DOI QR코드

DOI QR Code

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)
  • 투고 : 2022.03.24
  • 심사 : 2022.06.28
  • 발행 : 2022.11.01

초록

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.

키워드

과제정보

This work was supported by the National Natural Science Foundation of China (no. 31460582, no. 31760659 and no. 32260822) and the Natural Science Foundation Key Project of Yunnan Province, China (no. 2014FA032 and no. 2007C0003Z).

참고문헌

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. Bartolomei MS, Zemel S, Tilghman SM. Parental imprinting of the mouse h19 gene. Nature 1991;351:153-5. https://doi.org/10.1038/351153a0
  8. 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
  9. 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
  10. 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
  11. Scherf BD. World watch list for domestic animal diversity. Rome, Italy: Food and Agriculture Organization (FAO); 2000.
  12. 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
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. Macias H, Hinck L. Mammary gland development. Wiley Interdiscip Rev Dev Biol 2012;1:533-57. https://doi.org/10.1002/wdev.35
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. 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
  41. 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
  42. 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
  43. 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
  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