Mitochondria as a central sensor for axonal degenerative stimuli

Trends in Neurosciences

Volumn 35, Issue 6, 2012, Pages 364-372

  Court, Felipe A ^a,b   Coleman, Michael P ^c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b Neurounion Biomedical Foundation   (Chile)

^c BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Axonal degeneration; Axonal transport; Mitochondria; Mitochondrial permeability transition pore; Reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; MITOCHONDRIAL PROTEIN; NUCLEAR PROTEIN; PROTEINASE; REACTIVE OXYGEN METABOLITE;

CALCIUM HOMEOSTASIS; CELL METABOLISM; CELL SURVIVAL; CELL TRANSPORT; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; HOMEOSTASIS; HUMAN; MITOCHONDRION; MUTATIONAL ANALYSIS; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; QUALITY CONTROL; REVIEW; STIMULUS RESPONSE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AXONAL TRANSPORT; AXONS; CALCIUM; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; REACTIVE OXYGEN SPECIES;

EID: 84861674629     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2012.04.001     Document Type: Review

References (115)

1. Adalbert R., et al. The slow Wallerian degeneration gene in vivo protects motor axons but not their cell bodies after avulsion and neonatal axotomy. Eur. J. Neurosci. 2006, 24:2163-2168.
2. Deckwerth T.L., Johnson E.M. Neurites can remain viable after destruction of the neuronal soma by programmed cell death (apoptosis). Dev. Biol. 1994, 165:63-72.
3. Misgeld T., et al. Imaging axonal transport of mitochondria in vivo. Nat. Methods 2007, 4:559-561.
4. 2+ -dependent regulation of kinesin-mediated mitochondrial motility. Cell 2009, 136:163-174.
5. Zuchner S., et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 2004, 36:449-451.
6. Delettre C., et al. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 2000, 26:207-210.
7. Ehses S., et al. Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 2009, 187:1023-1036.
8. Ferreirinha F., et al. Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. J. Clin. Invest. 2004, 113:231-242.
9. Cassereau J., et al. Mitochondrial dysfunction and pathophysiology of Charcot-Marie-Tooth disease involving GDAP1 mutations. Exp. Neurol. 2011, 227:31-41.
10. Ishihara N., et al. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell Biol. 2009, 11:958-966.
11. Waterham H.R., et al. A lethal defect of mitochondrial and peroxisomal fission. N. Engl. J. Med. 2007, 356:1736-1741.
12. Arnold B., et al. Integrating multiple aspects of mitochondrial dynamics in neurons: age-related differences and dynamic changes in a chronic rotenone model. Neurobiol. Dis. 2011, 41:189-200.
13. Cheng H.C., et al. Clinical progression in Parkinson disease and the neurobiology of axons. Ann. Neurol. 2010, 67:715-725.
14. Narendra D.P., et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010, 8:e1000298.
15. Suen D.F., et al. Parkin overexpression selects against a deleterious mtDNA mutation in heteroplasmic cybrid cells. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11835-11840.
16. Cai Q., et al. Spatial Parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr. Biol. 2012, 22:545-552.
17. Valente E.M., et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004, 304:1158-1160.
18. Kitada T., et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism [see comments]. Nature 1998, 392:605-608.
19. Yang Y., et al. Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10793-10798.
20. Matsuda W., et al. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J. Neurosci. 2009, 29:444-453.
21. Maday S., et al. Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J. Cell Biol. 2012, 196:407-417.
22. Shidara Y., Hollenbeck P.J. Defects in mitochondrial axonal transport and membrane potential without increased reactive oxygen species production in a Drosophila model of Friedreich ataxia. J. Neurosci. 2010, 30:11369-11378.
23. Wang X., et al. PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 2011, 147:893-906.
