Nuclear mRNA retention and aberrant doppel protein expression in human astrocytic tumor cells

Oncology Reports

Volumn 16, Issue 6, 2006, Pages 1325-1332

  Comincini, Sergio ^a   Chiarelli, Laurent R ^a   Zelini, Paola ^a   Del Vecchio, Igor ^a   Azzalin, Alberto ^a   Arias, Agustina ^a   Ferrara, Valentina ^a   Rognoni, Paola ^a   Dipoto, Antonella ^a   Nano, Rosanna ^a   Valentini, Giovanna ^a   Ferretti, Luca ^a  

^a UNIVERSITY OF PAVIA   (Italy)

Author keywords

Astrocytoma cell lines; Dpl; Glial tumor; Glycosylation; Nucleus; PRND

Indexed keywords

MESSENGER RNA; PRND PROTEIN, HUMAN;

ARTICLE; ASTROCYTOMA; BIOSYNTHESIS; BRAIN TUMOR; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; NORTHERN BLOTTING; PRION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ASTROCYTOMA; BLOTTING, NORTHERN; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; PRIONS; PROTEIN BIOSYNTHESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 33845920974     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.16.6.1325     Document Type: Article

References (47)

1. Moore RC, Lee IY, Silverman GL, Harrison PM, Strome R, Heinrich C, Karunaratne A, Pasternak SH, Chishti MA, Liang Y, Mastrangelo P, Wang K, Smit AF, Katamine S, Carlson GA, Cohen FE, Prusiner SB, Melton DW, Tremblay P, Hood LE and Westaway D: Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J Mol Biol 292: 797-817, 1999. (Pubitemid 29465475)
2. Li A, Sakaguchi S, Atarashi R, Roy BC, Nakaoke R, Arima K, Okimura N, Kopacek J and Shigematsu K: Identification of a novel gene encoding a PrP-like protein expressed as chimeric transcripts fused to PrP exon 1/2 in ataxic mouse line with a disrupted PrP gene. Cell Mol Neurobiol 20: 553-567, 2000. (Pubitemid 30481893)
3. Mead S, Beck J, Dickinson A, Fisher EM and Collinge J: Examination of the human prion protein-like gene doppel for genetic susceptibility to sporadic and variant Creutzfeldt-Jakob disease. Neurosci Lett 290: 117-220, 2000.
4. Tranulis MA, Espenes A, Comincini S, Skretting G and Harbitz I: The PrP-like protein Doppel gene in sheep and cattle: cDNA sequence and expression. Mamm Genome 12: 376-379, 2001. (Pubitemid 32430059)
5. Uboldi C, Del Vecchio I, Foti MG, Azzalin A, Paulis M, Raimondi E, Vaccari G, Agrimi U, i Di Guardo G, Comincini S and Ferretti L: The prion-like Doppel gene (PRND) in the goat: genomic structure, cDNA and polymorphisms. Mamm Genome 16: 963-971, 2005.
6. Fournier JG: Nonneuronal cellular prion protein. Int Rev Cytol 208: 121-161, 2001.
7. Peoc'h K, Volland H, De Gassart A, Beaudry P, Sazdovitch V, Sorgato MC, Creminon C, Laplanche JL and Lehmann S: Prion-like protein Doppel expression is not modified in scrapie-infected cells and in the brains of patients with Creutzfeldt-Jakob disease. FEBS Lett 536: 61-65, 2003. (Pubitemid 36206407)
8. Makrinou E, Collinge J and Antoniou M: Genomic characterization of the human prion protein (PrP) gene locus. Mamm Genome 13: 696-703, 2002. (Pubitemid 36056865)
9. Behrens A, Genoud N, Naumann H, Rulicke T, Janett F, Heppner FL, Ledermann B and Aguzzi A: Absence of the prion protein homologue Doppel causes male sterility. EMBO J 21: 3652-3658, 2002. (Pubitemid 34787039)
10. Peoc'h K, Serres C, Frobert Y, Martin C, Lehmann S, Chasseigneaux S, Sazdovitch V, Grassi J, Jouannet P, Launay JM and Laplanche JL: The human 'prion-like' protein Doppel is expressed in both Sertoli cells and spermatozoa. J Biol Chem 277: 43071-43078, 2002. (Pubitemid 35285689)
