Live-cell imaging in Caenorhabditis elegans reveals the distinct roles of dynamin self-assembly and guanosine triphosphate hydrolysis in the removal of apoptotic cells

Molecular Biology of the Cell

Volumn 21, Issue 4, 2010, Pages 610-629

  He, Bin ^a   Yu, Xiaomeng ^a,c   Margolis, Moran ^b   Liu, Xianghua ^a   Leng, Xiaohong ^a,d   Etzion, Yael ^b   Zheng, Fei ^a   Lu, Nan ^a   Quiocho, Florante A ^a   Danino, Dganit ^b   Zhou, Zheng ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; RAB 7 PROTEIN; RAB PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CELL MATURATION; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; GENE MUTATION; NONHUMAN; OLIGOMERIZATION; PHAGOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN HYDROLYSIS;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL MEMBRANE; DYNAMINS; GUANOSINE TRIPHOSPHATE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PHAGOSOMES; PROTEIN STRUCTURE, TERTIARY; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RATS; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

CAENORHABDITIS ELEGANS; PSEUDOPODA;

EID: 76649095298     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-05-0440     Document Type: Article

References (63)

1. Bashkirov, P. V., Akimov, S. A., Evseev, A. I., Schmid, S. L., Zimmerberg, J., and Frolov, V. A. (2008). GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135, 1276-1286.
2. Bloom, L., and Horvitz, H. R. (1997). The Caenorhabditis elegans gene unc-76 and its human homologs define a new gene family involved in axonal outgrowth and fasciculation. Proc. Natl. Acad. Sci. USA 94, 3414-3419.
3. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94. Cai, H., Reinisch, K., and Ferro-Novick, S. (2007). Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev. Cell 12, 671-682.
4. Clark, S. G., Shurland, D. L., Meyerowitz, E. M., Bargmann, C. I., and van der Bliek, A. M. (1997). A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. Proc. Natl. Acad. Sci. USA 94, 10438-10443.
5. Collins, C. A., and Vallee, R. B. (1986). A microtubule-activated ATPase from sea urchin eggs, distinct from cytoplasmic dynein and kinesin. Proc. Natl. Acad. Sci. USA 83, 4799-4803.
6. Danino, D., Bernheim-Groswasser, A., and Talmon, Y. (2001). Digital cryogenic transmission electron microscopy: an advanced tool for direct imaging of complex fluids colloids and surfaces A. Physicochem. Eng. Asp. 183-185, 113-122.
7. Danino, D., Moon, K. H., and Hinshaw, J. E. (2004). Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. J. Struct. Biol. 147, 259-267.
8. Dawson, J. C., Legg, J. A., and Machesky, L. M. (2006). Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol. 16, 493-498.
9. Desai, A., and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell. Dev. Biol. 13, 83-117.
10. Di, A., Nelson, D. J., Bindokas, V., Brown, M. E., Libunao, F., and Palfrey, H. C. (2003). Dynamin regulates focal exocytosis in phagocytosing macrophages. Mol. Biol. Cell 14, 2016-2028.
11. Evergren, E., Tomilin, N., Vasylieva, E., Sergeeva, V., Bloom, O., Gad, H., Capani, F., and Shupliakov, O. (2004). A pre-embedding immunogold approach for detection of synaptic endocytic proteins in situ. J. Neurosci. Methods 135, 169-174.
12. Gold, E. S., Underhill, D. M., Morrissette, N. S., Guo, J., McNiven, M. A., and Aderem, A. (1999). Dynamin 2 is required for phagocytosis in macrophages. J. Exp. Med. 190, 1849-1856.
13. Grant, B., and Hirsh, D. (1999). Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326.
14. Harrison, R. E., Bucci, C., Vieira, O. V., Schroer, T. A., and Grinstein, S. (2003). Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol. Cell. Biol. 23, 6494-6506.
