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Transcriptome profile and association study revealed STAT3 gene as a potential quality marker of bovine gametes

Published online by Cambridge University Press:  13 January 2020

Nasser Ghanem Open the ORCID record for Nasser Ghanem [Opens in a new window] ,
Dessie Salilew-Wondim ,
Michael Hoelker ,
Karl Schellander  and
Dawit Tesfaye Open the ORCID record for Dawit Tesfaye [Opens in a new window]
Nasser Ghanem
Affiliation:
Animal Production Department, Faculty of Agriculture, Cairo University, Giza, Egypt
Dessie Salilew-Wondim
Affiliation:
Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115Bonn, Germany
Michael Hoelker
Affiliation:
Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115Bonn, Germany
Karl Schellander
Affiliation:
Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115Bonn, Germany
Dawit Tesfaye*
Affiliation:
Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115Bonn, Germany Department of Biomedical Sciences, Animal Reproduction and Biotechnology Laboratory (ARBL), Colorado State University, Fort Collins, CO, USA
*
Author for correspondence: Dawit Tesfaye, Department of Biomedical Sciences, Animal Reproduction and Biotechnology Laboratory (ARBL), Colorado State University, 1351 Rampart Rd, Fort Collins, CO, USA. Tel: +1 970 491 891. E-mail: Dawit.Tesfaye@colostate.edu
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Summary

The present study was aimed to investigate differences in molecular signatures in oocytes derived from Holstein-Friesian heifers with different genetic merit for fertility, euthanized during day 0 or day 12 of the estrous cycle. Moreover, association between single nucleotide polymorphisms (SNPs) of ODC1 and STAT3 genes and bull fertility traits was investigated. The gene expression patterns were analyzed using cDNA array and validated with quantitative real-time polymerase chain reaction (PCR). The result revealed that several genes have shown not only to be regulated by fertility merit but also by the day of oocyte recovery during the estrous cycle. The STAT3 gene was found to be upregulated in oocytes recovered from animals with high fertility merit at both day 0 and day 12. Some other genes like PTTG1, ODC1 and TUBA1C were downregulated at day 0 and upregulated at day 12 in high, compared with low, fertility merit recovered oocytes. In contrast, the transcript abundance of TPM3 was upregulated at day 0 and downregulated at day 12 in high, compared with low, fertility merit recovered oocytes. In addition, ODC1 and STAT3 were found to be associated (P < 0.05) with sperm quality traits as well as flow cytometry parameters. Therefore, the expression of several candidate genes including ODC1 and STAT3 was related to the genetic merit of the cow. In addition polymorphisms in these two genes were found to be associated with bull semen quality.

Keywords

Developmental competenceGene expressionOocyteSperm
Type
Research Article
Information
Zygote , Volume 28 , Issue 2 , April 2020 , pp. 116 - 130
Copyright
© Cambridge University Press 2020

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References

Alcivar, AA, Hake, LE, Mali, P, Kaipia, A, Parvinen, M and Hecht, NB (1989) Developmental and differential expression of the ornithine decarboxylase gene in rodent testis. Biol Reprod 41, 1133–42.CrossRefGoogle ScholarPubMed
Aparicio, IM, Garcia-Herreros, M, O’Shea, LC, Hensey, C, Lonergan, P and Fair, T (2011) Expression, regulation and function of genomic and nongenomic progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol Reprod 84, 910–21.CrossRefGoogle ScholarPubMed
