|Year : 2015 | Volume
| Issue : 1 | Page : 44-52
Microscopic and histochemical characterization of the bovine uterine tube during the follicular and luteal phases of estrous cycle
Doaa M Mokhtar
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Egypt
|Date of Web Publication||1-Feb-2018|
Doaa M Mokhtar
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526
Source of Support: None, Conflict of Interest: None
The morphometrical and morphological features of the infundibulum and ampulla of the uterine tubes of adult cattle were studied. The materials used in this study were consisted of 12 pairs of uterine tube of healthy cows at age of 16–36 months, collected from Assiut slaughterhouses. Through observations of the ovaries, follicular and luteal phases of estrous cycle of each cattle were specified. Semithin sections of ampulla and infundibulum at follicular and luteal phases were made and histochemical analysis of the ampulla by use of PAS, Alcian Blue, Sudan Black B was also done. In addition, acid phosphatase activity of the ampullar epithelium was demonstrated. Histological analysis of the epithelium of bovine oviduct revealed that it was consisted of non-ciliated secretory cells, two populations of ciliated cells (CC), basal cells and Peg cells. At the luteal phase, the secretory cells possessed many cytoplasmic protrusions that extended beyond the luminal borders of the ciliated cells and exocytosis of secretory materials was observed. While at the follicular phase, the ciliated cells were predominated. The histochemistry of the ampullar epithelium revealed increase in secretions of neutral, acidic mucopolysaccarides and lipid from the secretory cells at the luteal phase with moderate acid phosphatase activity. Histomorphometric examinations of infundibulum and ampulla indicated that the mean number and height of primary folds as well as the thickness of the epithelium were increased significantly at the follicular phase.
Keywords: Uterine tube, Estrous cycle, Morphology, Morphometry, Histochemistry, Cattle
|How to cite this article:|
Mokhtar DM. Microscopic and histochemical characterization of the bovine uterine tube during the follicular and luteal phases of estrous cycle. J Microsc Ultrastruct 2015;3:44-52
|How to cite this URL:|
Mokhtar DM. Microscopic and histochemical characterization of the bovine uterine tube during the follicular and luteal phases of estrous cycle. J Microsc Ultrastruct [serial online] 2015 [cited 2021 Apr 15];3:44-52. Available from: https://www.jmau.org/text.asp?2015/3/1/44/224532
| 1. Introduction|| |
The oviduct plays an essential role in reproduction, as it creates an important microenvironment for the final maturation of male gametes, fertilization and early development of embryos . The bovine oviduct could be divided into infundibulum, ampulla and isthmus. Many studies have been done in order to describe the characteristic morphological changes in the oviduct of several domestic species including cows , goats , pigs  and bitches  in relation to estrous cycle.
The epithelium lining of uterine tube of mammals is consisted mainly of ciliated and non-ciliated secretory cells. These cells show atrophy and hypertrophy according to the endocrine status, and thus the ratio of these cells may undergo changes during the estrous cycle . Moreover, it is known that the oviductal epithelial cells show marked regional variations in ultrastructural, histochemical and physiological features in many mammals .
The ciliated cells aid in transport of both gamete and embryo , while the secretory cells may be involved in secretion of the oviductal fluid that plays an important role in many sperm functions and embryo development . The secretory product is mainly produced by ampulla as the fertilization occurs in it .
Not only cattle are important agricultural species but their ovarian follicular dynamics also make them to be an ideal model for different aspects of human reproduction , due to distinct similarities between bovine and human ovarian physiology . However, many details about the morphology and morphometry of oviduct of cattle at the critical estrous phases are still lacking ,.
A main topic of this study is to describe the histological, histochemical and morphometrical changes in uterine tube of cattle in Egypt (Bos indicus) at follicular and luteal phases of estrous cycle.
| 2. Materials and methods|| |
2.1. Tissue collection
The material used in this study consists of 12 pairs of bovine uterine tubes of healthy adult cows (B. indicus) at age of 16–36 months. The samples were collected within 30 min after routinely slaughter from Assiut slaughterhouses. The stages of estrous cycle were estimated by the appearance of ovarian follicles and corpora lutea.
