Glycosylation-related gene expression profiling in the brain and spleen of scrapie-affected mouse

Glycobiology

Volumn 19, Issue 8, 2009, Pages 879-889

  Guillerme Bosselut, Florence ^a   Forestier, Lionel ^a   Jayat Vignoles, Chantal ^b   Vilotte, Jean Luc ^c   Popa, Iuliana ^d,e   Portoukalian, Jacques ^d   Le Dur, Annick ^f   Laude, Hubert ^f   Julien, Raymond ^a   Gallet, Paul François ^a  

^a UNIVERSITY OF LIMOGES   (France)

^b UNIVERSITÉ DE LIMOGES   (France)

^c UMR1313 GÉNÉTIQUE ANIMALE ET BIOLOGIE INTÉGRATIVE   (France)

^d UNIVERSITÉ LYON 1   (France)

^e PETRU PONI INSTITUTE OF MACROMOLECULAR CHEMISTRY   (Romania)

^f INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Brain; Gene expression; Microarray; Prion disease; Speen

Indexed keywords

GALACTOSYLCERAMIDASE; GANGLIOSIDE GM3; GLYCOSIDASE; GLYCOSYLTRANSFERASE; LECTIN; MESSENGER RNA; SULFOTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC VARIABILITY; GLYCOSYLATION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SCRAPIE; SPLEEN; UPREGULATION;

ANIMALS; BRAIN; FEMALE; GENE EXPRESSION PROFILING; GLYCOPROTEINS; GLYCOSYLATION; MICE; MICROARRAY ANALYSIS; PRPSC PROTEINS; SCRAPIE; SPLEEN;

MUS;

EID: 66249119564     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp062     Document Type: Article

References (74)

