DM, Welsh MJ, Smith AE, Functional activation of the cystic fibrosis trafficking mutant ΔF508-CFTR by overexpression, Am J Physiol 268, L615-24 (1995).
41. Duthel S, Revol A, Glycan microheterogeneity of α 1 -antitripsin in serum and meconium from normal and cystic fibrosis patients by crossed immuno-affinoelectrophoresis with different lectins (Con A, LCA, WGA), Clin Chim Acta 215, 173-87 (1993).
42. Lukacs GL, Chang X-B, Kartner N, Rotstein OD, Riordan JR, Grinstein S, The cystic fibrosis transmembrane regulator is present and functional in endosomes, J Biol Chem 267, 14568-72 (1994).
43. Chen EY, Bartlett MC, Clarke DM, Cystic fibrosis transmembrane conductance regulator has an altered structure when its mutation is inhibited, Biochemistry-USA 39, 3797-803 (2000).
44. Kopito RR, Biosynthesis degradation of CFTR, Physiol Rev 79, S167-73 (1999).
45. Scanlin TF, Glick MC, Glycosylation and the cystic fibrosis transmembrane conductance regulator, Respir Res 2, 276-9 (2001).
46. Wei X, Eisman R, Xu J, Harsch AD, Mulberg AE, Bevins CL, Glick MC, Scanlin TF, Turnover of the cystic fibrosis transmembrane conductance regulator (CFTR): Slow degradation of wild-type and ΔF508 CFTR in surface membrane preparations of immortalized airway epithelial cells, J Cell Physiol 168, 373-84 (1996).
47. Bebok Z, Mazzochi C, King SA, Hong JS, Sorscher EJ, The mechanism underlying cystic fibrosis transmembrane conductance regulator transport from the endoplasmic reticulum to the proteasome includes sec 61b and a cytosolic deglycosylated intermediary, J Biol Chem 6, 29873-8 (1998).
48. O'Riordan CR, Lachapelle Al, Marshall J, Higgins EA, Cheng AH, Characterization of the oligosaccharide structures associated with cystic fibrosis transmembrane conductance regulator, Glycobiology 17, 1225-33 (2000).
49. Casey JR, Pirraglia CA, Reithmeier RA, Enzymatic deglycosylation of human band 3, the anion transport protein of the erythrocyte membrane. Effect on protein structure and transport properties, J Biol Chem 267, 11940-8 (1992).
50. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, Welsh MJ, Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature sensitive, Nature 358, 761-4 (1992).
51. Seksek O, Biwersi J, Verkman AS, Evidence against defective trans-Golgi acidification in cystic fibrosis, J Biol Chem 271, 15542-8 (1996).
52. Gibson GA, Warren GH, Weisz OA, Evidence against the acidification hypothesis in cystic fibrosis, Am J Physiol Cell Physiol 279, C1088-99 (2000).
53. Schwiebert EM, Benos DJ, Egan ME, Stutts MJ, Guggino WB, CFTR is a conductance regulator as well as a chloride channel, Physiol Rev 79, S145-66 (1999).
54. Allan BB, Balch WE, Protein sorting by directed maturation of golgi compartments, Science 285, 63-6 (1999).
55. Weiss M, Nilsson T, Hypothesis. Protein sorting in the Golgi apparatus: A consequence of maturation and triggered sorting, FEBS Lett 486, 2-9 (2000).
56. Rozmahel R, Nguyen V, Corey M, Haston CK, Kent G, Bear C, Durie P, Tsui L-C, Modulation of disease severity in cystic fibrosis transmembrane conductance regulator deficient mice by a secondary genetic factor, Nature Genetics 12, 280-7 (1996).
57. Bronsveld I, Mekus F, Bijman J, Ballmann M, de Jonge HR, Laabs U, Halley DJ, Ellemunter H, Mastella G, Thomas S, Veeze HJ, Tummler B, Chloride conductance and genetic background modulate the cystic fibrosis phenotype of Delta F508 homozygous twins and siblings, J Clin Inv 108, 1705-15 (2001).
