CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Reproduction, Fertility and Development   
Reproduction, Fertility and Development
Journal Banner
  Vertebrate Reproductive Science & Technology
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Board
Contacts
Content
Online Early
Current Issue
Just Accepted
All Issues
Special Issues
Research Fronts
Sample Issue
For Authors
General Information
Instructions to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review Article
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates

blue arrow e-Alerts
blank image
Subscribe to our email Early Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook   youtube

Affiliated Societies

RFD is the official journal of the International Embryo Transfer Society and the Society for Reproductive Biology.


 

Article << Previous     |     Next >>        Online Early    

Follicular dynamics and gene expression in granulosa cells, corpora lutea and oocytes from gilts of breeds with low and high ovulation rates

P. V. Silva A, S. E. F. Guimarães A E, J. D. Guimarães B, C. S. Nascimento A, P. S. Lopes A, J. B. Siqueira A, L. S. Amorim B, F. Fonseca e Silva C and G. R. Foxcroft D

A Departamento de Zootecnia, Universidade Federal de Vicosa, Vicosa 36570-000, MG, Brasil.
B Departamento de Veterinária, Universidade Federal de Vicosa, Vicosa 36570-000, MG, Brasil.
C Departamento de Estatística, Universidade Federal de Vicosa, Vicosa 36570-000, MG, Brasil.
D Swine Reproduction-Development Program, Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton T6G 2P5, AB, Canada.
E Corresponding author. Email: sfacioni@ufv.br

Reproduction, Fertility and Development - http://dx.doi.org/10.1071/RD12257
Submitted: 7 August 2012  Accepted: 12 January 2013   Published online: 7 March 2013


 
PDF (1.2 MB) $25
 Supplementary Material
 Export Citation
 Print
  
Abstract

Follicular dynamics and the expression of candidate genes using real-time polymerase chain reaction (PCR) were compared during the oestrous cycle of pig breeds with high (commercial line; n = 24) and low (local Brazilian Piau; n = 21) ovulation rates and prolificacy. Gilts were killed on Days 0, 4, 10 and 18 of the oestrous cycle and visible ovarian follicles were classified by follicular diameter. Recovered cumulus–oocyte complexes were classified as normal or atretic and frozen in liquid nitrogen until RNA extraction. Low ovulation rates and/or prolificacy in Piau gilts was associated with a different pattern of follicle development, with lower numbers of small follicles on Day 18, fewer large follicles on Days 0 and 18 (P ≤ 0.05) and a higher proportion of atretic follicles on Days 0 and 18 (P ≤ 0.05). Compared with commercial line gilts, less-prolific Piau gilts exhibited higher expression of apoptotic genes during luteolysis (CASP3 and FASL; P ≤ 0.05), decreased expression of TGFBR2 and BAX mRNA in the corpus luteum (P ≤ 0.05), higher expression of apoptotic genes (FAS, BCL2 and CASP8; P ≤ 0.05) in granulosa cells and a greater abundance (P ≤ 0.05) of genes controlling oocyte-secreted factors (GDF9, BMP15 and BMP6), suggesting underlying mechanisms controlling differences in follicular development, ovulation rate and inherent prolificacy in this pig breed.

Additional keywords: growth factors, litter size, ovulation.


References

Bazer, F. W., Thatcher, W. W., Martinat-Botte, F., and Terqui, M. (1988a). Conceptus development in Large White and prolific Chinese Meishan pigs. J. Reprod. Fertil. 84, 37–42.
CrossRef | CAS | PubMed |

Bazer, F. W., Thatcher, W. W., Martinat-Botte, F., and Terqui, M. (1988b). Sexual maturation and morphological development of the reproductive tract in large white and prolific Chinese Meishan pigs. J. Reprod. Fertil. 83, 723–728.
CrossRef | CAS | PubMed |

Berardinelli, ., Russo, V., Martelli, A., Nardinocchi, D., Di Giacinto, O., Barboni, B., and Mattioli, M. (2004). Colocalization of DNA fragmentation and caspase-3 activation during atresia in pig antral follicles. Anat. Histol. Embryol. 33, 23–27.
CrossRef | CAS | PubMed |