1. Adjou KT, Simoneau S, Sales N, Lamoury F, Dormont D, Papy-Garcia D, Barritault D, Deslys JP, Lasmezas CI. 2003. A novel generation of heparan sulfate mimetics for the treatment of prion diseases. J Gen Virol. 84:2595-2603.
2. Aguzzi A, Heikenwalder M. 2006. Pathogenesis of prion diseases:CUrrent status and future outlook. Nat Rev Microbiol. 4:765-775.
3. Ando S, Toyoda Y, Nagai Y, Ikuta F. 1984. Alterations in brain gangliosides and other lipids of patients with Creutzfeldt-Jakob disease and subacute sclerosing panencephalitis (SSPE). Japan J Exp Med. 54:229-234.
4. Azuma Y, Sato H, Higai K, Matsumoto K. 2007. Enhanced expression of membrane-associated sialidase Neu3 decreases GD3 and increases GM3 on the surface of Jurkat cells during etoposide-induced apoptosis. Biol Pharm Bull. 30:1680-1684.
5. 4 hyposulfation. J Biol Chem. 280:10516-10523.
6. Bodennec J, Brichon G, Zwingelstein G, Portoukalian J. 2000. Purification of sphingolipid classes by solid-phase extraction with aminopropyl and weak cation exchanger cartridges. Methods Enzymol. 312:101-114.
7. Bouchon B, Portoukalian J, Bornet H. 1985. Sex-specific difference of the galabiosylceramide level in the glycosphingolipids of human thyroid. Biochim Biophys Acta. 836:143-152.
8. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248-254.
9. Brown AR, Rebus S, McKimmie CS, Robertson K, Williams A, Fazakerley JK. 2005. Gene expression profiling of the preclinical scrapie-infected hippocampus. Biochem Biophys Res Commun. 334:86-95.
10. Caughey B, Baron GS. 2006. Prions and their partners in crime. Nature 443:803-810.
11. Comelli EM, Head SR, Gilmartin T, Whisenant T, Haslam SM, North SJ,Wong NK, Kudo T, Narimatsu H, Esko JD, et al. 2006. A focused microarray approach to functional glycomics: Transcriptional regulation of the glycome. Glycobiology. 16:117-131.
12. Cosseddu GM, Andreoletti O, Maestrale C, Robert B, Ligios C, Piumi F, Agrimi U, Vaiman D. 2007. Gene expression profiling on sheep brain reveals differential transcripts in scrapie-affected/not-affected animals. Brain Res. 1142:217-222.
13. Dandoy-Dron F, Guillo F, Benboudjema L, Deslys JP, Lasmezas C, Dormont D, Tovey MG, Dron M. 1998. Gene expression in scrapie. Cloning of a new scrapie-responsive gene and the identification of increased levels of seven other mRNA transcripts. J Biol Chem. 273:7691-7697.
14. Di Martino A, Safar J, Callegaro L, Salem N Jr, Gibbs CJ Jr. 1993. Ganglioside composition changes in spongiform encephalopathies: Analyses of 263K scrapie-infected hamster brains. Neurochem Res. 18:907-913.
15. Diaz C, Vitezica ZG, Rupp R, Andreoletti O, Elsen JM. 2005. Polygenic variation and transmission factors involved in the resistance/ susceptibility to scrapie in a Romanov flock. J Gen Virol. 86:849-857.
16. Dong DL, Hart GW. 1994. Purification and characterization of an O GlcNAc selective N-acetyl-beta-d-glucosaminidase from rat spleen cytosol. J Biol Chem. 269:19321-19330.
17. Endo T, Groth D, Prusiner SB, Kobata A. 1989. Diversity of oligosaccharide structures linked to asparagines of the scrapie prion protein. Biochemistry. 28:8380-8388.
18. Fantini J, Garmy N, Mahfoud R, Yahi N. 2002. Lipid rafts: Structure, function and role in HIV, Alzheimer's and prion diseases. Expert Rev Mol Med. 4:1-22.
19. Fewster ME, Burns BJ, Mead JF. 1969. Quantitative densitometric thin-layer chromatography of lipids using copper acetate reagent. J Chromatogr. 43:120-126.
20. Fusco M, Vantini G, Schiavo N, Zanotti A, Zanoni R, Facci L, Skaper SD. 1993. Gangliosides and neurotrophic factors in neurodegenerative diseases: From experimental findings to clinical perspectives. Ann N Y Acad Sci. 695:314-317.
21. Giraudo CG, Maccioni HJ. 2003. Ganglioside glycosyltransferases organize in distinct multienzyme complexes in CHO-K1 cells. J Biol Chem. 278:40262-40271.
22. Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA, Samyn-Petit B, Julien S, Delannoy P. 2001. The human sialyltransferase family. Biochimie. 83:727-737.
23. Hong Y, Ohishi K, Watanabe R, Endo Y, Maeda Y, Kinoshita T. 1999. GPI1 stabilizes an enzyme essential in the first step of glycosylphosphatidylinositol biosynthesis. J Biol Chem. 274:18582-18588.
24. Hounsell EF. 2004. Prions in control of cell glycosylation. Biochem J 380:e5-6.
25. Ichikawa S, Sakiyama H, Suzuki G, Hidari KI, Hirabayashi Y. 1996. Expression cloning of a cDNA for human ceramide glucosyltransferase that catalyzes the first glycosylation step of glycosphingolipid synthesis. Proc Natl Acad Sci USA. 93:12654.
26. Inoue Y, Yamakawa Y, Sakudo A, Kinumi T, Nakamura Y, Matsumoto Y, Saeki K, Kamiyama T, Onodera T, Nishijima M. 2005. Infection route-independent accumulation of splenic abnormal prion protein. Japan J Infect Dis 58:78-82.
