Skip to main content
Log in

Developmental expression patterns and association study with growth traits of bovine Bhlhe40 gene

  • Genomics. Transcriptomics
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

As a member of the basic helix-loop-helix (bHLH) family of transcription factors, Bhlhe40 plays an important role in the regulation of adipogenesis, myogenesis and the development of the metabolic syndrome. In this study, we investigated the tissue expression patterns and differences of bovine Bhlhe40 gene during three developmental stages. The result showed that Bhlhe40 was ubiquitously expressed in most tissues of cattle. In addition, the expression of bovine Bhlhe40 gene showed a decreasing trend in skeletal muscle and fat during the developmental stages. Then, two novel mutations (EX5 + 114 T>C, L166P and EX5 + 733 A > G, S372S) of bovine Bhlhe40 gene were identified by BamHI and ApaI ACRS PCR-RFLP in 1226 individuals from five indigenous cattle breeds in China. Frequencies of allele C at the BamHI locus varied from 0.210 to 0.340 among breeds, while frequencies of allele C at the ApaI locus varied from 0.030 to 0.114. Association analysis revealed no significant association of the ApaI locus with growth traits in Nanyang breed. However, the BamHI locus was significantly associated with the average daily gain at 18 months in Nanyang cattle (P < 0.05). This study aimed to lay the groundwork to further study of Bhlhe40 function at myogenesis and adipogenesis in bovine and should significantly contribute to cattle breeding and genetics through the MAS program.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

bHLH:

basic helix-loop-helix

Bhlhe40:

basic helix-loop-helix family member e40

MRFs:

myogenic regulatory factors

MyoD:

myogenic differentiation factor D

Myf5:

myogenic factor 5

MRF4:

myogenic regulatory factor 4

PGC-lα:

peroxisome-proliferator activated receptor γ co-activator lα

PPARγ2:

peroxisome-proliferator activated receptor γ2

SREBP-1:

sterol regulatory element binding protein 1

C/EBPβ:

CCAAT/Enhancer Binding Protein β

MSC:

mesenchymal stem cell

GAPDH:

glyceraldehyde-3-phosphate dehydrogenase

SNP:

single nucleotide polymorphism

AMP:

Adenosine monophosphate

MAS:

marker-assisted selection

PIC:

polymorphism information content

References

  1. Ross S.E., Greenberg M.E., Stiles C.D. 2003. Basic helix-loop-helix factors in cortical development. Neuron. 39(1), 13–25.

    Article  PubMed  CAS  Google Scholar 

  2. Arnold H.H., Winter B. 1998. Muscle differentiation: More complexity to the network of myogenic regulators. Curr. Opin. Genet. Dev. 8(5), 539–544.

    Article  PubMed  CAS  Google Scholar 

  3. Azmi S., Ozog A., Taneja R. 2004. Sharp-1/DEC2 inhibits skeletal muscle differentiation through repression of myogenic transcription factors. J. Biol. Chem. 279(50), 52643–52652.

    Article  PubMed  CAS  Google Scholar 

  4. Atchley W.R., Fitch W.M. 1997. A natural classification of the basic helix-loop-helix class of transcription factors. Proc. Natl. Acad. Sci. U. S. A. 94(10), 5172–5176.

    Article  PubMed  CAS  Google Scholar 

  5. Sabourin L.A., Rudnicki M.A. 2000. The molecular regulation of myogenesis. Clin. Genet. 57(1), 16–25.

    Article  PubMed  CAS  Google Scholar 

  6. Shen M., Kawamoto T., Yan W., Nakamasu K., Tamagami M., Koyano Y., Noshiro M., Kato Y. 1997. Molecular characterization of the novel basic helixloop-helix protein DEC1 expressed in differentiated human embryo chondrocytes. Biochem. Biophys. Res. Commun. 236(2), 294–298.

    Article  PubMed  CAS  Google Scholar 

  7. Hsiao S.P., Huang K.M., Chang H.Y., Chen S.L. 2009. P/CAF rescues the Bhlhe40-mediated repression of MyoD transactivation. Biochem. J. 422(2), 343–352.

