A Rab5 endosomal pathway mediates Parkin-dependent mitochondrial clearance

Nature Communications

Volumn 8, Issue , 2017, Pages

  Hammerling, Babette C ^a   Najor, Rita H ^a   Cortez, Melissa Q ^a   Shires, Sarah E ^a   Leon, Leonardo J ^a   Gonzalez, Eileen R ^a   Boassa, Daniela ^b   Phan, Sébastien ^b   Thor, Andrea ^b   Jimenez, Rebecca E ^a   Li, Hong ^c   Kitsis, Richard N ^d   Ii, Gerald W Dorn ^e   Sadoshima, Junichi ^c   Ellisman, Mark H ^b   Gustafsson, Åsa B ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; ESCRT PROTEIN; PARKIN; RAB PROTEIN; ATG5 PROTEIN, MOUSE; AUTOPHAGY RELATED PROTEIN 5; BECN1 PROTEIN, MOUSE; BECN1 PROTEIN, RAT; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE;

BIOCHEMISTRY; CELLS AND CELL COMPONENTS; DEGRADATION; MATURATION; MITOCHONDRION; PROTEIN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BIOACCUMULATION; CARDIAC MUSCLE CELL; CELL DEATH; CONTROLLED STUDY; EMBRYO; ENDOSOME; FIBROBLAST; LYSOSOME; MITOCHONDRIAL CLEARANCE; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; MITOPHAGY; MOUSE; NONHUMAN; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL LINE; ELECTRON MICROSCOPY; FEMALE; GENE KNOCKDOWN; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; PHYSIOLOGY; PRIMARY CELL CULTURE; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; UBIQUITINATION; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 5; BECLIN-1; CELL LINE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; FEMALE; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; LYSOSOMES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MYOCYTES, CARDIAC; PRIMARY CELL CULTURE; RAB5 GTP-BINDING PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 85010931361     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14050     Document Type: Article

References (69)

