Wu Guan-Chung, Tomy Sherly, Nakamura Masaru, Chang Ching-Fong
Institute of Bioscience and Biotechnology, National Taiwan Ocean University, Keelung 202, Taiwan.
Biol Reprod. 2008 Dec;79(6):1111-20. doi: 10.1095/biolreprod.108.069146. Epub 2008 Jul 30.
Protandrous black porgy fish, Acanthopagrus schlegeli, have a striking life cycle, with male sex differentiation at the juvenile stage, a bisexual gonad during first 2 yr of life, and a male-to-female sex change (with vitellogenic oocytes) at 3 yr of age. The present study investigated the role of aromatase (cyp19a1a/Cyp19a1a) in gonadal development in this species, especially in relation to sexual differentiation and sex change. Fish of various ages were treated with estradiol (E2) or aromatase inhibitor (AI) to determine whether manipulation of the hormonal environment has an impact on these processes. We report an integrative immunohistochemical, cellular, and molecular data set describing these interesting phenomena. During male sex differentiation, high levels of cyp19a1a/Cyp19a1a expression were observed in the undifferentiated gonad (4 mo of age), in marked contrast to the low cyp19a1a/Cyp19a1a levels detected in the differentiated testis at the age of 5-6 mo. A low dose of E2 (0.25 mg/kg feed) stimulated testicular growth and function in sexually differentiated fish, whereas a high dose of E2 (6 mg/kg feed) induced female development. Furthermore, administration of AI suppressed male development and promoted female sexual differentiation. An increased number of figla transcripts (an oocyte-specific gene) were observed prior to cyp19a1a expression, concomitant with the development of oogonia and early primary oocytes in the ovaries of both E2- and AI-treated groups. Immunohistochemical Pcna staining showed that the regression of testicular tissue occurred prior to the development of ovarian tissue in both E2- and AI-induced females. The importance of cyp19a1a in female development was further demonstrated by the increase in cyp19a1a transcripts during the naturally occurring sex change. Transcripts of foxl2 increased in the gonads of 2- to 3-yr-old black porgy during the early stages of the natural sex change, followed by a gradual elevation of cyp19a1a levels. The levels of both genes peaked in the resulting ovarian tissue. Thus, cyp19a1a/Cyp19a1a plays dual roles in the gonadal development, namely, in testicular development during the initial period of sexual differentiation and later in ovarian development during the natural sex change.
雄性先熟的黑鲷（Acanthopagrus schlegeli）具有独特的生命周期，幼鱼阶段为雄性性别分化，生命的前两年具有两性性腺，3岁时发生雄性向雌性的性逆转（伴有卵黄生成期卵母细胞）。本研究调查了芳香化酶（cyp19a1a/Cyp19a1a）在该物种性腺发育中的作用，特别是与性别分化和性逆转的关系。用雌二醇（E2）或芳香化酶抑制剂（AI）处理不同年龄的鱼，以确定激素环境的改变是否会对这些过程产生影响。我们报告了一组综合的免疫组织化学、细胞和分子数据，描述了这些有趣的现象。在雄性性别分化期间，未分化性腺（4月龄）中观察到高水平的cyp19a1a/Cyp19a1a表达，这与5-6月龄分化睾丸中检测到的低cyp19a1a/Cyp19a1a水平形成鲜明对比。低剂量的E2（0.25 mg/kg饲料）刺激了性分化鱼的睾丸生长和功能，而高剂量的E2（6 mg/kg饲料）诱导了雌性发育。此外，AI的施用抑制了雄性发育并促进了雌性性别分化。在cyp19a1a表达之前，观察到figla转录本（一种卵母细胞特异性基因）数量增加，这与E2和AI处理组卵巢中卵原细胞和早期初级卵母细胞的发育同时发生。免疫组织化学Pcna染色显示，在E2和AI诱导的雌性中，睾丸组织的退化发生在卵巢组织发育之前。cyp19a1a在雌性发育中的重要性在自然发生的性逆转过程中cyp19a1a转录本的增加中进一步得到证明。在自然性逆转的早期阶段，2至3岁黑鲷性腺中foxl2转录本增加，随后cyp19a1a水平逐渐升高。这两个基因的水平在最终形成的卵巢组织中达到峰值。因此，cyp19a1a/Cyp19a1a在性腺发育中发挥双重作用，即在性别分化初期的睾丸发育中以及自然性逆转后期的卵巢发育中发挥作用。
