Expression of Deep Brain Photoreceptors in the Pekin Drake: a Possible Role in the Maintenance of Testicular Function
Total Page:16
File Type:pdf, Size:1020Kb
Edinburgh Research Explorer Expression of deep brain photoreceptors in the Pekin drake: a possible role in the maintenance of testicular function Citation for published version: Haas, R, Alenciks, E, Meddle, S & Fraley, GS 2017, 'Expression of deep brain photoreceptors in the Pekin drake: a possible role in the maintenance of testicular function', Poultry Science, vol. 96, no. 8, pp. 2908- 2919. https://doi.org/10.3382/ps/pex037 Digital Object Identifier (DOI): 10.3382/ps/pex037 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: Poultry Science Publisher Rights Statement: ©The Author 2017. Published by Oxford University Press on behalf of Poultry Science Association. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 07. Oct. 2021 Expression of deep brain photoreceptors in the Pekin drake: a possible role in the maintenance of testicular function R. Haas,∗ E. Alenciks,∗ S. Meddle,† and G. S. Fraley∗,1 ∗Biology Department, Hope College, Holland, MI; and †The Roslin Institute and Royal (Dick) School of Veterinary Studies, The Roslin Institute Building, The University of Edinburgh, Easter Bush Campus, Midlothian EH25 9RG, Scotland. UK ABSTRACT Several putative deep brain photorecep- further investigate this photoperiodic response, we ex- tors (DBPs) have been identified, such as melanopsin, posed drakes to chronic red, long-day white, short-day opsin 5, and vertebrate ancient opsin. The aim of this white, or blue light. Blue light elicited gonadal regres- study was to elucidate the role of DBPs in gonadal reg- sion, as testes weight (P < 0.001) and plasma luteiniz- ulation in the Pekin drake. As previously reported, we ing hormone (LH) levels (P < 0.001) were lower com- observed opsin-like immunoreactivity (-ir) in the lat- pared to drakes housed under long-day white light. eral septum (LS), melanopsin-ir in the premammillary Photo-regressed drakes experienced complete gonadal nucleus (PMM), and opsin 5-ir in the periventricular recrudescence when housed under long-day red and organ. To determine the sensitivity of the DBPs to spe- blue light. qRT-PCR analyses showed that gonadally cific wavelengths of light, drakes were given an acute regressed drakes showed reduced levels (P < 0.01) of exposure to red, blue, or white light. Blue light stim- gonadotropin releasing hormone (GnRH) mRNA but ulated an increase (P < 0.01) in the immediate early not photoreceptor or GnIH mRNAs compared to go- gene fra-2-ir co-expression in melanopsin-ir neurons in nadally functional drakes. Our data suggest DBP in the PMM, and red light increased (P < 0.05) fra-2- the LS may be rhodosin and multiple DBPs are re- ir co-expression in opsin-ir neurons, suggesting these quired to fully maintain gonadal function in Pekin neurons are blue- and red-receptive, respectively. To drakes. Key words: rhodopsin, melanopsin, opsin 5, vertebrate ancient opsin, gonadal recrudescence, luteinizing hormone 2017 Poultry Science 0:1–12 http://dx.doi.org/10.3382/ps/pex037 INTRODUCTION productively active size, and to a near pre-pubertal state of seminiferous tubule differentiation (Cherry and Pekin ducks were domesticated from the wild mal- Morris, 2005). However, during breeding season, the ac- lard (Anas platyrhynchos) between 4,000 to 10,000 tivation of the drake’s hypothalamic-pituitary-gonadal years ago in southern China. Despite domestication, axis (HPG) ultimately stimulates testicular hypertro- the Pekin duck has maintained many of the growth phy, spermatogenesis, and androgen secretion. Despite and reproductive characteristics of its wild predeces- decades of research, the precise neural mechanisms sor (Cherry and Morris, 2008). A prominent physio- within the hypothalamus that underlie photoactivation logical characteristic is seasonal reproduction and their of gonadotropin releasing hormone (GnRH) remains photosensitivity to increasing day length that triggers unclear. a rapid gonadal recrudescence as a component of sea- In mammals, photoreceptivity includes the activ- sonal breeding. During the non-breeding season, the ity of rods and cones within the retina, as well as drake’s testes regress to less than 10% of their re- non-image forming photosensitive retinal ganglion cells. Non-image-forming retinal cells regulate environmental C The Author 2017. Published by Oxford University Press light responses, including circadian entrainment (Panda on behalf of Poultry Science Association. This is an Open Ac- et al., 2002; Panda et al., 2003a,b) and the pupillary cess article distributed under the terms of the Creative Commons light reflex (Heaton, 1971; Hattar et al., 2002;Lin Attribution Non-Commercial License (http://creativecommons.org/ et al., 2008). These cells are also known to activate licenses/by-nc/4.0/), which permits non-commercial re-use, distri- bution, and reproduction in any medium, provided the original diencephalic nuclei, such as the suprachiasmatic nu- work is properly cited. For commercial re-use, please contact jour- cleus, and in turn affect melatonin secretion from the [email protected] pineal gland (for review, see Wagner et al., 2008). In Received September 20, 2016. Accepted February 4, 2017. birds, the removal of these retinal cells does not affect 1Corresponding author: [email protected] the seasonal changes in the HPG (Oliver and Bayle, 1 2 HAAS ET AL. 1982). However, if light is prevented from penetrating DBPs and reproduction in the Pekin drake. We found the skull, a loss in photoresponsiveness leads to go- that blue light was not able to maintain gonadal ac- nadal regression (Menaker et al., 1970; Underwood and tivity in drakes following either an acute or long-term Menaker, 1970a,b,c). Hence, in birds there is compelling exposure. Further, our data suggests that the Ret-P1-ir evidence that photoresponsiveness is mediated—at in lateral septum (LS)may be indicative of rhodopsin least in part—by non-retinal neurons that express (OPN2). photosensitive chemicals. These neurons have been referred to as deep brain photoreceptors (DBPs; METHODS reviewed in (Li and Kuenzel, 2008)). The identities of the DBPs have been somewhat elu- sive. Over the past 2 decades, some success in identi- Animals and Housing fying putative DBPs has come from using anti-Ret-P1 All ducks were sexually active Pekin drakes (∼45 wk antibodies. Photo-responsive receptors are transmem- of age) obtained from Maple Leaf Farms, Inc. (Lees- brane G-protein coupled receptors that transduce light burg, IN) and housed in the Hope College aviary at a energy into a neuronal signal (Hattar et al., 2002). Suc- density of about ≥0.3 m2 per duck. Lights were set on cess in identifying putative DBPs has come by stain- a 18:6 h light:dark cycle. Birds arrived at Hope Col- ing for 4 different, albeit related, photoreceptors: opsin lege in early May; they were housed in floor pens and (Ret-P1; Silver et al., 1988; Saldanha et al., 2001), allowed ad libitum access to water via pin-metered wa- opsin 5 (neuropsin or OPN5; Nakane et al., 2010), ver- ter lines. Ducks were fed standard Pekin duck breeder tebrate ancient opsin (VA; Halford et al., 2009), and chow and given access to the feed for 7 h/d, following melanopsin (ONPN4; Hattar et al., 2002; Panda et typical standards of care for breeder ducks. Ducks were al., 2002; Nayak et al., 2007). The VA opsin has been raised on pine litter with fresh litter spread over the en- found in the mediobasal preoptic area and paraventric- tire pen twice daily. Birds were housed for 1 wk prior to ular nucleus with fiber terminals shown in the medial the start of the experiment. All housing and experimen- basal hypothalamus, particularly the median eminence tal procedures were approved by Hope College Animal (Halford et al., 2009). OPN5 has been found in the par- Care and Use Committee. aventricular organ in the medial basal hypothalamus. OPN4 is a member of a well-conserved family of photoreceptive proteins and its gene has been identi- Experiment 1: Immunocytochemistry for fied in numerous species including humans, birds, am- Localization of Ret-P1, OPN4, and OPN5 phibians and fish (for review see (Bellingham et al., 2006)). In birds, OPN4 immunoreactivity (-ir) has been Antibodies Several primary antibodies were utilized localized to the premammillary nucleus (PMM)and for this experiment. The first is a commercially avail- is co-localized with tyrosine hydroxylase-ir neurons— able mouse anti-Ret-P1 (Ret-P1, Abcam, Inc., Cam- presumably dopaminergic (El Halawani et al., 2009; bridge, MA) monoclonal antibody raised against the Kang et al., 2010). Several studies have suggested that extracellular fragment of the Ret-P1 (opsin) peptide. melanopsin receptors are responsive to blue-specific This antibody has been successfully utilized in other light wavelengths in several species (Iyilikci et al., 2009; non-mammalian species (Silver et al., 1988). The sec- Bailes and Lucas, 2013; Tsunematsu et al., 2013; Ramos ond primary antibody was a rabbit anti-OPN4 poly- et al., 2014; Takeuchi et al., 2014; Walmsley et al., clonal that was generously provided by Dr.