Grass Carp Prolactin Gene: Structural Characterization and Signal Transduction for PACAP-induced Prolactin Promoter Activity

Overview

Journal Sci Rep

Specialty Science

Date 2018 Mar 17

PMID 29545542

Citations 4

Authors

Chengyuan Lin

Jin Bai

Mulan He

Anderson O L Wong

Affiliations

Soon will be listed here.

Abstract

In this study, structural analysis of grass carp prolactin (PRL) gene was performed and the signaling mechanisms for pituitary adenylate cyclase-activating peptide (PACAP) regulation of PRL promoter activity were investigated. In αT3-1 cells, PRL promoter activity could be induced by oPACAP which was blocked by PACAP antagonist but not the VIP antagonist. The stimulatory effect of oPACAP was mimicked by activation of AC/cAMP and voltage-sensitive Ca channel (VSCC) signaling, or induction of Ca entry. In parallel, PACAP-induced PRL promoter activity was negated or inhibited by suppressing cAMP production, inhibiting PKA activity, removal of extracellular Ca, VSCC blockade, calmodulin (CaM) antagonism, and inactivation of CaM kinase II. Similar sensitivity to L-type VSCC, CaM and CaM kinase II inhibition were also observed by substituting cAMP analog for oPACAP as the stimulant for PRL promoter activity. Moreover, PACAP-induced PRL promoter activity was also blocked by inhibition of PLC signaling, attenuation of [Ca]i immobilization via IP3 receptors, and blockade of PI3K/P pathway. The PACAP-induced PRL promoter activation may involve transactivation of the transcription factor CREB. These results suggest that PACAP can stimulate PRL promoter activation by PAC1 mediated functional coupling of the Ca/CaM/CaM kinase II cascades with the AC/cAMP/PKA pathway. Apparently, other signaling pathways, including PLC/IP3 and PI3K/P cascades, may also be involved in PACAP induction of PRL gene transcription.

Citing Articles

Differential involvement of cAMP/PKA-, PLC/PKC- and Ca/calmodulin-dependent pathways in GnRH-induced prolactin secretion and gene expression in grass carp pituitary cells.

Li W, Ye C, He M, Ko W, Cheng C, Chan Y Front Endocrinol (Lausanne). 2024; 15:1399274.

PMID: 38894746 PMC: 11183098. DOI: 10.3389/fendo.2024.1399274.

Activation of the PACAP/PAC1 Signaling Pathway Accelerates the Repair of Impaired Spatial Memory Caused by an Ultradian Light Cycle.

Xu D, Zhang Y, Feng J, Fu H, Li J, Wang W ASN Neuro. 2023; 15:17590914231169140.

PMID: 37071544 PMC: 10123913. DOI: 10.1177/17590914231169140.

Calcium/Calmodulin-Dependent Kinases in the Hypothalamus, Pituitary, and Pineal Gland: An Overview.

Cimini V, Van Noorden S, Terlizzi C, Altobelli G Int J Endocrinol. 2023; 2022:1103346.

PMID: 36601542 PMC: 9807307. DOI: 10.1155/2022/1103346.

Novel Mechanisms for IGF-I Regulation by Glucagon in Carp Hepatocytes: Up-Regulation of HNF1α and CREB Expression via Signaling Crosstalk for IGF-I Gene Transcription.

Bai J, Jiang X, He M, Chan B, Wong A Front Endocrinol (Lausanne). 2019; 10:605.

PMID: 31551932 PMC: 6734168. DOI: 10.3389/fendo.2019.00605.

References

Gerhold L, Sellix M, Freeman M . Antagonism of vasoactive intestinal peptide mRNA in the suprachiasmatic nucleus disrupts the rhythm of FRAs expression in neuroendocrine dopaminergic neurons. J Comp Neurol. 2002; 450(2):135-43. DOI: 10.1002/cne.10307. View

Jarry H, Leonhardt S, Schmidt W, Creutzfeldt W, Wuttke W . Contrasting effects of pituitary adenylate cyclase activating polypeptide (PACAP) on in vivo and in vitro prolactin and growth hormone release in male rats. Life Sci. 1992; 51(11):823-30. DOI: 10.1016/0024-3205(92)90609-s. View

Takakura M, Kyo S, Inoue M, Wright W, Shay J . Function of AP-1 in transcription of the telomerase reverse transcriptase gene (TERT) in human and mouse cells. Mol Cell Biol. 2005; 25(18):8037-43. PMC: 1234330. DOI: 10.1128/MCB.25.18.8037-8043.2005. View

Racz B, Tamas A, Kiss P, Toth G, Gasz B, Borsiczky B . Involvement of ERK and CREB signaling pathways in the protective effect of PACAP in monosodium glutamate-induced retinal lesion. Ann N Y Acad Sci. 2006; 1070:507-11. DOI: 10.1196/annals.1317.070. View

