2021, Vol. 28 
2. 南京农业大学无锡渔业学院, 江苏 无锡 214081
2. Wuxi Fisheries College, Nanjing Agricultural University, Wuxi 214081, China
水产养殖业健康可持续发展离不开充足且稳定的鱼苗供应。鱼卵的品质直接影响其与精子结合后受精率、孵化率, 进而影响苗种成活率与质量。了解鱼类卵子质量的特点, 掌握其繁殖生物学规律, 不仅有助于满足鱼类扩繁需求, 也为新品种开发与选育提供技术支撑。
多项研究表明, 卵子质量受鱼体内在遗传因子与各种外源因子的影响。遗传因子主要有养殖品种或品系等[1,2,3], 外源因子主要有温度、光照周期以及亲鱼规格、育龄等[4,5,6]。卵泡发育过程一般可分为原始卵泡、初级卵泡、次级卵泡和成熟卵泡阶段。哺乳动物卵巢内的多数卵泡发育到一定阶段后停止发育并且退化, 发生卵泡闭锁。卵泡闭锁是卵母细胞优胜劣汰的一个重要的生理过程, 该过程可能在限制每个周期产生的卵数与提高卵子质量方面起着重要作用[7]。本文描述了鱼类卵巢发育过程, 卵子发生、成熟与排卵, 并重点介绍了卵泡闭锁对于鱼类繁殖力的影响及其潜在调控机制。
1 鱼类卵子发育 1.1 鱼类卵巢发育模式根据某一时期卵巢组织中卵母细胞的发育特点, 大多数鱼类可分为同步产卵型或非同步分批产卵型。同步产卵型鱼类在繁殖季节卵巢中通常存在两个发育阶段的卵母细胞: 初级卵母细胞(后期发育成卵子)与一批“同步”发育的次级卵母细胞或者卵黄发生期的卵母细胞(即将成熟的卵子)[8]。同步产卵的鱼类, 海水鱼如鲑(一年产一次卵)[9]和海鳟(Salmo trutta)[8]等, 淡水鱼如我国传统的四大家鱼等。非同步分批产卵型鱼类中, 卵子来源于不同阶段分批成熟的卵母细胞。此类鱼可以在繁育季节分批多次产卵, 海水鱼如海鲈(Dicentrarchus labrax)[10]、紫红笛鲷(Lutjanus argentimaculatus)[11]、狭鳞庸鲽(Hippoglossus stenolepis)[12]等; 淡水鱼如尼罗罗非鱼(Oreochromis niloticus) 13]、鲤(Cyprinus carpio) [14]和美洲鲥(Alosa sapidissima) [15]等。尼罗罗非鱼属于典型的非同步分批产卵型鱼类, 卵巢组织中存在I~IV期的卵母细胞。IV期成熟卵母细胞排出后, 卵巢内Ⅰ、Ⅱ和Ⅲ期卵子会很快启动促成熟程序, 向Ⅳ期成熟卵母细胞发育[13]。同时, 一些非同步分批产卵型鱼类为了适应环境变化, 卵巢发育模式发生了变化。雌性三刺鱼(Gasterosteus aculeatus williamsoni)和尖嘴鱼(Tylosurus crocodilus crocodilus)虽然在繁育季节分批多次排卵, 但在卵巢中仅存在3种卵母细胞: 原始细胞、快速生长的细胞(卵黄发生期)和即将成熟排出体外的细胞[16]。了解不同鱼类的排卵特点可为深入研究鱼类卵子发育与卵泡闭锁规律提供科学依据。
1.2 卵巢生长与卵子发育影响因素自然水体中, 同步产卵型鱼类在繁殖期间的性腺指数[性腺指数=性腺重量/(体重–性腺重量)×100]通常在18~25。有些鱼类可能具有较高的性腺指数(达到甚至超过40), 如日本鳗鲡(Anguilla japonica)[8]。然而, 在人工繁育条件下, 通过注入鲤垂体提取物, 欧洲鳗鲡(A. anguilla)可能具有更高的性腺指数(高于60)[17]。非同步分批产卵型鱼类的性腺指数通常小于同步产卵型鱼类(介于1~30之间), 其卵巢组织呈现出更有规律的周期性增长。尼罗罗非鱼(Oreochromis niloticus)的性腺指数最高很少超过5, 在繁育季节2次连续产卵之间, 其性腺指数可能在1~5之间反复, 增加5倍[18]。
