Treatment with normal prion protein delays differentiation and helps to maintain high proliferation activity in human embryonic stem cells

Journal of Neurochemistry

Volumn 114, Issue 2, 2010, Pages 362-373

  Lee, Young Jin ^a   Baskakov, Ilia V ^a,b  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

embryonic stem cells; neural differentiation; prion protein; proliferation; self renewal

Indexed keywords

PRION PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; DOWN REGULATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; HUMAN DEVELOPMENT; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; HUMANS; PROTEIN STRUCTURE, SECONDARY; PRPC PROTEINS; RECOMBINANT PROTEINS;

EID: 77953846750     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06601.x     Document Type: Article

References (71)

1. Antonacopoulou A. G., Grivas P. D., Skarlas L., Kalofonos M., Scopa C. D. Kalofonos H. P. (2008) POLR2F, ATP6V0A1 and PRNP Expression in Colorectal Cancer: New Molecules with Prognostic Significance? Anticancer Res. 28, 1221 1228.
2. Bocharova O. V., Breydo L., Parfenov A. S., Salnikov V. V. Baskakov I. V. (2005) In vitro conversion of full length mammalian prion protein produces amyloid form with physical property of PrPSc. J. Mol. Biol. 346, 645 659.
3. Borchelt D. R., Rogers M., Stahl N., Telling G. Prusiner S. B. (1993) Release of the cellular prion protein from cultured cells after loss of its glycoinositol phospholipid anchor. Glycobiology 3, 319 329.
4. Bosque P. J., Ryou C., Telling G., Peretz D., Legname G., DeArmond S. Prusiner S. B. (2002) Prions in skeletal muscle. Proc. Acad. Natl Sci. USA 99, 3812 3817.
5. Bounhar Y., Zhang Y., Goodyer C. G. LeBlanc A. (2001) Prion protein protects human neurons against Bax-mediated apoptosis. J. Biol. Chem. 276, 39145 39149.
6. Boyer L. A., Lee T. I., Cole M. F. et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947 956.
7. Brivanlou A. H., Gage F. H., Jaenisch R., Jessell T., Melton D. Rossant J. (2003) Setting standards for human embryonic stem cells. Science 300, 913 916.
8. Brown D. R., Wong B.-S., Hafiz F., Clive C., Haswell S. J. Jones I. M. (1999) Normal prion protein has an activity like that of superoxide dismutase. Biochem. J. 344, 1 5.
9. Büeler H., Fisher M., Lang Y., Bluethmann H., Lipp H.-P., DeArmond S. J., Prusiner S. B., Aguet M. Weissmann C. (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577 582.
10. Chadwick K., Wang L., Li L., Menendez P., Murdoch B., Rouleau A. Bhatia M. (2003) Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102, 906 915.
11. Chen S., Mange A., Dong L., Lehmann S. Schachner M. (2003) Prion protein as trans-ineracting partner for neurons is involved in neurite outgrowth and neuronal survival. Mol. Cell. Neurosci. 22, 227 233.
12. Chiarini L. B., Freitas A. R. O., Zanata S. M., Brentani R. R., Martins V. R. Linden R. (2002) Cellular prion protein transduces neuroprotective signals. EMBO J. 21, 3317 3326.
13. Coitinho A. S., Freitas A. R. O., Lopes M. H. et al. (2006) The interaction between prion protein and laminin modulates memory consolidation. Eur. J. Neurosci. 24, 3255 3264.
14. Diarra-Mehrpour M., Arrabal S., Jalil A. et al. (2004) Prion protein prevents human breast carcinoma cell line from tumor necrosis factor alfa-induced cell death. Cancer Res. 64, 719 727.
