Artículo

Melani, M.; Valko, A.; Romero, N.M.; Aguilera, M.O.; Acevedo, J.M.; Bhujabal, Z.; Perez-Perri, J.; De La Riva-Carrasco, R.V.; Katz, M.J.; Sorianello, E.; D'Alessio, C.; Juhász, G.; Johansen, T.; Colombo, M.I.; Wappner, P. "Zonda is a novel early component of the autophagy pathway in Drosophila" (2017) Molecular Biology of the Cell. 28(22):3070-3081
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Abstract:

Autophagy is an evolutionary conserved process by which eukaryotic cells undergo self-digestion of cytoplasmic components. Here we report that a novel Drosophila immunophilin, which we have named Zonda, is critically required for starvation-induced autophagy. We show that Zonda operates at early stages of the process, specifically for Vps34-mediated phosphatidylinositol 3-phosphate (PI3P) deposition. Zonda displays an even distribution under basal conditions and, soon after starvation, nucleates in endoplasmic reticulum-associated foci that colocalize with omegasome markers. Zonda nucleation depends on Atg1, Atg13, and Atg17 but does not require Vps34, Vps15, Atg6, or Atg14. Zonda interacts physically with Atg1 through its kinase domain, as well as with Atg6 and Vps34. We propose that Zonda is an early component of the autophagy cascade necessary for Vps34-dependent PI3P deposition and omegasome formation. © 2017 Melani, Valko, Romero, et al.

Registro:

Documento: Artículo
Título:Zonda is a novel early component of the autophagy pathway in Drosophila
Autor:Melani, M.; Valko, A.; Romero, N.M.; Aguilera, M.O.; Acevedo, J.M.; Bhujabal, Z.; Perez-Perri, J.; De La Riva-Carrasco, R.V.; Katz, M.J.; Sorianello, E.; D'Alessio, C.; Juhász, G.; Johansen, T.; Colombo, M.I.; Wappner, P.
Filiación:Fundación Instituto Leloir, Buenos Aires, 1405, Argentina
Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Buenos Aires, Argentina
Laboratorio de Biologia Celular y Molecular-Instituto de Histologia y Embriologia, Facultad de Ciencias Médicas, Universidad Nacional de Cuyo, Mendoza, 5500, Argentina
Molecular Cancer Research Group, Department of Medical Biology, University of Tromsø, Arctic University of Norway, Tromsø, 9037, Norway
Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales-Universidad de Buenos Aires, Buenos Aires, 1428, Argentina
Department of Anatomy, Cell and Developmental Biology, Eötvös Loránd University, Budapest, 1053, Hungary
Institute of Genetics, Biological Research Centre, Szeged, 6726, Hungary
University of Nice-Sophia Antipolis, Institute of Biology Valrose, Nice, 06108, France
German Cancer Research Center, Heidelberg, 69120, Germany
European Molecular Biology Laboratory, Heidelberg, 69117, Germany
Palabras clave:autophagy related protein; autophagy related protein 1; autophagy related protein 13; autophagy related protein 14; autophagy related protein 17; beclin 1; immunophilin; phosphatidylinositol 3 phosphate; protein serine threonine kinase VPS15; unclassified drug; zonda; autophagy related protein; Drosophila protein; immunophilin; phosphatidylinositol 3 kinase; phosphatidylinositol 3 phosphate; polyphosphoinositide; Article; autophagosome; autophagy; carboxy terminal sequence; controlled study; Drosophila melanogaster; endoplasmic reticulum; gene expression; gene function; gene locus; nonhuman; organelle biogenesis; priority journal; protein localization; protein protein interaction; protein structure; transmission electron microscopy; animal; autophagy; Drosophila melanogaster; genetics; metabolism; phagosome; physiology; signal transduction; Animals; Autophagy; Autophagy-Related Proteins; Class III Phosphatidylinositol 3-Kinases; Drosophila melanogaster; Drosophila Proteins; Immunophilins; Phagosomes; Phosphatidylinositol 3-Kinases; Phosphatidylinositol Phosphates; Signal Transduction
Año:2017
Volumen:28
Número:22
Página de inicio:3070
Página de fin:3081
DOI: http://dx.doi.org/10.1091/mbc.E16-11-0767
Título revista:Molecular Biology of the Cell
Título revista abreviado:Mol. Biol. Cell
ISSN:10591524
CODEN:MBCEE
CAS:phosphatidylinositol 3 kinase, 115926-52-8; Autophagy-Related Proteins; Class III Phosphatidylinositol 3-Kinases; Drosophila Proteins; Immunophilins; Phosphatidylinositol 3-Kinases; phosphatidylinositol 3-phosphate; Phosphatidylinositol Phosphates
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_10591524_v28_n22_p3070_Melani

