DOI QR코드

DOI QR Code

Mechanisms and Physiological Roles of Mitophagy in Yeast

  • Fukuda, Tomoyuki (Department of Cellular Physiology, Niigata University Graduate School of Medical and Dental Sciences) ;
  • Kanki, Tomotake (Department of Cellular Physiology, Niigata University Graduate School of Medical and Dental Sciences)
  • Received : 2017.09.13
  • Accepted : 2017.12.05
  • Published : 2018.01.31

Abstract

Mitochondria are responsible for supplying of most of the cell's energy via oxidative phosphorylation. However, mitochondria also can be deleterious for a cell because they are the primary source of reactive oxygen species, which are generated as a byproduct of respiration. Accumulation of mitochondrial and cellular oxidative damage leads to diverse pathologies. Thus, it is important to maintain a population of healthy and functional mitochondria for normal cellular metabolism. Eukaryotes have developed defense mechanisms to cope with aberrant mitochondria. Mitochondria autophagy (known as mitophagy) is thought to be one such process that selectively sequesters dysfunctional or excess mitochondria within double-membrane autophagosomes and carries them into lysosomes/vacuoles for degradation. The power of genetics and conservation of fundamental cellular processes among eukaryotes make yeast an excellent model for understanding the general mechanisms, regulation, and function of mitophagy. In budding yeast, a mitochondrial surface protein, Atg32, serves as a mitochondrial receptor for selective autophagy that interacts with Atg11, an adaptor protein for selective types of autophagy, and Atg8, a ubiquitin-like protein localized to the isolation membrane. Atg32 is regulated transcriptionally and post-translationally to control mitophagy. Moreover, because Atg32 is a mitophagy-specific protein, analysis of its deficient mutant enables investigation of the physiological roles of mitophagy. Here, we review recent progress in the understanding of the molecular mechanisms and functional importance of mitophagy in yeast at multiple levels.

Keywords

E1BJB7_2018_v41n1_35_f0001.png 이미지

Fig. 1. Mitophagy in yeast. (A) Schematic represen-tation of autophagy. When autophagy is induced,isolation membranes nucleate at the preautoph-agosomal structure/phagophore assembly site(PAS). They grow and engulf cytoplasmic cargosto form a double-membrane vesicle called anautophagosome. Autophagosomes subsequentlyfuse with the lysosome/ vacuole and release the

References

  1. Abeliovich, H., Zarei, M., Rigbolt, K.T., Youle, R.J., and Dengjel, J. (2013). Involvement of mitochondrial dynamics in the segregation of mitochondrial matrix proteins during stationary phase mitophagy. Nat. Commun. 4, 2789.
  2. Aihara, M., Jin, X., Kurihara, Y., Yoshida, Y., Matsushima, Y., Oku, M., Hirota, Y., Saigusa, T., Aoki, Y., Uchiumi, T., et al. (2014). Tor and the Sin3-Rpd3 complex regulate expression of the mitophagy receptor protein Atg32 in yeast. J. Cell Sci. 127, 3184-3196. https://doi.org/10.1242/jcs.153254
  3. Aoki, Y., Kanki, T., Hirota, Y., Kurihara, Y., Saigusa, T., Uchiumi, T., and Kang, D. (2011). Phosphorylation of Serine 114 on Atg32 mediates mitophagy. Mol. Biol. Cell 22, 3206-3217. https://doi.org/10.1091/mbc.E11-02-0145
  4. Barth, P.G., Scholte, H.R., Berden, J.A., Van der Klei-Van Moorsel, J.M., Luyt-Houwen, I.E., Van 't Veer-Korthof, E.T., Van der Harten, J.J., and Sobotka-Plojhar, M.A. (1983). An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J. Neurol. Sci. 62, 327-355. https://doi.org/10.1016/0022-510X(83)90209-5
  5. Belgareh-Touze, N., Cavellini, L., and Cohen, M.M. (2017). Ubiquitination of ERMES components by the E3 ligase Rsp5 is involved in mitophagy. Autophagy 13, 114-132. https://doi.org/10.1080/15548627.2016.1252889
  6. Bernhardt, D., Muller, M., Reichert, A.S., and Osiewacz, H.D. (2015). Simultaneous impairment of mitochondrial fission and fusion reduces mitophagy and shortens replicative lifespan. Sci. Rep. 5, 7885. https://doi.org/10.1038/srep07885
  7. Bockler, S., and Westermann, B. (2014). Mitochondrial ER contacts are crucial for mitophagy in yeast. Dev. Cell 28, 450-458. https://doi.org/10.1016/j.devcel.2014.01.012
  8. Campbell, C.L., and Thorsness, P.E. (1998). Escape of mitochondrial DNA to the nucleus in yme1 yeast is mediated by vacuolardependent turnover of abnormal mitochondrial compartments. J. Cell Sci. 111, 2455-2464.
