Steroidogenic acute regulatory protein in fish

in Journal of Endocrinology
Authors:
Jannet Kocerha Department of Biochemistry, Chemistry and Physics, Georgia Southern University, Statesboro, Georgia, USA

Search for other papers by Jannet Kocerha in
Current site
Google Scholar
PubMed Close
and
Nancy D Denslow Department of Physiological Sciences and Center for Environmental and Human Toxicology, University of Florida, Gainesville, Florida, USA

Search for other papers by Nancy D Denslow in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0002-3946-3112

Correspondence should be addressed to N D Denslow: ndenslow@ufl.edu

This paper forms part of a special collection marking 30 Years Since the Identification and Characterization of the StAR Protein. The guest editors for this collection were Doug Stocco, Barbara Clark and Ernesto Podesta.

DOI:
https://doi.org/10.1530/JOE-24-0232
Volume/Issue:
Volume 265: Issue 1
Article Type:
Review Article
Article ID:
e240232
Online Publication Date:
17 Feb 2025
Copyright:
© the author(s) 2025
Restricted access
Rent on DeepDyve

Sign up for journal news

The importance of steroidogenesis is underscored by its vital and conserved functions from higher to lower vertebrate species, such as stress, immune and inflammatory responses, sexual development and reproduction, osmoregulation and even the ability to adapt to the environment and environmental changes. Correspondingly, the rate-limiting step of steroidogenesis mediated by the steroidogenic acute regulatory protein is an ongoing target for scientific investigation. An expanding collection of studies has now reported key similarities, as well as some differences, in the transcriptional and translational regulation of steroidogenic acute regulatory protein across species. This review will discuss the current understanding of steroidogenic acute regulatory protein in fish, as these lower vertebrate models uniquely rely on steroid hormones for osmotic balance, reproductive functions, responses to environmental stimuli and much more.

Journal of Endocrinology is committed to supporting researchers in demonstrating the impact of their articles published in the journal.

The two types of article metrics we measure are (i) more traditional full-text views and pdf downloads, and (ii) Altmetric data, which shows the wider impact of articles in a range of non-traditional sources, such as social media.

More information is on the Reasons to publish page.

Sept 2018 onwards Past Year Past 30 Days
Full Text Views 29 29 15
PDF Downloads 41 41 24

 

  • Collapse
  • Expand
Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© the author(s) 2025
Article ID:
e240232
Article Type:
Review Article
Received Date:
01 Aug 2024
Rev-recd:
03 Jan 2025
Accepted Date:
31 Jan 2025
Print Publication Date:
01 Apr 2025
Online Publication Date:
17 Feb 2025
Keywords:
fish reproduction; stress axis; interrenal; endocrine disruption

  • Aesoy R , Mellgren G , Morohashi K , et al. 2002 Activation of cAMP-dependent protein kinase increases the protein level of steroidogenic factor-1. Endocrinology 143 295–303. (https://doi.org/10.1210/endo.143.1.8599)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Alsop D & Vijayan M 2009 The zebrafish stress axis: molecular fallout from the teleost-specific genome duplication event. Gen Comp Endocrinol 161 62–66. (https://doi.org/10.1016/j.ygcen.2008.09.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Aluru N & Vijayan MM 2006 Aryl hydrocarbon receptor activation impairs cortisol response to stress in rainbow trout by disrupting the rate-limiting steps in steroidogenesis. Endocrinology 147 1895–1903. (https://doi.org/10.1210/en.2005-1143)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Antoni FA 2012 New paradigms in cAMP signalling. Mol Cell Endocrinol 353 3–9. (https://doi.org/10.1016/j.mce.2011.10.034)

  • Arukwe A 2005 Modulation of brain steroidogenesis by affecting transcriptional changes of steroidogenic acute regulatory (StAR) protein and cholesterol side chain cleavage (P450scc) in juvenile Atlantic salmon (Salmo salar) is a novel aspect of nonylphenol toxicity. Environ Sci Technol 39 9791–9798. (https://doi.org/10.1021/es0509937)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Arukwe A 2008 Steroidogenic acute regulatory (StAR) protein and cholesterol side-chain cleavage (P450scc)-regulated steroidogenesis as an organ-specific molecular and cellular target for endocrine disrupting chemicals in fish. Cell Biol Toxicol 24 527–540. (https://doi.org/10.1007/s10565-008-9069-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bird IM , Hanley NA , Word RA , et al. 1993 Human NCI-H295 adrenocortical carcinoma cells: a model for angiotensin-II-responsive aldosterone secretion. Endocrinology 133 1555–1561. (https://doi.org/10.1210/en.133.4.1555)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bury NR & Sturm A 2007 Evolution of the corticosteroid receptor signalling pathway in fish. Gen Comp Endocrinol 153 47–56. (https://doi.org/10.1016/j.ygcen.2007.03.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bury NR , Sturm A , Le Rouzic P , et al. 2003 Evidence for two distinct functional glucocorticoid receptors in teleost fish. J Mol Endocrinol 31 141–156. (https://doi.org/10.1677/jme.0.0310141)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Castillo J , Castellana B , Acerete L , et al. 2008 Stress-induced regulation of steroidogenic acute regulatory protein expression in head kidney of Gilthead seabream (Sparus aurata). J Endocrinol 196 313–322. (https://doi.org/10.1677/joe-07-0440)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Castillo AF , Fan J , Papadopoulos V , et al. 2011 Hormone-dependent expression of a steroidogenic acute regulatory protein natural antisense transcript in MA-10 mouse tumor Leydig cells. PLoS One 6 e22822. (https://doi.org/10.1371/journal.pone.0022822)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chen C , Kuo J , Wong A , et al. 2014 Estradiol modulates translocator protein (TSPO) and steroid acute regulatory protein (StAR) via protein kinase A (PKA) signaling in hypothalamic astrocytes. Endocrinology 155 2976–2985. (https://doi.org/10.1210/en.2013-1844)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cooke PS , Simon L & Denslow ND 2013 Endocrine disruptors. In Handbook of Toxicologic Pathology. Ed HA Rousseaux . Academic Press.

  • Coumailleau P , Pellegrini E , Adrio F , et al. 2015 Aromatase, estrogen receptors and brain development in fish and amphibians. Biochim Biophys Acta 1849 152–162. (https://doi.org/10.1016/j.bbagrm.2014.07.002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • De Maria M , Kroll KJ , Yu F , et al. 2022 Endocrine, immune and renal toxicity in male largemouth bass after chronic exposure to glyphosate and Rodeo®. Aquat Toxicol 246 106142. (https://doi.org/10.1016/j.aquatox.2022.106142)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Diotel N , Do Rego JL , Anglade I , et al. 2011 The brain of teleost fish, a source, and a target of sexual steroids. Front Neurosci 5 137. (https://doi.org/10.3389/fnins.2011.00137)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Diotel N , Charlier TD , Lefebvre D'Hellencourt C , et al. 2018 Steroid transport, local synthesis, and signaling within the brain: roles in neurogenesis, neuroprotection, and sexual behaviors. Front Neurosci 12 84. (https://doi.org/10.3389/fnins.2018.00084)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dong W & Willett KL 2008 Local expression of CYP19A1 and CYP19A2 in developing and adult killifish (Fundulus heteroclitus). Gen Comp Endocrinol 155 307–317. (https://doi.org/10.1016/j.ygcen.2007.05.018)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Evans AN & Nunez BS 2010 Regulation of mRNAs encoding the steroidogenic acute regulatory protein and cholesterol side-chain cleavage enzyme in the elasmobranch interrenal gland. Gen Comp Endocrinol 168 121–132. (https://doi.org/10.1016/j.ygcen.2010.04.018)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Faheem M , Khaliq S & Lone KP 2017 Disruption of the reproductive axis in freshwater fish, catla catla, after bisphenol-A exposure. Zoolog Sci 34 438–444. (https://doi.org/10.2108/zs170009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Forlano PM , Deitcher DL , Myers DA , et al. 2001 Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J Neurosci 21 8943–8955. (https://doi.org/10.1523/jneurosci.21-22-08943.2001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gallo-Payet N & Payet MD 2003 Mechanism of action of ACTH: beyond cAMP. Microsc Res Tech 61 275–287. (https://doi.org/10.1002/jemt.10337)

