Dynamin-related protein 1 (Drp1) mediating mitophagy contributes to the pathophysiology of nervous system diseases and brain injury

Histology and Histopathology

Volumn 32, Issue 6, 2017, Pages 551-559

  Wu, Qiong ^a   Luo, Cheng Liang ^a   Tao, Lu Yang ^a  

^a MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

Author keywords

Brain injury; Drp1; Mitochondria; Mitochondrial dynamic; Mitophagy; Nervous system diseases

Indexed keywords

DNM1L PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL PROTEIN;

ANIMAL; AUTOPHAGY; BRAIN INJURY; DEGENERATIVE DISEASE; HUMAN; METABOLISM; MITOPHAGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; BRAIN INJURIES; GTP PHOSPHOHYDROLASES; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL PROTEINS; NEURODEGENERATIVE DISEASES;

EID: 85015190484     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: 10.14670/HH-11-841     Document Type: Review

References (90)

1. Anesti V. and Scorrano L. (2006). The relationship between mitochondrial shape and function and the cytoskeleton. Biochem. Biophys. Acta 1757, 692-699.
2. Bayrhuber M., Meins T., Habeck M., Becker S., Giller K., Villinger S., Vonrhein C., Griesinger C., Zweckstetter M. and Zeth K. (2008). Structure of the human voltage-dependent anion channel. Proc. Natl. Acad. Sci. USA 105, 15370-15375.
3. Bratic A. and Larsson N.G. (2013). The role of mitochondria in aging. J. Clin. Invest. 123, 951-957.
4. Cereghetti G.M., Stangherlin A., Martins D.B.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.
5. Chan D.C. (2006). Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol. 22: 79-99.
6. Chan N.C., Salazar A.M., Pham A.H., Sweredoski M.J., Kolawa N.J., Graham R.L., Hess S. and Chan D.C. (2011). Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum. Mol. Genet. 20, 1726-1737.
7. Chang C.R., Manlandro C.M., Arnoult D., Stadler J., Posey A.E., Hill R.B. and Blackstone C. (2010). A lethal de novo mutation in the middle domain of the dynamin-related GTPase Drp1 impairs higher order assembly and mitochondrial division. J. Biol. Chem. 285, 32494-32503.
8. 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.
9. Chang C.R. and Blackstone C. (2010). Dynamic regulation of mitochondrial fission through modification of the dynamin-related protein Drp1. Ann. N. Y. Acad. Sci. 1201, 34-39.
10. Chen Y. and Dorn G.N. (2013). PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 340, 471-475.
11. Chen S.D., Lin T.K., Yang D.I., Lee S.Y., Shaw F.Z., Liou C.W. and Chuang Y.C. (2015). Roles of PTEN-induced putative kinase 1 and dynamin-related protein 1 in transient global ischemia-induced hippocampal neuronal injury. Biochem. Biophys. Res. Commun. 460, 397-403.
12. Corsetti V., Florenzano F., Atlante A., Bobba A., Ciotti M.T., Natale F., Della V.F., Borreca A., Manca A., Meli G., Ferraina C., Feligioni M., D'Aguanno S., Bussani R., Ammassari-Teule M., Nicolin V., Calissano P. and Amadoro G. (2015). NH2-truncated human tau induces deregulated mitophagy in neurons by aberrant recruitment of Parkin and UCHL-1: implications in Alzheimer's disease. Hum. Mol. Genet. 24, 3058-3081.
13. 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.
14. De Vos K.J., Sable J., Miller K.E. and Sheetz M.P. (2003). Expression of phosphatidylinositol (4,5) bisphosphate-specific pleckstrin homology domains alters direction but not the level of axonal transport of mitochondria. Mol. Biol. Cell. 14, 3636-3649.
15. Detmer S.A. and Chan D.C. (2007). Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8, 870-879.
16. Ding W.X., Li M., Chen X., Ni H.M., Lin C.W., Gao W., Lu B., Stolz D.B., Clemens D.L. and Yin X.M. (2010). Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice. Gastroenterology. 139, 1740-1752.
17. Ding W.X. and Yin X.M. (2012). Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol. Chem. 393, 547-564.
18. Elgass K., Pakay J., Ryan M.T. and Palmer C.S. (2013). Recent advances into the understanding of mitochondrial fission. Biochim. Biophys. Acta 1833, 150-161.
19. 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.
20. Friedman J.R. and Nunnari J. (2014). Mitochondrial form and function. Nature 505, 335-343.
