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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION |
,1
ska
* Centre for Medical Biology, Polish Academy of Sciences, Lodz, 93-232 Poland; Department of Pharmacodynamics, Medical University of Lodz, 90-151 Poland; Department of Pharmacology, Medical University of Lodz, 90-752 Poland; Institut des Neurosciences Cellulaires et Intégratives, Départment de Neurobiologie des Rythmes, Unité Mixte de Recherche 7168/LC2 Université Louis Pasteur—Centre National de la Recherche Scientifique, Strasbourg, 67000 France; and || Centre for Chronobiology, School of Biomedical and Molecular Sciences, University of Surrey, Guildford GU2 7XH, United Kingdom
1 Corresponding author: jzawilska{at}pharm.am.lodz.pl
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: melatonin • turkey • pineal gland • retina • photoperiod
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Although many avian species are photoperiodic, regulatory mechanisms responsible for adjusting their physiology and behavior to annual changes in day-length are less well understood than in mammals. Initially, it was postulated that birds, in contrast to mammals, do not use seasonal changes in nocturnal melatonin production to time their reproductive activity, and the role of melatonin in avian physiology has remained enigmatic for many years (Wilson, 1991; Juss et al., 1993; Pévet, 2001; Underwood et al., 2001). Despite this, evidence is accumulating for a relationship between melatonin and several seasonal processes, including gonadal size and activity (Ramachandran et al., 1996; Sudhakumari et al., 2001; Singh and Haldar, 2007), sexual development (Guyomarc’h et al., 2001), egg production (Siopes and Underwood, 1987), cellular and humoral immune responses (Moore and Siopes, 2000, 2002; Moore et al., 2002; Singh and Haldar, 2007), cold resistance and thermogenesis (Saarela and Heldmaier, 1987), and endocrine activity of the adrenal glands (Ramachandran et al., 1996; Sudhakumari et al., 2001). Moreover, it has recently been postulated that melatonin, by stimulating expression of a newly discovered gonadotropin-inhibitory hormone, may provide an important photoperiodic signal to influence the reproductive axis of birds (Ubuka et al., 2005; Tsutsui et al., 2006).
The turkey (Meleagris gallopavo), a representative of galli-forms, is an avian species in which several physiological processes (including growth, sexual development, egg production), and changes in plasma concentrations of luteinizing hormone and prolactin are potently influenced by photoperiod (Siopes et al., 1993; Siopes, 1994; Bedecarrats et al., 1997; Yang et al., 1999; Noirault et al., 2006). Until now, the regulatory mechanisms governing photoperiod-dependent responses in the turkey were unknown. One of the likely candidates for transducing environmental photic information might be melatonin. To begin to define a putative role for melatonin in photoperiodic time measurement in the turkey, it is imperative to obtain data on the regulation of melatonin production. We previously demonstrated that the turkey pineal gland and retina synthesize melatonin in a circadian manner (Zawilska et al., 2006). In the present study, we investigated whether melatonin production in the turkey is sensitive to changes in day-length. Melatonin content and the activity of the melatonin-synthesizing enzymes, serotonin N-acetyltransferase (AA-NAT; EC 2.3.1.87 [EC] ) and hydroxyindole-O-methyltransferase (HIOMT; EC 2.1.1.4 [EC] ), were thus measured in the pineal gland, retina, and plasma at regular time intervals from turkeys that were adapted to 3 different photoperiods, namely, a long photoperiod of 16L:8D, a regular photoperiod of 12L:12D, and a short photoperiod of 8L:16D. In addition, we analyzed whether the responsiveness of pineal and retinal AANAT activity to the suppressive action of light at night is modified by the photoperiodic history of the turkey.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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After adaptation for a month, the turkeys were decapitated at 3-h intervals over a 24-h period, starting from the beginning of the dark phase of the imposed L:D cycle. Additionally, groups of animals that were maintained under the long photoperiod and the short photoperiod were killed at the end of the dark phase. Pineal glands and retinas were quickly isolated, frozen on dry ice, and stored at –70°C (maximally for 3 d) before biochemical analysis. Trunk blood was collected in heparinized tubes. After centrifugation (at 3,000 x g for 30 min at 4°C), the plasma was stored at –70°C until melatonin analysis. Decapitation of the turkeys and tissue isolation during the dark phase of an imposed L:D cycle were performed under dim (3-lx) red light. In another set of experiments, in the middle of the dark phase of the imposed L:D cycle (i.e., 4, 6, and 8 h after lights off in the long, regular, and short photoperiod, respectively), groups of turkeys were exposed to white light (150 lx) for 0.5, 2, 10, or 30 min, and killed immediately afterward. Pineal glands and retinas were quickly isolated, frozen on dry ice, and stored at –70°C (maximally for 3 d) before measurement of AANAT activity.
