TY - JOUR
T1 - Jak-STAT regulation of cyst stem cell development in the Drosophila testis
AU - Sinden, D.
AU - Badgett, M.
AU - Fry, J.
AU - Jones, T.
AU - Palmen, R.
AU - Sheng, X.
AU - Simmons, A.
AU - Matunis, E.
AU - Wawersik, M.
N1 - Funding Information:
We are grateful to all our colleagues who have supplied us with suggestions, antibodies, stocks and technical assistance. We would also like to acknowledge the Bloomington Stock Center at the Indiana University for maintaining and providing fly stocks, and the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biology. We specifically thank Andrea Lin and Rebecca Obniski for assistance with analysis of adult testes, as well as Stephen DiNardo, Mark Van Doren, Mathias Leu and members of the Wawersik and Matunis labs for helpful discussions. This work was supported by NSF Grant no. IOS-0823151 (MW), NIH Grant no. RO1HD040307 (EM), William & Mary Summer Research Grants (DS and MB), and the HHMI Undergraduate Science Education Program (Summer Research Grants to JF & TJ).
PY - 2012/12/1
Y1 - 2012/12/1
N2 - Establishment and maintenance of functional stem cells is critical for organ development and tissue homeostasis. Little is known about the mechanisms underlying stem establishment during organogenesis. Drosophila testes are among the most thoroughly characterized systems for studying stem cell behavior, with germline stem cells (GSCs) and somatic cyst stem cells (CySCs) cohabiting a discrete stem cell niche at the testis apex. GSCs and CySCs are arrayed around hub cells that also comprise the niche and communication between hub cells, GSCs, and CySCs regulates the balance between stem cell maintenance and differentiation. Recent data has shown that functional, asymmetrically dividing GSCs are first established at ~23. h after egg laying during Drosophila testis morphogenesis (Sheng et al., 2009). This process correlates with coalescence of the hub, but development of CySCs from somatic gonadal precursors (SGPs) was not examined. Here, we show that functional CySCs are present at the time of GSC establishment, and that Jak-STAT signaling is necessary and sufficient for CySC maintenance shortly thereafter. Furthermore, hyper-activation of Jak in CySCs promotes expansion of the GSC population, while ectopic Jak activation in the germline induces GSC gene expression in GSC daughter cells but does not prevent spermatogenic differentiation. Together, these observations indicate that, similar to adult testes, Jak-STAT signaling from the hub acts on both GSCs and CySC to regulate their development and differentiation, and that additional signaling from CySCs to the GSCs play a dominant role in controlling GSC maintenance during niche formation.
AB - Establishment and maintenance of functional stem cells is critical for organ development and tissue homeostasis. Little is known about the mechanisms underlying stem establishment during organogenesis. Drosophila testes are among the most thoroughly characterized systems for studying stem cell behavior, with germline stem cells (GSCs) and somatic cyst stem cells (CySCs) cohabiting a discrete stem cell niche at the testis apex. GSCs and CySCs are arrayed around hub cells that also comprise the niche and communication between hub cells, GSCs, and CySCs regulates the balance between stem cell maintenance and differentiation. Recent data has shown that functional, asymmetrically dividing GSCs are first established at ~23. h after egg laying during Drosophila testis morphogenesis (Sheng et al., 2009). This process correlates with coalescence of the hub, but development of CySCs from somatic gonadal precursors (SGPs) was not examined. Here, we show that functional CySCs are present at the time of GSC establishment, and that Jak-STAT signaling is necessary and sufficient for CySC maintenance shortly thereafter. Furthermore, hyper-activation of Jak in CySCs promotes expansion of the GSC population, while ectopic Jak activation in the germline induces GSC gene expression in GSC daughter cells but does not prevent spermatogenic differentiation. Together, these observations indicate that, similar to adult testes, Jak-STAT signaling from the hub acts on both GSCs and CySC to regulate their development and differentiation, and that additional signaling from CySCs to the GSCs play a dominant role in controlling GSC maintenance during niche formation.
KW - Cyst stem cell
KW - Gametogenesis
KW - Jak-STAT
KW - Organogenesis
KW - Stem cell niche
KW - Testis
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U2 - 10.1016/j.ydbio.2012.09.009
DO - 10.1016/j.ydbio.2012.09.009
M3 - Article
C2 - 23010510
AN - SCOPUS:84867901890
SN - 0012-1606
VL - 372
SP - 5
EP - 16
JO - Developmental biology
JF - Developmental biology
IS - 1
ER -