Chen Katherine Q, Kawakami Hiroko, Anderson Aaron, Corcoran Dylan, Soni Aditi, Nishinakamura Ryuichi, Kawakami Yasuhiko
Department of Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, MN 55455, USA.
Stem Cell Institute, University of Minnesota, Minneapolis, MN 55455, USA.
Genetics. 2024 May 7;227(1). doi: 10.1093/genetics/iyae029.
Vertebrate limbs start to develop as paired protrusions from the lateral plate mesoderm at specific locations of the body with forelimb buds developing anteriorly and hindlimb buds posteriorly. During the initiation process, limb progenitor cells maintain active proliferation to form protrusions and start to express Fgf10, which triggers molecular processes for outgrowth and patterning. Although both processes occur in both types of limbs, forelimbs (Tbx5), and hindlimbs (Isl1) utilize distinct transcriptional systems to trigger their development. Here, we report that Sall1 and Sall4, zinc finger transcription factor genes, regulate hindlimb initiation in mouse embryos. Compared to the 100% frequency loss of hindlimb buds in TCre; Isl1 conditional knockouts, Hoxb6Cre; Isl1 conditional knockout causes a hypomorphic phenotype with only approximately 5% of mutants lacking the hindlimb. Our previous study of SALL4 ChIP-seq showed SALL4 enrichment in an Isl1 enhancer, suggesting that SALL4 acts upstream of Isl1. Removing 1 allele of Sall4 from the hypomorphic Hoxb6Cre; Isl1 mutant background caused loss of hindlimbs, but removing both alleles caused an even higher frequency of loss of hindlimbs, suggesting a genetic interaction between Sall4 and Isl1. Furthermore, TCre-mediated conditional double knockouts of Sall1 and Sall4 displayed a loss of expression of hindlimb progenitor markers (Isl1, Pitx1, Tbx4) and failed to develop hindlimbs, demonstrating functional redundancy between Sall1 and Sall4. Our data provides genetic evidence that Sall1 and Sall4 act as master regulators of hindlimb initiation.
脊椎动物的四肢最初是作为侧板中胚层在身体特定部位的成对突出物开始发育的,前肢芽在前部发育,后肢芽在后部发育。在起始过程中,肢体祖细胞保持活跃增殖以形成突出物,并开始表达Fgf10,这触发了肢体生长和模式形成的分子过程。尽管这两个过程在两种类型的肢体中都会发生,但前肢(Tbx5)和后肢(Isl1)利用不同的转录系统来触发它们的发育。在这里,我们报告锌指转录因子基因Sall1和Sall4调节小鼠胚胎中的后肢起始。与TCre; Isl1条件性敲除中后肢芽100%的缺失频率相比,Hoxb6Cre; Isl1条件性敲除导致一种亚效表型,只有约5%的突变体没有后肢。我们之前对SALL4 ChIP-seq的研究表明SALL4在一个Isl1增强子中富集,这表明SALL4在Isl1的上游起作用。从亚效的Hoxb6Cre; Isl1突变体背景中去除一个Sall4等位基因会导致后肢缺失,但去除两个等位基因会导致更高频率的后肢缺失,这表明Sall4和Isl1之间存在遗传相互作用。此外,TCre介导的Sall1和Sall4条件性双敲除显示后肢祖细胞标记物(Isl1、Pitx1、Tbx4)的表达缺失,并且无法发育出后肢,这证明了Sall1和Sall4之间的功能冗余。我们的数据提供了遗传证据,表明Sall1和Sall4作为后肢起始的主要调节因子发挥作用。