Infectious prion protein alters manganese transport and neurotoxicity in a cell culture model of prion disease

NeuroToxicology

Volumn 32, Issue 5, 2011, Pages 554-562

  Martin, Dustin P ^a   Anantharam, Vellareddy ^a   Jin, Huajun ^a   Witte, Travis ^b   Houk, Robert ^b   Kanthasamy, Arthi ^a   Kanthasamy, Anumantha G ^a  

^a Department of Biomedical Sciences   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Manganese; Metals; Neurotoxicity; Prion

Indexed keywords

CASPASE 3; MANGANESE; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; PRION PROTEIN; TRANSFERRIN;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; DNA FRAGMENTATION; MASS SPECTROMETRY; NERVE CELL NECROSIS; NEUROTOXICITY; OXIDATIVE STRESS; PRION DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SCRAPIE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL CULTURE TECHNIQUES; CELLS, CULTURED; MANGANESE; NEURONS; PRION DISEASES; PRIONS;

EID: 82455164097     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.07.008     Document Type: Article

References (99)

1. Abdelraheim S.R., Kralovicova S., Brown D.R. Hydrogen peroxide cleavage of the prion protein generates a fragment able to initiate polymerisation of full length prion protein. Int J Biochem Cell Biol 2006, 38:1429-1440.
2. Afeseh Ngwa H., Kanthasamy A., Anantharam V., Song C., Witte T., Houk R., et al. Vanadium induces dopaminergic neurotoxicity via protein kinase Cdelta dependent oxidative signaling mechanisms: relevance to etiopathogenesis of Parkinson's disease. Toxicol Appl Pharmacol 2009, 240:273-285.
3. Aguzzi A., Heikenwalder M. Pathogenesis of prion diseases: current status and future outlook. Nat Rev Microbiol 2006, 4:765-775.
4. Alikunju S., Abdul Muneer P.M., Zhang Y., Szlachetka A.M., Haorah J. The inflammatory footprints of alcohol-induced oxidative damage in neurovascular components. Brain Behav Immun 2011, 25(Suppl 1):S129-S136.
5. Anantharam V., Kanthasamy A., Choi C.J., Martin D.P., Latchoumycandane C., Richt J.A., et al. Opposing roles of prion protein in oxidative stress- and ER stress-induced apoptotic signaling. Free Radic Biol Med 2008, 45:1530-1541.
6. Anantharam V., Kitazawa M., Wagner J., Kaul S., Kanthasamy A.G. Caspase-3-dependent proteolytic cleavage of protein kinase Cdelta is essential for oxidative stress-mediated dopaminergic cell death after exposure to methylcyclopentadienyl manganese tricarbonyl. J Neurosci 2002, 22:1738-1751.
7. Aschner M., Erikson K.M., Herrero Hernandez E., Tjalkens R. Manganese and its role in Parkinson's disease: from transport to neuropathology. Neuromolecular Med 2009, 11:252-266.
8. Aschner M., Vrana K.E., Zheng W. Manganese uptake and distribution in the central nervous system (CNS). Neurotoxicology 1999, 20:173-180.
9. Basu S., Mohan M.L., Luo X., Kundu B., Kong Q., Singh N. Modulation of proteinase K-resistant prion protein in cells and infectious brain homogenate by redox iron: implications for prion replication and disease pathogenesis. Mol Biol Cell 2007, 18:3302-3312.
10. Bishop G.M., Robinson S.R., Liu Q., Perry G., Atwood C.S., Smith M.A. Iron: a pathological mediator of Alzheimer disease?. Dev Neurosci 2002, 24:184-187.
11. Bolton D.C., Meyer R.K., Prusiner S.B. Scrapie PrP 27-30 is a sialoglycoprotein. J Virol 1985, 53:596-606.
12. Bossy-Wetzel E., Schwarzenbacher R., Lipton S.A. Molecular pathways to neurodegeneration. Nat Med 2004, 10(Suppl):S2-S9.
13. Brandner S. CNS pathogenesis of prion diseases. Br Med Bull 2003, 66:131-139.
14. Brazier M.W., Davies P., Player E., Marken F., Viles J.H., Brown D.R. Manganese binding to the prion protein. J Biol Chem 2008, 283:12831-12839.
15. Brown D.R. Mayhem of the multiple mechanisms: modelling neurodegeneration in prion disease. J Neurochem 2002, 82:209-215.
