Evidence that dendritic mitochondria negatively regulate dendritic branching in pyramidal neurons in the neocortex

Journal of Neuroscience

Volumn 34, Issue 20, 2014, Pages 6938-6951

  Kimura, Toshiya ^a,b   Murakami, Fujio ^a  

^a OSAKA UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Dendritic development; Mitochondria; Neocortex; Organelle; Subcellular distribution

Indexed keywords

ADAPTOR PROTEIN; MITOFUSIN 1; TRAFFICKING KINESIN PROTEIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CELL STRUCTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; FEMALE; IMMUNOFLUORESCENCE TEST; MITOCHONDRIAL MEMBRANE POTENTIAL; MORPHOGENESIS; MOUSE; NEOCORTEX; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL;

DENDRITIC DEVELOPMENT; MITOCHONDRIA; NEOCORTEX; ORGANELLE; SUBCELLULAR DISTRIBUTION;

ANIMALS; CELL SHAPE; DENDRITES; GTP PHOSPHOHYDROLASES; MICE; MICE, TRANSGENIC; MITOCHONDRIA; NEOCORTEX; PROTEIN TRANSPORT; PYRAMIDAL CELLS;

EID: 84900408012     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5095-13.2014     Document Type: Article

References (50)

1. Ai HW, Shaner NC, Cheng Z, Tsien RY, Campbell RE (2007) Exploration of new chromophore structures leads to the identification of improved blue fluorescent proteins. Biochemistry 46:5904-5910. CrossRef Medline
2. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576. CrossRef Medline
3. Brickley K, Stephenson FA (2011) Trafficking kinesin protein (TRAK)-mediated transport of mitochondria in axons of hippocampal neurons. J Biol Chem 286:18079-18092. CrossRef Medline
4. Brickley K, Smith MJ, Beck M, Stephenson FA (2005) 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 280:14723-14732. CrossRef Medline
5. Chan DC (2006) Mitochondria: dynamic organelles in disease, aging and development. Cell 125:1241-1252. CrossRef Medline
6. Chandrasekaran K, Hazelton JL, Wang Y, Fiskum G, Kristian T (2006) Neuron-specific conditional expression of a mitochondrially targeted fluorescent protein in mice. J Neurosci 26:13123-13127. CrossRef Medline
7. Chen H, McCaffery JM, Chan DC (2007) Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130:548-562. CrossRef Medline
8. Cline HT (2001) Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11:118-126. CrossRef Medline
9. Cole NB, Smith CL, Sciaky N, Terasaki M, Edidin M, Lippincott-Schwartz J (1996) Diffusional mobility of Golgi proteins in membranes of living cells. Science 273:797-801. CrossRef Medline
10. Fliegel L, Burns K, MacLennan DH, Reithmeier RA, Michalak M (1989) Molecular cloning of the high affinity calcium-binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 264:21522-21528. Medline
11. Fransson S, Ruusala A, Aspenström P (2006) The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem Biophys Res Commun 344:500-510. CrossRef Medline
12. Gulledge AT, Kampa BM, Stuart GJ (2005) Synaptic integration in dendritic trees. J Neurobiol 64:75-90. CrossRef Medline
13. Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, Schoenfield M, Marin L, Charlton MP, Atwood HL, Zinsmaier KE (2005) The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47:379-393. CrossRef Medline
14. Hatanaka Y, Hisanaga S, Heizmann CW, Murakami F (2004) Distinct migratory behavior of early-and late-born neurons derived from the cortical ventricular zone. J Comp Neurol 479:1-14. CrossRef Medline
15. Horton AC, Rácz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48:757-771. CrossRef Medline
16. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, Masuda K, Otera H, Nakanishi Y, Nonaka I, Goto Y, Taguchi N, Morinaga H, Maeda M, Takayanagi R, Yokota S, Mihara K (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11:958-966. CrossRef Medline
17. Jan YN, Jan LY (2010) Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 11:316-328. CrossRef Medline
18. Kanegae Y, Lee G, Sato Y, Tanaka M, Nakai M, Sakaki T, Sugano S, Saito I (1995) Efficient gene activation in mammalian cells by using recombinant adenovirus expressing site-specific Cre recombinase. Nucleic Acids Res 23:3816-3821. CrossRef Medline
19. Kennedy KA, Sandiford SD, Skerjanc IS, Li SS (2012) Reactive oxygen species and the neuronal fate. Cell Mol Life Sci 69:215-221. CrossRef Medline
20. Konur S, Ghosh A (2005) Calcium signaling and the control of dendritic development. Neuron 46:401-405. CrossRef Medline
