The doppel gene biology: A scientific journey from brain to testis, and return

Central European Journal of Biology

Volumn 1, Issue 4, 2006, Pages 494-505

  Comincini, Sergio ^a   Del Vecchio, Igor ^a   Azzalin, Alberto ^a  

^a UNIVERSITY OF PAVIA   (Italy)

Author keywords

Doppel; Neurodegeneration; Prion like protein; Tumor marker

Indexed keywords

EID: 33845935837     PISSN: 1895104X     EISSN: 16443632     Source Type: Journal    
DOI: 10.2478/s11535-006-0040-4     Document Type: Article

References (57)

1. S.B. Prusiner: "Prions", Proc. Natl. Acad. Sci. USA, Vol. 95, (1998), pp. 13363-13383.
2. B. Oesch, D.B. Teplow, N. Stahl, D. Serben, L.E. Hood and S.B. Prusiner: "Identification of cellular proteins binding to the scrapie prion protein", Biochemistry, Vol. 29, (1990), pp. 5848-5555.
3. R.C. Moore, I.Y. Lee, G.L. Silverman, P.M. Harrison, R. Strome, C. Heinrich, A. Karunaratne, S.H. Pasternak, M.A. Chishti, Y. Liang, P. Mastrangelo, K. Wang, A.F. Smit, S. Katamine, G.A. Carlson, F.E. Cohen, S.B. Prusiner, D.W. Melton, P. Tremblay, L.E. Hood and D. Westaway: "Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel", J. Mol. Biol, Vol. 292, (1999), pp. 797-817.
4. M.A. Tranulis, A. Espenes, S. Comincini, G. Skretting and I. Harbitz: "The PrP-like protein Doppel gene in sheep and cattle: cDNA sequence and expression", Mamm. Genome, Vol. 12, (2001), pp. 376-379.
5. E. Makrinou, J. Collinge and M. Antoniou: "Genomic characterization of the human prion protein (PrP) gene locus", Mamm. Genome, Vol. 13, (2002), pp. 696-703.
6. A. Li, S. Sakaguchi, K. Shigematsu, R. Atarashi, B.C. Roy, R. Nakaoke, K. Arima, N. Okimura, J. Kopacek and S. Katamine: "Physiological expression of the gene for PrP-like protein, PrPLP/Dpl, by brain endothelial cells and its ectopic expression in neurons of PrP-deficient mice ataxic due to Purkinje cell degeneration", Am. J. Pathol, Vol. 157, (2000), pp. 1447-1452.
7. C. Weissmann and A. Aguzzi: "Perspectives: neurobiology. PrP's double causes trouble", Science, Vol. 286, (1999), pp. 914-915.
8. G.L. Silverman, K. Qin, R.C. Moore, Y. Yang, P. Mastrangelo, P. Tremblay, S.B. Prusiner, F.E. Cohen and D. Westaway: "Doppel is an N-glycosylated, glycosylphosphatidylinositol-anchored protein. Expression in testis and ectopic production in the brains of Prnp(0/0) mice predisposed to Purkinje cell loss", J. Biol. Chem., Vol. 275, (2000), pp. 26834-26841.
9. K. Lu, W. Wang, Z. Xie, B.S. Wong, R. Li, R.B. Petersen, M.S. Sy and S.G. Chen: "Expression and structural characterization of the recombinant human doppel protein", Biochemistry, Vol. 39, (2000), pp. 13575-13583.
10. R. Zahn, P. Guntert, C. von Schroetter and K. Wuthrich: "NMR structure of a variant human priori protein with two disulfide bridges", J. Mol. Biol, Vol. 326, (2003), pp. 225-234.
11. T. Luhrs, R. Riek, P. Guntert and K. Wuthrich: "NMR structure of the human doppel protein", J. Mol. Biol., Vol. 326, (2003), pp. 1549-1557.
12. H. Mo, R.C. Moore, F.E. Cohen, D. Westaway, S.B. Prusiner, P.E. Wright and H.J. Dyson: "Two different neurodegenerative diseases caused by proteins with similar structures", Proc. Natl. Acad. Sci. USA, Vol. 98, (2001), pp. 2352-2357.
13. E.M. Nicholson, H. Mo, S.B. Prusiner, F.E. Cohen and S. Marqusee: "Differences between the prion protein and its homolog Doppel: a partially structured state with implications for scrapie formation", J. Mol. Biol., Vol. 316, (2002), pp. 807-815.
