An Unusual Architecture of Occluding Junctions between Surface Cells in Teleost Ovarian Follicles (&lt;i&gt;Plecoglossus altivelis&lt;/i&gt;)

Toshimori, Kiyotaka; Ōura, Chikayoshi

doi:10.1679/aohc1950.42.543

Cited by 2 publications

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“…In the Atlantic croaker (Micropogonias undulatus) [6,7] and the red sea bream (Pagrus major) [8], an increase in the number of GJs between granulosa cells and oocytes has been observed by electron microscopy during the acquisition of OMC. Additionally, in the ayu, the presence of gapjunction-like structures between granulosa cells and oocytes, and between granulosa cells themselves, has been confirmed by electron microscopy [9][10][11]. However, the detailed function of the GJs between granulosa cells and oocytes in the LH-induced acquisition of OMC has previously remained unclear.…”

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confidence: 88%

Heterologous Gap Junctions between Granulosa Cells and Oocytes in Ayu (Plecoglossus altivelis): Formation and Role during Luteinizing Hormone-dependent Acquisition of Oocyte Maturational Competence

Yamamoto

Yoshizaki

2008

J. Reprod. Dev.

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Abstract. Gap junctions (GJs) are intercellular channels. Molecules with a molecular weight of 1 kDa or less can pass back and forth between adjacent cells through GJs. Communication between oocytes and the somatic cells that surround them via GJs is known to play key roles to initiate oocyte maturation in many vertebrates. However, little is known of the detailed functions of ovarian GJs during oocyte maturation in fish. The oocyte maturation of fish is induced by a maturation-inducing steroid (MIS). The sensitivity of oocytes to the MIS is known as oocyte maturational competence (OMC) and is induced by luteinizing hormone (LH). However, LH receptors are found on the surface of granulosa cells rather than oocytes. We therefore proposed that the LH signals received by granulosa cells were passed to oocytes via GJs. This review describes current knowledge of the role of GJs between granulosa cells and oocytes during the LH-induced acquisition of OMC in fish. ammalian oocytes are surrounded by cumulus cells, and their maturation is induced by luteinizing hormone (LH) stimulation. By contrast, fish oocytes are surrounded by a layer of granulosa cells, a basement membrane, and a further layer of theca cells (Fig. 1). LH stimulates these two layers to produce a maturation-inducing steroid (MIS). Oocyte maturation is induced by direct stimulation from the MIS. In most fish, the MIS is thought to be either 17,20β, [1].Sensitivity of oocyte to MIS is known to be crucial for oocyte maturation in many teleost species including our model fish ayu (Plecoglossus altivelis). This sensitivity, which is known as oocyte maturational competence (OMC), is induced by LH [1,2] (Fig. 2). LH therefore has two important functions in oocyte maturation: inducing the acquisition of OMC by stimulating the oocytes, and inducing MIS synthesis by the follicle cells. LH-induced acquisition of OMC and the subsequent MIS-induced oocyte maturation are separate steps both physiologically and mechanistically [1,2]. We found that incubating ayu post-vitellogenic follicle-enclosed oocytes in a culture medium containing MIS did not induce oocyte maturation [3]. However, pre-treating the follicle-enclosed oocytes with a culture medium containing human chorionic gonadotropin (hCG), which is known to have an LH-like function, caused them to respond to MIS and induced oocyte maturation [3]. We therefore proposed that the ayu follicle-enclosed oocytes acquired OMC via LH stimulation. However, the LH receptors are localized on the surface of the follicle cells, and are not present on the oocytes themselves [4]. Therefore, the mechanism by which LH induces the acquisition of OMC in cells without receptors has previously remained unclear.Our research has focused on the channels known as gap junctions (GJs) that are formed between granulosa cells and oocytes. Ions and second-messenger molecules can pass freely through GJs by means of diffusion [5] (Fig. 1). In the Atlantic croaker (Micropogonias undulatus) [6,7] and the red sea bream (Pagrus major) [8], an in...

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confidence: 88%

Heterologous Gap Junctions between Granulosa Cells and Oocytes in Ayu (Plecoglossus altivelis): Formation and Role during Luteinizing Hormone-dependent Acquisition of Oocyte Maturational Competence

Yamamoto

Yoshizaki

2008

J. Reprod. Dev.

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“…The ayu (Plecoglossus altivelis) is an amphidromous teleost from East Asia. GJ-like structures have been observed between the oocytes and granulosa cells of this fish using electron microscopy (Toshimori and Ō ura, 1979;Toshimori and Yasuzumi, 1979a,b). Furthermore, the acquisition of OMC is known to be regulated by LH in this species (Soyano et al, 1996).…”

Section: Introductionmentioning

confidence: 94%

Differential expression and localization of four connexins in the ovary of the ayu (Plecoglossus Altivelis)

Yamamoto

Yoshizaki

Takeuchi

et al. 2007

Molecular Reproduction Devel

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The post-vitellogenic oocytes of teleost fish are generally unresponsive to maturation-inducing hormone (MIH) until a luteinizing hormone (LH) surge stimulates sensitivity via the acquisition of oocyte-maturational competence (OMC). Heterologous gap junctions (GJs) between granulosa cells and the oocyte have been previously implicated in the regulation of oocyte maturation in various vertebrate species. Although heterologous GJ are present in ovarian follicles of ayu (Plecoglossus altivelis), their role in maturation remains unclear. In the present study, we cloned and characterized complementary DNAs for GJ protein connexin (Cx), and examined the expression pattern of Cx messenger RNAs in the ayu ovary. Four Cx cDNAs with predicted molecular masses of 32.1 (Cx32.1), 34.9 (Cx34.9), 44.1 (Cx44.1), and 44.2 (Cx44.2) kDa, respectively, were cloned. Northern blot analysis revealed that the levels of Cx44.1 and Cx44.2 transcripts were similar during the vitellogenic and ovulatory stages. Cx32.1 transcripts were more abundant during the vitellogenic stage, but their levels declined thereafter. Cx34.9 transcript levels increased during the vitellogenic stage and remained high during the acquisition of OMC. In situ hybridization revealed that Cx44.1 and Cx44.2 signals were restricted to the oocyte, whereas the Cx32.1 and Cx34.9 signals were detected in both cellular fractions. Furthermore, a dye-transfer assay revealed the presence of functional GJs between the oocytes and follicle cells. These results suggest that Cx34.9 contributes to the formation of heterologous GJs between oocytes and granulosa cells. Moreover, GJs formed by Cx34.9 may function during the LH-dependent acquisition of OMC and the MIH-dependent resumption of meiosis in ayu.

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An Unusual Architecture of Occluding Junctions between Surface Cells in Teleost Ovarian Follicles (<i>Plecoglossus altivelis</i>)

Cited by 2 publications

References 8 publications

Heterologous Gap Junctions between Granulosa Cells and Oocytes in Ayu (Plecoglossus altivelis): Formation and Role during Luteinizing Hormone-dependent Acquisition of Oocyte Maturational Competence

Heterologous Gap Junctions between Granulosa Cells and Oocytes in Ayu (Plecoglossus altivelis): Formation and Role during Luteinizing Hormone-dependent Acquisition of Oocyte Maturational Competence

Differential expression and localization of four connexins in the ovary of the ayu (Plecoglossus Altivelis)

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