SciELO - Scientific Electronic Library Online

 
vol.18 issue6Characterization of the acetohydroxyacid synthase multigene family in the tetraploide plant Chenopodium quinoa author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google

Share


Electronic Journal of Biotechnology

On-line version ISSN 0717-3458

Electron. J. Biotechnol. vol.18 no.6 Valparaíso Nov. 2015

http://dx.doi.org/10.1016/j.ejbt.2015.08.003 

RESEARCH ARTICLE

Evidence of a role for prolactin as regulators of ovarian follicular development in goose

 

Rong Ma1, Dongmei Jiang1, Ziyu Chen, Bo Kang*

College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan 611130, PR China
Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan 611130, PR China
1 Contributed equally to this work.


ABSTRACT

Background

Prolactin (PRL) regulates development and reproduction, and its effects are mediated by the prolactin receptor (PRLR). In order to clarify the role of PRLR and PRL in the process of follicular development in the goose ovary, the level of PRLR mRNA expression in the ovary and follicles of the Sichuan white goose was determined, as well as the PRL concentration in ovarian follicles.

Results

The level of PRLR mRNA in the hierarchical follicles (HFs) initially increased, and subsequently decreased, whereas PRLR expression was initially low and later increased in postovulatory follicles (POFs). The level of PRLR mRNA expression was the highest in the F4 follicles, and lowest in the F1 follicles in all of the examined follicles. Compared with the level of PRLR mRNA expression in the small white follicles (SWFs), the level of PRLR mRNA was 2.86- and 1.44-fold higher in the F4 and small yellow follicles (SYFs), respectively (P < 0.05). The level of PRLR mRNA expression in the F4 follicles was highest (P < 0.05) in HFs. The highest PRL concentration in all of the examined samples was observed in SYFs and F1, with concentration of 6162 mLU/g and 6197 mLU/g, respectively. The PRL concentration in SYFs was significantly higher compared with SWFs (P < 0.05).

Conclusions

The change of PRL concentration was similar to the PRLR mRNA expression level in preovulatory follicles. These results suggest that the PRL mediated by the PRLR plays a stimulatory role in the SWF to SYF transition.

Keywords: Postovulatory follicle; Preovulatory follicle; Prolactin receptor; Prolactin; Sichuan white goose


 

1. Introduction

Prolactin (PRL) is a polypeptide hormone that is produced primarily in the anterior pituitary gland, and belongs to the prolactin/growth hormone family [1]. The PRL hormone is involved in a wide range of physiological processes in vertebrates, including metabolism, energy balance, and immunoregulation, and is essential for animal reproduction [2] and [3]. The effects of PRL are mediated by the prolactin receptor (PRLR) [4]. The binding of the PRL polypeptide to the PRLR activates intracellular signaling cascades, such as the JAK2/STAT5 signaling pathway, and regulates the expression of its various target genes [5] and [6]. In birds, the PRL is involved in the regulation of gonadal development and egg laying [7] and [8]. Previous studies have shown that PRL can suppress reproduction and induce nesting behavior in birds. The PRL hormone suppresses FSH-induced aromatase expression and estradiol production, and stimulates FSH-induced progesterone production in granulose cells [9]. However, recent studies have shown that PRL plays an important role in promoting follicular development [10], and that PRLR knockdown suppresses reproduction in female mice, indicating that PRLR may regulate reproduction [11]. The expression level of PRLR increases during the development of the mouse ovary, which suggested that PRLR was critical to ovarian function and fertility. The expression of PRLR increased at 12 h after treatment using pregnant mare serum gonadotrophin. It suggests that PRLR may affect follicular development and maturation [12]. The PRLR protein is expressed in oocytes, and prenatal mouse follicles treated with PRL have demonstrated an increased rate of oocyte maturation [13]. Thus, PRL plays an important dual role in animal reproductive processes. However, the level of PRLR gene expression and the concentration of PRL in the ovarian follicles of geese were unclear during the follicular development. The aim of our study was to determine the expression profile of the PRLR and the concentration of PRL in the ovarian follicles of Sichuan white geese. Our findings increase our understanding of the molecular mechanisms of follicular development and ovulation in geese.

