Role of UDP-N-Acetylglucosamine2-Epimerase/N-Acetylmannosamine Kinase (GNE) in β1-Integrin-Mediated Cell Adhesion

Molecular Neurobiology

Volumn 50, Issue 2, 2014, Pages 257-273

  Grover, Sonam ^a   Arya, Ranjana ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

Adhesion; GNE; HIBM; Localization; Sialic acid

Indexed keywords

BETA1 INTEGRIN; FIBRONECTIN; FOCAL ADHESION KINASE; LECTIN; N ACETYLMANNOSAMINE KINASE; PHOSPHOTRANSFERASE; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE 2 EPIMERASE; EPIMERASE; N ACETYLNEURAMINIC ACID; UDP ACETYLGLUCOSAMINE-2-EPIMERASE;

ARTICLE; CELL ADHESION; CELL FRACTIONATION; CELL FUNCTION; CELL INCLUSION; CELL LYSATE; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; ENZYME ACTIVITY; FOCAL ADHESION; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; HEK293 CELL LINE; HEREDITARY INCLUSION BODY MYOPATHY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; MUSCLE TISSUE; MYOPATHY; SIALYLATION; SITE DIRECTED MUTAGENESIS; VECTOR CONTROL; CELL CULTURE; GENETICS; METABOLISM; MUSCLE DISEASE; MUTATION; PHYSIOLOGY;

ANTIGENS, CD29; CARBOHYDRATE EPIMERASES; CELL ADHESION; CELL MEMBRANE; CELLS, CULTURED; HEK293 CELLS; HUMANS; MUSCULAR DISEASES; MUTATION; N-ACETYLNEURAMINIC ACID;

EID: 84911005296     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8604-6     Document Type: Article

References (64)

