RPTPζ/phosphacan is abnormally glycosylated in a model of muscle-eye-brain disease lacking functional POMGnT1

Neuroscience

Volumn 220, Issue , 2012, Pages 47-61

  Dwyer, C A ^a   Baker, E ^a   Hu, H ^a   Matthews, R T ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Human Natural Killer 1 (HNK 1); Muscle eye brain disease (MEB); Phosphacan; Protein glycosylation; Protein O mannose 1,2 N acetylglucosaminyltransferase 1 (POMGnT1); Receptor protein tyrosine phosphatase (RPTP )

Indexed keywords

CAT 315 ANTIBODY; MANNOSE BETA 1,2 N ACETYLGLUCOSAMINYLTRANSFERASE; MONOCLONAL ANTIBODY; N ACETYLGLUCOSAMINYLTRANSFERASE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE EPSILON; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; DEGLYCOSYLATION; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; MOLECULAR WEIGHT; MOUSE; MUSCLE EYE BRAIN DISEASE; NONHUMAN; PATHOGENESIS; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION;

ANIMALS; BLOTTING, WESTERN; BRAIN; DISEASE MODELS, ANIMAL; GLYCOSYLATION; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; N-ACETYLGLUCOSAMINYLTRANSFERASES; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 5; WALKER-WARBURG SYNDROME;

EID: 84864763681     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.06.026     Document Type: Article

References (84)

1. Abbott K.L., Matthews R.T., Pierce M. Receptor tyrosine phosphatase beta (RPTPbeta) activity and signaling are attenuated by glycosylation and subsequent cell surface galectin-1 binding. J Biol Chem 2008, 283:33026-33035.
2. Bakker H., Friedmann I., Oka S., Kawasaki T., Nifant'ev N., Schachner M., Mantei N. Expression cloning of a cDNA encoding a sulfotransferase involved in the biosynthesis of the HNK-1 carbohydrate epitope. J Biol Chem 1997, 272:29942-29946.
3. Beltran-Valero de Bernabe D., Currier S., Steinbrecher A., Celli J., van Beusekom E., van der Zwaag B., Kayserili H., Merlini L., Chitayat D., Dobyns W.B., Cormand B., Lehesjoki A.E., Cruces J., Voit T., Walsh C.A., van Bokhoven H., Brunner H.G. Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am J Hum Genet 2002, 71:1033-1043.
4. Bleckmann C., Geyer H., Lieberoth A., Splittstoesser F., Liu Y., Feizi T., Schachner M., Kleene R., Reinhold V., Geyer R. O-glycosylation pattern of CD24 from mouse brain. Biol Chem 2009, 390:627-645.
5. Brasseur-Daudruy M, Viver PH, Ickowicz V, Eurin D, Verspyck E (2011) Walker-Warburg syndrome diagnosed by findings of typical ocular abnormalities on prenatal ultrasound. Pediatr Radiol Epub ahead of print.
6. Brockington M., Blake D.J., Prandini P., Brown S.C., Torelli S., Benson M.A., Ponting C.P., Estournet B., Romero N.B., Mercuri E., Voit T., Sewry C.A., Guicheney P., Muntoni F. Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin alpha2 deficiency and abnormal glycosylation of alpha-dystroglycan. Am J Hum Genet 2001, 69:1198-1209.
7. Brockington M., Yuva Y., Prandini P., Brown S.C., Torelli S., Benson M.A., Herrmann R., Anderson L.V., Bashir R., Burgunder J.M., Fallet S., Romero N., Fardeau M., Straub V., Storey G., Pollitt C., Richard I., Sewry C.A., Bushby K., Voit T., Blake D.J., Muntoni F. Mutations in the fukutin-related protein gene (FKRP) identify limb girdle muscular dystrophy 2I as a milder allelic variant of congenital muscular dystrophy MDC1C. Hum Mol Genet 2001, 10:2851-2859.
8. Browning C.A., Grewal P.K., Moore C.J., Hewitt J.E. A rapid PCR method for genotyping the Large(myd) mouse, a model of glycosylation-deficient congenital muscular dystrophy. Neuromuscul Disord 2005, 15:331-335.
9. Canoll P.D., Petanceska S., Schlessinger J., Musacchio J.M. Three forms of RPTP-beta are differentially expressed during gliogenesis in the developing rat brain and during glial cell differentiation in culture. J Neurosci Res 1996, 44:199-215.
10. Celio M.R., Spreafico R., De Biasi S., Vitellaro-Zuccarello L. Perineuronal nets: past and present. Trends Neurosci 1998, 21:510-515.
11. Chai W., Yuen C.T., Kogelberg H., Carruthers R.A., Margolis R.U., Feizi T., Lawson A.M. High prevalence of 2-mono- and 2,6-di-substituted manol-terminating sequences among O-glycans released from brain glycopeptides by reductive alkaline hydrolysis. Eur J Biochem 1999, 263:879-888.
12. Deepa S.S., Carulli D., Galtrey C., Rhodes K., Fukuda J., Mikami T., Sugahara K., Fawcett J.W. Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J Biol Chem 2006, 281:17789-17800.
13. Dino M.R., Harroch S., Hockfield S., Matthews R.T. Monoclonal antibody Cat-315 detects a glycoform of receptor protein tyrosine phosphatase beta/phosphacan early in CNS development that localizes to extrasynaptic sites prior to synapse formation. Neuroscience 2006, 142:1055-1069.
14. Dobyns W.B., Kirkpatrick J.B., Hittner H.M., Roberts R.M., Kretzer F.L. Syndromes with lissencephaly. II: Walker-Warburg and cerebro-oculo-muscular syndromes and a new syndrome with type II lissencephaly. Am J Med Genet 1985, 22:157-195.
15. Ervasti J.M., Campbell K.P. Membrane organization of the dystrophin-glycoprotein complex. Cell 1991, 66:1121-1131.
16. Ervasti J.M., Campbell K.P. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 1993, 122:809-823.
17. Faissner A., Clement A., Lochter A., Streit A., Mandl C., Schachner M. Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties. J Cell Biol 1994, 126:783-799.
18. Finne J., Krusius T., Margolis R.K., Margolis R.U. Novel mannitol-containing oligosaccharides obtained by mild alkaline borohydride treatment of a chondroitin sulfate proteoglycan from brain. J Biol Chem 1979, 254:10295-10300.
19. Garwood J., Heck N., Reichardt F., Faissner A. Phosphacan short isoform, a novel non-proteoglycan variant of phosphacan/receptor protein tyrosine phosphatase-beta, interacts with neuronal receptors and promotes neurite outgrowth. J Biol Chem 2003, 278:24164-24173.
20. Garwood J., Schnadelbach O., Clement A., Schutte K., Bach A., Faissner A. DSD-1-proteoglycan is the mouse homolog of phosphacan and displays opposing effects on neurite outgrowth dependent on neuronal lineage. J Neurosci 1999, 19:3888-3899.
21. Grewal P.K., Holzfeind P.J., Bittner R.E., Hewitt J.E. Mutant glycosyltransferase and altered glycosylation of alpha-dystroglycan in the myodystrophy mouse. Nat Genet 2001, 28:151-154.
22. Grumet M., Friedlander D.R., Sakurai T. Functions of brain chondroitin sulfate proteoglycans during developments: interactions with adhesion molecules. Perspect Dev Neurobiol 1996, 3:319-330.
23. Grumet M., Milev P., Sakurai T., Karthikeyan L., Bourdon M., Margolis R.K., Margolis R.U. Interactions with tenascin and differential effects on cell adhesion of neurocan and phosphacan, two major chondroitin sulfate proteoglycans of nervous tissue. J Biol Chem 1994, 269:12142-12146.
24. Haltia M., Leivo I., Somer H., Pihko H., Paetau A., Kivela T., Tarkkanen A., Tome F., Engvall E., Santavuori P. Muscle-eye-brain disease: a neuropathological study. Ann Neurol 1997, 41:173-180.
25. Harroch S., Furtado G.C., Brueck W., Rosenbluth J., Lafaille J., Chao M., Buxbaum J.D., Schlessinger J. A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat Genet 2002, 32:411-414.
