Mitochondrial dysfunction in a neural cell model of spinal muscular atrophy

Journal of Neuroscience Research

Volumn 87, Issue 12, 2009, Pages 2748-2756

  Acsadi, Gyula ^a,b   Lee, Icksoo ^b   Li, Xingli ^a   Khaidakov, Magomed ^b   Pecinova, Alena ^b   Parker, Graham C ^a   Hüttemann, Maik ^b  

^a CHILDREN'S HOSPITAL OF MICHIGAN   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cytochrome c oxidase; Free radicals; Mitochondria; Motor neuron disease

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; FREE RADICAL; SMALL INTERFERING RNA; SURVIVAL MOTOR NEURON PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CELL ENERGY; CELL STRAIN NSC 34; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; GENETIC TRANSFECTION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL MUSCULAR ATROPHY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELLS, CULTURED; DOWN-REGULATION; ELECTRON TRANSPORT COMPLEX IV; ENERGY METABOLISM; FREE RADICALS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MOTOR NEURONS; MUSCULAR ATROPHY, SPINAL; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; RNA, SMALL INTERFERING; SPINAL CORD; SURVIVAL OF MOTOR NEURON 1 PROTEIN;

EID: 67651140516     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22106     Document Type: Article

References (55)

1. Acin-Perez R, Bayona-Bafaluy MP, Bueno M, Machicado C, Fernandez- Silva P, Perez-Martos A, Montoya J, Lopez-Perez MJ, Sancho J, Enriquez JA. 2003. An intragenic suppressor in the cytochrome c oxidase I gene of mouse mitochondrial DNA. Hum Mol Genet 12:329-339. (Pubitemid 36204429)
2. Arnold S, Kadenbach B. 1999. The intramitochondrial ATP/ADP-ratio controls cytochrome c oxidase activity allosterically. FEBS Lett 443:105-108. (Pubitemid 29078611)
3. Berger A, Mayr JA, Meierhofer D, Fotschl U, Bittner R, Budka H, Grethen C, Huemer M, Kofler B, Sperl W. 2003. Severe depletion of mitochondrial DNA in spinal muscular atrophy. Acta Neuropathol 105:245-251. (Pubitemid 36798816)
4. Brand MD, Brindle KM, Buckingham JA, Harper JA, Rolfe DF, Stuart JA. 1999. The significance and mechanism of mitochondrial proton conductance. Int J Obes Rel Metab Disord 23(Suppl 6):S4-S11.
5. Brzustowicz LM, Lehner T, Castilla LH, Penchaszadeh GK, Wilhelmsen KC, Daniels R, Davies KE, Leppert M, Ziter F, Wood D, et al. 1990. Genetic mapping of chronic childhood-onset spinal muscular atrophy to chromosome 5q11.2-13.3. Nature 344:540-541. (Pubitemid 20124429)
6. Cashman NR, Durham HD, Blusztajn JK, Oda K, Tabira T, Shaw IT, Dahrouge S, Antel JP. 1992. Neuroblastoma 3 spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev Dyn 194:209-221.
7. Dutta R, McDonough J, Yin X, Peterson J, Chang A, Torres T, Gudz T, Macklin WB, Lewis DA, Fox RJ, Rudick R, Mirnics K, Trapp BD. 2006. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 59:478-489. (Pubitemid 43358068)
8. Duvigneau JC, Piskernik C, Haindl S, Kloesch B, Hartl RT, Hüttemann M, Lee I, Ebel T, Moldzio R, Gemeiner M, Redl H, Kozlov AV. 2008. A novel endotoxin-induced pathway: upregulation of heme oxygenase 1, accumulation of free iron, and free iron-mediated mitochondrial dysfunction. Lab Invest 88:70-77.
9. Eggert C, Chari A, Laggerbauer B, Fischer U. 2006. Spinal muscular atrophy: the RNP connection. Trends Mol Med 12:113-121.
10. Fan L, Simard LR. 2002. Survival motor neuron (SMN) protein: role in neurite outgrowth and neuromuscular maturation during neuronal differentiation and development. Hum Mol Genet 11:1605-1614. (Pubitemid 34812256)
11. Fischer U, Liu Q, Dreyfuss G. 1997. The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis. Cell 90:1023-1029. (Pubitemid 27408516)
12. Francis JW, Sandrock AW, Bhide PG, Vonsattel JP, Brown RH Jr. 1998. Heterogeneity of subcellular localization and electrophoretic mobility of survival motor neuron (SMN) protein in mammalian neural cells and tissues. Proc Natl Acad Sci U S A 95:6492-6497.
13. Green DR, Reed JC. 1998. Mitochondria and apoptosis. Science 281:1309-1312.
14. Gubitz AK, Feng W, Dreyfuss G. 2004. The SMN complex. Exp Cell Res 296:51-56.
15. Hüttemann M, Lee I, Samavati L, Yu H, Doan JW. 2007. Regulation of mitochondrial oxidative phosphorylation through cell signaling. Biochim Biophys Acta 1773:1701-1720. (Pubitemid 350191980)
16. Jablonka S, Schrank B, Kralewski M, Rossoll W, Sendtner M. 2000. Reduced survival motor neuron (Smn) gene dose in mice leads to motor neuron degeneration: an animal model for spinal muscular atrophy type III. Hum Mol Genet 9:341-346. (Pubitemid 30098726)
17. Jablonka S, Bandilla M, Wiese S, Buhler D, Wirth B, Sendtner M, Fischer U. 2001. Co-regulation of survival of motor neuron (SMN) protein and its interactor SIP1 during development and in spinal muscular atrophy. Hum Mol Genet 10:497-505. (Pubitemid 32181672)
18. Jongpiputvanich S, Sueblinvong T, Norapucsunton T. 2005. Mitochondrial respiratory chain dysfunction in various neuromuscular diseases. J Clin Neurosci 12:426-428. (Pubitemid 40745228)
19. Kadenbach B, Arnold S, Lee I, Huttemann M. 2004. The possible role of cytochrome c oxidase in stress-induced apoptosis and degenerative diseases. Biochim Biophys Acta 1655:400-408. (Pubitemid 38526204)
20. Kaim G, Dimroth P. 1999. ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J 18:4118-4127. (Pubitemid 29364115)
21. Karthikeyan G, Santos JH, Graziewicz MA, Copeland WC, Isaya G, Van Houten B, Resnick MA. 2003. Reduction in frataxin causes progressive accumulation of mitochondrial damage. Hum Mol Genet 12:3331-3342. (Pubitemid 37541078)
22. Korshunov SS, Skulachev VP, Starkov AA. 1997. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15-18.
23. La Bella V, Kallenbach S, Pettmann B. 2000. Expression and subcellular localization of two isoforms of the survival motor neuron protein in different cell types. J Neurosci Res 62:346-356. (Pubitemid 30822716)
24. Le TT, Coovert DD, Monani UR, Morris GE, Burghes AH. 2000. The survival motor neuron (SMN) protein: effect of exon loss and mutation on protein localization. Neurogenetics 3:7-16.
25. Lee I, Salomon AR, Ficarro S, Mathes I, Lottspeich F, Grossman LI, Hüttemann M. 2005. cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J Biol Chem 280:6094-6100. (Pubitemid 40280094)
26. Lefebvre S, Burglen L, Reboullet S, Clermont O, Burlet P, Viollet L, Benichou B, Cruaud C, Millasseau P, Zeviani M, et al. 1995. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80:155-165.
27. Lefebvre S, Burlet P, Liu Q, Bertrandy S, Clermont O, Munnich A, Dreyfuss G, Melki J. 1997. Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet 16:265-269. (Pubitemid 27280210)
28. Liu SS. 1999. Cooperation of a "reactive oxygen cycle" with the Q cycle and the proton cycle in the respiratory chain - superoxide generating and cycling mechanisms in mitochondria. J Bioenerg Biomembr 31:367-376.
29. Mancuso M, Salviati L, Sacconi S, Otaegui D, Camano P, Marina A, Bacman S, Moraes CT, Carlo JR, Garcia M, Garcia-Alvarez M, Monzon L, Naini AB, Hirano M, Bonilla E, Taratuto AL, DiMauro S, Vu TH. 2002. Mitochondrial DNA depletion: mutations in thymidine kinase gene with myopathy and SMA. Neurology 59:1197-1202. (Pubitemid 35192389)
30. Manfredi G, Beal MF. 2000. The role of mitochondria in the pathogenesis of neurodegenerative diseases. Brain Pathol 10:462-472. (Pubitemid 30431299)
31. Mattiazzi M, D'Aurelio M, Gajewski CD, Martushova K, Kiaei M, Beal MF, Manfredi G. 2002. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J Biol Chem 277:29626-29633. (Pubitemid 41079252)
32. Mattson MP. 2000. Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 1:120-129.
33. Monani UR, Sendtner M, Coovert DD, Parsons DW, Andreassi C, Le TT, Jablonka S, Schrank B, Rossoll W, Prior TW, Morris GE, Burghes AH. 2000. The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy. Hum Mol Genet 9:333-339. (Pubitemid 30098725)