1. Edelman GM, Crossin KL (1991) Cell adhesion molecules: implications for a molecular histology. Annu Rev Biochem 60:155–190. doi:10.1146/annurev.bi.60.070191.001103
2. Severi E, Hood DW, Thomas GH (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153(Pt 9):2817–2822. doi:10.1099/mic.0.2007/009480-0
3. Qian J, Zhu CH, Tang S, Shen AJ, Ai J, Li J, Geng MY, Ding J (2009) Alpha2,6-hyposialylation of c-Met abolishes cell motility of ST6Gal-I-knockdown HCT116 cells. Acta Pharmacol Sin 30(7):1039–1045. doi:10.1038/aps.2009.84
4. Frenzel R, Krohn K, Eszlinger M, Tonjes A, Paschke R (2005) Sialylation of human thyrotropin receptor improves and prolongs its cell-surface expression. Mol Pharmacol 68(4):1106–1113. doi:10.1124/mol.105.012906
5. Kitazume S, Imamaki R, Ogawa K, Komi Y, Futakawa S, Kojima S, Hashimoto Y, Marth JD, Paulson JC, Taniguchi N (2010) Alpha2,6-sialic acid on platelet endothelial cell adhesion molecule (PECAM) regulates its homophilic interactions and downstream antiapoptotic signalling. J Biol Chem 285(9):6515–6521. doi:10.1074/jbc.M109.073106
6. Bennett E, Urcan MS, Tinkle SS, Koszowski AG, Levinson SR (1997) Contribution of sialic acid to the voltage dependence of sodium channel gating—a possible electrostatic mechanism. J Gen Physiol 109(3):327–343. doi:10.1085/jgp.109.3.327
7. Bi S, Baum LG (2009) Sialic acids in T cell development and function. Biochem Biophys Acta 1790(12):1599–1610. doi:10.1016/j.bbagen.2009.07.027
8. Narayanan S (1994) Sialic-acid as a tumor-marker. Ann Clin Lab Sci 24(4):376–384
9. Stasche 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-acetyl-glucosamine 2-epimerase/N-acetylmannosamine kinase. J Biol Chem 272(39):24319–24324. doi:10.1074/jbc.272.39.24319
10. Ghaderi D, Strauss HM, Reinke S, Cirak S, Reutter W, Lucka L, Hinderlich S (2007) Evidence for dynamic interplay of different oligomeric states of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase by biophysical methods. J Mol Biol 369(3):746–758. doi:10.1016/j.jmb.2007.03.037
11. Villavicencio-Lorini P, Laabs S, Danker K, Reutter W, Horstkorte R (2002) Biochemical engineering of the acyl side chain of sialic acids stimulates integrin-dependent adhesion of HL60 cells to fibronectin. J Mol Med-Jmm 80(10):671–677. doi:10.1007/s00109-002-0382-y
12. 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(6):1563–1569. doi:10.1086/302411
13. Hinderlich S, Stasche 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(39):24313–24318. doi:10.1074/jbc.272.39.24313
14. Noguchi S, Keira Y, Murayama K, Ogawa M, Fujita M, Kawahara G, Oya Y, Imazawa M, Goto Y, Hayashi YK, Nonaka I, Nishino I (2004) Reduction of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase activity and sialylation in distal myopathy with rimmed vacuoles. J Biol Chem 279(12):11402–11407. doi:10.1074/jbc.M313171200
15. Krause S, Hinderlich S, Amsili S, Horstkorte R, Wiendl H, Argov Z, Mitrani-Rosenbaum S, Lochmuller H (2005) Localization of UDP-GlcNAc 2-epimerase/ManAc kinase (GNE) in the Golgi complex and the nucleus of mammalian cells. Exp Cell Res 304(2):365–379. doi:10.1016/j.yexcr.2004.11.010
16. 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(28–29):6649–6654. doi:10.1016/j.febslet.2006.11.015
17. Amsili S, Zer H, Hinderlich S, Krause S, Becker-Cohen M, MacArthur DG, North KN, Mitrani-Rosenbaum S (2008) UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase (GNE) binds to alpha-actinin 1: novel pathways in skeletal muscle? Plos One 3(6):e2477. doi:10.1371/journal.pone.0002477
18. Wang Z, Sun Z, Li AV, Yarema KJ (2006) Roles for UDP-GlcNAc 2-epimerase/ManNAc 6-kinase outside of sialic acid biosynthesis: modulation of sialyltransferase and BiP expression, GM3 and GD3 biosynthesis, proliferation, and apoptosis, and ERK1/2 phosphorylation. J Biol Chem 281(37):27016–27028. doi:10.1074/jbc.M604903200