15. Hiatt, S. M., Shyu, Y. J., Duren, H. M., and Hu, C. D. (2008). Bimolecular fluorescence complementation (BiFC) analysis of protein interactions in Caenorhabditis elegans. Methods 45, 185-191.
16. Hinshaw, J. E. (2000). Dynamin and its role in membrane fission. Annu. Rev. Cell. Dev. Biol. 16, 483-519.
17. Hinshaw, J. E., and Schmid, S. L. (1995). Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190-192.
18. Hoppins, S., and Nunnari, J. (2009). The molecular mechanism of mitochondrial fusion. Biochim. Biophys. Acta 1793, 20-26.
19. Hu, C. D., Chinenov, Y., and Kerppola, T. K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9, 789-798.
20. Jin, Y. (1999). Transformation. In: C. elegans, a Practical Approach, ed. I. A. Hope, Oxford, United Kingdom: Oxford University Press, 69-96.
21. Kavran, J. M., Klein, D. E., Lee, A., Falasca, M., Isakoff, S. J., Skolnik, E. Y., and Lemmon, M. A. (1998). Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J. Biol. Chem. 273, 30497-30508.
22. Kelly, W. G., Xu, S., Montgomery, M. K., and Fire, A. (1997). Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene. Genetics 146, 227-238.
23. Kerppola, T. K. (2006). Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat. Protoc. 1, 1278-1286.
24. Kinchen, J. M., Doukoumetzidis, K., Almendinger, J., Stergiou, L., Tosello-Trampont, A., Sifri, C. D., Hengartner, M. O., and Ravichandran, K. S. (2008).
25. A pathway for phagosome maturation during engulfment of apoptotic cells. Nat. Cell Biol. 10, 556-566.
26. Kinchen, J. M., and Ravichandran, K. S. (2008). Phagosome maturation: going through the acid test. Nat. Rev. Mol. Cell Biol. 9, 781-795.
27. Kitano, M., Nakaya, M., Nakamura, T., Nagata, S., and Matsuda, M. (2008). Imaging of Rab5 activity identifies essential regulators for phagosome maturation. Nature 453, 241-245.
28. Klein, D. E., Lee, A., Frank, D. W., Marks, M. S., and Lemmon, M. A. (1998). The pleckstrin homology domains of dynamin isoforms require oligomerization for high affinity phosphoinositide binding. J. Biol. Chem. 273, 27725-27733.
29. Konikoff, F. M., Danino, D., Weihs, D., Rubin, M., and Talmon, Y. (2000). Microstructural evolution of lipid aggregates in nucleating model and human biles visualized by cryogenic transmission electron microscopy. Hepatology 31, 261-268.
30. Labrousse, A. M., Shurland, D. L., and van der Bliek, A. M. (1998). Contribution of the GTPase domain to the subcellular localization of dynamin in the nematode Caenorhabditis elegans. Mol. Biol. Cell 9, 3227-3239.
31. Lu, N., Yu, X., He, X., and Zhou, Z. (2009). Detecting apoptotic cells and monitoring their clearance in the nematode Caenorhabditis elegans. Methods Mol. Biol. 559, 357-370.
32. Metzstein, M. M., Stanfield, G. M., and Horvitz, H. R. (1998). Genetics of programmed cell death in C. elegans: past, present and future. Trends Genet. 14, 410-416.
33. Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K., and Miyawaki, A. (2002). A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90.
34. Narayanan, R., Leonard, M., Song, B. D., Schmid, S. L., and Ramaswami, M. (2005). An internal GAP domain negatively regulates presynaptic dynamin in vivo: a two-step model for dynamin function. J. Cell Biol. 169, 117-126.
35. Niemann, H. H., Knetsch, M. L., Scherer, A., Manstein, D. J., and Kull, F. J. (2001). Crystal structure of a dynamin GTPase domain in both nucleotide-free and GDP-bound forms. EMBO J. 20, 5813-5821.
36. Orth, J. D., and McNiven, M. A. (2003). Dynamin at the actin-membrane interface. Curr. Opin. Cell Biol. 15, 31-39.
37. Peters, C., Baars, T. L., Buhler, S., and Mayer, A. (2004). Mutual control of membrane fission and fusion proteins. Cell 119, 667-678.
38. Praefcke, G. J., and McMahon, H. T. (2004). The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5, 133-147.
