Browse > Article
http://dx.doi.org/10.14348/molcells.2019.0210

march5 Governs the Convergence and Extension Movement for Organization of the Telencephalon and Diencephalon in Zebrafish Embryos  

Jung, Jangham (Department of Life Science, BK21 Plus Program, Graduate School, Chungnam National University)
Choi, Issac (Department of Life Science, BK21 Plus Program, Graduate School, Chungnam National University)
Ro, Hyunju (Department of Life Science, BK21 Plus Program, Graduate School, Chungnam National University)
Huh, Tae-Lin (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University)
Choe, Joonho (Department of Biological Sciences, Korea Advanced Institute of Science and Technology)
Rhee, Myungchull (Department of Life Science, BK21 Plus Program, Graduate School, Chungnam National University)
Publication Information
Molecules and Cells / v.43, no.1, 2020 , pp. 76-85 More about this Journal
Abstract
MARCH5 is a RING finger E3 ligase involved in mitochondrial integrity, cellular protein homeostasis, and the regulation of mitochondrial fusion and fission. To determine the function of MARCH5 during development, we assessed transcript expression in zebrafish embryos. We found that march5 transcripts were of maternal origin and evenly distributed at the 1-cell stage, except for the mid-blastula transition, with expression predominantly in the developing central nervous system at later stages of embryogenesis. Overexpression of march5 impaired convergent extension movement during gastrulation, resulting in reduced patterning along the dorsoventral axis and alterations in the ventral cell types. Overexpression and knockdown of march5 disrupted the organization of the developing telencephalon and diencephalon. Lastly, we found that the transcription of march5 was tightly regulated by the transcriptional regulators CHOP, C/EBPα, Staf, Znf143a, and Znf76. These results demonstrate the essential role of March5 in the development of zebrafish embryos.
Keywords
convergence and extension movement; diencephalon; March5/MITOL; telencephalon; ubiquitin proteasome system;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Ramel, M.C. and Lekven, A.C. (2004). Repression of the vertebrate organizer by Wnt8 is mediated by Vent and Vox. Development 131, 3991-4000.   DOI
2 Reifers, F., Bohli, H., Walsh, E.C., Crossley, P.H., Stainier, D., and Brand, M. (1998). Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125, 2381-2395.   DOI
3 Ro, H., Soun, K., Kim, E.J., and Rhee, M. (2004). Novel vector systems optimized for injecting in vitro-synthesized mRNA into zebrafish embryos. Mol. Cells 17, 373-376.
4 Ron, D. and Habener, J.F. (1992). CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6, 439-453.   DOI
5 Schaub, M., Myslinski, E., Schuster, C., Krol, A., and Carbon, P. (1997). Staf, a promiscuous activator for enhanced transcription by RNA polymerases II and III. EMBO J. 16, 173-181.   DOI
6 Schulte-Merker, S., Hammerschmidt, M., Beuchle, D., Cho, K., De Robertis, E., and Nusslein-Volhard, C. (1994). Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development 120, 843-852.   DOI
7 Schuster, C., Myslinski, E., Krol, A., and Carbon, P. (1995). Staf, a novel zinc finger protein that activates the RNA polymerase III promoter of the selenocysteine tRNA gene. EMBO J. 14, 3777-3787.   DOI
8 Sepich, D.S., Calmelet, C., Kiskowski, M., and Solnica-Krezel, L. (2005). Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation. Dev. Dyn. 234, 279-292.   DOI
9 Solnica-Krezel, L. (2005). Conserved patterns of cell movements during vertebrate gastrulation. Curr. Biol. 15, R213-R228.   DOI
10 Sugiura, A., Nagashima, S., Tokuyama, T., Amo, T., Matsuki, Y., Ishido, S., Kudo, Y., McBride, H.M., Fukuda, T., and Matsushita, N. (2013). MITOL regulates endoplasmic reticulum-mitochondria contacts via Mitofusin2. Mol. Cell 51, 20-34.   DOI
11 Szabadkai, G., Bianchi, K., Várnai, P., De Stefani, D., Wieckowski, M.R., Cavagna, D., Nagy, A.I., Balla, T., and Rizzuto, R. (2006). Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J. Cell Biol. 175, 901-911.   DOI
12 Talukder, A.H., Wang, R.A., and Kumar, R. (2002). Expression and transactivating functions of the bZIP transcription factor GADD153 in mammary epithelial cells. Oncogene 21, 4289-4300.   DOI
13 Thisse, C., Thisse, B., Schilling, T., and Postlethwait, J. (1993). Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119, 1203-1215.   DOI
