The prion protein and its paralogue doppel affect calcium signaling in Chinese hamster ovary cells

Molecular Biology of the Cell

Volumn 16, Issue 6, 2005, Pages 2799-2808

  Brini, Marisa ^a   Miuzzo, Manuela ^a   Pierobon, Nicola ^a   Negro, Alessandro ^a   Sorgato, Maria Catia ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; PRION PROTEIN; PROTEIN DOPPEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DEATH; CELLULAR DISTRIBUTION; CHINESE HAMSTER; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; MITOCHONDRION; NONHUMAN; OVARY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CALCIUM; CALCIUM SIGNALING; CELL CULTURE TECHNIQUES; CELL MEMBRANE; CHELATING AGENTS; CHO CELLS; CRICETINAE; CRICETULUS; CYTOSOL; DENSITOMETRY; ENDOPLASMIC RETICULUM; FURA-2; GREEN FLUORESCENT PROTEINS; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MITOCHONDRIA; PRIONS; PRPC PROTEINS; RECOMBINANT PROTEINS;

CRICETINAE; CRICETULUS GRISEUS;

EID: 19644370391     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-10-0915     Document Type: Article

References (75)

1. Arnaudeau, S., Frieden, M., Nakamura, K., Castelbou, C., Michalak, M., and Demaurex, N. (2002). Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. J. Biol. Chem. 277, 46696-46705.
2. Atarashi, R., Nishida, N., Shigematsu, K., Goto, S., Kondo, T., Sakaguchi, S., and Katamine, S. (2003). Deletion of N-terminal residues 23-88 from prion protein (PrP) abrogates the potential to rescue PrP-deficient mice from PrP-like protein/doppel-induced neurodegeneration. J. Biol. Chem. 278, 28944-28949.
3. 2+] in the endoplasmic reticulum and cytoplasm of intact HeLa cells: a comparative study. J. Biol. Chem. 272, 27694-27699.
4. Barrow, P. A., Holmgren, C. D., Tapper, A. J., and Jefferys, J. G. (1999). Intrinsic physiological and morphological properties of principal cells of the hippocampus and neocortex in hamsters infected with scrapie. Neurobiol. Dis. 6, 406-423.
5. Behrens, A., and Aguzzi, A. (2002). Small is not beautiful: antagonizing functions for the prion protein PrP(C) and its homologue Dpl. Trends Neurosci. 25, 150-154.
6. Bernardi, P. (1999). Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 79, 1127-1155.
7. 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.
8. 2+ signalling in mitochondria: mechanism and role in physiology and pathology. Cell Calcium 34, 399-405.
9. 2+ signalling. EMBO J 19, 4926-4935.
10. c): a critical evaluation. J. Biol. Chem. 270, 9896-9903.
11. Brown, D. R., Nicholas, R. S., and Canevari, L. (2002). Lack of prion protein expression results in a neuronal phenotype sensitive to stress. J. Neurosci. Res. 67, 211-224.
12. Brown, D. R. et al. (1997). The cellular priori protein binds copper in vivo. Nature 390, 684-687.
13. Bueler, H., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H. P., DeArmond, S. J., Prusiner, S. B., Aguet, M., and Weissmann, C. (1992). Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582.
14. Cathala, F., and Baron, H. (1987). Clinical aspects of Creutzfeldt-Jakob disease. In: Prions: Novel Infectious Pathogens Causing Scrapie and CreutzfeldtJakob Disease, ed. S. B. Prusiner and M. P. McKinley, San Diego: Academic Press, 467-509.
15. Cereghetti, G. M., Negro, A., Vinck, E., Massimino, M. L., Sorgato, M. C., and Van Doorslaer, S. (2004). Copper(II) binding to the human Doppel protein may mark its functional diversity from the prion protein. J. Biol. Chem. 279, 36497-36503.
16. Chiarini, L. B., Freitas, A. R., Zanata, S. M., Brentani, R. R., Martins, V. R., and Linden, R. (2002). Cellular prion protein transduces neuroprotective signals. EMBO J. 21, 3317-3326.
17. + currents. Neurosci. Lett. 209, 49-52.
18. Cryns, V., and Yuan, J. (1998). Proteases to die for. Genes Dev. 12, 1551-1570.
19. 2+ entry, and spontaneous transmitter release. Neuron 29, 197-208.
20. 2+ entry. J. Biol. Chem. 275, 40187-40194.
21. Filippin, L., Magalhaes, P. J., Di Benedetto, G., Colella, M., and Pozzan, T. (2003). Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J. Biol. Chem. 278, 39224-39234.
