Neuronal mitochondrial transport and dysfunction

Mitochondrial Dysfunction in Neurodegenerative Disorders

Volumn , Issue , 2012, Pages 157-173

  Atkin, Talia A ^a   MacAskill, Andrew F ^a   Kittler, Josef T ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Alzheimer s disease; Amyloid lateral sclerosis; Charcot Marie Tooth Disease; Huntington s disease; Mitochondria; Parkinson s disease; Trafficking; Transport

Indexed keywords

EID: 84948177283     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-85729-701-3_10     Document Type: Chapter

References (105)

1. Mattson MP, Gleichmann M, Cheng A. Mitochondria in neuroplasticity and neurological disorders. Neuron. 2008;60(5):748-66.
2. Hirokawa N, Takemura R. Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci. 2005;6(3):201-14.
3. Baas PW, Deitch JS, Black MM, et al. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc Natl Acad Sci USA. 1988;85(21):8335-9.
4. Hirokawa N, Niwa S, Tanaka Y. Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron. 2010;68(4):610-38.
5. Nangaku M, Sato-Yoshitake R, Okada Y, et al. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell. 1994;79(7):1209-20.
6. Tanaka Y, Kanai Y, Okada Y, et al. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell. 1998;93(7): 1147-58.
7. Macaskill AF, Rinholm JE, Twelvetrees AE, et al. Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron. 2009;61(4):541-55.
8. Glater EE, Megeath LJ, Stowers RS, et al. Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J Cell Biol. 2006;173(4):545-57.
9. Stowers RS, Megeath LJ, Gorska-Andrzejak J, et al. Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron. 2002;36(6):1063-77.
10. Brickley K, Smith MJ, Beck M, et al. GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J Biol Chem. 2005;280(15):14723-32.
11. MacAskill AF, Brickley K, Stephenson FA, et al. GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol Cell Neurosci. 2009; 40(3):301-12.
12. Webber E, Li L, Chin LS. Hypertonia-associated protein Trak1 is a novel regulator of endosome- to-lysosome trafficking. J Mol Biol. 2008;382(3):638-51.
13. Kirk E, Chin LS, Li L. GRIF1 binds Hrs and is a new regulator of endosomal trafficking. J Cell Sci. 2006;119(Pt 22):4689-701.
14. Gilbert SL, Zhang L, Forster ML, et al. Trak1 mutation disrupts GABA(A) receptor homeostasis in hypertonic mice. Nat Genet. 2006;38(2):245-50.
15. Beck M, Brickley K, Wilkinson HL, et al. Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J Biol Chem. 2002;277(33): 30079-90.
16. Grishin A, Li H, Levitan ES, et al. Identification of λ-aminobutyric acid receptor-interacting factor 1 (TRAK2) as a trafficking factor for the K+ channel Kir21. J Biol Chem. 2006;281(40):30104-11.
17. Fujita T, Maturana AD, Ikuta J, et al. Axonal guidance protein FEZ1 associates with tubulin and kinesin motor protein to transport mitochondria in neurites of NGF-stimulated PC12 cells. Biochem Biophys Res Commun. 2007;361(3):605-10.
18. Cho KI, Cai Y, Yi H, et al. Association of the kinesin-binding domain of RanBP2 to KIF5B and KIF5C determines mitochondria localization and function. Traffic. 2007;8(12):1722-35.
19. Santama N, Er CP, Ong LL, et al. Distribution and functions of kinectin isoforms. J Cell Sci. 2004;117(Pt 19):4537-49.
20. Cai Q, Gerwin C, Sheng ZH. Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J Cell Biol. 2005;170(6):959-69.
21. Yokoyama N, Hayashi N, Seki T, et al. A giant nucleopore protein that binds Ran/TC4. Nature. 1995;376(6536):184-8.
22. Gindhart JG, Chen J, Faulkner M, et al. The kinesin-associated protein UNC-76 is required for axonal transport in the Drosophila nervous system. Mol Biol Cell. 2003;14(8):3356-65.
23. Ong LL, Lim AP, Er CP, et al. Kinectin-kinesin binding domains and their effects on organelle motility. J Biol Chem. 2000;275(42):32854-60.
24. Cai Q, Pan PY, Sheng ZH. Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J Neurosci. 2007;27(27):7284-96.
25. Su Q, Cai Q, Gerwin C, et al. Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol. 2004;6(10):941-53.
