210
Views
68
CrossRef citations to date
0
Altmetric
Article

Atg13 Is Essential for Autophagy and Cardiac Development in Mice

&
Pages 585-595 | Received 07 Nov 2015, Accepted 23 Nov 2015, Published online: 17 Mar 2023

REFERENCES

  • Levine B, Kroemer G. 2008. Autophagy in the pathogenesis of disease. Cell 132:27–42. http://dx.doi.org/10.1016/j.cell.2007.12.018.
  • Tooze SA, Yoshimori T. 2010. The origin of the autophagosomal membrane. Nat Cell Biol 12:831–835. http://dx.doi.org/10.1038/ncb0910-831.
  • Mizushima N, Komatsu M. 2011. Autophagy: renovation of cells and tissues. Cell 147:728–741. http://dx.doi.org/10.1016/j.cell.2011.10.026.
  • Cecconi F, Levine B. 2008. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev Cell 15:344–357. http://dx.doi.org/10.1016/j.devcel.2008.08.012.
  • Levine B, Mizushima N, Virgin HW. 2011. Autophagy in immunity and inflammation. Nature 469:323–335. http://dx.doi.org/10.1038/nature09782.
  • Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. 2009. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10:458–467. http://dx.doi.org/10.1038/nrm2708.
  • Mizushima N, Yoshimori T, Ohsumi Y. 2011. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27:107–132. http://dx.doi.org/10.1146/annurev-cellbio-092910-154005.
  • Mizushima N. 2010. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22:132–139. http://dx.doi.org/10.1016/j.ceb.2009.12.004.
  • Wong PM, Puente C, Ganley IG, Jiang X. 2013. The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy 9:124–137. http://dx.doi.org/10.4161/auto.23323.
  • Lynch-Day MA, Klionsky DJ. 2010. The Cvt pathway as a model for selective autophagy. FEBS Lett 584:1359–1366. http://dx.doi.org/10.1016/j.febslet.2010.02.013.
  • Cheong H, Nair U, Geng J, Klionsky DJ. 2008. The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol Biol Cell 19:668–681.
  • Kawamata T, Kamada Y, Kabeya Y, Sekito T, Ohsumi Y. 2008. Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell 19:2039–2050. http://dx.doi.org/10.1091/mbc.E07-10-1048.
  • Hara T, Takamura A, Kishi C, Iemura S, Natsume T, Guan JL, Mizushima N. 2008. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 181:497–510. http://dx.doi.org/10.1083/jcb.200712064.
  • Chan EYW, Longatti A, McKnight NC, Tooze SA. 2009. Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domain using an Atg13-independent mechanism. Mol Cell Biol 29:157–171. http://dx.doi.org/10.1128/MCB.01082-08.
  • Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, Guan JL, Oshiro N, Mizushima N. 2009. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20:1981–1991. http://dx.doi.org/10.1091/mbc.E08-12-1248.
  • Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DH. 2009. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20:1992–2003. http://dx.doi.org/10.1091/mbc.E08-12-1249.
  • Ganley IG, Lam DH, Wang J, Ding X, Chen S, Jiang X. 2009. ULK1-ATG13-FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 284:12297–12305. http://dx.doi.org/10.1074/jbc.M900573200.
  • Mercer CA, Kaliappan A, Dennis PB. 2009. A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 5:649–662. http://dx.doi.org/10.4161/auto.5.5.8249.
  • Hosokawa N, Sasaki T, Iemura S, Natsume T, Hara T, Mizushima N. 2009. Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 5:973–979. http://dx.doi.org/10.4161/auto.5.7.9296.
  • Gan B, Peng X, Nagy T, Alcaraz A, Gu H, Guan JL. 2006. Role of FIP200 in cardiac and liver development and its regulation of TNFα and TSC-mTOR signaling pathways. J Cell Biol 175:121–133. http://dx.doi.org/10.1083/jcb.200604129.
  • Sou YS, Waguri S, Iwata J, Ueno T, Fujimura T, Hara T, Sawada N, Yamada A, Mizushima N, Uchiyama Y, Kominami E, Tanaka K, Komatsu M. 2008. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice. Mol Biol Cell 19:4762–4775. http://dx.doi.org/10.1091/mbc.E08-03-0309.
  • Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. 2004. The role of autophagy during the early neonatal starvation period. Nature 432:1032–1036. http://dx.doi.org/10.1038/nature03029.
  • Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T. 2005. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169:425–434. http://dx.doi.org/10.1083/jcb.200412022.
