Cell fate specification along the anterior–posterior axis of the intermediate mesoderm

Abstract

The vertebrate intermediate mesoderm (IM) is highly patterned along the anterior-posterior (A-P) axis. In the chick embryo, the kidney tissue, which is a derivative of the IM, is generated only from IM located posterior to the sixth somite axial level, which also marks the border between cranial and trunk segments. The cellular and molecular mechanisms that govern the formation of the anterior border of the kidney morphogenetic field are currently unknown. In this study, we asked whether specific A-P patterning information is conveyed by the movement of cells through the primitive streak (PS) at different time points that consequently affects the expression of kidney genes, or by the environment that these cells encounter during their migration to the IM. In this study, we show that kidney-inductive signals are present along the whole axis, including anterior non-kidney-generating regions. These inductive signals are generated by tissues that are located medial to the anterior IM. We also demonstrate that cells that migrate through the PS of early embryonic stages (Hamburger and Hamilton stage 3-4 and earlier), which will give rise to anterior nonkidney IM, are competent to respond to these inductive factors. This prospective anterior IM tissue loses its competence to respond to kidney inducing signals during its migration from the PS to its final location in the anterior IM. We present here a model in which changes in cell competence determine the formation of the anterior border of kidney gene expression and discuss the possible evolutionary implications of this developmental mechanism. Developmental Dynamics 232:901-914, 2005.

Comparative spatiotemporal analysis of Hox gene expression in early stages of intermediate mesoderm formation

“…Although the focus and theme of this article is Hox gene expression in early stages of kidney field specification, we also describe the kinetics of the expression of these genes in other mesodermal tissues. This is particularly important as several previous studies, including studies from our lab, show the crucial effect of neighboring tissues on IM specification at early developmental stages and the establishment of the kidney morphogenetic field (Mauch et al, 2000;Obara-Ishihara et al, 1999; and Schultheiss, 2003Barak et al, 2005;Preger-Ben Noon et al, 2009).…”

“…The embryonic patterning events governing the formation of the pronephric primordium (the anteriormost part of the developing kidney field) in chick IM have been documented in several publications, including Mauch et al (2000), Obara (2006), and Barak et al (2005). A detailed fate mapping of the primitive streak (PS) shows that prospective IM cells migrate from a narrow region, approximately 1/3 to 1/2 the length of the PS posterior to Hensen's node (Hn; Garcia-Martinez and Schoenwolf, 1992;Psychoyos and Stern, 1996;James and Schultheiss, 2003) ( Fig.…”

“…Cells forming the kidney duct primordium (IM adjacent to somites 7-10) leave the PS at HH stage 5/6. While still in the PS, the prospective IM has the potential to develop into a kidney fate but requires extrinsic signals to become specify (a degree of the determination state; Slack, 1983;Barak et al, 2005). These signals, including Activin/nodal like factors, are emanating from the dorsal neural tube along the entire axis including anterior non-kidney generating IM (Barak et al, 2005;Preger-Ben Noon et al, 2009).…”

“…While still in the PS, the prospective IM has the potential to develop into a kidney fate but requires extrinsic signals to become specify (a degree of the determination state; Slack, 1983;Barak et al, 2005). These signals, including Activin/nodal like factors, are emanating from the dorsal neural tube along the entire axis including anterior non-kidney generating IM (Barak et al, 2005;Preger-Ben Noon et al, 2009). Moreover, HH stage 4 PS cells that fate anterior non-kidney IM are competent to respond to these signals and express the kidney markers, Pax2 and Lim1, if they are bridged over their migratory pathway and are transplanted directly into the anterior non-kidney IM.…”

“…Moreover, HH stage 4 PS cells that fate anterior non-kidney IM are competent to respond to these signals and express the kidney markers, Pax2 and Lim1, if they are bridged over their migratory pathway and are transplanted directly into the anterior non-kidney IM. (Barak et al, 2005). A recent study has shown the role that Hoxb4 is playing in conferring the competence of IM cells to respond to kidney-inductive signals and specify them into becoming pronephric tissue (Preger-Ben Noon et al, 2009).…”