产蛋期鸟类蛋壳钙化的钙离子转运：机制及其调控

Calcium transport in strongly calcifying laying birds: Mechanisms and regulation

产蛋期鸟类蛋壳钙化的钙离子转运：机制及其调控

Author links open overlay panel Arie Bar¹

Institute of Animal Science, ARO, the Volcani Ctr., Bet Dagan 50250, Israel

Received 15 October 2008, Revised 25 November 2008, Accepted 25 November 2008, Available online 6 December 2008.

Abstract

Birds that lay long clutches, among them the high-producing, strongly-calcifying domestic hen, transfer about 10% of their total body calcium daily. They appear, therefore, to be the most efficient calcium-transporters among vertebrates. Such intensive transport imposes severe demands on ionic calcium (Ca²⁺) homeostasis, and activates at least two extremely effective mechanisms for Ca²⁺ transfer from food and bone to the eggshell.

其中高产蛋长爪鸟类，例如强钙化的家养母鸡，每天需要转运全身约10％的钙。因此，它们似乎是脊椎动物中最有效的钙转运蛋白。这种强化运输对离子钙（Ca2 +）动态平衡提出了严格的要求，并激活了至少两种非常有效的从食物和骨骼向蛋壳转移的Ca2 +机制。

Birds that lay long clutches (series of eggs laid sequentially before a “pause day”), among them the high-producing, strongly-calcifying Gallus gallus domesticus (domestic hen) and Coturnix coturnix japonica (Japanese quail), transfer about 10% of their total body calcium daily. They appear, therefore, to be the most efficient calcium-transporters among vertebrates. Such intensive transport imposes severe demands on ionic calcium (Ca²⁺) homeostasis, and activates at least two extremely effective mechanisms for Ca²⁺ transfer from food and bone to the eggshell.

在一个“暂停日”之前依次产下一系列鸡蛋，其中包括长爪的高产鸟类，强烈钙化的原鸡属的家鸡（家养母鸡）和鹑属的日本鹌鹑（日本鹌鹑），需要每天转移约它们全身10％的钙。因此，它们似乎是脊椎动物中最有效的钙转运蛋白。这种强化运输对离子钙（Ca2 +）动态平衡提出了严格的要求，并激活了至少两种非常有效的从食物和骨骼向蛋壳转移的Ca2 +机制。

This review focuses on the development, action and regulation of the mechanisms associated with paracellular and transcellular Ca²⁺ transport in the intestine and the eggshell gland (ESG); it also considers some of the proteins (calbindin, Ca²⁺ATPase, Na⁺/Ca²⁺ exchange, epithelial calcium channels (TRPVs), osteopontin and carbonic anhydrase (CA) associated with this phenomenon. Calbindins are discussed in some detail, as they appear to be a major component of the transcellular transport system, and as only they have been studied extensively in birds.

本综述侧重于与肠和蛋壳（ESG）中细胞旁和跨细胞Ca2 +转运有关的机制的发展，作用和调控;它还考虑了与这种现象相关的一些蛋白质（钙结合蛋白，Ca2 + ATP酶，Na + / Ca2 +交换，上皮钙离子通道（TRPV），骨桥蛋白和碳酸酐酶（CA）），详细讨论Calbindins，因为它们似乎是这是跨细胞运输系统的一个主要组成部分，只有它们在鸟类中被广泛研究。

The review aims to gather old and new knowledge, which could form a conceptual basis, albeit not a completely accepted one, for our understanding of the mechanisms associated with this phenomenon. In the intestine, the transcellular pathway appears to compensate for low Ca²⁺ intake, but in birds fed adequate calcium the major drive for calcium absorption remains the electrochemical potential difference (ECPD) that facilitates paracellular transport. However, the mechanisms involved in Ca²⁺ transport into the ESG lumen are not yet established. In the ESG, the presence of Ca²⁺-ATPase and calbindin—two components of the transcellular transport pathway—and the apparently uphill transport of Ca²⁺ support the idea that Ca²⁺ is transported via the transcellular pathway. However, the positive (plasma with respect to mucosa) electrical potential difference (EPD) in the ESG, among other findings, indicates that there may be major alternative or complementary paracellular passive transport pathways. The available evidence hints that the flow from the gut to the ESG, which occurs during a relatively short period (11 to 14 h out the 24- to 25.5-h egg cycle), is primarily driven by carbonic anhydrase (CA) activity in the ESG, which results in high HCO₃⁻ content that, in turn, “sucks out” Ca²⁺ from the intestinal lumen via the blood and ESG cells, and deposits it in the shell crystals. The increased CA activity appears to be dependent on energy input, whereas it seems most likely that the Ca²⁺ movement is secondary, that it utilizes passive paracellular routes that fluctuate in accordance with the appearance of the energy-dependent CA activity, and that the level of Ca²⁺ movement mimics that of the CA activity. The on-off signals for the overall phenomenon have not yet been identified.

审查旨在收集新旧知识，这可能形成一个概念基础，虽然不是完全可以接受的概念基础，但我们理解与此现象相关的机制。在肠道中，跨细胞途径似乎弥补了低Ca2 +的摄入量，但在饲喂足够钙的鸡中，钙吸收的主要驱动力仍然是促进细胞外转运的电化学电位差（ECPD）。然而，Ca2 +转运入ESG腔的机制尚未确定。在ESG中，Ca2 + -ATPase和calbindin-2跨细胞转运通路的组成部分的存在以及Ca2 +明显上升的转运支持Ca2 +通过跨细胞途径转运的观点。然而，ESG中的阳性（与粘膜相关的血浆）电位差（EPD）等发现表明，可能存在主要的替代或补充的细胞旁被动转运通路。现有的证据表明，从相对较短的时间（从24到25.5小时的蛋循环中出现11到14小时），从肠道流向ESG主要由碳酸酐酶（CA）活性驱动ESG，这导致高HCO3-含量，反过来，通过血液和ESG细胞从肠腔“吸走”Ca2 +，并将其沉积在壳晶体中。增加的CA活动似乎取决于能量输入，而它最有可能的是Ca2 +运动是次要的，它利用被动细胞旁路线，其根据能量依赖性CA活动的出现而波动，并且水平Ca2 +运动模拟CA活动的运动。整体现象的开关信号尚未确定。

They appear to be associated with the circadian cycle of gonadal hormones, coupled with the egg cycle: it is most likely that progesterone acts as the “off” signal, and that the “on” signal is provided by the combined effect of an as-yet undefined endocrine factor associated with ovulation and with the mechanical strain that results from “egg white” formation and “plumping”. This strain may initially trigger the formation of the mammillae and the seeding of shell calcium crystals in the isthmus, and thereafter initiate the formation of the shell in the ESG.