Expression profile of interferon-stimulated gene 15 in leukocytes during early pregnancy in Capra hircus
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Abstract
Interferon-stimulated gene 15 (ISG15) is induced by conceptus-derived interferon tau (IFNT) in the endometrium during early pregnancy in ruminants, including goats. The expression of ISG15 in extra-uterine tissues, such as peripheral blood leukocytes (PBLs), suggests its potential as a novel pregnancy biomarker. The onset and length of the breeding season in goats are influenced by various factors such as breed, latitude, climate, photoperiod, etc. The Osmanabadi, an Indian goat breed, known for its early maturity, prolificacy, and good dressing percentage, was the focus of the current study. The present investigation was designed to study the messenger ribonucleic acid (mRNA) profile of Caprine ISG15 (cpISG15) in PBLs using real-time reverse transcription PCR (qPCR) on days 0, 13, 17, 21, 25 and 30 post-service in this breed. Pregnancies were confirmed by measuring plasma progesterone (P4) concentration and conducting trans-abdominal ultrasound scanning. The study revealed that the expression of cpISG15 mRNA was 5 to 8-fold higher (P < 0.05) during early pregnancy on days 17, 21, and 25 compared to day 0. There was no significant difference in the expression of cpISG15 mRNA between days 0 and 30 post-service. Progesterone concentration was higher on days 17, 21, and 25 in pregnant does compared to day 0. The presence of fetal parts was observed by ultrasound between 45 and 90 d of pregnancy. It is concluded that the detection of elevated ISG15 expression in PBLs during the early stages of pregnancy may be used as a marker for pregnancy detection in does.
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Bazer FW, Song G, Thatcher WW. Roles of conceptus secretory proteins in establishment and maintenance of pregnancy in ruminants. Asian-Australasian Journal Animal Sciences. 2012;25(1):1−16. doi: 10.5713/ajas.2011.r.08.
Vallet JL, Barker PJ, Lamming GE, Skinner N, Huskinsson, NS. A low molecular weight endometrial secretory protein which is increased by ovine trophoblast protein-1 is a β2- microglobulin like protein. Journal of Endocrinology.1991;130(2):R1−R4. doi: 10.1677/joe.0.130R001.
Bazer FW, Spencer TE, Johnson GA. Burghardt RC. Uterine receptivity to implantation of blastocyst in mammals. Frontiers in Bioscience. 2011;3(2):745−767. doi: 10.2741/s184.
Mirando MA, Short EC, Jr Geisert RD, Vallet JL, Bazer FW. Stimulation of 2',5'- oligoadenylate synthetase activity in sheep endometrium during pregnancy, by intrauterine infusion of ovine trophoblast protein-1, and by intramuscular administration of recombinant bovine interferon-alpha1. Journal Reproduction Fertility. 1991;93(2):599−607. doi: 10.1530/jrf.0.0930599.
Rueda BR, Naivar KA, George EM, Austin KJ, Francis H, Hansen TR. Recombinant interferon-tau regulates secretion of two bovine endometrial proteins. Journal of Interferon Research. 1993;13(4):303−309. doi: 10.1089/jir.1993.13.303.
Naivar KA, Ward SK, Austin KJ, Moore DW, Hansen TR. Secretion of bovine uterine proteins in response to type I interferons. Biology of Reproduction. 1995;52(4):848−854. doi: 10.1095/biolreprod52.4.848.
Johnson GA, Austin KJ, Collins AM, Murdoch WJ, Hansen TR. Endometrial ISG17 mRNA and a related mRNA are induced by interferon tau and localized to glandular epithelial and stromal cells from pregnant cows. Endocrinology. 1999;10:243–252. doi: 10.1007/BF02738623.
Johnson GA, Austin KJ, Kirk AV, Spencer TE, Burghardt RC, Hansen TR, et al. Expression of the Interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus. Biology Reproduction. 1999;61(1):312−318. doi: 10.1095/biolreprod61.1.312.
Joyce M, Hansen T, Johnson G. Interferon-stimulated gene 17 is expressed in the porcine uterus and may be critical to placental development across species. In: Society for the Study of Reproduction: Annual Meeting. Baltimore, Maryland. US; 2002.
Jain A, Baviskar PS, Kandasamy S, Kumar R, Singh R, Kumar S, et al. Interferon stimulated gene 15 (ISG15): Molecular characterization and expression profile in endometrium of buffalo. Animal Reproduction Science. 2012;133(3−4):159−168. doi: 10.1016/j.anireprosci.2012.06.023.
Chandrakar K, Jain A, Khan JR, Jain T, Singh M, Mishra OP. Molecular characterization and expression profile of interferon stimulated gene 15 (ISG15) in the endometrium of goat (Capra hircus). Theriogenology. 2020;142:348−354. doi: 10.1016/j.theriogenology.2019.10.013.
Han H, Austin KJ, Rempel LA, Hansen TR. Low blood ISG15 mRNA and progesterone levels are predictive of non-pregnant dairy cows. Journal of Endocrinology. 2006;191(2): 505–512. doi: 10.1677/joe.1.07015.
Takino T, Taku O, Tatsuya A, Katsuro H. Change in the responsiveness of interferon stimulated genes during early pregnancy in cows with Borna virus-1 infection. BMC Veterinary Research. 2016;12:253. doi: 10.1186/s12917-016-0883-5.
Cheng L, Xiang M, Hu X, Yu J, Xia Y, Tao B, et al. Duplex quantitative polymerase chain reaction of ISG15 and RSAD2 increases accuracy of early pregnancy diagnosis in dairy cows. Annals of Animal Science. 2019;19(2):383–401. doi: 10.2478/aoas-2019-0001.
Buragohain L, Kumar R, Nanda T, Phulia SK, Mohanty AK, Kumar S, et al. Serum MX2 protein as candidate biomarker for early pregnancy diagnosis in buffalo. Reproduction in Domestic Animal. 2016;51(4):453–460. doi: 10.1111/rda.12700.
Thakur N, Singh G, Paul A, Bharati J, Rajesh G, Vidyalakshmi GM, et al. Expression and molecular cloning of interferon stimulated genes in buffalo (Bubalus bubalis). Theriogenology. 2017;100:50−58. doi: 10.1016/j.theriogenology.2017.05.027.
Oliveira JF, Henkes LE, Ashley RL, Purcell SH, Smirnova NP, Veeramachaneni, DN, et al. Expression of interferon (IFN)-stimulated genes in extrauterine tissues during early pregnancy in sheep is the consequence of endocrine IFN-τ release from the uterine vein. Endocrinology. 2008;149(3):1252–1259. doi: 10.1210/en.2007-0863.
Kose M, Kaya MS, AydileK N, Kucukaslan I, Bayril T, Bademkiran S, et al. Expression profile of interferon tau-stimulated genes in ovine peripheral blood leukocytes during embryonic death. Theriogenology. 2016;85(6):1161−1166. doi: 10.1016/j.theriogenology.2015.11.032.
Aziz MA. Present status of the world goat populations and their productivity. Lohman Information. 2010;45:42.
Rathod P, Dixit S. Effect of improved management practices on productive and reproductive performance of Osmanabadi goats under semi-intensive rearing systems. The Indian Journal of Animal Sciences. 2021;91(6): 499–504. doi: 10.56093/ijans.v91i6.115455.
Fatet A, Pellicer-Rubio MT, Leboeuf B. Reproductive cycle of goats. Animal Reproduction Science. 2011;124(3−4):211−219. doi: 10.1016/j.anireprosci.2010.08.029.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25(4):402−408. doi: 10.1006/meth.2001.1262.
Kubasic NP, Hallauer GD, Brodows RG. Evaluation of direct solid – phase RIA for progesterone, useful for monitoring luteal function. Clinical Chemistry. 1984;30(2):284−286. doi: 10.1093/clinchem/30.2.284.
Brooks K, Burns G, Spencer TE. Conceptus elongation in ruminants: roles of progesterone, prostaglandin, interferon tau and cortisol. Journal of Animal Science and Biotechnology. 2014;5:53. doi: 10.1186/2049-1891-5-53.
Joyce MM, White FJ, Burghardt RC, Muniz JJ, Spencer TE, Bazer FW, et al. Interferon stimulated gene 15 conjugates to endometrial cytosolic proteins and is expressed at the uterine-placental interface throughout pregnancy in sheep. Endocrinology. 2005;146(2):675−684. doi: 10.1210/en.2004-1224.
Bott RC, Ashley RL, Henkes LE, Antoniazzi AQ, Bruemmer JE, Niswender GD, et al. Uterine vein infusion of interferon tau (IFNT) extends luteal life span in ewes. Biology of Reproduction. 2010;82(4):725−735. doi: 10.1095/biolreprod.109.079467.
Jain A, Jain T, Chandrakar K, Shakya S, Mukherjee K. Interferon-stimulated gene 15 (ISG15): Expression profile and role in the corpus luteum of goat (Capra hircus). The Indian Journal of Animal Sciences. 2022;92(8):957−960. doi: 10.56093/ijans.v92i8.109419.
Al-Samawi K, Al-Hassan M, Migdadi H, Ammar M, Alghamdi S. Interferon-stimulated gene 15 and interferon-1 stimulated gene 17 messenger RNA-based detection of early pregnancy in Aardi goats in Saudi Arabia. Pakistan Journal of Zoology. 2021;53(3):1005−1013. doi: 10.17582/journal.pjz/20180329180335.
Austin KJ, Carr AL, Pru JK, Hearne CE, George EL, Belden EL, et al. Localization of ISG15 and conjugated proteins in bovine endometrium using immunohistochemistry and electron microscopy. Endocrinology. 2004;145(2):967−975. doi: 10.1210/en.2003-1087.
Hansen TR, Austin KJ, Johnson GA. Transient ubiquitin cross-reactive protein gene expression in the bovine endometrium. Endocrinology. 1997;138(11):5079−5082. doi: 10.1210/endo.138.11.5655.
Boerboom D, Brown KA, Vaillancourt D, Poitras P, Goff AK, Watanabe K, et al. Expression of key prostaglandin synthases in equine endometrium during late diestrus and early pregnancy. Biology of Reproduction. 2004;70(2):391–399. doi: 10.1095/biolreprod.103.020800.
Frade JP, Warnock DW, Arthington-Skaggs BA. Rapid quantification of drug resistance gene expression in Candida albicans by reverse transcriptase LightCycler PCR and fluorescent probe hybridization. Journal of Clinical Microbiology. 2004;42(5):2085–2093. doi: 10.1128/JCM.42.5.2085-2093.2004.
Hida S, Ogasawara K, Sato K, Abe M, Takayanagi H, Yokochi, T, et al. CD8+ T cell mediated skin disease in mice lacking IRF-2, the transcriptional attenuator of interferon-α/β signaling. Immunity. 2000;13(5):643–655. doi: 10.1016/s1074-7613(00)00064-9.
Gifford CA, Racicot K, Clark DS, Austin KJ, Hansen TR, Lucy MC, et al. Regulation of interferon-stimulated genes in peripheral blood leukocytes in pregnant and bred, non-pregnant dairy cows. Journal of Dairy Science. 2007;90(1):274–280. doi: 10.3168/jds.S0022-0302(07)72628-0.
Carvalho PD, Consentini CC, Weaver SR, Barleta RV, Hernandez LL, Fricke PM. Temporarily decreasing progesterone after timed artificial insemination decreased expression of interferon-tau stimulated gene 15 (ISG15) in blood leukocytes, serum pregnancy-specific protein B concentrations, and embryo size in lactating Holstein cows. Journal of Dairy Science. 2017;100(4):3233−3242. doi: 10.3168/jds.2016-11996.
Green JC, Okamura CS, Poock SE, Lucy MC. Measurement of interferon-tau (IFN-T) stimulated gene expression in blood leukocytes for pregnancy diagnosis within 18–20 d after insemination in dairy cattle. Animal Reproduction Science. 2010;121(1-2):24−33. doi: 10.1016/j.anireprosci.2010.05.010.
Soumya NP, Das DN, Jeyakumar S, Mondal S, Mor A, Mundhe UT. Differential expression of ISG 15 mRNA in peripheral blood mononuclear cells of nulliparous and multiparous pregnant versus non-pregnant Bos indicus cattle. Reproduction of Domestic Animals. 2017;52(1):97−106. doi: 10.1111/rda.12815.
Haq IU, Han Y, Ali T, Wang Y, Gao H, Lin L, et al. Expression of interferon-stimulated gene ISG15 and ubiquitination enzymes is upregulated in peripheral blood monocyte during early pregnancy in dairy cattle. Reproduction Biology. 2016;16(4):255−260. doi: 10.1016/j.repbio.2016.10.001.
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. Reproductive Biology and Endocrinology. 2012;10:21. doi: 10.1186/1477-7827-10-21.
Sheikh AA, Om KH, Ajay KD. Interferon tau stimulated gene expression and pro-inflammatory cytokine profile relative to insemination in dairy cows. Biological Rhythm Research. 2019;50(3):335−345. doi: 10.1080/09291016.2018.1440777.
Nag BSP, Arunmozhi N, Sarath T, Asokan SA, Vijayarani K, Monica G, et al. Interferon stimulated gene 15 and Myxovirus resistance 2 gene are Upregulated during early pregnancy in buffaloes. International Journal of Current Microbiology and Applied Sciences. 2018;7(12):1755−1762. doi:10.20546/ijcmas.2018.712.204.
Bazer FW, Spencer TE, Johnson GA. Interferons and uterine receptivity. Seminars in Reproductive Medicine. 2009;27(1):90−102. doi: 10.1055/s-0028-1108013.
Farin CE, Imakawa K, Hansen TR, McDonnell JJ, Murphy, CN. Expression of trophoblastic interferon genes in sheep and cattle. Biology of Reproduction.1990;43(2):210−218. doi: 10.1095/biolreprod43.2.210.
Schmitt RA, Geisert RD, Zavy MT, Short EC, Blair RM. Uterine cellular changes in 2',5'- oligoadenylate synthetase during the bovine estrous cycle and early pregnancy. Biology of Reproduction. 1993;48(3):460−466. doi: 10.1095/biolreprod48.3.460.
Johnson GA, Stewart MD, Gray CA, Choi Y, Burghardt RC, Yu-Lee LY, et al. Effects of the estrous cycle, pregnancy, and interferon tau on 2’,5’- oligoadenylate synthetase expression in the ovine uterus. Biology Reproduction. 2001;64(5):1392−1399. doi: 10.1095/biolreprod64.5.1392.
Panicker SS, Kanakkaparambil R, Kanjirakuzhiyil P, Koodathil R. Progesterone profile of goats subjected to oestrus synchronization and its relevance in predicting pregnancy outcome. Advances in Animal and Veterinary Sciences. 2015;3(4):207−210. doi: 10.14737/journal.aavs/2015/3.4.207.210.
Boscos CM, Samartzi FC, Lymberopoulos AG, Stefanakis A, Belibasaki S. Assessment of progesterone concentration using enzyme immunoassay, for early pregnancy diagnosis in sheep and goats. Reproduction in Domestic Animal. 2003;38(3):170−174. doi: 10.1046/j.1439-0531.2003.00407.x.
Devalal K, Joseph M, Kurien MO, Aravind A, Ajitkumar S. Serum progesterone and oestradiol profile in pseudopregnant and pregnant goats below 3 months post-service. Journal of Veterinary and Animal Sciences. 2019;50(1):63−67.
Rahman, ANMA. Hormonal changes in the uterus during pregnancy lessons from the ewe: a review. Journal of Agricultural and Rural Development. 2008;4(1):1−7. doi: 10.3329/jard.v4i1.761.
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