The cellular form of the prion protein is involved in controlling cell cycle dynamics, self-renewal, and the fate of human embryonic stem cell differentiation

Journal of Neurochemistry

Volumn 124, Issue 3, 2013, Pages 310-322

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

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

Author keywords

human embryonic stem cells; prion protein; self renewal; stem cell differentiation; stem cell fate

Indexed keywords

LENTIVIRUS VECTOR; PRION PROTEIN;

ARTICLE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; ECTODERM; EMBRYONIC STEM CELL; GERM LAYER; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SELF RENEWAL;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; EMBRYONIC STEM CELLS; FIBROBLASTS; GENE SILENCING; HUMANS; MICE; MOLECULAR DYNAMICS SIMULATION; PRPC PROTEINS;

EID: 84872084807     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07913.x     Document Type: Article

References (55)

1. Adle-Biassette H., Verney C., Peoc'h K., Dauge M. C., Razavi F., Choudat L., Gressens P., Budka H., and, Henin D., (2006) Immunohistochemical expression of prion protein (PrPC) in the human forebrain during development. J. Neuropathol. Exp. Neurol. 65, 698-706.
2. Antonacopoulou A. G., Grivas P. D., Skarlas L., Kalofonos M., Scopa C. D., and, Kalofonos H. P., (2008) POLR2F, ATP6V0A1 and PRNP expression in colorectal cancer: new molecules with prognostic significance? Anticancer Res. 28, 1221-1228.
3. Arantes C., Nomizo R., Lopes M. H., Hajj G. N., Lima F. R., and, Martins V. R., (2009) Prion protein and its ligand stress inducible protein 1 regulate astrocyte development. Glia 57, 1439-1449.
4. Becker K. A., Ghule P. N., Therrien J. A., Lian J. B., Stein J. L., Wijnen A. J., and, Stein G. S., (2006) Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. J. Cell. Physiol. 209, 883-893.
5. Bounhar Y., Zhang Y., Goodyer C. G., and, LeBlanc A., (2001) Prion protein protects human neurons against Bax-mediated apoptosis. J. Biol. Chem. 276, 39145-39149.
6. Bueler H., Aguzzi A., Sailer A., Greiner R. A., Autenried P., Aguet M., and, Weissmann C., (1993) Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347.
7. Burdon T., Smith A., and, Savatier P., (2002) Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol. 12, 432-438.
8. Chen S., Mange A., Dong L., Lehmann S., and, 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.
9. Chiarini L. B., Freitas A. R. O., Zanata S. M., Brentani R. R., Martins V. R., and, Linden R., (2002) Cellular prion protein transduces neuroprotective signals. EMBO J. 21, 3317-3326.
10. 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., and, Moura Neto V., (2007) STI1 promotes glioma proliferation through MAPK and PI3K pathways. Glia 55, 1690-1698.
11. Fluckiger A. C., Marcy G., Marchand M., Négre D., Cosset F. L., Mitalipov S., Wolf D., Savatier P., and, Dehay C., (2006) Cell cycle features of primate embryonic stem cells. Stem Cells 24, 547-556.
12. 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.
13. Kanaani J., Prusiner S. B., Diacovo J., Baekkeskov S., and, 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.
14. Khalifé M., Young R., Passet B., et al,. (2011) Transcriptomic analysis brings new insight into the biological role of the prion protein during mouse embryogenesis. PLoS ONE 6, e23253.
15. Lee Y. J., and, Baskakov I. V., (2010) Treatment with normal prion protein delays differentiation and helps to maintain proliferating activity in human embryonic stem cells. J. Neurochem. 114, 362-373.
16. Li A., Christensen H. M., Stewart L. R., Roth K. A., Chiesa R., and, Harris D. A., (2007) Neonatal lethality in transgenic mice expressing prion protein with a deletion of residues 105-125. EMBO J. 26, 548-558.
17. Liang J., and, Slingerland J. M., (2003) Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2, 339-345.
18. Liang J., Pan Y. L., Ning X. X., et al,. (2006) Overexpression of PrPC and its antiapoptosis function in gastric cancer. Tumor Biol. 27, 84-91.
19. Liang J., Pan Y., Zhang D., et al,. (2007) Cellular prion protein promotes proliferation and G1/S transition of human gastric cancer cells SGC7901 and AGS. FASEB J. 21, 2247-2256.
20. Lima F. R., Arantes C. P., Muras A. G., Nomizo R., Brentani R. R., and, Martins V. R., (2007) Cellular prion protein expression in astrocytes modulates neuronal survival and differentiation. J. Neurochem. 103, 2164-2176.
21. Lopes M. H., and, Santos T. G., (2012) Prion potency in stem cell biology. Prion 6, 1-5.
22. 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., and, 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.
23. Loubet D., Dakowski C., Pietri M., et al,. (2012) Neuritogenesis: the prion protein controls β1 integrin signaling activity. FASEB J. 26, 678-690.
24. Malaga-Trillo E., Solis G., Schrock Y., Geiss C., Luncz L., Thomanetz V., and, Stuermer C. A. O., (2009) Regulation of embryonic cell adhesion by the prion protein. PLoS Biol. 7, e1000055.
25. Manson J., West J. D., Thomson V., McBride P., Kaufman M. H., and, Hope J., (1992) The prion protein gene: a role in mouse embryogenesis? Development 115, 117-122.
