Mitochondrial quality, dynamics and functional capacity in Parkinson's disease cybrid cell lines selected for Lewy body expression

Molecular Neurodegeneration

Volumn 8, Issue 1, 2013, Pages

  Cronin Furman, Emily N ^a,b   Borland, M Kathleen ^c   Bergquist, Kristen E ^b   Bennett, James P ^b,d   Trimmer, Patricia A ^b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CYTOCHROME C OXIDASE; DNA BINDING PROTEIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ARTICLE; BLEACHING; BRAIN MITOCHONDRION; CELL STRUCTURE; CYBRID; GENE DOSAGE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; LEWY BODY; MOLECULAR CLONING; NERVE FIBER TRANSPORT; NONHUMAN; OXYGEN CONSUMPTION; PARKINSON DISEASE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FOLDING;

ADULT; AGED; DNA, MITOCHONDRIAL; ENERGY METABOLISM; FEMALE; HUMANS; HYBRID CELLS; LEWY BODIES; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; MITOCHONDRIA; NEURONS; PARKINSON DISEASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84872790484     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-8-6     Document Type: Article

References (79)

1. Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson's disease (preclinical and clinical stages). Braak H, Del TK, Bratzke H, Hamm-Clement J, Sandmann-Keil D, Rub U, J Neurol 2002 249 3 II/1 III/5
2. Dissecting the role of the mitochondrial chaperone mortalin in Parkinson's disease: functional impact of disease-related variants on mitochondrial homeostasis. Burbulla LF, Schelling C, Kato H, Rapaport D, Woitalla D, Schiesling C, Schulte C, Sharma M, Illig T, Bauer P, et al. Hum Mol Genet 2010 19 4437 4452 10.1093/hmg/ddq370 20817635
3. The cybrid model of sporadic Parkinson's disease. Trimmer PA, Bennett JP Jr, Exp Neurol 2009 218 320 325 10.1016/j.expneurol.2009.03.016 19328199
4. Mitochondrial function in Parkinson's disease cybrids containing an nt2 neuron-like nuclear background. Esteves AR, Domingues AF, Ferreira IL, Januario C, Swerdlow RH, Oliveira CR, Cardoso SM, Mitochondrion 2008 8 219 228 10.1016/j.mito.2008.03.004 18495557
5. Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. Exner N, Lutz AK, Haass C, Winklhofer KF, EMBO J 2012 31 3038 3062 10.1038/emboj.2012.170 22735187
6. Mitochondrial respiration and respiration-associated proteins in cell lines created through Parkinson's subject mitochondrial transfer. Esteves AR, Lu J, Rodova M, Onyango I, Lezi E, Dubinsky R, Lyons KE, Pahwa R, Burns JM, Cardoso SM, Swerdlow RH, J Neurochem 2010 113 674 682 10.1111/j.1471-4159.2010. 06631.x 20132468
7. Cybrid models of Parkinson's disease show variable mitochondrial biogenesis and genotype-respiration relationships. Keeney PM, Dunham LD, Quigley CK, Morton SL, Bergquist KE, Bennett JP Jr, Exp Neurol 2009 220 374 382 10.1016/j.expneurol.2009.09.025 19815014
8. Parkinson's disease transgenic mitochondrial cybrids generate Lewy inclusion bodies. Trimmer PA, Borland MK, Keeney PM, Bennett JP Jr, Parker WD Jr, J Neurochem 2004 88 800 812 10.1046/j.1471-4159.2003.02168.x 14756800 (Pubitemid 38199300)
9. Proteomic identification of novel proteins in cortical lewy bodies. Leverenz JB, Umar I, Wang Q, Montine TJ, McMillan PJ, Tsuang DW, Jin J, Pan C, Shin J, Zhu D, Zhang J, Brain Pathol 2007 17 139 145 10.1111/j.1750-3639.2007. 00048.x 17388944 (Pubitemid 46466133)
10. Proteomic identification of novel proteins associated with Lewy bodies. Xia Q, Liao L, Cheng D, Duong DM, Gearing M, Lah JJ, Levey AI, Peng J, Front Biosci 2008 13 3850 3856 18508479 (Pubitemid 351594664)