Referencias:

  • Albu, S., Romanowski, C.P., Letizia Curzi, M., Jakubcakova, V., Flachskamm, C., Gassen, N.C., Hartmann, J., Rein, T., Deficiency of FK506-binding protein (FKBP) 51 alters sleep architecture and recovery sleep responses to stress in mice (2014) J Sleep Res, 23, pp. 176-185
  • Anding, A.L., Baehrecke, E.H., Vps15 is required for stress induced and developmentally triggered autophagy and salivary gland protein secretion in drosophila (2015) Cell Death Differ, 22, pp. 457-464
  • Axe, E.L., Walker, S.A., Manifava, M., Chandra, P., Roderick, H.L., Habermann, A., Griffiths, G., Ktistakis, N.T., Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum (2008) J Cell Biol, 182, pp. 685-701
  • Barth, J.M., Szabad, J., Hafen, E., Kohler, K., Autophagy in drosophila ovaries is induced by starvation and is required for oogenesis (2011) Cell Death Differ, 18, pp. 915-924
  • Barth, S., Edlich, F., Berchner-Pfannschmidt, U., Gneuss, S., Jahreis, G., Hasgall, P.A., Fandrey, J., Camenisch, G., Hypoxia-inducible factor prolyl-4-hydroxylase PHD2 protein abundance depends on integral membrane anchoring of FKBP38 (2009) J Biol Chem, 284, pp. 23046-23058
  • Bhujabal, Z., Birgisdottir, A.B., Sjottem, E., Brenne, H.B., Overvatn, A., Habisov, S., Kirkin, V., Johansen, T., FKBP8 recruits LC3A to mediate parkin-independent mitophagy (2017) EMBO Rep, 18, pp. 947-961
  • Biazik, J., Yla-Anttila, P., Vihinen, H., Jokitalo, E., Eskelinen, E.L., Ultrastructural relationship of the phagophore with surrounding organelles (2015) Autophagy, 11, pp. 439-451
  • Bjorkoy, 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 huntingtininduced cell death (2005) J Cell Biol, 171, pp. 603-614
  • Chang, Y.Y., Neufeld, T.P., An atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation (2009) Mol Biol Cell, 20, pp. 2004-2014
  • Chen, Y., Klionsky, D.J., The regulation of autophagy-unanswered questions (2011) J Cell Sci, 124, pp. 161-170
  • Entchev, E.V., Schwabedissen, A., Gonzalez-Gaitan, M., Gradient formation of the TGF-beta homolog dpp (2000) Cell, 103, pp. 981-991
  • Eskelinen, E.L., Maturation of autophagic vacuoles in Mammalian cells (2005) Autophagy, 1, pp. 1-10
  • Gillooly, D.J., Morrow, I.C., Lindsay, M., Gould, R., Bryant, N.J., Gaullier, J.M., Parton, R.G., Stenmark, H., Localization of phosphatidylinositol 3-phosphate in Yeast and Mammalian cells (2000) EMBO J, 19, pp. 4577-4588
  • Gu, W., Wan, D., Qian, Q., Yi, B., He, Z., Gu, Y., Wang, L., He, S., Ambra1 is an essential regulator of autophagy and apoptosis in SW620 cells: Prosurvival role of ambra1 (2014) PLoS One, 9, p. e90151
  • Hara, T., Mizushima, N., Role of ULK-FIP200 complex in Mammalian autophagy: FIP200, a counterpart of Yeast atg17? (2009) Autophagy, 5, pp. 85-87
  • Itakura, E., Mizushima, N., Characterization of autophagosome formation site by a hierarchical analysis of Mammalian atg proteins (2010) Autophagy, 6, pp. 764-776
  • Juhasz, G., Hill, J.H., Yan, Y., Sass, M., Baehrecke, E.H., Backer, J.M., Neufeld, T.P., The class III PI(3)K vps34 promotes autophagy and endocytosis but not TOR signaling in drosophila (2008) J Cell Biol, 181, pp. 655-666
  • Juhasz, G., Puskas, L.G., Komonyi, O., Erdi, B., Maroy, P., Neufeld, T.P., Sass, M., Gene expression profiling identifies FKBP39 as an inhibitor of autophagy in larval drosophila fat body (2007) Cell Death Differ, 14, pp. 1181-1190
  • Kamada, Y., Yoshino, K., Kondo, C., Kawamata, T., Oshiro, N., Yonezawa, K., Ohsumi, Y., Tor directly controls the atg1 kinase complex to regulate autophagy (2010) Mol Cell Biol, 30, pp. 1049-1058
  • Kang, C.B., Hong, Y., Dhe-Paganon, S., Yoon, H.S., FKBP family proteins: Immunophilins with versatile biological functions (2008) Neurosignals, 16, pp. 318-325
  • Karanasios, E., Ktistakis, N.T., Live-cell imaging for the assessment of the dynamics of autophagosome formation: Focus on early steps (2015) Methods, 75, pp. 54-60
  • Kishi-Itakura, C., Koyama-Honda, I., Itakura, E., Mizushima, N., Ultrastructural analysis of autophagosome organization using Mammalian autophagy-deficient cells (2014) J Cell Sci, 127, pp. 4089-4102