    Article  PubMed  CAS  Google Scholar 

  8. Lecomte V., Meugnier E., Euthine V., Durand C., Freyssenet D., Nemoz G., Rome S., Vidal H., Lefai E. 2010. A new role for sterol regulatory element binding protein 1 transcription factors in the regulation of muscle mass and muscle cell differentiation. Mol. Cell. Biol. 30(5), 1182–1198.

    Article  PubMed  CAS  Google Scholar 

  9. Rome S., Meugnier E., Lecomte V., Berbe V., Besson J., Cerutti C., Pesenti S., Granjon A., Disse E., Clement K., Lefai E., Laville M., Vidal H. 2009. Microarray analysis of genes with impaired insulin regulation in the skeletal muscle of type 2 diabetic patients indicates the involvement of basic helix-loop-helix domain-containing, class B, 2 protein (BHLHB2). Diabetologia. 52(9), 1899–1912.

    Article  PubMed  CAS  Google Scholar 

  10. Grechez-Cassiau A., Panda S., Lacoche S., Teboul M., Azmi S., Laudet V., Hogenesch J.B., Taneja R., Delaunay F. 2004. The transcriptional repressor STRA13 regulates a subset of peripheral circadian outputs. J. Biol. Chem. 279(2), 1141–1150.

    Article  PubMed  CAS  Google Scholar 

  11. Turley H., Wykoff C.C., Troup S., Watson P.H., Gatter K.C., Harris A.L. 2004. The hypoxia-regulated transcription factor DEC1 (Stra13, SHARP-2) and its expression in human tissues and tumours. J. Pathol. 203(3), 808–813.

    Article  PubMed  CAS  Google Scholar 

  12. Giatromanolaki A., Koukourakis M.I., Sivridis E., Turley H., Wykoff C.C., Gatter K.C., Harris A.L. 2003. DEC1 (STRA13) protein expression relates to hypoxiainducible factor 1-alpha and carbonic anhydrase-9 overexpression in non-small cell lung cancer. J. Pathol. 200(2), 222–228.

    Article  PubMed  CAS  Google Scholar 

  13. Thin T.H., Li L., Chung T.K., Sun H., Taneja R. 2007. Stra13 is induced by genotoxic stress and regulates ionizing-radiation-induced apoptosis. EMBO Rep. 8(4), 401–407.

    Article  PubMed  CAS  Google Scholar 

  14. Park Y.K., Park H. 2012. Differentiated embryo chondrocyte 1 (DEC1) represses PPARgamma2 gene through interacting with CCAAT/enhancer binding protein beta (C/EBPbeta). Mol. Cells. 33(6), 575–581.

    Article  PubMed  CAS  Google Scholar 

  15. Choi S.M., Cho H.J., Cho H., Kim K.H., Kim J.B., Park H. 2008. Stra13/DEC1 and DEC2 inhibit sterol regulatory element binding protein-1c in a hypoxiainducible factor-dependent mechanism. Nucleic Acids Res. 36(20), 6372–6385.

    Article  PubMed  CAS  Google Scholar 

  16. Iizuka K., Horikawa Y. 2008. Regulation of lipogenesis via BHLHB2/DEC1 and ChREBP feedback looping. Biochem. Biophys. Res. Commun. 374(1), 95–100.

    Article  PubMed  CAS  Google Scholar 

  17. Shen M., Yoshida E., Yan W., Kawamoto T., Suardita K., Koyano Y., Fujimoto K., Noshiro M., Kato Y. 2002. Basic helix-loop-helix protein DEC1 promotes chondrocyte differentiation at the early and terminal stages. J. Biol. Chem. 277(51), 50112–50120.

    Article  PubMed  CAS  Google Scholar 

  18. Sambrook J.J., Russel D.W. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor lab. Press.

    Google Scholar 

  19. Sham P., Bader J.S., Craig I., O’Donovan M., Owen M. 2002. DNA pooling: A tool for large-scale association studies. Nature Rev. Genet. 3(11), 862–871.

