J Comp Physiol A (2008) 194:907–913 DOI 10.1007/s00359-008-0363-x

ORIGINAL PAPER

Turkey retina and pineal gland diVerentially respond to constant environment Anna Lorenc-Duda · Maigorzata Berezijska · Béatrice Bothorel · Paul Pévet · Jolanta B. Zawilska

Received: 29 May 2008 / Revised: 27 July 2008 / Accepted: 19 August 2008 / Published online: 28 August 2008 © Springer-Verlag 2008

Abstract Dynamics of rhythmic oscillations in the activity of arylalkylamine N-acetyltransferase (AA-NAT, the penultimate and key regulatory enzyme in melatonin biosynthesis) were examined in the retina and pineal gland of turkeys maintained for 7 days in the environment without daily light–dark (LD) changes, namely constant darkness (DD) or continuous light (LL). The two tissues diVerentially responded to constant environment. In the retina, a circadian AA-NAT activity rhythm disappeared after 5 days of DD, while in the pineal gland it persisted for the whole experiment. No circadian rhythm was observed in the retinas of turkeys exposed to LL, although rhythmic oscillations in both AA-NAT and melatonin content were found in the pineal glands. Both tissues required one or two cycles of the re-installed LD for the full recovery of the high-amplitude AA-NAT rhythm suppressed under constant conditions. It is suggested that the retina of turkey

A. Lorenc-Duda · M. Berezijska Department of Pharmacology, Medical University of Lodz, Lodz, Poland B. Bothorel · P. Pévet Institut des Neurosciences Cellulaires et Intégratives, Départment de Neurobiologie des Rythmes, Unité Mixte de Recherche 7168/LC2, Centre National de la Recherche ScientiWque, Strasbourg, France J. B. Zawilska (&) Department of Pharmacodynamics, Medical University of Lodz, 1 Muszynskiego Str., 90-151 Lodz, Poland e-mail: [email protected] J. B. Zawilska Institute for Medical Biology, Polish Academy of Sciences, Lodz, Poland

is less able to maintain rhythmicity in constant environment and is more sensitive to changes in the environmental lighting conditions than the pineal gland. Our results indicate that, in contrast to mammals, pineal glands of light-exposed galliformes maintain the limited capacity to rhythmically produce melatonin. Keywords Retina · Pineal gland · Melatonin · Circadian rhythm · Turkey Abbreviations AA-NAT arylalkylamine N-acetyltransferase (serotonin N-acetyltransferase) CT circadian time DD constant darkness LD light–dark cycle LL continuous light SCN suprachiasmatic nuclei ZT zeitgeber time

Introduction Several biochemical, physiological and behavioral processes follow distinct day/night oscillations. A majority of daily rhythmic changes persists when an organism is held in constant environmental conditions, demonstrating that they are driven by an endogenous circadian clock(s) (Schibler 2006). In mammals, the generation and regulation of circadian rhythmicity is performed mainly by a master clock located in suprachiasmatic nuclei (SCN) of the anterior hypothalamus (Buijs et al. 2006). In birds, circadian organization is more complex than that of mammals. It is thought that an avian homologue of the SCN together with the pineal gland and retina act integrally, feedback and

