Temporal Regulation of the Muscle Gene Cascade by Macho1 and Tbx6 Transcription Factors in Ciona Intestinalis

Overview

Journal J Cell Sci

Specialty Cell Biology

Date 2010 Jul 2

PMID 20592183

Citations 17

Authors

Jamie E Kugler

Stefan Gazdoiu

Izumi Oda-Ishii

Yale J Passamaneck

Albert J Erives

Anna Di Gregorio

Affiliations

Soon will be listed here.

Abstract

For over a century, muscle formation in the ascidian embryo has been representative of 'mosaic' development. The molecular basis of muscle-fate predetermination has been partly elucidated with the discovery of Macho1, a maternal zinc-finger transcription factor necessary and sufficient for primary muscle development, and of its transcriptional intermediaries Tbx6b and Tbx6c. However, the molecular mechanisms by which the maternal information is decoded by cis-regulatory modules (CRMs) associated with muscle transcription factor and structural genes, and the ways by which a seamless transition from maternal to zygotic transcription is ensured, are still mostly unclear. By combining misexpression assays with CRM analyses, we have identified the mechanisms through which Ciona Macho1 (Ci-Macho1) initiates expression of Ci-Tbx6b and Ci-Tbx6c, and we have unveiled the cross-regulatory interactions between the latter transcription factors. Knowledge acquired from the analysis of the Ci-Tbx6b CRM facilitated both the identification of a related CRM in the Ci-Tbx6c locus and the characterization of two CRMs associated with the structural muscle gene fibrillar collagen 1 (CiFCol1). We use these representative examples to reconstruct how compact CRMs orchestrate the muscle developmental program from pre-localized ooplasmic determinants to differentiated larval muscle in ascidian embryos.

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References

Kim G, Yamada A, Nishida H . An FGF signal from endoderm and localized factors in the posterior-vegetal egg cytoplasm pattern the mesodermal tissues in the ascidian embryo. Development. 2000; 127(13):2853-62. DOI: 10.1242/dev.127.13.2853. View

Meedel T, Crowther R, Whittaker J . Determinative properties of muscle lineages in ascidian embryos. Development. 1987; 100(2):245-60. DOI: 10.1242/dev.100.2.245. View

Passamaneck Y, Hadjantonakis A, Di Gregorio A . Dynamic and polarized muscle cell behaviors accompany tail morphogenesis in the ascidian Ciona intestinalis. PLoS One. 2007; 2(8):e714. PMC: 1934933. DOI: 10.1371/journal.pone.0000714. View

Christiaen L, Stolfi A, Davidson B, Levine M . Spatio-temporal intersection of Lhx3 and Tbx6 defines the cardiac field through synergistic activation of Mesp. Dev Biol. 2009; 328(2):552-60. DOI: 10.1016/j.ydbio.2009.01.033. View

Deno T, Nishida H, Satoh N . Autonomous muscle cell differentiation in partial ascidian embryos according to the newly verified cell lineages. Dev Biol. 1984; 104(2):322-8. DOI: 10.1016/0012-1606(84)90087-3. View

Kim G, Nishida H . Suppression of muscle fate by cellular interaction is required for mesenchyme formation during ascidian embryogenesis. Dev Biol. 1999; 214(1):9-22. DOI: 10.1006/dbio.1999.9402. View

Sardet C, Nishida H, Prodon F, Sawada K . Maternal mRNAs of PEM and macho 1, the ascidian muscle determinant, associate and move with a rough endoplasmic reticulum network in the egg cortex. Development. 2003; 130(23):5839-49. DOI: 10.1242/dev.00805. View

Nishida H . Developmental potential for tissue differentiation of fully dissociated cells of the ascidian embryo. Rouxs Arch Dev Biol. 2017; 201(2):81-87. DOI: 10.1007/BF00420418. View

Sawada K, Fukushima Y, Nishida H . Macho-1 functions as transcriptional activator for muscle formation in embryos of the ascidian Halocynthia roretzi. Gene Expr Patterns. 2005; 5(3):429-37. DOI: 10.1016/j.modgep.2004.09.003. View

10.

Satou Y, Takatori N, Yamada L, Mochizuki Y, Hamaguchi M, Ishikawa H . Gene expression profiles in Ciona intestinalis tailbud embryos. Development. 2001; 128(15):2893-904. DOI: 10.1242/dev.128.15.2893. View

11.

Lemaire P . Unfolding a chordate developmental program, one cell at a time: invariant cell lineages, short-range inductions and evolutionary plasticity in ascidians. Dev Biol. 2009; 332(1):48-60. DOI: 10.1016/j.ydbio.2009.05.540. View

12.

Meinertzhagen I, Okamura Y . The larval ascidian nervous system: the chordate brain from its small beginnings. Trends Neurosci. 2001; 24(7):401-10. DOI: 10.1016/s0166-2236(00)01851-8. View

13.

Erives A . Non-homologous structured CRMs from the Ciona genome. J Comput Biol. 2009; 16(2):369-77. DOI: 10.1089/cmb.2008.20TT. View

14.

Uchiyama H, Kobayashi T, Yamashita A, Ohno S, Yabe S . Cloning and characterization of the T-box gene Tbx6 in Xenopus laevis. Dev Growth Differ. 2001; 43(6):657-69. DOI: 10.1046/j.1440-169x.2001.00606.x. View

15.

Satou Y, Yamada L, Mochizuki Y, Takatori N, Kawashima T, Sasaki A . A cDNA resource from the basal chordate Ciona intestinalis. Genesis. 2002; 33(4):153-4. DOI: 10.1002/gene.10119. View

16.

Delsuc F, Brinkmann H, Chourrout D, Philippe H . Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature. 2006; 439(7079):965-8. DOI: 10.1038/nature04336. View

17.

Yagi K, Takatori N, Satou Y, Satoh N . Ci-Tbx6b and Ci-Tbx6c are key mediators of the maternal effect gene Ci-macho1 in muscle cell differentiation in Ciona intestinalis embryos. Dev Biol. 2005; 282(2):535-49. DOI: 10.1016/j.ydbio.2005.03.029. View

18.

Kusakabe T, Yoshida R, Ikeda Y, Tsuda M . Computational discovery of DNA motifs associated with cell type-specific gene expression in Ciona. Dev Biol. 2004; 276(2):563-80. DOI: 10.1016/j.ydbio.2004.09.037. View

19.

Davidson B, Shi W, Levine M . Uncoupling heart cell specification and migration in the simple chordate Ciona intestinalis. Development. 2005; 132(21):4811-8. DOI: 10.1242/dev.02051. View

20.

Merzdorf C . Emerging roles for zic genes in early development. Dev Dyn. 2007; 236(4):922-40. DOI: 10.1002/dvdy.21098. View