繁殖季节, 鱼类卵巢中存在大量卵泡。卵泡的生长大致分为卵黄发生前期与卵黄形成期。卵母细胞中包含有大量初孵仔鱼发育所需的主要脂质和蛋白质营养物质[19]。卵黄发生前卵母细胞中性脂质开始积累, 这些脂质以脂肪滴的形式存在于卵母细胞中, 卵黄形成期, 富含磷脂的脂蛋白在卵母细胞内累积。卵黄形成期结束后, 卵母细胞内充满卵黄, 这些卵母细胞随后会成熟并排出体外。卵黄发生与形成期亲鱼的培育直接影响后期亲鱼的产卵量与卵子的受精率和孵化率[20]。同时, 适当调节环境因素或饲料蛋白水平, 改善饲料脂肪酸组成等有助于亲鱼产出高质量的卵子(图1)。
1.2.1 亲鱼来源对卵子发育的影响野生型亲鱼与人工选育的亲鱼, 由于其生存环境与食物链的差异, 造成卵子中类胡萝卜素、脂质或必需脂肪酸组成的不同, 特别是高度不饱和脂肪酸组成直接影响鱼类繁殖力与卵子质量[21,22]。在大西洋鳕(Gadus morhua L.)繁育中, 人工培育的亲鱼卵子受精率和孵化率远低于野生亲鱼的卵子。人工培育的亲鱼其卵子中较低的磷脂酰肌醇、花生四烯酸与类胡萝卜素水平可能影响了卵子的质量[23]。Czesny等[24]分析了来源于3个不同地区(一种人工培育群体与两种野生群体)的大眼狮鲈(Stizostedion vitreum)卵子, 发现两种野生群体卵子中较高的多不饱和脂肪酸含量可能有助于提高卵子质量, 增加初孵仔鱼的成活率。Ashton等[25]也发现, 野生型大鳞大麻哈鱼(Oncorhynchus tshawytscha)在天然海洋食物链下其卵子中较高的n-3/n-6脂肪酸比例有助于提高卵子质量。因此, 野生型亲本的食物来源更为广泛, 从而有助于提高卵子质量。
1.2.2 亲鱼育龄对卵子发育的影响多项研究表明, 生育年龄会影响哺乳动物卵子的质量[26]。例如, 青春期和第三次发情期后备母猪的卵子细胞遗传学比较显示, 与第三次发情期相比, 青春期的母猪排卵中未成熟卵子比例更大[27]。对于人类而言, 女性的生殖力从25岁到35岁下降了50%, 这可能与卵母细胞质量下降有关[26]。在鱼类中, 虹鳟(Oncorhynchus mykiss)第二次产卵的成活率明显高于第一次。同时, 3龄雌性虹鳟卵子受精后在发眼期的成活率(75%)显著高于2龄雌鱼的卵子(58%)[28]。在尼罗罗非鱼中, 24月龄的雌鱼产卵数量显著高于9月龄和16月龄的雌鱼, 但是两次产卵间隔时间延长, 卵子的受精率与孵化率均显著下降[4]。不同鱼类的性成熟时间差异可能影响亲本繁育时期的卵子质量。
1.2.3 环境因素对卵子发育的影响水温、光照周期、盐度和pH的变化影响鱼类卵子质量。水产养殖中, 调节光照周期可以促进或延迟鱼类产卵。Dabrowski等[29]研究发现, 延长光照时间可以延迟排卵, 增加虹鳟发眼卵的死亡率(从60%~ 80%范围下降至5%)。Taranger等[30]发现, 缩短光照时间(8L∶16D)有助于大西洋鲑(Salmo salar)提前排卵, 然而发眼卵的成活率仅为64.2%, 显著低于自然光照下的92.5%。Bonnet等[31]采用先长光后短光处理虹鳟雌鱼时发现, 调节光照强度显著降低卵子质量, 发眼期卵子的成活率从自然光照强度下的93%下降至49%。同时, 延长或缩短光照周期可能促进尼罗罗非鱼首次产卵时间提前, 但是繁殖效率显著低于自然光照周期下的繁殖效率[32]。
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图1 卵母细胞生长、卵巢成熟以及胚胎早期和晚期发生的重要事件概略图[19] Fig. 1 Overview of important events in oocyte growth, ovary maturation, and early and late embryogenesis[19] |
亲鱼产卵与卵子孵化期间, 水温可能通过改变卵子发育以及胚胎发育时代谢、活力和膜结构来影响受精卵的孵化率。温度影响大西洋大比目鱼(Hippoglossus hippoglossus)的产卵性能。水温为6 ℃时, 大比目鱼卵子活力显著高于其他温度。因此, 在自然水体中, 野生大比目鱼通常栖息于环境条件较为稳定的低温深水区[33]。Pountney等[34]发现, 高温(14 ℃)直接影响海参斑鱼(Cyclopterus lumpus)繁育亲本的卵子质量; 然而低温(6 ℃)会延长卵子发育周期, 降低胚胎活力。Ashton等[35]报道, 当水温从2 ℃上升到6 ℃, 江鳕(Lota lota)产卵期由18 d提前到6~7 d, 然而发眼卵的成活率由86.7%下降至0.1%。Tveiten等[36]也发现, 水温为12 ℃时, 狼鱼(Anarhichas lupus)正常卵裂的卵子(32细胞期)与发眼卵的成活率显著低于4 ℃与8 ℃的实验组。对于喜温性鱼类来说, 温度变化可能影响性腺的最终成熟与配子释放。产卵前、中、后期, 水温的异常或波动会破坏雌鱼的繁殖。当水温超出适宜温度时, 鱼类的性腺会延迟成熟或提前成熟。暖冬会导致一些第二年春末性成熟的鱼类提前早熟。然而低温经常会延迟产卵高峰期。相反, 鱼类最终性成熟期发生在高温环境时, 其排卵也会延迟或被抑制。
另外, 盐度也能影响卵子质量, 并能调节温度对于海水或半咸水鱼类胚胎发育的生理效应。例如, 盐度会影响欧鲽(Salvelinus alpinus)胚胎发育速率[37]。Atse等[37]发现, 天然海水培育的雌鱼与淡水培育雌鱼相比, 卵子内具有较多的蛋白质、脂肪与总能量物质, 因此有助于提高繁育成功率。盐度对卵母细胞膜渗透性的调节可能影响了胚胎发育。Su等[38]也发现, 金鼓鱼(Scatophagus argus)性腺成熟与胚胎早期发育所需的盐度存在差异: 在盐度25条件下, 雌鱼拥有最大性腺指数, 而其胚胎发育与仔鱼培育的最适盐度为15。因此, 适宜的光照周期、温度与盐度有助于促进雌鱼性腺发育, 提高胚胎发育速率和出苗率。
1.2.4 饲料营养对卵子发育的影响饲料营养成分也会影响鱼类卵子质量。饲料蛋白含量、脂肪含量(极性与非极性脂肪)、脂肪酸组成以及饲料中添加抗坏血酸、类胡萝卜素等均会影响卵子质量与胚胎存活。饲料蛋白含量对于不同鱼类卵子质量的影响存在一定的差异。饲料中粗蛋白含量会影响尼罗罗非鱼雌鱼的产卵时间、鱼苗存活率和脂质含量[39]。Al Hafedh等[40]发现, 将饲料蛋白含量增加到40%能显著提高尼罗罗非鱼雌鱼生长和初孵仔鱼存活率, 同时亲鱼的脂肪含量也会下降; 然而, 摄食低蛋白水平的尼罗罗非鱼实验组(25%~35%), 其繁殖力显著高于摄食高蛋白的实验组(40%~45%)。Watanabe等[41]也发现虹鳟摄食低蛋白饲料(30%)后, 其配子质量显著高于摄食高蛋白饲料组(57%)。Abidin 等[42]报道, 增加饲料蛋白水平有助于促进丝尾鳠(Mystus nemurus)雌鱼的生长与提高卵子质量。Afzal-Khan等[43]也发现, 南亚野鲮(Labeo rohita)摄食低蛋白水平饲料能显著降低GSI, 但不会影响卵的规格; 相对繁殖力、卵子的受精率和孵化率也随饲料蛋白的增加而上升。同时, Manissery等[44]和Santiago等[45]也发现增加饲料蛋白水平能够提高鲤与鳙(Aristichthys nobilis)的繁殖力与卵子受精率。
脂质不仅是细胞膜、能量存储和信号传导的重要组成成分, 同时, 在胚胎发育阶段, 脂质与蛋白质是卵黄的主要组成成分。脂质结构的多样性赋予了其丰富的生物学功能。同时, 某些脂质也是维生素的重要来源或载体。脂质作为亲鱼饲料的重要组成, 影响着卵子的质量、发育与初孵仔鱼的存活。Bentley等[46]研究发现, 增加饲料脂肪含量有助于提高美洲黑石斑鱼(Centropristis striata)受精卵的孵化成功率。Durland等[47]发现, 杂交鲇(Ictalurus punctatus×I. furcatus)摄食高脂肪饲料后, 其产卵数量增加, 卵的重量与卵径也更大。Bogevik等[48]也发现, 在胁迫环境下, 大西洋鳕摄食高脂肪的饲料比低脂肪饲料更有助于保持较高的受精率与孵化率。