Bonnet, A., Lê, C. K., Sancristobal, M., Benne, F., Robert-Granié, C., Law-So, G., Fabre, S., Besse, ., De Billy, E., Quesnel, H., Hatey, F., and Tosser-Klopp, G. (2008). In vivo gene expression in granulosa cells during pig terminal follicular development. Reproduction 136, 211–224.
CrossRef | CAS | PubMed |

Boone, D. L., and Tsang, B. K. (1998). Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol. Reprod. 58, 1533–1539.
CrossRef | CAS | PubMed |

Choi, D., Hwang, S., Lee, E., Yoon, S., Yoon, B. K., and Bae, D. (2004). Expression of mitochondria-dependent apoptosis genes (p53, Bax, and Bcl-2) in rat granulosa cells during follicular development. J. Soc. Gynecol. Invest. 11, 311–317.
CrossRef | CAS |

Clark, J. R., Eday, T. N., First, N. L., Chapman, A. B., and Casida, L. E. (1973). The effects of four genetic groups and two feed levels of feeding on ovulation rate and follicular development in pubertal gilts. J. Anim. Sci. 36, 1164–1169.
| CAS | PubMed |

Dharma, S. J., Kelkar, R. L., and Nandedkar, T. D. (2003). Fas and Fas ligand protein and mRNA in normal and atretic mouse ovarian follicles. Reproduction 126, 783–789.
CrossRef | CAS | PubMed |

Erickson, G. F., and Shimasaki, S. (2003). The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod. Biol. Endocrinol. 1, 1–20.

Faillace, L. S., and Hunter, M. G. (1994). Follicle development and oocyte maturation during the immediate preovulatory period in Meishan and White hybrid gilts. J. Reprod. Fertil. 101, 571–576.
CrossRef | CAS | PubMed |

Feary, E. S., Juengel, J. L., Smith, ., French, M. C., O’connell, A. R., Lawrence, S. B., Galloway, S. M., Davis, G. H., and Mcnatty, K. . (2007). Patterns of expression of messenger RNAs encoding GDF9, BMP15, TGFBR1, BMPR1B, and BMPR2 during follicular development and characterization of ovarian follicular populations in ewes carrying the Woodlands FecX2W mutation. Biol. Reprod. 77, 990–998.
CrossRef | CAS | PubMed |

Foxcroft, G. R., and Hunter, M. G. (1985). Basic physiology of follicular maturation in the pig. J. Reprod. Fertil. Suppl. 33, 1–19.
| CAS | PubMed |

Foxcroft, G. R., Cosgrove, J., Ding, J., Hofacker, S., and Wiesak, T. (1994). Reproductive function: current concepts. In ‘Principles of Pig Science’. (Eds D. J. A. Cole, J. Wiseman and M. Varley.) pp. 225–252. (Nottingham University Press: Nottingham, UK.)

Gilchrist, R. B., and Ritter, L. J. (2011). Differences in the participation of TGFB superfamily signalling pathways mediating porcine and murine cumulus cell expansion. Reproduction 142, 647–657.
CrossRef | CAS | PubMed |

Gilchrist, R. B., Ritter, L. J., and Armstrong, D. T. (2004). Oocyte–somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82–83, 431–446.
CrossRef | PubMed |

Gilchrist, R. B., Lane, M., and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–177.
CrossRef | CAS | PubMed |

Glister, C., Kemp, C. F., and Knight, . G. (2004). Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4,-6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin. Reproduction 127, 239–254.
CrossRef | CAS | PubMed |

Goodman, S. B., Kugu, K., Chen, S. H., Preutthipan, S., Tilly, K. I., Tilly, J. L., and Dharmarajan, A. M. (1998). Estradiol-mediated suppression of apoptosis in the rabbit corpus luteum is associated with a shift in expression of bcl-2 family members favoring cellular survival. Biol. Reprod. 59, 820–827.
CrossRef | CAS | PubMed |

Grant, S. A., Hunter, M. G., and Foxcroft, G. R. (1989). Morphological and biochemical characteristics during ovarian follicular development in the pig. J. Reprod. Fertil. 86, 171–183.
CrossRef | CAS | PubMed |

Griffin, T. J., Gygi, S. ., Ideker, T., Rist, B., Eng, J., Hood, L., and Aebersold, R. (2002). Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol. Cell. Proteomics 1, 323–333.
CrossRef | CAS | PubMed |

Guthrie, H. D. (2005). The follicular phase in pigs: follicle populations, circulating hormones, follicle factors and oocytes. J. Anim. Sci. 83, 79–89.

