Browse > Article
http://dx.doi.org/10.5713/ab.22.0120

Genome-wide identification of long noncoding RNA genes and their potential association with mammary gland development in water buffalo  

Jin, Yuhan (Faculty of Animal Science and Technology, Yunnan Agricultural University)
Ouyang, Yina (Faculty of Animal Science and Technology, Yunnan Agricultural University)
Fan, Xinyang (Faculty of Animal Science and Technology, Yunnan Agricultural University)
Huang, Jing (Faculty of Animal Science and Technology, Yunnan Agricultural University)
Guo, Wenbo (Faculty of Animal Science and Technology, Yunnan Agricultural University)
Miao, Yongwang (Faculty of Animal Science and Technology, Yunnan Agricultural University)
Publication Information
Animal Bioscience / v.35, no.11, 2022 , pp. 1656-1665 More about this Journal
Abstract
Objective: Water buffalo, an important domestic animal in tropical and subtropical regions, play an important role in agricultural economy. It is an important source for milk, meat, horns, skin, and draft power, especially its rich milk that is the great source of cream, butter, yogurt, and many cheeses. In recent years, long noncoding RNAs (lncRNAs) have been reported to play pivotal roles in many biological processes. Previous studies for the mammary gland development of water buffalo mainly focus on protein coding genes. However, lncRNAs of water buffalo remain poorly understood, and the regulation relationship between mammary gland development/milk production traits and lncRNA expression is also unclear. Methods: Here, we sequenced 22 samples of the milk somatic cells from three lactation stages and integrated the current annotation and identified 7,962 lncRNA genes. Results: By comparing the lncRNA genes of the water buffalo in the early, peak, and late different lactation stages, we found that lncRNA gene lnc-bbug14207 displayed significantly different expression between early and late lactation stages. And lnc-bbug14207 may regulate neighboring milk fat globule-EGF factor 8 (MFG-E8) and hyaluronan and proteoglycan link protein 3 (HAPLN3) protein coding genes, which are vital for mammary gland development. Conclusion: This study provides the first genome-wide identification of water buffalo lncRNAs and unveils the potential lncRNAs that impact mammary gland development.
Keywords
Lactation Stages; lnc-bbug14207; LncRNAs Identification; Mammary Gland Development; RNA-seq; Water Buffalo;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Hung T, Wang Y, Lin MF, et al. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet 2011;43:621-29. https://doi.org/10.1038/ng.848   DOI
2 Bhan A, Soleimani M, Mandal SS. Long noncoding RNA and cancer: A new paradigm. Cancer Res 2017; 77:3965-81. https://doi.org/10.1158/0008-5472.CAN-16-2634   DOI
3 Bartolomei MS, Zemel S, Tilghman SM. Parental imprinting of the mouse h19 gene. Nature 1991;351:153-5. https://doi.org/10.1038/351153a0   DOI
4 Zhou ZY, Li AM, Adeola AC, et al. Genome-wide identification of long intergenic noncoding RNA genes and their potential association with domestication in pigs. Genome Biol Evol 2014;6:1387-92. https://doi.org/10.1093/gbe/evu113   DOI
5 Zheng X, Ning C, Zhao P, et al. Integrated analysis of long noncoding RNA and mRNA expression profiles reveals the potential role of long noncoding RNA in different bovine lactation stages. J Dairy Sci 2018;101:11061-73. https://doi.org/10.3168/jds.2018-14900   DOI
6 Cai W, Li C, Liu S, et al. Genome wide identification of novel long non-coding rnas and their potential associations with milk proteins in chinese holstein cows. Front Genet 2018;9:281. https://doi.org/10.3389/fgene.2018.00281   DOI
7 Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using david bioinformatics resources. Nat Protoc 2009;4:44-57. https://doi.org/10.1038/nprot.2008.211   DOI
