Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Autophagosome formation: core machinery and adaptations

Abstract

Eukaryotic cells employ autophagy to degrade damaged or obsolete organelles and proteins. Central to this process is the formation of autophagosomes, double-membrane vesicles responsible for delivering cytoplasmic material to lysosomes. In the past decade many autophagy-related genes, ATG, have been identified that are required for selective and/or nonselective autophagic functions. In all types of autophagy, a core molecular machinery has a critical role in forming sequestering vesicles, the autophagosome, which is the hallmark morphological feature of this dynamic process. Additional components allow autophagy to adapt to the changing needs of the cell.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Schematic depiction of autophagy.
Figure 2: The phagophore assembly site.
Figure 3: Adaptations of the core machinery.

Similar content being viewed by others

References

  1. Klionsky, D. J. The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 118, 7–18 (2005).

    Article  CAS  PubMed  Google Scholar 

  2. Yorimitsu, T. & Klionsky, D. J. Autophagy: molecular machinery for self-eating. Cell Death Differ. 12, 1542–1552 (2005).

    CAS  PubMed  Google Scholar 

  3. Kunz, J. B., Schwarz, H. & Mayer, A. Determination of four sequential stages during microautophagy in vitro. J. Biol. Chem. 279, 9987–9996 (2004).

    CAS  PubMed  Google Scholar 

  4. Majeski, A. E. & Dice, J. F. Mechanisms of chaperone-mediated autophagy. Int. J. Biochem. Cell Biol. 36, 2435–2444 (2004).

    CAS  PubMed  Google Scholar 

  5. Kvam, E. & Goldfarb, D. S. Nucleus-vacuole junctions and piecemeal microautophagy of the nucleus in S. cerevisiae. Autophagy 3, 85–92 (2007).

    CAS  PubMed  Google Scholar 

  6. Levine, B. & Klionsky, D. J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6, 463–477 (2004).

    CAS  PubMed  Google Scholar 

  7. Münz, C. Autophagy and antigen presentation. Cell. Micro. 8, 891–898 (2006).

    Google Scholar 

  8. Shintani, T. & Klionsky, D. J. Autophagy in health and disease: a double-edged sword. Science 306, 990–995 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Klionsky, D. J. et al. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5, 539–545 (2003).

    CAS  PubMed  Google Scholar 

  10. 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 

  11. 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 

  12. Mizushima, N. et al. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J. Cell Sci. 116, 1679–1688 (2003).

    CAS  PubMed  Google Scholar 

  13. 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 

  14. Yamada, T. et al. Endothelial nitric-oxide synthase antisense (NOS3AS) gene encodes an autophagy-related protein (APG9-like2) highly expressed in trophoblast. J. Biol. Chem. 280, 18283–18290 (2005).

    CAS  PubMed  Google Scholar 

  15. Young, A. R. J. et al. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell. Sci. 119, 3888–3900 (2006).

    CAS  PubMed  Google Scholar 

  16. Kirisako, T. et al. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147, 435–446 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  18. He, C. et al. Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J. Cell Biol. 175, 925–935 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Reggiori, F., Shintani, T., Nair, U. & Klionsky, D. J. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 1, 101–109 (2005).

    Article  CAS  PubMed  Google Scholar 

  20. Reggiori, F., Tucker, K. A., Stromhaug, P. E. & Klionsky, D. J. The Atg1–Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev. Cell 6, 79–90 (2004).

    CAS  PubMed  Google Scholar 

  21. Reggiori, F. & Klionsky, D. J. Atg9 sorting from mitochondria is impaired in early secretion and VFT-complex mutants in Saccharomyces cerevisiae. J. Cell Sci. 119, 2903–2911 (2006).

    CAS  PubMed  Google Scholar 

  22. Yen, W.-L., Legakis, J. E., Nair, U. & Klionsky, D. J. Atg27 is required for autophagy-dependent cycling of Atg9. Mol. Biol. Cell 18, 581–593 (2006).

    PubMed  Google Scholar 

  23. Legakis, J. E., Yen, W.-L. & Klionsky, D. J. A cycling protein complex required for selective autophagy. Autophagy 3, 422–432 (2007).

