- Open Access
Structural and histological characterization of oviductal magnum and lectin-binding patterns in Gallus domesticus
© Jung et al; licensee BioMed Central Ltd. 2011
- Received: 11 March 2011
- Accepted: 8 May 2011
- Published: 8 May 2011
Although chicken oviduct is a useful model and target tissue for reproductive biology and transgenesis, little is known because of the highly specific hormonal regulation and the lack of fundamental researches, including lectin-binding activities and glycobiology. Because lectin is attached to secreted glycoproteins, we hypothesized that lectin could be bound to secretory egg-white proteins, and played a crucial role in the generation of egg-white protein in the oviduct. Hence, the purpose of this study was to investigate the structural, histological and lectin-binding characteristics of the chicken oviductal magnum from juvenile and adult hens.
The oviductal magnums from juvenile and adult hens were prepared for ultrastructural analysis, qRT-PCR and immunostaining. Immunohistochemistry of anti-ovalbumin, anti-ESR1 and anti-PGR, and mRNA expression of egg-white genes and steroid hormone receptor genes were evaluated. Lectin histochemical staining was also conducted in juvenile and adult oviductal magnum tissues.
The ultrastructural analysis showed that ciliated cells were rarely developed on luminal surface in juvenile magnum, but not tubular gland cells. In adult magnum, two types of epithelium and three types of tubular gland cells were observed. qRT-PCR analysis showed that egg-white genes were highly expressed in adult oviduct compared with the juvenile. However, mRNA expressions of ESR1 and PGR were considerably higher in juvenile oviduct than adult (P < 0.05). The immunohistochemical analysis showed that anti-ovalbumin antibody was detected in adult oviduct not in juvenile, unlikely anti-ESR1 and anti-PGR antibodies that were stained in both oviducts. In histological analysis, Toluidine blue was stained in juvenile and adult oviductal epithelia, and adult tubular glands located in the outer layer of oviductal magnum. In contrast, PAS was positive only in adult oviductal tubular gland. Lectins were selectively bound to oviductal epithelium, stroma, and tubular gland cells. Particularly, lectin-ConA and WGA were bound to electron-dense secretory granules in tubular gland.
The observation of ultrastructural analysis, mRNA expression, immunohistochemistry and lectin staining showed structural and physiological characterization of juvenile and adult oviductal magnum. Consequently, oviduct study could be helped to in vitro culture of chicken oviductal cells, to develop epithelial or tubular gland cell-specific markers, and to understand female reproductive biology and endocrinology.
- Wheat Germ Agglutinin
- Luminal Epithelium
- Tubular Gland
- Oviductal Epithelium
- Helix Pomatia Agglutinin
The oviduct of oviparous animals such as chicken and quail is an amazing organ. It produces each structural component of the laid egg, including the egg-white and eggshell. The mechanisms underlying the egg-laying process are sensitively regulated by steroid hormones, which orchestrate the proliferation and growth of oviductal epithelial cells. For example, diethylstilbestrol (DES) administration leads to massive growth of the juvenile oviduct  and induces cytodifferentiation of epithelial cells into tubular gland cells, goblet cells, and ciliated cells . The oviductal magnum is regarded as an important target tissue [3, 4] for transgenic research and the production of glycosylated pharmaceutical proteins in chickens because most egg-white proteins are synthesized and secreted in the magnum segment to the oviductal lumen during the 24-h egg production cycle, and this process is mediated by a series of hormones.
The egg-laying hen oviduct is divided into several parts: the infundibulum (place of fertilization), magnum (place of egg-white protein production), isthmus (formation of the shell membrane), shell gland (formation of the egg shell), and vagina (oviposition). While the oviduct mucosa of 10-week-old juvenile chickens is simply lined by a thin layer of pseudostratified columnar epithelial cells upon compact stroma cells , the oviductal magnum mucosa from egg-laying hens consists of surface oviductal epithelium lined by ciliated non-secretory cells, non-ciliated secretory granular cells (also referred to as goblet cells), and three different types of tubular gland cells under the epithelium . The ciliated cells rarely show secretory activity and consist of cilia in the luminal mucosa  but non-ciliated cells are mainly involved in the release of secretory granules that are synthesized by tubular gland cells.
On the other hand, granular cells have a unique intracellular structure of highly conserved glycoprotein and actively release the egg-white protein mass into the lumen when an egg is proceeding through the magnum segment . Glycoprotein, carbohydrates, and lectin have been commonly shown to have different distributions and binding patterns depending on the species, age, sexual maturity, and hormonal effects [7–12]. In addition, these materials are involved in sperm binding to the oviductal epithelium [13, 14], sperm trapping in the oviductal mucosa [15, 16], and secretory activity of oviductal ampulla during the estrous cycle . Despite the importance of lectin and carbohydrates in reproductive biology, little is known about chicken oviduct. Traditionally, the characterization of the chicken oviduct has been limited to immunohistochemical staining against egg-white proteins, including ovalbumin, ovomucoid, lysozyme  and steroid hormone receptors [18, 19].
Although chicken is regarded as a useful tool for transgenesis as a bioreactor [3, 20–22], the production mechanism of recombinant humanized proteins are not well understood because of difficulties of transgenic chicken production, lack of in vitro verification system of transgene and fundamental researches of chicken oviduct, and highly sensitive hormone reaction in oviduct. In this study, we conducted a series of experiments using electron microscopy, quantitative RT-PCR, immunohistochemical analysis, and lectin histochemistry in juvenile oviductal magnum and that of egg-laying hens. The results obtained in this study should aid in our understanding of bird reproduction, mechanism of egg-white protein production, glycosylation, and the in vitro culture of chicken oviductal cells.
Experimental animals and animal care
The care and experimental use of chickens was approved by the Institute of Laboratory Animal Resources, Seoul National University (SNU-070823-5). Chickens were maintained according to a standard management program at the University Animal Farm, Seoul National University, Korea. The procedures for animal management, reproduction, and embryo manipulation adhered to the standard operating protocols of our laboratory.
Scanning electron microscopy (SEM) and transmission electron microscopy (TEM)
The magnum segment of chicken oviducts from juvenile (10-week-old) and actively egg-laying (30-week-old) hens were obtained, fixed primarily at 4°C for 2-4 h with modified Karnovsky's fixative (2% glutaraldehyde and 2% formaldehyde in 0.05 M sodium cacodylate buffer, pH 7.2), washed three times with cacodylate buffer, fixed secondarily for 2 h with 1% osmium tetroxide in cacodylate buffer, and stained overnight with 0.5% uranyl acetate at 4°C. To observe specimens for scanning electron microscopy (SEM), samples were dried twice with 100% isoamyl acetate for 15 min in a critical point dryer, mounted on metal stubs, coated with gold, and observed under field emission (FE)-SEM (SUPRA 55VP; Carl Zeiss). To prepare specimens for transmission electron microscopy (TEM), samples were dehydrated through a graded ethanol series, embedded in Spurr's resin, and cut on an ultramicrotome (MT-X; RMC, Tucson, AZ, USA). Samples were then stained with 2% uranyl acetate and Reynold's lead citrate for 7 min each and observed under TEM (LIBRA 120; Carl Zeiss).
Total RNA extraction and real-time PCR analysis
Primer sequences for RT-PCR
Sequence (5' to 3'): Forward and Reverse
GenBank Accession No.
Product Size (bp)
estrogen receptor alpha
Immunohistochemistry and lectin staining
The oviductal magnum segments of juvenile (10-week-old) and egg-laying adult (30-week-old) chickens were fixed in 4% buffered paraformaldehyde after strong washing with phosphate-buffered saline (PBS). Segments were subsequently embedded into a paraffin block and the paraffin-embedded oviductal tissue was sectioned at a thickness of 6 μm. The deparaffinized and rehydrated samples were heated in a microwave for 10 min after immersion in a sodium citrate buffer solution at pH 6.0 for heat-induced epitope retrieval (HIER). For immunohistochemical analysis, samples were permeabilized with 0.1% Triton X-100 in PBS for 5 min and incubated with 0.1% normal goat serum for 1 h to block nonspecific binding. Samples were serially stained at 4°C for overnight by indirect labeling using the following primary antibodies; mouse anti-chicken OVA antibody (1:200 dilution; Sigma), rabbit anti-human ESR1 antibody (1:100 dilution; Sigma), and mouse anti-human PGR antibody (1:100 dilution; Biocare Medical, Concord, CA, USA). To detect the primary antibodies, an AP detection system (Dako Universal LSAB2 kit; DakoCytomation, Carpinteria, CA, USA) was conducted  and then samples were observed under an inverted microscope (TE2000-U; Nikon).
