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Poult Sci 2007. 86:112-117
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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION

Deficiency of Growth Hormone Receptor Does Not Affect Male Reproduction in Dwarf Chickens

J. X. Zheng, Z. Z. Liu and N. Yang1

Department of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural University, Beijing 100094, China

1 Corresponding author: nyang{at}cau.edu.cn


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sex-linked dwarf chickens caused by the mutation of the growth hormone receptor gene are characterized by normal growth hormone (GH), very low insulin-like growth factor I (IGF-I) level in the blood, and reduced growth. It has been demonstrated that the sex-linked dwarfing gene has negative effects on female reproduction. In the current study, dwarf cocks and their phenotypic normal siblings were used to investigate the effects of dwarf gene on male reproduction. Dwarf cocks grew slower than the normal cocks did, and at 20 wk of age, their BW were 36.4% smaller. However, all parameters for semen quality, including volume, sperm concentration, viability, mobility, pH, and percentage of abnormal sperms, examined at 30 wk of age showed no significant difference between normal and dwarf cocks. The fertility of dwarf cocks was 95.2%, and the normal was 92.4%. The concentrations of GH and IGF-I in serum and seminal plasma were measured with RIA and ELISA, respectively. The serum GH in the dwarf cocks was significantly higher than their normal siblings (P < 0.05), whereas the serum IGF-I in the dwarf cocks was very low. However, the concentration of seminal IGF-I in dwarf cocks was similar to that of their normal siblings, indicating that IGF-I might be produced and acted independently in testis. In conclusion, the deficiency in GH receptor did not affect the male reproduction in dwarf chickens, and the fertility of dwarf cocks could be satisfactory for production when artificial insemination was adopted.

Key Words: dwarf chicken • growth hormone receptor • semen quality • fertility • growth hormone


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Dwarf chickens, as an important genetic resource for breeding application and biological studies, are caused by the sex-linked dwarfing gene (dw; Hutt, 1959). They are characterized by low BW and long bone growth (Guillaume, 1976), with reduced levels of plasma insulin-like growth factor I (IGF-I; Huybrechts et al., 1985), despite normal or high levels of circulating growth hormone (GH; Scanes et al., 1983; Stewart et al., 1984). It has been found that dw is the only gene that reduces body size without any marked detrimental effect upon reproductive ability and livability (Guillaume, 1976). It is demonstrated that the dw gene causes deficiency in GH receptor (GHR), consequently resulting in dwarfism (Burnside et al., 1992; Agarwal et al., 1994).

Previous studies have shown that the female reproduction of dwarf chickens is affected by the dw gene. The laying rate is reduced by about 10% in medium or light-type chicken but is unchanged or improved in heavy types (Guillaume, 1976). Egg weight is reduced, and sexual maturity of dwarf hens compared with normal sisters is generally delayed by 7 to 10 d (Hutt, 1959). Although effects of GHR deficiency on female reproduction have been well understood, knowledge of the effects of the dw gene on male reproduction is limited. In mammals, the important role of GH in male reproduction has been discussed (Hull and Harvey, 2000). Sexual maturation is delayed in men with Laron syndrome (Laron, 1984), of which the clinical feature is associated with mutated GHR genes and subsequent resistance to GH. A lack of GH secretion results in a delay in testicular growth and differentiation of germinal cells in rats (Bartlett et al., 1990), and in mice, the absence of IGF-I causes the adult Leydig cells to fail to mature (Wang et al., 2003). Insulin-like growth factor I nullizygous mutants are infertile dwarfs in mice and only sustain spermatogenesis at 18% of the normal level (Baker et al., 1996). These studies suggest that IGF-I has significant effects on male reproduction. Like GHR-knockout mice and men with Laron syndrome, dwarf chicken is a heritable form of GH resistance resulting from a GHR dysfunction, exhibits reduced or undetectable circulating IGF-I levels, and appears to be a suitable experimental model to assess the effects of GH and IGF-I on male reproduction.

