Interactome analyses identify ties of prpc and its mammalian paralogs to oligomannosidic n-glycans and endoplasmic reticulum-derived chaperones

PLoS Pathogens

Volumn 5, Issue 10, 2009, Pages

  Watts, Joel C ^a,b,e   Huo, Hairu ^a   Bai, Yu ^a   Ehsani, Sepehr ^a,b,f   Won, Amy Hye ^a,b   Shi, Tujin ^a   Daude, Nathalie ^c   Lau, Agnes ^c   Young, Rebecca ^d   Xu, Lei ^d   Carlson, George A ^d   Williams, David ^b   Westaway, David ^c   Schmitt Ulms, Gerold ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

^d MCLAUGHLIN RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIA;

CHAPERONE; LACTIC ACID; MANNOSE OLIGOSACCHARIDE; MEMBRANE PROTEIN; NERVE PROTEIN; OLIGOSACCHARIDE; PRION PROTEIN; PRND PROTEIN, MOUSE; PROTEIN DISULFIDE ISOMERASE; SHADOO PROTEIN, MOUSE;

ANIMAL; ARTICLE; BIOLOGY; CELL ADHESION; ELECTROSPRAY MASS SPECTROMETRY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; METHODOLOGY; MOUSE; PHYSIOLOGY; PRION; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL ADHESION; CELL LINE, TUMOR; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPUTATIONAL BIOLOGY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; LACTIC ACID; MEMBRANE PROTEINS; MICE; MOLECULAR CHAPERONES; NERVE TISSUE PROTEINS; OLIGOSACCHARIDES; PRIONS; PROTEIN DISULFIDE-ISOMERASES; PRPC PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRANSFECTION;

EID: 73349140865     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000608     Document Type: Article

References (70)

1. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 117: 421-434
2. Taylor DR, Hooper NM (2006) The prion protein and lipid rafts. Mol Membr Biol 23: 89-99
3. Supattapone S, Deleault NR, Rees JR (2008) Amplification of purified prions in vitro. Methods Mol Biol 459: 117-130
4. Watts JC, Westaway D (2007) The prion protein family: diversity, rivalry, and dysfunction. Biochim Biophys Acta 1772: 654-672
5. Ben-Zaken O, Tzaban S, Tal Y, Horonchik L, Esko JD, et al. (2003) Cellular heparan sulfate participates in the metabolism of prions. J Biol Chem 278: 40041-40049
6. Horonchik L, Tzaban S, Ben-Zaken O, Yedidia Y, Rouvinski A, et al. (2005) Heparan sulfate is a cellular receptor for purified infectious prions. J Biol Chem 280: 17062-17067
7. Fischer MB, Roeckl C, Parizek P, Schwarz HP, Aguzzi A (2000) Binding of disease-associated prion protein to plasminogen. Nature 408: 479-483
8. Nelson J, McFerran NV, Pivato G, Chambers E, Doherty C, et al. (2008) The 67 kDa laminin receptor: structure, function and role in disease. Biosci Rep 28: 33-48
9. Rieger R, Edenhofer F, Lasmezas CI, Weiss S (1997) The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells. Nat Med 3: 1383-1388
10. Schmitt-Ulms G, Legname G, Baldwin MA, Ball HL, Bradon N, et al. (2001) Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J Mol Biol 314: 1209-1225
11. Hundt C, Peyrin JM, Haik S, Gauczynski S, Leucht C, et al. (2001) Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor. EMBO J 20: 5876-5886
12. 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
13. Gauczynski S, Peyrin JM, Haik S, Leucht C, Hundt C, et al. (2001) The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J 20: 5863-5875
14. Mouillet-Richard S, Ermoval M, Chebassier CL, Laplanche JL, Lehmann S, Launay JM, et al. (2000) Signal transduction through prion protein. Science 2000: 1925-1928
15. Santuccione A, Sytnyk V, Leshchns’ka I, Schachner M (2005) Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J Cell Biol 169: 341-354
16. Schmitt-Ulms G, Hansen K, Liu J, Cowdrey C, Yang J, et al. (2004) Time controlled transcardiac perfusion crosslinking for the study of protein interactions in complex tissues. Nat Biotechnol 22: 724-731
17. Race RE, Fadness LH, Chesebro B (1987) Characterization of scrapie infection in mouse neuroblastoma cells. J Gen Virol 68: 1391-1399
18. Telling GC, Tremblay P, Torchia M, DeArmond SJ, Cohen FE, et al. (1997) Nterminally tagged prion protein supports prion propagation in transgenic mice. Protein Science 6: 825-833
19. Einhauer A, Jungbauer A (2001) The FLAG peptide, a versatile fusion tag for the purification of recombinant proteins. J Biochem Biophys Methods 49: 455-465
20. Watts JC, Drisaldi B, Ng V, Yang J, Strome B, et al. (2007) The CNS glycoprotein Shadoo has PrP(C)-like protective properties and displays reduced levels in prion infections. EMBO J 26: 4038-4050
21. Zieske LR (2006) A perspective on the use of iTRAQ reagent technology for protein complex and profiling studies. J Exp Bot 57: 1501-1508
22. Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214
23. Moore RC, Lee IY, Silverman GL, Harrison PM, Strome R, et al. (1999) Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J Mol Biol 292: 797-817
24. Altruda F, Cervella P, Gaeta ML, Daniele A, Giancotti F, et al. (1989) Cloning of cDNA for a novel mouse membrane glycoprotein (gp42): shared identity to histocompatibility antigens, immunoglobulins and neural-cell adhesion molecules. Gene 85: 445-452
25. Heller M, Von der Ohe M, Kleene R, Mohajeri MH, Schachner M (2003) The immunoglobulin-superfamily molecule basigin is a binding protein for oligomannosidic carbohydrates: an anti-idiotypic approach. J Neurochem 84: 557-565
26. Horstkorte R, Schachner M, Magyar JP, Vorherr T, Schmitz B (1993) The fourth immunoglobulin-like domain of NCAM contains a carbohydrate recognition domain for oligomannosidic glycans implicated in association with L1 and neurite outgrowth. J Cell Biol 121: 1409-1421