多不饱和脂肪酸是胚胎发育的基础, 同时它们也是鱼类各器官形成的结构成分(如大脑、视网膜、肌肉等)[49,50]和生理活性分子的前体, 例如前列腺素等[51]。因此, 多不饱和脂肪酸是胚胎和仔鱼的发育与存活必需的[52]。然而, 不同鱼类对于脂肪酸组成和添加水平存在差异。n-3高不饱和脂肪酸(HUFA)对于亲鱼培养至关重要, 因为鱼体自身无法合成多不饱和脂肪酸。Carrillo等[53]发现改变亲鱼饲料脂质组成能显著提高卵子中n-3脂肪酸组成, 尤其是DHA与EPA含量, 从而提高卵子质量。Fernández-Palacios等[54]发现, 如果金头鲷(Sparus aurata)在产卵前摄食的饲料中缺乏n-3高不饱和脂肪酸, 成熟卵子活力会下降。同时, 饲料中n-3高不饱和脂肪酸水平与卵子极性与中性脂肪含量密切相关。Durland等[47]研究发现, 提高饲料中DHA、EPA与n-3脂肪酸含量有助于提高杂交鲇产卵数量以及卵径和卵重。淡水鱼类, 特别是喜温性鱼类, 亲鱼培育需要添加亚油酸18∶2(n-6)和α-亚麻酸18∶3(n-3), 而海洋鱼类需要二十碳五烯酸20∶5(n-3)和二十二碳六烯酸22∶6(n-3), 这些脂肪酸的变化影响着鱼类卵子质量与胚胎存活。
类胡萝卜素作为脂质的衍生物, 可以用于维生素A的重要来源与补充。在不缺乏维生素的情况下, 类胡萝卜素作为自由基的分解剂, 能够清除活性氧, 降低自由基对卵膜完整性的影响。饲料中缺乏维生素A会降低虹鳟繁殖性能, 阻碍卵子成熟、排卵与仔鱼发育[55]。由于目前未有直接证据表明类胡萝卜素添加会影响卵子质量, 不同物种, 或者添加不同类型的类胡萝卜素对卵子质量的影响存在差异。例如, Craik[56]研究发现, 饲料中低类胡萝卜素含量会影响虹鳟的卵子活力; 然而, 低类胡萝卜素含量不会影响大西洋鲑的卵子质量。同时, Watanabe等[57]研究发现, 添加虾青素(一种酮类胡萝卜素)可以提高红鲷(Lutjanus campechanus)的卵子质量, 但是添加β-类胡萝卜素对卵子质量没有影响。
亲鱼饲料中维生素A、维生素E(α-生育酚)、维生素C以及抗坏血酸的添加能够影响卵子质量。增加维生素E能够提高香鱼(Plecoglossus altivelis)与真鲷的卵子质量[58,59], 饲料缺乏维生素E会阻碍鲤和海鲷的性腺发育, 降低孵化率与仔鱼成活率[60,61]。Eskelinen[62]也报道, 增加饲料维生素C含量有助于提高大西洋鲑的卵子质量与初孵仔鱼成活率。饲料中维生素C的添加能够影响虹鳟胚胎发育过程中胶原蛋白的合成, 进而调节其繁殖性能。同时, 饲料中缺乏抗坏血酸会不利于大西洋鲑与虹鳟胚胎存活[62]。因此, 亲鱼培育期间的饲料营养组成可能会改变其卵子内蛋白、脂肪以及脂肪酸组成, 进而影响卵子的受精率和出苗率。
1.3 影响卵子质量的基因、miRNA与蛋白筛选母体基因转录物主要指的是在整个卵子发生过程中, 正在发育的卵母细胞中的mRNA。其中, 绝大多数的mRNA要在卵子受精后才能得到翻译与表达, 用于指导早期胚胎发育。随着转录组、蛋白质组学技术的应用与推广, 卵子发生过程中越来越多的调控基因被发掘。这些基因可能对卵子质量以及卵子与精子结合后几小时内的受精率至关重要。表1中列举了一些与鱼类卵子质量有关的基因。Tingaud-Sequeira等[63]采用基因芯片技术鉴定出118个差异表达的基因富集于塞内加尔鳎(Solea senegalensis)卵巢发育(卵黄形成)与成熟阶段。同时, 母体遗传物质的改变会影响斑马鱼(Danio rerio)与条纹鲈(Morone saxatilis)的胚胎存活和受精后的成活率。Chapman等[64]和Sullivan等[65]对转录组数据解析后均发现, 条纹鲈卵母细胞中的母体基因转录物与卵子质量密切相关。
