Historical landmarks of autophagy research

Cell Research - Tập 24 Số 1 - Trang 9-23 - 2014
Yoshinori Ohsumi1
1Frontier Research Center, Tokyo Institute of Technology, Yokohama 226–8503, Japan

Tóm tắt

Từ khóa


Tài liệu tham khảo

Schoenheimer R . The Dynamic State of Body Constituents. The Edward K. Dunham Lectures for the Promotion of the Medical Sciences. Harvard University Press, 1942.

Schoenheimer R, Ratner S, Rittenberg D . The process of continuous deamination and reamination of amino acids in the proteins of normal animals. Science 1939; 89:272–273.

Ganschow RE, Schimke RT . Independent genetic control of the catalytic activity and the rate of degradation of catalase in mice. J Biol Chem 1969; 244:4649–4658.

Kalish F, Chovick N, Dice JF . Rapid in vivo degradation of glycoproteins isolated from cytosol. J Biol Chem 1979; 254:4475–4481.

de Duve C, Pressman BC, Gianetto R, Wattiaux R, Appelmans F . Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J 1955; 60:604–617.

de Duve C . The lysosome turns fifty. Nat Cell Biol 2005; 7:847–849.

Novikoff AB, Beaufay H, de Duve C . Electron microscopy of lysosome-rich fractions from rat liver. J Biophys Biochem Cytol 1956; 2:179–184.

de Duve C, Wattiaux R . Functions of lysosomes. Annu Rev Physiol 1966; 28:435–492.

Clark SLJ . Cellular differentiation in the kidneys of newborn mice studies with the electron microscope. J Biophys Biochem Cytol 1957; 3:349–362.

Ashford TP, Porter KR . Cytoplasmic components in hepatic cell lysosomes. J Cell Biol 1962; 12:198–202.

Arstila AU, Trump BF . Studies on cellular autophagocytosis. The formation of autophagic vacuoles in the liver after glucagon administration. Am J Pathol 1968; 53:687–733.

de Duve C, Foundation C . Ciba Foundation Symposium: Lysosome. De Reuck A, Cameron MP, eds. Little, Brown, 1963.

Matile P . Biochemistry and function of vacuoles. Annu Rev Plant Physiol 1978; 29:193–213.

Deter RL, Baudhuin P, de Duve C . Participation of lysosomes in cellular autophagy induced in rat liver by glucagon. J Cell Biol 1967; 35:C11–C16.

Pfeifer U, Strauss P . Autophagic vacuoles in heart muscle and liver. A comparative morphometric study including circadian variations in meal-fed rats. J Mol Cell Cardiol 1981; 13:37–49.

Pfeifer U, Warmuth-Metz M . Inhibition by insulin of cellular autophagy in proximal tubular cells of rat kidney. Am J Physiol 1983; 244:E109–E114.

Mortimore GE, Ward WF . Behavior of the lysosomal system during organ perfusion. An inquiry into the mechanism of hepatic proteolysis. Front Biol 1976; 45:157–184.

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 USA 1983; 80:2179–2183.

Seglen PO, Gordon PB, Poli A . Amino acid inhibition of the autophagic/lysosomal pathway of protein degradation in isolated rat hepatocytes. Biochim Biophys Acta 1980; 630:103–118.

Nicklin P, Bergman P, Zhang B, et al. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 2009; 136:521–534.

Sheen JH, Zoncu R, Kim D, Sabatini DM . Defective regulation of autophagy upon leucine deprivation reveals a targetable liability of human melanoma cells in vitro and in vivo. Cancer Cell 2011; 19:613–628.

Seglen PO, Gordon PB . 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci USA 1982; 79:1889–1892.

Blommaart EF, Krause U, Schellens JP, Vreeling-Sindelarova H, Meijer AJ . The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 1997; 243:240–246.

Furuya N, Kanazawa T, Fujimura S, Ueno T, Kominami E, Kadowaki M . Leupeptin-induced appearance of partial fragment of betaine homocysteine methyltransferase during autophagic maturation in rat hepatocytes. J Biochem 2001; 129:313–320.

