Novel Kv3 glycoforms differentially expressed in adult mammalian brain contain sialylated N-glycans

Biochemistry and Cell Biology

Volumn 86, Issue 1, 2008, Pages 21-30

  Schwalbe, Ruth A ^a   Corey, Melissa J ^a   Cartwright, Tara A ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Glycoforms; Mammalian brain; N glycans; Potassium channels; Sialic acid

Indexed keywords

GLYCOFORMS; MAMMALIAN BRAIN; N-GLYCANS; POTASSIUM CHANNELS; SIALIC ACID;

CELL MEMBRANES; NEUROLOGY; PROTEINS; RATS;

BRAIN;

GLYCOPROTEIN; SHAW POTASSIUM CHANNEL; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL KV3.1; VOLTAGE GATED POTASSIUM CHANNEL KV3.3; VOLTAGE GATED POTASSIUM CHANNEL KV3.4;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN TISSUE; CELL DIFFERENTIATION; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ELECTROPHORESIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIALYLATION;

ANIMALS; BRAIN; N-ACETYLNEURAMINIC ACID; POLYSACCHARIDES; PROTEIN CONFORMATION; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; SHAW POTASSIUM CHANNELS;

MAMMALIA; RATTUS;

EID: 39049161608     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/O07-152     Document Type: Article

References (33)

1. Albach, C., Klein, R.A., and Schmitz, B. 2001. Do rodent and human brains have different N-glycosylation patterns? Biol. Chem. 382: 187-194. doi:10.1515/BC.2001.026.
2. Angata, K., and Fukuda, M. 2003. Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie, 85: 195-206. doi:10.1016/S0300-9084(03)00051-8.
3. Benoit, A., Vargas, M.A., Desgroseillers, L., and Boileau, G. 2004. Endothelin-converting enzyme-like 1 (ECEL1) is present both in the plasma membrane and in the endoplasmic reticulum. Biochem. J. 380: 881-888. doi:10.1042/BJ20040215.
4. Brooks, N.L., Corey, M.J., and Schwalbe, R.A. 2006. Characterization of N-glycosylation consensus sequences in the Kv3.1 channel. Febs J.
5. Cartwright, T.A., Corey, M.J., and Schwalbe, R.A. 2007. Complex oligosaccharides are N-linked to Kv3 voltage-gated K+ channels in rat brain. Biochim. Biophys. Acta, 1770: 666-671.
6. Drickamer, K., and Taylor, M.E. 1998. Evolving views of protein glycosylation. Trends Biochem. Sci. 23: 321-324. doi:10.1016/S0968- 0004(98)01246-8.
7. Du, J., Zhang, L., Weiser, M., Rudy, B., and McBain, C.J. 1996. Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J. Neurosci. 16: 506-518.
8. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., et al. 2000. Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J. Neurosci. 20: 5234-5244.
9. Freeze, H.H., and Aebi, M. 1999. Molecular basis of carbohydrate- deficient glycoprotein syndromes type I with normal phosphomannomutase activity. Biochim. Biophys. Acta, 1455: 167-178.
10. Gahmberg, C.G., and Tolvanen, M. 1996. Why mammalian cell surface proteins are glycoproteins. Trends Biochem. Sci. 21: 308-311.
11. Galuska, S.P., Oltmann-Norden, I., Geyer, H., Weinhold, B., Kuchelmeister, K., Hildebrandt, H., et al. 2006. Polysialic acid profiles of mice expressing variant allelic combinations of the polysialyltransferases ST8SiaII and ST8SiaIV. J. Biol. Chem. 281: 31605-31615. doi:10.1074/jbc.M606516200.
12. Gelband, C.H., Warth, J.D., Mason, H.S., Zhu, M., Moore, J.M., Kenyon, J.L., Horowitz, B., and Sumners, C. 1999. Angiotensin II type 1 receptor-mediated inhibition of K+ channel subunit kv2.2 in brain stem and hypothalamic neurons. Circ. Res. 84: 352-359.
13. Ioffe, E., and Stanley, P. 1994. Mice lacking N- acetylglucosaminyltransferase I activity die at mid-gestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc. Natl. Acad. Sci. U.S.A. 91: 728-732. doi:10.1073/pnas.91.2.728.
14. Jiang, Y., Lee, A., Chen, J., Ruta, V., Cadene, M., Chait, B.T., and MacKinnon, R. 2003. X-ray structure of a voltage-dependent K+ channel. Nature, 423: 33-41. doi:10.1038/nature01580.
15. Jones, J., Krag, S.S., and Betenbaugh, M.J. 2005. Controlling N-linked glycan site occupancy. Biochim. Biophys. Acta, 1726: 121-137.
16. Kornfeld, R., and Kornfeld, S. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54: 631-664. doi:10.1146/annurev. bi.54.070185.003215.
17. Lindholm, D., Wootz, H., and Korhonen, L. 2006. ER stress and neurodegenerative diseases. Cell Death Differ. 13: 385-392. doi:10.1038/sj.cdd.4401778.
18. Manganas, L.N., and Trimmer, J.S. 2000. Subunit composition determines Kv1 potassium channel surface expression. J. Biol. Chem. 275: 29685-29693. doi:10.1074/jbc.M005010200.
19. Metzler, M., Gertz, A., Sarkar, M., Schachter, H., Schrader, J.W., and Marth, J.D. 1994. Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J. 13: 2056-2065.
20. Misonou, H., and Trimmer, J.S. 2004. Determinants of voltage-gated potassium channel surface expression and localization in Mammalian neurons. Crit. Rev. Biochem. Mol. Biol. 39: 125-145. doi:10.1080/ 10409230490475417.
21. Perney, T.M., Marshall, J., Martin, K.A., Hockfield, S., and Kaczmarek, L.K. 1992. Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. J. Neurophysiol. 68: 756-766.
22. Peterson, G.L. 1979. Review of the Folin phenol protein quantitation method of Lowry, Rosebrough, Farr and Randall. Anal. Biochem. 100: 201-220. doi:10.1016/0003-2697(79)90222-7.
23. Prime, S., Dearnley, J., Ventom, A.M., Parekh, R.B., and Edge, C.J. 1996. Oligosaccharide sequencing based on exo- and endoglycosidase digestion and liquid chromatographic analysis of the products. J. Chromatogr. A. 720: 263-274. doi:10.1016/0021-9673(95)00029-1.
24. Rudy, B., Kentros, C., Weiser, M., Fruhling, D., Serodio, P., Vega-Saenz de Miera, E., et al. 1992. Region-specific expression of a K+ channel gene in brain. Proc. Natl. Acad. Sci. U.S.A. 89: 4603-4607. doi:10.1073/pnas.89. 10.4603.
25. Schachter, H. 2002. The role of the GlcNAc(beta)1,2Man(alpha)-moiety in mammalian development. Null mutations of the genes encoding UDP-N- acetylglucosamine:alpha-3-D-mannoside beta-1,2-N-acetylglucosaminyltransferase I and UDP-N-acetylglucosamine: alpha-D-mannoside beta-1,2-N- acetylglucosaminyltransferase I.2 cause embryonic lethality and congenital muscular dystrophy in mice and men, respectively. Biochim. Biophys. Acta, 1573: 292-300.
26. Schwalbe, R.A., Wang, Z., Wible, B.A., and Brown, A.M. 1995. Potassium channel structure and function as reported by a single glycosylation sequon. J. Biol. Chem. 270: 15336-15340. doi:10.1074/jbc.270.25.15336.
27. Schwalbe, R.A., Rudin, A., Xia, S.L., and Wingo, C.S. 2002. Site-directed glycosylation tagging of functional Kir2.1 reveals that the putative pore-forming segment is extracellular. J. Biol. Chem. 277: 24382-24389. doi:10.1074/jbc.M201668200.
28. Shi, G., and Trimmer, J.S. 1999. Differential asparagine-linked glycosylation of voltage-gated K+ channels in mammalian brain and in transfected cells. J. Membr. Biol. 168: 265-273. doi:10.1007/s002329900515.
29. Thornhill, W.B., Wu, M.B., Jiang, X., Wu, X., Morgan, P.T., and Margiotta, J.F. 1996. Expression of Kv1.1 delayed rectifier potassium channels in Lec mutant Chinese hamster ovary cell lines reveals a role for sialidation in channel function. J. Biol. Chem. 271: 19093-19098. doi:10.1074/jbc.271. 32.19093.
30. Wang, Y., Schachter, H., and Marth, J.D. 2002. Mice with a homozygous deletion of the Mgat2 gene encoding UDP-N-acetylglucosamine: alpha-6-D-mannoside beta1,2-N-acetylglucosaminyltransferase II: a model for congenital disorder of glycosylation type IIa. Biochim. Biophys. Acta, 1573: 301-311.
31. Weiser, M., Vega-Saenz de Miera, E., Kentros, C., Moreno, H., Franzen, L., Hillman, D., Baker, H., and Rudy, B. 1994. Differential expression of Shaw-related K+ channels in the rat central nervous system. J. Neurosci. 14: 949-972.
32. Weiser, M., Bueno, E., Sekirnjak, C., Martone, M.E., Baker, H., Hillman, D., et al. 1995. The potassium channel subunit KV3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons. J. Neurosci. 15: 4298-4314.
33. Yan, A., and Lennarz, W.J. 2005. Unraveling the mechanism of protein N-glycosylation. J. Biol. Chem. 280: 3121-3124. doi:10.1074/jbc. R400036200.