  9. Chen, G., Han, Z., Feng, D., Chen, Y., Chen, L., Wu, H., Huang, L., Zhou, C., Cai, X., Fu, C., et al. (2014). A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptormediated mitophagy. Mol. Cell 54, 362-377. https://doi.org/10.1016/j.molcel.2014.02.034
  10. Chu, C.T., Ji, J., Dagda, R.K., Jiang, J.F., Tyurina, Y.Y., Kapralov, A.A., Tyurin, V.A., Yanamala, N., Shrivastava, I.H., Mohammadyani, D., et al. (2013). Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat. Cell Biol. 15, 1197-1205. https://doi.org/10.1038/ncb2837
  11. Deffieu, M., Bhatia-Kissova, I., Salin, B., Galinier, A., Manon, S., and Camougrand, N. (2009). Glutathione participates in the regulation of mitophagy in yeast. J. Biol. Chem. 284, 14828-14837. https://doi.org/10.1074/jbc.M109.005181
  12. Deffieu, M., Bhatia-Kissova, I., Salin, B., Klionsky, D.J., Pinson, B., Manon, S., and Camougrand, N. (2013). Increased levels of reduced cytochrome b and mitophagy components are required to trigger nonspecific autophagy following induced mitochondrial dysfunction. J. Cell Sci. 126, 415-426. https://doi.org/10.1242/jcs.103713
  13. Eiyama, A., and Okamoto, K. (2015). Protein N-terminal Acetylation by the NatA Complex Is Critical for Selective Mitochondrial Degradation. J. Biol. Chem. 290, 25034-25044. https://doi.org/10.1074/jbc.M115.677468
  14. Farre, J.C., and Subramani, S. (2016). Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat. Rev. Mol. Cell Biol. 17, 537-552.
  15. Farre, J.C., Manjithaya, R., Mathewson, R.D., and Subramani, S. (2008). PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev. Cell 14, 365-376. https://doi.org/10.1016/j.devcel.2007.12.011
  16. Farre, J.C., Burkenroad, A., Burnett, S.F., and Subramani, S. (2013). Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11. EMBO Rep. 14, 441-449. https://doi.org/10.1038/embor.2013.40
  17. Gaspard, G.J., and McMaster, C.R. (2015). The mitochondrial quality control protein Yme1 is necessary to prevent defective mitophagy in a yeast model of Barth syndrome. J. Biol. Chem. 290, 9284-9298. https://doi.org/10.1074/jbc.M115.641878
  18. Greene, A.W., K. Grenier, M.A. Aguileta, S. Muise, R. Farazifard, M.E. Haque, H.M. McBride, D.S. Park, and E.A. Fon. (2012). Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep. 13, 378-385. https://doi.org/10.1038/embor.2012.14
  19. Hamasaki, M., Furuta, N., Matsuda, A., Nezu, A., Yamamoto, A., Fujita, N., Oomori, H., Noda, T., Haraguchi, T., Hiraoka, Y., et al. (2013). Autophagosomes form at ER-mitochondria contact sites. Nature 495, 389-393. https://doi.org/10.1038/nature11910
  20. Hsu, P., Liu, X., Zhang, J., Wang, H.G., Ye, J.M., and Shi, Y. (2015). Cardiolipin remodeling by TAZ/tafazzin is selectively required for the initiation of mitophagy. Autophagy 11, 643-652. https://doi.org/10.1080/15548627.2015.1023984
  21. 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. https://doi.org/10.1083/jcb.201008084
  22. Journo, D., Mor, A., and Abeliovich, H. (2009). Aup1-mediated regulation of Rtg3 during mitophagy. J. Biol. Chem. 284, 35885-35895. https://doi.org/10.1074/jbc.M109.048140
  23. Kanki, T., and Klionsky, D.J. (2008). Mitophagy in yeast occurs through a selective mechanism. J. Biol. Chem. 283, 32386-32393. https://doi.org/10.1074/jbc.M802403200
  24. Kanki, T., Wang, K., Baba, M., Bartholomew, C.R., Lynch-Day, M.A., Du, Z., Geng, J., Mao, K., Yang, Z., Yen, W.L., et al. (2009a). A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol. Biol. Cell 20, 4730-4738. https://doi.org/10.1091/mbc.E09-03-0225
