Evolution of Mammalian Opn5 as a Specialized UV-absorbing Pigment by a Single Amino Acid Mutation

Evolution of Mammalian Opn5 as a Specialized UV-absorbing Pigment by a Single Amino Acid Mutation
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DOI:
10.1074/jbc.m113.514075
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发表时间:
2014-02-14
影响因子:
4.8
通讯作者:
Shichida, Yoshinori
Shichida, Yoshinori
中科院分区:
生物学2区
文献类型:
--
作者:
Yamashita, Takahiro;Ono, Katsuhiko;Shichida, Yoshinori

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Opn5是最近发现的一种视蛋白群,它负责动物的非视觉光接受。我们之前的研究表明,哺乳动物Opn5 (Opn5m)的鸡同源物是一种G(i)偶联紫外传感器,具有双稳性色素的典型分子特性。在这里,我们证明了哺乳动物Opn5m通过失去双稳性色素的特征之一,直接结合全反式视网膜,进化成一个更专门的光敏器。我们首先证实了斑马鱼、热带爪蟾、小鼠和人类的Opn5m蛋白也是紫外线敏感色素。然后我们发现只有哺乳动物的Opn5m蛋白缺乏直接结合全反式视网膜的能力。突变分析表明,这些特征是通过在168位替换一个氨基酸获得的。通过比较哺乳动物和鸡的Opn5m的表达模式,我们发现哺乳动物的Opn5m与鸡的Opn5m一样,定位于视网膜神经节细胞层和内核层。然而,小鼠和灵长类动物(普通狨猴)的视蛋白并不分布在鸡Opn5m所在的下丘脑后部(包括沿第三脑室的区域),而是分布在视前下丘脑。有趣的是,RPE65,一种在视觉周期中形成11-顺式视网膜的必需酶,在小鼠和普通狨猴大脑的视前下丘脑附近表达,但不在鸡大脑表达Opn5m的区域附近表达。因此,哺乳动物的Opn5m在11-顺式视网膜供应系统的帮助下,可能只在大脑和视网膜中作为短波长的传感器工作。
Opn5 is one of the recently identified opsin groups that is responsible for nonvisual photoreception in animals. We previously showed that a chicken homolog of mammalian Opn5 (Opn5m) is a G(i)-coupled UV sensor having molecular properties typical of bistable pigments. Here we demonstrated that mammalian Opn5m evolved to be a more specialized photosensor by losing one of the characteristics of bistable pigments, direct binding of all-trans-retinal. We first confirmed that Opn5m proteins in zebrafish, Xenopus tropicalis, mouse, and human are also UV-sensitive pigments. Then we found that only mammalian Opn5m proteins lack the ability to directly bind all-trans-retinal. Mutational analysis showed that these characteristics were acquired by a single amino acid replacement at position 168. By comparing the expression patterns of Opn5m between mammals and chicken, we found that, like chicken Opn5m, mammalian Opn5m was localized in the ganglion cell layer and inner nuclear layer of the retina. However, the mouse and primate (common marmoset) opsins were distributed not in the posterior hypothalamus (including the region along the third ventricle) where chicken Opn5m is localized, but in the preoptic hypothalamus. Interestingly, RPE65, an essential enzyme for forming 11-cis-retinal in the visual cycle is expressed near the preoptic hypothalamus of the mouse and common marmoset brain but not near the region of the chicken brain where chicken Opn5m is expressed. Therefore, mammalian Opn5m may work exclusively as a short wavelength sensor in the brain as well as in the retina with the assistance of an 11-cis-retinal-supplying system.