Oxidative damage to mitochondria at the nodes of Ranvier precedes axon degeneration in ex vivo transected axons

Experimental Neurology

Volumn 261, Issue , 2014, Pages 127-135

  Bros, Helena ^a   Millward, Jason M ^a   Paul, Friedemann ^a   Niesner, Raluca ^b   Infante Duarte, Carmen ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

Author keywords

Axonal degeneration; Mitochondria; Neurodegenerative disease; Node of Ranvier; Oxidative stress

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE; OXOACID; PYRUVIC ACID METHYL ESTER; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; HYDROGEN PEROXIDE; OXYGEN RADICAL; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; METHYL PYRUVATE; PYRUVIC ACID DERIVATIVE;

ADULT; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; BIOENERGY; CELL ELONGATION; CELL MOTILITY; CELL STRUCTURE; CELL TRANSPORT; CONTROLLED STUDY; DEPOLARIZATION; EX VIVO STUDY; FEMALE; MITOCHONDRION; MOUSE; MYELINATED NERVE; NERVE FIBER DEGENERATION; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RANVIER NODE; VENTRAL ROOT; ANIMAL EXPERIMENT; CONFOCAL MICROSCOPY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; INTERNODE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MORPHOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; ENERGY METABOLISM; NERVE DEGENERATION; NERVE FIBER; NONPARAMETRIC TEST; OXIDATION REDUCTION REACTION; PATHOLOGY; PHYSIOLOGY; RHIZOTOMY; SPINAL ROOT; SURGERY; ULTRASTRUCTURE;

ANIMALS; AXONS; ENERGY METABOLISM; FEMALE; HYDROGEN PEROXIDE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NAD; NERVE DEGENERATION; OXIDATION-REDUCTION; OXIDATIVE STRESS; PYRUVATES; RANVIER'S NODES; RHIZOTOMY; SPINAL NERVE ROOTS; STATISTICS, NONPARAMETRIC;

EID: 84905254531     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.06.018     Document Type: Article

References (52)