58. Freeze HH, Disorders in protein glycosylation and potential therapy: Tip of an iceberg?, J Pediatrics 133, 593-600 (1998).
59. Adam EC, Mitchel BS, Schumacher DU, Grant G, Schumacher U, Pseudomonas aeroginosa II lectin stops human ciliary beating: Therapeutic implications of fucose, Am J Respir Crit Care Med 55, 2102-4 (1997).
60. Cohen JC, Morrow SL, Cork RJ, Delcarpio JB, Larson JE, Molecular pathophysiology of cystic fibrosis based on the rescued knockout mouse model, Mol Genet Metab 64, 108-18 (1998).
61. Kube D, Perez A, Davis PB, Quantitative fluorescent microscopy reveals altered cell surface glycoconjugated on 9HTEo-cells transfected with the regulatory domain of CFTR or ΔF508 CFTR, Pediatr Pulmonol 12, 209A (1995).
62. Scanlin TF, Liu A, Park PJ, Rhim AD, Kothari V, Weiser JN, Glick MC, Fucosylation and sialylation of cystic fibrosis (CF) airway epithelial cells, Glycobiology 8, 150 (1998).
63. Bryan R, Kube D, Davis P, Prince A, Overproduction of the CFTR R domain leads to increased levels of asialoGM1 and increased Pseudomonas aeroginosa binding by epithelial cells, Am J Respir Cell Mol Biol 19, 269-77 (1998).
64. Oriol R, Mollicone R, α2-Fucosyltransferases (FUT1, FUT2, and Sec 1). In Handbook of Glycosyltransferases and Related Genes, edited by Taniguchi N, Honke K, Fukuda M (Springer-Verlag, Tokyo, 2002), p. 205.
65. De Vries T, Srnka CA, Palcic MM, Swiedler SJ, van den Eijnden DH, Macher BA, Acceptor specificity of different length constructs of human recombinant α 1,3/4-fucosyltransferases. Replacement of the stem region and the transmembrane domain of fucosyltransferase V by protein A results in an enzyme with GDP-fucose hydrolysing activity, J Biol Chem 270, 712-22 (1995).
66. Mollicone R, Gibaud A, Francois A, Ratcliffe M, Oriol R, Acceptor specificity and tissue distribution of three human α-3-fucosyltransferases, Eur J Biochem 191, 169-76 (1990).
67. Holmes E, Xu Z, Sherwood AL, Macher BA, Structure-function analysis of human α1,3 fucosyltransferases. A GDP-fucose-protected, N-ethylmaleimide-sensistive site in Fuc-III and Fuc-TV corresponds to Ser 178 in Fuc-TIV, J Biol Chem 270, B145-51 (1995).
68. Sasaki K, Kurata K, Funayama K, Nagata M, Watanabe E, Ohta S, Hanai N, Nishi T, Expression cloning of a novel alpha 1,3-fucosyltransferase that is involved in biosynthesis of the sialyl Lewis X carbohydrate determinants in leukocytes, J Biol Chem 269, 14730-7 (1994).
69. Natsuka S, Gersten KM, Zenita K, Kannagi R, Lowe JB, Molecular cloning of a cDNA encoding a novel human leukocyte alpha 1,3-fucosyltransferase capable of synthesizing the sialyl Lewis X determinant, J Biol Chem 269, 16789-94 (1994).
70. Wilson JR WD, Schachter H, The control of glycoprotein synthesis: N-acetyl glucosamine linkage to α-mannose residue as a signal of L-fucose to the asparagine linked N-acetylglucosamine residue of glycopeptide from α 1-acid glycoprotein, Biochem Biophys Res Commun 72, 909-16 (1976).
