Gaston-Massuet Carles, McCabe Mark J, Scagliotti Valeria, Young Rodrigo M, Carreno Gabriela, Gregory Louise C, Jayakody Sujatha A, Pozzi Sara, Gualtieri Angelica, Basu Basudha, Koniordou Markela, Wu Chun-I, Bancalari Rodrigo E, Rahikkala Elisa, Veijola Riitta, Lopponen Tuija, Graziola Federica, Turton James, Signore Massimo, Mousavy Gharavy Seyedeh Neda, Charolidi Nicoletta, Sokol Sergei Y, Andoniadou Cynthia Lilian, Wilson Stephen W, Merrill Bradley J, Dattani Mehul T, Martinez-Barbera Juan Pedro
Birth Defects Research Centre, Developmental Biology and Cancer Programme, University College London Institute of Child Health, London, WC1N 1EH, United Kingdom;
Genetics and Epigenetics in Health and Disease Section, Genetics and Genomic Medicine Programme, University College London Institute of Child Health, London WC1N 1EH, United Kingdom;
Proc Natl Acad Sci U S A. 2016 Feb 2;113(5):E548-57. doi: 10.1073/pnas.1503346113. Epub 2016 Jan 13.
Aberrant embryonic development of the hypothalamus and/or pituitary gland in humans results in congenital hypopituitarism (CH). Transcription factor 7-like 1 (TCF7L1), an important regulator of the WNT/β-catenin signaling pathway, is expressed in the developing forebrain and pituitary gland, but its role during hypothalamo-pituitary (HP) axis formation or involvement in human CH remains elusive. Using a conditional genetic approach in the mouse, we first demonstrate that TCF7L1 is required in the prospective hypothalamus to maintain normal expression of the hypothalamic signals involved in the induction and subsequent expansion of Rathke's pouch progenitors. Next, we reveal that the function of TCF7L1 during HP axis development depends exclusively on the repressing activity of TCF7L1 and does not require its interaction with β-catenin. Finally, we report the identification of two independent missense variants in human TCF7L1, p.R92P and p.R400Q, in a cohort of patients with forebrain and/or pituitary defects. We demonstrate that these variants exhibit reduced repressing activity in vitro and in vivo relative to wild-type TCF7L1. Together, our data provide support for a conserved molecular function of TCF7L1 as a transcriptional repressor during HP axis development in mammals and identify variants in this transcription factor that are likely to contribute to the etiology of CH.
人类下丘脑和/或垂体的异常胚胎发育会导致先天性垂体功能减退(CH)。转录因子7样1(TCF7L1)是WNT/β-连环蛋白信号通路的重要调节因子,在发育中的前脑和垂体中表达,但其在下丘脑-垂体(HP)轴形成过程中的作用或与人类CH的关系仍不清楚。我们在小鼠中采用条件性基因方法,首先证明在前脑下丘脑中需要TCF7L1来维持参与拉特克囊祖细胞诱导和后续扩增的下丘脑信号的正常表达。接下来,我们揭示TCF7L1在HP轴发育过程中的功能仅取决于TCF7L1的抑制活性,而不需要其与β-连环蛋白的相互作用。最后,我们报告在一组患有前脑和/或垂体缺陷的患者中鉴定出人类TCF7L1中的两个独立错义变体,即p.R92P和p.R400Q。我们证明,相对于野生型TCF7L1,这些变体在体外和体内均表现出降低的抑制活性。总之,我们的数据支持了TCF7L1在哺乳动物HP轴发育过程中作为转录抑制因子的保守分子功能,并鉴定出该转录因子中可能导致CH病因的变体。