1. Bajic A., Spasic M., Andjus P.R., Savic D., Parabucki A., Nikolic-Kokic A., Spasojevic I. Fluctuating vs. continuous exposure to H(2)O(2): the effects on mitochondrial membrane potential, intracellular calcium, and NF-kappaB in astroglia. PLoS ONE 2013, 8:e76383.
2. Barrientos S.A., Martinez N.W., Yoo S., Jara J.S., Zamorano S., Hetz C., Twiss J.L., Alvarez J., Court F.A. Axonal degeneration is mediated by the mitochondrial permeability transition pore. J. Neurosci. 2011, 31:966-978.
3. 2+ channel, and actin define the sites of spheroids in axons undergoing oxidative stress. J. Neurosci. 2012, 32:12028-12037.
4. Bernardi P., Krauskopf A., Basso E., Petronilli V., Blachly-Dyson E., Di Lisa F., Forte M.A. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J. 2006, 273:2077-2099.
5. Bilsland L.G., Sahai E., Kelly G., Golding M., Greensmith L., Schiavo G. Deficits in axonal transport precede ALS symptoms in vivo. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20523-20528.
6. Buckman J.F., Hernandez H., Kress G.J., Votyakova T.V., Pal S., Reynolds I.J. MitoTracker labeling in primary neuronal and astrocytic cultures: influence of mitochondrial membrane potential and oxidants. J. Neurosci. Methods 2001, 104:165-176.
7. Calkins M.J., Manczak M., Mao P., Shirendeb U., Reddy P.H. Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer's disease. Hum. Mol. Genet. 2011, 20:4515-4529.
8. Chen H., Chan D.C. Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 2009, 18:R169-R176.
9. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
10. Court F.A., Coleman M.P. Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci. 2012, 35:364-372.
11. Czarna M., Mathy G., Mac'Cord A., Dobson R., Jarmuszkiewicz W., Sluse-Goffart C.M., Leprince P., De Pauw E., Sluse F.E. Dynamics of the Dictyostelium discoideum mitochondrial proteome during vegetative growth, starvation and early stages of development. Proteomics 2010, 10:6-22.
12. De Vos K.J., Chapman A.L., Tennant M.E., Manser C., Tudor E.L., Lau K.F., Brownlees J., Ackerley S., Shaw P.J., McLoughlin D.M., Shaw C.E., Leigh P.N., Miller C.C., Grierson A.J. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum. Mol. Genet. 2007, 16:2720-2728.
13. Ferlini C., Scambia G., Fattorossi A. Is chloromethyl-X-rosamine useful in measuring mitochondrial transmembrane potential?. Cytometry 1998, 31:74-75.
14. Ferri A., Sanes J.R., Coleman M.P., Cunningham J.M., Kato A.C. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr. Biol. 2003, 13:669-673.
15. Finkel T. Oxygen radicals and signaling. Curr. Opin. Cell Biol. 1998, 10:248-253.
16. Fischer L.R., Culver D.G., Tennant P., Davis A.A., Wang M., Castellano-Sanchez A., Khan J., Polak M.A., Glass J.D. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 2004, 185:232-240.
17. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
18. Gould T.W., Buss R.R., Vinsant S., Prevette D., Sun W., Knudson C.M., Milligan C.E., Oppenheim R.W. Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J. Neurosci. 2006, 26:8774-8786.
19. Hollenbeck P.J., Saxton W.M. The axonal transport of mitochondria. J. Cell Sci. 2005, 118:5411-5419.
20. Ikegami K., Koike T. Non-apoptotic neurite degeneration in apoptotic neuronal death: pivotal role of mitochondrial function in neurites. Neuroscience 2003, 122:617-626.
21. Jaarsma D., Rognoni F., van Duijn W., Verspaget H.W., Haasdijk E.D., Holstege J.C. CuZn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol. 2001, 102:293-305.
22. Kaasik A., Safiulina D., Choubey V., Kuum M., Zharkovsky A., Veksler V. Mitochondrial swelling impairs the transport of organelles in cerebellar granule neurons. J. Biol. Chem. 2007, 282:32821-32826.
23. Kerr P.M., Suleiman M.S., Halestrap A.P. Reversal of permeability transition during recovery of hearts from ischemia and its enhancement by pyruvate. Am. J. Physiol. 1999, 276:H496-H502.
24. Kessel D. Reversible effects of photodamage directed toward mitochondria. Photochem. Photobiol. 2014.
25. Li H., Li S.H., Yu Z.X., Shelbourne P., Li X.J. Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. J. Neurosci. 2001, 21:8473-8481.
26. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
27. Macho A., Decaudin D., Castedo M., Hirsch T., Susin S.A., Zamzami N., Kroemer G. Chloromethyl-X-rosamine is an aldehyde-fixable potential-sensitive fluorochrome for the detection of early apoptosis. Cytometry 1996, 25:333-340.
28. Mattson M.P., Magnus T. Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 2006, 7:278-294.
29. Matylevitch N.P., Schuschereba S.T., Mata J.R., Gilligan G.R., Lawlor D.F., Goodwin C.W., Bowman P.D. Apoptosis and accidental cell death in cultured human keratinocytes after thermal injury. Am. J. Pathol. 1998, 153:567-577.
30. Medana I.M., Esiri M.M. Axonal damage: a key predictor of outcome in human CNS diseases. Brain 2003, 126:515-530.
31. Misgeld T., Kerschensteiner M., Bareyre F.M., Burgess R.W., Lichtman J.W. Imaging axonal transport of mitochondria in vivo. Nat. Methods 2007, 4:559-561.
32. Misko A., Jiang S., Wegorzewska I., Milbrandt J., Baloh R.H. Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J. Neurosci. 2010, 30:4232-4240.
33. Nikic I., Merkler D., Sorbara C., Brinkoetter M., Kreutzfeldt M., Bareyre F.M., Bruck W., Bishop D., Misgeld T., Kerschensteiner M. A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat. Med. 2011, 17:495-499.
34. Orr A.L., Li S., Wang C.E., Li H., Wang J., Rong J., Xu X., Mastroberardino P.G., Greenamyre J.T., Li X.J. N-terminal mutant huntingtin associates with mitochondria and impairs mitochondrial trafficking. J. Neurosci. 2008, 28:2783-2792.
35. Park J.Y., Jang S.Y., Shin Y.K., Koh H., Suh D.J., Shinji T., Araki T., Park H.T. Mitochondrial swelling and microtubule depolymerization are associated with energy depletion in axon degeneration. Neuroscience 2013, 238:258-269.
36. Perlson E., Maday S., Fu M.M., Moughamian A.J., Holzbaur E.L. Retrograde axonal transport: pathways to cell death?. Trends Neurosci. 2010, 33:335-344.
37. Perry S.W., Norman J.P., Barbieri J., Brown E.B., Gelbard H.A. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques 2011, 50:98-115.
38. Persson A.K., Kim I., Zhao P., Estacion M., Black J.A., Waxman S.G. Sodium channels contribute to degeneration of dorsal root ganglion neurites induced by mitochondrial dysfunction in an in vitro model of axonal injury. J. Neurosci. 2013, 33:19250-19261.
39. Poliak S., Peles E. The local differentiation of myelinated axons at nodes of Ranvier. Nat. Rev. Neurosci. 2003, 4:968-980.
40. Rasband M.N. The axon initial segment and the maintenance of neuronal polarity. Nat. Rev. Neurosci. 2010, 11:552-562.
41. Rasola A., Bernardi P. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 2007, 12:815-833.
42. Rhee S.G. Redox signaling: hydrogen peroxide as intracellular messenger. Exp. Mol. Med. 1999, 31:53-59.
43. Scorrano L., Petronilli V., Colonna R., Di Lisa F., Bernardi P. Chloromethyltetramethylrosamine (MitoTracker Orange) induces the mitochondrial permeability transition and inhibits respiratory complex I. Implications for the mechanism of cytochrome c release. J. Biol. Chem. 1999, 274:24657-24663.
44. Stokin G.B., Lillo C., Falzone T.L., Brusch R.G., Rockenstein E., Mount S.L., Raman R., Davies P., Masliah E., Williams D.S., Goldstein L.S. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 2005, 307:1282-1288.
45. Stys P.K. General mechanisms of axonal damage and its prevention. J. Neurol. Sci. 2005, 233:3-13.
46. Tegenge M.A., Rajbhandari L., Shrestha S., Mithal A., Hosmane S., Venkatesan A. Curcumin protects axons from degeneration in the setting of local neuroinflammation. Exp. Neurol. 2013, 253:102-110.
47. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., Bo L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 1998, 338:278-285.
48. Tsao J.W., George E.B., Griffin J.W. Temperature modulation reveals three distinct stages of Wallerian degeneration. J. Neurosci. 1999, 19:4718-4726.
49. Vande Velde C., McDonald K.K., Boukhedimi Y., McAlonis-Downes M., Lobsiger C.S., Bel Hadj S., Zandona A., Julien J.P., Shah S.B., Cleveland D.W. Misfolded SOD1 associated with motor neuron mitochondria alters mitochondrial shape and distribution prior to clinical onset. PLoS ONE 2011, 6:e22031.
50. Wang J., Zhai Q., Chen Y., Lin E., Gu W., McBurney M.W., He Z. A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 2005, 170:349-355.
51. Waxman S.G. Axonal conduction and injury in multiple sclerosis: the role of sodium channels. Nat. Rev. Neurosci. 2006, 7:932-941.
52. Zhang C.L., Ho P.L., Kintner D.B., Sun D., Chiu S.Y. Activity-dependent regulation of mitochondrial motility by calcium and Na/K-ATPase at nodes of Ranvier of myelinated nerves. J. Neurosci. 2010, 30:3555-3566.