Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Long non-coding RNAs in Sus scrofa ileum under starvation stress

  • Wang, Shu (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Ma, Yi Jia (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Li, Yong Shi (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Ge, Xu Sheng (Inner Mongolia Mengniu Dairy(GROUP) CO., LTD) ;
  • Lu, Chang (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Cai, Chun Bo (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Yang, Yang (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Zhao, Yan (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Liang, Guo Ming (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Guo, Xiao Hong (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Cao, Guo Qing (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Li, Bu Gao (Department of Animal Sciences, Shanxi Agricultural University) ;
  • Gao, Peng Fei (Department of Animal Sciences, Shanxi Agricultural University)
  • Received : 2021.10.26
  • Accepted : 2022.02.04
  • Published : 2022.07.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: In this study, we aimed to identify long non-coding RNAs (lncRNAs) that play important roles in starvation stress, analyze their functions, and discover potential molecular targets to alleviate starvation stress to provide a theoretical reference for subsequent in-depth research. Methods: We generated a piglet starvation stress animal model. Nine Yorkshire weaned piglets were randomly divided into a long-term starvation stress group (starved for 72 h), short-term starvation stress group (starved for 48 h), and the control group. LncRNA libraries were constructed using high-throughput sequencing of piglet ileums. Results: We obtained 11,792 lncRNAs, among which, 2,500 lncRNAs were novel. In total, 509 differentially expressed (DE)lncRNAs were identified in this study. Target genes of DElncRNAs were predicted via cis and trans interactions, and functional and pathway analyses were performed. Gene ontology functions and Kyoto encyclopedia of genes and genomes analysis revealed that lncRNA-targeted genes mainly participated in metabolic pathways, cellular processes, immune system processes, digestive systems, and transport activities. To reveal the mechanism underlying starvation stress, the interaction network between lncRNAs and their targets was constructed based on 26 DElncRNAs and 72 DEmRNAs. We performed an interaction network analysis of 121 DElncRNA-DEmRNA pairs with a Pearson correlation coefficient greater than 0.99. Conclusion: We found that MSTRG.19894.13, MSTRG.16726.3, and MSTRG.12176.1 might play important roles in starvation stress. This study not only generated a library of enriched lncRNAs in piglets, but its outcomes also provide a strong foundation to screen key lncRNAs involved in starvation stress and a reference for subsequent in-depth research.

Keywords

Acknowledgement

We would like to thank all the staff of Gene Denovo Biotechnology Co. for technical help and Editage 360 (www.editage.cn) for English language editing during the preparation of this manuscript.

