Drp1-mediated mitochondrial dynamics and survival of developing chick motoneurons during the period of normal programmed cell death

FASEB Journal

Volumn 27, Issue 1, 2013, Pages 51-62

  Choi, So Yoen ^a   Kim, Joo Yeon ^a   Kim, Hyun Wook ^a   Cho, Bongki ^a   Cho, Hyo Min ^a   Oppenheim, Ronald W ^b   Kim, Hyun ^a   Rhyu, Im Joo ^a   Sun, Woong ^a  

^a Korea University College of Medicine   (South Korea)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Chick embryo; Mitochondria

Indexed keywords

ADENOSINE TRIPHOSPHATE; DYNAMIN I;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL POLARITY; CELL SURVIVAL; CELL VIABILITY; CHICK; ELECTROPORATION; EMBRYO; EMBRYO DEVELOPMENT; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC TRANSFECTION; IN VIVO STUDY; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; MOTONEURON; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL SURVIVAL; CHICK EMBRYO; DNA PRIMERS; DYNAMINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROSCOPY, ELECTRON, SCANNING; MITOCHONDRIA; MOTOR NEURONS; REAL-TIME POLYMERASE CHAIN REACTION; SPINAL CORD;

EID: 84871857529     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-211920     Document Type: Article

References (51)

