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Cells  2012 

The Selectivity and Specificity of Autophagy in Drosophila

DOI: 10.3390/cells1030248

Keywords: autophagy, development, Drosophila, p62, Ref(2)P, programmed cell death, selective autophagy receptors

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Abstract:

Autophagy is a process of cellular self-degradation and is a major pathway for elimination of cytoplasmic material by the lysosomes. Autophagy is responsible for the degradation of damaged organelles and protein aggregates and therefore plays a significant role in cellular homeostasis. Despite the initial belief that autophagy is a nonselective bulk process, there is growing evidence during the last years that sequestration and degradation of cellular material by autophagy can be accomplished in a selective and specific manner. Given the role of autophagy and selective autophagy in several disease related processes such as tumorigenesis, neurodegeneration and infections, it is very important to dissect the molecular mechanisms of selective autophagy, in the context of the system and the organism. An excellent genetically tractable model organism to study autophagy is Drosophila, which appears to have a highly conserved autophagic machinery compared with mammals. However, the mechanisms of selective autophagy in Drosophila have been largely unexplored. The aim of this review is to summarize recent discoveries about the selectivity of autophagy in Drosophila.

References

[1]  Yang, Z.; Klionsky, D.J. Eaten alive: A history of macroautophagy. Nat. Cell Biol. 2010, 12, 814–822, doi:10.1038/ncb0910-814.
[2]  Simonsen, A.; Tooze, S.A. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J. Cell Biol. 2009, 186, 773–782, doi:10.1083/jcb.200907014.
[3]  Johansen, T.; Lamark, T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011, 7, 279–296, doi:10.4161/auto.7.3.14487.
[4]  Malagoli, D.; Abdalla, F.C.; Cao, Y.; Feng, Q.; Fujisaki, K.; Gregorc, A.; Matsuo, T.; Nezis, I.P.; Papassideri, I.S.; Sass, M.; et al. Autophagy and its physiological relevance in arthropods: Current knowledge and perspectives. Autophagy 2010, 6, 575–588, doi:10.4161/auto.6.5.11962.
[5]  Mizushima, N.; Komatsu, M. Autophagy: Renovation of cells and tissues. Cell 2011, 147, 728–741, doi:10.1016/j.cell.2011.10.026.
[6]  McPhee, C.K.; Baehrecke, E. Autophagy in Drosophila melanogaster. Biochim. Biophys. Acta 2009, 1793, 1452–1460, doi:10.1016/j.bbamcr.2009.02.009. 19264097
[7]  Onodera, J.; Ohsumi, Y. Ald6p is a preferred target for autophagy in yeast, Saccharomyces cerevisiae. J. Biol. Chem. 2004, 279, 16071–16076, doi:10.1074/jbc.M312706200.
[8]  Yu, L.; Wan, F.; Dutta, S.; Welsh, S.; Liu, Z.; Freundt, E.; Baehrecke, E.H.; Lenardo, M.J. Autophagic programmed cell death by selective catalase degradation. Proc. Natl. Acad. Sci. USA 2006, 103, 4952–4957, doi:10.1073/pnas.0511288103. 16547133
[9]  Webb, J.L.; Ravikumar, B.; Atkins, J.; Skepper, J.N.; Rubinsztein, D.C. Alpha-Synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 2003, 278, 25009–25013, doi:10.1074/jbc.M300227200. 12719433
[10]  Yu, L.; Strandberg, L.; Lenardo, M.J. The selectivity of autophagy and its role in cell death and survival. Autophagy 2008, 4, 567–573. 18362514
[11]  Nezis, I.P.; Shravage, B.V.; Sagona, A.P.; Lamark, T.; Bj?rk?y, G.; Johansen, T.; Rusten, T.E.; Brech, A.; Baehrecke, E.H.; Stenmark, H. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J. Cell Biol. 2010, 190, 523–531, doi:10.1083/jcb.201002035.
[12]  Nezis, I.P.; Stravopodis, D.J.; Papassideri, I.; Robert-Nicoud, M.; Margaritis, L.H. Stage-specific apoptotic patterns during Drosophila oogenesis. Eur. J. Cell Biol. 2000, 79, 610–620, doi:10.1078/0171-9335-00088.