  25. Kanki, T., Wang, K., Cao, Y., Baba, M., and Klionsky, D.J. (2009b). Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17, 98-109. https://doi.org/10.1016/j.devcel.2009.06.014
  26. Kanki, T., Kurihara, Y., Jin, X., Goda, T., Ono, Y., Aihara, M., Hirota, Y., Saigusa, T., Aoki, Y., Uchiumi, T., et al. (2013). Casein kinase 2 is essential for mitophagy. EMBO Rep. 14, 788-794. https://doi.org/10.1038/embor.2013.114
  27. Karavaeva, I.E., Golyshev, S.A., Smirnova, E.A., Sokolov, S.S., Severin, F.F., and Knorre, D.A. (2017). Mitochondrial depolarization in yeast zygotes inhibits clonal expansion of selfish mtDNA. J. Cell Sci. 130, 1274-1284. https://doi.org/10.1242/jcs.197269
  28. Kawamata, T., Kamada, Y., Kabeya, Y., Sekito, T., and Ohsumi, Y. (2008). Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol. Biol. Cell 19, 2039-2050. https://doi.org/10.1091/mbc.E07-10-1048
  29. Kim, J., Kamada, Y., Stromhaug, P.E., Guan, J., Hefner-Gravink, A., Baba, M., Scott, S.V., Ohsumi, Y., Dunn, W.A., Jr., and Klionsky, D.J. (2001). Cvt9/Gsa9 functions in sequestering selective cytosolic cargo destined for the vacuole. J. Cell Biol. 153, 381-396. https://doi.org/10.1083/jcb.153.2.381
  30. Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., Noda, T., and Ohsumi, Y. (1999). Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147, 435-446. https://doi.org/10.1083/jcb.147.2.435
  31. Kissova, I., Deffieu, M., Manon, S., and Camougrand, N. (2004). Uth1p is involved in the autophagic degradation of mitochondria. J. Biol. Chem. 279, 39068-39074. https://doi.org/10.1074/jbc.M406960200
  32. Kissova, I., Salin, B., Schaeffer, J., Bhatia, S., Manon, S., and Camougrand, N. (2007). Selective and non-selective autophagic degradation of mitochondria in yeast. Autophagy 3, 329-336. https://doi.org/10.4161/auto.4034
  33. Klecker, T., Bockler, S., and Westermann, B. (2014). Making connections: interorganelle contacts orchestrate mitochondrial behavior. Trends Cell Biol. 24, 537-545. https://doi.org/10.1016/j.tcb.2014.04.004
  34. Klionsky, D.J., Cregg, J.M., Dunn, W.A., Jr., Emr, S.D., Sakai, Y., Sandoval, I.V., Sibirny, A., Subramani, S., Thumm, M., Veenhuis, M., et al. (2003). A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5, 539-545. https://doi.org/10.1016/S1534-5807(03)00296-X
  35. Kondo-Okamoto, N., Noda, N.N., Suzuki, S.W., Nakatogawa, H., Takahashi, I., Matsunami, M., Hashimoto, A., Inagaki, F., Ohsumi, Y., and Okamoto, K. (2012). Autophagy-related protein 32 acts as autophagic degron and directly initiates mitophagy. J. Biol. Chem. 287, 10631-10638. https://doi.org/10.1074/jbc.M111.299917
  36. Kraft, C., Deplazes, A., Sohrmann, M., and Peter, M. (2008). Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 10, 602-610. https://doi.org/10.1038/ncb1723
  37. Kurihara, Y., Kanki, T., Aoki, Y., Hirota, Y., Saigusa, T., Uchiumi, T., and Kang, D. (2012). Mitophagy plays an essential role in reducing mitochondrial production of reactive oxygen species and mutation of mitochondrial DNA by maintaining mitochondrial quantity and quality in yeast. J. Biol. Chem. 287, 3265-3272. https://doi.org/10.1074/jbc.M111.280156
  38. Lazarou, M., Sliter, D.A., Kane, L.A., Sarraf, S.A., Wang, C., Burman, J.L., Sideris, D.P., Fogel, A.I., and Youle, R.J. (2015). The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 524, 309-314. https://doi.org/10.1038/nature14893
  39. Leadsham, J.E., Miller, K., Ayscough, K.R., Colombo, S., Martegani, E., Sudbery, P., and Gourlay, C.W. (2009). Whi2p links nutritional sensing to actin-dependent Ras-cAMP-PKA regulation and apoptosis in yeast. J. Cell Sci. 122, 706-715. https://doi.org/10.1242/jcs.042424
