The role of prion protein in stem Cell regulation

Reproduction

Volumn 146, Issue 3, 2013, Pages

  Miranda, A ^a   Ramos Ibeas, P ^a   Pericuesta, E ^a   Ramirez, M A ^a   Gutierrez Adan, A ^a  

^a INIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CALCIUM; COPPER; COPPER PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; DISULFIDE; GLUCOSE; GLYCAN; GROWTH FACTOR; LAMININ; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE P38; NESTIN; PRION PROTEIN; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; RNA; SUPEROXIDE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTOME;

AEROBIC METABOLISM; AMINO ACID SEQUENCE; ANTIOXIDANT ACTIVITY; BINDING SITE; BRAIN DAMAGE; CELL DIFFERENTIATION; CELL EXPANSION; CELL MATURATION; CELL PROLIFERATION; CELL REGENERATION; CELL RENEWAL; CELL TRANSPLANTATION; CONFORMATION; DIFFERENTIATION; EMBRYO DEVELOPMENT; EMBRYOID BODY; EMBRYONIC STEM CELL; FEMALE GENITAL SYSTEM; GAMETOGENESIS; GLYCOSYLATION; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; HUMAN; IN VITRO STUDY; MALE GENITAL SYSTEM; MEMBRANE VESICLE; METABOLISM; MUSCLE CELL; NERVE CELL; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; POLYADENYLATION; PRION DISEASE; PRIORITY JOURNAL; REGENERATION; REGENERATIVE MEDICINE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPERMATOCYTE; SPERMATOGONIUM; STEM CELL; SUBVENTRICULAR ZONE; TISSUE REGENERATION; TRANSCRIPTION REGULATION; ZEBRA FISH;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; GERM CELLS; HUMANS; MALE; REGENERATION; SPERM MATURATION;

EID: 84885052285     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-13-0100     Document Type: Review

References (81)

1. Behrens A 2003 Physiological and pathological functions of the prion protein homologue Dpl. British Medical Bulletin 66 35-42. (doi:10.1093/bmb/66.1. 35) (Pubitemid 37173490)
2. Behrens A, Genoud N, Naumann H, Rulicke T, Janett F, Heppner FL, Ledermann B & Aguzzi A 2002 Absence of the prion protein homologue Doppel causes male sterility. EMBO Journal 21 3652-3658. (doi:10.1093/emboj/cdf386) (Pubitemid 34787039)
3. Bendheim PE, Brown HR, Rudelli RD, Scala LJ, Goller NL, Wen GY, Kascsak RJ, Cashman NR & Bolton DC 1992 Nearly ubiquitous tissue distribution of the scrapie agent precursor protein. Neurology 42 149-156. (doi:10.1212/WNL.42.1. 149)
4. Bremer J, Baumann F, Tiberi C, Wessig C, Fischer H, Schwarz P, Steele AD, Toyka KV, Nave KA, Weis J et al. 2010 Axonal prion protein is required for peripheral myelin maintenance. Nature Neuroscience 13 310-318. (doi:10.1038/nn. 2483)
5. Brown DR 2001 Prion and prejudice: normal protein and the synapse. Trends in Neurosciences 24 85-90. (doi:10.1016/S0166-2236 (00) 01689-1) (Pubitemid 32115438)
6. Brown D, Qin K, Herms J, Madlung A, Manson J, Strome R, Fraser P, Kruck T, von Bohlen A, Schulz-Schaeffer W et al. 1997 The cellular prion protein binds copper in vivo. Nature 390 684-687. (doi:10.1038/37733) (Pubitemid 28016346)
7. Brown DR, Schmidt B, Groschup MH & Kretzschmar HA 1998 Prion protein expression in muscle cells and toxicity of a prion protein fragment. European Journal of Cell Biology 75 29-37. (doi:10.1016/S0171-9335 (98) 80043-5) (Pubitemid 28080644)
8. Brown D, Wong B, Hafiz F, Clive C, Haswell S & Jones I 1999 Normal prion protein has an activity like that of superoxide dismutase. Biochemical Journal 344 1-5. (doi:10.1042/0264-6021:3440001)
9. Brown KL, Ritchie DL, McBride PA & Bruce ME 2000 Detection of PrP in extraneural tissues. Microscopic Research and Technique 50 40-45. (doi:10.1002/1097-0029 (20000701) 50:1<40::AID-JEMT7>3.0. CO;2-M) (Pubitemid 30497404)
