Dlp-mediated Hh and Wnt Signaling Interdependence is Critical in the Niche for Germline Stem Cell Progeny Differentiation

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2020 May 20

PMID 32426496

Citations 12

Authors

Renjun Tu

Bo Duan

Xiaoqing Song

Ting Xie

Affiliations

Soon will be listed here.

Abstract

Although multiple signaling pathways work synergistically in various niches to control stem cell self-renewal and differentiation, it remains poorly understood how they cooperate with one another molecularly. In the ovary, Hh and Wnt pathways function in the niche to promote germline stem cell (GSC) progeny differentiation. Here, we show that glypican Dlp-mediated Hh and Wnt signaling interdependence operates in the niche to promote GSC progeny differentiation by preventing BMP signaling. Hh/Wnt-mediated repression is essential for their signaling interdependence in niche cells and for GSC progeny differentiation by preventing BMP signaling. Mechanistically, Hh and Wnt downstream transcription factors directly bind to the same regulatory region and recruit corepressors composed of transcription factor Croc and Egg/H3K9 trimethylase to repress Dlp expression. Therefore, our study reveals a novel mechanism for Hh/Wnt signaling-mediated direct repression and a novel regulatory mechanism for Dlp-mediated Hh/Wnt signaling interdependence in the GSC differentiation niche.

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References

Ward E, Shcherbata H, Reynolds S, Fischer K, Hatfield S, Ruohola-Baker H . Stem cells signal to the niche through the Notch pathway in the Drosophila ovary. Curr Biol. 2006; 16(23):2352-8. DOI: 10.1016/j.cub.2006.10.022. View

Luo L, Wang H, Fan C, Liu S, Cai Y . Wnt ligands regulate Tkv expression to constrain Dpp activity in the Drosophila ovarian stem cell niche. J Cell Biol. 2015; 209(4):595-608. PMC: 4442805. DOI: 10.1083/jcb.201409142. View

Song X, Call G, Kirilly D, Xie T . Notch signaling controls germline stem cell niche formation in the Drosophila ovary. Development. 2007; 134(6):1071-80. DOI: 10.1242/dev.003392. View

Clough E, Tedeschi T, Hazelrigg T . Epigenetic regulation of oogenesis and germ stem cell maintenance by the Drosophila histone methyltransferase Eggless/dSetDB1. Dev Biol. 2014; 388(2):181-91. PMC: 4689207. DOI: 10.1016/j.ydbio.2014.01.014. View

Takashima S, Murakami R . Regulation of pattern formation in the Drosophila hindgut by wg, hh, dpp, and en. Mech Dev. 2001; 101(1-2):79-90. DOI: 10.1016/s0925-4773(00)00555-4. View

Housden B, Millen K, Bray S . Drosophila Reporter Vectors Compatible with ΦC31 Integrase Transgenesis Techniques and Their Use to Generate New Notch Reporter Fly Lines. G3 (Bethesda). 2012; 2(1):79-82. PMC: 3276196. DOI: 10.1534/g3.111.001321. View

Han Y, Shi Q, Jiang J . Multisite interaction with Sufu regulates Ci/Gli activity through distinct mechanisms in Hh signal transduction. Proc Natl Acad Sci U S A. 2015; 112(20):6383-8. PMC: 4443367. DOI: 10.1073/pnas.1421628112. View

Li F, Shi W, Capurro M, Filmus J . Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J Cell Biol. 2011; 192(4):691-704. PMC: 3044117. DOI: 10.1083/jcb.201008087. View

Sahai-Hernandez P, Nystul T . A dynamic population of stromal cells contributes to the follicle stem cell niche in the Drosophila ovary. Development. 2013; 140(22):4490-8. PMC: 3817939. DOI: 10.1242/dev.098558. View

10.

Blauwkamp T, Chang M, Cadigan K . Novel TCF-binding sites specify transcriptional repression by Wnt signalling. EMBO J. 2008; 27(10):1436-46. PMC: 2396397. DOI: 10.1038/emboj.2008.80. View

11.

Yan D, Wu Y, Yang Y, Belenkaya T, Tang X, Lin X . The cell-surface proteins Dally-like and Ihog differentially regulate Hedgehog signaling strength and range during development. Development. 2010; 137(12):2033-44. PMC: 2875843. DOI: 10.1242/dev.045740. View

12.

Dominguez M, Brunner M, Hafen E, Basler K . Sending and receiving the hedgehog signal: control by the Drosophila Gli protein Cubitus interruptus. Science. 1996; 272(5268):1621-5. DOI: 10.1126/science.272.5268.1621. View

13.

Sarkar A, Parikh N, Hearn S, Fuller M, Tazuke S, Schulz C . Antagonistic roles of Rac and Rho in organizing the germ cell microenvironment. Curr Biol. 2007; 17(14):1253-8. DOI: 10.1016/j.cub.2007.06.048. View

14.

Kirilly D, Wang S, Xie T . Self-maintained escort cells form a germline stem cell differentiation niche. Development. 2011; 138(23):5087-97. PMC: 3210492. DOI: 10.1242/dev.067850. View

15.

Wang X, Pan L, Wang S, Zhou J, McDowell W, Park J . Histone H3K9 trimethylase Eggless controls germline stem cell maintenance and differentiation. PLoS Genet. 2012; 7(12):e1002426. PMC: 3245301. DOI: 10.1371/journal.pgen.1002426. View

16.

Yan D, Lin X . Shaping morphogen gradients by proteoglycans. Cold Spring Harb Perspect Biol. 2010; 1(3):a002493. PMC: 2773635. DOI: 10.1101/cshperspect.a002493. View

17.

Morrison S, Spradling A . Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 2008; 132(4):598-611. PMC: 4505728. DOI: 10.1016/j.cell.2008.01.038. View

18.

Xie T . Control of germline stem cell self-renewal and differentiation in the Drosophila ovary: concerted actions of niche signals and intrinsic factors. Wiley Interdiscip Rev Dev Biol. 2013; 2(2):261-73. DOI: 10.1002/wdev.60. View

19.

Capurro M, Xu P, Shi W, Li F, Jia A, Filmus J . Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev Cell. 2008; 14(5):700-11. DOI: 10.1016/j.devcel.2008.03.006. View

20.

Bluske K, Vue T, Kawakami Y, Taketo M, Yoshikawa K, Johnson J . β-Catenin signaling specifies progenitor cell identity in parallel with Shh signaling in the developing mammalian thalamus. Development. 2012; 139(15):2692-702. PMC: 3392701. DOI: 10.1242/dev.072314. View