Biochemical Assays
Pineal glands and retinas were sonicated in ice-cold 0.05 M sodium phosphate buffer (pH 6.8) in a proportion of 1 pineal/200 µL, and 1 mg of wet retina/10 µL. The homogenate was centrifuged at 10,000 x g for 5 min at 4°C, and aliquots of the supernatant were assayed for AANAT activity, HIOMT activity, and melatonin.
Serotonin N-acetyltransferase activity was determined according to our routine radioisotopic procedure (Nowak et al., 1989), using acetyl coenzyme A (152 µM) containing 16 nCi of [acetyl-1-14C]coenzyme A and tryptamine-HCl as substrates. To measure HIOMT activity, aliquots of pineal and retinal supernatants were adjusted to pH 7.9 with 0.05 mM sodium phosphate buffer (pH 9.0). Hydroxyindole-O-methyltransferase activity was measured by a radiosotopic method (Nowak et al., 1993), using N-acetylserotonin and S-adenosyl-L-methionine (100 µM) containing 20 nCi of S-[methyl-14C]adenosyl-L-methionine as substrates.
Melatonin was extracted from retinal supernatants and plasma using dichloromethane as described previously (Rudolf et al., 1992); melatonin standards were extracted using the same procedure. To measure pineal melatonin content, aliquots of tissue supernatant were diluted in ice-cold 0.1 M tricine buffer (pH 5.0, containing 0.9% NaCl and 0.1% gelatin). Melatonin was measured by RIA, using a rabbit antiserum (batch no. R19540; INRA, Nouzilly, France) at a final dilution of 1:200,000 and [125I]iodomelatonin as a tracer (Rudolf et al., 1992). Polyethylene glycol in combination with sheep antirabbit antiserum (INRA) was used to separate the bound and free tracer. The limit of sensitivity of the assay was 1.0 pg/tube. Measurements of quality controls containing 6, 30, and 150 pg of melatonin/tube gave interassay coefficients of 13.6, 14.2, and 12.0%, respectively. The RIA was validated by assessing the parallelism between serial dilutions of pineal supernatants or dichloromethane extracts of plasma and retinal samples and the melatonin standard curve. Furthermore, quantitative recovery experiments showed that the amount of melatonin measured by RIA was closely correlated with the amount of standard melatonin (25 to 500 pg/mL) added to pools of the tissue samples analyzed (Zawilska et al., 2006).
Acetyl coenzyme A, N-acetylserotonin, S-adenosyl-L-methionine, and melatonin were purchased from Sigma Chemical Co. (St. Louis, MO), tryptamine was obtained from Serva (Heildelberg, Germany). [Acetyl-1-14C]Coenzyme A (specific activity, 60 mCi/mmol), and S-[methyl-14C]adenosyl-L-methionine (specific activity, 52.7 mCi/mmol) were purchased from PerkinElmer Life Sciences (Boston, MA). Other chemicals were of analytical purity and were purchased mainly from Sigma Chemical Co.
Data Analysis
Data are expressed as the means ± SEM values and were analyzed for statistical significance by one-way ANOVA followed by a posthoc Student-Newman-Keuls test using GraphPad InStat version 3.05 for Windows 95 (GraphPad, San Diego, CA). To test for rhythmicity, we used the traditional F-test, which compares the (reparameterized) cosine model [c = M + A x cos(F x t + 
) + 
t, where c is the observed mean concentration of the compound at a given time t, F is the angular frequency, A is the amplitude, is the acrophase expressed in radians, and t is the deviation of observed values from the fitted curve] with the nonrhythmic model (c = M + t). The F-test was performed using GraphPad InPlot version 4.00 for Windows (GraphPad). The area under the curve (AUC) was calculated with the aid of SigmaPlot, version 8.02 (Systat Software Inc., Chicago, IL).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Both melatonin content and AANAT activity were high during the dark phase and low during the light phase of the imposed L:D cycle. The nighttime increase in pineal melatonin content and AANAT activity in turkeys kept under a short photoperiod was slower compared with changes observed in birds kept under the long and regular photoperiods. During the long photoperiod, the maximum pineal AANAT activity was significantly greater (P < 0.05) than peak values found during the regular and short photoperiods (Figure 1). During the light phase of the L:D cycle, mean pineal melatonin concentrations in turkeys kept under the long photoperiod (172 ± 19 pg/mg of pineal; n = 34) were significantly higher (P < 0.001) than those found in pineals isolated from birds maintained under the regular (75 ± 7 pg/mg of pineal; n = 20) and short photoperiods (94 ± 17 pg/mg of pineal; n = 17). The dark-phase melatonin constituted 77% (long photoperiod), 91% (regular photoperiod), and 94% (short photoperiod) of the total amount of melatonin (AUC) produced during the 24-h period. Computer-assisted analysis revealed that pineal HIOMT activity did not exhibit significant rhythmic variation throughout the 24-h period in any of the photoperiods tested (Figure 1).