For lectin histochemistry, the oviductal samples were reacted with FITC-conjugated lectins (Sigma) such as peanut agglutinin (PNA), Helix pomatia agglutinin (HPA), concanavalin A (ConA), Ulex europaeus agglutinin-1 (UEA-1), Wisteria floribunda agglutinin (WFA), and wheat germ agglutinin (WGA) at 10 μg/ml [9, 24] for 30 min. For double staining, juvenile and adult oviductal samples were incubated with anti-OVA, anti-PGR and anti-ESR1 antibodies at 4°C for overnight, respectively, and serially reacted with 10 μg/ml Cyanine (Cy) 3 or PE-conjugated anti-mouse IgG or rabbit IgG antibodies for 1 h at RT, and each samples were incubated with FITC-conjugated lectin-WGA for 30 min. These fluorescent samples were counterstained with diamidino-2-phenylindole (DAPI) and observed under a confocal microscope (LSM-700; Carl Zeiss, Wetzlar, Germany).
For histological and chemical dye staining, sections were stained with hematoxylin-eosin (HE; Sigma, St. Louis, MO, USA) for 2 min and 20 min, respectively , Periodic acid-Schiff's staining (PAS; Sigma) for 5 min and 15 min, respectively, or Toluidine blue (TB; Sigma) for 2 min. All procedures were performed at room temperature, and stained cells were observed under an inverted microscope (TE2000-U; Nikon, Tokyo, Japan).
The PROC-GLM model of the SAS program (SAS Institute, Cary, NC, USA), which employs an analysis of variance (ANOVA) and the least-squares method, was used to statistically analyze the numerical data, i.e., oviductal samples from juveniles and adults, and muscle samples as controls. A significant difference was determined when the P value was less than 0.05.
Ultrastructure of the oviductal magnum from juvenile and egg-laying adult chickens
Magnum-specific gene expression in both juvenile and egg-laying adult chickens
Immunohistochemical analysis in the oviductal magnum from juvenile and egg-laying adult chickens
To confirm the result of mRNA expression, immunohistochemical analyses were conducted with anti-OVA antibody, the most abundant secretory egg-white protein, and anti-hormone receptors antibodies, such as anti-ESR1 and anti-PGR antibodies. Figure 3B showed that anti-OVA antibody was barely bound to the juvenile oviduct, but abundantly and predominantly localized on the tubular gland layer in the adult oviduct. Notably, anti-ESR1 and anti-PGR antibodies were detected in the apical surface of the luminal epithelium of both the juvenile and adult oviduct and these antibodies were also localized on the tubular gland layer in the adult oviduct (Figure 3B).
Histological characterization of oviductal magnum from juvenile and egg-laying adult chickens
The paraffin-embedded magnum samples were stained with HE, TB, and PAS reagents (Figure 4). Morphologically, the magnum of the juvenile oviduct was simply lined by surface luminal epithelium, subepithelial stroma, and an outer longitudinal muscularis layer (Figure 4a-c). The juvenile oviduct had not completely developed the fine structures of a typical adult oviduct, which developmentally classified with epithelial cells and tubular gland cells. In the juvenile oviduct, TB was specifically stained the basal layer of the luminal epithelium. However, in the adult oviductal magnum, TB was strongly stained the pyramidal cells of the tubular glands with acidophilic cytoplasm and flat basal nuclei. This result suggests that TB was bound to the processed egg-white materials that were ready to be secreted into the lumen. In addition, PAS did not stain the juvenile oviduct, but predominantly stained both outer and inner layer of the tubular gland from the adult oviductal magnum. In adult, there was a critical difference between PAS reagent for glycogen and proteoglycan, and TB reagent for proteoglycan and glycosaminoglycan. This staining result indicates that secretory granules in the tubular gland layer can be divided into the outer and the inner layers and contain different types of polysaccharides, e.g., glycogen or proteoglycans in the inner layer and proteoglycans or glycosaminoglycan in the outer layer.
Lectin histochemical stating in the oviductal magnum
Summary of lectin-binding patterns in the juvenile and adult oviductal magnum
Source of Lectin
N-acetylglucosaminyl, sialic acid
In next experiment, the double-staining was also conducted with antibodies for OVA, ESR1 and PGR, and FITC-conjugated lectin WGA (Figure 6). Lectin WGA was broadly bound to the tubular gland, apical surface, and basal layer of luminal epithelium in the adult oviduct. The anti-OVA antibodies was strongly stained the tubular gland located in the outer layer of the oviductal magnum (Figure 6d), but not in the luminal epithelium which was positive for lectin WGA only (Figure 6g). The anti-ESR1 antibody was strongly stained the tubular gland located in the outer layer and luminal epithelium (Figure 6e, h), but not the inner layer of the tubular gland (Figure 6k). The anti-PGR antibody was stained both the tubular gland (Figure 6f, l) and epithelium (Figure 6i).
