Abstract
Corticotropin-releasing hormone (CRH) is mainly secreted by the hypothalamus to regulate stress when environmental factors change. Gills contact with water directly and may also secrete CRH to maintain local homeostasis. Ocean acidification changes water chemical parameters and is becoming an important environmental stressor for marine fish. The response of brain and gill CRH systems to ocean acidification remains unclear. In this study, marine medaka were exposed to CO2-acidified seawater (440 ppm, 1000 ppm, and 1800 ppm CO2) for 2 h, 4 h, 24 h, and 7 d, respectively. At 2 h and 4 h, the expression of crh mRNA in gills increased with increasing CO2 concentration. Crh protein is expressed mainly in the lamellae cells. crhbp and crhr1 expression also increased significantly. However, at 2 h and 4 h, acidification caused little changes in these genes and Crh protein expression in the brain. At 7 d, Crh-positive cells were detected in the hypothalamus; moreover, Crh protein expression in the whole brain increased. It is suggested that CRH autocrine secretion in gills is responsible for local acid–base regulation rather than systemic mobilization after short-term acidification stress, which may help the rapid regulation of body damage caused by environmental stress.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be made available on request.
Abbreviations
- ACTH:
-
Adrenocorticotropic hormone
- CO2 :
-
Carbon dioxide
- CRH:
-
Corticotropin-releasing hormone
- Crhbp:
-
CRH binding protein
- Crhr:
-
CRH receptors
- HPI:
-
Hypothalamic-pituitary-interrenal
- HRP:
-
Horseradish peroxidase
- NPO:
-
Neurosecretory preoptic
- PBS:
-
Phosphate-buffered saline
- PD:
-
Periventricularis dorsalis
- PV:
-
Periventricular ventralis
- RIPA:
-
Radio immunoprecipitation assay
- SE:
-
Standard error
- TBST:
-
Tris-buffered saline with Tween 20
References
Aguilera G, Liu Y (2012) The molecular physiology of CRH neurons. Front Neuroendocrinol 33(1):67–84. https://doi.org/10.1016/j.yfrne.2011.08.002
Aguilera G, Nikodemova M, Wynn PC, Catt KJ (2004) Corticotropin releasing hormone receptors: two decades later. Peptides 25(3):319–329. https://doi.org/10.1016/j.peptides.2004.02.002
Aruna A, Wang TP, Cao JC, Lan DS, Nagarajan G, Chang CF (2021) Differential expression of hypothalamic and gill-crh system with osmotic stress in the Euryhaline black porgy. Acanthopagrus Schlegelii Front Physiol 12:768122. https://doi.org/10.3389/fphys.2021.768122
Baumann H, Jones LF, Murray CS, Siedlecki SA, Alexander M, Cross EL (2022) Impaired hatching exacerbates the high CO2 sensitivity of embryonic sand lance Ammodytes dubius. Mar Ecol Prog Ser 687:147–162. https://doi.org/10.3354/meps14010
Brauner CJ, Shartau RB, Damsgaard C, Esbaugh AJ, Wilson RW, Grosell M (2019) 3 - Acid-base physiology and CO2 homeostasis: regulation and compensation in response to elevated environmental CO2. Fish Physiol 37:169–132. https://doi.org/10.1016/bs.fp.2019.08.003
Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425(6956):365. https://doi.org/10.1038/425365a
Cattano C, Fine M, Quattrocchi F, Holzman R, Milazzo M (2019) Behavioural responses of fish groups exposed to a predatory threat under elevated CO2. Mar Environ Res 147:179–184. https://doi.org/10.1016/j.marenvres.2019.04.011
Chung S, Son GH, Kim K (2011) Circadian rhythm of adrenal glucocorticoid: its regulation and clinical implications. Biochim Biophys Acta 1812(5):581–591. https://doi.org/10.1016/j.bbadis.2011.02.003
Conde-Sieira M, Chivite M, Míguez JM, Soengas JL (2018) Stress effects on the mechanisms regulating appetite in teleost fish. Front Endocrinol (lausanne) 9:631. https://doi.org/10.3389/fendo.2018.00631
Dautzenberg FM, Hauger RL (2002) The CRF peptide family and their receptors: yet more partners discovered. Trends Pharmacol Sci 23(2):71–77. https://doi.org/10.1016/s0165-6147(02)01946-6
De Marco RJ, Thiemann T, Groneberg AH, Herget U, Ryu S (2016) Optogenetically enhanced pituitary corticotroph cell activity post-stress onset causes rapid organizing effects on behaviour. Nat Commun 7:12620. https://doi.org/10.1038/ncomms12620