22. Gray, F., Chretien, F., Adle-Biassette, H., Dorandeu, A., Ereau, T., Delisle, M. B., Kopp, N., Ironside, J. W., and Vital, C. (1999). Neuronal apoptosis in Creutzfeldt-Jakob disease. J. Neuropathol. Exp. Neurol. 58, 321-328.
23. + currents in cerebellar Purkinje cells. Neurobiol. Dis. 8, 324-330.
24. Herms, J. W., Korte, S., Gall, S., Schneider, I., Dunker, S., and Kretzschmar, H. A. (2000). Altered intracellular calcium homeostasis in cerebellar granule cells of prion protein-deficient mice. J. Neurochem. 75, 1487-1492.
25. Hetz, C., Maundrell, K., and Soto, C. (2003a). Is loss of function of the prion protein the cause of prion disorders? Trends Mol. Med. 9, 237-243.
26. Hetz, C., Russelakis-Carneiro, M., Maundrell, K., Castilla, J., and Soto, C. (2003b). Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J. 22, 5435-5445.
27. Jefferys, J. G., Empson, R. M., Whittington, M. A., and Prusiner, S. B. (1994). Scrapie infection of transgenic mice leads to network and intrinsic dysfunction of cortical and hippocampal neurones. Neurobiol. Dis. 3, 25-30.
28. Jin, T., Gu, Y., Zanusso, G., Sy, M., Kumar, A., Cohen, M., Gambetti, P., and Singh, N. (2000). The chaperone protein BiP binds to a mutant prion protein and mediates its degradation by the proteasome. J. Biol. Chem. 275, 38699-38704.
29. Johnston, A. R., Fraser, J. R., Jeffrey, M., and MacLeod, N. (1998). Synaptic plasticity in the CA1 area of the hippocampus of scrapie-infected mice. Neurobiol. Dis. 5, 188-195.
30. Jouaville, L. S., Pinton, P., Bastianutto, C., Rutter, G. A., and Rizzuto, R. (1999). Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc. Natl. Acad. Sci. USA 96, 13807-13812.
31. 2+ pool. J. Biol. Chem. 264, 15192-15198.
32. Krause, K. H., and Michalak, M. (1997). Calreticulin. Cell 88, 439-443.
33. Kuwahara, C. et al. (1999). Prions prevent neuronal cell-line death. Nature 400, 225-226.
34. Li, A., Sakaguchi, S., Shigematsu, K., Atarashi, R., Roy, B. C., Nakaoke, R., Arima, K., Okimura, N., Kopacek, J., and Katamine, S. (2000). 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. 157, 1447-1452.
35. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptoric protease cascade. Cell 91, 479-489.
36. 2+ monolayers and suspensions of various cell types of animal cells. J. Cell Biol. 105, 2145-2155.
37. Mallucci, G. R., Ratte, S., Asante, E. A., Linehan, J., Gowland, I., Jefferys, J. G., and Collinge, J. (2002). Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 21, 202-210.
38. Manson, J. C., Clarke, A. R., Hooper, M. L., Aitchison, L., McConnell, I., and Hope, J. (1994). 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol. 8, 121-127.
39. 2+ beneath the plasma membrane of living A7r5 cells. EMBO J. 16, 1575-1581.
40. Massimino, M. L., Ballarin, C., Bertoli, A., Casonato, S., Genovesi, S., Negro, A., and Sorgato, M. C. (2004). Human Doppel and prion protein share common membrane microdomains and internalization pathways. Int. J. Biochem. Cell Biol. 36, 2016-2031.
41. Mattson, M. P., LaFerla, F. M., Chan, S. L., Leissring, M. A., Shepel, P. N., and Geiger, J. D. (2000). Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 23, 222-229.
42. Mo, H., Moore, R. C., Cohen, F. E., Westaway, D., Prusiner, S. B., Wright, P. E., and Dyson, H. J. (2001). Two different neurodegenerative diseases caused by proteins with similar structures. Proc. Natl. Acad. Sci. USA 98, 2352-2357.
43. 2+ entry through basal membrane patch. Cell 88, 49-55.
44. 2+ concentration in the endoplasmic reticulum of intact cells. EMBO J. 14, 5467-5475.
45. 2+ transients that modulate secretion. Nat. Cell. Biol. 2, 57-61.
46. Moore, R. C., Mastrangelo, P., Bouzamondo, E., Heinrich, C., Legname, G., Prusiner, S. B., Hood, L., Westaway, D., DeArmond, S. J., and Tremblay, P. (2001). Doppel-induced cerebellar degeneration in transgenic mice, Proc. Natl. Acad. Sci. USA 98, 15288-15293.
47. Moore, R. C. et al. (1999). Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J. Mol. Biol. 292, 797-817.
48. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B. A., and Yuan, J. (2000). Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403, 98-103.
49. Negro, A., Ballarin, C., Bertoli, A., Massimino, M. L., and Sorgato, M. C. (2001). The metabolism and imaging in live cells of the bovine prion protein in its native form or carrying single amino acid substitutions. Mol. Cell Neurosci, 17, 521-538.
50. Negro, A., Meggio, F., Bertoli, A., Battistutta, R., Sorgato, M. C., and Pinna, L. A. (2000). Susceptibility of the prion protein to enzymic phosphorylation. Biochem, Biophys. Res. Commun. 273, 337-341.
51. Orrenius, S., Zhivotovsky, B., and Nicotera, P. (2003). Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell. Biol. 4, 552-565.
52. Paschen, W. (2001). Dependence of vital cell function on endoplasmic reticulum calcium levels: implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell Calcium 29, 1-11.
53. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J. 20, 2690-2701.
54. 2+ influx in Bcl-2-overexpressing cells. J. Cell Biol. 148, 857-862.
55. Prusiner, S. B. (1998). Prions. Proc. Natl. Acad. Sci. USA 95, 13363-13383.
56. Putney, J. W., Jr. (2003). Capacitative calcium entry in the nervous system. Cell Calcium 34, 339-344.
57. Putney, J. W., Jr., Broad, L. M., Braun, F. J., Lievremont, J. P., and Bird, G. S. (2001). Mechanisms of capacitative calcium entry. J. Cell Sci. 334, 2223-2229.
58. 2+ revealed by specifically targeted recombinant aequorin. Nature 358, 325-328.
59. Rizzuto, R., Brini, M., Bastianutto, C., Marsault, R., and Pozzan, T. (1995). Photoprotein-mediated measurement of calcium ion concentration in mitochondria of living cells. Methods Enzymol. 260, 417-428.
60. 2+ responses. Science 280, 1763-1766.
61. Rossi, D., Cozzio, A., Flechsig, E., Klein, M. A., Rulicke, T., Aguzzi, A., and Weissmann, C. (2001). Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpi level in brain. EMBO J. 20, 694-702.
62. Sakaguchi, S. et al. (1996). Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature 380, 528-531.
63. Sakudo, A., Lee, D. C., Saeki, K., Nakamura, Y., Inoue, K., Matsumoto, Y., Itohara, S., and Onodera, T. (2003). Impairment of Superoxide dismutase activation by N-terminally truncated prion protein (PrP) in PrP-deficient neuronal cell line. Biochem. Biophys. Res. Commun. 308, 660-667.
64. Sakudo, A. et al. (2004). Prion protein suppresses perturbation of cellular copper homeostasis under oxidative conditions. Biochem. Biophys. Res. Commun. 333, 850-855.
65. Shmerling, D. et al. (1998). Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 93, 203-214.
66. 0/0 mice predisposed to Purkinje cell loss. J. Biol. Chem. 275, 26834-26842.
67. Singh, N., Zanusso, G., Chen, S. G., Fujioka, H., Richardson, S., Gambetti, P., and Petersen, R. B. (1997). Prion protein aggregation reverted by low temperature in transfected cells carrying a prion protein gene mutation. J. Biol. Chem. 272, 28461-28470.
68. 2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 306, 67-69.
69. 2+-ATPase. Proc. Natl. Acad. Sci. USA 87, 2466-2470.
70. Toescu, E. C., and Verkhratsky, A. (2003). Neuronal ageing from an intraneuronal perspective: roles of endoplasmic reticulum and mitochondria. Cell Calcium 34, 311-323.
71. 2+ store. Cell Calcium 35, 115-121.
72. Whatley, S. A., Powell, J. F., Politopoulou, G., Campbell, I. C., Brammer, M. J., and Percy, N. S. (1995). Regulation of intracellular free calcium levels by the cellular prion protein. Neuroreport 6, 2333-2337.
73. Wong, B. S. et al. (2001). Induction of HO-1 and NOS in doppel-expressing mice devoid of PrP: implications for doppel function. Mol. Cell. Neurosci. 17, 768-775.
74. Yamaguchi, N., Sakaguchi, S., Shigematsu, K., Okimura, N., and Katamine, S. (2004). Doppel-induced Purkinje cell death is stoichiometrically abrogated by prion protein. Biochem. Biophys. Res. Commun. 319, 1247-1252.
75. Zanusso, G., Petersen, R. B., Jin, T., Jing, Y., Kanoush, R., Ferrari, S., Gambetti, P., and Singh, N. (1999). Proteasomal degradation and N-terminal protease resistance of the codon 145 mutant prion protein. J. Biol. Chem. 274, 23396-23404.