Selective Mitophagy in Budding Yeast, a Mitochondrial Self-Eating Quality Control
European Journal of Biophysics
Volume 2, Issue 5, October 2014, Pages: 49-60
Received: Aug. 11, 2014; Accepted: Aug. 26, 2014; Published: Nov. 10, 2014
Views 2363      Downloads 159
Author
Ziyad Tariq Muhseen, Key Laboratory of Molecular Biophysics, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Rd., Wuhan 430074, Hubei, China
Article Tools
Follow on us
Abstract
Mitochondria are responsible for the essential role in the cell survival by regulating the cellular energy, homeostasis, oxidative phosphorylation process, fatty acid oxidation and in the cell death process by regulating apoptosis. However, reactive oxygen species (ROS) is produced by mitochondria that pose oxidative damage to lipids, protein and mitochondrial DNA and additional production of ROS is triggered by this damage. On the other hand, the host cell control the life and death of mitochondria that include degradation, fission and growth. Recent research has been focused on the autophagic degradation of mitochondria, which is also mitophagy that results in significant discovery of the mechanism, function and regulation of mitophagy in eukaryotic cell especially in budding yeast. Mitophagy has been found to be important quality control mechanism for mitochondria. It has a key role in the eliminating of damaged mitochondria. Many studies have been done to unravel the mechanism and regulatory features of proteins involved in mitophagy but the results are inconsistent and conflicting. Mitochondrial surface receptor involved in mitochondrial autophagy has been recently identified using yeast genetics. Recent studies have been discovered specific regulators of Mitophagy that ensure selective sequestration of mitochondria as cargo. According to our understanding, in this paper we will review recent advances of different pathways of Mitophagy in the yeast. We will review the main proteins which play an essential role in controlling this process and the main pathways which lead to a highly controlled Mitophagy process.
Keywords
Mitochondria, Mitophagy, Yeast, Autophagy
To cite this article
Ziyad Tariq Muhseen, Selective Mitophagy in Budding Yeast, a Mitochondrial Self-Eating Quality Control, European Journal of Biophysics. Vol. 2, No. 5, 2014, pp. 49-60. doi: 10.11648/j.ejb.20140205.11
References
[1]
Kiel, J.A., Autophagy in unicellular eukaryotes. Philos Trans R Soc Lond B Biol Sci, 2010. 365(1541): p. 819-30.
[2]
Yu, Z.Q., et al., Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy, 2012. 8(6): p. 883-92.
[3]
Cabrera, S., et al., Autophagy, proteases and the sense of balance. Autophagy, 2010. 6(7): p. 961-3.
[4]
Suzuki, K. and Y. Ohsumi, Molecular machinery of auto-phagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett, 2007. 581(11): p. 2156-61.
[5]
Devenish, R.J. and D.J. Klionsky, Autophagy: mechanism and physiological relevance 'brewed' from yeast studies. Front Biosci (Schol Ed), 2012. 4: p. 1354-63.
[6]
Nakatogawa, H., et al., Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol, 2009. 10(7): p. 458-67.
[7]
Rubinsztein, D.C., T. Shpilka, and Z. Elazar, Mechanisms of auto-phagosome biogenesis. Curr Biol, 2012. 22(1): p. R29-34.
[8]
Mizushima, N., Autophagy: process and function. Genes Dev, 2007. 21(22): p. 2861-73.
[9]
Clark, S.L., Jr., Cellular differentiation in the kidneys of newborn mice studies with the electron microscope. J Biophys Biochem Cytol, 1957. 3(3): p. 349-62.
[10]
Takeshige, K., et al., Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol, 1992. 119(2): p. 301-11.
[11]
Kissova, I., et al., Selective and non-selective autophagic degradation of mitochondria in yeast. Autophagy, 2007. 3(4): p. 329-36.
[12]
Kissova, I., et al., Uth1p is involved in the autophagic degradation of mitochondria. J Biol Chem, 2004. 279(37): p. 39068-74.
[13]
Cover, C., et al., Peroxynitrite-induced mitochondrial and endonuclease-mediated nuclear DNA damage in acetaminophen hepatotoxicity. J Pharmacol Exp Ther, 2005. 315(2): p. 879-87.
[14]
Twig, G., et al., Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J, 2008. 27(2): p. 433-46.
[15]
Twig, G., B. Hyde, and O.S. Shirihai, Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta, 2008. 1777(9): p. 1092-7.
[16]
Kim, I. and J.J. Lemasters, Mitophagy selectively degrades individual damaged mitochondria after photoirradiation. Antioxid Redox Signal, 2011. 14(10): p. 1919-28.
[17]
Zhang, Y., et al., Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proc Natl Acad Sci U S A, 2009. 106(47): p. 19860-5.
[18]
Okamoto, K., N. Kondo-Okamoto, and Y. Ohsumi, Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell, 2009. 17(1): p. 87-97.
[19]
Kanki, T., et al., Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell, 2009. 17(1): p. 98-109.
[20]
Farre, J.C., et al., Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11. EMBO Rep, 2013.
[21]
Motley, A.M., J.M. Nuttall, and E.H. Hettema, Atg36: the Saccharomyces cerevisiae receptor for pexophagy. Autophagy, 2012. 8(11): p. 1680-1.
[22]
Motley, A.M., J.M. Nuttall, and E.H. Hettema, Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J, 2012. 31(13): p. 2852-68.
[23]
Huang, W.P. and D.J. Klionsky, Autophagy in yeast: a review of the molecular machinery. Cell Struct Funct, 2002. 27(6): p. 409-20.
[24]
Rock, K.L., et al., Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell, 1994. 78(5): p. 761-71.
[25]
Lilienbaum, A., Relationship between the proteasomal system and autophagy. Int J Biochem Mol Biol, 2013. 4(1): p. 1-26.
[26]
Gelino, S. and M. Hansen, Autophagy - An Emerging Anti-Aging Mechanism. J Clin Exp Pathol, 2012. Suppl 4.
[27]
Wallace, D.C., A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet, 2005. 39: p. 359-407.
[28]
Damsky, C.H., Environmentally induced changes in mitochondria and endoplasmic reticulum of Saccharomyces carlsbergensis yeast. J Cell Biol, 1976. 71(1): p. 123-35.
[29]
Thorsness, P.E., Structural dynamics of the mitochondrial compartment. Mutat Res, 1992. 275(3-6): p. 237-41.
[30]
Kim, I., S. Rodriguez-Enriquez, and J.J. Lemasters, Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys, 2007. 462(2): p. 245-53.
[31]
Beaulaton, J. and R.A. Lockshin, Ultrastructural study of the normal degeneration of the intersegmental muscles of Anthereae polyphemus and Manduca sexta (Insecta, Lepidoptera) with particular reference of cellular autophagy. J Morphol, 1977. 154(1): p. 39-57.
[32]
Campbell, C.L. and P.E. Thorsness, Escape of mitochondrial DNA to the nucleus in yme1 yeast is mediated by vacuolar-dependent turnover of abnormal mitochondrial compartments. J Cell Sci, 1998. 111 ( Pt 16): p. 2455-64.
[33]
Priault, M., et al., Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ, 2005. 12(12): p. 1613-21.
[34]
Nowikovsky, K., et al., Mdm38 protein depletion causes loss of mitochondrial K+/H+ exchange activity, osmotic swelling and mitophagy. Cell Death Differ, 2007. 14(9): p. 1647-56.
[35]
Tal, R., et al., Aup1p, a yeast mitochondrial protein phosphatase homolog, is required for efficient stationary phase mitophagy and cell survival. J Biol Chem, 2007. 282(8): p. 5617-24.
[36]
Abeliovich, H., Mitophagy: the life-or-death dichotomy includes yeast. Autophagy, 2007. 3(3): p. 275-7.
[37]
Kanki, T. and D.J. Klionsky, Mitophagy in yeast occurs through a selective mechanism. J Biol Chem, 2008. 283(47): p. 32386-93.
[38]
Zhang, Y., et al., The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy, 2007. 3(4): p. 337-46.
[39]
Sakai, Y., et al., Pexophagy: autophagic degradation of peroxisomes. Biochim Biophys Acta, 2006. 1763(12): p. 1767-75.
[40]
Camougrand, N., et al., Uth1p: a yeast mitochondrial protein at the crossroads of stress, degradation and cell death. FEMS Yeast Res, 2004. 5(2): p. 133-40.
[41]
DiMauro, S., Mitochondrial diseases. Biochim Biophys Acta, 2004. 1658(1-2): p. 80-8.
[42]
Kundu, M. and C.B. Thompson, Macro-autophagy versus mitochondrial autophagy: a question of fate? Cell Death Differ, 2005. 12 Suppl 2: p. 1484-9.
[43]
Skulachev, V.P., Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis, 2006. 11(4): p. 473-85.
[44]
Narendra, D., et al., Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol, 2008. 183(5): p. 795-803.
[45]
Jin, S., p53, Autophagy and tumor suppression. Autophagy, 2005. 1(3): p. 171-3.
[46]
Lemasters, J.J., Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res, 2005. 8(1): p. 3-5.
[47]
Fliss, M.S., et al., Facile detection of mitochondrial DNA mutations in tumors and bodily fluids. Science, 2000. 287(5460): p. 2017-9.
[48]
Penta, J.S., et al., Mitochondrial DNA in human malignancy. Mutat Res, 2001. 488(2): p. 119-33.
[49]
Reggiori, F. and D.J. Klionsky, Autophagosomes: biogenesis from scratch? Curr Opin Cell Biol, 2005. 17(4): p. 415-22.
[50]
Ishihara, N., et al., Auto-phagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell, 2001. 12(11): p. 3690-702.
[51]
Farre, J.C., et al., PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev Cell, 2008. 14(3): p. 365-76.
[52]
Kondo-Okamoto, N., et al., Autophagy-related protein 32 acts as autophagic degron and directly initiates mitophagy. J Biol Chem, 2012. 287(13): p. 10631-8.
[53]
Kanki, T., et al., A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol Biol Cell, 2009. 20(22): p. 4730-8.
[54]
Tang, H.W., et al., Atg1-mediated myosin II activation regulates auto-phagosome formation during starvation-induced autophagy. EMBO J, 2011. 30(4): p. 636-51.
[55]
Simonsen, A. and S.A. Tooze, Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol, 2009. 186(6): p. 773-82.
[56]
Jung, C.H., et al., mTOR regulation of autophagy. FEBS Lett, 2010. 584(7): p. 1287-95.
[57]
Webber, J.L. and S.A. Tooze, New insights into the function of Atg9. FEBS letters, 2010. 584(7): p. 1319-1326.
[58]
Di Bartolomeo, S., et al., The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol, 2010. 191(1): p. 155-68.
[59]
Ohsumi, Y., Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol, 2001. 2(3): p. 211-6.
[60]
Eskelinen, E.L., New insights into the mechanisms of macro-autophagy in mammalian cells. Int Rev Cell Mol Biol, 2008. 266: p. 207-47.
[61]
Geng, J. and D.J. Klionsky, The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep, 2008. 9(9): p. 859-64.
[62]
Mizushima, N., et al., Dissection of auto-phagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol, 2001. 152(4): p. 657-68.
[63]
Xie, Z. and D.J. Klionsky, Auto-phagosome formation: core machinery and adaptations. Nat Cell Biol, 2007. 9(10): p. 1102-9.
[64]
Huang, W.P., et al., The itinerary of a vesicle component, Aut7p/Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways. J Biol Chem, 2000. 275(8): p. 5845-51.
[65]
Kabeya, Y., et al., LC3, a mammalian homologue of yeast Apg8p, is localized in auto-phagosome membranes after processing. EMBO J, 2000. 19(21): p. 5720-8.
[66]
Kirisako, T., et al., Formation process of auto-phagosome is traced with Apg8/Aut7p in yeast. J Cell Biol, 1999. 147(2): p. 435-46.
[67]
Xie, Z., U. Nair, and D.J. Klionsky, Atg8 controls phagophore expansion during auto-phagosome formation. Mol Biol Cell, 2008. 19(8): p. 3290-8.
[68]
Ichimura, Y., et al., A ubiquitin-like system mediates protein lipidation. Nature, 2000. 408(6811): p. 488-92.
[69]
Kim, J. and D.J. Klionsky, Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu Rev Biochem, 2000. 69: p. 303-42.
[70]
Monastyrska, I., et al., Atg11 directs auto-phagosome cargoes to the PAS along actin cables. Autophagy, 2006. 2(2): p. 119-21.
[71]
Shintani, T., et al., Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway. Dev Cell, 2002. 3(6): p. 825-37.
[72]
Kanki, T. and D.J. Klionsky, Atg32 is a tag for mitochondria degradation in yeast. Autophagy, 2009. 5(8): p. 1201-2.
[73]
Kurihara, Y., et al., 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, 2012. 287(5): p. 3265-72.
[74]
Mao, K., et al., Two MAPK-signaling pathways are required for mitophagy in Saccharomyces cerevisiae. J Cell Biol, 2011. 193(4): p. 755-67.
[75]
Aoki, Y., et al., Phosphorylation of Serine 114 on Atg32 mediates mitophagy. Mol Biol Cell, 2011. 22(17): p. 3206-17.
[76]
Manjithaya, R., et al., A yeast MAPK cascade regulates pexophagy but not other autophagy pathways. J Cell Biol, 2010. 189(2): p. 303-10.
[77]
Kanki, T., K. Wang, and D.J. Klionsky, A genomic screen for yeast mutants defective in mitophagy. Autophagy, 2010. 6(2): p. 278-80.
[78]
Mendl, N., et al., Mitophagy in yeast is independent of mitochondrial fission and requires the stress response gene WHI2. J Cell Sci, 2011. 124(Pt 8): p. 1339-50.
[79]
Muller, M. and A.S. Reichert, Mitophagy, mitochondrial dynamics and the general stress response in yeast. Biochem Soc Trans, 2011. 39(5): p. 1514-9.
[80]
Radcliffe, P., et al., Deregulation of CLN1 and CLN2 in the Saccharomyces cerevisiae whi2 mutant. Yeast, 1997. 13(8): p. 707-15.
[81]
Kaida, D., et al., Yeast Whi2 and Psr1-phosphatase form a complex and regulate STRE-mediated gene expression. Genes Cells, 2002. 7(6): p. 543-52.
[82]
Austriaco, N.R., Jr., Review: to bud until death: the genetics of ageing in the yeast, Saccharomyces. Yeast, 1996. 12(7): p. 623-30.
[83]
Camougrand, N.M., et al., The "SUN" family: UTH1, an ageing gene, is also involved in the regulation of mitochondria biogenesis in Saccharomyces cerevisiae. Arch Biochem Biophys, 2000. 375(1): p. 154-60.
[84]
Camougrand, N. and M. Rigoulet, Aging and oxidative stress: studies of some genes involved both in aging and in response to oxidative stress. Respir Physiol, 2001. 128(3): p. 393-401.
[85]
Ogier-Denis, E. and P. Codogno, Autophagy: a barrier or an adaptive response to cancer. Biochim Biophys Acta, 2003. 1603(2): p. 113-28.
[86]
Journo, D., A. Mor, and H. Abeliovich, Aup1-mediated regulation of Rtg3 during mitophagy. J Biol Chem, 2009. 284(51): p. 35885-95.
[87]
Deffieu, M., et al., Glutathione participates in the regulation of mitophagy in yeast. J Biol Chem, 2009. 284(22): p. 14828-37.
[88]
Suzuki, S.W., J. Onodera, and Y. Ohsumi, Starvation induced cell death in autophagy-defective yeast mutants is caused by mitochondria dysfunction. PLoS One, 2011. 6(2): p. e17412.
[89]
Graef, M. and J. Nunnari, Mitochondria regulate autophagy by conserved signalling pathways. EMBO J, 2011. 30(11): p. 2101-14.
ADDRESS
Science Publishing Group
1 Rockefeller Plaza,
10th and 11th Floors,
New York, NY 10020
U.S.A.
Tel: (001)347-983-5186