Characteristics and requirements of basal autophagy in HEK 293 cells

Autophagy

Volumn 9, Issue 9, 2013, Pages 1407-1417

  Musiwaro, Patience ^a   Smith, Matthew ^a   Manifava, Maria ^a   Walker, Simon A ^a   Ktistakis, Nicholas T ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Autophagosomes; Bafilomycin A1; Basal autophagy; Chloroquine; Target of rapamycin; Vinblastine

Indexed keywords

AMINO ACID; BAFILOMYCIN A1; CHLOROQUINE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; VINBLASTINE; WORTMANNIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL GROWTH; CELL MATURATION; CELL STRAIN HEK293; CONTROLLED STUDY; DRUG TARGETING; ENDOPLASMIC RETICULUM; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; STARVATION;

ANIMALIA; MAMMALIA;

AUTOPHAGOSOMES; BAFILOMYCIN A1; BASAL AUTOPHAGY; CHLOROQUINE; TARGET OF RAPAMYCIN; VINBLASTINE;

ANDROSTADIENES; AUTOPHAGY; BIOLOGICAL MARKERS; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; MACROLIDES; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; PHAGOSOMES; PHOSPHATIDYLINOSITOL PHOSPHATES; TOR SERINE-THREONINE KINASES;

EID: 84884337145     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.25455     Document Type: Article

References (49)

