Ascorbate and dehydroascorbate influence cell cycle progression in a tobacco cell suspension

Ascorbate and dehydroascorbate influence cell cycle progression in a tobacco cell suspension
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DOI:
10.1104/pp.124.1.17
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发表时间:
2000-09-01
期刊:
影响因子:
7.4
通讯作者:
Asard, H
Asard, H
中科院分区:
生物学1区
文献类型:
--
作者:
Potters, G;Horemans, N;Asard, H

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除了众所周知的抗氧化特性外,抗坏血酸 (ASC) 还能够影响植物的正常细胞周期进程。在这项工作中,我们证明氧化分子脱氢抗坏血酸(DHA)是这方面的活性氧化还原形式。我们的结果表明,DHA 的减少可能是导致这种效果的第一步。在过去的几年中,越来越多的证据表明 ASC 在细胞分裂调节中的作用。例如,De Cabo 等人(1993)证明,由于单脱氢抗坏血酸的作用,分裂洋葱根分生组织细胞的 G1 期缩短。 Kerk 和 Feldman (1995) 能够在玉米 (Zea mays) 静止中心的 ASC 氧化还原状态和细胞增殖率之间建立直接相关性。此外,在烟草(Nicotiana tabacum L. cv Bright Yellow-2 [BY-2])细胞悬浮液的生长周期中,内源 ASC 水平显着下降,同时氧化还原状态总体下降(De Pinto 等人,1999 年;Kato 和 Esaka,1999 年)。 Kato 和 Esaka (1999) 通过证明 DHA 浓度出现瞬时峰值,并伴随 M 期 ASC 与 DHA 比率的降低,提供了进一步的证据,表明 ASC 可能介导的细胞周期氧化还原控制。这种增加还与 ASC 氧化酶表达的暂时增加相关。这些结果表明细胞内 DHA 水平可能通过 ASC 氧化酶的表达受细胞周期控制。此外,DHA 的减少也可能构成细胞进入 S 期的必要且积极的信号(Kato 和 Esaka,1999)。 De Pinto 等人 (1999) 还提出 DHA 作为质外体和细胞质之间的特定氧化还原连接的作用。由于 ASC 是质外体中的主要抗氧化剂,因此它很可能在质外体到细胞质的信号传导中发挥作用,这些信号与可能的应激环境的氧化特性有关。最近已证明高等植物细胞的质膜上存在 DHA 转运蛋白(Horemans 等,2000)。该转运蛋白协助细胞摄取质外体 DHA,这是由于质外体 ASC 在各种不同可能的氧化反应中被消耗而产生的;因此,转运蛋白可能会将质外体氧化还原状态传递到细胞内部。添加外部 DHA 可能会影响内部氧化还原平衡,可能是通过谷胱甘肽依赖性还原作用实现的。在这方面,Reichheld 等人 (1999) 提出了氧化应激检查点途径的存在,该途径控制环境应激条件下的细胞周期进程,并且似乎对一个或多个氧化还原传感系统有反应。例如,甲萘醌(已知会通过产生氧自由基引起氧化应激)已被证明会损害 BY-2 细胞的 G1/S 相变(Reichheld 等人,1999)。因此,ASC分子逐渐被认为不仅是一种重要的抗氧化剂,而且在植物细胞信号传导中也发挥着关键作用。
In addition to its well-known antioxidant properties, ascorbate (ASC) is capable of influencing normal cell cycle progression in plants. In this work we demonstrate that the oxidized molecule dehydroascorbate (DHA) is the active redox form in this respect. Our results indicate that the reduction of DHA might constitute the first step leading to this effect. During the last few years, evidence has already been accumulating, indicating the role of ASC in the regulation of cell division. For example, De Cabo et al.(1993) demonstrated a shortening of the G1 phase in dividing onion root meristem cells due to the action of monodehydroascorbate. Kerk and Feldman (1995) were able to establish a direct correlation between ASC redox status and cell proliferation rates in the maize (Zea mays) quiescent center. Also, during the growth cycle of a tobacco (Nicotiana tabacum L. cv Bright Yellow-2 [BY-2]) cell suspension, a significant decrease in the endogenous ASC level was shown, accompanied by an overall decrease in redox status (De Pinto et al., 1999; Kato and Esaka, 1999). Kato and Esaka (1999) provided further evidence pointing at a possible ASC-mediated redox control of the cell cycle by demonstrating a transient peak in the DHA concentration, with a concomitant decrease in the ASC to DHA ratio during M phase. This increase also correlated with a temporary increase in ASC-oxidase expression. These results suggested the hypothesis that intracellular levels of DHA might be controlled by the cell cycle through the expression of ASC-oxidase. In addition the decrease in DHA could also constitute a necessary and positive signal for the cell to proceed into S phase (Kato and Esaka, 1999). De Pinto et al.(1999) also suggested a role for DHA as a specific redox link between the apoplast and the cytoplasm. Because ASC is the major antioxidant in the apoplast, it is a likely candidate to play a role in the signaling from the apoplast to the cytoplasm related to the oxidative properties of a possibly stressful environment. The presence of a DHA transporter has recently been demonstrated at the plasma membrane of higher plant cells (Horemans et al., 2000). This transporter assists in the uptake into the cell of apoplastic DHA, resulting from the consumption of apoplastic ASC in a variety of different possible oxidative reactions; therefore, the transporter might relay the apoplastic redox status to the interior of the cell. The addition of external DHA is likely to affect the internal redox balances, possibly through its glutathione-dependent reduction. In this respect Reichheld et al.(1999) suggested the existence of an oxidative stress checkpoint pathway that controls cell cycle progression in environmental stress conditions and is seemingly responsive to one or more redoxsensing systems. For example, menadione (known to cause oxidative stress by generating oxygen radicals) has been shown to impair the G1/S phase transition in BY-2 cells (Reichheld et al., 1999). Thus, the ASC molecule is gradually considered not only an essential antioxidant, but it also plays a key role in plant cell signaling.