11. The Lewy body in Parkinson's disease: molecules implicated in the formation and degradation of alpha-synuclein aggregates. Wakabayashi K, Tanji K, Mori F, Takahashi H, Neuropathology 2007 27 494 506 10.1111/j.1440-1789.2007. 00803.x 18018486 (Pubitemid 47459715)
12. Pathobiology of the Lewy body. Galvin JE, Lee VM, Schmidt ML, Tu PH, Iwatsubo T, Trojanowski JQ, Adv Neurol 1999 80 313 324 10410736
13. Lewy bodies. Shults CW, Proc Natl Acad Sci USA 2006 103 1661 1668 10.1073/pnas.0509567103 16449387 (Pubitemid 43228751)
14. Gene expression profiling of Lewy body-bearing neurons in Parkinson's disease. Lu L, Neff F, Alvarez-Fischer D, Henze C, Xie Y, Oertel WH, Schlegel J, Hartmann A, Exp Neurol 2005 195 27 39 10.1016/j.expneurol.2005.04.011 15944136 (Pubitemid 41116811)
15. Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Conway KA, Harper JD, Lansbury PT Jr, Biochemistry 2000 39 2552 2563 10.1021/bi991447r 10704204 (Pubitemid 30148907)
16. Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Sanchez I, Mahlke C, Yuan J, Nature 2003 421 373 379 10.1038/nature01301 12540902 (Pubitemid 36157935)
17. Endogenous amyloidogenesis in long-term rat hippocampal cell cultures. Bertrand SJ, Aksenova MV, Aksenov MY, Mactutus CF, Booze RM, BMC Neurosci 2011 12 38 10.1186/1471-2202-12-38 21569253
18. Parkinson's disease and parkinsonism: neuropathology. Dickson DW, Cold Spring Harb Perspect Med 2012 2 009258 22908195
19. Lewy-body formation is an aggresome-related process: a hypothesis. Olanow CW, Perl DP, DeMartino GN, McNaught KS, Lancet Neurol 2004 3 496 503 10.1016/S1474-4422(04)00827-0 15261611 (Pubitemid 38903101)
20. Parkinson's disease. Lees AJ, Hardy J, Revesz T, Lancet 2009 373 2055 2066 10.1016/S0140-6736(09)60492-X 19524782
21. A stable proportion of Lewy body bearing neurons in the substantia nigra suggests a model in which the Lewy body causes neuronal death. Greffard S, Verny M, Bonnet AM, Seilhean D, Hauw JJ, Duyckaerts C, Neurobiol Aging 2010 31 99 103 10.1016/j.neurobiolaging.2008.03.015 18457903
22. Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. Rujano MA, Bosveld F, Salomons FA, Dijk F, van Waarde MA, van der Want JJ, de Vos RA, Brunt ER, Sibon OC, Kampinga HH, PLoS Biol 2006 4 417 10.1371/journal.pbio.0040417 17147470 (Pubitemid 44917621)
23. Asymmetric mitosis: Unequal segregation of proteins destined for degradation. Fuentealba LC, Eivers E, Geissert D, Taelman V, De Robertis EM, Proc Natl Acad Sci USA 2008 105 7732 7737 10.1073/pnas.0803027105 18511557 (Pubitemid 351872707)
24. Staging/typing of Lewy body related alpha-synuclein pathology: a study of the BrainNet Europe Consortium. Alafuzoff I, Ince PG, Arzberger T, Al-Sarraj S, Bell J, Bodi I, Bogdanovic N, Bugiani O, Ferrer I, Gelpi E, et al. Acta Neuropathol 2009 117 635 652 10.1007/s00401-009-0523-2 19330340
25. Extrusion of misfolded and aggregated proteins-a protective strategy of aging neurons? Doehner J, Genoud C, Imhof C, Krstic D, Knuesel I, Eur J Neurosci 2012 35 1938 1950 10.1111/j.1460-9568.2012.08154.x 22708604
26. Mitochondrial shape changes: orchestrating cell pathophysiology. Campello S, Scorrano L, EMBO Rep 2010 11 678 684 10.1038/embor.2010.115 20725092
27. Abnormal mitochondrial morphology in sporadic Parkinson's and Alzheimer's disease cybrid cell lines. Trimmer PA, Swerdlow RH, Parks JK, Keeney P, Bennett JP Jr, Miller SW, Davis RE, Parker WD Jr, Exp Neurol 2000 162 37 50 10.1006/exnr.2000.7333 10716887 (Pubitemid 30170099)
28. Mitochondrial fragmentation in neurodegeneration. Knott AB, Perkins G, Schwarzenbacher R, Bossy-Wetzel E, Nat Rev Neurosci 2008 9 505 518 18568013 (Pubitemid 351873464)
29. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Gomes LC, Di Benedetto G, Scorrano L, Nat Cell Biol 2011 13 589 598 10.1038/ncb2220 21478857
30. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Twig G, Hyde B, Shirihai OS, Biochim Biophys Acta 2008 1777 1092 1097 10.1016/j.bbabio.2008.05.001 18519024
31. The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery. Palmer CS, Osellame LD, Stojanovski D, Ryan MT, Cell Signal 2011 23 1534 1545 10.1016/j.cellsig.2011.05.021 21683788
32. Cristae formation-linking ultrastructure and function of mitochondria. Zick M, Rabl R, Reichert AS, Biochim Biophys Acta 2009 1793 5 19 10.1016/j.bbamcr.2008.06.013 18620004
33. Alberts B, Molecular biology of the cell New York: Garland Pub 1983
34. Loss of mitochondrial membrane potential is associated with increase in mitochondrial volume: physiological role in neurones. Safiulina D, Veksler V, Zharkovsky A, Kaasik A, J Cell Physiol 2006 206 347 353 10.1002/jcp.20476 16110491 (Pubitemid 43062802)
35. Advances in measuring cellular bioenergetics using extracellular flux. Ferrick DA, Neilson A, Beeson C, Drug Discov Today 2008 13 268 274 10.1016/j.drudis.2007.12.008 18342804
36. Assessing bioenergetic function in response to oxidative stress by metabolic profiling. Dranka BP, Benavides GA, Diers AR, Giordano S, Zelickson BR, Reily C, Zou L, Chatham JC, Hill BG, Zhang J, et al. Free Radic Biol Med 2011 51 1621 1635 10.1016/j.freeradbiomed.2011.08.005 21872656
37. Assessing mitochondrial dysfunction in cells. Brand MD, Nicholls DG, Biochem J 2011 435 297 312 10.1042/BJ20110162 21726199
38. Alterations in bioenergetic function induced by Parkinson's disease mimetic compounds: lack of correlation with superoxide generation. Dranka BP, Zielonka J, Kanthasamy AG, Kalyanaraman B, J Neurochem 2012 122 941 951 10.1111/j.1471-4159.2012.07836.x 22708893
39. Alterations in axonal transport motor proteins in sporadic and experimental Parkinson's disease. Chu Y, Morfini GA, Langhamer LB, He Y, Brady ST, Kordower JH, Brain 2012 135 2058 2073 10.1093/brain/aws133 22719003
40. Organelles in developing neurons: essential regulators of neuronal morphogenesis and function. Sekine S, Miura M, Chihara T, Int J Dev Biol 2009 53 19 27 10.1387/ijdb.082618ss 19123123
41. Regulation of axonal mitochondrial transport and its impact on synaptic transmission. Cai Q, Davis ML, Sheng ZH, Neurosci Res 2011 70 9 15 10.1016/j.neures.2011.02.005 21352858
42. Three-layered structure shared between Lewy bodies and lewy neurites-three-dimensional reconstruction of triple-labeled sections. Kanazawa T, Uchihara T, Takahashi A, Nakamura A, Orimo S, Mizusawa H, Brain Pathol 2008 18 415 422 10.1111/j.1750-3639.2008.00140.x 18394008 (Pubitemid 351782850)
43. The axonal transport of mitochondria. Saxton WM, Hollenbeck PJ, J Cell Sci 2012 125 2095 2104 10.1242/jcs.053850 22619228
44. Reduced axonal transport in Parkinson's disease cybrid neurites is restored by light therapy. Trimmer PA, Schwartz KM, Borland MK, De Taboada L, Streeter J, Oron U, Mol Neurodegener 2009 4 26 10.1186/1750-1326-4-26 19534794
45. Chronic, low-dose rotenone reproduces Lewy neurites found in early stages of Parkinson's disease, reduces mitochondrial movement and slowly kills differentiated SH-SY5Y neural cells. Borland MK, Trimmer PA, Rubinstein JD, Keeney PM, Mohanakumar K, Liu L, Bennett JP Jr, Mol Neurodegener 2008 3 21 10.1186/1750-1326-3-21 19114014