21. Gegg M.E., Cooper J.M., Chau K.Y., Rojo M., Schapira A.H. and Taanman J.W. (2010). Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum. Mol. Genet. 19, 4861-4870.
22. Geisler S., Holmstrom K.M., Skujat D., Fiesel F.C., Rothfuss O.C., Kahle P.J. and Springer W. (2010). PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131.
23. Gray M.W., Lang B.F., Cedergren R., Golding G.B., Lemieux C., Sankoff D., Turmel M., Brossard N., Delage E., Littlejohn T.G., Plante I., Rioux P., Saint-Louis D., Zhu Y. and Burger G. (1998). Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res. 26, 865-878.
24. Han J.Y., Kang M.J., Kim K.H., Han P.L., Kim H.S., Ha J.Y. and Son J.H. (2015). Nitric oxide induction of Parkin translocation in PTEN-induced putative kinase 1 (PINK1) deficiency: functional role of neuronal nitric oxide synthase during mitophagy. J. Biol. Chem. 290, 10325-10335.
25. Hollenbeck P.J. and Saxton W.M. (2005). The axonal transport of mitochondria. J. Cell Sci. 118, 5411-5419.
26. Hoppins S., Lackner L. and Nunnari J. (2007). The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751-780.
27. Huang C., Andres A.M., Ratliff E.P., Hernandez G., Lee P. and Gottlieb R.A. (2011). Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS One. 6, e20975.
28. Iguchi M., Kujuro Y., Okatsu K., Koyano F., Kosako H., Kimura M., Suzuki N., Uchiyama S., Tanaka K. and Matsuda N. (2013). Parkin-catalyzed ubiquitin-ester transfer is triggered by PINK1-dependent phosphorylation. J. Biol. Chem. 288, 22019-22032.
29. Ikeda Y., Shirakabe A., Brady C., Zablocki D., Ohishi M. and Sadoshima J. (2015a). Molecular mechanisms mediating mitochondrial dynamics and mitophagy and their functional roles in the cardiovascular system. J. Mol. Cell. Cardiol. 78, 116-122.
30. Ikeda Y., Shirakabe A., Maejima Y., Zhai P., Sciarretta S., Toli J., Nomura M., Mihara K., Egashira K., Ohishi M., Abdellatif M. and Sadoshima J. (2015b). Endogenous Drp1 mediates mitochondrial autophagy and protects the heart against energy stress. Circ. Res. 116, 264-278.
31. Itoh K., Nakamura K., Iijima M. and Sesaki H. (2013). Mitochondrial dynamics in neurodegeneration. Trends Cell Biol. 23, 64-71.
32. Jahani-Asl A., Huang E., Irrcher I., Rashidian J., Ishihara N., Lagace D.C., Slack R.S. and Park D.S. (2015). CDK5 phosphorylates DRP1 and drives mitochondrial defects in NMDA-induced neuronal death. Hum. Mol. Genet. 24, 4573-4583.
33. Jin S.M., Lazarou M., Wang C., Kane L.A., Narendra D.P. and Youle R.J. (2010). Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 191, 933-942.
34. Kageyama Y., Hoshijima M., Seo K., Bedja D., Sysa-Shah P., Andrabi S.A., Chen W., Hoke A., Dawson V.L., Dawson T.M., Gabrielson K., Kass D.A., Iijima M. and Sesaki H. (2014). Parkin-independent mitophagy requires Drp1 and maintains the integrity of mammalian heart and brain. EMBO J. 33, 2798-2813.
35. Kane L. A., Lazarou M., Fogel A.I., Li Y., Yamano K., Sarraf S.A., Banerjee S. and Youle R.J. (2014). PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 205, 143-153.
36. 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.
37. Kasahara A. and Scorrano L. (2014). Mitochondria: from cell death executioners to regulators of cell differentiation. Trends Cell Biol. 24, 761-770.
38. Kawajiri S., Saiki S., Sato S., Sato F., Hatano T., Eguchi H. and Hattori N. (2010). PINK1 is recruited to mitochondria with parkin and associates with LC3 in mitophagy. FEBS Lett. 584, 1073-1079.
39. Kim I. and Lemasters J.J. (2011). Mitochondrial degradation by autophagy (mitophagy) in GFP-LC3 transgenic hepatocytes during nutrient deprivation. Am. J. Physiol. Cell Physiol. 300, C308-C317.
40. Kondapalli C., Kazlauskaite A., Zhang N., Woodroof H.I., Campbell D.G., Gourlay R., Burchell L., Walden H., Macartney T.J., Deak M., Knebel A., Alessi D.R. and Muqit M.M. (2012). PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol. 2, 120080.
41. Koyano F., Okatsu K., Kosako H., Tamura Y., Go E., Kimura M., Kimura Y., Tsuchiya H., Yoshihara H., Hirokawa T., Endo T., Fon E.A., Trempe J.F., Saeki Y., Tanaka K. and Matsuda N. (2014). Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 510, 162-166.
42. Kubli D.A., Ycaza J.E. and Gustafsson A.B. (2007). Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak. Biochem. J. 405, 407-415.
43. Kuhlbrandt W. (2015). Structure and function of mitochondrial membrane protein complexes. BMC Biol. 13, 89.
44. Lee Y., Lee H.Y., Hanna R.A. and Gustafsson A.B. (2011). Mitochondrial autophagy by Bnip3 involves Drp1-mediated mitochondrial fission and recruitment of Parkin in cardiac myocytes. Am. J. Physiol. Heart. Circ. Physiol. 301, H1924-H1931.
45. 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.
46. Lin J.R., Shen W.L., Yan C. and Gao P.J. (2015). Downregulation of dynamin-related protein 1 contributes to impaired autophagic flux and angiogenic function in senescent endothelial cells. Arterioscler. Thromb. Vasc. Biol. 35, 1413-1422.
47. Lionaki E., Markaki M. and Tavernarakis N. (2013). Autophagy and ageing: insights from invertebrate model organisms. Ageing Res. Rev. 12, 413-428.
48. Manley S., Williams J.A. and Ding W.X. (2013). Role of p62/SQSTM1 in liver physiology and pathogenesis. Exp. Biol. Med. (Maywood). 238,525-538.
49. Matsuda N., Sato S., Shiba K., Okatsu K., Saisho K., Gautier C.A., Sou Y.S., Saiki S., Kawajiri S., Sato F., Kimura M., Komatsu M., Hattori N. and Tanaka K. (2010). PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J. Cell Biol. 189, 211-221.
50. Narendra D.P., Jin S.M., Tanaka A., Suen D.F., Gautier C.A., Shen J., Cookson M.R. and Youle R.J. (2010). PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298.
51. Nogales E. (2000). Structural insights into microtubule function. Annu. Rev. Biochem. 69, 277-302.
52. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., Rogov V., Lohr F., Popovic D., Occhipinti A., Reichert A.S., Terzic J., Dotsch V., Ney P.A. and Dikic I. (2010). Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11, 45-51.
53. Nunnari J. and Suomalainen A. (2012). Mitochondria: in sickness and in health. Cell 148, 1145-1159.
54. Okamoto K. and Shaw J.M. (2005). Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 39, 503-536.
55. Ong S.B., Hall A.R. and Hausenloy D.J. (2013). Mitochondrial dynamics in cardiovascular health and disease. Antioxid. Redox. Signal. 19, 400-414.
56. Ordureau A., Sarraf S.A., Duda D.M., Heo J.M., Jedrychowski M.P., Sviderskiy V.O., Olszewski J.L., Koerber J.T., Xie T., Beausoleil S.A., Wells J.A., Gygi S.P., Schulman B.A. and Harper J.W. (2014). Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol. Cell. 56, 360-375.
57. Osellame L.D., Blacker T.S. and Duchen M.R. (2012). Cellular and molecular mechanisms of mitochondrial function. Best Pract. Res. Clin. Endocrinol. Metab. 26,711-723.
58. Otera H. and Mihara K. (2011). Molecular mechanisms and physiologic functions of mitochondrial dynamics. J. Biochem. 149, 241-251.
59. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D. and Levine B. (2005). Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939.
60. Poole A.C., Thomas R.E., Yu S., Vincow E.S. and Pallanck L. (2010). The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINK1/parkin pathway. PLoS One 5, e10054.
61. 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.
62. Quinsay M.N., Thomas R.L., Lee Y. and Gustafsson A.B. (2010). Bnip3-mediated mitochondrial autophagy is independent of the mitochondrial permeability transition pore. Autophagy 6, 855-862.
63. Reddy P.H., Reddy T.P., Manczak M., Calkins M. J., Shirendeb U. and Mao P. (2011). Dynamin-related protein 1 and mitochondrial fragmentation in neurodegenerative diseases. Brain Res. Rev. 67, 103-118.
64. Rintoul G.L., Filiano A.J., Brocard J.B., Kress G.J. and Reynolds I.J. (2003). Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J. Neurosci. 23, 7881-7888.
65. Saito T. and Sadoshima J. (2015). Molecular mechanisms of mitochondrial autophagy/mitophagy in the heart. Circ. Res. 116, 1477-1490.
66. Schapira A.H. (2012). Targeting mitochondria for neuroprotection in Parkinson's disease. Antioxid. Redox Signal. 16, 965-973.
67. Schiavi A. and Ventura N. (2014). The interplay between mitochondria and autophagy and its role in the aging process. Exp. Gerontol. 56, 147-153.