  • Laplante, M., Sabatini, D.M., MTOR signaling at a glance (2009) J Cell Sci, 122, pp. 3589-3594
  • Lee, S.B., Kim, S., Lee, J., Park, J., Lee, G., Kim, Y., Kim, J.M., Chung, J., ATG1, an autophagy regulator, inhibits cell growth by negatively regulating S6 kinase (2007) EMBO Rep, 8, pp. 360-365
  • Lindmo, K., Brech, A., Finley, K.D., Gaumer, S., Contamine, D., Rusten, T.E., Stenmark, H., The PI 3-kinase regulator vps15 is required for autophagic clearance of protein aggregates (2008) Autophagy, 4, pp. 500-506
  • Lu, Q., Yang, P., Huang, X., Hu, W., Guo, B., Wu, F., Lin, L., Zhang, H., The WD40 repeat PtdIns(3)P-binding protein EPG-6 regulates progression of omegasomes to autophagosomes (2011) Dev Cell, 21, pp. 343-357
  • Marquez, R.T., Xu, L., Bcl-2: Beclin 1 complex: Multiple, mechanisms regulating autophagy/apoptosis toggle switch (2012) Am J Cancer Res, 2, pp. 214-221
  • Matsunaga, K., Morita, E., Saitoh, T., Akira, S., Ktistakis, N.T., Izumi, T., Noda, T., Yoshimori, T., Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via atg14l (2010) J Cell Biol, 190, pp. 511-521
  • Mizushima, N., Levine, B., Cuervo, A.M., Klionsky, D.J., Autophagy fights disease through cellular self-digestion (2008) Nature, 451, pp. 1069-1075
  • Newsome, T.P., Asling, B., Dickson, B.J., Analysis of drosophila photoreceptor axon guidance in eye-specific mosaics (2000) Development, 127, pp. 851-860
  • Perrimon, N., Gans, M., Clonal analysis of the tissue specificity of recessive female-sterile mutations of drosophila melanogaster using a dominant female-sterile mutation Fs(1)K1237 (1983) Dev Biol, 100, pp. 365-373
  • Proikas-Cezanne, T., Takacs, Z., Donnes, P., Kohlbacher, O., WIPI proteins: Essential PtdIns3P effectors at the nascent autophagosome (2015) J Cell Sci, 128, pp. 207-217
  • Pulipparacharuvil, S., Akbar, M.A., Ray, S., Sevrioukov, E.A., Haberman, A.S., Rohrer, J., Kramer, H., Drosophila vps16a is required for trafficking to lysosomes and biogenesis of pigment granules (2005) J Cell Sci, 118, pp. 3663-3673
  • Roberts, R., Ktistakis, N.T., Omegasomes: PI3P platforms that manufacture autophagosomes (2013) Essays Biochem, 55, pp. 17-27
  • Russell, R.C., Tian, Y., Yuan, H., Park, H.W., Chang, Y.Y., Kim, J., Kim, H., Guan, K.L., ULK1 induces autophagy by phosphorylating beclin-1 and activating VPS34 lipid kinase (2013) Nat Cell Biol, 15, pp. 741-750
  • Saftig, P., Klumperman, J., Lysosome biogenesis and lysosomal membrane proteins: Trafficking meets function (2009) Nat Rev Mol Cell Biol, 10, pp. 623-635
  • Sanchez-Wandelmer, J., Ktistakis, N.T., Reggiori, F., ERES: Sites for autophagosome biogenesis and maturation? (2015) J Cell Sci, 128, pp. 185-192
  • Scott, R.C., Juhasz, G., Neufeld, T.P., Direct induction of autophagy by atg1 inhibits cell growth and induces apoptotic cell death (2007) Curr Biol, 17, pp. 1-11
  • Scott, R.C., Schuldiner, O., Neufeld, T.P., Role and regulation of starvation-induced autophagy in the drosophila fat body (2004) Dev Cell, 7, pp. 167-178
  • Shirane, M., Nakayama, K.I., Inherent calcineurin inhibitor FKBP38 targets bcl-2 to mitochondria and inhibits apoptosis (2003) Nat Cell Biol, 5, pp. 28-37
  • Shravage, B.V., Hill, J.H., Powers, C.M., Wu, L., Baehrecke, E.H., Atg6 is required for multiple vesicle trafficking pathways and hematopoiesis in drosophila (2013) Development, 140, pp. 1321-1329
  • Simonsen, A., Tooze, S.A., Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes (2009) J Cell Biol, 186, pp. 773-782
  • Spradling, A.C., Rubin, G.M., Transposition of cloned P elements into drosophila germ line chromosomes (1982) Science, 218, pp. 341-347
  • Tapon, N., Ito, N., Dickson, B.J., Treisman, J.E., Hariharan, I.K., The drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation (2001) Cell, 105, pp. 345-355
  • Wucherpfennig, T., Wilsch-Brauninger, M., Gonzalez-Gaitan, M., Role of drosophila rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release (2003) J Cell Biol, 161, pp. 609-624
  • Zhang, J., Schulze, K.L., Hiesinger, P.R., Suyama, K., Wang, S., Fish, M., Acar, M., Scott, M.P., Thirty-one flavors of drosophila rab proteins (2007) Genetics, 176, pp. 1307-1322

