Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-26T13:01:42.293Z Has data issue: false hasContentIssue false

Cloning and characterization of ifitm1 and ifitm3 expression during early zebrafish development

Published online by Cambridge University Press:  23 January 2015

Wei-Wei Xue*
Affiliation:
The Laboratory of Molecular Genetics and Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, Hubei, China.
Huan-Nan Wang
Affiliation:
The Laboratory of Molecular Genetics and Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, Hubei, China.
Zhi-Meng Wang
Affiliation:
The Laboratory of Molecular Genetics and Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, Hubei, China.
Meng-Xi Qiu
Affiliation:
The Laboratory of Molecular Genetics and Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, Hubei, China.
Jing Che
Affiliation:
The Laboratory of Molecular Genetics and Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, Hubei, China.
Feng-Jiao Deng
Affiliation:
The Laboratory of Molecular Genetics and Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, Hubei, China.
Jiang-Dong Liu
Affiliation:
The Laboratory of Molecular Genetics and Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, Hubei, China.
*
All correspondence to: Wei-Wei Xue. The Laboratory of Molecular Genetics and Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, Hubei, China. e-mail: [email protected].

Summary

The family of interferon-inducible transmembrane proteins (IFITMs) plays a crucial role in inhibiting proliferation, promoting homotypic cell adhesion and mediating germ cell development. In the present study, the full-length cDNAs of zebrafish ifitm1 (744 bp) and ifitm3 (702 bp) were obtained by rapid amplification of cDNA ends (RACE). Reverse transcription polymerase chain reaction (RT-PCR) analysis showed that ifitm1 mRNA was expressed in the ovary, testis, brain, muscle, liver and kidney, while ifitm3 mRNA was only detected in the ovary. Based on in situ hybridization, ifitm1 mRNA was found to be strongly expressed in the ooplasm from stage I to stage II and ifitm3 mRNA was also strongly expressed in the ooplasm from stage I to stage II, furthermore ifitm3 expression ultimately localized to the cortex region beneath the plasma membrane of stage IV oocytes. During development, ifitm1 expression was initially detected in the enveloping layer cells and deep layer cells of shield stage embryos. Then, throughout the segmentation phase (10.25–24 hours post-fertilization (hpf)), ifitm1 expression was mainly detected in the head, trunk and tail regions. Unlike ifitm1, ifitm3 expression was initially detected in sphere stage embryos and was then broadly expressed throughout the embryo from the 70% epiboly stage to 24 hpf. Interestingly, ifitm3 was also expressed in primordial germ cells (PGCs) from the bud stage to 24 hpf. This expression analysis indicates that zebrafish ifitm1 may play a critical role in early organogenesis and may perform immune or hematopoietic functions and ifitm3 might be necessary for PGC migration and the formation of female germ cells.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Afonso, L.O., Campbell, P.M., Iwama, G.K., Devlin, R.H. & Donaldson, E.M. (1997). The effect of the aromatase inhibitor fadrozole and two polynuclear aromatic hydrocarbons on sex steroid secretion by ovarian follicles of coho salmon. Gen. Comp. Endocrinol. 106, 169–74.Google Scholar
Akam, M. (1987). The molecular basis for metameric pattern in the Drosophila embryo. Development 101, 122.Google Scholar
Brem, R., Oraszlan-Szovik, K., Foser, S., Bohrmann, B. & Certa, U. (2003). Inhibition of proliferation by 1–8U in interferon-alpha-responsive and non-responsive cell lines. Cell. Mol. Life Sci. 60, 1235–48.CrossRefGoogle ScholarPubMed
