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Differential expression of microRNAs associated with thermal stress in Frieswal (Bos taurus x Bos indicus) crossbred dairy cattle

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Cell Stress and Chaperones Aims and scope

Abstract

Environmental temperature is one of the important abiotic factors that influence the normal physiological function and productive performance of dairy cattle. Temperature stress evokes complex responses that are essential for safeguarding of cellular integrity and animal health. Post-transcriptional regulation of gene expression by miRNA plays a key role cellular stress responses. The present study investigated the differential expression of miRNA in Frieswal (Holstein Friesian × Sahiwal) crossbred dairy cattle that are distinctly adapted to environmental temperature stress as they were evolved by using the temperate dairy breed Holstein Friesian. The results indicated that there was a significant variation in the physiological and biochemical indicators estimated under summer stress. The differential expression of miRNA was observed under heat stress when compared to the normal winter season. Out of the total 420 miRNAs, 65 were differentially expressed during peak summer temperatures. Most of these miRNAs were found to target heat shock responsive genes especially members of heat shock protein (HSP) family, and network analysis revealed most of them having stress-mediated effects on signaling mechanisms. Being greater in their expression profile during peak summer, bta-miR-2898 was chosen for reporter assay to identify its effect on the target HSPB8 (heat shock protein 22) gene in stressed bovine PBMC cell cultured model. Comprehensive understanding of the biological regulation of stress responsive mechanism is critical for developing approaches to reduce the production losses due to environmental heat stress in dairy cattle.

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References

  • Ashok K, Praveen K, Singh SV (2007) Oxidative stress markers profile in erythrocytes of natural and heat exposed cattle and buffalos. Indian J Dairy Sci 60:114–118

    Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116:281–297

    Article  CAS  PubMed  Google Scholar 

  • Baskerville S, Bartel DP (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11(3):241–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belhadj Slimen I, Najar T, Ghram A, Abdrrabba M (2015) Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J Anim Physiol Anim Nutr 100(3):401–412

    Article  Google Scholar 

  • Bernabucci U, Ronchi B, Lacetera N, Nardone A (2005) Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. J Dairy Sci 88(6):2017–2026

    Article  CAS  PubMed  Google Scholar 

  • Bhanuprakash V, Singh U, Sengar G, Sajjanar B, Bhusan B, Raja TV, Alex R, Kumar S, Singh R, Kumar A, Alyethodi RR (2016) Differential effect of thermal stress on Hsp70 expression, nitric oxide production and cell proliferation among native and crossbred dairy cattle. J Therm Biol 59:18–25

    Article  CAS  PubMed  Google Scholar 

  • Bianca W (1965) Reviews of the progress of dairy science. Section A Physiology: Cattle in a hot environment. J Dairy Res 32:291–345

    Article  Google Scholar 

  • Charoensook R, Gatphayak K, Sharifi AR, Chaisongkram C, Brenig B, Knorr C (2012) Polymorphisms in the bovine HSP90AB1 gene are associated with heat tolerance in Thai indigenous cattle. Trop Anim Health Prod 44:921–928

    Article  PubMed  Google Scholar 

  • Chen K, Rajewsky N (2006) Deep conservation of microRNA-target relationships and 3′UTR motifs in vertebrates, flies, and nematodes. Cold Spring Harb Symp Quant Biol 71:149–156

    Article  CAS  PubMed  Google Scholar 

  • Craven RA, Egerton M, Stirling CJ (1996) A novel Hsp70 of the yeast ER lumen is required for the efficient translocation of a number of protein precursors. EMBO J 15:2640–2650

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deb R, Sajjanar B, Singh U, Kumar S, Singh R, Sengar G, Sharma A (2014) Effect of heat stress on the expression profile of Hsp90 among Sahiwal (Bos Indicus) and Frieswal (Bos Indicus × Bos Taurus) breed of cattle: a comparative study. Gene 536(2):435–440

