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Cited by 2,230Autophagy in Disease and TherapyCellular transport and secretionCalcium signaling and nucleotide metabolism

Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes

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Klionsky, Daniel J., Abeliovich, Hagai, Agostinis, Patrizia, Agrawal, Devendra K., Aliev, Gjumrakch, Askew, David S., Baba, Misuzu, Baehrecke, Eric H. +224 more·2008·Autophagy
DOI 10.4161/auto.5338PMC PMC2654259
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Abstract

Research in autophagy continues to accelerate,(1) and as a result many new scientists are entering the field. Accordingly, it is important to establish a standard set of criteria for monitoring macroautophagy in different organisms. Recent reviews have described the range of assays that have been used for this purpose.(2,3) There are many useful and convenient methods that can be used to monitor macroautophagy in yeast, but relatively few in other model systems, and there is much confusion regarding acceptable methods to measure macroautophagy in higher eukaryotes. A key point that needs to be emphasized is that there is a difference between measurements that monitor the numbers of autophagosomes versus those that measure flux through the autophagy pathway; thus, a block in macroautophagy that results in autophagosome accumulation needs to be differentiated from fully functional autophagy that includes delivery to, and degradation within, lysosomes (in most higher eukaryotes) or the vacuole (in plants and fungi). Here, we present a set of guidelines for the selection and interpretation of the methods that can be used by investigators who are attempting to examine macroautophagy and related processes, as well as by reviewers who need to provide realistic and reasonable critiques of papers that investigate these processes. This set of guidelines is not meant to be a formulaic set of rules, because the appropriate assays depend in part on the question being asked and the system being used. In addition, we emphasize that no individual assay is guaranteed to be the most appropriate one in every situation, and we strongly recommend the use of multiple assays to verify an autophagic response.

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  • LC3B is widely used as a fusion with GFP (GFP-LC3) to follow autophagosome formation using fluorescence microscopy.

    “LC3B is the protein that is widely used as a fusion with GFP (GFP-LC3) to follow autophagosome formation using fluorescence microscopy [31].”

    From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [31]

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  1. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8:931-7.
  2. Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy 2007; 3:181-206.
  3. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 2004; 36:2491- 502.
  4. Kovács AL, Reith A, Seglen PO. Accumulation of autophagosomes after inhibition of hepa- tocytic protein degradation by vinblastine, leupeptin or a lysosomotropic amine. Exp Cell Res 1982; 137:191-201.
  5. Seglen PO. Regulation of autophagic protein degradation in isolated liver cells. In: Glaumann H, Ballard FJ, eds. Lysosomes: Their Role in Protein Breakdown. London: Academic Press, 1987:369-414.
  6. Dunn WA, Jr. Autophagy and related mechanisms of lysosome-mediated protein degrada- tion. Trends Cell Biol 1994; 4:139-43.
  7. Dunn WA, Jr. Studies on the mechanisms of autophagy: formation of the autophagic vacu- ole. J Cell Biol 1990; 110:1923-33.
  8. Ishihara N, Hamasaki M, Yokota S, Suzuki K, Kamada Y, Kihara A, Yoshimori T, Noda T, Ohsumi Y. Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 2001; 12:3690-702.
  9. Reggiori F, Wang C-W, Nair U, Shintani T, Abeliovich H, Klionsky DJ. Early stages of the secretory pathway, but not endosomes, are required for Cvt vesicle and autophagosome assembly in Saccharomyces cerevisiae. Mol Biol Cell 2004; 15:2189-204.
  10. Gonzalez-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquere S, Eskelinen E-L, Pierron G, Saftig P, Kroemer G. The apoptosis/autophagy paradox: autophagic vacuoliza- tion before apoptotic death. J Cell Sci 2005; 118:3091-102.
  11. Eskelinen E-L. Maturation of autophagic vacuoles in mammalian cells. Autophagy 2005; 1:1-10.
  12. Weibel ER. Practical Methods for Biological Morphometry. Academic Press, New York, 1979.
  13. Williams MA. Quantitative methods in biology: Practical methods in electron microscopy. Amsterdam, New York, Oxford: North-Holland Publishing Company, 1977.
  14. Shelburne JD, Arstila AU, Trump BF. Studies on cellular autophagocytosis. The relationship of autophagocytosis to protein synthesis and to energy metabolism in rat liver and flounder kidney tubules in vitro. Am J Pathol 1973; 73:641-70.
  15. Kovács AL, Pálfia Z, Réz G, Vellai T, Kovács J. Sequestration revisited: integrating tradi- tional electron microscopy, de novo assembly and new results. Autophagy 2007; 3:655-62.
  16. Klionsky DJ. Protein transport from the cytoplasm into the vacuole. J Membr Biol 1997; 157:105-15.
  17. Mayhew TM. Quantitative immunoelectron microscopy: alternative ways of assessing sub- cellular patterns of gold labeling. Methods Mol Biol 2007; 369:309-29.
  18. Mayhew TM, Lucocq JM, Griffiths G. Relative labelling index: a novel stereological approach to test for non-random immunogold labelling of organelles and membranes on transmission electron microscopy thin sections. J Microsc 2002; 205:153-64.
  19. Kovács AL, Grinde B, Seglen PO. Inhibition of autophagic vacuole formation and protein degradation by amino acids in isolated hepatocytes. Exp Cell Res 1981; 133:431-6.
  20. Mortimore GE, Hutson NJ, Surmacz CA. Quantitative correlation between proteolysis and macro-and microautophagy in mouse hepatocytes during starvation and refeeding. Proc Natl Acad Sci U S A 1983; 80:2179-83.
  21. Mortimore GE, Lardeux BR, Adams CE. Regulation of microautophagy and basal protein turnover in rat liver. Effects of short-term starvation. J Biol Chem 1988; 263:2506-12.
  22. Zhu JH, Horbinski C, Guo F, Watkins S, Uchiyama Y, Chu CT. Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium- induced cell death. Am J Pathol 2007; 170:75-86.
  23. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Øvervatn 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; 171:603-14.
  24. Massey AC, Kaushik S, Sovak G, Kiffin R, Cuervo AM. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci USA 2006; 103:5805-10.
  25. Huang W-P, Scott SV, Kim J, Klionsky DJ. The itinerary of a vesicle component, Aut7p/ Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways. J Biol Chem 2000; 275:5845-51.
  26. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15:1101-11.
  27. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-acti- vated protein kinase and Beclin 1 in mediating autophagy. Circ Res 2007; 100:914-22.
  28. He H, Dang Y, Dai F, Guo Z, Wu J, She X, Pei Y, Chen Y, Ling W, Wu C, Zhao S, Liu JO, Yu L. Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J Biol Chem 2003; 278:29278-87.
  29. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152:657-68.
  30. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8:1124-32.
  31. Meléndez A, Tallóczy Z, Seaman M, Eskelinen E-L, Hall DH, Levine B. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 2003; 301:1387-91.
  32. Otto GP, Wu MY, Kazgan N, Anderson OR, Kessin RH. Macroautophagy is required for multicellular development of the social amoeba Dictyostelium discoideum. J Biol Chem 2003; 278:17636-45.
  33. Rusten TE, Lindmo K, Juhasz G, Sass M, Seglen PO, Brech A, Stenmark H. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell 2004; 7:179-92.
  34. Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell 2004; 7:167-78.
  35. Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y. Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 2004; 16:2967-83.
  36. Elsasser A, Vogt AM, Nef H, Kostin S, Mollmann H, Skwara W, Bode C, Hamm C, Schaper J. Human hibernating myocardium is jeopardized by apoptotic and autophagic cell death. J Am Coll Cardiol 2004; 43:2191-9.
  37. Knaapen MW, Davies MJ, De Bie M, Haven AJ, Martinet W, Kockx MM. Apoptotic versus autophagic cell death in heart failure. Cardiovasc Res 2001; 51:304-12.
  38. Kostin S, Pool L, Elsasser A, Hein S, Drexler HC, Arnon E, Hayakawa Y, Zimmermann R, Bauer E, Klovekorn WP, Schaper J. Myocytes die by multiple mechanisms in failing human hearts. Circ Res 2003; 92:715-24.
  39. Amer AO, Swanson MS. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol 2005; 7:765-78.
  40. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753-66.
  41. Ogawa M, Sasakawa C. Intracellular survival of Shigella. Cell Microbiol 2006; 8:177-84.
  42. Willig KI, Kellner RR, Medda R, Hein B, Jakobs S, Hell SW. Nanoscale resolution in GFP- based microscopy. Nat Methods 2006; 3:721-3.
  43. Monastyrska I, Klionsky DJ. Autophagy in organelle homeostasis: peroxisome turnover. Mol Aspects Med 2006; 27:483-94.
  44. Nair U, Klionsky DJ. Molecular mechanisms and regulation of specific and nonspecific autophagy pathways in yeast. J Biol Chem 2005; 280:41785-8.
  45. Dunn WA, Jr., Cregg JM, Kiel JAKW, van der Klei IJ, Oku M, Sakai Y, Sibirny AA, Stasyk OV, Veenhuis M. Pexophagy: the selective autophagy of peroxisomes. Autophagy 2005; 1:75-83.
  46. Birmingham CL, Brumell JH. Autophagy recognizes intracellular Salmonella enterica serovar Typhimurium in damaged vacuoles. Autophagy 2006; 2:156-8.
  47. Colombo MI, Gutierrez MG, Romano PS. The two faces of autophagy: Coxiella and Mycobacterium. Autophagy 2006; 2:162-4.
  48. Vergne I, Singh S, Roberts E, Kyei G, Master S, Harris J, de Haro S, Naylor J, Davis A, Delgado M, Deretic V. Autophagy in immune defense against Mycobacterium tuberculosis. Autophagy 2006; 2:175-8.
  49. Yoshimori T. Autophagy vs. Group A Streptococcus. Autophagy 2006; 2:154-5.
  50. Tallóczy Z, Virgin HW, IV, Levine B. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2006; 2:24-9.
  51. Young ARJ, Chan EYW, Hu XW, Köchl R, Crawshaw SG, High S, Hailey DW, Lippincott- Schwartz J, Tooze SA. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 2006; 119:3888-900.
  52. Reggiori F, Tucker KA, Stromhaug PE, Klionsky DJ. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 2004; 6:79-90.
  53. Brady NR, Hamacher-Brady A, Yuan H, Gottlieb RA. The autophagic response to nutrient deprivation in the HL-1 cardiac myocyte is modulated by Bcl-2 and sarco/endoplasmic reticulum calcium stores. FEBS J 2007; 274:3184-97.
  54. Lee HK, Lund JM, Ramanathan B, Mizushima N, Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 2007; 315:1398-401.
  55. Wu JQ, Pollard TD. Counting cytokinesis proteins globally and locally in fission yeast. Science 2005; 310:310-4.
  56. Szeto J, Kaniuk NA, Canadien V, Nisman R, Mizushima N, Yoshimori T, Bazett-Jones DP, Brumell JH. ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2006; 2:189-99.
  57. Kaniuk NA, Kiraly M, Bates H, Vranic M, Volchuk A, Brumell JH. Ubiquitinated-protein aggregates form in pancreatic β-cells during diabetes-induced oxidative stress and are regu- lated by autophagy. Diabetes 2007; 56:930-9.
  58. Pierre P. Dendritic cells, DRiPs, and DALIS in the control of antigen processing. Immunol Rev 2005; 207:184-90.
  59. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441:885-9.
  60. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K. Loss of autophagy in the central nervous system causes neuro- degeneration in mice. Nature 2006; 441:880-4.
  61. Ciechomska IA, Tolkovsky AM. Non-autophagic GFP-LC3 puncta induced by saponin and other detergents. Autophagy 2007; 3:586-90.
  62. Köchl R, Hu XW, Chan EYW, Tooze SA. Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 2006; 7:129-45.
  63. Bampton ET, Goemans CG, Niranjan D, Mizushima N, Tolkovsky AM. The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lyso- somes. Autophagy 2005; 1:23-36.
  64. Schmid D, Pypaert M, Münz C. Antigen-loading compartments for major histocompatibil- ity complex class II molecules continuously receive input from autophagosomes. Immunity 2007; 26:79-92.
  65. Stromhaug PE, Reggiori F, Guan J, Wang C-W, Klionsky DJ. Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol Biol Cell 2004; 15:3553-66.
  66. Erlich S, Alexandrovich A, Shohami E, Pinkas-Kramarski R. Rapamycin is a neuroprotec- tive treatment for traumatic brain injury. Neurobiol Dis 2007; 26:86-93.
  67. Lavieu G, Scarlatti F, Sala G, Carpentier S, Levade T, Ghidoni R, Botti J, Codogno P. Regulation of autophagy by sphingosine kinase 1 and its role in cell survival during nutrient starvation. J Biol Chem 2006; 281:8518-27.
  68. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 2000; 150:1507-13.
  69. Djavaheri-Mergny M, Amelotti M, Mathieu J, Besancon F, Bauvy C, Souquere S, Pierron G, Codogno P. NF-kB activation represses tumor necrosis factor-α-induced autophagy. J Biol Chem 2006; 281:30373-82.
  70. Liu Z, Lenardo MJ. Reactive oxygen species regulate autophagy through redox-sensitive proteases. Dev Cell 2007; 12:484-5.
  71. Scarlatti F, Bauvy C, Ventruti A, Sala G, Cluzeaud F, Vandewalle A, Ghidoni R, Codogno P. Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regula- tion of beclin 1. J Biol Chem 2004; 279:18384-91.
  72. Nara A, Mizushima N, Yamamoto A, Kabeya Y, Ohsumi Y, Yoshimori T. SKD1 AAA ATPase-dependent endosomal transport is involved in autolysosome formation. Cell Struct Funct 2002; 27:29-37.
  73. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E, Momoi T. ER stress (PERK/eIF2α phosphorylation) mediates the polygluta- mine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007; 14:230-9.
  74. Lee C-Y, Clough EA, Yellon P, Teslovich TM, Stephan DA, Baehrecke EH. Genome-wide analyses of steroid-and radiation-triggered programmed cell death in Drosophila. Curr Biol 2003; 13:350-7.
  75. Martinet W, De Meyer GR, Andries L, Herman AG, Kockx MM. In situ detection of starvation-induced autophagy. J Histochem Cytochem 2006; 54:85-96.
  76. Pattingre S, Petiot A, Codogno P. Analyses of Gα-interacting protein and activator of G- protein-signaling-3 functions in macroautophagy. Methods Enzymol 2004; 390:17-31.
  77. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, Yin XM. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007; 171:513-24.
  78. Iwata A, Riley BE, Johnston JA, Kopito RR. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 2005; 280:40282-92.
  79. Taylor GS, Long HM, Haigh TA, Larsen M, Brooks J, Rickinson AB. A role for intercellular antigen transfer in the recognition of EBV-transformed B cell lines by EBV nuclear antigen- specific CD4+ T cells. J Immunol 2006; 177:3746-56. 103
  80. Venerando R, Miotto G, Kadowaki M, Siliprandi N, Mortimore GE. Multiphasic control of proteolysis by leucine and alanine in the isolated rat hepatocyte. Am J Physiol 1994; 266: C455-61. 104
  81. Häussinger D, Hallbrucker C, vom Dahl S, Lang F, Gerok W. Cell swelling inhibits prote- olysis in perfused rat liver. Biochem J 1990; 272:239-42. 105
  82. vom Dahl S, Häussinger D. Cell hydration and proteolysis control in liver. Biochem J 1995; 312:988-9. 106
  83. Fass E, Shvets E, Degani I, Hirschberg K, Elazar Z. Microtubules support production of starvation-induced autophagosomes but not their targeting and fusion with lysosomes. J Biol Chem 2006; 281:36303-16. 108
  84. Karim MR, Kanazawa T, Daigaku Y, Fujimura S, Miotto G, Kadowaki M. Cytosolic LC3 ratio as a sensitive index of macroautophagy in isolated rat hepatocytes and H4-II-E cells. Autophagy 2007; 3:553-60. 109
  85. Iwata J, Ezaki J, Komatsu M, Yokota S, Ueno T, Tanida I, Chiba T, Tanaka K, Kominami E. Excess peroxisomes are degraded by autophagic machinery in mammals. J Biol Chem 2006; 281:4035-41. 110
  86. Gutierrez MG, Saka HA, Chinen I, Zoppino FC, Yoshimori T, Bocco JL, Colombo MI. Protective role of autophagy against Vibrio cholerae cytolysin, a pore-forming toxin from V. cholerae. Proc Natl Acad Sci USA 2007; 104:1829-34. 111
  87. Hosokawa N, Hara Y, Mizushima N. Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett 2006; 580:2623-9. 112
  88. Shintani T, Klionsky DJ. Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J Biol Chem 2004; 279:29889-94. 113
  89. Patterson GH, Lippincott-Schwartz J. Selective photolabeling of proteins using photoacti- vatable GFP. Methods 2004; 32:445-50. 114
  90. Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 2006; 281:29776-87. 115
  91. Patterson GH, Knobel SM, Sharif WD, Kain SR, Piston DW. Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys J 1997; 73:2782- 90. 116
  92. Rekas A, Alattia JR, Nagai T, Miyawaki A, Ikura M. Crystal structure of venus, a yellow fluorescent protein with improved maturation and reduced environmental sensitivity. J Biol Chem 2002; 277:50573-8. 118
  93. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Øvervatn 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; 171:603-14. 119
  94. Komatsu M, Waguri S, Koike M, Sou Y-s, Ueno T, Hara T, Mizushima N, Iwata J-i, Ezaki J, Murata S, Hamazaki J, Nishito Y, Iemura S-i, Natsume T, Yanagawa T, Uwayama J, Warabi E, Yoshida H, Ishii T, Kobayashi A, Yamamoto M, Yue Z, Uchiyama Y, Kominami E, Tanaka K. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131:149-63. 122
  95. Bardag-Gorce F, Francis T, Nan L, Li J, He Lue Y, French BA, French SW. Modifications in p62 occur due to proteasome inhibition in alcoholic liver disease. Life Sci 2005; 77:2594- 602. 123
  96. Nakaso K, Yoshimoto Y, Nakano T, Takeshima T, Fukuhara Y, Yasui K, Araga S, Yanagawa T, Ishii T, Nakashima K. Transcriptional activation of p62/A170/ZIP during the formation of the aggregates: possible mechanisms and the role in Lewy body formation in Parkinson's disease. Brain Res 2004; 1012:42-51. 124
  97. Seglen PO, Gordon PB, Tolleshaug H, Høyvik H. Use of [ 3 H]raffinose as a specific probe of autophagic sequestration. Exp Cell Res 1986; 162:273-7. 125
  98. Kopitz J, Kisen GO, Gordon PB, Bohley P, Seglen PO. Nonselective autophagy of cytosolic enzymes by isolated rat hepatocytes. J Cell Biol 1990; 111:941-53. 126
  99. Plomp PJ, Gordon PB, Meijer AJ, Høyvik H, Seglen PO. Energy dependence of different steps in the autophagic-lysosomal pathway. J Biol Chem 1989; 264:6699-704. 127
  100. Hoyvik H, Gordon PB, Berg TO, Stromhaug PE, Seglen PO. Inhibition of autophagic- lysosomal delivery and autophagic lactolysis by asparagine. J Cell Biol 1991; 113:1305-12. 128
  101. Rodriguez-Enriquez S, Kim I, Currin RT, Lemasters JJ. Tracker dyes to probe mitochondrial autophagy (mitophagy) in rat hepatocytes. Autophagy 2006; 2:39-46. 129
  102. Lorenz H, Hailey DW, Lippincott-Schwartz J. Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat Methods 2006; 3:205- 10. 130
  103. McNeil PL, Murphy RF, Lanni F, Taylor DL. A method for incorporating macromolecules into adherent cells. J Cell Biol 1984; 98:1556-64. 131
  104. Kovács AL, Laszlo L, Kovács J. Effect of amino acids and cycloheximide on changes caused by vinblastine, leupeptin and methylamine in the autophagic/lysosomal system of mouse hepatocytes in vivo. Exp Cell Res 1985; 157:83-94. 132
  105. Kovács AL, Réz G, Pálfia Z, Kovács J. Autophagy in the epithelial cells of murine seminal vesicle in vitro. Formation of large sheets of nascent isolation membranes, sequestration of the nucleus and inhibition by wortmannin and 3-methyladenine. Cell Tissue Res 2000; 302:253-61. 133
  106. Kovács J, Fellinger E, Karpati AP, Kovács AL, Laszlo L, Réz G. Morphometric evaluation of the turnover of autophagic vacuoles after treatment with Triton X-100 and vinblastine in murine pancreatic acinar and seminal vesicle epithelial cells. Virchows Arch B Cell Pathol Incl Mol Pathol 1987; 53:183-90. 134
  107. Kovács J, Laszlo L, Kovács AL. Regression of autophagic vacuoles in pancreatic acinar, seminal vesicle epithelial, and liver parenchymal cells: a comparative morphometric study of the effect of vinblastine and leupeptin followed by cycloheximide treatment. Exp Cell Res 1988; 174:244-51. 135
  108. Jomain-Baum M, Garber AJ, Farber E, Hanson RW. The effect of cycloheximide on the interaction between mitochondrial respiration and gluconeogenesis in guinea pig and rat liver. J Biol Chem 1973; 248:1536-43. 136
  109. Toyooka K, Moriyasu Y, Goto Y, Takeuchi M, Fukuda H, Matsuoka K. Protein aggregates are transported to vacuoles by a macroautophagic mechanism in nutrient-starved plant cells. Autophagy 2006; 2:96-106. 137
  110. Deter RL. Quantitative characterization of dense body, autophagic vacuole, and acid phos- phatase-bearing particle populations during the early phases of glucagon-induced autophagy in rat liver. J Cell Biol 1971; 48:473-89. 138
  111. Deter RL. Analog modeling of glucagon-induced autophagy in rat liver. I. Conceptual and mathematical model of telolysosome-autophagosome-autolysosome interaction. Exp Cell Res 1975; 94:122-6. 139
  112. Deter RL. Analog modeling of glucagon-induced autophagy in rat liver. II. Evaluation of iron labeling as a means for identifying telolysosome, autophagosome and autolysosome populations. Exp Cell Res 1975; 94:127-39. 140
  113. Deter RL, de Duve C. Influence of glucagon, an inducer of cellular autophagy, on some physical properties of rat liver lysosomes. J Cell Biol 1967; 33:437-49. 142
  114. Marzella L, Ahlberg J, Glaumann H. Isolation of autophagic vacuoles from rat liver: mor- phological and biochemical characterization. J Cell Biol 1982; 93:144-54. 145
  115. Wattiaux R, Wattiaux-De Coninck S, Ronveaux-Dupal M-F, Dubois F. Isolation of rat liver lysosomes by isopycnic centrifugation in a metrizamide gradient. J Cell Biol 1978; 78:349- 68. 146
  116. Baudhuin P, Evrard P, Berthet J. Electron microscopic examination of subcellular fractions. I. The preparation of representative samples from suspensions of particles. J Cell Biol 1967; 32:181-91. 148
  117. Baudhuin P, Berthet J. Electron microscopic examination of subcellular fractions. II. Quantitative analysis of the mitochondrial population isolated from rat liver. J Cell Biol 1967; 35:631-48. 149
  118. Storrie B, Madden EA. Isolation of subcellular organelles. Methods Enzymol 1990; 182:203-25. 150
  119. Cuervo AM, Dice JF, Knecht E. A population of rat liver lysosomes responsible for the selective uptake and degradation of cytosolic proteins. J Biol Chem 1997; 272:5606-15. 151
  120. Isahara K, Ohsawa Y, Kanamori S, Shibata M, Waguri S, Sato N, Gotow T, Watanabe T, Momoi T, Urase K, Kominami E, Uchiyama Y. Regulation of a novel pathway for cell death by lysosomal aspartic and cysteine proteinases. Neuroscience 1999; 91:233-49. 152
  121. Tomas-Zapico C, Caballero B, Sierra V, Vega-Naredo I, Alvarez-Garcia O, Tolivia D, Rodriguez-Colunga MJ, Coto-Montes A. Survival mechanisms in a physiological oxidative stress model. FASEB J 2005; 19:2066-8. 153
  122. Martinet W, De Meyer GR, Andries L, Herman AG, Kockx MM. Detection of autophagy in tissue by standard immunohistochemistry: possibilities and limitations. Autophagy 2006; 2:55-7. 154
  123. Uchiyama Y. Autophagic cell death and its execution by lysosomal cathepsins. Arch Histol Cytol 2001; 64:233-46. 155
  124. Bursch W, Hochegger K, Torok L, Marian B, Ellinger A, Hermann RS. Autophagic and apoptotic types of programmed cell death exhibit different fates of cytoskeletal filaments. J Cell Sci 2000; 113:1189-98. 156
  125. Biolo G, Fleming RY, Maggi SP, Wolfe RR. Transmembrane transport and intracellular kinetics of amino acids in human skeletal muscle. Am J Physiol 1995; 268:E75-84. 157
  126. Svanberg E, Moller-Loswick AC, Matthews DE, Korner U, Andersson M, Lundholm K. The role of glucose, long-chain triglycerides and amino acids for promotion of amino acid balance across peripheral tissues in man. Clin Physiol 1999; 19:311-20. 158
  127. Denne SC, Liechty EA, Liu YM, Brechtel G, Baron AD. Proteolysis in skeletal muscle and whole body in response to euglycemic hyperinsulinemia in normal adults. Am J Physiol 1991; 261:E809-14. 160
  128. Fukagawa NK, Minaker KL, Young VR, Matthews DE, Bier DM, Rowe JW. Leucine metabolism in aging humans: effect of insulin and substrate availability. Am J Physiol 1989; 256:E288-94. 161
  129. Gelfand RA, Barrett EJ. Effect of physiologic hyperinsulinemia on skeletal muscle protein synthesis and breakdown in man. J Clin Invest 1987; 80:1-6. 162
  130. Mortimore GE, Poso AR. Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu Rev Nutr 1987; 7:539-64. 163
  131. Pozefsky T, Felig P, Tobin JD, Soeldner JS, Cahill GF, Jr. Amino acid balance across tissues of the forearm in postabsorptive man. Effects of insulin at two dose levels. J Clin Invest 1969; 48:2273-82. 164
  132. Finley KD, Edeen PT, Cumming RC, Mardahl-Dumesnil MD, Taylor BJ, Rodriguez MH, Hwang CE, Benedetti M, McKeown M. blue cheese mutations define a novel, conserved gene involved in progressive neural degeneration. J Neurosci 2003; 23:1254-64. 165
  133. Niemann A, Baltes J, Elsasser HP. Fluorescence properties and staining behavior of monodansylpentane, a structural homologue of the lysosomotropic agent monodansylca- daverine. J Histochem Cytochem 2001; 49:177-85. 166
  134. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, Domingo D, Yahalom J. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 2001; 61:439-44. 167
  135. Florez-McClure ML, Linseman DA, Chu CT, Barker PA, Bouchard RJ, Le SS, Laessig TA, Heidenreich KA. The p75 neurotrophin receptor can induce autophagy and death of cerebellar Purkinje neurons. J Neurosci 2004; 24:4498-509. 168
  136. Biederbick A, Kern HF, Elsasser HP. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 1995; 66:3-14. 169
  137. Høyer-Hansen M, Bastholm L, Mathiasen IS, Elling F, Jaattela M. Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ 2005; 12:1297-309. 170
  138. Munafo DB, Colombo MI. A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. J Cell Sci 2001; 114:3619-29. 171
  139. Gutierrez MG, Munafo DB, Beron W, Colombo MI. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 2004; 117:2687-97. 172
  140. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. Potential therapeutic applica- tions of autophagy. Nat Rev Drug Discov 2007; 6:304-12. 173
  141. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P. Distinct classes of phos- phatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 2000; 275:992-8. 174
  142. Kovács AL, Seglen PO. Inhibition of hepatocytic protein degradation by methylaminopu- rines and inhibitors of protein synthesis. Biochim Biophys Acta 1981; 676:213-20. 175
  143. Cantino D, Mosso R, Baccino FM. Changes induced by fasting and cycloheximide in the vacuolar apparatus of rat hepatocytes. A morphometric investigation. Boll Soc Ital Biol Sper 1979; 55:1884-9. 176
  144. Kovács J. Regression of autophagic vacuoles in seminal vesicle cells following cycloheximide treatment. Exp Cell Res 1983; 144:231-4. 177
  145. Kovács J. Morphometric study of the effect of leupeptin, vinblastine, estron acetate and cycloheximide on the autophagic vacuole-lysosomal compartments in mouse seminal vesicle cells. Virchows Arch B Cell Pathol Incl Mol Pathol 1983; 42:83-93. 178
  146. Kovács J, Fellinger E, Karpati PA, Kovács AL, Laszlo L. The turnover of autophagic vacuoles: evaluation by quantitative electron microscopy. Biomed Biochim Acta 1986; 45:1543-7. 179
  147. Papadopoulos T, Pfeifer U. Regression of rat liver autophagic vacuoles by locally applied cycloheximide. Lab Invest 1986; 54:100-7. 180
  148. Rumpelt HJ, Albring M, Thoenes W. Prevention of D-galactosamine-induced hepatocel- lular autophagocytosis by cycloheximide. Virchows Arch B Cell Pathol 1974; 16:195-203. 181
  149. Rumpelt HJ, Weisbach T. Effect of cycloheximide on glucagon-induced autophagy. Quantitative examinations on hepatocytes in the rat. Am J Pathol 1978; 91:49-55. 182
  150. 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. 183
  151. Sasaki K, Murata M, Yasumoto T, Mieskes G, Takai A. Affinity of okadaic acid to type-1 and type-2A protein phosphatases is markedly reduced by oxidation of its 27-hydroxyl group. Biochem J 1994; 298:259-62. 184
  152. Arstila AU, Nuuja IJ, Trump BF. Studies on cellular autophagocytosis. Vinblastine-induced autophagy in the rat liver. Exp Cell Res 1974; 87:249-52. 185
  153. Hirsimaki Y, Arstila AU, Trump BF. Autophagocytosis: in vitro induction by microtuble poisons. Exp Cell Res 1975; 92:11-4. 186
  154. Kominami E, Hashida S, Khairallah EA, Katunuma N. Sequestration of cytoplasmic enzymes in an autophagic vacuole-lysosomal system induced by injection of leupeptin. J Biol Chem 1983; 258:6093-100. 187
  155. Réz G, Csak J, Fellinger E, Laszlo L, Kovács AL, Oliva O, Kovács J. Time course of vinblas- tine-induced autophagocytosis and changes in the endoplasmic reticulum in murine pancre- atic acinar cells: a morphometric and biochemical study. Eur J Cell Biol 1996; 71:341-50. 188
  156. Réz G, Fellinger E, Reti M, Biczo I, Kovács AL. Time course of quantitative morphological changes of the autophagic-lysosomal compartment of murine seminal vesicle epithelial cells under the influence of vinblastine. J Submicrosc Cytol Pathol 1990; 22:529-34. 189
  157. Oliva O, Réz G, Pálfia Z, Fellinger E. Dynamics of vinblastine-induced autophagocytosis in murine pancreatic acinar cells: influence of cycloheximide post-treatments. Exp Mol Pathol 1992; 56:76-86. 190
  158. Sakagami H, Kawase M, Wakabayashi H, Kurihara T. Factors that affect the type of cell death induced by chemicals. Autophagy 2007; 3:493-5. 191
  159. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, Cecconi F. Ambra1 regulates autophagy and development of the nervous system. Nature 2007; 447:1121-5. 192
  160. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. The role of autophagy during the early neonatal starvation period. Nature 2004; 432:1032-6. 193
  161. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122:927-39. 194
  162. Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, Gottlieb RA, Gustafsson AB. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 2007; 14:146-57. 195
  163. Blommaart EF, Luiken JJ, Blommaart PJ, van Woerkom GM, Meijer AJ. Phosphorylation of ribosomal protein S6 is inhibitory for autophagy in isolated rat hepatocytes. J Biol Chem 1995; 270:2320-6. 197
  164. Klionsky DJ, Meijer AJ, Codogno P, Neufeld TP, Scott RC. Autophagy and p70S6 kinase. Autophagy 2005; 1:59-61. 198
  165. Noda T, Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 1998; 273:3963-6. 199
  166. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 2005; 170:1101-11. 200
  167. Sarkar S, Perlstein EO, Imarisio S, Pineau S, Cordenier A, Maglathlin RL, Webster JA, Lewis TA, O'Kane CJ, Schreiber SL, Rubinsztein DC. Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat Chem Biol 2007; 3:331-8. 202
  168. Zhang L, Yu J, Pan H, Hu P, Hao Y, Cai W, Zhu H, Yu AD, Xie X, Ma D, Yuan J. Small molecule regulators of autophagy identified by an image-based high-throughput screen Proc Natl Acad Sci U S A 2007; 104:19023-8. 203
  169. Gordon PB, Kisen GO, Kovács AL, Seglen PO. Experimental characterization of the autophagic-lysosomal pathway in isolated rat hepatocytes. Biochem Soc Symp 1989; 55:129-43. 204
  170. Poli A, Gordon PB, Schwarze PE, Grinde B, Seglen PO. Effects of insulin and anchorage on hepatocytic protein metabolism and amino acid transport. J Cell Sci 1981; 48:1-18. 205
  171. Schliess F, Reissmann R, Reinehr R, vom Dahl S, Häussinger D. Involvement of integrins and Src in insulin signaling toward autophagic proteolysis in rat liver. J Biol Chem 2004; 279:21294-301. 206
  172. vom Dahl S, Dombrowski F, Schmitt M, Schliess F, Pfeifer U, Häussinger D. Cell hydration controls autophagosome formation in rat liver in a microtubule-dependent way downstream from p38MAPK activation. Biochem J 2001; 354:31-6. 207
  173. vom Dahl S, Stoll B, Gerok W, Häussinger D. Inhibition of proteolysis by cell swelling in the liver requires intact microtubular structures. Biochem J 1995; 308:529-36. 208
  174. Seleverstov O, Zabirnyk O, Zscharnack M, Bulavina L, Nowicki M, Heinrich JM, Yezhelyev M, Emmrich F, O'Regan R, Bader A. Quantum dots for human mesenchymal stem cells labeling. A size-dependent autophagy activation. Nano Lett 2006; 6:2826-32.

