Sperm-oviduct interaction: Differential gene expression of growth factors induced by sperm DNA fragmentation.


Journal

Andrologia
ISSN: 1439-0272
Titre abrégé: Andrologia
Pays: Germany
ID NLM: 0423506

Informations de publication

Date de publication:
Jun 2022
Historique:
revised: 27 12 2021
received: 15 10 2021
accepted: 11 01 2022
pubmed: 12 3 2022
medline: 21 5 2022
entrez: 11 3 2022
Statut: ppublish

Résumé

The present study investigated the effects of DNA fragmentation of spermatozoa on the growth factors expression by a human oviduct epithelial cell line (OE-E6/E7). Two separate groups were examined in this study. The cell line was cultured in the presence of spermatozoa with normal DNA fragmentation index (DFI) or abnormal DFI. Total RNA from the cell line in each group was isolated, and relative expression of objective genes was analysed using PCR array. Also, the concentration of VEGF, BMP-2, BMP-7 and MSTN in the supernatant of cell culture was analysed by the ELISA method. The PCR array analysis revealed that most of the growth factors had been upregulated in the abnormal group. However, the differences between groups were statistically significant (p < 0.05) for five genes, including VEGF-A, BMP-2, BMP-6, BMP-7 and OSM. Furthermore, MSTN was the only gene that down-regulated significantly under the influence of the spermatozoa with abnormal DFI. Moreover, the results of ELISA analysis were in agreement with the data of the PCR array. It has been concluded that DNA fragmentation in human spermatozoa can probably change regular events throughout the oviducts. Consequently, the genes of interest may change sperm function and probably its fate in the female reproductive tract.

Identifiants

pubmed: 35274330
doi: 10.1111/and.14378
doi:

Substances chimiques

Bone Morphogenetic Protein 7 0
Intercellular Signaling Peptides and Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14378

Subventions

Organisme : Royan Institute for Reproductive Biomedicine

Informations de copyright

© 2022 Wiley-VCH GmbH.

