Profiles of growth hormone and insulin secretion, and glucose response to insulin in growing Japanese Black heifers (beef type): comparison with Holstein heifers (dairy type)

Comparative Biochemistry and Physiology Part C 130 Ž2001. 259᎐270

Profiles of growth hormone and insulin secretion, and glucose response to insulin in growing Japanese Black heifers ž beef type/ : comparison with Holstein heifers ž dairy type/ Hiroyuki Shingua,U , Koichi Hodateb, Shiro Kushibiki a , Yasuko Uedaa , Akira Watanabe a , Mitsuru Shinodaa , Mitsuto Matsumoto b a

Department of Animal Production and Grasslands Farming, National Agricultural Research Center for Tohoku Region, Morioka, Iwate, 020-0198, Japan b Department of Animal Physiology and Nutrition, National Institute of Li¨ estock and Grassland Science, P.O. Box 5, Tsukuba, Ibaraki, 305-0901, Japan Received 6 December 2000; received in revised form 15 July 2001; accepted 19 July 2001

Abstract Nine Japanese Black and 10 Holstein heifers ranging from 1 week Žwk. to 18 months Žmo. old received a single bolus intravenous injection of GH-releasing factor ŽGRF, 0.25-␮grkg BW., glucose Ž112.5-mgrkg BW. or insulin Ž0.2-Urkg BW. at various stages through 18 mo of age. The GH secretory response to exogenous GRF in Japanese Black heifers was lower than that in Holstein heifers at all stages of growth. While insulin secretory function was not very different in both breeds from 1 to 12 mo of age, the insulin response was much higher in Japanese Black heifers than in Holstein heifers after sexual maturation. The degree of decrease in plasma glucose following insulin injection was similar in both breeds at each stage of growth. It is concluded that compared with Holstein heifers, Japanese Black heifers have lower GH and higher insulin secretory functions, and that the two breeds have similar glucose response to insulin. 䊚 2001 Elsevier Science Inc. All rights reserved. Keywords: Age; Breed; Comparison; Glucose; Growth hormone; Heifer; Holstein; Insulin; Japanese Black

U

Corresponding author. Tel.: q81-19-643-3546; fax: q81-19-643-3547. E-mail address: [email protected] ŽH. Shingu..

1532-0456r01r$ - see front matter 䊚 2001 Elsevier Science Inc. All rights reserved. PII: S 1 5 3 2 - 0 4 5 6 Ž 0 1 . 0 0 2 4 9 - 6

260

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

1. Introduction The secretion of growth hormone ŽGH. from the anterior pituitary gland is regulated chiefly by growth hormone-releasing factor ŽGRF. and somatostatin ŽSRIF., which are released from the hypothalamus. GH plays essential roles in postnatal somatic growth and development of animals by promoting protein synthesis ŽSpencer, 1985. and by affecting glucose metabolism Žreviewed by Bauman and McCutcheon, 1986.. Insulin is essential for the regulation of glucose and lipid metabolism. Insulin also affects growth through its promotion of the uptake of nutrients into body tissues ŽMartin et al., 1984.. Japanese Black cattle are bred and reared as the representative beef cattle in Japan. Japanese Black cattle have a higher rate of deposition of intramuscular fat or marbling ŽLunt et al., 1993; Mir et al., 1997., and produce high quality meat with good marbling. In Japan, Japanese Black cattle therefore play an important role in production of high quality beef as compared to purebred Holstein cattle and hybrids of Holstein and Japanese Black cattle. However, Japanese Black heifers have some disadvantages, such as lower growth rate during the growth period, and smaller body weight ŽBW. and frame at maturity ŽJapanese Feeding Standard, 1995., as compared with Holstein heifers. It is possible that secretion of GH and insulin are essential for growth and development, and contribute to the characteristic growth patterns and meat properties in the respective breeds. From the 1980s onwards, a series of findings have been reported concerning the differences in GH andror insulin profiles between American and European beef and dairy breeds ŽOhlson et al., 1981; Gray et al., 1986; Grigsby and Trenkle, 1986.. However, there is little information on these profiles for Japanese Black heifers. Satou et al. Ž1998b. reported that Japanese Black heifers have lower basal plasma GH and higher insulin concentrations than Holstein heifers; they measured these levels at only one stage, 22 months Žmo. of age. Likewise, the profile of basal insulin level in Japanese Black steers at 300᎐600 kg BW ŽMatsuzaki et al., 1997., and the basal GH and insulin concentrations plus the respective secretory functions in Japanese Black male calves from 1 week Žwk. to 6 mo of age ŽShingu et al., 1998. have been reported. However, little information is