2. Materials and methods

2.1. Experimental geese and tissue collection

Five healthy female Sichuan white geese were selected randomly from a local breeding farm and were conducted in accordance with the guidelines used at the farm. All of the geese were fed under uniform standard management in conditions of nature light. The geese were killed by exsanguinations to obtain ovaries along with the ovarian follicles. The follicles were separated from the ovary and weighed to identify the small white follicles (SWFs), small yellow follicles (SYFs), hierarchical follicles (from F5 to F1), postovulatory follicles (from POF1 to POF4), and ovary. All of the follicles were operated transversely along the stigma to completely eliminate the yolk material. The follicular membranes were washed with the ice-cold sterile saline, paying attention to ensuring that there was no adherent yolk material.

2.2. Extraction of total RNA and reverse transcription PCR

Total RNA was prepared from the geese hierarchical follicles by the Trizol reagent method (Takara Bio Inc., Dalian, China), and then stored at -80°C until analysis. cDNA was synthesized using PrimeScript® RT reagent Kit (Takara Bio Inc., Dalian, China), according to the manufacturer's instruction. Briefly, the 10 μL reaction consisted of 2.0 μL of total RNA, 2.0 μL of 5 × PrimeScript® Buffer, 0.5 μL of PrimeScript® RT Enzyme Mix, 0.5 μL of Random 6-mers, 0.5 μL of oligo dT Primer, and 4.5 μL of RNase Free H2O. Thermal cycling was performed with 15 min at 37°C, and then 5 s at 85°C. According to the reported CDS sequence of Anser anser (accession number: DQ209271) and Anas platyrhynchos (accession number: KC183720), gene-specific primers were designed by using Primer Premier 5.0, and then synthesized commercially by Shanghai Sangon (Shanghai, China). Primers for amplifying PRLR and glyceraldehydes-3-phosphate dehydrogenase (GAPDH) were as follows: PRLR forward primer: 5′-GCCTTTATCCTACCACCAGTTCC-3′ and PRLR reverse primer 5′-GATCCTCGCTGTCCTCTACCTCT-3′, GAPDH forward primer: 5′-GTGGTGCAAGAGGCATTGCTGAC-3′ and GAPDH reverse primer: 5′-GCTGATGCTCCCATGTTCGTGAT -3′. The 25 μL reaction consisted of 0.5 μL of cDNA, 4 μL of 2.5 mM deoxynucleoside triphosphate (dNTP) Mix, 1 μL of 20 μM of PCR forward primer and PCR reverse primer, 2.5 μL of 10 × PCR Buffer, 0.25 μL of 5U/μL Taq™ (Takara Bio Inc., Dalian, China), and 16.75 μL sterile Milli-Q water. Thermal cycling was performed with an initial denaturation step of 5 min at 95°C, followed by 35 cycles of 30 s at 95°C, 55°C for 30 s, and then 72°C for 30 s, and then a final extension at 72°C for 10 min.

2.3. Construction of PRLR and GAPDH cDNA plasmid

The recombinant plasmids containing PRLR and GAPDH cDNA were termed pPRLR and pGAPDH, respectively. The constructs were prepared from total RNA in the hierarchical follicles of the goose ovaries during the egg-laying stage, and the complementary double stranded cDNA fragments were subcloned into the pMD®19-T Vector (Takara Bio In, Dalian, China) as described.

2.4. qRT-PCR with SYBR Green I chemistry

The qRT-PCR was performed on the first strand cDNA using the Bio-Rad CFX Real-time PCR Detection System and software (BIO-RAD, California, USA) with SYBR® Premix Ex Taq™ (Takara Bio Inc., Dalian, China). Briefly, the 50 μL reaction consisted of 1 μL of cDNA, 25 μL of SYBR® Premix Ex Taq™ (2 × concentration), 2 μL of 20 μM of PCR forward primer and PCR reverse primer, and 22 μL of nuclease-free water. Thermal cycling was performed with an initial denaturation step of 10 s at 94°C, followed by 39 cycles of 5 s at 94°C, and 55°C for 30 s, and then a final extension at 72°C for 10 s. For generation of the standard curves, the pPRLR and pGAPDH standards were also run.