26. Matveeva O., Nechipurenko Y., Rossi L., Moore B., Saetrom P., Ogurtsov A. Y., Atkins J. F., and, Shabalina S. A., (2007) Comparison of approaches for rational siRNA design leading to a new efficient and transparent method. Nucleic Acids Res. 35, e63.
27. McEwan J. F., Windsor M. L., and, Cullis-Hill S. D., (2009) Antibodies to prion protein inhibit human colon cancer cell growth. Tumour Biol. 30, 141-147.
28. Menchon C., Edel M. J., and, Izpisua Belmonte J. C., (2011) The cell cycle inhibitor p27(Kip)Â controls self-renewal and pluripotency of human embryonic stem cells by regulating the cell cycle, Brachyury and Twist. Cell Cycle 10, 1435-1447.
29. Meslin F., Hamai A., Gao P., Jalil A., Cahuzac N., Chouaib S., and, Mehrpour M., (2007) Silencing of prion protein sensitizes breast adriamycin-resistant carcinoma cells to TRAIL-mediated cell death. Cancer Res. 67, 10910-10919.
30. Miranda A., Pericuesta E., Ramirez M. A., and, Gutierrez-Adan A., (2011) Prion protein expression regulates embryonic stem cell pluripotency and differentiation. PLoS ONE 6, e18422.
31. Mouillet-Richard S., Laurendeau I., Vidaud M., Kellermann O., and, Laplamche J. L., (1999) Prion protein and neuronal differentiation: quantitative analysis of prnp gene expression in a murine inducible neuroectodermal progenitor. Microbes Infect. 1, 969-976.
32. Mouillet-Richard S., Ermonval M., Chebassier C., Laplanche J. L., Lehmann S., Launay J. M., and, Kellermann O., (2000) Signal transduction through prion protein. Science 289, 1925-1928.
33. Moya K. L., Hassig R., Breen K. C., Volland H., and, Giamberardino L. D., (2005) Axonal transport of the cellular prion protein is increased during axon regeneration. J. Neurochem. 92, 1044-1053.
34. Neganova I., Zhang X., Atkinson S., and, Lako M., (2009) Expression and functional analysis of G1 to S regulatory components reveals an important role for CDK2 in cell cycle regulation in human embryonic stem cells. Oncogene 28, 20-30.
35. Nishikawa S. I., Jakt L. M., and, Era T., (2007) Embryonic stem-cell culture as a tool for developmental cell biology. Nat. Rev. Mol. Cell Biol. 8, 502-507.
36. Panigaj M., Glier H., Wildova M., and, Holada K., (2011) Expression of prion protein in mouse erythroid progenitors and differentiating murine erythroleukemia cells. PLoS ONE 6, e24599.
37. Peralta O. A., Huckle W. R., and, Eyestone W. H., (2011) Expression and knockdown of cellular prion protein (PrPC) in differentiating mouse embryonic stem cells. Differentiation 81, 68-77.
38. Prusiner S. B., (1997) Prion diseases and the BSE crisis. Science 278, 245-251.
39. Roucou X., Giannopoulos P. N., Zhang Y., Jodoin J., Goodyer C. G., and, 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.
40. Ruiz S., Panopoulos A. D., Herrerias A., Bissig K. D., Lutz M., Berggren W. T., Verma I. M., and, Belmonte J. C. I., (2011) A high proliferation rate is required for cell reprogramming and maintenance of human embryonic stem cell identity. Curr. Biol. 21, 45-52.
41. Sales N., Hassig R., Rudolfo K., Giamberardino L. D., Traiffort E., Ruat M., Fre'tier P., and, Moya K. L., (2002) Developmental expression of the cellular prion protein in elongating axons. Eur. J. Neurosci. 15, 1163-1177.
42. Santos T. G., Silva I. R., Costa-Silva B., Lepigue A. P., Martins V. R., and, Lopes M. H., (2011) Enhanced neural progenitor/stem cells self-renewal via the interaction of stress-inducible protein 1 with the prion protein. Stem Cells 29, 1126-1136.
43. Santuccione A., Syntyk V., Leshchyns'ka I., and, 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.
44. 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.
45. Stahl N., Borchelt D. R., Hsiao K., and, Prusiner S. B., (1987) Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51, 229-240.
46. Steele A. D., Emsley J. G., Ozdinler P. H., Lindquist S., and, 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.
47. Stella R., Massimino M. L., Sandri M., Sorgato M. C., and, Bertoli A., (2010) Cellular prion protein promotes regeneration of adult muscle tissue. Mol. Cell. Biol. 30, 4864-4876.
48. Syed M., Nourizadeh-Lillabadi R., Press C. M., and, Alestrøm P., (2011) Prion protein function and the disturbance of early embryonic development in zebrafish. Prion 5, 88-92.
49. Thompson J. A., Itskovitz-Eldor J., Shapiro S. S., Waknitz M. A., Swiergiel J. J., Marshall V. S., and, Jones J. M., (1998) Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.
50. 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.
51. Tremblay P., Bouzamondo-Bernstein E., Heinrich C., Prusiner S. B., and, DeArmond S. J., (2007) Developmental expression of PrP in the post-implantation embryo. Brain Res. 1139, 60-67.
52. Viegas P., Chaverot N., Enslen H., Perriere N., Couraud P. O., and, 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.
53. White J., and, Dalton S., (2005) Cell cycle control of embryonic stem cells. Stem Cell Rev. 1, 131-138.
54. Young R., Passet B., Vilotte M., Cribiu E. P., Béringue V., Le Provost F., Laude H., and, Vilotte J. L., (2009) The prion or the related Shadoo protein is required for early mouse embryogenesis. FEBS Lett. 583, 3296-3300.
55. Zhang C. C., Steele A. D., Lindquist S., and, 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.