In chickens, GH and IGF-I mRNA are expressed in the testis, in which GH mRNA is discretely localized in primary spermatocytes (Harvey et al., 2004). Furthermore, the IGF-I mRNA expression is remarkably enhanced in testes of dwarf chickens (Tanaka et al., 1996). In the current study, the semen quality and fertility of dwarf cocks are evaluated, and the roles of GH and IGF-I in male reproductive function are explored.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Birds

A segregation population at dw gene was constructed by mating dwarf females (ZdwW) with normal males (ZDWZdw), in which 186 chicks with 4 genotypes, ZDWZdw, ZdwZdw, ZDWW, and ZdwW were produced. The ZDWZdw and ZDWW individuals showed normal body size, whereas the phenotype of ZdwZdw and ZdwW exhibited dwarfism during development. Because the dwarf chickens in the present study were caused by a large deletion including a portion of the 10th exon and the 3' untranslated region of the GHR gene, the genotype of each chicken was determined by PCR analysis using a procedure described by Agarwal et al. (1994). Blood samples were collected via wing vein for each bird at 2 wk of age, and genomic DNA was isolated by a phenol-chloroform method (Sambrook et al., 1989). Polymerase chain reaction was performed to amplify the sequences of GHR, including the deletion fragment. The 20-µL PCR system included 50 ng of DNA template, 0.20 mM dNTP, 2.5 mM MgCl2, 0.20 mM primer, and 0.5 U of Taq DNA polymerase (Dingguo Biotechnology Company, Beijing, China). The PCR protocol was 94°C for 5 min followed by 35 cycles of 94°C for 30 s, 58°C for 30 s, and 72°C for 2 min and a final extension at 72°C for 10 min. The sex of chicks was identified by PCR using the procedure suggested by Hu et al., (2003). The PCR protocol was 94°C for 5 min followed by 35 cycles of 94°C for 30 s, 55°C for 30 s, and 72°C for 30 s and a final extension at 72°C for 10 min. The ZW females were characterized by displaying 2 fragments (CHD1-W and CHD1-Z), whereas ZZ males showed only 1 fragment (CHD1-Z) clearly different from the female-specific CHD1-W fragment in size.

After genotyping, the number of chickens with genotype ZDWZdw, ZdwZdw, ZDWW, and ZdwW were 44, 49, 46, and 47, respectively. Forty phenotypic normal (ZDwZdw) and forty dwarf (ZdwZdw) males were kept for the study. Body weight at hatch at 4, 8, 16, and 20 wk and shank length at 8 wk were measured for each chicken.

All chicks were reared in a heated battery brooder for 6 wk and then transferred to wire cages. At 16 wk of age, they were placed in individual battery cages. All chickens were fed ad libitum with a standard diet for egg-type chickens and managed in a normal procedure. Birds were handled in accordance with the principles and procedures outlined by the university’s Animal Care and Use Committee.

Hormone Assays

Serum and seminal plasma of 12 dwarf and 12 normal cocks were assayed for the concentration of GH. Because the secretion of GH in chicken was pulsatile and the GH level was not constant in a day-night period (Moellers and Cogburn, 1995), we collected blood samples in the morning and within a short period (0800 to 0900 h) at 20 wk. Semen sample was collected by the abdominal massage technique at 30 wk. The serum and seminal plasma were separated by centrifugation at 800 x g for 15 min and then stored at –20°C for the assay of GH. Serum GH concentrations were determined in duplicate by RIA. The chicken GH (no. AFP-7678B) and antiserum to chicken GH (rabbit) (no. AFP-551-11-1-86) were provided by A. F. Parlow (National Hormone and Pituitary Program, Torrance, CA). Chicken GH antigen was labeled with 125I as directed in the iodination kit from Du Pont (Boston, MA). The procedure for RIA of chicken GH was as follows: all reagents were added to the RIA tubes at refrigerator temperature in the sequence a) buffer, b) standard of unknown, c) radiolabeled antigen, and d) antiserum at a final tube dilution of 1:400,000. The reagents were then incubated at room temperature for 24 h, before the addition of the second antibody, donkey-anti-rabbit IgG in a dilution of 1:10. The GH standard ranged from 0 to 100 ng/mL (0, 1.5625, 3.125, 6.25, 12.5, 25, 50, and 100). The intraassay CV for GH was 5.5%.

For the IGF-I assays, a chook IGF-I ELISA kit was used (RapidBio Lab, Calabasas, CA). Insulin-like growth factor binding proteins were removed from the serum and seminal plasma by a method described previously (Chandrashekar and Bartke, 1993), and the protocol was performed as directed by the supplier. Every sample was run in duplicate, and the mean was used for data analysis. The IGF-I standard ranged from 0 to 2,000 ng/mL (0, 31.25, 62.5, 125, 250, 500, 1,000, and 2,000 ng/mL). The intraassay CV for IGF-I was 3%.

Evaluation of the Semen Quality and Fertility

Semen samples of 12 dwarf and 12 normal cocks were collected by the abdominal massage technique at 30 wk. The tubes with semen were stored on a laboratory thermal desk at 35°C. Sperm concentration (billion/mL), viability (%), and motility (%) were analyzed by a computer-assisted sperm analyzer AKPACE-2 (Beijing Zhongke Hengye Technology Ltd., China). The definitions of sperm motion parameters for the computer assistant sperm analyzer were established by Beijing Zhongke Hengye Technology Ltd. as follows: frames acquired: 30; frame rate: 60 Hz; straightness threshold: 80.0%; medium average path velocity threshold: 25.0 mm/s; and duration of the tracking time: 0.5 s. The semen was diluted with 0.9% NaCl in a ratio of 1 to 9 and then placed in a tube and shaken for 10 min. An aliquot of the sperm suspension was placed on a microscope slide and covered with a cover slip, and at least 4 different fields were analyzed from each sample. We defined percentage of motile sperm as World Health Organization (1992) grade A sperm (rapidly progressive with a velocity >25 mm/s at 37°C) plus grade B sperm (slow and sluggish progressive with a velocity >5 mm/s but <25 mm/s). Sperm morphology was determined by referring to the World Health Organization (1992) criteria and expressed as percentage of abnormal sperm. The pH was analyzed by EcoScan 5 pH meter (Eutech Instruments Pte Ltd., Singapore), and the volume of semen was measured by semen collection cup to the minimum 10 µL.

Two groups of White Leghorn females at 30 wk of age, each with 100 individuals, were artificially inseminated with mixed semen produced by 12 dwarf and 12 normal cocks, respectively. Five hundred eggs were collected in 1 wk from each group and incubated to 10 d for fertility test by candling.

Statistical Analysis

Student’s t-test was used to compare the means of 2 groups. All data were expressed as mean ± SEM. Values were considered significant at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
BW

The BW of day-old dwarf male chicks did not differ from that of normal male chicks. Dwarf cocks grew slower than normal cocks and showed smaller BW from 4 wk of age(P < 0.05; Table 1Go). The shank at 8 wk was also shorter than that of normal cocks. At 20 wk of age, dwarf cocks were 36.4% smaller than normal cocks.


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  		Table 1. Body weights and shank length of dwarf and normal cocks1
 
GH and IGF-I Concentrations in Serum and Seminal Plasma

The levels of circulating and seminal GH were significantly higher in dwarf cocks than those in normal cocks, and the GH levels in seminal plasma for both groups were lower than those in serum (P < 0.05; Figure 1Go). On the other hand, serum IGF-I was measurable in all normal cocks, but the concentration of IGF-I was very low. Two groups, however, showed similar seminal IGF-I concentrations (Figure 2Go).


Figure 1
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  		Figure 1. Serum and seminal plasma growth hormone (GH) concentrations of dwarf and normal cocks at 20 wk; n = 12. Values are means. Vertical lines represent the SEM. a,bValues without a common letter are significantly different (P < 0.05). Data for dwarf cocks are presented in darkened bars, and data for normal cocks are presented in gray bars.

 

Figure 2
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  		Figure 2. Serum and seminal plasma insulin-like growth factor I (IGF-I) concentrations of dwarf and normal cocks at 20 wk; n = 12. Values are means. Vertical lines represent the SEM. a,bValues without a common letter are significantly different (P < 0.05). Data for dwarf cocks are presented in darkened bars, and data for normal cocks are presented in gray bars.

 
Semen Quality and Fertility

Results of semen quality testing for 12 dwarf and 12 normal cocks showed no significant difference concerning semen volume, pH, sperm concentration, viability, motility, and percentage of abnormal sperms (Table 2Go). Dwarf cocks ejaculated slightly more semen, but the concentration of sperm was relatively lower than that of normal cocks. Both types of cocks produced almost same number of spermatozoa per ejaculation. The viability for the 2 genotypes was all >90%, and motility was >85%, which were indications of good semen quality. The percentage of abnormal sperm was low for both dwarf and normal cocks. The fertility for dwarf and normal cocks was 95.2 and 92.4%, respectively, and the difference was not significant between the 2 groups.


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  		Table 2. Semen quality and fertility of dwarf and normal cocks1
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The current study showed that dwarf cocks had similar semen quality as their normal siblings. Dwarf chicken had been recognized as more efficient in feed conversion of egg production, and could be used as broiler breeders and commercial layers (Guillaume, 1976; Zhang et al., 2005). It was demonstrated in the current study that dwarf cocks could have satisfactory fertility for breeding and production. The shorter legs might cause difficulties in mating behaviors of dwarf cocks, but the fertility of dwarf cocks could be maintained at a high level when artificial insemination is adopted.