References

  1. Bluher M. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol 2019;15:288-98. https://doi.org/10.1038/s41574-019-0176-8
  2. Yan T, Xiao R, Wang N, Shang R, Lin G. Obesity and severe coronavirus disease 2019: molecular mechanisms, paths forward, and therapeutic opportunities. Theranostics 2021;11:8234-53. https://doi.org/10.7150/thno.59293
  3. Wardzinski E, Hyzy C, Duysen K, Melchert UH, Jauch-Chara K, Oltmanns KM. Hypocaloric dieting unsettles the neuroenergetic homeostasis in humans. Nutrients 2021;13:3433. https://doi.org/10.3390/nu13103433
  4. Varady K, Cienfuegos S, Ezpeleta M, Gabel K. Cardiometabolic benefits of intermittent fasting. Ann Rev Nutr 2021;41:333-61. https://doi.org/10.1146/annurev-nutr-052020-041327
  5. Lee SR, Ko TH, Kim HK, et al. Influence of starvation on heart contractility and corticosterone level in rats. Pflugers Arch 2015;467:2351-60. https://doi.org/10.1007/s00424-015-1701-9
  6. Martinez KB, Pierre JF, Chang EB. The gut microbiota: the gateway to improved metabolism. Gastroenterol Clin North Am 2016;45:601-14. https://doi.org/10.1016/j.gtc.2016.07.001
  7. Christian VJ, Miller KR, Martindale RG. Food insecurity, malnutrition, and the microbiome. Curr Nutr Rep 2020;9:356-60. https://doi.org/10.1007/s13668-020-00342-0
  8. Kazimierczyk M, Kasprowicz M, Kasprzyk M, Wrzesinski J. Human long noncoding RNA interactome: detection, characterization and function. Int J Mol Sci 2020;21:1027. https://doi.org/10.3390/ijms21031027
  9. Zhang X, Hong R, Chen W, Xu M, Wang L. The role of long noncoding RNA in major human disease. Bioorg Chem 2019;92:103214. https://doi.org/10.1016/j.bioorg.2019.103214
  10. Zou T, Jaladanki SK, Liu L, et al. H19 long noncoding RNA regulates intestinal epithelial barrier function via MicroRNA 675 by interacting with RNA-binding protein HuR. Mol Cell Biol 2016;36:1332-41. https://doi.org/10.1128/mcb.01030-15
  11. Xiao L, Wu J, Wang JY, et al. Long noncoding RNA uc.173 promotes renewal of the intestinal mucosa by inducing degradation of microRNA 195. Gastroenterology 2018;154:599-611. https://doi.org/10.1053/j.gastro.2017.10.009
  12. Wu F, Huang Y, Dong F, Kwon J. Ulcerative colitis-associated long noncoding RNA, BC012900, regulates intestinal epithelial cell apoptosis. Inflamm Bowel Dis 2016;22:782-95. https://doi.org/10.1097/mib.0000000000000691
  13. Raychaudhuri S, Fan S, Kraus O, Shahinozzaman M, Obanda DN. Kale supplementation during high fat feeding improves metabolic health in a mouse model of obesity and insulin resistance. PloS one 2021;16:e0256348. https://doi.org/10.1371/journal.pone.0256348
  14. DeBry RW, Seldin MF. Human/mouse homology relationships. Genomics 1996;33:337-51. https://doi.org/10.1006/geno.1996.0209
  15. Schook LB, Collares TV, Darfour-Oduro KA, et al. Unraveling the swine genome: implications for human health. Annu Rev Anim Biosci 2015;3:219-44. https://doi.org/10.1146/annurevanimal-022114-110815
  16. Fouhse JM, Dawson K, Graugnard D, Dyck M, Willing BP. Dietary supplementation of weaned piglets with a yeast-derived mannan-rich fraction modulates cecal microbial profiles, jejunal morphology and gene expression. Animal 2019;13:1591-8. https://doi.org/10.1017/s1751731118003361
  17. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics (Oxford, England) 2018;34:i884-i90. https://doi.org/10.1093/bioinformatics/bty560
  18. Langmead B, Salzberg S. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9:357-9. https://doi.org/10.1038/nmeth.1923
  19. Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005;102:15545-50. https://doi.org/10.1073/pnas.0506580102
  20. Cipriano A, Macino M, Buonaiuto G, et al. Wnt7bEpigenetic regulation of expression by the -acting long noncoding RNA Lnc-Rewind in muscle stem cells. eLife 2021;10:e54782. https://doi.org/10.7554/eLife.54782
  21. Cai B, Li Z, Ma M, et al. Six1LncRNA-Six1 encodes a micro-peptide to activate in and is involved in cell proliferation and muscle growth. Front Physiol 2017;8:230. https://doi.org/10.3389/fphys.2017.00230
  22. Li J, Gao Z, Wang X, et al. Identification and functional analysis of long intergenic noncoding RNA genes in porcine preimplantation embryonic development. Sci Rep 2016;6:38333. https://doi.org/10.1038/srep38333
  23. Jayakumar T, Chang CC, Lin SL, et al. Brazilin ameliorates high glucose-induced vascular inflammation via inhibiting ROS and CAMs production in human umbilical vein endothelial cells. Biomed Res Int 2014;2014:403703. https://doi.org/10.1155/2014/403703
  24. Phillips IR, Shephard EA. Drug metabolism by flavin-containing monooxygenases of human and mouse. Expert Opin Drug Metab Toxicol 2017;13:167-81. https://doi.org/10.1080/17425255.2017.1239718