    Article  PubMed  CAS  Google Scholar 

  20. Lan X.Y.P.C., Chen H., Zhang C.L., Li J.Y., Zhao M., Lei C.Z., Zhang A.L., Zhang L. 2007. An AluI PCRRFLP detecting a silent allele at the goat POU1F1 locus and its association with production traits. Small Rumin. Res. 73(1), 8–12.

    Article  Google Scholar 

  21. Zhang C., Liu B., Chen H., Lan X., Lei C., Zhang Z., Zhang R. 2009. Associations of a HinfI PCR-RFLP of POU1F1 gene with growth traits in Qinchuan cattle. Anim. Biotechnol. 20(2), 71–74.

    Article  PubMed  CAS  Google Scholar 

  22. Zhang C.L., Wang Y.H., Lei C.Z., Fang X.T., Chen H. 2011. The polymorphisms of bovine melanocortin-3 receptor pseudogene. Res. Vet. Sci. 90(2), 241–244.

    Article  PubMed  CAS  Google Scholar 

  23. Lai X., Lan X., Chen H., Wang X., Wang K., Wang M., Yu H., Zhao M. 2009. A novel SNP of the Hesx1 gene in bovine and its associations with average daily gain. Mol. Biol. Rep. 36(7), 1677–1681.

    Article  PubMed  CAS  Google Scholar 

  24. Rossner M.J., Dorr J., Gass P., Schwab M.H., Nave K.A. 1997. SHARPs: Mammalian enhancer-of-split- and hairy-related proteins coupled to neuronal stimulation. Mol. Cell. Neurosci. 10(3–4), 460–475.

    Article  PubMed  CAS  Google Scholar 

  25. Sun H., Taneja R. 2000. Stra13 expression is associated with growth arrest and represses transcription through histone deacetylase (HDAC)-dependent and HDAC-independent mechanisms. Proc. Natl. Acad. Sci. U. S. A. 97(8), 4058–4063.

    Article  PubMed  CAS  Google Scholar 

  26. Sun H., Li L., Vercherat C., Gulbagci N.T., Acharjee S., Li J., Chung T.K., Thin T.H., Taneja R. 2007. Stra13 regulates satellite cell activation by antagonizing Notch signaling. J. Cell Biol. 177(4), 647–657.

    Article  PubMed  CAS  Google Scholar 

  27. Yun Z., Maecker H.L., Johnson R.S., Giaccia A.J. 2002. Inhibition of PPAR gamma 2 gene expression by the HIF-1-regulated gene DEC1/Stra13: A mechanism for regulation of adipogenesis by hypoxia. Dev. Cell. 2(3), 331–341.

    Article  PubMed  CAS  Google Scholar 

  28. Iwata T., Kawamoto T., Sasabe E., Miyazaki K., Fujimoto K., Noshiro M., Kurihara H., Kato Y. 2006. Effects of overexpression of basic helix-loop-helix transcription factor Dec1 on osteogenic and adipogenic differentiation of mesenchymal stem cells. Eur. J. Cell Biol. 85(5), 423–431.

    Article  PubMed  CAS  Google Scholar 

  29. Yao J., Wang L., Chen L., Zhang S., Zhao Q., Jia W., Xue J. 2006. Cloning and developmental expression of the DEC1 ortholog gene in zebrafish. Gene Exp. Patterns. 6(8), 919–927.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to X. S. Lai.

Additional information

Published in Russian in Molekulyarnaya Biologiya, 2013, Vol. 47, No. 5, pp. 774–781.

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lai, X.S., Zhang, C.G., Wang, J. et al. Developmental expression patterns and association study with growth traits of bovine Bhlhe40 gene. Mol Biol 47, 674–680 (2013). https://doi.org/10.1134/S0026893313050105

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893313050105

Keywords

Navigation