26. Harroch S., Palmeri M., Rosenbluth J., Custer A., Okigaki M., Shrager P., Blum M., Buxbaum J.D., Schlessinger J. No obvious abnormality in mice deficient in receptor protein tyrosine phosphatase beta. Mol Cell Biol 2000, 20:7706-7715.
27. Haunso A., Celio M.R., Margolis R.K., Menoud P.A. Phosphacan immunoreactivity is associated with perineuronal nets around parvalbumin-expressing neurones. Brain Res 1999, 834:219-222.
28. Hayashi N., Mizusaki M.J., Kamei K., Harada S., Miyata S. Chondroitin sulfate proteoglycan phosphacan associates with parallel fibers and modulates axonal extension and fasciculation of cerebellar granule cells. Mol Cell Neurosci 2005, 30:364-377.
29. Hu H., Yang Y., Eade A., Xiong Y., Qi Y. Breaches of the pial basement membrane and disappearance of the glia limitans during development underlie the cortical lamination defect in the mouse model of muscle-eye-brain disease. J Comp Neurol 2007, 502:168-183.
30. Ibraghimov-Beskrovnaya O., Ervasti J.M., Leveille C.J., Slaughter C.A., Sernett S.W., Campbell K.P. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 1992, 355:696-702.
31. Ida M., Shuo T., Hirano K., Tokita Y., Nakanishi K., Matsui F., Aono S., Fujita H., Fujiwara Y., Kaji T., Oohira A. Identification and functions of chondroitin sulfate in the milieu of neural stem cells. J Biol Chem 2006, 281:5982-5991.
32. Inamori K.-i. Dystroglycan function requires xylosyl- and glucuronyltransferase activities of LARGE. Science 2012, 335:93-96.
33. Ito Y., Hikino M., Yajima Y., Mikami T., Sirko S., von Holst A., Faissner A., Fukui S., Sugahara K. Structural characterization of the epitopes of the monoclonal antibodies 473HD, CS-56, and MO-225 specific for chondroitin sulfate D-type using the oligosaccharide library. Glycobiology 2005, 15:593-603.
34. Jimenez-Mallebrera C., Brown S.C., Sewry C.A., Muntoni F. Congenital muscular dystrophy: molecular and cellular aspects. Cell Mol Life Sci 2005, 62:809-823.
35. Kano H., Kobayashi K., Herrmann R., Tachikawa M., Manya H., Nishino I., Nonaka I., Straub V., Talim B., Voit T., Topaloglu H., Endo T., Yoshikawa H., Toda T. Deficiency of alpha-dystroglycan in muscle-eye-brain disease. Biochem Biophys Res Commun 2002, 291:1283-1286.
36. Kim D.S., Hayashi Y.K., Matsumoto H., Ogawa M., Noguchi S., Murakami N., Sakuta R., Mochizuki M., Michele D.E., Campbell K.P., Nonaka I., Nishino I. POMT1 mutation results in defective glycosylation and loss of laminin-binding activity in alpha-DG. Neurology 2004, 62:1009-1011.
37. Kogelberg H., Chai W., Feizi T., Lawson A.M. NMR studies of mannitol-terminating oligosaccharides derived by reductive alkaline hydrolysis from brain glycoproteins. Carbohydr Res 2001, 331:393-401.
38. Krusius T., Finne J., Margolis R.K., Margolis R.U. Identification of an O-glycosidic mannose-linked sialylated tetrasaccharide and keratan sulfate oligosaccharides in the chondroitin sulfate proteoglycan of brain. J Biol Chem 1986, 261:8237-8242.
39. Kuga A., Kanagawa M., Sudo A., Chan Y.M., Tajiri M., Manya H., Kikkawa Y., Nomizu M., Kobayashi K., Endo T., Lu Q.L., Wada Y., Toda T. Absence of post-phosphoryl modification in dystroglycanopathy mouse models and wild-type tissues expressing non-laminin binding form of alpha-dystroglycan. J Biol Chem 2012, 287:9560-9567.
