One of the most definitive examples of a vertebrate extraorganismal structural protein can be found in three-spined sticklebacks (Gasterosteus aculeatus). In the breeding male the kidney hypertrophies and synthesizes an adhesive protein called "spiggin," which is secreted into the urinary bladder from where it is employed as a structural thread for nest building. This paper describes the first molecular characterization of spiggin and demonstrates that this adhesive is a protein complex assembled from a potential of three distinct subunits (␣, , and ␥). These subunits arise by alternative splicing, and 11-ketoandrogens induce their expression in stickleback kidneys. Analysis of the predicted amino acid sequence of each subunit reveals a modular organization whose structural elements display a similarity to the multimerization domains found within von Willebrand Factor-related proteins. These results implicate that spiggin utilizes a conserved multimerization mechanism for the formation of a viscous agglutinate from its constituent subunits in the urinary bladders of male sticklebacks. This novel extraorganismal structural protein is therefore ideally suited to its function as an adhesive thread.Extrorganismal proteins are common among invertebrates. Examples range from the fibroin threads forming spider webs and silkworm cocoons (1, 2) to the collagen-based matrixes of the byssus threads of Mytilus and the Drosophila sgs family (3, 4).
In sticklebacks, sexual maturation is stimulated by long photoperiods but not by short photoperiods, even at high temperatures. Extra-retinal photoreception can mediate this response, and appears to be more important than retinal photoreception. Although plasma melatonin levels are high at night and low during the day, experiments using melatonin administration via the water indicate that melatonin is of no or little importance for the photoperiodic response. Androgens can be aromatised to estrogens in the stickleback brain. Treatment with aromatase inhibitors stimulates maturation of males also under short photoperiod, suggesting that aromatase is involved in the suppressive actions of short photoperiod. Expression of both follicle stimulating hormone (FSH)-β and luteinizing hormone (LH)-β is higher under long than under short photoperiod. FSH-β is controlled by a negative steroid feedback on the brain-pituitary-gonad axis under short photoperiod and by a positive steroid feedback under long photoperiod. It is suggested that the former can suppress reproduction under short photoperiod and the latter can stimulate breeding under long photoperiod.
Although 11-ketotestosterone is a potent androgen and induces male secondary sex characteristics in many teleosts, androgen receptors with high binding affinity for 11-ketotestosterone or preferential activation by 11-ketotestosterone have not been identified. So, the mechanism by which 11-ketotestosterone exhibits such high potency remains unclear. Recently we cloned the cDNA of an 11-ketotestosterone regulated protein, spiggin, from three-spined stickleback renal tissue. As spiggin is the only identified gene product regulated by 11-ketotestosterone, the stickleback kidney is ideal for determination of the mechanism of 11-ketotestosterone gene regulation. A single androgen receptor gene with two splicing variants, belonging to the androgen receptor-β subfamily was cloned from stickleback kidney. A high affinity, saturable, single class of androgen specific binding sites, with the characteristics of an androgen receptor, was identified in renal cytosolic and nuclear fractions. Measurement of ligand binding moieties in the cytosolic and nuclear fractions as well as to the recombinant receptor revealed lower affinity for 11-ketotestosterone than for dihydrotestosterone. Treatment with different androgens did not upregulate androgen receptor mRNA level or increase receptor abundance, suggesting that autoregulation is not involved in differential ligand activation. However, comparison of the transactivation potential of the stickleback androgen receptor with the human androgen receptor, in both human HepG2 cells and zebrafish ZFL cells, revealed preferential activation by 11-ketotestosterone of the stickleback receptor, but not of the human receptor. These findings demonstrate the presence of a receptor preferentially activated by 11-ketotestosterone in the three-spined stickleback, so far the only one known in any animal.
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