2.2. Histological analysis
Specimens from infundibulum and ampulla were washed by physiological saline and immediately fixed in Bouin’s fluid for 20 h. The fixed materials were dehydrated in graded series of alcohols, cleared in methyl benzoate and embedded in paraffin wax. The embedding time was not more than 8 h. Serial longitudinal and transverse sections were obtained at 3 μm and stained with Harris Haematoxylin and Eosin . Van Gieson Resorcin Fuchsin  and Goldener’s Trichome stain .
2.3. Histochemical analysis
Acidic and neutral mucus were detected by Alcian Blue stain (pH 2.5) and PAS stain, respectively ,. Lipid was demonstrated by Sudan Black B . Acid phosphatase activity of ampullar epithelium was identified with Gomori’ Lead Nitrate  at both follicular and luteal phases of the estrous cycle.
2.4. For semithin sections
Small specimens of infundibulum and ampulla at both follicular and luteal phase were fixed in a mixture of 2.5% paraformaldehyde and 2.5% glutaraldehyde in 0.1 M Na-cacodylate buffer, pH 7.3 for 4 h at 4 °C. They were washed in the same buffer used and then post-fixed in 1% osmic acid in 0.1 M Na-cacodylate buffer for further 2 h at room temperature. The samples were then dehydrated in ethanol and embedded in Araldite–Epon mixture. Semithin sections (1 μm in thickness) were cut and stained with Toluidine blue.
2.5. Morphometric and statistical analysis
Morphometrical measurements to infundibulum and ampulla at follicular and luteal phases were performed by using Image Analysis Tools (IT system). Measurements included the number of primary mucosal folds/cross section as well as height and thickness of primary mucosal folds. In addition, height of epithelium and number of secretory to ciliated cells at follicular and luteal phases were assessed and all respective data analyzed statistically and significance was assigned at P <0.05. Student’s t test Graph pad Software was used to compare differences between each parameter.
| 3. Results|| |
The mucosa of the infundibulum was highly folded with primary and secondary folds. The primary folds were tall and somewhat irregular that gave rise to many secondary folds and sometimes tertiary folds in some areas [Figure 1]A. The mean number of the mucosal folds at the follicular phase was 52 and that at the luteal phase was 46 [Table 1]. The epithelium was of simple columnar type and was consisted of two main cell types: ciliated and non-ciliated secretory cells. Two types of ciliated cells (CC) in infundibulum were observed. The first type characterized by its large size and pale staining cytoplasm with enlarged rounded to ovoid nucleus located at the apical third of the cell. These cells were provided with few short cilia or even completely lacking of cilia. The second type was smaller in size, possessed long cilia with basal bodies and its nucleus was more compressed than the first type and centrally located [Figure 1]B and [Figure 1]C.
|Figure 1: Infundibulum of cattle during follicular and luteal phases stained by H &E. (A) General view of the infundibulum showing highly folded mucosa with primary folds (arrow) and secondary ones (arrowhead). (B and C) Infundibular epithelium at luteal phase was consisted of dark ciliated cells with clear cilia (white arrowhead), light ciliated cells with few or no cilia (stars), secretory cells with apical secretory protrusions (two stars) and narrow slender peg cells (black arrowhead). (D) Infundibular epithelium at follicular phase characterized by predominance of ciliated cells (arrowheads) and absence of secretory activity. Note presence of light ciliated cells (star).|
Click here to view
|Table 1: Morphometrical and statistical analysis of the uterine tube at the luteal and follicular phases of estrous cycle.|
Click here to view
At the luteal phase, the mean number of secretory to ciliated cells was 57:51 and the secretory cells were demonstrated by increase of cellular activity by the way of apical cytoplasmic projections. Merocrine mode of secretion was identified in many secretory cells that were characterized by irregular apical surfaces and little released materials were detected in the lumen [Figure 1]C. Few “Peg cells” or “Intercalary cells” were interspersed between the ciliated cells of the infundibulum that appeared as rod-like slender cells with a dark compressed nucleus. These cells were more frequently distributed at the basal portion of the mucosal folds and possessed no cilia [Figure 1]B and [Figure 1]C. At the follicular phase, the ciliated cells were more demonstrated than the secretory ones as the mean number of secretory to ciliated cells was 48:56 and these ciliated cells were characterized by its rectangular shape and centrally oval vesicular nucleus [Figure 1]D.