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). During the light phase of the L:D cycle, mean melatonin concentrations in the retinas of turkeys kept under the long photoperiod (17.3 ± 1.9 pg/mg of retina; n = 34) were significantly higher (P < 0.001) than those found in tissues isolated from birds maintained under the regular (6.7 ± 0.6 pg/mg of retina; n = 19) and short photoperiods (7.1 ± 0.9 pg/mg of retina; n = 18). Melatonin produced during the dark phase constituted 60% (long photoperiod), 88% (regular photoperiod), and 92% (short photoperiod) of the total amount of melatonin (AUC) produced during the 24-h period.
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Effect of Photoperiod on Plasma Melatonin Concentrations
In each photoperiod studied, plasma melatonin concentrations exhibited a clear diurnal change (Figure 3). During the short photoperiod, the amplitude of the plasma melatonin rhythm (102 ± 5 pg/mL) was significantly lower (P < 0.001) than the amplitude observed under the long (174 ± 10 pg/mL) and regular (207 ± 11 pg/mL) photoperiods. In the long photoperiod, the total AUC of the melatonin profile was markedly higher by 18 and 22% when compared with the regular and short photoperiods, respectively. In the long photoperiod, nighttime melatonin corresponded to only 48% of the total AUC; this proportion was markedly lower compared with the 72 and 77% found in the regular and short photoperiods, respectively.
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). In turkeys maintained under the regular and short photoperiods, a 2-, 10-, and 30-min pulse of light produced a statistically significant decline in pineal AANAT activity compared with the no-light condition. In turkeys adapted to the long photoperiod, only a 30-min exposure to light markedly decreased AANAT activity in the pineal gland; shorter light pulses were ineffective. In the retina, all tested light pulses produced statistically significant decreases of nighttime AANAT activity. The magnitude of the observed changes did not differ among the 3 different photoperiodic groups, with the exception of the response to a 0.5-min pulse. The response to this light pulse of very short duration was significantly weaker in the retinas of turkeys kept under the long photoperiod compared with those birds maintained in the regular and short photoperiods. The present results also revealed that the pineal gland appeared to be less sensitive to the suppressive action of light than the retina (Table 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The indoleamine hormone melatonin is synthesized by the vertebrate pineal gland and, additionally, in some species, by the retina in a light-dependent rhythmic fashion controlled by an endogenous circadian clock (reviewed by Arendt, 1995; and Iuvone et al., 2005). We previously showed that the turkey pineal gland and retina produce melatonin in a high-amplitude circadian rhythm (Zawilska et al., 2006). The present study extends these findings and demonstrates that the duration of elevated melatonin in the turkey pineal gland and retina changes potently in response to the length of the dark phase of the imposed L:D cycle. Thus, in both tissues the duration of melatonin production was significantly longer under the short photoperiod compared with the long and regular photoperiods. Similarly, the duration of elevated plasma melatonin levels (reflecting primarily pineal melatonin; Siopes and Underwood, 1987) gradually increased with the lengthening of the dark phase. These photoperiodic-dependent variations in melatonin synthesis appear to be driven by the enzyme AANAT, because changes in AANAT activity were closely correlated with changes in melatonin. By contrast, the activity of HIOMT, the final enzyme in the melatonin-synthesizing pathway, did not exhibit any significant variation throughout the 24-h period in the pineal glands and retinas isolated from turkeys kept under the 3 different photoperiods.
The photoperiod-dependent changes observed in the turkey are in agreement with the existing literature. Photoperiodic modifications of the melatonin (or AANAT activity) rhythm in the pineal gland, retina, and blood have been reported in several avian species, namely, the Japanese quail (Underwood and Siopes, 1985; Zeman and Illnerová, 1988), chicken (Binkley et al., 1977), European starling (Dawson and Van’t, 2002), house sparrow (Brandstätter et al., 2000), emperor penguin (Miché et al., 1991), and Svalbard ptarmigan (Reierth et al., 1999), with the nighttime increase reflecting the duration of the dark phase. Additionally, lengthening of the dark phase has been shown to result in reducing the amplitude of the melatonin rhythm (Underwood and Siopes, 1985; Miché et al., 1991; Reierth et al., 1999; Brandstätter et al., 2000).
Despite this agreement across studies, the physiological relevance of these photoperiod-induced changes in the melatonin signal is less clear. Changes in both the intensity and duration of the nocturnal melatonin profile might provide an important "seasonal" signal to the turkey. In addition, it may be that by manipulating the day-length, and thus the melatonin level, beneficial modulation of the immune system can be achieved. There is increasing experimental evidence demonstrating a functional link between melatonin and immune responses, not only in mammals (reviewed by Carrillo-Vico et al., 2006), but also in birds. Pinealectomy has potently reduced immune responses in the ring-dove and Japanese quail (Rodriguez and Lea, 1994; Moore et al., 2002), suggesting that immune function may be regulated by melatonin. In the Japanese quail, exogenous melatonin counteracted the immunosuppressive effect of pinealectomy or constant-light treatment (Moore and Siopes, 2000; Moore et al., 2002). Exogenous melatonin has also been shown to enhance white blood cell counts and activate B and T lymphocytes in immature chickens (Brennan et al., 2002). In addition, both embronic and posthatched exposure to melatonin accelerated the development of cell-mediated and humoral immune activities in the turkey (Moore and Siopes, 2002, 2005). Noticeably, in the turkey and chicken, mortality caused by infectious diseases is prevalent during the first few weeks post-hatch (Alexander, 1990; Law and Payne, 1990; Cook, 2000), and a strong correlation between immune dysfunction and the pathogenesis of certain diseases in neonatal birds has been demonstrated (Sharma et al., 1994; Bounous et al., 1995; Qureshi et al., 1997). Thus, as already emphasized by Moore and Siopes (2005), the immune-enhancing effect of melatonin appears to be especially important in the early stage of a turkey’s life. Whether endogenous melatonin has a similar immune-enhancing function remains to be determined.
Photoperiod-dependent changes in melatonin level might also play a regulatory role in the turkey reproductive system. Involvement of melatonin in the regulation of seasonally changing gonadal activity and gonadotropin secretion has been demonstrated for some avian species (e.g., Ohta et al., 1989; Ramachandran et al., 1996; Guyomarc’h et al., 2001; Sudhakumari et al., 2001; Trivedi et al., 2004, Singh and Haldar, 2007). In the turkey, pinealectomy of breeder hens significantly delayed the onset of egg laying and depressed egg production (Siopes and Underwood, 1987). It has recently been proposed that in birds (and likely also in mammals), melatonin regulates gonadotropin release by stimulating expression of gonadotropin-inhibitory hormone (Ubuka et al., 2005; Tsutsui et al., 2006). Gonadotropin-inhibitory hormone is the first hypothalamic neuropeptide shown to directly inhibit gonadotropin release at the pituitary level (Yin et al., 2005). Gonadotropin-inhibitory hormone may also act on the hypothalamus to inhibit release of gonadotropin-releasing hormone (Yin et al., 2005; Bentley et al., 2006). However, whether melatonin can also act directly on the pituitary to regulate changes in prolactin secretion, as has already been demonstrated in mammals (reviewed by Lincoln et al., 2003; and Hazlerigg and Wagner, 2006), remains to be elucidated.
Light is the dominant environmental factor controlling melatonin biosynthesis in both the pineal gland and retina. Light at night acutely suppresses melatonin synthesis. In addition, pulses of light properly timed adjust and reset the circadian oscillator generating the melatonin rhythm (Arendt, 1995; Zawilska et al., 2000; Iuvone et al., 2005). The responsiveness of the mammalian circadian clock to these phase-shifting effects of light is known to be altered by the photoperiodic history of the animal, with phase shifts being larger after entrainment to short days (e.g., Vuillez et al., 1996; Evans et al., 2004). Studies in humans have also shown that light responses (e.g., light-induced melatonin suppression) are affected by an individual’s previous light history (Owen and Arendt, 1992; Hebert et al., 2002; Smith et al., 2004). Results of the present study, indicating that the suppressive action of light on nighttime melatonin synthesis is modified by the birds’ photoperiodic history, support the previous studies in mammals. In addition to its acute effect on melatonin synthesis, the photoperiod may modulate other light responses, including induction of early response genes and clock genes (e.g., Meddle and Follet, 1997; Sumová et al., 2004).
In conclusion, photoperiod-induced changes in melatonin synthesis were observed in the turkey pineal gland and retina. In addition, the light-responsiveness of the melatonin-generating system was shown to be affected by the photoperiodic history. It is suggested that these photoperiod-dependent changes in the melatonin signal may play an important role in modulating the immune function and reproductive status of the turkey.
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ACKNOWLEDGMENTS |
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Received for publication February 1, 2007. Accepted for publication March 7, 2007.
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