Defective mitochondrial dynamics is an early event in skeletal muscle of an Amyotrophic lateral sclerosis mouse model

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Luo, Guo ^a,b   Yi, Jianxun ^a   Ma, Changling ^a   Xiao, Yajuan ^a   Yi, Frank ^a   Yu, Tian ^b   Zhou, Jingsong ^a  

^a RUSH MEDICAL COLLEGE   (United States)

^b ZUNYI MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE;

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DISEASE COURSE; ENZYME LOCALIZATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MUSCLE MITOCHONDRION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SKELETAL MUSCLE; SOD1 GENE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CYTOSOL; DISEASE MODELS, ANIMAL; DYNAMINS; GREEN FLUORESCENT PROTEINS; LIGHT; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, TRANSGENIC; MITOCHONDRIAL DYNAMICS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MUTANT PROTEINS; MUTATION; PROTEIN TRANSPORT; SUPEROXIDE DISMUTASE;

EID: 84891909212     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082112     Document Type: Article

References (42)

1. Pasinelli P, Brown RH (2006) Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 7:710-723. doi: 10.1038/nrn1971. PubMed: 16924260. (Pubitemid 44267495)
2. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY et al. (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264:1772-1775. doi:10.1126/science.8209258. PubMed: 8209258. (Pubitemid 24227760)
3. Boillée S, Vande Velde C, Cleveland DW (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52:39-59. doi:10.1016/j.neuron. 2006.09.018. PubMed: 17015226. (Pubitemid 44466358)
4. Dobrowolny G, Giacinti C, Pelosi L, Nicoletti C, Winn N et al. (2005) Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. J Cell Biol 168:193-199. doi:10.1083/jcb. 200407021. PubMed: 15657392. (Pubitemid 40248217)
5. Nguyen QT, Son YJ, Sanes JR, Lichtman JW (2000) Nerve terminals form but fail to mature when postsynaptic differentiation is blocked: in vivo analysis using mammalian nerve-muscle chimeras. J Neurosci Off J Soc Neurosci 20:6077-6086. PubMed: 10934257. (Pubitemid 30658401)
6. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M et al. (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185:232-240. doi:10.1016/j.expneurol. 2003.10.004. PubMed: 14736504. (Pubitemid 38084849)
7. Frey D, Schneider C, Xu L, Borg J, Spooren W et al. (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci Off J Soc Neurosci 20:2534-2542. PubMed: 10729333. (Pubitemid 30220340)
8. Gonzalez de Aguilar J-L, Niederhauser-Wiederkehr C, Halter B, De Tapia M, Di Scala F et al. (2008) Gene profiling of skeletal muscle in an amyotrophic lateral sclerosis mouse model. Physiol Genomics 32:207-218. doi:10.1152/ physiolgenomics.00017.2007. PubMed: 18000159. (Pubitemid 351186328)
9. Dobrowolny G, Aucello M, Rizzuto E, Beccafico S, Mammucari C et al. (2008) Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metab 8:425-436. doi:10.1016/j.cmet.2008.09.002. PubMed: 19046573.
10. Wong M, Martin LJ (2010) Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Hum Mol Genet 19:2284-2302. doi:10.1093/hmg/ddq106. PubMed: 20223753.
11. Miller TM, Kim SH, Yamanaka K, Hester M, Umapathi P et al. (2006) Gene transfer demonstrates that muscle is not a primary target for noncellautonomous toxicity in familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 103:19546-19551. doi:10.1073/pnas. 0609411103. PubMed: 17164329. (Pubitemid 46026068)
12. Eisenberg BR (1983) Quantitative ultrastructure of mammailian skeletal muscle. Bethesda, MD: American Physiological Society. 95 p.
13. Appel SH (2006) Is ALS a systemic disorder? Evidence from muscle mitochondria. Exp Neurol 198:1-3. doi:10.1016/j.expneurol. 2005.12.025. PubMed: 16458887. (Pubitemid 43243738)
14. Krasnianski A, Deschauer M, Neudecker S, Gellerich FN, Müller T et al. (2005) Mitochondrial changes in skeletal muscle in amyotrophic lateral sclerosis and other neurogenic atrophies. Brain 128:1870-1876. doi: 10.1093/brain/awh540. PubMed: 15901649. (Pubitemid 41373659)
15. Dupuis L, di Scala F, Rene F, de Tapia M, Oudart H et al. (2003) Upregulation of mitochondrial uncoupling protein 3 reveals an early muscular metabolic defect in amyotrophic lateral sclerosis. FASEB J 17:2091-2093. doi:10.1096/fj.02-1182fje. PubMed: 14500553.
16. Leclerc N, Ribera F, Zoll J, Warter JM, Poindron P et al. (2001) Selective changes in mitochondria respiratory properties in oxidative or glycolytic muscle fibers isolated from G93AhumanSOD1 transgenic mice. Neuromuscul Disord NMD 11:722-727. doi:10.1016/S0960-8966 (01) 00240-1. PubMed: 11595514. (Pubitemid 32930020)
17. Mahoney DJ, Kaczor JJ, Bourgeois J, Yasuda N, Tarnopolsky MA (2006) Oxidative stress and antioxidant enzyme upregulation in SOD1-G93A mouse skeletal muscle. Muscle Nerve 33:809-816. doi:10.1002/mus.20542. PubMed: 16583367. (Pubitemid 43856799)
18. Park K H J, Vincent I (2008) Presymptomatic biochemical changes in hindlimb muscle of G93A human Cu/Zn superoxide dismutase 1 transgenic mouse model of amyotrophic lateral sclerosis. Biochim Biophys Acta 1782:462-468. doi:10.1016/j.bbadis.2008.04.001. PubMed: 18485920.
19. Zhou J, Yi J, Fu R, Liu E, Siddique T et al. (2010) Hyperactive intracellular calcium signaling associated with localized mitochondrial defects in skeletal muscle of an animal model of amyotrophic lateral sclerosis. J Biol Chem 285:705-712. doi:10.1074/jbc. M109.041319. PubMed: 19889637.
20. Yi J, Ma C, Li Y, Weisleder N, Rös E et al. (2011) Mitochondrial calcium uptake regulates rapid calcium transients in skeletal muscle during excitation-contraction (E-C) coupling. J Biol Chem 286:32436-32443. doi:10.1074/jbc. M110.217711. PubMed: 21795684.
21. Liu X, Weaver D, Shirihai O, Hajnóczky G (2009) Mitochondrial "kissandrun": interplay between mitochondrial motility and fusion-fission dynamics. EMBO J 28:3074-3089. doi:10.1038/emboj.2009.255. PubMed: 19745815.
22. Chen H, Chan DC (2009) Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum Mol Genet 18:R169-R176. doi:10.1093/hmg/ddp326. PubMed: 19808793.
23. Lu B (2009) Mitochondrial dynamics and neurodegeneration. Curr Neurol Neurosci Rep 9:212-219. doi:10.1007/s11910-009-0032-7. PubMed: 19348710.
24. Cho D-H, Nakamura T, Lipton SA (2010) Mitochondrial dynamics in cell death and neurodegeneration. Cell Mol Life Sci 67:3435-3447. doi: 10.1007/s00018-010-0435-2. PubMed: 20577776.
25. Song W, Song Y, Kincaid B, Bossy B, Bossy-Wetzel E (2012) Mutant SOD1 (G93A) triggers mitochondrial fragmentation in spinal cord motor neurons: Neuroprotection by SIRT3 and PGC-1α. Neurobiol Dis. doi: 10.1016/j.nbd.2012.07.004.
26. Magrané J, Hervias I, Henning MS, Damiano M, Kawamata H et al. (2009) Mutant SOD1 in neuronal mitochondria causes toxicity and mitochondrial dynamics abnormalities. Hum Mol Genet 18:4552-4564. doi:10.1093/hmg/ddp421. PubMed: 19779023.
27. Eisner V, Csordás G, Hajnóczky G (2013) Interactions between sarcoendoplasmic reticulum and mitochondria in cardiac and skeletal muscle - pivotal roles in Ca2+ and reactive oxygen species signaling. J Cell Sci 126:2965-2978. doi:10.1242/jcs.093609. PubMed: 23843617.
28. Pouvreau S, Royer L, Yi J, Brum G, Meissner G et al. (2007) Ca (2+) sparks operated by membrane depolarization require isoform 3 ryanodine receptor channels in skeletal muscle. Proc Natl Acad Sci U S A 104:5235-5240. doi:10.1073/pnas.0700748104. PubMed: 17360329. (Pubitemid 47186205)
29. Givvimani S, Munjal C, Tyagi N, Sen U, Metreveli N et al. (2012) Mitochondrial division/mitophagy inhibitor (Mdivi) ameliorates pressure overload induced heart failure. PLOS ONE 7:e32388. doi:10.1371/journal.pone.0032388. PubMed: 22479323.
30. Deng H-X, Shi Y, Furukawa Y, Zhai H, Fu R et al. (2006) Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proc Natl Acad Sci U S A 103:7142-7147. doi:10.1073/pnas. 0602046103. PubMed: 16636275.
31. Carrì MT, Cozzolino M (2011) SOD1 and mitochondria in ALS: a dangerous liaison. J Bioenerg Biomembr 43:593-599. doi:10.1007/s10863-011-9394- z. PubMed: 22081209.
32. Ogata T, Yamasaki Y (1997) Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers. Anat Rec 248:214-223. doi:10.1002/(SICI) 1097-0185 (199706) 248:2. PubMed: 9185987. (Pubitemid 27246816)
33. Picard M, White K, Turnbull DM (2013) Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study. J Appl Physiol Bethesda MD 1985(114):161-171. doi:10.1152/japplphysiol.01096.2012. PubMed: 23104694.
34. Okado-Matsumoto A, Fridovich I (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 276:38388-38393. doi:10.1074/jbc. M105395200. PubMed: 11507097.
35. Higgins C M J, Jung C, Ding H, Xu Z (2002) Mutant Cu, Zn superoxide dismutase that causes motoneuron degeneration is present in mitochondria in the CNS. J Neurosci Off J Soc Neurosci 22:RC215.
36. Liu J, Lillo C, Jonsson PA, Vande Velde C, Ward CM et al. (2004) Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43:5-17. doi:10.1016/j.neuron. 2004.06.016. PubMed: 15233913. (Pubitemid 38952815)
37. Vijayvergiya C, Beal MF, Buck J, Manfredi G (2005) Mutant superoxide dismutase 1 forms aggregates in the brain mitochondrial matrix of amyotrophic lateral sclerosis mice. J Neurosci Off J Soc Neurosci 25:2463-2470. doi:10.1523/JNEUROSCI.4385-04.2005. PubMed: 15758154. (Pubitemid 40365156)
38. Vande Velde C, Miller TM, Cashman NR, Cleveland DW (2008) Selective association of misfolded ALS-linked mutant SOD1 with the cytoplasmic face of mitochondria. Proc Natl Acad Sci U S A 105:4022-4027. doi:10.1073/pnas. 0712209105. PubMed: 18296640. (Pubitemid 351723517)
39. Cozzolino M, Pesaresi MG, Amori I, Crosio C, Ferri A et al. (2009) Oligomerization of mutant SOD1 in mitochondria of motoneuronal cells drives mitochondrial damage and cell toxicity. Antioxid Redox Signal 11:1547-1558. doi:10.1089/ARS.2009.2545. PubMed: 19344252.
40. Barsoum MJ, Yuan H, Gerencser AA, Liot G, Kushnareva Y et al. (2006) Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J 25:3900-3911. doi: 10.1038/sj.emboj.7601253. PubMed: 16874299. (Pubitemid 44300275)
41. Gomez-Lazaro M, Bonekamp NA, Galindo MF, Jordán J, Schrader M (2008) 6-Hydroxydopamine (6-OHDA) induces Drp1-dependent mitochondrial fragmentation in SH-SY5Y cells. Free Radic Biol Med 44:1960-1969. doi:10.1016/j.freeradbiomed.2008.03.009. PubMed: 18395527.
42. Huang X, Sun L, Ji S, Zhao T, Zhang W et al. (2013) Kissing and nanotunneling mediate intermitochondrial communication in the heart. Proc Natl Acad Sci U S A 110:2846-2851. doi:10.1073/pnas. 1300741110. PubMed: 23386722.