available about the comparison of basal plasma concentrations and secretagogue-induced secretory functions of GH and insulin between Japanese Black and dairy breed ŽHolstein. heifers at more subdivided growth stages. These hormones may affect the growth rate, body frame and weight, and the degree of marbling during the growth periods, in consideration of the specific differences between Japanese Black and Holstein heifers at maturity. The aim of the present study was to determine the profiles of GH and insulin secretory functions and glucose response to insulin by performing GRF, glucose and insulin challenge tests in Japanese Black heifers ranging from 1 wk to 18 mo of age, and to compare these with the respective profiles of Holstein heifers.

2. Materials and methods 2.1. Animals and feeding Nine Japanese Black heifers and 10 Holstein heifers born during winter in our center herd were studied until 18 mo of age. These heifers received humane care as outlined in the Guide for the Care and Use of Experimental Animals ŽNational Agricultural Research Center for Tohoku Region, Animal Care Committee. based on the Guide for the Care and Use of Agricultural Animals in Agricultural Research and Teaching ŽConsortium, 1988.. Newborn calves fed dam’s colostrum on the first day were housed in individual pens until 6 mo of age and thereafter, in a stanchion barn with free access to water. The calves were fed whole milk w3᎐4 kgrday Žd.x until the weaning day Ž6 wk after birth.. After 2 wk of age, the calves’ diet was gradually supplemented with commercial concentrate ŽTDN 70.0%, DCP 15.5%. and finally, they were consuming 1 kgrd of the concentrate at weaning. After weaning, the animals were given 2 kgrd of the concentrate with continuously available timothy-grass hay and trace-mineralized salt. Starting at 4 mo of age, the animals were given timothy-grass hay, alfalfa hay cubes, corn silage and the concentrate at a level that met the nutrient requirements for the Japanese Feeding Standard Ž1995.. The level of feeding was adjusted according to the heifers’ BW. All heifers were non-pregnant through the experimental period regardless of breed. The ani-

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

mals were fed twice daily at 08.30 and 16.00 h. On the experimental days, the animals fasted from 10.30 to 14.00 h Žfor the GRF or glucose challenge test. or to 16.00 h Žfor the insulin challenge test.. A catheter was inserted into one of the external jugular veins at least 1 h before each injection. Afterwards, the animals were allowed to calm down and received a GRF, glucose or insulin injection at 12.00 h. 2.2. Experimental procedures The following test agents were administered: bovine GRF ŽGRF, 0.25-␮grkg BW.; glucose Ž112.5-mgrkg BW, Otsuka Pharmaceutical Co., Tokyo, Japan.; and bovine insulin Ž0.2-Urkg BW, Wako Pure Chemical Industries Ltd, Osaka, Japan.. Powdered GRF or insulin from the same lot was used for each challenge test. The GRF or insulin solution injected into the experimental animals was made by dissolving the powdered chemical in sterilized Saline. The solution was stored at y30⬚C and was used within 1 mo after preparation. To examine the GH or insulin secretory function, GRF or glucose challenge tests were performed by a single bolus intravenous injection of GRF or glucose through the indwelling catheter at 1 wk or 10 d of age, respectively. In addition, both challenge tests were performed at 1, 3, 6, 12 and 18 mo of age. Blood samples Ž3᎐4 ml. were collected into heparinized tubes via the catheter at y30, y15, 0 Žjust before injection., 5, 10, 15, 20, 30, 45, 60, 90 and 120 min after each injection. The response of glucose to insulin was investigated by a single bolus intravenous injection of insulin at 2 wk, and 1, 3, 6, 12 and 18 mo of age. In the insulin challenge test, blood samples were also obtained at 75, 105, 150, 180, 210 and 240 min after the insulin injection, in addition to the above-mentioned sampling times Žin the GRF or glucose challenge test.. At and after 1 mo of age, the intervals between any of the challenge tests were more than 3 days. All blood samples were immediately chilled on ice. The plasma obtained after centrifugation at 1600 = g at 4⬚C for 25 min was stored at y30⬚C until assayed for GH, insulin and glucose concentrations. 2.3. Analytical methods The plasma GH concentrations were de-

