The basal position of nuclei is one pre-requisite for asymmetric cell divisions in the early mouse embryo

Developmental Biology

Volumn 392, Issue 2, 2014, Pages 133-140

  Ajduk, Anna ^a,c   Biswas Shivhare, Sourima ^a,d   Zernicka Goetz, Magdalena ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF WARSAW   (Poland)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cell polarity; Cytoskeleton; Division plane; Mammalian embryo; Preimplantation development

Indexed keywords

TRANSCRIPTION FACTOR CDX2;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL COUNT; CELL CYCLE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL NUCLEUS; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; MICROTUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

MAMMALIA;

CELL POLARITY; CYTOSKELETON; DIVISION PLANE; MAMMALIAN EMBRYO; PREIMPLANTATION DEVELOPMENT;

ANIMALS; ASYMMETRIC CELL DIVISION; CELL NUCLEUS; CELL POLARITY; CLEAVAGE STAGE, OVUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; MICROINJECTIONS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; PROTEIN KINASE C; TRANSCRIPTION FACTORS;

EID: 84904396372     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.05.009     Document Type: Article

References (46)

1. Ajduk A., Ilozue T., Windsor S., Yu Y., Seres K.B., Bomphrey R.J., Tom B.D., Swann K., Thomas A., Graham C., Zernicka-Goetz M. Rhythmic actomyosin-driven contractions induced by sperm entry predict mammalian embryo viability. Nat. Commun. 2011, 2:417.
2. Bischoff M., Parfitt D.E., Zernicka-Goetz M. Formation of the embryonic-abembryonic axis of the mouse blastocyst: relationships between orientation of early cleavage divisions and pattern of symmetric/asymmetric divisions. Development 2008, 135:953-962.
3. Cai Y., Singh B.B., Aslanukov A., Zhao H., Ferreira P.A. The docking of kinesins, KIF5B and KIF5C, to Ran-binding protein 2 (RanBP2) is mediated via a novel RanBP2 domain. J. Biol. Chem. 2001, 276:41594-41602.
4. Chawengsaksophak K., James R., Hammond V.E., Kontgen F., Beck F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 1997, 386:84-87.
5. Crisp M., Liu Q., Roux K., Rattner J.B., Shanahan C., Burke B., Stahl P.D., Hodzic D. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 2006, 172:41-53.
6. Dietrich J.E., Hiiragi T. Stochastic patterning in the mouse pre-implantation embryo. Development 2007, 134:4219-4231.
7. Dujardin D.L., Vallee R.B. Dynein at the cortex. Curr. Opin. Cell Biol. 2002, 14:44-49.
8. Gao N., White P., Kaestner K.H. Establishment of intestinal identity and epithelial-mesenchymal signaling by Cdx2. Dev. Cell 2009, 16:588-599.
9. Gonczy P. Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell Biol. 2008, 9:355-366.
10. Gong X., Ming X., Deng P., Jiang Y. Mechanisms regulating the nuclear translocation of p38 MAP kinase. J. Cell Biochem. 2010, 110:1420-1429.
11. Hadjantonakis A.K., Papaioannou V.E. Dynamic in vivo imaging and cell tracking using a histone fluorescent protein fusion in mice. BMC Biotechnol. 2004, 4:33.
12. Hirokawa N. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 1998, 279:519-526.
13. Jedrusik A., Bruce A.W., Tan M.H., Leong D.E., Skamagki M., Yao M., Zernicka-Goetz M. Maternally and zygotically provided Cdx2 have novel and critical roles for early development of the mouse embryo. Dev. Biol. 2010, 344:66-78.
14. Jedrusik A., Parfitt D.E., Guo G., Skamagki M., Grabarek J.B., Johnson M.H., Robson P., Zernicka-Goetz M. Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev. 2008, 22:2692-2706.
15. Johnson M.H., Ziomek C.A. The foundation of two distinct cell lineages within the mouse morula. Cell 1981, 24:71-80.
16. Johnson M.H., Ziomek C.A. Induction of polarity in mouse 8-cell blastomeres: specificity, geometry, and stability. J. Cell Biol. 1981, 91:303-308.
17. Kaneda M., Tang F., O'Carroll D., Lao K., Surani M.A. Essential role for Argonaute2 protein in mouse oogenesis. Epigenet. Chromat. 2009, 2:9.
18. Laan L., Pavin N., Husson J., Romet-Lemonne G., van Duijn M., Lopez M.P., Vale R.D., Julicher F., Reck-Peterson S.L., Dogterom M. Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters. Cell 2012, 148:502-514.
19. Laan L., Roth S., Dogterom M. End-on microtubule-dynein interactions and pulling-based positioning of microtubule organizing centers. Cell Cycle 2012, 11:3750-3757.
20. McDole K., Zheng Y. Generation and live imaging of an endogenous Cdx2 reporter mouse line. Genesis 2012, 50:775-782.