21. Kulkarni VA, Firestein BL (2012) The dendritic tree and brain disorders. Mol Cell Neurosci 50:10-20. CrossRef Medline
22. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51:283-290. CrossRef Medline
23. Li Z, Okamoto K, Hayashi Y, Sheng M (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119:873-887. CrossRef Medline
24. MacAskill AF, Brickley K, Stephenson FA, Kittler JT (2009) GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol Cell Neurosci 40:301-312. CrossRef Medline
25. Matsuda T, Cepko CL (2007) Controlled expression of transgenes introduced by in vivo electroporation. Proc Natl Acad Sci U S A 104:1027-1032. CrossRef Medline
26. Miller M (1981) Maturation of rat visual cortex. I. A quantitative study of Golgi-impregnated pyramidal neurons. J Neurocytol 10:859-878. CrossRef Medline
27. Misgeld T, Kerschensteiner M, Bareyre FM, Burgess RW, Lichtman JW (2007) Imaging axonal transport of mitochondria in vivo. Nat Methods 4:559-561. CrossRef Medline
28. Morris RL, Hollenbeck PJ (1993) The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J Cell Sci 104:917-927. Medline
29. Munro S, Pelham HR (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48:899-907. CrossRef Medline
30. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108:193-199. CrossRef Medline
31. Reers M, Smith TW, Chen LB (1991) J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30:4480-4486. CrossRef Medline
32. Rizzuto R, Brini M, Pizzo P, Murgia M, Pozzan T (1995) Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr Biol 5:635-642. CrossRef Medline
33. Rizzuto R, De Stefani D, Raffaello A, MammucariC (2012) Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 13: 566-578. CrossRef Medline
34. Santel A, Fuller MT (2001) Control of mitochondrial morphology by a human mitofusin. J Cell Sci 114:867-874. Medline
35. 2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc Natl Acad SciU S A 105:20728-20733. CrossRef Medline
36. Satoh D, Sato D, Tsuyama T, Saito M, Ohkura H, Rolls MM, Ishikawa F, Uemura T (2008) Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat Cell Biol 10: 1164-1171. CrossRef Medline
37. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22:1567-1572. CrossRef Medline
38. Sheng ZH, Cai Q (2012) Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat Rev Neurosci 13:77-93. CrossRef Medline
39. Smirnova E, Griparic L, Shurland DL, van der Bliek AM (2001) Dynaminrelated protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell 12:2245-2256. CrossRef Medline
40. Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9:206-221. CrossRef Medline
41. van Spronsen M, Mikhaylova M, Lipka J, Schlager MA, van den Heuvel DJ, Kuijpers M, Wulf PS, Keijzer N, Demmers J, Kapitein LC, Jaarsma D, Gerritsen HC, Akhmanova A, Hoogenraad CC (2013) TRAK/Milton motor-adaptor proteins steer mitochondrial trafficking to axons and dendrites. Neuron 77:485-502. CrossRef Medline
42. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, Bellen HJ (2005) Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47:365-378. CrossRef Medline
43. Vonderheit A, Helenius A (2005) Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3:e233. CrossRef Medline
44. Wang X, Zhu S, Drozda M, Zhang W, Stavrovskaya IG, Cattaneo E, Ferrante RJ, Kristal BS, Friedlander RM (2003) Minocycline inhibits caspaseindependent and-dependent mitochondrial cell death pathways in models of Huntington's disease. Proc Natl Acad Sci U S A 100:10483-10487. CrossRef Medline
45. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW (2006) Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9:1234-1236. CrossRef Medline
46. Wong RO, Ghosh A (2002) Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3:803-812. CrossRef Medline
47. Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130:717-729. CrossRef Medline
48. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47-59. CrossRef Medline
49. Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, Younger SH, Zimmerman S, Jan LY, Jan YN (2008) Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat Cell Biol 10:1172-1180. CrossRef Medline
50. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu DC, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417: 74-78. CrossRef Medline