40. Lander C., Zhang H., Hockfield S. Neurons produce a neuronal cell surface-associated chondroitin sulfate proteoglycan. J Neurosci 1998, 18:174-183.
41. Liu J., Ball S.L., Yang Y., Mei P., Zhang L., Shi H., Kaminski H.J., Lemmon V.P., Hu H. A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech Dev 2006, 123:228-240.
42. Longman C., Brockington M., Torelli S., Jimenez-Mallebrera C., Kennedy C., Khalil N., Feng L., Saran R.K., Voit T., Merlini L., Sewry C.A., Brown S.C., Muntoni F. Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of alpha-dystroglycan. Hum Mol Genet 2003, 12:2853-2861.
43. Maeda N., Hamanaka H., Oohira A., Noda M. Purification, characterization and developmental expression of a brain-specific chondroitin sulfate proteoglycan, 6B4 proteoglycan/phosphacan. Neuroscience 1995, 67:23-35.
44. Maeda N., Hamanaka H., Shintani T., Nishiwaki T., Noda M. Multiple receptor-like protein tyrosine phosphatases in the form of chondroitin sulfate proteoglycan. FEBS Lett 1994, 354:67-70.
45. Maeda N., He J., Yajima Y., Mikami T., Sugahara K., Yabe T. Heterogeneity of the chondroitin sulfate portion of phosphacan/6B4 proteoglycan regulates its binding affinity for pleiotrophin/heparin binding growth-associated molecule. J Biol Chem 2003, 278:35805-35811.
46. Maeda N., Ichihara-Tanaka K., Kimura T., Kadomatsu K., Muramatsu T., Noda M. A receptor-like protein-tyrosine phosphatase PTPzeta/RPTPbeta binds a heparin-binding growth factor midkine. Involvement of arginine 78 of midkine in the high affinity binding to PTPzeta. J Biol Chem 1999, 274:12474-12479.
47. Maeda N., Nishiwaki T., Shintani T., Hamanaka H., Noda M. 6B4 proteoglycan/phosphacan, an extracellular variant of receptor-like protein-tyrosine phosphatase zeta/RPTPbeta, binds pleiotrophin/heparin-binding growth-associated molecule (HB-GAM). J Biol Chem 1996, 271:21446-21452.
48. Manya H., Chiba A., Yoshida A., Wang X., Chiba Y., Jigami Y., Margolis R.U., Endo T. Demonstration of mammalian protein O-mannosyltransferase activity: coexpression of POMT1 and POMT2 required for enzymatic activity. Proc Natl Acad Sci U S A 2004, 101:500-505.
49. Matthews R.T., Kelly G.M., Zerillo C.A., Gray G., Tiemeyer M., Hockfield S. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J Neurosci 2002, 22:7536-7547.
50. Maurel P., Rauch U., Flad M., Margolis R.K., Margolis R.U. Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosine phosphatase. Proc Natl Acad Sci U S A 1994, 91:2512-2516.
51. McGarry R.C., Helfand S.L., Quarles R.H., Roder J.C. Recognition of myelin-associated glycoprotein by the monoclonal antibody HNK-1. Nature 1983, 306:376-378.
52. McRae P.A., Rocco M.M., Kelly G., Brumberg J.C., Matthews R.T. Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 2007, 27:5405-5413.
53. Meng K., Rodriguez-Pena A., Dimitrov T., Chen W., Yamin M., Noda M., Deuel T.F. Pleiotrophin signals increased tyrosine phosphorylation of beta beta-catenin through inactivation of the intrinsic catalytic activity of the receptor-type protein tyrosine phosphatase beta/zeta. Proc Natl Acad Sci U S A 2000, 97:2603-2608.
54. Michele D.E., Barresi R., Kanagawa M., Saito F., Cohn R.D., Satz J.S., Dollar J., Nishino I., Kelley R.I., Somer H., Straub V., Mathews K.D., Moore S.A., Campbell K.P. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 2002, 418:417-422.
55. Milev P., Friedlander D.R., Sakurai T., Karthikeyan L., Flad M., Margolis R.K., Grumet M., Margolis R.U. Interactions of the chondroitin sulfate proteoglycan phosphacan, the extracellular domain of a receptor-type protein tyrosine phosphatase, with neurons, glia, and neural cell adhesion molecules. J Cell Biol 1994, 127:1703-1715.
56. Milev P., Meyer-Puttlitz B., Margolis R.K., Margolis R.U. Complex-type asparagine-linked oligosaccharides on phosphacan and protein-tyrosine phosphatase-zeta/beta mediate their binding to neural cell adhesion molecules and tenascin. J Biol Chem 1995, 270:24650-24653.
57. Montanaro F., Lindenbaum M., Carbonetto S. Alpha-Dystroglycan is a laminin receptor involved in extracellular matrix assembly on myotubes and muscle cell viability. J Cell Biol 1999, 145:1325-1340.
58. Moore S.A., Saito F., Chen J., Michele D.E., Henry M.D., Messing A., Cohn R.D., Ross-Barta S.E., Westra S., Williamson R.A., Hoshi T., Campbell K.P. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 2002, 418:422-425.
59. Morita I., Kakuda S., Takeuchi Y., Itoh S., Kawasaki N., Kizuka Y., Kawasaki T., Oka S. HNK-1 glyco-epitope regulates the stability of the glutamate receptor subunit GluR2 on the neuronal cell surface. J Biol Chem 2009, 284:30209-30217.
60. Morita I., Kakuda S., Takeuchi Y., Kawasaki T., Oka S. HNK-1 (human natural killer-1) glyco-epitope is essential for normal spine morphogenesis in developing hippocampal neurons. Neuroscience 2009, 164:1685-1694.
61. Morita I., Kizuka Y., Kakuda S., Oka S. Expression and function of the HNK-1 carbohydrate. J Biochem 2008, 143:719-724.
62. Muntoni F., Voit T. The congenital muscular dystrophies in 2004: a century of exciting progress. Neuromuscul Disord 2004, 14:635-649.
63. Niisato K., Fujikawa A., Komai S., Shintani T., Watanabe E., Sakaguchi G., Katsuura G., Manabe T., Noda M. Age-dependent enhancement of hippocampal long-term potentiation and impairment of spatial learning through the Rho-associated kinase pathway in protein tyrosine phosphatase receptor type Z-deficient mice. J Neurosci 2005, 25:1081-1088.
64. Ong E., Yeh J.C., Ding Y., Hindsgaul O., Fukuda M. Expression cloning of a human sulfotransferase that directs the synthesis of the HNK-1 glycan on the neural cell adhesion molecule and glycolipids. J Biol Chem 1998, 273:5190-5195.
65. Peles E., Schlessinger J., Grumet M. Multi-ligand interactions with receptor-like protein tyrosine phosphatase beta: implications for intercellular signaling. Trends Biochem Sci 1998, 23:121-124.
66. Ranjan M., Hudson L.D. Regulation of tyrosine phosphorylation and protein tyrosine phosphatases during oligodendrocyte differentiation. Mol Cell Neurosci 1996, 7:404-418.
67. Reed U.C. Congenital muscular dystrophy. Part II: a review of pathogenesis and therapeutic perspectives. Arq Neuropsiquiatr 2009, 67:343-362.
68. Saitoh Y., Matsui F., Chiba Y., Kawamura N., Keino H., Satoh M., Kumagai N., Ishii S., Yoshikawa K., Shimada A., Maeda N., Oohira A., Hosokawa M. Reduced expression of MAb6B4 epitopes on chondroitin sulfate proteoglycan aggrecan in perineuronal nets from cerebral cortices of SAMP10 mice. a model for age-dependent neurodegeneration. J Neurosci Res 2008, 86:1316-1323.
69. Sakurai T., Lustig M., Nativ M., Hemperly J.J., Schlessinger J., Peles E., Grumet M. Induction of neurite outgrowth through contactin and Nr-CAM by extracellular regions of glial receptor tyrosine phosphatase beta. J Cell Biol 1997, 136:907-918.
70. Satz J.S., Ostendorf A.P., Hou S., Turner A., Kusano H., Lee J.C., Turk R., Nguyen H., Ross-Barta S.E., Westra S., Hoshi T., Moore S.A., Campbell K.P. Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J Neurosci 2010, 30:14560-14572.