  • Saitoh T, Fujita N, Hayashi T, Takahara K, Satoh T, Lee H, Matsunaga K, Kageyama S, Omori H, Noda T, Yamamoto N, Kawai T, Ishii K, Takeuchi O, Yoshimori T, Akira S. 2009. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci U S A 106:20842–20846. http://dx.doi.org/10.1073/pnas.0911267106.
  • Malhotra R, Warne JP, Salas E, Xu AW, Debnath J. 2015. Loss of Atg12, but not Atg5, in pro-opiomelanocortin neurons exacerbates diet-induced obesity. Autophagy 11:145–154. http://dx.doi.org/10.1080/15548627.2014.998917.
  • Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, Tanaka K, Kawai T, Tsujimura T, Takeuchi O, Yoshimori T, Akira S. 2008. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production. Nature 456:264–268. http://dx.doi.org/10.1038/nature07383.
  • Kojima T, Yamada T, Akaishi R, Furuta I, Saitoh T, Nakabayashi K, Nakayama KI, Nakayama K, Akira S, Minakami H. 2015. Role of the Atg9a gene in intrauterine growth and survival of fetal mice. Reprod Biol 15:131–138. http://dx.doi.org/10.1016/j.repbio.2015.05.001.
  • Cheong H, Wu J, Gonzales LK, Guttentag SH, Thompson CB, Lindsten T. 2014. Analysis of a lung defect in autophagy-deficient mouse strains. Autophagy 10:45–56. http://dx.doi.org/10.4161/auto.26505.
  • Gan B, Guan JL. 2008. FIP200, a key signaling node to coordinately regulate various cellular processes. Cell Signal 20:787–794. http://dx.doi.org/10.1016/j.cellsig.2007.10.021.
  • Choi JD, Ryu M, Ae Park M, Jeong G, Lee JS. 2013. FIP200 inhibits β-catenin-mediated transcription by promoting APC-independent beta-catenin ubiquitination. Oncogene 32:2421–2432. http://dx.doi.org/10.1038/onc.2012.262.
  • Koinuma D, Shinozaki M, Nagano Y, Ikushima H, Horiguchi K, Goto K, Chano T, Saitoh M, Imamura T, Miyazono K, Miyazawa K. 2011. RB1CC1 positively regulates transforming growth factor-β signaling through the modulation of Arkadia E3 ubiquitin ligase activity. J Biol Chem 286:32502–32512. http://dx.doi.org/10.1074/jbc.M111.227561.
  • Ogura K, Wicky C, Magnenat L, Tobler H, Mori I, Muller F, Ohshima Y. 1994. Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase. Genes Dev 8:2389–2400. http://dx.doi.org/10.1101/gad.8.20.2389.
  • Ogura K, Shirakawa M, Barnes TM, Hekimi S, Ohshima Y. 1997. The UNC-14 protein required for axonal elongation and guidance in Caenorhabditis elegans interacts with the serine/threonine kinase UNC-51. Genes Dev 11:1801–1811. http://dx.doi.org/10.1101/gad.11.14.1801.
  • Lai T, Garriga G. 2004. The conserved kinase UNC-51 acts with VAB-8 and UNC-14 to regulate axon outgrowth in C. elegans. Development 131:5991–6000. http://dx.doi.org/10.1242/dev.01457.
  • Ogura K, Goshima Y. 2006. The autophagy-related kinase UNC-51 and its binding partner UNC-14 regulate the subcellular localization of the Netrin receptor UNC-5 in Caenorhabditis elegans. Development 133:3441–3450. http://dx.doi.org/10.1242/dev.02503.
  • Ogura K, Okada T, Mitani S, Gengyo-Ando K, Baillie DL, Kohara Y, Goshima Y. 2010. Protein phosphatase 2A cooperates with the autophagy-related kinase UNC-51 to regulate axon guidance in Caenorhabditis elegans. Development 137:1657–1667. http://dx.doi.org/10.1242/dev.050708.
  • Tian E, Wang F, Han J, Zhang H. 2009. epg-1 functions in autophagy-regulated processes and may encode a highly divergent Atg13 homolog in C. elegans. Autophagy 5:608–615. http://dx.doi.org/10.4161/auto.5.5.8624.
  • Liang Q, Yang P, Tian E, Han J, Zhang H. 2012. The C. elegans ATG101 homolog EPG-9 directly interacts with EPG-1/Atg13 and is essential for autophagy. Autophagy 8:1426–1433. http://dx.doi.org/10.4161/auto.21163.
  • Toda H, Mochizuki H, Flores R, III, Josowitz R, Krasieva TB, Lamorte VJ, Suzuki E, Gindhart JG, Furukubo-Tokunaga K, Tomoda T. 2008. UNC-51/ATG1 kinase regulates axonal transport by mediating motor-cargo assembly. Genes Dev 22:3292–3307. http://dx.doi.org/10.1101/gad.1734608.