15. Donadio S., Alfaidy N., De Keukeleire B., Micoud J., Feige J. J., Challis J. R. G. Benharouga M. (2007) Expression and localization of cellular prion and COMMD1 proteins in human placenta throughout pregnancy. Placenta 28, 907 911.
16. Du J., Pan Y., Shi Y., Guo C., Jin X., Sun L., Liu N., Qiao T. Fan D. (2005) Overexpression and significance of prion protein in gastric cancer and multidrug-resistant gastric carcinoma cell line SGC7901/ADR. Int. J. Cancer 113, 213 220.
17. Erlich R. B., Kahn S. A., Lima F. R. S., Muras A. G., Martins R. A. P., Linden R., Chiarini L. B., Martins V. R. Moura Neto V. (2007) STI1 promotes glioma proliferation through MAPK and PI3K pathways. Glia 55, 1690 1698.
18. Gonzalez-Iglesias R., Pajares M. A., Espinosa C. O. J. C., Oesch B. Gasset M. (2002) Prion protein interaction with glycosaminoglycan occurs with the formation of oligomeric complexes stabilized by Cu(II) bridges. J. Mol. Biol. 319, 527 540.
19. Graner E., Mercadante A. F., Zanata S. M. et al. (2000a) Cellular prion protein binds laminin and mediates neuritogenesis. Mol. Brain Res. 76, 85 92.
20. Graner E., Mercadante A. F., Zanata S. M., Martins V. R., Jay D. G. Brentani R. (2000b) Laminin-induced PC-12 cell differentiation is inhibited following laser inactivation of cellular prion protein. FEBS Lett. 482, 257 260.
21. Green H., Easley K. Iuchi S. (2003) Marker succession during the development of keratinocytes from cultured human embryonic stem cells. Proc. Acad. Natl Sci. USA 100, 15625 15630.
22. Hajj G. N. M., Lopes M. H., Mercadante A. F. et al. (2007) Cellular prion protein interaction with vitronectin supports axonal growth and is compensated by integrins. J. Cell Sci. 120, 1915 1926.
23. Harris D. A. (1999) Cellular biology of prion diseases. Clin. Microbiol. Rev. 12, 429 444.
24. Harris D. A., Huber M. T., van Dijken P., Shyng S. L., Chait B. T. Wang R. (1993) Processing of a cellular prion protein: identification of N- and C-terminal cleavage sites. Biochemistry 32, 1009 1016.
25. Johnston D. S., Wright W. W., DiCandeloro P., Wilson E., Kopf G. S. Jelinsky S. A. (2008) Stage-specific gene expression is a fundamental charactersistic of rat spermatogenic cells and Sertoli cells. Proc. Natl Acad. Sci. USA 105, 8315 8320.
26. Kanaani J., Prusiner S. B., Diacovo J., Baekkeskov S. Legname G. (2005) Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hipocampal neurons in vitro. J. Neurochem. 95, 1373 1386.
27. Lavon N., Yanuka O. Benvenisty N. (2004) Differentiation and isolation of hepatic-like cells from human embryonic stem cells. Differentiation 72, 230 238. (Pubitemid 41702132)
28. Liang J., Wang J. B., Pan Y. L. et al. (2006) High frequency occurrence of 1-OPRD variant of PRNP gene in gastric cancer cell lines and Chinese population with gastric cancer. Cell Biol. Int. 30, 920 923.
29. Lopes M. H., Hajj G. N. M., Muras A. G., Mancini G. L., Castro R. M. P. S., Ribeiro K. C. B., Brentani R. R., Linden R. Martins V. M. (2005) Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signalling pathways. J. Neurosci. 25, 11330 11339.
30. Makarava N., Lee C. I., Ostapchenko V. G. Baskakov I. V. (2007) Highly promiscuous nature of prion polymerization. J. Biol. Chem. 282, 36704 36713.
31. Malaga-Trillo E., Solis G., Schrock Y., Geiss C., Luncz L., Thomanetz V. Stuermer C. A. O. (2009) Regulation of Embryonic Cell Adhesion by the Prion Protein. PLoS Biol. 7, e1000055.
