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Endocrinology Vol. 148, No. 6 2788-2792
Copyright © 2007 by The Endocrine Society

Involvement of Transforming Growth Factor {alpha} in the Photoperiodic Regulation of Reproduction in Birds

Tsuyoshi Takagi1, Takashi Yamamura1, Tsubasa Anraku, Shinobu Yasuo, Nobuhiro Nakao, Miwa Watanabe, Masayuki Iigo, Shizufumi Ebihara and Takashi Yoshimura

Division of Biomodeling, Graduate School of Bioagricultural Sciences (T.T., T.Ya., T.A., S.Y., N.N., M.W., S.E., T.Yo.), Institute for Advanced Research (T.Yo.), Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan; and Department of Applied Biochemistry (M.I.), Faculty of Agriculture, Utsunomiya University, Mine-machi, Utsunomiya, Tochigi 321-8505, Japan

Address all correspondence and requests for reprints to: Takashi Yoshimura, Ph.D., Division of Biomodeling, Graduate School of Bioagricultural Sciences and Institute for Advanced Research, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan. E-mail: takashiy{at}agr.nagoya-u.ac.jp.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
The molecular mechanism underlying photoperiodism is not well understood in any organism. Long-day-induced conversion of prohormone T4 to bioactive T3 within the mediobasal hypothalamus (MBH) is critical for the photoperiodic regulation of reproduction. However, because thyroidectomy does not completely block the photoperiodic response in some species, the existence of a thyroid hormone-independent regulatory mechanism appears certain. To identify this novel mechanism, differential subtractive hybridization analysis was performed using MBH of quail kept under short-day and long-day conditions. This analysis identified a gene encoding TGF{alpha}. Expression of TGF{alpha} mRNA was induced in the median eminence by the stimulus of long days, and this induction was observed at dusk on the first long day. This rapid induction of TGF{alpha} mRNA was similar to induction of the thyroid hormone-activating enzyme gene [Dio2 (type 2 iodothyronine deiodinase)], which is the earliest event yet determined in the photoinduction process. Expression analysis of epidermal growth factor receptors revealed strong expression of erbB4 and weak expression of erbB1 and erbB2 in the median eminence. Intracerebroventricular infusion of physiological dose of TGF{alpha} induced LH secretion and testicular growth under short-day conditions. Finally, we demonstrate that T3 implantation and TGF{alpha} infusion into the MBH, either of which causes testicular growth, do not affect the expression of TGF{alpha} and Dio2, respectively. Thus, long-day-induced activation of the TGF{alpha} signaling pathway appears to mediate a thyroid hormone-independent pathway for the photoperiodic regulation of reproduction.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
PHOTOPERIODIC CONTROL OF seasonal reproduction ensures the birth of offspring in spring or summer, as needed for survival. Most organisms use annual changes in day length as a cue to adapt to seasonal changes in environment. Birds have evolved especially sophisticated photoperiodic mechanisms. Among them, the Japanese quail (Coturnix japonica) is an excellent model for studying this phenomenon (1, 2). In birds, the components required for seasonal time measurement such as a photoreceptor, a "clock" to measure day length, and neural circuitry to trigger the increased secretion of GnRH and hence of gonadotropin from the pituitary gland, are thought to be localized in the mediobasal hypothalamus (MBH). Using Japanese quail as a model organism, molecular components for these effects have recently been uncovered. Within the MBH, long day lengths induce mRNA expression for type 2 iodothyronine deiodinase (Dio2), a thyroid hormone-activating enzyme, and reduce the expression of type 3 iodothyronine deiodinase, a thyroid hormone-inactivating enzyme (1, 3). These gene changes result in increased T3 levels within the MBH under long-day conditions (1). This local activation of thyroid hormones by changing day length is, by definition, the key regulator of photoperiodism. Although there is no doubt about the involvement of thyroid hormone in photoperiodism, the existence of other regulatory mechanisms has been suggested (1). That is, although animals such as European starling, house sparrow, and sheep become photoperiodically blind after thyroidectomy, quail can still respond to photostimulation (4, 5, 6, 7, 8, 9). Exploration of this novel mechanism is indispensable for our eventual understanding of the complete molecular machinery of photoperiodism. In the present study, we found that photoperiodic regulation of the TGF{alpha} gene by differential subtractive hybridization analysis and long-day-induced TGF{alpha} signaling pathway appeared to mediate a thyroid hormone-independent pathway involved in the photoperiodic regulation of reproduction.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Animals
Male Japanese quail were obtained from a local dealer at 4 wk of age and kept under short-day conditions [8-h light, 16-h dark cycle (8L16D)] in light-tight boxes held at 24 ± 1 C. Light was supplied by fluorescent lamps delivering an intensity of 200 lux at the level of the bird’s head. All birds were maintained under these short-day conditions for 1 month before any exposure to long days of 16-h light, 8-h dark cycle (16L8D). Food and water were available ad libitum, and the quail were treated in accordance with the guidelines of Nagoya University.

