Morphological and functional abnormalities in mitochondria associated with synaptic degeneration in prion disease

American Journal of Pathology

Volumn 177, Issue 3, 2010, Pages 1411-1421

  Sisková, Zuzana ^a   Mahad, Don Joseph ^b   Pudney, Carianne ^a   Campbell, Graham ^b   Cadogan, Mark ^b   Asuni, Ayodeji ^c   O'Connor, Vincent ^a   Perry, Victor Hugh ^c  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; MITOCHONDRIAL MEMBRANE; MOUSE; NERVE DEGENERATION; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE;

EID: 77956556520     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.091037     Document Type: Article

References (57)

1. Taylor RW, Turnbull DM: Mitochondrial DNA mutations in human disease. Nat Rev Genet 2005, 6:389-402
2. DiMauro S, Schon EA: Mitochondrial respiratory-chain diseases. N Engl J Med 2003, 348:2656-2668
3. Perkins GA, Renken CW, Frey TG, Ellisman MH: Membrane architecture of mitochondria in neurons of the central nervous system. J Neurosci Res 2001, 66:857-865
4. Shepherd GM, Harris KM: Three-dimensional structure and composition of CA3->CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J Neurosci 1998, 18:8300-8310
5. Rowland KC, Irby NK, Spirou GA: Specialized synapse-associated structures within the calyx of Held. J Neurosci 2000, 20:9135-9144
6. Stowers RS, Megeath LJ, Gorska-Andrzejak J, Meinertzhagen IA, Schwarz TL: Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 2002, 36:1063-1077
7. Li Z, Okamoto K, Hayashi Y, Sheng M: The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 2004, 119:873-887
8. Trimmer PA, Swerdlow RH, Parks JK, Keeney P, Bennett JP, Jr., Miller SW, Davis RE, Parker WD, Jr.: Abnormal mitochondrial morphology in sporadic Parkinson's and Alzheimer's disease cybrid cell lines. Exp Neurol 2000, 162:37-50
9. Castellani R, Hirai K, Aliev G, Drew KL, Nunomura A, Takeda A, Cash AD, Obrenovich ME, Perry G, Smith MA: Role of mitochondrial dysfunction in Alzheimer's disease. J Neurosci Res 2002, 70:357-360
10. Dawson TM, Dawson VL: Molecular pathways of neurodegeneration in Parkinson's disease. Science 2003, 302:819-822
11. Beal MF: Mitochondria take center stage in aging and neurodegeneration. Ann Neurol 2005, 58:495-505 (Pubitemid 41377212)
12. Mannella CA: Structural diversity of mitochondria: functional implications. Ann NY Acad Sci 2008, 1147:171-179
13. Prusiner SB: The prion diseases. Brain Pathol 1998, 8:499-513
14. Jeffrey M, Halliday WG, Bell J, Johnston AR, MacLeod NK, Ingham C, Sayers AR, Brown DA, Fraser JR: Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathol Appl Neurobiol 2000, 26:41-54 (Pubitemid 30145305)
15. Cunningham C, Deacon R, Wells H, Boche D, Waters S, Diniz CP, Scott H, Rawlins JN, Perry VH: Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur J Neurosci 2003, 17:2147-2155 (Pubitemid 36713975)
16. Fuhrmann M, Mitteregger G, Kretzschmar H, Herms J: Dendritic pathology in prion disease starts at the synaptic spine. J Neurosci 2007, 27:6224-6233 (Pubitemid 46890034)
17. Gray BC, Siskova Z, Perry VH, O'Connor V: Selective presynaptic degeneration in the synaptopathy associated with ME7-induced hippocampal pathology. Neurobiol Dis 2009, 35:63-74
18. Siskova Z, Page A, O'Connor V, Perry VH: Degenerating synaptic boutons in prion disease. Microglia activation without synaptic stripping. Am J Pathol 2009, 175:1610-1621
19. Cunningham C, Deacon RM, Chan K, Boche D, Rawlins JN, Perry VH: Neuropathologically distinct prion strains give rise to similar temporal profiles of behavioral deficits. Neurobiol Dis 2005, 18:258-269 (Pubitemid 40431109)
20. Mahad D, Ziabreva I, Lassmann H, Turnbull D: Mitochondrial defects in acute multiple sclerosis lesions. Brain 2008, 131:1722-1735 (Pubitemid 351957459)
21. Mahad DJ, Ziabreva I, Campbell G, Laulund F, Murphy JL, Reeve AK, Greaves L, Smith KJ, Turnbull DM: Detection of cytochrome c oxidase activity and mitochondrial proteins in single cells. J Neurosci Methods 2009, 184:310-319
22. Asuni AA, Cunningham C, Vigneswaran P, Perry VH, O'Connor V: Unaltered SNARE complex formation in an in vivo model of prion disease. Brain Res 2008, 1233:1-7
23. Bourne JN, Harris KM: Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 2008, 31:47-67
24. Mattson MP, Gleichmann M, Cheng A: Mitochondria in neuroplasticity and neurological disorders. Neuron 2008, 60:748-766
25. Witter RF, Watson ML, Cottone MA: Morphology and ATP-ase of isolated mitochondria. J Biophys Biochem Cytol 1955, 1:127-138
26. Arbustini E, Diegoli M, Fasani R, Grasso M, Morbini P, Banchieri N, Bellini O, Dal Bello B, Pilotto A, Magrini G, Campana C, Fortina P, Gavazzi A, Narula J, Vigano M: Mitochondrial DNA mutations and mitochondrial abnormalities in dilated cardiomyopathy. Am J Pathol 1998, 153:1501-1510 (Pubitemid 28509907)
27. Old SL, Johnson MA: Methods of microphotometric assay of succinate dehydrogenase and cytochrome c oxidase activities for use on human skeletal muscle. Histochem J 1989, 21:545-555
28. Cottrell DA, Borthwick GM, Johnson MA, Ince PG, Turnbull DM: The role of cytochrome c oxidase deficient hippocampal neurones in Alzheimer's disease. Neuropathol Appl Neurobiol 2002, 28:390-396
29. Muller-Hocker J: Cytochrome-c-oxidase deficient cardiomyocytes in the human heart - an age-related phenomenon. A histochemical ultracytochemical study. Am J Pathol 1989, 134:1167-1173
30. Tanaka M, Kovalenko SA, Gong JS, Borgeld HJ, Katsumata K, Hayakawa M, Yoneda M, Ozawa T: Accumulation of deletions and point mutations in mitochondrial genome in degenerative diseases. Ann NY Acad Sci 1996, 786:102-111 (Pubitemid 26273157)
31. Cree LM, Samuels DC, de Sousa Lopes SC, Rajasimha HK, Wonnapinij P, Mann JR, Dahl HH, Chinnery PF: A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat Genet 2008, 40:249-254 (Pubitemid 351171395)
32. Adams I, Jones DG: Quantitative ultrastructural changes in rat cortical synapses during early-, mid- and late-adulthood. Brain Res 1982, 239:349-363 (Pubitemid 12116488)
33. Chiti Z, Knutsen OM, Betmouni S, Greene JR: An integrated, temporal study of the behavioural, electrophysiological and neuropathological consequences of murine prion disease. Neurobiol Dis 2006, 22:363-373
34. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, Wang N, Caspersen C, Chen X, Pollak S, Chaney M, Trinchese F, Liu S, Gunn-Moore F, Lue LF, Walker DG, Kuppusamy P, Zewier ZL, Arancio O, Stern D, Yan SS, Wu H: ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 2004, 304:448-452
35. Zhu D, Lai Y, Shelat PB, Hu C, Sun GY, Lee JC: Phospholipases A2 mediate amyloid-beta peptide-induced mitochondrial dysfunction. J Neurosci 2006, 26:11111-11119 (Pubitemid 44772199)
36. Aiken JM, Williamson JL, Marsh RF: Evidence of mitochondrial involvement in scrapie infection. J Virol 1989, 63:1686-1694
37. Hachiya NS, Yamada M, Watanabe K, Jozuka A, Ohkubo T, Sano K, Takeuchi Y, Kozuka Y, Sakasegawa Y, Kaneko K: Mitochondrial localization of cellular prion protein (PrPC) invokes neuronal apoptosis in aged transgenic mice overexpressing PrPC. Neurosci Lett 2005, 374:98-103 (Pubitemid 40092204)
38. Gray BC, Skipp P, O'Connor VM, Perry VH: Increased expression of glial fibrillary acidic protein fragments and mu-calpain activation within the hippocampus of prion-infected mice. Biochem Soc Trans 2006, 34:51-54 (Pubitemid 43235532)
39. Almer G, Vukosavic S, Romero N, Przedborski S: Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 1999, 72:2415-2425 (Pubitemid 29242192)
40. Stadelmann C, Ludwin S, Tabira T, Guseo A, Lucchinetti CF, Leel-Ossy L, Ordinario AT, Bruck W, Lassmann H: Tissue preconditioning may explain concentric lesions in Balo's type of multiple sclerosis. Brain 2005, 128:979-987 (Pubitemid 40675454)
41. Bolanos JP, Almeida A, Fernandez E, Medina JM, Land JM, Clark JB, Heales SJ: Potential mechanisms for nitric oxide-mediated impairment of brain mitochondrial energy metabolism. Biochem Soc Trans 1997, 25:944-949
42. Cleeter MW, Cooper JM, Darley-Usmar VM, Moncada S, Schapira AH: Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett 1994, 345:50-54
43. Smith KJ, Lassmann H: The role of nitric oxide in multiple sclerosis. Lancet Neurol 2002, 1:232-241
44. Zhang J, Jin B, Li L, Block ER, Patel JM: Nitric oxide-induced persistent inhibition and nitrosylation of active site cysteine residues of mitochondrial cytochrome-c oxidase in lung endothelial cells. Am J Physiol Cell Physiol 2005, 288:C840-C849
45. Walsh DT, Betmouni S, Perry VH: Absence of detectable IL-1beta production in murine prion disease: a model of chronic neurodegeneration. J Neuropathol Exp Neurol 2001, 60:173-182
46. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH: Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 2005, 25:9275-9284
47. Picanco-Diniz CW, Boche D, Gomes-Leal W, Perry VH, Cunningham C: Neuropil and neuronal changes in hippocampal NADPH-diaphorase histochemistry in the ME7 model of murine prion disease. Neuropathol Appl Neurobiol 2004, 30:292-303
48. Sunico CR, Gonzalez-Forero D, Dominguez G, Garcia-Verdugo JM, Moreno-Lopez B: Nitric oxide induces pathological synapse loss by a protein kinase G-. Rho kinase-dependent mechanism preceded by myosin light chain phosphorylation. J Neurosci 2010, 30:973-984
49. Miele G, Jeffrey M, Turnbull D, Manson J, Clinton M: Ablation of cellular prion protein expression affects mitochondrial numbers and morphology. Biochem Biophys Res Commun 2002, 291:372-377
50. Lee DW, Sohn HO, Lim HB, Lee YG, Kim YS, Carp RI, Wisniewski HM: Alteration of free radical metabolism in the brain of mice infected with scrapie agent. Free Radic Res 1999, 30:499-507
51. Caron F, Jacq C, Rouviere-Yaniv J: Characterization of a histone-like protein extracted from yeast mitochondria. Proc Natl Acad Sci USA 1979, 76:4265-4269
52. Patel TB, Clark JB: Synthesis of N-acetyl-L-aspartate by rat brain mitochondria and its involvement in mitochondrial/cytosolic carbon transport. Biochem J 1979, 184:539-546
53. Broom KA, Anthony DC, Lowe JP, Griffin JL, Scott H, Blamire AM, Styles P, Perry VH, Sibson NR: MRI and MRS alterations in the preclinical phase of murine prion disease: association with neuropathological and behavioural changes. Neurobiol Dis 2007, 26:707-717
54. Paterson AW, Curtis JC, Macleod NK: Complex I specific increase in superoxide formation and respiration rate by PrP-null mouse brain mitochondria. J Neurochem 2008, 105:177-191
55. Lobao-Soares B, Bianchin MM, Linhares MN, Carqueja CL, Tasca CI, Souza M, Marques W, Jr., Brentani R, Martins VR, Sakamoto AC, Carlotti CG, Jr., Walz R: Normal brain mitochondrial respiration in adult mice lacking cellular prion protein. Neurosci Lett 2005, 375:203-206
56. Reeve AK, Krishnan KJ, Turnbull D: Mitochondrial DNA mutations in disease, aging, and neurodegeneration. Ann NY Acad Sci 2008, 1147:21-29
57. Davison AN, Dobbing J: Metabolic stability of body constituents. Nature 1961, 191:844-848