Integrated analysis of miRNA and mRNA paired expression profiling of prenatal skeletal muscle development in three genotype pigs

Scientific Reports

Volumn 5, Issue 1, 2015, Pages

  Tang, Zhonglin ^a   Yang, Yalan ^a   Wang, Zishuai ^a   Zhao, Shuanping ^a,b   Mu, Yulian ^a   Li, Kui ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b RICE RESEARCH INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA;

ANIMAL; EMBRYOLOGY; FETUS DEVELOPMENT; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENETICS; GENOTYPE; METABOLISM; MUSCLE DEVELOPMENT; PHYSIOLOGY; PIG; SKELETAL MUSCLE;

ANIMALS; FETAL DEVELOPMENT; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENOTYPE; MICRORNAS; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; RNA, MESSENGER; SUS SCROFA;

EID: 85008398719     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/SREP15544     Document Type: Article

References (84)

1. Brennecke, J., Hipfner, D. R., Stark, A., Russell, R. B. & Cohen, S. M. Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113, 25–36 (2003).
2. Xu, P. Z., Vernooy, S. Y., Guo, M. & Hay, B. A. The Drosophila MicroRNA mir-14 suppresses cell death and is required for normal fat metabolism. Curr Biol 13, 790–795 (2003).
3. Brennecke, J., Stark, A. & Cohen, S. M. Not miR-ly muscular: microRNAs and muscle development. Gene Dev 19, 2261–2264 (2005).
4. Giraldez, A. J. et al. MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833–838 (2005).
5. Chen, C. Z., Li, L., Lodish, H. F. & Bartel, D. P. MicroRNAs modulate hematopoietic lineage differentiation. Science 303, 83–86 (2004).
6. Rajewsky, N. MicroRNA target predictions in animals. Nat Genet 38, S8–S13 (2006).
7. Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20 (2005).
8. Krek, A. et al. Combinatorial microRNA target predictions. Nat Genet 37, 495–500 (2005).
9. Betel, D., Wilson, M., Gabow, A., Marks, D. S. & Sander, C. The microRNA. org resource: targets and expression. Nucleic Acids Res 36, D149–D153 (2008).
10. Sethupathy, P., Megraw, M. & Hatzigeorgiou, A. G. A guide through present computational approaches for the identification of mammalian microRNA targets. Nat Methods 3, 881–886 (2006).
11. Selbach, M. et al. Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58–63 (2008).
12. Farh, K. K.-H. et al. The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310, 1817–1821 (2005).
13. Stark, A., Brennecke, J., Bushati, N., Russell, R. B. & Cohen, S. M. Animal microRNAs confer robustness to gene expression and have a significant impact on 3′UTR evolution. Cell 123, 1133–1146 (2005).
14. Huang, J. C. et al. Using expression profiling data to identify human microRNA targets. Nat Methods 4, 1045–1049 (2007).
15. Ruike, Y. et al. Global correlation analysis for micro-RNA and mRNA expression profiles in human cell lines. J Hum Genet 53, 515–523 (2008).
16. Tian, Z., Greene, A. S., Pietrusz, J. L., Matus, I. R. & Liang, M. MicroRNA–target pairs in the rat kidney identified by microRNA microarray, proteomic, and bioinformatic analysis. Genome Res 18, 404–411 (2008).
17. Gennarino, V. A. et al. MicroRNA target prediction by expression analysis of host genes. Genome Res 19, 481–490 (2009).
18. Van der Auwera, I. et al. Integrated miRNA and mRNA expression profiling of the inflammatory breast cancer subtype. Brit J Cancer 103, 532–541 (2010).
19. Shah, M. S. et al. Integrated microRNA and mRNA expression profiling in a rat colon carcinogenesis model: effect of a chemo-protective diet. Physiol Genomics 43, 640–654 (2011).
20. Anderson, C., Catoe, H. & Werner, R. MIR-206 regulates connexin43 expression during skeletal muscle development. Nucleic Acids Res 34, 5863–5871 (2006).
21. Chen, J.-F. et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38, 228–233 (2006).
22. Yin, H. et al. MicroRNA-133 controls brown adipose determination in skeletal muscle satellite cells by targeting Prdm16. Cell Metab 17, 210–224 (2013).
23. Sun, Q. et al. Transforming growth factor-β-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res 36, 2690–2699 (2008).
24. Williams, A. H., Liu, N., van Rooij, E. & Olson, E. N. MicroRNA control of muscle development and disease. Curr Opin Cell Biol 21, 461–469 (2009).
25. Townley-Tilson, W. D., Callis, T. E. & Wang, D. MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. Int J Biochem Cell Biol 42, 1252–1255 (2010).
