Top

Reproductive Biology and Endocrinology

Published in:

Open Access 01-12-2011 | Research

Structural and histological characterization of oviductal magnum and lectin-binding patterns in Gallus domesticus

Authors: Jin Gyoung Jung, Whasun Lim, Tae Sub Park, Jin Nam Kim, Beom Ku Han, Gwonhwa Song, Jae Yong Han

Published in: Reproductive Biology and Endocrinology | Issue 1/2011

Abstract

Background

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.

Methods

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.

Results

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.

Conclusions

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.

Available only for authorised users

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.PubMedCentralCrossRefPubMed

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.PubMedCentralCrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

10.

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.CrossRefPubMed

11.

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.PubMed

12.

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.PubMedCentralCrossRefPubMed

13.

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.CrossRefPubMed

14.

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.CrossRefPubMed

15.

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.CrossRefPubMed

16.

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.CrossRefPubMed

17.

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.CrossRefPubMed

18.

King WJ, Greene GL: Monoclonal antibodies localize oestrogen receptor in the nuclei of target cells. Nature. 1984, 307: 745-747. 10.1038/307745a0.CrossRefPubMed

19.

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.CrossRefPubMed

20.

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.CrossRefPubMed

21.

Sang H: Transgenesis sunny-side up. Nat Biotechnol. 2006, 24: 955-956. 10.1038/nbt0806-955.CrossRefPubMed

22.

Han JY: Germ cells and transgenesis in chickens. Comp Immunol Microbiol Infect Dis. 2009, 32: 61-80. 10.1016/j.cimid.2007.11.010.CrossRefPubMed

23.

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.CrossRefPubMed

24.

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.CrossRefPubMed

25.

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.PubMed

26.

Wyburn GM, Johnston HS, Draper MH: The magnum of the hen's oviduct as a protein secreting organ. J Anat. 1970, 106: 174-PubMed

27.

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.PubMedCentralCrossRefPubMed

28.

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.CrossRefPubMed

29.

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.CrossRefPubMed

30.

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.CrossRefPubMed

31.

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.PubMedCentralCrossRefPubMed

32.

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.CrossRefPubMed

33.

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.CrossRefPubMed

34.

Goldstein IJ, Hayes CE: The lectins: carbohydrate-binding proteins of plants and animals. Adv Carbohydr Chem Biochem. 1978, 35: 127-340.CrossRefPubMed

35.

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.CrossRefPubMed

36.

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.CrossRefPubMed

37.

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.CrossRefPubMed

38.

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.CrossRefPubMed

39.

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.CrossRefPubMed

40.

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.CrossRefPubMed

41.

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.CrossRefPubMed

42.

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.CrossRefPubMed

43.

Hossler P, Khattak SF, Li ZJ: Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology. 2009, 19: 936-949. 10.1093/glycob/cwp079.CrossRefPubMed

44.

Varki A: Biological roles of oligosaccharides: all of the theories are correct. Glycobiology. 1993, 3: 97-130. 10.1093/glycob/3.2.97.CrossRefPubMed

45.

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.CrossRefPubMed

46.

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.PubMed

47.

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.CrossRefPubMed

48.

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.CrossRefPubMed

49.

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.CrossRefPubMed

Title: Structural and histological characterization of oviductal magnum and lectin-binding patterns in Gallus domesticus
Authors: Jin Gyoung Jung
Whasun Lim
Tae Sub Park
Jin Nam Kim
Beom Ku Han
Gwonhwa Song
Jae Yong Han
Publication date: 01-12-2011
Publisher: BioMed Central
Published in: Reproductive Biology and Endocrinology / Issue 1/2011
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/1477-7827-9-62

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Structural and histological characterization of oviductal magnum and lectin-binding patterns in Gallus domesticus

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2011

An efficient protocol for inducing pseudopregnancy using estradiol dipropionate and follicular development associated with changes in reproductive hormones after prostaglandin F2alpha treatment in pseudopregnant sows

Comparison of the effect of a CIDR-Select Synch versus a long-term CIDR based AI protocol on reproductive performance in multiparous dairy cows in Swiss dairy farms

Levels of soluble fms-like tyrosine kinase one in first trimester and outcomes of pregnancy: a systematic review

Ficus platyphylla promotes fertility in female Rattus norvegicus Wistar strain: a preliminary study

Co-culturing of follicles with interstitial cells in collagen gel reproduce follicular development accompanied with theca cell layer formation

Modulation of small leucine-rich proteoglycans (SLRPs) expression in the mouse uterus by estradiol and progesterone