1. DiMauro, S., and Schon, E. A. (2008) Mitochondrial disorders in the nervous system. Annu. Rev. Neurosci. 31, 91-123
2. Brenner, D., and Mak, T. W. (2009) Mitochondrial cell death effectors. Curr. Opin. Cell Biol. 21, 871-877
3. Wang, C., and Youle, R. J. (2009) The role of mitochondria in apoptosis. Annu. Rev. Genet. 43, 95-118
4. Praefcke, G. J., and McMahon, H. T. (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell. Biol. 5, 133-147 (Pubitemid 38160256)
5. Frank, S., Gaume, B., Bergmann-Leitner, E. S., Leitner, W. W., Robert, E. G., Catez, F., Smith, C. L., and Youle, R. J. (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525 (Pubitemid 33586103)
6. Karbowski, M., Lee, Y. J., Gaume, B., Jeong, S. Y., Frank, S., Nechushtan, A., Santel, A., Fuller, M., Smith, C. L., and Youle, R. J. (2002) Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 159, 931-938 (Pubitemid 36055748)
7. Parone, P. A., James, D. I., Da Cruz, S., Mattenberger, Y., Donze, O., Barja, F., and Martinou, J. C. (2006) Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol. Cell. Biol. 26, 7397-7408 (Pubitemid 44547692)
8. Goyal, G., Fell, B., Sarin, A., Youle, R. J., and Sriram, V. (2007) Role of mitochondrial remodeling in programmed cell death in Drosophila melanogaster. Dev. Cell 12, 807-816 (Pubitemid 46667740)
9. Jagasia, R., Grote, P., Westermann, B., and Conradt, B. (2005) DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death in C. elegans. Nature 433, 754-760 (Pubitemid 40292985)
10. Ishihara, N., Nomura, M., Jofuku, A., Kato, H., Suzuki, S. O., Masuda, K., Otera, H., Nakanishi, Y., Nonaka, I., Goto, Y., Taguchi, N., Morinaga, H., Maeda, M., Takayanagi, R., Yokota, S., and Mihara, K. (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell Biol. 11, 958-966
11. Wakabayashi, J., Zhang, Z., Wakabayashi, N., Tamura, Y., Fukaya, M., Kensler, T. W., Iijima, M., and Sesaki, H. (2009) The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J. Cell Biol. 186, 805-816
12. Buss, R. R., Sun, W., and Oppenheim, R. W. (2006) Adaptive roles of programmed cell death during nervous system development. Annu. Rev. Neurosci. 29, 1-35 (Pubitemid 44476838)
13. Hamburger, V. (1992) The stage series of the chick embryo. Dev. Dyn. 195, 273-275
14. Sun, W., Gould, T. W., Newbern, J., Milligan, C., Choi, S. Y., Kim, H., and Oppenheim, R. W. (2005) Phosphorylation of c-Jun in avian and mammalian motoneurons in vivo during programmed cell death: an early reversible event in the apoptotic cascade. J. Neurosci. 25, 5595-5603 (Pubitemid 40800651)
15. Caldero, J., Prevette, D., Mei, X., Oakley, R. A., Li, L., Milligan, C., Houenou, L., Burek, M., and Oppenheim, R. W. (1998) Peripheral target regulation of the development and survival of spinal sensory and motor neurons in the chick embryo. J. Neurosci. 18, 356-370 (Pubitemid 28046794)
16. Wang, G., and Scott, S. A. (2000) The "waiting period" of sensory and motor axons in early chick hindlimb: its role in axon pathfinding and neuronal maturation. J. Neurosci. 20, 5358-5366 (Pubitemid 30457733)
17. Fiala, J. C. (2005) Reconstruct: a free editor for serial section microscopy. J. Microsc. 218, 52-61
18. Chang, K. T., Niescier, R. F., and Min, K. T. (2011) Mitochondrial matrix Ca2+ as an intrinsic signal regulating mitochondrial motility in axons. Proc. Natl. Acad. Sci. U. S. A. 108, 15456-15461
19. Karbowski, M., Jeong, S. Y., and Youle, R. J. (2004) Endophilin B1 is required for the maintenance of mitochondrial morphology. J. Cell Biol. 166, 1027-1039 (Pubitemid 39304766)
20. Choi, S. Y., Kim, D. K., Eun, B., Kim, K., Sun, W., and Kim, H. (2006) Anti-apoptotic function of thymosin-beta in developing chick spinal motoneurons. Biochem. Biophys. Res. Commun. 346, 872-878
21. Santel, A., Frank, S., Gaume, B., Herrler, M., Youle, R. J., and Fuller, M. T. (2003) Mitofusin-1 protein is a generally expressed mediator of mitochondrial fusion in mammalian cells. J. Cell Sci. 116, 2763-2774 (Pubitemid 36857227)
22. Smirnova, E., Shurland, D. L., Ryazantsev, S. N., and van der Bliek, A. M. (1998) A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143, 351-358 (Pubitemid 28487855)
23. McKay, S. E., and Oppenheim, R. W. (1991) Lack of evidence for cell death among avian spinal cord interneurons during normal development and following removal of targets and afferents. J. Neurobiol. 22, 721-733
24. Pilar, G., Landmesser, L., and Burstein, L. (1980) Competition for survival among developing ciliary ganglion cells. J. Neurophysiol. 43, 233-254 (Pubitemid 10187651)
25. Pittman, R. H., and Oppenheim, R. W. (1978) Neuromuscular blockade increases motoneurone survival during normal cell death in the chick embryo. Nature 271, 364-366 (Pubitemid 8260855)
26. Verburg, J., and Hollenbeck, P. J. (2008) Mitochondrial membrane potential in axons increases with local nerve growth factor or semaphorin signaling. J. Neurosci. 28, 8306-8315