26. Li, T., Wu, R., Zhang, Y. & Zhu, D. A systematic analysis of the skeletal muscle miRNA transcriptome of chicken varieties with divergent skeletal muscle growth identifies novel miRNAs and differentially expressed miRNAs. BMC Genomics 12, 186 (2011).
27. Liu, N. et al. MicroRNA-206 promotes skeletal muscle regeneration and delays progression of Duchenne muscular dystrophy in mice. J Clin Invest 122, 2054–2065 (2012).
28. Wei, W. et al. miR-29 targets Akt3 to reduce proliferation and facilitate differentiation of myoblasts in skeletal muscle development. Cell Death Dis 4, e668 (2013).
29. Yang, Y. et al. Wnt antagonist, secreted frizzled-related protein 1, is involved in prenatal skeletal muscle development and is a target of miRNA-1/206 in pigs. BMC Mol Biol 16, 4 (2015).
30. Kim, H. K., Lee, Y. S., Sivaprasad, U., Malhotra, A. & Dutta, A. Muscle-specific microRNA miR-206 promotes muscle differentiation. J Cell Biol 174, 677–687 (2006).
31. Rao, P. K., Kumar, R. M., Farkhondeh, M., Baskerville, S. & Lodish, H. F. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci 103, 8721–8726 (2006).
32. Liu, N. et al. An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc Natl Acad Sci 104, 20844–20849 (2007).
33. Sweetman, D. et al. Specific requirements of MRFs for the expression of muscle specific microRNAs, miR-1, miR-206 and miR-133. Dev Biol 321, 491–499 (2008).
34. Katta, A. et al. Overload induced heat shock proteins (HSPs), MAPK and miRNA (miR-1 and miR133a) response in insulin-resistant skeletal muscle. Cell Physiol Biochem 31, 219–229 (2013).
35. Koutsoulidou, A., Mastroyiannopoulos, N. P., Furling, D., Uney, J. B. & Phylactou, L. A. Expression of miR-1, miR-133a, miR-133b and miR-206 increases during development of human skeletal muscle. BMC Dev Biol 11, 34 (2011).
36. Zhao, Y., Samal, E. & Srivastava, D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436, 214–220 (2005).
37. Sokol, N. S. & Ambros, V. Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Gene Dev 19, 2343–2354 (2005).
38. Goljanek-Whysall, K. et al. Regulation of multiple target genes by miR-1 and miR-206 is pivotal for C2C12 myoblast differentiation. J Cell Sci 125, 3590–3600 (2012).
39. Zhang, J., Ying, Z., Tang, Z., Long, L. & Li, K. MicroRNA-148a promotes myogenic differentiation by targeting the ROCK1 gene. J Biol Chem 287, 21093–21101 (2012).
40. Ludolph, D. C. & Konieczny, S. Transcription factor families: muscling in on the myogenic program. Faseb J 9, 1595–1604 (1995).
41. Muráni, E., Murániová, M., Ponsuksili, S., Schellander, K. & Wimmers, K. Identification of genes differentially expressed during prenatal development of skeletal muscle in two pig breeds differing in muscularity. BMC Dev Biol 7, 109 (2007).
42. Rehfeldt, C., Fiedler, I., Dietl, G. & Ender, K. Myogenesis and postnatal skeletal muscle cell growth as influenced by selection. Livest Prod Sci 66, 177–188 (2000).
43. Foxcroft, G. et al. The biological basis for prenatal programming of postnatal performance in pigs. J Anim Sci 84, E105–E112 (2006).
44. Perry, R. & Rudnick, M. A. Molecular mechanisms regulating myogenic determination and differentiation. Front Biosci 5, 148 (2000).
45. Te Pas, M. F. et al. Transcriptome expression profiles in prenatal pigs in relation to myogenesis. J Muscle Res Cell M 26, 157–165 (2005).
46. Tang, Z. et al. LongSAGE analysis of skeletal muscle at three prenatal stages in Tongcheng and Landrace pigs. Genome Biol 8, R115 (2007).
47. Vodička, P. et al. The miniature pig as an animal model in biomedical research. Ann Ny Acad Sci 1049, 161–171 (2005).
48. Ibrahim, Z. et al. Selected physiologic compatibilities and incompatibilities between human and porcine organ systems. Xenotransplantation 13, 488–499 (2006).
49. Lunney, J. K. Advances in swine biomedical model genomics. Int J Biol Sci 3, 179 (2007).
50. Critser, J. K., Laughlin, M. H., Prather, R. S. & Riley, L. K. Proceedings of the conference on swine in biomedical research. ILAR Journal 50, 89–94 (2009).
51. Ferenc, K. et al. Intrauterine growth retarded piglet as a model for humans–Studies on the perinatal development of the gut structure and function. Reprod Biol 14, 51–60 (2014).
52. Bendixen, E., Danielsen, M., Larsen, K. & Bendixen, C. Advances in porcine genomics and proteomics—a toolbox for developing the pig as a model organism for molecular biomedical research. Briefings in Functional Genomics 9, 208–219 (2010).
53. Womack, J. E. Advances in livestock genomics: opening the barn door. Genome Res 15, 1699–1705 (2005).
54. Huang, Q., Xu, H., Yu, Z., Gao, P. & Liu, S. Inbred Chinese Wuzhishan (WZS) minipig model for soybean glycinin and β-conglycinin allergy. J Agr Food Chem 58, 5194–5198 (2010).
55. Wang, X. et al. Genetic characteristics of inbred Wuzhishan miniature pigs, a native Chinese breed. J Reprod Develop 52, 639–643 (2006).
56. Ponsuksili, S. et al. Correlated mRNAs and miRNAs from co-expression and regulatory networks affect porcine muscle and finally meat properties. BMC Genomics 14, 533 (2013).
57. Ponsuksili, S. et al. Identification of Common Regulators of Genes in Co-Expression Networks Affecting Muscle and Meat Properties. PLoS One 10, e0123678 (2015).
58. Capozza, F. et al. Muscle-specific interaction of caveolin isoforms: differential complex formation between caveolins in fibroblastic vs. muscle cells. Am J Physiol-cell Ph 288, C677–C691 (2005).
59. Van Laere, A. S. et al. A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature 425, 832–836 (2003).
60. Fukawa, T. et al. DDX31 regulates the p53-HDM2 pathway and rRNA gene transcription through its interaction with NPM1 in renal cell carcinomas. Cancer Res 72, 5867–5877 (2012).
61. Vock, C., Döring, F. & Nitz, I. Transcriptional regulation of HMG-CoA synthase and HMG-CoA reductase genes by human ACBP. Cell Physiol Biochem 22, 515–524 (2008).
62. Lin, C. T., Lin, Y. T. & Kuo, T. F. Investigation of mRNA expression for secreted frizzled-related protein 2 (sFRP2) in chick embryos. J Reprod Develop 53, 801–810 (2007).
63. Strmecki, L., Hudler, P., Benedik-Dolničar, M. & Komel, R. De novo mutation in DMD gene in a patient with combined hemophilia A and Duchenne muscular dystrophy. Int J Hematol 99, 184–187 (2014).
64. Hayashi, Y. K. et al. Mutations in the integrin α7 gene cause congenital myopathy. Nat Genet 19, 94–97 (1998).
65. Friedman, R. C., Farh, K. K.-H., Burge, C. B. & Bartel, D. P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19, 92–105 (2009).
66. Peterson, S. M. et al. Common features of microRNA target prediction tools. Frontiers in Genetics 5 (2014).
67. Wang, L. et al. Genome-wide transcriptional profiling reveals microRNA-correlated genes and biological processes in human lymphoblastoid cell lines. PLoS One 4, e5878 (2009).
68. Akgül, B. & Göktaş, Ç. Gene Reporter Assay to Validate MicroRNA Targets in Drosophila S2 Cells. in miRNomics: MicroRNA Biology and Computational Analysis 233–242 (Springer, 2014).
69. Zhao, S. et al. OLFML3 expression is decreased during prenatal muscle development and regulated by microRNA-155 in pigs. Int J Biol Sci 8, 459 (2012).
70. Hou, X. et al. Discovery of MicroRNAs associated with myogenesis by deep sequencing of serial developmental skeletal muscles in pigs. PLoS One 7, e52123 (2012).
71. Wang, X., Jothikumar, N. & Griffiths, M. W. Enrichment and DNA extraction protocols for the simultaneous detection of Salmonella and Listeria monocytogenes in raw sausage meat with multiplex real-time PCR. J Food Protect 67, 189–192 (2004).
72. Wigmore, P. & Stickland, N. Muscle development in large and small pig fetuses. J Anat 137, 235 (1983).
73. Gautier, L., Cope, L., Bolstad, B. M. & Irizarry, R. A. Affy—analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307–315 (2004).
74. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249–264 (2003).
75. Chen, C. et al. Real-time quantification of microRNAs by stem–loop RT–PCR. Nucleic Acids Res 33, e179–e179 (2005).
76. Peltier, H. J. & Latham, G. J. Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 14, 844–852 (2008).
77. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408 (2001).
78. Ernst, J. & Bar-Joseph, Z. STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7, 191 (2006).
79. Huber, W., Carey, V. J., Long, L., Falcon, S. & Gentleman, R. Graphs in Molecular Biology. BMC Bioinformatics 8, S8 (2007).
80. Kozomara, A. & Griffiths-Jones, S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42, D68–73 (2013).
81. Guo, C. J., Pan, Q., Li, D. G., Sun, H. & Liu, B. W. MiR-15b and miR-16 are implicated in activation of the rat hepatic stellate cell: An essential role for apoptosis. J Hepatol 50, 766–778 (2009).
82. Huntley, R. P. et al. The GOA database: gene ontology annotation updates for 2015. Nucleic Acids Res 43, D1057–D1063 (2015).
83. Franceschini, A. et al. STRING v9. 1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41, D808–D815 (2013).
84. Cline, M. S. et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2, 2366–2382 (2007).