24. Calkins M.J., Reddy P.H. Assessment of newly synthesized mitochondrial DNA using BrdU labeling in primary neurons from Alzheimer's disease mice: Implications for impaired mitochondrial biogenesis and synaptic damage. Biochim. Biophys. Acta 2011, 1812:1182-1189.
25. Amiri M., Hollenbeck P.J. Mitochondrial biogenesis in the axons of vertebrate peripheral neurons. Dev. Neurobiol. 2008, 68:1348-1361.
26. Boore J.L. Animal mitochondrial genomes. Nucleic Acids Res. 1999, 27:1767-1780.
27. Aschrafi A., et al. MicroRNA-338 regulates local cytochrome c oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympathetic neurons. J. Neurosci. 2008, 28:12581-12590.
28. Bilsland L.G., et al. Deficits in axonal transport precede ALS symptoms in vivo. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20523-20528.
29. Stamer K., et al. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J. Cell Biol. 2002, 156:1051-1063.
30. Gilley J., et al. Age-dependent axonal transport and locomotor changes and tau hypophosphorylation in a 'P301L' tau knockin mouse. Neurobiol. Aging 2012, 33:621.e1-621.e15.
31. Kasher P.R., et al. Direct evidence for axonal transport defects in a novel mouse model of mutant spastin-induced hereditary spastic paraplegia (HSP) and human HSP patients. J. Neurochem. 2009, 110:34-44.
32. Misko A., et al. Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J. Neurosci. 2010, 30:4232-4240.
33. Baloh R.H., et al. Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations. J. Neurosci. 2007, 27:422-430.
34. Calkins M.J., et al. 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.
35. Shirendeb U., et al. Abnormal mitochondrial dynamics, mitochondrial loss and mutant huntingtin oligomers in Huntington's disease: implications for selective neuronal damage. Hum. Mol. Genet. 2011, 20:1438-1455.
36. Vossel K.A., et al. Tau reduction prevents Abeta-induced defects in axonal transport. Science 2010, 330:198.
37. Cartelli D., et al. Microtubule dysfunction precedes transport impairment and mitochondria damage in MPP+ -induced neurodegeneration. J. Neurochem. 2010, 115:247-258.
38. Kim-Han J.S., et al. The Parkinsonian mimetic, MPP+, specifically impairs mitochondrial transport in dopamine axons. J. Neurosci. 2011, 31:7212-7221.
39. Marinkovic P., et al. Axonal transport deficits and degeneration can evolve independently in mouse models of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:4296-4301.
40. Zhu Y.B., Sheng Z.H. Increased axonal mitochondrial mobility does not slow amyotrophic lateral sclerosis (ALS)-like disease in mutant SOD1 mice. J. Biol. Chem. 2011, 286:23432-23440.
41. Sheng Z.H., Cai Q. Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat. Rev. Neurosci. 2012, 13:77-93.
42. Baqri R.M., et al. Disruption of mitochondrial DNA replication in Drosophila increases mitochondrial fast axonal transport in vivo. PLoS ONE 2009, 4:e7874.
43. Twig G., et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008, 27:433-446.
44. Shirendeb U.P., et al. Mutant huntingtin's interaction with mitochondrial protein Drp1 impairs mitochondrial biogenesis and causes defective axonal transport and synaptic degeneration in Huntington's disease. Hum. Mol. Genet. 2012, 21:406-420.
45. Wang X., et al. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J. Neurosci. 2009, 29:9090-9103.
46. Adalbert R., et al. Severely dystrophic axons at amyloid plaques remain continuous and connected to viable cell bodies. Brain 2009, 132:402-416.
47. Nakamura K., et al. Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein. J. Biol. Chem. 2011, 286:20710-20726.
48. Komatsu M., et al. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:14489-14494.
49. Liang C.C., et al. Neural-specific deletion of FIP200 leads to cerebellar degeneration caused by increased neuronal death and axon degeneration. J. Biol. Chem. 2010, 285:3499-3509.
50. Zambonin J., et al. Identification and investigation of mitochondria lacking cytochrome c oxidase activity in axons. J. Neurosci. Methods 2010, 192:115-120.
51. Coleman M.P., Freeman M.R. Wallerian degeneration, wld(s), and nmnat. Annu. Rev. Neurosci. 2010, 33:245-267.