39. Pucadyil, T. J., and Schmid, S. L. (2008). Real-time visualization of dynamin-catalyzed membrane fission and vesicle release. Cell 135, 1263-1275.
40. Ramachandran, R., Surka, M., Chappie, J. S., Fowler, D. M., Foss, T. R., Song, B. D., and Schmid, S. L. (2007). The dynamin middle domain is critical for tetramerization and higher-order self-assembly. EMBO J. 26, 559-566.
41. Riddle, D. L., Blumenthal, T., Meyer, B. J., and Priess, J. R. (eds.) (1997). C. elegans II, Plainview, NY: Cold Spring Harbor Laboratory Press.
42. Salim, K., et al. (1996). Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J 15, 6241-6250.
43. Savill, J., and Fadok, V. (2000). Corpse clearance defines the meaning of cell death. Nature 407, 784-788.
44. Schmid, S. L., McNiven, M. A., and De Camilli, P. (1998). Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10, 504-512.
45. Sever, S., Muhlberg, A. B., and Schmid, S. L. (1999). Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481-486.
46. Shyu, Y. J., Hiatt, S. M., Duren, H. M., Ellis, R. E., Kerppola, T. K., and Hu, C. D. (2008). Visualization of protein interactions in living Caenorhabditis elegans using bimolecular fluorescence complementation analysis. Nat. Protoc. 3, 588-596.
47. Song, B. D., Leonard, M., and Schmid, S. L. (2004). Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin-mediated endocytosis. J. Biol. Chem. 279, 40431-40436.
48. Stowell, M. H., Marks, B., Wigge, P., and McMahon, H. T. (1999). Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat. Cell Biol. 1, 27-32.
49. Stringham, E. G., Dixon, D. K., Jones, D., and Candido, E. P. (1992). Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol. Biol. Cell 3, 221-233.
50. Sulston, J. E., and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156.
51. Sulston, J. E., Schierenberg, E., White, J. G., and Thomson, N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119.
52. Sweitzer, S. M., and Hinshaw, J. E. (1998). Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029.
53. Szafer, E., Rotman, M., and Cassel, D. (2001). Regulation of GTP hydrolysis on ADP-ribosylation factor-1 at the Golgi membrane. J. Biol. Chem. 276, 47834-47839.
54. Takei, K., Haucke, V., Slepnev, V., Farsad, K., Salazar, M., Chen, H., and De Camilli, P. (1998). Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94, 131-141.
55. Takei, K., McPherson, P. S., Schmid, S. L., and De Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374, 186-190.
56. Touret, N., et al. (2005). Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 123, 157-170.
57. Vieira, O. V., Botelho, R. J., and Grinstein, S. (2002). Phagosome maturation: aging gracefully. Biochem. J. 366, 689-704.
58. Warnock, D. E., Hinshaw, J. E., and Schmid, S. L. (1996). Dynamin self-assembly stimulates its GTPase activity. J. Biol. Chem. 271, 22310-22314.
59. Yu, X., Lu, N., and Zhou, Z. (2008). Phagocytic receptor CED-1 initiates a signaling pathway for degrading engulfed apoptotic cells. PLoS Biol. 6, e61.
60. Yu, X., Odera, S., Chuang, C. H., Lu, N., and Zhou, Z. (2006). C. elegans Dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev. Cell 10, 743-757.
61. Zheng, J., Cahill, S. M., Lemmon, M. A., Fushman, D., Schlessinger, J., and Cowburn, D. (1996). Identification of the binding site for acidic phospholipids on the pH domain of dynamin: implications for stimulation of GTPase activity. J. Mol. Biol. 255, 14-21.
62. Zhou, Z., Hartwieg, E., and Horvitz, H. R. (2001b). CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104, 43-56.
63. Zhou, Z., and Yu, X. (2008). Phagosome maturation during the removal of apoptotic cells: receptors lead the way. Trends Cell Biol. 18, 474-485.