Skip to main content

Advertisement

SpringerLink
Log in

Sex steroids modulate morphological and functional features of the bovine oviduct

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

In cattle, the oviduct plays a major role in the reproductive process; however, molecular control of oviduct receptivity to the embryo is poorly understood. A model for receptivity based on size of the pre-ovulatory follicle (POF) was used to compare oviductal morphology, cellular proliferation, and candidate transcript abundance. Growth of the POF of Nelore (Bos indicus) cows was manipulated to produce two groups: a large POF-large corpus luteum (CL) group (LF-LCL; greater receptivity) and a small POF-small CL group (SF-SCL). Samples of the ampulla and isthmus ipsilateral and contralateral to CL were collected 4 days after GnRH-induced ovulation. Tissues were either embedded in paraffin for Harris-Hematoxylin and Eosin and periodic acid-Schiff staining and KI67 immunostaining, followed by morphological analyses, or stored at −80 °C for RNA extraction, cDNA synthesis, and qPCR analyses. The effects of group (LF-LCL and SF-SCL), region (ampulla and isthmus), and side (ipsilateral and contralateral) were analyzed using three-way nested ANOVA. The ipsilateral ampulla of the LF-LCL group presented more primary mucosal folds, a greater mucosal-folding grade and luminal perimeter, and more secretory cells and proliferating cells when compared with the ampulla of the SF-SCL group and with the contralateral ampulla of both groups. There were no morphological differences in the isthmus between groups and sides. Changes in transcript abundance are suggestive of LF-LCL-stimulated secretory activity. In summary, ovulation of a larger POF generates a periovulatory endocrine milieu that modulates morphological and functional features of the bovine oviduct which may support embryo survival and development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abe H (1996) The mammalian oviductal epithelium: regional variations in cytological and functional aspects of the oviductal secretory cells. Histol Histopathol 11:743–768

    CAS  PubMed  Google Scholar 

  • Agduhr E (1927) Studies on the structure and development of the bursa ovarica and the tuba uterina in the mouse. Acta Zool 8:1–133

    Article  Google Scholar 

  • Aguilar J, Reyley M (2005) The uterine tubal fluid: secretion, composition and biological effects. Anim Reprod 2:91–105

    Google Scholar 

  • Ahumada CJ, Salvador I, Cebrian-Serrano A, Lopera R, Silvestre MA (2013) Effect of supplementation of different growth factors in embryo culture medium with a small number of bovine embryos on in vitro embryo development and quality. Animal 7:455–462

    Article  CAS  PubMed  Google Scholar 

  • Ashworth CJ, Sales DI, Wilmut I (1989) Evidence of an association between the survival of embryos and the periovulatory plasma progesterone concentration in the ewe. J Reprod Fertil 87:23–32

    Article  CAS  PubMed  Google Scholar 

  • Aviles M, Gutierrez-Adan A, Coy P (2010) Oviductal secretions: will they be key factors for the future ARTs? Mol Hum Reprod 16:896–906

    Article  PubMed  Google Scholar 

  • Ayen E, Shahrooz R, Kazemie S (2012) Histological and histomorphometrical changes of different regions of oviduct during follicular and lutealphases of estrus cycle in adult Azarbaijan buffalo. Iran J Vet Res 13:42–48

    Google Scholar 

  • Bacha WJ, Bacha LM (2012) Color atlas of veterinary histology, 3rd edn. Wiley-Blackwell, New York

  • Besenfelder U, Havlicek V, Brem G (2012) Role of the oviduct in early embryo development. Reprod Domest Anim 47:156–163

    Article  PubMed  Google Scholar 

  • Brower L, Anderson E (1969) Cytological events associated with the secretory process in the rabbit oviduct. Biol Reprod 1:130–148

    Article  CAS  PubMed  Google Scholar 

  • Buhi WC, Bazer FW, Alvarez IM, Mirando MA (1991) In vitro synthesis of oviductal proteins associated with estrus and 17 beta-estradiol-treated ovariectomized ewes. Endocrinology 128:3086–3095

