DOI QR코드

DOI QR Code

Novel Nucleotide Variations, Haplotypes Structure and Associations with Growth Related Traits of Goat AT Motif-Binding Factor (ATBF1) Gene

  • Zhang, Xiaoyan (College of Animal Science and Technology, Northwest A&F University, Shaanxi Key Laboratory of Molecular Biology for Agriculture) ;
  • Wu, Xianfeng (College of Animal Science and Technology, Northwest A&F University, Shaanxi Key Laboratory of Molecular Biology for Agriculture) ;
  • Jia, Wenchao (College of Life Sciences, Northwest A&F University) ;
  • Pan, Chuanying (College of Animal Science and Technology, Northwest A&F University, Shaanxi Key Laboratory of Molecular Biology for Agriculture) ;
  • Li, Xiangcheng (Institute of Beijing Animal Science and Veterinary, Chinese Academy of Agricultural Science) ;
  • Lei, Chuzhao (College of Animal Science and Technology, Northwest A&F University, Shaanxi Key Laboratory of Molecular Biology for Agriculture) ;
  • Chen, Hong (College of Animal Science and Technology, Northwest A&F University, Shaanxi Key Laboratory of Molecular Biology for Agriculture) ;
  • Lan, Xianyong (College of Animal Science and Technology, Northwest A&F University, Shaanxi Key Laboratory of Molecular Biology for Agriculture)
  • Received : 2014.11.06
  • Accepted : 2015.04.01
  • Published : 2015.10.01

Abstract

The AT motif-binding factor (ATBF1) not only interacts with protein inhibitor of activated signal transducer and activator of transcription 3 (STAT3) (PIAS3) to suppress STAT3 signaling regulating embryo early development and cell differentiation, but is required for early activation of the pituitary specific transcription factor 1 (Pit1) gene (also known as POU1F1) critically affecting mammalian growth and development. The goal of this study was to detect novel nucleotide variations and haplotypes structure of the ATBF1 gene, as well as to test their associations with growth-related traits in goats. Herein, a total of seven novel single nucleotide polymorphisms (SNPs) (SNP 1-7) within this gene were found in two well-known Chinese native goat breeds. Haplotypes structure analysis demonstrated that there were four haplotypes in Hainan black goat while seventeen haplotypes in Xinong Saanen dairy goat, and both breeds only shared one haplotype (hap1). Association testing revealed that the SNP2, SNP5, SNP6, and SNP7 loci were also found to significantly associate with growth-related traits in goats, respectively. Moreover, one diplotype in Xinong Saanen dairy goats significantly linked to growth related traits. These preliminary findings not only would extend the spectrum of genetic variations of the goat ATBF1 gene, but also would contribute to implementing marker-assisted selection in genetics and breeding in goats.

Keywords

ATBF1 Gene;Single Nucleotide Polymorphisms;Haplotypes;Growth-related Traits;Association

Acknowledgement

Supported by : National Natural Science Foundation of China

References

  1. Akcay, A., K. Ulucan, N. Taskin, M. Boyraz, T. Akcay, O. Zurita, A. Gomez, K. E. Heath, and A. Campos-Barros. 2013. Suprasellar mass mimicking a hypothalamic glioma in a patient with a complete PROP1 deletion. Eur. J. Med. Genet. 56:445-451. https://doi.org/10.1016/j.ejmg.2013.06.006
  2. Araujo, R. V., C. V. Chang, V. A. S. Cescato, M. C. B. V. Fragoso, M. D. Bronstein, B. B. Mendonca, I. J. P. Arnhold, and L. R. S. Carvalho. 2013. PROP1 overexpression in corticotrophinomas: evidence for the role of PROP1 in the maintenance of cells committed to corticotrophic differentiation. Clinics 68:887-891. https://doi.org/10.6061/clinics/2013(06)26
  3. Bastos, E., S. Avila, A. Cravador, R. Renaville, P. H Guedes, and C. J Luis. 2006. Identification and characterization of four splicing variants of ovine POU1F1 gene. Gene 382:12-19. https://doi.org/10.1016/j.gene.2006.05.028
  4. Benjamin, E. J., K. M. Rice, D. E. Arking, A. Pfeufer, C. van Noord, A. V. Smith, R. B. Schnabel, J. C. Bis, E. Boerwinkle, and M. F. Sinner et al. 2009. Variants in ZFHX3 are associated with atrial fibrillation in individuals of European ancestry. Nat. Genet. 41:879-881. https://doi.org/10.1038/ng.416
  5. Carvalho, L., R. D. Ward, M. L. Brinkmeier, M. A. Potok, A. H. Vesper, and S. A. Camper. 2006. Molecular basis for pituitary dysfunction: Comparison of Prop1 and Pit1 mutant mice. Dev. Biol. 295:340.
  6. Chamary, J. V. and L. D. Hurst. 2005. Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol. 6:R75. https://doi.org/10.1186/gb-2005-6-9-r75
  7. Choudhary, V., P. Kumar, T. K. Bhattacharya, B. Bhushan, A. Sharma, and A. Shukla. 2007. DNA polymorphism of insulin-like growth factor-binding protein-3 gene and its association with birth weight and body weight in cattle. J. Anim. Breed. Genet. 124:29-34. https://doi.org/10.1111/j.1439-0388.2007.00626.x
  8. Cleton-Jansen, A. M., R. van Eijk, M. Lombaerts, M. K. Schmidt, L. J. Van't Veer, K. Philippo, R. M. E. Zimmerman, J. L. Peterse, V. T. B. H. M. Smit, T. van Wezel, C. J. Cornelisse, A. M. Cleton-Jansen, R. Van Eijk, and M. Lombaerts. 2008. ATBF1 and NQO1 as candidate targets for allelic loss at chromosome arm 16q in breast cancer: Absence of somatic ATBF1 mutations and no role for the C609T NQO1 polymorphism. BMC Cancer 8:105. https://doi.org/10.1186/1471-2407-8-105
  9. Darnell, J. E. 1997. STATs and gene regulation. Science 277(5332):1630-1635. https://doi.org/10.1126/science.277.5332.1630
  10. Davis, S. W., F. Castinetti, L. R. Carvalho, B. S. Ellsworth, M. A. Potok, R. H. Lyons, M. L. Brinkmeier, L. T. Raetzman, P. Carninci, A. H. Mortensen, Y. Hayashizaki, I. J. P. Arnhold, B. B. Mendonca, T. Brue, and S. A. Camper. 2010. Molecular mechanisms of pituitary organogenesis: In search of novel regulatory genes. Mol. Cell. Endocrinol. 323:4-19. https://doi.org/10.1016/j.mce.2009.12.012
  11. Fang, Q., A. M. Giordimaina, D. F. Dolan, S. A. Camper, and M. Mustapha. 2012. Genetic Background of Prop1(df) mutants provides remarkable protection against hypothyroidism-induced hearing impairment. J. Assoc. Res. Otolaryngol. 13:173-184. https://doi.org/10.1007/s10162-011-0302-3
  12. Fang, X. T., H. X Xu, C. L. Zhang, J. M. Zhang, X. Y. Lan, C. W. Gu, and H. Chen. 2010. Polymorphisms in BMP-2 gene and their associations with growth traits in goats. Genes Genomics 32:29-35. https://doi.org/10.1007/s13258-010-0762-6
  13. Gilbert, R. P., D. R. Bailey, and N. H. Shannon. 1993 Linear body measurements of cattle before and after twenty years of selection for post weaning gain when fed two different diets. J. Anim. Sci. 71:1712-1720. https://doi.org/10.2527/1993.7171712x
  14. Godi, M., S. Mellone, L. Tiradani, R. Marabese, C. Bardelli, M. Salerno, F. Prodam, S. Bellone, A. Petri, P. Momigliano-Richiardi, G. Bona, and M. Giordano. 2012. Functional SNPs within the intron 1 of the PROP1 gene contribute to combined growth hormone deficiency (CPHD). J. Clin. Endocrinol. Metab. 97:E1791-E1797. https://doi.org/10.1210/jc.2012-1527
  15. Green, M. R. and J. Sambrook. 2012. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, USA. 65-73.
  16. Gudbjartsson, D. F., H. Holm, S. Gretarsdottir, and G. Thorleifsson, G. B. Walters, G. Thorgeirsson, J. Gulcher, E. B. Mathiesen, I. Njolstad, and A. Nyrnes et al. 2009. A sequence variant in ZFHX3 on 16q22 associates with atrial fibrillation and ischemic stroke. Nat. Genet. 41:876-878. https://doi.org/10.1038/ng.417
  17. Guy, J. C., C. S. Hunter, A. D. Showalter, T. P. L. Smith, K. Charoonpatrapong, K. W. Sloop, J. P. Bidwell, and S. J. Rhodes. 2004. Conserved amino acid sequences confer nuclear localization upon the Prophet of Pit-1 pituitary transcription factor protein. Gene 336:263-273. https://doi.org/10.1016/j.gene.2004.04.022
  18. He, H., H. L. Zhang, Z. X. Li, Y. Liu, and X. L. Liu. 2014. Expression, SNV identification, linkage disequilibrium, and combined genotype association analysis of the muscle-specific gene CSRP3 in Chinese cattle. Gene 535:17-23. https://doi.org/10.1016/j.gene.2013.11.014
  19. Heinrich, P. C., I. Behrmann, G. Muller-Newen, F. Schaper, and L. Graeve. 1998. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 334:297-314. https://doi.org/10.1042/bj3340297
  20. Ishii, Y., M. Kawaguchi, K. Takagawa, T. Oya, S. Nogami, A. Tamura, Y. Miura, A. Ido, N. Sakata, T. Hashimoto-Tamaoki, T. Kimura, T. Saito, T. Tamaoki, and M. Sasahara. 2003. ATBF1­A protein, but not ATBF1-B, is preferentially expressed in developing rat brain. J. Comp. Neurol. 465:57-71. https://doi.org/10.1002/cne.10807
  21. Jiang, Q., B. Ni, J. Shi, Z. L. Han, R. D. Qi, W. H. Xu, D. Wang, D. W. Wang, and M. L. Chen. 2014. Down-regulation of ATBF1 activates STAT3 signaling via PIAS3 in pacing-induced HL-1 atrial myocytes. Biochem. Biophys. Res. Commun. 449:278-283. https://doi.org/10.1016/j.bbrc.2014.05.041
  22. Jung, C. G., H. J. Kim, M. Kawaguchi, K. K. Khanna, H. Hida, K. Asai, H. Nishino, and Y. Miura. 2005. Homeotic factor ATBF1 induces the cell cycle arrest associated with neuronal differentiation. Development 132:5137-5145. https://doi.org/10.1242/dev.02098
  23. Jung, C. G., K. O. Uhm, Y. Miura, T. Hosono, H. Horike, K. K. Khanna, M. J. Kim, and M. Michikawa. 2011. Beta-amyloid increases the expression level of ATBF1 responsible for death in cultured cortical neurons. Mol. Neurodegener. 6:47. https://doi.org/10.1186/1750-1326-6-47
  24. Kai, K., Z. Zhang, H. Yamashita, Y. Yamamoto, Y. Miura, and H. Iwase. 2008. Loss of heterozygosity at the ATBF1-A locus located in the 16q22 minimal region in breast cancer. BMC Cancer 8:262. https://doi.org/10.1186/1471-2407-8-262
  25. Kamohara, Y., N. Sugiyama, T. Mizuguchi, D. Inderbitzin, H. Lilja, Y. Middleton, T. Neuman, A. A. Demetriou, and J. Rozga. 2000. Inhibition of signal transducer and activator transcription factor 3 in rats with acute hepatic failure. Biochem. Biophys. Res. Commun. 273:129-135. https://doi.org/10.1006/bbrc.2000.2881
  26. Lan, X. Y., C. Y. Pan, H. Chen, C. L. Zhang, J. Y. Li, M. Zhao, C. Z. Lei, A. L. Zhang, and L. Zhang. 2007. An AluI PCR-RFLP detecting a silent allele at the goat POU1F1 locus and its association with production traits. Small Rumin. Res. 73:8-12. https://doi.org/10.1016/j.smallrumres.2006.10.009
  27. Lan, X. Y., H. Y. Zhao, Z. J. Li, R. Zhou, C. Y. Pan, C. Z. Lei, and H. Chen. 2013. Exploring the novel genetic variant of PITX1 gene and its effect on milk performance in dairy goats. J. Integr. Agric. 12:118-126. https://doi.org/10.1016/S2095-3119(13)60212-9