27. Irie F, Hashikawa T, Tai T, Seyama Y, Hirabayashi Y. 1994. Distribution of cholinergic neuron-specific gangliosides (GT1a alpha and GQ1b alpha) in the rat central nervous system. Brain Res. 665:161-166.
28. Ishikura N, Clever JL, Bouzamondo-Bernstein E, Samayoa E, Prusiner SB, Huang EJ, DeArmond SJ. 2005. Notch-1 activation and dendritic atrophy in prion disease. Proc Natl Acad Sci USA. 102:886-891.
29. Jou I, Lee JH, Park SY,Yoon HJ, Joe EH, Park EJ. 2006. Gangliosides trigger inflammatory responses via TLR4 in brain glia. Am J Pathol 168:1619-1630.
30. Jourdian GW, Dean L, Roseman S. 1971. The sialic acids: XI. A periodate-resorcinol method for the quantitative estimation of free sialic acids and their glycosides. J Biol Chem. 246:430-435.
31. Katoh Y, Katoh M. 2006. Hedgehog signaling pathway and gastrointestinal stem cell signaling network (review). Int J Mol Med. 18:1019-1023.
32. Klein TR, Kirsch D, Kaufmann R, Riesner D. 1998. Prion rods contain small amounts of two host sphingolipids as revealed by thin-layer chromatography and mass spectrometry. Biol Chem. 379:655-666.
33. Kono M, Takashima S, Liu H, Inoue M, Kojima N, Lee YC, Hamamoto T, Tsuji S. 1998. Molecular cloning and functional expression of a fifth-type alpha 2,3-sialyltransferase (mST3Gal V:GM3 synthase). Biochem Biophys Res Commun. 253:170-175.
34. Kopacek J, Sakaguchi S, Shigematsu K, Nishida N, Atarashi R, Nakaoke R, Moriuchi R, Niwa M, Katamine S. 2000. Upregulation of the genes encoding lysosomal hydrolases, a perforin-like protein, and peroxidases in the brains of mice affected with an experimental prion disease. J Virol 74:411-417.
35. Laszlo L, Lowe J, Self T, Kenward N, Landon M, McBride T, Farquhar C, McConnell I, Brown J, Hope J, et al. 1992. Lysosomes as key organelles in the pathogenesis of prion encephalopathies. J Pathol. 166:333-341.
36. Laude H, Vilette D, Le Dur A, Archer F, Soulier S, Besnard N, Essalmani R, Vilotte JL. 2002. New in vivo and ex vivo models for the experimental study of sheep scrapie: Development and perspectives. C R Biol. 325:49-57.
37. Lowe JB. 2003. Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr Opin Cell Biol. 15:531-538.
38. Mattei V, Barenco MG, Tasciotti V, Garofalo T, Longo A, Boller K, Lower J, Misasi R, Montrasio F, Sorice M. 2009. Paracrine diffusion of PrP(C) and propagation of prion infectivity by plasma membrane-derived microvesicles. PLoS ONE. 4:e5057.
39. Mattei V, Garofalo T, Misasi R, Circella A, Manganelli V, Lucania G, Pavan A, Sorice M. 2004. Prion protein is a component of the multimolecular signaling complex involved in T cell activation. FEBS Lett. 560:14-18.
40. Mattei V, Garofalo T, Misasi R, Gizzi C, Mascellino MT, Dolo V, Pontieri GM, Sorice M, Pavan A. 2002. Association of cellular prion protein with gangliosides in plasma membrane microdomains of neural and lymphocytic cells. Neurochem Res. 27:743-749.
41. McGovern G, Jeffrey M. 2007. Scrapie-specific pathology of sheep lymphoid tissues. PLoS ONE. 2:e1304.
42. McKinley MP, Taraboulos A, Kenaga L, Serban D, Stieber A, DeArmond SJ, Prusiner SB, Gonatas N. 1991. Ultrastructural localization of scrapie prion proteins in cytoplasmic vesicles of infected cultured cells. Lab Invest. 65:622-630.
43. Milhiet PE, Vacherot F, Caruelle JP, Barritault D, Caruelle D, Courty J. 1998. Upregulation of the angiogenic factor heparin affin regulatory peptide by progesterone in rat uterus. J Endocrinol. 158:389-399.
44. Nasirikenari M, Segal BH, Ostberg JR, Urbasic A, Lau JT. 2006. Altered granulopoietic profile and exaggerated acute neutrophilic inflammation in mice with targeted deficiency in the sialyltransferase ST6Gal I. Blood. 108:3397-3405.
45. Naslavsky N, Stein R, Yanai A, Friedlander G, Taraboulos A. 1997. Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J Biol Chem. 272:6324-6331.
46. Nielsen D, Gyllberg H, Ostlund P, Bergman T, Bedecs K. 2004. Increased levels of insulin and insulin-like growth factor-1 hybrid receptors and decreased glycosylation of the insulin receptor alpha- and beta-subunits in scrapie-infected neuroblastoma N2a cells. Biochem J. 380:571-579.
47. Ohtani Y, Tamai Y, Ohnuki Y, Miura S. 1996. Ganglioside alterations in the central and peripheral nervous systems of patients with Creutzfeldt-Jakob disease. Neurodegeneration. 5:331-338.
48. Pan T, Wong BS, Liu T, Li R, Petersen RB, Sy MS. 2002. Cell-surface prion protein interacts with glycosaminoglycans. Biochem J. 368:81-90.
49. Paulick MG, Bertozzi CR. 2008. The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry. 47:6991-7000.
50. Perry VH, Bell MD, Brown HC, Matyszak MK. 1995. Inflammation in the nervous system. Curr Opin Neurobiol. 5:636-641.