27. Lindahl, P. E., and Oberg, K. E. (1961) The effect of rotenone on respiration and its point of attack. Exp. Cell Res. 23, 228-237
28. Tada-Oikawa, S., Hiraku, Y., Kawanishi, M., and Kawanishi, S. (2003) Mechanism for generation of hydrogen peroxide and change of mitochondrial membrane potential during rotenone-induced apoptosis. Life Sci. 73, 3277-3288 (Pubitemid 37237579)
29. De Graaf, A. O., van den Heuvel, L. P., Dijkman, H. B., de Abreu, R. A., Birkenkamp, K. U., de Witte, T., van der Reijden, B. A., Smeitink, J. A., and Jansen, J. H. (2004) Bcl-2 prevents loss of mitochondria in CCCP-induced apoptosis. Exp. Cell Res. 299, 533-540 (Pubitemid 39179817)
30. Martin, J., Mahlke, K., and Pfanner, N. (1991) Role of an energized inner membrane in mitochondrial protein import. Delta psi drives the movement of presequences. J. Biol. Chem. 266, 18051-18057 (Pubitemid 21908046)
31. Wyss, M., and Kaddurah-Daouk, R. (2000) Creatine and creatinine metabolism. Physiol. Rev. 80, 1107-1213 (Pubitemid 30452013)
32. Beard, E., and Braissant, O. (2010) Synthesis and transport of creatine in the CNS: importance for cerebral functions. J. Neurochem. 115, 297-313
33. Steiber, A., Kerner, J., and Hoppel, C. L. (2004) Carnitine: a nutritional, biosynthetic, and functional perspective. Mol. Aspects Med. 25, 455-473 (Pubitemid 39195071)
34. He, M. D., Xu, S. C., Lu, Y. H., Li, L., Zhong, M., Zhang, Y. W., Wang, Y., Li, M., Yang, J., Zhang, G. B., Yu, Z. P., and Zhou, Z. (2011) L-carnitine protects against nickel-induced neurotoxicity by maintaining mitochondrial function in Neuro-2a cells. Toxicol. Appl. Pharmacol. 253, 38-44
35. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T., and Mihara, K. (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282, 11521-11529 (Pubitemid 47100787)
36. Chen, H., Chomyn, A., and Chan, D. C. (2005) Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280, 26185-26192 (Pubitemid 41022214)
37. Park, K. S., Wiederkehr, A., Kirkpatrick, C., Mattenberger, Y., Martinou, J. C., Marchetti, P., Demaurex, N., and Wollheim, C. B. (2008) Selective actions of mitochondrial fission/fusion genes on metabolism-secretion coupling in insulin-releasing cells. J. Biol. Chem. 283, 33347-33356
38. Li, Z., Okamoto, K., Hayashi, Y., and Sheng, M. (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873-887 (Pubitemid 40017692)
39. Grohm, J., Kim, S. W., Mamrak, U., Tobaben, S., Cassidy-Stone, A., Nunnari, J., Plesnila, N., and Culmsee, C. (2012) Inhibition of Drp1 provides neuroprotection in vitro and in vivo. Cell Death Differ. 19, 1446-1458
40. Song, W., Chen, J., Petrilli, A., Liot, G., Klinglmayr, E., Zhou, Y., Poquiz, P., Tjong, J., Pouladi, M. A., Hayden, M. R., Masliah, E., Ellisman, M., Rouiller, I., Schwarzenbacher, R., Bossy, B., Perkins, G., and Bossy-Wetzel, E. (2011) Mutant huntingtin binds the mitochondrial fission GTPase dynamin-related protein-1 and increases its enzymatic activity. Nat. Med. 17, 377-382
41. Hollyday, M., and Hamburger, V. (1976) Reduction of the naturally occurring motor neuron loss by enlargement of the periphery. J. Comp. Neurol. 170, 311-320
42. D'Costa, A. P., Prevette, D. M., Houenou, L. J., Wang, S., Zackenfels, K., Rohrer, H., Zapf, J., Caroni, P., and Oppenheim, R. W. (1998) Mechanisms of insulin-like growth factor regulation of programmed cell death of developing avian motoneurons. J. Neurobiol. 36, 379-394 (Pubitemid 28397148)
43. Parone, P. A., Da Cruz, S., Tondera, D., Mattenberger, Y., James, D. I., Maechler, P., Barja, F., and Martinou, J. C. (2008) Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS One 3, e3257
44. Baixauli, F., Martin-Cofreces, N. B., Morlino, G., Carrasco, Y. R., Calabia-Linares, C., Veiga, E., Serrador, J. M., and Sanchez- Madrid, F. (2011) The mitochondrial fission factor dynamin-related protein 1 modulates T-cell receptor signalling at the immune synapse. EMBO J. 30, 1238-1250
45. Cheng, A., Hou, Y., and Mattson, M. P. (2010) Mitochondria and neuroplasticity. ASN Neuro. 2, e00045
46. Morris, R. L., and Hollenbeck, P. J. (1993) The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J. Cell Sci. 104, 917-927 (Pubitemid 23123484)
47. Dickey, A. S., and Strack, S. (2011) PKA/AKAP1 and PP2A/Bbeta2 regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics. J. Neurosci. 31, 15716-15726
48. Lee, C. W., and Peng, H. B. (2008) The function of mitochondria in presynaptic development at the neuromuscular junction. Mol. Biol. Cell 19, 150-158
49. Chada, S. R., and Hollenbeck, P. J. (2003) Mitochondrial movement and positioning in axons: the role of growth factor signaling. J. Exp. Biol. 206, 1985-1992 (Pubitemid 36761801)
50. Verstreken, P., Ly, C. V., Venken, K. J., Koh, T. W., Zhou, Y., and Bellen, H. J. (2005) Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47, 365-378 (Pubitemid 41073878)
51. Miller, K. E., and Sheetz, M. P. (2004) Axonal mitochondrial transport and potential are correlated. J. Cell Sci. 117, 2791-2804 (Pubitemid 38997261)