Effects of Prolactin Inhibition on Lipid Metabolism in Goats

Overview

Journal Animals (Basel)

Date 2024 Dec 17

PMID 39682330

Authors

Xiaona Liu

Chunhui Duan

Xuejiao Yin

Xianglong Li

Meijing Chen

Jiaxin Chen

Wen Zhao

Lechao Zhang

Yueqin Liu

Yingjie Zhang

Affiliations

Soon will be listed here.

Abstract

Prolactin (PRL) has recently been found to play a role in lipid metabolism in addition to its traditional roles in lactation and reproduction. However, the effects of PRL on lipid metabolism in liver and adipose tissues are unclear. Therefore, we aimed to study the role of PRL on lipid metabolism in goats. Twenty healthy eleven-month-old Yanshan cashmere goats with similar body weights (BWs) were selected and randomly divided into a control (CON) group and a bromocriptine (BCR, a PRL inhibitor, 0.06 mg/kg, BW) group. The experiment lasted for 30 days. Blood was collected on the day before BCR treatment (day 0) and on the 15th and 30th days after BCR treatment (days 15 and 30). On day 30 of treatment, all goats were slaughtered to collect their liver, subcutaneous adipose, and perirenal adipose tissues. A portion of all collected tissues was stored in 4% paraformaldehyde for histological observation, and another portion was immediately stored in liquid nitrogen for RNA extraction. The PRL inhibition had inconclusive effects found on BW and average daily feed intake (ADFI) in goats ( > 0.05). PRL inhibition decreased the hormone-sensitive lipase (HSL) levels on day 30 ( < 0.05), but the effects were inconclusive on days 0 and 15. PRL inhibition had inconclusive effects found on total cholesterol (TCH), triglyceride (TG), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), fatty acid synthase (FAS), 3-hydroxy-3-methylglutaryl-CoA reductase (HMGR), and acetyl-CoA carboxylase (ACC) on days 0, 15, and 30 ( > 0.05). Furthermore, hematoxylin-eosin (HE) staining of the liver, subcutaneous adipose, and perirenal adipose sections showed that PRL inhibition had inconclusive effects on the pathological changes in their histomorphology ( > 0.05), but measuring adipocytes showed that the area of perirenal adipocytes decreased in the BCR group ( < 0.05). The qPCR results showed that PRL inhibition increased the expression of , long-form PRL receptor and short-form PRL receptor genes, as well as the expression of genes related to lipid metabolism, including sterol regulatory element binding transcription factor 1 (); sterol regulatory element binding transcription factor 2 (); acetyl-CoA carboxylase alpha (); fatty acid synthase (); 3-hydroxy-3-methylglutaryl-CoA reductase (); 7-dehydrocholesterol reductase (); peroxisome proliferator-activated receptor gamma (); and lipase E, hormone-sensitive type () in the liver ( < 0.05). In the subcutaneous adipose tissue, PRL inhibition increased gene expression ( < 0.05) and decreased the expression of genes related to lipid metabolism, including and ( < 0.05). In the perirenal adipose tissue, the inhibition of PRL decreased the expression of the , and genes ( < 0.05). In conclusion, the inhibition of PRL decreases the serum HSL levels in cashmere goats; the effects of PRL on lipid metabolism are different in different tissues; and PRL affects lipid metabolic activity by regulating different PRLRs in liver and subcutaneous adipose tissues, as well as by decreasing the expression of the and genes in perirenal adipose tissue.

References

Eisemann J, Bauman D, HOGUE D, TRAVIS H . Influence of photoperiod and prolactin on body composition and in vitro lipid metabolism in wether lambs. J Anim Sci. 1984; 59(1):95-104. DOI: 10.2527/jas1984.59195x. View

Harvey S, Aramburo C, Sanders E . Extrapituitary production of anterior pituitary hormones: an overview. Endocrine. 2011; 41(1):19-30. DOI: 10.1007/s12020-011-9557-z. View

Le J, Wilson H, Shehu A, Devi Y, Aguilar T, Gibori G . Prolactin activation of the long form of its cognate receptor causes increased visceral fat and obesity in males as shown in transgenic mice expressing only this receptor subtype. Horm Metab Res. 2011; 43(13):931-7. PMC: 3799815. DOI: 10.1055/s-0031-1291182. View

Bernard V, Young J, Chanson P, Binart N . New insights in prolactin: pathological implications. Nat Rev Endocrinol. 2015; 11(5):265-75. DOI: 10.1038/nrendo.2015.36. View

Macotela Y, Ruiz-Herrera X, Vazquez-Carrillo D, Ramirez-Hernandez G, Martinez de la Escalera G, Clapp C . The beneficial metabolic actions of prolactin. Front Endocrinol (Lausanne). 2022; 13:1001703. PMC: 9539817. DOI: 10.3389/fendo.2022.1001703. View

Doknic M, Pekic S, Zarkovic M, Medic-Stojanoska M, Dieguez C, Casanueva F . Dopaminergic tone and obesity: an insight from prolactinomas treated with bromocriptine. Eur J Endocrinol. 2002; 147(1):77-84. DOI: 10.1530/eje.0.1470077. View

Freeman M, Kanyicska B, Lerant A, Nagy G . Prolactin: structure, function, and regulation of secretion. Physiol Rev. 2000; 80(4):1523-631. DOI: 10.1152/physrev.2000.80.4.1523. View

Wang S, Liu J, Zhao W, Wang G, Gao S . Selection of candidate genes for differences in fat metabolism between cattle subcutaneous and perirenal adipose tissue based on RNA-seq. Anim Biotechnol. 2021; 34(3):633-644. DOI: 10.1080/10495398.2021.1991937. View

Landgraf R, Weissmann A, Horl R, von Werder K, Scriba P . Prolactin: a diabetogenic hormone. Diabetologia. 1977; 13(2):99-104. DOI: 10.1007/BF00745135. View

10.

Zhang P, Ge Z, Wang H, Feng W, Sun X, Chu X . Prolactin improves hepatic steatosis via CD36 pathway. J Hepatol. 2018; 68(6):1247-1255. DOI: 10.1016/j.jhep.2018.01.035. View

11.

Manning B, Toker A . AKT/PKB Signaling: Navigating the Network. Cell. 2017; 169(3):381-405. PMC: 5546324. DOI: 10.1016/j.cell.2017.04.001. View

12.

Liu X, Duan C, Yin X, Zhang L, Chen M, Zhao W . Inhibition of Prolactin Affects Epididymal Morphology by Decreasing the Secretion of Estradiol in Cashmere Bucks. Animals (Basel). 2024; 14(12). PMC: 11201029. DOI: 10.3390/ani14121778. View

13.

Bina K, Cincotta A . Dopaminergic agonists normalize elevated hypothalamic neuropeptide Y and corticotropin-releasing hormone, body weight gain, and hyperglycemia in ob/ob mice. Neuroendocrinology. 2000; 71(1):68-78. DOI: 10.1159/000054522. View

14.

Li Y, Wang M, Li Q, Gao Y, Li Q, Li J . Transcriptome profiling of longissimus lumborum in Holstein bulls and steers with different beef qualities. PLoS One. 2020; 15(6):e0235218. PMC: 7316285. DOI: 10.1371/journal.pone.0235218. View

15.

Brelje T, Stout L, Bhagroo N, Sorenson R . Distinctive roles for prolactin and growth hormone in the activation of signal transducer and activator of transcription 5 in pancreatic islets of langerhans. Endocrinology. 2004; 145(9):4162-75. DOI: 10.1210/en.2004-0201. View

16.

Strader A, Buntin J . Changes in agouti-related peptide during the ring dove breeding cycle in relation to prolactin and parental hyperphagia. J Neuroendocrinol. 2003; 15(11):1046-53. DOI: 10.1046/j.1365-2826.2003.01092.x. View

17.

Zinger M, McFarland M, Ben-Jonathan N . Prolactin expression and secretion by human breast glandular and adipose tissue explants. J Clin Endocrinol Metab. 2003; 88(2):689-96. DOI: 10.1210/jc.2002-021255. View

18.

Schoettl T, Fischer I, Ussar S . Heterogeneity of adipose tissue in development and metabolic function. J Exp Biol. 2018; 221(Pt Suppl 1). DOI: 10.1242/jeb.162958. View

19.

Eisemann J, Bauman D, HOGUE D, TRAVIS H . Evaluation of a role for prolactin in growth and the photoperiod-induced growth response in sheep. J Anim Sci. 1984; 59(1):86-94. DOI: 10.2527/jas1984.59186x. View

20.

Sollier C, Capel E, Aguilhon C, Smirnov V, Auclair M, Douillard C . LIPE-related lipodystrophic syndrome: clinical features and disease modeling using adipose stem cells. Eur J Endocrinol. 2020; 184(1):155-168. DOI: 10.1530/EJE-20-1013. View