Références

Ajdary, M., Ashrafi, M., Aflatoonian, R., & Mehdizadeh, M. (2021). The role of sperm in inducing genomic changes in the implantation: An experimental study. Andrologia, 53(7), e14077. https://doi.org/10.1111/and.14077
Ajdary, M., Keyhanfar, F., Aflatoonian, R., Amani, A., Amjadi, F., Zandieh, Z., & Mehdizadeh, M. (2020). Design and evaluation of a novel nanodrug delivery system for reducing the side effects of clomiphene citrate on endometrium. DARU Journal of Pharmaceutical Sciences, 28, 423-432. https://doi.org/10.1007/s40199-019-00310-2
Barratt, C. L. R., & Cooke, I. D. (1991). Review sperm transport in the human female reproductive tract-A dynamic interaction. International Journal of Andrology, 14(6), 394-411. https://doi.org/10.1111/j.1365-2605.1991.tb01268.x
Bisht, S., Faiq, M., Tolahunase, M., & Dada, R. (2017). Oxidative stress and male infertility. Nature Reviews Urology, 14(8), 470-485. https://doi.org/10.1038/nrurol.2017.69
Bongso, A., Ho, J., Fong, C.-Y., Ng, S.-C., & Ratnam, S. (1993). Human sperm function after coculture with human fallopian tubal epithelial cell monolayers: in vitro model for studying cell interactions in early human conception. Archives of Andrology, 31(3), 183-190. https://doi.org/10.3109/01485019308988398
Chang, H.-M., Fang, L., Cheng, J.-C., Klausen, C., Sun, Y.-P., & Leung, P. C. K. (2015). Growth differentiation factor 8 down-regulates pentraxin 3 in human granulosa cells. Molecular and Cellular Endocrinology, 404, 82-90. https://doi.org/10.1016/j.mce.2015.01.036
D’Cruz, O. J., Vassilev, A. O., & Uckun, F. M. (2001). Members of the Janus kinase/signal transducers and activators of transcription (JAK/STAT) pathway are present and active in human sperm. Fertility and Sterility, 76(2), 258-266. https://doi.org/10.1016/S0015-0282(01)01896-9
Ellington, J. E., Evenson, D. P., Fleming, J. E., Brisbois, R. S., Hiss, G. A., Broder, S. J., & Wright, R. W. Jr (1998). Coculture of human sperm with bovine oviduct epithelial cells decreases sperm chromatin structural changes seen during culture in media alone. Fertility and Sterility, 69(4), 643-649. https://doi.org/10.1016/S0015-0282(98)00023-5
Evans, J. P., & Florman, H. M. (2002). The state of the union: the cell biology of fertilization. Nature Medicine, 8(10), S57-S63. https://doi.org/10.1038/nm-fertilityS57
France, J. T., Graham, F. M., Gosling, L., Hair, P., & Knox, B. S. (1992). Characteristics of natural conceptual cycles occurring in a prospective study of sex preselection: Fertility awareness symptoms, hormone levels, sperm survival, and pregnancy outcome. International Journal of Fertility, 37(4), 244-255.
Fu, T., Zheng, H., Zhang, H., Chen, Z., Li, B., & Yang, Z. (2019). Oncostatin M expression in the mouse uterus during early pregnancy promotes embryo implantation and decidualization. FEBS Letters, 593(15), 2040-2050. https://doi.org/10.1002/1873-3468.13468
García, E. V., Hamdi, M., Barrera, A. D., Sánchez-Calabuig, M. J., Gutiérrez-Adán, A., & Rizos, D. (2017). Bovine embryo-oviduct interaction in vitro reveals an early cross talk mediated by BMP signaling. Reproduction, 153(5), 631-643. https://doi.org/10.1530/REP-16-0654
García, E. V., Miceli, D. C., Rizo, G., Valdecantos, P. A., & Barrera, A. D. (2015). Effect of early addition of bone morphogenetic protein 5 (BMP5) to embryo culture medium on in vitro development and expression of developmentally important genes in bovine preimplantation embryos. Theriogenology, 84(4), 589-599.
Georgiou, A. S., Snijders, A. P. L., Sostaric, E., Aflatoonian, R., Vazquez, J. L., Vazquez, J. M., Roca, J., Martinez, E. A., Wright, P. C., & Fazeli, A. (2007). Modulation of the oviductal environment by gametes. Journal of Proteome Research, 6(12), 4656-4666. https://doi.org/10.1021/pr070349m
Georgiou, A. S., Sostaric, E., Wong, C. H., Snijders, A. P. L., Wright, P. C., Moore, H. D., & Fazeli, A. (2005). Gametes alter the oviductal secretory proteome. Molecular & Cellular Proteomics, 4(11), 1785-1796. https://doi.org/10.1074/mcp.M500119-MCP200
Guo, J., & Wu, G. (2012). The signaling and functions of heterodimeric bone morphogenetic proteins. Cytokine & Growth Factor Reviews, 23(1-2), 61-67. https://doi.org/10.1016/j.cytogfr.2012.02.001
Hassanen, E., Elqusi, K., Zaki, H., Henkel, R., & Agarwal, A. (2019). TUNEL assay: Establishing a sperm DNA fragmentation cut-off value for Egyptian infertile men. Andrologia, 51(10), e13375. https://doi.org/10.1111/and.13375
Holt, W. V., & Fazeli, A. (2015). Do sperm possess a molecular passport? Mechanistic insights into sperm selection in the female reproductive tract. MHR: Basic Science of Reproductive Medicine, 21(6), 491-501. https://doi.org/10.1093/molehr/gav012
