Cystic ovary disease (COD) alters structure and function of the bovine oviduct.
cystic ovary disease
oviduct
sperm reservoir
structure and function
Journal
Molecular reproduction and development
ISSN: 1098-2795
Titre abrégé: Mol Reprod Dev
Pays: United States
ID NLM: 8903333
Informations de publication
Date de publication:
Jan 2024
Jan 2024
Historique:
revised:
26
09
2023
received:
22
05
2023
accepted:
14
12
2023
medline:
29
1
2024
pubmed:
29
1
2024
entrez:
29
1
2024
Statut:
ppublish
Résumé
Cystic ovary disease (COD) is a common cause of subfertility in dairy cattle. Therefore, the aim of this study was to provide novel concepts for cyst classification and to investigate the effects of COD on tubal microarchitecture, oviductal metabolic function, and the formation of the sperm reservoir. Bovine Fallopian tubes affected by follicular cysts, follicular cysts with luteinization and luteal cysts were investigated by a variety of microscopic and histological techniques and compared to control cows in metestrus and diestrus. We defined three types of cysts involved in COD, each of which had a characteristic wall thickness, inner wall appearance and cellular pattern within the cyst aspirate. Regarding the Fallopian tube, each cyst type was associated with a characteristic morphology, specifically the microarchitecture of the folds in ampulla, epithelial cell ratios, and ciliated/secretory cell size and form. Furthermore, each cyst type showed different patterns of tubal glycoprotein and acidic mucopolysaccharide synthesis, which was highly variable as compared to the controls. Our studies are the first to characterize the effects of COD on the Fallopian tube, which promotes the establishment of novel, cyst-specific therapeutic concepts in cattle and helps gain a holistic view of the causes of subfertility in cows with COD.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23725Informations de copyright
© 2024 The Authors. Molecular Reproduction and Development published by Wiley Periodicals LLC.
Références
Abe, H., & Oikawa, T. (1993). Observations by scanning electron microscopy of oviductal epithelial cells from cows at follicular and luteal phases. The Anatomical Record, 235(3), 399-410. https://doi.org/10.1002/ar.1092350309
Arosh, J. A., Parent, J., Chapdelaine, P., Sirois, J., & Fortier, M. A. (2002). Expression of cyclooxygenases 1 and 2 and prostaglandin E synthase in bovine endometrial tissue during the estrous cycle. Biology of Reproduction, 67(1), 161-169. https://doi.org/10.1095/biolreprod67.1.161
Bastos, N. M., Ferst, J. G., Goulart, R. S., & Coelho da Silveira, J. (2022). The role of the oviduct and extracellular vesicles during early embryo development in bovine. Animal Reproduction, 19(1), 1-13. https://doi.org/10.1590/1984-3143-AR2022-0015
Binelli, M., Gonella-diaza, A. M., Mesquita, F. S., & Membrive, C. (2018). Sex steroid-mediated control of oviductal function in cattle. Biology, 7(15). https://doi.org/10.3390/biology7010015
Bjorkman, N., & Fredricsson, B. (1961). The bovine oviduct epithelium and its secretory process as studied with the electron microscope and histochemical tests. Zeitschrift fur Zellforschung und mikroskopische Anatomie (Vienna, Austria: 1948), 55, 500-513. https://doi.org/10.1007/BF00325415
Borş, S., & Borş, A. (2020). Ovarian cysts, an anovulatory condition in dairy cattle. Journal of Veterinary Medical Science, 82(10), 1515-1522. https://doi.org/10.1292/jvms.20-0381
Brenner, R. M. (1969). Renewal of oviduct cilia during the menstrual cycle of the rhesus monkey. Fertility and Sterility, 20(4), 599-611. https://doi.org/10.1016/S0015-0282(16)37086-8
Brodzki, P., Brodzki, A., Krakowski, L., Dąbrowski, R., Szczubiał, M., & Bochniarz, M. (2019). Levels of selected cytokines and acute-phase proteins in the serum of dairy cows with cystic ovarian disease and those in follicular and luteal phases of normal ovarian cycle. Research in Veterinary Science, 123(December 2018), 20-25. https://doi.org/10.1016/j.rvsc.2018.12.007
Camara Pirez, M., Steele, H., Reese, S., & Kölle, S. (2020). Bovine sperm-oviduct interactions are characterized by specific sperm behaviour, ultrastructure and tubal reactions which are impacted by sex sorting. Scientific Reports, 10(1), 16522. https://doi.org/10.1038/s41598-020-73592-1
Cattaneo, L., Signorini, M., Bertoli, J., Bartolomé, J., Gareis, N., Díaz, P., Bó, G., & Ortega, H. (2014). Epidemiological description of cystic ovarian disease in Argentine dairy herds: Risk factors and effects on the reproductive performance of lactating cows. Reproduction in Domestic Animals, 49, 1028-1033. https://doi.org/10.1111/rda.12432
Çolakoğlu, H. E., Küplülü, S., Polat, I. M., Pekcan, M., Özenç, E., Baklacı, C., Seyrek-İntaş, K., Gümen, A., & Vural, M. R. (2020). Association among lipopolysaccharide, the transforming growth factor-beta superfamily, follicular growth, and transcription factors in spontaneous bovine ovarian cysts. Domestic Animal Endocrinology, 70, 106398. https://doi.org/10.1016/j.domaniend.2019.106398
Croxatto, H. B. (2002). Physiology of gamete and embryo transport through the fallopian tube. Reproductive BioMedicine Online, 4(2), 160-169. https://doi.org/10.1016/S1472-6483(10)61935-9
Dixon, R. E., Hwang, S. J., Kim, B. H., Sanders, K. M., & Ward, S. M. (2019). Myosalpinx contractions are essential for egg transport along the oviduct and are disrupted in reproductive tract diseases. Advances in Experimental Medicine and Biology, 1124, 265-294. https://doi.org/10.1007/978-981-13-5895-1_11
Douthwaite, R., & Dobson, H. (2000). Comparison of different methods of diagnosis of cystic ovarian disease in cattle and an assessment of its treatment with a progesterone-releasing intravaginai device. Veterinary Record, 147, 355-359. https://doi.org/10.1136/vr.147.13.355
Eriksen, T., Terkelsen, O., Hyttel, P., & Greve, T. (1994). Ultrastructural features of secretory cells in the bovine oviduct epithelium. Anatomy and Embryology, 190, 583-590. https://doi.org/10.1007/BF00190108
Fernandez-Fuertes, B., Rodríguez-alonso, B., Sánchez, J. M., Simintiras, C. A., Lonergan, P., & Rizos, D. (2018). Looking at the big picture: Understanding how the oviduct’ s dialogue with gametes and the embryo shapes reproductive success. Animal Reproduction, 15, 751-764. https://doi.org/10.21451/1984-3143-AR2018-0036
Gareis, N. C., Rodríguez, F. M., Cattaneo Moreyra, M. L., Stassi, A. F., Angeli, E., Etchevers, L., Salvetti, N. R., Ortega, H. H., Hein, G. J., & Rey, F. (2023). Contribution of key elements of nutritional metabolism to the development of cystic ovarian disease in dairy cattle. Theriogenology, 197, 209-223. https://doi.org/10.1016/j.theriogenology.2022.12.003
Ghosh, A., Syed, S. M., & Tanwar, P. S. (2017). In vivo genetic cell lineage tracing reveals that oviductal secretory cells self-renew and give rise to ciliated cells. Development (Cambridge, England), 144(17), 3031-3041. https://doi.org/10.1242/dev.149989
Ginther, O. J. (2020a). Intraovarianism. Local mechanisms that affect follicle and luteal dynamics in heifers and women. Biology of Reproduction, 102(2), 265-275. https://doi.org/10.1093/biolre/ioz199
Ginther, O. J. (2020b). Selection of side of ovulation by intraovarianism in Bos Taurus heifers. Biology of Reproduction, 103(4), 711-716. https://doi.org/10.1093/biolre/ioaa118
Gobikrushanth, M., Salehi, R., Ambrose, D. J., & Colazo, M. G. (2016). Categorization of endometritis and its association with ovarian follicular growth and ovulation, reproductive performance, dry matter intake, and milk yield in dairy cattle. Theriogenology, 86(7), 1842-1849. https://doi.org/10.1016/j.theriogenology.2016.06.003
Ireland, J. J., Murphee, R. L., & Coulson, P. B. (1980). Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. Journal of Dairy Science, 63(1), 155-160. https://doi.org/10.3168/jds.S0022-0302(80)82901-8
Ito, S., Kobayashi, Y., Yamamoto, Y., Kimura, K., & Okuda, K. (2016). Remodeling of bovine oviductal epithelium by mitosis of secretory cells. Cell and Tissue Research, 366, 403-410. https://doi.org/10.1007/s00441-016-2432-8
Ito, S., Yamaguchi, Y., Kubota, S., Yamamoto, Y., & Kimura, K. (2023). Immunohistochemical identification of epithelial cell types in the isthmus of bovine oviduct: Comparison with the ampulla. Journal of Reproduction and Development, 69(1), 18-24. https://doi.org/10.1262/jrd.2022-104
Ito, S., Yamamoto, Y., & Kimura, K. (2020). Analysis of ciliogenesis process in the bovine oviduct based on immunohistochemical classification. Molecular Biology Reports, 47(2), 1003-1012. https://doi.org/10.1007/s11033-019-05192-w
Kölle, S. (2022). Sperm-oviduct interactions: Key factors for sperm survival and maintenance of sperm fertilizing capacity. Andrology, 10(5), 837-843. https://doi.org/10.1111/andr.13179
Kölle, S., Dubielzig, S., Reese, S., Wehrend, A., König, 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. Biology of Reproduction, 81(2), 267-274. https://doi.org/10.1095/biolreprod.108.073874
Kölle, S., Hughes, B., & Steele, H. (2020). Early embryo-maternal communication in the oviduct: A review. Molecular Reproduction and Development, 87(6), 650-662. https://doi.org/10.1002/mrd.23352
Lüttgenau, J., Kögel, T., & Bollwein, H. (2016). Effects of GnRH or PGF2α in week 5 postpartum on the incidence of cystic ovarian follicles and persistent corpora lutea and on fertility parameters in dairy cows. Theriogenology, 85(5), 904-913. https://doi.org/10.1016/j.theriogenology.2015.10.040
Machado-Neves, M., Assis, W. A., Gomes, M. G., & Oliveira, C. A. (2019). Oviduct morphology and estrogen receptors ERα and ERβ expression in captive Chinchilla lanigera (Hystricomorpha: Chinchillidae. General and Comparative Endocrinology, 273(January), 32-39. https://doi.org/10.1016/j.ygcen.2018.03.023
McDaniel, J. W., Scalzi, H., & Black, D. L. (1968). Influence of ovarian hormones on histology and histochemistry of the bovine oviduct. Journal of Dairy Science, 51(5), 754-761. https://doi.org/10.3168/jds.S0022-0302(68)87067-5
Noakes, D. E., Parkinson, T. J., & England, G. C. W. (2001). Arthur's Veterinary Reproduction and Obstetrics (8th ed.). Elsevier.
Ortega, H., Díaz, P., Salvetti, N., Hein, G., Marelli, B., Rodríguez, F., Stassi, A., & Rey, F. (2016). Follicular cysts: A single sign and different diseases. A view from comparative medicine. Current Pharmaceutical Design, 22, 5634-5645. https://doi.org/10.2174/1381612822666160804
Owhor, L. E., Reese, S., & Kölle, S. (2019). Salpingitis impairs bovine tubal function and Sperm-Oviduct interaction. Scientific Reports, 9, 10893. https://doi.org/10.1038/s41598-019-47431-x
Özen, A., Ergün, E., & Kürüm, A. (2010). Histomorphology of the oviduct epithelium in the Angora rabbit. Turkish Journal of Veterinary Animal Science, 34(3), 219-226. https://doi.org/10.3906/vet-0710-39
Peter, A. (2004). An update on cystic ovarian degeneration in cattle. Reproduction in Domestic Animals, 39(1), 1-7. https://doi.org/10.1046/j.0936-6768.2003.00466.x
Peter, A. T., Bosu, W. T., & DeDecker, R. J. (1989). Suppression of preovulatory luteinizing hormone surges in heifers after intrauterine infusions of Escherichia coli endotoxin. American Journal of Veterinary Research, 50(3), 368-373.
Purba, F. Y., Suzuki, N., & Isobe, N. (2021). Association of endometritis and ovarian follicular cyst with mastitis in dairy cows. Journal of Veterinary Medical Science, 83(2), 338-343. https://doi.org/10.1292/jvms.20-0652
Roberts, J. F., & Huang, C.-C. J. (2022). Bovine models for human ovarian diseases. In Progress in Molecular Biology and Translational Science (pp. 101-154). Elsevier. https://doi.org/10.1016/bs.pmbts.2022.02.001
Scully, D. M., Campion, D., McCartney, F., Dulohery, K., Reese, S., & Kölle, S. (2021). Cystic ovary disease impairs transport speed, smooth muscle contraction, and epithelial ion transport in the bovine oviduct. Molecular Reproduction and Development, 88(8), 558-570. https://doi.org/10.1002/mrd.23521
Sheldon, I., Noakes, D., Rycroft, A., Pfeiffer, D., & Dobson, H. (2002). Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction, 123(6), 837-845.
Steffl, M., Schweiger, M., Sugiyama, T., & Amselgruber, W. M. (2008). Review of apoptotic and non-apoptotic events in non-ciliated cells of the mammalian oviduct. Annals of Anatomy - Anatomischer Anzeiger, 190(1), 46-52. https://doi.org/10.1016/j.aanat.2007.04.003
Suarez, S. S., & Pacey, A. A. (2006). Sperm transport in the female reproductive tract. Human Reproduction Update, 12(1), 23-37. https://doi.org/10.1093/humupd/dmi047
Suarez, S. S. (2008). Regulation of sperm storage and movement in the mammalian oviduct. The International Journal of Developmental Biology, 52(5-6), 455-462. https://doi.org/10.1387/ijdb.072527ss
Trottmann, M., Kölle, S., Leeb, R., Doering, D., Reese, S., Stief, C. G., Dulohery, K., Leavy, M., Kuznetsova, J., Homann, C., & Sroka, R. (2016). Ex vivo investigations on the potential of optical coherence tomography (OCT) as a diagnostic tool for reproductive medicine in a bovine model. Journal of Biophotonics, 9(1-2), 129-137. https://doi.org/10.1002/jbio.201500009
Turner, Z. B., Lima, F. S., Conley, A. J., McNabb, B. R., Rowe, J. D., Garzon, A., Urbano, T. M., Morris, C. M., & Pereira, R. V. (2023). Cystic ovarian disease in dairy cattle: Diagnostic accuracy when using B-mode and color Doppler ultrasound. Journal of Dairy Science, 106(5), 3411-3420. https://doi.org/10.3168/jds.2022-22498
Vanholder, T., Opsomer, G., & de Kruif, A. (2006). Aetiology and pathogenesis of cystic ovarian follicles in dairy cattle: A review. Reproduction, Nutrition, Development, 46, 105-119. https://doi.org/10.1051/rnd
Verhage, H. C., Abel, J. H., Tietz, W. J., & Barrau, M. D. (1973). Development and maintenance of the oviductal epithelium during the estrous cycle in the bitch. Biology of Reproduction, 9, 460-474. https://doi.org/10.1093/biolreprod/9.5.460
Williams, E. J., Fischer, D. P., Noakes, D. E., England, G. C. W., Rycroft, A., Dobson, H., & Sheldon, I. M. (2007). The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow. Theriogenology, 68(4), 549-559. https://doi.org/10.1016/j.theriogenology.2007.04.056