10. Bueler H, Fischer M, Lang Y, Bluethmann H, Lipp HP, DeArmond SJ, Prusiner SB, Aguet M & Weissmann C 1992 Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356 577-582. (doi:10.1038/356577a0)
11. Castilla J, Gutierrez Adan A, Brun A, Pintado B, Ramirez MA, Parra B, Doyle D, Rogers M, Salguero FJ, Sanchez C et al. 2003 Early detection of PrPres in BSE-infected bovine PrP transgenic mice. Archives of Virology 148 677-691. (doi:10.1007/s00705-002-0958-4) (Pubitemid 36425158)
12. Cotto E, Andre M, Forgue J, Fleury H & Babin P 2005 Molecular characterization, phylogenetic relationships, and developmental expression patterns of prion genes in zebrafish (Danio rerio). FEBS Journal 272 500-513. (doi:10.1111/j.1742-4658.2004.04492.x)
13. Criado JR, Sanchez-Alavez M, Conti B, Giacchino JL, Wills DN, Henriksen SJ, Race R, Manson JC, Chesebro B & Oldstone MB 2005 Mice devoid of prion protein have cognitive deficits that are rescued by reconstitution of PrP in neurons. Neurobiology of Disease 19 255-265. (doi:10.1016/j.nbd.2005.01.001) (Pubitemid 40544743)
14. Daude N, Wohlgemuth S, Brown R, Pitstick R, Gapeshina H, Yang J, Carlson GA & Westaway D 2012 Knockout of the prion protein (PrP)-like Sprn gene does not produce embryonic lethality in combination with PrP (C)-deficiency. PNAS 109 9035-9040. (doi:10.1073/pnas.12021 30109)
15. Ecroyd H, Sarradin P, Dacheux JL & Gatti JL 2004 Compartmentalization of prion isoforms within the reproductive tract of the ram. Biology of Reproduction 71 993-1001. (doi:10.1095/biolreprod.104.029801) (Pubitemid 39108664)
16. Faustino RS, Behfar A, Perez-Terzic C & Terzic A 2008 Genomic chart guiding embryonic stem cell cardiopoiesis. Genome Biology 9 R6. (doi:10.1186/gb-2008-9-1-r6) (Pubitemid 351911941)
17. Ford MJ, Burton LJ, Morris RJ & Hall SM 2002 Selective expression of prion protein in peripheral tissues of the adult mouse. Neuroscience 113 177-192. (doi:10.1016/S0306-4522 (02) 00155-0) (Pubitemid 34786023)
18. Fujisawa M, Kanai Y, Nam SY, Maeda S, Nakamuta N, Kano K, Kurohmaru M & Hayashi Y 2004 Expression of Prnp mRNA (prion protein gene) in mouse spermatogenic cells. Journal of Reproduction and Development 50 565-570. (doi:10.1262/jrd.50.565) (Pubitemid 40631781)
19. Gatti JL, Metayer S, Moudjou M, Andreoletti O, Lantier F, Dacheux JL & Sarradin P 2002 Prion protein is secreted in soluble forms in the epididymal fluid and proteolytically processed and transported in seminal plasma. Biology of Reproduction 67 393-400. (doi:10.1095/biolreprod67.2.393) (Pubitemid 34803920)
20. Goh A, Li C, Sy M & Wong B 2007 Altered prion protein glycosylation in the aging mouse brain. Journal of Neurochemistry 100 841-854. (doi:10.1111/j.1471-4159.2006.04268.x) (Pubitemid 46095632)
21. Graner E, Mercadante AF, Zanata SM, Forlenza OV, Cabral AL, Veiga SS, Juliano MA, Roesler R, Walz R, Minetti A et al. 2000 Cellular prion protein binds laminin and mediates neuritogenesis. Brain Research. Molecular Brain Research 76 85-92. (doi:10.1016/S0169-328X (99) 00334-4) (Pubitemid 30133236)
22. Grskovic M, Chaivorapol C, Gaspar-Maia A, Li H & Ramalho-Santos M 2007 Systematic identification of cis-regulatory sequences active in mouse and human embryonic stem cells. PLoS Genetics 3 e145. (doi:10.1371/journal.pgen. 0030145)
23. Hager G, Pawelzik H, Kreutzberg GW & Zieglgansberger W 1998 A peptide derived from a neurite outgrowth-promoting domain on the gamma 1 chain of laminin modulates the electrical properties of neocortical neurons. Neuroscience 86 1145-1154. (doi:10.1016/S0306-4522 (98) 00082-7) (Pubitemid 28318540)
24. Hailesellasse Sene K, Porter CJ, Palidwor G, Perez-Iratxeta C, Muro EM, Campbell PA, Rudnicki MA & Andrade-Navarro MA 2007 Gene function in early mouse embryonic stem cell differentiation. BMC Genomics 8 85. (doi:10.1186/1471-2164-8-85) (Pubitemid 46579171)
25. Hajj GN, Santos TG, Cook ZS & Martins VR 2009 Developmental expression of prion protein and its ligands stress-inducible protein 1 and vitronectin. Journal of Comparative Neurology 517 371-384. (doi:10.1002/cne. 22157)
26. Harris DA, Lele P & Snider WD 1993 Localization of the mRNA for a chicken prion protein by in situ hybridization. PNAS 90 4309-4313. (doi:10.1073/pnas.90.9.4309) (Pubitemid 23134216)
27. Kanaani J, Prusiner S, Diacovo J, Baekkeskov S & Legname G 2005 Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. Journal of Neurochemistry 95 1373-1386. (doi:10.1111/j.1471-4159.2005.03469.x) (Pubitemid 41779262)
28. Kibbey MC, Jucker M, Weeks BS, Neve RL, Van Nostrand WE & Kleinman HK 1993 β-Amyloid precursor protein binds to the neuritepromoting IKVAV site of laminin. PNAS 90 10150-10153. (doi:10.1073/pnas.90.21.10150) (Pubitemid 23328269)
29. Koch M, Olson PF, Albus A, Jin W, Hunter DD, Brunken WJ, Burgeson RE & Champliaud MF 1999 Characterization and expression of the laminin gamma3 chain: a novel, non-basement membrane-associated, laminin chain. Journal of Cell Biology 145 605-618. (doi:10.1083/jcb. 145.3.605)
30. Lazzari C, Peggion C, Stella R, Massimino ML, Lim D, Bertoli A & Sorgato MC 2011 Cellular prion protein is implicated in the regulation of local Ca2C movements in cerebellar granule neurons. Journal of Neurochemistry 116 881-890. (doi:10.1111/j.1471-4159.2010.07015.x)
31. Lee YJ & Baskakov IV 2010 Treatment with normal prion protein delays differentiation and helps to maintain high proliferation activity in human embryonic stem cells. Journal of Neurochemistry 114 362-373. (doi:10.1111/j.1471-4159.2010.06601.x)
32. Lee YJ & Baskakov IV 2013 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 124 310-322. (doi:10.1111/j.1471-4159.2012.07913.x)
33. Li A & Harris DA 2005 Mammalian prion protein suppresses Bax-induced cell death in yeast. Journal of Biological Chemistry 280 17430-17434. (doi:10.1074/jbc. C500058200) (Pubitemid 41389214)
34. Liao MJ, Zhang CC, Zhou B, Zimonjic DB, Mani SA, Kaba M, Gifford A, Reinhardt F, Popescu NC, Guo Wet al. 2007 Enrichment of a population of mammary gland cells that form mammospheres and have in vivo repopulating activity. Cancer Research 67 8131-8138. (doi:10.1158/0008-5472. CAN-06-4493) (Pubitemid 47395148)
35. Linden R, Martins VR, Prado MA, Cammarota M, Izquierdo I & Brentani RR 2008 Physiology of the prion protein. Physiological Reviews 88 673-728. (doi:10.1152/physrev. 00007.2007) (Pubitemid 351520090)
36. Liu T, Li R, Wong BS, Liu D, Pan T, Petersen RB, Gambetti P & Sy MS 2001 Normal cellular prion protein is preferentially expressed on subpopulations of murine hemopoietic cells. Journal of Immunology 166 3733-3742. (Pubitemid 32224896)
37. Lopes MH & Santos TG 2012 Prion potency in stem cells biology. Prion 6 142-146. (doi:10.4161/pri.19035)
38. Malaga-Trillo E & Sempou E 2009 PrPs: proteins with a purpose: lessons from the zebrafish. Prion 3 129-133. (doi:10.4161/pri.3.3.9651)
39. Malaga-Trillo E, Solis GP, Schrock Y, Geiss C, Luncz L, Thomanetz V & Stuermer CA 2009 Regulation of embryonic cell adhesion by the prion protein. PLoS Biology 7 e55. (doi:10.1371/journal.pbio.1000055)
40. Manson J, West JD, Thomson V, McBride P, Kaufman MH & Hope J 1992 The prion protein gene: a role in mouse embryogenesis? Development 115 117-122.
