Mechanistic insights into selective autophagy pathways: Lessons from yeast

Nature Reviews Molecular Cell Biology

Volumn 17, Issue 9, 2016, Pages 537-552

  Farré, Jean Claude ^a   Subramani, Suresh ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATG8 PROTEIN; PHOSPHOTRANSFERASE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; AUTOPHAGY RELATED PROTEIN;

CELL ORGANELLE; GENE ACTIVATION; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SELECTIVE AUTOPHAGY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; YEAST; ANIMAL; AUTOPHAGY; CLASSIFICATION; CYTOLOGY; EUKARYOTIC CELL; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; PATHOLOGY; PHOSPHORYLATION;

ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEINS; EUKARYOTIC CELLS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; MITOCHONDRIA; PHOSPHORYLATION;

EID: 84977137836     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm.2016.74     Document Type: Review

References (170)

1. Ryter, S. W., Cloonan, S. M. & Choi, A. M. Autophagy: a critical regulator of cellular metabolism and homeostasis. Mol. Cells 36, 7-16 (2013).
2. Choi, A. M., Ryter, S. W. & Levine, B. Autophagy in human health and disease. N. Engl. J. Med. 368, 651-662 (2013).
3. Gozuacik, D. & Kimchi, A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23, 2891-2906 (2004).
4. Frake, R. A., Ricketts, T., Menzies, F. M. & Rubinsztein, D. C. Autophagy and neurodegeneration. J. Clin. Invest. 125, 65-74 (2015).
5. Rubinsztein, D. C., Marino, G. & Kroemer, G. Autophagy and aging. Cell 146, 682-695 (2011).
6. Netea-Maier, R. T., Plantinga, T. S., Van De Veerdonk, F. L., Smit, J. W. & Netea, M. G. Modulation of inflammation by autophagy: consequences for human disease. Autophagy 12, 1-16 (2015).
7. Gomes, L. C. & Dikic, I. Autophagy in antimicrobial immunity. Mol. Cell 54, 224-233 (2014).
8. Nowikovsky, K., Devenish, R. J., Froschauer, E. & Schweyen, R. J. Determination of yeast mitochondrial KHE activity, osmotic swelling and mitophagy. Methods Enzymol. 457, 305-317 (2009).
9. Walter, K. M. et al. Hif-2α promotes degradation of mammalian peroxisomes by selective autophagy. Cell. Metab. 20, 882-897 (2014).
10. Wang, X., Li, S., Liu, Y. & Ma, C. Redox regulated peroxisome homeostasis. Redox Biol. 4, 104-108 (2015).
11. Ohsumi, Y. Historical landmarks of autophagy research. Cell Res. 24, 9-23 (2014).
12. Suzuki, S. W. et al. Atg13 HORMA domain recruits Atg9 vesicles during autophagosome formation. Proc. Natl Acad. Sci. USA 112, 3350-3355 (2015).
13. Shemi, A., Ben-Dor, S. & Vardi, A. Elucidating the composition and conservation of the autophagy pathway in photosynthetic eukaryotes. Autophagy 11, 701-715 (2015).
14. Kubo, Y. Function of peroxisomes in plant-pathogen interactions. Subcell. Biochem. 69, 329-345 (2013).
15. Mizumura, K., Choi, A. M. & Ryter, S. W. Emerging role of selective autophagy in human diseases. Front. Pharmacol. 5, 244 (2014).
16. van der Vaart, A., Mari, M. & Reggiori, F. A picky eater: exploring the mechanisms of selective autophagy in human pathologies. Traffic 9, 281-289 (2008).
17. Zhang, J. et al. ATM functions at the peroxisome to induce pexophagy in response to ROS. Nat. Cell Biol. 17, 1259-1269 (2015).
18. Lynch-Day, M. A. & Klionsky, D. J. The Cvt pathway as a model for selective autophagy. FEBS Lett. 584, 1359-1366 (2010).
19. Tuttle, D. L., Lewin, A. S. & Dunn, W. A. Jr. Selective autophagy of peroxisomes in methylotrophic yeasts. Eur. J. Cell Biol. 60, 283-290 (1993).
