The prion protein controls polysialylation of neural cell adhesion molecule 1 during cellular morphogenesis

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Mehrabian, Mohadeseh ^a,b   Brethour, Dylan ^a,b   Wang, Hansen ^a   Xi, Zhengrui ^a   Rogaeva, Ekaterina ^a,b   Schmitt Ulms, Gerold ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE 1; PRION PROTEIN; PROTEOME; SIALYLTRANSFERASE; SIALYLTRANSFERASE ST8SIA2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CD56 ANTIGEN; CMP-N-ACETYLNEURAMINATE-POLY-ALPHA-2,8-SIALOSYL SIALYLTRANSFERASE; NCAM1 PROTEIN, MOUSE; PRION;

ANIMAL CELL; ARTICLE; CELLULAR MORPHOGENESIS; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PHENOTYPE; POLYSIALYLATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; REGULATORY MECHANISM; SIALYLATION; ST8SIA2 GENE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL LINE; METABOLISM; PHYSIOLOGY; PRION; PROCEDURES; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD56; BETA CATENIN; CELL LINE; EPITHELIAL-MESENCHYMAL TRANSITION; MICE; MORPHOGENESIS; PRIONS; PROTEOMICS; SIALYLTRANSFERASES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84942693490     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133741     Document Type: Article

References (71)

1. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 1982; 216: 136-144. PMID: 6801762
2. Aguzzi A, Baumann F, Bremer J. The Prion's Elusive Reason for Being. Annu Rev Neurosci 2008; 31: 439-477. doi: 10.1146/annurev.neuro.31.060407.125620 PMID: 18558863
3. Sakudo A, Ikuta K. Prion protein functions and dysfunction in prion diseases. Curr Med Chem 2009; 16: 380-389. PMID: 19149584
4. Nicolas O, Gavin R, del Rio JA. New insights into cellular prion protein (PrPc) functions: the "ying and yang" of a relevant protein. Brain Res Rev 2009; 61: 170-184. doi: 10.1016/j.brainresrev.2009.06.002 PMID: 19523487
5. Hu W, Kieseier B, Frohman E, Eagar TN, Rosenberg RN, Hartung HP, et al. Prion proteins: physiological functions and role in neurological disorders. J Neurol Sci 2008; 264: 1-8. PMID: 17707411
6. Watts JC, Westaway D. The prion protein family: diversity, rivalry, and dysfunction. Biochim Biophys Acta 2007; 1772: 654-672. PMID: 17562432
7. Lauren J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 2009; 457: 1128-1132. doi: 10.1038/nature07761 PMID: 19242475
8. Kocher T, Superti-Furga G. Mass spectrometry-based functional proteomics: from molecular machines to protein networks. Nat Meth 2007; 4: 807-815.
9. Mendelsohn AR, Brent R. Protein interaction methods-toward an endgame. Science 1999; 284: 1948-1950. PMID: 10400537
10. Livstone MS, Oughtred R, Heinicke S, Vernot B, Huttenhower C, Durand D, et al. Inferring protein function from homology using the Princeton Protein Orthology Database (P-POD). Curr Prot Bioinform 2011; Chapter 6: Unit 6 11.
11. White JK, Gerdin AK, Karp NA, Ryder E, Buljan M, Bussell JN, et al. Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 2013; 154: 452-464. doi: 10.1016/j.cell.2013.06.022 PMID: 23870131
12. Rutishauser D, Mertz KD, Moos R, Brunner E, Rulicke T, Calella AM, et al. The comprehensive native interactome of a fully functional tagged prion protein. PloS One 2009; 4: e4446. doi: 10.1371/journal. pone.0004446 PMID: 19209230
13. Watts JC, Huo H, Bai Y, Ehsani S, Jeon AH, Shi T, et al. Interactome analyses identify ties of PrP and its mammalian paralogs to oligomannosidic N-glycans and endoplasmic reticulum-derived chaperones. PLoS Pathog 2009; 5: e1000608. doi: 10.1371/journal.ppat.1000608 PMID: 19798432
14. Schmitt-Ulms G, Hansen K, Liu J, Cowdrey C, Yang J, DeArmond SJ, et al. Time-controlled transcardiac perfusion cross-linking for the study of protein interactions in complex tissues. Nat Biotech 2004; 22: 724-731.
15. Schmitt-Ulms G, Legname G, Baldwin MA, Ball HL, Bradon N, Bosque PJ, et al. Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J Mol Biol 2001; 314: 1209-1225. PMID: 11743735
16. Santuccione A, Sytnyk V, Leshchyns'ka I, Schachner M. Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J Cell Biol 2005; 169: 341-354. PMID: 15851519
17. Lehembre F, Yilmaz M, Wicki A, Schomber T, Strittmatter K, Ziegler D, et al. NCAM-induced focal adhesion assembly: a functional switch upon loss of E-cadherin. EMBO J 2008; 27: 2603-2615. doi: 10.1038/emboj.2008.178 PMID: 18772882
18. Schmitt-Ulms G, Ehsani S, Watts JC, Westaway D, Wille H. Evolutionary descent of prion genes from the ZIP family of metal ion transporters. PLoS One 2009; 4: e7208. doi: 10.1371/journal.pone.0007208 PMID: 19784368
19. Ehsani S, Tao R, Pocanschi CL, Ren H, Harrison PM, Schmitt-Ulms G. Evidence for retrogene origins of the prion gene family. PLoS One 2011; 6: e26800. doi: 10.1371/journal.pone.0026800 PMID: 22046361
20. Yamashita S, Miyagi C, Fukada T, Kagara N, Che YS, Hirano T. Zinc transporter LIVI controls epithelial- mesenchymal transition in zebrafish gastrula organizer. Nature 2004; 429: 298-302. PMID: 15129296
21. Mathews WR, Wang F, Eide DJ, Van Doren M. Drosophila fear of intimacy encodes a Zrt/IRT-like protein (ZIP) family zinc transporter functionally related to mammalian ZIP proteins. J Biol Chem 2005; 280: 787-795. PMID: 15509557
22. Van Doren M, Mathews WR, Samuels M, Moore LA, Broihier HT, Lehmann R. fear of intimacy encodes a novel transmembrane protein required for gonad morphogenesis in Drosophila. Development 2003; 130: 2355-2364. PMID: 12702650
23. Cotto E, Andre M, Forgue J, Fleury HJ, Babin PJ. Molecular characterization, phylogenetic relationships, and developmental expression patterns of prion genes in zebrafish (Danio rerio). FEBS J 2005; 272: 500-513. PMID: 15654888
24. Premzl M, Sangiorgio L, Strumbo B, Marshall Graves JA, Simonic T, Gready JE. Shadoo, a new protein highly conserved from fish to mammals and with similarity to prion protein. Gene 2003; 314: 89-102. PMID: 14527721
25. Malaga-Trillo E, Solis GP, Schrock Y, Geiss C, Luncz L, Thomanetz V, et al. Regulation of embryonic cell adhesion by the prion protein. PLoS Biol 2009; 7: e55. doi: 10.1371/journal.pbio.1000055 PMID: 19278297
26. Mehrabian M, Ehsani S, Schmitt-Ulms G An emerging role of the cellular prion protein as a modulator of a morphogenetic program underlying epithelial-to-mesenchymal transition. Front Cell Dev Biol 2014; 2.
27. Miettinen PJ, Ebner R, Lopez AR, Derynck R. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 1994; 127: 2021-2036. PMID: 7806579
28. David G, Van der Schueren B, Bernfield M. Basal lamina formation by normal and transformed mouse mammary epithelial cells duplicated in vitro. J Natl Cancer Inst 1981; 67: 719-728. PMID: 6944539
29. Mehrabian M, Brethour D, MacIsaac S, Kim JK, Gunawardana CG, Wang H, et al. CRISPR-Cas9- Based Knockout of the Prion Protein and Its Effect on the Proteome. PloS One 2014; 9: e114594. doi: 10.1371/journal.pone.0114594 PMID: 25490046
30. Dayon L, Sanchez JC. Relative protein quantification by MS/MS using the tandem mass tag technology. Meth Mol Biol 2012; 893: 115-127.
31. Hoffman S, Sorkin BC, White PC, Brackenbury R, Mailhammer R, Rutishauser U, et al. Chemical characterization of a neural cell adhesion molecule purified from embryonic brain membranes. J Biol Chem 1982; 257: 7720-7729. PMID: 7085646
32. Kojima N, Yoshida Y, Tsuji S. A developmentally regulated member of the sialyltransferase family (ST8Sia II, STX) is a polysialic acid synthase. FEBS Lett 1995; 373: 119-122. PMID: 7589448
33. Eckhardt M, Muhlenhoff M, Bethe A, Koopman J, Frosch M, Gerardy-Schahn R. Molecular characterization of eukaryotic polysialyltransferase-1. Nature 1995; 373: 715-718. PMID: 7854457
34. Angata K, Nakayama J, Fredette B, Chong K, Ranscht B, Fukuda M. Human STX polysialyltransferase forms the embryonic form of the neural cell adhesion molecule. Tissue-specific expression, neurite outgrowth, and chromosomal localization in comparison with another polysialyltransferase, PST. J Biol Chem 1997; 272: 7182-7190. PMID: 9054414
35. Kojima N, Tachida Y, Yoshida Y, Tsuji S. Characterization of mouse ST8Sia II (STX) as a neural cell adhesion molecule-specific polysialic acid synthase. Requirement of core alpha1, 6-linked fucose and a polypeptide chain for polysialylation. J Biol Chem 1996; 271: 19457-19463. PMID: 8702635
36. Suzuki M, Angata K, Nakayama J, Fukuda M. Polysialic acid and mucin type o-glycans on the neural cell adhesion molecule differentially regulate myoblast fusion. J Biol Chem 2003; 278: 49459-49468. PMID: 13679364
37. Herbst A, Banser P, Velasquez CD, Mays CE, Sim VL, Westaway D, et al. Infectious Prions Accumulate to High Levels in Non Proliferative C2C12 Myotubes. PLoS Pathog 2013; 9: e1003755. doi: 10.1371/journal.ppat.1003755 PMID: 24244171
38. Park CH, Chang JY, Hahm ER, Park S, Kim HK, Yang CH. Quercetin, a potent inhibitor against betacatenin/Tcf signaling in SW480 colon cancer cells. Biochem Biophys Res Commun 2005; 328: 227-234. PMID: 15670774
39. Emami KH, Nguyen C, Ma H, Kim DH, Jeong KW, Eguchi M, et al. A small molecule inhibitor of betacatenin/CREB-binding protein transcription [corrected]. Proc Natl Acad Sci USA 2004; 101: 12682-12687. PMID: 15314234
40. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, et al. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 2004; 6: 931-940. PMID: 15448698
41. Bullock BP, Habener JF. Phosphorylation of the cAMP response element binding protein CREB by cAMP-dependent protein kinase A and glycogen synthase kinase-3 alters DNA-binding affinity, conformation, and increases net charge. Biochemistry 1998; 37: 3795-3809. PMID: 9521699
42. Puckett C, Concannon P, Casey C, Hood L. Genomic structure of the human prion protein gene. Amer J Hum Genet 1991; 49: 320-329. PMID: 1678248
43. Basler K, Oesch B, Scott M, Westaway D, Walchli M, Groth DF, et al. Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene. Cell 1986; 46: 417-428. PMID: 2873895
44. Saeki K, Matsumoto Y, Hirota Y, Onodera T. Three-exon structure of the gene encoding the rat prion protein and its expression in tissues. Virus Genes 1996; 12: 15-20. PMID: 8879116
45. Karapetyan YE, Sferrazza GF, Zhou M, Ottenberg G, Spicer T, Chase P, et al. Unique drug screening approach for prion diseases identifies tacrolimus and astemizole as antiprion agents. Proc Natl Acad Sci USA 2013.
46. Misiewicz M, Dery MA, Foveau B, Jodoin J, Ruths D, Leblanc AC. Identification of a novel Endoplasmic Reticulum Stress Response Element regulated by XBP1. J Biol Chem 2013.
47. Unno J, Satoh K, Hirota M, Kanno A, Hamada S, Ito H, et al. LIV-1 enhances the aggressive phenotype through the induction of epithelial to mesenchymal transition in human pancreatic carcinoma cells. Int J Oncol 2009; 35: 813-821. PMID: 19724917
48. Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ. Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem 2005; 280: 11740-11748. PMID: 15647282
49. Kiss JZ, Muller D. Contribution of the neural cell adhesion molecule to neuronal and synaptic plasticity. Rev Neurosci 2001; 12: 297-310.PMID: 11783716
50. Senkov O, Tikhobrazova O, Dityatev A. PSA-NCAM: synaptic functions mediated by its interactions with proteoglycans and glutamate receptors. Int J Biochem Cell Biol 2012; 44: 591-595. doi: 10.1016/j. biocel.2012.01.008 PMID: 22300986
51. Angata K, Long JM, Bukalo O, Lee W, Dityatev A, Wynshaw-Boris A, et al. Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J Biol Chem 2004; 279: 32603-32613. PMID: 15140899
52. Drake PM, Nathan JK, Stock CM, Chang PV, Muench MO, Nakata D, et al. Polysialic acid, a glycan with highly restricted expression, is found on human and murine leukocytes and modulates immune responses. J Immunol 2008; 181: 6850-6858. PMID: 18981104
53. Drake PM, Stock CM, Nathan JK, Gip P, Golden KP, Weinhold B, et al. Polysialic acid governs T-cell development by regulating progenitor access to the thymus. Proc Natl Acad Sci USA 2009; 106: 11995-12000. doi: 10.1073/pnas.0905188106 PMID: 19587240
54. Senkov O, Sun M, Weinhold B, Gerardy-Schahn R, Schachner M, Dityatev A. Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. J Neurosci 2006; 26: 10888-109898. PMID: 17050727
55. Hammond MS, Sims C, Parameshwaran K, Suppiramaniam V, Schachner M, Dityatev A. Neural cell adhesion molecule-associated polysialic acid inhibits NR2B-containing N-methyl-D-aspartate receptors and prevents glutamate-induced cell death. J Biol Chem 2006; 281: 34859-34869. PMID: 16987814
56. Kochlamazashvili G, Senkov O, Grebenyuk S, Robinson C, Xiao MF, Stummeyer K, et al. Neural cell adhesion molecule-associated polysialic acid regulates synaptic plasticity and learning by restraining the signaling through GluN2B-containing NMDA receptors. J Neurosci 2010; 30: 4171-4183. doi: 10.1523/JNEUROSCI.5806-09.2010 PMID: 20237287
57. Glass JD, Lee W, Shen H, Watanabe M. Expression of immunoreactive polysialylated neural cell adhesion molecule in the suprachiasmatic nucleus. Neuroendocrin 1994; 60: 87-95.
58. Shen H, Watanabe M, Tomasiewicz H, Glass JD. Genetic deletions of NCAM and PSA impair circadian function in the mouse. Physiol Behav 2001; 73: 185-193. PMID: 11399310
59. Glass JD, Watanabe M, Fedorkova L, Shen H, Ungers G, Rutishauser U. Dynamic regulation of polysialylated neural cell adhesion molecule in the suprachiasmatic nucleus. Neuroscience 2003; 117: 203-211. PMID: 12605906
60. Prosser RA, Rutishauser U, Ungers G, Fedorkova L, Glass JD. Intrinsic role of polysialylated neural cell adhesion molecule in photic phase resetting of the Mammalian circadian clock. J Neurosci 2003; 23: 652-658. PMID: 12533624
61. Shen H, Watanabe M, Tomasiewicz H, Rutishauser U, Magnuson T, Glass JD. Role of neural cell adhesion molecule and polysialic acid in mouse circadian clock function. J Neurosci 1997; 17: 5221-5229. PMID: 9185559
62. Jungnickel J, Eckhardt M, Haastert-Talini K, Claus P, Bronzlik P, Lipokatic-Takacs E, et al. Polysialyltransferase overexpression in Schwann cells mediates different effects during peripheral nerve regeneration. Glycobiology 2012; 22: 107-115. doi: 10.1093/glycob/cwr113 PMID: 21840969
63. Carratu MR, Steardo L, Cuomo V. Role of polysialic acid in peripheral myelinated axons. Microsc Res Tech 1996; 34: 489-491. PMID: 8842018
64. Mehanna A, Mishra B, Kurschat N, Schulze C, Bian S, Loers G, et al. Polysialic acid glycomimetics promote myelination and functional recovery after peripheral nerve injury in mice. Brain 2009; 132: 1449-1462. doi: 10.1093/brain/awp128 PMID: 19454531
65. Massaro AR. The role of NCAM in remyelination. Neurol Sci 2002; 22: 429-435. PMID: 11976973
66. Theodosis DT, Rougon G, Poulain DA. Retention of embryonic features by an adult neuronal system capable of plasticity: polysialylated neural cell adhesion molecule in the hypothalamo-neurohypophysial system. Proc Natl Acad Sci USA 1991; 88: 5494-5498. PMID: 2062831
67. Bonfanti L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 2006; 80: 129-164. PMID: 17029752
68. Gascon E, Vutskits L, Kiss JZ. The role of PSA-NCAM in adult neurogenesis. Adv Exp Med Biol 2010; 663: 127-136. doi: 10.1007/978-1-4419-1170-4-8 PMID: 20017019
69. Steele AD, Lindquist S, Aguzzi A. The prion protein knockout mouse: a phenotype under challenge. Prion 2007; 1: 83-93. PMID: 19164918
70. Vizcaino JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Rios D, et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 2014; 32: 223-226. doi: 10.1038/nbt.2839 PMID: 24727771
71. Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 2013; 41: D1063- 1069. doi: 10.1093/nar/gks1262 PMID: 23203882