Condition-dependent functional shift of two Drosophila Mtmr lipid phosphatases in autophagy control

References

• Robinson FL, Dixon JE. Myotubularin phosphatases: policing 3-phosphoinositides. Trends Cell Biol. 2006 Aug;16(8):403–412.
   PubMed Web of Science ®Google Scholar
• Alonso A, Sasin J, Bottini N, et al. Protein tyrosine phosphatases in the human genome. Cell. 2004 Jun 11 117;(6):699–711.
   PubMed Web of Science ®Google Scholar
• Raess MA, Friant S, Cowling BS, et al. WANTED - Dead or alive: myotubularins, a large disease-associated protein family. Adv Biol Regul. 2017 Jan;63:49–58.
   PubMedGoogle Scholar
• Laporte J, Hu LJ, Kretz C, et al. A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nature Genet. 1996 Jun 13;(2):175–182.
   PubMed Web of Science ®Google Scholar
• Laporte J, Bedez F, Bolino A, et al. Myotubularins, a large disease-associated family of cooperating catalytically active and inactive phosphoinositides phosphatases. Hum Mol Genet. 12(2): Spec No. R285–92. 2003 Oct 15.
   PubMedGoogle Scholar
• Hnia K, Vaccari I, Bolino A, et al. Myotubularin phosphoinositide phosphatases: cellular functions and disease pathophysiology. Trend Molecul Med. 2012 Jun;18:(6)317–327.
   PubMed Web of Science ®Google Scholar
• Dall’Armi C, Devereaux KA, Di Paolo G. The role of lipids in the control of autophagy. Curr Biol. 2013 Jan 7;23(1):R33–45.
   PubMed Web of Science ®Google Scholar
• Martens S, Nakamura S, Yoshimori T. Phospholipids in Autophagosome Formation and Fusion. J Mol Biol. 2016 Oct;428:4819–4827.
   Web of Science ®Google Scholar
• Billes V, Kovacs T, Manzeger A, et al. Developmentally regulated autophagy is required for eye formation in Drosophila. Autophagy. 2018;14(9):1499–1519.
   PubMed Web of Science ®Google Scholar
• Fodor E, Sigmond T, Ari E, et al. Methods to Study Autophagy in Zebrafish. Methods Enzymol. 2017;588:467–496.
   PubMed Web of Science ®Google Scholar
• Sigmond T, Barna J, Toth ML, et al. Autophagy in Caenorhabditis elegans. Methods Enzymol. 2008;451:521–540.
   PubMed Web of Science ®Google Scholar
• Varga M, Fodor E, Vellai T. Autophagy in zebrafish. Methods. 2015 Mar;75:172–180.
   PubMed Web of Science ®Google Scholar
• Vellai T, Takacs-Vellai K. Regulation of protein turnover by longevity pathways. Adv Exp Med Biol. 2010;694:69–80.
   PubMed Web of Science ®Google Scholar
• Takacs-Vellai K, Bayci A, Vellai T. Autophagy in neuronal cell loss: a road to death. Bioessays 2006 Nov;28(11):1126–1131.
   PubMed Web of Science ®Google Scholar
• Feng Y, He D, Yao Z, et al. The machinery of macroautophagy. Cell Res. 2014 Jan;24(1):24–41.
   PubMed Web of Science ®Google Scholar
• Meijer WH, Van Der Klei IJ, Veenhuis M, et al. ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective Cvt and pexophagy pathways also require organism-specific genes. Autophagy. 2007 Mar-Apr;3(2):106–116.
   PubMed Web of Science ®Google Scholar
• Gillooly DJ, Morrow IC, Lindsay M, et al. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. Embo J. 2000 Sep 1;19(17):4577–4588.
   PubMed Web of Science ®Google Scholar
• Petiot A, Ogier-Denis E, Blommaart EF, et al. Distinct classes of phosphatidylinositol 3ʹ-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem. 2000 Jan 14;275(2):992–998.
   PubMed Web of Science ®Google Scholar
• Roggo L, Bernard V, Kovacs AL, et al. Membrane transport in Caenorhabditis elegans: an essential role for VPS34 at the nuclear membrane. Embo J. 2002 Apr 2;21(7):1673–1683.