In dwarf cocks, the dysfunction of GHR did not have adverse effects on the semen quality and fertility, whereas the concentration of seminal GH was higher and IGF-I was lower than those of normal cocks. In mammals, it has been suggested that a strong link exists between GH and male reproduction. The sperm motility was impaired in GH-deficient rats and mice and restored by GH administration (Gravance et al., 1997). Growth hormone resistance (e.g., Laron syndrome) was associated with impaired fertility (Laron, 1984). Suppression of GH, however, did not affect maintenance of spermatogenesis, and it was concluded that GH did not play a role in the maintenance of spermatogenesis in adult rats but might be required for the replenishment of germ cells in experimentally induced regressed rat testes (Awoniyi et al., 1989, 1990). It appeared likely that GH affected sperm motility directly, or mediated through Sertoli cells, and might also act indirectly on the testis via the stimulation of IGF-I. Growth hormone did not play a major role in the regulation of testicular IGF-I production at puberty of the rat (Spiteri-Grech et al., 1991). Other studies with human males indicate that seminal IGF-I concentration is correlated with sperm morphology but not with sperm motility (Glander et al., 1996) or concentration (Breier et al., 1998).

The seminal IGF-I concentration in dwarf cocks was not significantly different from that of their normal siblings. It was reported that IGF-I is produced without GH action in Sertoli and Leydig cells (Tres et al., 1986; Vannelli et al., 1988) and plays a role in spermatogenesis and in the control of the endocrine function of the testis in rats (Chandrashekar et al., 2004). Although the major source of serum IGF-I is known to be the liver, where IGF-I synthesis is stimulated by binding of GH to its specific receptor (Bick et al., 1990), other researches have revealed that in addition to the liver, other tissues could synthesize IGF-I in rats (Lund et al., 1986) and chickens (Kajimoto and Rotwein, 1989; Kikuchi et al., 1991). Tanaka et al. (1996) found that in the GHR-deficient chicken, IGF-I mRNA expression in testis was increased, whereas hepatic IGF-I expression was completely abolished. In the current study, the level of seminal plasma IGF-I in dwarf chicken was similar with that of their normal sibling, although the circulating IGF-I was low. The result of IGF-I concentration was in agreement with that of IGF-I mRNA expression (Tanaka et al., 1996), suggesting that the seminal IGF-I in chicken was derived from testis, where IGF-I was synthesized independently on the GHR or GH.

Mutation of the GHR gene resulted in decreased BW of dwarf chicken compared with their normal siblings. Serum level of IGF-I was reduced dramatically by the absence of normal GHR, although dwarf chicken secreted large amounts of GH. The observation confirmed that for normal growth of chicken, physiological amounts of GH, GHR, and IGF-I were required (Vanderpooten et al., 1991). Dwarf chicken has been regarded as the best characterized animal model of GH resistance and was the first animal model proposed for Laron syndrome (Hull et al., 1993). Although there are large physiological differences between birds and mammals in terms of their discrepant GH axes, the dwarf chicken is also used to distinguish GH-dependent and GH-independent IGF-I production and growth (Tanaka et al., 1996). In this regard, the dwarf chicken could provide a unique model for assessment of GH and IGF-I action on testicular functions with respect to both endocrinology and spermatogenesis. The mechanism that is responsible for the maintenance of fertility in dwarf chicken is likely to be related to GH-independent production of IGF-I or GH action independently of IGF-I within the testis. However, factors that stimulate the expression of IGF-I in testis and the molecular basis for the tissue differences in GH responsiveness are to be explored in the future.

In the current study, the deficiency of the GHR gene in dwarf chickens led to abnormal levels of circulating IGF-I, but seminal IGF-I derived directly from testis was only slightly affected by the mutation. This mechanism may have helped the dwarf cocks maintain good semen quality and high fertility. The GHR-deficient dwarf chickens would continually be used to elucidate the mechanisms of GH and IGF-I function in avian testis.

In conclusion, the deficiency in GHR does not affect male reproduction in dwarf chickens, and the fertility of dwarf cocks can be satisfactory for production when artificial insemination is used.


   ACKNOWLEDGMENTS
 
This work is supported in part by a grant from the National Outstanding Youth Science Foundation of China (no. 30225032) and the National Basic Research Program of China (no. 2006CB102102).

Received for publication August 1, 2006. Accepted for publication September 16, 2006.


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