In this study, it revealed that the chicken oviductal magnums from juvenile and egg-laying adult hens were physiologically and functionally different, based on the studies of the ultrastructural analysis, quantitative RT-PCR analysis, immunohistochemical analysis of ovalbumin and steroid hormone receptors, and lectin histochemistry. Our results also indicated that the juvenile oviductal magnum was not differentiated into functional tubular gland cells, even though ciliated non-secretory cells were rarely observed on the luminal surface.
In chicken, juvenile oviductal magnum is simply lined up by undifferentiated oviductal epithelia, which could be cytodifferentiated into tubular gland cells by estrogen . Two types of columnar epithelial cells on the surface of the granular lumen and three types of tubular gland cells located under the luminal epithelium of the magnum mucosa were observed in the oviductal magnum from the egg-laying hen. Ciliated non-secretory cells were broadly scattered and covered the surface of the glandular lumen. Non-ciliated secretory cells were surrounded by numerous ciliated cells and secreted large masses of egg-white components such as ovalbumin. In the oviductal magnum, tubular gland cells are classified into another three different types: type A cells, filled with electron-dense granules; type B cells, filled with a large mass of homogenous material with low amounts of electron-dense granules; and type C cells, which are occupied by GER cisternae and a large and prominent Golgi area. The type C cells are regarded as recovered type A cells that have transferred their granules during passage of the egg . In the present study, we confirmed previous studies of the adult oviductal magnum comparing with the ultrastructural observations on the juvenile magnum region.
During development of the chicken oviduct, oviduct-specific gene expression and cytodifferentiation of epithelial to tubular gland cells is mainly triggered by steroid hormones. Basically, estrogen initiates the differentiation of progenitor cells of the epithelium into tubular gland cells in the magnum [1, 27, 28]. These cells then synthesize and secrete large amounts of major egg-white proteins (ovalbumin, conalbumin, lysozyme, and ovomucoid) . It is therefore no wonder that chicken oviductal epithelial cells express steroid/nuclear hormone receptors, including PGR and ESR [18, 19, 30, 31], which are induced by primary stimulation of estrogen and secondary stimulation of estrogen, progesterone, and glucocorticoids [1, 27, 32]. In this study, the mRNA expression levels of ESR1 and PGR in the juvenile oviductal magnum were significantly higher than those of the adult oviductal magnum. This result represents ESR1 and PGR are expressed in the oviductal epithelia and may receive steroid hormone signals, which regulate the vigorous proliferation and cytodifferentiation from the epithelium to the tubular gland at the juvenile stage. These signals result in a massive increase in oviduct size and weight before sexual maturation. However, directly comparing ESR1 and PGR mRNA expression in the juvenile and adult oviductal magnum was difficult because cell types and their populations in juvenile and adult oviduct were obviously different. Furthermore, anti-OVA, anti-ESR1, and anti-PGR antibodies were more strongly and obviously bound to the outer layer of the tubular gland, compared with the inner layer of adult oviduct. In contrast, lectin WGA and ConA were localized in the tubular gland cells of both layers of tubular gland. This result suggests that tubular gland cells located in the inner layer are not activated and differentiated enough to secret granules as compared with those in the outer layer of the tubular gland.
With respect to reproductive biology, lectins are known to act as functional molecules that regulate cell adhesion binding to glycoproteins. Lectins allow the sperm reservoir to interact with the oviductal epithelium . Specifically, they bind to a soluble carbohydrate or to a carbohydrate moiety that is part of extracellular and intracellular glycoproteins. In numerous studies on the mammalian oviduct, lectins have been used to detect a variety of carbohydrate residues such as mannose , fucose , galactose (N-acetylgalactosamine) [35–37], N-acetylglucosamine , and N-acetylneuraminic acid (sialic acid) . These studies also revealed that lectins such as Con A (concanavalin A; α-D-mannose and α-D-glucose) , HPA (Helix pomatia agglutinin; D-N-acetyl-galactosamine) [35, 36], LTA (Lotus tetragonolobus agglutinin; α-L-fucose), RCA 1 (Ricinus communis agglutinin 1; β-D-galactose), UEA-1 (Ulex europaeus agglutinin-1; α-L-fucose) , and WGA (Triticum vulgaris agglutinin; D-N-acetyl-glucosamine, and sialic acid)  can be exploited to identify certain components such as epithelial cell types in the oviduct. Those lectins play a crucial role in the binding of spermatozoa to epithelial cells and gamete interactions . Lectin-binding sites on the oviduct show different patterns depending on age, region, sex cycle, and estrous cycle [14, 40, 41]. Lectin studies, however, have primarily focused on the mammalian oviduct, and little is known regarding the chicken oviduct and glycoconjugates. In the present study, we revealed that lectins are selectively bound to the oviductal epithelium, stroma, and tubular gland layers. Particularly, lectin WGA and ConA bound to the electron-dense tubular gland cells in the chicken oviduct, which means that secretory granules of tubular gland are contained N-acetylglucosaminyl, sialic acid, D-mannosyl, and D-glucosyl residues in adult oviduct. These results also indicate that changes in hormonal responsiveness in the oviductal magnum during development can generate differences in the expression of sugars and glycosylation patterns of egg-white proteins . We hypothesize that these carbohydrate modifications might be involved in oviduct-specific gene expression, such as ovalbumin, and sperm adhesion for the fertilization. However, further studies are necessary to confirm this postulate.
In the biopharmaceutical industry, glycosylation is critically related to protein reactivity and modulates the efficacy of therapeutic proteins [43, 44]. The production of human pharmaceutical glycosylated proteins derived from mammalian cell lines have limited production capacity and require glycoengineering processes to add N-linked glycosylation . Potential advantages of using transgenic chickens as bioreactors include the simplistic egg mixture, which is composed of approximately 11 major proteins, the massive production of eggs, and similarities with the glycosylation of N- and O-linked glycans of humans as compared with other mammals [46, 47], which leads to a reduced potential risk for adverse immune responses to pharmaceutical proteins produced in eggs . For example, a study examining the glycosylation of IgGs in different species revealed that IgG from cows, sheep, and goats contain oligosaccharides with N-glycoyslneuraminic acid (NGNA), whereas humans and chickens only incorporate N-acethylneuraminic acid (NANA, referred to as sialic acid) , which shows a prolonged serum half-life and increased biological activity . Pathways for both N- and O-linked glycosylation are highly activated in the tubular gland cells of the oviduct, which secrete egg-white proteins that are almost all glycosylated. In this study, lectin-binding patterns in egg-laying hens demonstrated the need for combination studies examining glycosylation profiles of lectins and egg-white proteins and their precursors in the oviductal magnum. These profiles could provide a better understanding of the glycosylation of pharmaceutical proteins generated from transgenic chickens, including N-linked glycan and sialic acid, because the target tissue for producing recombinant proteins is the oviductal magnum. However, further studies would be necessary to characterize egg-white proteins and their precursors in the tubular gland of the oviductal magnum, classify sialic acid and N-acetyl-glucosamine that bind to lectin WGA, and identify the glycosylation profiles of therapeutic proteins from the oviduct.
Consequently, it is the first study to combine ultrastructural analysis, immunohistochemistry, and lectin-binding patterns of the juvenile and adult oviductal magnum in chickens. This study contributes to our understanding of the mechanisms underlying avian reproductive biology and transgenesis. In addition, these results can help to conduct further studies such as in vitro culture of oviductal cells, development of novel markers, glycoengineering for bioreactors, female reproductive biology, and immortalized cell-lines for producing exogenous proteins in vitro.
This work was supported by WCU (World Class University) Program (R31-10056) through the National Research Foundation of Korea funded by the Ministry of Education, Science and Technology. This work was also supported by a grant from the Next-Generation BioGreen 21 Program, Rural Development Administration, Republic of Korea.