14 Tommerup, N. and Vissing, H. (1995). Isolation and fine mapping of 16 novel human zinc finger-encoding cDNAs identify putative candidate genes for developmental and malignant disorders. Genomics 27, 259-264.   DOI
15 Trinkaus, J. (1993). The yolk syncytial layer of Fundulus: its origin and history and its significance for early embryogenesis. J. Exp. Zool. 265, 258-284.   DOI
16 Ubeda, M., Wang, X.Z., Zinszner, H., Wu, I., Habener, J.F., and Ron, D. (1996). Stress-induced binding of the transcriptional factor CHOP to a novel DNA control element. Mol. Cell. Biol. 16, 1479-1489.   DOI
17 Viktorin, G., Chiuchitu, C., Rissler, M., Varga, Z.M., and Westerfield, M. (2009). Emx3 is required for the differentiation of dorsal telencephalic neurons. Dev. Dyn. 238, 1984-1998.   DOI
18 Barth, K.A., Kishimoto, Y., Rohr, K.B., Seydler, C., Schulte-Merker, S., and Wilson, S.W. (1999). Bmp activity establishes a gradient of positional information throughout the entire neural plate. Development 126, 4977-4987.   DOI
19 Carlson, B.A., Schweizer, U., Perella, C., Shrimali, R.K., Feigenbaum, L., Shen, L., Speransky, S., Floss, T., Jeong, S.J., and Watts, J. (2009). The selenocysteine tRNA STAF-binding region is essential for adequate selenocysteine tRNA status, selenoprotein expression and early age survival of mice. Biochem. J. 418, 61-71.   DOI
20 Chen, H., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E., and Chan, D.C. (2003). Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160, 189-200.   DOI
21 Cherok, E., Xu, S., Li, S., Das, S., Meltzer, W.A., Zalzman, M., Wang, C., and Karbowski, M. (2017). Novel regulatory roles of Mff and Drp1 in E3 ubiquitin ligase MARCH5-dependent degradation of MiD49 and Mcl1 and control of mitochondrial dynamics. Mol. Biol. Cell 28, 396-410.   DOI
22 Chuang, J.C., Mathers, P.H., and Raymond, P.A. (1999). Expression of three Rx homeobox genes in embryonic and adult zebrafish. Mech. Dev. 84, 195-198.   DOI
23 D'Amico, L.A. and Cooper, M.S. (1997). Spatially distinct domains of cell behavior in the zebrafish organizer region. Biochem. Cell Biol. 75, 563-577.   DOI
24 De Brito, O.M. and Scorrano, L. (2008). Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610.   DOI
25 Fisher, S. and Halpern, M.E. (1999). Patterning the zebrafish axial skeleton requires early chordin function. Nat. Genet. 23, 442-446.   DOI
26 Wang, X.Z., Lawson, B., Brewer, J.W., Zinszner, H., Sanjay, A., Mi, L.J., Boorstein, R., Kreibich, G., Hendershot, L.M., and Ron, D. (1996). Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 16, 4273-4280.   DOI
27 Westerfield, M. (2000). The zebrafish book: a guide for the laboratory use of zebrafish. http://zfin.org/zf_info/zfbook/zfbk.html.
28 Fox, M.D. and Bruce, A.E. (2009). Short-and long-range functions of Goosecoid in zebrafish axis formation are independent of Chordin, Noggin 1 and Follistatin-like 1b. Development 136, 1675-1685.   DOI
29 Horndasch, M., Lienkamp, S., Springer, E., Schmitt, A., Pavenstädt, H., Walz, G., and Gloy, J. (2006). The C/EBP homologous protein CHOP (GADD153) is an inhibitor of Wnt/TCF signals. Oncogene 25, 3397-3407.   DOI
30 Jung, J., Udhaya Kumar, S., Choi, I., Huh, T.L., and Rhee, M. (2019). Znf76 is associated with development of the eyes, midbrain, MHB, and hindbrain in zebrafish embryos. Anim. Cells Syst. 23, 26-31.   DOI
31 Kim, E.J., Ro, H., Huh, T.L., Lee, C.J., Choi, J., and Rhee, M. (2008). A novel Kinesin‐like protein, Surhe is associated with dorsalization in the zebrafish embryos. Anim. Cells Syst. 12, 219-230.   DOI
32 Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., and Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.   DOI
33 Kimmel, C.B., Warga, R.M., and Schilling, T.F. (1990). Origin and organization of the zebrafish fate map. Development 108, 581-594.   DOI
34 Wu, X., Wu, F.H., Wu, Q., Zhang, S., Chen, S., and Sima, M. (2017). Phylogenetic and molecular evolutionary analysis of Mitophagy receptors under hypoxic conditions. Front. Physiol. 8, 539.   DOI
35 Xu, S., Cherok, E., Das, S., Li, S., Roelofs, B.A., Ge, S.X., Polster, B.M., Boyman, L., Lederer, W.J., and Wang, C. (2016). Mitochondrial E3 ubiquitin ligase MARCH5 controls mitochondrial fission and cell sensitivity to stress-induced apoptosis through regulation of MiD49 protein. Mol. Biol. Cell 27, 349-359.   DOI