Citas:

---------- APA ----------
Melani, M., Valko, A., Romero, N.M., Aguilera, M.O., Acevedo, J.M., Bhujabal, Z., Perez-Perri, J.,..., Wappner, P. (2017) . Zonda is a novel early component of the autophagy pathway in Drosophila. Molecular Biology of the Cell, 28(22), 3070-3081.
http://dx.doi.org/10.1091/mbc.E16-11-0767
---------- CHICAGO ----------
Melani, M., Valko, A., Romero, N.M., Aguilera, M.O., Acevedo, J.M., Bhujabal, Z., et al. "Zonda is a novel early component of the autophagy pathway in Drosophila" . Molecular Biology of the Cell 28, no. 22 (2017) : 3070-3081.
http://dx.doi.org/10.1091/mbc.E16-11-0767
---------- MLA ----------
Melani, M., Valko, A., Romero, N.M., Aguilera, M.O., Acevedo, J.M., Bhujabal, Z., et al. "Zonda is a novel early component of the autophagy pathway in Drosophila" . Molecular Biology of the Cell, vol. 28, no. 22, 2017, pp. 3070-3081.
http://dx.doi.org/10.1091/mbc.E16-11-0767
---------- VANCOUVER ----------
Melani, M., Valko, A., Romero, N.M., Aguilera, M.O., Acevedo, J.M., Bhujabal, Z., et al. Zonda is a novel early component of the autophagy pathway in Drosophila. Mol. Biol. Cell. 2017;28(22):3070-3081.
http://dx.doi.org/10.1091/mbc.E16-11-0767