8 Wang KC, Yang YW, Liu B, et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 2011;472:120-24. https://doi.org/10.1038/nature09819   DOI
9 Atabai K, Fernandez R, Huang X, et al. Mfge8 is critical for mammary gland remodeling during involution. Mol Biol Cell 2005;16:5528-37. https://doi.org/10.1091/mbc.e05-02-0128   DOI
10 Macias H, Hinck L. Mammary gland development. Wiley Interdiscip Rev Dev Biol 2012;1:533-57. https://doi.org/10.1002/wdev.35   DOI
11 Lu Q, Chen Z, Ji D, et al. Progress on the regulation of ruminant milk fat by noncoding RNAs and cernas. Front Genet 2021;12:733925. https://doi.org/10.3389/fgene.2021.733925   DOI
12 Hanayama R, Tanaka M, Miyasaka K, et al. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 2004;304:1147-50. https://doi.org/10.1126/science.1094359   DOI
13 Matsuda A, Jacob A, Wu R, et al. Novel therapeutic targets for sepsis: regulation of exaggerated inflammatory responses. J Nippon Med Sch 2012;79:4-18. https://doi.org/10.1272/jnms.79.4   DOI
14 Sandhu GK, Milevskiy MJG, Wilson W, Shewan AM, Brown MA. Non-coding rnas in mammary gland development and disease. Adv Exp Med Biol 2016;886:121-53. In: Wilhelm D, Bernard P, editors. Non-coding RNA and the reproductive system. Advances in experimental medicine and biology, vol 886. Dordrecht, The Netherlands: Springer; 2016. https://doi.org/10.1007/978-94-017-7417-8_7   DOI
15 Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010;11:R106. https://doi.org/10.1186/gb-2010-11-10-r106   DOI
16 Canovas A, Rincon G, Bevilacqua C, et al. Comparison of five different RNA sources to examine the lactating bovine mammary gland transcriptome using rna-sequencing. Sci Rep 2014;4:5297. https://doi.org/10.1038/srep05297   DOI
17 Stubbs JD, Lekutis C, Singer KL, Parry G. cDNA cloning of a mouse mammary epithelial cell surface protein reveals the existence of epidermal growth factor-like domains linked to factor viii-like sequences. Proc Natl Acad Sci USA 1990;87:8417-21. https://doi.org/10.1073/pnas.87.21.8417   DOI
18 Hanayama R, Tanaka M, Miyasaka K, et al. Autoimmune disease and impaired uptake of apoptotic cells in mfg-e8-deficient mice. Science 2004;304:1147-50. https://doi.org/10.1126/science.1094359   DOI
19 Ensslin MA, Shur BD. The egf repeat and discoidin domain protein, sed1/mfg-e8, is required for mammary gland branching morphogenesis. Proc Natl Acad Sci USA 2007;104:2715-20. https://doi.org/10.1073/pnas.0610296104   DOI
20 Spicer AP, Joo A, Bowling RA, Jr. A hyaluronan binding link protein gene family whose members are physically linked adjacent to chrondroitin sulfate proteoglycan core protein genes: the missing links. J Biol Chem 2003;278:21083-91. https://doi.org/10.1074/jbc.M213100200   DOI
21 Oshima K, Aoki N, Kato T, Kitajima K, Matsuda T. Secretion of a peripheral membrane protein, MFG-E8, as a complex with membrane vesicles. Eur J Biochem 2002;269:1209-18. https://doi.org/10.1046/j.1432-1033.2002.02758.x   DOI
22 Ravichandran K, Lorenz U. Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol 2007;7:964-74. https://doi.org/10.1038/nri2214   DOI
23 Bogu GK, Vizan P, Stanton LW, Beato M, Di Croce L, MartiRenom MA. Chromatin and RNA maps reveal regulatory long noncoding RNAs in mouse. Mol Cell Biol 2016;36: 809-19. https://doi.org/10.1128/MCB.00955-15   DOI
24 Kern C, Wang Y, Chitwood J, et al. Genome-wide identification of tissue-specific long non-coding RNA in three farm animal species. BMC Genomics 2018;19:684. https://doi.org/10.1186/s12864-018-5037-7   DOI
25 Cui X, Hou Y, Yang S, et al. Transcriptional profiling of mammary gland in holstein cows with extremely different milk protein and fat percentage using rna sequencing. BMC Genomics 2014;15:226. https://doi.org/10.1186/1471-2164-15-226   DOI