2.5. Determination of PRL concentration in each follicle

The PRL concentration was measured using the Goose Prolactin ELISA Kit (Beijing Gersion Bio-Technology Co. Ltd., Beijing, China). Following manufacturers' instructions, 0.1 g follicular samples were added to 1.0 mL saline and homogenized and then the supernatant was extracted. The standards and samples were added to the Microelisa Stripplate in two replicates and three replicates for each sample. For the set standard wells and the testing sample wells, 50 μL standard was added to the standard well and 10 μL testing sample was added to the testing sample well. Next, 40 μL Sample Diluent was added to the testing ample wells; nothing was added to the Blank wells. Then, 100 μL of HRP-conjugate reagent was added to each well, covered with an adhesive strip and incubated for 60 min at 37°C. Each well was aspirated and washed, repeating the process five times. Then, 50 μL of chromogen solution A and 50 μL of chromogen solution B were added to each well; the wells were gently mixed and incubated for 15 min at 37°C, protected from light. Then 50 μL Stop Solution was added to each well, and the Optical Density (OD) at 450 nm was read using a microtitre plate reader within 15 min.

2.6. Statistical analysis

Threshold and Ct (threshold cycle) values were determined automatically by the Bio-Rad CFX Real-time PCR Detection software, using default parameters. The relative level of expression for PRLR was calculated relative to GAPDH (the normalizer) using the 2− ΔΔCt method. The level of PRLR mRNA expression and the concentration of PRL was expressed as the mean of three means ± SD. The abundance of PRLR in the SWF of geese was assigned a value of 1. All data were analyzed using SAS statistical software for Windows (SAS Institute Inc., Cary, NC, USA). The data were analyzed by one-way ANOVA followed by Duncan's test. Differences were considered to be significant at P < 0.05.

3. Results

The RT-PCR analysis showed that the PRLR and GAPDH mRNAs were present in the hierarchical follicles during the egg-laying stages. The RT-PCR products for the PRLR and GAPDH mRNAs were 175 and 86 bp, respectively (Fig. 1), which corresponded to the predicted size for each, indicating an acceptable level of specificity for the qRT-PCR method. The qRT-PCR results showed that the expression of the PRLR mRNA in the hierarchical follicles increased during the early stages of follicular development, and subsequently decreased. The level of PRLR expression was the highest in the F4 follicles, and was lowest in F1 follicles. Except for the F1 follicles, the level of PRLR mRNA in the hierarchical follicles was significantly higher than that of the SWFs (P < 0.05), and the level of PRLR mRNA in the F4 follicles was 2.86-fold higher than that in the SWFs (P < 0.05). Furthermore, the level of PRLR mRNA in the F4 follicles was significantly greater than that in the F5, F3, F2, and F1 follicles (P < 0.05). No significant difference in the level of PRLR mRNA in the F5, F3, and F2 follicles was observed. With the exception of POF1, the level of PRLR mRNA in POFs increased over time. With the exception of POF2, the level of PRLR mRNA was significantly greater in the POFs than that in the SWFs, the F1 follicles, and the ovary (P < 0.05), and the level of PRLR mRNA in the SYFs was 1.44-fold higher than that in the SWFs (P < 0.05) (Fig. 2).

Fig. 1. Electrophoresis photograph of RT-PCR products for GAPDH and PRLR in the hierarchical follicles of Sichuan white goose ovary. The amplicons of 86 bp GAPDH, and 175 bp PRLR were separated on 15 g agarose L- 1 gels, stained with ethidium bromide, examined with ultraviolet light and visualized with a Gel-Pro Imager (Media Cybernetics, Maryland, USA). A 2000 bp molecular weight marker (M) was used.

Fig. 2. Relative expression of PRLR mRNA in the hierarchical follicles of Sichuan white goose ovary (n = 3). The expression levels of PRLR were normalized to GAPDH. The expression levels, calculated by the relative standard curve method, are presented in arbitrary units (AU). Values are means ± SD. The significance of differences in the levels of expression of PRLR mRNA was determined by ANOVA. Means with the same letter are not significantly different (P > 0.05).

 

The concentration of PRL in the preovulatory follicles increased from SWF to SYF, then decreased from SYF to F4, and finally increased. The highest PRL concentration of all samples that we observed in SYF and F1, with concentrations of 6162 mLU/g and 6197 mLU/g, respectively. The PRL concentration of SYF was significantly higher compared with SWF (P < 0.05). With the exception of POF1, the PRL concentration in POFs increased over time (Fig. 3).

Fig. 3. PRL concentration in the follicles measured using ELISA (n = 5). Values are means ± SD. The significance of differences in the PRL concentration in each follicle was determined by one-way ANOVA. All experiments were replicated three times. Means with the same letter are not significantly different (P < 0.05).

 

4. Discussion

The PRL hormone regulates reproduction in birds by inhibiting the secretion of luteinizing hormone [14]. In Gray geese, prolonged illumination has been shown to cause a short-term increase in egg production through increased PRL secretion [15]. Previous studies have suggested that PRL might enhance the effects of steroid hormones by promoting the expression of the PRLR and the luteinizing hormone receptor in follicular cells, which promotes follicular growth and increases egg production. Our results showed that the expression of PRLR mRNA increased during the initial stages of follicle maturation in the Sichuan white goose, and decreased during the later stages of follicular development. In birds, studies have shown that, the expression of PRL promotes the early stages of follicular development, but suppresses follicular development at later stages [10]. Therefore, PRL plays dual roles in stimulating and inhibiting reproduction in birds.

The expression of PRLR is regulated by sex hormones [16]. The expression profile of the PRLR hierarchical follicles observed in our study was similar to data from a previous study regarding the fluctuations in estrogen concentration in hierarchical follicles in geese [17]. Moreover, He et al. [18] reported that the estrogen concentration in follicles of the Sichuan white goose was similar to the expression of PRLR in HFs, there is high estrogen concentration and high expression level of PRLR in SYF, F4, F3, and F2 [18]. Thus, the expression of the PRLR may be regulated by estrogen.

In addition, SWF development was arrested in Gray geese immunized with a recombinant PRL fusion protein, preventing the formation of SYFs. These results suggest that PRL can stimulate follicular development because it is a key mediator of the SWF to SYF transition [10]. In our study, the PRL concentration of SYF was significantly higher compared with SWF (P < 0.05), which suggested that PRL might serve as a key mediator of SWF to SYF transition stimulating follicular development. Other studies have shown that treatment with anti-PRL antibodies inhibited the SWF to SYF transition, indicating that PRL is required for the development of SWFs. Thus, PRL plays a stimulatory role in ovarian follicular development [19]. Our data showed that the level of PRLR mRNA in SYFs was 1.44-fold higher than that in the SWF (P < 0.05), suggesting that the activation of SWF development by PRL might be mediated through the PRLR. The expression of PRLR in the sheep ovary has also been shown to be low during the early phases of follicular development [20], which is similar to our qRT-PCR results which showed that the level of PRLR mRNA was low in the SWFs of the Sichuan white goose.

Previous studies have suggested that decreased PRLR expression attenuates PRL actions in a number of peri-ovulatory events in certain ovarian cell types [21]. Our data showed that the level of PRLR mRNA in the F1 follicles was significantly lower than that in the F5, F4, F3, and F2 follicles (P < 0.05) and the PRL concentration was the highest in all HFs. In the F1 follicles, reduced PRLR expression may attenuate the PRL-mediated inhibition of follicular development, ultimately promoting ovulation. However, future studies will be employed to clarify our findings.

Both increasing the expression of the PRLR and stimulating the phosphorylation of the PRLR at Ser-349 can stimulate endocytosis and the degradation of the cell; ultimately result in reduced PRLR expression [22]. Physiologic follicular levels of PRL were associated with a significant increase in progesterone production in porcine cultured granulosa cells [23]. The PRL concentration was the highest in F1 follicles, which was able to increase the progesterone production. In addition, progesterone can suppress PRLR expression in the fallopian tube [16], and the concentration of progesterone peaks in the F1 follicle [17] and [24], suggesting that PRLR expression begins to decrease in the F1 follicle as a result of an increased level of progesterone.

Interestingly, the expression of PRLR and the PRL concentration had an almost opposite tendency in HFs. Previous studies have shown that hormones could decrease the expression of the receptor and reduced the affinity of receptor which was called down-regulation of receptor [25]. Thus, this phenomenon might be caused by down regulation of PRLR. When the secretion of PRL was excessive, the expression of PRLR would be gradually decreased, also decreased the affinity.

Postovulatory follicles do not form a corpus luteum in birds, but nonetheless serve a luteal function. The expression of PRLR is further enhanced during luteinization [26] and [27]. Our data showed that the expression of PRLR and PRL concentration have the same trend in POFs, which coincided with luteinization. Therefore, the PRLR-mediated effects of PRL might play a role in the regulation of postovulatory follicles in birds, that is similar to that of the mammalian corpus luteum. However, future studies are required to confirm our findings.