Guthrie, H. D., Grimes, R. W., Cooper, B. S., and Hammond, J. M. (1995). Follicular atresia in pigs: measurement and physiology. J. Anim. Sci. 73, 2834–2844.
| CAS | PubMed |

Haley, C. S., and Lee, G. J. (1993). Genetic basis of prolificacy in Meishan pigs. J. Reprod. Fertil. Suppl. 48, 247–259.
| CAS | PubMed |

Hsu, S. Y., Lai, R. J., Finegold, M., and Hsueh, A. J. (1996). Targeted overexpression of Bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. Endocrinology 137, 4837–4843.
CrossRef | CAS | PubMed |

Hunter, M. G., and Paradis, F. (2009). Intra-follicular regulatory mechanisms in the porcine ovary. Soc. Reprod. Fertil. Suppl. 66, 149–164.
| CAS | PubMed |

Hunter, M. G., and Picton, H. M. (1995). Effect of hCG administration at the onset of oestrus on early embryo survival and development in Meishan gilts. Anim. Reprod. Sci. 38, 231–238.
CrossRef | CAS |

Hunter, M. G., and Wiesak, T. (1990). Evidence for and implications of follicular heterogeneity in pigs. J. Reprod. Fertil. Suppl. 40, 163–177.
| CAS | PubMed |

Hunter, M. G., Biggs, C., Foxcroft, G. R., McNeilly, A. S., and Tilton, J. E. (1993). Comparisons of endocrinology and behavioural events during the periovulatory period in Meishan and Large–White hybrid gilts. J. Reprod. Fertil. 97, 475–480.
CrossRef | CAS | PubMed |

Hunter, M. G., Robinson, R. S., Mann, G. E., and Webb, R. (2004). Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim. Reprod. Sci. 82–83, 461–477.
CrossRef | PubMed |

Hussein, M. R. (2005). Apoptosis in the ovary: molecular mechanisms. Hum. Reprod. Update 11, 162–178.
| PubMed |

Inoue, N., Maeda, A., Matsuda-Minehata, F., Fukuta, K., and Manabe, N. (2006). Expression and localization of Fas ligand and Fas during atresia in porcine ovarian follicles. J. Reprod. Dev. 52, 723–730.
CrossRef | CAS | PubMed |

Inoue, N., Matsuda, F., Goto, Y., and Manabe, N. (2011). Role of cell-death ligand–receptor system of granulosa cells in selective follicular atresia in porcine ovary. J. Reprod. Dev. 57, 169–175.
CrossRef | CAS | PubMed |

Juengel, J. L., and McNatty, K. . (2005). The role of proteins of the transforming growth factor-β superfamily in the intraovarian regulation of follicular development. Hum. Reprod. 11, 144–161.

Juengel, J. L., Garverick, H. A., Johnson, A. L., Youngquist, R. S., and Smith, M. F. (1993). Apoptosis during luteal regression in cattle. Endocrinology 132, 249–254.
CrossRef | CAS | PubMed |

Knox, R. V. (2005). Recruitment and selection of ovarian follicles for determination of ovulation rate in the pig. Domest. Anim. Endocrinol. 29, 385–397.
CrossRef | CAS | PubMed |

Kondo, H., Maruo, T., Peng, X., and Mochizuki, M. (1996). Immunological evidence for the expression of the Fas antigen in the infant and adult human ovary during follicular regression and atresia. J. Clin. Endocrinol. Metab. 81, 2702–2710.
CrossRef | CAS | PubMed |

Krajewska, M., Wang, H. G., Krajewski, S., Zapata, J. M., Shabaik, A., Gascoyne, R., and Reed, J. C. (1997). Immunohistochemical analysis of in vivo patterns of expression of CPP32 (caspase-3), a cell death protease. Cancer Res. 57, 1605–1613.
| CAS | PubMed |

Li, H. K., Kuo, T. Y., Yang, H. S., Chen, L. R., Li, S. S.-L., and Huang, H. W. (2008). Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos. Anim. Reprod. Sci. 103, 312–322.
CrossRef | CAS | PubMed |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCt method. Methods 25, 402–408.
CrossRef | CAS | PubMed |

Manabe, N., Goto, Y., Matsuda-Minehata, F., Inoue, N., Maeda, A., Sakamaki, K., and Miyano, T. (2004). Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J. Reprod. Dev. 50, 493–514.
CrossRef | PubMed |

Matsuda-Minehata, F., Maeda, A., Cheng, Y., Sai, T., Gonda, H., Goto, Y., and Manabe, N. (2008). Regulation of granulosa cell apoptosis by death ligand–receptor signaling. Anim. Sci. 79, 1–10.
| CAS |

McNatty, K. ., Moore, L. G., Hudson, N. L., Quirke, L. D., Lawrence, S. B., Reader, K., Hanrahan, J. ., Smith, ., Groome, N. ., Laitinen, M., Ritvos, O., and Luengel, J. L. (2004). The oocyte and its role in regulating ovulation rate: a new paradigm in reproductive biology. Reproduction 128, 379–386.
CrossRef | CAS | PubMed |

Miller, A. T., Picton, H. M., Craigon, J., and Hunter, M. G. (1998). Follicle dynamics and aromatase activity in high-ovulating Meishan sows and in Large–White hybrid contemporaries. Biol. Reprod. 58, 1372–1378.
CrossRef | CAS | PubMed |

Miyashita, T., Krajewski, S., Krajewska, M., Wang, H. G., Lin, H. K., Liebermann, D., Hoffman, A. B., and Reed, J. C. (1994). Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9, 1799–1805.
| CAS | PubMed |

Oltval, Z. N., Milliman, C. L., and Korsmeyer, S. J. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609–619.
CrossRef |

Otsuka, F., Moore, R. K., and Shimasaki, S. (2001). Biological function and cellular mechanism of bone morphogenetic protein-6 in the ovary. J. Biol. Chem. 276, 32 889–32 895.
CrossRef | CAS |

Paradis, F., Novak, S., Murdoch, G. K., Dyck, M. K., Dixon, W. T., and Foxcroft, G. R. (2009). Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction 138, 115–129.
CrossRef | CAS | PubMed |

Porter, D. A., Harman, R. M., Cowan, R. G., and Quirk, S. M. (2001). Relationship of Fas ligand expression and atresia during bovine follicle development. Reproduction 121, 561–566.
CrossRef | CAS | PubMed |

Pretheeban, T., Balendran, A., Gordon, M. B., and Rajamahendran, R. (2010). mRNA of luteal genes associated with progesterone synthesis, maintenance, and apoptosis in dairy heifers and lactating dairy cows. Anim. Reprod. Sci. 121, 218–224.
CrossRef | CAS | PubMed |

Quinn, R. L., Shuttleworth, G., and Hunter, M. G. (2004). Immunohistochemical localization of the bone morphogenetic protein receptors in the porcine ovary. J. Anat. 205, 15–23.
CrossRef | CAS | PubMed |

R Development Core Team (2008). ‘R: A Language and Environment for Statistical Computing’. (R Foundation for Statistical Computing: Vienna.) Available from http://www.R-project.org [Verified 8 August 2012].

Rátky, J., Torner, H., Egerszegi, I., Schneider, F., Sarlos, ., Manabe, N., and Brüssow, K. . (2005). Ovarian activity and oocyte development during follicular development in pigs at different reproductive phases estimated by the repeated endoscopic method. J. Reprod. Dev. 51, 109–115.
CrossRef | PubMed |

Rodger, F. E., Fraser, H. M., Duncan, W. C., and Illingworth, . J. (1995). Immunolocalization of Bcl-2 in the human corpus luteum. Hum. Reprod. 10, 1566–1570.
CrossRef | CAS | PubMed |

Rueda, B. R., Hamernik, D. L., Hoyer, P. B., and Tilly, J. L. (1997). Potential regulators of physiological cell death in the corpus luteum. In ‘Cell Death in Reproductive Physiology. Serono Symposia’. (Eds J. L. Tilly, J. Strauss and M. Tenniswood.) pp. 161–181. (Springer Verlag: New York.)

