Zebrafish Pou5f1-dependent Transcriptional Networks in Temporal Control of Early Development

Overview

Journal Mol Syst Biol

Specialty Molecular Biology

Date 2010 Mar 10

PMID 20212526

Citations 39

Authors

Daria Onichtchouk

Florian Geier

Bozena Polok

Daniel M Messerschmidt

Rebecca Mossner

Bjorn Wendik

Sungmin Song

Verdon Taylor

Jens Timmer

Wolfgang Driever

Affiliations

Soon will be listed here.

Abstract

The transcription factor POU5f1/OCT4 controls pluripotency in mammalian ES cells, but little is known about its functions in the early embryo. We used time-resolved transcriptome analysis of zebrafish pou5f1 MZspg mutant embryos to identify genes regulated by Pou5f1. Comparison to mammalian systems defines evolutionary conserved Pou5f1 targets. Time-series data reveal many Pou5f1 targets with delayed or advanced onset of expression. We identify two Pou5f1-dependent mechanisms controlling developmental timing. First, several Pou5f1 targets are transcriptional repressors, mediating repression of differentiation genes in distinct embryonic compartments. We analyze her3 gene regulation as example for a repressor in the neural anlagen. Second, the dynamics of SoxB1 group gene expression and Pou5f1-dependent regulation of her3 and foxD3 uncovers differential requirements for SoxB1 activity to control temporal dynamics of activation, and spatial distribution of targets in the embryo. We establish a mathematical model of the early Pou5f1 and SoxB1 gene network to demonstrate regulatory characteristics important for developmental timing. The temporospatial structure of the zebrafish Pou5f1 target networks may explain aspects of the evolution of the mammalian stem cell networks.

Citing Articles

Kick-starting the zygotic genome: licensors, specifiers, and beyond.

Zou Z, Wang Q, Wu X, Schultz R, Xie W EMBO Rep. 2024; 25(10):4113-4130.

PMID: 39160344 PMC: 11467316. DOI: 10.1038/s44319-024-00223-5.

Novel cell states arise in embryonic cells devoid of key reprogramming factors.

Youlten S, Miao L, Hoppe C, Boswell C, Musaev D, Abdelmessih M bioRxiv. 2024; .

PMID: 38798464 PMC: 11118305. DOI: 10.1101/2024.05.13.593729.

Activator-blocker model of transcriptional regulation by pioneer-like factors.

Riesle A, Gao M, Rosenblatt M, Hermes J, Hass H, Gebhard A Nat Commun. 2023; 14(1):5677.

PMID: 37709752 PMC: 10502082. DOI: 10.1038/s41467-023-41507-z.

A network of Notch-dependent and -independent her genes controls neural stem and progenitor cells in the zebrafish thalamic proliferation zone.

Sigloch C, Spitz D, Driever W Development. 2023; 150(7).

PMID: 37009986 PMC: 10112928. DOI: 10.1242/dev.201301.

Zebrafish her3 knockout impacts developmental and cancer-related gene signatures.

Kent M, Calderon D, Silvius K, Kucinski J, LaVigne C, Cannon M Dev Biol. 2023; 496:1-14.

PMID: 36696714 PMC: 10054701. DOI: 10.1016/j.ydbio.2023.01.003.

References

Camp E, Sanchez-Sanchez A, Garcia-Espana A, DeSalle R, Odqvist L, OConnor J . Nanog regulates proliferation during early fish development. Stem Cells. 2009; 27(9):2081-91. DOI: 10.1002/stem.133. View

Chan T, Chao C, Wang H, Yu Y, Yuh C . Functional analysis of the evolutionarily conserved cis-regulatory elements on the sox17 gene in zebrafish. Dev Biol. 2008; 326(2):456-70. DOI: 10.1016/j.ydbio.2008.11.010. View

Frankenberg S, Pask A, Renfree M . The evolution of class V POU domain transcription factors in vertebrates and their characterisation in a marsupial. Dev Biol. 2009; 337(1):162-70. DOI: 10.1016/j.ydbio.2009.10.017. View

Niwa H, Miyazaki J, Smith A . Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet. 2000; 24(4):372-6. DOI: 10.1038/74199. View

