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MiR-1246 is upregulated and regulates lung cell apoptosis during heat stress in feedlot cattle

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Cell Stress and Chaperones Aims and scope

Abstract

Globally, heat stress seriously threatens productivity of cattle. The objective of this study was to identify novel miRNAs that regulated heat stress in feedlot cattle. Experiment was conducted under heat stress and normal conditions. With profiling miRNAs of each feedlot cattle, our results showed the level of miR-1246 was significantly increased in these heat-stressed cattle (P < 0.05). Furthermore, by using bioinformatics analysis and luciferase reporter assays combined with qPCR and western blot, we found miR-1246 negatively regulated poly (C) binding protein 2 (PCBP2) and cAMP response element binding protein-like 2 (CREBL2) mRNA and protein levels through binding to the 3′-UTR region (P < 0.05); further, it inhibited heat-induced apoptosis in lung cells. Finally, our results suggested that miR-1246 plays an important role in heat stress and it has the potential to be a novel modulation factor for heat stress in feedlot cattle.

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References

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

    Article  CAS  Google Scholar 

  • Armstrong DV (1994) Symposium—nutrition and heat-stress heat-stress interaction with shade and cooling. J Dairy Sci 77:2044–2050

    Article  CAS  Google Scholar 

  • Bartel DP (2007) MicroRNAs: genomics, biogenesis, mechanism, and function (Reprinted from Cell, vol 116, pg 281–297, 2004). Cell 131:11–29

    Google Scholar 

  • Basu R, Malig B (2011) High ambient temperature and mortality in California: Exploring the roles of age, disease, and mortality displacement. Environ Res 111:1286–1292

    Article  CAS  Google Scholar 

  • Belhadj Slimen I, Najar T, Ghram A, Abdrrabba M (2016) Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J Anim Physiol Anim Nutr 100:401–412

    Article  CAS  Google Scholar 

  • Broccard AF, Hotchkiss JR, Kuwayama N, Olson DA, Jamal S, Wangensteen DO, Marini JJ (1998) Consequences of vascular flow on lung injury induced by mechanical ventilation. Am J Resp Crit Care 157:1935–1942

    Article  CAS  Google Scholar 

  • Buzan JR, Oleson K, Huber M (2015) Implementation and comparison of a suite of heat stress metrics within the Community Land Model version 4.5. Geosci Model Dev 8:151–170

    Article  Google Scholar 

  • Chen X, Ba Y, Ma LJ, Cai X, Yin Y, Wang KH, Guo JG, Zhang YJ, Chen JN, Guo X, Li QB, Li XY, Wang WJ, Zhang Y, Wang J, Jiang XY, Xiang Y, Xu C, Zheng PP, Zhang JB, Li RQ, Zhang HJ, Shang XB, Gong T, Ning G, Wang J, Zen K, Zhang JF, Zhang CY (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18:997–1006

    Article  CAS  Google Scholar 

  • Chen KL, Fu YY, Shi MY, Li HX (2017) Down-regulation of miR-181a can reduce heat stress damage in PBMCs of Holstein cows (vol 52, pg 864, 2016). In Vitro Cell Dev-Anim 53:381–381

    Article  Google Scholar 

  • Cheung WL, Ajiro K, Samejima K, Kloc M, Cheung P, Mizzen CA, Beeser A, Etkin LD, Chernoff J, Earnshaw WC, Allis CD (2003) Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113:507–517

    Article  CAS  Google Scholar 

  • Choi AMK, Alam J (1996) Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Resp Cell Mol 15:9–19

    Article  CAS  Google Scholar 

  • Guan QM, Lu XY, Zeng HT, Zhang YY, Zhu JH (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74:840–851

    Article  CAS  Google Scholar 

  • Harvey KF, Pfleger CM, Hariharan IK (2003) The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114:457–467

    Article  CAS  Google Scholar 

  • Hunter MP, Ismail N, Zhang XL, Aguda BD, Lee EJ, Yu LB, Xiao T, Schafer J, Lee MLT, Schmittgen TD, Nana-Sinkam SP, Jarjoura D, Marsh CB (2008) Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3:1–11

