Getting to know your neighbor: Cell polarization in early embryos

Journal of Cell Biology

Volumn 206, Issue 7, 2014, Pages 823-832

  Nance, Jeremy ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE C; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 6; UNCLASSIFIED DRUG; WNT PROTEIN;

BLASTOMA; CAENORHABDITIS ELEGANS; CELL FATE; CELL POLARITY; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM CELL; HIPPO SIGNALING; MORPHOGENESIS; MOUSE EMBRYO; NONHUMAN; RADIAL POLARIZATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; XENOPUS LAEVIS; ANIMAL; ANIMAL EMBRYO; CELL ADHESION; CELL COMMUNICATION; CYTOLOGY; HUMAN; PHYSIOLOGY;

ANIMALS; BLASTOMERES; CELL ADHESION; CELL COMMUNICATION; CELL POLARITY; EMBRYO, MAMMALIAN; EPITHELIAL CELLS; HUMANS; SIGNAL TRANSDUCTION;

EID: 84907718541     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201407064     Document Type: Review

References (83)

1. Aceto, D., M. Beers, and K.J. Kemphues. 2006. Interaction of PAR-6 with CDC-42 is required for maintenance but not establishment of PAR asymmetry in C. elegans. Dev. Biol. 299:386-397. http://dx.doi.org/10.1016/j.ydbio.2006.08.002
2. Achilleos, A., A.M. Wehman, and J. Nance. 2010. PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins during C. elegans intestinal epithelial cell polarization. Development. 137:1833- 1842. http://dx.doi.org/10.1242/dev.047647
3. Alarcon, V.B. 2010. Cell polarity regulator PARD6B is essential for trophectoderm formation in the preimplantation mouse embryo. Biol. Reprod. 83:347-358. http://dx.doi.org/10.1095/biolreprod.110.084400
4. Anani, S., S. Bhat, N. Honma-Yamanaka, D. Krawchuk, and Y. Yamanaka. 2014. Initiation of Hippo signaling is linked to polarity rather than to cell position in the pre-implantation mouse embryo. Development. 141:2813- 2824. http://dx.doi.org/10.1242/dev.107276
5. Anderson, D.C., J.S. Gill, R.M. Cinalli, and J. Nance. 2008. Polarization of the C. elegans embryo by RhoGAP-mediated exclusion of PAR-6 from cell contacts. Science. 320:1771-1774. http://dx.doi.org/10.1126/science.1156063
6. Bilder, D., M. Schober, and N. Perrimon. 2003. Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat. Cell Biol. 5:53-58. http://dx.doi.org/10.1038/ncb897
7. Bluemink, J.G., and S.W. de Laat. 1973. New membrane formation during cytokinesis in normal and cytochalasin B-treated eggs of Xenopus laevis. I. Electron microscope observations. J. Cell Biol. 59:89-108. http://dx.doi.org/10.1083/jcb.59.1.89
8. Cardellini, P., G. Davanzo, and S. Citi. 1996. Tight junctions in early amphibian development: detection of junctional cingulin from the 2-cell stage and its localization at the boundary of distinct membrane domains in dividing blastomeres in low calcium. Dev. Dyn. 207:104-113. http://dx.doi.org/10.1002/(SICI)1097-0177(199609)207:1<104::AID-AJA10<3.0.CO;2-0
9. Chalmers, A.D., D. Welchman, and N. Papalopulu. 2002. Intrinsic differences between the superficial and deep layers of the Xenopus ectoderm control primary neuronal differentiation. Dev. Cell. 2:171-182. http://dx.doi.org/10.1016/S1534-5807(02)00113-2
10. Chalmers, A.D., B. Strauss, and N. Papalopulu. 2003. Oriented cell divisions asymmetrically segregate aPKC and generate cell fate diversity in the early Xenopus embryo. Development. 130:2657-2668. http://dx.doi.org/10.1242/dev.00490
