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Hypothalamic-Pituitary-Gonadal Axis Social Regulation of Gene Social Regulation of Gene Expression in the Hypothalamic-Pituitary-Gonadal Axis Karen P. Maruska and Russell D. Fernald Physiology 26:412-423, 2011. doi:10.1152/physiol.00032.2011 You might find this additional info useful... This article cites 152 articles, 51 of which can be accessed free at: http://physiologyonline.physiology.org/content/26/6/412.full.html#ref-list-1 Updated information and services including high resolution figures, can be found at: http://physiologyonline.physiology.org/content/26/6/412.full.html Additional material and information about Physiology can be found at: http://www.the-aps.org/publications/physiol Downloaded from This infomation is current as of December 15, 2011. physiologyonline.physiology.org on December 15, 2011 Physiology (formerly published as News in Physiological Science) publishes brief review articles on major physiological developments. It is published bimonthly in February, April, June, August, October, and December by the American Physiological Society, 9650 Rockville Pike, Bethesda MD 20814-3991. Copyright © 2011 by the American Physiological Society. ISSN: 1548-9213, ESSN: 1548-9221. Visit our website at http://www.the-aps.org/. REVIEWS PHYSIOLOGY 26: 412–423, 2011; doi:10.1152/physiol.00032.2011 Karen P. Maruska and Social Regulation of Gene Expression in Russell D. Fernald Department of Biology, Stanford University, Stanford, California the Hypothalamic-Pituitary-Gonadal Axis [email protected] Reproduction is a critically important event in every animals’ life and in all vertebrates is controlled by the brain via the hypothalamic-pituitary-gonadal (HPG) axis. In many species, this axis, and hence reproductive fitness, can be profoundly influenced by the social environment. Here, we review how the reception of information in a social context causes genomic changes at each level of the HPG axis. Reproduction is arguably the most important event cal roles in HPG axis function, we discuss the social in any animals’ life. Thus understanding how repro- influence of these upstream regulators of GnRH duction is regulated offers important insights into the neurons as well. We use examples from the social evolution of a species. In particular, learning how African cichlid fish Astatotilapia (formerly Haplo- Downloaded from social and physiological factors collaborate to control chromis) burtoni as a model to illustrate how rap- reproductive activity is essential for understanding idly the social environment can influence the selective pressures that have shaped reproductive genome at every level of the HPG axis. Finally, we control. For example, how does reception of social discuss how little is actually known about the neu- information reach brain regions responsible for ini- ral pathways and mechanisms that translate social tiating reproductive behaviors, how is gamete information into a genomic response that ulti- physiologyonline.physiology.org (sperm, oocyte) production and steroid hormone re- mately changes the activity of the reproductive lease controlled, and, ultimately, how do social inter- axis. This sociogenomic frontier awaits future com- actions influence gene expression to control parative research in diverse taxa. reproduction? Although there are many studies on regulation of social behaviors from molecular or GnRH and the HPG Axis in Fishes genomic perspectives (120, 121), much less is known and Mammals about how social information directly influences the reproductive genome from the brain to the gonads. Reproduction in all vertebrates is controlled by the Here, we review how social information can influ- highly conserved HPG axis (FIGURE 1). At its apex ence plasticity in gene expression of the highly con- are the GnRH neurons in the hypothalamic-preop- on December 15, 2011 served vertebrate hypothalamic-pituitary-gonadal tic area of the brain that ultimately control repro- (HPG) reproductive control system. duction by integrating information from social and For the purpose of this review, we define social environmental signals with internal information behaviors as interactions among members of the such as nutritional and hormonal state. The output same species that influence immediate or future of this integration controls GnRH production in behaviors (120). Importantly, these interactions in- the brain and its release to the pituitary gland. clude the production, reception, and interpreta- GnRH, a decapeptide, is conserved across all ver- tion of communicative signals that influence tebrates and was recently also found in several individual behaviors in a context-dependent man- invertebrates, emphasizing its evolutionary impor- ner. Specifically, we concentrate on how commu- tance (91, 140). There are multiple GnRH forms nication signals in a social context produce found across taxa, all of which have close phyloge- genomic changes to alter the function of the HPG netic relationships and putative common origin axis. We focus on key elements in the signaling (20, 150). Teleost fishes have two or three different pathway initiated by gonadotropin-releasing hor- forms located in distinct brain regions, whereas mone (GnRH) neurons in the brain, their impact most mammals express only two forms (20, 131). on gonadotrope-producing cells [luteinizing hor- GnRH3 ({Trp7Leu8}-GnRH) has only been found in mone (LH); follicle-stimulating hormone (FSH)] of fishes, where it is localized in the terminal nerve the anterior pituitary gland, and the activation ganglia, olfactory bulb, and ventral forebrain, and of LH and FSH receptors in the testes that leads some evidence suggests it may be a neuromodula- to stimulation of steroid biosynthesis and sperm tor (1, 57, 58, 85, 100). GnRH2 ({His5Trp7Tyr8}- production. In light of the recent evidence show- GnRH) is identical in all species examined to ing the RFamides, including kisspeptin and date, including humans, and is produced by neu- gonadotropin inhibitory hormone, also play criti- rons in the midbrain tegmentum. Limited data are 412 1548-9213/11 ©2011 Int. Union Physiol. Sci./Am. Physiol. Soc. REVIEWS Downloaded from physiologyonline.physiology.org on December 15, 2011 FIGURE 1. Schematic representation of the hypothalamic-pituitary-gonadal axis in teleost fishes and mammals Information from social contexts is ultimately integrated by gonadotropin-releasing hormone (GnRH1) neurons in the preoptic-hypothalamic re- gion of the brain to regulate the output of the reproductive axis. In fishes, GnRH1 neurons project directly to the pituitary gland (shown in red), whereas in mammals GnRH1 neurons release peptide into the median eminence (ME) where it is then transported via the hypothalamic-hypophy- seal portal system to the anterior pituitary. In both taxa, LH and FSH are released from the pituitary and travel through the bloodstream to their target receptors in the testes to stimulate sperm production and steroid hormone synthesis and release. The organization of the testes also dif- fers between fishes and mammals, as well as the cellular localization of LH and FSH receptors. In fishes, the testes is organized into membrane- bound spermatocysts that contain a group of synchronously developing germ cells derived from the same spermatogonial stem cell, followed by release of the mature spermatozoa into a central lumen. In mammals, spermatogenesis takes place in the seminiferous tubules where germ cells develop from the tubule wall in a centripetal direction toward the central lumen. POA, preoptic area. PHYSIOLOGY • Volume 26 • December 2011 • www.physiologyonline.org 413 REVIEWS consistent with a role for GnRH2 in coordinating general circulation to the testes where they bind to reproduction with metabolic state (56, 86), modu- LH and FSH receptors, a family of rhodopsin-like lating pineal gland activity (127), modulating sen- G-protein-coupled receptors. Here again, there are sory system function (85), and possibly influencing noteworthy differences in cellular localization of motor reproductive pathways (18, 77). GnRH1 is the receptors and how LH and FSH act in the testes the hypophysiotrophic form produced by neurons between fishes and mammals. In mammals, LHR is in the hypothalamic-preoptic area that stimulates expressed in Leydig cells and primarily functions to the pituitary gland. Despite its conserved function, stimulate steroid biosynthesis and release, whereas the amino acid sequence of GnRH1 differs slightly FSHR is found in Sertoli cells and plays a major role among species (see Refs. 20, 60, 91 for reviews). in sperm production (72, 97, 146). In teleosts, how- Although the functional actions of the HPG axis are ever, LHR is expressed in both Leydig and Sertoli conserved across all vertebrates, the basic anatomi- cells, and FSHR is found in Leydig, Sertoli, and cal organization of the hypothalamic-pituitary con- early germ cells (41, 42, 72). Thus the duality of nection differs fundamentally between fishes and gonadotropin function found in mammals is not mammals (FIGURE 1). In teleost fishes, GnRH1 neu- apparent in most fishes because both LH and FSH are often equipotent in stimulating steroid produc- rons in the preoptic area of the brain send axonal tion and can regulate spermatogenesis at different projections directly to the anterior pituitary gland stages (42, 72). Downloaded from where GnRH1 is released from nerve terminals in the vicinity of the gonadotrope cells, binds to mem- The African Cichlid Fish brane-bound G-protein-coupled GnRH receptors, Astatotilapia Burtoni as a Model and causes synthesis and release of the two gonado-
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