Holen I, Gordon PB, Seglen PO . Protein kinase-dependent effects of okadaic acid on hepatocytic autophagy and cytoskeletal integrity. Biochem J 1992; 284:633–636.

Holen I, Gordon PB, Seglen PO . Inhibition of hepatocytic autophagy by okadaic acid and other protein phosphatase inhibitors. Eur J Biochem 1993; 215:113–122.

Masaki R, Yamamoto A, Tashiro Y . Cytochrome P-450 and NADPH-cytochrome P-450 reductase are degraded in the autolysosomes in rat liver. J Cell Biol 1987; 104:1207–1215.

van der Klei IJ, Harder W, Veenhuis M . Biosynthesis and assembly of alcohol oxidase, a peroxisomal matrix protein in methylotrophic yeasts: a review. Yeast 1991; 7:195–209.

Marzella L, Ahlberg J, Glaumann H . Autophagy, heterophagy, microautophagy and crinophagy as the means for intracellular degradation. Virchows Archiv B Cell Pathology Zell-pathologie 1981; 36:219–234.

Sakai Y, Koller A, Rangell LK, Keller GA, Subramani S . Peroxisome degradation by microautophagy in Pichia pastoris: identification of specific steps and morphological intermediates. J Cell Biol 1998; 141:625–636.

Dice JF, Walker CD, Byrne B, Cardiel A . General characteristics of protein degradation in diabetes and starvation. Proc Natl Acad Sci USA 1978; 75:2093–2097.

Mortimore GE, Woodside KH, Henry JE . Compartmentation of free valine and its relation to protein turnover in perfused rat liver. J Biol Chem 1972; 247:2776–2784.

Kakinuma Y, Ohsumi Y, Anraku Y . Properties of H+-translocating adenosine triphosphatase in vacuolar membranes of Saccharomyces cerevisiae. J Biol Chem 1981; 256:10859–10863.

Jones EW . Vacuolar proteases and proteolytic artifacts in Saccharomyces cerevisiae. Methods Enzymol 2002; 351:127–150.

Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y . Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol 1992; 119:301–311.

Baba M, Takeshige K, Baba N, Ohsumi Y . Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. J Cell Biol 1994; 124:903–913.

Baba M, Osumi M, Ohsumi Y . Analysis of the membrane structures involved in autophagy in yeast by freeze-replica method. Cell Struct Funct 1995; 20:465–471.

Noda T, Klionsky DJ . The quantitative Pho8Delta60 assay of nonspecific autophagy. Methods Enzymol 2008; 451:33–42.

Tsukada M, Ohsumi Y . Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 1993; 333:169–174.

Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y . Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009; 10:458–467.

Thumm M, Egner R, Koch B, et al. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett 1994; 349:275–280.

Harding TM, Morano KA, Scott SV, Klionsky DJ . Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 1995; 131:591–602.

Baba M, Osumi M, Scott SV, Klionsky DJ, Ohsumi Y . Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J Cell Biol 1997; 139:1687–1695.

Yuan W, Tuttle DL, Shi YJ, Ralph GS, Dunn WAJ . Glucose-induced microautophagy in Pichia pastoris requires the alpha-subunit of phosphofructokinase. J Cell Sci 1997; 110:1935–1945.

Yuan W, Stromhaug PE, Dunn WAJ . Glucose-induced autophagy of peroxisomes in Pichia pastoris requires a unique E1-like protein. Mol Biol Cell 1999; 10:1353–1366.

Mukaiyama H, Oku M, Baba M, et al. Paz2 and 13 other PAZ gene products regulate vacuolar engulfment of peroxisomes during micropexophagy. Genes Cells 2002; 7:75–90.

Titorenko VI, Keizer I, Harder W, Veenhuis M . Isolation and characterization of mutants impaired in the selective degradation of peroxisomes in the yeast Hansenula polymorpha. J Bacteriol 1995; 177:357–363.

Ohsumi Y . Protein turnover. IUBMB Life 2006; 58:363–369.

Matsuura A, Tsukada M, Wada Y, Ohsumi Y . Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 1997; 192:245–250.

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 2001; 152:519–530.

Mizushima N, Noda T, Yoshimori T, et al. A protein conjugation system essential for autophagy. Nature 1998; 395:395–398.

Mizushima N, Noda T, Ohsumi Y . Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J 1999; 18:3888–3896.

Kuma A, Mizushima N, Ishihara N, Ohsumi Y . Formation of the approximately 350-kDa Apg12-Apg5.Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J Biol Chem 2002; 277:18619–18625.

Kirisako T, Baba M, Ishihara N, et al. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol 1999; 147:435–446.

Ichimura Y, Kirisako T, Takao T, et al. A ubiquitin-like system mediates protein lipidation. Nature 2000; 408:488–492.

Kirisako T, Ichimura Y, Okada H, 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 2000; 151:263–276.

Xie Z, Nair U, Klionsky DJ . Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 2008; 19:3290–3298.

Yamaguchi M, Matoba K, Sawada R, et al. Noncanonical recognition and UBL loading of distinct E2s by autophagy-essential Atg7. Nat Struct Mol Biol 2012; 19:1250–1256.

Hanada T, Noda NN, Satomi Y, et al. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 2007; 282:37298–37302.

Sakoh-Nakatogawa M, Matoba K, Asai E, et al. Atg12-Atg5 conjugate enhances E2 activity of Atg3 by rearranging its catalytic site. Nat Struct Mol Biol 2013; 20:433–439.

Nakatogawa H, Ichimura Y, Ohsumi Y . Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 2007; 130:165–178.

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; 150:1507–1513.

Kabeya Y, Kamada Y, Baba M, Takikawa H, Sasaki M, Ohsumi Y . Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol Biol Cell 2005; 16:2544–2553.

Kawamata T, Kamada Y, Kabeya Y, Sekito T, Ohsumi Y . Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell 2008; 19:2039–2050.

Kabeya Y, Noda NN, Fujioka Y, Suzuki K, Inagaki F, Ohsumi Y . Characterization of the Atg17-Atg29-Atg31 complex specifically required for starvation-induced autophagy in Saccharomyces cerevisiae. Biochem Biophys Res Commun 2009; 389:612–615.

Ragusa MJ, Stanley RE, Hurley JH . Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 2012; 151:1501–1512.

Obara K, Sekito T, Ohsumi Y . Assortment of phosphatidylinositol 3-kinase complexes--Atg14p directs association of complex I to the pre-autophagosomal structure in Saccharomyces cerevisiae. Mol Biol Cell 2006; 17:1527–1539.

Araki K, Ku WC, Akioka M, et al. Atg38 is required for autophagy-specific phosphatidylinositol 3-kinase complex integrity. J Cell Biol 2013; 203:299–313.

Obara K, Noda T, Niimi K, Ohsumi Y . Transport of phosphatidylinositol 3-phosphate into the vacuole via autophagic membranes in Saccharomyces cerevisiae. Genes Cells 2008; 13:537–547.

Stromhaug PE, Reggiori F, Guan J, Wang CW, 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; 15:3553–3566.

Krick R, Henke S, Tolstrup J, Thumm M . Dissecting the localization and function of Atg18, Atg21 and Ygr223c. Autophagy 2008; 4:896–910.

Noda T, Kim J, Huang WP, et al. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 2000; 148:465–480.

Yamamoto H, Kakuta S, Watanabe TM, et al. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 2012; 198:219–233.

Hutchins MU, Klionsky DJ . Vacuolar localization of oligomeric alpha-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J Biol Chem 2001; 276:20491–20498.

Scott SV, Baba M, Ohsumi Y, Klionsky DJ . Aminopeptidase I is targeted to the vacuole by a nonclassical vesicular mechanism. J Cell Biol 1997; 138:37–44.

Suzuki K, Morimoto M, Kondo C, Ohsumi Y . Selective autophagy regulates insertional mutagenesis by the Ty1 retrotransposon in Saccharomyces cerevisiae. Dev Cell 2011; 21:358–365.

Suzuki K, Kondo C, Morimoto M, Ohsumi Y . Selective transport of alpha-mannosidase by autophagic pathways: identification of a novel receptor, Atg34p. J Biol Chem 2010; 285:30019–30025.

Yorimitsu T, Klionsky DJ . Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol Biol Cell 2005; 16:1593–1605.

Shintani T, Klionsky DJ . Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J Biol Chem 2004; 279:29889–29894.

Dunn WAJ, Cregg JM, Kiel JA, et al. Pexophagy: the selective autophagy of peroxisomes. Autophagy 2005; 1:75–83.

Tuttle DL, Dunn WAJ . Divergent modes of autophagy in the methylotrophic yeast Pichia pastoris. J Cell Sci 1995; 108:25–35.

Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ . Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 2009; 17:98–109.

Kanki T, Klionsky DJ . Atg32 is a tag for mitochondria degradation in yeast. Autophagy 2009; 5:1201–1202.

Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, Ohsumi Y . The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J 2001; 20:5971–5981.

Suzuki K, Ohsumi Y . [The pre-autophagosomal structure (PAS), required for the formation of autophagosome membrane]. Seikagaku 2003; 75:492–499.

Suzuki K, Kubota Y, Sekito T, Ohsumi Y . Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 2007; 12:209–218.

Suzuki K, Noda T, Ohsumi Y . Interrelationships among Atg proteins during autophagy in Saccharomyces cerevisiae. Yeast 2004; 21:1057–1065.

Geng J, Baba M, Nair U, Klionsky DJ . Quantitative analysis of autophagy-related protein stoichiometry by fluorescence microscopy. J Cell Biol 2008; 182:129–140.

Mizushima N, Sugita H, Yoshimori T, Ohsumi Y . A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential forautophagy. J Biol Chem 1998; 273:33889–33892.

Mizushima N, Kuma A, Kobayashi Y, et al. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 2003; 116:1679–1688.

Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720–5728.

Mizushima N, Yamamoto A, Hatano M, et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152:657–668.

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; 15:1101–1111.

Jung CH, Jun CB, Ro SH, et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992–2003.

Matsunaga K, Saitoh T, Tabata K, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 2009; 11:385–396.

Itakura E, Kishi C, Inoue K, Mizushima N . Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008; 19:5360–5372.

Zhong Y, Wang QJ, Li X, et al. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol 2009; 11:468–476.

Young AR, Chan EY, Hu XW, et al. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 2006; 119:3888–3900.

Velikkakath AK, Nishimura T, Oita E, Ishihara N, Mizushima N . Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol Biol Cell 2012; 23:896–909.

Koyama-Honda I, Itakura E, Fujiwara TK, Mizushima N . Temporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site. Autophagy 2013; 9:1491–1499.

Kuma A, Mizushima N . Chromosomal mapping of the GFP-LC3 transgene in GFP-LC3 mice. Autophagy 2008; 4:61–62.

Kuma A, Mizushima N . Physiological role of autophagy as an intracellular recycling system: with an emphasis on nutrient metabolism. Semin Cell Dev Biol 2010; 21:683–690.

Levine B, Kroemer G . Autophagy in the pathogenesis of disease. Cell 2008; 132:27–42.

Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD . The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem 2002; 277:33105–33114.

Hanaoka H, Noda T, Shirano Y, et al. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 2002; 129:1181–1193.

Melendez A, Levine B . Autophagy in C. elegans. WormBook 2009; 1–26.

Hara T, Nakamura K, Matsui M, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441:885–889.

Komatsu M, Waguri S, Koike M, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131:1149–1163.

Tsukamoto S, Kuma A, Murakami M, Kishi C, Yamamoto A, Mizushima N . Autophagy is essential for preimplantation development of mouse embryos. Science 2008; 321:117–120.

Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402:672–676.

Okamoto K, Kondo-Okamoto N, Ohsumi Y . Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 2009; 17:87–97.

Youle RJ, Narendra DP . Mechanisms of mitophagy. Nat Rev Mol Cell Biol 2011; 12:9–14.

Nakagawa I, Amano A, Mizushima N, et al. Autophagy defends cells against invading group A Streptococcus. Science 2004; 306:1037–1040.

Randow F, Munz C . Autophagy in the regulation of pathogen replication and adaptive immunity. Trends Immunol 2012; 33:475–487.