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inXuence the activity of each other by humoral or/and neural mechanisms, and form functional components of the avian biological clock (Cantwell and Cassone 2006; Cassone and Menaker 1984; Gwinner and Brandstätter 2001; Oishi et al. 2001; Steele et al. 2003; Underwood et al. 2001). However, the relative roles of the pineal gland and retina in producing overt rhythmicity vary markedly among avian species. Thus, for example, in the house sparrow, pineal removal disturbs/abolishes circadian rhythms of temperature, locomotor activity and feeding (Binkley et al. 1971; Chabot and Menaker 1992; Kumar and Gwinner 2005). The eyes are the dominant circadian oscillator in the Japanese quail (Steele et al. 2003), whereas in the pigeon both the pineal gland and retina act as major pacemakers (Ebihara et al. 1984). Although the avian retina and pineal gland share several common features in mechanisms involved in circadian rhythmicity, each of these structures is characterized by its own trait of control and expression of circadian rhythms (e.g., Chaurasia et al. 2005; Chong et al. 2003; Iuvone et al. 2005; Okano and Fukada 2003; Yoshimura et al. 2000). Along with this, melatonin synthesis in retina and pineal goes in parallel, but is independently regulated (Iuvone et al. 2005; Natesan et al. 2002; Underwood et al. 2001; Zawilska and Wawrocka 1993; Zawilska et al. 2003b, 2006). Despite of the rapidly increasing knowledge on the structure and functioning of the circadian system in birds, there still remains a gap in our understanding of how this system adapts to photic input from the external environment in a living organism. We have previously demonstrated that the retina and pineal gland of two closely related species of fowls, chicken (Gallus domesticus) and turkey (Meleagris gallopavo), produce melatonin in a circadian rhythm (Zawilska and Wawrocka 1993; Zawilska et al. 2006). Transfer of birds, that were adapted to a light– dark cycle (LD), into constant darkness (DD) caused a dramatic decline in the amplitude of melatonin and arylalkylamine N-acetyltransferase [AA-NAT, the penultimate and rate-limiting enzyme in melatonin biosynthesis; (Klein 2007)] activity rhythm in the pineal gland and retina of turkey (Zawilska et al. 2006), while in the chicken these changes were much less pronounced, particularly in the pineal (Zawilska and Wawrocka 1993). In the present work, we extend previous studies on circadian rhythms in the turkey pineal gland and retina (Zawilska et al. 2006) by analyzing changes in AA-NAT activity in animals maintained for 1 week under continuous illumination (LL). Furthermore, in order to reveal an adaptive plasticity of the system to changes in the environmental lighting, dynamics of a restoration of high-amplitude pineal and retinal rhythms after moving the turkeys, kept under constant conditions (DD and LL), back into the LD cycle were also examined.

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Materials and methods Animal housing Newly hatched white turkeys (M. gallopavo) of both sexes were purchased on the day of hatching. Birds were kept in temperature-controlled warmed brooders (34 § 1°C for the Wrst 3 days, and 30 § 1°C afterward) with ad libitum standard food and tap water. The animals were maintained under a 12 h light:12 h dark cycle [LD; lights on and oV at a zeitgeber time (ZT) 0 and 12, respectively] for 10–12 days prior to the study. The lighting cycle was produced by overhead cool Xuorescent lamps providing light intensity at the level of the animals’ heads of approximately 150 lux. Experimental design The experiments were carried out in strict accordance with the Polish governmental regulations concerning experiments on animals (Dz.U.05.33.289). All the experimental protocols were approved by the Local Ethical Commission for Experimentation on Animals. In experiment 1 turkeys, adapted to the LD cycle, were transferred into DD at the time of the dark-to-light transition. In experiment 2, the birds were moved into LL at the time of light-to-dark transition. Turkeys were kept under DD or LL for 7 days, and then transferred back into the LD cycle, to which they were originally adapted. In order to avoid an eVect of non-photic signals on examined rhythms, delivery of food and water was done on irregular time intervals. In both sets of experiments, groups of turkeys (5–6 animals/group) were killed at 4-h intervals over a total period of 264 h: 1 day of LD, 7 days of DD or LL, and then 3 days of re-installed LD. Retinas and pineal glands were quickly isolated, frozen on dry ice and stored in liquid nitrogen until biochemical analysis. Decapitation of the turkeys and isolation of tissues during the dark phase of the LD cycle and in DD conditions were performed under dim red light (3 lux). AA-NAT activity assay Retinas and pineal glands were sonicated in an ice-cold 0.05 M sodium phosphate buVer (pH 6.8) in a proportion: 1 mg of wet retina/10
l and 1 pineal/200
l. The homogenate was centrifuged at 10,000 £g for 5 min at 4°C, and the aliquots of the supernatant were assayed for AA-NAT activity. AA-NAT activity was determined according to our routine radioisotopic method (Nowak et al. 1989), using acetyl coenzyme A (152
M; Sigma Chemicals Co., St. Louis, MO, USA) containing 16 nCi of [acetyl-14C]coenzyme A (sp. act. 2.20 GBq/mmol; Perkin-Elmer Life Sci.,

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Fig. 1 Changes in AA-NAT activity in retinas (Wlled circles) and pineal glands (open circles) of turkeys exposed to constant darkness (DD). White bars represent the duration of the light phase, black bars

the duration of the (subjective) dark phase and gray bars the duration of the subjective light phase. Arrows point to the beginning and end of DD. Values shown are means § SEM (n = 4–6 animals/time point)

Fig. 2 Changes in AA-NAT activity in retinas (Wlled circles) and pineal glands (open circles) of turkeys exposed to continuous light (LL). Black bars represent the duration of the dark phase, white bars the

duration of the (subjective) light phase and hatched bars the duration of the subjective dark phase. Arrows point to the beginning and end of LL. Values shown are means § SEM (n = 4–6 animals/time point)

Boston, MA, USA) and tryptamine-HCl (Serva, Heidelberg, Germany) as substrates.

(GraphPad Software, San Diego, CA, USA). This program was also used for the calculation of period (
), amplitude and mesor of the AA-NAT activity rhythm. To test for statistical signiWcance of diVerences unpaired Student’s t test was used.

Melatonin assay To measure melatonin content, aliquots of pineal supernatant were diluted in an ice-cold 0.1 M Tricine buVer (pH 5.0, containing 0.9% NaCl, and 0.1% gelatine). Melatonin was measured by radioimmunoassay (Rudolf et al. 1992), using a rabbit antiserum (batch No. R19540; INRA, Nouzilly, France) at a Wnal dilution of 1:200,000 and [125I]-iodomelatonin (sp. act. 81.4 TBq/mmol; Perkin-Elmer Life Sci., Boston, MA, USA) as a tracer. Polyethylene glycol in combination with sheep antirabbit antiserum (INRA, Nouzilly, France) was used to separate the bound and free tracer. Statistical analysis Data are expressed as the means § SEM values. To test for rhythmicity, the traditional F test, which compares the (re-parameterized) cosine model with the non-rhythmic model was employed using the GraphPad Prism program

Results As reported earlier (Zawilska et al. 2006), in retinas and pineal glands of turkeys kept under the 12 h light: 12 h dark (LD) illumination cycle AA-NAT activity oscillated in a high-amplitude rhythm, with low values during the light phase and high values during the dark phase of the cycle (Figs. 1 and 2). In turkeys kept under DD AA-NAT activity in the retina oscillated in a circadian rhythm for 5 days, with lower values during the subjective light phase than during the subjective dark phase (Fig. 1). The calculated period (
) was 23.67 § 0.05 h (groups’ number n = 31). The amplitude of this circadian rhythm progressively dampened with time, from 47 to 16% of that recorded under the LD cycle

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Fig. 3 Changes in melatonin content in pineal glands of turkeys exposed to continuous light (LL). Black bars represent the duration of the dark phase, white bars the duration of the (subjective) light phase and hatched bars the duration of the subjective dark phase. Arrows point to the beginning and end of LL. Values shown are means § SEM (n = 4–6 animals/time point)

on the Wrst and Wfth day of DD, respectively. On the sixth day of DD, no circadian rhythm in AA-NAT activity was detected in the retina. When a group of turkeys kept for 1 week under DD was transferred back into the LD cycle a progressive restoration of the high-amplitude AA-NAT activity rhythm in the retina was observed. On the third day of the re-installed LD cycle, the amplitude (53 § 4 pmol/h/ mg tissue) and mesor (68 § 3 pmol/h/mg tissue) were not signiWcantly diVerent (P > 0.1) from these recorded under the LD cycle introduced prior to DD (amplitude: 62 § 6 pmol/h/mg tissue; mesor: 71 § 4 pmol/h/mg tissue). AA-NAT activity in the pineal glands of turkeys Xuctuated in a well-expressed circadian rhythm for the entire duration, 7 days, of DD, with a
of 23.84 § 0.02 h (n = 43) (Fig. 1). The enzyme activity was low in the subjective light phase and high in the subjective dark phase. Transferring the birds from LD into DD resulted, however, in a potent decline in both the amplitude and mesor of pineal AA-NAT rhythm, by 64 and 26%, respectively. During the next 6 days of DD, the amplitude and mesor values did not change very markedly. On the seventh day of DD, the peak (750 § 150 pmol/h/mg tissue; CT20) to nadir (324 § 33 pmol/h/mg tissue; CT8) ratio was 2.3. In turkeys transferred from DD back into LD, a fast and progressive restoration of the high-amplitude AA-NAT activity rhythm in the pineal gland was observed. On the second day of the re-installed LD cycle, the amplitude (806 § 82 pmol/h/mg tissue) and mesor (653 § 57 pmol/h/mg tissue) were not signiWcantly diVerent (P > 0.1) from these found in the primary LD cycle (amplitude: 755 § 78 pmol/h/mg tissue; mesor: 572 § 32 pmol/h/mg tissue). Exposure of turkeys to light potently decreased AANAT activity in the retina (Fig. 2). Although some Xuctuations in the enzyme activity were observed, especially during the Wrst 2 days of LL, a computer-assisted analysis did not conWrm the presence of a circadian rhythm. A return of turkeys kept for 1 week under LL to the environment with daily LD changes quickly re-instated a high-amplitude AA-NAT activity rhythm in the retina. On the Wrst day of

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the re-installed LD the amplitude (74 § 4 pmol/h/mg tissue) and mesor (95 § 4 pmol/h/mg tissue) were not signiWcantly diVerent (P > 0.1) from these recorded in the LD cycle introduced prior to LL (amplitude: 72 § 5 pmol/h/mg tissue; mesor: 85 § 5 pmol/h/mg tissue). In contrast to the retina, cyclic changes in AA-NAT activity were present in the pineal glands of turkeys maintained under LL (Fig. 2). Although exposure of animals to light potently decreased pineal AA-NAT activity during the subjective dark phase, and delayed the Wrst peak by 4 h, the enzyme activity oscillated in a low-amplitude circadian rhythm for 7 days, with a
of 24.33 § 0.04 h (n = 43). On the seventh day of LL, the peak (491 § 46 pmol/h/mg tissue; CT4) to nadir (332 § 43 pmol/h/mg tissue; CT16) ratio was 1.5. When the turkeys exposed to LL for 1 week were transferred back into the LD cycle, a fast recovery of the high-amplitude pineal AA-NAT activity rhythm was observed. On the second day of the re-installed LD, the amplitude (489 § 62 pmol/h/mg tissue) and mesor (491 § 44 pmol/h/mg tissue) resembled values found in the LD cycle introduced prior to LL (amplitude: 481 § 61 pmol/h/mg tissue; mesor: 507 § 43 pmol/h/mg tissue). In order to conWrm the ability of the turkey pineal gland to express rhythmic activity upon constant light exposure, melatonin content was also measured. Changes in pineal melatonin content run in parallel with AA-NAT activity (Fig. 3). On the Wrst day of LL, the melatonin peak time was delayed by 4 h relative to the LD cycle. A peakto-through melatonin ratio was 54.7 in LD, potently decreased in LL (from 10.0 to 2.6 on the Wrst and seventh day of LL, respectively), and then increased in the reinstalled LD cycle (from 34.4 to 62.6 on the Wrst and third day of LD, respectively).

Discussion We have previously demonstrated the ability of the pineal gland and retina of turkey to synthesize melatonin in a

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circadian rhythm (Zawilska et al. 2006). A potent decline in the amplitude of AA-NAT activity rhythm was visible in both tissues already on the Wrst day of DD, but its dampening markedly progressed along time of dark adaptation in the retina only. This observation let us to suggest that these two melatonin-producing tissues and the key components of the avian circadian system, could substantially diVer in their responses to constant environment. As one of the basic properties of the circadian system is its ability to sustain rhythmicity in a constant environment (Fukada 2003; Schibler 2006), in the present study we analyzed rhythmic changes in AA-NAT activity in the pineal gland and retina of turkeys that were subjected to continuous illumination, and compared them with those recorded in animals kept under DD. The present results provide additional support to the working concept stated above. In the pineal AA-NAT rhythm persisted for up to 7 days of DD. A reduction in its amplitude was attributable to a potent decrease in AA-NAT activity during the subjective dark phase, already seen on the Wrst day of DD, and small increases of nadir values in the subjective light phase of the cycle. In the retina AA-NAT activity rhythm was less stable than in the pineal gland. A damping of its amplitude progressed towards the mean enzyme activity, with relatively consistent decreases in the peak and increases in the trough values, Wnally leading to the loss of the rhythm on the sixth day of DD. A similar dampening pattern has been previously observed in a closely related representative of the Phasianidae galliformes, i.e., Gallus gallus domesticus, although in this species a compression of retinal AA-NAT rhythm was weaker and prolonged over time (Zawilska and Wawrocka 1993). A gradual decrease in the amplitude of the circadian ocular melatonin rhythm (measured by in vivo microdialysis), that resulted primarily from the reduction of peak values, was shown in pigeons (Columba livia) kept under dim red light (Adachi et al. 1995). LL shut down circadian oscillation of AA-NAT activity in the turkey retina, from the Wrst day of exposure. Despite of this loss in rhythmicity, a restoration of the high-amplitude AA-NAT rhythm after the transfer of birds into the cycling lighting conditions was fast, and was completed within one full cycle of LD. In pineal glands of the same animals AA-NAT activity and melatonin Xuctuated in a low-amplitude circadian rhythm for the entire, 1 week long, duration of LL. In the light-exposed turkeys (present results) and chickens (Doi et al. 1983; Zawilska and Wawrocka 1993), the peak time of melatonin and AA-NAT activity was signiWcantly delayed on the Wrst day of LL relatively to that seen under LD, and the period (calculated for AA-NAT) lengthened. In cell culture of chick pinealocytes, the circadian rhythm of melatonin release persisted for up to 4 days in LL, but its amplitude was strongly

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decreased, and the period was signiWcantly lengthened (Robertson and Takahashi 1988). Mechanisms that could account for the maintenance of rhythmic changes in melatonin synthesis in the turkey pineal gland in LL remain to be elucidated. One hypothetical explanation might be the presence in the pineal gland of turkey of two pools of AANAT, photolabile and photostable, as suggested by Wainwright and Wainwright (1980) for the chicken pineal gland. It was proposed that an increase in AA-NAT activity of chicken pineal glands cultured under LL, observed after a certain lag period, corresponds to photostable AA-NAT activity (Wainwright and Wainwright 1980). In addition to that, the change in the period’s length indicates that LL acts on the circadian oscillator generating melatonin rhythm in the turkey pineal gland. The maintenance of melatonin rhythm in the pineal gland of turkey and chicken under LL is in sharp contrast to the situation described in mammals where exposure to light abolishes pineal rhythmicity (reviewed by Schomerus and Korf 2005; Simonneaux and Ribelayga 2003). EVects of LL on circadian rhythmicity have, so far, been evaluated in a few vertebrate species only. Studies were mainly conducted in natural conditions, during a polar day. In birds: emperor penguin (Miché et al. 1991), Adelie penguin (Cockrem 1991), Svalbard ptarmigan (Lagopus mutus hyperboreus) (Reierth et al. 1999), and Lapland longspurs (Calcarius lapponicus) (Hau et al. 2002), a large decrease in plasma melatonin levels was observed. In Lapland longspurs plasma melatonin, although being strongly suppressed under polar day, still showed a signiWcant daily rhythm (Hau et al. 2002). It is suggested that the reduced amplitude of the melatonin rhythm may increase the sensitivity of avian circadian system for minute changes in light intensity, which, in turn, makes easier to sustain 24-h rhythms in the polar day condition (Gwinner and Brandstätter 2001). A question as to why galliformes retain the capacity to rhythmically produce melatonin in constant lighting regimen remains to be answered. When compared with the pineal gland, the retina of turkey appears less able to maintain rhythmicity and its melatonin-generating system is more sensitive to changes in the environmental lighting. Although mechanisms underlying these diVerences remain to be elucidated, several hypothetical factors might contribute to the above phenomena. Among them are: an initially markedly lower amplitude of melatonin/AA-NAT activity rhythm in the retina (present results; Zawilska et al. 2006), less eVective coupling mechanism among individual biological clocks within retinal photoreceptors, weaker dependence of pineal versus retinal rhythms on central circadian oscillator(s), and an inhibitory action of a neurotransmitter dopamine (whose retinal levels are elevated by light exposure; e.g., Zawilska et al. 2003a; reviewed by Witkovsky 2004) on AA-NAT

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and melatonin in the retina (reviewed by Iuvone et al. 2005; Witkovsky 2004). In retinas of the dark-adapted turkeys increased levels of AA-NAT activity sustained for a longer time in the subjective dark phase than at night in LD, and the enzyme activity in the subjective light phase was signiWcantly higher than day-time values found under the LD cycle. These results, together with Wndings of others (reviewed by Iuvone et al. 2005), provide evidence for the importance of the retinal melatonin as a dark-adaptive signal in the avian retinal physiology. The ability of the turkey pineal gland, which is considered as the major/sole source of circulating melatonin in this species (Siopes and Underwood 1987), to rhythmically produce the hormone in constant conditions for several days speaks in favor of an idea that in the turkey pineal melatonin encodes time of the day information for the use by diVerent tissues. Acknowledgments This work was supported by the grant no. 2 PO6D 025 29 from the Ministry of Science and Higher Education, Warsaw, Poland. The authors thank Dr. J.-P. Ravault (INRA, Nouzilly, France) for kindly providing the melatonin antibody. The technical assistance of Teresa Kwapisz is highly appreciated.

References Adachi A, Hasegawa M, Ebihara S (1995) Measurement of circadian rhythms of ocular melatonin in the pigeon by in vivo microdialysis. Neuroreport 7:286–288 Binkley S, Kluth E, Menaker M (1971) Pineal function in sparrows: circadian rhythms and body temperature. Science 174:311–314 Buijs RM, Scheer FA, Kreier F, Yi C, Bos N, Goncharuk VD, Kalsbeek A (2006) Organization of circadian functions: interaction with the body. Prog Brain Res 153:341–360 Cantwell EL, Cassone VM (2006) Chicken suprachiasmatic nuclei: II. autoradiographic and immunohistochemical analysis. J Comp Neurol 499:442–457 Cassone VM, Menaker M (1984) Is the avian circadian system a neuroendocrine loop? J Exp Zool 232:539–549 Chabot CC, Menaker M (1992) Circadian feeding and locomotor rhythms in pigeons and house sparrows. J Biol Rhythms 7:287–299 Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R, Natesan A, Zatz M, Tosini G, Liu C, Korf HW, Iuvone PM, Provencio I (2005) Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): diVerential regulation of expression in pineal and retinal cell types. J Neurochem 92:158–170 Chong NW, Chaurasia SS, Haque R, Klein DC, Iuvone PM (2003) Temporal-spatial characterization of chicken clock genes: circadian expression in retina, pineal gland, and peripheral tissues. J Neurochem 85:851–860 Cockrem JF (1991) Plasma melatonin in the Adelie penguin (Pygoscelis adeliae) under conditions daylight in Antarctica. J Pineal Res 10:2–8 Ebihara S, Uchijama K, Oshima I (1984) Circadian organization in the pigeon, Columba livia: the role of the pineal organ and the eye. J Comp Physiol 154:59–69 Doi O, Koyama E, Nakamura T, Tanabe Y (1983) Photoperiodic regulation of serotonin N-acetyltransferase activity in the pineal gland of chicken. Comp Biochem Physiol 74A:195–198

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J Comp Physiol A (2008) 194:907–913 Fukada Y (2003) Molecular oscillation behind the clockface. J Biochem 34:773–775 Gwinner E, Brandstätter R (2001) Complex bird clocks. Philos Trans R Soc Lond B Biol Sci 356:1801–1810 Hau M, Romero LM, Brawn JD, Van’t Hof TJ (2002) EVect of polar day on plasma proWles of melatonin, testosterone, and estradiol in high-Arctic Lapland Longspurs. Gen Comp Endocrinol 126:101–112 Iuvone PM, Tosini G, Pozdeyev N, Haque R, Klein DC, Chaurasia SS (2005) Circadian clocks, clock networks, arylalkylamine N-acetyltransferase, and melatonin in the retina. Prog Retin Eye Res 24:433–456 Klein DC (2007) Arylalkylamine N-acetyltransferase: “the Timezyme”. J Biol Chem 282:4233–4237 Kumar V, Gwinner E (2005) Pinealectomy shortens resynchronisation times of house sparrow (Passer domesticus) circadian rhythms. Naturwissenschaften 92:419–422 Miché F, Vivien-Roels B, Pévet P, Spehner C, Robin JP, Le Maho Y (1991) Daily pattern of melatonin secretion in an antarctic bird, the emperor penguin, Aptenodytes forsteri: seasonal variations, eVect of constant illumination and of administration of isoproterenol or propranolol. Gen Comp Endocrinol 84:249–263 Natesan A, Geetha L, Zatz M (2002) Rhythm and soul in the avian pineal. Cell Tissue Res 309:35–45 Nowak JZ, ôurawska E, Zawilska J (1989) Melatonin and its generating system in vertebrate retina: circadian rhythm, eVect of environmental light and interaction with dopamine. Neurochem Int 14:397–406 Oishi T, Yamao M, Kondo C, Haida Y, Masuda A, Tamotsu S (2001) Multiphotoreceptor and multioscillator system in avian circadian organization. Microsc Res Tech 53:43–47 Okano T, Fukada Y (2003) Chicktacking pineal clock. J Biochem 134:791–797 Reierth E, Van’t Hof TJ, Stokkan KA (1999) Seasonal and daily variations in plasma melatonin in the high-arctic Svalbard ptarmigan (Lagopus mutus hyperboreus). J Biol Rhythms 14:314–319 Robertson LM, Takahashi JS (1988) Circadian clock in cell culture: I. Oscillation of melatonin release from dissociated chick pineal cells in Xow-through microcarrier culture. J Neurosci 8:12–21 Rudolf G, Vivien-Roels B, Pévet P, Kempf E, Wioland N (1992) Dopamine and melatonin interactions in the intact chicken eye. Electrooculographic and biochemical study. Brain Res 584:64–70 Schibler U (2006) Circadian time keeping: the daily ups and downs of genes, cells, and organisms. Prog Brain Res 153:271–282 Schomerus C, Korf HW (2005) Mechanisms regulating melatonin synthesis in the mammalian pineal organ. Ann NY Acad Sci 1057:372–383 Simonneaux V, Ribelayga C (2003) Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacol Rev 55:325–395 Siopes TD, Underwood HA (1987) Pineal gland and ocular inXuences on turkey breeder hens. 1. Reproductive performance. Poult Sci 66:521–527 Steele CT, Zivkovic BD, Siopes T, Underwood H (2003) Ocular clocks are tightly coupled and act as pacemakers in the circadian system of Japanese quail. Am J Physiol Regul Integr Comp Physiol 284:R208–R218 Underwood H, Steele CT, Zivkovic B (2001) Circadian organization and the role of the pineal in birds. Microsc Res Tech 53:48–62 Yoshimura T, Suzuki Y, Makino E, Suzuki T, Kuroiwa A, Matsuda Y, Namikawa T, Ebihara S (2000) Molecular analysis of avian circadian clock genes. Mol Brain Res 78:207–215 Wainwright SD, Wainwright LK (1980) Regulation of the cycle in chick pineal serotonin N-acetyltransferase activity in vitro by light. J Neurochem 34:451–457

J Comp Physiol A (2008) 194:907–913 Witkovsky P (2004) Dopamine and retinal function. Doc Ophthalmol 108:17–40 Zawilska JB, Wawrocka M (1993) Chick retina and pineal gland diVerentially respond to constant light and darkness: in vivo studies on serotonin N-acetyltransferase (NAT) activity and melatonin content. Neurosci Lett 153:21–24 Zawilska JB, Bednarek A, Berezijska M, Nowak JZ (2003a) Rhythmic changes in metabolism of dopamine in the chick retina: the importance of light versus biological clock. J Neurochem 84:717–724

913 Zawilska JB, Berezijska M, Rosiak J, Vivien-Roels B, Skene DJ, Pévet P, Nowak JZ (2003b) Daily variation in the concentration of melatonin and 5-methoxytryptophol in the goose pineal gland, retina, and plasma. Gen Comp Endocrinol 134:296–302 Zawilska JB, Lorenc A, Berezijska M, Vivien-Roels B, Pévet P, Skene DJ (2006) Daily oscillation in melatonin synthesis in the turkey pineal gland and retina: diurnal and circadian rhythms. Chronobiol Int 23:341–350

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