26. Fransson A, Ruusala A, Aspenstrom P. Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J Biol Chem. 2003;278(8):6495-502.
27. Fransson S, Ruusala A, Aspenstrom P. The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem Biophys Res Commun. 2006;344(2):500-10.
28. Vallee RB, Williams JC, Varma D, et al. Dynein: an ancient motor protein involved in multiple modes of transport. J Neurobiol. 2004;58(2):189-200.
29. Waterman-Storer CM, Karki SB, Kuznetsov SA, et al. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc Natl Acad Sci USA. 1997;94(22): 12180-5.
30. Hollenbeck PJ, Saxton WM. The axonal transport of mitochondria. J Cell Sci. 2005; 118(Pt 23):5411-9.
31. Schwarzer C, Barnikol-Watanabe S, Thinnes FP, et al. Voltage-dependent anion-selective channel (VDAC) interacts with the dynein light chain Tctex1 and the heat-shock protein PBP74. Int J Biochem Cell Biol. 2002;34(9):1059-70.
32. Horiuchi D, Barkus RV, Pilling AD, et al. APLIP1, a kinesin binding JIP-1/JNK scaffold protein, influences the axonal transport of both vesicles and mitochondria in Drosophila. Curr Biol. 2005;15(23):2137-41.
33. Verhey KJ, Meyer D, Deehan R, et al. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol. 2001;152(5):959-70.
34. Ly CV, Verstreken P. Mitochondria at the synapse. Neuroscientist. 2006;12(4):291-9.
35. MacAskill AF, Atkin TA, Kittler JT. Mitochondrial trafficking and the provision of energy and calcium buffering at excitatory synapses. Eur J Neurosci. 2010;32(2):231-40.
36. Billups B, Forsythe ID. Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci. 2002;22(14):5840-7.
37. Verstreken P, Ly CV, Venken KJ, et al. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron. 2005;47(3):365-78.
38. Ma H, Cai Q, Lu W, et al. KIF5B motor adaptor syntabulin maintains synaptic transmission in sympathetic neurons. J Neurosci. 2009;29(41):13019-29.
39. David G, Barrett EF. Stimulation-evoked increases in cytosolic [Ca(2+)] in mouse motor nerve terminals are limited by mitochondrial uptake and are temperature-dependent. J Neurosci. 2000;20(19):7290-6.
40. Tang Y, Zucker RS. Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron. 1997;18(3):483-91.
41. Kang JS, Tian JH, Pan PY, et al. Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell. 2008;132(1):137-48.
42. Li Z, Okamoto K, Hayashi Y, et al. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell. 2004;119(6):873-87.
43. Guo X, Macleod GT, Wellington A, et al. The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron. 2005;47(3):379-93.
44. Wang X, Su B, Lee HG, et al. Impaired balance of mitochondrial fission and fusion in Alzheimer’s disease. J Neurosci. 2009;29(28):9090-103.
45. Li H, Chen Y, Jones AF, et al. Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons. Proc Natl Acad Sci USA. 2008;105(6):2169-74.
46. D’Amelio M, Cavallucci V, Middei S, et al. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer’s disease. Nat Neurosci. 2010;14(1):69-76.
47. Li Z, Jo J, Jia J-M, et al. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell. 2010;141(5):859-71.
48. Cai Q, Sheng ZH. Moving or stopping mitochondria: Miro as a traffic cop by sensing calcium. Neuron. 2009;61(4):493-6.
49. Chang DT, Honick AS, Reynolds IJ. Mitochondrial trafficking to synapses in cultured primary cortical neurons. J Neurosci. 2006;26(26):7035-45.
50. Rintoul GL, Filiano AJ, Brocard JB, et al. Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J Neurosci. 2003;23(21):7881-8.
51. Saotome M, Safiulina D, Szabadkai G, et al. Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc Natl Acad Sci USA. 2008;105(52):20728-33.
52. Wang X, Schwarz TL. The mechanism of Ca2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell. 2009;136(1):163-74.
53. Rintoul GL, Bennett VJ, Papaconstandinou NA, et al. Nitric oxide inhibits mitochondrial movement in forebrain neurons associated with disruption of mitochondrial membrane potential. J Neurochem. 2006;97(3):800-6.
54. Zanelli SA, Trimmer PA, Solenski NJ. Nitric oxide impairs mitochondrial movement in cortical neurons during hypoxia. J Neurochem. 2006;97(3):724-36.
55. Chen S, Owens GC, Crossin KL, et al. Serotonin stimulates mitochondrial transport in hippocampal neurons. Mol Cell Neurosci. 2007;36(4):472-83.
56. Morfini G, Szebenyi G, Elluru R, et al. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J. 2002;21(3):281-93.
57. Chen S, Owens GC, Edelman DB. Dopamine inhibits mitochondrial motility in hippocampal neurons. PLoS One. 2008;3(7):e2804.
58. Mironov SL. ADP regulates movements of mitochondria in neurons. Biophys J. 2007;92(8): 2944-52.
59. Miller KE, Sheetz MP. Axonal mitochondrial transport and potential are correlated. J Cell Sci. 2004;117(Pt 13):2791-804.
60. Iijima-Ando K, Hearn SA, Shenton C, et al. Mitochondrial mislocalization underlies Aβ42- induced neuronal dysfunction in a Drosophila model of Alzheimer’s disease. PLoS One. 2009;4(12):e8310.
61. Chang DT, Rintoul GL, Pandipati S, et al. Mutant huntingtin aggregates impair mitochondrial movement and trafficking in cortical neurons. Neurobiol Dis. 2006;22(2):388-400.
62. Weihofen A, Thomas KJ, Ostaszewski BL, et al. Pink1 forms a multiprotein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking. Biochemistry. 2009;48(9): 2045-52.
63. De Vos KJ, Chapman AL, Tennant ME, et al. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum Mol Genet. 2007;16(22):2720-8.
64. Atkin TA, MacAskill AF, Brandon NJ, et al. Disrupted in Schizophrenia-1 regulates intracellular trafficking of mitochondria in neurons. Mol Psychiatry. 2011;16(2):122-4.
65. Delettre C, Lenaers G, Griffoin JM, et al. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet. 2000;26(2):207-10.
66. Zuchner S, Mersiyanova IV, Muglia M, et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet. 2004;36(5):449-51.
67. Roze E, Saudou F, Caboche J. Pathophysiology of Huntington’s disease: from huntingtin functions to potential treatments. Curr Opin Neurol. 2008;21(4):497-503.
68. Gu M, Gash MT, Mann VM, et al. Mitochondrial defect in Huntington’s disease caudate nucleus. Ann Neurol. 1996;39(3):385-9.
69. Orr AL, Li S, Wang CE, et al. N-terminal mutant huntingtin associates with mitochondria and impairs mitochondrial trafficking. J Neurosci. 2008;28(11):2783-92.
70. Twelvetrees AE, Yuen EY, Arancibia-Carcamo IL, et al. Delivery of GABAARs to synapses is mediated by HAP1-KIF5 and disrupted by mutant huntingtin. Neuron. 2010;65(1):53-65.
71. Gauthier LR, Charrin BC, Borrell-Pages M, et al. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell. 2004;118(1):127-38.
72. Trushina E, Dyer RB, Badger 2nd JD, et al. Mutant huntingtin impairs axonal trafficking in mammalian neurons in vivo and in vitro. Mol Cell Biol. 2004;24(18):8195-209.
73. Morfini GA, You YM, Pollema SL, et al. Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin. Nat Neurosci. 2009;12(7):864-71.
74. Reed NA, Cai D, Blasius TL, et al. Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol. 2006;16(21):2166-72.
75. Dompierre JP, Godin JD, Charrin BC, et al. Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington’s disease by increasing tubulin acetylation. J Neurosci. 2007;27(13):3571-83.
76. Caviston JP, Ross JL, Antony SM, et al. Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc Natl Acad Sci USA. 2007;104(24):10045-50.
77. Caviston JP, Zajac AL, Tokito M, et al. Huntingtin coordinates the dynein-mediated dynamic positioning of endosomes and lysosomes. Mol Biol Cell. 2011;22(4):478-92.
78. Colin E, Zala D, Liot G, et al. Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J. 2008;27(15):2124-34.
79. Zala D, Colin E, Rangone H, et al. Phosphorylation of mutant huntingtin at S421 restores anterograde and retrograde transport in neurons. Hum Mol Genet. 2008;17(24):3837-46.
80. Pineda JR, Pardo R, Zala D, et al. Genetic and pharmacological inhibition of calcineurin corrects the BDNF transport defect in Huntington’s disease. Mol Brain. 2009;2(1):33.
81. Thies E, Mandelkow EM. Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J Neurosci. 2007;27(11):2896-907.
82. Dixit R, Ross JL, Goldman YE, et al. Differential regulation of dynein and kinesin motor proteins by tau. Science. 2008;319(5866):1086-9.
83. Jimenez-Mateos EM, Gonzalez-Billault C, Dawson HN, et al. Role of MAP1B in axonal retrograde transport of mitochondria. Biochem J. 2006;397(1):53-9.
84. Vossel KA, Zhang K, Brodbeck J, et al. Tau reduction prevents Aβ-induced defects in axonal transport. Science. 2010;330(6001):198.
85. Decker H, Lo KY, Unger SM, et al. Amyloid-βpeptide oligomers disrupt axonal transport through an NMDA receptor-dependent mechanism that is mediated by glycogen synthase kinase 3βin primary cultured hippocampal neurons. J Neurosci. 2010;30(27):9166-71.
86. Rui Y, Tiwari P, Xie Z, et al. Acute impairment of mitochondrial trafficking by β-amyloid peptides in hippocampal neurons. J Neurosci. 2006;26(41):10480-7.
87. Cho DH, Nakamura T, Fang J, et al. S-nitrosylation of Drp1 mediates β-amyloid-related mitochondrial fission and neuronal injury. Science. 2009;324(5923):102-5.
88. Lacor PN, Buniel MC, Furlow PW, et al. Aβoligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer’s disease. J Neurosci. 2007;27(4):796-807.
89. Rui Y, Gu J, Yu K, et al. Inhibition of AMPA receptor trafficking at hippocampal synapses by β-amyloid oligomers: the mitochondrial contribution. Mol Brain. 2010;3:10.
90. Cutler RG, Kelly J, Storie K, et al. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer’s disease. Proc Natl Acad Sci USA. 2004;101(7):2070-5.
91. Chen H, Chan DC. Emerging functions of mammalian mitochondrial fusion and fission. Hum Mol Genet. 2005;14(Spec No. 2):R283-9.
92. Barsoum MJ, Yuan H, Gerencser AA, et al. Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J. 2006;25(16):3900-11.
93. Wang X, Su B, Siedlak SL, et al. Amyloid-βoverproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc Natl Acad Sci USA. 2008;105(49):19318-23.
94. Bruijn LI, Miller TM, Cleveland DW. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci. 2004;27:723-49.
95. Sasaki S, Iwata M. Mitochondrial alterations in the spinal cord of patients with sporadic amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 2007;66(1):10-6.
96. Munch C, Sedlmeier R, Meyer T, et al. Point mutations of the p150 subunit of dynactin (DCTN1) gene in ALS. Neurology. 2004;63(4):724-6.
97. Puls I, Jonnakuty C, LaMonte BH, et al. Mutant dynactin in motor neuron disease. Nat Genet. 2003;33(4):455-6.
98. Cartelli D, Ronchi C, Maggioni MG, et al. Microtubule dysfunction precedes transport impairment and mitochondria damage in MPP+-induced neurodegeneration. J Neurochem. 2010;115(1):247-58.
99. Gandhi S, Wood-Kaczmar A, Yao Z, et al. PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death. Mol Cell. 2009;33(5):627-38.
100. Venderova K, Kabbach G, Abdel-Messih E, et al. Leucine-rich repeat kinase 2 interacts with Parkin, DJ-1 and PINK-1 in a Drosophila melanogaster model of Parkinson’s disease. Hum Mol Genet. 2009;18(22):4390-404.
101. Cartoni R, Martinou JC. Role of mitofusin 2 mutations in the physiopathology of Charcot- Marie-Tooth disease type 2A. Exp Neurol. 2009;218(2):268-73.
102. Misko A, Jiang S, Wegorzewska I, et al. Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J Neurosci. 2010;30(12):4232-40.
103. Cartoni R, Arnaud E, Medard JJ, et al. Expression of mitofusin 2(R94Q) in a transgenic mouse leads to Charcot-Marie-Tooth neuropathy type 2A. Brain. 2010;133(Pt 5):1460-9.
104. Baxter RV, Ben Othmane K, Rochelle JM, et al. Ganglioside-induced differentiation-associated protein-1 is mutant in Charcot-Marie-Tooth disease type 4A/8q21. Nat Genet. 2002; 30(1):21-2.
105. Iijima-Ando K, Hearn SA, Granger L, et al. http://www.ncbi.nlm.nih.gov/pubmed/18463098 Overexpression of neprilysin reduces alzheimer amyloid-β42 (Aβ42)-induced neuron loss and intraneuronal Aβ42 deposits but causes a reduction in cAMP-responsive element-binding protein-mediated transcription, age-dependent axon pathology, and premature death in Drosophila. J Biol Chem. 2008 Jul 4;283(27):19066-76. Epub 2008 May 7.