Lessons from GNE-deficient embryonic stem cells: Sialic acid biosynthesis is involved in proliferation and gene expression

Glycobiology

Volumn 20, Issue 1, 2010, Pages 107-117

  Weidemann, Wenke ^a   Klukas, Christian ^b   Klein, Andreas ^c   Simm, Andreas ^d   Schreiber, Falk ^a,b   Horstkorte, Rüdiger ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d Department of Cardio Thoracic Surgery ^*  (Germany)

Author keywords

Cell differentiation; N acetylmannosamine; N acetylmannosamine kinase; UDP N acetylglucosamine 2 epimerase

Indexed keywords

AMINOSUGAR; N ACETYLMANNOSAMINE KINASE; SIALIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME ACTIVITY; ENZYME INACTIVATION; GENE EXPRESSION; GENE FREQUENCY; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC TRAIT; GENETIC VARIABILITY; GENOTYPE; INTRON; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; WILD TYPE;

ALLELES; ANIMALS; CELL PROLIFERATION; EMBRYONIC STEM CELLS; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; HEXOSAMINES; MICE; N-ACETYLNEURAMINIC ACID; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EUKARYOTA; MUS;

EID: 70849098887     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp153     Document Type: Article

References (54)

1. Amsili S, Zer H, Hinderlich S, Krause S, Becker-Cohen M, MacAthur DG, North KN, Mitrani-Rosenbaum S. 2008. UDP-A-acetylglucosamine 2-epimerase/ N-acetylmannosamine kinase (GNE) binds to alpha actinin1: Novel pathway in skeletal muscle? Plos One. 3(6):e2477.
2. Barbacid M. 1995. Neurotrophic factors and their receptors. Curr Opin Cell Biol. 7(2):148-155.
3. Cainarca S, Messali S, Ballabio A, Meroni G. 1999. Functional characterization of the Opitz syndrome gene product (midin): Evidence for homodimerization and association with microtubules throughout the cell cycle. Hum Mol Genet. 8(8):1387-1396.
4. Eisenberg I, Avidan N, Potikha T, Hochner H, Chen M, Olender T, Barash M, Shemesh M, Sadeh M, Grabov-Nardini G, et al. 2001. The UDP-N acetylglucosamine 2-epimerase/N-acetylmannosamine kinase gene is mutated in recessive hereditary inclusion body myopathy. Nat Genet 29:83-87.
5. Eisenberg I, Novershtern N, Itzhaki Z, Becker-CohenM, Sadeh M, Willems PH, Friedman N, Koopman WJ, Mitrani-Rosenbaum S. 2008. Mitochondrial processes are impaired in hereditary inclusion body myopathy. Hum Mol Genet. 17(23):3663-3674.
6. Gagiannis D, Orthmann A, Danßmann I, Schwarzkopf M, Weidemann W, Horstkorte R. 2007. Reduced sialylation status in UDP-N acetylglucosamine-2-epimerase/N-acetylmannosamine kinase (GNE)-deficient mice. Glycoconj J. 24:125-130.
7. Hahnel AC, Rappolee DA, Millan JL, Manes T, Ziomek CA, Theodosiou NG, Werb Z, Pedersen RA, Schultz GA. 1990. Two alkaline phosphates genes are expressed during early development in the mouse embryo. Development 110:555-564.
8. Hinderlich S, Stäsche R, Zeitler R, Reutter W. 1997. A bifunctional enzyme catalyzes the first two steps in N-acetylneuraminic acid biosynthesis of rat liver. Purification and characterization of UDP-N acetylglucosamine 2-epimerase/N-acetylmannosamine kinase. J Biol Chem. 272:24313-24318.
9. Hishikawa K, Marumo T, Miura S, Nakanishi A, Matsuzaki Y, Shibata K, Ichiyanagi T, Kohike H, Komori T, Takahashi I, et al. 2005. Musculin/ MyoR is expressed in kidney side population cells and can regulate their function. J Cell Biol. 169(6):921-928.
10. Horstkorte R, Nöhring S, Reutter W, Effertz K, Lucka L, Danker K. 2000. Protein kinase C phosphorylates and activates UDP-N acetylglucosamine-2-epimerase/N-acetyl-mannosaminekinase. FEBS Lett. 470:315-318.
11. Horstkorte R, Nöhring S, Wiechens N, Schwarzkopf M, Danker K, Reutter W, Lucka L. 1999. Tissue expression and amino acid sequence of the murine UDP-N-acetylglucosamine-2-epimerase/N acetylmannosaminekinase. Eur J Biochem. 260:923-927.
12. Inoue J, Gohda J, Akiyama T. 2007. Characteristics and biological functions of TRAF6. Adv Exp Med Biol. 597:72-79.
13. Itoh N. 2007. The Fgf families in humans, mice, and zebrafish: Their evolutional processes and roles in development, metabolism, and disease. Biol Pharm Bull. 30:1819-1825.
14. Ivatt RJ. 1987. Transient expression of sialylated glycans during glycoprotein processing by embryonal carcinomas. Biochem Biophys Res Commun. 142:489-495.
15. Junker BH, Klukas C, Schreiber F. 2006. VANTED: A system for advanced data analysis and visualization in the context of biological networks. BMC Bioinformatics. 7:e109.
16. Kanehisa M, Goto S, Kawashima S, Nakaya A. 2002. The KEGG databases at GenomeNet. Nucl Acids Res. 30(1):42-46.
17. Keppler O, Horstkorte R, Pawlita M, Schmidt C, Reutter W. 2001. Biochemical engineering of the N-acyl side chain of sialic acid: Biological implications. Glycobiology. 11:11R-18R.
18. Kontou M, Bauer C, Reutter W, Horstkorte R. 2008. Sialic acid metabolism is involved in the regulation of gene expression during neuronal differentiation of PC12 cells. Glycoconj J. 25:237-244.
19. Lanctot PM, Gage FH, Varki AP. 2007. The glycans of stem cells. Curr Opin Chem Biol. 11:373-380.
20. Lucka L, Krause M, Danker K, Reutter W, Horstkorte R. 1999. Primary structure and expression analysis of the human UDP-N acetylglucosamine-2-epimerase/N-acetylmannosaminekinase, the bifunctional enzyme in neuraminic acid biosynthesis. FEBS Lett. 454:341-344.
21. Malicdan MC, Noguchi S, Hayashi YK, Nonaka I, Nishino I. 2009. Prophylactic treatment with sialic acid metabolites precludes the development of the myopathic phenotype in the DMRV-hIBM mouse model. Nat Med. 15(6):690-695.
22. MalicdanMC, Noguchi S, Nishino I. 2008. Recent advances in distal myopathy with rimmed vacuoles(DMRV) or hIBM: Treatment perspectives. Curr Opin Neurol. 21:596-600.
23. Maness LM, Kastian AJ,Weber JT, BanksWA, Beckman BS, Zadina JE. 1994. The neurotrophins and their receptors: Structure, function, and neuropathology. Neurosci Biobehav Rev. 18(1):143-159.
24. Morrison DK, Davis RJ. 2003. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol. 19:91-118.
25. Pease S, Braghetta P, Gearing D, Grail D, Williams RL. 1990. Isolation of embryonic stem (ES) cells in media supplemented with recombinant leukemia inhibitory factor (LIF). Dev Biol. 141(2):344-352.
26. Pietsch EC, Sykes SM, McMahon SB, Murphy ME. 2008. The p53 family and programmed cell death. Oncogene. 27(50):6507-6521.
27. Qiao X, Lu JY, Hofmann SL. 2007. Gene expression profiling in a mouse model of infatile neuronal ceroid lipofuscinosis reveals upregulation of immediate early genes and mediators of the inflammatory response. BMC Neurosci. 8:95.
28. Qin W, Zhou Q, Yang LC, Li Z, Su BH, Luo H, Fan JM. 2005. Peripheral B lymphocyte β1,3-galactosyltransferase and chaperone expression in immunoglobulin A nephropathy. J Intern Med. 258(5):467-477.
29. Quaderi NA, Schweiger S, Gaudenz K, Rugarli EI, Berger W, Feldman GJ, Volta M, Andolfi G, Gilgenkrantz S, Marion RW et al. 1997. Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22. Nat Genet. 17(3):285-291.
30. Robb L, Hartley L, Wang CC, Harvey RP, Begley CG. 1998. Musculin: A murine basic helix-loop-helix transcription factor gene expressed in embryonic skeletal muscle. Mech Dev. 76(1-2):197-201.
31. Schauer R. 1982. Chemistry, metabolism and biological functions of sialic acids. Adv Carbohydr Chem Biochem. 40:131-234.
32. Schauer R. 2000. Achievements and challenges of sialic acid research. Glycoconj J. 17:485-499.
33. Schöler HR, Dressler GR, Balling R, Rohdewohld H, Gruss P. 1990. Oct-4: A germlinespecific transcription factor mapping to the mouse t-complex. EMBO J. 9:2185-2195.
34. Schwarzkopf M, Knobeloch KP, Rohde E, Hinderlich S, Wiechens N, Lucka L, Horak I, Reutter W, Horstkorte R. 2002. Sialylation is essential for early development in mice. Proc Natl Acad Sci USA. 99:5267-5270.
