The ESCRT-II proteins are involved in shaping the sarcoplasmic reticulum in C. elegans

Journal of Cell Science

Volumn 129, Issue 7, 2016, Pages 1490-1499

  Lefebvre, Christophe ^a   Largeau, Céline ^a   Michelet, Xavier ^b   Fourrage, Cécile ^a   Maniere, Xavier ^c   Matic, Ivan ^c   Legouis, Renaud ^a   Culetto, Emmanuel ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Caenorhabditis elegans; ESCRT II; Organelle shape; Sarcoplasmic reticulum

Indexed keywords

BIOLOGICAL MARKER; CALCIUM; ESCRT II PROTEIN; ESCRT PROTEIN; RYANODINE RECEPTOR; UNC 68 PROTEIN; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; UNC-68 PROTEIN, C ELEGANS;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; MOLECULAR DYNAMICS; MUSCLE FIBER CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SARCOMERE; SARCOPLASMIC RETICULUM; STRIATED MUSCLE CELL; ANIMAL; METABOLISM; MUSCLE CELL; MUSCLE CONTRACTION; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; MUSCLE CELLS; MUSCLE CONTRACTION; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM;

EID: 84964053044     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.178467     Document Type: Article

References (47)

1. Ackermann, M. A., Ziman, A. P., Strong, J., Zhang, Y., Hartford, A. K., Ward, C. W., Randall, W. R., Kontrogianni-Konstantopoulos, A. and Bloch, R. J. (2011). Integrity of the network sarcoplasmic reticulum in skeletal muscle requires small ankyrin 1. J. Cell Sci. 124, 3619-3630.
2. Amoasii, L., Hnia, K., Chicanne, G., Brech, A., Cowling, B. S., Müller, M. M., Schwab, Y., Koebel, P., Ferry, A., Payrastre, B. et al. (2013). Myotubularin and PtdIns3P remodel the sarcoplasmic reticulum in muscle in vivo. J. Cell Sci. 126, 1806-1819.
3. Bagnato, P., Barone, V., Giacomello, E., Rossi, D. and Sorrentino, V. (2003). Binding of an ankyrin-1 isoform to obscurin suggests a molecular link between the sarcoplasmic reticulum and myofibrils in striated muscles. J. Cell Biol. 160, 245-253.
4. Bauer, I., Brune, T., Preiss, R. and Kölling, R. (2015). Evidence for a Nonendosomal Function of the Saccharomyces cerevisiae ESCRT-III-Like Protein Chm7. Genetics 201, 1439-1452.
5. Benian, G. M. and Epstein, H. F. (2011). Caenorhabditis elegans muscle: a genetic and molecular model for protein interactions in the heart. Circ. Res. 109, 1082-1095.
6. Boura, E., Ivanov, V., Carlson, L.-A., Mizuuchi, K. and Hurley, J. H. (2012). Endosomal sorting complex required for transport (ESCRT) complexes induce phase-separated microdomains in supported lipid bilayers. J. Biol. Chem. 287, 28144-28151.
7. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
8. Carlton, J. G. and Martin-Serrano, J. (2007). Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912.
9. Cho, J. H., Oh, Y. S., Park, K. W., Yu, J., Choi, K. Y., Shin, J. Y., Kim, D. H., Park, W. J., Hamada, T., Kagawa, H. et al. (2000). Calsequestrin, a calcium sequestering protein localized at the sarcoplasmic reticulum, is not essential for body-wall muscle function in Caenorhabditis elegans. J. Cell Sci. 113, 3947-3958.
10. Choudhuri, K., Llodrá, J., Roth, E.W., Tsai, J., Gordo, S., Wucherpfennig, K.W., Kam, L. C., Stokes, D. L. and Dustin, M. L. (2014). Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature 507, 118-123.
11. Colombo, M., Moita, C., van Niel, G., Kowal, J., Vigneron, J., Benaroch, P., Manel, N., Moita, L. F., Théry, C. and Raposo, G. (2013). Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell Sci. 126, 5553-5565.