11. Paisley D, Banks S, Selfridge J, McLennan NF, Ritchie AM, McEwan C, Irvine DS, Saunders PT, Manson JC and Melton DW: Male infertility and DNA damage in Doppel knockout and prion protein/Doppel double-knockout mice. Am J Pathol 164: 2279-2288, 2004. (Pubitemid 38669373)
12. Zahn R, Liu A, Luhrs T, Riek R, von Schroetter C, Lopez Garcia F, Billeter M, Calzolai L, Wider G and Wuthrich K: NMR solution structure of the human prion protein. Proc Natl Acad Sci USA 97: 145-150, 2002.
13. Luhrs T, Riek R, Guntert P and Wuthrich K: NMR structure of the human doppel protein. J Mol Biol 326: 1549-1557, 2003. (Pubitemid 36269094)
14. Mastrangelo P and Westaway D: The prion gene complex encoding PrP(C) and Doppel: insights from mutational analysis. Gene 275: 1-18, 2002.
15. Weissmann C and Aguzzi A: PrP's double causes trouble. Science 286: 914-915, 1999.
16. Rossi D, Cozzio A, Flechsig E, Klein MA, Rulicke T, Aguzzi A and Weissmann C: Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpl level in brain. EMBO J 20: 694-702, 2001. (Pubitemid 32167634)
17. Behrens A and Aguzzi A: Small is not beautiful: antagonizing functions for the prion protein PrP(C) and its homologue Dpl. Trends Neurosci 25: 150-154, 2002. (Pubitemid 34164340)
18. Comincini S, Foti MG, Tranulis MA, Hills D, Di Guardo G, Vaccari G, Williams JL, Harbitz I and Ferretti L: Genomic organization, comparative analysis, and genetic polymorphism of the bovine and ovine prion Doppel genes (PRND). Mamm Genome 12: 729-733, 2001. (Pubitemid 32800564)
19. Tuzi NL, Gall E, Melton D and Manson JC: Expression of doppel in the CNS of mice does not modulate transmissible spongiform encephalopathy disease. J Gen Virol 83: 705-711, 2002. (Pubitemid 34183015)
20. Ferrer I, Freixas M, Blanco R, Carmona M and Puig B: Selective PrP-like protein, doppel immunoreactivity in dystrophic neurites of senile plaques in Alzheimer's disease. Neuropathol Appl Neurobiol 30: 329-337, 2004. (Pubitemid 39120294)
21. Comincini S, Facoetti A, Del Vecchio I, Peoc'h K, Laplanche JL, Magrassi L, Ceroni M, Ferretti L and Nano R: Differential expression of the prion-like protein doppel gene (PRND) in astrocytomas: a new molecular marker potentially involved in tumor progression. Anticancer Res 24: 1507-1517, 2004. (Pubitemid 38954671)
22. Travaglino E, Comincini S, Benatti C, Azzalin A, Nano R, Rosti V, Ferretti L and Invernizzi R: Overexpression of the Doppel protein in acute myeloid leukaemias and myelodysplastic syndromes. Br J Haematol 128: 877-884, 2005. (Pubitemid 40444883)
23. Zhu Y and Parada LF: The molecular and genetic basis of neurological tumours. Nature Rev Cancer 2: 616-626, 2002. (Pubitemid 37328928)
24. Comincini S: Searching for molecular markers of human gliomas. Funct Neurol 16: 291-298, 2001.
25. Holland EC: Gliomagenesis: genetic alterations and mouse models. Nat Rev Genet 2: 120-129, 2000.
26. Rasheed BK, McLendon RE, Herndon JE, Friedman HS, Friedman AH, Bigner DD and Bigner SH: Alterations of the TP53 gene in human gliomas. Cancer Res 54: 1324-1330, 1994. (Pubitemid 24108076)
27. Nozaki M, Tada M, Kobayashi H, Zhang CL, Sawamura Y, Abe H, Ishii N and Van Meir EG: Roles of the functional loss of p53 and other genes in astrocytoma tumorigenesis and progression. J Neurooncol 1: 124-137, 1999.
28. Kimura T, Budka H and Soler-Federsppiel S: An immunocytochemical comparison of the glial-associated proteins glial fibrillary acidic protein (GFAP) and S-100 protein (S100P) in human brain tumors. Clin Neuropathol 5: 21-27, 1996.
29. Sallinen SL, Sallinen PK, Haapasalo HK, Helin HJ, Helen PT, Schraml P, Kallioniemi OP and Kononen J: Identification of differentially expressed genes in human gliomas by DNA microarray and tissue chip techniques. Cancer Res 60: 6617-6622, 2000.
30. Godard S, Getz G, Delorenzi M, Farmer P, Kobayashi H, Desbaillets I, Nozaki M, Diserens AC, Hamou MF, Dietrich PY, Regli L, Janzer RC, Bucher P, Stupp R, de Tribolet N, Domany E and Hegi ME: Classification of human astrocytic gliomas on the basis of gene expression: a correlated group of genes with angiogenic activity emerges as a strong predictor of subtypes. Cancer Res 63: 6613-6625, 2003. (Pubitemid 37322939)
31. Mischel PS, Shai R, Shi T, Horvath S, Lu KV, Choe G, Seligson D, Kremen TJ, Palotie A, Liau LM, Cloughesy TF and Nelson SF: Identification of molecular subtypes of glioblastoma by gene expression profiling. Oncogene 22: 2361-2373, 2003. (Pubitemid 36566791)
32. Zhang R, Tremblay TL, McDermid A, Thibault P and Stanimirovic D: Identification of differentially expressed proteins in human glioblastoma cell lines and tumors. Glia 42: 194-208, 2003. (Pubitemid 36565123)
33. Bacciocchi G, Gibelli N, Zibera C, Pedrazzoli P, Bergamaschi G, De Piceis Polver P, Danova M, Mazzini G, Palomba L and Tupler R: Establishment and characterization of two cell lines derived from human glioblastoma multiforme. Anticancer Res 12: 853-861, 1992.
34. Kleihues P and Cavenee WK: World Health Organization Classification of Tumors of the Nervous System. Lyon, France: WHO/IARC, 2000.
35. Lowry OM, Rosebrough MJ, Farr AL and Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
36. Edge ASB, Faltynek CR, Hof L, Reichert LE and Weber P: Deglycosylation of glycoproteins by trifluoromethanesulfonic acid. Anal Biochem 118: 131-137, 1981.
37. Stark LA and Dunlop MG: Nucleolar sequestration of RelA (p65) regulates NF-kappaB-driven transcription and apoptosis. Mol Cell Biol 25: 5985-6004, 2005. (Pubitemid 40946553)
38. Bentley DL: Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr Opin Cell Biol 17: 251-256, 2005.
39. Saguez C, Olesen JR and Jensen TH: Formation of export-competent mRNP: escaping nuclear destruction. Curr Opin Cell Biol 17: 287-293, 2005. (Pubitemid 40719919)
40. Dube DH and Bertozzi CR: Glycans in cancer and inflammation potential for therapeutics and diagnostics. Nat Rev Drug Discov 4: 477-488, 2005. (Pubitemid 40861990)
41. Dennis JW, Granovsky M and Warren CE: Glycoprotein glycosylation and cancer progression. Biochim Biophys Acta 1473: 21-34, 1999.
42. Silverman GL, Qin K, Moore RC, Yang Y, Mastrangelo P, Tremblay P, Prusiner SB, Cohen FE and Westaway D: 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 275: 26834-26841, 2000.
43. Rondena M, Ceciliani F, Comazzi S, Pocacqua V, Bazzocchi C, Luvoni C, Chigioni S and Paltrinieri S: Identification of bovine doppel protein in testis, ovary and ejaculated spermatozoa. Theriogenology 63: 1195-1206, 2005. (Pubitemid 40234522)
44. Mayor S and Riezman H: Sorting GPI-anchored proteins. Nat Rev Mol Cell Biol 5: 110-120, 2004. (Pubitemid 38160254)
45. Wong BS, Liu T, Paisley D, Li R, Pan T, Chen SG, Perry G, Petersen RB, Smith MA, Melton DW, Gambetti P, Brown DR and Sy MS: Induction of HO-1 and NOS in doppel-expressive mice devoid of PrP: implications for doppel function. Mol Cell Neurosci 17: 768-775, 2001. (Pubitemid 32430051)
46. Atarashi R, Sakaguchi S, Shigematsu K, Arima K, Okimura N, Yamaguchi N, Li A, Kopacecek J and Katamine S: Abnormal activation of glial cells in the brains of prion protein deficient mice ectopically expressing prion protein-like protein PrPLP/Dpl. Mol Med 7: 803-809, 2001. (Pubitemid 34175303)
47. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] method. Methods 25: 402-408, 2001. (Pubitemid 34164012)