35. Schweiger S, Foerster J, Lehmann T, Suckow V, Muller YA, Walter G, Davies T, Porter H, van Bokhoven H, Lunt PW et al. 1999. The Opitz syndrome gene product, MID1, assiciates with microtubules. Proc Natl Acad Sci. 96(6):2794-2799.
36. Seppala R, Lehto VP, Gahl WA. 1999. Mutations in the human UDP-N acetylglucosamine 2-epimerase gene define the disease sialuria and the allosteric site of the enzyme. Am J Hum Genet. 64:1563-1569.
37. Settleman J. 2007. PAK-in' up cGMP for the move. Cell. 128:237-238.
38. Shoyab M, Bachhawat BK. 1969. Partial purification and properties of cytidin 5′-monophospho-N-acetyl neuraminic acid degrading enzyme from sheep liver. Indian J Biochem. 6(2):56-62.
39. Solter D, Knowles BB. 1978. Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci USA. 75:5565-5569.
40. Soulet L, Chevet E, Lemaitre G, Blanquaert F, Meddahi A, Barritault D. 1994. FGFs and their receptors, in vitro and in vivo studies: New FGF receptor in the brain, FGF-1 in muscle, and the use of functional analogues of low-affinity heparin-binding growth factor receptors in tissue repair. Mol Reprod Dev. 39(1):49-54.
41. Stachowiak MK, Maher PA, Stachowiak EK. 2007. Integrative nuclear signalling in cell development - a role for FGF receptor-1. DNA Cell Biol. 26(12):811-826.
42. Stäsche R, Hinderlich S, Weise C, Effertz K, Lucka L, Moormann P, Reutter W. 1997. A bifunctional enzyme catalyzes the first two steps in N-acetylneuraminic acid biosynthesis of rat liver. Molecular cloning and functional expression of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase. J Biol Chem. 272:24319-24324.
43. Trockenbacher A, Suckow V, Foerster J, Winter J, Krauss S, Ropers HH, Schneider R, Schweiger S. 2001. MID1, mutated in Opitz syndrome, encodes an ubiquitin ligase that targets phosphatase 2A for degradation. Nat Genet. 29(3):287-294.
44. Van Den Veyver IB, Cormier TA, Jurecic V, Baldini A, Zoghbi HY. 1998. Characterization and physical mapping in human and mouse of a novel RING finger gene in Xp22. Genomics. 51(2):251-261.
45. Van Dijk W, Lasthuis AM, Trippelvitz LA, Muilerman HG. 1983. Increased glycosylation capacity in regenerating rat liver is paralleled by decreased activities of CMP-N-acetylneuraminate hydrolase and UDP-galactose pyrophosphatase. Biochem J. 214(3):1003-1006.
46. Van Dijk W, Maier H, Van Den Eijnden DH. 1977. CMP-N acetylneuraminic acid hydrolase, an ectoenzyme distributed unevenly over the hepatocyte surface. Biochim Biophys Acta. 466(1):187-197.
47. Varki A. 1992. Diversity in the sialic acids. Glycobiology. 2:25-40.
48. Wang Z, Sun Z, Li AV, Yaremea KJ. 2006. Roles for UDP-GlcNAc 2-epimease/ ManNAc-kinase outside if sialic acid biosynthesis. J Biol Chem. 281:27016-27028.
49. Weidemann W, Stelzl U, Lisewski U, Bork K, Wanker EE, Hinderlich S, Horstkorte R. 2006. The collapsin response mediator protein 1 (CRMP-1) and the promyelocytic leukemia zinc finger protein (PLZF) bind to UDP- N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase (GNE), the key enzyme of sialic acid biosynthesis. FEBS Lett. 580:6649-6654.
50. Werner S. 1998. Keratinocyte growth factor: A unique player in epithelial repair processes. Cytokine Growth Factor Rev. 9(2):153-165.
51. Xia L, McEver RP. 2006. Targeted disruption of the gene encoding core 1 beta1-3-galactosyltransferase (T-synthase) causes embryonic lethality and defective angiogenesis in mice. Methods Enzymol. 416:314-331.
52. Yu L, Sangster N, Perez A, McCormick PJ. 2004. The bHLH protein MyoR inhibits the differentiation of early embryonic endoderm. Differentiation. 72(7):341-347.
53. Zeitler R, Banzer JP, Bauer C, Reutter W. 1992. Inhibition of the biosynthesis of N-acetylneuraminic acid by metal ions and selenium in vitro. Biometals. 5:103-109.
54. Zhao P, Hoffman EP. 2006. Musculin isoforms and repression of MyoD in muscle regeneration. Biochem Biophys Res Commun. 342(3):835-842.