41. Manson JC, Clarke AR, Hooper ML, Aitchison L, McConnell I & Hope J 1994 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Molecular Neurobiology 8 121-127. (doi:10.1007/BF02780662)
42. Massimino ML, Ferrari J, Sorgato MC & Bertoli A 2006 Heterogeneous PrPC metabolism in skeletal muscle cells. FEBS Letters 580 878-884. (doi:10.1016/j.febslet.2006.01.008) (Pubitemid 43152308)
43. McLennan NF, Brennan PM, McNeill A, Davies I, Fotheringham A, Rennison KA, Ritchie D, Brannan F, Head MW, Ironside JW et al. 2004 Prion protein accumulation and neuroprotection in hypoxic brain damage. American Journal of Pathology 165 227-235. (doi:10.1016/S0002-9440 (10) 63291-9) (Pubitemid 38821830)
44. Mehrpour M & Codogno P 2009 Prion protein: from physiology to cancer biology. Cancer Letters 290 1-23. (doi:10.1016/j.canlet.2009.07.009)
45. Miele G, Alejo Blanco AR, Baybutt H, Horvat S, Manson J & Clinton M 2003 Embryonic activation and developmental expression of the murine prion protein gene. Gene Expression 11 1-12. (doi:10.3727/000000003783992324) (Pubitemid 36395880)
46. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, Schorderet P, Bernstein BE, Jaenisch R, Lander ES & Meissner A 2008 Dissecting direct reprogramming through integrative genomic analysis. Nature 454 49-55. (doi:10.1038/ nature07056) (Pubitemid 351931978)
47. Miranda A, Pericuesta E, Ramirez MA & Gutierrez-Adan A. 2011a Prion protein in ESC regulation. Prion 5 169-171. (doi:10.4161/pri.5.3.16797)
48. Miranda A, Pericuesta E, Ramírez MÁ & Gutierrez-Adan A. 2011b Prion protein expression regulates embryonic stem cell pluripotency and differentiation. PLoS ONE 6 e18422. (doi:10.1371/journal.pone. 0018422)
49. Mohanty ST, Cairney CJ, Chantry AD, Madan S, Fernandes JA, Howe SJ, Moore HD, Thompson MJ, Chen B, Thrasher A et al. 2012 A small molecule modulator of prion protein increases human mesenchymal stem cell lifespan, ex vivo expansion, and engraftment to bone marrow in NOD/SCID mice. Stem Cells 30 1134-1143. (doi:10.1002/stem.1065)
50. Nazor KE, Seward T & Telling GC 2007 Motor behavioral and neuropathological deficits in mice deficient for normal prion protein expression. Biochimica et Biophysica Acta 1772 645-653. (doi:10.1016/j.bbadis. 2007.04.004) (Pubitemid 46880209)
51. Nourizadeh-Lillabadi R, Seilo Torgersen J, Vestrheim O, Konig M, Alestrom P & Syed M 2010 Early embryonic gene expression profiling of zebrafish prion protein (Prp2) morphants. PLoS ONE 5 e13573. (doi:10.1371/journal.pone. 0013573)
52. Novitskaya V, Makarava N, Sylvester I, Bronstein IB & Baskakov IV 2007 Amyloid fibrils of mammalian prion protein induce axonal degeneration in NTERA2-derived terminally differentiated neurons. Journal of Neurochemistry 102 398-407. (doi:10.1111/j.1471-4159.2007.04537.x) (Pubitemid 47000598)
53. Ohta H, Sekulovic S, Bakovic S, Eaves CJ, Pineault N, Gasparetto M, Smith C, Sauvageau G & Humphries RK 2007 Near-maximal expansions of hematopoietic stem cells in culture using NUP98-HOX fusions. Experimental Hematology 35 817-830. (doi:10.1016/j.exphem.2007. 02.012) (Pubitemid 46601757)
54. Paisley D, Banks S, Selfridge J, McLennan NF, Ritchie AM, McEwan C, Irvine DS, Saunders PT, Manson JC & Melton DW 2004 Male infertility and DNA damage in Doppel knockout and prion protein/Doppel double-knockout mice. American Journal of Pathology 164 2279-2288. (doi:10.1016/S0002-9440 (10) 63784-4) (Pubitemid 38669373)
55. Palmqvist L, Pineault N, Wasslavik C & Humphries RK 2007 Candidate genes for expansion and transformation of hematopoietic stem cells by NUP98-HOX fusion genes. PLoS ONE 2 e768. (doi:10.1371/journal. pone.0000768)
56. Pan Y, Zhao L, Liang J, Liu J, Shi Y, Liu N, Zhang G, Jin H, Gao J, Xie H et al. 2006 Cellular prion protein promotes invasion and metastasis of gastric cancer. FASEB Journal 20 1886-1888. (doi:10.1096/fj.06-6138fje) (Pubitemid 44933770)
57. Passet B, Young R, Makhzami S, Vilotte M, Jaffrezic F, Halliez S, Bouet S, Marthey S, Khalife M, Kanellopoulos-Langevin C et al. 2012 Prion protein and Shadoo are involved in overlapping embryonic pathways and trophoblastic development. PLoS ONE 7 e41959. (doi:10.1371/journal.pone.0041959)
58. Peoc'h K, Serres C, Frobert Y, Martin C, Lehmann S, Chasseigneaux S, Sazdovitch V, Grassi J, Jouannet P, Launay JM et al. 2002 The human "prion-like" protein Doppel is expressed in both Sertoli cells and spermatozoa. Journal of Biological Chemistry 277 43071-43078. (doi:10.1074/jbc. M206357200) (Pubitemid 35285689)
59. Peralta OA, Huckle WR & Eyestone WH 2011 Expression and knockdown of cellular prion protein (PrPC) in differentiating mouse embryonic stem cells. Differentiation 81 68-77. (doi:10.1016/j.diff.2010.09.181)
60. Peralta O, Huckle W & Eyestone W 2012 Developmental expression of the cellular prion protein (PrP (C)) in bovine embryos. Molecular Reproduction and Development 79 488-498. (doi:10.1002/mrd.22057)
61. Pineault N, Abramovich C, Ohta H & Humphries RK 2004 Differential and common leukemogenic potentials of multiple NUP98-Hox fusion proteins alone or with Meis1. Molecular and Cellular Biology 24 1907-1917. (doi:10.1128/MCB.24.5. 1907-1917.2004) (Pubitemid 38248932)
62. Prestori F, Rossi P, Bearzatto B, Laine J, Necchi D, Diwakar S, Schiffmann SN, Axelrad H & D'AngeloE 2008 Altered neuron excitability and synaptic plasticity in the cerebellar granular layer of juvenile prion protein knock-out mice with impaired motor control. Journal of Neuroscience 28 7091-7103. (doi:10.1523/JNEUROSCI.0409-08.2008)
63. Prusiner SB 1982 Novel proteinaceous infectious particles cause scrapie. Science 216 136-144. (doi:10.1126/science.6801762) (Pubitemid 12089840)
64. Rivera-Milla E, Oidtmann B, Panagiotidis CH, Baier M, Sklaviadis T, Hoffmann R, Zhou Y, Solis GP, Stuermer CA & Malaga-Trillo E 2006 Disparate evolution of prion protein domains and the distinct origin of Doppel- and prion-related loci revealed by fish-to-mammal comparisons. FASEB Journal 20 317-319. (doi:10.1096/fj.05-4279fje) (Pubitemid 46671156)
65. Robakis NK, Sawh PR, Wolfe GC, Rubenstein R, Carp RI & Innis MA 1986 Isolation of a cDNA clone encoding the leader peptide of prion protein and expression of the homologous gene in various tissues. PNAS 83 6377-6381. (doi:10.1073/pnas.83.17.6377) (Pubitemid 17174739)
66. Sakaguchi S, Katamine S, Nishida N, Moriuchi R, Shigematsu K, Sugimoto T, Nakatani A, Kataoka Y, Houtani T, Shirabe S et al. 1996 Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature 380 528-531. (doi:10.1038/380528a0) (Pubitemid 26110641)