19. Eisenberg I, Avidan N, Potikha T, Hochner H, Chen M, Olender T, Barash M, Shemesh M, Sadeh M, Grabov-Nardini G, Shmilevich I, Friedmann A, Karpati G, Bradley WG, Baumbach L, Lancet D, Ben Asher E, Beckmann JS, Argov Z, Mitrani-Rosenbaum S (2001) The UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase gene is mutated in recessive hereditary inclusion body myopathy. Nat Genet 29(1):83–87. doi:10.1038/ng718
20. Seppala R, Tietze F, Krasnewich D, Weiss P, Ashwell G, Barsh G, Thomas GH, Packman S, Gahl WA (1991) Sialic acid metabolism in sialuria fibroblasts. J Biol Chem 266(12):7456–7461
21. Tasca G, Ricci E, Monforte M, Laschena F, Ottaviani P, Rodolico C, Barca E, Silvestri G, Iannaccone E, Mirabella M, Broccolini A (2012) Muscle imaging findings in GNE myopathy. J Neurol 259(7):1358–1365. doi:10.1007/s00415-011-6357-6
22. Yoshimura M, Monma K, Suzuki N, Aoki M, Kumamoto T, Tanaka K, Tomimitsu H, Nakano S, Sonoo M, Shimizu J, Sugie K, Nakamura H, Oya Y, Hayashi YK, Malicdan MC, Noguchi S, Murata M, Nishino I (2012) Heterozygous UDP-GlcNAc 2-epimerase and N-acetylmannosamine kinase domain mutations in the GNE gene result in a less severe GNE myopathy phenotype compared to homozygous N-acetylmannosamine kinase domain mutations. J Neurol Sci 318(1–2):100–105. doi:10.1016/j.jns.2012.03.016
23. Argov Z, Eisenberg I, Grabov-Nardini G, Sadeh M, Wirguin I, Soffer D, Mitrani-Rosenbaum S (2003) Hereditary inclusion body myopathy: the Middle Eastern genetic cluster. Neurology 60(9):1519–1523
24. Park YE, Kim HS, Choi ES, Shin JH, Kim SY, Son EH, Lee CH, Kim DS (2012) Limb-girdle phenotype is frequent in patients with myopathy associated with GNE mutations. J Neurol Sci 321(1–2):77–81. doi:10.1016/j.jns.2012.07.061
25. 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 U S A 99(8):5267–5270. doi:http://www.ncbi.nlm.nih.gov/pubmed/11929971
26. Malicdan MC, Noguchi S, Nonaka I, Hayashi YK, Nishino I (2007) A Gne knockout mouse expressing human GNE D176V mutation develops features similar to distal myopathy with rimmed vacuoles or hereditary inclusion body myopathy. Hum Mol Genet 16(22):2669–2682. doi:10.1093/hmg/ddm220
27. Ito M, Sugihara K, Asaka T, Toyama T, Yoshihara T, Furuichi K, Wada T, Asano M (2012) Glycoprotein hyposialylation gives rise to a nephrotic-like syndrome that is prevented by sialic acid administration in GNE V572L point-mutant mice. PLoS One 7(1):e29873. doi:10.1371/journal.pone.0029873
28. Sela I, Milman Krentsis I, Shlomai Z, Sadeh M, Dabby R, Argov Z, Ben-Bassat H, Mitrani-Rosenbaum S (2011) The proteomic profile of hereditary inclusion body myopathy. PLoS One 6(1):e16334. doi:10.1371/journal.pone.0016334
29. Carson JA, Wei L (2000) Integrin signalling’s potential for mediating gene expression in hypertrophying skeletal muscle. J Appl Physiol 88(1):337–343
30. Perkins AD, Ellis SJ, Asghari P, Shamsian A, Moore ED, Tanentzapf G (2010) Integrin-mediated adhesion maintains sarcomeric integrity. Dev Biol 338(1):15–27. doi:10.1016/j.ydbio.2009.10.034
31. Semel AC, Seales EC, Singhal A, Eklund EA, Colley KJ, Bellis SL (2002) Hyposialylation of integrins stimulates the activity of myeloid fibronectin receptors. J Biol Chem 277(36):32830–32836. doi:10.1074/jbc.M202493200
32. Ricci E, Broccolini A, Gidaro T, Morosetti R, Gliubizzi C, Frusciante R, Di Lella GM, Tonali PA, Mirabella M (2006) NCAM is hyposialylated in hereditary inclusion body myopathy due to GNE mutations. Neurology 66(5):755–758