  • Mochizuki H, Toda H, Ando M, Kurusu M, Tomoda T, Furukubo-Tokunaga K. 2011. Unc-51/ATG1 controls axonal and dendritic development via kinesin-mediated vesicle transport in the Drosophila brain. PLoS One 6:e19632. http://dx.doi.org/10.1371/journal.pone.0019632.
  • Ahantarig A, Chadwell LV, Terrazas IB, Garcia CT, Nazarian JJ, Lee HK, Lundell MJ, Cassill JA. 2009. Molecular characterization of Pegarn: a Drosophila homolog of UNC-51 kinase. Mol Biol Rep 36:1311–1321. http://dx.doi.org/10.1007/s11033-008-9314-4.
  • Tomoda T, Bhatt RS, Kuroyanagi H, Shirasawa T, Hatten ME. 1999. A mouse serine/threonine kinase homologous to C. elegans UNC51 functions in parallel fiber formation of cerebellar granule neurons. Neuron 24:833–846. http://dx.doi.org/10.1016/S0896-6273(00)81031-4.
  • Tomoda T, Kim JH, Zhan C, Hatten ME. 2004. Role of Unc51.1 and its binding partners in CNS axon outgrowth. Genes Dev 18:541–558. http://dx.doi.org/10.1101/gad.1151204.
  • Zhou X, Babu JR, da Silva S, Shu Q, Graef IA, Oliver T, Tomoda T, Tani T, Wooten MW, Wang F. 2007. Unc-51-like kinase 1/2-mediated endocytic processes regulate filopodia extension and branching of sensory axons. Proc Natl Acad Sci U S A 104:5842–5847. http://dx.doi.org/10.1073/pnas.0701402104.
  • Sander JD, Joung JK. 2014. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32:347–355. http://dx.doi.org/10.1038/nbt.2842.
  • Ota S, Hisano Y, Muraki M, Hoshijima K, Dahlem TJ, Grunwald DJ, Okada Y, Kawahara A. 2013. Efficient identification of TALEN-mediated genome modifications using heteroduplex mobility assays. Genes Cells 18:450–458. http://dx.doi.org/10.1111/gtc.12050.
  • Cheong H, Lindsten T, Wu J, Lu C, Thompson CB. 2011. Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc Natl Acad Sci U S A 108:11121–11126. http://dx.doi.org/10.1073/pnas.1107969108.
  • McAlpine F, Williamson LE, Tooze SA, Chan EY. 2013. Regulation of nutrient-sensitive autophagy by uncoordinated 51-like kinases 1 and 2. Autophagy 9:361–373. http://dx.doi.org/10.4161/auto.23066.
  • Nishimura T, Kaizuka T, Cadwell K, Sahani MH, Saitoh T, Akira S, Virgin HW, Mizushima N. 2013. FIP200 regulates targeting of Atg16L1 to the isolation membrane. EMBO Rep 14:284–291. http://dx.doi.org/10.1038/embor.2013.6.
  • Quy PN, Kuma A, Pierre P, Mizushima N. 2013. Proteasome-dependent activation of mammalian target of rapamycin complex 1 (mTORC1) is essential for autophagy suppression and muscle remodeling following denervation. J Biol Chem 288:1125–1134. http://dx.doi.org/10.1074/jbc.M112.399949.
  • Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, Natsume T, Ohsumi Y, Yoshimori T. 2003. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 116:1679–1688. http://dx.doi.org/10.1242/jcs.00381.
  • Itakura E, Kishi-Itakura C, Koyama-Honda I, Mizushima N. 2012. Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J Cell Sci 125:1488–1499. http://dx.doi.org/10.1242/jcs.094110.
  • Itakura E, Kishi C, Inoue K, Mizushima N. 2008. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19:5360–5372. http://dx.doi.org/10.1091/mbc.E08-01-0080.
  • Itakura E, Mizushima N. 2010. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 6:764–776. http://dx.doi.org/10.4161/auto.6.6.12709.
  • Shang L, Chen S, Du F, Li S, Zhao L, Wang X. 2011. Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK. Proc Natl Acad Sci U S A 108:4788–4793. http://dx.doi.org/10.1073/pnas.1100844108.
  • Hieke N, Loffler AS, Kaizuka T, Berleth N, Bohler P, Driessen S, Stuhldreier F, Friesen O, Assani K, Schmitz K, Peter C, Diedrich B, Dengjel J, Holland P, Simonsen A, Wesselborg S, Mizushima N, Stork B. 2015. Expression of a ULK1/2 binding-deficient ATG13 variant can partially restore autophagic activity in ATG13-deficient cells. Autophagy 11:1471–1483. http://dx.doi.org/10.1080/15548627.2015.1068488.
  • Mizushima N, Yoshimori T, Levine B. 2010. Methods in mammalian autophagy research. Cell 140:313–326. http://dx.doi.org/10.1016/j.cell.2010.01.028.
  • Russell RC, Tian Y, Yuan H, Park HW, Chang YY, Kim J, Kim H, Neufeld TP, Dillin A, Guan KL. 2013. ULK1 induces autophagy by phosphorylating beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol 15:741–750. http://dx.doi.org/10.1038/ncb2757.
  • Itakura E, Mizushima N. 2011. p62 targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J Cell Biol 192:17–27. http://dx.doi.org/10.1083/jcb.201009067.
  • Papaioannou VE, Behringer RR. 2012. Early embryonic lethality in genetically engineered mice: diagnosis and phenotypic analysis. Vet Pathol 49:64–70. http://dx.doi.org/10.1177/0300985810395725.
  • Watson ED, Cross JC. 2005. Development of structures and transport functions in the mouse placenta. Physiology 20:180–193. http://dx.doi.org/10.1152/physiol.00001.2005.
  • Varfolomeev EE, Ashkenazi A. 2004. Tumor necrosis factor: an apoptosis JuNKie? Cell 116:491–497. http://dx.doi.org/10.1016/S0092-8674(04)00166-7.
  • Oberst A, Green DR. 2011. It cuts both ways: reconciling the dual roles of caspase 8 in cell death and survival. Nat Rev Mol Cell Biol 12:757–763. http://dx.doi.org/10.1038/nrm3214.
  • Kreuz S, Siegmund D, Scheurich P, Wajant H. 2001. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol Cell Biol 21:3964–3973. http://dx.doi.org/10.1128/MCB.21.12.3964-3973.2001.
  • Lee E, Koo Y, Ng A, Wei Y, Luby-Phelps K, Juraszek A, Xavier RJ, Cleaver O, Levine B, Amatruda JF. 2014. Autophagy is essential for cardiac morphogenesis during vertebrate development. Autophagy 10:572–587. http://dx.doi.org/10.4161/auto.27649.
  • Yang L, Wang L, Zheng Y. 2006. Gene targeting of Cdc42 and Cdc42GAP affirms the critical involvement of Cdc42 in filopodia induction, directed migration, and proliferation in primary mouse embryonic fibroblasts. Mol Biol Cell 17:4675–4685. http://dx.doi.org/10.1091/mbc.E06-05-0466.
  • Wang L, Yang L, Burns K, Kuan CY, Zheng Y. 2005. Cdc42GAP regulates c-Jun N-terminal kinase (JNK)-mediated apoptosis and cell number during mammalian perinatal growth. Proc Natl Acad Sci U S A 102:13484–13489. http://dx.doi.org/10.1073/pnas.0504420102.
  • Alers S, Loffler AS, Paasch F, Dieterle AM, Keppeler H, Lauber K, Campbell DG, Fehrenbacher B, Schaller M, Wesselborg S, Stork B. 2011. Atg13 and FIP200 act independently of Ulk1 and Ulk2 in autophagy induction. Autophagy 7:1423–1433.
  • Kim M, Park HL, Park HW, Ro SH, Nam SG, Reed JM, Guan JL, Lee JH. 2013. Drosophila Fip200 is an essential regulator of autophagy that attenuates both growth and aging. Autophagy 9:1201–1213. http://dx.doi.org/10.4161/auto.24811.
  • Kalie E, Razi M, Tooze SA. 2013. ULK1 regulates melanin levels in MNT-1 cells independently of mTORC1. PLoS One 8:e75313. http://dx.doi.org/10.1371/journal.pone.0075313.
  • Yeh WC, Itie A, Elia AJ, Ng M, Shu HB, Wakeham A, Mirtsos C, Suzuki N, Bonnard M, Goeddel DV, Mak TW. 2000. Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12:633–642. http://dx.doi.org/10.1016/S1074-7613(00)80214-9.
  • Dillon CP, Oberst A, Weinlich R, Janke LJ, Kang TB, Ben-Moshe T, Mak TW, Wallach D, Green DR. 2012. Survival function of the FADD-CASPASE-8-cFLIP(L) complex. Cell Rep 1:401–407. http://dx.doi.org/10.1016/j.celrep.2012.03.010.
  • Jin Z, Li Y, Pitti R, Lawrence D, Pham VC, Lill JR, Ashkenazi A. 2009. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 137:721–735. http://dx.doi.org/10.1016/j.cell.2009.03.015.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.