Deblandre, G.A., Marinx, O.P., Evans, S.S., Majjaj, S., Leo, O., Caput, D., Huez, G.A. & Wathelet, M.G. (1995). Expression cloning of an interferon-inducible 17-kDa membrane protein implicated in the control of cell growth. J. Biol. Chem. 270, 23860–6.Google Scholar
Dijkman, H., Mentzel, S., De Jong, A. & Assmann, K. (1995). RNA in situ hybridization using DIG-labeled cRNA probes. Biochemica (US version) 2, 23.Google Scholar
Friedman, R.L., Manly, S.P., McMahon, M., Kerr, I.M. & Stark, G.R. (1984). Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell 38, 745–55.CrossRefGoogle ScholarPubMed
Giraldez, A.J., Mishima, Y., Rihel, J., Grocock, R.J., Van Dongen, S., Inoue, K., Enright, A.J. & Schier, A.F. (2006). Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312, 75–9.Google Scholar
Hoar, W.S., Randall, D.J., Iwama, G. & Nakanishi, T. (1997). The Fish Immune System: Organism, Pathogen, and Environment. Academic Press.Google Scholar
Howley, C. & Ho, R.K. (2000). mRNA localization patterns in zebrafish oocytes. Mech. Dev. 92, 305–9.Google Scholar
Johnson, M.C., Sangrador-Vegas, A., Smith, T.J. & Cairns, M.T. (2006). Cloning and characterization of two genes encoding rainbow trout homologues of the IFITM protein family. Vet. Immunol. Immunopathol. 110, 357–62.Google Scholar
Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B. & Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253310.Google Scholar
Köprunner, M., Thisse, C., Thisse, B. & Raz, E. (2001). A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev. 15, 2877–85.CrossRefGoogle ScholarPubMed
Lange, U.C., Saitou, M., Western, P.S., Barton, S.C. & Surani, M.A. (2003). The fragilis interferon-inducible gene family of transmembrane proteins is associated with germ cell specification in mice. BMC Dev. Biol. 3, 1.CrossRefGoogle ScholarPubMed
Lewin, A.R., Reid, L.E., McMahon, M., Stark, G.R. & Kerr, I.M. (1991). Molecular analysis of a human interferon-inducible gene family. Eur. J. Biochem. 199, 417–23.CrossRefGoogle ScholarPubMed
Mich, J.K., Blaser, H., Thomas, N.A., Firestone, A.J., Yelon, D., Raz, E. & Chen, J.K. (2009). Germ cell migration in zebrafish is cyclopamine-sensitive but smoothened-independent. Dev. Biol. 328, 342–54.Google Scholar
Saitou, M., Barton, S.C. & Surani, M.A. (2002). A molecular programme for the specification of germ cell fate in mice. Nature 418, 293300.Google Scholar
Samuel, C.E. (2001). Antiviral actions of interferons. Clin. Microbiol. Rev. 14, 778809.Google Scholar
Selman, K., Wallace, R.A., Sarka, A. & Qi, X. (1993). Stages of oocyte development in the zebrafish, Brachydanio rerio. J. Morphol. 218, 203–24.CrossRefGoogle ScholarPubMed
Tanaka, S.S. & Matsui, Y. (2002). Developmentally regulated expression of mil-1 and mil-2, mouse interferon-induced transmembrane protein like genes, during formation and differentiation of primordial germ cells. Mech. Dev. 119 (Suppl 1), S261–7.Google Scholar
Tanaka, S.S., Nagamatsu, G., Tokitake, Y., Kasa, M., Tam, P.P. & Matsui, Y. (2004). Regulation of expression of mouse interferon-induced transmembrane protein like gene-3, Ifitm3 (mil-1, fragilis), in germ cells. Dev. Dyn. 230, 651–9.Google Scholar
Tanaka, S.S., Yamaguchi, Y.L., Tsoi, B., Lickert, H. & Tam, P.P. (2005). IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion. Dev. Cell 9, 745–56.Google Scholar
Thompson, E.M., Legouy, E. & Renard, J.-P. (1998). Mouse embryos do not wait for the MBT: chromatin and RNA polymerase remodeling in genome activation at the onset of development. Dev. Genet. 22, 3142.Google Scholar
Wan, X. & Chen, X. (2008). Molecular cloning and expression analysis of interferon-inducible transmembrane protein 1 in large yellow croaker Pseudosciaena crocea . Vet. Immunol. Immunopathol. 124, 99106.CrossRefGoogle ScholarPubMed
Westerfield, M. (1993). The Zebrafish Book: A Guide For The Laboratory Use of Zebrafish (Brachydanio rerio). Eugene, OR, USA: University of Oregon Press.Google Scholar