Abstract
β-Catenin plays a crucial role in embryonic development and responds to the activation of several signal transduction pathways. In this paper, in order to understand the functions of β-catenin gene in early embryonic development of Artemia sinica, the complete cDNA sequence was cloned for the first time using RACE technology, then the sequence was analyzed by some bioinformatic methods. The expression of the β-catenin gene was investigated at various stages during the embryonic development using quantitative real-time PCR and immunohistochemistry assay. Through the investigation, the result of real-time PCR illustrated that β-catenin gene might relate to the response of A. sinica’s immune system and osmotic pressure system in early embryonic developmental stage. Meanwhile, Immunohistochemistry assay demonstrated that during embryonic development, β-catenin was mainly expressed in the cephalothorax. Besides, we discovered that β-catenin might not be a maternal gene in A. sinica, and this new phenomenon may explain a constitutive and regional expression during the early embryonic development of A. sinica.
Similar content being viewed by others
Abbreviations
- LEF:
-
Lymphoid enhancer factor
- TCF:
-
T-cell factor
- GSK-3β:
-
Glycogen synthase kinase-3β
- LRP:
-
LDL-receptor-related protein
- Fz:
-
Frizzled
- Dsh:
-
Dishevelled
- APC:
-
Adenomatous polyposis coli
- ARM:
-
Armadillo
- REST:
-
Relative expression software tool
References
Jiang LJ, Hou L, Zou HL, Zhang XY, Wang RF, Sun JQ, Zhao WJ, An JL (2007) Cloning and expression analysis of p26 gene in Artemia sinica. Acta Biochem Biophys Sin 39(5):351–358
Imai K, Takada N, Satoh N, Satou Y (2000) β-Catenin mediates the specification of endoderm cells in ascidian embryos. Development 127:3009–3020
Yasui K, Li G, Wang Y, Saiga H, Zhang P, Aizawa S (2002) β-Catenin in early development of the lancelet embryo indicates specific determination of embryonic polarity. Dev Growth Differ 44(6):467–475
Pillai MC, Vines CA, Wikramanayake AH, Cherr GN (2003) Polycyclic aromatic hydrocarbons disrupt axial development in sea urchin embryos through a β-catenin dependent pathway. Toxicology 186:93–108
Range RC, Venuti JM, McClay DR (2005) LvGroucho and nuclear β-catenin functionally compete for Tcf binding to influence activation of the endomesoderm gene regulatory network in the sea urchin embryo. Dev Biol 279:252–267
Schneider S, Steinbeisser H, Warga RM, Hausen P (1996) β-Catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech Dev 57:191–198
Vleminckx K, Kemler R, Hecht A (1999) The C-terminal transactivation domain of β-catenin is necessary and sufficient or signaling by the LEF-1/β-catenin complex in Xenopus laevis. Mech Dev 81:65–74
Moon RT, Miller JR (1996) Signal transduction through β-catenin and specification of cell fate during embryogenesis. Gene Dev 10:2527–2539
Fu XY, Sun HX, Klein WH, Mu XQ (2006) β-Catenin is essential for lamination but not neurogenesis in mouse retinal development. Dev Biol 299:424–437
Roobol K, Möller W (1981) Protein synthesis in Artemia salina. Eucaryotic elongation factor eEF-Ts is a transphosphorylase. Mol Biol Rep 7(4):197–202
Nagafuchi A, Takeichi M (1989) Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell Regul 1:37–44
Ozawa M, Baribault H, Kemler R (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8:1711–1717
Aberle H, Butz S, Stappert J, Weissig H, Kemler R, Hoschuetzky H (1994) Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J Cell Sci 107:3655–3663