    Article  CAS  PubMed  Google Scholar 

  • Buhi WC, Ashworth CJ, Bazer FW, Alvarez IM (1992) In vitro synthesis of oviductal secretory proteins by estrogen-treated ovariectomized gilts. J Exp Zool 262:426–435

    Article  CAS  PubMed  Google Scholar 

  • Buhi WC, Alvarez IM, Kouba AJ (2000) Secreted proteins of the oviduct. Cells Tissues Organs 166:165–179

    Article  CAS  PubMed  Google Scholar 

  • Chanrota M, Guoa Y, Dalina AM, Perssonb E, Bågea R, Svenssona A, Gustafssona H, Humblota P (2017) Dose related effects of LPS on endometrial epithelial cell populations from dioestrus cows. Anim Reprod Sci 177:12–24

    Article  Google Scholar 

  • Demetrio DG, Santos RM, Demetrio CG, Vasconcelos JL (2007) Factors affecting conception rates following artificial insemination or embryo transfer in lactating Holstein cows. J Dairy Sci 90:5073–5082

    Article  CAS  PubMed  Google Scholar 

  • Donnez J, Casanas-Roux F, Caprasse J, Ferin J, Thomas K (1985) Cyclic changes in ciliation, cell height, and mitotic activity in human tubal epithelium during reproductive life. Fertil Steril 43:554–559

    Article  CAS  PubMed  Google Scholar 

  • Eriksen T, Terkelsen O, Hyttel P, Greve T (1994) Ultrastructural features of secretory-cells in the bovine oviduct epithelium. Anat Embryol 190:583–590

    Article  CAS  PubMed  Google Scholar 

  • Gandolfi F, Brevini TAL, Richardson L, Brown CR, Moor RM (1989) Characterization of proteins secreted by sheep oviduct epithelial-cells and their function in embryonic-development. Development 106:303–312

    CAS  PubMed  Google Scholar 

  • García EV, Hamdi M, Barrera AD, Sánchez-Calabuig MJ, Gutiérrez-Adán A, Rizos D (2017) Bovine embryo-oviduct interaction in vitro reveals an early cross talk mediated by BMP signaling. Reproduction 153:631–643

    Article  PubMed  Google Scholar 

  • Gonella-Diaza A, Andrade S, Sponchiado M, Pugliesi G, Mesquita F, Van Hoeck V, Strefezzi R, Gasparin G, Coutinho L, Binelli M (2015) Size of the ovulatory follicle dictates spatial differences in the oviductal transcriptome in cattle. PLoS ONE 10:e0145321

    Article  PubMed  PubMed Central  Google Scholar 

  • Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA, Bazer FW, Spencer TE (2001) Developmental biology of uterine glands. Biol Reprod 65:1311–1323

    Article  CAS  PubMed  Google Scholar 

  • Hunter RH (1998) Have the fallopian tubes a vital role in promoting fertility? Acta Obstet Gynecol Scand 77:475–486

    Article  CAS  PubMed  Google Scholar 

  • Hunter RH (2012) Components of oviduct physiology in eutherian mammals. Biol Rev Camb Philos Soc 87:244–255

    Article  CAS  PubMed  Google Scholar 

  • Hunter RH, Cook B, Poyser NL (1983) Regulation of oviduct function in pigs by local transfer of ovarian steroids and prostaglandins: a mechanism to influence sperm transport. Eur J Obstet Gynecol Reprod Biol 14:225–232

    Article  CAS  PubMed  Google Scholar 

  • Ito S, Kobayashi Y, Yamamoto Y, Kimura K, Okuda K (2016) Remodeling of bovine oviductal epithelium by mitosis of secretory cells. Cell Tissue Res 366:403–410

    Article  CAS  PubMed  Google Scholar 

  • Jordaens L, Van Hoeck V, Maillo V, Gutierrez-Adan A, Marei WFA, Vlaeminck B, Thys S, Sturmey RG, Bols PEJ, Leroy JLMR (2017) Maternal metabolic stress may affect oviduct gatekeeper function. Reproduction 153:759–773

    Article  CAS  PubMed  Google Scholar 

  • Kenngott RA, Sinowatz F (2007) Prenatal development of the bovine oviduct. Anat Histol Embryol 36:272–283

    Article  PubMed  Google Scholar 

  • Kolle S, Dubielzig S, Reese S, Wehrend A, Konig P, Kummer W (2009) Ciliary transport, gamete interaction, and effects of the early embryo in the oviduct: ex vivo analyses using a new digital videomicroscopic system in the cow. Biol Reprod 81:267–274

    Article  PubMed  Google Scholar 

  • Konishi I, Fujii S, Parmley TH, Mori T (1987) Development of ciliated cells in the human fetal oviduct: an ultrastructural study. Anat Rec 219:60–68

    Article  CAS  PubMed  Google Scholar 

  • Leese HJ (1988) The formation and function of oviduct fluid. J Reprod Fertil 82:843–856

    Article  CAS  PubMed  Google Scholar 

  • McDaniel JW, Scalzi H, Black D (1968) Influence of ovarian hormones on histology and histochemistry of the bovine oviduct. J Dairy Sci 51:754–761

    Article  CAS  PubMed  Google Scholar 

  • Mesquita FS, Pugliesi G, Scolari SC, Franca MR, Ramos RS, Oliveira M, Papa PC, Bressan FF, Meirelles FV, Silva LA, Nogueira GP, Membrive CM, Binelli M (2014) Manipulation of the periovulatory sex steroidal milieu affects endometrial but not luteal gene expression in early diestrus Nelore cows. Theriogenology 81:861–869

    Article  CAS  PubMed  Google Scholar 

  • Mesquita FS, Ramos RS, Pugliesi G, Andrade SC, Van Hoeck V, Langbeen A, Oliveira ML, Gonella-Diaza AM, Gasparin G, Fukumasu H, Pulz LH, Membrive CM, Coutinho LL, Binelli M (2015) The receptive endometrial transcriptomic signature indicates an earlier shift from proliferation to metabolism at early Diestrus in the cow. Biol Reprod 93:52

    Article  CAS  PubMed  Google Scholar 

  • Mokhtar DM (2015) Microscopic and histochemical characterization of the bovine uterine tube during the follicular and luteal phases of estrous cycle. J Microsc Ultrastruct 3:44–52

    Article  Google Scholar 

  • Morris D, Diskin M (2008) Effect of progesterone on embryo survival. Animal 2:1112–1119

    Article  CAS  PubMed  Google Scholar 

  • Peres RF, Claro I Jr, Sa Filho OG, Nogueira GP, Vasconcelos JL (2009) Strategies to improve fertility in Bos indicus postpubertal heifers and non-lactating cows submitted to fixed-time artificial insemination. Theriogenology 72:681–689

    Article  CAS  PubMed  Google Scholar 

  • Pugliesi G, Santos FB, Lopes E, Nogueira É, Maio JR, Binelli M (2016) Improved fertility in suckled beef cows ovulating large follicles or supplemented with long-acting progesterone after timed-AI. Theriogenology 85:1239–1248

    Article  CAS  PubMed  Google Scholar 

  • Restall BJ (1966) Histological observations on the reproductive tract of the ewe. Aust J Biol Sci 19:673–686

    Article  CAS  PubMed  Google Scholar 

  • Rizos D, Fair T, Papadopoulos S, Boland MP, Lonergan P (2002a) Developmental, qualitative, and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro. Mol Reprod Dev 62:320–327

    Article  CAS  PubMed  Google Scholar 

  • Rizos D, Lonergan P, Boland MP, Arroyo-Garcia R, Pintado B, de la Fuente J, Gutierrez-Adan A (2002b) Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality. Biol Reprod 66:589–595

    Article  CAS  PubMed  Google Scholar 

  • Rizos D, Ward F, Duffy P, Boland MP, Lonergan P (2002c) Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev 61:234–248

    Article  CAS  PubMed  Google Scholar 

  • Simintiras CA, Fröhlich T, Sathyapalan T, Arnold GJ, Ulbrich SE, Leese HJ, Sturmey RG (2016) Modelling oviduct fluid formation in vitro. Reproduction 153:23–33

    Article  Google Scholar 

  • Smit A, Hubley R, Green P (1996-2010) RepeatMasker Open-3.0. http://www.repeatmasker.org

  • Vasconcelos JLM, Sartori R, Oliveira HN, Guenther JG, Wiltbank MC (2001) Reduction in size of the ovulatory follicle reduces subsequent luteal size and pregnancy rate. Theriogenology 56:307–314

    Article  CAS  PubMed  Google Scholar 

  • Wang CK, Robinson RS, Flint APF, Mann GE (2007) Quantitative analysis of changes in endometrial gland morphology during the bovine oestrous cycle and their association with progesterone levels. Reproduction 134:365–371

    Article  CAS  PubMed  Google Scholar 

  • Wetscher F, Havlicek V, Huber T, Muller M, Brem G, Besenfelder U (2005) Effect of morphological properties of transferred embryonic stages on tubal migration implications for in vivo culture in the bovine oviduct. Theriogenology 64:41–48

    Article  CAS  PubMed  Google Scholar 

  • Wijayagunawardane MPB, Cerbito WA, Miyamoto A, Acosta TJ, Takagi M, Miyazawa K, Sato K (1996) Oviductal progesterone concentration and its spatial distribution in cyclic and early pregnant cows. Theriogenology 46:1149–1158

    Article  CAS  PubMed  Google Scholar 

  • Wijayagunawardane MPB, Miyamoto A, Cerbito WA, Acosta TJ, Takagi M, Sato K (1998) Local distributions of oviductal estradiol, progesterone, prostaglandins, oxytocin and endothelin-1 in the cyclic cow. Theriogenology 49:607–618

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka S, Abe H, Sakumoto OK (2013) Proliferation of luteal steroidogenic cells in cattle. PLoS ONE 8:e84186

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank M. R. França, R. S. Ramos, E. Lopes, E. R. Araujo, M. L. Oliveira, and C. M. Membrive for technical assistance; and the administration of the Pirassununga campus of the University of São Paulo for assistance in animal handling.

Author information

Authors and Affiliations

  1. Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Pirassununga, São Paulo, Brazil

    Angela Maria Gonella-Diaza, Kauê Ribeiro da Silva, Júlio Cesar de Carvalho Balieiro & Mario Binelli

  2. Curso de Medicina Veterinária, Universidade Federal do Pampa, Uruguaiana, Rio Grande do Sul, Brazil

    Fernando Silveira Mesquita

  3. Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, São Paulo, Brazil

    Nilton Pedro dos Santos, Guilherme Pugliesi & Ricardo de Francisco Strefezzi

Authors
  1. Angela Maria Gonella-Diaza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando Silveira Mesquita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kauê Ribeiro da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Júlio Cesar de Carvalho Balieiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nilton Pedro dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guilherme Pugliesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ricardo de Francisco Strefezzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mario Binelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mario Binelli.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.

Funding

This research was funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) PEC-PG program: AMGD grant number 15068–12-9; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP): MB grant number 2011/03226–4. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gonella-Diaza, A.M., Mesquita, F.S., da Silva, K.R. et al. Sex steroids modulate morphological and functional features of the bovine oviduct. Cell Tissue Res 370, 319–333 (2017). https://doi.org/10.1007/s00441-017-2666-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-017-2666-0

Keywords

Search

Navigation