11. Chalmers, A.D., M. Pambos, J. Mason, S. Lang, C. Wylie, and N. Papalopulu. 2005. aPKC, Crumbs3 and Lgl2 control apicobasal polarity in early vertebrate development. Development. 132:977-986. http://dx.doi.org/10.1242/dev.01645
12. Chan, E., and J. Nance. 2013. Mechanisms of CDC-42 activation during contactinduced cell polarization. J. Cell Sci. 126:1692-1702. http://dx.doi.org/10.1242/jcs.124594
13. Cherfils, J., and M. Zeghouf. 2013. Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol. Rev. 93:269-309. http://dx.doi.org/10.1152/physrev.00003.2012
14. Cockburn, K., S. Biechele, J. Garner, and J. Rossant. 2013. The Hippo pathway member Nf2 is required for inner cell mass specification. Curr. Biol. 23:1195-1201. http://dx.doi.org/10.1016/j.cub.2013.05.044
15. Danilchik, M.V., W.C. Funk, E.E. Brown, and K. Larkin. 1998. Requirement for microtubules in new membrane formation during cytokinesis of Xenopus embryos. Dev. Biol. 194:47-60. http://dx.doi.org/10.1006/dbio.1997.8815
16. Danilchik, M.V., S.D. Bedrick, E.E. Brown, and K. Ray. 2003. Furrow microtubules and localized exocytosis in cleaving Xenopus laevis embryos. J. Cell Sci. 116:273-283. http://dx.doi.org/10.1242/jcs.00217
17. Dard, N., T. Le, B. Maro, and S. Louvet-Vallee. 2009. Inactivation of aPKClambda reveals a context dependent allocation of cell lineages in preimplantation mouse embryos. PLoS ONE. 4:e7117. http://dx.doi.org/10.1371/journal.pone.0007117
18. Dollar, G.L., U. Weber, M. Mlodzik, and S.Y. Sokol. 2005. Regulation of Lethal giant larvae by Dishevelled. Nature. 437:1376-1380. http://dx.doi.org/10.1038/nature04116
19. Ducibella, T., T. Ukena, M. Karnovsky, and E. Anderson. 1977. Changes in cell surface and cortical cytoplasmic organization during early embryogenesis in the preimplantation mouse embryo. J. Cell Biol. 74:153-167. http://dx.doi.org/10.1083/jcb.74.1.153
20. Etemad-Moghadam, B., S. Guo, and K.J. Kemphues. 1995. Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell. 83:743-752. http://dx.doi.org/10.1016/0092-8674(95)90187-6
21. Feng, B., H. Schwarz, and S. Jesuthasan. 2002. Furrow-specific endocytosis during cytokinesis of zebrafish blastomeres. Exp. Cell Res. 279:14-20. http://dx.doi.org/10.1006/excr.2002.5579
22. Fesenko, I., T. Kurth, B. Sheth, T.P. Fleming, S. Citi, and P. Hausen. 2000. Tight junction biogenesis in the early Xenopus embryo. Mech. Dev. 96:51-65. http://dx.doi.org/10.1016/S0925-4773(00)00368-3
23. Fleming, T.P., J. McConnell, M.H. Johnson, and B.R. Stevenson. 1989. Development of tight junctions de novo in the mouse early embryo: control of assembly of the tight junction-specific protein, ZO-1. J. Cell Biol. 108:1407-1418. http://dx.doi.org/10.1083/jcb.108.4.1407
24. Gawantka, V., H. Ellinger-Ziegelbauer, and P. Hausen. 1992. β 1-integrin is a maternal protein that is inserted into all newly formed plasma membranes during early Xenopus embryogenesis. Development. 115:595-605.
25. Gotta, M., M.C. Abraham, and J. Ahringer. 2001. CDC-42 controls early cell polarity and spindle orientation in C. elegans. Curr. Biol. 11:482-488. http://dx.doi.org/10.1016/S0960-9822(01)00142-7
