BNIP3 protein suppresses PINK1 kinase proteolytic cleavage to promote mitophagy

Journal of Biological Chemistry

Volumn 291, Issue 41, 2016, Pages 21616-21629

  Zhang, Tongmei ^a   Xue, Liang ^b   Li, Li ^a   Tang, Chengyuan ^a   Wan, Zhengqing ^a   Wang, Ruoxi ^a   Tan, Jieqiong ^a   Tan, Ya ^a   Han, Hailong ^a   Tian, Runyi ^a   Billiar, Timothy R ^a,c   Tao, W Andy ^b   Zhang, Zhuohua ^a,d  

^a Central South University   (China)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; MAMMALS; PROTEINS;

MAMMALIAN CELLS; OUTER MEMBRANE; PARKINSON'S DISEASE; PHYSIOLOGICAL CONDITION; PROTEOLYTIC CLEAVAGE; PROTEOLYTIC PROCESS; PROTEOLYTIC PROCESSING; THERAPEUTIC STRATEGY;

MITOCHONDRIA;

ADENOSINE TRIPHOSPHATE; PARKIN; PROTEIN BNIP3; BNIP3 PROTEIN, HUMAN; BNIP3 PROTEIN, MOUSE; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; ONCOPROTEIN; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL HYPOXIA; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; FLIGHT MUSCLE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL OUTER MEMBRANE; MITOPHAGY; MOUSE; MUSCLE ATROPHY; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; KNOCKOUT MOUSE; METABOLISM; PARKINSON DISEASE; PATHOLOGY;

ANIMALS; CELL HYPOXIA; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE, KNOCKOUT; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; PARKINSON DISEASE; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS;

EID: 84990224594     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.733410     Document Type: Article

References (55)

1. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., and Shimizu, N. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608
2. Farrer, M. J. (2006) Genetics of Parkinson disease: paradigm shifts and future prospects. Nat. Rev. Genet. 7, 306-318
3. Valente, E. M., Abou-Sleiman, P. M., Caputo, V., Muqit, M. M., Harvey, K., Gispert, S., Ali, Z., Del Turco, D., Bentivoglio, A. R., Healy, D. G., Albanese, A., Nussbaum, R., González-Maldonado, R., Deller, T., Salvi, S., et al. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304, 1158-1160
4. Muqit, M. M., Abou-Sleiman, P. M., Saurin, A. T., Harvey, K., Gandhi, S., Deas, E., Eaton, S., Payne Smith, M. D., Venner, K., Matilla, A., Healy, D. G., Gilks, W. P., Lees, A. J., Holton, J., Revesz, T., et al. (2006) Altered cleavage and localization of PINK1 to aggresomes in the presence of proteasomal stress. J. Neurochem. 98, 156-169
5. Lin, W., and Kang, U. J. (2008) Characterization of PINK1 processing, stability, and subcellular localization. J. Neurochem. 106, 464-474
6. 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
7. Imai, Y., Soda, M., and Takahashi, R. (2000) Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J. Biol. Chem. 275, 35661-35664
8. Zhang, Y., Gao, J., Chung, K. K., Huang, H., Dawson, V. L., and Dawson, T. M. (2000) 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. U.S.A. 97, 13354-13359
9. 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. Nat. Genet. 25, 302-305
10. Wenzel, D. M., Lissounov, A., Brzovic, P. S., and Klevit, R. E. (2011) UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature 474, 105-108
11. Xiong, H., Wang, D., Chen, L., Choo, Y. S., Ma, H., Tang, C., Xia, K., Jiang, W., Ronai, Z., Zhuang, X., and Zhang, Z. (2009) Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation. J. Clin. Invest. 119, 650-660
12. Geisler, S., Holmström, K. M., Treis, A., Skujat, D., Weber, S. S., Fiesel, F. C., Kahle, P. J., and Springer, W. (2010) The PINK1/Parkin-mediated mitophagy is compromised by PD-associated mutations. Autophagy 6, 871-878
13. Narendra, D., Tanaka, A., Suen, D. F., and Youle, R. J. (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803
14. Vives-Bauza, C., Zhou, C., Huang, Y., Cui, M., de Vries, R. L., Kim, J., May, J., Tocilescu, M. A., Liu, W., Ko, H. S., Magrané, J., Moore, D. J., Dawson, V. L., Grailhe, R., Dawson, T. M., et al. (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc. Natl. Acad. Sci. U.S.A. 107, 378-383
15. 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
16. 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
17. 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
18. 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
19. 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
20. Regula, K. M., Ens, K., and Kirshenbaum, L. A. (2002) Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes. Circ. Res. 91, 226-231
21. Vande Velde, C., Cizeau, J., Dubik, D., Alimonti, J., Brown, T., Israels, S., Hakem, R., and Greenberg, A. H. (2000) BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol. Cell. Biol. 20, 5454-5468
22. Chen, Y., Lewis, W., Diwan, A., Cheng, E. H., Matkovich, S. J., and Dorn, G. W., 2nd (2010) Dual autonomous mitochondrial cell death pathways are activated by Nix/BNip3L and induce cardiomyopathy. Proc. Natl. Acad. Sci. U.S.A. 107, 9035-9042
23. Rikka, S., Quinsay, M. N., Thomas, R. L., Kubli, D. A., Zhang, X., Murphy, A. N., and Gustafsson, Å. B. (2011) Bnip3 impairs mitochondrial bioenergetics and stimulates mitochondrial turnover. Cell Death Differ. 18, 721-731
24. Bellot, G., Garcia-Medina, R., Gounon, P., Chiche, J., Roux, D., Pouysségur, J., and Mazure, N. M. (2009) Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell. Biol. 29, 2570-2581
25. Dorn, G. W., 2nd.(2010) Mitochondrial pruning by Nix and BNip3: an essential function for cardiac-expressed death factors. J. Cardiovasc. Transl. Res. 3, 374-383
26. Hanna, R. A., Quinsay, M. N., Orogo, A. M., Giang, K., Rikka, S., and Gustafsson, Å. B. (2012) 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
27. Zhu, Y., Massen, S., Terenzio, M., Lang, V., Chen-Lindner, S., Eils, R., Novak, I., Dikic, I., Hamacher-Brady, A., and Brady, N. R. (2013) Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J. Biol. Chem. 288, 1099-1113
28. Ding, W. X., Ni, H. M., Li, M., Liao, Y., Chen, X., Stolz, D. B., Dorn, G. W., 2nd, and Yin, X. M. (2010) Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62-mediated mitochondrial priming. J. Biol. Chem. 285, 27879-27890
29. Whitworth, A. J., Theodore, D. A., Greene, J. C., Benes, H., Wes, P. D., and Pallanck, L. J. (2005) Increased glutathione S-transferase activity rescues dopaminergic neuron loss in a Drosophila model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 102, 8024-8029
30. Kubli, D. A., Quinsay, M. N., Huang, C., Lee, Y., and Gustafsson, A. B. (2008) Bnip3 functions as a mitochondrial sensor of oxidative stress during myocardial ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 295, H2025-H2031