16. Brown D.R. Metallic prions. Biochem Soc Symp 2004, 193-202.
17. Brown D.R. Brain proteins that mind metals: a neurodegenerative perspective. Dalton Trans 2009, 4069-4076.
18. Brown D.R., Clive C., Haswell S.J. Antioxidant activity related to copper binding of native prion protein. J Neurochem 2001, 76:69-76.
19. Brown D.R., Hafiz F., Glasssmith L.L., Wong B.S., Jones I.M., Clive C., et al. Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J 2000, 19:1180-1186.
20. Brown D.R., Wong B.S., Hafiz F., Clive C., Haswell S.J., Jones I.M. Normal prion protein has an activity like that of superoxide dismutase. Biochem J 1999, 344(Pt. 1):1-5.
21. Brown L.R., Harris D.A. Copper and zinc cause delivery of the prion protein from the plasma membrane to a subset of early endosomes and the Golgi. J Neurochem 2003, 87:353-363.
22. Bush A.I., Curtain C.C. Twenty years of metallo-neurobiology: where to now?. Eur Biophys J 2008, 37:241-245.
23. Cahill C.M., Lahiri D.K., Huang X., Rogers J.T. Amyloid precursor protein and alpha synuclein translation, implications for iron and inflammation in neurodegenerative diseases. Biochim Biophys Acta 2009, 1790:615-628.
24. Cereghetti G.M., Schweiger A., Glockshuber R., Van Doorslaer S. Stability and Cu(II) binding of prion protein variants related to inherited human prion diseases. Biophys J 2003, 84:1985-1997.
25. Chen S., Mange A., Dong L., Lehmann S., Schachner M. Prion protein as trans-interacting partner for neurons is involved in neurite outgrowth and neuronal survival. Mol Cell Neurosci 2003, 22:227-233.
26. Chiarini L.B., Freitas A.R., Zanata S.M., Brentani R.R., Martins V.R., Linden R. Cellular prion protein transduces neuroprotective signals. EMBO J 2002, 21:3317-3326.
27. Choi C.J., Anantharam V., Martin D.P., Nicholson E.M., Richt J.A., Kanthasamy A., et al. Manganese upregulates cellular prion protein and contributes to altered stabilization and proteolysis: relevance to role of metals in pathogenesis of prion disease. Toxicol Sci 2010, 115:535-546.
28. Choi C.J., Anantharam V., Saetveit N.J., Houk R.S., Kanthasamy A., Kanthasamy A.G. Normal cellular prion protein protects against manganese-induced oxidative stress and apoptotic cell death. Toxicol Sci 2007, 98:495-509.
29. Choi C.J., Kanthasamy A., Anantharam V., Kanthasamy A.G. Interaction of metals with prion protein: possible role of divalent cations in the pathogenesis of prion diseases. Neurotoxicology 2006, 27:777-787.
30. Collinge J. Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 2001, 24:519-550.
31. Collinge J. Molecular neurology of prion disease. J Neurol Neurosurg Psychiatry 2005, 76:906-919.
32. Crossgrove J., Zheng W. Manganese toxicity upon overexposure. NMR Biomed 2004, 17:544-553.
33. Di Natale G., Grasso G., Impellizzeri G., La Mendola D., Micera G., Mihala N., et al. Copper(II) interaction with unstructured prion domain outside the octarepeat region: speciation, stability, and binding details of copper(II) complexes with PrP106-126 peptides. Inorg Chem 2005, 44:7214-7225.
34. Erikson K.M., Aschner M. Increased manganese uptake by primary astrocyte cultures with altered iron status is mediated primarily by divalent metal transporter. Neurotoxicology 2006, 27:125-130.
35. Fernaeus S., Land T. Increased iron-induced oxidative stress and toxicity in scrapie-infected neuroblastoma cells. Neurosci Lett 2005, 382:217-220.
36. Fernaeus S., Reis K., Bedecs K., Land T. Increased susceptibility to oxidative stress in scrapie-infected neuroblastoma cells is associated with intracellular iron status. Neurosci Lett 2005, 389:133-136.
37. Fevrier B., Vilette D., Laude H., Raposo G. Exosomes: a bubble ride for prions?. Traffic 2005, 6:10-17.
