Abstract
Mongolian sheep and Dorper sheep as keystone sheep breed present excellent adaptability to the surroundings, but the heat-responsive genes of two sheep breeds are rarely explored, especially non-coding RNA gene. The three Mongolian sheep and three Dorper sheep were treated under heat condition, and the livers of six sheep were sampled and arranged to sequence. Using bioinformatics analysis to investigate RNA-seq data, 335 differentially expressed protein-coding genes and 65 long non-coding RNA (lncRNA) genes were emerged. In the liver of Mongolian sheep, 5 protein-coding genes relevant to heat response were inspected, including COMMD10, ABCA9, NIPAL1, APOA4 and LIN7A while 8 genes containing NUP62, PLIN2, ACACB, NIPAL1, EXO1, LGALS3, TRPM1 and TRPV2 were screened in liver of Dorper sheep. The biological effects of the 12 protein-coding genes were involved in heat shock protein binding, lipid homeostasis and storage, fatty acid oxidation, magnesium/calcium ions import, anti-oxidation and DNA repair. Among above heat response-centric genes, ABCA9 was predicted as target gene of significantly differential XLOC_476131. The selected 12 protein-coding genes and 1 lncRNA genes were considered to provide an understanding of how sheep positively respond to heat stress, and further to provide molecular evidence on heat-tolerance.
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Abbreviations
- FPKM:
-
fragments per kilo-base of exon per million
- HSP:
-
heat shock protein
- GABA:
-
γ-aminobutyric acid
- GO:
-
Gene Ontology
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
- lncRNA:
-
long non-coding RNA
References
Abu-Elheiga L, Matzuk MM, Abo-Hashema KA, Wakil SJ (2001) Continuous fatty acid oxidation and reduced fat storage in mice lacking acetyl-CoA carboxylase 2. Science 291:2613–2616. https://doi.org/10.1126/science.1056843
Abu-Elheiga L, Oh W, Kordari P, Wakil SJ (2003) Acetyl-CoA carboxylase 2 mutant mice are protected against obesity and diabetes induced by high-fat/high-carbohydrate diets. Proc Natl Acad Sci U S A 100:10207–10212. https://doi.org/10.1073/pnas.1733877100
Bakhtiarizadeh MR, Salehi A, Alamouti AA, Abdollahi-Arpanahi R, Salami SA (2019) Deep transcriptome analysis using RNA-Seq suggests novel insights into molecular aspects of fat-tail metabolism in sheep. Sci Rep 9:9203. https://doi.org/10.1038/s41598-019-45665-3
Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276–280. https://doi.org/10.1093/nar/30.1.276
Beladjal L, Gheysens T, Clegg JS, Amar M, Mertens J (2018) Life from the ashes: survival of dry bacterial spores after very high temperature exposure. Extremophiles 22:751–759. https://doi.org/10.1007/s00792-018-1035-6
Birch RM, Walker GM (2000) Influence of magnesium ions on heat shock and ethanol stress responses of Saccharomyces cerevisiae. Enzyme Microb Technol 26:678–687. https://doi.org/10.1016/s0141-0229(00)00159-9
Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115. https://doi.org/10.1016/j.tplants.2004.01.006
Briggs P (2018) Weather & Climate-South Africa. SafariBookings
Burstein E, Hoberg JE, Wilkinson AS, Rumble JM, Csomos RA, Komarck CM, Maine GN, Wilkinson JC, Mayo MW, Duckett CS (2005) COMMD proteins, a novel family of structural and functional homologs of MURR1. J Biol Chem 280:22222–22232. https://doi.org/10.1074/jbc.M501928200