Bastida, MC, Tejada, F, Cremades, A and Peñafiel, R (2002) The preovulatory rise of murine ovarian ornithine decarboxylase is required for progesterone secretion by the corpus luteum. Biochem Biophys Res Commun 293, 106–11.CrossRefGoogle ScholarPubMed
Butler, WR, Calaman, JJ and Beam, SW (1996) Plasma and milk urea nitrogen in relation to pregnancy rate in lactating dairy cattle. J Anim Sci 74, 858–65.CrossRefGoogle ScholarPubMed
Carter, F, Forde, N, Duffy, P, Wade, M, Fair, T, Crowe, MA, Evans, AC, Kenny, DA, Roche, JF and Lonergan, P (2008) Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod Fertil Dev 20, 368–75.CrossRefGoogle ScholarPubMed
Coffino, P (2000) Polyamines in spermiogenesis: not now, darling. Proc Natl Acad Sci USA 97, 4421–23.CrossRefGoogle ScholarPubMed
Conneely, OM, Lydon, JP, DeMayo, F and O’Malley, BW (2000) Reproductive functions of the progesterone receptor. J Soc Gynecol Invest 7, 525–32.CrossRefGoogle ScholarPubMed
Cummins, JM (2001) Cytoplasmic inheritance and its implications for animal biotechnology. Theriogenology 55, 1381–99.CrossRefGoogle ScholarPubMed
Demetrio, DG, Santos, RM, Demetrio, CG and Vasconcelos, JL (2007) Factors affecting conception rates following artificial insemination or embryo transfer in lactating Holstein cows. J Dairy Sci 90, 5073–82.CrossRefGoogle ScholarPubMed
Duncan, SA, Zhong, Z, Wen, Z and Darnell, JE Jr (1997) STAT signaling is active during early mammalian development. Dev Dynam 208, 190–98.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Duranthon, V and Renard, JP (2003) Storage and functional recovery of molecules in oocytes. In Biology and Pathology of the Oocyte, Cambridge University Press, Cambridge, pp. 81–105.CrossRefGoogle Scholar
El-Sayed, A, Hoelker, M, Rings, F, Salilew, D, Jennen, D, Tholen, E, Sirard, MA, Schellander, K, Tesfaye, D (2006) Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiol Genomics 28, 84–96.CrossRefGoogle ScholarPubMed
Farin, PW, Piedrahita, JA and Farin, CE (2006) Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology 65, 178–91.CrossRefGoogle ScholarPubMed
Fathi, M, Ashry, M, Salama, A and Badr, MR (2017) Developmental competence of Dromedary camel (Camelus dromedarius) oocytes selected using brilliant cresyl blue staining. Zygote 25, 529–36.CrossRefGoogle ScholarPubMed
Feng, WG, Sui, HS, Han, ZB, Chang, ZL, Zhou, P, Liu, DJBao, S, Tan, JH (2007) Effects of follicular atresia and size on the developmental competence of bovine oocytes: a study using the well-in-drop culture system. Theriogenology 67, 1339–50.CrossRefGoogle ScholarPubMed
Fernandes, JRD, Jain, S and Banerjee, A (2017) Expression of ODC1, SPD, SPM and AZIN1 in the hypothalamus, ovary and uterus during rat estrous cycle. Gene Comp Endocrinol 246, 9–22.CrossRefGoogle ScholarPubMed
Feugang, JM, Kaya, A, Page, GP, Chen, L, Mehta, T, Hirani, KNazareth, L, Topper, E, Gibbs, R, Memili, E (2009) Two-stage genome-wide association study identifies integrin beta 5 as having potential role in bull fertility. BMC Genomics 24, 176.CrossRefGoogle Scholar
França, MR, da Silva, MIS, Pugliesi, G, Van Hoeck, V and Binelli, M (2017) Evidence of endometrial amino acid metabolism and transport modulation by peri-ovulatory endocrine profiles driving uterine receptivity. J Anim Sci Biotechnol 8, 54.CrossRefGoogle ScholarPubMed
Ghanem, N, Hölker, M, Rings, F, Jennen, D, Tholen, E, Sirard, MATorner, H, Kanitz, W, Schellander, K, Tesfaye, D (2007) Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave. BMC Dev Biol 27, 90.CrossRefGoogle Scholar
Govignon, A, Rohou, A, Ponsart, C, Delcroix, P and Humblot, P (2000) Sources of variation of embryo production after superovulation in Prim Holstein dairy cows. In 16eme R´eunion de la A.E.T.E. p. 158.Google Scholar
Green, MP, Hunter, MG and Mann, GE (2005) Relationships between maternal hormone secretion and embryo development on day 5 of pregnancy in dairy cows. Anim Reprod Sci 88, 179–89.CrossRefGoogle ScholarPubMed
Hakovirta, H, Keiski, A, Toppari, J, Halmekytö, M, Alhonen, L, Jänne, J and Parvinen, M (1993) Polyamines and regulation of spermatogenesis: selective stimulation of late spermatogonia in transgenic mice overexpressing the human ornithine decarboxylase gene. Mol Endocrinol 7, 1430–36.Google ScholarPubMed
Hedge, P, Qi, R, Abernathy, R, Gay, C, Dharap, S, Gaspard, R, Hughes, JE, Snesrud, E, Lee, N and Quackenbush, J (2000) A concise guide to cDNA microarray analysis. BioTechniques 29, 548–46.Google Scholar
Ivanov, IP, Rohrwasser, A, Terreros, DA, Gesteland, RF and Atkins, JF (2000) Discovery of a spermatogenesis stage-specific ornithine decarboxylase antizyme: antizyme 3. Proc Natl Acad Sci USA 97, 4808–13.CrossRefGoogle ScholarPubMed
Kaipia, A, Toppari, J, Mali, P, Kangasniemi, M, Alcivar, AA, Hecht, NBParvinen, M (1990) Stage- and cell-specific expression of the ornithine decarboxylase gene during rat and mouse spermatogenesis. Mol Cell Endocrinol 73, 45–52.CrossRefGoogle ScholarPubMed
Khatib, H, Monson, RL, Schutzkus, V, Kohl, DM, Rosa, GJ and Rutledge, JJ (2008) Mutations in the STAT5A gene are associated with embryonic survival and milk composition in cattle. J Dairy Sci 91, 784–93.CrossRefGoogle ScholarPubMed
Khatib, H, Huang, W, Mikheil, D, Schutzkus, V and Monson, RL (2009a) Effects of signal transducer and activator of transcription (STAT) genes STAT1 and STAT3 genotypic combinations on fertilization and embryonic survival rates in Holstein cattle. J Dairy Sci 92, 6186–91.CrossRefGoogle ScholarPubMed
Khatib, H, Maltecca, C, Monson, RL, Schutzkus, V and Rutledge, JJ (2009b) Monoallelic maternal expression of STAT5A affects embryonic survival in cattle. BMC Genetics 10, 13.CrossRefGoogle ScholarPubMed
Khatib, H, Monson, RL, Huang, W, Khatib, R, Schutzkus, V, Khateeb, H and Parrish, JJ (2010) Short communication: Validation of in vitro fertility genes in a Holstein bull population. J Dairy Sci 93, 2244–49.CrossRefGoogle Scholar
Kommadath, A, Mulder, HA, de Wit, AA, Woelders, H, Smits, MA, Beerda, B, Veerkamp, RF, Frijters, AC and Te Pas, MF (2010) Gene expression patterns in anterior pituitary associated with quantitative measure of oestrous behaviour in dairy cows. Animal 4, 1297–307.CrossRefGoogle ScholarPubMed
Krisher, RL (2004) The effect of oocyte quality on development. J Anim Sci 82, E-Suppl14–23.Google ScholarPubMed
Lachance, C, Goupil, S, Leclerc, P and Stattic, V (2013) A STAT3 inhibitor, affects human spermatozoa through regulation of mitochondrial activity. J Cell Physiol 228, 704–13.CrossRefGoogle ScholarPubMed
Larsson, B and Rodríguez-Martínez, H (2000) Can we use in vitro fertilization tests to predict semen fertility? Anim Reprod Sci 60–61, 327–36.CrossRefGoogle ScholarPubMed
Leibfried-Rutledge, ML (1999) Factors determining competence of in vitro produced cattle embryos. Theriogenology 51, 473–85.CrossRefGoogle ScholarPubMed
Lonergan, P and Fair, T (2008) In vitro-produced bovine embryos – dealing with the warts. Theriogenology 69, 17–22.CrossRefGoogle ScholarPubMed
Lucy, MC (2007) Fertility in high-producing dairy cows: reasons for decline and corrective strategies for sustainable improvement. Soc Reprod Fertil Suppl 64, 237–54.Google ScholarPubMed
Lydon, JP, DeMayo, FJ, Funk, CR, Mani, SKHughes, ARMontgomery, CA Jr, Shyamala, G, Conneely, OM, and O’Malley, BW (1995) Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9, 2266–78.CrossRefGoogle ScholarPubMed