  40. Lemasters, J.J. (2005). Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 8, 3-5. https://doi.org/10.1089/rej.2005.8.3
  41. Levchenko, M., Lorenzi, I., and Dudek, J. (2016). The degradation pathway of the mitophagy receptor Atg32 is re-routed by a posttranslational modification. PLoS One 11, e0168518. https://doi.org/10.1371/journal.pone.0168518
  42. Liu, L., D. Feng, G. Chen, M. Chen, Q. Zheng, P. Song, Q. Ma, C. Zhu, R. Wang, W. Qi, L., et al. (2012). Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 14, 177-185. https://doi.org/10.1038/ncb2422
  43. Mao, K., Wang, K., Liu, X., and Klionsky, D.J. (2013). The scaffold protein Atg11 recruits fission machinery to drive selective mitochondria degradation by autophagy. Dev. Cell 26, 9-18. https://doi.org/10.1016/j.devcel.2013.05.024
  44. Mendl, N., Occhipinti, A., Muller, M., Wild, P., Dikic, I., and Reichert, A.S. (2011). Mitophagy in yeast is independent of mitochondrial fission and requires the stress response gene WHI2. J. Cell Sci. 124, 1339-1350. https://doi.org/10.1242/jcs.076406
  45. Mochida, K., Oikawa, Y., Kimura, Y., Kirisako, H., Hirano, H., Ohsumi, Y., and Nakatogawa, H. (2015). Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 522, 359-362. https://doi.org/10.1038/nature14506
  46. Motley, A.M., Nuttall, J.M., and Hettema, E.H. (2012). Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 31, 2852-2868. https://doi.org/10.1038/emboj.2012.151
  47. Muller, M., and Reichert, A.S. (2011). Mitophagy, mitochondrial dynamics and the general stress response in yeast. Biochem. Soc. Trans. 39, 1514-1519. https://doi.org/10.1042/BST0391514
  48. Muller, M., Kotter, P., Behrendt, C., Walter, E., Scheckhuber, C.Q., Entian, K.D., and Reichert, A.S. (2015). Synthetic quantitative array technology identifies the Ubp3-Bre5 deubiquitinase complex as a negative regulator of mitophagy. Cell Rep. 10, 1215-1225. https://doi.org/10.1016/j.celrep.2015.01.044
  49. Murakawa, T., O. Yamaguchi, A. Hashimoto, S. Hikoso, T. Takeda, T. Oka, H. Yasui, H. Ueda, Y. Akazawa, H. Nakayama, M., et al. (2015). Bcl-2-like protein 13 is a mammalian Atg32 homologue that mediates mitophagy and mitochondrial fragmentation. Nature Commun. 6, 7527. https://doi.org/10.1038/ncomms8527
  50. Nagi, M., Tanabe, K., Nakayama, H., Ueno, K., Yamagoe, S., Umeyama, T., Ohno, H., and Miyazaki, Y. (2016). Iron-depletion promotes mitophagy to maintain mitochondrial integrity in pathogenic yeast Candida glabrata. Autophagy 12, 1259-1271. https://doi.org/10.1080/15548627.2016.1183080
  51. 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. https://doi.org/10.1083/jcb.200809125
  52. Narendra, D.P., S.M. Jin, A. Tanaka, D.F. Suen, C.A. Gautier, J. Shen, M.R. Cookson, and R.J. Youle. (2010). PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298. https://doi.org/10.1371/journal.pbio.1000298
  53. Nice, D.C., Sato, T.K., Stromhaug, P.E., Emr, S.D., and Klionsky, D.J. (2002). Cooperative binding of the cytoplasm to vacuole targeting pathway proteins, Cvt13 and Cvt20, to phosphatidylinositol 3-phosphate at the pre-autophagosomal structure is required for selective autophagy. J. Biol. Chem. 277, 30198-30207. https://doi.org/10.1074/jbc.M204736200
  54. Noda, N.N., Ohsumi, Y., and Inagaki, F. (2010). Atg8-family interacting motif crucial for selective autophagy. FEBS Lett. 584, 1379-1385. https://doi.org/10.1016/j.febslet.2010.01.018