Rueda, B. R., Hendry, I. R., Tilly, J. L., and Hamernik, D. L. (1999). Accumulation of caspase-3 messenger ribonucleic acid and induction of caspase activity in the ovine corpus luteum following prostaglandin F2alpha treatment in vivo. Biol. Reprod. 60, 1087–1092.
CrossRef | CAS | PubMed |

Sakamaki, K., Yoshida, H., Nishimura, Y., Nishikawa, S., Manabe, N., and Yonehara, S. (1997). Involvement of Fas antigen in ovarian follicular atresia and luteolysis. Mol. Reprod. Dev. 47, 11–18.
CrossRef | CAS | PubMed |

Shimasaki, S., Moore, R. K., Otsuka, F., and Erickson, G. F. (2004). The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25, 72–101.
CrossRef | CAS | PubMed |

Silva, P. V., Guimarães, S. E. F., Oliver, G., Patterson, J., Smit, M., Dixon, W. T., and Foxcroft, G. R. (2011). Comparison of gene expression between High and Low birth weight phenotype in pigs using EmbryoGENE microarray. PowerPoint presented at EmbryoGENE Annual General Meeting, 2011. Quebec City, Quebec, Canada. Available from http://embryogene.ca/kms/files/Priscila%20Silva[1].pdf [Verified 3 February 2013].

Singh, B., Barbe, G. J., and Armstrong, D. T. (1993). Factors influencing resumption of meiotic maturation and cumulus expansion of porcine oocyte-cumulus cell complexes in vitro. Mol. Reprod. Dev. 36, 113–119.
CrossRef | CAS | PubMed |

Sirois, J., and Fortune, J. E. (1988). Ovarian follicular dynamics during the estrous cycle in heifers monitored by real-time ultrasonography. Biol. Reprod. 39, 308–317.
CrossRef | CAS | PubMed |

Sriperumbudur, R., Zorrilla, L., and Gadsby, J. E. (2010). Transforming growth factor-β (TGF-β) and its signaling components in peri-ovulatory pig follicles. Anim. Reprod. Sci. 120, 84–94.
CrossRef | CAS | PubMed |

Sugino, N., Suzuki, T., Kashida, S., Karube, A., Takiguchi, S., and Kato, H. (2000). Expression of Bcl-2 and Bax in the human corpus luteum during the menstrual cycle and in early pregnancy: regulation by human chorionic gonadotropin. J. Clin. Endocrinol. Metab. 85, 4379–4386.
CrossRef | CAS | PubMed |

Sun, R. Z., Lei, L., Cheng, L., Jin, Z. F., Zu, S. J., Shan, Z. Y., Wang, Z. D., Zhang, J. X., and Liu, Z. H. (2010). Expression of GDF-9, BMP-15 and their receptors in mammalian ovary follicles. J. Mol. Histol. 41, 325–332.
CrossRef | CAS | PubMed |

Tilly, J. L. (1996). Apoptosis and ovarian function. Rev. Reprod. 1, 162–172.
CrossRef | CAS | PubMed |

Webb, R., Garnsworthy, . C., Campbell, B. K., and Hunter, M. G. (2007). Intra-ovarian regulation of follicular development and oocyte competence in farm animals. Theriogenology 68, S22–S29.
CrossRef | CAS | PubMed |

Xu, X., Faillace, L. S., Harding, R. T., Foxcroft, G. R., and Hunter, M. G. (1998). Evidence that Meishan and Large–White hybrid preovulatory follicles may differentially affect oocyte in vitro maturation and fertilization. Anim. Reprod. Sci. 51, 307–319.
CrossRef | CAS | PubMed |

Zeng, F., Baldwin, D., and Schultz, R. M. (2004). Transcript profiling during preimplantation mouse development. Dev. Biol. 272, 483–496.
CrossRef | CAS | PubMed |

Zhu, G., Guo, B., Pan, D., Mu, Y., and Feng, S. (2008). Expression of bone morphogenetic proteins and receptors in porcine cumulus–oocyte complexes during in vitro maturation. Anim. Reprod. Sci. 104, 275–283.
CrossRef | CAS | PubMed |


   
Subscriber Login
Username:
Password:  

 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2013