  • Garcia-Reyero N , Barber DS , Gross TS , et al. 2006 Dietary exposure of largemouth bass to OCPs changes expression of genes important for reproduction. Aquat Toxicol 78 358–369. (https://doi.org/10.1016/j.aquatox.2006.05.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gennotte V , Melard C , D’Cotta H , et al. 2014 The sensitive period for male-to-female sex reversal begins at the embryonic stage in the Nile tilapia and is associated with the sexual genotype. Mol Reprod Dev 81 1146–1158. (https://doi.org/10.1002/mrd.22436)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gorelick DA , Watson W & Halpern ME 2008 Androgen receptor gene expression in the developing and adult zebrafish brain. Dev Dyn 237 2987–2995. (https://doi.org/10.1002/dvdy.21700)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Grier HJ , Uribe MC , Lo Nostro FL , et al. 2016 Conserved form and function of the germinal epithelium through 500 million years of vertebrate evolution. J Morphol 277 1014–1044. (https://doi.org/10.1002/jmor.20554)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gross TS , Wieser CM , Sepulveda MS , et al. 2002 Characterization of annual reproductive cycles for pond-reared Florida largemouth bass, micropterus salmoides floridanus. In Black Bass: Ecology, Conservation, and Management. Bethesda, MD, USA: American Fisheries Society.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hagen IJ , Kusakabe M & Young G 2006 Effects of ACTH and cAMP on steroidogenic acute regulatory protein and P450 11β-hydroxylase messenger RNAs in rainbow trout interrenal cells: relationship with in vitro cortisol production. Gen Comp Endocrinol 145 254–262. (https://doi.org/10.1016/j.ygcen.2005.09.014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hontela A , Rasmussen JB , Audet C , et al. 1992 Impaired cortisol stress response in fish from environments polluted by PAHs, PCBs, and mercury. Arch Environ Contam Toxicol 22 278–283. (https://doi.org/10.1007/bf00212086)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ings JS & Van Der Kraak GJ 2006 Characterization of the mRNA expression of StAR and steroidogenic enzymes in zebrafish ovarian follicles. Mol Reprod Dev 73 943–954. (https://doi.org/10.1002/mrd.20490)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ings JS , Servos MR & Vijayan MM 2011 Exposure to municipal wastewater effluent impacts stress performance in rainbow trout. Aquat Toxicol 103 85–91. (https://doi.org/10.1016/j.aquatox.2011.02.013)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Irusta G , Parborell F , Peluffo M , et al. 2003 Steroidogenic acute regulatory protein in ovarian follicles of gonadotropin-stimulated rats is regulated by a gonadotropin-releasing hormone agonist. Biol Reprod 68 1577–1583. (https://doi.org/10.1095/biolreprod.102.009944)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jeffcoat CR , Artemenko IP & Zhao D 2000 Relationship of StAR expression tomitochondrial cholesterol transfer and metabolism. Endocr Res 26 663–680. (https://doi.org/10.3109/07435800009048586)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jensen KM , Korte JJ , Kahl MD , et al. 2001 Aspects of basic reproductive biology and endocrinology in the fathead minnow (Pimephales promelas). Comp Biochem Physiol C Toxicol Pharmacol 128 127–141. (https://doi.org/10.1016/s1532-0456(00)00185-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Johns SM , Kane MD , Denslow ND , et al. 2009 Characterization of ontogenetic changes in gene expression in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 28 873–880. (https://doi.org/10.1897/08-213r.1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Johns SM , Denslow ND , Kane MD , et al. 2011 Effects of estrogens and antiestrogens on gene expression of fathead minnow (Pimephales promelas) early life stages. Environ Toxicol 26 195–206. (https://doi.org/10.1002/tox.20545)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Judson RS , Houck KA , Kavlock RJ , et al. 2010 In vitro screening of environmental chemicals for targeted testing prioritization: the ToxCast project. Environ Health Perspect 118 485–492. (https://doi.org/10.1289/ehp.0901392)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kelce WR , Lambright CR , Gray LE Jr , et al. 1997 Vinclozolin and p,p′-DDE alter androgen-dependent gene expression: in vivo confirmation of an androgen receptor-mediated mechanism. Toxicol Appl Pharmacol 142 192–200. (https://doi.org/10.1006/taap.1996.7966)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kocerha J , Prucha MS , Kroll KJ , et al. 2010 Regulation of steroidogenic acute regulatory protein transcription in largemouth bass by orphan nuclear receptor signaling pathways. Endocrinology 151 341–349. (https://doi.org/10.1210/en.2009-0551)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kojima H , Katsura E , Takeuchi S , et al. 2004 Screening for estrogen and androgen