67. Sales N, Hassig R, Rodolfo K, Di Giamberardino L, Traiffort E, Ruat M, Fretier P & Moya K 2002 Developmental expression of the cellular prion protein in elongating axons. European Journal of Neuroscience 15 1163-1177. (doi:10.1046/j.1460-9568.2002.01953.x) (Pubitemid 35463617)
68. Santos TG, Silva IR, Costa-Silva B, Lepique AP, Martins VR & Lopes MH 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. (doi:10.1002/stem.664)
69. Shaked Y, Rosenmann H, Talmor G & Gabizon R 1999 A C-terminaltruncated PrP isoform is present in mature sperm. Journal of Biological Chemistry 274 32153-32158. (doi:10.1074/jbc.274.45.32153) (Pubitemid 29522955)
70. Singh A, Kong Q, Luo X, Petersen RB, Meyerson H & Singh N 2009 Prion protein (PrP) knock-out mice show altered iron metabolism: a functional role for PrP in iron uptake and transport. PLoS ONE 4 e6115. (doi:10.1371/journal.pone. 0006115)
71. Steele AD, Emsley JG, Ozdinler PH, Lindquist S & Macklis JD 2006 Prion protein (PrPc) positively regulates neural precursor proliferation during developmental and adult mammalian neurogenesis. PNAS 103 3416-3421. (doi:10.1073/pnas.0511290103) (Pubitemid 43346483)
72. Stella R, Massimino ML, Sandri M, Sorgato MC & Bertoli A 2010 Cellular prion protein promotes regeneration of adult muscle tissue. Molecular and Cellular Biology 30 4864-4876. (doi:10.1128/MCB.01040-09)
73. Stockel J, Safar J, Wallace A, Cohen F & Prusiner S 1998 Prion protein selectively binds copper (II) ions. Biochemistry 37 7185-7193. (doi:10.1021/bi972827k) (Pubitemid 28235199)
74. Tanji K, Saeki K, Matsumoto Y, Takeda M, Hirasawa K, Doi K, Matsumoto Y & Onodera T 1995 Analysis of PrPc mRNA by in situ hybridization in brain, placenta, uterus and testis of rats. Intervirology 38 309-315. (Pubitemid 26305780)
75. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS & Jones JM 1998 Embryonic stem cell lines derived from human blastocysts. Science 282 1145-1147. (doi:10.1126/science.282. 5391.1145) (Pubitemid 28516247)
76. Tremblay P, Bouzamondo-Bernstein E, Heinrich C, Prusiner S & DeArmond S 2007 Developmental expression of PrP in the postimplantation embryo. Brain Research 1139 60-67.
77. Watts JC & Westaway D 2007 The prion protein family: diversity, rivalry, and dysfunction. Biochimica et Biophysica Acta 1772 654-672. (doi:10.1016/j.bbadis.2007.05.001) (Pubitemid 46880210)
78. Weise J, Sandau R, Schwarting S, Crome O, Wrede A, Schulz-Schaeffer W, Zerr I & Bahr M 2006 Deletion of cellular prion protein results in reduced Akt activation, enhanced postischemic caspase-3 activation, and exacerbation of ischemic brain injury. Stroke 37 1296-1300. (doi:10.1161/01. STR.0000217262.03192.d4) (Pubitemid 43731879)
79. Weissmann C & Flechsig E 2003 PrP knock-out and PrP transgenic mice in prion research. British Medical Bulletin 66 43-60. (doi:10.1093/bmb/66. 1.43) (Pubitemid 37173491)
80. Young R, Passet B, Vilotte M, Cribiu EP, Beringue V, Le Provost F, Laude H & Vilotte JL 2009 The prion or the related Shadoo protein is required for early mouse embryogenesis. FEBS Letters 583 3296-3300. (doi:10.1016/j.febslet. 2009.09.027)
81. Zhang CC, Steele AD, Lindquist S & Lodish HF 2006 Prion protein is expressed on long-term repopulating hematopoietic stem cells and is important for their self-renewal. PNAS 103 2184-2189. (doi:10.1073/pnas.0510577103) (Pubitemid 43271644)