34. Murayama S, Bouldin TW, Suzuki K. 1991. Immunocytochemical and ultrastructural studies of Werdnig-Hoffmann disease. Acta Neuropathol 81:408-417.
35. Napiwotzki J, Shinzawa-Itoh K, Yoshikawa S, Kadenbach B. 1997. ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol Chem 378:1013-1021. (Pubitemid 27438023)
36. Nguyen thi Man, Humphrey E, Lam LT, Fuller HR, Lynch TA, Sewry CA, Goodwin PR, Mackenzie AE, Morris GE. 2008. A two-site ELISA can quantify upregulation of SMN protein by drugs for spinal muscular atrophy. Neurology 71:1752-1753.
37. Oprea GE, Krober S, McWhorter ML, Rossoll W, Muller S, Krawczak M, Bassell GJ, Beattie CE, Wirth B. 2008. Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science 320:524-527. (Pubitemid 351590664)
38. Parker GC, Li X, Anguelov RA, Toth G, Cristescu A, Acsadi G. 2008. Survival motor neuron protein regulates apoptosis in an in vitro model of spinal muscular atrophy. Neurotox Res 13:39-48.
39. Prior TW. 2007. Spinal muscular atrophy diagnostics. J Child Neurol 22:952-956.
40. Ranganathan S, Harmison GG, Meyertholen K, Pennuto M, Burnett BG, Fischbeck KH. 2009. Mitochondrial abnormalities in spinal and bulbar muscular atrophy. Hum Mol Genet 18:27-42.
41. Rossignol R, Faustin B, Rocher C, Malgat M, Mazat JP, Letellier T. 2003. Mitochondrial threshold effects. Biochem J 370:751-762.
42. Rossoll W, Jablonka S, Andreassi C, Kroning AK, Karle K, Monani UR, Sendtner M. 2003a. Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J Cell Biol 163:801-812. (Pubitemid 37517887)
43. Rossoll W, Jablonka S, Andreassi C, Kroning AK, Karle K, Monani UR, Sendtner M. 2003b. Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J Cell Biol 163:801-812. (Pubitemid 37517887)
44. Samavati L, Lee I, Mathes I, Lottspeich F, Hüttemann M. 2008. Tumor necrosis factor alpha inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit I of cytochrome c oxidase. J Biol Chem 283:21134-21144.
45. Schapira AH. 1999. Mitochondrial DNA in Parkinson's disease. Adv Neurol 80:233-237.
46. Schrank B, Gotz R, Gunnersen JM, Ure JM, Toyka KV, Smith AG, Sendtner M. 1997. Inactivation of the survival motor neuron gene, a candidate gene for human spinal muscular atrophy, leads to massive cell death in early mouse embryos. Proc Natl Acad Sci U S A 94:9920-9925. (Pubitemid 27408166)
47. She P, Reid TM, Bronson SK, Vary TC, Hajnal A, Lynch CJ, Hutson SM. 2007. Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metab 6:181-194. (Pubitemid 47324140)
48. Sperl W, Skladal D, Gnaiger E, Wyss M, Mayr U, Hager J, Gellerich FN. 1997. High resolution respirometry of permeabilized skeletal muscle fibers in the diagnosis of neuromuscular disorders. Mol Cell Biochem 174:71-78. (Pubitemid 27404171)
49. Talbot K, Davies KE. 2001. Spinal muscular atrophy. Semin Neurol 21:189-197.
50. Trulzsch B, Davies K, Wood M. 2004. Survival of motor neuron gene downregulation by RNAi: towards a cell culture model of spinal muscular atrophy. Brain Res Mol Brain Res 120:145-150. (Pubitemid 38115811)
51. Villani G, Greco M, Papa S, Attardi G. 1998. Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J Biol Chem 273:31829-31836. (Pubitemid 29177118)
52. Wan B, Doumen C, Duszynski J, Salama G, Vary TC, LaNoue KF. 1993. Effects of cardiac work on electrical potential gradient across mitochondrial membrane in perfused rat hearts. Am J Physiol 265:H453-H460. (Pubitemid 23273578)
53. Xu H, Somers ZB, Robinson ML 2nd, Hebert MD. 2005. Tim50a, a nuclear isoform of the mitochondrial Tim50, interacts with proteins involved in snRNP biogenesis. BMC Cell Biol 6:29.
54. Zhang H, Huang HM, Carson RC, Mahmood J, Thomas HM, Gibson GE. 2001. Assessment of membrane potentials of mitochondrial populations in living cells. Anal Biochem 298:170-180. (Pubitemid 33105231)
55. Zhang Z, Lotti F, Dittmar K, Younis I, Wan L, Kasim M, Dreyfuss G. 2008. SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 133:585-600. (Pubitemid 351636302)