Transcriptional Changes in the Hypothalamus, Pituitary, and Mammary Gland Underlying Decreased Lactation Performance in Mice Under Heat Stress

Overview

Journal FASEB J

Specialties Biology
Physiology

Date 2019 Sep 5

PMID 31480864

Citations 17

Authors

Jialiang Han

Juanjuan Shao

Qiong Chen

Huizeng Sun

Leluo Guan

Yongxin Li

Jianxin Liu

Hongyun Liu

Affiliations

Soon will be listed here.

Abstract

Because of climate change, heat stress (HS) causes more and more impacts on dairy animals to decrease lactation performance. The neuroendocrine system is key in regulating systemic physiological processes and milk synthesis. However, the hypothalamic-pituitary axis response to HS is still unclear. In this study, a group of lactating mice underwent a daily 2-h heat treatment (36°C) for 14 d to explore possible cross-talk between the hypothalamic-pituitary axis and mammary gland under HS. Transcriptome analyses by multitissue RNA-Seq indicated the possible mechanisms of reduced lactation performance in animals under HS. In the hypothalamus, the cAMP signaling pathway was activated to resist neuronal death, and the expression of downstream genes was increased to promote cell survival under HS. Reduced food intake might be caused by down-regulated appetite-related peptide, whereas up-regulated neuropeptide Y acted to attenuate reduced food intake. In pituitary, energy stress from lower food intake might result in reduced secretion of prolactin and growth hormone. Under HS, the mammary gland may undergo hypoxic stress, causing mammary epithelial cell apoptosis. Together, these data showed systemic changes in tissues to accommodate the effects of HS on lactation.-Han, J., Shao, J., Chen, Q., Sun, H., Guan, L., Li, Y., Liu, J., Liu, H. Transcriptional changes in the hypothalamus, pituitary, and mammary gland underlying decreased lactation performance in mice under heat stress.

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References

VanHouten J, Dann P, Stewart A, Watson C, Pollak M, Karaplis A . Mammary-specific deletion of parathyroid hormone-related protein preserves bone mass during lactation. J Clin Invest. 2003; 112(9):1429-36. PMC: 228471. DOI: 10.1172/JCI19504. View

Haldar J, Bade V . Involvement of opioid peptides in the inhibition of oxytocin release by heat stress in lactating mice. Proc Soc Exp Biol Med. 1981; 168(1):10-4. DOI: 10.3181/00379727-168-41227. View

Pratt W, Toft D . Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood). 2003; 228(2):111-33. DOI: 10.1177/153537020322800201. View

Kovacs C, Chik C . Hyperprolactinemia caused by lactation and pituitary adenomas is associated with altered serum calcium, phosphate, parathyroid hormone (PTH), and PTH-related peptide levels. J Clin Endocrinol Metab. 1995; 80(10):3036-42. DOI: 10.1210/jcem.80.10.7559893. View

Bakker W, Harris I, Mak T . FOXO3a is activated in response to hypoxic stress and inhibits HIF1-induced apoptosis via regulation of CITED2. Mol Cell. 2007; 28(6):941-53. DOI: 10.1016/j.molcel.2007.10.035. View

Shao Y, Wellman T, Lounsbury K, Zhao F . Differential regulation of GLUT1 and GLUT8 expression by hypoxia in mammary epithelial cells. Am J Physiol Regul Integr Comp Physiol. 2014; 307(3):R237-47. DOI: 10.1152/ajpregu.00093.2014. View

Folley S, Greenbaum A . Effects of adrenalectomy and of treatment with adrenal cortex hormones on the arginase and phosphatase levels of lactating rats. Biochem J. 1946; 40(1):46-51. PMC: 1258292. DOI: 10.1042/bj0400046. View

Stocker R, Glazer A, Ames B . Antioxidant activity of albumin-bound bilirubin. Proc Natl Acad Sci U S A. 1987; 84(16):5918-22. PMC: 298974. DOI: 10.1073/pnas.84.16.5918. View

Azara C, Maia I, Rangel C, Silva-Neto M, Serpa R, de Jesus E . Ethanol intake during lactation alters milk nutrient composition and growth and mineral status of rat pups. Biol Res. 2009; 41(3):317-30. DOI: /S0716-97602008000300008. View

10.

Sampson D, Jansen G . Measurement of milk yield in the lactating rat from pup weight and weight gain. J Pediatr Gastroenterol Nutr. 1984; 3(4):613-7. DOI: 10.1097/00005176-198409000-00023. View

11.

Bernabucci U, Basirico L, Morera P . Impact of hot environment on colostrum and milk composition. Cell Mol Biol (Noisy-le-grand). 2013; 59(1):67-83. View

12.

Greene E, Khaldi S, Ishola P, Bottje W, Ohkubo T, Anthony N . Heat and oxidative stress alter the expression of orexin and its related receptors in avian liver cells. Comp Biochem Physiol A Mol Integr Physiol. 2015; 191:18-24. DOI: 10.1016/j.cbpa.2015.08.016. View

13.

Zhao Z, Chi Q, Cao J . Milk energy output during peak lactation in shaved Swiss mice. Physiol Behav. 2010; 101(1):59-66. DOI: 10.1016/j.physbeh.2010.04.017. View

14.

Vogel Z, Barg J, Levy R, Saya D, Heldman E, Mechoulam R . Anandamide, a brain endogenous compound, interacts specifically with cannabinoid receptors and inhibits adenylate cyclase. J Neurochem. 1993; 61(1):352-5. DOI: 10.1111/j.1471-4159.1993.tb03576.x. View

15.

Raynes D, Guerriero Jr V . Inhibition of Hsp70 ATPase activity and protein renaturation by a novel Hsp70-binding protein. J Biol Chem. 1998; 273(49):32883-8. DOI: 10.1074/jbc.273.49.32883. View

16.

Zhu K, Zhang Q, Foo L, Trube A, Ma G, Hu X . Growth, bone mass, and vitamin D status of Chinese adolescent girls 3 y after withdrawal of milk supplementation. Am J Clin Nutr. 2006; 83(3):714-21. DOI: 10.1093/ajcn.83.3.714. View

17.

White M, Emery M, Nonner D, Barrett J . Caspase activation contributes to delayed death of heat-stressed striatal neurons. J Neurochem. 2003; 87(4):958-68. DOI: 10.1046/j.1471-4159.2003.02077.x. View

18.

Rhoads M, Kim J, Collier R, Crooker B, Boisclair Y, Baumgard L . Effects of heat stress and nutrition on lactating Holstein cows: II. Aspects of hepatic growth hormone responsiveness. J Dairy Sci. 2010; 93(1):170-9. DOI: 10.3168/jds.2009-2469. View

19.

Bahry M, Chowdhury V, Yang H, Tran P, Do P, Han G . Central administration of neuropeptide Y differentially regulates monoamines and corticosterone in heat-exposed fed and fasted chicks. Neuropeptides. 2016; 62:93-100. DOI: 10.1016/j.npep.2016.11.008. View

20.

Davis S, Fadel P, Cui J, Thomas G, Crandall C . Skin blood flow influences near-infrared spectroscopy-derived measurements of tissue oxygenation during heat stress. J Appl Physiol (1985). 2005; 100(1):221-4. DOI: 10.1152/japplphysiol.00867.2005. View