71. Voynow JA, Kaiser RS, Scanlin TF, Glick MC, Purification and characterization of GDP L-Fuc: N-acetyl-β-D-glucosamine α 1-6-fucosyltransferase from cultured human fibroblasts, J Biol Chem 266, 21572-7 (1991).
72. Uozumi N, Yanagidani S, Miyoshi E, Ihara Y, Sakuma T, Gao C-X, Teshima T, Fujii S, Shiba T, Taniguchi N, Purification and cDNA cloning of porcine brain GDP-L-Fuc: N-acetyl-β-D-glucosamine α 1,6fucosyltransferase, J Biol Chem 271, 385-92 (1996).
73. Kudo T, Ikehara Y, Togayashi A, Kaneko M, Hiraga T, Sasaki K, Narimatsu H, Expression cloning and characterization of a novel murine α 1,3-fucosyltransferase, mFuc-TIX, that synthesizes the Lewis x (CD15) epitope in brain and kidney, J Biol Chem 273, 26729-38 (1998).
74. Gillespie W, Kelm S, Paulson JC, Cloning and expression of Galβ 1,3GalNAcα2,3 sialyltransferase, J Biol Chem 267, 21004-10 (1992).
75. Lee YC, Kurosawa N, Hamamoto T, Nakaoka T, Tsuji S, Molecular cloning and expression of Galβ 1,3GalNAc α2,3-sialyltransferase from mouse brain, Eur J Biochem 216, 377-85 (1993).
76. Basu M, De T, Das KK, Kyle JW, Chon H-C, Schaeper RJ, Basu S, Glycolipids, Method Enzymol 138, 575-607 (1987).
77. Lee YC, Kojima N, Wada E, Kurosawa N, Nakaoka T, Hamamoto T, Tsuji S, Cloning and expression of cDNA for a new type of Galβ 1,3GalNAc α2,3-sialyltransferase, J Biol Chem 269, 10028-33 (1994).
78. Weinstein J, de Souza-e-Silva U, Paulson JC, Sialylation of glycoprotein oligosaccharides N-linked to asparagine, J Biol Chem 257, 13845-53 (1982).
79. Kitagawa H, Paulson JC, Cloning and expression of human Galα 1,3(4)GlcNAc α2,3-sialyltransferase, Biochem Biophys Res Commun 194, 375-82 (1993).
80. Sasaki K, Watanabe E, Kawashima K, Sekine S, Dohi T, Oshima M, Hanai N, Nishi T, Hasegawa M, Expression cloning of a novel Galβ(1-3/1-4)GlcNAc-α2,3-sialyltransferase using lectin resistance selection, J Biol Chem 268, 22782-7 (1993).
81. Kaufmann B, Basu S, Roseman S, Enzymatic synthesis of disialogangliosides from monosialogangliosides by sialyltransferases from embryonic chicken brain, J Biol Chem 243, 5804-7 (1968).
82. Preuss U, Gum X, Gu T, Yu RK, Purification and characterization of CMP-N-acetylneuraminic acid: Lactosylceramide (α2,3) sialyltransferase (GM3-synthase) from rat brain, J Biol Chem 268, 26273-8 (1993).
83. Okajima T, Fukumoto S, Miyazaki H, Ishida H, Kiso M, Furukawa K, Urano T, Furukawa K, Molecular cloning of a novel α2,3-sialyltransferase (ST3Gal VI) that sialylates type II lactosamine structures on glycoproteins and glycolipids, J Biol Chem 274, 11479-86 (1999).
84. Weinstein J, de Souza-e-Silva U, Paulson JC, Purification of a Galβ1 to 4GlcNAc α2 to 6 sialyltransferase and a Galβ1 to 3(4) GlcNAc α 2 to 3 sialyltransferase to homogenity from rat liver, J Biol Chem 257, 13835-44 (1982).
85. Joziasse DH SW, Van den Eijnden DH, Van Kuik JA, Van Halbeek H, Vliegenthart JFG, Branch specificity of bovine colostrum CMP-sialic acid: N-acetyllactosaminide α 2-6-sialyltransferase. Interaction with biantennary oligosaccharides and glycopeptides of N-glycoproteins, J Biol Chem 260, 714-9 (1985).
86. Hamamoto T, Kurosawa N, Lee Y-C, Tsuji S, Donor substrate specificities of Galβ1,4GlcNAc α2,6-sialyltransferase and Galβ1,3GalNAc α2,3-sialyltransferase: Comparison of N-acetyl and N-glycolylneuraminic acids, Biochem Biophys Acta 124, 223-8 (1995).
87. Weinstein J, Lee EU, McEntee K, Lai PH, Paulson JC, Primary structure of β-galactoside α2,6-sialyltransferse. Conversion of membrane-bound enzyme to soluble forms by cleavage of the NH2-terminal signal anchor, J Biol Chem 262, 17735-43 (1987).
88. Kurosawa N, Hamamoto T, Lee Y-C, Nakaoka T, Tsuji S, Molecular cloning and expression of GalNAc α2,6-sialyltransferase, J Biol Chem 269, 1402-9 (1994).
89. Sadler JE, Rearick JI, Hill RL, Purification to homogeneity and enzymatic characterization of an α-N-acetylgalactosaminide α2,6 sialyltransferase from porcine submaxillary glands, J Biol Chem 254, 5934-41 (1979).
90. Ikehara Y, Kojima N, Kurosawa N, Kudo T, Kono M, Nishihara S, Issiki S, Morozumi K, Itzkowitz S, Tsuda T, Nishimura S-I, Tsuji S, Narimatsu H, Cloning and expression of a human gene encoding an N-acetylgalactosamine-α2,6-sialyltransferase (ST6GalNAc-I) which is a candidate for synthesis of cancer-associated sialyl-Tn, Glycobiology 9, 1213-24 (1999).
91. Kurosawa N, Kojima N, Inoue M, Hamamoto T, Tsuji S, Cloning and expression of Galβ1,3GalNAc-specific GalNAc α2,6-sialyltransferase, J Biol Chem 269, 19048-53 (1994).
92. Lee Y, Kaufmann M, Kitazume-Kawaguchi S, Kono M, Takashima S, Kurosawa N, Liu H, Pircher H, Tsuji S, Molecular cloning and functional expression of two members of mouse NeuAcα2,3Galβ1,3GalNAc GalNAcα2,6-sialyltransferase family ST6GalNAc-III and -IV, J Biol Chem 274, 11958-67 (1999).
93. Sjoberg ER, Kitagawa H, Glushka J, van Halbeek H, Paulson JC, Molecular cloning of a developmentally regulated N-acetylgalactosamine α2,6-sialyltransferase specific for sialylated glycoconjugates, J Biol Chem 271, 7450-9 (1996).
94. Ikehara Y, Shimizu N, Kono M, Nishihara S, Nakanishi H, Kitamura T, Narimatsu H, Tsuji S, Tatematsu M, A novel glycosyltransferase with a polyglutamine repeat: A new candidate for GD1α synthase (ST6GalNAc-V), FEBS Lett 463, 92-6 (1999).
95. Okajima T, Fukumoto S, Ito H, Kiso M, Hirabayashi Y, Urano T, Furukawa K, Molecular cloning of brain-specific GD1α synthase (ST6GalNAc-V) containing CAG/glutamine repeats, J Biol Chem 274, 30557-62 (1999).
96. Okajima T, Chen HH, Ito H, Kiso M, Furukawa K, Urano T, Furukawa K, Molecular cloning and expression of mouse GD1α/GT1aα/GQ1bα synthase (ST6GalNAc-VI) gene, J Biol Chem 275, 6717-23 (2000).
97. Taniguchi T, Honke K, Fukuda M (eds.), Handbook of Glycosyltransferases and Related Genes (Springer-Verlag, Tokyo, 2002).