Interferon-Stimulated Gene Expression in Peripheral Blood Leucocytes as a Convenient Prediction Marker for Embryo Status in Embryo-Transferred Japanese Black Cows during the Peri-Implantation Period
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Sample Collection, RNA Extraction, and Real-Time Quantitative Polymerase Chain Reaction (RT-qPCR)
2.3. Estimation of Threshold Values
2.4. Statistical Analysis
3. Results
3.1. Classical ISG Expression in ET Cattle and ROC Curve Analysis
3.2. Prediction of Gestational Statuses during the Peri-Implantation Period in ET Cattle
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Martal, J.; Chêne, N.; Camous, S.; Huynh, L.; Lantier, F.; Hermier, P.; L’Haridon, R.; Charpigny, G.; Charlier, M.; Chaouat, G. Recent developments and potentialities for reducing embryo mortality in ruminants: The role of IFN-τ and other cytokines in early pregnancy. Reprod. Fertil. Dev. 1997, 9, 355–380. [Google Scholar] [CrossRef] [PubMed]
- Roberts, R.M. Conceptus inferteons and maternal recognition of pregnancy. Biol. Reprod. 1989, 40, 449–452. [Google Scholar] [CrossRef] [PubMed]
- Hansen, T.R.; Sinedino, L.D.P.; Spencer, T.E. Paracrine and endocrine actions of interferon tau (IFNT). Reproduction 2017, 154, F45–F59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shirasuna, K.; Matsumoto, H.; Matsuyama, S.; Kimura, K.; Bollwein, H.; Miyamoto, A. Possible role of interferon tau on the bovine corpus luteum and neutrophils during the early pregnancy. Reproduction 2015, 150, 217–225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wijma, R.; Stangaferro, M.L.; Kamat, M.M.; Vasudevan, S.; Ott, T.L.; Giordano, J.O. Embryo mortality around the period of maintenance of the corpus luteum causes alterations to the ovarian function of lactating dairy cows. Biol. Reprod. 2016, 95, 112. [Google Scholar] [CrossRef]
- Ruhmann, B.; Giller, K.; Hankele, A.K.; Ulbrich, S.E.; Schmicke, M. Interferon-τ induced gene expression in bovine hepatocytes during early pregnancy. Theriogenology 2017, 104, 198–204. [Google Scholar] [CrossRef]
- Alhussien, M.N.; Kamboj, A.; Aljader, M.A.; Panda, B.S.K.; Yadav, M.L.; Sharma, L.; Mohammed, S.; Sheikh, A.A.; Lotfan, M.; Kapila, R.; et al. Effect of tropical thermal stress on peri-implantation immune responses in cows. Theriogenology 2018, 114, 149–158. [Google Scholar] [CrossRef]
- Forde, N.; Bazer, F.W.; Spencer, T.E.; Lonergan, P. ‘Conceptualizing’ the endometrium: Identification of conceptus-derived proteins during early pregnancy in cattle1. Biol. Reprod. 2015, 92, 156. [Google Scholar] [CrossRef]
- Bazer, F.W.; Thatcher, W.W. Chronicling the discovery of interferon tau. Reproduction 2017, 154, F11–F20. [Google Scholar] [CrossRef] [Green Version]
- Au-Yeung, N.; Horvath, C.M. Transcriptional and chromatin regulation in interferon and innate antiviral gene expression. Cytokine Growth Factor Rev. 2018, 44, 11–17. [Google Scholar] [CrossRef]
- Williams, B.R.G.; Williams, B.R.G. Transcriptional regulation of interferon-stimulated genes. Eur. J. Biochem. 1991, 200, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Schoggins, J.W. Interferon-stimulated genes: What do they all do? Annu. Rev. Virol. 2019, 6, 567–584. [Google Scholar] [CrossRef]
- Fricke, P.M.; Ricci, A.; Giordano, J.O.; Carvalho, P.D. Methods for and implementation of pregnancy diagnosis in dairy cows. Vet. Clin. North Am.-Food Anim. Pract. 2016, 32, 165–180. [Google Scholar] [CrossRef] [PubMed]
- Stevenson, J.S.; Britt, J.H. A 100-year review: Practical female reproductive management. J. Dairy Sci. 2017, 100, 10292–10313. [Google Scholar] [CrossRef] [PubMed]
