Dissociating Mechanisms That Underlie Seasonal and Developmental Programs for the Neuroendocrine Control of Physiology in Birds

Overview

Journal eNeuro

Specialty Neurology

Date 2024 Mar 28

PMID 38548332

Authors

Timothy Adam Liddle

Gaurav Majumdar

Calum Stewart

Maureen M Bain

Tyler John Stevenson

Affiliations

Soon will be listed here.

Abstract

Long-term programmed rheostatic changes in physiology are essential for animal fitness. Hypothalamic nuclei and the pituitary gland govern key developmental and seasonal transitions in reproduction. The aim of this study was to identify the molecular substrates that are common and unique to developmental and seasonal timing. Adult and juvenile quail were collected from reproductively mature and immature states, and key molecular targets were examined in the mediobasal hypothalamus (MBH) and pituitary gland. qRT-PCR assays established deiodinase type 2 () and type 3 () expression in adults changed with photoperiod manipulations. However, and remain constitutively expressed in juveniles. Pituitary gland transcriptome analyses established that 340 transcripts were differentially expressed across seasonal photoperiod programs and 1,189 transcripts displayed age-dependent variation in expression. Prolactin () and follicle-stimulating hormone subunit beta () are molecular markers of seasonal programs and are significantly upregulated in long photoperiod conditions. Growth hormone expression was significantly upregulated in juvenile quail, regardless of photoperiodic condition. These findings indicate that a level of cell autonomy in the pituitary gland governs seasonal and developmental programs in physiology. Overall, this paper yields novel insights into the molecular mechanisms that govern developmental programs and adult brain plasticity.

References

Misztal T, Romanowicz K, Barcikowski B . Melatonin--a modulator of the GnRH/LH axis in sheep. Reprod Biol. 2003; 2(3):267-75. View

Stevenson T, Ball G . Disruption of neuropsin mRNA expression via RNA interference facilitates the photoinduced increase in thyrotropin-stimulating subunit β in birds. Eur J Neurosci. 2012; 36(6):2859-65. DOI: 10.1111/j.1460-9568.2012.08209.x. View

Tang B, Hu S, Ouyang Q, Wu T, Lu Y, Hu J . Comparative transcriptome analysis identifies crucial candidate genes and pathways in the hypothalamic-pituitary-gonadal axis during external genitalia development of male geese. BMC Genomics. 2022; 23(1):136. PMC: 8848681. DOI: 10.1186/s12864-022-08374-2. View

Chen Y, Lun A, Smyth G . From reads to genes to pathways: differential expression analysis of RNA-Seq experiments using Rsubread and the edgeR quasi-likelihood pipeline. F1000Res. 2016; 5:1438. PMC: 4934518. DOI: 10.12688/f1000research.8987.2. View

Yasuo S, Watanabe M, Iigo M, Yamamura T, Nakao N, Takagi T . Molecular mechanism of photoperiodic time measurement in the brain of Japanese quail. Chronobiol Int. 2006; 23(1-2):307-15. DOI: 10.1080/07420520500521913. View

Stevenson T, Liddle T, Stewart C, Marshall C, Majumdar G . Neural programming of seasonal physiology in birds and mammals: A modular perspective. Horm Behav. 2022; 142:105153. DOI: 10.1016/j.yhbeh.2022.105153. View

Scanes C, Lauterio T . Growth hormone: its physiology and control. J Exp Zool. 1984; 232(3):443-52. DOI: 10.1002/jez.1402320310. View

Barrett P, Ebling F, Schuhler S, Wilson D, Ross A, Warner A . Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology. 2007; 148(8):3608-17. DOI: 10.1210/en.2007-0316. View

Hong Y, Pang Y, Zhao H, Chen S, Tan S, Xiang H . The Morphology of Cross-Beaks and Gene Expression in Huiyang Bearded Chickens. Animals (Basel). 2019; 9(12). PMC: 6940792. DOI: 10.3390/ani9121143. View

10.

San J, Du Y, Wu G, Xu R, Yang J, Hu J . Transcriptome analysis identifies signaling pathways related to meat quality in broiler chickens - the extracellular matrix (ECM) receptor interaction signaling pathway. Poult Sci. 2021; 100(6):101135. PMC: 8105667. DOI: 10.1016/j.psj.2021.101135. View

11.

FOLLETT B, Maung S . Rate of testicular maturation, in relation to gonadotrophin and testosterone levels, in quail exposed to various artificial photoperiods and to natural daylengths. J Endocrinol. 1978; 78(2):267-80. DOI: 10.1677/joe.0.0780267. View

12.

Zhao S, Fernald R . Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol. 2005; 12(8):1047-64. PMC: 2716216. DOI: 10.1089/cmb.2005.12.1047. View

13.

Payton L, Sow M, Massabuau J, Ciret P, Tran D . How annual course of photoperiod shapes seasonal behavior of diploid and triploid oysters, Crassostrea gigas. PLoS One. 2017; 12(10):e0185918. PMC: 5636115. DOI: 10.1371/journal.pone.0185918. View

14.

Perez J, Tolla E, Bishop V, Foster R, Peirson S, Dunn I . Functional inhibition of deep brain non-visual opsins facilitates acute long day induction of reproductive recrudescence in male Japanese quail. Horm Behav. 2023; 148:105298. DOI: 10.1016/j.yhbeh.2022.105298. View

15.

Prendergast B, Pyter L, Kampf-Lassin A, Patel P, Stevenson T . Rapid induction of hypothalamic iodothyronine deiodinase expression by photoperiod and melatonin in juvenile Siberian hamsters (Phodopus sungorus). Endocrinology. 2013; 154(2):831-41. PMC: 3548179. DOI: 10.1210/en.2012-1990. View

16.

Prendergast B, Hotchkiss A, Bilbo S, Nelson R . Peripubertal immune challenges attenuate reproductive development in male Siberian hamsters (Phodopus sungorus). Biol Reprod. 2003; 70(3):813-20. DOI: 10.1095/biolreprod.103.023408. View

17.

Wood S, Loudon A . Clocks for all seasons: unwinding the roles and mechanisms of circadian and interval timers in the hypothalamus and pituitary. J Endocrinol. 2014; 222(2):R39-59. PMC: 4104039. DOI: 10.1530/JOE-14-0141. View

18.

Sherman B, Hao M, Qiu J, Jiao X, Baseler M, Lane H . DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Res. 2022; 50(W1):W216-W221. PMC: 9252805. DOI: 10.1093/nar/gkac194. View

19.

Yasuo S, Watanabe M, Nakao N, Takagi T, Follett B, Ebihara S . The reciprocal switching of two thyroid hormone-activating and -inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology. 2005; 146(6):2551-4. DOI: 10.1210/en.2005-0057. View

20.

Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K . Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature. 2003; 426(6963):178-81. DOI: 10.1038/nature02117. View