文献资料显示, 泛素连接酶、26S-蛋白酶体通路、剪接体、细胞信号传导以及细胞分裂等的调控与卵子质量密切联系[64,65]。首先, 泛素连接酶将某些蛋白质指定为26S-蛋白酶体降解的蛋白质, 其中可能包括一些受损的蛋白质, 还有重要的信号分子, 其在细胞内的半衰期较短。这些信号分子中的许多是信号转导通路的成员, 例如有丝分裂原激活的蛋白激酶(MAPK或MAP激酶)和细胞周期蛋白。MAP激酶将信号从细胞膜受体传递到细胞核[66]。细胞周期蛋白是与细胞分裂周期相关的一大类蛋白质, 可调节细胞有丝分裂和减数分裂。Aegerter等[67]研究发现, 虹鳟卵母细胞中细胞周期蛋白B mRNA (CycB)的表达丰度在排卵后衰老的卵巢中显著增加; 在产卵时CycB基因的高表达水平会导致仔鱼的畸形率上升。Mathavan等[68]和Fernández等[69]发现, Cyclin-A2基因的表达水平在斑马鱼和金头鲷未受精的卵子与卵裂过程较高。同时, 发现产卵质量差的条纹鲈雌性卵巢中Cnnb3和Ccne2表达水平显著下调。细胞周期蛋白依赖性激酶是另一类重要的信号分子, 包括细胞周期调节因子, 参与调节基因转录、RNA加工和细胞分化。通常, 这些细胞周期调节蛋白在细胞中半衰期较短。因此, 这些蛋白在传递信息后会被26S-蛋白酶体泛素化并降解, 信号无法持续存在。在产卵质量差的条纹鲈雌性卵巢中, 所有与26S-蛋白酶体有关的基因通常是下调的[64]。细胞周期信号通路上的基因表达异常可能与卵子质量较差有关, 增加了早期胚胎死亡。最终, 剪接体参与RNA编辑以及转录和翻译的控制。许多调节蛋白不仅参与细胞周期和细胞分裂的调节, 还在剪接体中起作用。
miRNA是一类小的非编码RNA, 可以通过与一个或多个靶基因3′-UTR结合来调节其表达活性。随着更多的miRNA被鉴定和深入研究, 越来越多的证据表明, miRNA在鱼类卵子发育中扮演重要角色[70]。Juanchich等[71]鉴定出13个差异表达的miRNA存在于虹鳟卵子发生过程中, 同时一些差异表达的miRNA潜在的靶基因在卵子发生, 卵巢成熟或胚胎发生中起着重要作用。miR-301在鱼类卵子发生过程中显著下调, 其潜在的靶基因是类固醇生成的急性调节蛋白与组织蛋白酶D[71]。类固醇急性调节蛋白参与鱼类卵巢类固醇激素合成, 在胆固醇转运到线粒体、卵泡生长、卵母细胞成熟中发挥着重要作用[72]。虹鳟鱼卵母细胞成熟期间卵巢卵泡中的类固醇急性调节蛋白mRNA表达显著上调[73]。组织蛋白酶D在卵黄加工过程中具有重要的作用。miR-101、miR-15和miR-202可以靶向调节青鳉(Oryzias latipes)的生殖系a因子, 从而启动几种卵母细胞特异性基因的表达, 进而影响卵子的受精和早期胚胎存活[74,75]。孵化酶2作为miR-101的潜在靶基因, 在鱼类卵巢发育后期的高表达有助于卵壳消化[75]。同时, miR-449和miR-203在虹鳟鱼卵中差异表达, 这些miRNA与卵母细胞的凋亡有关[76]。在性腺发育成熟的尼罗罗非鱼卵巢中, miR-727、miR-129、miR-29家族的表达显著上调[77]。Wang等[78]发现两个新型miRNA: novel_77和novel_147在1龄、2龄、3龄黄颡鱼雌鱼性腺发育中特异性表达, 可用作鉴定性腺发育的重要标记。尽管近年来mRNA与miRNA基因在鱼类卵子发育中的作用研究取得了一定进展, 但是整体研究水平仍落后于哺乳动物, 很多基因的生物学功能与调控机制有待进一步阐明。