Mamo, E, Sargent, CA, Affara, NA, Tesfaye, D, El-Halawany, N, Wimmers, K, Gilles, M, Schellander, K and Ponsuksili, S (2006) Transcripts profiles of some developmentally important genes detected in bovine oocytes and in vitro-produced blastocysts using RNA amplification and cDNA microarrays. Reprod Domest Anim 41, 527–34CrossRefGoogle ScholarPubMed
Mann, GE, Mann, SJ, Blache, D and Webb, R (2005) Metabolic variables and plasma leptin concentrations in dairy cows exhibiting reproductive cycle abnormalities identified through milk progesterone monitoring during the post partum period Anim Reprod Sci 88, 191–202.CrossRefGoogle ScholarPubMed
McMillan, WH and Donnison, MJ (1999) Understanding maternal contributions to fertility in recipient cattle: development of herds with contrasting pregnancy rates Anim Reprod Sci 57, 127–40.CrossRefGoogle ScholarPubMed
McNeill, RE, Diskin, MG, Sreenan, JM and Morris, DG (2006) Associations between milk progesterone concentration on different days and with embryo survival during the early luteal phase in dairy cows. Theriogenology 65, 1435–41.CrossRefGoogle ScholarPubMed
Misirlioglu, M, Page, GP, Sagirkaya, H, Kaya, A, Parrish, JJ, First, NL and Memili, E (2006) Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proc Natl Acad Sci USA 103, 18905–910.CrossRefGoogle ScholarPubMed
Mohammadi-Sangcheshmeh, A, Held, E, Ghanem, N, Rings, F, Salilew-Wondim, D, Tesfaye, D, Sieme, H, Schellander, K and Hoelker, M (2011) G6PDH-activity in equine oocytes correlates with morphology, expression of candidate genes for viability, and preimplantative in vitro development. Theriogenology 76, 1215–26.CrossRefGoogle ScholarPubMed
Moore, K and Thatcher, WW (2006) Major advances associated with reproduction in dairy cattle. J Dairy Sci 89, 1254–66.CrossRefGoogle ScholarPubMed
Mota, RR, Guimarães, SEF, Fortes, MRSHayes, B, Silva, FF, Verardo, LLKelly, MJ, de Campos, CF, Guimarães, JD, Wenceslau, RRPenitente-Filho, JM, Garcia, JF and Moore, S (2017) Genome-wide association study and annotating candidate gene networks affecting age at first calving in Nellore cattle. J Anim Breed Genetics 134, 484–92.CrossRefGoogle ScholarPubMed
NRS (2009) The Royal Dutch Cattle Syndicate (NRS) Handbook. Available at: https://www.cr-delta.nl/nl/fokwaarden/pdf/E17.pdf.Google Scholar
Pendeville, H, Carpino, N, Marine, JC, Takahashi, Y, Muller, M, Martial, JA and Cleveland, JL (2001) The ornithine decarboxylase gene is essential for cell survival during early murine development. Mol Cell Biol 21, 6549–58.CrossRefGoogle ScholarPubMed
Picton, HM (2001) Activation of follicle development: the primordial follicle. Theriogenology 55, 1193–210.CrossRefGoogle ScholarPubMed
Rizos, D, Ward, F, Duffy, P, Boland, MP and Lonergan, P (2002) 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, 234–48.CrossRefGoogle ScholarPubMed
Robker, RL, Watson, LN, Robertson, SA, Dunning, KR, McLaughlin, EA and Russell, DL (2014) Identification of sites of STAT3 action in the female reproductive tract through conditional gene deletion. PLoS One 9, e101182.CrossRefGoogle ScholarPubMed
Rosenkrans, CF Jr and First, NL (1994) Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro. J Anim Sci 72, 434–37.CrossRefGoogle ScholarPubMed
Sadeesh, EM, Fozia, S, and Meena, K (2017) Combined positive effect of oocyte extracts and brilliant cresyl blue stained recipient cytoplasts on epigenetic reprogramming and gene expression in buffalo nuclear transfer embryos. Cytotechnology 69, 289–305.CrossRefGoogle ScholarPubMed
Salilew-Wondim, D, Hölker, MRings, F, Ghanem, N, Ulas-Cinar, M, Peippo, J, Tholen, E, Looft, C, Schellander, K and Tesfaye, D (2010) Bovine pretransfer endometrium and embryo transcriptome fingerprints as predictors of pregnancy success after embryo transfer. Physiol Genomics 42, 201–18.CrossRefGoogle ScholarPubMed
Sartori, R, Gümen, A, Guenther, JN, Souza, AH, Caraviello, DZ and Wiltbank, MC (2006) Comparison of artificial insemination versus embryo transfer in lactating dairy cows. Theriogenology 65, 1311–21.CrossRefGoogle ScholarPubMed
Sirard, MA, Dufort, I, Vallee, M, Massicotte, L, Gravel, C, Reghenas, H, Watson, AJ, King, WA and Robert, C (2005) Potential and limitations of bovine-specific arrays for the analysis of mRNA levels in early development: preliminary analysis using a bovine embryonic array. Reprod Fertil Dev 17, 47–57.CrossRefGoogle ScholarPubMed
Snijders, SEM, Dillon, P, O’Callaghan, D and Boland, MP (2000) Effect of genetic merit, milk yield, body condition and lactation number on in vitro oocyte development in dairy cows. Theriogenology, 53, 981–89.CrossRefGoogle ScholarPubMed
Spencer, TE, Forde, N and Lonergan, P (2016) The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants. J Dairy Sci 99, 5941–50.CrossRefGoogle ScholarPubMed
Stronge, AJ, Sreenan, JM, Diskin, MG, Mee, JF, Kenny, DA and Morris, DG (2005) Post-insemination milk progesterone concentration and embryo survival in dairy cows. Theriogenology 64, 1212–24.CrossRefGoogle ScholarPubMed
Takeda, K, Noguchi, K, Shi, W, Tanaka, T, Matsumoto, M, Yoshida, N, Kishimoto, T and Akira, S (1997) Targeted disruption of the mouse Stat3 gene leads to embryonic lethality. Proc Natl Acad Sci USA 94, 3801–04.CrossRefGoogle ScholarPubMed
Tamassia, M, Heyman, Y, Lavergne, Y, Richard, C, Gelin, V, Renard, JP and Chastant-Maillard, S (2003) Evidence of oocyte donor cow effect over oocyte production and embryo development in vitro. Reproduction 126, 629–37.CrossRefGoogle ScholarPubMed
Teglund, S, McKay, C, Schuetz, E, van Deursen, JM, Stravopodis, D, Wang, D, Brown, M, Bodner, S, Grosveld, G, Ihle, JN (1998) Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93, 841–50.CrossRefGoogle ScholarPubMed
Torner, H, Ghanem, N, Ambros, C, Hölker, M, Tomek, W, Phatsara, C, Alm, H, Sirard, MA, Kanitz, W, Schellander, K and Tesfaye, D (2008) Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. Reproduction 135, 197–212.CrossRefGoogle ScholarPubMed
Truchet, S, Chebrout, M, Djediat, C, Wietzerbin, J and Debey, P (2004) Presence of permanently activated signal transducers and activators of transcription in nuclear interchromatin granules of unstimulated mouse oocytes and preimplantation embryos. Biol Reprod 71, 1330–39.CrossRefGoogle ScholarPubMed
Tscherner, A, Brown, AC, Stalker, L, Kao, J, Dufort, I, Sirard, MA, LaMarre, J (2018) STAT3 signalling stimulates miR-21 expression in bovine cumulus cells during in vitro oocyte maturation. Sci Rep 8, 11527.CrossRefGoogle Scholar
Van Eerdenburg, FJCM (2006) Estrus detection in dairy cattle: How to beat the bull. Vlaams Diergeneeskundig Tijdschrift 75, 61–69.Google Scholar
Watson, AJ, Westhusin, ME, De Sousa, PA, Betts, DH and Barcroft, LC (1999) Gene expression regulating blastocyst formation. Theriogenology 51, 117–33.CrossRefGoogle ScholarPubMed
Yang, XY, Zhao, JG, Li, H, Liu, HF, Huang, Y, Huang, SZZeng, F and Zeng, YT (2008) Effect of individual heifer oocyte donors on cloned embryo development in vitro. Anim Reprod Sci 104, 28–37.CrossRefGoogle ScholarPubMed
Zhao, YC, Chi, YJ, Yu, YS, Liu, JL, Su, RW, Ma, XH, Shan, CH and Yang, ZM (2008) Polyamines are essential in embryo implantation: expression and function of polyamine-related genes in mouse uterus during peri-implantation period. Endocrinology 149, 2325–32.CrossRefGoogle ScholarPubMed