- Palmiter RD, Wrenn JT: Interaction of estrogen and progesterone in chick oviduct development. 3. Tubular gland cell cytodifferentiation. J Cell Biol. 1971, 50: 598-615. 10.1083/jcb.50.3.598.PubMed CentralView ArticlePubMedGoogle Scholar
- Kohler PO, Grimley PM, O'Malley BW: Estrogen-induced cytodifferentiation of the ovalbumin-secreting glands of the chick oviduct. J Cell Biol. 1969, 40: 8-27. 10.1083/jcb.40.1.8.PubMed CentralView ArticlePubMedGoogle Scholar
- Kwon SC, Choi JW, Jang HJ, Shin SS, Lee SK, Park TS, Choi IY, Lee GS, Song G, Han JY: Production of biofunctional recombinant human interleukin 1 receptor antagonist (rhIL1RN) from transgenic quail egg white. Biol Reprod. 2010, 82: 1057-1064. 10.1095/biolreprod.109.081687.View ArticlePubMedGoogle Scholar
- Zhu L, van de Lavoir MC, Albanese J, Beenhouwer DO, Cardarelli PM, Cuison S, Deng DF, Deshpande S, Diamond JH, Green L, et al: Production of human monoclonal antibody in eggs of chimeric chickens. Nat Biotechnol. 2005, 23: 1159-1169. 10.1038/nbt1132.View ArticlePubMedGoogle Scholar
- Fertuck HC, Newstead JD: Fine structural observations on magnum mucosa in quail and hen oviducts. Z Zellforsch Mikrosk Anat. 1970, 103: 447-459. 10.1007/BF00337520.View ArticlePubMedGoogle Scholar
- Chousalkar KK, Roberts JR: Ultrastructural changes in the oviduct of the laying hen during the laying cycle. Cell Tissue Res. 2008, 332: 349-358. 10.1007/s00441-007-0567-3.View ArticlePubMedGoogle Scholar
- Magerd S, Somrit M, Prachaney P, Thongpan A, Chatchavalvanich K, Sretarugsa P, Weerachatyanukul W: Effect of progesterone administration on the distribution of oviductal carbohydrates in Rana tigrina. Cell Tissue Res. 2009, 336: 267-276. 10.1007/s00441-009-0772-3.View ArticlePubMedGoogle Scholar
- Sant'ana FJ, Nascimento EF, Gimeno EJ, Barbeito CG: Cyclic related and pathological changes in the lectin-binding sites on the swine oviduct. Reprod Domest Anim. 2005, 40: 40-45. 10.1111/j.1439-0531.2004.00551.x.View ArticlePubMedGoogle Scholar
- Desantis S, Acone F, Corriero A, Deflorio M, Zubani D, Ventriglia G, Palmieri G, De Metrio G: Distribution of sialoglycoconjugates in the oviductal isthmus of the horse during anoestrus, oestrus and pregnancy: a lectin histochemistry study. Eur J Histochem. 2004, 48: 403-412.View ArticlePubMedGoogle Scholar
- El-Mestrah M, Kan FW: Differential distribution of lectin-binding glycoconjugates in the secretory granules of hamster oviductal ampulla during the estrous cycle: a quantitative cytochemical analysis. Histochem Cell Biol. 1999, 111: 23-32. 10.1007/s004180050329.View ArticlePubMedGoogle Scholar
- Gheri G, Noci I, Sgambati E, Borri P, Taddei G, Bryk SG: Aging of the human oviduct: lectin histochemistry. Histol Histopathol. 2001, 16: 21-28.PubMedGoogle Scholar
- Walter I, Bavdek S: Lectin binding patterns of porcine oviduct mucosa and endometrium during the oestrous cycle. J Anat. 1997, 190: 299-307. 10.1046/j.1469-7580.1997.19020299.x.PubMed CentralView ArticlePubMedGoogle Scholar
- Cortes PP, Orihuela PA, Zuniga LM, Velasquez LA, Croxatto HB: Sperm binding to oviductal epithelial cells in the rat: role of sialic acid residues on the epithelial surface and sialic acid-binding sites on the sperm surface. Biol Reprod. 2004, 71: 1262-1269. 10.1095/biolreprod.104.027474.View ArticlePubMedGoogle Scholar
- Apichela SA, Valz-Gianinet JN, Schuster S, Jimenez-Diaz MA, Roldan-Olarte EM, Miceli DC: Lectin binding patterns and carbohydrate mediation of sperm binding to llama oviductal cells in vitro. Anim Reprod Sci. 2010, 118: 344-353. 10.1016/j.anireprosci.2009.07.008.View ArticlePubMedGoogle Scholar
- Flechon JE, Hunter RH: Distribution of spermatozoa in the utero-tubal junction and isthmus of pigs, and their relationship with the luminal epithelium after mating: a scanning electron microscope study. Tissue Cell. 1981, 13: 127-139. 10.1016/0040-8166(81)90043-4.View ArticlePubMedGoogle Scholar