Yang Y, Yang J, Liu R, Li H, Luo X, Yang G (2010) Accumulation of β-catenin by lithium chloride in porcine myoblast cultures accelerates cell differentiation. Mol Biol Rep 38:2043–2049
Moreno MP, Jamora C, Fuchs E (2003) Sticky business: orchestrating cellular signals at adherens junctions orchestrating cellular signals at adherens junctions. Cell 112:535–548
Chen G, Jiang Q, You Z, Yao J, Mou L, Lin X, Shen X, You T, Lin Q, Wen J, Lin L (2010) Regulation of GSK-3 beta in the proliferation and apoptosis of human thyrocytes investigated using a GSK-3 beta-targeting RNAi adenovirus expression vector: involvement the Wnt/β-catenin pathway. Mol Biol Rep 37:2773–2779
Li Q, Liu X, Zhang M, Ye G, Qiao Q, Ling Y, Wu Y, Zhang Y, Yu L (2010) Characterization of a novel human CDK5 splicing variant that inhibits Wnt/β-catenin signaling. Mol Biol Rep 37(5):2415–2421
Gottardi CJ, Gumbiner BM (2004) Distinct molecular forms of β-catenin are targeted to adhesive or transcriptional complexes. J Cell Biol 167:339–349
Peifer M, Polakis P (2000) Wnt signaling in oncogenesis and embryogenesis—a look outside the nucleus. Science 287(5458):1606–1609
Wang XP, O’Connell DJ, Lund JJ, Saadi I, Kuraguchi M, Turbe-Doan A, Cavallesco R, Kim H, Park PJ, Harada H, Kucherlapati R, Maas RL (2009) Apc inhibition of Wnt signaling regulates supernumerary tooth formation during embryogenesis and throughout adulthood. Development 136(11):1939–1949
Yan D, Wiesmann M, Rohan M, Chan V, Jefferson AB, Guo L, Sakamoto D, Caothien RH, Fuller JH, Reinhard C, Garcia PD, Randazzo FM, Escobedo J, Fantl WJ, Williams LT (2001) Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/β-catenin signaling is activated in human colon tumors. Cell Biol 98:14973–14978
Cong F, Schweizer L, Chamorro M, Varmus H (2003) Requirement for a nuclear function of requirement for a nuclear function of β-catenin in Wnt signaling-catenin in Wnt signaling. Mol Cell Biol 23:8462–8470
Vandesompele J, Preter KD, Pattyn F, Poppe B, Roy NV, Paepe AD, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genorme Biol 3(7): RESEARCH0034
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45
Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415:914–917. doi:10.1038/nature716
Kanwar AS (2007) Brine shrimp (Artemia salina)—a marine animal for simple and rapid biological assays. J Chin Clin Med 2:236–240
Hsia CC, Paré AC, Hannon M, Ronshaugen M, McGinnis W (2010) Silencing of an abdominal Hox gene during early development is correlated with limb development in a crustacean trunk. Evol Dev 12(2):131–143. doi:10.1111/j.1525-142X.2010.00399.x
Patel HN (1994) Imaging drosophila embryos and larvae antibody probes. http://patelweb.berkeley.edu/Images/Protocols/pdf%20files/Antibody%20Methods%202006.pdf
Milde P, Merke J, Ritz E, Haussler MR, Rauterberg EW (1989) Immunohistochemical detection of 1,25-dihydroxyvitamin D3 receptors and estrogen receptors by monoclonal antibodies: comparison of four immunoperoxidase methods. J Histochem Cytochem 37(11):1609–1617
Giorno R (1984) A comparison of two immunoperoxidase staining methods based on the avidin-biotin interaction. Diagn Immunol 2(3):161–166
Shi ZR, Itzkowitz SH, Kim YS (1988) A comparison of three immunoperoxidase techniques for antigen detection in colorectal carcinoma tissues. J Histochem Cytochem 36:317–322
Blenis J (1993) Signal transduction via the MAP kinases: proceed at your own RSK. Proc Natl Acad Sci USA 90:5889–5892
June CH, Fletcher MC, Ledbetter JA, Schieven GL, Siegel JN, Philips AF, Samelson LE (1990) Inhibition of tyrosine phosphoorylation prevents T-cell receptor-mediated signal transduction. Proc Natl Acad Sci USA 87:7722–7726
Larabell CA, Torres M, Rowning BA, Yost C, Miller JR, Wu M, Kimelman D, Moon RT (1997) Establishment of the dorso-ventral axis in Xenopus embryos is presaged by early asymmetries in β-catenin that are modulated by the Wnt signaling pathway. J Cell Biol 136:1123–1136
Peleari FA, Maischein HM (1998) Function of zebrafish β-catenin and TCF-3 in dorsoventral patterning. Mech Dev 77:63–74
Church VL, Francis-West P (2002) Wnt signaling during limb development. Int J Dev Biol 46:927–936
Sadot E, Geiger B, Oren M, Ben-Ze’ev A (2001) Down-regulation of β-catenin by activated p53. Mol Cell Biol 21:6768–6781
Lickert H, Domon C, Huls G, Wehrle C, Duluc I, Clevers H, Meyer BI, Freund JN, Kemler R (2000) Wnt/β-catenin signaling regulates the expression of the homeobox gene Cdx1 in embryonic intestine. Development 127:3805–3813
Willert K, Nusse R (1998) β-catenin: a key mediator of Wnt signaling. Curr Opin Genet Dev 8:95–102
Clevers H (2006) Wnt/β-catenin signaling in development and disease. Cell 127:469–480
Hingwing K, Lee S, Nykilchuk L, Wasston T, Hardin J, Hawkins N (2009) CWN-1 functions with DSH-2 to regulate C elegans asymmetric neuroblast division in a β-catenin independent Wnt pathway. Dev Biol 15:45–56
Agius E, Oelgeschlager M, Wessely O, Kemp C, De Robertis EM (2000) Endodermal nodal-related signals and mesoderm induction in xenopus. Development 127:1173–1183
Birsoy B, Kofron M, Schaible K, Wylie C, Heasman J (2006) Vg1 is an essential signaling molecule in xenopus development. Development 133:15–20
Pai LM, Kirpatrick C, Blanton J, Oda H, Takeichi M, Peifer M (1996) Drosophila α-catenin and E-cadherin bind to distinct regions of drosophila armadillo. J Biol Chem 271:32411–32420
Liu H-Y, Pan L-Q, Zheng D (2008) Effects of salinity on biogenic amines, hemolymph osmotic pressure, and activity of Gill’s Na+/K+-ATPase in Charybdis japonica (Crustacea, Decapoda). J World Aquacult Soc 39(6):812–820. doi:10.1111/j.1749-7345.2008.00218.x
Elmadfa I, Klein P, Meyer AL (2010) Immune-stimulating effects of lactic acid bacteria in vivo and in vitro. Proc Nutr Soc 69(3):416–420
Farkas A, Szatmári E, Orbók A, Wilhelm I, Wejksza K, Nagyoszi P, Hutamekalin P, Bauer H, Bauer HC, Traweger A, Krizbai IA (2005) Hyperosmotic mannitol induces Src kinase-dependent phosphorylation of beta-catenin in cerebral endothelial cells. J Neurosci Res 80(6):855–861
Sokabe T, Fukumi-Tominaga T, Yonemura S, Mizuno A, Tominaga M (2010) The TRPV4 channel contributes to intercellular junction formation in keratinocytes. J Biol Chem. doi:10.1074/jbc.M110.103606
Warr E, Das S, Dong Y, Dimopoulos G (2008) The Gram-negative bacteria-binding protein gene family: Its role in the innate immune system of Anopheles gambiae and in anti-Plasmodium defence. Insect Mol Biol 17(1):39–51. doi:10.1111/j.1365-2583.2008.00778.x
Acknowledgments
We thank Dr. He Chongbo, Liaoning Ocean and Fisheries Science Research Institute, for his help in carrying out real-time PCR experiment. This work was supported by National Science Foundation of China (30271035, 31071876).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, X., Hou, L., Ma, J. et al. Cloning and characterization of β-catenin gene in early embryonic developmental stage of Artemia sinica . Mol Biol Rep 39, 701–707 (2012). https://doi.org/10.1007/s11033-011-0788-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-011-0788-0