Deussing JM, Chen A (2018) The corticotropin-releasing factor family: physiology of the stress response. Physiol Rev 98(4):2225–2286. https://doi.org/10.1152/physrev.00042.2017
Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192. https://doi.org/10.1146/annurev.marine.010908.163834
Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85(1):97–177. https://doi.org/10.1152/physrev.00050.2003
Faught E, Vijayan MM (2022) Coordinated action of corticotropin-releasing hormone and cortisol shapes the acute stress-induced behavioural response in zebrafish. Neuroendocrinology 112(1):74–87. https://doi.org/10.1159/000514778
Flik G, Klaren PH, Van den Burg EH, Metz JR, Huising MO (2006) CRF and stress in fish. Gen Comp Endocrinol 146(1):36–44. https://doi.org/10.1016/j.ygcen.2005.11.005
Grammatopoulos DK, Chrousos GP (2002) Functional characteristics of CRH receptors and potential clinical applications of CRH-receptor antagonists. Trends Endocrinol Metab 13(10):436–444. https://doi.org/10.1016/s1043-2760(02)00670-7
Grone BP, Maruska KP (2015) Divergent evolution of two corticotropin-releasing hormone (CRH) genes in teleost fishes. Front Neurosci 9:365. https://doi.org/10.3389/fnins.2015.00365
Guh YJ, Lin CH, Hwang PP (2015) Osmoregulation in zebrafish: ion transport mechanisms and functional regulation. Excli J 14:627–659. https://doi.org/10.17179/excli2015-246
Hayashi M, Kita J, Ishimatsu A (2004) Acid-base responses to lethal aquatic hypercapnia in three marine fishes. Mar Biol 144(1):153–160. https://doi.org/10.1007/s00227-003-1172-y
Hosono K, Kikuchi Y, Miyanishi H, Hiraki-Kajiyama T, Takeuchi A, Nakasone K, Maehiro S, Okubo K (2015) Teleocortin: a novel member of the CRH family in teleost fish. Endocrinology 156(8):2949–2957. https://doi.org/10.1210/en.2015-1042
Jarrold MD, Welch MJ, McMahon SJ, McArley T, Allan BJM, Watson SA, Parsons DM, Pether SMJ, Pope S, Nicol S, Smith N, Herbert N, Munday PL (2020) Elevated CO2 affects anxiety but not a range of other behaviours in juvenile yellowtail kingfish. Mar Environ Res 157:104863. https://doi.org/10.1016/j.marenvres.2019.104863
Juster RP, McEwen BS, Lupien SJ (2010) Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev 35(1):2–16. https://doi.org/10.1016/j.neubiorev.2009.10.002
Justice NJ, Yuan ZF, Sawchenko PE, Vale W (2008) Type 1 corticotropin-releasing factor receptor expression reported in BAC transgenic mice: implications for reconciling ligand-receptor mismatch in the central corticotropin-releasing factor system. J Comp Neurol 511(4):479–496. https://doi.org/10.1002/cne.21848
Kültz D (2015) Physiological mechanisms used by fish to cope with salinity stress. J Exp Biol 218(12):1907–1914. https://doi.org/10.1242/jeb.118695
Larsen BK, Jensen FB (1997) Influence of ionic composition on acid-base regulation in rainbow trout (Oncorhynchus mykiss) exposed to environmental hypercapnia. Fish Physiol Biochem 16(2):157–170. https://doi.org/10.1007/bf00004672
Lin CC, Lin LY, Hsu HH, Thermes V, Prunet P, Horng JL, Hwang PP (2012) Acid secretion by mitochondrion-rich cells of medaka (Oryzias latipes) acclimated to acidic freshwater. Am J Physiol Regul Integr Comp Physiol 302(2):R283–R291. https://doi.org/10.1152/ajpregu.00483.2011
Ma XM, Aguilera G (1999) Differential regulation of corticotropin-releasing hormone and vasopressin transcription by glucocorticoids. Endocrinology 140(12):5642–5650. https://doi.org/10.1210/endo.140.12.7214
Maugars G, Mauvois X, Martin P, Aroua S, Rousseau K, Dufour S (2022) New insights into the evolution of corticotropin-releasing hormone family with a special focus on teleosts. Front Endocrinol (lausanne) 13:937218. https://doi.org/10.3389/fendo.2022.937218
McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43(1):2–15. https://doi.org/10.1016/s0018-506x(02)00024-7
Montgomery DW, Kwan GT, Davison WG, Finlay J, Berry A, Simpson SD, Engelhard GH, Birchenough SNR, Tresguerres M, Wilson RW (2022) Rapid blood acid-base regulation by European sea bass (Dicentrarchus labrax) in response to sudden exposure to high environmental CO2. J Exp Biol 225(2):jeb242735. https://doi.org/10.1242/jeb.242735
Nagpal J, Herget U, Choi MK, Ryu S (2019) Anatomy, development, and plasticity of the neurosecretory hypothalamus in zebrafish. Cell Tissue Res 375(1):5–22. https://doi.org/10.1007/s00441-018-2900-4