   PubMed Web of Science ®Google Scholar
• Wucherpfennig T, Wilsch-Brauninger M, Gonzalez-Gaitan M. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J Cell Biol. 2003 May 12;161(3):609–624.
   PubMed Web of Science ®Google Scholar
• Gary JD, Wurmser AE, Bonangelino CJ, et al. Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol. 1998 Oct 5;143(1):65–79.
   PubMed Web of Science ®Google Scholar
• Nicot AS, Fares H, Payrastre B. The Phosphoinositide Kinase PIKfyve/Fab1p Regulates Terminal Lysosome Maturation in Caenorhabditis elegans? Mol Biol Cell. 2006;17(7):3062–3074.
   PubMed Web of Science ®Google Scholar
• Rusten TE, Vaccari T, Lindmo K, et al. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol. 2007 Oct 23;17(20):1817–1825.
   PubMed Web of Science ®Google Scholar
• Ferguson CJ, Lenk GM, Meisler MH. Defective autophagy in neurons and astrocytes from mice deficient in PI(3,5)P2. Hum Mol Genet. 2009 Dec 15;18(24):4868–4878.
   PubMed Web of Science ®Google Scholar
• Vicinanza M, Korolchuk VI, Ashkenazi A, et al. PI(5)P Regulates Autophagosome Biogenesis. Mol Cell. 2015 Jan 22;57(2):219–234.
   PubMed Web of Science ®Google Scholar
• Vergne I, Deretic V. The role of PI3P phosphatases in the regulation of autophagy. FEBS Lett. 2010 Apr 2;584(7):1313–1318.
   PubMed Web of Science ®Google Scholar
• Al-Qusairi L, Prokic I, Amoasii L, et al. Lack of myotubularin (MTM1) leads to muscle hypotrophy through unbalanced regulation of the autophagy and ubiquitin-proteasome pathways. Faseb J. 2013 Aug 27;(8):3384–3394.
   PubMed Web of Science ®Google Scholar
• Dowling JJ, Low SE, Busta AS, et al. Zebrafish MTMR14 is required for excitation-contraction coupling, developmental motor function and the regulation of autophagy. Hum Mol Genet. 2010 Jul 1;19(13):2668–2681.
   PubMed Web of Science ®Google Scholar
• Hao F, Itoh T, Morita E, et al. The PtdIns3-phosphatase MTMR3 interacts with mTORC1 and suppresses its activity. FEBS Lett. 2016 Jan;590(1):161–173.
   PubMed Web of Science ®Google Scholar
• Taguchi-Atarashi N, Hamasaki M, Matsunaga K, et al. Modulation of local PtdIns3P levels by the PI phosphatase MTMR3 regulates constitutive autophagy. Traffic. 2010 Apr;11(4):468–478.
   PubMed Web of Science ®Google Scholar
• Velichkova M, Juan J, Kadandale P, et al. Drosophila Mtm and class II PI3K coregulate a PI(3)P pool with cortical and endolysosomal functions. J Cell Biol. 2010 Aug 9;190(3):407–425.
   PubMed Web of Science ®Google Scholar
• Yu X, Ma J, Lin F, et al. Myotubularin family phosphatase ceMTM3 is required for muscle maintenance by preventing excessive autophagy in Caenorhabditis elegans. BMC Cell Biol. 2012;13(1):28.
   PubMedGoogle Scholar
• Wu Y, Cheng S, Zhao H, et al. PI3P phosphatase activity is required for autophagosome maturation and autolysosome formation. EMBO Rep. 2014 Aug;15(9):14.
   Web of Science ®Google Scholar
• Vergne I, Roberts E, Elmaoued RA, et al. Control of autophagy initiation by phosphoinositide 3-phosphatase Jumpy. Embo J. 2009 Aug 5;28(15):2244–2258.
   PubMed Web of Science ®Google Scholar
• Zou J, Majerus PW, Wilson DB, et al. The role of myotubularin-related phosphatases in the control of autophagy and programmed cell death. Adv Biol Regul. 2012 Jan;52(1):282–289.
   PubMedGoogle Scholar
• Weidner P, Sohn M, Gutting T, et al. Myotubularin-related protein 7 inhibits insulin signaling in colorectal cancer. Oncotarget. 2016 Aug 02;7(31):50490–50506.