Ohkubo T, Tanaka M, Nakashima K . Molecular cloning of the chicken prolactin gene and activation by Pit-1 and cAMP-induced factor in GH3 cells. Gen Comp Endocrinol. 2000; 119(2):208-16. DOI: 10.1006/gcen.2000.7507. View

Bredow S, Kacsoh B, Obal Jr F, Fang J, Krueger J . Increase of prolactin mRNA in the rat hypothalamus after intracerebroventricular injection of VIP or PACAP. Brain Res. 1994; 660(2):301-8. DOI: 10.1016/0006-8993(94)91303-x. View

Meinkoth J, Montminy M, Fink J, Feramisco J . Induction of a cyclic AMP-responsive gene in living cells requires the nuclear factor CREB. Mol Cell Biol. 1991; 11(3):1759-64. PMC: 369493. DOI: 10.1128/mcb.11.3.1759-1764.1991. View

Liu J, Baker R, Chow W, Sun C, Elsholtz H . Epigenetic mechanisms in the dopamine D2 receptor-dependent inhibition of the prolactin gene. Mol Endocrinol. 2005; 19(7):1904-17. DOI: 10.1210/me.2004-0111. View

Gomez O, Balsa J . Autocrine/paracrine action of pituitary vasoactive intestinal peptide on lactotroph hyperplasia induced by estrogen. Endocrinology. 2003; 144(10):4403-9. DOI: 10.1210/en.2003-0261. View

10.

Christian H, Chapman L, Morris J . Thyrotrophin-releasing hormone, vasoactive intestinal peptide, prolactin-releasing peptide and dopamine regulation of prolactin secretion by different lactotroph morphological subtypes in the rat. J Neuroendocrinol. 2007; 19(8):605-13. DOI: 10.1111/j.1365-2826.2007.01567.x. View

11.

Chen H, Chiou C, Chang W . Cloning and characterization of the carp prolactin gene. Biochim Biophys Acta. 1991; 1088(2):315-8. DOI: 10.1016/0167-4781(91)90071-s. View

12.

Kawauchi H, Sower S . The dawn and evolution of hormones in the adenohypophysis. Gen Comp Endocrinol. 2005; 148(1):3-14. DOI: 10.1016/j.ygcen.2005.10.011. View

13.

Astola A, Ortiz M, Calduch-Giner J, Perez-Sanchez J, Valdivia M . Isolation of Sparus auratus prolactin gene and activity of the cis-acting regulatory elements. Gen Comp Endocrinol. 2003; 134(1):57-61. DOI: 10.1016/s0016-6480(03)00214-4. View

14.

Duan R, Ginsburg E, Vonderhaar B . Estrogen stimulates transcription from the human prolactin distal promoter through AP1 and estrogen responsive elements in T47D human breast cancer cells. Mol Cell Endocrinol. 2007; 281(1-2):9-18. DOI: 10.1016/j.mce.2007.10.004. View

15.

Cartin L, Lounsbury K, Nelson M . Coupling of Ca(2+) to CREB activation and gene expression in intact cerebral arteries from mouse : roles of ryanodine receptors and voltage-dependent Ca(2+) channels. Circ Res. 2000; 86(7):760-7. DOI: 10.1161/01.res.86.7.760. View

16.

Adamson A, Friedrichsen S, Semprini S, Harper C, Mullins J, White M . Human prolactin gene promoter regulation by estrogen: convergence with tumor necrosis factor-alpha signaling. Endocrinology. 2007; 149(2):687-94. PMC: 2342177. DOI: 10.1210/en.2007-1066. View

17.

Lin C, Jiang X, He M, Zhao L, Huang T, Bian Z . Mechanisms for PACAP-induced prolactin gene expression in grass carp pituitary cells. J Endocrinol. 2017; 233(1):37-51. DOI: 10.1530/JOE-16-0433. View

18.

Mijiddorj T, Kanasaki H, Purwana I, Oride A, Miyazaki K . Stimulatory effect of pituitary adenylate-cyclase activating polypeptide (PACAP) and its PACAP type I receptor (PAC1R) on prolactin synthesis in rat pituitary somatolactotroph GH3 cells. Mol Cell Endocrinol. 2011; 339(1-2):172-9. DOI: 10.1016/j.mce.2011.04.010. View

19.

Monnier D, Loeffler J . Pituitary adenylate cyclase-activating polypeptide stimulates proenkephalin gene transcription through AP1- and CREB-dependent mechanisms. DNA Cell Biol. 1998; 17(2):151-9. DOI: 10.1089/dna.1998.17.151. View

20.

Yan G, Chen X, Bancroft C . A constitutively active form of CREB can activate expression of the rat prolactin promoter in non-pituitary cells. Mol Cell Endocrinol. 1994; 101(1-2):R25-30. DOI: 10.1016/0303-7207(94)90255-0. View