68. Schon E.A., DiMauro S. and Hirano M. (2012). Human mitochondrial DNA: roles of inherited and somatic mutations. Nat. Rev. Genet. 13, 878-890.
69. Schweers R.L., Zhang J., Randall M.S., Loyd M.R., Li W., Dorsey F.C., Kundu M., Opferman J.T., Cleveland J.L., Miller J.L. and Ney P.A. (2007). NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. USA 104,19500-19505.
70. Shiba-Fukushima K., Imai Y., Yoshida S., Ishihama Y., Kanao T., Sato S. and Hattori N. (2012). PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci. Rep. 2, 1002.
71. Shimura H., Hattori N., Kubo S., Mizuno Y., Asakawa S., Minoshima S., Shimizu N., Iwai K., Chiba T., Tanaka K. and Suzuki T. (2000). Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nature Genet. 25, 302-305.
72. Shirakabe A., Zhai P., Ikeda Y., Saito T., Maejima Y., Hsu C.P., Nomura M., Egashira K., Levine B. and Sadoshima J. (2016). Drp1-dependent mitochondrial autophagy plays a protective role against pressure overload-Induced mitochondrial dysfunction and heart failure. Circulation 133, 1249-1263.
73. Shirihai O.S., Song M. and Dorn G.N. (2015). How mitochondrial dynamism orchestrates mitophagy. Circ. Res. 116, 1835-1849.
74. 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.
75. Song Y., Ding W., Xiao Y. and Lu K.J. (2015). The progress of mitophagy and related pathogenic mechanisms of the neurodegenerative diseases and tumor. Neurosci. J. 543758.
76. Suen D.F., Narendra D.P., Tanaka A., Manfredi G. and Youle R.J. (2010). Parkin overexpression selects against a deleterious mtDNA mutation in heteroplasmic cybrid cells. Proc. Natl. Acad. Sci. USA 107, 11835-11840.
77. Sutovsky P., Van Leyen K., McCauley T., Day B.N. and Sutovsky M. (2004). Degradation of paternal mitochondria after fertilization: implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance. Reprod. Biomed. Online 8, 24-33.
78. 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.
79. Tanaka A., Cleland M.M., Xu S., Narendra D.P., Suen D.F., Karbowski M. and Youle R.J. (2010). Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 191, 1367-1380.
80. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., Stiles L., Haigh S.E., Katz S., Las G., Alroy J., Wu M., Py B.F., Yuan J., Deeney J.T., Corkey B.E. and Shirihai O.S. (2008). Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446.
81. Wang X., Winter D., Ashrafi G., Schlehe J., Wong Y.L., Selkoe D., Rice S., Steen J., LaVoie M.J. and Schwarz T.L. (2011). PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell. 147, 893-906.
82. Williams J.A. and Ding W.X. (2015). A mechanistic review of mitophagy and Its role in protection against alcoholic liver disease. Biomolecules 5, 2619-2642.
83. Wu Q., Xia S.X., Li Q.Q., Gao Y., Shen X., Ma L., Zhang M.Y., Wang T., Li Y.S., Wang Z.F., Luo C.L. and Tao L.Y. (2016). Mitochondrial division inhibitor 1 (Mdivi-1) offers neuroprotection through diminishing cell death and improving functional outcome in a mouse model of traumatic brain injury. Brain Res. 1630, 134-143.
84. Ye X., Sun X., Starovoytov V. and Cai Q. (2015). Parkin-mediated mitophagy in mutant hAPP neurons and Alzheimer's disease patient brains. Hum. Mol. Genet. 24, 2938-2951.
85. Yoshii S.R., Kishi C., Ishihara N. and Mizushima N. (2011). Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J. Biol. Chem. 286, 19630-19640.
86. Youle R.J. and Narendra D.P. (2011). Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9-14.
87. Youle R.J. and van der Bliek A.M. (2012). Mitochondrial fission, fusion, and stress. Science 337, 1062-1065.
88. Zhang Z., Liu L., Jiang X., Zhai S. and Xing D. (2016). The essential role of Drp1 and its regulation by S-nitrosylation of Parkin in dopaminergic neurodegeneration: implications for Parkinson's disease. Antioxid. Redox Signal. 25, 609-622.
89. Zhu J., Wang K.Z. and Chu C.T. (2013). After the banquet: mitochondrial biogenesis, mitophagy, and cell survival. Autophagy 9, 1663-1676.
90. Zuo W., Yang P.F., Chen J., Zhang Z. and Chen N.H. (2016). Drp-1, a potential therapeutic target for brain ischaemic stroke. Br. J. Pharmacol. 173, 1665-1677.