51. Popa I, Vlad C, Bodennec J, Portoukalian J. 2002. Recovery of gangliosides from aqueous solutions on styrene-divinylbenzene copolymer columns. J Lipid Res. 43:1335-1340.
52. Prusiner SB. 1998. Prions. Proc Natl Acad Sci USA. 95:13363-13383.
53. Riemer C, Queck I, Simon D, Kurth R, Baier M. 2000. Identification of upregulated genes in scrapie-infected brain tissue. J Virol. 74:10245-10248.
54. Ritchie MA, Gill AC, Deery MJ, Lilley K. 2002. Precursor ion scanning for detection and structural characterization of heterogeneous glycopeptide mixtures. J Am Soc Mass Spectrom. 13:1065-1077.
55. Rudd PM, Endo T, Colominas C, Groth D, Wheeler SF, Harvey DJ, Wormald MR, Serban H, Prusiner SB, Kobata A, et al. 1999. Glycosylation differences between the normal and pathogenic prion protein isoforms. Proc Natl Acad Sci USA. 96:13044-13049.
56. Rudd PM, Wormald MR, Wing DR, Prusiner SB, Dwek RA. 2001. Prion glycoprotein: Structure, dynamics, and roles for the sugars. Biochemistry. 40:3759-3766.
57. Russelakis-Carneiro M, Saborio GP, Anderes L, Soto C. 2002. Changes in the glycosylation pattern of prion protein in murine scrapie. Implications for the mechanism of neurodegeneration in prion diseases. J Biol Chem. 277:36872-36877.
58. Shevchuk NA, Hathout Y, Epifano O, Su Y, Liu Y, Sutherland M, Ladisch S. 2007. Alteration of ganglioside synthesis by GM3 synthase knockout in murine embryonic fibroblasts. Biochim Biophys Acta. 1771:1226-1234.
59. Shyng SL, Lehmann S, Moulder KL, Harris DA. 1995. Sulfated glycans stimulate endocytosis of the cellular isoform of the prion protein, PrPC, in cultured cells. J Biol Chem. 270:30221-30229.
60. Silveyra MX, Garcia-Ayllon MS, Calero M, Saez-Valero J. 2006. Altered glycosylation of acetylcholinesterase in the Creutzfeldt-Jakob cerebrospinal fluid. J Mol Neurosci. 30:65-66.
61. Skinner PJ, Abbassi H, Chesebro B, Race RE, Reilly C, Haase AT. 2006. Gene expression alterations in brains of mice infected with three strains of scrapie. BMC Genomics. 7:114.
62. Sorensen G, Medina S, Parchaliuk D, Phillipson C, Robertson C, Booth SA. 2008. Comprehensive transcriptional profiling of prion infection in mouse models reveals networks of responsive genes. BMC Genomics. 9: 114.
63. Stimson E, Hope J, Chong A, Burlingame AL. 1999. Site-specific characterization of the N-linked glycans of murine prion protein by high-performance liquid chromatography/electrospray mass spectrometry and exoglycosidase digestions. Biochemistry. 38:4885-4895.
64. Stuermer CA, Langhorst MF, Wiechers MF, Legler DF, Von Hanwehr SH, Guse AH, Plattner H. 2004. PrPc capping in T cells promotes its association with the lipid raft proteins reggie-1 and reggie-2 and leads to signal transduction. FASEB J. 18:1731-1733.
65. Svennerholm L. 1963. Chromatographic separation of human brain gangliosides. J Neurochem. 10:613-623.
66. Tamguney G, Giles K, Glidden DV, Lessard P, Wille H, Tremblay P, Groth DF, Yehiely F, Korth C, Moore RC, et al. 2008. Genes contributing to prion pathogenesis. J Gen Virol. 89:1777-1788.
67. Tiede A, Daniels RJ, Higgs DR, Mehrein Y, Schmidt RE, Schubert J. 2001. The human GPI1 gene is required for efficient glycosylphosphatidylinositol biosynthesis. Gene. 271:247-254.
68. Tsuchida A, Okajima T, Furukawa K, Ando T, Ishida H, Yoshida A, Nakamura Y, Kannagi R, Kiso M, Furukawa K. 2003. Synthesis of disialyl Lewis a (Lea) structure in colon cancer cell lines by a sialyltransferase, ST6GalNAc VI, responsible for the synthesis of alpha-series gangliosides. J Biol Chem. 278:22787-22794.
69. Uliana AS, Crespo PM, Martina JA, Daniotti JL, Maccioni HJ. 2006. Modulation of GalT1 and SialT1 sub-Golgi localization by SialT2 expression reveals an organellar level of glycolipid synthesis control. J Biol Chem. 281:32852-32860.
70. Vaccaro AM, Ciaffoni F, Mandara I, Suzuki K. 1988. Presence of activator proteins for the enzymatic degradation of glucosylceramide in several human tissues. Clin Chim Acta. 172:323-334.
71. Vilotte JL, Soulier S, Essalmani R, Stinnakre MG, Vaiman D, Lepourry L, Da Silva JC, Besnard N, Dawson M, Buschmann A, et al. 2001. Markedly increased susceptibility to natural sheep scrapie of transgenic mice expressing ovine PrP. J Virol. 75:5977-5984.
72. Warner RG, Hundt C, Weiss S, Turnbull JE. 2002. Identification of the heparan sulfate binding sites in the cellular prion protein. J Biol Chem. 277:18421-18430.
73. Xiang W, Windl O, Wunsch G, Dugas M, Kohlmann A, Dierkes N, Westner IM, Kretzschmar HA. 2004. Identification of differentially expressed genes in scrapie-infected mouse brains by using global gene expression technology. J Virol. 78:11051-11060.
74. Zech T, Ejsing CS, Gaus K, de Wet B, Shevchenko A, Simons K, Harder T. 2009. Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signalling. Embo J. 28:466-476.