Cao Y, Ohwatari N, Matsumoto T, Kosaka M, Ohtsuru A, Yamashita S (1999) TGF-beta1 mediates 70-kDa heat shock protein induction due to ultraviolet irradiation in human skin fibroblasts. Pflugers Arch 438:239–244. https://doi.org/10.1007/s004240050905
Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–441. https://doi.org/10.1038/18906
Chi HC, Tsai CY, Tsai MM, Yeh CT, Lin KH (2019) Molecular functions and clinical impact of thyroid hormone-triggered autophagy in liver-related diseases. J Biomed Sci 26:24. https://doi.org/10.1186/s12929-019-0517-x
Cotta-Ramusino C, Fachinetti D, Lucca C, Doksani Y, Lopes M, Sogo J, Foiani M (2005) Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol Cell 17:153–159. https://doi.org/10.1016/j.molcel.2004.11.032
Dayan O, Ben-Yona A, Kanner BI (2014) The aromatic and charge pairs of the thin extracellular gate of the γ-aminobutyric acid transporter GAT-1 are differently impacted by mutation. J Biol Chem 289:28172–28178. https://doi.org/10.1074/jbc.M114.589721
De Maio A (1999) Heat shock proteins: facts, thoughts, and dreams. Shock 11:1–12. https://doi.org/10.1097/00024382-199901000-00001
Devi S, Markandeya Y, Maddodi N, Dhingra A, Vardi N, Balijepalli RC, Setaluri V (2013) Metabotropic glutamate receptor 6 signaling enhances TRPM 1 calcium channel function and increases melanin content in human melanocytes. Pigment Cell Melanoma Res 26:348–356. https://doi.org/10.1111/pcmr.12083
Echeverría PC, Mazaira G, Erlejman A, Gomez-Sanchez C, Piwien Pilipuk G, Galigniana MD (2009) Nuclear import of the glucocorticoid receptor-hsp90 complex through the nuclear pore complex is mediated by its interaction with Nup62 and importin β. Mol Cell Biol 29:4788–4797. https://doi.org/10.1128/MCB.00649-09
Faber J, Thomsen HF, Lumholtz IB, Kirkegaard C, Siersbaek-Nielsen K, Friis T (1981) Kinetic studies of thyroxine, 3,5,3’-triiodothyronine, 3,3,5’-triiodothyronine, 3’,5’-diiodothyronine, 3,3’-diiodothyronine, and 3’-monoiodothyronine in patients with liver cirrhosis. J Clin Endocrinol Metab 53:978–984. https://doi.org/10.1210/jcem-53-5-978
Fiorentini P, Huang KN, Tishkoff DX, Kolodner RD, Symington LS (1997) Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol Cell Biol 17:2764–2773. https://doi.org/10.1128/mcb.17.5.2764
Gambade A, Zreika S, Guéguinou M, Chourpa I, Fromont G, Bouchet AM, Burlaud-Gaillard J, Potier-Cartereau M, Roger S, Aucagne V, Chevalier S, Vandier C, Goupille C, Weber G (2016) Activation of TRPV2 and BKCa channels by the LL-37 enantiomers stimulates calcium entry and migration of cancer cells. Oncotarget 7:23785–23800. https://doi.org/10.18632/oncotarget.8122
Goytain A, Hines RM, Quamme GA (2008) Functional characterization of NIPA2, a selective Mg2 + transporter. Am J Physiol Cell Physiol 295:C944–C953. https://doi.org/10.1152/ajpcell.00091.2008
Hall DM, Xu L, Drake VJ, Oberley LW, Oberley TD, Moseley PL, Kregel KC (2000) Aging reduces adaptive capacity and stress protein expression in the liver after heat stress. J Appl Physiol 89:749–759. https://doi.org/10.1152/jappl.2000.89.2.749
Hardie DG, Carling D (1997) The AMP-activated protein kinase: Fuel gauge of the mammalian cell? Eur J Biochem 246:259–273. https://doi.org/10.1111/j.1432-1033.1997.00259.x
Hou CL (2014) Genome sequencing of Mongolia sheep and genetic basis of cold resistance traits based on transcriptome analysis. Inner Mongolia Agricultural University, Hohhot, Inner Mongolia, China. (in Chinese)
Hu S, Ni W, Sai W, Zi H, Qiao J, Wang P, Sheng J, Chen C (2013) Knockdown of myostatin expression by RNAi enhances muscle growth in transgenic sheep. PLoS One 8:e58521. https://doi.org/10.1371/journal.pone.0058521
Huang DW, Sherman BT, Lempicki RA (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1–13. https://doi.org/10.1093/nar/gkn923
Huang DW, Sherman BT, Lempicki RA (2009b) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc 4:44–57. https://doi.org/10.1038/nprot.2008.211
Huang H, Bogstie JN, Vogel HJ (2012) Biophysical and structural studies of the human calcium- and integrin-binding protein family: understanding their functional similarities and differences. Biochem Cell Biol 90:646–656. https://doi.org/10.1139/o2012-021
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36. https://doi.org/10.1186/gb-2013-14-4-r36
King TA, Ghazaleh RA, Juhn SK, Adams GL, Ondrey FG (2005) Induction of heat shock protein 70 inhibits NF-kappa-B in squamous cell carcinoma. Otolaryngol Head Neck Surg 133:70–79. https://doi.org/10.1016/j.otohns.2004.04.038
Kirkpatrick DT, Ferguson JR, Petes TD, Symington LS (2000) Decreased meiotic intergenic recombination and increased meiosis I nondisjunction in exo1 mutants of Saccharomyces cerevisiae. Genetics 156:1549–1557
Kolupaev IuE, Oboznyĭ AI (2012) Participation of the active oxygen forms in the induction of ascorbate peroxidase and guaiacol peroxidase under heat hardening of wheat seedlings. Ukr Biokhim Zh 84:131–138
Konczal M, Koteja P, Stuglik MT, Radwan J, Babik W (2014) Accuracy of allele frequency estimation using pooled RNA-SEq. Mol Ecol Resour 14:381–392. https://doi.org/10.1111/1755-0998.12186
Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349. https://doi.org/10.1093/nar/gkm391
Kregel KC, Moseley PL (1996) Differential effects of exercise and heat stress on liver HSP70 accumulation with aging. J Appl Physiol 80:547–551. https://doi.org/10.1152/jappl.1996.80.2.547
Krones-Herzig A, Mittal S, Yule K, Liang H, English C, Urcis R, Soni T, Adamson ED, Mercola D (2005) Early growth response 1 acts as a tumor suppressor in vivo and in vitro via regulation of p53. Cancer Res 65:5133–5143. https://doi.org/10.1158/0008-5472.CAN-04-3742
Kuan YC, Hashidume T, Shibata T, Uchida K, Shimizu M, Inoue J, Sato R (2017) Heat shock protein 90 modulates lipid homeostasis by regulating the stability and function of sterol regulatory element-binding protein (SREBP) and SREBP cleavage-activating protein. J Biol Chem 292:3016–3028. https://doi.org/10.1074/jbc.M116.767277
Laplante AF, Moulin V, Auger FA, Landry J, Li H, Morrow G, Tanguay RM, Germain L (1998) Expression of heat shock proteins in mouse skin during wound healing. J Histochem Cytochem 46:1291–1301. https://doi.org/10.1177/002215549804601109
Li CW, Wang KC, Luo QY, Tang XL (2012) Effect of exogenous Ca2 + on protective infection of Pinellia ternata and accumulation of major components under high temperature stress. Zhongguo Zhong Yao Za Zhi 37:2875–2878
Liao Y, Shikapwashya ON, Shteyer E, Dieckgraefe BK, Hruz PW, Rudnick DA (2004) Delayed hepatocellular mitotic progression and impaired liver regeneration in early growth response-1-deficient mice. J Biol Chem 279:43107–43116. https://doi.org/10.1074/jbc.M407969200
Lin MF, Jungreis I, Kellis M (2011) PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics 27:i275–i282. https://doi.org/10.1093/bioinformatics/btr209
Lu N, Zang X, Zhang X, Chen H, Feng X, Zhang L (2012) Gene cloning, expression and activity analysis of manganese superoxide dismutase from two strains of Gracilaria lemaneiformis (Gracilariaceae, Rhodophyta) under heat stress. Molecules 17:4522–4532. https://doi.org/10.3390/molecules17044522
Lu Y, Wu Z, Song Z, Xiao P, Liu Y, Zhang P, You F (2016) Insight into the heat resistance of fish via blood: Effects of heat stress on metabolism, oxidative stress and antioxidant response of olive flounder Paralichthys olivaceus and turbot Scophthalmus maximus. Fish Shellfish Immunol 58:125–135. https://doi.org/10.1016/j.fsi.2016.09.008
Ma L, Bajic VB, Zhang Z (2013) On the classification of long non-coding RNAs. RNA Biol 10:924–933. https://doi.org/10.4161/rna.24604
Maher SK, Wojnarowicz P, Ichu TA, Veldhoen N, Lu L, Lesperance M, Propper CR, Helbing CC (2016) Rethinking the biological relationships of the thyroid hormones, l-thyroxine and 3,5,3’-triiodothyronine. Comp Biochem Physiol Part D Genom Proteomics 218:44–53. https://doi.org/10.1016/j.cbd.2016.04.002
Mahjoubi E, Yazdi MH, Aghaziarati N, Noori GR, Afsarian O, Baumgard LH (2015) The effect of cyclical and severe heat stress on growth performance and metabolism in Afshari lambs. J Anim Sci 93:1632–1640. https://doi.org/10.2527/jas.2014-8641
Matthews E Jr, Rahnama-Vaghef A, Eskandari S (2009) Inhibitors of the gamma-aminobutyric acid transporter 1 (GAT1) do not reveal a channel mode of conduction. Neurochem Int 55:732–740. https://doi.org/10.1016/j.neuint.2009.07.005
Matz JM, Blake MJ, Tatelman HM, Lavoi KP, Holbrook NJ (1995) Characterization and regulation of cold-induced heat shock protein expression in mouse brown adipose tissue. Am J Physiol 269:R38–R47. https://doi.org/10.1152/ajpregu.1995.269.1.R38
McManaman JL, Zabaronick W, Schaack J, Orlicky DJ (2003) Lipid droplet targeting domains of adipophilin. J Lipid Res 44:668–673. https://doi.org/10.1194/jlr.C200021-JLR200
Milne C (2000) The history of the Dorper sheep. Small Rumin Res 36:99–102. https://doi.org/10.1016/s0921-4488(99)00154-6
Nadal-Ribelles M, Solé C, Xu Z, Steinmetz LM, de Nadal E, Posas F (2014) Control of Cdc28 CDK1 by a stress-induced lncRNA. Mol Cell 53:549–561. https://doi.org/10.1016/j.molcel.2014.01.006
Nayyar H, Kaur R, Kaur S, Singh R (2014) γ-Aminobutyric acid (GABA) imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J Plant Growth Regul 33:408–419. https://doi.org/10.1007/s00344-013-9389-6
Oliveira JA, Egito AAD, Crispim BDA, Vargas Junior FM, Seno LO, Barufatti A (2020) Importance of naturalized breeds as a base for the formation of exotic sheep (Ovis aries) breeds in tropical altitude regions. Genet Mol Biol 43:e20190054. https://doi.org/10.1590/1678-4685-GMB-2019-0054
Perkel JM (2013) Visiting “noncodarnia”. Biotechniques 54:301–304. https://doi.org/10.2144/000114037
Piehler A, Kaminski WE, Wenzel JJ, Langmann T, Schmitz G (2002) Molecular structure of a novel cholesterol-responsive A subclass ABC transporter, ABCA9. Biochem Biophys Res Commun 295:408–416. https://doi.org/10.1016/s0006-291x(02)00659-9
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301. https://doi.org/10.1093/nar/gkr1065
Rathwa SD, Vasava AA, Pathan MM, Madhira SP, Patel YG, Pande AM (2017) Effect of season on physiological, biochemical, hormonal, and oxidative stress parameters of indigenous sheep. Vet World 10:650–654. https://doi.org/10.14202/vetworld.2017.650-654
Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in drosophila. Experientia 18:571–573. https://doi.org/10.1007/BF02172188
Sano H, Hsu DK, Yu L, Apgar JR, Kuwabara I, Yamanaka T, Hirashima M, Liu FT (2000) Human galectin-3 is a novel chemoattractant for monocytes and macrophages. J Immunol 165:2156–2164. https://doi.org/10.4049/jimmunol.165.4.2156
Shelly M, Mosesson Y, Citri A, Lavi S, Zwang Y, Melamed-Book N, Aroeti B, Yarden Y (2003) Polar expression of ErbB-2/HER2 in epithelia: bimodal regulation by Lin-7. Dev Cell 5:475–486. https://doi.org/10.1016/j.devcel.2003.08.001
Sprake PM, Hubertus C, Bissett WT, Porter BF, Russell KE, Garland T, Young BD, Washburn KE (2013) Neurological disease in lambs associated with exposure to high environmental temperature and humidity. J Vet Intern Med 27:1242–1247. https://doi.org/10.1111/jvim.12157
Sun L, Luo H, Bu D, Zhao G, Yu K, Zhang C, Liu Y, Chen R, Zhao Y (2013) Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res 41:e166. https://doi.org/10.1093/nar/gkt646
Sun Y, Wang G, Ji Z, Chao T, Liu Z, Wang X, Liu G, Wu C, Wang J (2016) Three slow skeletal muscle troponin genes in small-tailed Han sheep (Ovis aries): molecular cloning, characterization and expression analysis. Mol Biol Rep 43:999–1010. https://doi.org/10.1007/s11033-016-4027-6
Tao W, Wu J, Zhang Q, Lai SS, Jiang S, Jiang C, Xu Y, Xue B, Du J, Li CJ (2015) EGR1 regulates hepatic clock gene amplitude by activating Per1 transcription. Sci Rep 5:15212–15212. https://doi.org/10.1038/srep15212
Tishkoff DX, Boerger AL, Bertrand P, Filosi N, Gaida GM, Kane MF, Kolodner RD (1997) Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc Natl Acad Sci U S A 94:7487–7492. https://doi.org/10.1073/pnas.94.14.7487
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. https://doi.org/10.1038/nbt.1621
Wong WM, Gerry AB, Putt W, Roberts JL, Weinberg RB, Humphries SE, Leake DS, Talmud PJ (2007) Common variants of apolipoprotein A-IV differ in their ability to inhibit low density lipoprotein oxidation. Atherosclerosis 192:266–274. https://doi.org/10.1016/j.atherosclerosis.2006.07.017
Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11:441–469. https://doi.org/10.1146/annurev.cb.11.110195.002301
Yan SF, Fujita T, Lu J, Okada K, Shan Zou Y, Mackman N, Pinsky DJ, Stern DM (2000) Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat Med 6:1355–1361. https://doi.org/10.1038/82168
Zhang Y, Han D, Dong X, Wang J, Chen J, Yao Y, Darwish H, Liu W, Deng X (2019) Genome-wide profiling of RNA editing sites in sheep. J Anim Sci Biotechnol 10:31. https://doi.org/10.1186/s40104-019-0331-z
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The authors would like to thank the financial support from the National Natural Science Foundation of China (31360271).
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Procedures involving animals, their care and humane kill were conducted in conformity with Guidelines on the Humane Treatment of Laboratory Animals (HTLA Pub. Chapter 2–6, revised 2006 in China) and were approved by Animal Care and Use Committee of the Inner Mongolia Agricultural University. The written informed consent of experimental research achieved by animal owner was obtained.
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Wang, S., Zhang, D., Zhou, H. et al. Screening of genes coupled to heat response in Mongolian and Dorper sheep breeds. Biologia 76, 949–958 (2021). https://doi.org/10.2478/s11756-020-00616-6
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DOI: https://doi.org/10.2478/s11756-020-00616-6