36 Yonashiro, R., Ishido, S., Kyo, S., Fukuda, T., Goto, E., Matsuki, Y., Ohmura-Hoshino, M., Sada, K., Hotta, H., and Yamamura, H. (2006). A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J. 25, 3618-3626.   DOI
37 Yonashiro, R., Kimijima, Y., Shimura, T., Kawaguchi, K., Fukuda, T., Inatome, R., and Yanagi, S. (2012). Mitochondrial ubiquitin ligase MITOL blocks S-nitrosylated MAP1B-light chain 1-mediated mitochondrial dysfunction and neuronal cell death. Proc. Natl. Acad. Sci. U. S. A. 109, 2382-2387.   DOI
38 Zhao, J., Liu, T., Jin, S., Wang, X., Qu, M., Uhlen, P., Tomilin, N., Shupliakov, O., Lendahl, U., and Nister, M. (2011). Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 30, 2762-2778.   DOI
39 Zinszner, H., Kuroda, M., Wang, X., Batchvarova, N., Lightfoot, R.T., Remotti, H., Stevens, J.L., and Ron, D. (1998). CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12, 982-995.   DOI
40 Kishimoto, Y., Lee, K.H., Zon, L., Hammerschmidt, M., and Schulte-Merker, S. (1997). The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 124, 4457-4466.   DOI
41 Kumar, A., Anuppalle, M., Maddirevula, S., Huh, T.L., Choe, J., and Rhee, M. (2019). Peli1b governs the brain patterning via ERK signaling pathways in zebrafish embryos. Gene 694, 1-6.   DOI
42 Kumar, A., Huh, T.L., Choe, J., and Rhee, M. (2017). Rnf152 is essential for NeuroD expression and Delta-notch signaling in the zebrafish embryos. Mol. Cells 40, 945.   DOI
43 Lackner, L.L., Horner, J.S., and Nunnari, J. (2009). Mechanistic analysis of a dynamin effector. Science 325, 874-877.   DOI
44 Mathers, P., Grinberg, A., Mahon, K., and Jamrich, M. (1997). The Rx homeobox gene is essential for vertebrate eye development. Nature 387, 603-607.   DOI
45 Maytin, E.V., Ubeda, M., Lin, J.C., and Habener, J.F. (2001). Stress-inducible transcription factor CHOP/gadd153 induces apoptosis in mammalian cells via p38 kinase-dependent and-independent mechanisms. Exp. Cell Res. 267, 193-204.   DOI
46 Mears, J.A., Lackner, L.L., Fang, S., Ingerman, E., Nunnari, J., and Hinshaw, J.E. (2011). Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat. Struct. Mol. Biol. 18, 20-26.   DOI
47 Morita, T., Nitta, H., Kiyama, Y., Mori, H., and Mishina, M. (1995). Differential expression of two zebrafish emx homeoprotein mRNAs in the developing brain. Neurosci. Lett. 198, 131-134.   DOI
48 Myslinski, E., Krol, A., and Carbon, P. (1992). Optimal tRNA (Ser) Sec gene activity requires an upstream SPH motif. Nucleic Acids Res. 20, 203-209.   DOI
49 Myslinski, E., Krol, A., and Carbon, P. (1998). ZNF76 and ZNF143 are two human homologs of the transcriptional activator Staf. J. Biol. Chem. 273, 21998-22006.   DOI
50 Nagashima, S., Tokuyama, T., Yonashiro, R., Inatome, R., and Yanagi, S. (2014). Roles of mitochondrial ubiquitin ligase MITOL/MARCH5 in mitochondrial dynamics and diseases. J. Biochem. 155, 273-279.   DOI
51 Nakamura, N., Kimura, Y., Tokuda, M., Honda, S., and Hirose, S. (2006). MARCH-V is a novel mitofusin 2-and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 7, 1019-1022.   DOI
52 Niehrs, C. (2004). Regionally specific induction by the Spemann-Mangold organizer. Nat. Rev. Genet. 5, 425-434.   DOI
53 Oxtoby, E. and Jowett, T. (1993). Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res. 21, 1087-1095.   DOI
54 Palmer, C.S., Osellame, L.D., Laine, D., Koutsopoulos, O.S., Frazier, A.E., and Ryan, M.T. (2011). MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 12, 565-573.   DOI
55 Park, Y.Y. and Cho, H. (2012). Mitofusin 1 is degraded at G2/M phase through ubiquitylation by MARCH5. Cell Div. 7, 25.   DOI
56 Park, Y.Y., Lee, S., Karbowski, M., Neutzner, A., Youle, R.J., and Cho, H. (2010). Loss of MARCH5 mitochondrial E3 ubiquitin ligase induces cellular senescence through dynamin-related protein 1 and mitofusin 1. J. Cell Sci. 123, 619-626.   DOI
57 Ragoussis, J., Senger, G., Mockridge, I., Sanseau, P., Ruddy, S., Dudley, K., Sheer, D., and Trowsdale, J. (1992). A testis-expressed Zn finger gene (ZNF76) in human 6p21. 3 centromeric to the MHC is closely linked to the human homolog of the t-complex gene tcp-11. Genomics 14, 673-679.   DOI
58 Ramel, M.C., Buckles, G.R., Baker, K.D., and Lekven, A.C. (2005). WNT8 and BMP2B co-regulate non-axial mesoderm patterning during zebrafish gastrulation. Dev. Biol. 287, 237-248.   DOI