  25. Matsunaga T, Endo S, Maeda S, et al. Characterization of human DHRS4: an inducible short-chain dehydrogenase/reductase enzyme with 3beta-hydroxysteroid dehydrogenase activity. Arch Biochem Biophys 2008;477:339-47. https://doi.org/10.1016/j.abb.2008.06.002
  26. Yamada T, Komoto J, Kasuya T, et al. A catalytic mechanism that explains a low catalytic activity of serine dehydratase like-1 from human cancer cells: crystal structure and site-directed mutagenesis studies. Biochim Biophys Acta 2008;1780:809-18. https://doi.org/10.1016/j.bbagen.2008.01.020
  27. Spicer AP, Kaback LA, Smith TJ, Seldin MF. Molecular cloning and characterization of the human and mouse UDP-glucose dehydrogenase genes. J Biol Chem 1998;273:25117-24. https://doi.org/10.1074/jbc.273.39.25117
  28. Zimmer BM, Barycki JJ, Simpson MA. Integration of sugar metabolism and proteoglycan synthesis by UDP-glucose dehydrogenase. J Histochem Cytochem 2021;69:13-23. https://doi.org/10.1369/0022155420947500
  29. Guaman L, Oliveira-Filho E, Barba-Ostria C, et al. xylA and xylB overexpression as a successful strategy for improving xylose utilization and poly-3-hydroxybutyrate production in Burkholderia sacchari. J Ind Microbiol Biotechnol 2018;45:165-73. https://doi.org/10.1007/s10295-018-2007-7
  30. Alzeer S, Ellis E. Metabolism of gamma hydroxybutyrate in human hepatoma HepG2 cells by the aldo-keto reductase AKR1A1. Biochem Pharmacol 2014;92:499-505. https://doi.org/10.1016/j.bcp.2014.09.004
  31. Ursini F, Abenavoli L. The emerging role of complement C3 as a biomarker of insulin resistance and cardiometabolic diseases: preclinical and clinical evidence. Rev Recent Clin Trials 2018;13:61-8. https://doi.org/10.2174/1574887112666171128134552
  32. Garcia-Gen E, Penades M, Merida S, et al. High myopia and the complement system: factor h in myopic maculopathy. J Clin Med 2021;10:2600. https://doi.org/10.3390/jcm10122600
  33. Wang LK, Yue HL, Peng XJ, Zhang SJ. GSTO1 regards as a meritorious regulator in cutaneous malignant melanoma cells. Mol Cell Probes 2019;48:101449. https://doi.org/10.1016/j.mcp.2019.101449
  34. Ciciro Y, Sala A. MYB oncoproteins: emerging players and potential therapeutic targets in human cancer. Oncogenesis 2021;10:19. https://doi.org/10.1038/s41389-021-00309-y
  35. Zeng B, Wang H, Luo J, et al. Porcine milk-derived small extracellular vesicles promote intestinal immunoglobulin production through pIgR. Animals 2021;11:1522. https://doi.org/10.3390/ani11061522
  36. Xu B, Deng C, Wu X, et al. CCR9 and CCL25: A review of their roles in tumor promotion. J Cell Physiol 2020;235:9121-32. https://doi.org/10.1002/jcp.29782
  37. Asgari-Karchekani S, Karimian M, Mazoochi T, Taheri M, Khamehchian T. CDX2 protein expression in colorectal cancer and itscorrelation with clinical and pathological characteristics, prognosis, and survival rate of patients. J Gastrointest Cancer 2020;51:844-9. https://doi.org/10.1007/s12029-019-00314-w
  38. Daude N, Gallaher TK, Zeschnigk M, et al. Molecular cloning, characterization, and mapping of a full-length cDNA encoding human UDP-galactose 4'-epimerase. Biochem Mol Med 1995;56:1-7. https://doi.org/10.1006/bmme.1995.1048
  39. He XX, Luo SS, Qin HQ, Mo XW. MicroRNA-766-3p-mediated downregulation of HNF4G inhibits proliferation in colorectal cancer cells through the PI3K/AKT pathway. Cancer Gene Ther 2021. https://doi.org/10.1038/s41417-021-00362-0
  40. Keller N, Mendoza-Ferreira N, Maroofian R, et al. Hereditary polyneuropathy with optic atrophy due to PDXK variant leading to impaired Vitamin B6 metabolism. Neuromuscul Disord 2020;30:583-9. https://doi.org/10.1016/j.nmd.2020.04.004
  41. Rimessi A, Bezzerri V, Salvatori F, et al. PLCB3 loss of function reduces pseudomonas aeruginosa-dependent IL-8 release in cystic fibrosis. Am J Respir Cell Mol Biol 2018;59:428-36. https://doi.org/10.1165/rcmb.2017-0267OC
  42. Jeon H, Kang SK, Lee MJ, et al. Rab27b regulates extracellular vesicle production in cells infected with Kaposi's sarcoma-associated herpesvirus to promote cell survival and persistent infection. J Microbiol (Seoul, Korea) 2021;59:522-9. https://doi.org/10.1007/s12275-021-1108-6
  43. Zwarts I, van Zutphen T, Kruit JK, et al. Identification of the fructose transporter GLUT5 (SLC2A5) as a novel target of nuclear receptor LXR. Sci Rep 2019;9:9299. https://doi.org/10.1038/s41598-019-45803-x
  44. Dhir G, Li D, Hakonarson H, Levine MA. Late-onset hereditary hypophosphatemic rickets with hypercalciuria (HHRH) due to mutation of SLC34A3/NPT2c. Bone 2017;97:15-9. https://doi.org/10.1016/j.bone.2016.12.001