71. Schessl J., Zou Y., Bonnemann C.G. Congenital muscular dystrophies and the extracellular matrix. Semin Pediatr Neurol 2006, 13:80-89.
72. Schmidt J.T., Schachner M. Role for cell adhesion and glycosyl (HNK-1 and oligomannoside) recognition in the sharpening of the regenerating retinotectal projection in goldfish. J Neurobiol 1998, 37:659-671.
73. Shitara K., Yamada H., Watanabe K., Shimonaka M., Yamaguchi Y. Brain-specific receptor-type protein-tyrosine phosphatase RPTP beta is a chondroitin sulfate proteoglycan in vivo. J Biol Chem 1994, 269:20189-20193.
74. Soh B.S., Song C.M., Vallier L., Li P., Choong C., Yeo B.H., Lim E.H., Pedersen R.A., Yang H.H., Rao M., Lim B. Pleiotrophin enhances clonal growth and long-term expansion of human embryonic stem cells. Stem cells 2007, 25:3029-3037.
75. Stalnaker S.H., Aoki K., Lim J.M., Porterfield M., Liu M., Satz J.S., Buskirk S., Xiong Y., Zhang P., Campbell K.P., Hu H., Live D., Tiemeyer M., Wells L. Glycomic analyses of mouse models of congenital muscular dystrophy. J Biol Chem 2011, 286:21180-21190.
76. Terayama K., Oka S., Seiki T., Miki Y., Nakamura A., Kozutsumi Y., Takio K., Kawasaki T. Cloning and functional expression of a novel glucuronyltransferase involved in the biosynthesis of the carbohydrate epitope HNK-1. Proc Natl Acad Sci U S A 1997, 94:6093-6098.
77. Viapiano M.S., Matthews R.T., Hockfield S. A novel membrane-associated glycovariant of BEHAB/brevican is up-regulated during rat brain development and in a rat model of invasive glioma. J Biol Chem 2003, 278:33239-33247.
78. Yagi H., Yanagisawa M., Suzuki Y., Nakatani Y., Ariga T., Kato K., Yu R.K. HNK-1 epitope-carrying tenascin-C spliced variant regulates the proliferation of mouse embryonic neural stem cells. J Biol Chem 2010, 285:37293-37301.
79. Yamamoto S., Oka S., Inoue M., Shimuta M., Manabe T., Takahashi H., Miyamoto M., Asano M., Sakagami J., Sudo K., Iwakura Y., Ono K., Kawasaki T. Mice deficient in nervous system-specific carbohydrate epitope HNK-1 exhibit impaired synaptic plasticity and spatial learning. J Biol Chem 2002, 277:27227-27231.
80. Yamamoto S., Oka S., Saito-Ohara F., Inazawa J., Kawasaki T. Molecular cloning and genomic analysis of mouse glucuronyltransferase involved in biosynthesis of the HNK-1 epitope. J Biochem 2002, 131:337-347.
81. Yoshida A., Kobayashi K., Manya H., Taniguchi K., Kano H., Mizuno M., Inazu T., Mitsuhashi H., Takahashi S., Takeuchi M., Herrmann R., Straub V., Talim B., Voit T., Topaloglu H., Toda T., Endo T. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 2001, 1:717-724.
82. Yoshida-Moriguchi T., Yu L., Stalnaker S.H., Davis S., Kunz S., Madson M., Oldstone M.B., Schachter H., Wells L., Campbell K.P. O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science 2010, 327:88-92.
83. Yoshihara T., Sugihara K., Kizuka Y., Oka S., Asano M. Learning/memory impairment and reduced expression of the HNK-1 carbohydrate in beta4-galactosyltransferase-II-deficient mice. J Biol Chem 2009, 284:12550-12561.
84. Yuen C.T., Chai W., Loveless R.W., Lawson A.M., Margolis R.U., Feizi T. Brain contains HNK-1 immunoreactive O-glycans of the sulfoglucuronyl lactosamine series that terminate in 2-linked or 2,6-linked hexose (mannose). J Biol Chem 1997, 272:8924-8931.