Holt, W. V., & Fazeli, A. (2016). Sperm selection in the female mammalian reproductive tract. Focus on the oviduct: hypotheses, mechanisms, and new opportunities. Theriogenology, 85(1), 105-112.
Holt, W. V., & Fazeli, A. (2016). Sperm storage in the female reproductive tract. Annual Review of Animal Biosciences, 4, 291-310. https://doi.org/10.1146/annurev-animal-021815-111350
Hourcade, J. D., Pérez-Crespo, M., Fernández-González, R., Pintado, B., & Gutiérrez-Adán, A. (2010). Selection against spermatozoa with fragmented DNA after postovulatory mating depends on the type of damage. Reproductive Biology and Endocrinology, 8(1), 1-11. https://doi.org/10.1186/1477-7827-8-9
Huminiecki, L., Chan, H. Y., Lui, S., Poulsom, R., Stamp, G., Harris, A. L., & Bicknell, R. (2001). Vascular endothelial growth factor transgenic mice exhibit reduced male fertility and placental rejection. Molecular Human Reproduction, 7(3), 255-264. https://doi.org/10.1093/molehr/7.3.255
Jiwakanon, J., Persson, E., Berg, M., & Dalin, A.-M. (2011). Influence of seminal plasma, spermatozoa and semen extender on cytokine expression in the porcine endometrium after insemination. Animal Reproduction Science, 123(3), 210-220. https://doi.org/10.1016/j.anireprosci.2010.11.016
Kervancioglu, M. E., Djahanbakhch, O., & Aitken, R. J. (1994). Epithelial cell coculture and the induction of sperm capacitation. Fertility and Sterility, 61(6), 1103-1108. https://doi.org/10.1016/S0015-0282(16)56764-8
Kervancioglu, M. E., Saridogan, E., Aitken, R. J., & Djahanbakhch, O. (2000). Importance of sperm-to-epithelial cell contact for the capacitation of human spermatozoa in fallopian tube epithelial cell cocultures. Fertility and Sterility, 74(4), 780-784. https://doi.org/10.1016/S0015-0282(00)01514-4
Lam, P. M., Briton-Jones, C., Cheung, C. K., Lok, I. H., Yuen, P. M., Cheung, L. P., & Haines, C. (2003). Vascular endothelial growth factor in the human oviduct: Localization and regulation of messenger RNA expression in vivo. Biology of Reproduction, 68(5), 1870-1876. https://doi.org/10.1095/biolreprod.102.012674
Lee, T.-C., & Ho, H.-C. (2011). Effects of prostaglandin E2 and vascular endothelial growth factor on sperm might lead to endometriosis-associated infertility. Fertility and Sterility, 95(1), 360-362. https://doi.org/10.1016/j.fertnstert.2010.08.040
Mahmoud, A. I., & Parrish, J. J. (1996). Oviduct fluid and heparin induce similar surface changes in bovine sperm during capacitation: a flow cytometric study using lectins. Molecular Reproduction and Development: Incorporating Gamete Research, 43(4), 554-560. https://doi.org/10.1002/(SICI)1098-2795(199604)43:4<554:AID-MRD19>3.0.CO;2-Z
Manceau, M., Gros, J., Savage, K., Thomé, V., McPherron, A., Paterson, B., & Marcelle, C. (2008). Myostatin promotes the terminal differentiation of embryonic muscle progenitors. Genes & Development, 22(5), 668-681. https://doi.org/10.1101/gad.454408
Mondéjar, I., Acuna, O. S., Izquierdo-Rico, M. J., Coy, P., & Avilés, M. (2012). The oviduct: functional genomic and proteomic approach. Reproduction in Domestic Animals, 47, 22-29. https://doi.org/10.1111/j.1439-0531.2012.02027.x
Morales, P., Palma, V., Salgado, M., & Villalón, M. (1996). Fertilization and early embryology: Sperm interaction with human oviductal cells in vitro. Human Reproduction, 11(7), 1504-1509. https://doi.org/10.1093/oxfordjournals.humrep.a019426
Mousavi, S. O., Mohammadi, R., Amjadi, F., Zandieh, Z., Aghajanpour, S., Aflatoonian, K., Sabbaghian, M., Eslami, M., Madani, T., & Aflatoonian, R. (2021). Immunological response of fallopian tube epithelial cells to spermatozoa through modulating cytokines and chemokines. Journal of Reproductive Immunology, 146, 103327. https://doi.org/10.1016/j.jri.2021.103327
Obermair, A., Obruca, A., Pöhl, M., Kaider, A., Vales, A., Leodolter, S., Wojta, J., & Feichtinger, W. (1999). Vascular endothelial growth factor and its receptors in male fertility. Fertility and Sterility, 72(2), 269-275. https://doi.org/10.1016/S0015-0282(99)00234-4
Organization, W. H. and Others (2010). WHO laboratory manual for the examination and processing of human semen.
Pastuschek, J., Poetzsch, J., Morales-Prieto, D. M., Schleußner, E., Markert, U. R., & Georgiev, G. (2015). Stimulation of the JAK/STAT pathway by LIF and OSM in the human granulosa cell line COV434. Journal of Reproductive Immunology, 108, 48-55. https://doi.org/10.1016/j.jri.2015.03.002
Pérez-Cerezales, S., Ramos-Ibeas, P., Acuña, O. S., Avilés, M., Coy, P., Rizos, D., & Gutiérrez-Adán, A. (2018). The oviduct: From sperm selection to the epigenetic landscape of the embryo. Biology of Reproduction, 98(3), 262-276. https://doi.org/10.1093/biolre/iox173