32. Manson J., West J. D., Thomson V., McBride P., Kaufman M. H. Hope J. (1992) The prion protein gene: a role in mouse embryogenesis? Development 115, 117 122.
33. McEwan J. F., Windsor M. L. Cullis-Hill S. D. (2009) Antibodies to prion protein inhibit human colon cancer cell growth. Tumour Biol. 30, 141 147.
34. Meslin F., Hamai A., Gao P., Jalil A., Cahuzac N., Chouaib S. Mehrpour M. (2007) Silencing of prion protein sensitizes breast adriamycin-resistant carcinoma cells to TRAIL-mediated cell death. Cancer Res. 67, 10910 10919.
35. Millhauser G. L. (2004) Copper binding in the prion protein. Acc. Chem. Res. 37, 79 85.
36. Mouillet-Richard S., Ermonval M., Chebassier C., Laplanche J. L., Lehmann S., Launay J. M. Kellermann O. (2000) Signal transduction through prion protein. Science 289, 1925 1928.
37. Moya K. L., Hassig R., Breen K. C., Volland H. Giamberardino L. D. (2005) Axonal transport of the cellular prion protein is increased during axon regeneration. J. Neurochem. 92, 1044 1053.
38. Mummery C., Ward D., van der Brink C. E. et al. (2002) Cardiomyocyte differentiation of mouse and human embryonic stem cells. J. Anat. 2000, 233 242.
39. Nishikawa S. I., Jakt L. M. Era T. (2007) Embryonic stem-cell culture as a tool for developmental cell biology. Nat. Rev. Mol. Cell Biol. 8, 502 507.
40. C glycoforms modulates the efficiency of PrPSc formation in vitro. Biochemistry 45, 14129 14139.
41. Novitskaya V., Bocharova O. V., Bronstein I. Baskakov I. V. (2006) Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons. J. Biol. Chem. 2006, 13828 13836.
42. Novitskaya V., Makarava N., Sylvester I., Bronstein I. B. Baskakov I. V. (2007) Amyloid fibrils of mammalian prion protein induce axonal degeneration in NTERA2-derived terminally differentiated neurons. J. Neurochem. 102, 398 407.
43. Pan Y., Zhao L., Liang J. et al. (2006) Cellular prion protein promotes invasion and metastasis of gastric cancer. FASEB J. 20, 1886 1888.
44. Pauly P. C. Harris D. A. (1998) Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273, 33107 33110.
45. Prusiner S. B. (1997) Prion diseases and the BSE crisis. Science 278, 245 251.
46. Rao R. R. Stice S. L. (2004) Gene expression profiling of embryonic stem cells leads to greater understanding of pluripotency and early developmental events. Biol. Reprod. 71, 1772 1778.
47. Reubinoff B. E., Pera M. F., Fong C. Y., Trounson A. Bongso A. (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat. Biotechnol. 18, 399 404.
48. Reya T., Morrison S. J., Clarke M. F. Weissman I. L. (2001) Stem cells, cancer, and cancer stem cells. Nature 414, 105 111.
49. Rivera-Milla E., Oidtmann B., Panagiotidis C. H. et al. (2006) Disparate evolution of prion protein domains and the distinct origin of Doppel- and prion-related loci revealed by fish-to-mammal comparisons. FASEB J. 20, 317 319.
50. Robertson C., Booth S. A., Beniac D. R., Coulthart M. B., Booth T. F. McNicol A. (2006) Cellular prion protein is released on exosomes from activated platelets. Blood 107, 3907 3911.
51. van Rosmalen J. W. G., Born J. M. Martens G. J. M. (2006) Prion protein mRNA expression in Xenopus Laevis: no induction during melanotrope cell activation. Brain Res. 1075, 20 25.
52. Roucou X. LeBlanc A. C. (2005) Cellular prion protein neuroprotective function: implications in prion diseases. J. Mol. Med. 83, 3 11.
