LC3 conjugation system in mammalian autophagy

International Journal of Biochemistry and Cell Biology

Volumn 36, Issue 12, 2004, Pages 2503-2518

  Tanida, Isei ^a   Ueno, Takashi ^a   Kominami, Eiki ^a  

^a JUNTENDO UNIVERSITY   (Japan)

Author keywords

Atg8; Autophagosomes; Autophagy; GABARAP; GATE 16

Indexed keywords

HYDROLASE; MARKER; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN; PROTEIN GABARAP; PROTEIN GATE 16; PROTEIN LC3; UNCLASSIFIED DRUG;

APOPTOSIS; AUTOPHAGY; BACTERIAL INFECTION; CARCINOGENESIS; CARDIOMYOPATHY; CELL DIFFERENTIATION; CELL MATURATION; CELL ORGANELLE; CELL VIABILITY; CONJUGATION; CYTOSOL; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DISTAL MYOPATHY; HEALTH; HUMAN; HUNTINGTON CHOREA; LYSOSOME; MALIGNANT NEOPLASTIC DISEASE; MAMMAL CELL; MOLECULAR MECHANICS; NEUROMUSCULAR DISEASE; NONHUMAN; ORTHOLOGY; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MODIFICATION; REVIEW; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STARVATION; STRUCTURE ANALYSIS; TISSUE DISTRIBUTION; UBIQUITINATION; VIRUS INFECTION; YEAST;

ANIMALS; AUTOPHAGY; BACTERIAL INFECTIONS; CELL DIFFERENTIATION; HUMANS; MAMMALS; MICROTUBULE-ASSOCIATED PROTEINS; NEOPLASMS; NEUROMUSCULAR DISEASES; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 4344624322     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2004.05.009     Document Type: Review

References (100)

1. Aki T., Yamaguchi K., Fujimiya T., Mizukami Y. Phosphoinositide 3-kinase accelerates autophagic cell death during glucose deprivation in the rat cardiomyocyte-derived cell line H9c2. Oncogene. 20:2003;8529-8535
2. Arico S., Petiot A., Bauvy C., Dubbelhuis P.F., Meijer A.J., Codogno P., et al. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J Biol Chem. 276:2001;35243-35246
3. Asanuma K., Tanida I., Shirato I., Ueno T., Takahara H., Nishitani T., et al. MAP-LC3, a promising autophagosomal marker, is processed during the differentiation and recovery of podocytes from PAN nephrosis. FASEB J. 17:2003;1165-1167
4. Baehrecke E.H. Autophagic programmed cell death in Drosophila. Cell Death Differ. 10:2003;940-945
5. Beron W., Gutierrez M.G., Rabinovitch M., Colombo M.I. Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immunol. 70:2002;5816-5821
6. Bursch W. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8:2001;569-581
7. Cuervo A.M. Autophagy and aging - when "all you can eat" is yourself. Sci Aging Knowledge Environ. 36:2003;25
8. Dorn B.R., Dunn W.A. Jr., Progulske-Fox A. Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect Immunol. 69:2001;5698-5708
9. Dorn B.R., Dunn W.A. Jr., Progulske-Fox A. Bacterial interactions with the autophagic pathway. Cell Microbiol. 4:2002;1-10
10. Edinger A.L., Thompson C.B. Defective autophagy leads to cancer. Cancer Cell. 4:2003;422-424
11. Eisenberg I., Avidan N., Potikha T., Hochner H., Chen M., Olender T., et al. The UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase gene is mutated in recessive hereditary inclusion body myopathy. Nat Genet. 29:2001;83-87
12. Eskelinen E.L., Tanaka Y., Saftig P. At the acidic edge: Emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13:2003;137-145
13. Harding T.M., Morano K.A., Scott S.V., Klionsky D.J. Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol. 131:1995;591-602
14. Hemelaar J., Lelyveld V.S., Kessler B.M., Ploegh H.L. A single protease, Apg4B, is specific for the autophagy-related ubiquitin-like proteins GATE-16, MAP1-LC3, GABARAP, and Apg8L. J Biol Chem. 278:2003;51841-51850
15. Houri J.J., Ogier-Denis E., De Stefanis D., Bauvy C., Baccino F.M., Isidoro C., et al. Differentiation-dependent autophagy controls the fate of newly synthesized N-linked glycoproteins in the colon adenocarcinoma HT-29 cell line. Biochem J. 309:1995;521-527
16. Ichimura Y., Kirisako T., Takao T., Satomi Y., Shimonishi Y., Ishihara N., et al. A ubiquitin-like system mediates protein lipidation. Nature. 408:2000;488-492
17. Ishikawa T., Furuno K., Kato K. Ultrastructural studies on autolysosomes in rat hepatocytes after leupeptin treatment. Exp Cell Res. 144:1983;15-24
18. Juhasz G., Csikos G., Sinka R., Erdelyi M., Sass M. The Drosophila homolog of Aut1 is essential for autophagy and development. FEBS Lett. 543:2003;154-158
19. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:2000;5720-5728
20. Kadowaki M., Venerando R., Miotto G., Mortimore G.E. Mechanism of autophagy in permeabilized hepatocytes: Evidence for regulation by GTP binding proteins. Adv Exp Med Biol. 389:1996;113-119
21. Kametaka S., Matsuura A., Wada Y., Ohsumi Y. Structural and functional analyses of APG5, a gene involved in autophagy in yeast. Gene. 178:1996;139-143
22. Kametaka S., Okano T., Ohsumi M., Ohsumi Y. Apg14p and Apg6/Vps30p form a protein complex essential for autophagy in the yeast, Saccharomyces cerevisiae. J Biol Chem. 273:1998;22284-22291
23. Kanzawa T., Germano I.M., Komata T., Ito H., Kondo Y., Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 11:2004;448-457
24. Kegel K.B., Kim M., Sapp E., McIntyre C., Castano J.G., Aronin N., et al. Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J Neurosci. 20:2000;7268-7278
25. Kihara A., Kabeya Y., Ohsumi Y., Yoshimori T. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2:2001;330-335
26. Kihara A., Noda T., Ishihara N., Ohsumi Y. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol. 152:2001;519-530
27. Kim J., Dalton V.M., Eggerton K.P., Scott S.V., Klionsky D.J. Apg7p/Cvt2p is required for the cytoplasm-to-vacuole targeting, macroautophagy, and peroxisome degradation pathways. Mol Biol Cell. 10:1999;1337-1351
28. Kirisako T., Ichimura Y., Okada H., Kabeya Y., Mizushima N., Yoshimori T., et al. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol. 151:2000;263-276
29. Kisen G.O., Tessitore L., Costelli P., Gordon P.B., Schwarze P.E., Baccino F.M., et al. Reduced autophagic activity in primary rat hepatocellular carcinoma and ascites hepatoma cells. Carcinogenesis. 14:1993;2501-2505
30. Klionsky D.J., Emr S.D. Autophagy as a regulated pathway of cellular degradation. Science. 290:2000;1717-1721
31. Klionsky D.J., Cregg J.M., Dunn W.A. Jr., Emr S.D., Sakai Y., Sandoval I.V., et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell. 5:2003;539-545
32. D.J. Klionsky (Ed.) (2004). Autophagy. Georgetown, Texas: Landes Bioscience.
33. Komatsu M., Tanida I., Ueno T., Ohsumi M., Ohsumi Y., Kominami E. The C-terminal region of an Apg7p/Cvt2p is required for homodimerization and is essential for its E1 activity and E1-E2 complex formation. J Biol Chem. 276:2001;9846-9854
34. Kumamoto T., Abe T., Nagao S., Ueyama H., Tsuda T. Immunohistochemical study of clathrin in distal myopathy with rimmed vacuoles. Acta Neuropathol (Berl). 95:1998;571-575
35. Lang T., Schaeffeler E., Bernreuther D., Bredschneider M., Wolf D.H., Thumm M. Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J. 17:1998;3597-3607
36. Larsen K.E., Sulzer D. Autophagy in neurons: A review. Histol Histopathol. 17:2002;897-908
37. Lemasters J.J., Qian T., He L., Kim J.S., Elmore S.P., Cascio W.E., et al. Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid Redox Signal. 4:2002;769-781
38. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 402:1999;672-676
39. Lockshin R.A., Zakeri Z. Caspase-independent cell deaths. Curr Opin Cell Biol. 14:2002;727-733
40. Mann S.S., Hammarback J.A. Molecular characterization of light chain. Part 3. A microtubule binding subunit of MAP1A and MAP1B. J Biol Chem. 269:1994;11492-11497
41. Marino G., Uria J.A., Puente X.S., Quesada V., Bordallo J., Lopez-Otin C. Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem. 278:2003;3671-3678
42. Matsuura A., Tsukada M., Wada Y., Ohsumi Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene. 192:1997;245-250
43. Meier P., Silke J. Programmed cell death: Superman meets Dr. Death. Nat Cell Biol. 5:2003;1035-1038
44. Meijer A.J., Dubbelhuis P.F. Amino acid signaling and the integration of metabolism. Biochem Biophys Res Commun. 313:2004;397-403
45. Mizushima N., Noda T., Yoshimori T., Tanaka Y., Ishii T., George M.D., et al. A protein conjugation system essential for autophagy. Nature. 395:1998;395-398
46. Mizushima N., Yamamoto A., Hatano M., Kobayashi Y., Kabeya Y., Suzuki K., et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol. 152:2001;657-668
47. Mizushima N., Kuma A., Kobayashi Y., Yamamoto A., Matsubae M., Takao T., et al. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci. 116:2003;1679-1688
48. Mizushima N., Noda T., Ohsumi Y. Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J. 18:1999;3888-3896
49. Mizushima N., Sugita H., Yoshimori T., Ohsumi Y. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J Biol Chem. 273:1998;33889-33892
50. 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. 15:2004;1101-1111
51. Mizushima N., Yoshimori T., Ohsumi Y. Mouse Apg10 as an Apg12-conjugating enzyme: Analysis by the conjugation-mediated yeast two-hybrid method. FEBS Lett. 532:2002;450-454
52. Mizushima N., Yoshimori T., Ohsumi Y. Role of the Apg12 conjugation system in mammalian autophagy. Int J Biochem Cell Biol. 35:2003;553-561
53. Nakanishi H. Neuronal and microglial cathepsins in aging and age-related diseases. Ageing Res Rev. 2:2003;367-381
54. Nemoto T., Tanida I., Tanida-Miyake E., Minematsu-Ikeguchi N., Yokota M., Ohsumi M., et al. The mouse APG10 homologue, an E2-like enzyme for Apg12p conjugation, facilitates MAP-LC3 modification. J Biol Chem. 278:2003;39517-39526
55. Nishino I., Fu J., Tanji K., Yamada T., Shimojo S., Koori T., et al. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature. 406:2000;906-910
56. Nishino I. Autophagic vacuolar myopathies. Curr Neurol Neurosci Rep. 3:2003;64-69
57. Noguchi S., Keira Y., Murayama K., Ogawa M., Fujita M., Kawahara G., et al. Reduction of UDP-GlcNAc 2-epimerase/ManNAc kinase activity and sialylation in distal myopathy with rimmed vacuoles. J Biol Chem. 279:2004;11402-11407
58. Ogier-Denis E., Codogno P. Autophagy: A barrier or an adaptive response to cancer. Biochim Biophys Acta. 1603:2003;113-128
59. Ohsumi Y. Molecular dissection of autophagy: Two ubiquitin-like systems. Nat Rev Mol Cell Biol. 2:2001;211-216
60. Okazaki N., Yan J., Yuasa S., Ueno T., Kominami E., Masuho Y., et al. Interaction of the Unc-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: Possible role of vesicular transport in axonal elongation. Brain Res Mol Brain Res. 85:2000;1-12
61. Otto G.P., Wu M.Y., Clarke M., Lu H., Anderson O.R., Hilbi H., et al. Macroautophagy is dispensable for intracellular replication of Legionella pneumophila in Dictyostelium discoideum. Mol Microbiol. 51:2004;63-72
62. Otto G.P., Wu M.Y., Kazgan N., Anderson O.R., Kessin R.H. Macroautophagy is required for multicellular development of the social amoeba Dictyostelium discoideum. J Biol Chem. 278:2003;17636-17645
63. Perlmutter D.H. Liver injury in alpha1-antitrypsin deficiency: An aggregated protein induces mitochondrial injury. J Clin Invest. 110:2002;1579-1583
64. Petersen A., Brundin P. Huntington's disease: The mystery unfolds? Int Rev Neurobiol. 53:2002;315-339
65. Prentice E., Jerome W.G., Yoshimori T., Mizushima N., Denison M.R. Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem. 279:2004;10136-10141
66. Qu X., Yu J., Bhagat G., Furuya N., Hibshoosh H., Troxel A., et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest. 112:2003;1809-1820
67. Ravikumar B., Stewart A., Kita H., Kato K., Duden R., Rubinsztein D.C. Raised intracellular glucose concentrations reduce aggregation and cell death caused by mutant huntingtin exon 1 by decreasing mTOR phosphorylation and inducing autophagy. Hum Mol Genet. 12:2003;985-994
68. Ravikumar B., Duden R., Rubinsztein D.C. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet. 11:2002;1107-1117
69. Reggiori F., Klionsky D.J. Autophagy in the eukaryotic cell. Eukaryot Cell. 1:2002;11-21
70. Rich K.A., Burkett C., Webster P. Cytoplasmic bacteria can be targets for autophagy. Cell Microbiol. 5:2003;455-468
71. Riddle D.L., Gorski S.M. Shaping and stretching life by autophagy. Dev Cell. 5:2003;364-365
72. Saftig P., Tanaka Y., Lullmann-Rauch R., von Figura K. Disease model: LAMP-2 enlightens Danon disease. Trends Mol Med. 7:2001;37-39
73. Sagiv Y., Legesse-Miller A., Porat A., Elazar Z. GATE-16, a membrane transport modulator. EMBO J. 19:2000;1494-1504
74. Scherz-Shouval R., Sagiv Y., Shorer H., Elazar Z. The COOH terminus of GATE-16, an intra-Golgi transport modulator, is cleaved by the human cysteine protease HsApg4A. J Biol Chem. 278:2003;14053-14058
75. Schlegel A., Giddings T.H. Jr., Ladinsky M.S., Kirkegaard K. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J Virol. 70:1996;6576-6588
76. Schworer C.M., Shiffer K.A., Mortimore G.E. Quantitative relationship between autophagy and proteolysis during graded amino acid deprivation in perfused rat liver. J Biol Chem. 256:1981;7652-7658
77. Seglen P.O., Berg T.O., Blankson H., Fengsrud M., Holen I., Stromhaug P.E. Structural aspects of autophagy. Adv Exp Med Biol. 389:1996;103-111
78. Shintani T., Mizushima N., Ogawa Y., Matsuura A., Noda T., Ohsumi Y. Apg10p, a novel protein-conjugating enzyme essential for autophagy in yeast. EMBO J. 18:1999;5234-5241
79. Stromhaug P.E., Klionsky D.J. Approaching the molecular mechanism of autophagy. Traffic. 2:2001;524-531
80. Suhy D.A., Giddings T.H. Jr., Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: An autophagy-like origin for virus-induced vesicles. J Virol. 74:2000;8953-8965
81. Suzuki T., Nakagawa M., Yoshikawa A., Sasagawa N., Yoshimori T., Ohsumi Y., et al. The first molecular evidence that autophagy relates rimmed vacuole formation in chloroquine myopathy. J Biochem (Tokyo). 131:2002;647-651
82. Tanaka Y., Guhde G., Suter A., Eskelinen E.L., Hartmann D., Lullmann-Rauch R., et al. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature. 406:2000;902-906
83. Tanida I., Mizushima N., Kiyooka M., Ohsumi M., Ueno T., Ohsumi Y., et al. Apg7p/Cvt2p: A novel protein-activating enzyme essential for autophagy. Mol Biol Cell. 10:1999;1367-1379
84. Tanida I., Tanida-Miyake E., Komatsu M., Ueno T., Kominami E. Human Apg3p/Aut1p homologue is an authentic E2 enzyme for multiple substrates, GATE-16, GABARAP, and MAP-LC3, and facilitates the conjugation of hApg12p to hApg5p. J Biol Chem. 277:2002a;13739-13744
85. Tanida I., Nishitani T., Nemoto T., Ueno T., Kominami E. Mammalian Apg12p, but not the Apg12p-Apg5p conjugate, facilitates LC3 processing. Biochem Biophys Res Commun. 296:2002b;1164-1170
86. Tanida I., Tanida-Miyake E., Nishitani T., Komatsu M., Yamazaki H., Ueno T., et al. Murine Apg12p has a substrate preference for murine Apg7p over three Apg8p homologs. Biochem Biophys Res Commun. 292:2002c;256-262
87. Tanida I., Komatsu M., Ueno T., Kominami E. GATE-16 and GABARAP are authentic modifiers mediated by Apg7 and Apg3. Biochem Biophys Res Commun. 300:2003;637-644
88. Tanida I., Tanida-Miyake E., Ueno T., Kominami E. The human homolog of Saccharomyces cerevisiaeApg7p is a Protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J Biol Chem. 276:2001;1701-1706
89. Thumm M., Kadowaki T. The loss of Drosophila APG4/AUT2 function modifies the phenotypes of cut and Notch signaling pathway mutants. Mol Genet Genom. 266:2001;657-663
90. Thumm M., Egner R., Koch B., Schlumpberger M., Straub M., Veenhuis M., et al. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349:1994;275-280
91. Thumm M. Structure and function of the yeast vacuole and its role in autophagy. Microsc Res Technol. 51:2000;563-572
92. Thumm M. Hitchhikers guide to the vacuole-mechanisms of cargo sequestration in the Cvt and autophagic pathways. Mol Cell. 10:2002;1257-1258
93. Thummel C.S. Steroid-triggered death by autophagy. Bioessays. 23:2001;677-682
94. Tolkovsky A.M., Xue L., Fletcher G.C., Borutaite V. Mitochondrial disappearance from cells: A clue to the role of autophagy in programmed cell death and disease? Biochimie. 84:2002;233-240
95. Tsukada M., Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333:1993;169-174
96. Ueno, T., Tanida, I., & Kominami, E. (2004). In D. Klionsky (Ed.), Autophagy and neuromuscular diseases in autophagy (pp. 264-286). Georgetown, TX: Landes Bioscience.
97. Wang H., Bedford F.K., Brandon N.J., Moss S.J., Olsen R.W. GABAA-receptor-associated protein links GABAA receptors and the cytoskeleton. Nature. 397:1999;69-72
98. Yoshimori T. Autophagy: A regulated bulk degradation process inside cells. Biochem Biophys Res Commun. 313:2004;453-458
99. Yuan W., Stromhaug P.E., Dunn W.A. Jr. Glucose-induced autophagy of peroxisomes in Pichia pastoris requires a unique E1-like protein. Mol Biol Cell. 10:1999;1353-1366
100. Yue Z., Jin S., Yang C., Levine A.J., Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA. 100:2003;15077-15082