- Ott, T.L. Symposium review: Immunological detection of the bovine conceptus during early pregnancy. J. Dairy Sci. 2019, 102, 3766–3777. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Senger, P.L. The estrus detection problem: New concepts, technologies, and possibilities. J. Dairy Sci. 1994, 77, 2745–2753. [Google Scholar] [CrossRef]
- Quintela, L.A.; Barrio, M.; Peña, A.I.; Becerra, J.J.; Cainzos, J.; Herradón, P.G.; Díaz, C. Use of ultrasound in the reproductive management of dairy cattle. Reprod. Domest. Anim. 2012, 47, 34–44. [Google Scholar] [CrossRef]
- Filho, R.V.O.; Franco, G.A.; Reese, S.T.; Dantas, F.G.; Fontes, P.L.P.; Cooke, R.F.; Rhinehart, J.D.; Thompson, K.W.; Pohler, K.G. Using pregnancy associated glycoproteins (PAG) for pregnancy detection at day 24 of gestation in beef cattle. Theriogenology 2020, 141, 128–133. [Google Scholar] [CrossRef]
- Hansen, P.J. The incompletely fulfilled promise of embryo transfer in cattle—Why aren’t pregnancy rates greater and what can we do about it? J. Anim. Sci. 2020, 98, skaa288. [Google Scholar] [CrossRef]
- Gifford, C.; Racicot, K.; Clark, D.S.; Austin, K.J.; Hansen, T.R.; Lucy, M.C.; Davies, C.J.; Ott, T.L. Regulation of interferon-stimulated genes in peripheral blood leukocytes in pregnant and bred, nonpregnant dairy cows. J. Dairy Sci. 2007, 90, 274–280. [Google Scholar] [CrossRef]
- Green, J.C.; Okamura, C.S.; Poock, S.E.; Lucy, M.C. Measurement of interferon-tau (IFN-τ) stimulated gene expression in blood leukocytes for pregnancy diagnosis within 18-20d after insemination in dairy cattle. Anim. Reprod. Sci. 2010, 121, 24–33. [Google Scholar] [CrossRef] [PubMed]
- Kizaki, K.; Shichijo-Kizaki, A.; Furusawa, T.; Takahashi, T.; Hosoe, M.; Hashizume, K. Differential neutrophil gene expression in early bovine pregnancy. Reprod. Biol. Endocrinol. 2013, 11, 6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stevenson, J.L.; Dalton, J.C.; Ott, T.L.; Racicot, K.E.; Chebel, R.C. Correlation between reproductive status and steady-state messenger ribonucleic acid levels of the myxovirus resistance gene, MX2, in peripheral blood leukocytes of dairy heifers. J. Anim. Sci. 2007, 85, 2163–2172. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Toji, N.; Shigeno, S.; Kizaki, K.; Koshi, K.; Matsuda, H.; Hashiyada, Y.; Imai, K.; Takahashi, T.; Ishiguro-Oonuma, T.; Hashizume, K. Evaluation of interferon-stimulated genes in peripheral blood granulocytes as sensitive responders to bovine early conceptus signals. Vet. J. 2017, 229, 37–44. [Google Scholar] [CrossRef]
- Yoshino, H.; Toji, N.; Sasaki, K.; Koshi, K.; Yamagishi, N.; Takahashi, T.; Ishiguro-Oonuma, T.; Matsuda, H.; Yamanouchi, T.; Hashiyada, Y.; et al. A predictive threshold value for the diagnosis of early pregnancy in cows using interferon-stimulated genes in granulocytes. Theriogenology 2018, 107, 188–193. [Google Scholar] [CrossRef]
- Yoshino, H.; Kizaki, K.; Iga, K.; Hirata, T.; Matsuda, H.; Yamanouchi, T.; Hashiyada, Y.; Toji, N.; Ishiguro-Oonuma, T.; Takahashi, T.; et al. Use of a prediction method for early pregnancy status utilizing receiver operating characteristic curve analysis of peripheral blood leukocyte interferon-stimulated genes in Japanese-black cattle. Anim. Reprod. Sci. 2020, 214, 106283. [Google Scholar] [CrossRef]
- Hasler, J.F. Forty years of embryo transfer in cattle: A review focusing on the journal Theriogenology, the growth of the industry in north america, and personal reminisces. Theriogenology 2014, 81, 152–169. [Google Scholar] [CrossRef]
- Hashiyada, Y.; Okada, M.; Imai, K. Transition of the pregnancy rate of bisected bovine embryos after co-transfer with trophoblastic vesicles prepared from in vivo-cultured in vitro-fertilized embryos. J. Reprod. Dev. 2005, 51, 749–756. [Google Scholar] [CrossRef] [Green Version]