26. Gunzel, D., and M. Fromm. 2012. Claudins and other tight junction proteins. Compr Physiol. 2:1819-1852.
27. Hao, Y., L. Boyd, and G. Seydoux. 2006. Stabilization of cell polarity by the C. elegans RING protein PAR-2. Dev. Cell. 10:199-208. http://dx.doi.org/10.1016/j.devcel.2005.12.015
28. Harris, K.P., and U. Tepass. 2010a. Cdc42 and vesicle trafficking in polarized cells. Traffic. 11:1272-1279. http://dx.doi.org/10.1111/j.1600-0854.2010.01102.x
29. Harris, T.J., and M. Peifer. 2004. Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila. J. Cell Biol. 167:135-147. http://dx.doi.org/10.1083/jcb.200406024
30. Harris, T.J., and U. Tepass. 2010b. Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11:502-514. http://dx.doi.org/10.1038/nrm2927
31. Herrera, A., M. Saade, A. Menendez, E. Marti, and S. Pons. 2014. Sustained Wnt/β-catenin signalling causes neuroepithelial aberrations through the accumulation of aPKC at the apical pole. Nat. Commun. 5:4168. http://dx.doi.org/10.1038/ncomms5168
32. Hirate, Y., and H. Sasaki. 2014. The role of angiomotin phosphorylation in the Hippo pathway during preimplantation mouse development. Tissue Barriers. 2:e28127. http://dx.doi.org/10.4161/tisb.28127
33. Hirate, Y., S. Hirahara, K. Inoue, A. Suzuki, V.B. Alarcon, K. Akimoto, T. Hirai, T. Hara, M. Adachi, K. Chida, et al. 2013. Polarity-dependent distribution of angiomotin localizes Hippo signaling in preimplantation embryos. Curr. Biol. 23:1181-1194. http://dx.doi.org/10.1016/j.cub.2013.05.014
34. Huang, Y.L., and C. Niehrs. 2014. Polarized Wnt signaling regulates ectodermal cell fate in Xenopus. Dev. Cell. 29:250-257. http://dx.doi.org/10.1016/j.devcel.2014.03.015
35. Hung, T.J., and K.J. Kemphues. 1999. PAR-6 is a conserved PDZ domaincontaining protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development. 126:127-135.
36. Hurov, J.B., J.L. Watkins, and H. Piwnica-Worms. 2004. Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Curr. Biol. 14:736-741. http://dx.doi.org/10.1016/j.cub.2004.04.007
37. Jesuthasan, S. 1998. Furrow-associated microtubule arrays are required for the cohesion of zebrafish blastomeres following cytokinesis. J. Cell Sci. 111:3695-3703.
38. Johnson, M.H. 2009. From mouse egg to mouse embryo: polarities, axes, and tissues. Annu. Rev. Cell Dev. Biol. 25:483-512. http://dx.doi.org/10.1146/annurev.cellbio.042308.113348
39. Johnson, M.H., and C.A. Ziomek. 1981. Induction of polarity in mouse 8-cell blastomeres: specificity, geometry, and stability. J. Cell Biol. 91:303-308. http://dx.doi.org/10.1083/jcb.91.1.303
40. Lecuit, T., and E. Wieschaus. 2000. Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo. J. Cell Biol. 150:849-860. http://dx.doi.org/10.1083/jcb.150.4.849
41. Lee, J.Y., and B. Goldstein. 2003. Mechanisms of cell positioning during C. elegans gastrulation. Development. 130:307-320. http://dx.doi.org/10.1242/dev.00211
42. Lehtonen, E., and R.A. Badley. 1980. Localization of cytoskeletal proteins in preimplantation mouse embryos. J. Embryol. Exp. Morphol. 55:211-225.
43. Leung, C.Y., and M. Zernicka-Goetz. 2013. Angiomotin prevents pluripotent lineage differentiation in mouse embryos via Hippo pathway-dependent and -independent mechanisms. Nat. Commun. 4:2251. http://dx.doi.org/10.1038/ncomms3251
44. Lorthongpanich, C., D.M. Messerschmidt, S.W. Chan, W. Hong, B.B. Knowles, and D. Solter. 2013. Temporal reduction of LATS kinases in the early preimplantation embryo prevents ICM lineage differentiation. Genes Dev. 27:1441-1446. http://dx.doi.org/10.1101/gad.219618.113
45. Louvet, S., J. Aghion, A. Santa-Maria, P. Mangeat, and B. Maro. 1996. Ezrin becomes restricted to outer cells following asymmetrical division in the preimplantation mouse embryo. Dev. Biol. 177:568-579. http://dx.doi.org/10.1006/dbio.1996.0186
46. Motegi, F., S. Zonies, Y. Hao, A.A. Cuenca, E. Griffin, and G. Seydoux. 2011. Microtubules induce self-organization of polarized PAR domains in Caenorhabditis elegans zygotes. Nat. Cell Biol. 13:1361-1367. http://dx.doi.org/10.1038/ncb2354
47. Muller, H.A., and P. Hausen. 1995. Epithelial cell polarity in early Xenopus development. Dev. Dyn. 202:405-420. http://dx.doi.org/10.1002/aja.1002020410
