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Effects of seasonal ambient heat stress on expression of microRNAs in the mammary gland of Holstein cows

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Abstract

This study was conducted to assess the link of miRNA expressions in cow’s mammary gland undergoing heat stress. Twelve Holstein cows were allocated either to undergo heat stress (HS) or remain in a thermoneutral environment (non-heat stress, NS), respectively. The experiment with HS cows was carried out in August, and the experiment with NS cows was done in November. After a month, three cows from each group were slaughtered, and mammary gland samples were obtained, and then miRNA were extracted from the samples for later sequencing. From the miRNA-seq, we obtained a total of 124 differentially expressed miRNAs in HS and NS cows’ mammary gland. The differentially expressed miRNA could be predicted to influence multiple target genes. The target interleukin-1 (IL-1), which play a role in regulating the function of mammary gland in dairy cows, could be affected by bta-let-7c, bta-let-7e, bta-miR-181d, bta-miR-452, and bta-miR-31. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that mitogen-activated protein kinase (MAPK) pathway plays an important role in the mammary glands of dairy cows and bta-miR-25 and bta-miR-382 may influence MAPK pathway through c-Jun N-terminal kinase (JNK) gene to affect the function of mammary gland in HS cows. In conclusion, this study characterized expression profile of miRNAs in the Holstein cows’ mammary gland under summer heat stress or not. We observed miRNA expression during heat stress, which was significantly different from non-heat stress states. A comprehensive analysis of the miRNA’s expression will be helpful to further study the link of miRNAs with mechanisms regulating heat stress in the cow mammary gland.

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Data availability

Raw sequenced data have been deposited in a NCBI Sequence Read Archive repository (accession number PRJNA516100). The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

References

  • Ambros V (2004) The functions of animal micrornas. Nature 431:350–355

    Article  CAS  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  Google Scholar 

  • Arthur JSC, Ley SC (2013) Mitogen-activated protein kinases in innate immunity. Nature Rev Immunol 13:679–692

    Article  CAS  Google Scholar 

  • Carroll NM, Elaraj DM, Puhlmann M et al (2004) Alterations in tumor necrosis factor–induced endothelial cell procoagulant activity by hyperthermia. International J Cancer 111:457–462

    Article  CAS  Google Scholar 

  • Collier RJ, Collier JL, Rhoads RP, Baumgard LH (2008) Invited review: genes involved in the bovine heat stress response. J Dairy Sci 91:0-454

  • Croce CM, Calin GA (2005) Mirnas, cancer, and stem cell division. Cell 122:0-7

  • Dorion S, Lambert H, Landry J (2002) Activation of the p38 signaling pathway by heat shock involves the dissociation of glutathione s-transferase mu from ask1. J Biol Chem 277:30792–30797

    Article  CAS  Google Scholar 

  • Du J, Li M, Yuan Z, Guo M, Chen Y (2016) A decision analysis model for kegg pathway analysis. BMC Bioinformatics 17(1):407

    Article  Google Scholar 

  • Friedlander MR, Mackowiak SD, Li N, Chen W, Rajewsky N (2012) Mirdeep2 accurately identifies known and hundreds of novel microrna genes in seven animal clades. Nucleic Acids Res 40:37–52

    Article  Google Scholar 

  • Guo L, Zhao Y, Yang S et al (2014) Integrative analysis of mirna-mrna and mirna-mirna interactions. Biomed Res Int 2014:907420

    Google Scholar 

  • Herbut P, Angrecka S (2012) Forming of temperature-humidity index (thi) and milk production of cows in the free-stall barn during the period of summer heat. Anim Sci Pap Rep 30:363–372

    Google Scholar 

  • Hu X, Macdonald DM, Huettner PC, Feng Z, el Naqa IM, Schwarz JK, Mutch DG, Grigsby PW, Powell SN, Wang X (2009) A mir-200 microrna cluster as prognostic marker in advanced ovarian cancer. Gynecol Oncol 114:457–464

    Article  CAS  Google Scholar 

  • Hu H, Wang J, Gao H, Li S, Zhang Y, Zheng N (2016) Heat-induced apoptosis and gene expression in bovine mammary epithelial cells. Anim Prod Sci 56:918

    Article  CAS  Google Scholar 

  • Inman JL, Robertson C, Mott JD, Bissell MJ (2015) Mammary gland development: cell fate specification, stem cells and the microenvironment. Development 142:1028–1042

    Article  CAS  Google Scholar 

  • Jay C, Nemunaitis J, Chen P, Fulgham P, Tong AW (2007) mi\r RNA profiling for diagnosis and prognosis of human cancer. DNA Cell Biol 26:293–300

    Article  CAS  Google Scholar 

  • Kadzere CT, Murphy MR, Silanikove N, Maltz E (2002) Heat stress in lactating dairy cows: a review. Livest Prod Sci 77:59–91

    Article  Google Scholar 

  • Lacetera N, Bernabucci U, Scalia DL, 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 89:0-4612

  • Langmead B, Trapnell C, Pop M et al (2009) Ultrafast and memory-efficient alignment of short dna sequences to the human genome. Genome Biol 10