20. Lu, K., Psakhye, I. & Jentsch, S. A new class of ubiquitin-Atg8 receptors involved in selective autophagy and polyQ protein clearance. Autophagy 10, 2381-2382 (2014).
21. Steele, S., Brunton, J. & Kawula, T. The role of autophagy in intracellular pathogen nutrient acquisition. Front. Cell. Infect. Microbiol. 5, 51 (2015).
22. Khaminets, A., Behl, C. & Dikic, I. Ubiquitin-dependent and independent signals in selective autophagy. Trends Cell Biol. 26, 6-16 (2016).
23. 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).
24. 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. 285, 30019-30025 (2010).
25. Lu, K., Psakhye, I. & Jentsch, S. Autophagic clearance of polyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family. Cell 158, 549-563 (2014).
26. Farre, J. C., Manjithaya, R., Mathewson, R. D. & Subramani, S. PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev. Cell 14, 365-376 (2008).
27. Motley, A. M., Nuttall, J. M. & Hettema, E. H. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 31, 2852-2868 (2012).
28. Burnett, S. F., Farre, J. C., Nazarko, T. Y. & Subramani, S. Peroxisomal Pex3 activates selective autophagy of peroxisomes via interaction with the pexophagy receptor Atg30. J. Biol. Chem. 290, 8623-8631 (2015).
29. Nazarko, T. Y. et al. Peroxisomal Atg37 binds Atg30 or palmitoyl-CoA to regulate phagophore formation during pexophagy. J. Cell Biol. 204, 541-557 (2014).
30. Kanki, T., Wang, K., Cao, Y., Baba, M. & Klionsky, D. J. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17, 98-109 (2009).
31. Okamoto, K., Kondo-Okamoto, N. & Ohsumi, Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17, 87-97 (2009).
32. Kondo-Okamoto, N. et al. Autophagy-related protein 32 acts as autophagic degron and directly initiates mitophagy. J. Biol. Chem. 287, 10631-10638 (2012).
33. Mochida, K. et al. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 522, 359-362 (2015).
34. Jin, M. & Klionsky, D. J. in Autophagy and Cancer (ed. Wang, H.-G.) 25-45 (Springer New York, 2013).
35. Cheong, H. et al. Atg17 regulates the magnitude of the autophagic response. Mol. Biol. Cell 16, 3438-3453 (2005).
36. Nazarko, T. Y., Farre, J. C. & Subramani, S. Peroxisome size provides insights into the function of autophagy-related proteins. Mol. Biol. Cell 20, 3828-3839 (2009).
37. Kanki, T. et al. A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol. Biol. Cell 20, 4730-4738 (2009).
38. Kabeya, Y. et al. Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol. Biol. Cell 16, 2544-2553 (2005).
39. Kamada, Y. et al. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 150, 1507-1513 (2000).
40. Kabeya, Y. et al. Characterization of the Atg17-Atg29-Atg31 complex specifically required for starvation-induced autophagy in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 389, 612-615 (2009).
41. Fujioka, Y. et al. Structural basis of starvation-induced assembly of the autophagy initiation complex. Nat. Struct. Mol. Biol. 21, 513-521 (2014).
42. Mao, K. et al. Atg29 phosphorylation regulates coordination of the Atg17-Atg31-Atg29 complex with the Atg11 scaffold during autophagy initiation. Proc. Natl Acad. Sci. USA 110, E2875-E2884 (2013).
43. Kamber, R. A., Shoemaker, C. J. & Denic, V. Receptor-bound targets of selective autophagy use a scaffold protein to activate the Atg1 kinase. Mol. Cell 59, 372-381 (2015).
44. Cheong, H., Nair, U., Geng, J. & Klionsky, D. J. The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol. Biol. Cell 19, 668-681 (2008).
45. Papinski, D. et al. Early steps in autophagy depend on direct phosphorylation of Atg9 by the Atg1 kinase. Mol. Cell 53, 471-483 (2014).
46. Lipatova, Z. et al. Regulation of selective autophagy onset by a Ypt/Rab GTPase module. Proc. Natl Acad. Sci. USA 109, 6981-6986 (2012).
47. Kakuta, S. et al. Atg9 vesicles recruit vesicle-tethering proteins Trs85 and Ypt1 to the autophagosome formation site. J. Biol. Chem. 287, 44261-44269 (2012).
48. Wang, J. et al. Ypt1 recruits the Atg1 kinase to the preautophagosomal structure. Proc. Natl Acad. Sci. USA 110, 9800-9805 (2013).
49. Wang, J. et al. Ypt1/Rab1 regulates Hrr25/CK1delta kinase activity in ER-Golgi traffic and macroautophagy. J. Cell Biol. 210, 273-285 (2015).
50. Tan, D. et al. The EM structure of the TRAPPIII complex leads to the identification of a requirement for COPII vesicles on the macroautophagy pathway. Proc. Natl Acad. Sci. USA 110, 19432-19437 (2013).
51. Ishihara, N. et al. Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol. Biol. Cell 12, 3690-3702 (2001).
52. Backues, S. K. et al. Atg23 and Atg27 act at the early stages of Atg9 trafficking in S. cerevisiae. Traffic 16, 172-190 (2015).
53. Suzuki, K., Kubota, Y., Sekito, T. & Ohsumi, Y. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12, 209-218 (2007).
54. Xie, Z., Nair, U. & Klionsky, D. J. Atg8 controls phagophore expansion during autophagosome formation. Mol. Biol. Cell 19, 3290-3298 (2008).
55. Noda, N. N. et al. Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells 13, 1211-1218 (2008).
56. Ho, K. H., Chang, H. E. & Huang, W. P. Mutation at the cargo-receptor binding site of Atg8 also affects its general autophagy regulation function. Autophagy 5, 461-471 (2009).
57. Kaufmann, A., Beier, V., Franquelim, H. G. & Wollert, T. Molecular mechanism of autophagic membrane-scaffold assembly and disassembly. Cell 156, 469-481 (2014).
58. 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).
59. Farre, J. C., Burkenroad, A., Burnett, S. F. & Subramani, S. Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11. EMBO Rep. 14, 441-449 (2013).
60. Yorimitsu, T. & Klionsky, D. J. Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol. Biol. Cell 16, 1593-1605 (2005).
61. Aoki, Y. et al. Phosphorylation of Serine 114 on Atg32 mediates mitophagy. Mol. Biol. Cell 22, 3206-3217 (2011).
62. Stephan, J. S., Yeh, Y. Y., Ramachandran, V., Deminoff, S. J. & Herman, P. K. The Tor and PKA signaling pathways independently target the Atg1/Atg13 protein kinase complex to control autophagy. Proc. Natl Acad. Sci. USA 106, 17049-17054 (2009).
63. Noda, N. N., Ohsumi, Y. & Inagaki, F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett. 584, 1379-1385 (2010).
64. Sawa-Makarska, J. et al. Cargo binding to Atg19 unmasks additional Atg8 binding sites to mediate membrane-cargo apposition during selective autophagy. Nat. Cell Biol. 16, 425-433 (2014).
65. Sawa-Makarska, J. & Martens, S. Excluding the unwanted during autophagy. Cell Cycle 13, 2313-2314 (2014).
66. Kim, J. et al. Cvt9/Gsa9 functions in sequestering selective cytosolic cargo destined for the vacuole. J. Cell Biol. 153, 381-396 (2001).
67. Pfaffenwimmer, T. et al. Hrr25 kinase promotes selective autophagy by phosphorylating the cargo receptor Atg19. EMBO Rep. 15, 862-870 (2014).
68. Tuttle, D. L. & Dunn, W. A. Jr. Divergent modes of autophagy in the methylotrophic yeast Pichia pastoris. J. Cell Sci. 108, 25-35 (1995).
69. Eiyama, A., Kondo-Okamoto, N. & Okamoto, K. Mitochondrial degradation during starvation is selective and temporally distinct from bulk autophagy in yeast. FEBS Lett. 587, 1787-1792 (2013).
70. Kanki, T. & Klionsky, D. J. Mitophagy in yeast occurs through a selective mechanism. J. Biol. Chem. 283, 32386-32393 (2008).
71. Aihara, M. et al. Tor and the Sin3-Rpd3 complex regulate expression of the mitophagy receptor protein Atg32 in yeast. J. Cell Sci. 127, 3184-3196 (2014).
72. Kanki, T. et al. Casein kinase 2 is essential for mitophagy. EMBO Rep. 14, 788-794 (2013).
73. Canton, D. A. & Litchfield, D. W. The shape of things to come: an emerging role for protein kinase CK2 in the regulation of cell morphology and the cytoskeleton. Cell Signal. 18, 267-275 (2006).
74. Mochida, K., Ohsumi, Y. & Nakatogawa, H. Hrr25 phosphorylates the autophagic receptor Atg34 to promote vacuolar transport of alpha-mannosidase under nitrogen starvation conditions. FEBS Lett. 588, 3862-3869 (2014).
75. Tanaka, C. et al. Hrr25 triggers selective autophagy-related pathways by phosphorylating receptor proteins. J. Cell Biol. 207, 91-105 (2014).
76. Lord, C. et al. Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 473, 181-186 (2011).
77. Nakatogawa, H. Hrr25: an emerging major player in selective autophagy regulation in Saccharomyces cerevisiae. Autophagy 11, 432-433 (2015).
78. Li, F. & Vierstra, R. D. Arabidopsis ATG11, a scaffold that links the ATG1-ATG13 kinase complex to general autophagy and selective mitophagy. Autophagy 10, 1466-1467 (2014).
79. Manjithaya, R., Jain, S., Farre, J. C. & Subramani, S. A yeast MAPK cascade regulates pexophagy but not other autophagy pathways. J. Cell Biol. 189, 303-310 (2010).
80. Mao, K. & Klionsky, D. J. MAPKs regulate mitophagy in Saccharomyces cerevisiae. Autophagy 7, 1564-1565 (2011).
81. Chen, R. E. & Thorner, J. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1773, 1311-1340 (2007).
82. Torres, J., Di Como, C. J., Herrero, E. & De La Torre-Ruiz, M. A. Regulation of the cell integrity pathway by rapamycin-sensitive TOR function in budding yeast. J. Biol. Chem. 277, 43495-43504 (2002).
83. Nazarko, T. Y. Atg37 regulates the assembly of the pexophagic receptor protein complex. Autophagy 10, 1348-1349 (2014).
84. Li, X. & Gould, S. J. The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J. Biol. Chem. 278, 17012-17020 (2003).
85. Kuravi, K. et al. Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J. Cell Sci. 119, 3994-4001 (2006).
86. Motley, A. M., Ward, G. P. & Hettema, E. H. Dnm1p-dependent peroxisome fission requires Caf4p, Mdv1p and Fis1p. J. Cell Sci. 121, 1633-1640 (2008).
87. Schrader, M. Shared components of mitochondrial and peroxisomal division. Biochim. Biophys. Acta 1763, 531-541 (2006).
88. Manivannan, S., de Boer, R., Veenhuis, M. & van der Klei, I. J. Lumenal peroxisomal protein aggregates are removed by concerted fission and autophagy events. Autophagy 9, 1044-1056 (2013).
89. Mao, K. & Klionsky, D. J. Participation of mitochondrial fission during mitophagy. Cell Cycle 12, 3131-3132 (2013).
90. Mao, K., Liu, X., Feng, Y. & Klionsky, D. J. The progression of peroxisomal degradation through autophagy requires peroxisomal division. Autophagy 10, 652-661 (2014).
91. Mao, K., Wang, K., Liu, X. & Klionsky, D. J. The scaffold protein Atg11 recruits fission machinery to drive selective mitochondria degradation by autophagy. Dev. Cell 26, 9-18 (2013).
92. Suzuki, K., Akioka, M., Kondo-Kakuta, C., Yamamoto, H. & Ohsumi, Y. Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae. J. Cell Sci. 126, 2534-2544 (2013).
93. Wullschleger, S., Loewith, R. & Hall, M. N. TOR signaling in growth and metabolism. Cell 124, 471-484 (2006).
94. Backues, S. K., Lynch-Day, M. A. & Klionsky, D. J. The Ume6-Sin3-Rpd3 complex regulates ATG8 transcription to control autophagosome size. Autophagy 8, 1835-1836 (2012).
95. Till, A. et al. Evolutionary trends and functional anatomy of the human expanded autophagy network. Autophagy 11, 1652-1667 (2015).
96. Kraft, C., Peter, M. & Hofmann, K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 12, 836-841 (2010).
97. Murakawa, T. et al. Bcl-2-like protein 13 is a mammalian Atg32 homologue that mediates mitophagy and mitochondrial fragmentation. Nat. Commun. 6, 7527 (2015).
98. Nordgren, M., Wang, B., Apanasets, O. & Fransen, M. Peroxisome degradation in mammals: mechanisms of action, recent advances, and perspectives. Front. Physiol. 4, 145 (2013).
99. Subramani, S. A mammalian pexophagy target. Nat. Cell Biol. 17, 1371-1373 (2015).
100. Katsuragi, Y., Ichimura, Y. & Komatsu, M. p62/SQSTM1 functions as a signaling hub and an autophagy adaptor. FEBS J. 282, 4672-4678 (2015).
101. Wild, P. et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228-233 (2011).
102. Richter, B. et al. Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc. Natl Acad. Sci. USA 113, 4039-4044 (2016).
103. Heo, J. M., Ordureau, A., Paulo, J. A., Rinehart, J. & Harper, J. W. The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol. Cell 60, 7-20 (2015).
104. Lazarou, M. et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 524, 309-314 (2015).
105. Khaminets, A. et al. Regulation of endoplasmic reticulum turnover by selective autophagy. Nature 522, 354-358 (2015).
106. Waters, S., Marchbank, K., Solomon, E., Whitehouse, C. & Gautel, M. Interactions with LC3 and polyubiquitin chains link NBR1 to autophagic protein turnover. FEBS Lett. 583, 1846-1852 (2009).
107. Kirkin, V. et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33, 505-516 (2009).
108. Deosaran, E. et al. NBR1 acts as an autophagy receptor for peroxisomes. J. Cell Sci. 126, 939-952 (2013).
109. Lin, L. et al. The scaffold protein EPG-7 links cargo-receptor complexes with the autophagic assembly machinery. J. Cell Biol. 201, 113-129 (2013).
110. Nagy, P. et al. Atg17/FIP200 localizes to perilysosomal Ref(2)P aggregates and promotes autophagy by activation of Atg1 in Drosophila. Autophagy 10, 453-467 (2014).
111. Ochaba, J. et al. Potential function for the Huntingtin protein as a scaffold for selective autophagy. Proc. Natl Acad. Sci. USA 111, 16889-16894 (2014).
112. Hara, T. & Mizushima, N. Role of ULK-FIP200 complex in mammalian autophagy: FIP200, a counterpart of yeast Atg17? Autophagy 5, 85-87 (2009).
113. Rui, Y. N. et al. Huntingtin functions as a scaffold for selective macroautophagy. Nat. Cell Biol. 17, 262-275 (2015).
114. Wang, K., Jin, M., Liu, X. & Klionsky, D. J. Proteolytic processing of Atg32 by the mitochondrial i-AAA protease Yme1 regulates mitophagy. Autophagy 9, 1828-1836 (2013).
115. Axe, E. L. et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182, 685-701 (2008).
116. Watanabe, Y. et al. Selective transport of α-mannosidase by autophagic pathways: structural basis for cargo recognition by Atg19 and Atg34. J. Biol. Chem. 285, 30026-30033 (2010).
117. Yuga, M., Gomi, K., Klionsky, D. J. & Shintani, T. Aspartyl aminopeptidase is imported from the cytoplasm to the vacuole by selective autophagy in Saccharomyces cerevisiae. J. Biol. Chem. 286, 13704-13713 (2011).
118. Hyttinen, J. M. et al. Clearance of misfolded and aggregated proteins by aggrephagy and implications for aggregation diseases. Ageing Res. Rev. 18, 16-28 (2014).
119. Svenning, S. & Johansen, T. Selective autophagy. Essays Biochem. 55, 79-92 (2013).
120. Orenstein, S. J. & Cuervo, A. M. Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. Semin. Cell Dev. Biol. 21, 719-726 (2010).
121. Seay, M., Hayward, A. P., Tsao, J. & Dinesh-Kumar, S. P. Something old, something new: plant innate immunity and autophagy. Curr. Top. Microbiol. Immunol. 335, 287-306 (2009).
122. Changou, C. A. et al. Arginine starvation-associated atypical cellular death involves mitochondrial dysfunction, nuclear DNA leakage, and chromatin autophagy. Proc. Natl Acad. Sci. USA 111, 14147-14152 (2014).
123. Cloonan, S. M., Lam, H. C., Ryter, S. W. & Choi, A. M. "Ciliophagy": the consumption of cilia components by autophagy. Autophagy 10, 532-534 (2014).
124. Watson, R. O., Manzanillo, P. S. & Cox, J. S. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150, 803-815 (2012).
125. Lipatova, Z. & Segev, N. A role for macro-ER-phagy in ER quality control. PLoS Genet. 11, e1005390 (2015).
126. Mancias, J. D. et al. Ferritinophagy via NCOA4 is required for erythropoiesis and is regulated by iron dependent HERC2-mediated proteolysis. eLife 4, e10308 (2015).
127. Mancias, J. D., Wang, X., Gygi, S. P., Harper, J. W. & Kimmelman, A. C. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 509, 105-109 (2014).
128. Jiang, S., Wells, C. D. & Roach, P. J. Starch-binding domain-containing protein 1 (Stbd1) and glycogen metabolism: identification of the Atg8 family interacting motif (AIM) in Stbd1 required for interaction with GABARAPL1. Biochem. Biophys. Res. Commun. 413, 420-425 (2011).
129. Kotoulas, O. B., Kalamidas, S. A. & Kondomerkos, D. J. Glycogen autophagy. Microsc. Res. Tech. 64, 10-20 (2004).
130. Kotoulas, O. B., Kalamidas, S. A. & Kondomerkos, D. J. Glycogen autophagy in glucose homeostasis. Pathol. Res. Pract. 202, 631-638 (2006).
131. Buchan, J. R., Kolaitis, R. M., Taylor, J. P. & Parker, R. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 153, 1461-1474 (2013).
132. Liu, K. & Czaja, M. J. Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ. 20, 3-11 (2013).
133. van Zutphen, T. et al. Lipid droplet autophagy in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 25, 290-301 (2014).
134. Maejima, I. et al. Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. EMBO J. 32, 2336-2347 (2013).
135. Hung, Y. H., Chen, L. M., Yang, J. Y. & Yang, W. Y. Spatiotemporally controlled induction of autophagy-mediated lysosome turnover. Nat. Commun. 4, 2111 (2013).
136. Kuo, T. C. et al. Midbody accumulation through evasion of autophagy contributes to cellular reprogramming and tumorigenicity. Nat. Cell Biol. 13, 1214-1223 (2011).
137. Pohl, C. & Jentsch, S. Midbody ring disposal by autophagy is a post-abscission event of cytokinesis. Nat. Cell Biol. 11, 65-70 (2009).
138. Kanki, T., Furukawa, K. & Yamashita, S. Mitophagy in yeast: molecular mechanisms and physiological role. Biochim. Biophys. Acta 1853, 2756-2765 (2015).
139. Liu, L., Sakakibara, K., Chen, Q. & Okamoto, K. Receptor-mediated mitophagy in yeast and mammalian systems. Cell Res. 24, 787-795 (2014).
140. Muller, M., Lu, K. & Reichert, A. S. Mitophagy and mitochondrial dynamics in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1853, 2766-2774 (2015).
141. Wong, Y. C. & Holzbaur, E. L. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc. Natl Acad. Sci. USA 111, E4439-E4448 (2014).
142. Youle, R. J. & Narendra, D. P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9-14 (2011).
143. Gomez-Sanchez, J. A. et al. Schwann cell autophagy, myelinophagy, initiates myelin clearance from injured nerves. J. Cell Biol. 210, 153-168 (2015).
144. Krick, R. et al. Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol. Biol. Cell 19, 4492-4505 (2008).
145. Mijaljica, D. & Devenish, R. J. Nucleophagy at a glance. J. Cell Sci. 126, 4325-4330 (2013).
146. Zientara-Rytter, K. et al. Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors. Autophagy 7, 1145-1158 (2011).
147. Vanhee, C., Zapotoczny, G., Masquelier, D., Ghislain, M. & Batoko, H. The Arabidopsis multistress regulator TSPO is a heme binding membrane protein and a potential scavenger of porphyrins via an autophagy-dependent degradation mechanism. Plant Cell 23, 785-805 (2011).
148. Michaeli, S., Honig, A., Levanony, H., Peled-Zehavi, H. & Galili, G. Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole. Plant Cell 26, 4084-4101 (2014).
149. Marshall, R. S., Li, F., Gemperline, D. C., Book, A. J. & Vierstra, R. D. Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/Ubiquitin receptor RPN10 in Arabidopsis. Mol. Cell 58, 1053-1066 (2015).
150. Kraft, C., Deplazes, A., Sohrmann, M. & Peter, M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 10, 602-610 (2008).
151. Ossareh-Nazari, B. et al. Cdc48 and Ufd3, new partners of the ubiquitin protease Ubp3, are required for ribophagy. EMBO Rep. 11, 548-554 (2010).
152. Mandell, M. A. et al. TRIM proteins regulate autophagy and can target autophagic substrates by direct recognition. Dev. Cell 30, 394-409 (2014).
153. Orvedahl, A. et al. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 480, 113-117 (2011).
154. Castrejon-Jimenez, N. S., Leyva-Paredes, K., Hernandez-Gonzalez, J. C., Luna-Herrera, J. & Garcia-Perez, B. E. The role of autophagy in bacterial infections. Biosci. Trends 9, 149-159 (2015).
155. Thurston, T. L., Wandel, M. P., von Muhlinen, N., Foeglein, A. & Randow, F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414-418 (2012).
156. Vaccaro, M. I. Zymophagy: selective autophagy of secretory granules. Int. J. Cell Biol. 2012, 396705 (2012).
157. 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).
158. Juris, L. et al. PI3P binding by Atg21 organises Atg8 lipidation. EMBO J. 34, 955-973 (2015).
159. 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).
160. Scott, S. V. et al. Apg13p and Vac8p are part of a complex of phosphoproteins that are required for cytoplasm to vacuole targeting. J. Biol. Chem. 275, 25840-25849 (2000).
161. Reggiori, F., Wang, C. W., Stromhaug, P. E., Shintani, T. & Klionsky, D. J. Vps51 is part of the yeast Vps fifty-three tethering complex essential for retrograde traffic from the early endosome and Cvt vesicle completion. J. Biol. Chem. 278, 5009-5020 (2003).
162. Reggiori, F., Monastyrska, I., Shintani, T. & Klionsky, D. J. The actin cytoskeleton is required for selective types of autophagy, but not nonspecific autophagy, in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 16, 5843-5856 (2005).
163. 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).
164. Monastyrska, I. et al. Arp2 links autophagic machinery with the actin cytoskeleton. Mol. Biol. Cell 19, 1962-1975 (2008).
165. Tamura, N., Oku, M. & Sakai, Y. Atg21 regulates pexophagy via its PI(3)P-binding activity in Pichia pastoris. FEMS Yeast Res. 14, 435-444 (2014).
166. 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).
167. Oku, M. et al. Peroxisome degradation requires catalytically active sterol glucosyltransferase with a GRAM domain. EMBO J. 22, 3231-3241 (2003).
168. Nazarko, V. Y. et al. Atg35, a micropexophagy-specific protein that regulates micropexophagic apparatus formation in Pichia pastoris. Autophagy 7, 375-385 (2011).
169. Fry, M. R., Thomson, J. M., Tomasini, A. J. & Dunn, W. A. Jr. Early and late molecular events of glucose-induced pexophagy in Pichia pastoris require Vac8. Autophagy 2, 280-288 (2006).
170. Hamasaki, M., Noda, T., Baba, M. & Ohsumi, Y. Starvation triggers the delivery of the endoplasmic reticulum to the vacuole via autophagy in yeast. Traffic 6, 56-65 (2005).