  55. Novak, I., V. Kirkin, D.G. McEwan, J. Zhang, P. Wild, A. Rozenknop, V. Rogov, F. Lohr, D. Popovic, A. Occhipinti, A.S., et al. (2010). Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11, 45-51. https://doi.org/10.1038/embor.2009.256
  56. Nowikovsky, K., Reipert, S., Devenish, R.J., and Schweyen, R.J. (2007). Mdm38 protein depletion causes loss of mitochondrial K+/H+ exchange activity, osmotic swelling and mitophagy. Cell Death Differ. 14, 1647-1656. https://doi.org/10.1038/sj.cdd.4402167
  57. Okamoto, K., and Shaw, J.M. (2005). Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 39, 503-536. https://doi.org/10.1146/annurev.genet.38.072902.093019
  58. Okamoto, K., Kondo-Okamoto, N., and Ohsumi, Y. (2009). Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17, 87-97. https://doi.org/10.1016/j.devcel.2009.06.013
  59. Polevoda, B., and Sherman, F. (2003). Composition and function of the eukaryotic N-terminal acetyltransferase subunits. Biochem. Biophys. Res. Commun. 308, 1-11. https://doi.org/10.1016/S0006-291X(03)01316-0
  60. Priault, M., Salin, B., Schaeffer, J., Vallette, F.M., di Rago, J.P., and Martinou, J.C. (2005). Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ. 12, 1613-1621. https://doi.org/10.1038/sj.cdd.4401697
  61. Richard, V.R., Leonov, A., Beach, A., Burstein, M.T., Koupaki, O., Gomez-Perez, A., Levy, S., Pluska, L., Mattie, S., Rafesh, R., et al. (2013). Macromitophagy is a longevity assurance process that in chronologically aging yeast limited in calorie supply sustains functional mitochondria and maintains cellular lipid homeostasis. Aging 5, 234-269. https://doi.org/10.18632/aging.100547
  62. Sakakibara, K., Eiyama, A., Suzuki, S.W., Sakoh-Nakatogawa, M., Okumura, N., Tani, M., Hashimoto, A., Nagumo, S., Kondo-Okamoto, N., Kondo-Kakuta, C., et al. (2015). Phospholipid methylation controls Atg32-mediated mitophagy and Atg8 recycling. EMBO J. 34, 2703-2719. https://doi.org/10.15252/embj.201591440
  63. Sandoval, H., Thiagarajan, P., Dasgupta, S.K., Schumacher, A., Prchal, J.T., Chen, M., and Wang, J. (2008). Essential role for Nix in autophagic maturation of erythroid cells. Nature 454, 232-235. https://doi.org/10.1038/nature07006
  64. 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., et al. (2007). NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. USA 104, 19500-19505. https://doi.org/10.1073/pnas.0708818104
  65. Scott, S.V., Guan, J., Hutchins, M.U., Kim, J., and Klionsky, D.J. (2001). Cvt19 is a receptor for the cytoplasm-to-vacuole targeting pathway. Mol. Cell 7, 1131-1141. https://doi.org/10.1016/S1097-2765(01)00263-5
  66. Shen, Z., Li, Y., Gasparski, A.N., Abeliovich, H., and Greenberg, M.L. (2017). Cardiolipin Regulates Mitophagy through the Protein Kinase C Pathway. J. Biol. Chem. 292, 2916-2923. https://doi.org/10.1074/jbc.M116.753574
  67. Shintani, T., Huang, W.P., Stromhaug, P.E., and Klionsky, D.J. (2002). Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway. Dev. Cell 3, 825-837. https://doi.org/10.1016/S1534-5807(02)00373-8
  68. Shiroma, S., Jayakody, L.N., Horie, K., Okamoto, K., and Kitagaki, H. (2014). Enhancement of ethanol fermentation in Saccharomyces cerevisiae sake yeast by disrupting mitophagy function. Appl. Environ. Microbiol. 80, 1002-1012. https://doi.org/10.1128/AEM.03130-13
  69. Stewart, J.B., and Chinnery, P.F. (2015). The dynamics of mitochondrial DNA heteroplasmy: implications for human health and disease. Nat. Rev. Genet. 16, 530-542. https://doi.org/10.1038/nrg3966
  70. Suzuki, K., Kondo, C., Morimoto, M., and Ohsumi, Y. (2010). Selective transport of alpha-mannosidase by autophagic pathways: identification of a novel receptor, Atg34p. J. Biol. Chem. 285, 30019-30025. https://doi.org/10.1074/jbc.M110.143511