48. Nance, J., and J.R. Priess. 2002. Cell polarity and gastrulation in C. elegans. Development. 129:387-397.
49. Nance, J., and J.A. Zallen. 2011. Elaborating polarity: PAR proteins and the cytoskeleton. Development. 138:799-809. http://dx.doi.org/10.1242/dev.053538
50. Nance, J., E.M. Munro, and J.R. Priess. 2003. C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development. 130:5339-5350. http://dx.doi.org/10.1242/dev.00735
51. Nelson, W.J., D.J. Dickinson, and W.I. Weis. 2013. Roles of cadherins and catenins in cell-cell adhesion and epithelial cell polarity. Prog. Mol. Biol. Transl. Sci. 116:3-23. http://dx.doi.org/10.1016/B978-0-12-394311-8.00001-7
52. Nishioka, N., S. Yamamoto, H. Kiyonari, H. Sato, A. Sawada, M. Ota, K. Nakao, and H. Sasaki. 2008. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech. Dev. 125:270-283. http://dx.doi.org/10.1016/j.mod.2007.11.002
53. Nishioka, N., K. Inoue, K. Adachi, H. Kiyonari, M. Ota, A. Ralston, N. Yabuta, S. Hirahara, R.O. Stephenson, N. Ogonuki, et al. 2009. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell. 16:398-410. http://dx.doi.org/10.1016/j.devcel.2009.02.003
54. Ossipova, O., J. Tabler, J.B. Green, and S.Y. Sokol. 2007. PAR1 specifies ciliated cells in vertebrate ectoderm downstream of aPKC. Development. 134:4297-4306. http://dx.doi.org/10.1242/dev.009282
55. Ossipova, O., J. Ezan, and S.Y. Sokol. 2009. PAR-1 phosphorylates Mind bomb to promote vertebrate neurogenesis. Dev. Cell. 17:222-233. http://dx.doi.org/10.1016/j.devcel.2009.06.010
56. Pauken, C.M., and D.G. Capco. 2000. The expression and stage-specific localization of protein kinase C isotypes during mouse preimplantation development. Dev. Biol. 223:411-421. http://dx.doi.org/10.1006/dbio.2000.9763
57. Plusa, B., S. Frankenberg, A. Chalmers, A.K. Hadjantonakis, C.A. Moore, N. Papalopulu, V.E. Papaioannou, D.M. Glover, and M. Zernicka-Goetz. 2005. Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. J. Cell Sci. 118:505-515. http://dx.doi.org/10.1242/jcs.01666
58. Rayon, T., S. Menchero, A. Nieto, P. Xenopoulos, M. Crespo, K. Cockburn, S. Canon, H. Sasaki, A.K. Hadjantonakis, J.L. de la Pompa, et al. 2014. Notch and hippo converge on cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev. Cell. 30:410-422. http://dx.doi.org/10.1016/j.devcel.2014.06.019
59. Reeve, W.J., and C.A. Ziomek. 1981. Distribution of microvilli on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction. J. Embryol. Exp. Morphol. 62:339-350.
60. Roberts, S.J., D.S. Leaf, H.P. Moore, and J.C. Gerhart. 1992. The establishment of polarized membrane traffic in Xenopus laevis embryos. J. Cell Biol. 118:1359-1369. http://dx.doi.org/10.1083/jcb.118.6.1359
61. Rodriguez-Boulan, E., and I.G. Macara. 2014. Organization and execution of the epithelial polarity programme. Nat. Rev. Mol. Cell Biol. 15:225-242. http://dx.doi.org/10.1038/nrm3775
62. Roignot, J., X. Peng, and K. Mostov. 2013. Polarity in mammalian epithelial morphogenesis. Cold Spring Harb. Perspect. Biol. 5:a013789. http://dx.doi.org/10.1101/cshperspect.a013789
63. Sabherwal, N., A. Tsutsui, S. Hodge, J. Wei, A.D. Chalmers, and N. Papalopulu. 2009. The apicobasal polarity kinase aPKC functions as a nuclear determinant and regulates cell proliferation and fate during Xenopus primary neurogenesis. Development. 136:2767-2777. http://dx.doi.org/10.1242/dev.034454
64. Schroeder, M.C., and G. Halder. 2012. Regulation of the Hippo pathway by cell architecture and mechanical signals. Semin. Cell Dev. Biol. 23:803-811. http://dx.doi.org/10.1016/j.semcdb.2012.06.001
65. Stephenson, R.O., Y. Yamanaka, and J. Rossant. 2010. Disorganized epithelial polarity and excess trophectoderm cell fate in preimplantation embryos lacking E-cadherin. Development. 137:3383-3391. http://dx.doi.org/10.1242/dev.050195
66. Stephenson, R.O., J. Rossant, and P.P. Tam. 2012. Intercellular interactions, position, and polarity in establishing blastocyst cell lineages and embryonic axes. Cold Spring Harb. Perspect. Biol. 4:a008235. http://dx.doi.org/10.1101/cshperspect.a008235
67. St Johnston, D., and J. Ahringer. 2010. Cell polarity in eggs and epithelia: parallels and diversity. Cell. 141:757-774. http://dx.doi.org/10.1016/j.cell.2010.05.011
68. Suwinska, A., R. Czolowska, W. Ozdzenski, and A.K. Tarkowski. 2008. Blastomeres of the mouse embryo lose totipotency after the fifth cleavage division: expression of Cdx2 and Oct4 and developmental potential of inner and outer blastomeres of 16- and 32-cell embryos. Dev. Biol. 322:133-144. http://dx.doi.org/10.1016/j.ydbio.2008.07.019
69. Suzuki, A., M. Hirata, K. Kamimura, R. Maniwa, T. Yamanaka, K. Mizuno, M. Kishikawa, H. Hirose, Y. Amano, N. Izumi, et al. 2004. aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr. Biol. 14:1425-1435. http://dx.doi.org/10.1016/j.cub.2004.08.021
70. Tabler, J.M., H. Yamanaka, and J.B. Green. 2010. PAR-1 promotes primary neurogenesis and asymmetric cell divisions via control of spindle orientation. Development. 137:2501-2505. http://dx.doi.org/10.1242/dev.049833
71. Tabuse, Y., Y. Izumi, F. Piano, K.J. Kemphues, J. Miwa, and S. Ohno. 1998. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development. 125:3607-3614.
72. Takayama, M., T. Noguchi, S. Yamashiro, and I. Mabuchi. 2002. Microtuble organization in Xenopus eggs during the first cleavage and its role in cytokinesis. Cell Struct. Funct. 27:163-171. http://dx.doi.org/10.1247/csf.27.163
73. Tanentzapf, G., and U. Tepass. 2003. Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 5:46-52. http://dx.doi.org/10.1038/ncb896
74. Tarkowski, A.K., A. Suwinska, R. Czolowska, and W. Ozdzenski. 2010. Individual blastomeres of 16- and 32-cell mouse embryos are able to develop into foetuses and mice. Dev. Biol. 348:190-198. http://dx.doi.org/10.1016/j.ydbio.2010.09.022
75. Vestweber, D., A. Gossler, K. Boller, and R. Kemler. 1987. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev. Biol. 124:451-456. http://dx.doi.org/10.1016/0012-1606(87)90498-2
76. Vinot, S., T. Le, S. Ohno, T. Pawson, B. Maro, and S. Louvet-Vallee. 2005. Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. Dev. Biol. 282:307-319. http://dx.doi.org/10.1016/j.ydbio.2005.03.001
77. Wang, S., S.W. Cha, A.M. Zorn, and C. Wylie. 2013. Par6b regulates the dynamics of apicobasal polarity during development of the stratified Xenopus epidermis. PLoS ONE. 8:e76854. http://dx.doi.org/10.1371/journal.pone.0076854
78. Wicklow, E., S. Blij, T. Frum, Y. Hirate, R.A. Lang, H. Sasaki, and A. Ralston. 2014. HIPPO pathway members restrict SOX2 to the inner cell mass where it promotes ICM fates in the mouse blastocyst. PLoS Genet. In press.
79. Yagi, R., M.J. Kohn, I. Karavanova, K.J. Kaneko, D. Vullhorst, M.L. DePamphilis, and A. Buonanno. 2007. Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development. 134:3827-3836. http://dx.doi.org/10.1242/dev.010223
80. Yu, F.X., and K.L. Guan. 2013. The Hippo pathway: regulators and regulations. Genes Dev. 27:355-371. http://dx.doi.org/10.1101/gad.210773.112
81. Ziomek, C.A., and M.H. Johnson. 1980. Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell. 21:935-942. http://dx.doi.org/10.1016/0092-8674(80)90457-2
82. Ziomek, C.A., and M.H. Johnson. 1982. The roles of phenotype and position in guiding the fate of 16-cell mouse blastomeres. Dev. Biol. 91:440-447. http://dx.doi.org/10.1016/0012-1606(82)90050-1
83. Ziomek, C.A., M.H. Johnson, and A.H. Handyside. 1982. The developmental potential of mouse 16-cell blastomeres. J. Exp. Zool. 221:345-355. http://dx.doi.org/10.1002/jez.1402210310