[13]  Chou, T.B.; Perrimon, N. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 1996, 144, 1673–1679. 8978054
[14]  Pritchett, T.L.; McCall, K. Role of the insulin/Tor signaling network in starvation-induced programmed cell death in Drosophila oogenesis. Cell Death Differ. 2012, 19, 1069–1079, doi:10.1038/cdd.2011.200.
[15]  Nezis, I.P. Tissue-array analysis of atg8a mutants in Drosophila. Centre for Cancer Biomedicine, Faculty of Medicine, University of Oslo, Montebello, N-0310 Oslo, Norway. Unpublished work.
[16]  Nezis, I.P.; Simonsen, A.; Sagona, A.P.; Finley, K.; Gaumer, S.; Contamine, D.; Rusten, T.E.; Stenmark, H.; Brech, A. Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. J. Cell Biol. 2008, 180, 1065–1071, doi:10.1083/jcb.200711108.
[17]  Nezis, I.P.; Sagona, A.P.; Stenmark, H. Mechanisms of selective autophagic sequestration of dBruce in Drosophila. Centre for Cancer Biomedicine, Faculty of Medicine, University of Oslo, Montebello, N-0310 Oslo, Norway. Unpublished work.
[18]  Bass, B.P.; Tanner, E.A.; Mateos San Martín, D.; Blute, T.; Kinser, R.D.; Dolph, P. Cell-autonomous requirement for DNaseII in nonapoptotic cell death. Cell Death Differ. 2009, 16, 1362–1371, doi:10.1038/cdd.2009.79.
[19]  Sakurai, A.; Nakano, Y.; Koganezawa, M.; Yamamoto, D. Phenotypic interactions of spinster with the genes encoding proteins for cell death control in Drosophila melanogaster. Arch. Insect Biochem. Physiol. 2010, 73, 119–127, doi:10.1002/arch.20345.
[20]  Arama, E.; Agapite, J.; Steller, H. Caspase activity and a specific cytochrome C are required for sperm differentiation in Drosophila. Dev. Cell. 2003, 4, 687–697, doi:10.1016/S1534-5807(03)00120-5.
[21]  Pritchett, T.L.; Tanner, E.A.; McCall, K. Cracking open cell death in the Drosophila ovary. Apoptosis 2009, 14, 969–979, doi:10.1007/s10495-009-0369-z.
[22]  Rumpf, S.; Lee, S.B.; Jan, L.Y.; Jan, Y.N. Neuronal remodeling and apoptosis require VCP-dependent degradation of the apoptosis inhibitor DIAP1. Development 2011, 138, 1153–1160, doi:10.1242/dev.062703.
[23]  Ju, J.S.; Fuentealba, R.A.; Miller, S.E.; Jackson, E.; Piwnica-Worms, D.; Baloh, R.H.; Weihl, C.C. Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J. Cell Biol. 2009, 187, 875–888, doi:10.1083/jcb.200908115.
[24]  Wang, T.; Lao, U.; Edgar, B.A. TOR-mediated autophagy regulates cell death in Drosophila neurodegenerative disease. J. Cell Biol. 2009, 186, 703–711, doi:10.1083/jcb.200904090.
[25]  Nisoli, I.; Chauvin, J.P.; Napoletano, F.; Calamita, P.; Zanin, V.; Fanto, M.; Charroux, B. Neurodegeneration by polyglutamine Atrophin is not rescued by induction of autophagy. Cell Death Differ. 2010, 10, 1577–1587.
[26]  Fouillet, A.; Levet, C.; Virgone, A.; Robin, M.; Dourlen, P.; Rieusset, J.; Belaidi, E.; Ovize, M.; Touret, M.; Nataf, S.; Mollereau, B. ER stress inhibits neuronal death by promoting autophagy. Autophagy 2012, 8. PMID: 22660271. 22874567
[27]  Chinchore, Y.; Mitra, A.; Dolph, P.J. Accumulation of rhodopsin in late endosomes triggers photoreceptor cell degeneration. PLoS Genetics 2009, 5, e1000377, doi:10.1371/journal.pgen.1000377.
[28]  Midorikawa, R.; Yamamoto-Hino, M.; Awano, W.; Hinohara, Y.; Suzuki, E.; Ueda, R.; Goto, S. Autophagy-dependentrhodopsindegradationprevents retinal degeneration in Drosophila. J. Neurosci. 2010, 30, 10703–10719, doi:10.1523/JNEUROSCI.2061-10.2010. 20702701
[29]  Shen, W.; Ganetzky, B. Autophagy promotes synapse development in Drosophila. J. Cell Biol. 2009, 187, 71–79, doi:10.1083/jcb.200907109.
[30]  Shen, W.; Ganetzky, B. Nibbling away at synaptic development. Autophagy 2010, 6, 168–169, doi:10.4161/auto.6.1.10625.
[31]  Tian, X.; Li, J.; Valakh, V.; DiAntonio, A.; Wu, C. Drosophila Rae1 controls the abundance of the ubiquitin ligase Highwire in post-mitotic neurons. Nat. Neurosci. 2011, 14, 1267–1275, doi:10.1038/nn.2922. 21874015
[32]  Youle, R.J.; Narendra, D.P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 2011, 12, 9–14, doi:10.1038/nrm3028.
[33]  Deretic, V. Autophagy as an innate immunity paradigm: Expanding the scope and repertoire of pattern recognition receptors. Curr. Opin. Immunol. 2012, 24, 21–31, doi:10.1016/j.coi.2011.10.006.
[34]  Kanki, T.; Wang, K.; Cao, Y.; Baba, M.; Klionsky, D.J. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 2009, 17, 98–109, doi:10.1016/j.devcel.2009.06.014.
[35]  Novak, I.; Kirkin, V.; McEwan, D.G.E.; Zhang, J.; Wild, P.; Rozenknop, A.; Rogov, V.; L?hr, F.; Popovic, D.; Occhipinti, A.; et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11, 45–51, doi:10.1038/embor.2009.256. 20010802
[36]  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. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. USA 2007, 104, 19500–19505, doi:10.1073/pnas.0708818104. 18048346
[37]  Clark, I.E.; Dodson, M.W.; Jiang, C.; Cao, J.H.; Huh, J.R.; Seol, J.H.; Yoo, S.J.; Hay, B.A.; Guo, M. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 2006, 441, 1162–1166, doi:10.1038/nature04779. 16672981
[38]  Deng, H.; Dodson, M.W.; Huang, H.; Guo, M. The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl. Acad. Sci. USA 2008, 105, 14503–14508, doi:10.1073/pnas.0803998105. 18799731
[39]  Ziviani, E.; Tao, R.N.; Whitworth, A.J. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. USA 2010, 107, 5018–5023, doi:10.1073/pnas.0913485107. 20194754
[40]  Liu, S.; Lu, B. Reduction of protein translation and activation of autophagy protect against PINK1 pathogenesis in Drosophila melanogaster. PLoS Genetics 2010, 6, e1001237, doi:10.1371/journal.pgen.1001237.
[41]  Pimenta de Castro, I.; Costa, A.C.; Lam, D.; Tufi, R.; Fedele, V.; Moisoi, N.; Dinsdale, D.; Deas, E.; Loh, S.H.; Martins, L.M. Genetic analysis of mitochondrial protein misfolding in Drosophila melanogaster. Cell Death Differ. 2012, doi:10.1038/cdd.2012.5.
[42]  Yano, T.; Mita, S.; Ohmori, H.; Oshima, Y.; Fujimoto, Y.; Ueda, R.; Takada, H.; Goldman, W.E.; Fukase, K.; Silverman, N.; et al. Autophagic control of listeria through intracellular innate immune recognition in Drosophila. Nat. Immunol. 2008, 9, 908–916, doi:10.1038/ni.1634.
[43]  Shelly, S.; Lukinova, N.; Bambina, S.; Berman, A.; Cherry, S. Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 2009, 30, 588–598, doi:10.1016/j.immuni.2009.02.009.
[44]  Nakamoto, M.; Moy, R.H.; Xu, J.; Bambina, S.; Yasunaga, A.; Shelly, S.S.; Gold, B.; Cherry, S. Virus recognition by toll-7 activates antiviral autophagy in Drosophila. Immunity 2012, 36, 658–667, doi:10.1016/j.immuni.2012.03.003.
[45]  Mijaljica, D.; Prescott, M.; Devenish, R.J. The intricacy of nuclear membrane dynamics during nucleophagy. Nucleus 2010, 1, 213–223, doi:10.4161/nucl.1.3.11738.
