Dynein light chain 1 is required for autophagy, protein clearance, and cell death in Drosophila

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 2, 2010, Pages 742-747

  Batlevi, Yakup ^a,b   Martin, Damali N ^c   Pandey, Udai Bhan ^d   Simon, Claudio R ^e   Powers, Christine M ^a   Taylor, J Paul ^d   Baehrecke, Eric H ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Bldg 142   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^e FEDERAL UNIVERSITY OF TRIÂNGULO MINEIRO   (Brazil)

Author keywords

Macroautophagy; Neurodegeneration; Protein degradation

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; DYNEIN LIGHT CHAIN 1 PROTEIN; POLYGLUTAMINE; PROTEIN P62; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL DEATH; CONTROLLED STUDY; DDLC1 GENE; DEGENERATIVE DISEASE; DROSOPHILA; GENE; GENE IDENTIFICATION; LARVA; MOTOR DEVELOPMENT; MUSCLE; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SALIVARY GLAND; SYNAPSE VESICLE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AUTOPHAGY; CASPASES; CELL DEATH; CONSERVED SEQUENCE; CROSSES, GENETIC; CYTOPLASMIC DYNEINS; DNA; DROSOPHILA; DROSOPHILA PROTEINS; IN SITU NICK-END LABELING; LARVA; MUTAGENESIS, INSERTIONAL; MUTATION; NERVE DEGENERATION; PUPA; SALIVARY GLANDS; SYNAPSES;

EID: 76249112500     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0907967107     Document Type: Article

References (47)

1. Mizushima N (2007) Autophagy: process and function. Genes Dev 21:2861-2873.
2. Harding TM, Morano KA, Scott SV, Klionsky DJ (1995) Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 131:591-602.
3. Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169-174.
4. Thumm M, et al. (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett 349:275-280.
5. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15:1101-1111.
6. Baehrecke EH (2005) Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol 6: 505-510.
7. Boya P, et al. (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25: 1025-1040.
8. Boland B, et al. (2008) Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J Neurosci 28: 6926-6937.
9. Pandey UB, et al. (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447:859-863.
10. Hara T, et al. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441:885-889.
11. Komatsu M, et al. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880-884.
12. Schweichel JU, Merker HJ (1973) The morphology of various types of cell death in prenatal tissues. Teratology 7:253-266.
13. Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 181:195-213.
14. Berry DL, Baehrecke EH (2007) Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131:1137-1148.
15. Qu X, et al. (2007) Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 128:931-946.
16. Mohseni N, McMillan SC, Chaudhary R, Mok J, Reed BH (2009) Autophagy promotes caspase-dependent cell death during Drosophila development. Autophagy 5:329-338.
17. Hou YC, Chittaranjan S, Barbosa SG, McCall K, Gorski SM (2008) Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J Cell Biol 182:1127-1139.
18. Lee CY, Baehrecke EH (2001) Steroid regulation of autophagic programmed cell death during development. Development 128:1443-1455.
19. Martin DN, Baehrecke EH (2004) Caspases function in autophagic programmed cell death in Drosophila. Development 131:275-284.
20. Ravikumar B, et al. (2005) Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat Genet 37:771-776.
21. Puthalakath H, Huang DC, O'Reilly LA, King SM, Strasser A (1999) The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 3:287-296.
22. King SM, et al. (1996) Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved Mr 8,000 light chain. J Biol Chem 271:19358-19366.
23. Dick T, Ray K, Salz HK, Chia W (1996) Cytoplasmic dynein (ddlc1) mutations cause morphogenetic defects and apoptotic cell death in Drosophila melanogaster. Mol Cell Biol 16:1966-1977.
24. Phillis R, Statton D, Caruccio P, Murphey RK (1996) Mutations in the 8 kDa dynein light chain gene disrupt sensory axon projections in the Drosophila imaginal CNS. Development 122:2955-2963.
25. Neufeld TP, Baehrecke EH (2008) Eating on the fly: function and regulation of autophagy during cell growth, survival and death in Drosophila. Autophagy 4:557-562.
26. Lee CY, et al. (2003) Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Curr Biol 13:350-357.
27. Rusten TE, et al. (2004) Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell 7:179-192.
28. Biyasheva A, Do TV, Lu Y, Vaskova M, Andres AJ (2001) Glue secretion in the Drosophila salivary gland: a model for steroid-regulated exocytosis. Dev Biol 231:234-251.
29. Ross CA, Poirier MA (2004) Protein aggregation and neurodegenerative disease. Nat Med 10 (suppl):S10-S17.
30. Maezawa I, et al. (2008) Congo red and thioflavin-T analogs detect Abeta oligomers. J Neurochem 104:457-468.
31. Ross CA, Pickart CM (2004) The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases. Trends Cell Biol 14:703-711.
32. Bjørkøy G, et al. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603-614.
33. Nezis IP, et al. (2008) Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. J Cell Biol 180:1065-1071.
34. Iwata A, Riley BE, Johnston JA, Kopito RR (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280:40282-40292.
35. Scott RC, Juhász G, Neufeld TP (2007) Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol 17:1-11.
36. La Spada AR, Wilson EM, Lubahn DB, Harding AE, Fischbeck KH (1991) Androgenreceptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 352:77-79.
37. Lo KW, et al. (2005) The 8-kDa dynein light chain binds to p53-binding protein 1 and mediates DNA damage-induced p53 nuclear accumulation. J Biol Chem 280:8172-8179.
38. Barbar E (2008) Dynein light chain LC8 is a dimerization hub essential in diverse protein networks. Biochemistry 47:503-508.
39. Köchl R, Hu XW, Chan EY, Tooze SA (2006) Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 7:129-145.
40. Kimura S, Noda T, Yoshimori T (2008) Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct Funct 33:109-122.
41. Komatsu M, et al. (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131:1149-1163.
42. Ichimura Y, et al. (2008) Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 283:22847-22857.
43. Garcia SM, Casanueva MO, Silva MC, Amaral MD, Morimoto RI (2007) Neuronal signaling modulates protein homeostasis in Caenorhabditis elegans post-synaptic muscle cells. Genes Dev 21:3006-3016.
44. Shen W, Ganetzky B (2009) Autophagy promotes synapse development in Drosophila. J Cell Biol 187:71-79.
45. Hay BA, Wolff T, Rubin GM (1994) Expression of baculovirus P35 prevents cell death in Drosophila. Development 120:2121-2129.
46. Budnik V, Gorczyca M, Prokop A (2006) Selected methods for the anatomical study of Drosophila embryonic and larval neuromuscular junctions. Int Rev Neurobiol 75:323-365.
47. Osterwalder T, Yoon KS, White BH, Keshishian H (2001) A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci USA 98: 12596-12601.