38. Fitsanakis V.A., Piccola G., Marreilha dos Santos A.P., Aschner J.L., Aschner M. Putative proteins involved in manganese transport across the blood-brain barrier. Hum Exp Toxicol 2007, 26:295-302.
39. Freixes M., Rodriguez A., Dalfo E., Ferrer I. Oxidation, glycoxidation, lipoxidation, nitration, and responses to oxidative stress in the cerebral cortex in Creutzfeldt-Jakob disease. Neurobiol Aging 2006, 27:1807-1815.
40. Gaeta A., Hider R.C. The crucial role of metal ions in neurodegeneration: the basis for a promising therapeutic strategy. Br J Pharmacol 2005, 146:1041-1059.
41. Gaggelli E., Jankowska E., Kozlowski H., Marcinkowska A., Migliorini C., Stanczak P., et al. Structural characterization of the intra- and inter-repeat copper binding modes within the N-terminal region of " prion related protein" (PrP-rel-2) of zebrafish. J Phys Chem B 2008, 112:15140-15150.
42. Garrick M.D., Kuo H.C., Vargas F., Singleton S., Zhao L., Smith J.J., et al. Comparison of mammalian cell lines expressing distinct isoforms of divalent metal transporter 1 in a tetracycline-regulated fashion. Biochem J 2006, 398:539-546.
43. Giese A., Levin J., Bertsch U., Kretzschmar H. Effect of metal ions on de novo aggregation of full-length prion protein. Biochem Biophys Res Commun 2004, 320:1240-1246.
44. Hesketh S., Sassoon J., Knight R., Brown D.R. Elevated manganese levels in blood and CNS in human prion disease. Mol Cell Neurosci 2008, 37:590-598.
45. Hesketh S., Sassoon J., Knight R., Hopkins J., Brown D.R. Elevated manganese levels in blood and central nervous system occur before onset of clinical signs in scrapie and bovine spongiform encephalopathy. J Anim Sci 2007, 85:1596-1609.
46. Hooper N.M., Taylor D.R., Watt N.T. Mechanism of the metal-mediated endocytosis of the prion protein. Biochem Soc Trans 2008, 36:1272-1276.
47. Hornshaw M.P., McDermott J.R., Candy J.M. Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem Biophys Res Commun 1995, 207:621-629.
48. Jackson G.S., Murray I., Hosszu L.L., Gibbs N., Waltho J.P., Clarke A.R., et al. Location and properties of metal-binding sites on the human prion protein. Proc Natl Acad Sci U S A 2001, 98:8531-8535.
49. Jones C.E., Abdelraheim S.R., Brown D.R., Viles J.H. Preferential Cu2+ coordination by His96 and His111 induces beta-sheet formation in the unstructured amyloidogenic region of the prion protein. J Biol Chem 2004, 279:32018-32027.
50. Jones C.E., Klewpatinond M., Abdelraheim S.R., Brown D.R., Viles J.H. Probing copper2+ binding to the prion protein using diamagnetic nickel2+ and 1H NMR: the unstructured N terminus facilitates the coordination of six copper2+ ions at physiological concentrations. J Mol Biol 2005, 346:1393-1407.
51. Kaul S., Kanthasamy A., Kitazawa M., Anantharam V., Kanthasamy A.G. Caspase-3 dependent proteolytic activation of protein kinase C delta mediates and regulates 1-methyl-4-phenylpyridinium (MPP+)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration. Eur J Neurosci 2003, 18:1387-1401.
52. Kim N.H., Choi J.K., Jeong B.H., Kim J.I., Kwon M.S., Carp R.I., et al. Effect of transition metals (Mn, Cu, Fe) and deoxycholic acid (DA) on the conversion of PrPC to PrPres. FASEB J 2005, 19:783-785.
53. Kitazawa M., Anantharam V., Yang Y., Hirata Y., Kanthasamy A., Kanthasamy A.G. Activation of protein kinase C delta by proteolytic cleavage contributes to manganese-induced apoptosis in dopaminergic cells: protective role of Bcl-2. Biochem Pharmacol 2005, 69:133-146.
54. Krasemann S., Zerr I., Weber T., Poser S., Kretzschmar H., Hunsmann G., et al. Prion disease associated with a novel nine octapeptide repeat insertion in the PRNP gene. Brain Res Mol Brain Res 1995, 34:173-176.
55. Latchoumycandane C., Anantharam V., Kitazawa M., Yang Y., Kanthasamy A., Kanthasamy A.G. Protein kinase Cdelta is a key downstream mediator of manganese-induced apoptosis in dopaminergic neuronal cells. J Pharmacol Exp Ther 2005, 313:46-55.