1. Mizushima N. Autophagy: process and function. Genes Dev 2007; 21: 2861-73; PMID:18006683; http://dx.doi.org/10.1101/gad.1599207 (Pubitemid 350133435)
2. Weidberg H, Shvets E, Elazar Z. Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 2011; 80: 125-56; PMID:21548784; http://dx.doi.org/10.1146/annurev-biochem-052709-094552
3. Rabinowitz JD, White E. Autophagy and metabolism. Science 2010; 330: 1344-8; PMID:21127245; http://dx.doi.org/10.1126/science.1193497
4. Abraham R, Hendy R, Grasso P. Formation of myeloid bodies in rat liver lysosomes after chloroquine administration. Exp Mol Pathol 1968; 9: 212-29; PMID:4952073; http://dx.doi.org/10.1016/0014-4800(68)90037-3
5. Gray RH, Sokol M, Brabec RK, Brabec MJ. Characterization of chloroquine-induced autophagic vacuoles isolated from rat liver. Exp Mol Pathol 1981; 34: 72-86; PMID:7193142; http://dx.doi.org/10.1016/0014-4800(81)90037-X (Pubitemid 11134211)
6. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441: 885- 9; PMID:16625204; http://dx.doi.org/10. 1038/nature04724
7. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 2007; 13: 619-24; PMID:17450150; http://dx.doi.org/10.1038/nm1574 (Pubitemid 46828485)
8. Yang S, Wang X, Contino G, Liesa M, Sahin E, Ying H, et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev 2011; 25: 717- 29; PMID:21406549; http://dx.doi.org/10.1101/gad.2016111
9. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 2005; 1: 84-91; PMID:16874052; http://dx.doi.org/10.4161/auto.1.2.1697
10. Klionsky DJ, Elazar Z, Seglen PO, Rubinsztein DC. Does bafilomycin A1 block the fusion of autophagosomes with lysosomes? Autophagy 2008; 4: 849-50; PMID:18758232
11. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
12. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140: 313- 26; PMID:20144757; http://dx.doi.org/10.1016/j. cell.2010.01.028
13. Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk V, Kaushik S, et al. In search of an "autophagomometer". Autophagy 2009; 5: 585- 9; PMID:19411822; http://dx.doi.org/10.4161/auto.5.5.8823
14. Efeyan A, Zoncu R, Sabatini DM. Amino acids and mTORC1: from lysosomes to disease. Trends Mol Med 2012; 18: 524-33; PMID:22749019; http://dx.doi.org/10. 1016/j.molmed.2012.05.007
15. Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science 2011; 334: 678- 83; PMID:22053050; http://dx.doi.org/10.1126/science.1207056
16. Juhász G. Interpretation of bafilomycin, pH neutralizing or protease inhibitor treatments in autophagic flux experiments: novel considerations. Autophagy 2012; 8: 1875-6; PMID:22874642; http://dx.doi.org/10. 4161/auto.21544
17. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Erdin S, et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 2012; 31: 1095-108; PMID:22343943; http://dx.doi.org/10. 1038/emboj.2012.32
18. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008; 182: 685-701; PMID:18725538; http://dx.doi.org/10. 1083/jcb.200803137
19. Polson HE, de Lartigue J, Rigden DJ, Reedijk M, Urbé S, Clague MJ, et al. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 2010; 6: 506-22; PMID:20505359; http://dx.doi.org/10.4161/auto.6.4.11863
20. Matsunaga K, Morita E, Saitoh T, Akira S, Ktistakis NT, Izumi T, et al. Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J Cell Biol 2010; 190: 511-21; PMID:20713597; http://dx.doi.org/10. 1083/jcb.200911141
21. Taguchi-Atarashi N, Hamasaki M, Matsunaga K, Omori H, Ktistakis NT, Yoshimori T, et al. Modulation of local PtdIns3P levels by the PI phosphatase MTMR3 regulates constitutive autophagy. Traffic 2010; 11: 468-78; PMID:20059746; http://dx.doi.org/10.1111/j.1600-0854.2010.01034.x
22. Hayashi-Nishino M, Fujita N, Noda T, Yamaguchi A, Yoshimori T, Yamamoto A. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 2009; 11: 1433- 7; PMID:19898463; http://dx.doi.org/10. 1038/ncb1991
23. Kovács AL, Kovács J. Autophagocytosis in mouse seminal vesicle cells in vitro. Temperature dependence and effects of vinblastine and inhibitors of protein synthesis. Virchows Arch B Cell Pathol Incl Mol Pathol 1980; 32: 97-104; PMID:6102826 (Pubitemid 10134000)
24. Arstila AU, Nuuja IJ, Trump BF. Studies on cellular autophagocytosis. Vinblastine-induced autophagy in the rat liver. Exp Cell Res 1974; 87: 249-52; PMID:4415937; http://dx.doi.org/10.1016/0014-4827(74)90477-7
25. Hirsimäki P, Reunanen H. Studies on vinblastineinduced autophagocytosis in mouse liver. II. Origin of membranes and acquisition of acid phosphatase. Histochemistry 1980; 67: 139-53; PMID:6105141; http://dx.doi.org/10.1007/BF00493232 (Pubitemid 10000057)
26. Köchl R, Hu XW, Chan EY, Tooze SA. Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 2006; 7: 129-45; PMID:16420522; http://dx.doi.org/10.1111/j.1600-0854.2005. 00368.x
27. Obara K, Ohsumi Y. Dynamics and function of PtdIns(3)P in autophagy. Autophagy 2008; 4: 952-4; PMID:18769109
28. Blommaart EF, Krause U, Schellens JP, Vreeling- Sindelárová H, Meijer AJ. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 1997; 243: 240-6; PMID:9030745; http://dx.doi.org/10.1111/j.1432-1033.1997.0240a.x (Pubitemid 27060408)
29. Ktistakis NT, Manifava M, Schoenfelder P, Rotondo S. How phosphoinositide 3-phosphate controls growth downstream of amino acids and autophagy downstream of amino acid withdrawal. Biochem Soc Trans 2012; 40: 37-43; PMID:22260663; http://dx.doi.org/10.1042/BST20110684
30. Codogno P, Mehrpour M, Proikas-Cezanne T. Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat Rev Mol Cell Biol 2012; 13: 7-12; PMID:22166994
31. Jaber N, Dou Z, Chen JS, Catanzaro J, Jiang YP, Ballou LM, et al. Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc Natl Acad Sci U S A 2012; 109: 2003- 8; PMID:22308354; http://dx.doi.org/10.1073/pnas.1112848109
32. Juhász G, Hill JH, Yan Y, Sass M, Baehrecke EH, Backer JM, et al. The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol 2008; 181: 655- 66; PMID:18474623; http://dx.doi.org/10.1083/jcb.200712051
33. McLeod IX, Zhou X, Li Q J, Wang F, He YW. The class III kinase Vps34 promotes T lymphocyte survival through regulating IL-7Rα surface expression. J Immunol 2011; 187: 5051-61; PMID:22021616; http://dx.doi.org/10. 4049/jimmunol.1100710
34. Zhou X, Takatoh J, Wang F. The mammalian class 3 PI3K (PIK3C3) is required for early embryogenesis and cell proliferation. PLoS One 2011; 6:e16358; PMID:21283715; http://dx.doi.org/10.1371/journal.pone.0016358
35. Zhou X, Wang L, Hasegawa H, Amin P, Han BX, Kaneko S, et al. Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway. Proc Natl Acad Sci U S A 2010; 107: 9424- 9; PMID:20439739; http://dx.doi.org/10.1073/pnas.0914725107
36. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43: 67-93; PMID:19653858; http://dx.doi.org/10. 1146/annurev-genet-102808-114910
37. Stocker H, Radimerski T, Schindelholz B, Wittwer F, Belawat P, Daram P, et al. Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nat Cell Biol 2003; 5: 559-65; PMID:12766775; http://dx.doi.org/10. 1038/ncb995 (Pubitemid 36781091)
38. Saucedo LJ, Gao X, Chiarelli DA, Li L, Pan D, Edgar BA. Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nat Cell Biol 2003; 5: 566-71; PMID:12766776; http://dx.doi.org/10.1038/ncb996 (Pubitemid 36781092)
39. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J. Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 2003; 13: 1259-68; PMID:12906785; http://dx.doi.org/10.1016/S0960-9822(03)00506-2 (Pubitemid 36953298)
40. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010; 141: 290- 303; PMID:20381137; http://dx.doi.org/10.1016/j.cell.2010.02.024
41. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, et al. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 2008; 320: 1496-501; PMID:18497260; http://dx.doi.org/10.1126/science. 1157535 (Pubitemid 351929429)
42. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149: 274- 93; PMID:22500797; http://dx.doi.org/10.1016/j.cell.2012. 03.017
43. Neufeld TP. Autophagy and cell growth - the yin and yang of nutrient responses. J Cell Sci 2012; 125: 2359- 68; PMID:22649254; http://dx.doi.org/10. 1242/jcs.103333
44. Kim E. Mechanisms of amino acid sensing in mTOR signaling pathway. Nutr Res Pract 2009; 3: 64- 71; PMID:20016704; http://dx.doi.org/10.4162/nrp.2009.3. 1.64
45. Mari M, Tooze SA, Reggiori F. The puzzling origin of the autophagosomal membrane. F1000 Biol Rep 2011; 3: 25; PMID:22162728; http://dx.doi.org/10.3410/ B3-25
46. Tooze SA, Yoshimori T. The origin of the autophagosomal membrane. Nat Cell Biol 2010; 12: 831- 5; PMID:20811355; http://dx.doi.org/10.1038/ncb0910-831
47. Rubinsztein DC, Shpilka T, Elazar Z. Mechanisms of autophagosome biogenesis. Curr Biol 2012; 22:R29- 34; PMID:22240478; http://dx.doi.org/10. 1016/j.cub.2011.11.034
48. Ylä-Anttila P, Vihinen H, Jokitalo E, Eskelinen EL. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009; 5: 1180-5; PMID:19855179; http://dx.doi.org/10.4161/auto.5.8.10274
49. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 2010; 141: 656-67; PMID:20478256; http://dx.doi.org/10.1016/j. cell.2010.04.009