Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes

Nature Cell Biology

Volumn 13, Issue 10, 2011, Pages 1252-1258

  Yi, Kexi ^a   Unruh, Jay R ^a   Deng, Manqi ^b   Slaughter, Brian D ^a   Rubinstein, Boris ^a   Li, Rong ^a,c  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; RAN PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICAL CAP; CYTOPLASM; ENZYME INHIBITION; FEMALE; IMAGE ANALYSIS; MEIOSIS; MEIOSIS SPINDLE; MOUSE; NONHUMAN; OOCYTE; OOCYTE CORTEX; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN METABOLISM; SPECTROSCOPY;

ACTIN CYTOSKELETON; ACTIN-RELATED PROTEIN 2; ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTIN-RELATED PROTEIN 3; ANIMALS; CELLS, CULTURED; CYTOPLASMIC STREAMING; FEMALE; FOURIER ANALYSIS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; INDOLES; KYMOGRAPHY; MEIOSIS; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, VIDEO; MITOTIC SPINDLE APPARATUS; MORPHOLINOS; MYOSIN TYPE II; NOCODAZOLE; OOCYTES; PROTEIN TRANSPORT; RAN GTP-BINDING PROTEIN; RECOMBINANT FUSION PROTEINS; TIME FACTORS;

MAMMALIA;

EID: 80053488949     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2320     Document Type: Article

References (42)

1. Sathananthan, A. H. Ultrastructure of the human egg. Hum. Cell 10, 21-38 (1997).
2. Webb, M., Howlett, S. K. & Maro, B. Parthenogenesis and cytoskeletal organization in ageing mouse eggs. J. Embryol. Exp. Morphol. 95, 131-145 (1986). (Pubitemid 16037128)
3. Kim, N. H., Moon, S. J., Prather, R. S. & Day, B. N. Cytoskeletal alteration in aged porcine oocytes and parthenogenesis. Mol. Reprod. Dev. 43, 513-518 (1996). (Pubitemid 26110817)
4. Maro, B., Johnson, M. H., Webb, M. & Flach, G. Mechanism of polar body formation in the mouse oocyte: an interaction between the chromosomes, the cytoskeleton and the plasma membrane. J. Embryol. Exp. Morphol. 92, 11-32 (1986). (Pubitemid 16133521)
5. Longo, F. J. & Chen, D. Y. Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. Dev. Biol. 107, 382-394 (1985). (Pubitemid 15110942)
6. Verlhac, M. H., Lefebvre, C., Guillaud, P., Rassinier, P. & Maro, B. Asymmetric division in mouse oocytes: with or without Mos. Curr. Biol. 10, 1303-1306 (2000).
7. Leader, B. et al. Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat. Cell Biol. 4, 921-928 (2002). (Pubitemid 35469421)
8. Deng, M., Suraneni, P., Schultz, R. M. & Li, R. The Ran GTPase mediates chromatin signaling to control cortical polarity during polar body extrusion in mouse oocytes. Dev. Cell 12, 301-308 (2007). (Pubitemid 46172900)
9. Deng, M. & Li, R. Sperm chromatin-induced ectopic polar body extrusion in mouse eggs after ICSI and delayed egg activation. PLoS One 4, e7171 (2009).
10. Brunet, S. & Maro, B. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 130, 801-811 (2005). (Pubitemid 41830090)
11. Siller, K. H. & Doe, C. Q. Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11, 365-374 (2009).
12. Zhu, Z. Y. et al. Rotation of meiotic spindle is controlled by microfilaments in mouse oocytes. Biol. Reprod. 68, 943-946 (2003).
13. Halet, G. & Carroll, J. Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev. Cell 12, 309-317 (2007). (Pubitemid 46172904)
14. Ayscough, K. R. et al. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137, 399-416 (1997). (Pubitemid 27181293)
15. Straight, A. F. et al. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299, 1743-1747 (2003). (Pubitemid 36337202)
16. Nolen, B. J. et al. Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034 (2009).
17. Goley, E. D. & Welch, M. D. The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7, 713-726 (2006). (Pubitemid 44450456)
18. Campellone, K. G. & Welch, M. D. A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 11, 237-251 (2010).
19. Padrick, S. B. et al. Hierarchical regulation of WASP/WAVE proteins. Mol. Cell 32, 426-438 (2008).
20. Higgs, H. N., Blanchoin, L. & Pollard, T. D. Influence of the C terminus of Wiskott-Aldrich syndrome protein (WASp) and the Arp2/3 complex on actin polymerization. Biochemistry 38, 15212-15222 (1999).
21. Wilde, A. et al. stimulates spindle assembly by altering microtubule dynamics and the balance of motor activities. Nat. Cell Biol. 3, 221-227 (2001). (Pubitemid 32201316)
22. Li, H., Guo, F., Rubinstein, B. & Li, R. Actin-driven chromosomal motility leads to symmetry breaking in mammalian meiotic oocytes. Nat. Cell Biol. 10, 1301-1308 (2008).
23. Schuh, M. & Ellenberg, J. A new model for asymmetric spindle positioning in mouse oocytes. Curr. Biol. 18, 1986-1992 (2008).
24. Azoury, J. et al. Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr. Biol. 18, 1514-1519 (2008).
25. Burkel, B. M., von Dassow, G. & Bement, W. M. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil. Cytoskeleton 64, 822-832 (2007). (Pubitemid 350035031)
26. Riedl, J. et al. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607 (2008). (Pubitemid 351911864)
27. Hebert, B., Costantino, S. & Wiseman, P. W. Spatiotemporal image correlation spectroscopy (STICS) theory, verification, and application to protein velocity mapping in living CHO cells. Biophys. J. 88, 3601-3614 (2005). (Pubitemid 40586608)
28. Cramer, L. P. Molecular mechanism of actin-dependent retrograde flow in lamellipodia of motile cells. Front. Biosci. 2, d260-d270 (1997).
29. Bubb, M. R., Senderowicz, A. M., Sausville, E. A., Duncan, K. L. & Korn, E. D. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J. Biol. Chem. 269, 14869-14871 (1994). (Pubitemid 24198320)
30. Chen, H., Bernstein, B. W. & Bamburg, J. R. Regulating actin-filament dynamics in vivo. Trends Biochem. Sci. 25, 19-23 (2000). (Pubitemid 30060425)
31. Keren, K., Yam, P. T., Kinkhabwala, A., Mogilner, A. & Theriot, J. A. Intracellular fluid flow in rapidly moving cells. Nat. Cell Biol. 11, 1219-1224 (2009).
32. Miao, Y. L., Kikuchi, K., Sun, Q. Y. & Schatten, H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum. Reprod. Update 15, 573-585 (2009).
33. Cohen, Y. et al. Spindle imaging: a new marker for optimal timing of ICSI? Hum. Reprod. 19, 649-654 (2004). (Pubitemid 38344530)
34. Moon, J. H. et al. Visualization of the metaphase II meiotic spindle in living human oocytes using the Polscope enables the prediction of embryonic developmental competence after ICSI. Hum. Reprod. 18, 817-820 (2003).
35. Zamir, E. A., Czirok, A., Rongish, B. J. & Little, C. D. A digital image-based method for computational tissue fate mapping during early avian morphogenesis. Ann. Biomed. Eng. 33, 854-865 (2005). (Pubitemid 40878492)
36. Ponti, A., Vallotton, P., Salmon, W. C., Waterman-Storer, C. M. & Danuser, G. Computational analysis of F-actin turnover in cortical actin meshworks using fluorescent speckle microscopy. Biophys. J. 84, 3336-3352 (2003). (Pubitemid 36531781)
37. Pudasaini, S. P., Hsiau, S-S., Wang, Y. & Hutter, K. Velocity measurements in dry granular avalanches using particle image velocimetry technique and comparison with theoretical predictions. Phys. Fluids 17, 093301 (2005).
38. Lueptow, R. M., Akonur, A. & Shinbrot, T. PIV for granular flows. Exp. Fluids 183-186 (1998).
39. Rossow, M., Mantulin, W. W. & Gratton, E. Spatiotemporal image correlation spectroscopy measurements offlow demonstrated in micro-uidic channels. J. Biomed. Opt. 14, 024014 (2009).
40. Rossow, M. J., Mantulin, W. W. & Gratton, E. Scanning laser image correlation for measurement offlow. J. Biomed. Opt. 15, 026003 (2010).
41. Sbalzarini, I. F. & Koumoutsakos, P. Feature point tracking and trajectory analysis for video imaging in cell biology. J. Struct. Biol. 151, 182-195 (2005). (Pubitemid 41074826)
42. Landau, L. D. & Lifshitz, E. M. Course of Theoretical Physics Vol. 6 (Pergamon, 1987