  71. Suzuki, S.W., Onodera, J., and Ohsumi, Y. (2011). Starvation induced cell death in autophagy-defective yeast mutants is caused by mitochondria dysfunction. PLoS One 6, e17412. https://doi.org/10.1371/journal.pone.0017412
  72. Takeda, K., Yoshida, T., Kikuchi, S., Nagao, K., Kokubu, A., Pluskal, T., Villar-Briones, A., Nakamura, T., and Yanagida, M. (2010). Synergistic roles of the proteasome and autophagy for mitochondrial maintenance and chronological lifespan in fission yeast. Proc. Natl. Acad. Sci. USA 107, 3540-3545. https://doi.org/10.1073/pnas.0911055107
  73. Takeshige, K., Baba, M., Tsuboi, S., Noda, T., and Ohsumi, Y. (1992). Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol. 119, 301-311. https://doi.org/10.1083/jcb.119.2.301
  74. Tal, R., Winter, G., Ecker, N., Klionsky, D.J., and Abeliovich, H. (2007). Aup1p, a yeast mitochondrial protein phosphatase homolog, is required for efficient stationary phase mitophagy and cell survival. J. Biol. Chem. 282, 5617-5624. https://doi.org/10.1074/jbc.M605940200
  75. Teixeira, V., Medeiros, T.C., Vilaca, R., Pereira, A.T., Chaves, S.R., Corte-Real, M., Moradas-Ferreira, P., and Costa, V. (2015). Ceramide signalling impinges on Sit4p and Hog1p to promote mitochondrial fission and mitophagy in Isc1p-deficient cells. Cell. Signal. 27, 1840-1849. https://doi.org/10.1016/j.cellsig.2015.06.001
  76. Thomas, R.L., D.A. Kubli, and A.B. Gustafsson. (2011). Bnip3-mediated defects in oxidative phosphorylation promote mitophagy. Autophagy 7, 775-777. https://doi.org/10.4161/auto.7.7.15536
  77. Thorsness, P.E., White, K.H., and Fox, T.D. (1993). Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 5418-5426. https://doi.org/10.1128/MCB.13.9.5418
  78. Vaena de Avalos, S., Okamoto, Y., and Hannun, Y.A. (2004). Activation and localization of inositol phosphosphingolipid phospholipase C, Isc1p, to the mitochondria during growth of Saccharomyces cerevisiae. J. Biol. Chem. 279, 11537-11545. https://doi.org/10.1074/jbc.M309586200
  79. Wallace, D.C. (2005). A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407. https://doi.org/10.1146/annurev.genet.39.110304.095751
  80. Wang, K., Jin, M., Liu, X., and Klionsky, D.J. (2013). Proteolytic processing of Atg32 by the mitochondrial i-AAA protease Yme1 regulates mitophagy. Autophagy 9, 1828-1836. https://doi.org/10.4161/auto.26281
  81. Welter, E., Montino, M., Reinhold, R., Schlotterhose, P., Krick, R., Dudek, J., Rehling, P., and Thumm, M. (2013). Uth1 is a mitochondrial inner membrane protein dispensable for post-logphase and rapamycin-induced mitophagy. FEBS J. 280, 4970-4982. https://doi.org/10.1111/febs.12468
  82. Wen, X., and Klionsky, D.J. (2016). An overview of macroautophagy in yeast. J. Mol. Biol. 428, 1681-1699. https://doi.org/10.1016/j.jmb.2016.02.021
  83. Yamano, K., and R.J. Youle. (2013). PINK1 is degraded through the N-end rule pathway. Autophagy. 9, 1758-1769. https://doi.org/10.4161/auto.24633
  84. Yamano, K., Matsuda, N., and Tanaka, K. (2016). The ubiquitin signal and autophagy: an orchestrated dance leading to mitochondrial degradation. EMBO Rep. 17, 300-316. https://doi.org/10.15252/embr.201541486
  85. Yamashita, S.I., Jin, X., Furukawa, K., Hamasaki, M., Nezu, A., Otera, H., Saigusa, T., Yoshimori, T., Sakai, Y., Mihara, K., et al. (2016). Mitochondrial division occurs concurrently with autophagosome formation but independently of Drp1 during mitophagy. J. Cell Biol. 215, 649-665. https://doi.org/10.1083/jcb.201605093
  86. Youle, R.J., and Narendra, D.P. (2011). Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9-14.
  87. Zhang, Y., Qi, H., Taylor, R., Xu, W., Liu, L.F., and Jin, S. (2007). The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 3, 337-346. https://doi.org/10.4161/auto.4127
  88. Zhao, D., Liu, X.M., Yu, Z.Q., Sun, L.L., Xiong, X., Dong, M.Q., and Du, L.L. (2016). Atg20- and Atg24-family proteins promote organelle autophagy in fission yeast. J. Cell Sci. 129, 4289-4304. https://doi.org/10.1242/jcs.194373
  89. 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. https://doi.org/10.1074/jbc.M112.399345

Cited by

  1. Comparative Transcriptomics Highlights New Features of the Iron Starvation Response in the Human Pathogen Candida glabrata vol.9, pp.None, 2018, https://doi.org/10.3389/fmicb.2018.02689
  2. Overview of the Minireviews on Autophagy vol.41, pp.1, 2018, https://doi.org/10.14348/molcells.2018.0400
  3. Mitophagy in Yeast vol.84, pp.suppl1, 2019, https://doi.org/10.1134/s000629791914013x
  4. Drosophila ADCK1 is critical for maintaining mitochondrial structures and functions in the muscle vol.15, pp.5, 2018, https://doi.org/10.1371/journal.pgen.1008184
  5. A Comprehensive Review of Autophagy and Its Various Roles in Infectious, Non-Infectious, and Lifestyle Diseases: Current Knowledge and Prospects for Disease Prevention, Novel Drug Design, and Therapy vol.8, pp.7, 2019, https://doi.org/10.3390/cells8070674
  6. The regulation of iron homeostasis in the fungal human pathogen Candida glabrata vol.165, pp.10, 2018, https://doi.org/10.1099/mic.0.000807
  7. A protein quality control pathway at the mitochondrial outer membrane vol.9, pp.None, 2018, https://doi.org/10.7554/elife.51065
  8. Atg43 tethers isolation membranes to mitochondria to promote starvation-induced mitophagy in fission yeast vol.9, pp.None, 2018, https://doi.org/10.7554/elife.61245
  9. Effects of 5′-3′ Exonuclease Xrn1 on Cell Size, Proliferation and Division, and mRNA Levels of Periodic Genes in Cryptococcus neoformans vol.11, pp.4, 2020, https://doi.org/10.3390/genes11040430
  10. Autophagic Proteome in Two Saccharomyces cerevisiae Strains during Second Fermentation for Sparkling Wine Elaboration vol.8, pp.4, 2018, https://doi.org/10.3390/microorganisms8040523
  11. Solid-phase inclusion as a mechanism for regulating unfolded proteins in the mitochondrial matrix vol.6, pp.32, 2020, https://doi.org/10.1126/sciadv.abc7288
  12. Spermidine inhibits neurodegeneration and delays aging via the PINK1-PDR1-dependent mitophagy pathway in C. elegans vol.12, pp.17, 2018, https://doi.org/10.18632/aging.103578
  13. Mitophagy Improves Ethanol Tolerance in Yeast: Regulation by Mitochondrial Reactive Oxygen Species in Saccharomyces cerevisiae vol.30, pp.12, 2020, https://doi.org/10.4014/jmb.2004.04073
  14. The Cell Wall Integrity Receptor Mtl1 Contributes to Articulate Autophagic Responses When Glucose Availability Is Compromised vol.7, pp.11, 2021, https://doi.org/10.3390/jof7110903