52. Coleman M.P., Perry V.H. Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci. 2002, 25:532-537.
53. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
54. Yahata N., et al. Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J. Neurosci. 2009, 29:6276-6284.
55. Beirowski B., et al. Non-nuclear Wld(S) determines its neuroprotective efficacy for axons and synapses in vivo. J. Neurosci. 2009, 29:653-668.
56. Sasaki Y., et al. Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. J. Neurosci. 2009, 29:5525-5535.
57. Aon M.A., et al. Redox-optimized ROS balance: a unifying hypothesis. Biochim. Biophys. Acta 2010, 1797:865-877.
58. Di Lisa F., Ziegler M. Pathophysiological relevance of mitochondria in NAD(+) metabolism. FEBS Lett. 2001, 492:4-8.
59. Gilley J., Coleman M.P. Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol. 2010, 8:e1000300.
60. Barrientos S.A., et al. Axonal degeneration is mediated by the mitochondrial permeability transition pore. J. Neurosci. 2011, 31:966-978.
61. Forte M., et al. Cyclophilin D inactivation protects axons in experimental autoimmune encephalomyelitis, an animal model of multiple sclerosis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:7558-7563.
62. Du H., et al. Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat. Med. 2008, 14:1097.
63. Martin L.J., et al. The mitochondrial permeability transition pore in motor neurons: involvement in the pathobiology of ALS mice. Exp. Neurol. 2009, 218:333-346.
64. Schinzel A.C., et al. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:12005-12010.
65. Halestrap A.P. What is the mitochondrial permeability transition pore?. J. Mol. Cell. Cardiol. 2009, 46:821-831.
66. 2+ buffering. Curr. Biol. 2012, 22:596-600.
67. Courchesne S.L., et al. Sensory neuropathy attributable to loss of Bcl-w. J. Neurosci. 2011, 31:1624-1634.
68. Brookes P.S., et al. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 2004, 287:C817-C833.
69. Dubinsky J.M. Heterogeneity of nervous system mitochondria: location, location, location!. Exp. Neurol. 2009, 218:293-307.
70. Joseph J., et al. Nutrition, brain aging, and neurodegeneration. J. Neurosci. 2009, 29:12795-12801.
71. Lennie P. The cost of cortical computation. Curr. Biol. 2003, 13:493-497.
72. Koilkonda R.D., Guy J. Leber's hereditary optic neuropathy-gene therapy: from benchtop to bedside. J. Ophthalmol. 2011, 2011:179412.
73. Agnew W.F., et al. Evolution and resolution of stimulation-induced axonal injury in peripheral nerve. Muscle Nerve 1999, 22:1393-1402.
74. Vasilescu C., et al. Neuronal type of Charcot-Marie-Tooth disease with a syndrome of continuous motor unit activity. J. Neurol. Sci. 1984, 63:11-25.
75. van Zundert B., et al. Neonatal neuronal circuitry shows hyperexcitable disturbance in a mouse model of the adult-onset neurodegenerative disease amyotrophic lateral sclerosis. J. Neurosci. 2008, 28:10864-10874.
76. García-Añoveros J., et al. Regulation of Caenorhabditis elegans degenerin proteins by a putative extracellular domain. Curr. Biol. 1995, 5:441-448.
77. Stirling D.P., Stys P.K. Mechanisms of axonal injury: internodal nanocomplexes and calcium deregulation. Trends Mol. Med. 2010, 16:160-170.
78. Yi M., et al. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J. Cell Biol. 2004, 167:661-672.
79. Mattson M.P. Calcium and neurodegeneration. Aging Cell 2007, 6:337-350.
80. Milakovic T., et al. Mutant huntingtin expression induces mitochondrial calcium handling defects in clonal striatal cells: functional consequences. J. Biol. Chem. 2006, 281:34785-34795.
81. 2+ homeostasis. PLoS ONE 2011, 6:e19290.
82. Forman H.J., et al. Signaling functions of reactive oxygen species. Biochemistry 2010, 49:835-842.
83. Mattson M.P., Magnus T. Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 2006, 7:278-294.
84. Press C., Milbrandt J. Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. J. Neurosci. 2008, 28:4861-4871.
85. Kregel K.C., Zhang H.J. An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R18-R36.