- Geary, T.W.; Burns, G.W.; Moraes, J.G.N.; Moss, J.I.; Denicol, A.C.; Dobbs, K.B.; Ortega, M.S.; Hansen, P.J.; Wehrman, M.E.; Neibergs, H.; et al. Identification of beef heifers with superior uterine capacity for pregnancy. Biol. Reprod. 2016, 95, 47. [Google Scholar] [CrossRef]
- Ealy, A.D.; Wooldridge, L.K.; McCoski, S.R. Board invited review: Post-transfer consequences of in vitro-produced embryos in cattle. J. Anim. Sci. 2019, 97, 2555–2568. [Google Scholar] [CrossRef]
- Matsuyama, S.; Kojima, T.; Kato, S.; Kimura, K. Relationship between quantity of IFNT estimated by IFN-stimulated gene expression in peripheral blood mononuclear cells and bovine embryonic mortality after AI or ET. Reprod. Biol. Endocrinol. 2012, 10, 21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirayama, H.; Moriyasu, S.; Kageyama, S.; Sawai, K.; Takahashi, H.; Geshi, M.; Fujii, T.; Koyama, T.; Koyama, K.; Miyamoto, A.; et al. Enhancement of maternal recognition of pregnancy with parthenogenetic embryos in bovine embryo transfer. Theriogenology 2014, 81, 1108–1115. [Google Scholar] [CrossRef]
- Hiraizumi, S.; Nishinomiya, H.; Oikawa, T.; Sakagami, N.; Sano, F.; Nishino, O.; Kurahara, T.; Nishimoto, N.; Ishiyama, O.; Hasegawa, Y.; et al. Superovulatory response in Japanese Black cows receiving a single subcutaneous porcine follicle–stimulating hormone treatment or six intramuscular treatments over three days. Theriogenology 2015, 83, 466–473. [Google Scholar] [CrossRef]
- Sugimura, S.; Akai, T.; Somfai, T.; Hirayama, M.; Aikawa, Y.; Ohtake, M.; Hattori, H.; Kobayashi, S.; Hashiyada, Y.; Konishi, K.; et al. Time-lapse cinematography-compatible polystyrene-based microwell culture system: A novel tool for tracking the development of individual bovine embryos. Biol. Reprod. 2010, 83, 970–978. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bustin, S.; Benes, V.; Garson, J.; Hellemans, J.; Huggett, J.; Kubista, M.; Mueller, R.; Nolan, T.; Pfaffl, M.W.; Shipley, G.L.; et al. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55, 611–622. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hanley, J.A.; McNeil, B.J. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 1982, 143, 29–36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schisterman, E.F.; Perkins, N.J.; Liu, A.; Bondell, H. Optimal Cut-point and its corresponding Youden Index to discriminate individuals using pooled blood samples. Epidemiology 2005, 16, 73–81. [Google Scholar] [CrossRef]
- Brooks, K.; Burns, G.; Spencer, T.E. Conceptus elongation in ruminants: Roles of progesterone, prostaglandin, interferon tau and cortisol. J. Anim. Sci. Biotechnol. 2014, 5, 53. [Google Scholar] [CrossRef] [Green Version]
- Romero, J.J.; Antoniazzi, A.Q.; Nett, T.M.; Ashley, R.L.; Webb, B.T.; Smirnova, N.P.; Bott, R.C.; Bruemmer, J.E.; Bazer, F.W.; Anthony, R.V.; et al. Temporal Release, paracrine and endocrine actions of ovine conceptus-derived interferon-tau during early pregnancy. Biol. Reprod. 2015, 93, 146. [Google Scholar] [CrossRef]
- Spencer, T.E.; Forde, N.; Lonergan, P. The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants. J. Dairy Sci. 2016, 99, 5941–5950. [Google Scholar] [CrossRef] [Green Version]
- Balhara, A.K.; Gupta, M.; Singh, S.; Mohanty, A.K.; Singh, I. Early pregnancy diagnosis in bovines: Current status and future directions. Sci. World J. 2013, 2013, 958540. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reese, S.T.; Pereira, M.C.; Vasconcelos, J.L.M.; Smith, M.F.; Green, J.A.; Geary, T.W.; Peres, R.F.G.; Perry, G.A.; Pohler, K.G. Markers of pregnancy: How early can we detect pregnancies in cattle using pregnancy-associated glycoproteins (PAGs) and microRNAs? Anim. Reprod. 2016, 13, 200–208. [Google Scholar] [CrossRef]
- Sasaki, K.; Yamagishi, N.; Kizaki, K.; Devkota, B.; Hashizume, K. Microarray-based gene expression profiling of peripheral blood mononuclear cells in dairy cows with experimental hypocalcemia and milk fever. J. Dairy Sci. 2014, 97, 247–258. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kizaki, K.; Kageyama, T.; Toji, N.; Koshi, K.; Sasaki, K.; Yamagishi, N.; Ishiguro-Oonuma, T.; Takahashi, T.; Hashizume, K. Gene expression profiles in bovine granulocytes reflect the aberration of liver functions. Anim. Sci. J. 2020, 91, e13324. [Google Scholar] [CrossRef]
Gene | Accession Number | Strand | Sequence (5′–3′) |
---|---|---|---|
ISG15 | NM_174366 | Forward | GCAGACCAGTTCTGGCTGTCT |
Reverse | CCAGCGGGTGCTCATCAT | ||
MX1 | NM_173940 | Forward | GAGGTGGACCCCCAAGGA |
Reverse | CCACCAGATCGGGCTTTGT | ||
MX2 | NM_173941 | Forward | GGGCAGCGGAATCATCAC |
Reverse | CTCCCGCTTTGTCAGTTTCAG | ||
OAS1 | NM_178108 | Forward | CCAAGTCAAACAAGCCATCGA |
Reverse | CACATCGGAAACACCTCTCCTT | ||
GAPDH | NM_001034034 | Forward | AAGGCCATCACCATCTTCCA |
Reverse | CCACCACATACTCAGCACCAGCAT |
Group | n | ISG15 | MX1 | MX2 | OAS1 |
---|---|---|---|---|---|
Pregnant | 10 | 0.71 ± 0.10 a | 0.28 ± 0.03 a | 0.64 ± 0.09 a | 0.66 ± 0.19 |
Non-pregnant | 23 | 0.20 ± 0.05 b | 0.13 ± 0.02 b | 0.25 ± 0.06 b | 0.37 ± 0.06 |
Non-pregnant with late embryonic death | 7 | 0.26 ± 0.12 b | 0.15 ± 0.03 b | 0.27 ± 0.09 b | 0.18 ± 0.04 |
Value | ISG15 | MX1 | MX2 | OAS1 |
---|---|---|---|---|
AUC | 0.903 | 0.883 | 0.883 | 0.623 |
Youden index | 0.386 | 0.174 | 0.380 | 0.986 |
Threshold Value = AVE | Threshold Value = Youden Index | |||||||
---|---|---|---|---|---|---|---|---|
ISG15 | MX1 | MX2 | OAS1 | ISG15 | MX1 | MX2 | OAS1 | |
TP | 10 | 10 | 10 | 6 | 8 | 9 | 9 | 4 |
FP | 11 | 27 | 19 | 10 | 5 | 6 | 6 | 0 |
FN | 0 | 0 | 0 | 4 | 2 | 1 | 1 | 6 |
TN | 19 | 3 | 11 | 20 | 25 | 24 | 24 | 30 |
Sensitivity a | 100 | 100 | 100 | 60.0 | 80.0 | 90.0 | 90.0 | 40.0 |
Specificity b | 63.3 | 10.0 | 36.7 | 66.6 | 83.3 | 80.0 | 80.0 | 100 |
Accuracy | 72.5 | 32.5 | 52.5 | 65.0 | 82.5 | 82.5 | 82.5 | 85.0 |
PPV | 47.6 | 27.0 | 34.5 | 37.5 | 61.5 | 60.0 | 60.0 | 100 |
NPV | 100 | 100 | 100 | 83.3 | 93.6 | 96.0 | 96.0 | 83.3 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yoshino, H.; Kizaki, K.; Hirata, T.-i.; Iga, K.; Matsuda, H.; Yamanouchi, T.; Hashiyada, Y.; Imai, K.; Ishiguro-Oonuma, T.; Kanazawa, T.; et al. Interferon-Stimulated Gene Expression in Peripheral Blood Leucocytes as a Convenient Prediction Marker for Embryo Status in Embryo-Transferred Japanese Black Cows during the Peri-Implantation Period. Vet. Sci. 2023, 10, 408. https://doi.org/10.3390/vetsci10070408
Yoshino H, Kizaki K, Hirata T-i, Iga K, Matsuda H, Yamanouchi T, Hashiyada Y, Imai K, Ishiguro-Oonuma T, Kanazawa T, et al. Interferon-Stimulated Gene Expression in Peripheral Blood Leucocytes as a Convenient Prediction Marker for Embryo Status in Embryo-Transferred Japanese Black Cows during the Peri-Implantation Period. Veterinary Sciences. 2023; 10(7):408. https://doi.org/10.3390/vetsci10070408
Chicago/Turabian StyleYoshino, Hitomi, Keiichiro Kizaki, Toh-ichi Hirata, Kosuke Iga, Hideo Matsuda, Tadayuki Yamanouchi, Yutaka Hashiyada, Kei Imai, Toshina Ishiguro-Oonuma, Tomomi Kanazawa, and et al. 2023. "Interferon-Stimulated Gene Expression in Peripheral Blood Leucocytes as a Convenient Prediction Marker for Embryo Status in Embryo-Transferred Japanese Black Cows during the Peri-Implantation Period" Veterinary Sciences 10, no. 7: 408. https://doi.org/10.3390/vetsci10070408