    CAS  PubMed  Google Scholar 

  24. Tucker, K. A., Reggiori, F., Dunn, W. A., Jr & Klionsky, D. J. Atg23 is essential for the cytoplasm to vacuole targeting pathway and efficient autophagy but not pexophagy. J. Biol. Chem. 278, 48445–48452 (2003).

    CAS  PubMed  Google Scholar 

  25. Kamada, Y. et al. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 150, 1507–1513 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 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 

  27. Kabeya, Y. et al. Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol. Biol. Cell 16, 2544–2553 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Nair, U. & Klionsky, D. J. Molecular mechanisms and regulation of specific and nonspecific autophagy pathways in yeast. J. Biol. Chem. 280, 41785–41788 (2005).

    CAS  PubMed  Google Scholar 

  29. Cheong, H. et al. Atg17 regulates the magnitude of the autophagic response. Mol. Biol. Cell 16, 3438–3453 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Kim, J. et al. Cvt9/Gsa9 functions in sequestering selective cytosolic cargo destined for the vacuole. J. Cell Biol. 153, 381–396 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Meijer, W. H., van der Klei, I. J., Veenhuis, M. & Kiel, J. A. K. W. ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective Cvt and pexophagy pathways also require organism-specific genes. Autophagy 3, 106–116 (2007).

    CAS  PubMed  Google Scholar 

  32. Guan, J. et al. Cvt18/Gsa12 is required for cytoplasm-to-vacuole transport, pexophagy, and autophagy in Saccharomyces cerevisiae and Pichia pastoris. Mol. Biol. Cell 12, 3821–3838 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Shintani, T., Suzuki, K., Kamada, Y., Noda, T. & Ohsumi, Y. Apg2p functions in autophagosome formation on the perivacuolar structure. J. Biol. Chem. 276, 30452–30460 (2001).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  35. Wang, C.-W. et al. Apg2 is a novel protein required for the cytoplasm to vacuole targeting, autophagy, and pexophagy pathways. J. Biol. Chem. 276, 30442–30451 (2001).

    CAS  PubMed  Google Scholar 

  36. Stromhaug, P. E., Reggiori, F., Guan, J., Wang, C.-W. & Klionsky, D. J. 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 15, 3553–3566 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Dove, S. K. et al. Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. EMBO J. 23, 1922–1933 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Proikas-Cezanne, T. et al. WIPI-1a (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene 23, 9314–9325 (2004).

    CAS  PubMed  Google Scholar 

  39. Lindmo, K. & Stenmark, H. Regulation of membrane traffic by phosphoinositide 3-kinases. J. Cell Sci. 119, 605–614 (2006).

    CAS  PubMed  Google Scholar 

  40. Panaretou, C., Domin, J., Cockcroft, S. & Waterfield, M. D. Characterization of p150, an adaptor protein for the human phosphatidylinositol (PtdIns) 3-kinase. Substrate presentation by phosphatidylinositol transfer protein to the p150·Ptdins 3-kinase complex. J. Biol. Chem. 272, 2477–2485 (1997).

    CAS  PubMed  Google Scholar 

  41. Stack, J. H., Herman, P. K., Schu, P. V. & Emr, S. D. A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J. 12, 2195–2204 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 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, 519–530 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 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 17, 1527–1539 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Liang, X. H. et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672–676 (1999).

    CAS  PubMed  Google Scholar 

  45. Furuya, N., Yu, J., Byfield, M., Pattingre, S. & Levine, B. The evolutionarily conserved domain of Beclin 1 is required for Vps34 binding, autophagy and tumor suppressor function. Autophagy 1, 46–52 (2005).

    CAS  PubMed  Google Scholar 

  46. Zeng, X., Overmeyer, J. H. & Maltese, W. A. Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J. Cell Sci. 119, 259–270 (2006).

    CAS  PubMed  Google Scholar 

  47. Ichimura, Y. et al. A ubiquitin-like system mediates protein lipidation. Nature 408, 488–492 (2000).

    CAS  PubMed  Google Scholar 

  48. Mizushima, N. et al. A protein conjugation system essential for autophagy. Nature 395, 395–398 (1998).

    CAS  PubMed  Google Scholar 

  49. Paz, Y., Elazar, Z. & Fass, D. Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p. J. Biol. Chem. 275, 25445–25450 (2000).

    CAS  PubMed  Google Scholar 

  50. Suzuki, N. N., Yoshimoto, K., Fujioka, Y., Ohsumi, Y. & Inagaki, F. The crystal structure of plant ATG12 and its biological implication in autophagy. Autophagy 1, 119–126 (2005).

    CAS  PubMed  Google Scholar 

  51. George, M. D. et al. Apg5p functions in the sequestration step in the cytoplasm-to-vacuole targeting and macroautophagy pathways. Mol. Biol. Cell 11, 969–982 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 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 

  53. Sou, Y-s., Tanida, I., Komatsu, M., Ueno, T. & Kominami, E. Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP, and GATE-16. J. Biol. Chem. 281, 3017–3024 (2006).

    CAS  PubMed  Google Scholar 

  54. 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, 51841–51850 (2003).

    CAS  PubMed  Google Scholar 

  55. Kim, J., Huang, W.-P. & Klionsky, D. J. Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut1p, Aut2p, and the autophagy conjugation complex. J. Cell Biol. 152, 51–64 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Kirisako, 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, 263–276 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 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, 1337–1351 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Tanida, I. et al. Apg7p/Cvt2p: A novel protein-activating enzyme essential for autophagy. Mol. Biol. Cell 10, 1367–1379 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Tanida, I., Tanida-Miyake, E., Ueno, T. & Kominami, E. The human homolog of Saccharomyces cerevisiae Apg7p is a protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J. Biol. Chem. 276, 1701–1706 (2001).

    CAS  PubMed  Google Scholar 

  60. 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, 13739–13744 (2002).

    CAS  PubMed  Google Scholar 

  61. Nemoto, T. et al. The mouse APG10 homologue, an E2-like enzyme for Apg12p conjugation, facilitates MAP-LC3 modification. J. Biol. Chem. 278, 39517–39526 (2003).

    CAS  PubMed  Google Scholar 

  62. Shintani, T. et al. Apg10p, a novel protein-conjugating enzyme essential for autophagy in yeast. EMBO J. 18, 5234–5241 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Ichimura, Y. et al. In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. J. Biol. Chem. 279, 40584–40592 (2004).

    CAS  PubMed  Google Scholar 

  64. Shao, Y., Gao, Z., Feldman, T. & Jiang, X. Stimulation of ATG12-ATG5 conjugation by ribonucleic acid. Autophagy 3, 10–16 (2007).

    CAS  PubMed  Google Scholar 

  65. 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. 277, 18619–18625 (2002).

    CAS  PubMed  Google Scholar 

  66. 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, 3888–3896 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Matsushita, M. et al. Structure of ATG5·ATG16, a complex essential for autophagy. J. Biol. Chem. 282, 6763–6772 (2007).

    CAS  PubMed  Google Scholar 

  68. 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 

  69. Huang, W.-P., Scott, S. V., Kim, J. & Klionsky, D. J. The itinerary of a vesicle component, Aut7p/Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways. J. Biol. Chem. 275, 5845–5851 (2000).

    CAS  PubMed  Google Scholar 

  70. Monastyrska, I. et al. Atg8 is essential for macropexophagy in Hansenula polymorpha. Traffic 6, 66–74 (2005).

    CAS  PubMed  Google Scholar 

  71. 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 

  72. Ogawa, M. et al. Escape of intracellular Shigella from autophagy. Science 307, 727–731 (2005).

    CAS  PubMed  Google Scholar 

  73. Sakai, Y., Koller, A., Rangell, L. K., Keller, G. A. & Subramani, S. Peroxisome degradation by microautophagy in Pichia pastoris: identification of specific steps and morphological intermediates. J. Cell Biol. 141, 625–636 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 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 

  75. 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 

  76. Oda, M. N., Scott, S. V., Hefner-Gravink, A., Caffarelli, A. D. & Klionsky, D. J. Identification of a cytoplasm to vacuole targeting determinant in aminopeptidase I. J. Cell Biol. 132, 999–1010 (1996).

    CAS  PubMed  Google Scholar 

  77. 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 

  78. Shintani, T. & Klionsky, D. J. Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J. Biol. Chem. 279, 29889–29894 (2004).

    CAS  PubMed  Google Scholar 

  79. Kim, J., Scott, S. V., Oda, M. N. & Klionsky, D. J. Transport of a large oligomeric protein by the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 137, 609–618 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Scott, S. V., Guan, J., Hutchins, M. U., Kim, J. & Klionsky, D. J. Cvt19 is a receptor for the cytoplasm-to-vacuole targeting pathway. Mol. Cell 7, 1131–1141 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Shintani, T., Huang, W.-P., Stromhaug, P. E. & Klionsky, D. J. Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway. Dev. Cell 3, 825–837 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Dunn, W. A., Jr et al. Pexophagy: the selective autophagy of peroxisomes. Autophagy 1, 75–83 (2005).

    CAS  PubMed  Google Scholar 

  83. Nakagawa, I. et al. Autophagy defends cells against invading group A Streptococcus. Science 306, 1037–1040 (2004).

    CAS  PubMed  Google Scholar 

  84. 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 

  85. Bjorkoy, G. et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171, 603–614 (2005).

    PubMed  PubMed Central  Google Scholar 

  86. 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 

  87. Tanida, I., Minematsu-Ikeguchi, N., Ueno, T. & Kominami, E. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1, 84–91 (2005).

    CAS  PubMed  Google Scholar 

  88. Bampton, E. T., Goemans, C. G., Niranjan, D., Mizushima, N. & Tolkovsky, A. M. The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. Autophagy 1, 23–36 (2005).

    CAS  PubMed  Google Scholar 

  89. Hamasaki, M., Noda, T. & Ohsumi, Y. The early secretory pathway contributes to autophagy in yeast. Cell Struct. Funct. 28, 49–54 (2003).

    CAS  PubMed  Google Scholar 

  90. Mukaiyama, H. et al. Modification of a ubiquitin-like protein Paz2 conducted micropexophagy through formation of a novel membrane structure. Mol. Biol. Cell 15, 58–70 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Chang, T. et al. PpATG9 encodes a novel membrane protein that traffics to vacuolar membranes, which sequester peroxisomes during pexophagy in Pichia pastoris. Mol. Biol. Cell 16, 4941–4953 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Nice, D. C., Sato, T. K., Stromhaug, P. E., Emr, S. D. & Klionsky, D. J. Cooperative binding of the cytoplasm to vacuole targeting pathway proteins, Cvt13 and Cvt20, to phosphatidylinositol 3-phosphate at the pre-autophagosomal structure is required for selective autophagy. J. Biol. Chem. 277, 30198–30207 (2002).

    CAS  PubMed  Google Scholar 

  93. Leao-Helder, A. N. et al. Atg21p is essential for macropexophagy and microautophagy in the yeast Hansenula polymorpha. FEBS Lett. 577, 491–495 (2004).

    CAS  PubMed  Google Scholar 

  94. Ano, Y. et al. A sorting nexin PpAtg24 regulates vacuolar membrane dynamics during pexophagy via binding to phosphatidylinositol-3-phosphate. Mol. Biol. Cell 16, 446–457 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Monastyrska, I. et al. The Hansenula polymorpha ATG25 gene encodes a novel coiled-coil protein that is required for macropexophagy. Autophagy 1, 92–100 (2005).

    CAS  PubMed  Google Scholar 

  96. Cao, Y. & Klionsky, D. J. Atg26 is not involved in autophagy-related pathways in Saccharomyces cerevisiae. Autophagy 3, 17–20 (2007).

    CAS  PubMed  Google Scholar 

  97. Nazarko, T. Y., Polupanov, A. S., Manjithaya, R. R., Subramani, S. & Sibirny, A. A. The requirement of sterol glucoside for pexophagy in yeast is dependent on the species and nature of peroxisome inducers. Mol. Biol. Cell 18, 106–118 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Oku, M. et al. Peroxisome degradation requires catalytically active sterol glucosyltransferase with a GRAM domain. EMBO J. 22, 3231–3241 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. 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 

  100. Kawamata, T. et al. Characterization of a novel autophagy-specific gene, ATG29. Biochem. Biophys. Res. Commun. 338, 1884–1889 (2005).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Institutes of Health Public Health Service grant GM53396 (to D.J.K.).

Author information

Authors and Affiliations

Authors

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xie, Z., Klionsky, D. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9, 1102–1109 (2007). https://doi.org/10.1038/ncb1007-1102

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/ncb1007-1102

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing