MicroRNAs as potential biomarkers in ruminant, avian and porcine

Year 2024, , 54 - 63, 30.04.2024

İsmail Bergutay Kalaycılar , Hasret Yardibi

https://doi.org/10.30704/http-www-jivs-net.1426005

Abstract

In recent years, studies on microRNAs have increased considerably. miRNAs are small RNA molecules, ranging from 19 to 25 nucleotides in length, that control the suppression of target genes after transcription. MiRNAs serve as fine-tuning factors that influence the expression of up to 60% of all mammalian protein-coding genes. Unlike proteins, miRNA sequences are widely conserved across species. This conservation strongly suggests that miRNAs emerged early in evolution and maintain their functional importance. It has been revealed that these small structures containing a small number of nucleotides can act as critical points in the organism. While traditional cancer biomarkers are mainly produced by tumor tissues or normal embryo tissues, they are absent or present in small amounts in tissue organs and the blood of healthy adults. MiRNAs can be easily detected in the blood, making them selectable candidates as biomarkers for disease. The ruminant family, one of the most diverse subspecies of terrestrial mammals, lives in a wide variety of environments worldwide and is known to have a major impact on various ecosystems and industries, including agriculture, daily activities, and cultures. MiRNAs have a significant impact on the physiology of farm animals, biological development, and cell differentiation. In this review, we will examine miRNAs that have been identified as candidates or potential candidates for the diagnosis and treatment of diseases seen in ruminants, pigs, and avians in recent years. In this way, we will provide a perspective to prevent diseases that can cause great economic losses in veterinary medicine and the production industry.

Keywords

biomarkers, micro RNA, veterinary medicine

References

• Ali, A., Murani, E., Hadlich, F., Liu, X., Wimmers, K., & Ponsuksili, S. (2021a). In utero fetal weight in pigs is regulated by microRNAs and their target genes. Genes, 12(8),1264.
• Ali, A., Murani, E., Hadlich, F., Liu, X., Wimmers, K., & Ponsuksili, S. (2021b). Prenatal skeletal muscle transcriptome analysis reveals novel microRNA-mRNA networks associated with intrauterine growth restriction in pigs. Cells, 10(5), 1007.
• Antunes, J., Lee, O., Alizadeh, A. H., LaMarre, J., & Koch, T. G. (2020). Why the hype—What are microRNAs and why do they provide unique investigative, diagnostic, and therapeutic opportunities in veterinary medicine? The Canadian Veterinary Journal, 61(8), 845.
• Bilinska, A., Pszczola, M., Stachowiak, M., Stachecka, J., Garbacz, F., Aksoy, M. O., & Szczerbal, I. (2023). Droplet digital PCR quantification of selected intracellular and extracellular microRNAs reveals changes in their expression pattern during porcine in vitro adipogenesis. Genes, 14(3).
• Chakraborty, N., Holmes-Hampton, G. P., Gautam, A., Kumar, R., Hritzo, B., Legesse, B., Dimitrov, G., Ghosh, S. P., & Hammamieh, R. (2023). Early to sustained impacts of lethal radiation on circulating miRNAs in a minipig model. Scientific Reports, 13(1), 18496.
• Chakraborty, S., Dhama, K., Tiwari, R., Iqbal Yatoo, M., Khurana, S. K., Khandia, R., Munjal, A., Munuswamy, P., Kumar, M. A., & Singh, M. (2019). Technological interventions and advances in the diagnosis of intramammary infections in animals with emphasis on bovine population—a review. Veterinary Quarterly, 39(1), 76-94. Chen, X., Wang, Z., Chen, Y., Akinci, I., Luo, W., Xu, Y., Jebessa, E., Blake, D., Sparks, N., Hanotte, O., & Nie, Q. (2022). Transcriptome analysis of differentially expressed circRNAs miRNAs and mRNAs during the challenge of coccidiosis. Frontiers in Immunology, 13, 910860.
• Chi, R., Lin, P. Y., Jhuo, Y. S., Cheng, F. Y., & Ho, J. A. (2024, Jan 15). Colorimetric detection of African swine fever (ASF)-associated microRNA based on rolling circle amplification and salt-induced gold nanoparticle aggregation. Talanta, 267, 125159.
• Ciliberti, M. G., Santillo, A., Sevi, A., Albenzio, M., De Leo, V., Ingrosso, C., Catucci, L., & Caroprese, M. (2023). First insight into extracellular vesicle-miRNA characterization in a sheep in vitro model of inflammation. Frontiers in Veterinary Science, 10.
• De Los Santos Funes, J. A., Andrade, J. P. N., Berndtson, J., & Parrish, J. (2023). Short communication: profiling the expression of Let-7d-5p microRNA in circulating blood of pregnant and nonpregnant cows. Journal of Animal Science, 101, skad054.
• Dixon, L. K., Sun, H., & Roberts, H. (2019). African swine fever. Antiviral Research, 165, 34-41.
• Dlamini, N. H., Nguyen, T., Gad, A., Tesfaye, D., Liao, S. F., Willard, S. T., Ryan, P. L., & Feugang, J. M. (2023). Characterization of extracellular vesicle-coupled miRNA profiles in seminal plasma of boars with divergent semen quality status. International Journal of Molecular Sciences, 24(4). 3194
• Do, D. N., Dudemaine, P.-L., Fomenky, B. E., & Ibeagha-Awemu, E. M. (2019). Integration of miRNA weighted gene co-expression network and miRNA-mRNA co-expression analyses reveals potential regulatory functions of miRNAs in calf rumen development. Genomics, 111(4), 849-859.
• Giles, T., van Limbergen, T., Sakkas, P., Quinn, L., Belkhiri, A., Maes, D., Kyriazakis, I., Barrow, P., & Foster, N. (2020). Diagnosis of sub-clinical coccidiosis in fast growing broiler chickens by microRNA profiling. Genomics, 112(5), 3218-3225.
• Grenier, B., Hackl, M., Skalicky, S., Thamhesl, M., Moll, W.-D., Berrios, R., Schatzmayr, G., & Nagl, V. (2019). MicroRNAs in porcine uterus and serum are affected by zearalenone and represent a new target for mycotoxin biomarker discovery. Scientific Reports, 9(1), 9408.
• Hamdi, M., Cañon‐Beltrán, K., Mazzarella, R., Cajas, Y. N., Leal, C. L., Gutierrez‐Adan, A., González, E. M., Da Silveira, J. C., & Rizos, D. (2021). Characterization and profiling analysis of bovine oviduct and uterine extracellular vesicles and their miRNA cargo through the estrous cycle. The FASEB Journal, 35(12), e22000.
• Hou, L., Ji, Z., Wang, G., Wang, J., Chao, T., & Wang, J. (2018). Identification and characterization of microRNAs in the intestinal tissues of sheep (Ovis aries). PLoS One, 13(2), e0193371.
• Hu, J., Dong, J., Zeng, Z., Wu, J., Tan, X., Tang, T., Yan, J., & Jin, C. (2020). Using exosomal miRNAs extracted from porcine follicular fluid to investigate their role in oocyte development. BMC Veterinary Research, 16(1), 485.
• Huang, Y., Zhang, C., Wang, Y., & Sun, X. (2022). Identification and analysis of miRNAs in the normal and fatty liver from the Holstein dairy cow. Animal Biotechnology, 33(3), 468-479.
• Kiss, A., Heber, S., Kramer, A. M., Hackl, M., Skalicky, S., Hallström, S., Podesser, B. K., & Santer, D. (2020). MicroRNA expression profile changes after cardiopulmonary bypass and ischemia/reperfusion-injury in a porcine model of cardioplegic arrest. Diagnostics, 10(4). 240
• Lai, Y.C., Habiby, G. H., Pathiranage, C. C. J., Rahman, M. M., Chen, H.-W., Husna, A. A., Kubota, C., & Miura, N. (2021). Bovine serum miR-21 expression affected by mastitis. Research in Veterinary Science, 135, 290-292.
• Lecchi, C., Zamarian, V., Gini, C., Avanzini, C., Polloni, A., Rota Nodari, S., & Ceciliani, F. (2020). Salivary microRNAs are potential biomarkers for the accurate and precise identification of inflammatory response after tail docking and castration in piglets. Journal of Animal Science, 98(5), skaa153.
• Li, N., Huang, K., Chen, Y., Huang, Z., Zhang, Y., Leng, C., Liu, Y., Shi, J., Xiao, S., & Yao, L. (2021). MicroRNA ssc-miR-124a exhibits antiviral activity against porcine reproductive and respiratory syndrome virus via suppression of host genes CD163. Veterinary Microbiology, 261, 109216.
• Li, R., Zhang, C.L., Liao, X.X., Chen, D., Wang, W.Q., Zhu, Y.H., Geng, X.H., Ji, D.J., Mao, Y.J., & Gong, Y.C. (2015). Transcriptome microRNA profiling of bovine mammary glands infected with Staphylococcus aureus. International Journal of Molecular Sciences, 16(3), 4997-5013.
• Li, Y. (2021). Comparing of backfat microRNAomes of Landrace and Neijiang pig by high-throughput sequencing. Genes Genomics, 43(5), 543-551.
• Liang, G., Malmuthuge, N., McFadden, T. B., Bao, H., Griebel, P. J., Stothard, P., & Guan, L. L. (2014). Potential regulatory role of microRNAs in the development of bovine gastrointestinal tract during early life. PLoS One, 9(3), e92592.
• Lin, X., Beckers, E., Mc Cafferty, S., Gansemans, Y., Joanna Szymańska, K., Chaitanya Pavani, K., Catani, J. P., Van Nieuwerburgh, F., Deforce, D., & De Sutter, P. (2019). Bovine embryo-secreted microRNA-30c is a potential non-invasive biomarker for hampered preimplantation developmental competence. Frontiers in genetics, 10, 315.
• Lu, T. X., & Rothenberg, M. E. (2018). MicroRNA. Journal of allergy and clinical immunology, 141(4), 1202-1207. Mahala, S., Kumar, A., Pandey, H. O., Saxena, S., Khanna, S., Kumar, M., Kumar, D., De, U. K., Pandey, A. K., & Dutt, T. (2024). Milk exosomal microRNA profiling identified miR-375 and miR-199-5p for regulation of immune response during subclinical mastitis of crossbred cattle. Molecular Biology Reports, 51(1), 59.
• Mendes, R. E. (2012). Ruminants: Anatomy, Behavior, and Diseases. Orleans, Santa Catarina State, Brazil: Nova Biomedical.
• Menezes, E. S., Badial, P. R., El Debaky, H., Husna, A. U., Ugur, M. R., Kaya, A., Topper, E., Bulla, C., Grant, K. E., & Bolden‐Tiller, O. (2020). Sperm miR‐15a and miR‐29b are associated with bull fertility. Andrologia, 52(1), e13412. Miretti, S., Lecchi, C., Ceciliani, F., & Baratta, M. (2020). MicroRNAs as biomarkers for animal health and welfare in livestock. Frontiers in Veterinary Science, 7, 578193.
• Naylor, D., Sharma, A., Li, Z., Monteith, G., Sullivan, T., Canovas, A., Mallard, B., Baes, C., & Karrow, N. (2020). Characterizing ovine serum stress biomarkers during endotoxemia. Journal of Dairy Science, 103(6), 5501-5508.
• Neerukonda, S. N., Tavlarides-Hontz, P., McCarthy, F., Pendarvis, K., & Parcells, M. S. (2019). Comparison of the transcriptomes and proteomes of serum exosomes from Marek’s disease virus-vaccinated and protected and lymphoma-bearing chickens. Genes, 10(2), 116.
• Núñez-Hernández, F., Pérez, L. J., Muñoz, M., Vera, G., Accensi, F., Sánchez, A., Rodríguez, F., & Núñez, J. I. (2017). Differential expression of porcine microRNAs in African swine fever virus infected pigs: a proof-of-concept study. Virology Journal, 14, 1-13.
• Ojo, O., Hajek, L., Johanns, S., Pacífico, C., Sener-Aydemir, A., Ricci, S., Rivera-Chacon, R., Castillo-Lopez, E., Reisinger, N., & Zebeli, Q. (2023). Evaluation of circulating microRNA profiles in blood as potential candidate biomarkers in a subacute ruminal acidosis cow model-a pilot study. BMC Genomics, 24(1), 1-15.
• Ojo, O. E., & Kreuzer-Redmer, S. (2023). MicroRNAs in ruminants and their potential role in nutrition and physiology. Veterinary Sciences, 10(1), 57.
• Ono, K., Okamoto, S., Ninomiya, C., Toji, N., Kanazawa, T., Ishiguro-Oonuma, T., Takahashi, T., Iga, K., & Kizaki, K. (2022). Analysis of circulating microRNA during early gestation in Japanese black cattle. Domestic Animal Endocrinology, 79, 106706.
• Otávio, K. S., Passos, J. R., Silva, R. F., Lima, L. F., Cadenas, J., Paes, V. M., Correia, H. H., Ferreira, A. C. A., Canafístula, F. G., & Bezerra, M. J. B. (2023). Comprehensive proteomic profiling of early antral follicles from sheep. Animal Reproduction Science, 248, 107153.
• Özdemir, S. (2020). Identification and comparison of exosomal microRNAs in the milk and colostrum of two different cow breeds. Gene, 743, 144609. Pang, Z., Chen, S., Cui, S., Zhai, W., Huang, Y., Gao, X., Wang, Y., Jiang, F., Guo, X., Hao, Y., Li, W., Wang, L., Zhu, H.,
• Wu, J., & Jia, H. (2023). Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV Infection. Animals, 13(7), 1246.
• Saenz-de-Juano, M. D., Silvestrelli, G., Bauersachs, S., & Ulbrich, S. E. (2022). Determining extracellular vesicles properties and miRNA cargo variability in bovine milk from healthy cows and cows undergoing subclinical mastitis. BMC Genomics, 23(1), 189.
• Santer, D., Kramer, A., Kiss, A., Aumayr, K., Hackl, M., Heber, S., Chambers, D. J., Hallström, S., & Podesser, B. K. (2019, Dec). St Thomas' Hospital polarizing blood cardioplegia improves hemodynamic recovery in a porcine model of cardiopulmonary bypass. J Thorac Cardiovasc Surg, 158(6), 1543-1554.e1548.
• Segura-Wang, M., Grenier, B., Ilic, S., Ruczizka, U., Dippel, M., Bünger, M., Hackl, M., & Nagl, V. (2021). MicroRNA Expression Profiling in Porcine Liver, Jejunum and Serum upon Dietary DON Exposure Reveals Candidate Toxicity Biomarkers. International Journal of Molecular Sciences, 22(21), 12043.
• haughnessy, R. G., Farrell, D., Stojkovic, B., Browne, J. A., Kenny, K., & Gordon, S. V. (2020). Identification of microRNAs in bovine faeces and their potential as biomarkers of Johne’s Disease. Scientific Reports, 10(1), 5908.
• Shokri, A., Asadpour, R., Jafari-Joozani, R., Babaei, E., Hajibemani, A., & Hamidian, G. (2023). Plasma microRNAs as non-invasive biomarkers in bovine endometritis caused by Gram-negative and Gram-positive bacteria. Veterinary Research Forum,
• Srikok, S., Patchanee, P., Boonyayatra, S., & Chuammitri, P. (2020). Potential role of MicroRNA as a diagnostic tool in the detection of bovine mastitis. Preventive veterinary medicine, 182, 105101.
• Sun, J., Letcher, R. J., Waugh, C. A., Jaspers, V. L. B., Covaci, A., & Fernie, K. J. (2021, May 20). Influence of perfluoroalkyl acids and other parameters on circulating thyroid hormones and immune-related microRNA expression in free-ranging nestling peregrine falcons. Sci Total Environ, 770, 145346.
• Swain, T., Deaver, C. M., Lewandowski, A., & Myers, M. J. (2021, Jul). Lipopolysaccharide (LPS) induced inflammatory changes to differentially expressed miRNAs of the host inflammatory response. Vet Immunol Immunopathol, 237, 110267.
• Tan, J., Sahaer, P., Li, H., Han, W., & Sun, H. (2024, Feb). The expression, function, and network regulation of circDNAJB6 in chicken macrophages under lipopolysaccharide (LPS) stimulation. Dev Comp Immunol, 151, 105095.
• Tewari, R. S., Ala, U., Accornero, P., Baratta, M., & Miretti, S. (2021). Circulating skeletal muscle related microRNAs profile in Piedmontese cattle during different age. Scientific Reports, 11(1), 15815.
• Tzelos, T., Ho, W., Charmana, V. I., Lee, S., & Donadeu, F. (2022). MiRNAs in milk can be used towards early prediction of mammary gland inflammation in cattle. Scientific Reports, 12(1), 5131.
• Wang, H., Peng, R., Wang, J., Qin, Z., & Xue, L. (2018). Circulating microRNAs as potential cancer biomarkers: the advantage and disadvantage. Clinical epigenetics, 10(1), 1-10. Wang, X., Gu, Z., & Jiang, H. (2013). MicroRNAs in farm animals. Animal, 7(10), 1567-1575.
• Wang, X., Yao, X., Xie, T., Chang, Z., Guo, Y., & Ni, H. (2020). Exosome‐derived uterine miR‐218 isolated from cows with endometritis regulates the release of cytokines and chemokines. Microbial Biotechnology, 13(4), 1103-1117.
• Winter, E., Cisilotto, J., Goetten, A. L., Veiga, Â., Ramos, A. T., Zimermann, F. C., Reck, C., & Creczynski-Pasa, T. B. (2022). MicroRNAs as serum biomarker for Senecio brasiliensis poisoning in cattle. Environmental Toxicology and Pharmacology, 94, 103906.
• Zhang, Q., Cai, R., Tang, G., Zhang, W., & Pang, W. (2021, Feb 3). MiR-146a-5p targeting SMAD4 and TRAF6 inhibits adipogenensis through TGF-β and AKT/mTORC1 signal pathways in porcine intramuscular preadipocytes. J Anim Sci Biotechnol, 12(1), 12.
• Zhang, Y., Wang, Y., Wang, H., Ma, X., & Zan, L. (2019). MicroRNA-224 impairs adipogenic differentiation of bovine preadipocytes by targeting LPL. Molecular and cellular probes, 44, 29-36.
• Zhong, T., Wang, C., Hu, J., Chen, X., Niu, L., Zhan, S., Wang, L., Guo, J., Cao, J., & Li, L. (2020). Comparison of MicroRNA transcriptomes reveals the association between MiR-148a-3p expression and rumen development in goats. Animals, 10(11), 195
• Zhou, C., Cai, G., Meng, F., Xu, Z., He, Y., Hu, Q., Zheng, E., Huang, S., Xu, Z., Gu, T., Hu, B., Wu, Z., & Hong, L. (2020). Deep-Sequencing Identification of MicroRNA Biomarkers in Serum Exosomes for Early Pig Pregnancy. Front Genet, 11, 536.
• Zhou, Y., Tian, W., Zhang, M., Ren, T., Sun, G., Jiang, R., Han, R., Kang, X., & Yan, F. (2019). Transcriptom analysis revealed regulation of dexamethasone induced microRNAs in chicken thymus. Journal of Cellular Biochemistry, 120(4), 6570-6579.