Rex, A. S., Aagaard, J., & Fedder, J. (2017). DNA fragmentation in spermatozoa: a historical review. Andrology, 5(4), 622-630. https://doi.org/10.1111/andr.12381
Rickard, J. P., & de Graaf, S. P. (2020). Sperm surface changes and their consequences for sperm transit through the female reproductive tract. Theriogenology, 150, 96-105. https://doi.org/10.1016/j.theriogenology.2020.02.018
Robertson, S. A., Sharkey, D. J., & Bromfield, J. J. (2007). Seminal plasma and male factor signalling in the female reproductive tract: Is 19. American Journal of Reproductive Immunology, 58(3), 188-189.
Shimasaki, S., Moore, R. K., Otsuka, F., & Erickson, G. F. (2004). The bone morphogenetic protein system in mammalian reproduction. Endocrine Reviews, 25(1), 72-101. https://doi.org/10.1210/er.2003-0007
Suarez, S. S. (2016). Mammalian sperm interactions with the female reproductive tract. Cell and Tissue Research, 363(1), 185-194. https://doi.org/10.1007/s00441-015-2244-2
Vilanova, L. T., Rauch, M. C., Mansilla, A., Zambrano, A., Brito, M., Werner, E., Alfaro, Vı́ctor, Cox, J. F., & Concha, I. I. (2003). Expression of granulocyte-macrophage colony stimulating factor (GM-CSF) in male germ cells: GM-CSF enhances sperm motility. Theriogenology, 60(6), 1083-1095. https://doi.org/10.1016/S0093-691X(03)00106-7
Wahl, A. F., & Wallace, P. M. (2001). Oncostatin M in the anti-inflammatory response. Annals of the Rheumatic Diseases, 60(suppl 3), iii75-iii80.
Xie, J., Zhu, H., Chang, H.-M., Klausen, C., Dong, M., & Leung, P. C. K. (2020). GDF8 promotes the cell invasiveness in human trophoblasts by upregulating the expression of follistatin-like 3 through the ALK5-SMAD2/3 signaling pathway. Frontiers in Cell and Developmental Biology, 8, 1152. https://doi.org/10.3389/fcell.2020.573781
Yao, Y., Ho, P., & Yeung, W. S. (1999). Effects of human oviductal cell coculture on various functional parameters of human spermatozoa. Fertility and Sterility, 71(2), 232-239. https://doi.org/10.1016/S0015-0282(98)00430-0
Yousef, M. S., Marey, M. A., Hambruch, N., Hayakawa, H., Shimizu, T., Hussien, H. A., Abdel-Razek, A.-R., Pfarrer, C., & Miyamoto, A. (2016). Sperm binding to oviduct epithelial cells enhances TGFB1 and IL10 expressions in epithelial cells as well as neutrophils in vitro: prostaglandin E2 as a main regulator of anti-inflammatory response in the bovine oviduct. PLoS One, 11(9), e0162309. https://doi.org/10.1371/journal.pone.0162309
Zandieh, Z., Ashrafi, M., Aflatoonian, K., & Aflatoonian, R. (2019). Human sperm DNA damage has an effect on immunological interaction between spermatozoa and fallopian tube. Andrology, 7(2), 228-234. https://doi.org/10.1111/andr.12574
Zandieh, Z., Ashrafi, M., Jameie, B., Amanpour, S., Mosaffa, N., Salman Yazdi, R., Pacey, A., & Aflatoonian, R. (2015). Evaluation of immunological interaction between spermatozoa and fallopian tube epithelial cells. Andrologia, 47(10), 1120-1130. https://doi.org/10.1111/and.12391
Ziskind, G., Paltieli, Y., Eibschitz, I., Ohel, G., & Weichselbaum, A. (2000). Andrology: The effect of human fallopian tube epithelium on human sperm velocity motility and binding. Journal of Assisted Reproduction and Genetics, 17(3), 147-150.

Auteurs

Roudabeh Mohammadi (R)

Department of Endocrinology and Female Infertility, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran.

Seyed Omidreza Mousavi (SO)

Department of Endocrinology and Female Infertility, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran.

Nadia Sheibak (N)

Department of Anatomical Science, School of Medicine, Iran University of Medical Sciences, Tehran, Iran.

Fatemehsadat Amjadi (F)

Shahid Akbarabadi Clinical Research Development Unit (ShACRDU), Iran University of Medical Science, Tehran, Iran.

Zahra Zandieh (Z)

Shahid Akbarabadi Clinical Research Development Unit (ShACRDU), Iran University of Medical Science, Tehran, Iran.

Samaneh Aghajanpour (S)

Department of Endocrinology and Female Infertility, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran.
Department of Anatomical Science, School of Medicine, Iran University of Medical Sciences, Tehran, Iran.

Khashayar Aflatoonian (K)

School of Medicine, Iran University of Medical Sciences, Tehran, Iran.

Marjan Sabbaghian (M)

Department of Andrology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran.

Maryam Eslami (M)

Applied Biotechnology Research Center, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran.

Reza Aflatoonian (R)

Department of Endocrinology and Female Infertility, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH