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Cooperation of luteinizing hormone signaling pathways in preovulatory avian follicles regulates circadian clock expression in granulosa cell

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Abstract

Ovulation in birds is triggered by a surge of luteinizing hormone (LH), and the ovulatory cycle is affected by the circadian rhythms of clock genes transcription levels in follicles. The influence of LH signaling cascades action on circadian clock genes was investigated using granulosa cells of preovulatory follicles from Roman hens cultured in a serum-free system. The expression of core oscillators (Bmal1, Clock, Cry1, Per2, and Rev-erbβ), clock-controlled gene (Star), Egr-1 and LHr was measured by quantitative real-time PCR. Significant changes in clock genes transcription levels were observed in control groups over 24 h, indicating that cell-autonomous rhythms exist in granulosa cells. Intriguingly, the transcript levels of clock genes increased with LH treatment during 24 h of culture; they peaked 4 h in advance of controls and second but weaker oscillations were also observed. It appeared that LH changed the cell-autonomous rhythm and cycle time of clock genes. To further investigate the LH signaling cascades, inhibitors of cyclic adenosine monophosphate (cAMP), p38 mitogen-activated protein kinases (p38MAPK) and extracellular signal-regulated kinases 1 and 2 (ERK1/2) pathways were used. The transcript levels of clock genes were suppressed by blocking cAMP, but increased with similar expression patterns by blocking the p38MPAK and ERK1/2 pathways over 24 h. Thus, the influence of LH signaling cascades in chicken ovulation is mediated by the cAMP pathway and also involves the p38MAPK and ERK1/2 pathways.

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Abbreviations

LH:

Luteinizing hormone

CT:

Cycle time

DXM:

Dexamethasone

qPCR:

Quantitative real-time PCR

cAMP:

Cyclic adenosine monophosphate

p38MAPK:

p38 mitogen-activated protein kinases

ERK1/2:

Extracellular signal-regulated kinases 1 and 2

SCN:

Suprachiasmatic nucleus

cDNA:

Complementary DNA

ZT:

Zeitgeber time

AREG:

EGF-like growth factor

VLDLR:

Very low-density-lipoprotein receptor

EGFR:

EGF receptor

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Acknowledgments

This work was supported by the breeding research project of Sichuan Province (No. 2011NZ0099-7), the support program of Sichuan Province (No. 2011NZ0073) and the major projects of the department of agriculture (No. CARS-41).

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Authors and Affiliations

  1. Laboratory of Animal Genetic and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Ya’an, 625014, Sichuan, China

    Liang Li, Zhichao Zhang, Jiyun Peng, Yagang Wang & Qing Zhu

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  1. Liang Li
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  2. Zhichao Zhang
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  3. Jiyun Peng
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  4. Yagang Wang
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  5. Qing Zhu
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Correspondence to Qing Zhu.

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Liang Li and Zhichao Zhang have contributed equally to this work.

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Li, L., Zhang, Z., Peng, J. et al. Cooperation of luteinizing hormone signaling pathways in preovulatory avian follicles regulates circadian clock expression in granulosa cell. Mol Cell Biochem 394, 31–41 (2014). https://doi.org/10.1007/s11010-014-2078-3

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  • DOI: https://doi.org/10.1007/s11010-014-2078-3

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