Membrane dynamics of dividing cells imaged by lattice light-sheet microscopy

Molecular Biology of the Cell

Volumn 27, Issue 22, 2016, Pages 3418-3435

  Aguet, François ^a,e,f   Upadhyayula, Srigokul ^a,e   Gaudin, Raphaël ^a,e   Chou, Yi Ying ^a   Cocucci, Emanuele ^a   He, Kangmin ^a   Chen, Bi Chang ^b   Mosaliganti, Kishore ^c   Pasham, Mithun ^a   Skillern, Wesley ^a   Legant, Wesley R ^b   Liu, Tsung Li ^b   Findlay, Greg ^a   Marino, Eric ^a   Danuser, Gaudenz ^a   Megason, Sean ^c   Betzig, Eric ^b   Kirchhausen, Tom ^a,d  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e OHIO STATE UNIVERSITY   (United States)

^f RESEARCH CENTER FOR APPLIED SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL GROWTH; CELL MEMBRANE; CELL SURFACE; CELL VOLUME; COATED PIT; CONTROLLED STUDY; CYTOKINESIS; EMBRYO; ENDOCYTOSIS; EYE DEVELOPMENT; FLUORESCENCE MICROSCOPE; HUMAN; IN VIVO STUDY; LATTICE LIGHT SHEET MICROSCOPY; METAPHASE; MICROSCOPY; MITOSIS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; SURFACE AREA; TELOPHASE; ZEBRA FISH; ANIMAL; CELL CYCLE; EMBRYOLOGY; ENDOSOME; FLUORESCENCE MICROSCOPY; METABOLISM; PHYSIOLOGY; PROCEDURES; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE;

ANIMALS; CELL CYCLE; CELL MEMBRANE; CLATHRIN; CYTOKINESIS; ENDOSOMES; IMAGING, THREE-DIMENSIONAL; METAPHASE; MICROSCOPY; MICROSCOPY, FLUORESCENCE; MITOSIS; ZEBRAFISH;

EID: 84994627608     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-03-0164     Document Type: Article

References (50)