- Hunter RH, Flechon B, Flechon JE: Distribution, morphology and epithelial interactions of bovine spermatozoa in the oviduct before and after ovulation: a scanning electron microscope study. Tissue Cell. 1991, 23: 641-656. 10.1016/0040-8166(91)90020-T.View ArticlePubMedGoogle Scholar
- Renkawitz R, Beug H, Graf T, Matthias P, Grez M, Schutz G: Expression of a chicken lysozyme recombinant gene is regulated by progesterone and dexamethasone after microinjection into oviduct cells. Cell. 1982, 31: 167-176. 10.1016/0092-8674(82)90416-0.View ArticlePubMedGoogle Scholar
- King WJ, Greene GL: Monoclonal antibodies localize oestrogen receptor in the nuclei of target cells. Nature. 1984, 307: 745-747. 10.1038/307745a0.View ArticlePubMedGoogle Scholar
- Renoir JM, Radanyi C, Yang CR, Baulieu EE: Antibodies against progesterone receptor from chick oviduct. Cross-reactivity with mammalian progesterone receptors. Eur J Biochem. 1982, 127: 81-86. 10.1111/j.1432-1033.1982.tb06840.x.View ArticlePubMedGoogle Scholar
- van de Lavoir MC, Diamond JH, Leighton PA, Mather-Love C, Heyer BS, Bradshaw R, Kerchner A, Hooi LT, Gessaro TM, Swanberg SE, et al: Germline transmission of genetically modified primordial germ cells. Nature. 2006, 441: 766-769. 10.1038/nature04831.View ArticlePubMedGoogle Scholar
- Sang H: Transgenesis sunny-side up. Nat Biotechnol. 2006, 24: 955-956. 10.1038/nbt0806-955.View ArticlePubMedGoogle Scholar
- Han JY: Germ cells and transgenesis in chickens. Comp Immunol Microbiol Infect Dis. 2009, 32: 61-80. 10.1016/j.cimid.2007.11.010.View ArticlePubMedGoogle Scholar
- Jung JG, Lee YM, Park TS, Park SH, Lim JM, Han JY: Identification, culture, and characterization of germline stem cell-like cells in chicken testes. Biol Reprod. 2007, 76: 173-182. 10.1095/biolreprod.106.056275.View ArticlePubMedGoogle Scholar
- Jung JG, Kim DK, Park TS, Lee SD, Lim JM, Han JY: Development of novel markers for the characterization of chicken primordial germ cells. Stem Cells. 2005, 23: 689-698. 10.1634/stemcells.2004-0208.View ArticlePubMedGoogle Scholar
- Draper MH, Davidson MF, Wyburn GM, Johnston HS: The fine structure of the fibrous membrane forming region of the isthmus of the oviduct of Gallus domesticus. Q J Exp Physiol Cogn Med Sci. 1972, 57: 297-310.PubMedGoogle Scholar
- Wyburn GM, Johnston HS, Draper MH: The magnum of the hen's oviduct as a protein secreting organ. J Anat. 1970, 106: 174-PubMedGoogle Scholar
- Oka T, Schimke RT: Interaction of estrogen and progesterone in chick oviduct development. I. Antagonistic effect of progesterone on estrogen-induced proliferation and differentiation of tubular gland cells. J Cell Biol. 1969, 41: 816-831. 10.1083/jcb.41.3.816.PubMed CentralView ArticlePubMedGoogle Scholar
- Pageaux JF, Dufrene L, Laugier C, Perche O, Sandoz D: Heterogeneity of progesterone receptor expression in epithelial cells of immature and differentiating quail oviduct. Biol Cell. 1989, 67: 135-140. 10.1016/0248-4900(89)90047-6.View ArticlePubMedGoogle Scholar
- Shepherd JH, Mulvihill ER, Thomas PS, Palmiter RD: Commitment of chick oviduct tubular gland cells to produce ovalbumin mRNA during hormonal withdrawal and restimulation. J Cell Biol. 1980, 87: 142-151. 10.1083/jcb.87.1.142.View ArticlePubMedGoogle Scholar
- Mester J, Baulieu EE: Progesterone receptors in the chick oviduct. Determination of the total concentration of binding sites in the cytosol and nuclear fraction and effect of progesterone on their distribution. Eur J Biochem. 1977, 72: 405-414. 10.1111/j.1432-1033.1977.tb11265.x.View ArticlePubMedGoogle Scholar
- Lebeau MC, Massol N, Baulieu EE: Oestrogen and progesterone receptors in chick oviduct chromatin after administration of oestradiol, progesterone or anti-oestrogen. Biochem J. 1982, 204: 653-662.PubMed CentralView ArticlePubMedGoogle Scholar
- Sanders MM, McKnight GS: Chicken egg white genes: multihormonal regulation in a primary cell culture system. Endocrinology. 1985, 116: 398-405. 10.1210/endo-116-1-398.View ArticlePubMedGoogle Scholar
- Topfer-Petersen E: Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum Reprod Update. 1999, 5: 314-329. 10.1093/humupd/5.4.314.View ArticlePubMedGoogle Scholar
- Goldstein IJ, Hayes CE: The lectins: carbohydrate-binding proteins of plants and animals. Adv Carbohydr Chem Biochem. 1978, 35: 127-340.View ArticlePubMedGoogle Scholar
- Hammarstrom S, Murphy LA, Goldstein IJ, Etzler ME: Carbohydrate binding specificity of four N-acetyl-D-galactosamine- "specific" lectins: Helix pomatia A hemagglutinin, soy bean agglutinin, lima bean lectin, and Dolichos biflorus lectin. Biochemistry. 1977, 16: 2750-2755. 10.1021/bi00631a025.View ArticlePubMedGoogle Scholar
- Roth J: Cytochemical localization of terminal N-acetyl-D-galactosamine residues in cellular compartments of intestinal goblet cells: implications for the topology of O-glycosylation. J Cell Biol. 1984, 98: 399-406. 10.1083/jcb.98.2.399.View ArticlePubMedGoogle Scholar
- Hartig W, Brauer K, Bruckner G: Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport. 1992, 3: 869-872. 10.1097/00001756-199210000-00012.View ArticlePubMedGoogle Scholar
- Debray H, Decout D, Strecker G, Spik G, Montreuil J: Specificity of twelve lectins towards oligosaccharides and glycopeptides related to N-glycosylproteins. Eur J Biochem. 1981, 117: 41-55.View ArticlePubMedGoogle Scholar
- Sughii S, Kabat EA, Baer HH: Further immunochemical studies on the combining sites of Lotus tetragonolobus and Ulex europaeus I and II lectins. Carbohydr Res. 1982, 99: 99-101. 10.1016/S0008-6215(00)80982-9.View ArticlePubMedGoogle Scholar
- Diekman AB: Glycoconjugates in sperm function and gamete interactions: how much sugar does it take to sweet-talk the egg?. Cell Mol Life Sci. 2003, 60: 298-308. 10.1007/s000180300025.View ArticlePubMedGoogle Scholar
- Raychoudhury SS, Suarez SS, Buhi WC: Distribution of lectin binding sites in the oviducts of cycling and hormone-treated pigs. J Exp Zool. 1993, 265: 659-668. 10.1002/jez.1402650608.View ArticlePubMedGoogle Scholar
- Ito K, Ishimaru T, Kimura F, Matsudomi N: Importance of N-glycosylation positioning for secretion and folding of ovalbumin. Biochem Biophys Res Commun. 2007, 361: 725-731. 10.1016/j.bbrc.2007.07.066.View ArticlePubMedGoogle Scholar
- Hossler P, Khattak SF, Li ZJ: Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology. 2009, 19: 936-949. 10.1093/glycob/cwp079.View ArticlePubMedGoogle Scholar
- Varki A: Biological roles of oligosaccharides: all of the theories are correct. Glycobiology. 1993, 3: 97-130. 10.1093/glycob/3.2.97.View ArticlePubMedGoogle Scholar
- Elliott S, Lorenzini T, Asher S, Aoki K, Brankow D, Buck L, Busse L, Chang D, Fuller J, Grant J, et al: Enhancement of therapeutic protein in vivo activities through glycoengineering. Nat Biotechnol. 2003, 21: 414-421. 10.1038/nbt799.View ArticlePubMedGoogle Scholar
- Galili U, Shohet SB, Kobrin E, Stults CL, Macher BA: Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. J Biol Chem. 1988, 263: 17755-17762.PubMedGoogle Scholar
- Raju TS, Briggs JB, Borge SM, Jones AJ: Species-specific variation in glycosylation of IgG: evidence for the species-specific sialylation and branch-specific galactosylation and importance for engineering recombinant glycoprotein therapeutics. Glycobiology. 2000, 10: 477-486. 10.1093/glycob/10.5.477.View ArticlePubMedGoogle Scholar
- Lillico SG, McGrew MJ, Sherman A, Sang HM: Transgenic chickens as bioreactors for protein-based drugs. Drug Discov Today. 2005, 10: 191-196. 10.1016/S1359-6446(04)03317-3.View ArticlePubMedGoogle Scholar
- Byrne B, Donohoe GG, O'Kennedy R: Sialic acids: carbohydrate moieties that influence the biological and physical properties of biopharmaceutical proteins and living cells. Drug Discov Today. 2007, 12: 319-326. 10.1016/j.drudis.2007.02.010.View ArticlePubMedGoogle Scholar
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