33. Huizing M, Rakocevic G, Sparks SE, Mamali L, Shatunov A, Goldfarb L, Krasnewich D, Gahl WA, Dalakas MC (2004) Hypoglycosylation of alpha-dystroglycan in patients with hereditary IBM due to GNE mutations. Mol Genet Metab 81(3):196–202. doi:10.1016/j.ymgme.2003.11.012
34. 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. Glycoconjugate J 24(2–3):125–130. doi:10.1007/s10719-006-9019-7
35. Broccolini A, Gidaro T, De Cristofaro R, Morosetti R, Gliubizzi C, Ricci E, Tonali PA, Mirabella M (2008) Hyposialylation of neprilysin possibly affects its expression and enzymatic activity in hereditary inclusion-body myopathy muscle. J Neurochem 105(3):971–981. doi:10.1111/j.1471-4159.2007.05208.x
36. Pretzlaff RK, Xue VW, Rowin ME (2000) Sialidase treatment exposes the beta1-integrin active ligand binding site on HL60 cells and increases binding to fibronectin. Cell Adhes Commun 7(6):491–500
37. Penner J, Mantey LR, Elgavish S, Ghaderi D, Cirak S, Berger M, Krause S, Lucka L, Voit T, Mitrani-Rosenbaum S, Hinderlich S (2006) Influence of UDP-GlcNAc 2-epimerase/ManNAc kinase mutant proteins on hereditary inclusion body myopathy. Biochemistry 45(9):2968–2977. doi:10.1021/bi0522504
38. Sparks SE, Ciccone C, Lalor M, Orvisky E, Klootwijk R, Savelkoul PJ, Dalakas MC, Krasnewich DM, Gahl WA, Huizing M (2005) Use of a cell-free system to determine UDP-N-acetylglucosamine 2-epimerase and N-acetylmannosamine kinase activities in human hereditary inclusion body myopathy. Glycobiology 15(11):1102–1110. doi:10.1093/glycob/cwi100
39. Effertz K, Hinderlich S, Reutter W (1999) Selective loss of either the epimerase or kinase activity of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase due to site-directed mutagenesis based on sequence alignments. J Biol Chem 274(40):28771–28778. doi:10.1074/jbc.274.40.28771
40. Blume A, Ghaderi D, Liebich V, Hinderlich S, Donner P, Reutter W, Lucka L (2004) UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase, functionally expressed in and purified from Escherichia coli, yeast, and insect cells. Protein Expres Purif 35(2):387–396. doi:10.1016/j.pep.2004.02.013
41. Harburger DS, Calderwood DA (2009) Integrin signalling at a glance. J Cell Sci 122(2):159–163. doi:10.1242/Jcs.018093
42. Shi Q, Boettiger D (2003) A novel mode for integrin-mediated signaling: tethering is required for phosphorylation of FAK Y397. Mol Biol Cell 14(10):4306–4315. doi:10.1091/mbc.E03-01-0046
43. Malicdan MCV, 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–U127. doi:10.1038/Nm.1956
44. Tomimitsu H, Ishikawa K, Shimizu J, Ohkoshi N, Kanazawa I, Mizusawa H (2002) Distal myopathy with rimmed vacuoles: novel mutations in the GNE gene. Neurology 59(3):451–454
45. Saito F, Tomimitsu H, Arai K, Nakai S, Kanda T, Shimizu T, Mizusawa H, Matsumura K (2004) A Japanese patient with distal myopathy with rimmed vacuoles: missense mutations in the epimerase domain of the UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase (GNE) gene accompanied by hyposialylation of skeletal muscle glycoproteins. Neuromuscul Disord 14(2):158–161. doi:10.1016/j.nmd.2003.09.006
46. Salama I, Hinderlich S, Shlomai Z, Eisenberg I, Krause S, Yarema K, Argov Z, Lochmuller H, Reutter W, Dabby R, Sadeh M, Ben-Bassat H, Mitrani-Rosenbaum S (2005) No overall hyposialylation in hereditary inclusion body myopathy myoblasts carrying the homozygous M712T GNE mutation. Biochem Bioph Res Co 328(1):221–226. doi:10.1016/j.bbrc.2004.12.157
47. Keppler OT, Hinderlich S, Langner J, Schwartz-Albiez R, Reutter W, Pawlita M (1999) UDP-GlcNAc 2-epimerase: a regulator of cell surface sialylation. Science 284(5418):1372–1376
48. Argov Z, Mitrani-Rosenbaum S (2008) The hereditary inclusion body myopathy enigma and its future therapy. Neurotherapeutics 5(4):633–637. doi:10.1016/j.nurt.2008.07.004