261

termined by radioimmunoassay ŽRIA. as described by Johke Ž1978.. The plasma insulin concentrations were determined using a commercially available RIA kit ŽInsulin Eiken RIA kit; Eiken Chemical Co., Ltd., Tokyo, Japan. that is suitable for the measurement of bovine insulin ŽItoh et al., 1998a.. The intra- and inter-assay coefficients of variation for the GH assay were 7 and 11%, respectively. Likewise, those for the insulin assay were 2.6 and 9.3%, respectively. Plasma concentrations of glucose were determined with a commercially available colorimetric kit wGlucose 2-HA Test Wako ŽWako Pure Chemical Industries Ltd., Osaka, Japan.x using a Hitachi 7070 auto-analyzer ŽHitachi Ltd., Tokyo, Japan.. 2.4. Calculations

As an index of the amount of GH or insulin released in response to the GRF or glucose injection, the area under the GH or insulin response curve ŽAUC. during 120 min following the GRF or glucose challenge was calculated for each animal. Moreover, as an index of the amount of glucose utilized by tissues following the insulin challenge, we subtracted the area under the glucose response curve during 240 min after the insulin injection from the area under the basal glucose level, and designated the differences as the ‘decreased AUC’ ŽdAUC.. The basal plasma levels of GH, insulin and glucose were designated as the average concentrations at the pre-injection times Žy30, y15 and 0 min.. Table 1 Daily gain Žkgrday. of Japanese Black ŽB. and Holstein ŽD. heifers through different periods of growtha,b Period

Breed B

1 wk᎐1 mo 1 mo᎐6 mo 6᎐12 mo 12᎐18 mo

D †

0.44" 0.03 0.66" 0.03U 0.63" 0.03† 0.60" 0.03U

0.62" 0.09 0.78" 0.04 0.74" 0.04 0.71" 0.04

a Data represent the mean " S.E. in B Ž n s 9. and D Ž n s 10. heifers. b Dagger symbols and asterisks indicate the significance of the differences from D heifers during each period: †P - 0.1; and U P - 0.05.

262

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

Table 2 Basal plasma GH and insulin concentrations of Japanese Black ŽB. and Holstein ŽD. heifers at various ages a,b Age

Insulin Ž␮Urml.

GH Žngrml. Breed

1 wk Ž10 days.c 1 mo 6 mo 12 mo 18 mo

Breed

B

D

B

D

5.25" 0.82a,† 2.87" 0.43b UU 2.10" 0.42b, U 0.82" 0.13c, 0.82" 0.10c,†

9.27" 2.14a 3.71" 0.85b 4.96" 0.78a,b 11.21" 4.20a,b 1.40" 0.28c

12.60" 1.77a,† 17.20" 3.01a 10.71" 0.65a U 13.94" 1.51a, b,UU 29.17" 4.67

9.15" 1.40a 16.82" 3.36b 12.42" 1.76a,b 9.85" 0.92a,b 12.75" 1.13a,b

a

Data represent the mean " S.E. in B Ž n s 9. and D Ž n s 10. heifers. Asterisks indicate the significance of the differences from D heifers at each stage: †P- 0.1; U P- 0.05; and within a column without a common superscript differ significantly Ž P- 0.05.. c Data at 1 wk and 10 d of age represent the basal levels of GH and insulin, respectively. b

2.5. Statistics Analysis was performed using statistical soft-

UU

P - 0.01. Values

ware for Macintosh ŽStatView version 5.0, Abicus, CA, USA.. All data were expressed as the mean " S.E. and subjected to two-way repeated-mea-

Fig. 1. Changes in plasma GH concentration in response to exogenous GRF Ž0.25-␮grkg BW. at various stages of growth in Japanese Black ŽB, 䢇. and Holstein ŽD, `. heifers. The arrows indicate the time of GRF injection. Asterisks indicate significant differences: U P- 0.05; UU P- 0.01; and UUU P- 0.001 compared with the corresponding values for D heifers.

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

263

Fig. 2. Comparison of GH AUC after the injection of exogenous GRF Ž0.25-␮grkg BW. at various stages of growth in Japanese Black ŽB, closed columns. and Holstein ŽD, open columns. heifers. Asterisks indicate significant differences: U P- 0.05; UU P - 0.01; and UUU P- 0.001 compared with the corresponding values for D heifers. Within a given breed, different letters indicate values, which differ with P - 0.05.

sures analysis of variance ŽANOVA.. The significance of differences in daily gain ŽDG. was determined using Fisher’s PLSD post-hoc test. When comparing the plasma concentrations of GH, insulin or glucose between the breeds, if the effect of breed or breed = time was found to be significant Ž P- 0.05., the significance of differences among means were determined using Fisher’s PLSD post-hoc test. Likewise, when comparing the AUC values, if a significant effect of breed or breed = stage was found Ž P- 0.05., the significance of differences among means of the AUC were estimated by Fisher’s PLSD post-hoc test.

3. Results 3.1. Body weight and daily gain Newborn Japanese Black calves weighed less Ž P- 0.001. than newborn Holstein calves Ž27 " 1 kg vs. 44 " 1 kg.. Japanese Black heifers tended to have lower Ž P- 0.1. DG than Holstein heifers during all periods examined between 1 wk and 18 mo of age ŽTable 1., although these heifers consumed almost of the feed offered, regardless of the breed.

3.2. GRF challenge test Japanese Black heifers tended to have lower Ž P- 0.1. basal plasma GH levels than Holstein heifers at all stages of growth except at 1 and 3 mo of age ŽTable 2.. Moreover, Japanese Black heifers showed a linear decrease in basal GH concentrations with advancing age, whereas Holstein heifers showed a marked decrease at 18 mo of age. After the GRF challenge, Japanese Black heifers had lower plasma GH concentrations than Holstein heifers at all stages of growth ŽFig. 1.. The maximum value of the GH concentration after GRF injection tended to decrease with progressing age in both breeds, although Holstein heifers had a lower value at 1 or 3 mo of age than at the next stage of growth, respectively. Japanese Black heifers had significantly lower GH AUCs than Holstein heifers at all stages of growth except at 1 mo of age ŽFig. 2.. In addition, the GH AUCs in both breeds tended to decrease between 12 and 18 mo of age. 3.3. Glucose challenge test After glucose injection, few differences between the breeds were found in the change of plasma

264

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

Fig. 3. Changes in plasma glucose concentration in response to glucose Ž112.5-mgrkg BW. at various stages of growth in Japanese Black ŽB, 䢇. and Holstein ŽD, `. heifers. The arrows indicate the time of glucose injection. Asterisks indicate significant differences: U P- 0.05; and UU P- 0.01 compared with the corresponding values for D heifers.

glucose concentration at any stage except for the suckling period ŽFig. 3.. Just after the glucose injection, similar maximum values of plasma glucose were observed in the two breeds at each stage of growth. Japanese Black heifers had significantly higher basal plasma insulin concentrations than Holstein heifers at and after 12 mo of age, and showed an increase of the basal insulin concentration at 18 mo of age, whereas Holstein heifers had similar basal insulin levels at all stages of growth ŽTable 2.. Changes of the plasma insulin concentration in response to injected glucose are depicted in Fig. 4. The maximum levels of plasma insulin were observed within 10 min after the glucose injection regardless of the breed or the stage of growth. Japanese Black heifers had significantly higher

maximum insulin levels than Holstein heifers during the suckling period and at 18 mo of age. Similarly, after the glucose challenge, Japanese Black heifers had greater Ž P- 0.01. insulin AUCs than Holstein heifers at the stages of 10 d and 18 mo of age ŽFig. 5.. In addition, the former showed a marked increase of the insulin AUC at 18 mo of age, whilst the latter had similar values at and after 1 mo of age. 3.4. Insulin challenge test There were no differences between the two breeds in the changes of plasma glucose concentration except at 3 and 6 mo of age, or in the glucose dAUC at any stage of growth, following insulin injection ŽFigs. 6 and 7.. In both breeds, the time required to reach the minimum values of