   PubMedGoogle Scholar
• Jean S, Cox S, Nassari S, et al. Starvation-induced MTMR13 and RAB21 activity regulates VAMP8 to promote autophagosome-lysosome fusion. EMBO Rep. 2015 Feb;16(3):3.
   Web of Science ®Google Scholar
• Hnia K, Kretz C, Amoasii L, et al. Primary T-tubule and autophagy defects in the phosphoinositide phosphatase Jumpy/MTMR14 knockout mice muscle. Adv Biol Regul. 2012 Jan;52(1):98–107.
   PubMedGoogle Scholar
• Liu J, Lv Y, Liu QH, et al. Deficiency of MTMR14 promotes autophagy and proliferation of mouse embryonic fibroblasts. Mol Cell Biochem. 13. 2014 Mar;392(1–2):31–37.
   PubMed Web of Science ®Google Scholar
• Kovács T, Billes V, Komlós M, et al. The small molecule AUTEN-99 (autophagy enhancer-99) prevents the progression of neurodegenerative symptoms. Sci Rep. 2017 Feb 16;7(1):42014.
   PubMedGoogle Scholar
• Papp D, Kovács T, Billes V, et al. AUTEN-67, an autophagy-enhancing drug candidate with potent antiaging and neuroprotective effects. Autophagy. 2016 Feb;12(2):273–286.
   PubMed Web of Science ®Google Scholar
• Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell. 2004 Aug;7(2):167–178.
   PubMed Web of Science ®Google Scholar
• Allen EA, Amato C, Fortier TM, et al. A conserved myotubularin-related phosphatase regulates autophagy by maintaining autophagic flux. J Cell Biol. 2020 Nov 2;219(11):11.
   Web of Science ®Google Scholar
• Mauvezin C, Ayala C, Braden CR, et al. Assays to monitor autophagy in Drosophila. Methods. 2014 Mar 22;68(1):134–139.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(1):1–222.
   PubMed Web of Science ®Google Scholar
• Takáts S, Nagy P, Á V, et al. Autophagosomal Syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila. J Cell Biol. 2013 May 13;201(4):531–539.
   PubMed Web of Science ®Google Scholar
• Jiang P, Nishimura T, Sakamaki Y, et al. The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol Biol Cell. 2014 Apr;25(8):1327–1337.
   PubMed Web of Science ®Google Scholar
• Chang YY, Neufeld TP. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol Biol Cell. 2009 Apr;20(7):2004–2014.
   PubMed Web of Science ®Google Scholar
• Nascimbeni AC, Codogno P, Morel E. Local detection of PtdIns3P at autophagosome biogenesis membrane platforms. Autophagy. 2017 Sep 2;13(9):1602–1612.
   PubMed Web of Science ®Google Scholar
• Itakura E, Kishi C, Inoue K, et al. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell. 2008 Dec;19(12):5360–5372.
   PubMed Web of Science ®Google Scholar
• Hegedűs K, Takáts S, Boda A, et al. The Ccz1-Mon1-Rab7 module and Rab5 control distinct steps of autophagy. Mol Biol Cell. 2016 Oct 15;27(20):3132–3142.
   PubMed Web of Science ®Google Scholar
• Rabinowitz JD, White E. Autophagy and metabolism. Science. 2010 Dec 03;330(6009):1344–1348.
   PubMed Web of Science ®Google Scholar
• Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Diff. 2009 Jul;16(7):1040–1052.
   PubMed Web of Science ®Google Scholar
• Nivon M, Richet E, Codogno P, et al. Autophagy activation by NFkappaB is essential for cell survival after heat shock. Autophagy. 2009 Aug 5;(6)766–783.
   PubMed Web of Science ®Google Scholar
• Wu H, Wang MC, Bohmann D. JNK protects Drosophila from oxidative stress by trancriptionally activating autophagy. Mech Dev. 2009 Aug-Sep;126(8–9):624–637.
   PubMed Web of Science ®Google Scholar
• Pircs K, Nagy P, Varga A, et al. Advantages and limitations of different p62-based assays for estimating autophagic activity in Drosophila. PloS One. 2012;7(8):e44214.
   PubMed Web of Science ®Google Scholar
• Cao C, Backer JM, Laporte J, et al. Sequential actions of myotubularin lipid phosphatases regulate endosomal PI(3)P and growth factor receptor trafficking. Mol Biol Cell. 2008 Aug;19(8):3334–3346.
   PubMed Web of Science ®Google Scholar
• Gillingham AK, Sinka R, Torres IL, et al. Toward a comprehensive map of the effectors of rab GTPases. Dev Cell. 2014 Nov 10;31(3):358–373.
   PubMed Web of Science ®Google Scholar
• Vellai T, Takacs-Vellai K, Sass M, et al. The regulation of aging: does autophagy underlie longevity? Trends Cell Biol. 2009 Oct;19(10):487–494.
   PubMed Web of Science ®Google Scholar
• Maekawa M, Terasaka S, Mochizuki Y, et al. Sequential breakdown of 3-phosphorylated phosphoinositides is essential for the completion of macropinocytosis. Proc Natl Acad Sci U S A. 2014 Mar 18;111(11):E978–87.
   PubMed Web of Science ®Google Scholar
• Lőrincz P, Lakatos Z, Maruzs T, et al. Atg6/UVRAG/Vps34-containing lipid kinase complex is required for receptor downregulation through endolysosomal degradation and epithelial polarity during Drosophila wing development. Biol Med Res Int. 2014;2014:851349.
   Web of Science ®Google Scholar
• Erdélyi P, Borsos E, Takács-Vellai K, et al. Shared developmental roles and transcriptional control of autophagy and apoptosis in Caenorhabditis elegans. J Cell Sci. 2011 May 1;124(Pt 9):1510–1518.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature. 2008 Feb 28;451(7182):1069–1075.
   PubMed Web of Science ®Google Scholar
• Towers CG, Thorburn A. Therapeutic Targeting of Autophagy. EBioMedicine. 2016 Dec;14:15–23.
   PubMed Web of Science ®Google Scholar
• Billes V, Kovács T, Hotzi B, et al. AUTEN-67 (Autophagy Enhancer-67) Hampers the Progression of Neurodegenerative Symptoms in a Drosophila model of Huntington’s Disease. J Huntington’s Dis. 2016 May 07 5;(2)133–147.
   PubMed Web of Science ®Google Scholar
• Vedelek V, Laurinyecz B, Kovács AL, et al. Testis-Specific Bb8 Is Essential in the Development of Spermatid Mitochondria. PloS One. 2016;11(8):e0161289.
   PubMed Web of Science ®Google Scholar
• Juhász G, Érdi B, Sass M, et al. Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila. Genes Dev. 2007 Dec 1 21;(23)3061–3066.
   PubMed Web of Science ®Google Scholar
• Nagy P, Hegedűs K, Pircs K, et al. Different effects of Atg2 and Atg18 mutations on Atg8a and Atg9 trafficking during starvation in Drosophila. FEBS Lett. 2013 Dec 588;(3)24.
   Web of Science ®Google Scholar
• Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993 Jun;118(2):401–415.
   PubMed Web of Science ®Google Scholar
• Bischof J, Maeda RK, Hediger M, et al. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3312–3317.
   PubMed Web of Science ®Google Scholar
• Venken KJ, Carlson JW, Schulze KL, et al. Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat Methods. 2009 Jun;6(6):431–434.
   PubMed Web of Science ®Google Scholar
• Nagy P, Karpati M, Varga A, et al. Atg17/FIP200 localizes to perilysosomal Ref(2)P aggregates and promotes autophagy by activation of Atg1 in Drosophila. Autophagy. 2014 Jan 6;10(3):3.
   PubMed Web of Science ®Google Scholar
• Schneider CA, Rasband WS, Eliceiri KWNIH. Image to ImageJ: 25 years of image analysis. Nat Methods. 2012 Jul;9(7):671–675.
   PubMed Web of Science ®Google Scholar
• Rao X, Huang X, Zhou Z, et al. An improvement of the 2ˆ(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat Bioinforma Biomath. [2013 Aug];3(3):71–85.
   PubMedGoogle Scholar
• Bland JM, Altman DG. Survival probabilities (the Kaplan-Meier method). BMJ (Clin Res Ed). 1998 Dec 5;317(7172):1572.
   PubMedGoogle Scholar