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狒狒月经周期中输卵管上皮形态和聚糖模式的改变

Modification of Morphology and Glycan Pattern of the Oviductal Epithelium of Baboon during the Menstrual Cycle.

作者信息

Desantis Salvatore, Albrizio Maria, Lacitignola Luca, Laricchiuta Pietro, Cinone Mario

机构信息

Department of Emergency and Organ Transplantation (DETO), University of Bari Aldo Moro, S.P. Casamassima Km 3, 70010 Valenzano, Italy.

Safari Zoo, 72015 Fasano, Italy.

出版信息

Animals (Basel). 2022 Oct 14;12(20):2769. doi: 10.3390/ani12202769.

Abstract

The mammalian oviduct is a highly specialized structure where fertilization and early embryonic development occur. Its mucosal epithelium is involved in maintaining and modulating a dynamic intraluminal fluid. The oviductal epithelium consists of ciliated and non-ciliated (secretory) cells whose differentiation and activity are sex hormone-dependent. In this study, we investigated for the first time both the morphology and the glycan composition of baboon oviductal epithelium during the menstrual cycle. Oviducts were laparoscopically removed from 14 healthy adult female whose menstrual cycle phase was assessed based on the sex hormone levels and the vaginal cytology features. Histological investigations were carried out on fimbriae, infundibulum, ampulla, and isthmus separately fixed in 4% (/) paraformaldehyde, embedded in paraffin wax, and stained with hematoxylin-eosin for morphological analyses and using a panel of nine fluorescent lectins for glycoconjugate characterization. The histomorphological analysis revealed that in the entire oviduct (i) the ciliated and non-ciliated cells were indistinguishable during the follicular and luteal phases, whereas they were highly differentiated during the preovulatory phase when the non-ciliated cells exhibited apical protrusions, (ii) the epithelium height was significantly higher in the preovulatory phase compared to other menstrual phases, and (iii) the number of ciliated cells significantly ( ≤ 0.05) increased from the fimbriae to the infundibulum and progressively reduced in the other oviductal segments with the lower presence of ciliated cells in the isthmus. The glycan characterization revealed a complex and region-specific composition during the different phases of the menstrual cycle. It can be summarized as follows: (i) high-mannosylated N-linked glycans (Con A reactivity) were present throughout the oviductal epithelium during the entire menstrual cycle and characteristically in the apical protrusions of non-ciliated cells of the ampulla during the preovulatory phase; (ii) sialoglycans with α2,3-linked sialic acids (MAL II binding) were expressed along the entire oviductal surface only during the preovulatory phase, whereas α2,6-linked ones (SNA affinity) were also detected in the surface of the luteal phase, although during the preovulatory phase they were characteristically found in the glycocalyx of the isthmus cilia, and O-linked sialoglycans with sialic acids linked to Galβl,3GalNAc (T antigen) (KsPNA) and terminal N-acetylgalactosamine (Tn antigen) (KsSBA) were found in the entire oviductal surface during all phases of the menstrual cycle; (iii) GalNAc terminating O-linked glycans (HPA staining) were mainly expressed in the entire oviducts of the luteal and preovulatory phases, and characteristically in the apical protrusions of the isthmus non-ciliated cells of the preovulatory phase; and (iv) fucosylated glycans with α1,2-linked fucose (LTA reactivity) occurred in the apical surface of fimbriae during the luteal phase, whereas α1,3/4-linked fucose (UEA I binders) were present in the apical protrusions of the ampulla non-ciliated cells and in the apical surface of isthmus during the preovulatory phase as well as in the isthmus apical surface of follicular-phase oviducts. These results demonstrate for the first time that morphological and glycan changes occur in the baboon oviductal epithelium during the menstrual cycle. Particularly, the sex hormone fluctuation affects the glycan pattern in a region-specific manner, probably related to the function of the oviductal segments. The findings add new data concerning baboons which, due to their anatomical similarity to humans, make an excellent model for female reproduction studies.

摘要

哺乳动物的输卵管是一个高度特化的结构,受精和早期胚胎发育在此发生。其黏膜上皮参与维持和调节动态的管腔内液体。输卵管上皮由纤毛细胞和非纤毛(分泌)细胞组成,它们的分化和活性依赖于性激素。在本研究中,我们首次调查了狒狒输卵管上皮在月经周期中的形态和聚糖组成。通过腹腔镜从14名健康成年雌性体内取出输卵管,根据性激素水平和阴道细胞学特征评估其月经周期阶段。分别对固定于4%多聚甲醛中的伞部、漏斗部、壶腹部和峡部进行组织学研究,石蜡包埋,苏木精-伊红染色用于形态学分析,并使用一组九种荧光凝集素进行糖缀合物表征。组织形态学分析显示,在整个输卵管中:(i)在卵泡期和黄体期,纤毛细胞和非纤毛细胞难以区分,而在排卵前期它们高度分化,此时非纤毛细胞呈现顶端突起;(ii)排卵前期的上皮高度显著高于其他月经周期阶段;(iii)纤毛细胞数量从伞部到漏斗部显著(P≤0.05)增加,在输卵管其他节段逐渐减少,峡部的纤毛细胞数量最少。聚糖表征显示在月经周期的不同阶段存在复杂且区域特异性的组成。可总结如下:(i)高甘露糖基化的N-连接聚糖(Con A反应性)在整个月经周期中存在于整个输卵管上皮,在排卵前期特异地存在于壶腹部非纤毛细胞的顶端突起中;(ii)具有α2,3-连接唾液酸的唾液聚糖(MAL II结合)仅在排卵前期沿整个输卵管表面表达,而α2,6-连接的唾液聚糖(SNA亲和力)在黄体期的表面也有检测到,尽管在排卵前期它们特异地存在于峡部纤毛的糖萼中,并且具有与Galβ1,3GalNAc连接的唾液酸的O-连接唾液聚糖(T抗原)(KsPNA)和末端N-乙酰半乳糖胺(Tn抗原)(KsSBA)在月经周期的所有阶段都存在于整个输卵管表面;(iii)以GalNAc结尾的O-连接聚糖(HPA染色)主要在黄体期和排卵前期的整个输卵管中表达,在排卵前期特异地存在于峡部非纤毛细胞的顶端突起中;(iv)具有α1,2-连接岩藻糖的岩藻糖基化聚糖(LTA反应性)在黄体期出现在伞部的顶端表面,而α1,3/4-连接的岩藻糖(UEA I结合物)在排卵前期存在于壶腹部非纤毛细胞的顶端突起和峡部的顶端表面,以及卵泡期输卵管峡部的顶端表面。这些结果首次证明狒狒输卵管上皮在月经周期中发生形态和聚糖变化。特别是,性激素波动以区域特异性方式影响聚糖模式,这可能与输卵管节段的功能有关。这些发现增加了关于狒狒的新数据,由于它们在解剖学上与人类相似,使其成为女性生殖研究的优秀模型。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/51f5/9597729/d9bc22552f3b/animals-12-02769-g001.jpg

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