[46]  Shoji, J.Y.; Kikuma, T.; Arioka, M.; Kitamoto, K. Macroautophagy-mediated degradation of whole nuclei in the filamentous fungus Aspergillus oryzae. PLoS One 2010, 5, e15650, doi:10.1371/journal.pone.0015650. 21187926
[47]  Lu, E.; Wolfe, J. Lysosomal enzymes in the macronucleus of Tetrahymena during its apoptosis-like degradation. Cell Death Differ. 2001, 8, 289–297, doi:10.1038/sj.cdd.4400807.
[48]  Krick, R.; Mühe, Y.; Prick, T.; Bredschneider, M.; Bremer, S.; Wenzel, D.; Eskelinen, E.L.; Thumm, M. Piecemeal microautophagy of the nucleus: Genetic and morphological traits. Autophagy 2009, 5, 270–272, doi:10.4161/auto.5.2.7639.
[49]  Park, Y.E.; Hayashi, Y.K.; Bonne, G.; Arimura, T.; Noguchi, S.; Nonaka, I.; Nishino, I. Autophagic degradation of nuclear components in mammalian cells. Autophagy 2009, 5, 795–804. 19550147
[50]  Rello-Varona, S.; Lissa, D.; Shen, S.; Niso-Santano, M.; Senovilla, L.; Mari?o, G.; Vitale, I.; Jemaá, M.; Harper, F.; Pierron, G.; et al. Autophagic removal of micronuclei. Cell Cycle 2012, 11, 170–176, doi:10.4161/cc.11.1.18564. 22185757
[51]  Wild, P.; Farhan, H.; McEwan, D.G.; Wagner, S.; Rogov, V.V.; Brady, N.R.; Richter, B.; Korac, J.; Waidmann, O.; Choudhary, C.; et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011, 333, 228–233, doi:10.1126/science.1205405. 21617041
[52]  Jiang, S.; Wells, C.D.; Roach, P.J. Starch-binding domain-containing protein 1 (Stbd1) and glycogen metabolism: Identification of the Atg8 family interacting motif (AIM) in Stbd1 required for interaction with GABARAPL1. Biochem. Biophys. Res. Commun. 2011, 413, 420–425, doi:10.1016/j.bbrc.2011.08.106.
[53]  Bj?rk?y, G.; Lamark, T.; Brech, A.; Outzen, H.; Perander, M.; Overvatn, A.; Stenmark, H.; Johansen, T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 2005, 171, 603–614, doi:10.1083/jcb.200507002.
[54]  Pankiv, S.; Clausen, T.H.; Lamark, T.; Brech, A.; Bruun, J.A.; Outzen, H. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282, 24131–24145, doi:10.1074/jbc.M702824200. 17580304
[55]  Moscat, J.; Diaz-Meco, M.T. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 2009, 137, 1001–1004, doi:10.1016/j.cell.2009.05.023.
[56]  Nezis, I.P.; Stenmark, H. p62 at the interphase of autophagy, oxidative stress signaling and cancer. Antioxid. Redox Sign. 2012. PMID: 22074114, in press.
[57]  Bartlett, B.J.; Isakson, P.; Lewerenz, J.; Sanchez, H.; Kotzebue, R.W.; Cumming, R.C.; Harris, G.L.; Nezis, I.P.; Schubert, D.R.; Simonsen, A.; et al. p62, Ref(2)P and ubiquitinated proteins are conserved markers of neuronal aging, aggregate formation and progressive autophagic defects. Autophagy 2011, 7, 572–583, doi:10.4161/auto.7.6.14943.
[58]  Taillebourg, E.; Gregoire, I.; Viargues, P.; Jacomin, A.C.; Thevenon, D.; Faure, M.; Fauvarque, M.O. The deubiquitinating enzyme USP36 controls selective autophagy activation by ubiquitinated proteins. Autophagy 2012, 8, 767–779, doi:10.4161/auto.19381.
[59]  Noda, N.N.; Ohsumi, Y.; Inagaki, F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett. 2010, 584, 1379–1385, doi:10.1016/j.febslet.2010.01.018.
[60]  Contamine, D.; Petitjean, A.M.; Ashburner, M. Genetic resistance to viral infection: The molecular cloning of a Drosophila gene that restricts infection by the rhabdovirus sigma. Genetics 1989, 123, 525–533. 2557263
[61]  Dezelee, S.; Bras, F.; Contamine, D.; Lopez-Ferber, M.; Segretain, D.; Teninges, D. Molecular analysis of ref(2)P, a Drosophila gene implicated in sigma rhabdovirus multiplication and necessary for male fertility. EMBO J. 1989, 8, 3437–3446. 2510997
[62]  Carré-Mlouka, A.; Gaumer, S.; Gay, P.; Petitjean, A.M.; Coulondre, C.; Dru, P.; Bras, F.; Dezélée, S.; Contamine, D. Control of sigma virus multiplication by the ref(2)P gene of Drosophila melanogaster: An in vivo study of the PB1 domain of Ref(2)P. Genetics 2007, 176, 409–419, doi:10.1534/genetics.106.063826.
[63]  Hogenhout, S.A.; Redinbaugh, M.G.; Ammarel, D. Plant and animal rhabdovirus host range: A bug’s view. Trends Microbiol. 2003, 11, 264–271, doi:10.1016/S0966-842X(03)00120-3.
[64]  Huszar, T.; Imler, J.L. Drosophila viruses and the study of antiviral host-defense. Adv. Virus Res. 2008, 72, 227–265, doi:10.1016/S0065-3527(08)00406-5.
[65]  Wyers, F.; Dru, P.; Simonet, B.; Contamine, D. Immunological cross-reactions and interactions between the Drosophila melanogaster ref(2)P protein and sigma rhabdovirus proteins. J. Virol. 1993, 67, 3208–3216. 7684462
[66]  Avila, A.; Silverman, N.; Diaz-Meco, M.T.; Moscat, J. The Drosophila atypical protein kinase C-ref(2)p complex constitutes a conserved module for signaling in the toll pathway. Mol. Cell. Biol. 2002, 22, 8787–8795, doi:10.1128/MCB.22.24.8787-8795.2002.
[67]  Goto, A.; Blandin, S.; Royet, J.; Reichhart, J.M.; Levashina, E.A. Silencing of Toll pathway components by direct injection of double-stranded RNA into Drosophila adult flies. Nucleic Acids Res. 2003, 31, 6619–6623, doi:10.1093/nar/gkg852. 14602922
[68]  Orvedahl, A.; MacPherson, S.; Sumpter, R., Jr.; Tallóczy, Z.; Zou, Z.; Levine, B. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 2010, 7, 15–127.
[69]  Kadandale, P.; Stender, J.D.; Glass, C.K.; Kiger, A.A. Conserved role for autophagy in Rho1-mediated cortical remodeling and blood cell recruitment. Proc. Natl. Acad. Sci. USA 2010, 107, 10502–10507, doi:10.1073/pnas.0914168107. 20498061
[70]  Simonsen, A.; Birkeland, H.C.; Gillooly, D.J.; Mizushima, N.; Kuma, A.; Yoshimori, T.; Slagsvold, T.; Brech, A.; Stenmark, H. Alfy, a novel FYVE-domain-containing protein associated with protein granules and autophagic membranes. J. Cell Sci. 2004, 117, 4239–4251, doi:10.1242/jcs.01287. 15292400
[71]  Filimonenko, M.; Isakson, P.; Finley, K.D.; Anderson, M.; Jeong, H.; Melia, T.J.; Bartlett, B.J.; Myers, K.M.; Birkeland, H.C.; Lamark, T.; et al. The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol. Cell 2010, 38, 265–279, doi:10.1016/j.molcel.2010.04.007.
[72]  Clausen, T.H.; Lamark, T.; Isakson, P.; Finley, K.; Larsen, K.B.; Brech, A. p62/SQSTM1 and ALFY interact to facilitate the formation of p62 bodies/ALIS and their degradation by autophagy. Autophagy 2010, 6, 330–344, doi:10.4161/auto.6.3.11226.
[73]  Finley, K.D.; Edeen, P.T.; Cumming, R.C.; Mardahl-Dumesnil, M.D.; Taylor, B.J.; Rodriguez, M.H.; Hwang, C.E.; Benedetti, M.; McKeown, M. blue cheese mutations define a novel, conserved gene involved in progressive neural degeneration. J. Neurosci. 2003, 23, 1254–1264. 12598614

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