In semithin sections, the exocytosis or eccrine mode of secretion was detected in many secretory cells by broken surfaces on some secretory cells with irregular apical cytoplasmic processes and deeper invaginations of plasma membrane [Figure 2]A and [Figure 2]B. While at the follicular phase, the ciliated cells were predominated with its clear cilia and light colored cytoplasm. The secretory cells possessed few secretory granules with no cytoplasmic protrusions [Figure 2]C.
|Figure 2: Semithin section of infundibulum at follicular and luteal phase stained by Toluidine blue. (A) Exocytosis of secretory products is evident at the luteal phase by broken surfaces of secretory cells and invaginations of plasmalemma (black arrowheads). Notice presence of ciliated cells with nucleus at the apical third (white arrowheads). (B) High secretory activity of the epithelium at luteal phase by means of cytoplasmic protrusions (black arrowheads) beyond the borders of ciliated cells (white arrowhead). (C) Large distribution of ciliated cells (arrowheads) at follicular phase with fewer darkly stained secretory cells with some apical secretory granules (stars). Lamina propria (LP) consisted of collagenous fibers and many connective tissue cells.|
Click here to view
The cytomorphometric data revealed significant increase in the mean number and length of the primary mucosal folds at the follicular phase (P < 0.05). There are no remarkable changes in the mean thickness of primary folds during follicular and luteal phases. Significant increase in the epithelium height at the follicular phase was recorded [Table 1].
The mucosa of ampulla was thrown into numerous elaborately branched leaf-like folds that formed of primary, secondary and tertiary ones [Figure 3]A. These folds may be interconnected with one another in a complex manner [Figure 3]B. The mean number of the primary folds of the ampulla at the follicular phase was 42, while at luteal phase was 36 and thus, the number of the folds decrease from infundibulum to ampulla [Table 1]. The lamina propria-submucosa was consisted of loose connective tissue with abundant collagenous fibers [Figure 3]C and [Figure 3]D. Tunica muscularis was consisted of smooth muscle bundles with many blood vessels were interspersed between them. Serosa was the outer connective tissue layer [Figure 3]C, [Figure 3]D and [Figure 4]A. The lining epithelium was of simple columnar type that consisted of two types of cells: ciliated and non-ciliated secretory ones [Figure 4]B.The ampullar epithelium during the follicular phase was significantly higher than that at the luteal phase [Table 1]. The secretory activity was very clear in the luteal phase, the bulging apices of the slender secretory cells exhibited constrictions and some secretory products were detached from the cell surfaces. Nuclei were situated at varying levels within the cell and may be extruded into the lumen [Figure 4]C. The follicular phase was characterized by predominance of ciliated cells with their numerous and prominent cilia [Figure 4]D.
|Figure 3: Structure of the wall of the ampulla at follicular and luteal phase stained by Van Geison Resorcin Fuchsin. (A) Cross section of the ampulla at luteal phase showing highly folded mucosa with large number of leaf-like folds (arrowhead). (B) Cross section of the ampulla at follicular phase stained showing some mucosal folds interconnected in complex manner (arrowhead). (C and D) Magnified squares in (A) and (B) respectively showing the wall of the ampulla consisted of mucosa (M), lamina propria-submucosa (S) and muscularis (Ms). Note distributions of blood vessels (BV) between the muscle layers.|
Click here to view
|Figure 4: The wall of ampulla by Goldner’s Trichrome. (A) The wall of ampulla was composed of mucosa (M), submucosa (S), muscularis (Ms) and serosa (Sr). Note presence of blood vessels (BV) in submucosa. (B) Mucosa of the ampulla was consisted of simple columnar epithelium (ep) and lamina propria (LP) that was continuous with submucosa (S) with abundant amount of collagenous fibers and fibroblasts. (C) Epithelium of ampulla by Goldner’s Trichrome at luteal phase showing high cellular activity, constrictions of secretory materials and released some of them to the lumen (arrowheads). (D) Epithelium of ampulla by Goldner’s Trichrome at follicular phase revealed absence of secretory activity and predominance of ciliated cells (arrowheads).|
Click here to view
The secretory cells were predominated in the luteal phase with various degrees of numerous apical cytoplasmic protrusions as the mean number of secretory to ciliated cells was 42:31 [Figure 5]A and [Table 5]. The nuclei of secretory cells were observed in the basal position and also were observed in the cytoplasmic protrusions [Figure 5]A. Basal cells were observed in the basal portion of the ampullar epithelium and were characterized by rounded dark nucleus surrounded by scant and lightly stained cytoplasm that were similar in appearance to lymphocytes [Figure 5]A. Cellular integrity disruption was markedly observed in the luteal phase [Figure 5]A. The ampullar epithelium at the follicular phase was characterized by an extensive distribution of ciliated cells as the mean number of secretory to ciliated cells was 33:45 [Table 1] and was characterized by its prominent cilia that were protruded into the uterine lumen with decrease in the number of secretory cells. Two populations of ciliated cells were observed in the epithelium of the ampulla: light staining and large CC with apical rounded nucleus as well as darker and smaller ones with central oval nucleus [Figure 5]B.