5. Conclusions

In conclusion, the level of PRLR mRNA in the HFs of the Sichuan white goose increased during the early stages of follicular development, and subsequently decreased. The level of PRLR mRNA in the SYFs was 1.44-fold higher than that in the SWFs (P < 0.05) and the PRL concentration in the SYFs was significantly higher than that in the SWFs (P < 0.05). Our results suggest that PRLR-mediated effects of PRL play a stimulatory role in the SWF to SYF transition. Future studies are warranted to determine the molecular mechanisms through which PRLR-mediated effects of PRL regulates the development of hierarchical and postovulatory follicles in birds.

Conflict of interest

There is no conflict of interest.

Financial support

The work was financially supported by the National Natural Science Foundation of China (No. 31201798) and the Specialized Research Fund for the Doctoral Program of Higher Education (No. 20105103120003).

References

1. Ben-Jonathan N, LaPensee CR, LaPensee EW.What can we learn from rodents about prolactin in humans? Endocr Rev 2008;29:1-41. http://dx.doi.org/10.1210/er.2007-0017.         [ Links ]

2. Bachelot A, Binart N. Reproductive role of prolactin. Reproduction 2007;133:361-9. http://dx.doi.org/10.1530/REP-06-0299.         [ Links ]

3. Grattan DR, Kokay IC. Prolactin: A pleiotropic neuroendocrine hormone. J Neuroendocrinol 2008;20:752-63. http://dx.doi.org/10.1111/j.1365-2826.2008.01736.x.         [ Links ]

4. Bu G, Wang CY, Cai G, Leung FC, Xu M, Wang H, et al. Molecular characterization of prolactin receptor (cPRLR) gene in chickens: Gene structure, tissue expression, promoter analysis, and its interaction with chicken prolactin (cPRL) and prolactin-like protein (cPRL-L). Mol Cell Endocrinol 2013;370:149-62. http://dx.doi.org/10.1016/j.mce.2013.03.001.         [ Links ]

5. Brooks CL. Molecularmechanisms of prolactin and its receptor. Endocr Rev 2012;33: 504-25. http://dx.doi.org/10.1210/er.2011-1040.         [ Links ]

6. Goffin V, Binart N, Touraine P, Kelly PA. Prolactin: The new biology of an old hormone. Annu Rev Physiol 2002;64:47-67. http://dx.doi.org/10.1146/annurev.physiol.64.081501.131049.         [ Links ]

7. March JB, Sharp PJ, Wilson PW, Sang HM. Effect of active immunization against recombinant-derived chicken prolactin fusion protein on the onset of broodiness and photoinduced egg laying in bantam hens. Reproduction 1994;101:227-33. http://dx.doi.org/10.1530/jrf.0.1010227.         [ Links ]

8. Sockman KW, Sharp PJ, Schwabl H. Orchestration of avian reproductive effort: An integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition. Biol Rev 2006;81:629-66. http://dx.doi.org/10.1111/j.1469-185X.2006.tb00221.x.         [ Links ]

9. Nakamura E, Otsuka F, Inagaki K, Miyoshi T, Yamanaka R, Tsukamoto N, et al. A novel antagonistic effect of the bonemorphogenetic protein systemon prolactin actions in regulating steroidogenesis by granulosa cells. Endocrinology 2010;151:5506-18. http://dx.doi.org/10.1210/en.2010-0265.         [ Links ]

10. Huang YM, Shi ZD, Tian YB. Research progress in effect of prolactin on promotion of follicles development in poultry. J Zhongkai Univ Agric Technol 2008;21:66-70.         [ Links ]

11. Kelly PA, Binart N, Lucas B, Bouchard B, Goffin V. Implications of multiple phenotypes observed in prolactin receptor knockout mice. Front Neuroendocrinol 2001;22:140-5. http://dx.doi.org/10.1006/frne.2001.0212.         [ Links ]

12. Luo A, Yang S, Shen W. Expression of ovarian prolactin receptor mRNA during follicular development and ovulation in the mouse. Chin J Histochem Cytochem 2010;19:390-3.         [ Links ]

13. Kiapekou E, Loutradis D, Mastorakos G, Bletsa R, Beretsos P, Zapanti E, et al. Effect of PRL on in vitro follicle growth, in vitro oocyte maturation, fertilization and early embryonic development in mice. Cloning Stem Cells 2009;11:293-300. http://dx.doi.org/10.1089/clo.2008.0046.         [ Links ]