12. Djeddi, A., Michelet, X., Culetto, E., Alberti, A., Barois, N. and Legouis, R. (2012). Induction of autophagy in ESCRT mutants is an adaptive response for cell survival in C. elegans. J. Cell Sci. 125, 685-694.
13. Fourest-Lieuvin, A., Rendu, J., Osseni, A., Pernet-Gallay, K., Rossi, D., Oddoux, S., Brocard, J., Sorrentino, V., Marty, I. and Fauré, J. (2012). Role of triadin in the organization of reticulum membrane at the muscle triad. J. Cell Sci. 125, 3443-3453.
14. Fyfe, I., Schuh, A. L., Edwardson, J. M. and Audhya, A. (2011). Association of the endosomal sorting complex ESCRT-II with the Vps20 subunit of ESCRT-III generates a curvature-sensitive complex capable of nucleating ESCRT-III filaments. J. Biol. Chem. 286, 34262-34270.
15. Garrus, J. E., von Schwedler, U. K., Pornillos, O. W., Morham, S. G., Zavitz, K. H., Wang, H. E., Wettstein, D. A., Stray, K. M., Côté, M., Rich, R. L. et al. (2001). Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 55-65.
16. Gokhin, D. S. and Fowler, V. M. (2011). Cytoplasmic gamma-actin and tropomodulin isoforms link to the sarcoplasmic reticulum in skeletal muscle fibers. J. Cell Biol. 194, 105-120.
17. Hammarlund, M., Davis, W. S. and Jorgensen, E. M. (2000). Mutations in beta-spectrin disrupt axon outgrowth and sarcomere structure. J. Cell Biol. 149, 931-942.
18. Hanson, P. I. and Cashikar, A. (2012). Multivesicular body morphogenesis. Annu. Rev. Cell Dev. Biol. 28, 337-362.
19. Hobert, O. (2002). PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32, 728-730.
20. Im, Y. J. and Hurley, J. H. (2008). Integrated structural model and membrane targeting mechanism of the human ESCRT-II complex. Dev. Cell 14, 902-913.
21. Irion, U. and St Johnston, D. (2007). bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445, 554-558.
22. Jimenez, A. J., Maiuri, P., Lafaurie-Janvore, J., Divoux, S., Piel, M. and Perez, F. (2014). ESCRT machinery is required for plasma membrane repair. Science 343, 1247136.
23. Jin, Y., Mancuso, J. J., Uzawa, S., Cronembold, D. and Cande, W. Z. (2005). The fission yeast homolog of the human transcription factor EAP30 blocks meiotic spindle pole body amplification. Dev. Cell 9, 63-73.
24. Kamura, T., Burian, D., Khalili, H., Schmidt, S. L., Sato, S., Liu, W.-J., Conrad, M. N., Conaway, R. C., Conaway, J. W. and Shilatifard, A. (2001). Cloning and characterization of ELL-associated proteins EAP45 and EAP20: a role for yeast EAP-like proteins in regulation of gene expression by glucose. J. Biol. Chem. 276, 16528-16533.
25. Kashyap, L., Perera, S. and Fisher, A. L. (2012). Identification of novel genes involved in sarcopenia through RNAi screening in Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 67, 56-65.
26. Kerr, R. A. (2006). Imaging the activity of neurons and muscles. WormBook 1-13.
27. Kolotuev, I., Schwab, Y. and Labouesse, M. (2010). A precise and rapid mapping protocol for correlative light and electron microscopy of small invertebrate organisms. Biol. Cell 102, 121-132.
28. Lange, S., Ouyang, K., Meyer, G., Cui, L., Cheng, H., Lieber, R. L. and Chen, J. (2009). Obscurin determines the architecture of the longitudinal sarcoplasmic reticulum. J. Cell Sci. 122, 2640-2650.
29. Manière, X., Lebois, F., Matic, I., Ladoux, B., Di Meglio, J.-M. and Hersen, P. (2011). Running worms: C. elegans self-sorting by electrotaxis. PLoS ONE 6, e16637.