46. Detection of mitochondrial DNA depletion in living human cells using PicoGreen staining. Ashley N, Harris D, Poulton J, Exp Cell Res 2005 303 432 446 10.1016/j.yexcr.2004.10.013 15652355 (Pubitemid 40126275)
47. The layered structure of human mitochondrial DNA nucleoids. Bogenhagen DF, Rousseau D, Burke S, J Biol Chem 2008 283 3665 3675 18063578
48. Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. He J, Cooper HM, Reyes A, Di Re M, Sembongi H, Litwin TR, Gao J, Neuman KC, Fearnley IM, Spinazzola A, et al. Nucleic Acids Res 2012 40 6109 6121 10.1093/nar/gks266 22453275
49. Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. Keeney PM, Xie J, Capaldi RA, Bennett JP Jr, J Neurosci 2006 26 5256 5264 10.1523/JNEUROSCI.0984- 06.2006 16687518 (Pubitemid 44315308)
50. Relationships among molecular genetic and respiratory properties of Parkinson's disease cybrid cells show similarities to Parkinson's brain tissues. Borland MK, Mohanakumar KP, Rubinstein JD, Keeney PM, Xie J, Capaldi R, Dunham LD, Trimmer PA, Bennett JP Jr, Biochim Biophys Acta 2008 1792 68 74 18973805
51. Mitochondrial respiratory chain dysfunction: Implications in neurodegeneration. Moran M, Moreno-Lastres D, Marin-Buera L, Arenas J, Martin MA, Ugalde C, Free Radic Biol Med 2012 53 595 609 10.1016/j.freeradbiomed.2012. 05.009 22595027
52. Distribution and dynamics of mitochondrial nucleoids in animal cells in culture. Bereiter-Hahn JaB M, Exp Biol Online 1997 1 1 17
53. PGC-1{alpha} and PGC-1{beta} regulate mitochondrial density in neurons. Wareski P, Vaarmann A, Choubey V, Safiulina D, Liiv J, Kuum M, Kaasik A, J Biol Chem 2009 284 21379 21385 10.1074/jbc.M109.018911 19542216
54. PGC-1alpha, a potential therapeutic target for early intervention in Parkinson's disease. Zheng B, Liao Z, Locascio JJ, Lesniak KA, Roderick SS, Watt ML, Eklund AC, Zhang-James Y, Kim PD, Hauser MA, et al. Sci Transl Med 2010 2 52 73
55. Transcriptional control of mitochondrial biogenesis and function. Hock MB, Kralli A, Annu Rev Physiol 2009 71 177 203 10.1146/annurev.physiol.010908. 163119 19575678
56. Transgenic expression and activation of PGC-1alpha protect dopaminergic neurons in the MPTP mouse model of Parkinson's disease. Mudo G, Makela J, Di Liberto V, Tselykh TV, Olivieri M, Piepponen P, Eriksson O, Malkia A, Bonomo A, Kairisalo M, et al. Cell Mol Life Sci: CMLS 2012 69 1153 1165 10.1007/s00018-011-0850-z 21984601
57. PGC-1alpha/beta induced expression partially compensates for respiratory chain defects in cells from patients with mitochondrial disorders. Srivastava S, Diaz F, Iommarini L, Aure K, Lombes A, Moraes CT, Hum Mol Genet 2009 18 1805 1812 10.1093/hmg/ddp093 19297390
58. Activation of peroxisome proliferator-activated receptor pathway stimulates the mitochondrial respiratory chain and can correct deficiencies in patients' cells lacking its components. Bastin J, Aubey F, Rotig A, Munnich A, Djouadi F, J Clin Endocrinol Metab 2008 93 1433 1441 10.1210/jc.2007-1701 18211970 (Pubitemid 351519745)
59. Activation of the PPAR/PGC-1alpha pathway prevents a bioenergetic deficit and effectively improves a mitochondrial myopathy phenotype. Wenz T, Diaz F, Spiegelman BM, Moraes CT, Cell Metab 2008 8 249 256 10.1016/j.cmet.2008.07.006 18762025
60. Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Scarpulla RC, Ann N Y Acad Sci 2008 1147 321 334 10.1196/annals.1427.006 19076454
61. The transcription machinery in mammalian mitochondria. Gaspari M, Larsson NG, Gustafsson CM, Biochim Biophys Acta 2004 1659 148 152 10.1016/j.bbabio. 2004.10.003 15576046 (Pubitemid 39575501)