14. Chaiseha Y, Halawani MEE. Neuroendocrinology of the female turkey reproductive cycle. J Poult Sci 2005;42:87-100. http://dx.doi.org/10.2141/jpsa.42.87.         [ Links ]

15. Huang YM, Shi ZD, Liu Z, Liu Y, Li XW. Endocrine regulations of reproductive seasonality, follicular development and incubation in Magang geese. Anim Reprod Sci 2008;104:344-58. http://dx.doi.org/10.1016/j.anireprosci.2007.02.005.         [ Links ]

16. Shao R, Nutu M, Weijdegard B, Egecioglu E, Rodriguez-Fernandez J, Tallet E, et al. Differences in prolactin receptor (PRLR) in mouse and human fallopian tubes: Evidence for multiple regulatory mechanisms controlling PRLR isoform expression in mice. Biol Reprod 2008;79:748-57. http://dx.doi.org/10.1095/biolreprod.108.070003.         [ Links ]

17. Chen X, Chen F, Jiang X, Ding J. Apoptosis of goose granulosa cells and its relationship with yolk 17β-estradiol and progesterone. J Yangzhou Univ Agric Life Sci Ed 2008; 29:30-4.         [ Links ]

18. He H, Jiang DM, Kang B, Ma R, Bai L, Wang X, et al. Gene expression profiling of melatonin receptor subtypes in the ovarian hierarchical follicles of the Sichuan white goose. Anim Reprod Sci 2014;145:62-8. http://dx.doi.org/10.1016/j.anireprosci.2013.12.012.         [ Links ]

19. LiWL, Liu Y, Yu YC, Huang YM, Liang SD, Shi ZD. Prolactin plays a stimulatory role in ovarian follicular development and egg laying in chicken hens. Domest Anim Endocrinol 2011;41:57-66. http://dx.doi.org/10.1016/j.domaniend.2011.03.002.         [ Links ]

20. Picazo RA, García Ruiz JP, Santiago Moreno J, González De Bulnes A, Muñoz J, Silván G, et al. Cellular localization and changes in expression of prolactin receptor isoforms in sheep ovary throughout the estrous cycle. Reproduction 2004;128:545-53. http://dx.doi.org/10.1530/rep.1.00343.         [ Links ]

21. Sangeeta Devi Y, Halperin J. Reproductive actions of prolactin mediated through short and long receptor isoforms. Mol Cell Endocrinol 2014;382:400-10. http://dx.doi.org/10.1016/j.mce.2013.09.016.         [ Links ]

22. Zhang F, Wang C, Huang J, Zhong J, Shi F. Progress in the study on prolactin receptor. Acta Ecol Anim Domastici 2009;30:6-9.         [ Links ]

23. Porter MB, Brumsted JR, Sites CK. Effect of prolactin on follicle-stimulating hormone receptor binding and progesterone production in cultured porcine granulosa cells. Fertil Steril 2000;73:99-105. http://dx.doi.org/10.1016/S0015-0282(99)00463-X.         [ Links ]

24. Qin Q, Sun A, Guo R, Lei M, Ying S, Shi Z. The characteristics of oviposition and hormonal and gene regulation of ovarian follicle development in Magang geese. Reprod Biol Endocrinol 2013;11:65. http://dx.doi.org/10.1186/1477-7827-11-65.         [ Links ]

25. Xu R, Jiang D. Effect of hormone on hormone receptor. Prog Physiol Sci 1983;14: 153-8.         [ Links ]

26. Stocco C, Telleria C, Gibori G. The molecular control of corpus luteum formation, function, and regression. Endocr Rev 2007;28:117-49. http://dx.doi.org/10.1210/er.2006-0022.         [ Links ]

27. Telleria CM, Parmer TG, Zhong L, Clarke DL, Albarracin CT, Duan WR, et al. The different forms of the prolactin receptor in the rat corpus luteum: Developmental expression and hormonal regulation in pregnancy. Endocrinology 1997;138: 4812-20. http://dx.doi.org/10.1210/endo.138.11.5479.         [ Links ]


*Corresponding author: E-mail address: albertkb119@163.com (B. Kang).

Received 4 April 2015, Accepted 4 August 2015, Available online 9 September 2015

Copyright © 2015 Pontificia Universidad Católica de Valparaíso. Production and hosting by Elsevier B.V. All rights reserved. Peer review under responsibility of Pontificia Universidad Católica de Valparaíso.

 

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License