21. McGee M.D., Rillo R., Anderson A.S., Starr D.A. UNC-83 IS a KASH protein required for nuclear migration and is recruited to the outer nuclear membrane by a physical interaction with the SUN protein UNC-84. Mol. Biol. Cell 2006, 17:1790-1801.
22. Morris S.A., Teo R.T., Li H., Robson P., Glover D.M., Zernicka-Goetz M. Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc. Natl. Acad. Sci. USA 2010, 107:6364-6369.
23. Neumuller R.A., Knoblich J.A. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 2009, 23:2675-2699.
24. Nguyen-Ngoc T., Afshar K., Gonczy P. Coupling of cortical dynein and G alpha proteins mediates spindle positioning in Caenorhabditis elegans. Nat. Cell Biol. 2007, 9:1294-1302.
25. Niclas J., Allan V.J., Vale R.D. Cell cycle regulation of dynein association with membranes modulates microtubule-based organelle transport. J. Cell Biol. 1996, 133:585-593.
26. Niwa H., Toyooka Y., Shimosato D., Strumpf D., Takahashi K., Yagi R., Rossant J. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005, 123:917-929.
27. Padmakumar V.C., Libotte T., Lu W., Zaim H., Abraham S., Noegel A.A., Gotzmann J., Foisner R., Karakesisoglou I. The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J. Cell Sci. 2005, 118:3419-3430.
28. Parfitt D.E., Zernicka-Goetz M. Epigenetic modification affecting expression of cell polarity and cell fate genes to regulate lineage specification in the early mouse embryo. Mol. Biol. Cell 2010, 21:2649-2660.
29. Park D.H., Rose L.S. Dynamic localization of LIN-5 and GPR-1/2 to cortical force generation domains during spindle positioning. Dev. Biol. 2008, 315:42-54.
30. Payne C., Rawe V., Ramalho-Santos J., Simerly C., Schatten G. Preferentially localized dynein and perinuclear dynactin associate with nuclear pore complex proteins to mediate genomic union during mammalian fertilization. J. Cell Sci. 2003, 116:4727-4738.
31. Plusa B., Frankenberg S., Chalmers A., Hadjantonakis A.K., Moore C.A., Papalopulu N., Papaioannou V.E., Glover D.M., Zernicka-Goetz M. Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. J. Cell Sci. 2005, 118:505-515.
32. Ralston A., Rossant J. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev. Biol. 2008, 313:614-629.
33. Reeve W.J., Kelly F.P. Nuclear position in the cells of the mouse early embryo. J. Embryol. Exp. Morphol. 1983, 75:117-139.
34. Reeve W.J., Ziomek C.A. Distribution of microvilli on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction. J. Embryol. Exp. Morphol. 1981, 62:339-350.
35. Skamagki M., Wicher K.B., Jedrusik A., Ganguly S., Zernicka-Goetz M. Asymmetric localization of Cdx2 mRNA during the first cell-fate decision in early mouse development. Cell Rep. 2013, 3:442-457.
36. Splinter D., Tanenbaum M.E., Lindqvist A., Jaarsma D., Flotho A., Yu K.L., Grigoriev I., Engelsma D., Haasdijk E.D., Keijzer N., Demmers J., Fornerod M., Melchior F., Hoogenraad C.C., Medema R.H., Akhmanova A. Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol. 2010, 8:e1000350.
37. Srinivasan D.G., Fisk R.M., Xu H., van den Heuvel S. A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C elegans. Genes Dev. 2003, 17:1225-1239.
38. Strumpf D., Mao C.A., Yamanaka Y., Ralston A., Chawengsaksophak K., Beck F., Rossant J. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005, 132:2093-2102.
39. Sutherland A.E., Speed T.P., Calarco P.G. Inner cell allocation in the mouse morula: the role of oriented division during fourth cleavage. Dev. Biol. 1990, 137:13-25.
40. Suzuki A., Ohno S. The PAR-aPKC system: lessons in polarity. J. Cell Sci. 2006, 119:979-987.
41. Tapley E.C., Starr D.A. Connecting the nucleus to the cytoskeleton by SUN-KASH bridges across the nuclear envelope. Curr. Opin. Cell Biol. 2013, 25:57-62.
42. Tarkowski A.K., Wroblewska J. Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J. Embryol. Exp. Morphol. 1967, 18:155-180.
43. Vinot S., Le T., Ohno S., Pawson T., Maro B., Louvet-Vallee S. Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. Dev. Biol. 2005, 282:307-319.
44. Yamanaka Y., Ralston A., Stephenson R.O., Rossant J. Cell and molecular regulation of the mouse blastocyst. Dev. Dyn. 2006, 235:2301-2314.
45. Zernicka-Goetz M., Morris S.A., Bruce A.W. Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo. Nat. Rev. Genet. 2009, 10:467-477.
46. Zernicka-Goetz M., Pines J., McLean Hunter S., Dixon J.P., Siemering K.R., Haseloff J., Evans M.J. Following cell fate in the living mouse embryo. Development 1997, 124:1133-1137.