NOAA (2022) 2022 Global climate report. NOAA. https://www.ncei.noaa.gov/access/monitoring/monthly-report/global/2022
Olson KR (1998) Hormone metabolism by the fish gill. Comp Biochem Physiol A Mol Integr Physiol 119(1):55–65. https://doi.org/10.1016/s1095-6433(97)00406-6
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-fist century and its impact on calcifying organisms. Nature 437(7059):681–686. https://doi.org/10.1038/nature04095
Pachauri RK, Meyer LA (2014) Climate change 2014: synthesis report. IPCC, Geneva, Switzerland, p 151. https://www.ipcc.ch/report/ar5/syr/
Perry SF, Gilmour KM (2006) Acid-base balance and CO2 excretion in fish: unanswered questions and emerging models. Respir Physiol Neurobiol 154(1–2):199–215. https://doi.org/10.1016/j.resp.2006.04.010
Porteus CS, Hubbard PC, Webster TMU, van Aerie R, Canario AVM, Santos EM, Wilson RW (2018) Near-future CO2 levels impair the olfactory system of a marine fish. Nat Clim Chang 8(8):737–743. https://doi.org/10.1038/s41558-018-0224-8
Reul JM, Holsboer F (2002) On the role of corticotropin-releasing hormone receptors in anxiety and depression. Dialogues Clin Neurosci 4(1):31–46. https://doi.org/10.31887/DCNS.2002.4.1/jreul
Rivier C, Vale W (1983) Modulation of stress-induced ACTH release by corticotropin-releasing factor, catecholamines and vasopressin. Nature 305(5932):325–327. https://doi.org/10.1038/305325a0
Schulkin J, Morgan MA, Rosen JB (2005) A neuroendocrine mechanism for sustaining fear. Trends Neurosci 28(12):629–635. https://doi.org/10.1016/j.tins.2005.09.009
Shartau RB, Damsgaard C, Brauner CJ (2019) Limits and patterns of acid-base regulation during elevated environmental CO2 in fish. Comp Biochem Physiol A Mol Integr Physiol 236:110524. https://doi.org/10.1016/j.cbpa.2019.110524
Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983) Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36(3):165–186. https://doi.org/10.1159/000123454
Vom Berg-Maurer CM, Trivedi CA, Bollmann JH, De Marco RJ, Ryu S (2016) The severity of acute stress is represented by increased synchronous activity and recruitment of hypothalamic CRH Neurons. J Neurosci 36(11):3350–3362. https://doi.org/10.1523/jneurosci.3390-15.2016
Wan Y, Zhang Z, Lin D, Wang X, Huang T, Su J, Zhang J, Li J, Wang Y (2022) Characterization of CRH-binding protein (CRHBP) in chickens: molecular cloning, tissue distribution and investigation of its role as a negative feedback regulator within the hypothalamus-pituitary-adrenal axis. Genes (basel) 13(10):1680. https://doi.org/10.3390/genes13101680
Wang X, Feng Y, Zhang Z, Li C, Han H (2023) Balance dysfunction in large yellow croaker in response to ocean acidification. Sci Total Environ 874:162444. https://doi.org/10.1016/j.scitotenv.2023.162444
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77(3):591–625. https://doi.org/10.1152/physrev.1997.77.3.591
Williams TA, Bergstrome JC, Scott J, Bernier NJ (2017) CRF and urocortin 3 protect the heart from hypoxia/reoxygenation-induced apoptosis in zebrafish. Am J Physiol Regul Integr Comp Physiol 313(2):R91–R100. https://doi.org/10.1152/ajpregu.00045.2017
Xie Y, Dorsky RI (2017) Development of the hypothalamus: conservation, modification and innovation. Development 144(9):1588–1599. https://doi.org/10.1242/dev.139055
Funding
This work was supported by the National Key Research and Development Program of China (2018YFD0900902).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Chen Haijin, Feng Yaoyi, and Cui Jinghui. The first draft of the manuscript was written by Feng Yaoyi and Chen Haijin. Wang Xiaojie and Chen Haijin revised the work and commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
All the animal experiments were approved by the College of Fisheries and Life Science at Shanghai Ocean University.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chen, H., Feng, Y., Cui, J. et al. Response of CRH system in brain and gill of marine medaka to seawater acidification. Fish Physiol Biochem (2024). https://doi.org/10.1007/s10695-024-01332-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10695-024-01332-7