1. Komatsu, M. et al. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc. Natl Acad. Sci. USA 104, 14489-14494 (2007).
2. Kuma, A. et al. The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036 (2004).
3. Kubli, D. A. & Gustafsson, A. B. Mitochondria and mitophagy: the yin and yang of cell death control. Circ. Res. 111, 1208-1221 (2012).
4. Nishida, Y. et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461, 654-658 (2009).
5. Hwang, S., Disatnik, M. H. & Mochly-Rosen, D. Impaired GAPDH-induced mitophagy contributes to the pathology of Huntington's disease. EMBO Mol. Med. 7, 1307-1326 (2015).
6. Kitada, T. et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608 (1998).
7. Kubli, D. A. et al. Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J. Biol. Chem. 288, 915-926 (2013).
8. Song, M. et al. Interdependence of Parkin-mediated mitophagy and mitochondrial fission in adult mouse hearts. Circ. Res. 117, 346-351 (2015).
9. Hoshino, A. et al. Cytosolic p53 inhibits Parkin-mediated mitophagy and promotes mitochondrial dysfunction in the mouse heart. Nat. Commun. 4, 2308 (2013).
10. Gong, G. et al. Parkin-mediated mitophagy directs perinatal cardiac metabolic maturation in mice. Science 350, aad2459 (2015).
11. Narendra, D., Tanaka, A., Suen, D. F. & Youle, R. J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803 (2008).
12. Matsui, M., Yamamoto, A., Kuma, A., Ohsumi, Y. & Mizushima, N. Organelle degradation during the lens and erythroid differentiation is independent of autophagy. Biochem. Biophys. Res. Commun. 339, 485-489 (2006).
13. Chen, Y. & Dorn, 2nd G. W. PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 340, 471-475 (2013).
14. Okatsu, K. et al. p62/SQSTM1 cooperates with Parkin for perinuclear clustering of depolarized mitochondria. Genes Cell 15, 887-900 (2010).
15. Ding, W. X. et al. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitinp62-mediated mitochondrial priming. J. Biol. Chem. 285, 27879-27890 (2010).
16. Sriram, S. R. et al. Familial-associated mutations differentially disrupt the solubility, localization, binding and ubiquitination properties of parkin. Hum. Mol. Genet. 14, 2571-2586 (2005).
17. Choudhury, A. et al. Rab proteins mediate Golgi transport of caveolainternalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Invest. 109, 1541-1550 (2002).
18. Kundu, M. et al. Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood 112, 1493-1502 (2008).
19. Marchese, A., Paing, M. M., Temple, B. R. & Trejo, J. G protein-coupled receptor sorting to endosomes and lysosomes. Annu. Rev. Pharmacol. Toxicol. 48, 601-629 (2008).
20. Zeigerer, A. et al. Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 485, 465-470 (2012).
21. Maxfield, F. R. & McGraw, T. E. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132 (2004).
22. Gaspar, A. H. & Machner, M. P. VipD is a Rab5-activated phospholipase A1 that protects Legionella pneumophila from endosomal fusion. Proc. Natl Acad. Sci. USA 111, 4560-4565 (2014).
23. Kanai, F. et al. The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat. Cell Biol. 3, 675-678 (2001).
24. Lam, S. S., Martell, J. D. & Kamer, K. J. Directed evolution of APEX2 for electron microscopy and proximity labeling. Nat. Methods 12, 51-54 (2015).
25. Campsteijn, C., Vietri, M. & Stenmark, H. Novel ESCRT functions in cell biology: spiraling out of control Curr. Opin. Cell Biol. 41, 1-8 (2016).
26. Goldman, A., Leinwand, L. & Spector, D. Cells: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 1998).
27. Chen, Y. R. & Zweier, J. L. Cardiac mitochondria and reactive oxygen species generation. Circ. Res. 114, 524-537 (2014).
28. Rink, J., Ghigo, E., Kalaidzidis, Y. & Zerial, M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749 (2005).
29. Twig, G. et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446 (2008).
30. Song, M., Mihara, K., Chen, Y., Scorrano, L. & Dorn, 2nd G. W. Mitochondrial fission and fusion factors reciprocally orchestrate mitophagic culling in mouse hearts and cultured fibroblasts. Cell Metab. 21, 273-285 (2015).
31. Ney, P. A. Mitochondrial autophagy: Origins, significance, and role of BNIP3 and NIX. Biochim. Biophys. Acta 1853, 2775-2783 (2015).
32. Hanna, R. A. et al. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J. Biol. Chem. 287, 19094-19104 (2012).
33. Martin, S. J., Lennon, S. V., Bonham, A. M. & Cotter, T. G. Induction of apoptosis (programmed cell death) in human leukemic HL-60 cells by inhibition of RNA or protein synthesis. J. Immunol. 145, 1859-1867 (1990).
34. Hirosako, K. et al. 3-Methyladenine specifically inhibits retrograde transport of cation-independent mannose 6-phosphate/insulin-like growth factor II receptor from the early endosome to the TGN. Biochem. Biophys. Res. Commun. 316, 845-852 (2004).
