Role of ATG8 and Autophagy in programmed nuclear degradation in Tetrahymena thermophila

Eukaryotic Cell

Volumn 11, Issue 4, 2012, Pages 494-506

  Liu, Ming Liang ^a,b   Yao, Meng Chao ^a,b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PROTOZOAL DNA; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; AUTOPHAGY; GENETICS; GERMLINE MICRONUCLEUS; MACRONUCLEUS; METABOLISM; MICROBIAL VIABILITY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN TRANSPORT; REPRODUCTION; TETRAHYMENA THERMOPHILA;

AMINO ACID SEQUENCE; AUTOPHAGY; CONSERVED SEQUENCE; DNA, PROTOZOAN; MACRONUCLEUS; MICROBIAL VIABILITY; MICRONUCLEUS, GERMLINE; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; REPRODUCTION; TETRAHYMENA THERMOPHILA;

PROTISTA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 84859154731     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05296-11     Document Type: Article

References (64)

1. Akematsu T, Endoh H. 2010. Role of apoptosis-inducing factor (AIF) in programmed nuclear death during conjugation in Tetrahymena thermophila. BMC Cell Biol. 11:13.
2. Akematsu T, Pearlman RE, Endoh H. 2010. Gigantic macroautophagy in programmed nuclear death of Tetrahymena thermophila. Autophagy 6:901-911.
3. Allewell NM, Oles J, Wolfe J. 1976. A physicochemical analysis of conjugation in Tetrahymena pyriformis. Exp. Cell Res. 97:394-405.
4. Alvarez VE, et al. 2008. Autophagy is involved in nutritional stress re-sponse and differentiation in Trypanosoma cruzi. J. Biol. Chem. 283: 3454-3464.
5. Benchimol M. 1999. Hydrogenosome autophagy: an ultrastructural and cytochemical study. Biol. Cell 91:165-174.
6. Besteiro S, Williams RA, Coombs GH, Mottram JC. 2007. Protein turnover and differentiation in Leishmania. Int. J. Parasitol. 37:1063-1075.
7. Besteiro S, Williams RA, Morrison LS, Coombs GH, Mottram JC. 2006. Endosome sorting and autophagy are essential for differentiation and virulence of Leishmania major. J. Biol. Chem. 281:11384-11396.
8. Bruns PJ, Cassidy-Hanley D. 2000. Biolistic transformation of macroand micronuclei. Methods Cell Biol. 62:501-512.
9. Calvo-Garrido J, et al. 2010. Autophagy in Dictyostelium: genes and pathways, cell death and infection. Autophagy 6:686-701.
10. Cassidy-Hanley D, et al. 1997. Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 146:135-147.
11. Chalker DL. 2008. Dynamic nuclear reorganization during genome remodeling of Tetrahymena. Biochim. Biophys. Acta 1783:2130-2136.
12. Chan EY, Kir S, Tooze SA. 2007. siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J. Biol. Chem. 282:25464-25474.
13. Chan EY, Longatti A, McKnight NC, Tooze SA. 2009. Kinaseinactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol. Cell. Biol. 29:157-171.
14. Cheng CY, Vogt A, Mochizuki K, Yao MC. 2010. A domesticated piggyBac transposase plays key roles in heterochromatin dynamics and DNA cleavage during programmed DNA deletion in Tetrahymena thermophila. Mol. Biol. Cell 21:1753-1762.
15. Coleman J, et al. 2010. A live-cell fluorescence microplate assay suitable for monitoring vacuolation arising from drug or toxic agent treatment. J. Biomol. Screen. 15:398-405.
16. Davis MC, Ward JG, Herrick G, Allis CD. 1992. Programmed nuclear death: apoptotic-like degradation of specific nuclei in conjugating Tetrahymena. Dev. Biol. 154:419-432.
17. Ejercito M, Wolfe J. 2003. Caspase-like activity is required for programmed nuclear elimination during conjugation in Tetrahymena. J. Eukaryot. Microbiol. 50:427-429.
18. Endoh H, Kobayashi T. 2006. Death harmony played by nucleus and mitochondria: nuclear apoptosis during conjugation of Tetrahymena. Autophagy 2:129-131.
19. Ganley IG, et al. 2009. ULK1/ATG13/FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem. 284:12297-12305.
20. Hanada T, et al. 2007. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 282:37298-37302.
21. Hara T, et al. 2008. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J. Cell Biol. 181:497-510.
22. Hemelaar J, Lelyveld VS, Kessler BM, Ploegh HL. 2003. 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.
23. Herman M, Gillies S, Michels PA, Rigden DJ. 2006. Autophagy and related processes in trypanosomatids: insights from genomic and bioinformatic analyses. Autophagy 2:107-118.
24. Hosokawa N, et al. 2009. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 20:1981-1991.
25. Ichimura Y, et al. 2000. A ubiquitin-like system mediates protein lipidation. Nature 408:488-492.
26. Johansson M, et al. 2007. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J. Cell Biol. 176:459-471.
27. Jung CH, et al. 2009. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 20:1992-2003.
28. Kabeya Y, et al. 2004. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117: 2805-2812.
29. Khalfan WA, Klionsky DJ. 2002. Molecular machinery required for autophagy and the cytoplasm to vacuole targeting (Cvt) pathway in S. cerevisiae. Curr. Opin. Cell Biol. 14:468-475.
30. Kimura S, Noda T, Yoshimori T. 2008. Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct. Funct. 33:109-122.
31. Kirisako T, et al. 2000. 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.
32. Klionsky DJ. 2007. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8:931-937.
33. Kobayashi T, Endoh H. 2003. Caspase-like activity in programmed nuclear death during conjugation of Tetrahymena thermophila. Cell Death Differ. 10:634-640.
34. Lu E, Wolfe J. 2001. Lysosomal enzymes in the macronucleus of Tetrahymena during its apoptosis-like degradation. Cell Death Differ. 8:289-297.
35. Matsui M, Yamamoto A, Kuma A, Ohsumi Y, Mizushima N. 2006. Organelle degradation during the lens and erythroid differentiation is independent of autophagy. Biochem. Biophys. Res. Commun. 339:485-489.
36. Michels PA, Bringaud F, Herman M, Hannaert V. 2006. Metabolic functions of glycosomes in trypanosomatids. Biochim. Biophys. Acta 1763:1463-1477.
37. Mijaljica D, Prescott M, Devenish RJ. 2006. Endoplasmic reticulum and Golgi complex: contributions to, and turnover by, autophagy. Traffic 7:1590-1595.
38. Mijaljica D, Prescott M, Devenish RJ. 2007. Nibbling within the nucleus: turnover of nuclear contents. Cell. Mol. Life Sci. 64:581-588.
39. Mizushima N, Levine B. 2010. Autophagy in mammalian development and differentiation. Nat. Cell Biol. 12:823-830.
40. Mochizuki K. 2008. High efficiency transformation of Tetrahymena using a codon-optimized neomycin resistance gene. Gene 425:79-83.
41. Mpoke S, Wolfe J. 1996. DNA digestion and chromatin condensation during nuclear death in Tetrahymena. Exp. Cell Res. 225:357-365.
42. Nagata S, Nagase H, Kawane K, Mukae N, Fukuyama H. 2003. Degradation of chromosomal DNA during apoptosis. Cell Death Differ. 10: 108-116.
43. Nilsson JR. 1984. On starvation-induced autophagy in Tetrahymena. Carlsberg Res. Commun. 49:323-340.
44. Otto GP, Wu MY, Kazgan N, Anderson OR, Kessin RH. 2003. Macroautophagy is required for multicellular development of the social amoeba Dictyostelium discoideum. J. Biol. Chem. 278:17636-17645.
45. Otto GP, Wu MY, Kazgan N, Anderson OR, Kessin RH. 2004. Dictyostelium macroautophagy mutants vary in the severity of their developmental defects. J. Biol. Chem. 279:15621-15629.
46. Pankiv S, et al. 2010. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J. Cell Biol. 188:253-269.
47. Paz Y, Elazar Z, Fass D. 2000. Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p. J. Biol. Chem. 275:25445-25450.
48. Punta M, et al. 2012. The Pfam protein families database. Nucleic Acids Res. 40:D290-D301.
49. Samejima K, Earnshaw WC. 2005. Trashing the genome: the role of nucleases during apoptosis. Nat. Rev. Mol. Cell Biol. 6:677-688.
50. Shang Y, et al. 2002. A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc. Natl. Acad. Sci. U. S. A. 99:3734-3739.
51. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E. 2005. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1:84-91.
52. Tanida I, Tanida-Miyake E, Komatsu M, Ueno T, Kominami E. 2002. 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.
53. Tanida I, Tanida-Miyake E, Ueno T, Kominami E. 2001. 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.
54. Tanida I, Ueno T, Kominami E. 2004. LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36:2503-2518.
55. Terman A, Gustafsson B, Brunk UT. 2007. Autophagy, organelles and ageing. J. Pathol. 211:134-143.
56. Weidberg H, et al. 2010. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J. 29:1792-1802.
57. Weiske-Benner A, Eckert WA. 1987. Differentiation of nuclear structure during the sexual cycle in Tetrahymena thermophila. Differentiation 34:1-12.
58. Williams RA, Tetley L, Mottram JC, Coombs GH. 2006. Cysteine peptidases CPA and CPB are vital for autophagy and differentiation in Leishmania mexicana. Mol. Microbiol. 61:655-674.
59. Williams RA, Woods KL, Juliano L, Mottram JC, Coombs GH. 2009. Characterization of unusual families of ATG8-like proteins and ATG12 in the protozoan parasite Leishmania major. Autophagy 5:159-172.
60. Xie Z, Nair U, Klionsky DJ. 2008. Atg8 controls phagophore expansion during autophagosome formation. Mol. Biol. Cell 19:3290-3298.
61. Yakisich JS, Kapler GM. 2004. The effect of phosphoinositide 3-kinase inhibitors on programmed nuclear degradation in Tetrahymena and fate of surviving nuclei. Cell Death Differ. 11:1146-1149.
62. Yang Z, Klionsky DJ. 2010. Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22:124-131.
63. Yao MC, Chao JL. 2005. RNA-guided DNA deletion in Tetrahymena: an RNAi-based mechanism for programmed genome rearrangements. Annu. Rev. Genet. 39:537-559.
64. Yorimitsu T, Klionsky DJ. 2005. Autophagy: molecular machinery for self-eating. Cell Death Differ. 12(Suppl. 2):1542-1552.