62. Mitochondrial biogenesis and turnover. Diaz F, Moraes CT, Cell Calcium 2008 44 24 35 10.1016/j.ceca.2007.12.004 18395251
63. Mitochondria and PGC-1alpha in Aging and Age-Associated Diseases. Wenz T, J Aging Res 2011 2011 810619 21629705
64. Formation and development of Lewy pathology: a critical update. Jellinger KA, J Neurol 2009 256 Suppl 3 270 279 19711116
65. Visual hallucinations in Lewy body disease relate to Lewy bodies in the temporal lobe. Harding AJ, Broe GA, Halliday GM, Brain 2002 125 391 403 10.1093/brain/awf033 11844739 (Pubitemid 34127441)
66. Clinical correlates of selective pathology in the amygdala of patients with Parkinson's disease. Harding AJ, Stimson E, Henderson JM, Halliday GM, Brain 2002 125 2431 2445 10.1093/brain/awf251 12390970 (Pubitemid 35303503)
67. Lewy bodies in Parkinson's disease: protectors or perpetrators? Harrower TP, Michell AW, Barker RA, Exp Neurol 2005 195 1 6 10.1016/j.expneurol.2005.06. 002 16023637 (Pubitemid 41116808)
68. Cell therapies for neurological disease-from bench to clinic to bench. Harrower T, Barker RA, Expert Opin Biol Ther 2005 5 289 291 10.1517/14712598.5. 3.289 15833067 (Pubitemid 40516740)
69. The role of the Lewy body in idiopathic Parkinsonism. de la Fuente-Fernandez R, Schulzer M, Mak E, Kishore A, Calne DB, Parkinsonism Relat Disord 1998 4 73 77 10.1016/S1353-8020(98)00016-9 18591092 (Pubitemid 28525353)
70. Ageing, neurodegeneration and Parkinson's disease. Hindle JV, Age Ageing 2010 39 156 161 10.1093/ageing/afp223 20051606
71. A reassessment of the Lewy body. Au WL, Calne DB, Acta Neurol Taiwan 2005 14 40 47 16008161 (Pubitemid 40922479)
72. Presynaptic alpha-synuclein aggregates, not Lewy bodies, cause neurodegeneration in dementia with Lewy bodies. Kramer ML, Schulz-Schaeffer WJ, J Neurosci: Offic J Soc Neurosci 2007 27 1405 1410 10.1523/JNEUROSCI.4564-06. 2007
73. Changes in the solubility and phosphorylation of alpha-synuclein over the course of Parkinson's disease. Zhou J, Broe M, Huang Y, Anderson JP, Gai WP, Milward EA, Porritt M, Howells D, Hughes AJ, Wang X, Halliday GM, Acta Neuropathol 2011 121 695 704 10.1007/s00401-011-0815-1 21400129
74. Inhibition of mitochondria- and endoplasmic reticulum stress-mediated autophagy augments temozolomide-induced apoptosis in glioma cells. Lin CJ, Lee CC, Shih YL, Lin CH, Wang SH, Chen TH, Shih CM, PLoS One 2012 7 38706 10.1371/journal.pone.0038706 22745676
75. Parkinson's disease and alpha-synuclein expression. Devine MJ, Gwinn K, Singleton A, Hardy J, Mov Disord 2011 26 2160 2168 10.1002/mds.23948 21887711
76. Neuropathology and neurochemistry of nonmotor symptoms in Parkinson's disease. Ferrer I, Parkinsons Dis 2011 2011 708404 21403906
77. Selective binding of nuclear alpha-synuclein to the PGC1alpha promoter under conditions of oxidative stress may contribute to losses in mitochondrial function: Implications for Parkinson's disease. Siddiqui A, Chinta SJ, Mallajosyula JK, Rajagopolan S, Hanson I, Rane A, Melov S, Andersen JK, Free Radic Biol Med 2012 53 993 1003 10.1016/j.freeradbiomed.2012.05.024 22705949
78. Origin and functional consequences of the complex I defect in Parkinson's disease. Swerdlow RH, Parks JK, Miller SW, Tuttle JB, Trimmer PA, Sheehan JP, Bennett JP Jr, Davis RE, Parker WD Jr, Ann Neurol 1996 40 663 671 10.1002/ana.410400417 8871587 (Pubitemid 26357892)
79. Creation and characterization of mitochondrial DNA-depleted cell lines with «neuronal-like» properties. Miller SW, Trimmer PA, Parker WD Jr, Davis RE, J Neurochem 1996 67 1897 1907 8863494 (Pubitemid 26349662)