    Google Scholar 

  • Irvin CG, Bates JH (2003) Measuring the lung function in the mouse: the challenge of size. Respir Res 4:1–9

    Article  Google Scholar 

  • Isik M, Blackwell TK, Berezikov E (2016) MicroRNA mir-34 provides robustness to environmental stress response via the DAF-16 network in C. elegans. Sci Rep-Uk 6:1–11

    Article  Google Scholar 

  • Kahle JJ, Neas LM, Devlin RB, Case MW, Schmitt MT, Madden MC, Diaz-Sanchez D (2015) Interaction effects of temperature and ozone on lung function and markers of systemic inflammation, coagulation, and fibrinolysis: a crossover study of healthy young volunteers. Environ Health Perspect 123:310–316

    Article  CAS  Google Scholar 

  • Kapila N, Sharma A, Kishore A, Sodhi M, Tripathi PK, Mohanty AK, Mukesh M (2018) Impact of heat stress on cellular and transcriptional adaptation of mammary epithelial cells in Riverine Buffalo (Bubalus bubalis) (vol 11, e0157237, 2017). PLoS One 13:1–28

    Article  Google Scholar 

  • Kishore A, Sodhi M, Kumari P, Mohanty AK, Sadana DK, Kapila N, Khate K, Shandilya U, Kataria RS, Mukesh M (2014) Peripheral blood mononuclear cells: a potential cellular system to understand differential heat shock response across native cattle (Bos indicus), exotic cattle (Bos taurus), and riverine buffaloes (Bubalus bubalis) of India. Cell Stress Chaperon 19:613–621

    Article  CAS  Google Scholar 

  • Kosaka N, Iguchi H, Ochiya T (2010) Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 101:2087–2092

    Article  CAS  Google Scholar 

  • Kronstad J, De Maria A, Funnell D, Laidlaw RD, Lee N, Ramesh MMDM (1998) Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways. Arch Microbiol 170:395–404

    Article  CAS  Google Scholar 

  • Kuo MY, Liao MF, Chen FL, Li YC, Yang ML, Lin RH, Kuan YH (2011) Luteolin attenuates the pulmonary inflammatory response involves abilities of antioxidation and inhibition of MAPK and NF kappa B pathways in mice with endotoxin-induced acute lung injury. Food Chem Toxicol 49:2660–2666

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li YJ, Lin L, Li ZG, Ye XC, Xiong K, Aryal B, Xu ZH, Paroo Z, Liu QH, He CA, Jin P (2012) Iron homeostasis regulates the activity of the microRNA pathway through poly(C)-binding protein 2. Cell Metab 15:895–904

    Article  CAS  Google Scholar 

  • Li W, Wu YF, Xu RH, Lu H, Hu C, Qian H (2014) miR-1246 releases RTKN2-dependent resistance to UVB-induced apoptosis in HaCaT cells. Mol Cell Biochem 394:299–306

    Article  CAS  Google Scholar 

  • Li FM, Bullough KZ, Vashisht AA, Wohlschlegel JA, Philpott CC (2016) Poly(rC)-binding Protein 2 regulates Hippo signaling to control growth in breast epithelial cells. Mol Cell Biol 36:2121–2131

    Article  CAS  Google Scholar 

  • Mitlohner FM, Morrow JL, Dailey JW, Wilson SC, Galyean ML, Miller MF, McGlone JJ (2001) Shade and water misting effects on behavior, physiology, performance, and carcass traits of heat-stressed feedlot cattle. J Anim Sci 79:2327–2335

    Article  CAS  Google Scholar 

  • Nair N, Kumar S, Gongora E, Gupta S (2013) Circulating miRNA as novel markers for diastolic dysfunction. Mol Cell Biochem 376:33–40

    Article  CAS  Google Scholar 

  • Nienaber JA, Hahn GL (2007) Livestock production system management responses to thermal challenges. Int J Biometeorol 52:149–157

    Article  CAS  Google Scholar 

  • Ogata-Kawata H, Izumiya M, Kurioka D, Honma Y, Yamada Y, Furuta K, Gunji T, Ohta H, Okamoto H, Sonoda H, Watanabe M, Nakagama H, Yokota J, Kohno T, Tsuchiya N (2014) Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS One 9:1–9

    Article  Google Scholar 

  • Poisky L, von Keyserlingk MAG (2017) Invited review: effects of heat stress on dairy cattle welfare. J Dairy Sci 100:8645–8657. https://doi.org/10.3168/jds.2017-12651

    Article  CAS  Google Scholar 

  • Renaudeau D, Collin A, Yahav S, de Basilio V, Gourdine JL, Collier RJ (2012) Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal 6:707–728

    Article  CAS  Google Scholar 

  • Sengar GS, Deb R, Singh U, Raja TV, Kant R, Sajjanar B, Alex R, Alyethodi RR, Kumar A, Kumar S, Singh R, Jakhesara SJ, Joshi CG (2018) Differential expression of microRNAs associated with thermal stress in Frieswal (Bos taurus x Bos indicus) crossbred dairy cattle. Cell Stress Chaperon 23:155–170

    Article  CAS  Google Scholar 

  • Takeshita N, Hoshino I, Mori M, Akutsu Y, Hanari N, Yoneyama Y, Ikeda N, Isozaki Y, Maruyama T, Akanuma N, Komatsu A, Jitsukawa M, Matsubara H (2013) Serum microRNA expression profile: miR-1246 as a novel diagnostic and prognostic biomarker for oesophageal squamous cell carcinoma. Brit J Cancer 108:644–652

    Article  CAS  Google Scholar 

  • Wang GK, Zhu JQ, Zhang JT, Li Q, Li Y, He J, Qin YW, Jing Q (2010) Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J 31:659–666

    Article  Google Scholar 

  • Yu J, Liu FH, Yin P, Zhu XY, Cheng GL, Wang N, Lu A, Luan WL, Zhang NW, Li JF, Guo KJ, Yin YL, Wang HC, Xu JQ (2011) Integrating miRNA and mRNA expression profiles in response to heat stress-induced injury in rat small intestine. Funct Integr Genomic 11:203–213

    Article  CAS  Google Scholar 

  • Zhao X, Zmijewski JW, Lorne E, Liu G, Park YJ, Tsuruta Y, Abraham E (2008) Activation of AMPK attenuates neutrophil proinflammatory activity and decreases the severity of acute lung injury. Am J Physiol Lung Cell 295:L497–L504

    Article  CAS  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 Chaperon 19:973–981

    Article  CAS  Google Scholar 

Download references

Funding

This work was financially supported by the Chongqing Municipal Science and Technology Commission project (no. cstc2017jcyjBX0013) The Research and Innovation Project of Chongqing Graduate Students ( no.CYB18074).

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Authors

Contributions

Y.H. and M.C.C. designed and performed the main experiments, Y.H. interpreted the results and wrote the manuscript. M.C.C. performed animal experiment; they equally contributed to this work. L.W. performed the qRT-PCR. T.H.Z. performed the vector construction. Z.G.L. performed the GO biological process enrichment and KEGG pathway network analyses. G.W.Z. amended the manuscript. F.Y.Z. designed the experiments and supervised the research. All authors read the final manuscript.

Corresponding author

Correspondence to Fu-Yuan Zuo.

Ethics declarations

All animal procedures were approved by the Southwest University Institutional Animal Care and Use Committee.

Competing interests

The authors declare that they have no competing interests.

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Hu, Y., Cai, MC., Wang, L. et al. MiR-1246 is upregulated and regulates lung cell apoptosis during heat stress in feedlot cattle. Cell Stress and Chaperones 23, 1219–1228 (2018). https://doi.org/10.1007/s12192-018-0927-9

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  • DOI: https://doi.org/10.1007/s12192-018-0927-9

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