27. Heiland PC, Griffith LS, Lange R, Schachner M, Hertlein B, et al. (1998) Tyrosine and serine phosphorylation of the neural cell adhesion molecule L1 is implicated in its oligomannosidic glycan dependent association with NCAM and neurite outgrowth. Eur J Cell Biol 75: 97-106
28. Orberger G, Geyer R, Stirm S, Tauber R (1992) Structure of the N-linked oligosaccharides of the human transferrin receptor. Eur J Biochem 205: 257-267
29. Schmitz B, Peter-Katalinic J, Egge H, Schachner M (1993) Monoclonal antibodies raised against membrane glycoproteins from mouse brain recognize N-linked oligomannosidic glycans. Glycobiology 3: 609-617
30. Ohe Y, Ohnishi H, Okazawa H, Tomizawa K, Kobayashi H, et al. (2003) Characterization of nucleotide pyrophosphatase-5 as an oligomannosidic glycoprotein in rat brain. Biochem Biophys Res Com 308: 719-725
31. Pesheva P, Horwitz AF, Schachner M (1987) Integrin, the cell surface receptor for fibronectin and laminin, expresses the L2/HNK-1 and L3 carbohydrate structures shared by adhesion molecules. Neurosci Let 83: 303-306
32. Borchelt DR, Taraboulos A, Prusiner SB (1992) Evidence for synthesis of scrapie prion proteins in the endocytic pathway. J Biol Chem 267: 16188-16199
33. Caughey B, Raymond GJ (1991) The scrapie-associated form of PrP is made from a cell surface precursor that is both protease-and phospholipase-sensitive. J Biol Chem 266: 18217-18223
34. Mandel R, Ryser HJ-P, Ghani F, Wu M, Peak D (1993) Inhibition of a reductive function of the plasma membrane by bacitracin and antibodies against protein disulfide-isomerase. Proc Natl Acad Sci U S A 90: 4112-4116
35. Caughey B, Raymond GJ, Ernst D, Race RE (1991) N-terminal truncation of the scrapie-associated form of PrP by lysosomal protease(s): implications regarding the site of conversion of PrP to the protease-resistant state. J Virol 65: 6597-6603
36. Taraboulos A, Raeber AJ, Borchelt DR, Serban D, Prusiner SB (1992) Synthesis and trafficking of prion proteins in cultured cells. Mol Biol Cell 3: 851-863
37. Moore RC, Mastrangelo P, Bouzamondo E, Heinrich C, Legname G, et al. (2001) Doppel-induced cerebellar degeneration in transgenic mice. Proc Natl Acad Sci U S A 98: 15288-15293
38. Rutishauser D, Mertz KD, Moos R, Brunner E, Rulicke T, et al. (2009) The comprehensive native interactome of a fully functional tagged prion protein. PLoS ONE 4: e4446. doi:10.1371/journal.pone.0004446
39. Fasano C, Campana VCZ (2006) Protein Only or Something More? Overview of Potential Prion Cofactors. J Mol Neurosci 29: 195-214
40. Hetz C, Russelakis-Carneiro M, Walchli S, Carboni S, Vial-Knecht E, et al. (2005) The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J Neurosci 25: 2793-2802
41. Turano C, Coppari S, Altieri F, Ferraro A (2002) Proteins of the PDI family: unpredicted non-ER locations and functions. J Cell Physiol 193: 154-163
42. Lucassen R, Nishina K, Supattapone S (2003) In vitro amplification of proteaseresistant prion protein requires free sulfhydryl groups. Biochemistry 42: 4127-4135
43. Ellgaard L, Ruddock LW (2005) The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO reports 6: 28-32
44. Weissmann C (2004) The state of the prion. Nat Rev Microbiol 2: 861-871
45. Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, et al. (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123: 321-334
46. Westergard L, Christensen HM, Harris DA (2007) The cellular prion protein (PrPC): its physiological function and role in disease. Biochim Biophys Acta 1772: 629-644
47. McDonnell JM, Jones GE, White TK, Tanzer ML (1996) Calreticulin binding affinity for glycosylated laminin. J Biol Chem 271: 7891-7894
48. White TK, Zhu Q, Tanzer ML (1995) Cell surface calreticulin is a putative mannoside lectin which triggers mouse melanoma cell spreading. J Biol Chem 270: 15926-15929
49. Kleene R, Loers G, Langer J, Frobert Y, Buck F, et al. (2007) Prion protein regulates glutamate-dependent lactate transport of astrocytes. J Neurosci 27: 12331-12340
50. Hemler ME, Crouse C, Takada Y, Sonnenberg A (1988) Multiple very late antigen (VLA) heterodimers on platelets. Evidence for distinct VLA-2, VLA-5 (fibronectin receptor), and VLA-6 structures. J Biol Chem 263: 7660-7665
51. Zhu Q, Zelinka P, White TK, Tanzer ML (1997) Calreticulin-integrin bidirectional signaling complex. Biochem Biophys Res Com 232: 354-358
52. Canfield SM, Khakoo AY (1999) The nonintegrin laminin binding protein (p67 LBP) is expressed on a subset of activated human T lymphocytes and, together with the integrin very late activation antigen-6, mediates avid cellular adherence to laminin. J Immunol 163: 3430-3440
53. Vana K, Zuber C, Pflanz H, Kolodziejczak D, Zemora G, et al. (2009) LRP/LR as an alternative promising target in therapy of prion diseases, Alzheimer’s disease and cancer. Infect Disord Drug Targets 9: 69-80
54. Zuber C, Mitteregger G, Schuhmann N, Rey C, Knackmuss S, et al. (2008) Delivery of single-chain antibodies (scFvs) directed against the 37/67 kDalaminin receptor into mice via recombinant adeno-associated viral vectors for prion disease gene therapy. J Gen Virol 89: 2055-2061
55. Pflanz H, Vana K, Mitteregger G, Renner-Muller I, Pace C, et al. (2009) Scrapie-infected transgenic mice expressing a laminin receptor decoy mutant reveal a prolonged incubation time associated with low levels of PrPres. J Mol Biol 388: 721-729
56. Hundt C, Weiss S (2004) The prion-like protein Doppel fails to interact with itself, the prion protein and the 37 kDa/67 kDa laminin receptor in the yeast two-hybrid system. Biochim Biophys Acta 1689: 1-5
57. Yin SM, Sy MS, Yang HY, Tien P (2004) Interaction of Doppel with the fulllength laminin receptor precursor protein. Arch Biochem Biophys 428: 165-169
58. Sato M, Saeki Y, Tanaka K, Kaneda Y (1999) Ribosome-Associated Protein LBP/p40 binds to S21 protein of 40S ribosome: Analysis using a yeast Two-Hybrid System. Biochem Biophys Res Com 256: 385-390
59. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, et al. (2005) A human protein-protein interaction network -a resource for annotating the proteome. Cell 122: 957-968
60. Cai S, Bulus N, Fonseca-Siesser PM, Chen D, Hanks SK, et al. (2004) CD98 modulates integrin b1 function in polarized epithelial cells. J Cell Sci 118: 889-899
61. Prager GW, Feral CC, Kim C, Han J, Ginsberg MH (2007) CD98hc (SLC3A2) interaction with the integrin beta subunit cytoplasmic domain mediates adhesive signaling. J Biol Chem 282: 24477-24484
62. Cho JY, Fox DA, Horejsi V, Saqawa K, Skubitz KM, et al. (2001) The functional interactions between CD98, beta-1integrins, and CD147 in the induction of U937 homotypic aggregation. Blood 98: 374-382
63. Xu D, Hemler ME (2005) Metabolic activation-related CD147-CD98 complex. Mol Cell Proteomics 4: 1061-1071
64. Mori K, Nishimura M, Tsurudome M, Ito M, Nishio M, et al. (2004) The functional interaction between CD98 and CD147 in regulation of virus-induced cell fusion and osteoclast formation. Med Microbiol Immunol 193: 155-162
65. Takahashi Y, Biqler D, Ito Y, White JM (2001) Sequence-specific interaction between the disintegrin domain of mouse ADAM3 and murine eggs: role of beta1 integrin-associated proteins CD9, CD81 and CD98. Mol Biol Cell 12: 809-820
66. Saxenam DK, Oh-Oka T, Kadomatsu K, Muramatsu T, Toshimori K (2002) Behaviour of a sperm surface transmembrane glycoprotein basigin during epididymal maturation and its role in fertilization in mice. Reproduction 123: 435-444
67. Behrens A, Genoud N, Naumann H, Ruelicke T, Janett F, et al. (2002) Absence of the prion protein homologue Doppel causes male sterility. EMBO J 21: 3652-3658
68. Hwang D, Lee IY, Yoo H, Gehlenborg N, Cho JH, et al. (2009) A systems approach to prion disease. Mol Syst Biol 5: 252
69. Chalkley RJ, Baker PR, Huang L, Hansen KC, Allen NP, et al. (2005) Comprehensive Analysis of a Multidimensional Liquid Chromatography Mass Spetrometry Dataset Acquired on a Quadrupole Selecting Quadrupole Collision Cell, Time-of-flight Mass Spectrometer. II. New Developments in Protein Prospector Allow for Reliable and Comprehensive Automatic Analysis of Large Datasets. Mol Cell Prot 4: 1194-1204
70. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.