|Figure 5: Epithelium of ampulla at follicular and luteal phases. (A) Epithelium of ampulla stained by HE at luteal phase showing abundance of secretory cells with many apical protrusions (stars) that extended beyond the ciliated ones (arrowheads). Note presence of basal cells (arrows) surrounded by light cytoplasm. (B) Epithelium of ampulla stained by HE at follicular phase showing abundance of ciliated cells. Note presence dark ciliated cells with clear cilia (arrowhead) and light large ciliated cells (stars). (C) Semithin sections of the epithelium of ampulla stained by Toluidine blue at luteal phase showing broad light ciliated cells (arrowheads) with reduction and detachment of cilia and narrow dark secretory cells (stars) without cellular activity. Note presence of mast cells (MC) with their metachromatic granules at the lamina propria. (D) Semithin sections of the epithelium of ampulla stained by Toluidine blue at follicular phase showing dark secretory cells (stars) and light ciliated cells (arrowheads) with prominent tall cilia. Note presence of dark compressed Peg cell (arrow).|
Click here to view
In semithin sections, the secretory cells of the luteal phase were characterized by their narrow slender shape with basal elongated nucleus and more densely stained cytoplasm than that of the ciliated cells. The shape of ciliated cells ranged from rectangular to pear shape, the nucleus was large ovoid, vesicular and more superficial than the nuclei of secretory cells [Figure 5]C. Reduction in size or even loss of cilia at the luteal phase was observed. Mast cells were demonstrated in the lamina propria of ampulla with their characteristic purple metachromatic granules by Toluidine blue [Figure 5]C. In the follicular phase, the secretory cells appeared dark in colure, slender in shape, narrow in diameter and possessed apical microvilli. Also the ciliated cells were characterized by large number of apical tall cilia [Figure 5]D.
3.3. Histochemistry of the ampullar epithelium
Large amount of cidic mucopolysaccaridies were identified in the secretory cells of the ampulla by Alcian Blue (pH 2.5) at the luteal phase [Figure 6]A and little amount of acidic mucopolysaccarides were identified in the follicular phase [Figure 6]B. The cytoplasm of secretory cells was granular in nature and characterized by positive reaction to PAS at both follicular and luteal phases [Figure 6]C and [Figure 6]D. But, the reaction increased in the luteal phase as the number of secretory cells increased and was abundant paticularly in the crypts [Figure 6]C. The lipid droplets were identified by Sudan Black B in the apical portion of the ampullar epithelium at the luteal phase more than those present in follicular phase [Figure 6]E and [Figure 6]F. Also, moderate acid phosphatase activity was demonstrated during the luteal phase at the apical region of the secretory cells by Gomori’s Lead Nitrate method and weak activity was recorded in the follicular phase [Figure 6]G and [Figure 6]H.
|Figure 6: Histochemical analysis of the ampullar epithelium at follicular and luteal phases. (A) The secretory granules at luteal phase showing strong positive reaction to Alcian Blue (arrowhead). (B) The fewer secretory cells at follicular phase showing positive reaction to Alcian Blue (arrows). (C) The secretory cells at luteal phase showing strong positive reaction to PAS (arrow). (D) The secretory cells at follicular phase showing moderate positive reaction to PAS (arrowhead). (E and F)The lipid droplets (arrowheads) were identified by Sudan Black B in the apical portion of the ampullar epithelium at both luteal and follicular phase respectively. (G) Moderate acid phosphatase activity (arrowheads) was demonstrated during the luteal phase at the apical region of the secretory cells by Gomori’s Lead Nitrate method. (H) Weak activity of acid phosphatase (arrowhead) was recorded in the follicular phase.|
Click here to view
The morphometric and statistic data of the ampulla revealed increase in number of mucosal folds and length of the primary folds at follicular phase (P < 0.05). There are no remarkable changes in the mean thickness of primary folds at follicular and luteal phases. Significant increase in the epithelium height at the follicular phase was recorded [Table 1].
| 4. Discussion|| |
Uterine tube is a part of the female genital tract, which picks up the oocyte and makes a suitable situation for fertilization, directing the ovum to the uterus. The epithelial structure of the oviduct has a basic role in oocyte nutrition and further embryonic development and survival . The aim of the present study is to identify the histological, histochemical and morphometrical features of uterine tube of cattle during the follicular and luteal phases. My results revealed differences in the histomorphometric structure of the different parts of the uterine tube during phases of the estrous cycle. These differences probably reflect different secretion rates of the ovarian hormones . It is well known that the mammalian oviduct is a target organ for the sex steroid hormones, estrogen and progesterone. These hormones cause various morphological changes in oviductal epithelial cells. In particular, estrogen induces hypertrophy and formation of secretory granules .
The results indicate that the mucosal folds were significantly increased in number and height during follicular phase and decreased from infundibulum to ampulla. These findings are consistent with some other investigations in ewe  and rabbit , which may be confirmed the role of infundibulum in receiving and transporting the oocyte from ovary to ampulla .
This study revealed that the epithelium of cattle (B. indicus) was lined by four types of cells: ciliated, nonciliated secretory cells, few Peg cells that were non-ciliated slender cells wedged in between them and basal cells resembling lymphocytes near the basement membrane. The number of ciliated cells reached maximum in the infundibulum and decreased gradually in the ampulla. The number of ciliated cells increased in the follicular phase and was greater in infundibulum compared to the ampulla, this may be due to action of estrogen that cause active ciliation of epithelial cells . It seems that the cyclic changes observed in the present study reflect the function of the cilia in the infundibulum and ampulla of the cattle. The action of cilia is thought to be the primary mechanism for transporting the oocyte rapidly from the infundibulum to the site of fertilization in the ampulla .
The present study suggests that the secretory product is mainly produced by the secretory cells in the ampulla. Moreover, the mucus content of the oviduct of cattle contains various mucopolysaccharides, which could be stained by PAS and Alcian Blue. In addition, numerous lipid droplets and moderate acid phosphatase activity were recorded in the ampulla at the luteal phase. I suggest that these products are capable of retaining, nutrition and protection of the spermatozoa until ovulation, and the increase in the amount of secretions during the follicular phase may provide spermatozoa with motility and fertilization capacity. Concerning the oviductal secretions, oviductin is a glycoprotein secreted by secretory cells around the time of ovulation, bind to the zona pellucida of postovulatory follicles during their transit to oviduct . Oviductal fluid has several functions: sperm capacitating, sperm hyperactivation, fertilization and early preimplantation development . These findings provide insight into the difference in cellular function.
The apocrine secretion seemed to be the main way by which the secretion of secretory cells was released and this was identified by apical protrusions of secretory materials and their construction and detaching from the cell surfaces. Exocytosis of secretory products also observed in oviduct epithelial cells. Some glycoproteins secreted by secretory cells of oviductal epithelium associate with ovulated ova and developing embryos and may play important roles in early embryonic development ,. Immunohistochemical studies on the bovine uterine tube epithelium are recommended.
Basal cells were demonstrated at this study and also called reserve or indifferent cells that were described by . Ozen et al.  suggested that the basal cells are undifferentiated cells that can be transformed to secretory and ciliated ones. Cells with similar appearance had been referred to be leukocytes or lymphocyte-like cells . The present study recorded presence of “Peg” or “Intercalary” cells for the first time in the oviduct of cattle (B. indicus). These cells were first demonstrated in oviduct of some farm animals by  who described them as depleted secretory cells and their secretions were consisted of mucoprotein and mucopolysaccarides. Finally, this detailed histological study of normal bovine oviducts will not only help to understand clearly the physiology of reproduction but also will assist in evaluating the pathological processes in the oviduct.