14. S.M. Whyte, I.D. Sylvester, S.R. Martin, A.C. Gill, F. Wopfner, H.M. Schatzl, G.G. Dodson and P.M. Bayley: "Stability and conformational properties of doppel, a prion-like protein, and its single-disulphide mutant", Biochem. J., Vol. 373, (2003), pp. 485-494.
15. H.A. Kretzschmar, T. Tings, A. Madlung, A. Giese and J. Herms: "Function of PrP(C) as a copper-binding protein at the synapse", Arch. Virol. Suppl., Vol. 16, (2000), pp. 239-249.
16. D. Shmerling, I. Hegyi, M. Fischer, T. Blattler, S. Brandner, J. Gotz, T. Rulicke, E. Flechsig, A. Cozzio, C. von Mering, C. Hangartner, A. Aguzzi and C. Weissmann: "Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions", Cell, Vol. 93, (1998), pp. 203-214.
17. D. Rossi, A. Cozzio, E. Flechsig, M.A. Klein, T. Rulicke, A. Aguzzi and C. Weissmann: "Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpi level in brain", EMBO J., Vol. 20, (2001), pp. 694-702.
18. N. Yamaguchi, S. Sakaguchi, K. Shigematsu, N. Okimura and S. Katamine: "Doppel-induced Purkinje cell death is stoichiometrically abrogated by prion protein", Biochem. Biophys. Res. Commun., Vol. 319, (2004), pp. 1247-1252.
19. A. Behrens and A. Aguzzi: "Small is not beautiful: antagonizing functions for the prion protein PrP(C) and its homologue Dpl", Trends Neurosci., Vol. 25, (2002), pp. 150-154.
20. P. Mastrangelo and D. Westaway: "The prion gene complex encoding PrP(C) and Doppel: insights from mutational analysis", Gene, Vol. 275, (2001), pp. 1-18.
21. S. Comincini, M.G. Foti, M.A. Tranulis, D. Hills, G. Di Guardo, G. Vaccari, J.L. Williams, I. Harbitz and L. Ferretti: "Genomic organization, comparative analysis, and genetic polymorphisms of the bovine and ovine prion Doppel genes (PRND)", Mamm. Genome, Vol. 12, (2001), pp. 729-733.
22. C. Uboldi, I. Del Vecchio, M.G. Foti, A. Azzalin, M. Paulis, E. Raimondi, G. Vaccari, U. Agrimi, G. Di Guardo, S. Comincini and L. Ferretti: "Prion-like Doppel gene (PRND) in the goat: genomic structure, cDNA, and polymorphisms", Mamm. Genome, Vol. 16, (2005), pp. 963-971.
23. S. Mead, J. Beck, A. Dickinson, E.M. Fisher and J. Collinge: "Examination of the human prion protein-like gene doppel for genetic susceptibility to sporadic and variant Creutzfeldt-Jakob disease", Neurosci. Lett., Vol. 290, (2000), pp. 117-120.
24. B.H. Jeong, N.H. Kim, J.I. Kim, R.I. Carp and Y.S. Kim: "Polymorphisms at codons 56 and 174 of the prion-like protein gene (PRND) are not associated with sporadic Creutzfeldt-Jakob disease", J. Hum. Genet., Vol. 50, (2005), pp. 311-314.
25. B. Schroder, B. Franz, P. Hempfling, M. Selbert, T. Jurgens, H.A. Kretzschmar, M. Bodemer, S. Poser and I. Zerr: "Polymorphisms within the prion-like protein gene (Prnd) and their implications in human prion diseases, Alzheimer's disease and other neurological disorders", Hum. Genet., Vol. 109, (2001), pp. 319-325.
26. N.L. Tuzi, E. Gall, D. Melton and J.C. Manson: "Expression of doppel in the CNS of mice does not modulate transmissible spongiform encephalopathy disease", J. Gen. Virol, Vol. 83, (2002), pp. 705-711.
27. K. Peoc'h, H. Volland, A. De Gassart, P. Beaudry, V. Sazdovitch, M.C. Sorgato, C. Creminon, J.L. Laplanche and S. Lehmann: "Prion-like protein Doppel expression is not modified in scrapie-infected cells and in the brains of patients with Creutzfeldt-Jakob disease", FEBS Lett., Vol. 536, (2003), pp. 61-65.
