Advertisement

Science China Life Sciences

, Volume 61, Issue 7, pp 826–835 | Cite as

Differential expression of FOXO1 during development and myoblast differentiation of Qinchuan cattle and its association analysis with growth traits

  • Yujia Sun
  • Kunpeng Liu
  • Yongzhen Huang
  • Xianyong Lan
  • Hong Chen
Research Paper
  • 26 Downloads

Abstract

Our previous work reported a relationship between FOXO1 mutations and growth of Qinchuan (QC) cattle. Here, we performed differential expression analysis of FOXO1 and its association analysis with growth traits in QC cattle. First, we measured the expression of the FOXO1 gene in nine tissues during three developmental stages. The results showed that FOXO1 was abundantly expressed in tissues of calves but was strongly repressed in adulthood, although there was significant transcription in skeletal muscle. FOXO1 expression showed gradual up-regulation during differentiation of primary bovine skeletal muscle cells. We also identified six SNPs of the bovine FOXO1 gene by sequencing DNA pools of samples from 488 individuals, and association analysis indicated that five SNPs were significantly associated with some growth traits in the QC population. We further analyzed four haplotype combinations of the six SNPs and found significant correlation with body length (P<0.01). In conclusion, FOXO1 participates in bovine myocyte differentiation and expression, and may be a strong candidate as a gene that affects growth traits that could be exploited in a QC cattle breeding program. More generally, our data provide a new theoretical basis for QC beef breeding and beef quality improvement.

Keywords

tissues expression myoblast differentiation sequence variants association analysis Qinchuan cattle 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31272408), Agricultural Science and Technology Innovation Projects of Shaanxi Province (2012NKC01-13), Program of National Beef Cattle Industrial Technology System (CARS-38) and National High Technology Research and Development Program of China (2013AA102505).

Supplementary material

11427_2017_9205_MOESM1_ESM.docx (17 kb)
Table S1 Primers information for PCR amplification of bovine FOXO1 gene

References

  1. Arnold, H.H., and Winter, B. (1998). Muscle differentiation: more complexity to the network of myogenic regulators. Curr Opin Genet Dev 8, 539–544.CrossRefPubMedGoogle Scholar
  2. Black, B.L., and Olson, E.N. (1998). Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol 14, 167–196.CrossRefPubMedGoogle Scholar
  3. Blackwell, T.K., and Weintraub, H. (1990). Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250, 1104–1110.CrossRefPubMedGoogle Scholar
  4. Boillée, S., Vande Velde, C., and Cleveland, D.W. (2006). ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52, 39–59.CrossRefPubMedGoogle Scholar
  5. Bong, J.J., Cho, K.K., and Baik, M. (2009). Comparison of gene expression profiling between bovine subcutaneous and intramusular adipose tissues by serial analysis of gene expression. Cell Biol Int in press doi: 10.1-042/CBI20090046.Google Scholar
  6. Chamary, J.V., and Hurst, L.D. (2005). Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol 6, R75.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cianzio, D.S., Topel, D.G., Whitehurst, G.B., Beitz, D.C., and Self, H.L. (1985). Adipose tissue growth and cellularity: changes in bovine adipocyte size and number. J Animal Sci 60, 970.CrossRefGoogle Scholar
  8. Don, R.H., Cox, P.T., Wainwright, B.J., Baker, K., and Mattick, J.S. (1991). ‘Touchdown’ PCR to circumvent spurious priming during gene amplification. Nucl Acids Res 19, 4008–4008.CrossRefPubMedGoogle Scholar
  9. Fredericks, W.J., Galili, N., Mukhopadhyay, S., Rovera, G., Bennicelli, J., Barr, F.G., and Rauscher 3rd, F.J. (1995). The PAX3-FKHR fusion protein created by the t(2;13) translocation in alveolar rhabdomyosarcomas is a more potent transcriptional activator than PAX3. Mol Cell Biol 15, 1522–1535.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Green M.R., and Sambrook J. (2012). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.Google Scholar
  11. Hoey, A.J., Reich, M.M., Davis, G., Shorthose, R., and Sillence, M.N. (1995). Beta 2-adrenoceptor densities do not correlate with growth, carcass quality, or meat quality in cattle. J Animal Sci 73, 3281.CrossRefGoogle Scholar
  12. Hribal, M.L., Nakae, J., Kitamura, T., Shutter, J.R., and Accili, D. (2003). Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors. J Cell Biol 162, 535–541.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kamei, Y., Miura, S., Suzuki, M., Kai, Y., Mizukami, J., Taniguchi, T., Mochida, K., Hata, T., Matsuda, J., Aburatani, H., Nishino, I., and Ezaki, O. (2004). Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated type I (Slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279, 41114–41123.CrossRefPubMedGoogle Scholar
  14. Lassar, A., and Münsterberg, A. (1994). Wiring diagrams: regulatory circuits and the control of skeletal myogenesis. Curr Opin Cell Biol 6, 432–442.CrossRefPubMedGoogle Scholar
  15. Minde, D.P., Anvarian, Z., Rüdiger, S.G., and Maurice, M.M. (2011). Messing up disorder: how do missense mutations in the tumor suppressor protein APC lead to cancer? Mol Cancer 10, 101.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Nakae, J., Kitamura, T., Kitamura, Y., Biggs Iii, W.H., Arden, K.C., and Accili, D. (2003). The forkhead transcription factor foxo1 regulates adipocyte differentiation. Dev Cell 4, 119–129.CrossRefPubMedGoogle Scholar
  17. Nei, M., and Roychoudhury, A.K. (1974). Sampling variances of heterozygosity and genetic distance. Genetics 76, 379–390.PubMedPubMedCentralGoogle Scholar
  18. Perry, R., and Rudnick, M.A. (2000). Molecular mechanisms regulating myogenic determination and differentiation. Front Biosci 5, 148.CrossRefGoogle Scholar
  19. Rached, M.T., Kode, A., Silva, B.C., Jung, D.Y., Gray, S., Ong, H., Paik, J. H., DePinho, R.A., Kim, J.K., Karsenty, G., and Kousteni, S. (2010). FoxO1 expression in osteoblasts regulates glucose homeostasis through regulation of osteocalcin in mice. J Clin Invest 120, 932–932.CrossRefPubMedCentralGoogle Scholar
  20. Schmittgen, T.D., and Livak, K.J. (2008). Analyzing real-time PCR data by the comparative Ct method. Nat Protocols 3, 1101–1108.CrossRefPubMedGoogle Scholar
  21. Senoo, N., Miyoshi, N., Kobayashi, E., Morita, A., Kamei, Y., and Miura, S. (2016). FOXO1-induced atrophy changes in phospholipid profiles of skeletal muscle. FASEB J 30, 659.2-.2.Google Scholar
  22. Sin, T.K., Yung, B.Y., and Siu, P.M. (2015). Modulation of SIRT1-Foxo1 signaling axis by resveratrol: implications in skeletal muscle aging and insulin resistance. Cell Physiol Biochem 35, 541–552.CrossRefPubMedGoogle Scholar
  23. Sun, Y.J., Xue, J., Guo, W.J., Li, M.X., Huang, Y.Z., Lan, X.Y., Lei, C.Z., Zhang, C.L., and Chen, H. (2013). Haplotypes of bovine FoxO1 gene sequence variants and association with growth traits in Qinchuan cattle. J Genet 92, e8–e14.PubMedGoogle Scholar
  24. Teixeira, C.C., Liu, Y., Thant, L.M., Pang, J., Palmer, G., and Alikhani, M. (2010). Foxo1, a novel regulator of osteoblast differentiation and skeletogenesis. J Biol Chem 285, 31055–31065.CrossRefPubMedPubMedCentralGoogle Scholar
  25. te Pas, M.F.W. (2004). Muscle Development of Livestock Animals Physiology Genetics and Meat Quality. (London: CAB International).CrossRefGoogle Scholar
  26. Wang, L., Li, J., Fu, C., Zhang, W., Wu, J., Huang, M., and Lai, S. (2010). cDNA cloning and tissue expression of FOXO1 gene in new calf. Chin J An Sci 46, 1–5.Google Scholar
  27. Wood, J.D., Enser, M., Fisher, A.V., Nute, G.R., Sheard, P.R., Richardson, R.I., Hughes, S.I., and Whittington, F.M. (2008). Fat deposition, fatty acid composition and meat quality: a review. Meat Sci 78, 343–358.CrossRefPubMedGoogle Scholar
  28. Zhou, Z., Wang, T., Pan, L., Huang, R., and Shi, F. (2007). FoxO4 is the main forkhead transcriptional factor localized in the gastrointestinal tracts of pigs. J Zhejiang Univ Sci B 8, 39–44.CrossRefPubMedGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Yujia Sun
    • 1
  • Kunpeng Liu
    • 1
  • Yongzhen Huang
    • 1
  • Xianyong Lan
    • 1
  • Hong Chen
    • 1
    • 2
  1. 1.College of Animal Science and TechnologyNorthwest A&F University, Shaanxi Key Laboratory of Molecular Biology for AgricultureYanglingChina
  2. 2.Institute of Cellular and Molecular BiologyJiangsu Normal UniversityXuzhouChina

Personalised recommendations