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Polymorphism, Genetic Effect and Association with Egg Production Traits of Chicken Matrix Metalloproteinases 9 Promoter

  • Zhu, Guiyu (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University) ;
  • Jiang, Yunliang (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University)
  • Received : 2014.03.20
  • Accepted : 2014.07.17
  • Published : 2014.11.01

Abstract

Matrix metalloproteinases (MMP) are key enzymes involved in cell and tissue remodeling during ovarian follicle development and ovulation. The control of MMP9 transcription in ovarian follicles occurs through a core promoter region (-2,400 to -1,700 bp). The aim of this study was to screen genetic variations in the core promoter region and examine MMP9 transcription regulation and reproduction performance. A single cytosine deletion/insertion polymorphism was found at -1954 $C^+/C^-$. Genetic association analysis indicated significant correlation between the deletion genotype ($C^-$) with total egg numbers at 28 weeks (p = 0.031). Furthermore, luciferase-reporter assay showed the deletion genotype ($C^-$) had significantly lower promoter activity than the insertion genotype ($C^+$) in primary granulosa cells (p<0.01). Therefore, the identified polymorphism could be used for marker-assisted selection to improve chicken laying performance.

References

  1. Baka, S., K. Zourla, E. Kouskouni, E. Makrakis, S. Demeridou, D. Tzanakaki, D. Hassiakos, and G. Creatsas. 2010. Matrix metalloproteinases 2 and 9 and their tissue inhibitors in the follicular fluid of patients with polycystic ovaries undergoing in vitro fertilisation. In Vivo 24:293-296.
  2. Curry, T. E., Jr., L. Song, and S. E. Wheeler. 2001. Cellular localization of gelatinases and tissue inhibitors of metalloproteinases during follicular growth, ovulation, and early luteal formation in the rat. Biol. Reprod. 65:855-865. https://doi.org/10.1095/biolreprod65.3.855
  3. Baka, S., K. Zourla, A. Malamitsi-Puchner, E. Makrakis, G. Kaparos, S. Demeridou, T. Moustakarias, D. Tzanakaki, D. Hassiakos, and E. Kouskouni. 2009. Intrafollicular levels of matrix metalloproteinases-2 and -9 in patients with polycystic ovaries are not associated with pregnancy rate during IVF cycle. In Vivo 23:89-92.
  4. Choi, J. W., S. E. Ahn, D. Rengaraj, H. W. Seo, W. Lim, G. Song, and J. Y. Han. 2011. Matrix metalloproteinase 3 is a stromal marker for chicken ovarian cancer. Oncol. Lett. 2:1047-1051.
  5. Curry, T. E., Jr. and K. G. Osteen. 2003. The matrix metalloproteinase system: Changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr. Rev. 24:428-465. https://doi.org/10.1210/er.2002-0005
  6. Dubois, B., B. Arnold, and G. Opdenakker. 2000. Gelatinase B deficiency impairs reproduction. J. Clin. Invest. 106:627-628. https://doi.org/10.1172/JCI10910
  7. Furuya, M., H. Ishikura, Y. Ogawa, Y. Kawarada, M. Shibata, S. Fujimoto, and T. Yoshiki. 2000. Analyses of matrix metalloproteinases and their inhibitors in cyst fluid of serous ovarian tumors. Pathobiology 68:239-244. https://doi.org/10.1159/000055932
  8. Hahn-Dantona, E. A., R. T. Aimes, and J. P. Quigley. 2000. The isolation, characterization, and molecular cloning of a 75-kDa gelatinase B-like enzyme, a member of the matrix metalloproteinase (MMP) family. An avian enzyme that is MMP-9-like in its cell expression pattern but diverges from mammalian gelatinase B in sequence and biochemical properties. J. Biol. Chem. 275:40827-40838. https://doi.org/10.1074/jbc.M006234200
  9. Heinemeyer, T., E. Wingender, I. Reuter, H. Hermjakob, A. E. Kel, O. V. Kel, E. V. Ignatieva, E. A. Ananko, O. A. Podkolodnaya, F. A. Kolpakov, N. L. Podkolodny, and N. A. Kolchanov. 1998. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucl. Acids Res. 26:362-367. https://doi.org/10.1093/nar/26.1.362
  10. Kang, L., N. B. Zhang, Y. J. Zhang, H. X. Yan, H. Tang, C. S. Yang, H. Wang, and Y. L. Jiang. 2012. Molecular characterization and identification of a novel polymorphism of 200 bp indel associated with age at first egg of the promoter region in chicken follicle-stimulating hormone receptor (FSHR) gene. Mol. Biol. Rep. 39:2967-2973. https://doi.org/10.1007/s11033-011-1058-x
  11. Henmi, H., T. Endo, K. Nagasawa, T. Hayashi, M. Chida, N. Akutagawa, M. Iwasaki, Y. Kitajima, T. Kiya, A. Nishikawa, K. Manase, and R. Kudo. 2001. Lysyl oxidase and MMP-2 expression in dehydroepiandrosterone-induced polycystic ovary in rats. Biol. Reprod. 64:157-162. https://doi.org/10.1095/biolreprod64.1.157
  12. Imai, K., M. A. Khandoker, M. Yonai, T. Takahashi, T. Sato, A. Ito, Y. Hasegawa, and K. Hashizume. 2003. Matrix metalloproteinases-2 and -9 activities in bovine follicular fluid of different-sized follicles: Relationship to intra-follicular inhibin and steroid concentrations. Domest. Anim. Endocrinol. 24:171-183. https://doi.org/10.1016/S0739-7240(02)00235-7
  13. Johnson, P. A. and J. R. Giles. 2013. The hen as a model of ovarian cancer. Nat. Rev. Cancer 13:432-436. https://doi.org/10.1038/nrc3535
  14. Kikkawa, F., K. Tamakoshi, A. Nawa, K. Shibata, S. Yamagata, T. Yamagata, and N. Suganuma. 1997. Positive correlation between inhibitors of matrix metalloproteinase 1 and matrix metalloproteinases in malignant ovarian tumor tissues. Cancer Lett. 120:109-115. https://doi.org/10.1016/S0304-3835(97)00295-4
  15. Lewandowski, K. C., J. Komorowski, C. J. O'Callaghan, B. K. Tan, J. Chen, G. M. Prelevic, and H. S. Randeva. 2006. Increased circulating levels of matrix metalloproteinase-2 and -9 in women with the polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 91:1173-1177. https://doi.org/10.1210/jc.2005-0648
  16. Liu, B., L. Y. Cai, H. M. Lv, L. Xia, Y. J. Zhang, H. X. Zhang, and Y. M. Guan. 2008. Raised serum levels of matrix metalloproteinase-9 in women with polycystic ovary syndrome and its association with insulin-like growth factor binding protein-1. Gynecol. Endocrinol. 24:285-288. https://doi.org/10.1080/09513590802056995
  17. Oksjoki, S., O. Rahkonen, M. Haarala, E. Vuorio, and L. Anttila. 2004. Differences in connective tissue gene expression between normally functioning, polycystic and postmenopausal ovaries. Mol. Hum. Reprod. 10:7-14. https://doi.org/10.1093/molehr/gah003
  18. Liu, B. H. 1998. Statistical Genomics: Linkage, Mapping, and QTL Analysis. CRC Press, Boca Raton, FL, USA.
  19. Liu, Y., H. U. Bernard, and D. Apt. 1997. NFI-B3, a novel transcriptional repressor of the nuclear factor I family, is generated by alternative RNA processing. J. Biol. Chem. 272:10739-10745. https://doi.org/10.1074/jbc.272.16.10739
  20. McCaffery, F. H., R. Leask, S. C. Riley, and E. E. Telfer. 2000. Culture of bovine preantral follicles in a serum-free system: markers for assessment of growth and development. Biol. Reprod. 63:267-273. https://doi.org/10.1095/biolreprod63.1.267
  21. Niu, B., F. Li, Y. Xiong, and X. Wang. 2013. Characterization and association analysis with litter size traits of porcine matrix metalloproteinase-9 gene (pMMP-9). Appl. Biochem. Biotechnol. 171:786-794. https://doi.org/10.1007/s12010-013-0396-7
  22. Page-McCaw, A., A. J. Ewald, and Z. Werb. 2007. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8:221-233. https://doi.org/10.1038/nrm2125
  23. Peluffo, M. C., M. J. Murphy, S. T. Baughman, R. L. Stouffer, and J. D. Hennebold. 2011. Systematic analysis of protease gene expression in the rhesus macaque ovulatory follicle: metalloproteinase involvement in follicle rupture. Endocrinology 152:3963-3974. https://doi.org/10.1210/en.2011-1172
  24. Pjanic, M., P. Pjanic, C. Schmid, G. Ambrosini, A. Gaussin, G. Plasari, C. Mazza, P. Bucher, and N. Mermod. 2011. Nuclear factor I revealed as family of promoter binding transcription activators. BMC Genomics 12:181. https://doi.org/10.1186/1471-2164-12-181
  25. Ribeiro, L. A., M. E. Turba, A. Zannoni, M. L. Bacci, and M. Forni. 2006. Gelatinases, endonuclease and Vascular Endothelial Growth Factor during development and regression of swine luteal tissue. BMC Dev. Biol. 6:58. https://doi.org/10.1186/1471-213X-6-58
  26. Takeuchi, K., S. Kubota, M. Kinoshita, H. Toyohara, and M. Sakaguchi. 2002. Cloning and characterization of cDNA for carp matrix metalloproteinase 9. Fish. Sci. 68:610-617. https://doi.org/10.1046/j.1444-2906.2002.00468.x
  27. Rodgers, R. J., H. F. Irving-Rodgers, and D. L. Russell. 2003. Extracellular matrix of the developing ovarian follicle. Reproduction 126:415-424. https://doi.org/10.1530/rep.0.1260415
  28. Sakata, K., K. Shigemasa, N. Nagai, and K. Ohama. 2000. Expression of matrix metalloproteinases (MMP-2, MMP-9, MT1-MMP) and their inhibitors (TIMP-1, TIMP-2) in common epithelial tumors of the ovary. Int. J. Oncol. 17:673-681.
  29. Shalev, E., S. Goldman, and I. Ben-Shlomo. 2001. The balance between MMP-9 and MMP-2 and their tissue inhibitor (TIMP)-1 in luteinized granulosa cells: comparison between women with PCOS and normal ovulatory women. Mol. Hum. Reprod. 7:325-331. https://doi.org/10.1093/molehr/7.4.325
  30. Tamakoshi, K., F. Kikkawa, A. Nawa, O. Maeda, M. Kawai, N. Sugamuma, S. Yamagata, and Y. Tomoda. 1994. Different pattern of zymography between human gynecologic normal and malignant tissues. Am. J. Obstet. Gynecol. 171:478-484. https://doi.org/10.1016/0002-9378(94)90286-0
  31. Van den Steen, P. E., B. Dubois, I. Nelissen, P. M. Rudd, R. A. Dwek, and G. Opdenakker. 2002. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit. Rev. Biochem. Mol. Biol. 37:375-536. https://doi.org/10.1080/10409230290771546
  32. Vandooren, J., P. E. Van den Steen, and G. Opdenakker. 2013. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9): The next decade. Crit. Rev. Biochem. Mol. Biol. 48:222-272. https://doi.org/10.3109/10409238.2013.770819
  33. Yeh, H. Y. and P. H. Klesius. 2008. Complete structure, genomic organization, and expression of channel catfish (Ictalurus punctatus, Rafinesque 1818) matrix metalloproteinase-9 gene. Biosci. Biotechnol. Biochem. 72:702-714. https://doi.org/10.1271/bbb.70579
  34. Zhu, G., L. Kang, Q. Wei, X. Cui, S. Wang, Y. Chen, and Y. Jiang. 2014. Expression and regulation of MMP1, MMP3, and MMP9 in the chicken ovary in response to gonadotropins, sex hormones, and TGFB1. Biol. Reprod. 90:57, 1-11.
  35. Zhu, G., L. Kang, C. Yang, X. Zhang, M. Wang, and Y. Jiang. 2012. Differential expression of CTGF in pre- and post-ovulatory granulosa cells in the hen ovary is regulated by TGFbeta1 and gonadotrophins. Gen. Comp. Endocrinol. 178:314-322. https://doi.org/10.1016/j.ygcen.2012.06.018

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