    Article  CAS  PubMed  Google Scholar 

  • Fatima A, Waters S, O’Boyle P, Seoighe C, Morris DG (2014) Alterations in hepatic miRNA expression during negative energy balance in postpartum dairy cattle. BMC Genomics 15(1):28

    Article  PubMed  PubMed Central  Google Scholar 

  • Gamerdinger M, Carra S, Behl C (2011) Emerging roles of molecular chaperones and co-chaperones in selective autophagy: focus on BAG proteins. J Molec Med 89(12):1175–1182

    Article  CAS  PubMed  Google Scholar 

  • Ganaie AH, Shanker G, Bumla NA, Ghasura RS, Mir NA (2013) Biochemical and physiological changes during thermal stress in bovines. J Vet Sci Technol 4:126

    Google Scholar 

  • Ghaoui R, Palmio J, Brewer J, Lek M, Needham M, Evilä A, Hackman P, Jonson PH, Penttilä S, Vihola A, Huovinen S (2016) Mutations in HSPB8 causing a new phenotype of distal myopathy and motor neuropathy. Neurology 86(4):391–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 57(5):715–724

    Google Scholar 

  • Hansen PJ (2004) Physiological and cellular adaptations of zebu cattle to thermal stress. Anim Reprod Sci. (82-83):349-360

  • Harfe BD (2005) MicroRNAs in vertebrate development. Curr Opin Genet Dev 15(4):410–415

    Article  CAS  PubMed  Google Scholar 

  • Islam A, Deuster PA, Devaney JM, Ghimbovschi S, Chen Y (2013) An exploration of heat tolerance in mice utilizing mRNA and microRNA expression analysis. PLoS One 8(8):72258

    Article  Google Scholar 

  • Jacobs AAA, Dijkstra J, Liesman JS, VandeHaar MJ, Lock AL, van Vuuren AM, Hendriks WH, van Baal J (2013) Effects of short- and long-chain fatty acids on the expression of stearoyl-CoA desaturase and other lipogenic genes in bovine mammary epithelial cells. Animal 7:1508–1516

    Article  CAS  PubMed  Google Scholar 

  • Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186

    Article  CAS  PubMed  Google Scholar 

  • Kropp J, Salih SM, Khatib H (2014) Expression of microRNAs in bovine and human pre-implantation embryo culture media. Front Genet 5:91

    Article  PubMed  PubMed Central  Google Scholar 

  • Lacetera N, Bernabucci U, Scalia D, Basiricò L, Morera P, Nardone A (2006) Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. J Dairy Sci 89:4606–4612

    Article  CAS  PubMed  Google Scholar 

  • Lallawmkimi CM (2009) Impact of thermal stress and vitamin-E supplementation on Heat shock protein 72 and antioxidant enzymes in Murrah buffaloes. Ph. D. Thesis National Dairy Research Institute (deemed University), Karnal, India

  • Leung AK, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40:205–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115:787–798

    Article  CAS  PubMed  Google Scholar 

  • Li R, Beaudoin F, Ammah AA, Bissonnette N, Benchaar C, Zhao X, Lei C, Ibeagha-Awemu EM (2015) Deep sequencing shows microRNA involvement in bovine mammary gland adaptation to diets supplemented with linseed oil or safflower oil. BMC Genomics 16(1):884

    Article  PubMed  PubMed Central  Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191

    Article  CAS  PubMed  Google Scholar 

  • Lindquist S, Craig EA (1988) The heat shock proteins. Ann Rev Genet 22:631–637 0066-4197

    Article  CAS  PubMed  Google Scholar 

  • Liu E, Lewis K, Al-Saffar H, Krall CM, Singh A, Kulchitsky VA, Corrigan JJ, Simons CT, Petersen SR, Musteata FM, Bakshi CS (2012) Naturally occurring hypothermia is more advantageous than fever in severe forms of lipopolysaccharide-and Escherichia Coli-induced systemic inflammation. Am J Phys Regul Integr Comp Phys 302(12):1372–1383

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Marsh NM, Wareham A, White BG, Miskiewicz EI, Landry J, MacPhee DJ (2015) HSPB8 and the Cochaperone BAG3 are highly expressed during the synthetic phase of rat myometrium programming during pregnancy. Biol Reprod 92(5):131 1-12

    Article  PubMed  Google Scholar 

  • McConnell JR, Alexander LA, McAlpine SR (2014) A heat shock protein 90 inhibitor that modulates the immunophilins and regulates hormone receptors without inducing the heat shock response. Bioorg Med Chem Lett 24:661–666

    Article  CAS  PubMed  Google Scholar 

  • McKenna LB, Schug J, Vourekas A, McKenna JB, Bramswig NC, Friedman JR, Kaestner KH (2010) MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterology 139:1654–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mehla K, Magotra A, Choudhary J, Singh AK, Mohanty AK, Upadhyay RC, Srinivasan S, Gupta P, Choudhary N, Antony B, Khan F (2014) Genome wide analysis of the heat stress response in zebu (Sahiwal) cattle. Gene 533:500–550

    Article  CAS  PubMed  Google Scholar 

  • Moncini S, Salvi A, Zuccotti P, Viero G, Quattrone A, Barlati S, De Petro G, Venturin M, Riva P (2011) The role of miR-103 and miR-107 in regulation of CDK5R1 expression and in cellular migration. PLoS One 6(5):20038

    Article  Google Scholar 

  • Morelli FF, Mediani L, Heldens L, Bertacchini J, Bigi I, Carrà AD, Vinet J, Carra S (2017) An interaction study in mammalian cells demonstrates weak binding of HSPB2 to BAG3, which is regulated by HSPB3 and abrogated by HSPB8. Cell Stress Chaperones 22(4):531–540

    Article  CAS  PubMed  Google Scholar 

  • Muroya S, Hagi T, Kimura A, Aso H, Matsuzaki M, Nomura M (2016) Lactogenic hormones alter cellular and extracellular microRNA expression in bovine mammary epithelial cell culture. J Anim Sci Biotechnol 7(1):8

    Article  PubMed  PubMed Central  Google Scholar 

  • Nehammer C, Podolska A, Mackowiak SD, Kagias K, Pocock R (2015) Specific microRNAs regulate heat stress responses in Caenorhabditis Elegans. Sci Rep 5:8866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paula-Lopes FF, Chase CC, Al-Katanani YM, Krininger CE, Rivera RM, Tekin S, Majewski AC, Ocon OM, Olson TA, Hansen PJ (2003) Genetic divergence in cellular resistance to heat shock in cattle: differences between breeds developed in temperate versus hot climates in responses of preimplantation embryos, reproductive tract tissues and lymphocytes to increased culture temperatures. Reproduction 125(2):285–294

    Article  CAS  PubMed  Google Scholar 

  • Place RF, Noonan EJ (2014) Non-coding RNAs turn up the heat: an emerging layer of novel regulators in the mammalian heat shock response. Cell Stress Chaperones 19(2):159–172

    Article  CAS  PubMed  Google Scholar 

  • Rajewsky N (2006) microRNA target predictions in animals. Nat Genet 38:8–13

    Article  Google Scholar 

  • Roman-Ponce H, Thatcher WW, Buffington DE, Wilcox CJ, Van Horn HH (1977) Physiological and production responses of dairy cattle to a shade structure in a subtropical Environment1. J Dairy Sci 60(3):424–430

    Article  Google Scholar 

  • Romao JM, Jin W, He M, McAllister T (2014) MicroRNAs in bovine adipogenesis: genomic context, expression and function. BMC Genomics 15(1):137

    Article  PubMed  PubMed Central  Google Scholar 

  • Sengar GS, Deb R, Raja TV, Singh U, Kant R, Bhanuprakash V, Alyethodi RR, Kumar S, Verma P, Chakraborty S, Alex R, Singh R (2017) RT-LAMP assay: an alternative approach for profiling of bovine heat shock protein 70 gene in PBMC cultured model. Molecular Biology Reports (in press)

  • Suzuki H, Matsushita S, Suzuki K, Yamada G (2017) 5α-dihydrotestosterone negatively regulates cell proliferation of the periurethral ventral mesenchyme during urethral tube formation in the murine male genital tubercle. Andrology 5(1):146–152

    Article  CAS  PubMed  Google Scholar 

  • Trevisan M, Browne R, Ram M, Muti P, Freudenheim J, Carosella AM, Armstrong D (2001) Correlates of markers of oxidative status in the general population. Am J Epidemiol 154(4):348–356

    Article  CAS  PubMed  Google Scholar 

  • Wang XP, Luoreng ZM, Zan LS, Raza SH, Li F, Li N, Liu S (2016) Expression patterns of miR-146a and miR-146b in mastitis infected dairy cattle. Mol Cell Probes 30(5):342–344

    Article  CAS  PubMed  Google Scholar 

  • Wang ZH, Zhang JL, Duan YL, Zhang QS, Li GF, Zheng DL (2015) MicroRNA-214 participates in the neuroprotective effect of resveratrol via inhibiting α-synuclein expression in MPTP-induced Parkinson’s disease mouse. Biomed Pharmacother 74:252–256

    Article  CAS  PubMed  Google Scholar 

  • Witkos TM, Koscianska E, Krzyzosiak WJ (2011) Practical aspects of microRNA target prediction. Curr Mol Med 11(2):93–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Yuan L, Zhang X, Hamblin MH, Zhu T, Meng F, Li Y, Chen YE, Yin KJ (2016) Altered long non-coding RNA transcriptomic profiles in brain microvascular endothelium after cerebral ischemia. Exp Neurol 277:162–170

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, He Q, Chen G, Wang L, Jin B (2016) Regulation of non-coding RNAs in heat stress responses of plants. Front Plant Sci 7:1213

    PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Chen KL, Zheng XM, Li HX, Wang GL (2014) Identification and bioinformatics analysis of microRNAs associated with stress and immune response in serum of heat-stressed and normal Holstein cows. Cell Stress Chaperones 19(6):973–981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors are thankful to the Director, ICAR-CIRC, Meerut for providing necessary facilities to carry out the present research. Authors acknowledge the Science and Engineering Research Board, Government of India, for providing financial support under the project YSS/2014/000279 to RD. We are also thankful to Military Farm, Meerut, India, for providing experimental animals; Ome Research Laboratory, Anand Agricultural University, Gujrat, India for deep sequencing.

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  1. Gyanendra Singh Sengar and Rajib Deb contributed equally

Authors and Affiliations

  1. Molecular Genetics Laboratory, ICAR-Central Institute for Research on Cattle, Meerut, Uttar Pradesh, 250 001, India

    Gyanendra Singh Sengar, Rajib Deb, Umesh Singh, T. V. Raja, Rani Alex, R. R. Alyethodi, Ashish Kumar, Sushil Kumar & Rani Singh

  2. Sam Higginbottom University of Agriculture Technology and Science, Allahabad, India

    Gyanendra Singh Sengar & Rajiv Kant

  3. School of Atmospheric Stress Management, National Institute of Abiotic Stress Management, Baramati, Maharashtra, India

    Basavraj Sajjanar

  4. Department of Animal Biotechnology, Anand Agricultural University, Anand, Gujarat, India

    Subhash J. Jakhesara & C. G. Joshi

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  1. Gyanendra Singh Sengar
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  2. Rajib Deb
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Correspondence to Gyanendra Singh Sengar or Rajib Deb.

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All the experimental procedures involving animals were approved by the Institutional Animal Ethics Committee (IAEC)

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Sengar, G.S., Deb, R., Singh, U. et al. Differential expression of microRNAs associated with thermal stress in Frieswal (Bos taurus x Bos indicus) crossbred dairy cattle. Cell Stress and Chaperones 23, 155–170 (2018). https://doi.org/10.1007/s12192-017-0833-6

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  • DOI: https://doi.org/10.1007/s12192-017-0833-6

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