35. Hamacher-Brady, A. et al. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ. 14, 146-157 (2007).
36. Henne, W. M., Buchkovich, N. J. & Emr, S. D. The ESCRT pathway. Dev. Cell 21, 77-91 (2011).
37. Li, W. W., Li, J. & Bao, J. K. Microautophagy: lesser-known self-eating. Cell. Mol. Life Sci. 69, 1125-1136 (2012).
38. Soubannier, V. et al. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr. Biol. 22, 135-141 (2012).
39. Davis, C. H. et al. Transcellular degradation of axonal mitochondria. Proc. Natl Acad. Sci. USA 111, 9633-9638 (2014).
40. Rubinsztein, D. C., Shpilka, T. & Elazar, Z. Mechanisms of autophagosome biogenesis. Curr. Biol. 22, R29-R34 (2012).
41. Kaushik, S., Massey, A. C., Mizushima, N. & Cuervo, A. M. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol. Biol. Cell 19, 2179-2192 (2008).
42. McKnight, N. C. et al. Beclin 1 is required for neuron viability and regulates endosome pathways via the UVRAG-VPS34 complex. PLoS Genet. 10, e1004626 (2014).
43. Jean, S., Cox, S., Nassari, S. & Kiger, A. A. Starvation-induced MTMR13 and RAB21 activity regulates VAMP8 to promote autophagosome-lysosome fusion. EMBO Rep. 16, 297-311 (2015).
44. Roy, S. G., Stevens, M. W., So, L. & Edinger, A. L. Reciprocal effects of rab7 deletion in activated and neglected T cells. Autophagy 9, 1009-1023 (2013).
45. Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452 (2009).
46. McLelland, G. L., Soubannier, V., Chen, C. X., McBride, H. M. & Fon, E. A. Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J. 33, 282-295 (2014).
47. McLelland, G. L. & Lee, S. A. Syntaxin-17 delivers PINK1/parkin-dependent mitochondrial vesicles to the endolysosomal system. J. Cell Biol. 214, 275-291 (2016).
48. Liu, X. M. et al. ESCRTs cooperate with a selective autophagy receptor to mediate vacuolar targeting of soluble cargos. Mol. Cell 59, 1035-1042 (2015).
49. Sahu, R. et al. Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 20, 131-139 (2011).
50. Geisler, S. et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131 (2010).
51. Kim, K. Y. et al. Parkin is a lipid-responsive regulator of fat uptake in mice and mutant human cells. J. Clin. Invest. 121, 3701-3712 (2011).
52. Cummins, T. D. et al. Metabolic remodeling of white adipose tissue in obesity. Am. J. Physiol. Endocrinol. Metab. 307, E262-E277 (2014).
53. Yamashiro, D. J., Fluss, S. R. & Maxfield, F. R. Acidification of endocytic vesicles by an ATP-dependent proton pump. J. Cell Biol. 97, 929-934 (1983).
54. Zoncu, R. et al. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H()-ATPase. Science 334, 678-683 (2011).
55. Zhang, C. S. et al. The lysosomal v-ATPase-Ragulator complex is a common activator for AMPK and mTORC1, acting as a switch between catabolism and anabolism. Cell Metab. 20, 526-540 (2014).
56. Roczniak-Ferguson, A. et al. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal 5, ra42 (2012).
57. Lee, I. H. et al. Atg7 modulates p53 activity to regulate cell cycle and survival during metabolic stress. Science 336, 225-228 (2012).
58. Karwatowska-Prokopczuk, E., Nordberg, J. A., Li, H. L., Engler, R. L. & Gottlieb, R. A. Effect of vacuolar proton ATPase on pHi, Ca2, and apoptosis in neonatal cardiomyocytes during metabolic inhibition/recovery. Circ. Res. 82, 1139-1144 (1998).
59. Zhang, Y. et al. Parkin functions as an E2-dependent ubiquitin-protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc. Natl Acad. Sci. USA 97, 13354-13359 (2000).
60. Sun, Q., Westphal, W., Wong, K. N., Tan, I. & Zhong, Q. Rubicon controls endosome maturation as a Rab7 effector. Proc. Natl Acad. Sci. USA 107, 19338-19343 (2010).
61. Day, R. N. & Davidson, M. W. The fluorescent protein palette: tools for cellular imaging. Chem. Soc. Rev. 38, 2887-2921 (2009).
62. Hayashida, K., Stahl, P. D. & Park, P. W. Syndecan-1 ectodomain shedding is regulated by the small GTPase Rab5. J. Biol. Chem. 283, 35435-35444 (2008).
63. Hariharan, N. et al. Autophagy plays an essential role in mediating regression of hypertrophy during unloading of the heart. PLoS ONE 8, e51632 (2013).
64. Kubli, D. A., Ycaza, J. E. & Gustafsson, A. B. Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak. Biochem. J. 405, 407-415 (2007).
65. Yoshii, S. R., Kishi, C., Ishihara, N. & Mizushima, N. Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J. Biol. Chem. 286, 19630-19640 (2011).
66. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108 (2008).
67. Kirchhofer, A. et al. Modulation of protein properties in living cells using nanobodies. Nat. Struct. Mol. Biol. 17, 133-138 (2010).
68. Phan, S. et al. 3D reconstruction of biological structures: automated procedures for alignment and reconstruction of multiple tilt series in electron tomography. Adv. Struct. Chem. Imaging 2, 8 (2017).
69. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).