31. Sulistijo, E. S., and MacKenzie, K. R. (2006) Sequence dependence of BNIP3 transmembrane domain dimerization implicates side-chain hydrogen bonding and a tandem GxxxG motif in specific helix-helix interactions. J. Mol. Biol. 364, 974-990
32. Vasagiri, N., and Kutala, V. K. (2014) Structure, function, and epigenetic regulation of BNIP3: a pathophysiological relevance. Mol. Biol. Rep. 41, 7705-7714
33. Ray, R., Chen, G., Vande Velde, C., Cizeau, J., Park, J. H., Reed, J. C., Gietz, R. D., and Greenberg, A. H. (2000) BNIP3 heterodimerizes with Bcl-2/Bcl-X(L) and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J. Biol. Chem. 275, 1439-1448
34. Bruick, R. K. (2000) Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. U.S.A. 97, 9082-9087
35. Clark, I. E., Dodson, M. W., Jiang, C., Cao, J. H., Huh, J. R., Seol, J. H., Yoo, S. J., Hay, B. A., and Guo, M. (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441, 1162-1166
36. Park, J., Lee, S. B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M., Kim, J. M., and Chung, J. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441, 1157-1161
37. Yang, Y., Gehrke, S., Imai, Y., Huang, Z., Ouyang, Y., Wang, J. W., Yang, L., Beal, M. F., Vogel, H., and Lu, B. (2006) Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl. Acad. Sci. U.S.A. 103, 10793-10798
38. Deng, H., Dodson, M. W., Huang, H., and Guo, M. (2008) The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 105, 14503-14508
39. Yun, J., Puri, R., Yang, H., Lizzio, M. A., Wu, C., Sheng, Z. H., and Guo, M. (2014) MUL1 acts in parallel to the PINK1/parkin pathway in regulating mitofusin and compensates for loss of PINK1/parkin. eLife 3, e01958
40. Choo, Y. S., Vogler, G., Wang, D., Kalvakuri, S., Iliuk, A., Tao, W. A., Bodmer, R., and Zhang, Z. (2012) Regulation of parkin and PINK1 by neddylation. Hum. Mol. Genet. 21, 2514-2523
41. Deas, E., Plun-Favreau, H., Gandhi, S., Desmond, H., Kjaer, S., Loh, S. H., Renton, A. E., Harvey, R. J., Whitworth, A. J., Martins, L. M., Abramov, A. Y., and Wood, N. W. (2011) PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum. Mol. Genet. 20, 867-879
42. Greene, A. W., Grenier, K., Aguileta, M. A., Muise, S., Farazifard, R., Haque, M. E., McBride, H. M., Park, D. S., and Fon, E. A. (2012) Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep. 13, 378-385
43. Venegas, V., Wang, J., Dimmock, D., and Wong, L. J. (2011) Real-time quantitative PCR analysis of mitochondrial DNA content. Curr. Protoc. Hum. Genet. 68, 19.7.1-19.7.12
44. Lee, Y., Lee, H. Y., Hanna, R. A., and Gustafsson, Å. 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. Ding, W. X., and Yin, X. M. (2012) Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol. Chem. 393, 547-564
46. Wei, H., Liu, L., and Chen, Q. (2015) Selective removal of mitochondria via mitophagy: distinct pathways for different mitochondrial stresses. Biochim. Biophys. Acta 1853, 2784-2790
47. Yang, Y., Ouyang, Y., Yang, L., Beal, M. F., McQuibban, A., Vogel, H., and Lu, B. (2008) Pink1 regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc. Natl. Acad. Sci. U.S.A. 105, 7070-7075
48. Liu, W., Acín-Peréz, R., Geghman, K. D., Manfredi, G., Lu, B., and Li, C. (2011) Pink1 regulates the oxidative phosphorylation machinery via mitochondrial fission. Proc. Natl. Acad. Sci. U.S.A. 108, 12920-12924
49. Poole, A. C., Thomas, R. E., Andrews, L. A., McBride, H. M., Whitworth, A. J., and Pallanck, L. J. (2008) The PINK1/Parkin pathway regulates mitochondrial morphology. Proc. Natl. Acad. Sci. U.S.A. 105, 1638-1643
50. Awan, M. U., Hasan, M., Iqbal, J., Lei, R., Lee, W. F., Hong, M., Qing, H., and Deng, Y. (2014) Neuroprotective role of BNIP3 under oxidative stress through autophagy in neuroblastoma cells. Mol. Biol. Rep. 41, 5729-5734
51. Zhang, H., Bosch-Marce, M., Shimoda, L. A., Tan, Y. S., Baek, J. H., Wesley, J. B., Gonzalez, F. J., and Semenza, G. L. (2008) Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 283, 10892-10903
52. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., and Zhang, F. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823
53. Choo, Y. S., Johnson, G. V., MacDonald, M., Detloff, P. J., and Lesort, M. (2004) Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Hum. Mol. Genet. 13, 1407-1420
54. Tan, J., Zhang, T., Jiang, L., Chi, J., Hu, D., Pan, Q., Wang, D., and Zhang, Z. (2011) Regulation of intracellular manganese homeostasis by Kufor-Rakeb syndrome-associated ATP13A2 protein. J. Biol. Chem. 286, 29654-29662
55. Zhang, Z., Hartmann, H., Do, V. M., Abramowski, D., Sturchler-Pierrat, C., Staufenbiel, M., Sommer, B., van de Wetering, M., Clevers, H., Saftig, P., De Strooper, B., He, X., and Yankner, B. A. (1998) Destabilization of β-catenin by mutations in presenilin-1 potentiates neuronal apoptosis. Nature 395, 698-702