  28. Li, M., X. Fu, G. Ma, X. D. Sun, X. Y. Dong, T. Nagy, C. S. Xing, J. Li, and J. T. Dong. 2012. Atbf1 regulates pubertal mammary gland development likely by inhibiting the pro-proliferative function of estrogen-ER signaling. PLoS One 7(12):e51283. https://doi.org/10.1371/journal.pone.0051283
  29. Li, M., D. Zhao, G. Ma, B. Zhang, X. Fu, Z. Zhu, L. Fu, X. Sun, and J. T. Dong. 2013. Upregulation of ATBF1 by progesterone-PR signaling and its functional implication in mammary epithelial cells. Biochem. Biophys. Res. Commun. 430:358-363. https://doi.org/10.1016/j.bbrc.2012.11.009
  30. Li, F., H. Chen, C. Z. Lei, G. Ren, J. Wang, Z. J. Li, and J. Q. Wang. 2010. Novel SNPs of the bovine NUCB2 gene and their association with growth traits in three native Chinese cattle breeds. Mol. Biol. Rep. 37:541-546. https://doi.org/10.1007/s11033-009-9732-y
  31. Li, Z. Q., Z. Zhang, Z. He, W. Tang, T. Li, Z. Zeng, L. He, and Y. Y. Shi. 2009. A partition-ligation-combination-subdivision EM algorithm for haplotype inference with multiallelic markers: update of the SHEsis. Cell Res. 19:519-523. https://doi.org/10.1038/cr.2009.33
  32. Massague, J. 2012. TGF-$\beta$ signalling in context. Nat. Rev. Mol. Cell Biol. 13:616-630. https://doi.org/10.1038/nrm3434
  33. Massague, J., J. Seoane, and D. Wotton. 2005. Smad transcription factors. Genes Dev. 19:2783-2810. https://doi.org/10.1101/gad.1350705
  34. Morinaga, T., H. Yasuda, T. Hashimoto, K. Higashio, and T. Tamaoki. 1991. A human alpha-fetoprotein enhancer-binding protein, ATBF1, contains four homeodomains and seventeen zinc fingers. Mol. Cell. Biol. 11:6041-6049. https://doi.org/10.1128/MCB.11.12.6041
  35. Moustakas, A. and C. H. Heldin. 2009. The regulation of TGF-$\beta$ signal transduction. Development 136:3699-3714. https://doi.org/10.1242/dev.030338
  36. Navardauskaite, R., P. Dusatkova, B. Obermannova, R. W. Pfaeffle, W. F. Blum, D. Adukauskiene, N. Smetanina, O. Cinek, R. Verkauskiene, and J. Lebl. 2014. High prevalence of PROP1 defects in Lithuania: Phenotypic findings in an ethnically homogenous cohort of patients with multiple pituitary hormone deficiency. J. Clin. Endocrinol. Metab. 99:299-306. https://doi.org/10.1210/jc.2013-3090
  37. Ninomiya, T., K. Mihara, K. Fushimi, Y. Hayashi, T. Hashimoto-Tamaoki, and T. Tamaoki. 2002. Regulation of the alpha­fetoprotein gene by the isoforms of ATBF1 transcription factor in human hepatoma. Hepatology 35:82-87. https://doi.org/10.1053/jhep.2002.30420
  38. Nishio, E., Y. Miura, M. Kawaguchi, and A. Morita. 2012. Nuclear translocation of ATBF1 is a potential prognostic marker for skin cancer. Acta Dermatovenerol. Croat. 20:239-245.
  39. Nojiri, S., T. Joh, Y. Miura, N. Sakata, T. Nomura, H. Nakao, S. Sobue, H. Oharra, K. Asai, and M. Ito. 2004. ATBF1 enhances the suppression of STAT3 signaling by interaction with PIAS3. Biochem. Biophys. Res. Commun. 314:97-103. https://doi.org/10.1016/j.bbrc.2003.12.054
  40. Pan, C. Y., C. Y. Wu, W. C. Jia, Y. Xu, C. Z. Lei, S. R. Hu, X. Y. Lan, and H. Chen. 2013. A critical functional missense mutation (H173R) in the bovine PROP1 gene significantly affects growth traits in cattle. Gene 531:398-402. https://doi.org/10.1016/j.gene.2013.09.002
  41. Perea, D., K. Molohon, K. Edwards, and F. J. Diaz-Benjumea. 2013. Multiple roles of the gene zinc finger homeodomain-2 in the development of the Drosophila wing. Mech. Dev. 130: 467-481. https://doi.org/10.1016/j.mod.2013.06.002
  42. Qi, Y. C., J. A. Ranish, X. Y. Zhu, A. Krones, J. Zhang, R. Aebersold, D. W. Rose, M. G. Rosenfeld, and C. Carriere. 2008. Atbf1 is required for the Pit1 gene early activation. Proc. Natl. Acad. Sci. USA 105:2481-2486. https://doi.org/10.1073/pnas.0712196105
  43. Sakata, N., S. Kaneko, S. Ikeno, Y. Miura, H. Nakabayashi, X. Y. Dong, J. T. Dong, T. Tamaoki, N. Nakano, and S. Itoh. 2014. TGF-$\beta$ Signaling Cooperates with AT Motif-Binding Factor-1 for Repression of the $\alpha$-Fetoprotein Promoter. J. Signal Transduct. Article ID 970346.
  44. Sambrock, J. and D. W. Russell. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, NY, USA.
  45. Schindler, C. and J. E. Darnell. 1995. Transcriptional responses to polypeptide ligands: The JAK-STAT pathway. Annu. Rev. Biochem. 64:621-652. https://doi.org/10.1146/annurev.bi.64.070195.003201
  46. Shuai, K. 1999. The STAT family of proteins in cytokine signaling. Prog. Biophys. Mol. Biol. 71:405-422. https://doi.org/10.1016/S0079-6107(98)00051-0
  47. Sun, X., X. Fu, J. Li, C. S. Xing, D. W. Martin, H. H. Zhang, Z. J. Chen, and J. T. Dong. 2012. Heterozygous deletion of Atbf1 by the Cre-loxP system in mice causes preweaning mortality. Genesis 50:819-827. https://doi.org/10.1002/dvg.22041
  48. Sun, X. D., X. Y. Fu, J. Li, C. S. Xing, H. F. Frierson, H. Wu, X. K. Ding, T. Z. Ju, R. D. Cummings, and J. T. Dong. 2014. Deletion of Atbf1/Zfhx3 in mouse prostate causes neoplastic lesions, likely by attenuation of membrane and secretory proteins and multiple signaling pathways. Neoplasia 16:377-389. https://doi.org/10.1016/j.neo.2014.05.001
  49. Sun, X. D., Y. F. Zhou, K. B. Otto, M. R. Wang, C. S. Chen, W. Zhou, K. Subramanian, P. M. Vertino, and J. T. Dong. 2007. Infrequent mutation of ATBF1 in human breast cancer. J. Cancer Res. Clin. 133:103-105.
  50. Van Laere, A. S., M. Nguyen, M. Braunschweig, C. Nezer, C. Collette, L. Moreau, A. L. Archibald, C. S. Haley, N. Buys, and M. Tally et al. 2003. A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature 425: 832-836. https://doi.org/10.1038/nature02064
  51. Wang, A. L., Y. Zhang, M. J. Li, X. Y. Lan, J. Q. Wang, and H. Chen. 2013. SNP identi.cation in FBXO32 gene and their associations with growth traits in cattle. Gene 515:181-186. https://doi.org/10.1016/j.gene.2012.11.054
  52. Wang, G., S. Zhang, S. Wei, Y. Zhang, Y. Li, C. Fu, C. Zhao, and L. Zan. 2014. Novel polymorphisms of SIX4 gene and their association with body measurement traits in Qinchuan cattle. Gene 539:107-110. https://doi.org/10.1016/j.gene.2014.01.042
  53. Yasuda, H., A. Mizuno, T. Tamaoki, and T. Morinaga. 1994. ATBF1, a multiple-homeodomain zinc finger protein, selectively down-regulates AT-rich elements of the human $\alpha$-fetoprotein gene. Mol. Cell. Biol. 14:1395-1401. https://doi.org/10.1128/MCB.14.2.1395
  54. Yeh, F. C., R. Yang, T. J. Boyle, Z. Ye, and J. M. Xiyan. 2000. PopGene32, Microsoft Windows-based freeware for population genetic analysis, version 1.32. Molecular Biology and Biotechnology Centre, University of Alberta, Edmonton, AB, Canada.
  55. Zhao, H. Y., X. F. Wu, H. F. Cai, C. Y. Pan, C. Z. Lei, H. Chen, X. Y. Lan. 2013. Genetic variants and effects on milk traits of the caprine paired-like homeodomain transcription factor 2 (PITX2) gene in dairy goats. Gene 532:203-210. https://doi.org/10.1016/j.gene.2013.09.062
  56. Zhong, Z., Z. L. Wen, and J. E. Darnell. 1994. Stat3: A STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264(5155):95-98. https://doi.org/10.1126/science.8140422

Cited by

  1. gene using mathematical expectation (ME) method vol.11, pp.2, 2017, https://doi.org/10.1080/19336896.2017.1300740
  2. ) and effects on Chinese and Mongolian sheep phenotypes vol.12, pp.3-4, 2018, https://doi.org/10.1080/19336896.2018.1467193
  3. Development of a touch-down multiplex PCR method for simultaneously rapidly detecting three novel insertion/deletions (indels) within one gene: an example for goat GHR gene pp.1532-2378, 2018, https://doi.org/10.1080/10495398.2018.1517770
  4. gene insertion/deletion (indel) on phenotypic traits in sheep vol.12, pp.1, 2018, https://doi.org/10.1080/19336896.2017.1405886
  5. gene is strongly associated with goat litter size pp.1532-2378, 2019, https://doi.org/10.1080/10495398.2018.1561459