Sallon Céline, Callebaut Isabelle, Boulay Ida, Fontaine Joel, Logeart-Avramoglou Delphine, Henriquet Corinne, Pugnière Martine, Cayla Xavier, Monget Philippe, Harichaux Grégoire, Labas Valérie, Canepa Sylvie, Taragnat Catherine
From the Unité Physiologie de la Reproduction et des Comportements, UMR85, Institut National de la Recherche Agronomique, CNRS, Institut Français du Cheval et de l'Equitation, Université de Tours, F-37380 Nouzilly, France.
CNRS UMR 7590, Sorbonne Universités, Université Pierre et Marie Curie-Paris 6, MNHN-IRD-IUC, F-75005 Paris, France.
J Biol Chem. 2017 Sep 15;292(37):15352-15368. doi: 10.1074/jbc.M116.736207. Epub 2017 Jul 26.
Bone morphogenetic proteins (BMPs) regulate diverse cellular responses during embryogenesis and in adulthood including cell differentiation, proliferation, and death in various tissues. In the adult pituitary, BMPs participate in the control of hormone secretion and cell proliferation, suggesting a potential endocrine/paracrine role for BMPs, but some of the mechanisms are unclear. Here, using a bioactivity test based on embryonic cells (C3H10T1/2) transfected with a BMP-responsive element, we sought to determine whether pituitary cells secrete BMPs or BMP antagonists. Interestingly, we found that pituitary-conditioned medium contains a factor that inhibits action of BMP-2 and -4. Combining surface plasmon resonance and high-resolution mass spectrometry helped pinpoint this factor as thrombospondin-1 (TSP-1). Surface plasmon resonance and co-immunoprecipitation confirmed that recombinant human TSP-1 can bind BMP-2 and -4 and antagonize their effects on C3H10T1/2 cells. Moreover, TSP-1 inhibited the action of serum BMPs. We also report that the von Willebrand type C domain of TSP-1 is likely responsible for this BMP-2/4-binding activity, an assertion based on sequence similarity that TSP-1 shares with the von Willebrand type C domain of Crossveinless 2 (CV-2), a BMP antagonist and member of the chordin family. In summary, we identified for the first time TSP-1 as a BMP-2/-4 antagonist and presented a structural basis for the physical interaction between TSP-1 and BMP-4. We propose that TSP-1 could regulate bioavailability of BMPs, either produced locally or reaching the pituitary via blood circulation. In conclusion, our findings provide new insights into the involvement of TSP-1 in the BMP-2/-4 mechanisms of action.
骨形态发生蛋白(BMPs)在胚胎发育和成年期调节多种细胞反应,包括各种组织中的细胞分化、增殖和死亡。在成年垂体中,BMPs参与激素分泌和细胞增殖的控制,提示BMPs可能具有潜在的内分泌/旁分泌作用,但其中一些机制尚不清楚。在此,我们利用基于转染了BMP反应元件的胚胎细胞(C3H10T1/2)的生物活性测试,试图确定垂体细胞是否分泌BMPs或BMP拮抗剂。有趣的是,我们发现垂体条件培养基中含有一种抑制BMP-2和-4作用的因子。结合表面等离子体共振和高分辨率质谱法有助于确定该因子为血小板反应蛋白-1(TSP-1)。表面等离子体共振和共免疫沉淀证实重组人TSP-1可结合BMP-2和-4并拮抗它们对C3H10T1/2细胞的作用。此外,TSP-1抑制血清BMPs的作用。我们还报告TSP-1的血管性血友病因子C结构域可能负责这种BMP-2/4结合活性,这一论断基于TSP-1与无横纹2(CV-2)的血管性血友病因子C结构域的序列相似性,CV-2是一种BMP拮抗剂,属于脊索蛋白家族成员。总之,我们首次确定TSP-1为BMP-2/-4拮抗剂,并提出了TSP-1与BMP-4之间物理相互作用的结构基础。我们提出TSP-1可能调节局部产生或通过血液循环到达垂体的BMPs的生物利用度。总之,我们的研究结果为TSP-1参与BMP-2/-4作用机制提供了新的见解。