Autophagy: from phenomenology to molecular understanding in less than a decade (original) (raw)

• de Duve, C., Pressman, B. C., Gianetto, R., Wattiaux, R. & Appelmans, F. Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem. J. 60, 604–617 (1955).
  CAS PubMed PubMed Central Google Scholar
• Ashford, T. P. & Porter, K. R. Cytoplasmic components in hepatic cell lysosomes. J. Cell Biol. 12, 198–202 (1962).
  CAS PubMed PubMed Central Google Scholar
• Clark, S. L. Jr. Cellular differentiation in the kidneys of newborn mice studied with the electron microscope. J. Biophys. Biochem. Cytol. 3, 349–362 (1957).
  PubMed PubMed Central Google Scholar
• de Duve, C. & Wattiaux, R. Functions of lysosomes. Annu. Rev. Physiol. 28, 435–492 (1966).
  CAS PubMed Google Scholar
• Novikoff, A. B. The proximal tubule cell in experimental hydronephrosis. J. Biophys. Biochem. Cytol. 6, 136–138 (1959).
  CAS PubMed PubMed Central Google Scholar
• Kopitz, J., Kisen, G. O., Gordon, P. B., Bohley, P. & Seglen, P. O. Nonselective autophagy of cytosolic enzymes by isolated rat hepatocytes. J. Cell Biol. 111, 941–953 (1990).
  CAS PubMed Google Scholar
• Fengsrud, M., Lunde Sneve, M., Øverbye, A. & Seglen, P. O. in Autophagy (ed. Klionsky, D. J.) 11–25 (Landes Bioscience, Texas, 2004).
  Google Scholar
• Seglen, P. O. in Lysosomes: Their Role in Protein Breakdown (eds Glaumann, H. & Ballard, F. J.) 371–414 (Academic Press, Florida, 1987).
  Google Scholar
• Gordon, P. B. & Seglen, P. O. Prelysosomal convergence of autophagic and endocytic pathways. Biochem. Biophys. Res. Commun. 151, 40–47 (1988).
  CAS PubMed Google Scholar
• Mizushima, N. et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152, 657–668 (2001).
  CAS PubMed PubMed Central Google Scholar
• 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. 119, 301–311 (1992).
  CAS PubMed Google Scholar
• Kim, J., Huang, W. -P., Stromhaug, P. E. & Klionsky, D. J. Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J. Biol. Chem. 277, 763–773 (2002).
  CAS PubMed Google Scholar
• Suzuki, K. et al. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20, 5971–5981 (2001).
  CAS PubMed PubMed Central Google Scholar
• Deter, R. L., Baudhuin, P. & de Duve, C. Participation of lysosomes in cellular autophagy induced in rat liver by glucagon. J. Cell Biol. 35, C11–C16 (1967).
  CAS PubMed PubMed Central Google Scholar
• Pfeifer, U. Inhibition by insulin of the physiological autophagic breakdown of cell organelles. Acta Biol. Med. Ger. 36, 1691–1694 (1977).
  CAS PubMed Google Scholar
• Mortimore, G. E. & Schworer, C. M. Induction of autophagy by amino-acid deprivation in perfused rat liver. Nature 270, 174–176 (1977).
  CAS PubMed Google Scholar
• Seglen, P. O. & Gordon, P. B. 3-methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl Acad. Sci. USA 79, 1889–1892 (1982).
  CAS PubMed PubMed Central Google Scholar
• Holen, I., Gordon, P. B. & Seglen, P. O. Protein kinase-dependent effects of okadaic acid on hepatocytic autophagy and cytoskeletal integrity. Biochem. J. 284, 633–636 (1992).
  CAS PubMed PubMed Central Google Scholar
• Kunz, J. et al. Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell 73, 585–596 (1993).
  CAS PubMed Google Scholar
• Blommaart, E. F., Luiken, J. J., Blommaart, P. J., van Woerkom, G. M. & Meijer, A. J. Phosphorylation of ribosomal protein S6 is inhibitory for autophagy in isolated rat hepatocytes. J. Biol. Chem. 270, 2320–2326 (1995).
  CAS PubMed Google Scholar
• Blommaart, E. F., Krause, U., Schellens, J. P., Vreeling-Sindelarova, H. & Meijer, A. J. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243, 240–246 (1997).
  CAS PubMed Google Scholar
• Petiot, A., Ogier-Denis, E., Blommaart, E. F., Meijer, A. J. & Codogno, P. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275, 992–998 (2000).
  CAS PubMed Google Scholar
• Arico, S. et al. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 276, 35243–35246 (2001).
  CAS PubMed Google Scholar
• Noda, T. & Ohsumi, Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273, 3963–3966 (1998).
  CAS PubMed Google Scholar
• Bolender, R. P. & Weibel, E. R. A morphometric study of the removal of phenobarbital-induced membranes from hepatocytes after cessation of treatment. J. Cell Biol. 56, 746–761 (1973).
  CAS PubMed PubMed Central Google Scholar
• Beaulaton, J. & Lockshin, R. A. Ultrastructural study of the normal degeneration of the intersegmental muscles of Anthereae polyphemus and Manduca sexta (Insecta, Lepidoptera) with particular reference of cellular autophagy. J. Morphol. 154, 39–57 (1977).
  CAS PubMed Google Scholar
• Veenhuis, M., Douma, A., Harder, W. & Osumi, M. Degradation and turnover of peroxisomes in the yeast Hansenula polymorpha induced by selective inactivation of peroxisomal enzymes. Arch. Microbiol. 134, 193–203 (1983).
  CAS PubMed Google Scholar
• Lemasters, J. J. et al. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta 1366, 177–196 (1998).
  CAS PubMed Google Scholar
• Elmore, S. P., Qian, T., Grissom, S. F. & Lemasters, J. J. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J. 15, 2286–2287 (2001).
  CAS PubMed Google Scholar
• Xue, L., Fletcher, G. C. & Tolkovsky, A. M. Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis. Curr. Biol. 11, 361–365 (2001).
  CAS PubMed Google Scholar
• 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, 591–602 (1995).
  CAS PubMed Google Scholar
• Baba, M., Osumi, M., Scott, S. V., Klionsky, D. J. & Ohsumi, Y. Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J. Cell Biol. 139, 1687–1695 (1997).
  CAS PubMed PubMed Central Google Scholar
• Harding, T. M., Hefner-Gravink, A., Thumm, M. & Klionsky, D. J. Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway. J. Biol. Chem. 271, 17621–17624 (1996).
  CAS PubMed Google Scholar
• Scott, S. V., Baba, M., Ohsumi, Y. & Klionsky, D. J. Aminopeptidase I is targeted to the vacuole by a nonclassical vesicular mechanism. J. Cell Biol. 138, 37–44 (1997).
  CAS PubMed PubMed Central Google Scholar
• Scott, S. V. et al. Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl Acad. Sci. USA 93, 12304–12308 (1996).
  CAS PubMed PubMed Central Google Scholar
• Hutchins, M. U. & Klionsky, D. J. Vacuolar localization of oligomeric α-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J. Biol. Chem. 276, 20491–20498 (2001).
  CAS PubMed Google Scholar
• Klionsky, D. J., Cueva, R. & Yaver, D. S. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J. Cell Biol. 119, 287–299 (1992).
  CAS PubMed Google Scholar
• Tsukada, M. & Ohsumi, Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333, 169–174 (1993).
  CAS PubMed Google Scholar
• Klionsky, D. J. et al. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5, 539–545 (2003).
  CAS PubMed Google Scholar
• Matsuura, A., Tsukada, M., Wada, Y. & Ohsumi, Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192, 245–250 (1997).
  CAS PubMed Google Scholar
• Kabeya, Y., Kawamata, T., Suzuki, K. & Ohsumi, Y. Cis1/Atg31 is required for autophagosome formation in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 356, 405–410 (2007).
  CAS PubMed Google Scholar
• Hutchins, M. U., Veenhuis, M. & Klionsky, D. J. Peroxisome degradation in Saccharomyces cerevisiae is dependent on machinery of macroautophagy and the Cvt pathway. J. Cell Sci. 112, 4079–4087 (1999).
  CAS PubMed Google Scholar
• Zhang, Y. et al. The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 3, 337–346 (2007).
  CAS PubMed Google Scholar
• Klionsky, D. J. The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 118, 7–18 (2005).
  CAS PubMed Google Scholar
• Klionsky, D. J., Cuervo, A. M. & Seglen, P. O. Methods for monitoring autophagy from yeast to human. Autophagy 3, 181–206 (2007).
  CAS PubMed Google Scholar
• Ohsumi, Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nature Rev. Mol. Cell Biol. 2, 211–216 (2001).
  CAS Google Scholar
• 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, 33889–33892 (1998).
  CAS PubMed Google Scholar
• Kabeya, Y. et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720–5728 (2000).
  CAS PubMed PubMed Central Google Scholar
• Liang, X. H. et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672–676 (1999).
  CAS PubMed Google Scholar
• Qu, X. et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809–1820 (2003).
  CAS PubMed PubMed Central Google Scholar
• 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, 15077–15082 (2003).
  CAS PubMed PubMed Central Google Scholar
• Pattingre, S. et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927–939 (2005).
  CAS PubMed Google Scholar
• Mathew, R. et al. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 21, 1367–1381 (2007).
  CAS PubMed PubMed Central Google Scholar
• Rikihisa, Y. Glycogen autophagosomes in polymorphonuclear leukocytes induced by Rickettsiae. Anat. Rec. 208, 319–327 (1984).
  CAS PubMed Google Scholar
• Beron, W., Gutierrez, M. G., Rabinovitch, M. & Colombo, M. I. Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect. Immun. 70, 5816–5821 (2002).
  CAS PubMed PubMed Central Google Scholar
• Swanson, M. S. & Isberg, R. R. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63, 3609–3620 (1995).
  CAS PubMed PubMed Central Google Scholar
• Gutierrez, M. G. et al. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753–766 (2004).
  CAS PubMed Google Scholar
• Nakagawa, I. et al. Autophagy defends cells against invading group A Streptococcus. Science 306, 1037–1040 (2004).
  CAS PubMed Google Scholar
• Ogawa, M. et al. Escape of intracellular Shigella from autophagy. Science 307, 727–731 (2005).
  CAS PubMed Google Scholar
• Liang, X. H. et al. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72, 8586–8596 (1998).
  CAS PubMed PubMed Central Google Scholar
• Orvedahl, A. et al. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1, 23–35 (2007).
  CAS PubMed Google Scholar
• Tallóczy, Z., Virgin, H. W. & Levine, B. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2, 24–29 (2006).
  PubMed Google Scholar
• Dengjel, J. et al. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc. Natl Acad. Sci. USA 102, 7922–7927 (2005).
  CAS PubMed PubMed Central Google Scholar
• Paludan, C. et al. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307, 593–596 (2005).
  CAS PubMed Google Scholar
• Rubinsztein, D. C. et al. Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy 1, 11–22 (2005).
  CAS PubMed Google Scholar
• Ravikumar, B., Duden, R. & Rubinsztein, D. C. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 11, 1107–1117 (2002).
  CAS PubMed Google Scholar
• Hara, T. et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885–889 (2006).
  CAS PubMed Google Scholar
• Komatsu, M. et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880–884 (2006).
  CAS PubMed Google Scholar
• Boya, P. et al. Inhibition of macroautophagy triggers apoptosis. Mol. Cell Biol. 25, 1025–1040 (2005).
  CAS PubMed PubMed Central Google Scholar
• Yu, L. et al. Regulation of an ATG7–beclin 1 program of autophagic cell death by caspase-8. Science 304, 1500–1502 (2004).
  CAS PubMed Google Scholar
• Sugawara, K. et al. The crystal structure of microtubule-associated protein light chain 3, a mammalian homologue of Saccharomyces cerevisiae Atg8. Genes Cells 9, 611–618 (2004).
  CAS PubMed Google Scholar
• Rubinsztein, D. C., Gestwicki, J. E., Murphy, L. O. & Klionsky, D. J. Potential therapeutic applications of autophagy. Nature Rev. Drug Discov. 6, 304–312 (2007).
  CAS Google Scholar
• Gozuacik, D. & Kimchi, A. Autophagy and cell death. Curr. Top. Dev. Biol. 78, 217–245 (2007).
  CAS PubMed Google Scholar
• Meijer, A. J. & Codogno, P. Signalling and autophagy regulation in health, aging and disease. Mol. Aspects Med. 27, 411–425 (2006).
  CAS PubMed Google Scholar
• Nobukuni, T., Kozma, S. C. & Thomas, G. hvps34, an ancient player, enters a growing game: mTOR Complex1/S6K1 signaling. Curr. Opin. Cell Biol. 19, 135–141 (2007).
  CAS PubMed Google Scholar
• Gordon, P. B. & Seglen, P. O. Autophagic sequestration of [14C]sucrose, introduced into rat hepatocytes by reversible electro-permeabilization. Exp. Cell Res. 142, 1–14 (1982).
  CAS PubMed Google Scholar
• Kawamata, T. et al. Characterization of a novel autophagy-specific gene, ATG29. Biochem. Biophys. Res. Commun. 338, 1884–1889 (2005).
  CAS PubMed Google Scholar
• Stasyk, O. V. et al. Atg28, a novel coiled-coil protein involved in autophagic degradation of peroxisomes in the methylotrophic yeast Pichia pastoris. Autophagy 2, 30–38 (2006).
  CAS PubMed Google Scholar
• Bergamini, E. Autophagy: a cell repair mechanism that retards ageing and age-associated diseases and can be intensified pharmacologically. Mol. Aspects Med. 27, 403–410 (2006).
  CAS PubMed Google Scholar
• Melendez, A. et al. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301, 1387–1391 (2003).
  CAS PubMed Google Scholar
• Shimizu, S. et al. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nature Cell Biol. 6, 1221–1228 (2004).
  CAS PubMed Google Scholar
• Liu, Y. et al. Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567–577 (2005).
  CAS PubMed Google Scholar
• Schmid, D. & Münz, C. Immune surveillance of intracellular pathogens via autophagy. Cell Death Differ. 12, 1519–1527 (2005).
  CAS PubMed Google Scholar
• Singh, S. B., Davis, A. S., Taylor, G. A. & Deretic, V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313, 1438–1441 (2006).
  CAS PubMed Google Scholar
• Kuma, A. et al. The role of autophagy during the early neonatal starvation period. Nature 432, 1032–1036 (2004).
  CAS PubMed Google Scholar