Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Mitochondrial Fission: Regulation and ER Connection

  • Lee, Hakjoo (Department of Physiology, Medical College of Georgia, Georgia Regents University) ;
  • Yoon, Yisang (Department of Physiology, Medical College of Georgia, Georgia Regents University)
  • Received : 2013.11.07
  • Accepted : 2014.11.10
  • Published : 2014.02.28
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Abstract

Fission and fusion of mitochondrial tubules are the main processes determining mitochondrial shape and size in cells. As more evidence is found for the involvement of mitochondrial morphology in human pathology, it is important to elucidate the mechanisms of mitochondrial fission and fusion. Mitochondrial morphology is highly sensitive to changing environmental conditions, indicating the involvement of cellular signaling pathways. In addition, the well-established structural connection between the endoplasmic reticulum (ER) and mitochondria has recently been found to play a role in mitochondrial fission. This minireview describes the latest advancements in understanding the regulatory mechanisms controlling mitochondrial morphology, as well as the ER-mediated structural maintenance of mitochondria, with a specific emphasis on mitochondrial fission.

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References

  1. Ban, T., Heymann, J.A., Song, Z., Hinshaw, J.E., and Chan, D.C. (2010). OPA1 disease alleles causing dominant optic atrophy have defects in cardiolipin-stimulated GTP hydrolysis and membrane tubulation. Hum. Mol. Genet. 19, 2113-2122. https://doi.org/10.1093/hmg/ddq088
  2. Ban-Ishihara, R., Ishihara, T., Sasaki, N., Mihara, K., and Ishihara, N. (2013). Dynamics of nucleoid structure regulated by mitochondrial fission contributes to cristae reformation and release of cytochrome c. Proc. Natl. Acad. Sci. USA 110, 11863-11868. https://doi.org/10.1073/pnas.1301951110
  3. Boldogh, I.R., Nowakowski, D.W., Yang, H.C., Chung, H., Karmon, S., Royes, P., and Pon, L.A. (2003). A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery. Mol. Biol. Cell 14, 4618-4627. https://doi.org/10.1091/mbc.E03-04-0225
  4. Burgess, S.M., Delannoy, M., and Jensen, R.E. (1994). MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J. Cell Biol. 126, 1375-1391. https://doi.org/10.1083/jcb.126.6.1375
  5. Cai, Q., and Sheng, Z.H. (2009). Moving or stopping mitochondria: Miro as a traffic cop by sensing calcium. Neuron 61, 493-496. https://doi.org/10.1016/j.neuron.2009.02.003
  6. Cereghetti, G.M., Stangherlin, A., Martins de Brito, O., Chang, C.R., Blackstone, C., Bernardi, P., and Scorrano, L. (2008). Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl. Acad. Sci. USA 105, 15803-15808. https://doi.org/10.1073/pnas.0808249105
  7. Chang, C.R., and Blackstone, C. (2007). Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 282, 21583-21587. https://doi.org/10.1074/jbc.C700083200
  8. Cho, D.H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z., and Lipton, S.A. (2009). S-nitrosylation of Drp1 mediates betaamyloid-related mitochondrial fission and neuronal injury. Science 324, 102-105. https://doi.org/10.1126/science.1171091
  9. Cribbs, J.T., and Strack, S. (2007). Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8, 939-944. https://doi.org/10.1038/sj.embor.7401062
  10. Csordas, G., Renken, C., Varnai, P., Walter, L., Weaver, D., Buttle, K.F., Balla, T., Mannella, C.A., and Hajnoczky, G. (2006). Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915-921. https://doi.org/10.1083/jcb.200604016
  11. de Brito, O.M., and Scorrano, L. (2008). Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610. https://doi.org/10.1038/nature07534
  12. Dickey, A.S., and Strack, S. (2011). PKA/AKAP1 and PP2A/$B{\beta}2$ regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics. J. Neurosci. 31, 15716-15726. https://doi.org/10.1523/JNEUROSCI.3159-11.2011
