C. elegans neurons jettison protein aggregates and mitochondria under neurotoxic stress

Nature

Volumn 542, Issue 7641, 2017, Pages 367-371

  Melentijevic, Ilija ^a   Toth, Marton L ^a   Arnold, Meghan L ^a   Guasp, Ryan J ^a   Harinath, Girish ^a   Nguyen, Ken C ^b   Taub, Daniel ^c,d   Parker, J Alex ^e   Neri, Christian ^f,g   Gabel, Christopher V ^c,d   Hall, David H ^b   Driscoll, Monica ^a  

^a RUTGERS UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BOSTON UNIVERSITY   (United States)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

^f Groupe Enzymologie Moléculaire et Fonctionnelle   (France)

^g SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; CHAPERONE; HEAT SHOCK TRANSCRIPTION FACTOR 1; PROTEASOME; PROTEIN AGGREGATE;

BRAIN; CELLS AND CELL COMPONENTS; GENETIC ANALYSIS; INHIBITION; MITOCHONDRION; NERVOUS SYSTEM DISORDER; PROTEIN; PROTEOMICS; TOXICITY;

ADULT; ANIMAL CELL; ARTICLE; AUTOPHAGY; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; EXOSOME; HUMAN; MITOCHONDRION; NERVE CELL; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; UNFOLDED PROTEIN RESPONSE; YOUNG ADULT; AGING; ANIMAL; CYTOLOGY; CYTOPLASM; DEGENERATIVE DISEASE; MEMBRANE MICROPARTICLE; METABOLISM; NEUROPROTECTION; OXIDATION REDUCTION REACTION; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS);

CAENORHABDITIS ELEGANS;

AGING; ANIMALS; AUTOPHAGY; CAENORHABDITIS ELEGANS; CELL-DERIVED MICROPARTICLES; CYTOPLASM; MITOCHONDRIA; MOLECULAR CHAPERONES; NEURODEGENERATIVE DISEASES; NEURONS; NEUROPROTECTION; OXIDATION-REDUCTION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN AGGREGATES;

EID: 85015323246     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature21362     Document Type: Article

References (49)

1. Yankner, B. A., Lu, T. & Loerch, P. The aging brain. Annu. Rev. Pathol. 3, 41-66 (2008).
2. Federico, A. et al. Mitochondria, oxidative stress and neurodegeneration. J. Neurol. Sci. 322, 254-262 (2012).
3. Morimoto, R. I. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427-1438 (2008).
4. Ben-Gedalya, T. & Cohen, E. Quality control compartments coming of age. Traffic 13, 635-642 (2012).
5. Lee, S. J., Desplats, P., Sigurdson, C., Tsigelny, I. & Masliah, E. Cell-to-cell transmission of non-prion protein aggregates. Nat. Rev. Neurol. 6, 702-706 (2010).
6. Davis, C. H. et al. Transcellular degradation of axonal mitochondria. Proc. Natl Acad. Sci. USA 111, 9633-9638 (2014).
7. Toth, M. L. et al. Neurite sprouting and synapse deterioration in the aging Caenorhabditis elegans nervous system. J. Neurosci. 32, 8778-8790 (2012).
8. Craig, A. L., Moser, S. C., Bailly, A. P. & Gartner, A. Methods for studying the DNA damage response in the Caenorhabdatis elegans germ line. Methods Cell Biol. 107, 321-352 (2012).
9. Perkins, L. A., Hedgecock, E. M., Thomson, J. N. & Culotti, J. G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117, 456-487 (1986).
10. Parker, J. A. et al. Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death. Proc. Natl Acad. Sci. USA 98, 13318-13323 (2001).
11. Vayndorf, E. M. et al. Morphological remodeling of C. elegans neurons during aging is modified by compromised protein homeostasis. NPJ Aging Mech. Dis. 2, 16001 (2016).
12. Labbadia, J. & Morimoto, R. I. Proteostasis and longevity: when does aging really begin? F1000Prime Rep. 6, 7 (2014).
13. Labbadia, J. & Morimoto, R. I. Repression of the heat shock response is a programmed event at the onset of reproduction. Mol. Cell 59, 639-650 (2015).
14. Liu, G., Rogers, J., Murphy, C. T. & Rongo, C. EGF signalling activates the ubiquitin proteasome system to modulate C. elegans lifespan. EMBO J. 30, 2990-3003 (2011).
15. Samann, J. et al. Caenorhabditits elegans LRK-1 and PINK-1 act antagonistically in stress response and neurite outgrowth. J. Biol. Chem. 284, 16482-16491 (2009).
16. Springer, W., Hoppe, T., Schmidt, E. & Baumeister, R. A Caenorhabditis elegans Parkin mutant with altered solubility couples alpha-synuclein aggregation to proteotoxic stress. Hum. Mol. Genet. 14, 3407-3423 (2005).
17. Benedetti, C., Haynes, C. M., Yang, Y., Harding, H. P. & Ron, D. Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 174, 229-239 (2006).
18. Cannon, M. B. & Remington, S. J. Redox-sensitive green fluorescent protein: probes for dynamic intracellular redox responses. A review. Methods Mol. Biol. 476, 50-64 (2008).
19. Ghose, P., Park, E. C., Tabakin, A., Salazar-Vasquez, N. & Rongo, C. Anoxiareoxygenation regulates mitochondrial dynamics through the hypoxia response pathway, SKN-1/Nrf, and stomatin-like protein STL-1/SLP-2. PLoS Genet. 9, e1004063 (2013).
20. Laker, R. C. et al. A novel MitoTimer reporter gene for mitochondrial content, structure, stress, and damage in vivo. J. Biol. Chem. 289, 12005-12015 (2014).
21. Ji, Y. B., Qu, Z. Y. & Zou, X. Juglone-induced apoptosis in human gastric cancer SGC-7901 cells via the mitochondrial pathway. Exp. Toxicol. Pathol. 63, 69-78 (2011).
22. Patton, A. et al. Endocytosis function of a ligand-gated ion channel homolog in Caenorhabditis elegans. Curr. Biol. 15, 1045-1050 (2005).
23. Nath, S. et al. Spreading of neurodegenerative pathology via neuron-to-neuron transmission of β-amyloid. J. Neurosci. 32, 8767-8777 (2012).
24. Nussbaum-Krammer, C. I., Park, K. W., Li, L., Melki, R. & Morimoto, R. I. Spreading of a prion domain from cell-to-cell by vesicular transport in Caenorhabditis elegans. PLoS Genet. 9, e1003351 (2013).
25. Costanzo, M. et al. Transfer of polyglutamine aggregates in neuronal cells occurs in tunneling nanotubes. J. Cell Sci. 126, 3678-3685 (2013).
26. Abounit, S. & Zurzolo, C. Wiring through tunneling nanotubes-from electrical signals to organelle transfer. J. Cell Sci. 125, 1089-1098 (2012).
27. Gousset, K. et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 11, 328-336 (2009).
28. Pearce, M. M., Spartz, E. J., Hong, W., Luo, L. & Kopito, R. R. Prion-like transmission of neuronal huntingtin aggregates to phagocytic glia in the Drosophila brain. Nat. Commun. 6, 6768 (2015).
29. Pasquier, J. et al. Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J. Transl. Med. 11, 94 (2013).
30. Hayakawa, K. et al. Transfer of mitochondria from astrocytes to neurons after stroke. Nature 535, 551-555 (2016).
31. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
32. Duan, Z. & Sesti, F. A Caenorhabditis elegans model system for amylopathy study. J. Vis. Exp. 75, 50435 (2013).
33. Mapes, J. et al. CED-1, CED-7, and TTR-52 regulate surface phosphatidylserine expression on apoptotic and phagocytic cells. Curr. Biol. 22, 1267-1275 (2012).
34. Neumann, B. et al. EFF-1-mediated regenerative axonal fusion requires components of the apoptotic pathway. Nature 517, 219-222 (2015).
35. Kachur, T. M., Audhya, A. & Pilgrim, D. B. UNC-45 is required for NMY-2 contractile function in early embryonic polarity establishment and germline cellularization in C. elegans. Dev. Biol. 314, 287-299 (2008).
36. Kamath, R. S. & Ahringer, J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321 (2003).
37. Calixto, A., Chelur, D., Topalidou, I., Chen, X. & Chalfie, M. Enhanced neuronal RNAi in C. elegans using SID-1. Nat. Methods 7, 554-559 (2010).
38. Liu, J. et al. Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell 147, 223-234 (2011).
39. Scerbak, C. et al. Insulin signaling in the aging of healthy and proteotoxically stressed mechanosensory neurons. Front. Genet. 5, 212 (2014).
40. Topalidou, I. et al. Genetically separable functions of the MEC-17 tubulin acetyltransferase affect microtubule organization. Curr. Biol. 22, 1057-1065 (2012).
41. Gabel, C. V., Antoine, F., Chuang, C. F., Samuel, A. D. & Chang, C. Distinct cellular and molecular mechanisms mediate initial axon development and adult-stage axon regeneration in C. elegans. Development 135, 1129-1136 (2008).
42. Kopito, R. R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524-530 (2000).
43. Hermann, G. J. et al. Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol. Biol. Cell 16, 3273-3288 (2005).
44. Zhou, Z., Hartwieg, E. & Horvitz, H. R. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104, 43-56 (2001).
45. Hong, Y., Roy, R. & Ambros, V. Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125, 3585-3597 (1998).
46. Kastelowitz, N. & Yin, H. Exosomes and microvesicles: identification and targeting by particle size and lipid chemical probes. ChemBioChem. 15, 923-928 (2014).
47. Cocucci, E. & Meldolesi, J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol. 25, 364-372 (2015).
48. Thery, C., Zitvogel, L. & Amigorena, S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569-579 (2002).
49. Ma, L. et al. Discovery of the migrasome, an organelle mediating release of cytoplasmic contents during cell migration. Cell Res. 25, 24-38 (2015).