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Authors
Klionsky, D. J., Abeliovich, H., Agostinis, P., Agrawal, D. K., Aliev, G., Askew, D. S., Baba, M., Baehrecke, E. H., Bahr, B. A., Ballabio, A., Bamber, B. A., Bassham, D. C., Bergamini, E., Bi, X., Biard-Piechaczyk, M., Blum, J. S., Bredesen, D. E., Brodsky, J. L., Brumell, J. H., Brunk, U. T., Bursch, W., Camougrand, N., Cebollero, E., Cecconi, F., Chen, Y., Chin, L.-S., Choi, A., Chu, C. T., Chung, J., Clark, R. S. B., Clarke, P. G. H., Clarke, S. G., Clave, C., Cleveland, J. L., Codogno, P., Colombo, M. I., Coto-Montes, A., Cregg, J. M., Cuervo, A. M., Debnath, J., Dennis, P. B., Dennis, P. A., Demarchi, F., Deretic, V., Devenish, R. J., Di Sano, F., Dice, J. F., Distelhorst, C. W., Dinesh-Kumar, S. P., Eissa, N. T., DiFiglia, M., Djavaheri-Mergny, M., Dorsey, F. C., Dröge, W., Dron, M., Dunn, Jr., Duszenko, M., Elazar, Z., Esclatine, A., Eskelinen, E.-L., Fésüs, L., Finley, K. D., Fuentes, J. M., Fueyo-Margareto, J., Fujisaki, K., Galliot, B., Gao, F.-B., Gewirtz, D. A., Gibson, S. B., Gohla, A., Goldberg, A. L., Gonzalez, R., González-Estévez, C., Gorski, S. M., Gottlieb, R. A., Häussinger, D., He, Y.-W., Heidenreich, K., Hill, J. A., Høyer-Hansen, M., Hu, X., Huang, W.-P., Iwasaki, A., Jäättelä, M., Jackson, W. T., Jiang, X., Jin, S. V., Johansen, T., Jung, J. U., Kadowaki, M., Kang, C., Kelekar, A., Kessel, D. H., Kiel, J. A. K. W., Kim, H. P., Kimchi, A., Kinsella, T. J., Kiselyov, K., Kitamoto, K., Knecht, E., Komatsu, M., Kominami, E., Kondo, S., Kovács, A. L., Kroemer, G., Kuan, C.-Y., Kumar, R., Kundu, M., Landry, J., Laporte, M., Le, W., Lei, H.-Y., Levine, B., Lieberman, A. P., Lim, K.-L., Lin, F.-C., Liou, W., Liu, L. F., Lopez-Berestein, G., López-Otín, C., Lu, B., Macleod, K. F., Malorni, W., Martinet, W., Matsuoka, K., Mautner, J., Meijer, A. J., Meléndez, A., Michels, P., Miotto, G., Mistiaen, W. P., Mizushima, N., Mograbi, B., Moore, M. N., Moreira, P. I., Moriyasu, Y., Motyl, T., Münz, C., Murphy, L. O., Naqvi, N. I., Neufeld, T. P., Nishino, I., Nixon, R. A., Noda, T., Nürnberg, B., Ogawa, M., Oleinick, N. L., Olsen, L. J., Ozpolat, B., Paglin, S., Palmer, G. E., Papassideri, I. S., Parkes, M., Perlmutter, D. H., Perry, G., Piacentini, M., Pinkas-Kramarski, R., Prescott, M., Proikas-Cezanne, T., Raben, N., Rami, A., Reggiori, F., Rohrer, B., Rubinsztein, D. C., Ryan, K. M., Sadoshima, J., Sakagami, H., Sakai, Y., Sandri, M., Sasakawa, C., Sass, M., Schneider, C., Seglen, P. O., Seleverstov, O., Settleman, J., Shacka, J. J., Shapiro, I. M., Sibirny, A. A., Silva-Zacarin, E. C. M., Simon, H.-U., Simone, C., Simonsen, A., Smith, M. A., Spanel-Borowski, K., Srinivas, V., Steeves, M., Stenmark, H., Stromhaug, P. E., Subauste, C. S., Sugimoto, S., Sulzer, D., Suzuki, T., Swanson, M. S., Tabas, I., Takeshita, F., Talbot, N. J., Tallóczy, Z., Tanaka, K., Tanaka, K., Tanida, I., Taylor, G. S., Taylor, J. P., Terman, A., Tettamanti, G., Thompson, C. B., Thumm, M., Tolkovsky, A. M., Tooze, S. A., Truant, R., Tumanovska, L. V., Uchiyama, Y., Ueno, T., Uzcátegui, N. L., van der Klei, I. J., Vaquero, E. C., Vellai, T., Vogel, M. W., Wang, H.-G., Webster, P., Xi, Z., Xiao, G., Yahalom, J., Yang, J.-M., Yap, G. S., Yin, X.-M., Yoshimori, T., Yue, Z., Yuzaki, M., Zabirnyk, O., Zheng, X., Zhu, X., & Deter, R. L.
Affiliations
  • University of Michigan (US)
  • Hebrew University of Jerusalem (IL)
  • KU Leuven (BE)
  • Creighton University (US)
  • The University of Texas at San Antonio (US)
  • University of Cincinnati (US)
  • Japan Women's University (JP)
  • University of Massachusetts Chan Medical School (US)
  • University of Connecticut (US)
  • Telethon Institute Of Genetics And Medicine (IT)
  • University of Toledo (US)
  • Iowa State University (US)
  • University of Pisa (IT)
  • Western University of Health Sciences (US)
  • Indiana University Indianapolis (US)
  • Buck Institute for Research on Aging (US)
  • University of Pittsburgh (US)
  • Hospital for Sick Children (CA)
  • Linköping University (SE)
  • Medical University of Vienna (AT)
  • Centre National de la Recherche Scientifique (FR)
  • Instituto de Fermentaciones Industriales (ES)
  • University of Rome Tor Vergata (IT)
  • Peking University (CN)
  • Emory University (US)
  • Brigham and Women's Hospital (US)
  • Korea Advanced Institute of Science and Technology (KR)
  • University of Lausanne (CH)
  • University of California, Los Angeles (US)
  • Scripps Research Institute (US)
  • Université Paris-Sud (FR)
  • Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
  • Universidad de Oviedo (ES)
  • University of California, San Francisco (US)
  • National Cancer Institute (US)
  • Consorzio Interuniversitario per le Biotecnologie (IT)
  • University of New Mexico (US)
  • Monash University (AU)
  • Tufts University (US)
  • University Hospitals of Cleveland (US)
  • Massachusetts General Hospital (US)
  • Québec-Océan (CA)
  • Virologie et Immunologie Moléculaires (FR)
  • University of Debrecen (HU)
  • Keck Graduate Institute (US)
  • Albert Einstein College of Medicine (US)
ORCID
Venue
Autophagy
Publisher
Informa UK Limited
Published
2008-02-16
Volume
4
Issue
2
Pages
151-175
ISSN
  • 1554-8627 (ISSN-L)
  • 1554-8635
DOI
10.4161/auto.5338
PMC
PMC2654259
OpenAlex
W2135574023
Cited by
2,230
References
29
Citations by year
2026: 33 · 2025: 29 · 2024: 44 · 2023: 48 · 2022: 42 · 2021: 55 · 2020: 78 · 2019: 58 · 2018: 82 · 2017: 88 · 2016: 112 · 2015: 144 · 2014: 133 · 2013: 226 · 2012: 331
FWCI
25.76
Type
journal article
Language
en
Open access
Locations
  • Autophagy (publishedVersion)
  • PubMed (publishedVersion)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
  • Archive ouverte UNIGE (University of Geneva) (publishedVersion)
  • PubMed Central (acceptedVersion)
  • BORIS (University Library Bern) (acceptedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (acceptedVersion, other-oa)
  • IRIS (submittedVersion)
  • Padua Research Archive (University of Padova) (submittedVersion, other-oa)
  • Iowa State University Digital Repository (Iowa State University) (submittedVersion)
  • National University of Singapore (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
  • HAL (submittedVersion)
  • Institutional Research Information System (University of Udine) (submittedVersion)
  • CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
  • Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
  • DIAL (Catholic University of Leuven) (submittedVersion)
  • Consultation of the Doctoral Thesis Database (TESEO) (Ministerio de Educación, Cultura y Deporte) (submittedVersion)
  • IrInSubria (University of Insubria) (submittedVersion)
  • Lirias (submittedVersion)
  • Site cant be reached (submittedVersion)
  • RIUR (Universidad de La Rioja) (submittedVersion, other-oa)
  • Pure Amsterdam UMC (submittedVersion)
  • University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
  • Bristol Research (University of Bristol) (submittedVersion)
  • SERVAL (Université de Lausanne) (submittedVersion, other-oa)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
Funders
  • Wellcome Trust (064354)
  • National Institutes of Health
  • Biotechnology and Biological Sciences Research Council (BB/E01030X/1)
  • National Institute on Aging (R01AG026389)
  • National Eye Institute (R01EY013520)
  • National Cancer Institute (R01CA023378)
  • National Institute of General Medical Sciences (GM 53396, R01GM075061, R01GM062509, R01GM053396)
  • National Institute of Allergy and Infectious Diseases (R01AI079065, R01AI073099, P01AI056097)
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR055255)
Topics
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords
macroautophagy, autophagic flux, autophagosome accumulation, lysosomal degradation, higher eukaryotes, assay interpretation, autophagy monitoring
MeSH terms
Autophagy-Related Protein 8 Family, Animals, Autophagy, Data Interpretation, Statistical, Eukaryotic Cells, Humans, Microscopy, Fluorescence, Microtubule-Associated Proteins, Models, Biological, Phagosomes, Plants, Protein Processing, Post-Translational, Guidelines as Topic, Clinical Laboratory Techniques, Protein Transport, Saccharomyces cerevisiae Proteins

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