Progressive Decrease of Mitochondrial Motility during Maturation of Cortical Axons In Vitro and In Vivo

Current Biology

Volumn 26, Issue 19, 2016, Pages 2602-2608

  Lewis, Tommy L ^a   Turi, Gergely F ^a   Kwon, Seok Kyu ^a   Losonczy, Attila ^a   Polleux, Franck ^a  

^a Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ANIMAL; AXON; MITOCHONDRION; MOUSE; PHYSIOLOGY;

AGING; ANIMALS; AXONS; MICE; MITOCHONDRIA;

EID: 84992200222     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.07.064     Document Type: Article

References (38)

1. 1 Chen, H., Chan, D.C., Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 18:R2 (2009), R169–R176.
2. 2 Schon, E.A., Przedborski, S., Mitochondria: the next (neurode)generation. Neuron 70 (2011), 1033–1053.
3. 3 Hirokawa, N., Niwa, S., Tanaka, Y., Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68 (2010), 610–638.
4. 4 Courchet, J., Lewis, T.L. Jr., Lee, S., Courchet, V., Liou, D.Y., Aizawa, S., Polleux, F., Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell 153 (2013), 1510–1525.
5. 5 Spillane, M., Ketschek, A., Merianda, T.T., Twiss, J.L., Gallo, G., Mitochondria coordinate sites of axon branching through localized intra-axonal protein synthesis. Cell Rep. 5 (2013), 1564–1575.
6. 6 Wang, X., Winter, D., Ashrafi, G., Schlehe, J., Wong, Y.L., Selkoe, D., Rice, S., Steen, J., LaVoie, M.J., Schwarz, T.L., PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147 (2011), 893–906.
7. 7 Brickley, K., Stephenson, F.A., Trafficking kinesin protein (TRAK)-mediated transport of mitochondria in axons of hippocampal neurons. J. Biol. Chem. 286 (2011), 18079–18092.
8. 8 Wang, X., Schwarz, T.L., The mechanism of Ca2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 136 (2009), 163–174.
9. 9 Vossel, K.A., Zhang, K., Brodbeck, J., Daub, A.C., Sharma, P., Finkbeiner, S., Cui, B., Mucke, L., Tau reduction prevents Abeta-induced defects in axonal transport. Science, 330, 2010, 198.
10. 10 Obashi, K., Okabe, S., Regulation of mitochondrial dynamics and distribution by synapse position and neuronal activity in the axon. Eur. J. Neurosci. 38 (2013), 2350–2363.
11. 11 Ashrafi, G., Schlehe, J.S., LaVoie, M.J., Schwarz, T.L., Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J. Cell Biol. 206 (2014), 655–670.
12. 12 Maday, S., Holzbaur, E.L., Autophagosome biogenesis in primary neurons follows an ordered and spatially regulated pathway. Dev. Cell 30 (2014), 71–85.
13. 13 Maday, S., Wallace, K.E., Holzbaur, E.L., Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J. Cell Biol. 196 (2012), 407–417.
14. 14 Verburg, J., Hollenbeck, P.J., Mitochondrial membrane potential in axons increases with local nerve growth factor or semaphorin signaling. J. Neurosci. 28 (2008), 8306–8315.
15. 15 Gazit, N., Vertkin, I., Shapira, I., Helm, M., Slomowitz, E., Sheiba, M., Mor, Y., Rizzoli, S., Slutsky, I., IGF-1 receptor differentially regulates spontaneous and evoked transmission via mitochondria at hippocampal synapses. Neuron 89 (2016), 583–597.
16. 16 Kwon, S.K., Sando, R. 3rd, Lewis, T.L., Hirabayashi, Y., Maximov, A., Polleux, F., LKB1 regulates mitochondria-dependent presynaptic calcium clearance and neurotransmitter release properties at excitatory synapses along cortical axons. PLoS Biol., 14, 2016, e1002516.
17. 17 Chang, K.T., Niescier, R.F., Min, K.T., Mitochondrial matrix Ca2+ as an intrinsic signal regulating mitochondrial motility in axons. Proc. Natl. Acad. Sci. USA 108 (2011), 15456–15461.
18. 18 MacAskill, A.F., Brickley, K., Stephenson, F.A., Kittler, J.T., GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol. Cell. Neurosci. 40 (2009), 301–312.
19. 19 Saotome, M., Safiulina, D., Szabadkai, G., Das, S., Fransson, A., Aspenstrom, P., Rizzuto, R., Hajnóczky, G., Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc. Natl. Acad. Sci. USA 105 (2008), 20728–20733.
20. 20 Owens, G.C., Walcott, E.C., Extensive fusion of mitochondria in spinal cord motor neurons. PLoS ONE, 7, 2012, e38435.
21. 21 McKinney, S.A., Murphy, C.S., Hazelwood, K.L., Davidson, M.W., Looger, L.L., A bright and photostable photoconvertible fluorescent protein. Nat. Methods 6 (2009), 131–133.
22. 22 Polleux, F., Giger, R.J., Ginty, D.D., Kolodkin, A.L., Ghosh, A., Patterning of cortical efferent projections by semaphorin-neuropilin interactions. Science 282 (1998), 1904–1906.
23. 23 Polleux, F., Morrow, T., Ghosh, A., Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404 (2000), 567–573.
24. 24 Kaifosh, P., Lovett-Barron, M., Turi, G.F., Reardon, T.R., Losonczy, A., Septo-hippocampal GABAergic signaling across multiple modalities in awake mice. Nat. Neurosci. 16 (2013), 1182–1184.
25. 25 Hara, K., Harris, R.A., The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth. Analg. 94 (2002), 313–318.
26. 26 Zaugg, M., Lucchinetti, E., Spahn, D.R., Pasch, T., Garcia, C., Schaub, M.C., Differential effects of anesthetics on mitochondrial K(ATP) channel activity and cardiomyocyte protection. Anesthesiology 97 (2002), 15–23.
27. 27 de Oliveira, L., Fraga, D.B., De Luca, R.D., Canever, L., Ghedim, F.V., Matos, M.P., Streck, E.L., Quevedo, J., Zugno, A.I., Behavioral changes and mitochondrial dysfunction in a rat model of schizophrenia induced by ketamine. Metab. Brain Dis. 26 (2011), 69–77.
28. 28 Sanchez, V., Feinstein, S.D., Lunardi, N., Joksovic, P.M., Boscolo, A., Todorovic, S.M., Jevtovic-Todorovic, V., General anesthesia causes long-term impairment of mitochondrial morphogenesis and synaptic transmission in developing rat brain. Anesthesiology 115 (2011), 992–1002.
29. 29 Misgeld, T., Kerschensteiner, M., Bareyre, F.M., Burgess, R.W., Lichtman, J.W., Imaging axonal transport of mitochondria in vivo. Nat. Methods 4 (2007), 559–561.
30. 30 Plucińska, G., Paquet, D., Hruscha, A., Godinho, L., Haass, C., Schmid, B., Misgeld, T., In vivo imaging of disease-related mitochondrial dynamics in a vertebrate model system. J. Neurosci. 32 (2012), 16203–16212.
31. 31 Sajic, M., Mastrolia, V., Lee, C.Y., Trigo, D., Sadeghian, M., Mosley, A.J., Gregson, N.A., Duchen, M.R., Smith, K.J., Impulse conduction increases mitochondrial transport in adult mammalian peripheral nerves in vivo. PLoS Biol., 11, 2013, e1001754.
32. 32 Sorbara, C.D., Wagner, N.E., Ladwig, A., Nikić, I., Merkler, D., Kleele, T., Marinković, P., Naumann, R., Godinho, L., Bareyre, F.M., et al. Pervasive axonal transport deficits in multiple sclerosis models. Neuron 84 (2014), 1183–1190.
33. 33 Kang, J.S., Tian, J.H., Pan, P.Y., Zald, P., Li, C., Deng, C., Sheng, Z.H., Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 132 (2008), 137–148.
34. 34 Ohno, N., Kidd, G.J., Mahad, D., Kiryu-Seo, S., Avishai, A., Komuro, H., Trapp, B.D., Myelination and axonal electrical activity modulate the distribution and motility of mitochondria at CNS nodes of Ranvier. J. Neurosci. 31 (2011), 7249–7258.
35. 35 Takihara, Y., Inatani, M., Eto, K., Inoue, T., Kreymerman, A., Miyake, S., Ueno, S., Nagaya, M., Nakanishi, A., Iwao, K., et al. In vivo imaging of axonal transport of mitochondria in the diseased and aged mammalian CNS. Proc. Natl. Acad. Sci. USA 112 (2015), 10515–10520.
36. 36 Jackson, J.G., O'Donnell, J.C., Takano, H., Coulter, D.A., Robinson, M.B., Neuronal activity and glutamate uptake decrease mitochondrial mobility in astrocytes and position mitochondria near glutamate transporters. J. Neurosci. 34 (2014), 1613–1624.
37. 37 Faits, M.C., Zhang, C., Soto, F., Kerschensteiner, D., Dendritic mitochondria reach stable positions during circuit development. eLife, 5, 2016, e11583.
38. 38 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. 30 (2010), 11369–11378.