86. Fischer L.R., Glass J.D. Oxidative stress induced by loss of Cu,Zn-superoxide dismutase (SOD1) or superoxide-generating herbicides causes axonal degeneration in mouse DRG cultures. Acta Neuropathol. 2010, 119:249-259.
87. Zhu S.S., et al. Wld (S) protects against peripheral neuropathy and retinopathy in an experimental model of diabetes in mice. Diabetologia 2011, 54:2440-2450.
88. Zipp F., Aktas O. The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases. Trends Neurosci. 2006, 29:518-527.
89. Smith K.J., et al. Electrically active axons degenerate when exposed to nitric oxide. Ann. Neurol. 2001, 49:470-476.
90. Misawa H., et al. Conditional knockout of Mn superoxide dismutase in postnatal motor neurons reveals resistance to mitochondrial generated superoxide radicals. Neurobiol. Dis. 2006, 23:169-177.
91. George E.B., et al. Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J. Neurosci. 1995, 15:6445-6452.
92. Hofer T., et al. Bioenergetics and permeability transition pore opening in heart subsarcolemmal and interfibrillar mitochondria: effects of aging and lifelong calorie restriction. Mech. Ageing Dev. 2009, 130:297-307.
93. Zorov D.B., et al. Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc. Res. 2009, 83:213-225.
94. 2+ ions. Acta Medica (Hradec Kralove) 2009, 52:69-72.
95. 2+overload than nonsynaptic mitochondria. J. Biol. Chem. 2006, 281:11658-11668.
96. Naga K.K., et al. High cyclophilin D content of synaptic mitochondria results in increased vulnerability to permeability transition. J. Neurosci. 2007, 27:7469-7475.
97. Tsukita S., Ishikawa H. Three-dimensional distribution of smooth endoplasmic reticulum in myelinated axons. J. Electron Microsc. (Tokyo) 1976, 25:141-149.
98. Yan Y., et al. Cross-talk between calcium and reactive oxygen species signaling. Acta Pharmacol. Sin. 2006, 27:821-826.
99. Csordas G., Hajnoczky G. SR/ER-mitochondrial local communication: calcium and ROS. Biochim. Biophys. Acta 2009, 1787:1352-1362.
100. de Brito O.M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456:605-610.
101. Friedman J.R., et al. ER tubules mark sites of mitochondrial division. Science 2011, 334:358-362.
102. Edgar J.M., et al. Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia. J. Cell Biol. 2004, 166:121-131.
103. Cartoni R., et al. Expression of mitofusin 2(R94Q) in a transgenic mouse leads to Charcot-Marie-Tooth neuropathy type 2A. Brain 2010, 133:1460-1469.
104. Evgrafov O.V., et al. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat. Genet. 2004, 36:602-606.
105. Ackerley S., et al. A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes. Hum. Mol. Genet. 2006, 15:347-354.
106. Irobi J., et al. Mutant HSPB8 causes motor neuron-specific neurite degeneration. Hum. Mol. Genet. 2010, 19:3254-3265.
107. Bross P., et al. The Hsp60-(p.V98I) mutation associated with hereditary spastic paraplegia SPG13 compromises chaperonin function both in vitro and in vivo. J. Biol. Chem. 2008, 283:15694-15700.
108. Beetz C., et al. REEP1 mutation spectrum and genotype/phenotype correlation in hereditary spastic paraplegia type 31. Brain 2008, 131:1078-1086.
109. Kamei S., et al. Expression of the Opa1 mitochondrial protein in retinal ganglion cells: its downregulation causes aggregation of the mitochondrial network. Invest. Ophthalmol. Vis. Sci. 2005, 46:4288-4294.
110. Carelli V., et al. Mitochondrial dysfunction as a cause of optic neuropathies. Prog. Retin. Eye Res. 2004, 23:53-89.
111. Andres-Mateos E., et al. DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:14807-14812.
112. Guzman J.N., et al. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 2010, 468:696-700.
113. Wang X., et al. LRRK2 regulates mitochondrial dynamics and function through direct interaction with DLP1. Hum. Mol. Genet. 2012, 21:1931-1944.
114. Strauss K.M., et al. Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease. Hum. Mol. Genet. 2005, 14:2099-2111.
115. Eerola J., et al. POLG1 polyglutamine tract variants associated with Parkinson's disease. Neurosci. Lett. 2010, 477:1-5.