Abstract
Apolipoprotein C1 (Apoc1) is associated with lipoprotein metabolism, but its physiological role during embryogenesis is largely unknown. We reveal a new function of Apoc1b, a transcript isoform of Apoc1, in epiboly during zebrafish gastrulation. Apoc1b is expressed in yolk syncytial layers and in deep cells of the ventral and lateral region of the embryos. It displays a radial gradient with high levels in the interior layer and low levels in the superficial layer. Knockdown of Apoc1b by injecting antisense morpholino (MO) caused the epiboly arrest in deep cells. Moreover, we show that the radial intercalation and the radial gradient distribution of E-cadherin are disrupted both in Apoc1b knockdown and overexpressed embryos. Therefore, Apoc1b controls epiboly via E-cadherin-mediated radial intercalation in a gradient-dependent manner.
Article PDF
Similar content being viewed by others
References
Warga R M, Kimmel C B. Cell movements during epiboly and gastrulation in zebrafish. Development, 1990, 108: 569–580
Solnica-Krezel L. Conserved patterns of cell movements during vertebrate gastrulation. Curr Biol, 2005, 15: R213–R228
Niu X B, Shi H, Peng J R. The role of mesodermal signals during liver organogenesis in zebrafish. Sci China Life Sci, 2010, 53: 455–461
Arendt D, Nübler-Jung K. Rearranging gastrulation in the name of yolk: Evolution of gastrulation in yolk-rich amniote eggs. Mech Dev, 1999, 81: 3–22
Solnica-Krezel L. Gastrulation in zebrafish—all just about adhesion? Curr Opin Genet Dev, 2006, 16: 433–441
Kane D A, Mcfarland K N, Warga R M. Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development, 2005, 132: 1105–1116
Kane D, Adams R. Life at the edge: Epiboly and involution in the zebrafish. Results Probl Cell Differ, 2002, 40: 117–135
Shimizu T, Yabe T, Muraoka O, et al. E-cadherin is required for gastrulation cell movements in zebrafish. Mech Dev, 2005, 122: 747–763
Solnica-Krezel L, Driever W. Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. Development, 1994, 120: 2443–2455
Wilkins S J, Yoong S, Verkade H, et al. Mtx2 directs zebrafish morphogenetic movements during epiboly by regulating microfilament formation. Dev Biol, 2008, 314: 12–22
Hsu H J, Liang M R, Chen C T, et al. Pregnenolone stabilizes micro tubules and promotes zebrafish embryonic cell movement. Nature, 2006, 439: 480–483
Cheng J C, Miller A L, Webb S E. Organization and function of microfilaments during late epiboly in zebrafish embryos. Dev Dyn, 2004, 231: 313–323
Siddiqui M, Sheikh H, Tran C, et al. The tight junction component Claudin E is required for zebrafish epiboly. Dev Dyn, 2010, 239: 715–722
Köppen M, Fernández B G, Carvalho L, et al. Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila. Development, 2006, 133: 2671–2681
Behrndt M, Salbreux G, Campinho P, et al. Forces driving epithelial spreading in zebrafish gastrulation. Science, 2012, 338: 257–260
Sharma D, Holets L, Zhang X, et al. Role of Fyn kinase in signaling associated with epiboly during zebrafish development. Dev Biol, 2005, 285: 462–476
Tsai W B, Zhang X, Sharma D, et al. Role of Yes kinase during early zebrafish development. Dev Biol, 2005, 277: 129–141
Bruce A E, Howley C, Dixon F M, et al. T-box gene eomesodermin and the homeobox-containing Mix/Bix gene mtx2 regulate epiboly movements in the zebrafish. Dev Dyn, 2005, 233: 105–114
Reim G, Mizoguchi T, Stainier D Y, et al. The POU domain protein Spg (Pou2/Oct4) is essential for endoderm formation in cooperation with the HMG domain protein Casanova. Dev Cell, 2004, 6: 91–101
Lachnit M, Kur E, Driever W. Alterations of the cytoskeleton in all three embryonic lineages contribute to the epiboly defect of Pou5f1/Oct4 deficient MZspg zebrafish embryos. Dev Biol, 2008, 315: 1–17
Lunde K, Belting H, Driever W. Zebrafish pou5f1/pou2, homolog of mammalian Oct4, functions in the endoderm specification cascade. Curr Biol, 2004, 14: 48–55
Giraldez A J, Cinalli R M, Glasner M E, et al. microRNAs regulate brain morphogenesis in zebrafish. Science, 2005, 308: 833–838
Cha Y I, Kim S H, Sepich D, et al. Cyclooxygenase-1-derived PGE2 promotes cell motility via the G-protein-coupled EP4 receptor during vertebrate gastrulation. Genes Dev, 2006, 20: 77–86
Leskow F C, Holloway B A, Wang H, et al. The zebrafish homologue of mammalian chimerin Rac-GAPs is implicated in epiboly progression during development. Proc Natl Acad Sci USA, 2006, 103: 5373–5378
Huang H, Lu F I, Jia S, et al. Amotl2 is essential for cell movements in zebrafish embryo and regulates c-Src translocation. Development, 2007, 134: 979–988
Carreira-Barbosa F, Kajita M, Morel V, et al. Flamingo regulates epiboly and convergence/extension movements through cell cohesive and signalling functions during zebrafish gastrulation. Development, 2009, 136: 383–392
Lin F, Chen S, Sepich D S, et al. Galpha12/13 regulate epiboly by inhibiting E-cadherin activity and modulating the actin cytoskeleton. J Cell Biol, 2009, 184: 909–921
Schepis A, Sepich D, Nelson W J. αE-catenin regulates cell-cell adhesion and membrane blebbing during zebrafish epiboly. Development, 2012, 139: 537–546
Dominiczak M H, Caslake M J. Apolipoproteins: Metabolic role and clinical biochemistry applications. Ann Clin Biochem, 2011, 48: 498–515
Bell R D, Winkler E A, Singh I, et al. Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature, 2012, 485: 512–516
Bu G. Apolipoprotein E and its receptors in Alzheimer’s disease: Pathways, pathogenesis and therapy. Nat Rev Neurosci, 2009, 10: 333–344
Hegele R A. Plasma lipoproteins: Genetic influences and clinical implications. Nat Rev Genet, 2009, 10: 109–121
Lusis A J, Pajukanta P. A treasure trove for lipoprotein biology. Nat Genet, 2008, 40: 129–130
Zou L, Huang Q, Li A. A genome-wide association study of Alzheimer’s disease using random forests and enrichment analysis. Sci China Life Sci, 2012, 55: 618–625
Gafencu A V, Robciuc M R, Fuior E, et al. Inflammatory signaling pathways regulating ApoE gene expression in macrophages. J Biol Chem, 2007, 282: 21776–21785
Cho T, Jung Y, Koschinsky M L. Apolipoprotein(a), through its strong lysine-binding site in KIV10, mediates increased endothelial cell contraction and permeability via a Rho/Rho kinase/MYPT1-dependent pathway. J Biol Chem, 2008, 283: 30503–30512
Liu L, Craig A W, Meldrum H D, et al. Apolipoprotein(a) stimulates vascular endothelial cell growth and migration and signals through integrin αVβ3. Biochem J, 2009, 418: 325–336
Xia J H, Liu J X, Zhou L, et al. Apo-14 is required for digestive system organogenesis during fish embryogenesis and larval development. Int J Dev Biol, 2008, 52: 1089–1098
Zhou L, Wang Y, Yao B, et al. Molecular cloning and expression pattern of 14 kDa apolipoprotein in orange-spotted grouper, Epinephelus coioides. Comp Biochem Physiol B-Biochem Mol Biol, 2005, 142: 432–437
Wang Y, Zhou L, Li Z, et al. Molecular cloning and expression characterization of ApoC-I in the orange-spotted grouper. Fish Physiol Biochem, 2008, 34: 339–348
Westerfield M. The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). 4th ed. Eugene: University of Oregon Press, 2000
Kimmel C B, Ballard W W, Kimmel S R, et al. Stages of embryonic development of the zebrafish. Dev Dyn, 1995, 203: 253–310
Mei J, Li Z, Gui J. Cooperation of Mtmr8 with PI3K regulates actin filament modeling and muscle development in zebrafish. PLoS ONE, 2009, 4: e4979
Liu J, Hu B, Wang Y, et al. Zebrafish eaf1 and eaf2/u19 mediate effective convergence and extension movements through the maintenance of wnt11 and wnt5 expression. J Biol Chem, 2009, 284: 16679–16692
Dolbeare F, Gratzner H, Pallavicini M G, et al. Flow cytometric measurement of total DNA content and incorporated bromodeoxyuridine. Proc Natl Acad Sci USA, 1983, 80: 5573–5577
Betchaku T, Trinkaus J P. Contact relations, surface activity, and cortical microfilaments of marginal cells of the enveloping layer and of the yolk syncytial and yolk cytoplasmic layers of Fundulus before and during epiboly. J Exp Zool, 1978, 206: 381–426
Lepage S E, Bruce A E. Zebrafish epiboly: Mechanics and mechanisms. Int J Dev Biol, 2010, 54: 1213–1228
Borghi N, Lowndes M, Maruthamuthu V, et al. Regulation of cell motile behavior by crosstalk between cadherin- and integrin-mediated adhesions. Proc Natl Acad Sci USA, 2010, 107: 13324–13329
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
About this article
Cite this article
Wang, Y., Zhou, L., Li, Z. et al. Apolipoprotein C1 regulates epiboly during gastrulation in zebrafish. Sci. China Life Sci. 56, 975–984 (2013). https://doi.org/10.1007/s11427-013-4563-4
Received:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1007/s11427-013-4563-4