Conflict of interest
There is no conflict of interest to declare.
I would like to express my great thanks to Dr Hanan H. Abd-Elhafeez for her help, willing assistance and special coordination.
| References|| |
Hafez ESE. Reproduction in farm animals. 6th ed. Philadelphia: Lea & Febiger; 1993.
Yaniz JL, Lopez-Gatius F, Santolaria P, June-Mullins K. Study of the functional anatomy of bovine oviductal mucosa. Anat Rec 2000;260(3):268-78.
Abe H, Onodeera M, Sugawara S, Satoh T, Hoshi H. Ultrastructural features of goat oviductal secretory cells at follicular and luteal phases of the estrous cycle. J Anat 1999;195:515-21.
Abe H, Hoshi H. Regional and cyclic variations in the ultrastructural features of secretory cells in the oviductal epithelium of the Chinese Meishan pig. Reprod Dom Anim 2007;42:292-8.
Steinhauer N, Boos A, Günzel-Apel AR. Morphological changes and proliferative activity in the oviductal epithelium during hormonally defined stages of the oestrous cycle in the bitch. Reprod Dom Anim 2004;39:110-9.
Abe H. The mammalian oviductal epithelium: regional variations in cytological and functional aspects of the oviductal secretory cells. Histol Histopathol 1996;11:743-68.
Odor DL, Gaddum-Rosse P, Rumery RE, Blandau RJ. Cyclic variations in the oviductal ciliated cells during the menstrual cycle and after estrogen treatment in the pig-tailed monkey, Macaca nemestrina
. Anat Rec 1980;198:35-57.
Adams GP, Pierson RA. Bovine model for study of ovarian follicular dynamics in humans. Theriogenology 1995;43: 113-20.
Vigne JL, Halburnt LL, Skinner MK. Characterization of bovine ovarian surface epithelium and stromal cells: identification of secreted proteins. J Biol Reprod 1994;51:1213-21.
Rao KT [B.V.Sc.] A histological study of the oviduct of the immature, mature and pregnant bovine. India: Madras University; 1947.
Thibodeaux JK, Goodeaux LL, Roussel JD, Menezo Y, Amboriki GF, Moreau JD, et al. Effects of stage of the bovine oestrous cycle on in-vitro
characteristics of uterine and oviductal epithelial cells. Hum Reprod 1991;6:751-60.
Harris HF. On the rapid conversion of haematoxylin into haematin in staining reactions. J Appl Microsc Lab Methods 1996;3:777, cited by Bancroft JD, Steven A. Theory and practice of histological techniques. 4th ed. New York, NY, USA: Churchill Livingstone; 1900.
Van-Gison J. Laboratory notes of technical method for the nervous system. J N Y Med 1889;50:57-60.
GoldnerJA. Modification of the masson trichrome technique for routine laboratory purposes. Am J Pathol 1938;14:237-43.
Mowry RW. Alcian blue techniques for the histochemical study of acidic carbohydrates. J Histochem Cytochem 1956;4:407-8.
McManus JFA. Histological demonstration of mucin after periodic acid. Nature 1946;158(4006):202.
Stevens A. Pigments and minerals. In: Bancroft, Stevens, editors. Theory and practice of histo-logical technique, 2nd ed. Churchill Living stone; 1982 (chapter 13).
Gomori G. An improved histochemical technique for acid phosphatase. Stain Technol 1950;25:81.
Killian GJ. Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. J Anim Reprod Sci 2004;82/83:141-53.
McDaniel JW, Scalzi H, Black DL. Influence of ovarian hormones on histology and histochemistry of the bovine oviduct. J Dairy Sci 1968;51:754.
Abe H, Oikawa T. Effects of estradiol and progesterone on the cyto-differentiation of epithelial cells in the newborn golden hamster. Anat Rec 1993;235:390-8.
Ozen A, Ergun E, Kurim A. Histochemistry of the oviduct epithelium in the Angora rabbit. Turk J Vet Anim Sci 2010;34(3):1-8.
Odor DL, Blandau RJ. Egg transport over the fimbrial surface of the rabbit oviduct under experimental conditions. J Fertil Steril 1973;24:292-300.
Verhage HG, Brenner RM. Estradiol-induced differentiation of the oviductal epithelium in ovariectomized cats. Biol Reprod 1975;13:104-11.
Hafez SE, Hafez B. Reproduction in farm animals. 7th ed. Philadelphia: Lippincott Williams and Wilkins; 2000. p. 13-81.
McBridge DS, Boisvert C, Bleau G, Kan WK. Detection of nascent and/or mature forms of oviductin in the female reproductive tract and postovulatory oocytes by use of a polyclonal antibody against recombinant hamster oviductin. J Histochem Cytochem 2004;52(8):1001-9.
Hunter RHF. Modulation of gamete and embryonic microenvironments by oviduct glycoproteins. J Mol Reprod Dev 1994;39:176-81.
Gandolfi F. Functions of proteins secreted by oviduct epithelial cells. Microsc Res Tech 1995;32:1-12.
Bjorkman N, Freddriccsson B. The bovine oviduct epithelium and its secretory process as studied with the electron microscope and histochemical tests. Z Zellfossch Mikrosk Anat 1961;55:500.
Odor DL. The question of ‘basal’ cells in oviductal and endocervical epithelium. J Fertil Steril 1974;25:1047-62.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
|This article has been cited by|
||Early embryo-maternal communication in the oviduct: A review
| ||Sabine Kölle,Barbara Hughes,Heather Steele |
| ||Molecular Reproduction and Development. 2020; |
|[Pubmed] | [DOI]|
||Local sex steroid hormone milieu in the bovine oviduct ipsilateral and contralateral to pre-ovulatory follicle or corpus luteum during the peri-ovulatory phase
| ||Ken HAZANO,Shingo HANEDA,Mitsunori KAYANO,Motozumi MATSUI |
| ||Domestic Animal Endocrinology. 2020; : 106515 |
|[Pubmed] | [DOI]|
||Salpingitis Impairs Bovine Tubal Function and Sperm-Oviduct Interaction
| ||Loveth E. Owhor,Sven Reese,Sabine Kölle |
| ||Scientific Reports. 2019; 9(1) |
|[Pubmed] | [DOI]|
||Fatty acid profile of blood plasma and oviduct and uterine fluid during early and late luteal phase in the horse
| ||B. Drews,V. Milojevic,K. Giller,S.E. Ulbrich |
| ||Theriogenology. 2018; 114: 258 |
|[Pubmed] | [DOI]|
||Sex Steroid-Mediated Control of Oviductal Function in Cattle
| ||Mario Binelli,Angela Gonella-Diaza,Fernando Mesquita,Claudia Membrive |
| ||Biology. 2018; 7(1): 15 |
|[Pubmed] | [DOI]|
||Prolonged in vivo functional assessment of the mouse oviduct using optical coherence tomography through a dorsal imaging window
| ||Shang Wang,Riana Syed,Olga A. Grishina,Irina V. Larina |
| ||Journal of Biophotonics. 2018; : e201700316 |
|[Pubmed] | [DOI]|
||Sex steroids modulate morphological and functional features of the bovine oviduct
| ||Angela Maria Gonella-Diaza,Fernando Silveira Mesquita,Kauę Ribeiro da Silva,Júlio Cesar de Carvalho Balieiro,Nilton Pedro dos Santos,Guilherme Pugliesi,Ricardo de Francisco Strefezzi,Mario Binelli |
| ||Cell and Tissue Research. 2017; 370(2): 319 |
|[Pubmed] | [DOI]|
||Mucosal immunity of the postpartum bovine genital tract
| ||Dinesh Dadarwal,Colin Palmer,Philip Griebel |
| ||Theriogenology. 2017; 104: 62 |
|[Pubmed] | [DOI]|
||Morphology and Aquaporin Immunohistochemistry of the Uterine Tube of Saanen Goats(Capra hircus): Comparison Throughout the Reproductive Cycle
| ||S Arrighi,G Bosi,S Frattini,B Coizet,D Groppetti,A Pecile |
| ||Reproduction in Domestic Animals. 2016; 51(3): 360 |
|[Pubmed] | [DOI]|