26 Bu HF, Zuo XL, Wang X, et al. Milk fat globule-EGF factor 8/lactadherin plays a crucial role in maintenance and repair of murine intestinal epithelium. J Clin Invest 2007;117:3673-83. https://doi.org/10.1172/JCI31841   DOI
27 Rangel LBA, Sherman-Baust CA, Wernyj RP, Schwartz DR, Cho KR, Morin PJ. Characterization of novel human ovarian cancer-specific transcripts (HOSTs) identified by serial analysis of gene expression. Oncogene 2003;22:7225-32. https://doi.org/10.1038/sj.onc.1207008   DOI
28 Ahmad S, Gaucher I, Rousseau F, et al. Effects of acidification on physico-chemical characteristics of buffalo milk: A comparison with cow's milk. Food Chem 2008;106:11-7. https://doi.org/10.1016/j.foodchem.2007.04.021   DOI
29 Iyer MK, Niknafs YS, Malik R, et al. The landscape of long noncoding rnas in the human transcriptome. Nat Genet 2015;47:199-208. https://doi.org/10.1038/ng.3192   DOI
30 Orom UA, Derrien T, Beringer M, et al. Long noncoding rnas with enhancer-like function in human cells. Cell 2010; 143:46-58. https://doi.org/10.1016/j.cell.2010.09.001   DOI
31 Wu CF, Liu LX, Huo JL, et al. Isolation, bioinformatic analysis and tissue expression profile of a novel water buffalo gene MFG-E8. Arch Anim Breed 2013;56:833-41. https://doi.org/10.7482/0003-9438-56-083   DOI
32 Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. Tophat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013;14:R36. https://doi.org/10.1186/gb-2013-14-4-r36   DOI
33 Scherf BD. World watch list for domestic animal diversity. Rome, Italy: Food and Agriculture Organization (FAO); 2000.
34 Huarte M, Guttman M, Feldser D, et al. A large intergenic noncoding rna induced by p53 mediates global gene repression in the p53 response. Cell 2010;142:409-19. https://doi.org/10.1016/j.cell.2010.06.040   DOI
35 Xu Z, Zuo Z, Dong D, et al. Downregulated lncRNA UCA1 accelerates proliferation and migration of vascular smooth muscle cells by epigenetic regulation of MMP9. Exp Ther Med 2020;19:3589-94. https://doi.org/10.3892/etm.2020.8639   DOI
36 Guttman M, Donaghey J, Carey BW, et al. LincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011;477:295-300. https://doi.org/10.1038/nature10398   DOI
37 Li J, Liu J, Liu S, et al. Genome-wide association study for buffalo mammary gland morphology. J Dairy Res 2020;87: 27-31. https://doi.org/10.1017/s0022029919000967   DOI
38 Carrascosa C, Obula R, Missiaglia E, et al. MFG-E8/lactadherin regulates cyclins D1/D3 expression and enhances the tumorigenic potential of mammary epithelial cells. Oncogene 2012;31:1521-32. https://doi.org/10.1038/onc.2011.356   DOI
39 Spicer AP, Joo A, Bowling RA. A hyaluronan binding link protein gene family whose members are physically linked adjacent to chrondroitin sulfate proteoglycan core protein genes. J Biol Chem 2003;278:21083-91. https://doi.org/10.1074/jbc.M213100200   DOI
40 Low WY, Tearle R, Bickhart DM, et al. Chromosome-level assembly of the water buffalo genome surpasses human and goat genomes in sequence contiguity. Nat Commun 2019; 10:260. https://doi.org/10.1038/s41467-018-08260-0   DOI
41 Boutinaud M, Rulquin H, Keisler DH, Djiane J, Jammes H. Use of somatic cells from goat milk for dynamic studies of gene expression in the mammary gland. J Anim Sci 2002; 80:1258-69. https://doi.org/10.2527/2002.8051258x   DOI
42 Trapnell C, Williams BA, Pertea G, et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010;28:511-5. https://doi.org/10.1038/nbt.1621   DOI
43 Kang YJ, Yang DC, Kong L, et al. Cpc2: A fast and accurate coding potential calculator based on sequence intrinsic features. Nucleic Acids Res 2017;45:W12-6. https://doi.org/10.1093/nar/gkx428   DOI
44 Kuo SJ, Chien SY, Lin C, et al. Significant elevation of CLDN16 and HAPLN3 gene expression in human breast cancer. Oncol Rep 2010;24:759-66. https://doi.org/10.3892/or_00000918   DOI