49. Li HH, Chen Q, Liu FC, Zhang XM, Li W, Liu SP, Zhao YY, Gong YQ, Yan CZ (2013) Unfolded protein response and activated degradative pathways regulation in GNE myopathy. PLoS One 8 (3). doi:10.1371/journal.pone.0058116
50. Bendas G, Borsig L (2012) Cancer cell adhesion and metastasis: selectins, integrins, and the inhibitory potential of heparins. Int J Cell Biol 2012:676731. doi:10.1155/2012/676731
51. Hynes RO, Yamada KM (1982) Fibronectins: multifunctional modular glycoproteins. J Cell Biol 95(2 Pt 1):369–377
52. Pan D, Song Y (2010) Role of altered sialylation of the I-like domain of beta1 integrin in the binding of fibronectin to beta1 integrin: thermodynamics and conformational analyses. Biophys J 99(1):208–217. doi:10.1016/j.bpj.2010.03.063
53. Seales EC, Shaikh FM, Woodard-Grice AV, Aggarwal P, McBrayer AC, Hennessy KM, Bellis SL (2005) A protein kinase C/Ras/ERK signaling pathway activates myeloid fibronectin receptors by altering beta1 integrin sialylation. J Biol Chem 280(45):37610–37615. doi:10.1074/jbc.M508476200
54. Disatnik MH, Boutet SC, Lee CH, Mochly-Rosen D, Rando TA (2002) Sequential activation of individual PKC isozymes in integrin-mediated muscle cell spreading: a role for MARCKS in an integrin signaling pathway. J Cell Sci 115(Pt 10):2151–2163
55. Lowin T, Straub RH, Neumann E, Bosserhoff A, Vogel C, Moissl C, Anders S, Muller-Ladner U, Schedel J (2009) Glucocorticoids increase alpha 5 integrin expression and adhesion of synovial fibroblasts but inhibit ERK signaling, migration, and cartilage invasion. Arthritis Rheum 60(12):3623–3632. doi:10.1002/Art.24985
56. Sinanan ACM, Machell JRA, Wynne-Hughes GT, Hunt NP, Lewis MR (2008) Alpha v beta 3 and alpha v beta 5 integrins and their role in muscle precursor cell adhesion. Biol Cell 100(8):465–477. doi:10.1042/Bc20070115
57. Mayer U (2003) Integrins: redundant or important players in skeletal muscle? J Biol Chem 278(17):14587–14590. doi:10.1074/jbc.R200022200
58. Galeano B, Klootwijk R, Manoli I, Sun M, Ciccone C, Darvish D, Starost MF, Zerfas PM, Hoffmann VJ, Hoogstraten-Miller S, Krasnewich DM, Gahl WA, Huizing M (2007) Mutation in the key enzyme of sialic acid biosynthesis causes severe glomerular proteinuria and is rescued by N-acetylmannosamine. J Clin Invest 117(6):1585–1594. doi:10.1172/Jci30954
59. Takeda T, McQuistan T, Orlando RA, Farquhar MG (2001) Loss of glomerular foot processes is associated with uncoupling of podocalyxin from the actin cytoskeleton. J Clin Invest 108(2):289–301. doi:10.1172/Jci12539
60. Arya R, Kedar V, Hwang JR, McDonough H, Li HH, Taylor J, Patterson C (2004) Muscle ring finger protein-1 inhibits PKC epsilon activation and prevents cardiomyocyte hypertrophy. J Cell Biol 167(6):1147–1159. doi:10.1083/jcb.200402033
61. William E, Balch WGD, Braell WA, Rothman JE (1984) Reconstitution of the transport of protein between successive compartments of the golgi measured by the coupled incorporation of N-acetylglucosamine. Cell 39:405–416
62. Homer KA, Roberts G, Byers HL, Tarelli E, Whiley RA, Philpott-Howard J, Beighton D (2001) Mannosidase production by viridans group streptococci. J Clin Microbiol 39(3):995–1001. doi:10.1128/JCM.39.3.995-1001.2001
63. Blume A, Chen H, Reutter W, Schmidt RR, Hinderlich S (2002) 2′,3′-Dialdehydo-UDP-N-acetylglucosamine inhibits UDP-N-acetylglucosamine 2-epimerase, the key enzyme of sialic acid biosynthesis. Febs Lett 521(1–3):127–132. doi:10.1016/S0014-5793(02)02856-9
64. Reissig JL, Storminger JL, Leloir LF (1955) A modified colorimetric method for the estimation of N-acetylamino sugars. J Biol Chem 217(2):959–966