56. Lee D.W., Sohn H.O., Lim H.B., Lee Y.G., Kim Y.S., Carp R.I., et al. Alteration of free radical metabolism in the brain of mice infected with scrapie agent. Free Radic Res 1999, 30:499-507.
57. Mahal S.P., Baker C.A., Demczyk C.A., Smith E.W., Julius C., Weissmann C. Prion strain discrimination in cell culture: the cell panel assay. Proc Natl Acad Sci U S A 2007, 104:20908-20913.
58. Mange A., Milhavet O., Umlauf D., Harris D., Lehmann S. PrP-dependent cell adhesion in N2a neuroblastoma cells. FEBS Lett 2002, 514:159-162.
59. Mead S., Webb T.E., Campbell T.A., Beck J., Linehan J.M., Rutherfoord S., et al. Inherited prion disease with 5-OPRI: phenotype modification by repeat length and codon 129. Neurology 2007, 69:730-738.
60. Milhavet O., McMahon H.E., Rachidi W., Nishida N., Katamine S., Mange A., et al. Prion infection impairs the cellular response to oxidative stress. Proc Natl Acad Sci U S A 2000, 97:13937-13942.
61. Molina-Holgado F., Hider R.C., Gaeta A., Williams R., Francis P. Metals ions and neurodegeneration. Biometals 2007, 20:639-654.
62. Nadal R.C., Abdelraheim S.R., Brazier M.W., Rigby S.E., Brown D.R., Viles J.H. Prion protein does not redox-silence Cu2+, but is a sacrificial quencher of hydroxyl radicals. Free Radic Biol Med 2007, 42:79-89.
63. Nunziante M., Gilch S., Schatzl H.M. Essential role of the prion protein N terminus in subcellular trafficking and half-life of cellular prion protein. J Biol Chem 2003, 278:3726-3734.
64. Owen F., Poulter M., Lofthouse R., Collinge J., Crow T.J., Risby D., et al. Insertion in prion protein gene in familial Creutzfeldt-Jakob disease. Lancet 1989, 1:51-52.
65. Palmer M.S., Collinge J. Human prion diseases. Curr Opin Neurol Neurosurg 1992, 5:895-901.
66. Palmer M.S., Collinge J. Mutations and polymorphisms in the prion protein gene. Hum Mutat 1993, 2:168-173.
67. Park R.M., Schulte P.A., Bowman J.D., Walker J.T., Bondy S.C., Yost M.G., et al. Potential occupational risks for neurodegenerative diseases. Am J Ind Med 2005, 48:63-77.
68. Pauly P.C., Harris D.A. Copper stimulates endocytosis of the prion protein. J Biol Chem 1998, 273:33107-33110.
69. Perera W.S., Hooper N.M. Ablation of the metal ion-induced endocytosis of the prion protein by disease-associated mutation of the octarepeat region. Curr Biol 2001, 11:519-523.
70. Peters P.J., Mironov A., Peretz D., van Donselaar E., Leclerc E., Erpel S., et al. Trafficking of prion proteins through a caveolae-mediated endosomal pathway. J Cell Biol 2003, 162:703-717.
71. Petersen R.B., Siedlak S.L., Lee H.G., Kim Y.S., Nunomura A., Tagliavini F., et al. Redox metals and oxidative abnormalities in human prion diseases. Acta Neuropathol 2005, 110:232-238.
72. Prado M.A., Alves-Silva J., Magalhaes A.C., Prado V.F., Linden R., Martins V.R., et al. PrPc on the road: trafficking of the cellular prion protein. J Neurochem 2004, 88:769-781.
73. Prusiner S.B. Molecular biology of prion diseases. Science 1991, 252:1515-1522.
74. Prusiner S.B., DeArmond S.J. Prion diseases of the central nervous system. Monogr Pathol 1990, 86-122.
75. Prusiner S.B., Kingsbury D.T. Prions-infectious pathogens causing the spongiform encephalopathies. CRC Crit Rev Clin Neurobiol 1985, 1:181-200.
76. Prusiner S.B., Scott M., Foster D., Pan K.M., Groth D., Mirenda C., et al. Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 1990, 63:673-686.
77. Renner C., Fiori S., Fiorino F., Landgraf D., Deluca D., Mentler M., et al. Micellar environments induce structuring of the N-terminal tail of the prion protein. Biopolymers 2004, 73:421-433.
78. Roth J.A., Horbinski C., Higgins D., Lein P., Garrick M.D. Mechanisms of manganese-induced rat pheochromocytoma (PC12) cell death and cell differentiation. Neurotoxicology 2002, 23:147-157.