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表1 已鉴定的一些与卵子质量有关的基因 Tab. 1 Identified genes related to egg quality |
蛋白质组学是集中于动态描述基因调节, 对基因表达的蛋白质水平进行定量测定, 从而解释基因表达调控的机制。Yilmaz等[79]发现不同质量的斑马鱼卵子中具有明显的蛋白质组学差异, 这些差异蛋白的信号通路主要涉及蛋白质合成、能量和脂质代谢以及一些卵黄蛋白原生成和凝集素等。同时, 卵黄蛋白原在河鲈(Perca fluviatilis)卵子发育中也发挥着重要作用[80]。此外, 质量较差的斑马鱼卵子中上皮透明带蛋白以及一些涉及溶酶体活性、自噬、细胞凋亡和某些癌基因生成的蛋白表达呈现上调[79]。与溶酶体活性有关的蛋白质表达上调可能与卵黄的蛋白水解, 进而影响卵母细胞的最终成熟有关[79]。与癌基因功能相关的蛋白质上调可能与亲鱼出现应激, 促进卵母细胞凋亡有关[79]。其中有两种特异的核糖体蛋白(rpl36-001和rpl36-002)存在于质量较好的斑马鱼卵子中; 然而质量较差的卵子中存在另外4种特异的蛋白(微管蛋白zgc: 55461-001, 羰基还原酶cbr1-001, 酪蛋白激酶zgc: 86598-001以及2′,3′-环核苷酸3′-磷酸二酯酶cnp-201)[80]。同时, Castets等[80]也发现, 热休克蛋白, 尤其是HSP70家族的成员在繁殖力较高的河鲈卵巢组织中显著上调。因此, 这些蛋白质因子也可以作为评价卵子质量的重要指标。
2 鱼类卵泡闭锁卵泡的发育是卵泡生长与闭锁之间的动态平衡。卵泡生长分为5个阶段: (1) 卵原细胞的生长, 涉及放射带、颗粒和鞘膜细胞层的形成。(2) 脂质体、皮层内生膜囊的形成和多唾液酸糖蛋白的表达。(3) 卵黄发生, 导致卵泡生长; 在鱼类中, 卵母细胞大小的变化主要是由于摄取了卵黄蛋白原, 卵黄蛋白原由肝脏产生, 经血液循环运输到卵巢, 再进入卵母细胞。(4) 促性腺激素激增引发卵母细胞成熟, 刺激促成熟激素的产生和减数分裂的恢复。(5) 排卵: 卵母细胞在减数分裂II的中期停滞并排入卵巢腔[81]。卵泡闭锁常见于哺乳动物卵巢中, 然而鱼类卵巢中闭锁卵泡通常与环境胁迫或激素变化有关。鱼类卵泡闭锁从形态学角度常分为4个阶段: (1) 卵母细胞折叠与破裂, 颗粒细胞和/或鞘膜细胞肿大; (2) 滤泡细胞侵袭卵母细胞所占据的空间并消除细胞残余物; (3) 颗粒细胞变性和橙色色素的出现; (4) 卵泡闭锁与退化[82]。
2.1 闭锁卵泡的鉴定与分类依据Hunter and Macewicz的标准, 闭锁卵泡可分为3类: (1) α闭锁卵泡, 闭锁的第一个细胞学特征是卵母细胞核和细胞质细胞器的崩解, 然后是放射带(绒毛膜)破裂; (2) β闭锁卵泡, 放射带和卵黄小球被完全吸收, 该卵泡就被称为β闭锁卵泡[83]; (3) γ和δ闭锁卵泡, 一些可见的已闭锁卵泡[84]。α和β闭锁卵泡如图2所示。一般鱼类卵泡闭锁研究中, 通常考虑α闭锁卵泡。因为不同鱼类的α闭锁卵泡较为相似, 同时α闭锁向β闭锁转变的时间较短。α闭锁卵黄卵泡的数目为具有透明放射带和卵黄颗粒清晰可见的卵黄形成期卵泡的数目[83]。
02-0239-14-F002.jpg "点击查看原图") |