Kamachi Y, Uchikawa M, Tanouchi A, Sekido R, Kondoh H . Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev. 2001; 15(10):1272-86. PMC: 313803. DOI: 10.1101/gad.887101. View

Hirata H, Tomita K, Bessho Y, Kageyama R . Hes1 and Hes3 regulate maintenance of the isthmic organizer and development of the mid/hindbrain. EMBO J. 2001; 20(16):4454-66. PMC: 125583. DOI: 10.1093/emboj/20.16.4454. View

Belting H, Hauptmann G, Meyer D, Abdelilah-Seyfried S, Chitnis A, Eschbach C . spiel ohne grenzen/pou2 is required during establishment of the zebrafish midbrain-hindbrain boundary organizer. Development. 2001; 128(21):4165-76. PMC: 4027960. DOI: 10.1242/dev.128.21.4165. View

Niwa H, Masui S, Chambers I, Smith A, Miyazaki J . Phenotypic complementation establishes requirements for specific POU domain and generic transactivation function of Oct-3/4 in embryonic stem cells. Mol Cell Biol. 2002; 22(5):1526-36. PMC: 134688. DOI: 10.1128/MCB.22.5.1526-1536.2002. View

Burgess S, Reim G, Chen W, Hopkins N, Brand M . The zebrafish spiel-ohne-grenzen (spg) gene encodes the POU domain protein Pou2 related to mammalian Oct4 and is essential for formation of the midbrain and hindbrain, and for pre-gastrula morphogenesis. Development. 2002; 129(4):905-16. DOI: 10.1242/dev.129.4.905. View

10.

Reim G, Brand M . Spiel-ohne-grenzen/pou2 mediates regional competence to respond to Fgf8 during zebrafish early neural development. Development. 2002; 129(4):917-33. DOI: 10.1242/dev.129.4.917. View

11.

Quirk J, Brown P . Hesx1 homeodomain protein represses transcription as a monomer and antagonises transactivation of specific sites as a homodimer. J Mol Endocrinol. 2002; 28(3):193-205. DOI: 10.1677/jme.0.0280193. View

12.

Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K . The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell. 2003; 113(5):631-42. DOI: 10.1016/s0092-8674(03)00393-3. View

13.

Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S . Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003; 113(5):643-55. DOI: 10.1016/s0092-8674(03)00392-1. View

14.

Remenyi A, Lins K, Nissen L, Reinbold R, Scholer H, Wilmanns M . Crystal structure of a POU/HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev. 2003; 17(16):2048-59. PMC: 196258. DOI: 10.1101/gad.269303. View

15.

Rhinn M, Lun K, Amores A, Yan Y, Postlethwait J, Brand M . Cloning, expression and relationship of zebrafish gbx1 and gbx2 genes to Fgf signaling. Mech Dev. 2003; 120(8):919-36. DOI: 10.1016/s0925-4773(03)00135-7. View

16.

Gering M, Yamada Y, Rabbitts T, Patient R . Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1. Development. 2003; 130(25):6187-99. DOI: 10.1242/dev.00875. View

17.

Lunde K, Belting H, Driever W . Zebrafish pou5f1/pou2, homolog of mammalian Oct4, functions in the endoderm specification cascade. Curr Biol. 2004; 14(1):48-55. DOI: 10.1016/j.cub.2003.11.022. View

18.

Reim G, Mizoguchi T, Stainier D, Kikuchi Y, Brand M . The POU domain protein spg (pou2/Oct4) is essential for endoderm formation in cooperation with the HMG domain protein casanova. Dev Cell. 2004; 6(1):91-101. DOI: 10.1016/s1534-5807(03)00396-4. View

19.

Hans S, Scheer N, Riedl I, v Weizsacker E, Blader P, Campos-Ortega J . her3, a zebrafish member of the hairy-E(spl) family, is repressed by Notch signalling. Development. 2004; 131(12):2957-69. DOI: 10.1242/dev.01167. View

20.

Gauchat D, Escriva H, Miljkovic-Licina M, Chera S, Langlois M, Begue A . The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates. Dev Biol. 2004; 275(1):104-23. DOI: 10.1016/j.ydbio.2004.07.037. View