53. Roucou X., Giannopoulos P. N., Zhang Y., Jodoin J., Goodyer C. G. LeBlanc A. (2005) Cellular prion protein inhibits proapoptotic Bax conformational change in human neurons and in breast carcinoma MCF-7 cells. Cell Death Differ. 12, 783 795.
54. Sales N., Hassig R., Rudolfo K., Giamberardino L. D., Traiffort E., Ruat M., Fre'tier P. Moya K. L. (2002) Developmental expression of the cellular prion protein in elongating axons. Eur. J. Neurosci. 15, 1163 1177.
55. Santuccione A., Syntyk V., Leshchyns'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.
56. Sato N., Meijer L., Skaltsounis L., Greengard P. Brivanlou A. H. (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10, 55 63.
57. Schmitt-Ulms G., Legname G., Baldwin M. A. et al. (2001) Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J. Mol. Biol. 314, 1209 1225.
58. Schulz T. C., Palmarini G. M., Noggle S. A., Weiler D. A., Mitalipova M. M. Condie B. G. (2003) Directed neuronal differentiation of human embryonic stem cells. BMC Neurosci. 4, 1 13.
59. Segev H., Fishman B., Ziskind A., Shulman M. Itskovitz-Eldor J. (2004) Differentiating of human embryonic stem cells into insulin-producing clusters. Stem Cells 22, 265 274. (Pubitemid 38736611)
60. Simak J., Holada K., D'Agnillo F., Janota J. Vostal J. G. (2002) Cellular prion protein is expressed on endothelial cells and is released during apoptosis on membrane microparticles found in human plasma. Transfusion 42, 334 342.
61. Stahl N., Borchelt D. R., Hsiao K. Prusiner S. B. (1987) Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51, 229 240.
62. Steele A. D., Emsley J. G., Ozdinler P. H., Lindquist S. Macklis J. D. (2006) Prion protein (PrPC) positively regulates neural precursor proliferation during developmental and adult mammalian neurogenesis. Proc. Acad. Natl Sci. USA 103, 3416 3421.
63. Taylor D. R., Parkin E. T., Cocklin S. L., Ault J. R., Ashcroft A. E., Turner A. J. Hooper N. M. (2009) Role of adams in the ectodomain shedding and conformational conversion of the prion protein. J. Biol. Chem. 284, 22590 22600.
64. Thompson J. A., Itskovitz-Eldor J., Shapiro S. S., Waknitz M. A., Swiergiel J. J., Marshall V. S. Jones J. M. (1998) Embryonic Stem Cell Lines Derived from Human Blastocysts. Science 282, 1145 1147.
65. Tobler I., Gaus S. E., Deboer T. et al. (1996) Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 380, 639 642.
66. Tremblay P., Bouzamondo-Bernstein E., Heinrich C., Prusiner S. B. DeArmond S. J. (2007) Developmental expression of PrP in the post-implantation embryo. Brain Res. 1139, 60 67.
67. Vassallo N. Herms J. (2003) Cellular prion protein function in copper homeostasis and redox signaling at the synaps. J. Neurochem. 86, 544.
68. Vella L. J., Sharples R. A., Lawson V. A., Masters C. L., Cappai R. Hill A. F. (2007) Packaging of prions into exosomes is associated with a novel pathway of PrP processing. J. Pathol. 211, 582 590.
69. Viegas P., Chaverot N., Enslen H., Perriere N., Couraud P. O. Cazaubon S. (2006) Junctional expression of the prion protein PrPC by brain endothelial cells: a role in trans-andothelial migration of human monocytes. J. Cell Sci. 119, 4634 4643.
70. Zanata S. M., Lopes M. H., Mercadante A. F. et al. (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 21, 3307 3316.
71. Zhang C. C., Steele A. D., Lindquist S. Lodish H. F. (2006) Prion protein is expressed on long-term repopulating hematopoietic stem cells and is important for their self-renewal. Proc. Acad. Natl Sci. USA 103, 21814 21819.