图2 吉富罗非鱼雌鱼成熟卵母细胞(A)与α闭锁卵泡和β闭锁卵泡(B)[85]A. 黑色箭头示成熟期卵母细胞; B. 蓝色箭头示α闭锁卵泡, 卵泡卵母细胞核和细胞质细胞器的解体, 然后是放射带的碎裂; 红色箭头示β闭锁卵泡, 卵泡卵母细胞结构完全消失. Fig. 2 Mature oocytes of genetically improved farmed female tilapia (GIFT, Oreochromis niloticus) (A) and atresia at α-stage and β-stage (B) (photos from our laboratory)[85]A. Black arrow shows mature oocytes. B. Blue arrow shows α-stage atresia, disintegration of the follicular oocyte nucleus and cytoplasmic organelles, and then fragmentation of the radiation zone. Red arrow shows β-stage atresia, the structure of the follicular oocyte completely disappeared. |
在非哺乳类脊椎动物, 尤其是硬骨鱼类中, 闭锁卵泡是野生雌鱼性腺常见的卵巢结构成分[86]。闭锁的强度, 即闭锁的卵黄发生期卵泡的比例在不同鱼类中差异较大, 主要取决于卵巢发育阶段、食物获取以及配子释放等[87]。同时, 许多外源因素也能诱导卵泡闭锁的发生, 如饥饿胁迫、pH、光照与温度调节、养殖密度等。Corriero等[87]采用3种应激方式(短期饥饿、长期网箱饲养和拥挤胁迫)研究野生蓝鳍金枪鱼(Thunnus thynnus)卵泡闭锁时发现, 短期饥饿与拥挤胁迫会降低卵巢重量, 增加α闭锁卵泡的比例。McCormick等[88]发现, 增加或降低水体pH会导致胖头鱥(Pimephales promelas)卵泡闭锁率增加, 降低繁育效率。人工养殖野外捕捞的鱼类会增加雌鱼性腺卵黄发生前与卵黄发生期卵泡闭锁的几率[89]。在一些养殖鱼类中, 闭锁主要发生在卵黄发生末期, 可以影响大多数卵黄卵母细胞。因此, 通过激素治疗可以防止卵母细胞变性并诱导卵母细胞成熟, 排卵和产卵[90]。
应激对卵巢发育与卵泡闭锁的影响机制尚不完全清楚, 大量研究表明, 胁迫对繁育的影响可能经由皮质醇介导。注射皮质醇会导致成熟的褐鳟和虹鳟以及不成熟的虹鳟的体重和性腺重量减少, 性类固醇的分泌量下降[91]。同时, 注射皮质醇也会降低莫桑比克罗非鱼(O. mossambicus)雌性血浆中的类固醇激素水平, 减少性腺重量和卵母细胞大小[92]。然而, 在虹鳟的体外研究中发现, 皮质醇可以抑制卵巢滤泡中的性类固醇激素的分泌与垂体中促性腺激素的分泌, 对于17β-雌二醇的调节却没有出现一致性的变化[93,94]。急性应激能够抑制鱼体性腺中的类固醇生成, 降低虹鳟等鱼类的卵子质量[95,96]。急性应激、慢性拥挤胁迫和高养殖密度会引起亲鱼血浆皮质醇和促肾上腺皮质激素激素增加, 降低血浆睾酮激素和17β-雌二醇水平[97]。Clearwater等[98]发现, 捕捞与空间胁迫会增加赤色绿鳍鱼(Chelidonichthys kumu)血浆皮质醇含量, 抑制17β-雌二醇和睾酮激素的水平, 提高卵黄发生期的卵泡闭锁比例。同时, 应激也会降低雌鱼性腺类固醇激素的生成, 进而抑制其繁殖力。在卵巢成熟期间, 频繁捕捞会导致雌鱼孕酮合成减少, 抑制排卵并引起繁育失败[19]。
养殖鱼类在极端胁迫情况下, 或当繁育的雌性亲鱼在其产卵期未能正常排卵时,易引起卵泡闭锁[99]。同时, 不适宜的养殖环境也易导致卵泡闭锁。闭锁是雌性鱼类中止产卵周期并重新吸收蛋黄营养的过程[99]。卵泡闭锁重要标志是卵巢组织中观察到的卵泡颗粒细胞层出现水肿, 这可能归因于卵巢细胞的凋亡。在闭锁后期, 卵破裂或缓慢分解, 因为卵母细胞重吸收的重要机制之一是产生绒毛膜溶血素酶, 从而破坏卵壳[100]。经历卵泡闭锁的雌鱼通常产生低质量的卵或畸形的胚胎, 大部分情况下无法正常受精。因此, 在亲鱼培育过程中, 应尽量减少胁迫源, 根据亲鱼的繁育特性与生殖周期进行培育, 从而保证获得高质量的卵子。
2.3 凋亡和自噬与鱼类卵泡闭锁程序性细胞死亡(programmed cell death, PCD)是多细胞生物体中一种受遗传调控且自主而有序的细胞死亡现象, 对于维持组织发育和体内平衡, 控制细胞数量和消除有害细胞至关重要[101]。细胞凋亡或I型细胞死亡是一种典型的PCD途径, 影响单个细胞脱离邻近细胞和基底膜[102,103]。自噬是一种高度调控的分解代谢过程, 可能与长寿蛋白质和细胞器的更新有关, 或者特异性针对损伤的细胞器[104,105]。细胞凋亡和自噬之间的关系十分复杂, 主要涉及与Bcl-2家族蛋白的相互作用[104]。在某些情况下, 自噬可作为避免细胞死亡的适应性调节。然而, 在绝大多数情况下, 自噬是细胞死亡的另一种途径, 称为自噬介导或II型程序性细胞死亡[106]。I型PCD的主要效应因子是含半胱氨酸的天冬氨酸蛋白水解酶, 通过激活Ca2+/Mg2+依赖性核酸内切酶, 可将DNA切割成180~200个碱基对的片段[102]。组织蛋白酶或蛋白酶体蛋白主要在II型PCD中具有活性, 而含半胱氨酸的天冬氨酸蛋白水解酶可能参与自噬后期的分解作用[107]。在营养和生长因子缺乏的情况下, 自噬的促生存功能已得到很好地验证, 然而这种分解代谢作用的确切机制尚不清楚。卵泡闭锁是由各种性激素控制的退化, 通过此程序, 哺乳动物卵巢卵泡丧失完整性, 并于排卵前消除。许多研究表明, 凋亡是消除哺乳动物卵巢滤泡闭锁和黄体溶解过程中颗粒细胞的主要作用机制。鱼类中的卵泡闭锁通常与环境胁迫或激素水平变化有关。尽管卵泡滤泡可以作为雌鱼受环境影响的重要指示, 但其卵泡闭锁的形成与调控机制尚未阐明。
3 卵子过熟卵子过度成熟也是影响卵子质量的重要因素之一, 尤其是在无法主动排卵, 需要人工协助排卵的养殖鱼类中。过度成熟的卵子可能在排卵后15~30 min丧失受精能力[19]。卵子过度成熟主要表现为排卵发生后, 卵母细胞以卵的形式从卵泡中释放出来, 从而无法从母体血液中获取营养和氧气。Mommens等[108]发现大西洋鲑卵子过度成熟会显著降低受精率与胚胎存活率, 增加仔鱼的畸形率。在一些鱼类的产卵季节, 如虹鳟、条纹鲈和罗非鱼等, 需要定期检查, 准确预测雌鱼的排卵时间, 通过人工挤卵的方式获取高质量的成熟卵子。同时, 检查亲鱼时需要轻柔缓慢, 避免对雌鱼造成胁迫, 进而影响卵子的质量。由于应激激素(例如肾上腺素和皮质醇)可能会抑制排卵时需要的GnRH和其他下游生殖激素, 因此需要着重关注和缓解操作压力和其他外源压力对亲鱼繁育的影响, 完善亲鱼繁育信息, 制定个性化的产卵方案, 包括营养需求、产卵诱导以及卵子过熟和闭锁的识别等。这对于全面了解影响卵子品质的因素至关重要, 也为后期建立、维持和改善产卵方案提供理论支撑。
4 展望卵泡闭锁是一种选择性的生理性细胞死亡过程, 保障了卵巢、卵泡、卵母细胞和胚胎的正常发育。正常发育的雌鱼卵巢中, 闭锁卵泡占25%~ 35%; 然而, 应激处理或亲鱼营养缺乏时, 闭锁卵泡可达55%~70%。闭锁卵泡比例的增加直接降低了鱼类高质量卵子数目。因此, 研究卵泡闭锁的调控机制与干预措施有助于更好地提高卵子质量。在鱼类卵子发育过程中, 研究者通常更多关注如何提高卵子质量, 对于闭锁卵泡的研究及其产生机制知之甚少, 闭锁卵泡的形成与调控的研究尚未成为关注的重点。在未来鱼类卵泡闭锁研究过程中,以下三方面值得关注: (1) 有关鱼类卵子发育的研究已从生殖激素、营养干预与环境调控等层面发展至关键基因与功能性miRNA和lncRNA筛选等分子层面, 但对于分子调控机制的研究还极为匮乏; (2) 随着测序技术的发展, 多组学联合研究必将有助于全面阐释鱼类卵泡闭锁相关基因功能及其调控通路; (3) 卵泡闭锁与鱼类繁育生理、神经内分泌等方面关系的研究也亟待加强。
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