Differential subtractive hybridization analysis
Differential analysis was performed as reported previously (3). MBHs were collected from quail kept under short-day (8L16D) and long-day (16L8D) conditions. Total RNA was prepared from 20 pooled MBHs using TRIzol reagent (Invitrogen, Gaithersburg, MD), and the polyadenylated RNA was purified using Oligotex-dt30 Super (Takara, Otsu, Japan). Differential analysis was performed according to the instructions of the manufacturer (PCR-Select cDNA Subtraction kit; BD Clontech, Palo Alto, CA).

In situ hybridization
Animals were killed by decapitation, and the brains were removed immediately to avoid acute changes in gene expression. In situ hybridization was performed as described previously (10). Antisense and sense 45-mer oligonucleotide probes were labeled with [33P]dATP (NEN Life Science Products, Boston, MA) using terminal deoxyribonucleotidyl transferase (Invitrogen): TGF{alpha}, 5'-gcagaactgccggtgggagtcggggcactcattgaagtgtgaccg-3'; erbB1, 5'-ctgggcacctttcctctgcaccggccagagcattgctgggcacag-3'; erbB2, 5'-cttcagctccgtctccttgaggatgcgcatctgcgcttggttggg-3'; erbB4, 5'-ggcagcagtcgctgacgtagggcccgtagcaccgtccatcacact-3'; Dio2, 5'-gatggttcagcctcaatgaatatcaagacggaaatacattctgta-3'; and aromatase (P450arom), 5'-gcagctggtatcaagtctggtaccaggctggtgtagtagttcagt-3'.

Hybridization was performed overnight at 42 C. After the glass slides were washed, they were air dried and apposed to Biomax-MR film (Eastman Kodak, Rochester, NY) for 2 wk with 14C standards (American Radiolabeled Chemicals, St. Louis, MO). Relative ODs were measured using a computed image-analyzing system (MCID Imaging Research, St. Catharines, Ontario, Canada) and were converted into the relative radioactive value (nanocuries) using 14C standards. Specific hybridization signals were obtained by subtracting background values obtained from adjacent brain areas that did not exhibit a hybridization signal.

Intracerebroventricular infusion
Intracerebroventricular (icv) infusion was performed at the age of 8 wk with an Alzet 2002 osmotic minipump (Alzet, Cupertino, CA) as described previously (1). Human recombinant TGF{alpha} (T7924; Sigma, St. Louis, MO) proven to act on avian erbB receptors was used (11, 12). The dose (100 ng/ml) of the TGF{alpha} used in the present study was within the physiological range (13, 14, 15, 16). To test the effect of TGF{alpha} on Dio2 expression, brains were collected 10 d after the beginning of infusion because this pump delivers solutions continuously for 2 wk. Testicular length was measured before the infusion and at the time of brain sampling. To test the effect of TGF{alpha} on testicular growth, testicular size was measured before and 3 wk after the beginning of infusion because of the time lag between gonadotropin secretion and gonadal development. The magnitude of testicular growth was calculated from these data. Placement and patency of the cannula were verified by injecting Evans blue dye after the experiment, as suggested by the manufacturer.

Implantation of continuous-release T3 pellet
Eight-week-old quail were deeply anesthetized with diethyl ether and then implanted with continuous-release T3 pellets (1/16-in. diameter, 1 x 103 ng/21 d; Innovative Research of America, Sarasota, FL) or a placebo in the right side of the MBH as described previously (17). After surgery, birds were kept under 8L16D, and brains were collected 20 d after implantation for TGF{alpha} expression analysis. Testicular size was measured before the surgery and at the time of brain sampling.