  13. Flinner, N., Ellenrieder, L., Stiller, S.B., Becker, T., Schleiff, E., and Mirus, O. (2013). Mdm10 is an ancient eukaryotic porin co-occurring with the ERMES complex. Biochim. Biophys. Acta 1833, 3314-3325. https://doi.org/10.1016/j.bbamcr.2013.10.006
  14. Friedman, J.R., Lackner, L.L., West, M., DiBenedetto, J.R., Nunnari, J., and Voeltz, G.K. (2011). ER tubules mark sites of mitochondrial division. Science 334, 358-362. https://doi.org/10.1126/science.1207385
  15. Gawlowski, T., Suarez, J., Scott, B., Torres-Gonzalez, M., Wang, H., Schwappacher, R., Han, X., Yates, J.R., 3rd, Hoshijima, M., and Dillmann, W. (2012). Modulation of dynamin-related protein 1 (DRP1) function by increased O-linked-beta-N-acetylglucosamine modification (O-GlcNAc) in cardiac myocytes. J. Biol. Chem. 287, 30024-30034. https://doi.org/10.1074/jbc.M112.390682
  16. Gomes, L.C., Di Benedetto, G., and Scorrano, L. (2011). During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 13, 589-598. https://doi.org/10.1038/ncb2220
  17. Griffin, E.E., Graumann, J., and Chan, D.C. (2005). The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J. Cell Biol. 170, 237-248. https://doi.org/10.1083/jcb.200503148
  18. Guo, C., Hildick, K.L., Luo, J., Dearden, L., Wilkinson, K.A., and Henley, J.M. (2013). SENP3-mediated deSUMOylation of dynaminrelated protein 1 promotes cell death following ischaemia. EMBO J. 32, 1514-1528. https://doi.org/10.1038/emboj.2013.65
  19. Han, X.J., Lu, Y.F., Li, S.A., Kaitsuka, T., Sato, Y., Tomizawa, K., Nairn, A.C., Takei, K., Matsui, H., and Matsushita, M. (2008). CaM kinase $I{\alpha}$-induced phosphorylation of Drp1 regulates mitochondrial morphology. J. Cell Biol. 182, 573-585. https://doi.org/10.1083/jcb.200802164
  20. Hanekamp, T., Thorsness, M.K., Rebbapragada, I., Fisher, E.M., Seebart, C., Darland, M.R., Coxbill, J.A., Updike, D.L., and Thorsness, P.E. (2002). Maintenance of mitochondrial morphology is linked to maintenance of the mitochondrial genome in Saccharomyces cerevisiae. Genetics 162, 1147-1156.
  21. Helle, S.C., Kanfer, G., Kolar, K., Lang, A., Michel, A.H., and Kornmann, B. (2013). Organization and function of membrane contact sites. Biochim. Biophys. Acta 1833, 2526-2541. https://doi.org/10.1016/j.bbamcr.2013.01.028
  22. Hinshaw, J.E. (2000). Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16, 483-519. https://doi.org/10.1146/annurev.cellbio.16.1.483
  23. Hobbs, A.E., Srinivasan, M., McCaffery, J.M., and Jensen, R.E. (2001). Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J. Cell Biol. 152, 401-410. https://doi.org/10.1083/jcb.152.2.401
  24. Horn, S.R., Thomenius, M.J., Johnson, E.S., Freel, C.D., Wu, J.Q., Coloff, J.L., Yang, C.S., Tang, W., An, J., Ilkayeva, O.R., et al. (2011). Regulation of mitochondrial morphology by APC/CCdh1-mediated control of Drp1 stability. Mol. Biol. Cell 22, 1207-1216. https://doi.org/10.1091/mbc.E10-07-0567
  25. Iwasawa, R., Mahul-Mellier, A.L., Datler, C., Pazarentzos, E., and Grimm, S. (2011). Fis1 and Bap31 bridge the mitochondria-ER interface to establish a platform for apoptosis induction. EMBO J. 30, 556-568. https://doi.org/10.1038/emboj.2010.346
  26. Karbowski, M., Neutzner, A., and Youle, R.J. (2007). The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 178, 71-84. https://doi.org/10.1083/jcb.200611064
  27. Kashatus, D.F., Lim, K.H., Brady, D.C., Pershing, N.L., Cox, A.D., and Counter, C.M. (2011). RALA and RALBP1 regulate mitochondrial fission at mitosis. Nat. Cell Biol. 13, 1108-1115. https://doi.org/10.1038/ncb2310
  28. Kim, H., Scimia, M.C., Wilkinson, D., Trelles, R.D., Wood, M.R., Bowtell, D., Dillin, A., Mercola, M., and Ronai, Z.A. (2011). Finetuning of Drp1/Fis1 availability by AKAP121/Siah2 regulates mitochondrial adaptation to hypoxia. Mol. Cell 44, 532-544. https://doi.org/10.1016/j.molcel.2011.08.045
  29. Kornmann, B., Currie, E., Collins, S.R., Schuldiner, M., Nunnari, J., Weissman, J.S., and Walter, P. (2009). An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481. https://doi.org/10.1126/science.1175088
  30. Kornmann, B., Osman, C., and Walter, P. (2011). The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections. Proc. Natl. Acad. Sci. USA 108, 14151-14156. https://doi.org/10.1073/pnas.1111314108
  31. Korobova, F., Ramabhadran, V., and Higgs, H.N. (2013). An actindependent step in mitochondrial fission mediated by the ERassociated formin INF2. Science 339, 464-467. https://doi.org/10.1126/science.1228360
  32. Loson, O.C., Song, Z., Chen, H., and Chan, D.C. (2013). Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 24, 659-667. https://doi.org/10.1091/mbc.E12-10-0721
  33. Macaskill, A.F., Rinholm, J.E., Twelvetrees, A.E., Arancibia-Carcamo, I.L., Muir, J., Fransson, A., Aspenstrom, P., Attwell, D., and Kittler, J.T. (2009). Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61, 541-555. https://doi.org/10.1016/j.neuron.2009.01.030
  34. McNiven, M.A., Cao, H., Pitts, K.R., and Yoon, Y. (2000). The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem. Sci. 25, 115-120. https://doi.org/10.1016/S0968-0004(99)01538-8
  35. Mears, J.A., Lackner, L.L., Fang, S., Ingerman, E., Nunnari, J., and Hinshaw, J.E. (2011). Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat. Struct. Mol. Biol. 18, 20-26. https://doi.org/10.1038/nsmb.1949
  36. Meeusen, S., and Nunnari, J. (2003). Evidence for a two membranespanning autonomous mitochondrial DNA replisome. J. Cell Biol. 163, 503-510. https://doi.org/10.1083/jcb.200304040
  37. Merrill, R.A., Dagda, R.K., Dickey, A.S., Cribbs, J.T., Green, S.H., Usachev, Y.M., and Strack, S. (2011). Mechanism of neuroprotective mitochondrial remodeling by PKA/AKAP1. PLoS Biol. 9, e1000612. https://doi.org/10.1371/journal.pbio.1000612
  38. Murley, A., Lackner, L.L., Osman, C., West, M., Voeltz, G.K., Walter, P., and Nunnari, J. (2013). ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. eLife 2, e00422.
  39. Nakamura, N., Kimura, Y., Tokuda, M., Honda, S., and Hirose, S. (2006). MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 7, 1019-1022. https://doi.org/10.1038/sj.embor.7400790
  40. Otera, H., Wang, C., Cleland, M.M., Setoguchi, K., Yokota, S., Youle, R.J., and Mihara, K. (2010). Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 191, 1141-1158. https://doi.org/10.1083/jcb.201007152
  41. Palmer, C.S., Osellame, L.D., Laine, D., Koutsopoulos, O.S., Frazier, A.E., and Ryan, M.T. (2011). MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 12, 565-573. https://doi.org/10.1038/embor.2011.54
  42. Palmer, C.S., Elgass, K.D., Parton, R.G., Osellame, L.D., Stojanovski, D., and Ryan, M.T. (2013). Adaptor proteins MiD49 and MiD51 can act independently of Mff and Fis1 in Drp1 recruitment and are specific for mitochondrial fission. J. Biol. Chem. 288, 27584-27593. https://doi.org/10.1074/jbc.M113.479873
  43. Qi, X., Disatnik, M.H., Shen, N., Sobel, R.A., and Mochly-Rosen, D. (2011). Aberrant mitochondrial fission in neurons induced by protein kinase $C{\delta}$ under oxidative stress conditions in vivo. Mol. Biol. Cell 22, 256-265. https://doi.org/10.1091/mbc.E10-06-0551
  44. Raturi, A., and Simmen, T. (2013). Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochim. Biophys. Acta 1833, 213-224. https://doi.org/10.1016/j.bbamcr.2012.04.013
  45. Slupe, A.M., Merrill, R.A., Flippo, K.H., Lobas, M.A., Houtman, J.C., and Strack, S. (2013). A calcineurin docking motif (LXVP) in dynamin- related protein 1 contributes to mitochondrial fragmentation and ischemic neuronal injury. J. Biol. Chem. 288, 12353-12365. https://doi.org/10.1074/jbc.M113.459677
  46. Smirnova, E., Griparic, L., Shurland, D.L., and van der Bliek, A.M. (2001). Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245-2256. https://doi.org/10.1091/mbc.12.8.2245
  47. Sogo, L.F., and Yaffe, M.P. (1994). Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. J. Cell Biol. 126, 1361-1373. https://doi.org/10.1083/jcb.126.6.1361
  48. Strack, S., Wilson, T.J., and Cribbs, J.T. (2013). Cyclin-dependent kinases regulate splice-specific targeting of dynamin-related protein 1 to microtubules. J. Cell Biol. 201, 1037-1051. https://doi.org/10.1083/jcb.201210045
  49. Stavru, F., Bouillaud, F., Sartori, A., Ricquier, D., and Cossart, P. (2011). Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc. Natl. Acad. Sci. USA 108, 3612-3617. https://doi.org/10.1073/pnas.1100126108
  50. Stavru, F., Palmer, A.E., Wang, C., Youle, R.J., and Cossart, P. (2013). Atypical mitochondrial fission upon bacterial infection. Proc. Natl. Acad. Sci. USA 110, 16003-16008. https://doi.org/10.1073/pnas.1315784110
  51. Sugiura, A., Nagashima, S., Tokuyama, T., Amo, T., Matsuki, Y., Ishido, S., Kudo, Y., McBride, H.M., Fukuda, T., Matsushita, N., et al. (2013). MITOL regulates endoplasmic reticulum-mitochondria contacts via Mitofusin2. Mol. Cell 51, 20-34. https://doi.org/10.1016/j.molcel.2013.04.023
  52. Szabadkai, G., Bianchi, K., Varnai, P., De Stefani, D., Wieckowski, M.R., Cavagna, D., Nagy, A.I., Balla, T., and Rizzuto, R. (2006). Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial $Ca^{2+}$ channels. J. Cell Biol. 175, 901-911. https://doi.org/10.1083/jcb.200608073
  53. 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. https://doi.org/10.1074/jbc.M607279200
  54. Tieu, Q., Okreglak, V., Naylor, K., and Nunnari, J. (2002). The WD repeat protein, Mdv1p, functions as a molecular adaptor by interacting with Dnm1p and Fis1p during mitochondrial fission. J. Cell Biol. 158, 445-452. https://doi.org/10.1083/jcb.200205031
  55. Wang, X., and Schwarz, T.L. (2009). The mechanism of $Ca^{2+}$ -dependent regulation of kinesin-mediated mitochondrial motility. Cell 136, 163-174. https://doi.org/10.1016/j.cell.2008.11.046
  56. Wang, J.X., Jiao, J.Q., Li, Q., Long, B., Wang, K., Liu, J.P., Li, Y.R., and Li, P.F. (2011). miR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1. Nat. Med. 17, 71-78. https://doi.org/10.1038/nm.2282
  57. Wang, W., Wang, Y., Long, J., Wang, J., Haudek, S.B., Overbeek, P., Chang, B.H., Schumacker, P.T., and Danesh, F.R. (2012a). Mitochondrial fission triggered by hyperglycemia is mediated by ROCK1 activation in podocytes and endothelial cells. Cell Metabol. 15, 186-200. https://doi.org/10.1016/j.cmet.2012.01.009
  58. Wang, Z., Jiang, H., Chen, S., Du, F., and Wang, X. (2012b). The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 148, 228-243. https://doi.org/10.1016/j.cell.2011.11.030
  59. Wasiak, S., Zunino, R., and McBride, H.M. (2007). Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177, 439-450. https://doi.org/10.1083/jcb.200610042
  60. Yonashiro, R., Ishido, S., Kyo, S., Fukuda, T., Goto, E., Matsuki, Y., Ohmura-Hoshino, M., Sada, K., Hotta, H., Yamamura, H., et al. (2006). A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J. 25, 3618-3626. https://doi.org/10.1038/sj.emboj.7601249
  61. Yoon, Y., Pitts, K.R., and McNiven, M.A. (2001). Mammalian dynamin- like protein DLP1 tubulates membranes. Mol. Biol. Cell 12, 2894-2905. https://doi.org/10.1091/mbc.12.9.2894
  62. Youngman, M.J., Hobbs, A.E., Burgess, S.M., Srinivasan, M., and Jensen, R.E. (2004). Mmm2p, a mitochondrial outer membrane protein required for yeast mitochondrial shape and maintenance of mtDNA nucleoids. J. Cell Biol. 164, 677-688. https://doi.org/10.1083/jcb.200308012
  63. Yu, T., Jhun, B.S., and Yoon, Y. (2011). High-glucose stimulation increases reactive oxygen species production through the calcium and mitogen-activated protein kinase-mediated activation of mitochondrial fission. Antioxid. Redox Signal. 14, 425-437. https://doi.org/10.1089/ars.2010.3284
  64. Zhao, J., Liu, T., Jin, S., Wang, X., Qu, M., Uhlen, P., Tomilin, N., Shupliakov, O., Lendahl, U., and Nister, M. (2011). Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 30, 2762-2778. https://doi.org/10.1038/emboj.2011.198

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