28. R.C. Moore, P. Mastrangelo, E. Bouzamondo, C. Heinrich, G. Legname, S.B. Prusiner, L. Hood, D. Westaway, S.J. DeArrnond and P. Tremblay: "Doppel-induced cerebellar degeneration in transgenic mice", Proc. Natl. Acad. Sci. USA, Vol. 18, (2001), pp. 15288-15293.
29. V.R. Martins, A.F. Mercadante, A.L. Cabral, A.R. Freitas and R.M. Castro: "Insights into the physiological function of cellular prion protein", Braz. J. Med. Biol. Res., Vol. 34, (2001), pp. 585-595.
30. A. Sakudo, T. Onodera, Y. Suganuma, T. Kobayashi, K. Saeki and K. Ikuta: "Recent advances in clarifying prion protein functions using knockout mice and derived cell lines", Mini Rev. Med. Chem., Vol. 6, (2006), pp. 589-601.
31. C. Hundt and S. Weiss: "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, Vol. 1689, (2004), pp. 1-5.
32. S.M. Yin, M.S. Sy, H.Y Yang, and P. Tien: "Interaction of Doppel with the full-length laminin receptor precursor protein", Arch. Biochem. Biophys., Vol. 428, (2004), pp. 165-169.
33. c proteins in human tumor astrocytic cells", Anticancer Res., Vol. 25, (2005), pp. 4369-4374.
34. A. Behrens, N. Genoud, H. Naumann, T. Rulicke, F. Janett, F.L. Heppner, B. Ledermann and A. Aguzzi: "Absence of the priori protein homologue Doppel causes male sterility", EMBO J., Vol. 21, (2002), pp. 3652-3658.
35. K. Peoc'h, C. Serres, Y. Frobert, C. Martin, S. Lehmann, S. Chasseigneaux, V. Sazdovitch, J. Grassi, P. Jouannet, J.M. Launay and J.L. Laplanche: "The human "prion-like" protein Doppel is expressed in both Sertoli cells and spermatozoa", J. Biol. Chem., Vol. 277, (2002), pp. 43071-43078.
36. N. Genoud, A. Behrens, I. Arrighi and A. Aguzzi: "Priori proteins and infertility: insight from mouse models", Cytogenet. Genome Res., Vol. 1.03, (2003), pp. 285-289.
37. D. Paisley, S. Banks, J. Selfridge, N.F. McLennan, A.M. Ritchie, C. McEwan, D.S. Irvine, P.T. Saunders, J.C. Manson and D.W. Melton: "Male infertility and DNA damage in Doppel knockout and prion protein/Doppel double-knockout mice", Am. J. Pathol., Vol. 164, (2004), pp. 2279-2288.
38. C. Serres, K. Peoc'h, A.M. Courtot, C. Lesaffre, P. Jouannet and J.L. Laplanche: "Spatio-developrnental distribution of the prion-like protein doppel in Mammalian testis: a comparative analysis focusing on its presence in the acrosome of spermatids", Biol. Reprod., Vol. 74, (2006), pp. 816-823.
39. A. Espenes, I. Harbitz, S. Skogtvedt, R. Fuglestveit, K.A. Berg, G. Dick, A. Krogenaes and M.A. Tranulis: "Dynamic expression of the prion-like protein Doppel in ovine testicular tissue", Int. J. Androl., Vol. 29, (2006), pp. 400-408.
40. M. Rondena, F. Ceciliani, S. Comazzi, V. Pocacqua, C. Bazzocchi, C. Luvoni, S. Chigioni and S. Paltrinieri: "Identification of bovine doppel protein in testis, ovary and ejaculated spermatozoa", Theriogenology, Vol. 63, (2005), pp. 1195-1206.
41. T. Cui, A. Holme, J. Sassoon and D.R. Brown: "Analysis of doppel protein toxicity", Mol. Cell. Neurosci., Vol. 23, (2003), pp. 144-155.
42. B.S. Wong, T. Liu, D. Paisley, R. Li, T. Pan, S.G. Chen, G. Perry, R.B. Petersen, M.A Smith, D.W. Melton, P. Gambetti, D.R. Brown and M.S. Sy: "Induction of HO-1 and NOS in doppel-expressing mice devoid of PrP: implications for doppel function", Mol. Cell. Neurosci, Vol. 17, (2001), pp. 768-775.
43. K. Qin, L. Zhao, Y. Tang, S. Bhatta, J.M. Simard and R.Y. Zhao: "Doppel-induced apoptosis and counteraction by cellular prion protein in neuroblastoma and astrocytes", Neuroscience, Vol. 141, (2006), pp. 1375-1388.