Castration and testosterone administration
At 6 wk of age, castration (CX) and a sham operation were conducted. At the age of 8 wk, half of the birds in each group (CX and sham) were transferred to 16L8D (long-day group). The other half was continuously kept under 8L16D (short-day group). In the middle of a light phase at 10 wk of age, brains were collected for in situ hybridization. To examine the effect of testosterone, two 2-cm SILASTIC brand capsules (external diameter of 2.41 mm, internal diameter of 1.57 mm; Dow Corning, Midland, MI) that were empty or filled with crystalline testosterone (Sigma) were sc implanted into CX quail at the age of 10 wk as in a previous report (18). Birds were kept under 8L16D, and brains were collected at 12 wk of age.

LH RIA
Plasma LH concentrations of the Japanese quail were determined by RIA using the chicken LH RIA kit [kindly supplied by Dr. John A. Proudman, United States Department of Agriculture (USDA)/Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD] as described previously (19). Labeled antigen was prepared by iodinating purified chicken LH (USDA-cLH-I-3) with [125I]Na (2200 Ci/mmol; GE Healthcare, Piscataway, NJ) by lactoperoxidase method. USDA-cLH-K-3 and USDA-AcLH-5 were used as the standard and the antibody (final concentration, x60,000), respectively. Parallelism of inhibition curves was proved between serial 2-fold dilution of the standard and the quail plasma (data not shown). Intraassay and interassay coefficients of variation were 10.6% (n = 3) and 9.6% (n = 5) at the 0.425 ng/tube level, respectively. The minimum detectable levels defined as 2 SD from the buffer control were less than 0.039 ng/tube.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Identification of a gene involved in photoperiodic regulation of reproduction
To identify a novel regulatory mechanism, differential subtractive hybridization analysis was performed using MBH of quail kept under short-day and long-day conditions. From this analysis, the photoperiodic regulation of TGF{alpha} mRNA (GenBank accession number AB258390) expression was identified in the median eminence, with high expression under long-day and low expression under short-day conditions (Student’s t test, P < 0.05) (Fig. 1Go, A and B). No signal was observed in the sense control assay (data not shown). When birds kept under short-day conditions were given a single long-day stimulus, induction of TGF{alpha} mRNA was observed at dusk on the first long day, and prolonged expression was observed for several days [one-way ANOVA, F(17,50) = 4.971, P < 0.0001; Fisher’s least significant difference (LSD) post hoc test, P < 0.05] (Fig. 1CGo).


Figure 1
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  		FIG. 1. Photoperiodic regulation of TGF{alpha} mRNA in the median eminence of Japanese quail. A, Representative autoradiograms of TGF{alpha} expression in transverse sections at the level of the median eminence. B, Quantitative results from the autoradiograms (mean ± SEM; n = 3) of TGF{alpha} expression of quail kept under short-day (SD) and long-day (LD) conditions. The high level under long days is significantly greater than under short days (*, P < 0.05). C, Result for the first day response of TGF{alpha} mRNA expression. Asterisksindicate a significant increase in TGF{alpha} expression compared with time 8 h on the first day (one-way ANOVA, F(17,50) = 4.971, P < 0.0001; Fisher’s LSD post hoc test, P < 0.05; n = 3–4).

 
Expression analysis of epidermal growth factor receptors
TGF{alpha} is a member of the epidermal growth factor (EGF) family, with which it shares the EGF receptors known as EGFR and erbB (20). Because erbB1, erbB2, and erbB4 have been identified in birds, expression of these three erbB receptors was examined in the MBH. Strong expression of erbB4 and weak expression of erbB1 and erbB2 were observed in the median eminence (Fig. 2AGo). No hybridization signal was observed in the sense control assay (data not shown). Expression of these receptors was not different between short-day and long-day conditions (P > 0.3, 0.9, and 0.8, respectively) (Fig. 2BGo).


Figure 2
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  		FIG. 2. Expression of EGF receptors in the median eminence of quail. A, Representative autoradiograms for erbB1, erbB2, and erbB4 in the median eminence under short-day (SD) and long-day (LD) conditions. B, Quantitative results from the autoradiograms (mean ± SEM; n = 5). No significant difference was observed between short-day and long-day conditions in any gene (erbB1, P > 0.3; erbB2, P > 0.9; erbB4, P > 0.8).

 
Effect of icv infusion of TGF{alpha} on LH secretion and testicular growth
To assess the functional significance of TGF{alpha} on photoperiodism, the effect of TGF{alpha} on plasma LH levels and testicular growth was examined. Under short-day conditions, icv infusion of TGF{alpha} with an osmotic minipump increased plasma LH levels and induced testicular growth compared with control birds infused with vehicle (P < 0.05) (Fig. 3Go, A and B). In addition to these, we examined the effect of combined administration of TGF{alpha} and T3 on testicular growth. Although no statistically significant difference was observed, testicular growth of combined administration tended to be larger than that of TGF{alpha} or T3 alone (Fig. 3CGo).


Figure 3
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  		FIG. 3. Intracerebroventricular infusion of TGF{alpha} mimics long-day effects on plasma LH levels and testicular growth. TGF{alpha} was infused with an Alzet osmotic minipump under short-day conditions. Plasma LH level and testicular size were measured before and 3 wk after the beginning of the infusion. Testicular length (A) and plasma LH level (B) were significantly greater in birds infused with TGF{alpha} than in birds infused with vehicle (*, P < 0.05; n = 4, 6). C, Although no statistically significant difference was observed, the testicular length of birds given TGF{alpha} and T3 in combination tended to be larger than that of birds given TGF{alpha} or T3 alone. Different characters(aand b) indicate significant differences (P < 0.05).

 
Effect of T3 on TGF{alpha} expression
To determine the interaction between thyroid hormone and the TGF{alpha} signaling pathway, the effect of T3 on TGF{alpha} expression and the effect of TGF{alpha} on Dio2 expression were examined. Consistent with our previous report, T3 administration induced testicular growth (P < 0.05) but did not affect TGF{alpha} expression in the median eminence (P > 0.8) (Fig. 4Go, A and B). Furthermore, TGF{alpha} infusion that induced testicular growth (P < 0.05) did not affect Dio2 expression (P > 0.6) (Fig. 4Go, C and D). These results suggest that the thyroid hormone and TGF{alpha} signaling pathways do not directly interact with each other.


Figure 4
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  		FIG. 4. Thyroid hormone and TGF{alpha} signaling pathways do not interact with each other. A and B, T3 pellet implantation in the MBH induced testicular growth (P < 0.05) but did not affect TGF{alpha} mRNA expression under short-day conditions (P > 0.8; n = 3). C and D, Intracerebroventricular TGF{alpha} infusion increased testicular growth (P < 0.05) but did not affect Dio2 mRNA expression under short-day conditions (P > 0.6). Note that the magnitude of testicular growth differs between T3 and TGF{alpha} administration. This is attributable to the sampling schedule, i.e. effects of TGF{alpha} and T3 were examined 10 and 20 d after infusion, respectively. See Materials and Methods. (*, P < 0.05.)

 
Effect of CX and testosterone on TGF{alpha} expression
We further examined the effect of CX and testosterone treatment on expression of TGF{alpha} mRNA (Fig. 5Go). Although expression of TGF{alpha} was higher with the long-day stimulus (one-way ANOVA, F(5,12) = 10.984, P < 0.0004; Fisher’s LSD post hoc test, P < 0.005), no significant difference was observed between sham-operated birds and castrated birds under short-day (P > 0.9) and long-day (P > 0.4) conditions (Fig. 5AGo). In addition, although testosterone implantation in castrated birds induced growth of the cloacal gland (P < 0.01) (Fig. 5BGo) and expression of the aromatase (P450arom) gene in the nucleus preopticus medialis (P < 0.01) (Fig. 5CGo), testosterone administration did not affect TGF{alpha} mRNA expression (P > 0.8).


Figure 5
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  		FIG. 5. Long-day-induced TGF{alpha} expression is not a secondary consequence of steroids from the gonads. A, Expression of TGF{alpha} mRNA was not affected by CX or testosterone administration (T) but was induced by the long-day stimulus (ANOVA, F(5,12) = 10.984, P < 0.001; Fisher’s LSD post hoc test, P < 0.005; n = 3). Different characters (a and b) indicate significant differences (P < 0.005). B and C, Area of cloacal gland and P450arom expression in the nucleus preopticus medialis were confirmed to be increased by the testosterone administration (*, P < 0.01; n = 3). Emp, Empty; LD, long-day condition; SD, short-day condition.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In the present study, we found that long days induced TGF{alpha} mRNA expression in the median eminence of Japanese quail. It is well established that, when quail kept under short-day conditions are exposed to a single long day and then returned to short days, induction in LH secretion is first detected by the end of the long day, builds up to peak approximately 3 d later, and lasts for more than 1 wk ("carryover"). This experimental model is referred to as the "first-day release model" (2, 21), and the exact timing of the changes in gene expression during the very first long day is of particular interest. Under this first-day release model, induction of TGF{alpha} mRNA was observed at dusk on the first long day, and prolonged expression was observed for several days thereafter. This temporal expression profile of TGF{alpha} mRNA was similar to that of the thyroid hormone-activating enzyme gene Dio2, which is the earliest event yet observed in the photoinduction process (3). This rapid induction of TGF{alpha} mRNA offers the potential to regulate photoinduction process. Although all known actions of TGF{alpha} are mediated by its binding to erbB1, heterodimerization between members of the erbB family is important for the biological outcome of TGF{alpha} stimulation (20). Expression of EGF receptors in the median eminence suggested that long-day-induced TGF{alpha} may act on the median eminence in an autocrine or/and paracrine manner. Intracerebroventricular infusion of TGF{alpha} increased plasma LH levels and induced testicular growth. Furthermore, although there was no statistically significant difference, combined infusion of TGF{alpha} and T3 induced larger testicular growth than the infusion of TGF{alpha} or T3 alone. Furthermore, T3 implantation and TGF{alpha} infusion into the MBH, either of which alone induces testicular growth, did not affect the expression of TGF{alpha} and Dio2 mRNA, respectively. We also demonstrated that CX and testosterone treatment do not affect TGF{alpha} expression. These results suggest that the change in TGF{alpha} expression is dependent on photoperiod but is not a secondary consequence of photoperiod-induced changes in steroid levels.

In mammals, it has been reported that TGF{alpha} is able to stimulate the release of GnRH from the median eminence (13), and it is considered to be one of the key factors in the neuroendocrine control of puberty because overexpression of TGF{alpha} accelerates the onset of puberty (22) and blockade of EGF receptors delays the onset (23, 24). TGF{alpha} acts on glial cells in an autocrine and/or paracrine manner by activating erbB receptors with the subsequent release of prostaglandin E2, which then acts on GnRH neurons to induce GnRH secretion (13, 25, 26). Recently, we demonstrated that seasonal morphological changes in the neuroglial interaction between GnRH nerve terminals and glial end feet in the quail median eminence are different under short-day and long-day conditions (27), and this morphological change was induced by the implantation of a T3 pellet into the MBH (17). It is noteworthy that TGF{alpha} has been reported to induce morphological plasticity in vitro (28), and it would be interesting to examine in future studies whether TGF{alpha} administration also causes morphological changes in the neuroglial interaction of the median eminence in vivo.

In conclusion, we have identified a thyroid hormone-independent pathway for photoperiodic regulation of reproduction. The similarity of the TGF{alpha} and Dio2 expression profiles in the first-day release model implies that these genes share some elements of transcriptional regulation. Determination of the transcriptional regulators of these genes is important to further clarify the molecular mechanisms of photoperiodic time measurement.


   Acknowledgments
 
We thank Nagoya University Radioisotope Centre for use of its facilities and Dr. John A. Proudman (United States Department of Agriculture/Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD) for providing the chicken LH RIA kit.


   Footnotes
 
First Published Online March 15, 2007

1 T.T. and T.Ya. contributed equally to this work. Back

Abbreviations: 16L8D, 16-h Light, 8-h dark cycle; 8L16D, 8-h light, 16-h dark cycle; CX, castration; Dio2, type 2 iodothyronine deiodinase; EGF, epidermal growth factor; icv, intracerebroventricular; LSD, least significant difference; MBH, mediobasal hypothalamus.

This work was supported in part by the Program for Promotion of Basic Research Activities for Innovative Biosciences (to T.Yo.).

The authors have nothing to disclose.

Received January 25, 2007.

Accepted for publication March 5, 2007.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals