Sekiguchi Toshio, Kuwasako Kenji, Ogasawara Michio, Takahashi Hiroki, Matsubara Shin, Osugi Tomohiro, Muramatsu Ikunobu, Sasayama Yuichi, Suzuki Nobuo, Satake Honoo
From the Noto Marine Laboratory, Division of Marine Environmental Studies, Institute of Nature and Environmental Technology, Kanazawa University, Housu-gun, Ishikawa 927-0553, Japan,
the Frontier Science Research Center, University of Miyazaki, 5200 Kihara, Kiyotake, Miyazaki, Miyazaki 889-1692, Japan.
J Biol Chem. 2016 Jan 29;291(5):2345-56. doi: 10.1074/jbc.M115.664003. Epub 2015 Dec 7.
The calcitonin (CT)/CT gene-related peptide (CGRP) family is conserved in vertebrates. The activities of this peptide family are regulated by a combination of two receptors, namely the calcitonin receptor (CTR) and the CTR-like receptor (CLR), and three receptor activity-modifying proteins (RAMPs). Furthermore, RAMPs act as escort proteins by translocating CLR to the cell membrane. Recently, CT/CGRP family peptides have been identified or inferred in several invertebrates. However, the molecular characteristics and relevant functions of the CTR/CLR and RAMPs in invertebrates remain unclear. In this study, we identified three CT/CGRP family peptides (Bf-CTFPs), one CTR/CLR-like receptor (Bf-CTFP-R), and three RAMP-like proteins (Bf-RAMP-LPs) in the basal chordate amphioxus (Branchiostoma floridae). The Bf-CTFPs were shown to possess an N-terminal circular region typical of the CT/CGRP family and a C-terminal Pro-NH2. The Bf-CTFP genes were expressed in the central nervous system and in endocrine cells of the midgut, indicating that Bf-CTFPs serve as brain and/or gut peptides. Cell surface expression of the Bf-CTFP-R was enhanced by co-expression with each Bf-RAMP-LP. Furthermore, Bf-CTFPs activated Bf-CTFP-R·Bf-RAMP-LP complexes, resulting in cAMP accumulation. These results confirmed that Bf-RAMP-LPs, like vertebrate RAMPs, are prerequisites for the function and translocation of the Bf-CTFP-R. The relative potencies of the three peptides at each receptor were similar. Bf-CTFP2 was a potent ligand at all receptors in cAMP assays. Bf-RAMP-LP effects on ligand potency order were distinct to vertebrate CGRP/adrenomedullin/amylin receptors. To the best of our knowledge, this is the first molecular and functional characterization of an authentic invertebrate CT/CGRP family receptor and RAMPs.
降钙素(CT)/降钙素基因相关肽(CGRP)家族在脊椎动物中是保守的。该肽家族的活性由两种受体,即降钙素受体(CTR)和CTR样受体(CLR),以及三种受体活性修饰蛋白(RAMP)共同调节。此外,RAMP通过将CLR转运到细胞膜而作为护送蛋白。最近,在几种无脊椎动物中已鉴定或推断出CT/CGRP家族肽。然而,无脊椎动物中CTR/CLR和RAMP的分子特征及相关功能仍不清楚。在本研究中,我们在基部脊索动物文昌鱼(佛罗里达文昌鱼)中鉴定出三种CT/CGRP家族肽(Bf-CTFP)、一种CTR/CLR样受体(Bf-CTFP-R)和三种RAMP样蛋白(Bf-RAMP-LP)。Bf-CTFP显示具有CT/CGRP家族典型的N端环状区域和C端Pro-NH2。Bf-CTFP基因在中枢神经系统和中肠内分泌细胞中表达,表明Bf-CTFP作为脑和/或肠肽发挥作用。与每种Bf-RAMP-LP共表达可增强Bf-CTFP-R的细胞表面表达。此外,Bf-CTFP激活Bf-CTFP-R·Bf-RAMP-LP复合物,导致cAMP积累。这些结果证实,Bf-RAMP-LP与脊椎动物RAMP一样,是Bf-CTFP-R功能和转运的先决条件。三种肽在每个受体上的相对效价相似。在cAMP测定中,Bf-CTFP2是所有受体的有效配体。Bf-RAMP-LP对配体效价顺序的影响与脊椎动物CGRP/肾上腺髓质素/胰淀素受体不同。据我们所知,这是对真正的无脊椎动物CT/CGRP家族受体和RAMP的首次分子和功能表征。