30. Manil-Ségalen, M., Culetto, E., Legouis, R. and Lefebvre, C. (2014). Interactions between endosomal maturation and autophagy: analysis of ESCRT machinery during Caenorhabditis elegans development. Methods Enzymol. 534, 93-118.
31. Maryon, E. B., Saari, B. and Anderson, P. (1998). Muscle-specific functions of ryanodine receptor channels in Caenorhabditis elegans. J. Cell Sci. 111, 2885-2895.
32. McCullough, J., Colf, L. A. and Sundquist, W. I. (2013). Membrane fission reactions of the mammalian ESCRT pathway. Annu. Rev. Biochem. 82, 663-692.
33. Mello, C. and Fire, A. (1995). DNA transformation. Methods Cell Biol. 48, 451-482.
34. Mercker, M. and Marciniak-Czochra, A. (2015). Bud-neck scaffolding as a possible driving force in ESCRT-induced membrane budding. Biophys. J. 108, 833-843.
35. Michelet, X., Alberti, A., Benkemoun, L., Roudier, N., Lefebvre, C. and Legouis, R. (2009). The ESCRT-III protein CeVPS-32 is enriched in domains distinct from CeVPS-27 and CeVPS-23 at the endosomal membrane of epithelial cells. Biol. Cell 101, 599-615.
36. Olmos, Y., Hodgson, L., Mantell, J., Verkade, P. and Carlton, J. G. (2015). ESCRT-III controls nuclear envelope reformation. Nature 522, 236-239.
37. Roudier, N., Lefebvre, C. and Legouis, R. (2005). CeVPS-27 is an endosomal protein required for the molting and the endocytic trafficking of the low-density lipoprotein receptor-related protein 1 in Caenorhabditis elegans. Traffic 6, 695-705.
38. Schnorrer, F., Schönbauer, C., Langer, C. C. H., Dietzl, G., Novatchkova, M., Schernhuber, K., Fellner, M., Azaryan, A., Radolf, M., Stark, A. et al. (2010). Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 464, 287-291.
39. Schuh, A. L., Hanna, M., Quinney, K., Wang, L., Sarkeshik, A., Yates, J. R. and Audhya, A. (2015). The VPS-20 subunit of the endosomal sorting complex ESCRT-III exhibits an open conformation in the absence of upstream activation. Biochem. J. 466, 625-637.
40. Schwarz, J., Lewandrowski, I. and Bringmann, H. (2011). Reduced activity of a sensory neuron during a sleep-like state in Caenorhabditis elegans. Curr. Biol. 21, R983-R984.
41. Schwarz, J., Spies, J.-P. and Bringmann, H. (2012). Reduced muscle contraction and a relaxed posture during sleep-like Lethargus. Worm 1, 12-14.
42. Vaccari, T., Rusten, T. E., Menut, L., Nezis, I. P., Brech, A., Stenmark, H. and Bilder, D. (2009). Comparative analysis of ESCRT-I, ESCRT-II and ESCRT-III function in Drosophila by efficient isolation of ESCRT mutants. J. Cell Sci. 122, 2413-2423.
43. Vietri, M., Schink, K. O., Campsteijn, C., Wegner, C. S., Schultz, S.W., Christ, L., Thoresen, S. B., Brech, A., Raiborg, C. and Stenmark, H. (2015). Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522, 231-235.
44. Warner, A., Qadota, H., Benian, G. M., Vogl, A. W. and Moerman, D. G. (2011). The Caenorhabditis elegans paxillin orthologue, PXL-1, is required for pharyngeal muscle contraction and for viability. Mol. Biol. Cell 22, 2551-2563.
45. Watanabe, S., Richards, J., Hollopeter, G., Hobson, R. J., Davis, W. M. and Jorgensen, E. M. (2012). Nano-fEM: protein localization using photo-activated localization microscopy and electron microscopy. J. Vis. Exp. 70, e3995.
46. Waterston, R. (1988). Muscle. In The Nematode C. elegans. (ed. W. B. Wood). pp. 281-335. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
47. Webster, B. M., Colombi, P., Jäger, J. and Lusk, C. P. (2014). Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159, 388-401.