1. Aguet F, Antonescu CN, Mettlen M, Schmid SL, Danuser G (2013). Advances in analysis of low signal-To-noise images link dynamin and AP2 to the functions of an endocytic checkpoint. Dev Cell 26, 279-291.
2. Ahle S, Mann A, Eichelsbacher U, Ungewickell E (1988). Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J 7, 919-929.
3. Boucrot E, Kirchhausen T (2007). Endosomal recycling controls plasma membrane area during mitosis. Proc Natl Acad Sci USA 104, 7939-7944.
4. Boucrot E, Kirchhausen T (2008). Mammalian cells change volume during mitosis. PLoS One 3, e1477.
5. Boucrot E, Saffarian S, Massol R, Kirchhausen T, Ehrlich M (2006). Role of lipids and actin in the formation of clathrin-coated pits. Exp Cell Res 312, 4036-4048.
6. Boulant S, Kural C, Zeeh J-C, Ubelmann F, Kirchhausen T (2011). Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13, 1124-1131.
7. Böcking T, Aguet F, Harrison SC, Kirchhausen T (2011). Single-molecule analysis of a molecular disassemblase reveals the mechanism of Hsc70-driven clathrin uncoating. Nat Struct Mol Biol 18, 295-301.
8. Burnham KP, Anderson DR (2002). Model Selection and Multimodel Inference, New York: Springer.
9. Chen B-C, Legant WR, Wang K, Shao L, Milkie DE, Davidson MW, Janetopoulos C, Wu XS, Hammer JA, Liu Z, et al. (2014). Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 346, 1257998.
10. Chou Y-Y, Cuevas C, Carocci M, Stubbs SH, Ma M, Cureton DK, Chao L, Evesson F, He K, Yang PL, et al. (2016). Identification and characterization of a novel broad spectrum virus entry inhibitor. J Virol 90, 4494-4510.
11. Clairmont KB, Boll W, Ericsson M, Kirchhausen T (1997). A role for the hinge/ear domain of the beta chains in the incorporation of AP complexes into clathrin-coated pits and coated vesicles. Cell Mol Life Sci 53, 611-619.
12. Cocucci E, Aguet F, Boulant S, Kirchhausen T (2012). The first five seconds in the life of a clathrin-coated pit. Cell 150, 495-507.
13. Cocucci E, Gaudin R, Kirchhausen T (2014). Dynamin recruitment and membrane scission at the neck of a clathrin-coated pit. Mol Biol Cell 25, 3595-3609.
14. Coupin GT, Muller CD, Rémy-Kristensen A, Kuhry JG (1999). Cell surface membrane homeostasis and intracellular membrane traffic balance in mouse L929 cells. J Cell Sci 112, 2431-2440.
15. Doyon JB, Zeitler B, Cheng J, Cheng AT, Cherone JM, Santiago Y, Lee AH, Vo TD, Doyon Y, Miller JC, et al. (2011). Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat Cell Biol 13, 331-337.
16. Ehrlich M, Boll W, van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T (2004). Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118, 591-605.
17. Fielding AB, Willox AK, Okeke E, Royle SJ (2012). Clathrin-mediated endocytosis is inhibited during mitosis. Proc Natl Acad Sci USA 109, 6572-6577.
18. Fischer-Friedrich E, Hyman AA, Jölicher F, Muller DJ, Helenius J (2014). Quantification of surface tension and internal pressure generated by single mitotic cells. Sci Rep 4, 6213.
19. Gao L, Shao L, Chen B-C, Betzig E (2014). 3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy. Nat Protoc 9, 1083-1101.
20. Grassart A, Cheng AT, Hong SH, Zhang F, Zenzer N, Feng Y, Briner DM, Davis GD, Malkov D, Drubin DG (2014). Actin and dynamin2 dynamics and interplay during clathrin-mediated endocytosis. J Cell Biol 205, 721-735.
21. Grove J, Metcalf DJ, Knight AE, Wavre-Shapton ST, Sun T, Protonotarios ED, Griffin LD, Lippincott-Schwartz J, Marsh M (2014). Flat clathrin lattices: stable features of the plasma membrane. Mol Biol Cell 25, 3581-3594.
22. Grover WH, Bryan AK, Diez-Silva M, Suresh S, Higgins JM, Manalis SR (2011). Measuring single-cell density. Proc Natl Acad Sci USA 108, 10992-10996.
23. Habela CW, Sontheimer H (2007). Cytoplasmic volume condensation is an integral part of mitosis. Cell Cycle 6, 1613-1620.
24. Hong SH, Cortesio CL, Drubin DG (2015). Machine-learning-based analysis in genome-edited cells reveals the efficiency of clathrin-mediated endocytosis. Cell Rep 12, 2121-2130.
25. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S, Schmid SL, Danuser G (2008). Robust single-particle tracking in live-cell time-lapse sequences. Nat Methods 5, 695-702.
26. Kaur S, Fielding AB, Gassner G, Carter NJ, Royle SJ (2014). An unmet actin requirement explains the mitotic inhibition of clathrin-mediated endocytosis. Elife 3, e00829.
27. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995). Stages of embryonic development of the zebrafish. Dev Dyn 203, 253-310.
28. Kirchhausen T (2009). Imaging endocytic clathrin structures in living cells. Trends Cell Biol 19, 596-605.
29. Kozik P, Francis RW, Seaman MNJ, Robinson MS (2010). A screen for endocytic motifs. Traffic 11, 843-855.
30. Kural C, Akatay AA, Gaudin R, Chen B-C, Legant WR, Betzig E, Kirchhausen T (2015). Asymmetric formation of coated pits on dorsal and ventral surfaces at the leading edges of motile cells and on protrusions of immobile cells. Mol Biol Cell 26, 2044-2053.
31. Kural C, Tacheva-Grigorova SK, Boulant S, Cocucci E, Baust T, Duarte D, Kirchhausen T (2012). Dynamics of intracellular clathrin/AP1-And clathrin/AP3-containing carriers. Cell Rep 2, 1111-1119.
32. Liu AP, Aguet F, Danuser G, Schmid SL (2010). Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol 191, 1381-1393.
33. Megason SG (2009). In toto imaging of embryogenesis with confocal time-lapse microscopy. Methods Mol Biol 546, 317-332.
34. Merrifield CJ, Kaksonen M (2014). Endocytic accessory factors and regulation of clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol 6, a016733.
35. Merrifield CJ, Feldman ME, Wan L, Almers W (2002). Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4, 691-698.
36. Merrifield CJ, Perrais D, Zenisek D (2005). Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121, 593-606.
37. Mosaliganti KR, Noche RR, Xiong F, Swinburne IA, Megason SG (2012). ACME: Automated cell morphology extractor for comprehensive reconstruction of cell membranes. PLoS Comput Biol 8, e1002780.
38. Ozlu N, Qureshi MH, Toyoda Y, Renard BY, Mollaoglu G, Ozkan NE, Bulbul S, Poser I, Timm W, Hyman AA, et al. (2014). Quantitative comparison of a human cancer cell surface proteome between interphase and mitosis. EMBO J 34, 251-265.
39. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F (2013). Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8, 2281-2308.
40. Robinson MS (1987). 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies. J Cell Biol 104, 887-895.
41. Saffarian S, Cocucci E, Kirchhausen T (2009). Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7, e1000191.
42. Saffarian S, Kirchhausen T (2008). Differential evanescence nanometry: live-cell fluorescence measurements with 10-nm axial resolution on the plasma membrane. Biophys J 94, 2333-2342.
43. Sanjana NE, Cong L, Zhou Y, Cunniff MM, Feng G, Zhang F (2012). A transcription activator-like effector toolbox for genome engineering. Nat Protoc 7, 171-192.
44. Son S, Kang JH, Oh S, Kirschner MW, Mitchison TJ, Manalis S (2015). Resonant microchannel volume and mass measurements show that suspended cells swell during mitosis. J Cell Biol 211, 757-763.
45. Stewart MP, Helenius J, Toyoda Y, Ramanathan SP, Muller DJ, Hyman AA (2011). Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469, 226-230.
46. Swinburne IA, Mosaliganti KR, Green AA, Megason SG (2015). Improved long-Term imaging of embryos with genetically encoded α-bungarotoxin. PLoS One 10, e0134005.
47. Tacheva-Grigorova SK, Santos AJM, Boucrot E, Kirchhausen T (2013). Clathrin-mediated endocytosis persists during unperturbed mitosis. Cell Rep 4, 659-668.
48. Taylor MJ, Perrais D, Merrifield CJ (2011). A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9, e1000604.
49. Zlotek-Zlotkiewicz E, Monnier S, Cappello G, Le Berre M, Piel M (2015). Optical volume and mass measurements show that mammalian cells swell during mitosis. J Cell Biol 211, 765-774.
50. Zoncu R, Perera RM, Sebastian R, Nakatsu F, Chen H, Balla T, Ayala G, Toomre D, De Camilli PV (2007). Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc Natl Acad Sci USA 104, 3793-3798.