44. L. Maskri, X. Zhu, S. Fritzen, K. Kuhn, C. Ullmer, P. Engels, M. Andriske, C.C. Stichel and H. Lubbert: "Influence of different promoters on the expression pattern of mutated human alpha-synuclein in transgenic mice", Neurodegener. Dis., Vol. 1, (2004), pp. 255-265.
45. M. Calissano, E. Ensor, D.R. Brown and D.S. Latchrnan: "Doppel expression is regulated by the Brn-3a and Brn-3b transcription factors", Neuroreport, Vol. 15, (2004), pp. 483-486.
46. J. Nagyova, J. Pastorek and J. Kopacek: "Identification of the critical cis-acting elements in the promoter of the mouse Prnd gene coding for Doppel protein", Biochim. Biophys. Acta, Vol. 1689, (2004), pp. 288-293.
47. I. Del Vecchio, A. Azzalin, E. Guidi, G. Amati, T. Caramori, C. Uboldi, S. Comincini and L. Ferretti: "Functional mapping of the bovine Doppel gene promoter region", Gene, Vol. 356, (2005), pp. 101-108.
48. J. Sepelakova, M. Takacova, S. Pastorekova and J. Kopacek: "Involvement of upstream stimulatory factor in regulation of the mouse Prnd gene coding for Doppel protein", Biochim. Biophys. Acta, Vol. 1731, (2005), pp. 209-214.
49. I. Ferrer, M. Freixas, R. Blanco, M. Carmona and B. Puig: "Selective PrP-like protein, doppel immunoreactivity in dystrophic neurites of senile plaques in Alzheimer's disease", Neuropathol. Appl. Neurobiol, Vol. 30, (2004), pp. 329-337.
50. S. Comincini, A. Facoetti, I. Del Vecchio, K. Peoc'h, J.L. Laplanche, L. Magrassi, M. Ceroni, L. Ferretti and R. Nano: "Differential expression of the prion-like protein doppel gene (PRND) in astrocytomas: a new molecular marker potentially involved in tumor progression", Anticancer Res., Vol. 24, (2004), pp. 1507-1517.
51. S. Comincini, L.R. Chiarelli, P. Zelini, I. Del Vecchio, A. Azzalin, A. Arias, V. Ferrara, P. Rognoni, A. Dipoto, R. Nano, G. Valentini and L. Ferretti: "Nuclear mRNA retention and aberrant doppel protein expression in human astrocytic tumor cells", Oncol Rep., Vol. 16, (2006), pp. 1325-1332.
52. E. Travaglino, S. Comincini, C. Benatti, A. Azzalin, R. Nano, V. Rosti, L. Ferretti and R. Invernizzi: "Overexpression of the Doppel protein in acute rnyeloid leukaemias and myelodysplastic syndromes", Br. J. Haematol, Vol. 128, (2005), pp. 877-884.
53. A. Suri: "Cancer testis antigens-their importance in immunotherapy and in the early detection of cancer", Expert Opin. Biol. Ther., Vol. 6, (2006), pp. 379-389.
54. M. Premzl, J.E. Gready, L.S. Jermiin, T. Simonic and J.A. Marshall Graves: "Evolution of vertebrate genes related to prion and Shadoo proteins: clues from comparative genornic analysis", Mol Biol. Evol., Vol. 21, (2004), pp. 2210-2231.
55. E. Rivera-Milla, B. Oidtmann, C.H. Panagiotidis, M. Baier, T. Sklaviadis, S. Hoffmann, R.Y. Zhou, G.P. Solis, C.A. Stuerrner and E. Malaga-Trillo: "Disparate evolution of prion protein domains and the distinct origin of Doppel- and prion-related loci revealed by fish-to-mammal comparisons", FASEB J., Vol. 20, (2006), pp. 317-319.
56. M. Premzl, L. Sangiorgio, B. Strumbo, J.A. Marshall Graves, T. Simonic and J.E. Gready: "Shadoo, a new protein highly conserved from fish to mammals and with similarity to priori protein", Gene, Vol. 314, (2003), pp. 89-102.
57. S. Colacino, G. Tiana and G. Colombo: "Similar folds with different stabilization mechanisms: the cases of Prion and Doppel proteins", BMC Struct Biol., Vol. 21, (2006), pp. 6-17.