receptor activities in 200 pesticides by in vitro reporter gene assays using Chinese hamster ovary cells. Environ Health Perspect 112 524–531. (https://doi.org/10.1289/ehp.6649)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kottler VA , Feron R , Nanda I , et al. 2020 Independent origin of XY and ZW sex determination mechanisms in mosquitofish sister species. Genetics 214 193–209. (https://doi.org/10.1534/genetics.119.302698)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kusakabe M , Todo T , Mcquillan HJ , et al. 2002 Characterization and expression of steroidogenic acute regulatory protein and MLN64 cDNAs in trout. Endocrinology 143 2062–2070. (https://doi.org/10.1210/en.143.6.2062)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kusakabe M , Zuccarelli MD , Nakamura I , et al. 2009 Steroidogenic acute regulatory protein in white sturgeon (Acipenser transmontanus): cDNA cloning, sites of expression and transcript abundance in corticosteroidogenic tissue after an acute stressor. Gen Comp Endocrinol 162 233–240. (https://doi.org/10.1016/j.ygcen.2009.02.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lacroix M & Hontela A 2001 Regulation of acute cortisol synthesis by cAMP-dependent protein kinase and protein kinase C in a teleost species, the rainbow trout (Oncorhynchus mykiss). J Endocrinol 169 71–78. (https://doi.org/10.1677/joe.0.1690071)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lai KP , Li JW , Tse AC , et al. 2016 Hypoxia alters steroidogenesis in female marine medaka through miRNAs regulation. Aquat Toxicol 172 1–8. (https://doi.org/10.1016/j.aquatox.2015.12.012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leblond VS & Hontela A 1999 Effects of in vitro exposures to cadmium, mercury, zinc, and 1-(2-chlorophenyl)-1-(4-chlorophenyl)-2,2-dichloroethane on steroidogenesis by dispersed interrenal cells of rainbow trout (Oncorhynchus mykiss). Toxicol Appl Pharmacol 157 16–22. (https://doi.org/10.1006/taap.1999.8660)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Li L , Wu Y , Zhao C , et al. 2021 The role of StAR2 gene in testicular differentiation and spermatogenesis in Nile tilapia (Oreochromis niloticus). J Steroid Biochem Mol Biol 214 105974. (https://doi.org/10.1016/j.jsbmb.2021.105974)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Liu S , Qin F , Wang H , et al. 2012 Effects of 17α-ethinylestradiol and bisphenol A on steroidogenic messenger ribonucleic acid levels in the rare minnow gonads. Aquat Toxicol 122–123 19–27. (https://doi.org/10.1016/j.aquatox.2012.05.010)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Manna PR , Dyson MT , Eubank DW , et al. 2002 Regulation of steroidogenesis and the steroidogenic acute regulatory protein by a member of the cAMP response-element binding protein family. Mol Endocrinol 16 184–199. (https://doi.org/10.1210/me.16.1.184)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Manna PR , Dyson MT & Stocco DM 2009 Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives. Mol Hum Reprod 15 321–333. (https://doi.org/10.1093/molehr/gap025)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Martyniuk CJ , Kroll KJ , Porak WF , et al. 2009 Seasonal relationship between gonadotropin, growth hormone, and estrogen receptor mRNA expression in the pituitary gland of largemouth bass. Gen Comp Endocrinol 163 306–317. (https://doi.org/10.1016/j.ygcen.2009.04.028)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Martyniuk CJ , Feswick A , Spade DJ , et al. 2010 Effects of acute dieldrin exposure on neurotransmitters and global gene transcription in largemouth bass (Micropterus salmoides) hypothalamus. Neurotoxicology 31 356–366. (https://doi.org/10.1016/j.neuro.2010.04.008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • McQuillan HJ , Kusakabe M & Young G 2011 Effects of chronic manipulation of adrenocorticotropic hormone levels in Chinook salmon on expression of interrenal steroidogenic acute regulatory protein and steroidogenic enzymes. Gen Comp Endocrinol 174 156–165. (https://doi.org/10.1016/j.ygcen.2011.08.014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Molina AM , Abril N , Morales-Prieto N , et al. 2018 Evaluation of toxicological endpoints in female zebrafish after bisphenol A exposure. Food Chem Toxicol 112 19–25. (https://doi.org/10.1016/j.fct.2017.12.026)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mommsen TP , Vijayan MM & Moon TW 1999 Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9 211–268. (https://doi.org/10.1023/a:1008924418720)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mouriec K , Lareyre JJ , Tong SK , et al. 2009 Early regulation of brain aromatase (cyp19a1b) by estrogen receptors during zebrafish development. Dev Dyn 238 2641–2651. (https://doi.org/10.1002/dvdy.22069)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nagahama Y 1994 Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38 217–229.

  • Nakamura I , Kusakabe M , Swanson P , et al. 2016 Regulation of sex steroid production and mRNAs encoding gonadotropin receptors and steroidogenic proteins by gonadotropins, cyclic AMP and insulin-like growth factor-I in ovarian follicles of rainbow trout (Oncorhynchus mykiss) at two stages of vitellogenesis. Comp Biochem Physiol A Mol Integr Physiol 201 132–140. (https://doi.org/10.1016/j.cbpa.2016.06.035)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nanba K , Blinder AR & Rainey WE 2021 Primary cultures and cell lines for in vitro modeling of the human adrenal cortex. Tohoku J Exp Med 253 217–232. (https://doi.org/10.1620/tjem.253.217)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nunez BS & Evans AN 2007 Hormonal regulation of the steroidogenic acute regulatory protein (StAR) in gonadal tissues of the Atlantic croaker (Micropogonias undulatus). Gen Comp Endocrinol 150 495–504. (https://doi.org/10.1016/j.ygcen.2006.11.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pasmanik M & Callard GV 1985 Aromatase and 5α-reductase in the teleost brain, spinal cord, and pituitary gland. Gen Comp Endocrinol 60 244–251. (https://doi.org/10.1016/0016-6480(85)90320-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pellegrini E , Diotel N , Vaillant-Capitaine C , et al. 2016 Steroid modulation of neurogenesis: focus on radial glial cells in zebrafish. J Steroid Biochem Mol Biol 160 27–36. (https://doi.org/10.1016/j.jsbmb.2015.06.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pezzi V , Mathis JM , Rainey WE , et al. 2003 Profiling transcript levels for steroidogenic enzymes in fetal tissues. J Steroid Biochem Mol Biol 87 181–189. (https://doi.org/10.1016/j.jsbmb.2003.07.006)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pikulkaew S , De Nadai A , Belvedere P , et al. 2010 Expression analysis of steroid hormone receptor mRNAs during zebrafish embryogenesis. Gen Comp Endocrinol 165 215–220. (https://doi.org/10.1016/j.ygcen.2009.06.024)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Prucha MS , Martyniuk CJ , Doperalski NJ , et al. 2020 Steroidogenic acute regulatory protein transcription is regulated by estrogen receptor signaling in largemouth bass ovary. Gen Comp Endocrinol 286 113300. (https://doi.org/10.1016/j.ygcen.2019.113300)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Reyland ME , Evans RM & White EK 2000 Lipoproteins regulate expression of the steroidogenic acute regulatory protein (StAR) in mouse adrenocortical cells. J Biol Chem 275 36637–36644. (https://doi.org/10.1074/jbc.m006456200)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rocha A , Zanuy S , Carrillo M , et al. 2009 Seasonal changes in gonadal expression of gonadotropin receptors, steroidogenic acute regulatory protein and steroidogenic enzymes in the European sea bass. Gen Comp Endocrinol 162 265–275. (https://doi.org/10.1016/j.ygcen.2009.03.023)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rosenblum PM , Brandt TM , Mayes KB , et al. 1994 Annual cycles of growth and reproduction in hatchery-reared Florida largemouth bass, Micropterus-salmoides floridanus, raised on forage or pelleted diets. J Fish Biol 44 1045–1059. (https://doi.org/10.1006/jfbi.1994.1096)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sandhoff TW & Mclean MP 1999 Repression of the rat steroidogenic acute regulatory (StAR) protein gene by PGF2alpha is modulated by the negative transcription factor DAX-1. Endocrine 10 83–91. (https://doi.org/10.1385/ENDO:10:1:83)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shang G , Peng X , Ji C , et al. 2019 Steroidogenic acute regulatory protein and luteinizing hormone are required for normal ovarian steroidogenesis and oocyte maturation in zebrafishdagger. Biol Reprod 101 760–770. (https://doi.org/10.1093/biolre/ioz132)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shi Y , Liu X , Zhu P , et al. 2013 G-protein-coupled estrogen receptor 1 is involved in brain development during zebrafish (Danio rerio) embryogenesis. Biochem Biophys Res Commun 435 21–27. (https://doi.org/10.1016/j.bbrc.2013.03.130)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Smith LC , Lavelle CM , Silva-Sanchez C , et al. 2018 Early phosphoproteomic changes for adverse outcome pathway development in the fathead minnow (Pimephales promelas) brain. Sci Rep 8 10212. (https://doi.org/10.1038/s41598-018-28395-w)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sridaran R , Philip GH , Li H , et al. 1999 GnRH agonist treatment decreases progesterone synthesis, luteal peripheral benzodiazepine receptor mRNA, ligand binding and steroidogenic acute regulatory protein expression during pregnancy. J Mol Endocrinol 22 45–54. (https://doi.org/10.1677/jme.0.0220045)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Stocco DM & Clark BJ 1997 The role of the steroidogenic acute regulatory protein in steroidogenesis. Steroids 62 29–36. (https://doi.org/10.1016/s0039-128x(96)00155-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Su Y , Wu Y , Ye M , et al. 2024 Star1 gene mutation reveals the essentiality of 11-ketotestosterone and glucocorticoids for male fertility in Nile Tilapia (Oreochromis niloticus). Comp Biochem Physiol B Biochem Mol Biol 273 110985. (https://doi.org/10.1016/j.cbpb.2024.110985)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sugawara T , Nomura E , Sakuragi N , et al. 2001 The effect of the arylhydrocarbon receptor on the human steroidogenic acute regulatory gene promoter activity. J Steroid Biochem Mol Biol 78 253–260. (https://doi.org/10.1016/s0960-0760(01)00100-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tugaeva KV & Sluchanko NN 2019 Steroidogenic acute regulatory protein: structure, functioning, and regulation. Biochemistry 84 S233–S253. (https://doi.org/10.1134/s0006297919140141)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vang SH , Kortner TM & Arukwe A 2007 Steroidogenic acute regulatory (StAR) protein and cholesterol side-chain cleavage (P450scc) as molecular and cellular targets for 17α-ethynylestradiol in salmon previtellogenic oocytes. Chem Res Toxicol 20 1811–1819. (https://doi.org/10.1021/tx700228g)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vijayan MM , Aluru N & Leatherland JF 2010 Stress response and the role of cortisol. In Fish Diseases and Disorders. Eds JF Leatherland & PTK Woo . Wallingford, UK: CAB International.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Villeneuve DL , Ankley GT , Makynen EA , et al. 2007 Comparison of fathead minnow ovary explant and H295R cell-based steroidogenesis assays for identifying endocrine-active chemicals. Ecotoxicol Environ Saf 68 20–32. (https://doi.org/10.1016/j.ecoenv.2007.03.001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Walsh LP , N Kuratko C & Stocco DM 2000a Econazole and miconazole inhibit steroidogenesis and disrupt steroidogenic acute regulatory (StAR) protein expression post-transcriptionally. J Steroid Biochem Mol Biol 75 229–236. (https://doi.org/10.1016/s0960-0760(00)00170-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Walsh LP , Mccormick C , Martin C , et al. 2000b Roundup inhibits steroidogenesis by disrupting steroidogenic acute regulatory (StAR) protein expression. Environ Health Perspect 108 769–776. (https://doi.org/10.2307/3434731)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wendelaar Bonga SE 1997 The stress response in fish. Physiol Rev 77 591–625. (https://doi.org/10.1152/physrev.1997.77.3.591)

  • Yang F , Wang Y , Lu W , et al. 2022 The comparative survey of coordinated regulation of steroidogenic pathway in Japanese flounder (Paralichthys olivaceus) and Chinese tongue sole (Cynoglossus semilaevis). Int J Mol Sci 23 5520. (https://doi.org/10.3390/ijms23105520)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yao M , Stenzel-Poore M & Denver RJ 2007 Structural and functional conservation of vertebrate corticotropin-releasing factor genes: evidence for a critical role for a conserved cyclic AMP response element. Endocrinology 148 2518–2531. (https://doi.org/10.1210/en.2006-1413)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yu X , Wu L , Xie L , et al. 2014 Characterization of two paralogous StAR genes in a teleost, Nile tilapia (Oreochromis niloticus). Mol Cell Endocrinol 392 152–162. (https://doi.org/10.1016/j.mce.2014.05.013)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhang Y , Gao J , Xu P , et al. 2014 Low-dose bisphenol A disrupts gonad development and steroidogenic genes expression in adult female rare minnow Gobiocypris rarus. Chemosphere 112 435–442. (https://doi.org/10.1016/j.chemosphere.2014.04.089)

    • PubMed
    • Search Google Scholar
    • Export Citation