  • Li X, Carthew RW (2005) A microrna mediates egf receptor signaling and promotes photoreceptor differentiation in the drosophila eye. Cell 123:0-1277

  • Li Z, Liu H, Jin X, Lo L, Liu J (2012) Expression profiles of micrornas from lactating and non-lactating bovine mammary glands and identification of mirna related to lactation. BMC Genomics 13:731

    Article  CAS  Google Scholar 

  • Li J, Zhen W, Long D et al (2016) KEGG annotation of DEGs. PLOS ONE. https://doi.org/10.1371/journal.pone.0164235.g007

  • Li Q, Yang C, Du J et al (2018) Characterization of mirna profiles in the mammary tissue of dairy cattle in response to heat stress. BMC Genomics 19:975

    Article  CAS  Google Scholar 

  • Macfarlane LA, Murphy PR (2010) Microrna: biogenesis, function and role in cancer. Curr Genomics 11:537–561

    Article  CAS  Google Scholar 

  • Maroni P, Bendinelli P, Zuccorononno C, Schiaffonati L, Piccoletti R (2000) Cellular signalling after in vivo heat shock in the liver. Cell Biol Intern 24:145–152

    Article  CAS  Google Scholar 

  • Martinez N, Sinedino LDP, Bisinotto RS, Ribeiro ES, Gomes GC, Lima FS, Greco LF, Risco CA, Galvão KN, Taylor-Rodriguez D, Driver JP, Thatcher WW, Santos JEP (2014) Effect of induced subclinical hypocalcemia on physiological responses and neutrophil function in dairy cows. J Dairy Sci 97:874–887

    Article  CAS  Google Scholar 

  • Matthew GA, Yishi J (2016) Context specificity of stress-activated mitogen-activated protein (map) kinase signaling: the story as told by Caenorhabditis elegans*. J Biol Chem 291:7796–7804

    Article  Google Scholar 

  • Muraoka RS, Lenferink AEG, Simpson J, Brantley DM, Roebuck LR, Yakes FM, Arteaga CL (2001) Cyclin-dependent kinase inhibitor p27kip1 is required for mouse mammary gland morphogenesis and function. J Cell Biol 153:917–932

    Article  CAS  Google Scholar 

  • Rubinfeld H, Seger R (2004) The erk cascade as a prototype of mapk signaling pathways. Methods in Mol Biol 250:1

    CAS  Google Scholar 

  • Santos-Marques MJ, Carvalho F, Sousa C, Remião F, Bastos MDL (2006) Cytotoxicity and cell signaling induced by continuous mild hyperthermia in freshly isolated mouse hepatocytes. Toxicology 224:210–218

    Article  CAS  Google Scholar 

  • Sebastian DM (2011) Identification of novel and known mirnas in deep-sequencing data with mirdeep2. Curr ProtBioinfor 36:1

    Google Scholar 

  • Sengar GS, Deb R, Singh U et al (2017) Differential expression of micrornas associated with thermal stress in frieswal (bos taurus x bos indicus) crossbred dairy cattle. Cell Stress Chap 23:1–16

    Google Scholar 

  • Shwartz, G, Rhoads ML, Vanbaale MJ et al (2009) Effects of a supplemental yeast culture on heat-stressed lactating holstein cows. J Dairy Sci 92:0-942

  • St-Pierre NR, Cobanov B, Schnitkey G et al (2003) Economic losses from heat stress by us livestock industries. J Dairy Sci 86(supp-S):E52–E77

    Article  Google Scholar 

  • Tan W, Liu B, Qu S et al (2017) Micrornas and cancer: key paradigms in molecular therapy (review). Oncol Lett 15:2735–2742

    Google Scholar 

  • Varghese J, Cohen SM (2007) Microrna mir-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in drosophila. Gene Dev 21:2277–2282

    Article  CAS  Google Scholar 

  • Zhang M, Sun H, Fei Z, Zhan F, Gao S (2015) Fastq_clean: an optimized pipeline to clean the Illumina sequencing data with quality control. 2014 IEEE International Conference on Bioinformatics and Biomedicine (BIBM). Belfast 2014:44–48

    Google Scholar 

  • Zhang R, Zhu W, Mao S (2016) High-concentrate feeding upregulates the expression of inflammation-related genes in the ruminal epithelium of dairy cattle. J Anim Sci Biotechn 7:42

    Article  Google Scholar 

Download references

Funding

This study was financially supported by the National Key Research and Development Program of China (2016YFD0500503), the Shanghai Science and Technology Promotion Project for Agriculture (Shanghai Agriculture Science Promotion Project (2019) No. 1-2), and Open Fund of Anhui Province Key Laboratory of Local Livestock and Poultry, Genetical Resource Conservation and Breeding (AKLGRCB2017006).

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Correspondence to Zhao Zhuo or Jianbo Cheng.

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Fan, C., Hu, R., Fan, H. et al. Effects of seasonal ambient heat stress on expression of microRNAs in the mammary gland of Holstein cows. Int J Biometeorol 65, 235–246 (2021). https://doi.org/10.1007/s00484-020-02025-5

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  • DOI: https://doi.org/10.1007/s00484-020-02025-5

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