79. Sakudo A., Lee D.C., Yoshimura E., Nagasaka S., Nitta K., Saeki K., et al. Prion protein suppresses perturbation of cellular copper homeostasis under oxidative conditions. Biochem Biophys Res Commun 2004, 313:850-855.
80. Sango K., Yanagisawa H., Kato K., Kato N., Hirooka H., Watabe K. Differential effects of high glucose and methylglyoxal on viability and polyol metabolism in immortalized adult mouse Schwann cells. Open Diabetes J 2008, 1-11.
81. Sayre L.M., Perry G., Smith M.A. Redox metals and neurodegenerative disease. Curr Opin Chem Biol 1999, 3:220-225.
82. Shum S.C., Neddersen R., Houk R.S. Elemental speciation by liquid chromatography-inductively coupled plasma mass spectrometry with direct injection nebulization. Analyst 1992, 117:577-582.
83. Singh A., Isaac A.O., Luo X., Mohan M.L., Cohen M.L., Chen F., et al. Abnormal brain iron homeostasis in human and animal prion disorders. PLoS Pathog 2009, 5:e1000336.
84. Smargiassi A., Mutti A. Peripheral biomarkers and exposure to manganese. Neurotoxicology 1999, 20:401-406.
85. Stredrick D.L., Stokes A.H., Worst T.J., Freeman W.M., Johnson E.A., Lash L.H., et al. Manganese-induced cytotoxicity in dopamine-producing cells. Neurotoxicology 2004, 25:543-553.
86. Tatzelt J., Schatzl H.M. Molecular basis of cerebral neurodegeneration in prion diseases. FEBS J 2007, 274:606-611.
87. Thackray A.M., Knight R., Haswell S.J., Bujdoso R., Brown D.R. Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem J 2002, 362:253-258.
88. Treiber C., Pipkorn R., Weise C., Holland G., Multhaup G. Copper is required for prion protein-associated superoxide dismutase-I activity in Pichia pastoris. FEBS J 2007, 274:1304-1311.
89. Viles J.H., Cohen F.E., Prusiner S.B., Goodin D.B., Wright P.E., Dyson H.J. Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc Natl Acad Sci U S A 1999, 96:2042-2047.
90. Viles J.H., Donne D., Kroon G., Prusiner S.B., Cohen F.E., Dyson H.J., et al. Local structural plasticity of the prion protein. Analysis of NMR relaxation dynamics. Biochemistry 2001, 40:2743-2753.
91. Wong B.S., Brown D.R., Pan T., Whiteman M., Liu T., Bu X., et al. Oxidative impairment in scrapie-infected mice is associated with brain metals perturbations and altered antioxidant activities. J Neurochem 2001, 79:689-698.
92. Wong B.S., Chen S.G., Colucci M., Xie Z., Pan T., Liu T., et al. Aberrant metal binding by prion protein in human prion disease. J Neurochem 2001, 78:1400-1408.
93. Worley C.G., Bombick D., Allen J.W., Suber R.L., Aschner M. Effects of manganese on oxidative stress in CATH.a cells. Neurotoxicology 2002, 23:159-164.
94. Wu J., Basha M.R., Zawia N.H. The environment, epigenetics and amyloidogenesis. J Mol Neurosci 2008, 34:1-7.
95. Yin S., Pham N., Yu S., Li C., Wong P., Chang B., et al. Human prion proteins with pathogenic mutations share common conformational changes resulting in enhanced binding to glycosaminoglycans. Proc Natl Acad Sci U S A 2007, 104:7546-7551.
96. Yin Z., Jiang H., Lee E.S., Ni M., Erikson K.M., Milatovic D., et al. Ferroportin is a manganese-responsive protein that decreases manganese cytotoxicity and accumulation. J Neurochem 2010, 112:1190-1198.
97. Yokel R.A. Manganese flux across the blood-brain barrier. Neuromolecular Med 2009, 11:297-310.
98. Yun S.W., Gerlach M., Riederer P., Klein M.A. Oxidative stress in the brain at early preclinical stages of mouse scrapie. Exp Neurol 2006, 201:90-98.
99. Zhu F., Davies P., Thompsett A.R., Kelly S.M., Tranter G.E., Hecht L., et al. Raman optical activity and circular dichroism reveal dramatic differences in the influence of divalent copper and manganese ions on prion protein folding. Biochemistry 2008, 47:2510-2517.