Abstract
Reproduction is one of the most important characteristics of all living organisms. In vertebrates, interactions among the hypothalamus, pituitary, and gonad are important for the regulation of reproduction. In spite of the wide variety of reproductive traits among species, the current knowledge regarding the central regulation of reproduction has mainly been acquired from mammalian studies until recently. This approach does not provide the information what is and is not common in vertebrates. Recently, molecular genetic tools became available that can be rather easily applied to the model teleost species, medaka and zebrafish. In particular, when these techniques are combined with classical surgeries developed in the twentieth century, medaka became one of the most powerful models for understanding the neuroendocrine regulation of reproduction in vertebrates. Moreover, single-cell physiological approaches, such as patch-clamp electrophysiology and Ca2+ imaging, can be performed in established transgenic lines to unveil the regulatory mechanisms at the cellular level. By combining such physiological results and results from recently developed genome editing techniques, mechanism of central regulation of reproduction has been getting clear in teleosts. In this chapter, I will discuss recent developments in understanding the central regulatory mechanisms of reproduction in teleosts in comparison with the knowledge in mammals. By comparing these two classes, a broader picture of the evolution of reproductive regulation in vertebrates will emerge.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsAbbreviations
- ARC:
-
Arcuate nucleus
- AVPV:
-
Anteroventral periventricular
- cmlc2:
-
Cardiac myosin light chain 2
- CRISPR:
-
Clustered regularly interspaced short palindromic repeats
- FSH:
-
Follicle-stimulating hormone
- FSHB:
-
Follicle-stimulating hormone β
- GnRH:
-
Gonadotropin-releasing hormone
- GPA:
-
Glycoprotein α
- HPG axis:
-
Hypothalamic-pituitary-gonadal axis
- LH:
-
Luteinizing hormone
- LHB:
-
Luteinizing hormone β
- OVX:
-
Ovariectomy
- PMSG:
-
Pregnant mare serum gonadotropin
- POA:
-
Preoptic area
- TALEN:
-
Transcription activator-like effector nuclease
References
Betancur RR, Broughton RE, Wiley EO, Carpenter K, Lopez JA, Li C, Holcroft NI, Arcila D, Sanciangco M, Cureton Ii JC, Zhang F, Buser T, Campbell MA, Ballesteros JA, Roa-Varon A, Willis S, Borden WC, Rowley T, Reneau PC, Hough DJ, Lu G, Grande T, Arratia G, Orti G (2013) The tree of life and a new classification of bony fishes. PLoS Curr 5. https://doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288
Chang JP, Peter RE (1983) Effects of pimozide and des Gly10,[D-Ala6]luteinizing hormone-releasing hormone ethylamide on serum gonadotropin concentrations, germinal vesicle migration, and ovulation in female goldfish, Carassius auratus. Gen Comp Endocrinol 52(1):30–37
Chu L, Li J, Liu Y, Hu W, Cheng CH (2014) Targeted gene disruption in zebrafish reveals noncanonical functions of LH signaling in reproduction. Mol Endocrinol 28(11):1785–1795. https://doi.org/10.1210/me.2014-1061
Chu L, Li J, Liu Y, Cheng CH (2015) Gonadotropin signaling in Zebrafish ovary and testis development: Insights from gene knockout study. Mol Endocrinol 29(12):1743–1758. https://doi.org/10.1210/me.2015-1126
Escobar S, Felip A, Gueguen MM, Zanuy S, Carrillo M, Kah O, Servili A (2013a) Expression of kisspeptins in the brain and pituitary of the European sea bass (Dicentrarchus labrax). J Comp Neurol 521(4):933–948. https://doi.org/10.1002/cne.23211
Escobar S, Servili A, Espigares F, Gueguen MM, Brocal I, Felip A, Gomez A, Carrillo M, Zanuy S, Kah O (2013b) Expression of kisspeptins and kiss receptors suggests a large range of functions for kisspeptin systems in the brain of the European sea bass. PLoS One 8(7):e70177. https://doi.org/10.1371/journal.pone.0070177
Fontaine R, Affaticati P, Yamamoto K, Jolly C, Bureau C, Baloche S, Gonnet F, Vernier P, Dufour S, Pasqualini C (2013) Dopamine inhibits reproduction in female zebrafish (Danio rerio) via three pituitary D2 receptor subtypes. Endocrinology 154(2):807–818. https://doi.org/10.1210/en.2012-1759
Hasebe M, Kanda S, Shimada H, Akazome Y, Abe H, Oka Y (2014) Kiss1 neurons drastically change their firing activity in accordance with the reproductive state: insights from a seasonal breeder. Endocrinology 155(12):4868–4880. https://doi.org/10.1210/en.2014-1472
Hasebe M, Kanda S, Oka Y (2016) Female-Specific Glucose Sensitivity of GnRH1 Neurons Leads to Sexually Dimorphic Inhibition of Reproduction in Medaka. Endocrinology 157(11):4318–4329. https://doi.org/10.1210/en.2016-1352
Hiraki T, Nakasone K, Hosono K, Kawabata Y, Nagahama Y, Okubo K (2014) Neuropeptide B is female-specifically expressed in the telencephalic and preoptic nuclei of the medaka brain. Endocrinology 155(3):1021–1032. https://doi.org/10.1210/en.2013-1806
Kanda S, Oka Y (2012) Evolutionary insights into the steroid sensitive kiss1 and kiss2 neurons in the vertebrate brain. Front Endocrinol 3(28). https://doi.org/10.3389/fendo.2012.00028
Kanda S, Akazome Y, Matsunaga T, Yamamoto N, Yamada S, Tsukamura H, Maeda K, Oka Y (2008) Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology 149(5):2467–2476. https://doi.org/10.1210/en.2007-1503
Kanda S, Nishikawa K, Karigo T, Okubo K, Isomae S, Abe H, Kobayashi D, Oka Y (2010) Regular pacemaker activity characterizes gonadotropin-releasing hormone 2 neurons recorded from green fluorescent protein-transgenic medaka. Endocrinology 151(2):695–701. https://doi.org/10.1210/en.2009-0842
Kanda S, Okubo K, Oka Y (2011) Differential regulation of the luteinizing hormone genes in teleosts and tetrapods due to their distinct genomic environments - Insights into gonadotropin beta subunit evolution. Gen Comp Endocrinol 173(2):253–258. https://doi.org/10.1016/j.ygcen.2011.05.015
Kanda S, Karigo T, Oka Y (2012) Steroid sensitive kiss2 neurones in the goldfish: evolutionary insights into the duplicate kisspeptin gene-expressing neurones. J Neuroendocrinol 24(6):897–906. https://doi.org/10.1111/j.1365-2826.2012.02296.x
Kanda S, Akazome Y, Mitani Y, Okubo K, Oka Y (2013) Neuroanatomical evidence that kisspeptin directly regulates isotocin and vasotocin neurons. PLoS One 8(4):e62776. https://doi.org/10.1371/journal.pone.0062776
Karigo T, Kanda S, Takahashi A, Abe H, Okubo K, Oka Y (2012) Time-of-Day-Dependent changes in GnRH1 neuronal activities and Gonadotropin mRNA expression in a daily spawning fish, Medaka. Endocrinology 153(7):3394–3404. https://doi.org/10.1210/en.2011-2022
Karigo T, Aikawa M, Kondo C, Abe H, Kanda S, Oka Y (2014) Whole brain-pituitary in vitro preparation of the transgenic medaka (Oryzias latipes) as a tool for analyzing the differential regulatory mechanisms of LH and FSH release. Endocrinology 155(2):536–547. https://doi.org/10.1210/en.2013-1642
Liu Y, Tang H, Xie R, Li S, Liu X, Lin H, Zhang Y, Cheng CH (2017) Genetic Evidence for Multifactorial Control of the Reproductive Axis in Zebrafish. Endocrinology 158(3):604–611. https://doi.org/10.1210/en.2016-1540
Maruyama K, Wang B, Ishikawa Y, Yasumasu S, Iuchi I (2012) 1kbp 5’ upstream sequence enables developmental stage-specific expressions of globin genes in the fish, medaka Oryzias latipes. Gene 492(1):212–219. https://doi.org/10.1016/j.gene.2011.10.026
Mitani Y, Kanda S, Akazome Y, Zempo B, Oka Y (2010) Hypothalamic Kiss1 but not Kiss2 neurons are involved in estrogen feedback in medaka (Oryzias latipes). Endocrinology 151(4):1751–1759. https://doi.org/10.1210/en.2009-1174
Murozumi N, Nakashima R, Hirai T, Kamei Y, Ishikawa-Fujiwara T, Todo T, Kitano T (2014) Loss of follicle-stimulating hormone receptor function causes masculinization and suppression of ovarian development in genetically female medaka. Endocrinology 155(8):3136–3145. https://doi.org/10.1210/en.2013-2060
Nakajo M, Kanda S, Karigo T, Takahashi A, Akazome Y, Uenoyama Y, Kobayashi M, Oka Y (2017) Evolutionally conserved function of kisspeptin neuronal system is non-reproductive regulation as revealed by non-mammalian study. Endocrinology 159(1):163-183. https://doi.org/10.1210/en.2017-00808
Ogiwara K, Fujimori C, Rajapakse S, Takahashi T (2013) Characterization of luteinizing hormone and luteinizing hormone receptor and their indispensable role in the ovulatory process of the medaka. PLoS One 8(1):e54482. https://doi.org/10.1371/journal.pone.0054482
Okubo K, Sakai F, Lau EL, Yoshizaki G, Takeuchi Y, Naruse K, Aida K, Nagahama Y (2006) Forebrain gonadotropin-releasing hormone neuronal development: insights from transgenic medaka and the relevance to X-linked Kallmann syndrome. Endocrinology 147(3):1076–1084. https://doi.org/10.1210/en.2005-0468
Spicer OS, Wong TT, Zmora N, Zohar Y (2016) Targeted Mutagenesis of the Hypophysiotropic Gnrh3 in Zebrafish (Danio rerio) Reveals No Effects on Reproductive Performance. PLoS One 11(6):e0158141. https://doi.org/10.1371/journal.pone.0158141
Takahashi T, Fujimori C, Hagiwara A, Ogiwara K (2013) Recent advances in the understanding of teleost medaka ovulation: the roles of proteases and prostaglandins. Zool Sci 30(4):239–247. https://doi.org/10.2108/zsj.30.239
Takahashi A, Islam MS, Abe H, Okubo K, Akazome Y, Kaneko T, Hioki H, Oka Y (2016a) Morphological analysis of the early development of telencephalic and diencephalic gonadotropin-releasing hormone neuronal systems in enhanced green fluorescent protein-expressing transgenic medaka lines. J Comp Neurol 524(4):896–913. https://doi.org/10.1002/cne.23883
Takahashi A, Kanda S, Abe T, Oka Y (2016b) Evolution of the hypothalamic-pituitary-gonadal axis regulation in vertebrates revealed by Knockout Medaka. Endocrinology 157(10):3994–4002. https://doi.org/10.1210/en.2016-1356
Zhang Z, Lau SW, Zhang L, Ge W (2015a) Disruption of zebrafish Follicle-Stimulating Hormone Receptor (fshr) but not Luteinizing Hormone Receptor (lhcgr) gene by TALEN leads to failed follicle activation in females followed by sexual reversal to males. Endocrinology 156(10):3747–3762. https://doi.org/10.1210/en.2015-1039
Zhang Z, Zhu B, Ge W (2015b) Genetic analysis of zebrafish gonadotropin (FSH and LH) functions by TALEN-mediated gene disruption. Mol Endocrinol 29(1):76–98. https://doi.org/10.1210/me.2014-1256
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Kanda, S. (2018). Small Teleosts Provide Hints Toward Understanding the Evolution of the Central Regulatory Mechanisms of Reproduction. In: Hirata, H., Iida, A. (eds) Zebrafish, Medaka, and Other Small Fishes. Springer, Singapore. https://doi.org/10.1007/978-981-13-1879-5_6
Download citation
DOI: https://doi.org/10.1007/978-981-13-1879-5_6
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-13-1878-8
Online ISBN: 978-981-13-1879-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)