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

265

Fig. 4. Changes in plasma insulin concentration in response to glucose Ž112.5-mgrkg BW. at various stages of growth in Japanese Black ŽB, 䢇. and Holstein ŽD, `. heifers. The arrows indicate the time of glucose injection. Asterisks indicate significant differences: U P- 0.05; UU P- 0.01; and UUU P- 0.001 compared with the corresponding values for D heifers.

plasma glucose after insulin injection tended to increase with increasing age. Moreover, both breeds showed a decrease in dAUCs with increasing age.

4. Discussion In the present study, we clarified the GRF-induced GH and glucose-induced insulin secretory functions, and the glucose response to insulin during the growth period in heifers of a Japanese native breed, Japanese Black. The breed has long been bred for production of meat preferred by Japanese consumers, and extensively reared as the chief beef cattle in Japan. In terms of physiological profiles, Japanese Black cattle have various unique aspects of somatic growth and devel-

opment before maturity, and meat traits at maturity: smaller body frame, BW, and DG ŽJapanese Feeding Standard, 1995.; higher deposition rate of intramuscular fat or marbling ŽLunt et al., 1993; Mir et al., 1997.; greater average muscle:bone ratio ŽZembayashi, 1987.; and higher fat percentage in the carcass ŽOzutsumi et al., 1984., compared with the respective profiles of Holstein cattle. Japanese Black heifers had lower basal GH level and GH secretory function than the respective values for Holstein heifers at all stages examined ŽTable 2, Figs. 1 and 2.. In bull calves, a larger, faster-growing breed Že.g. Simmental. had greater secretory activity of GH than a smaller, slower-growing breed Že.g. Hereford; Ohlson et al., 1981.. Thus, the present findings that Japanese Black cattle Žsmaller, slower-growing breed. have

266

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

Fig. 5. Comparison of insulin AUC after the injection of glucose Ž112.5-mgrkg BW. at various stages of growth in Japanese Black ŽB, closed columns. and Holstein ŽD, open columns. heifers. Asterisks indicate significant differences: UU P - 0.01; and UUU P- 0.001 compared with the corresponding values for D heifers. Within a given breed, different letters indicate values, which differ with P- 0.05.

lower GH secretory function strongly support the results observed by Ohlson et al. Ž1981.. Also, compared with Holsteins, lower basal plasma GH concentrations in Japanese Black male calves until 6 mo of age ŽShingu et al., 1998. and heifers at 22 mo of age ŽSatou et al., 1998b. have been reported. Generally, in addition to its effects on glucose and protein metabolism, GH affects epiphyseal development and facilitates bone development of growing animals before maturity. Starting at 6 mo of age, breed-specific differences of GH secretory function tended to become more pronounced. This would mean that the growth rate of the skeletal structure is decreased earlier in Japanese Black heifers than in Holstein heifers. Moreover, this difference of GH secretion may be responsible for the status of somatotrophs in the hypophysis. In fact, it has been demonstrated that Japanese Black steers have a lower percentage of somatotrophs in the anterior pituitary gland than Holstein steers ŽMatsuzaki et al., 1998.. Japanese Black heifers showed a decrease in the response of GH release to GRF with advancing age ŽFigs. 1 and 2.. Especially, GRF injection induced little GH response in Japanese Black heifers at 18 mo of age. Although the reasons for the decline of GRF-induced GH secretion with aging remain unclear, it is possible that the num-

bers of somatotrophs andror the ability to synthesize GH, the affinity of GRF-binding sites on pituitary cells, and the secretion of GRF andror SRIF may be altered with aging. Sato et al. Ž1999. have demonstrated that the proportion of somatotrophs declines with advancing age in Japanese Black cattle. After sexual maturation, Japanese Black heifers had markedly higher basal levels of plasma insulin than Holstein heifers at 18 mo of age ŽTable 2.. Likewise, the former had significantly higher glucose-induced insulin secretory function at 18 mo of age than the latter, although not at 12 mo of age ŽFigs. 4 and 5.. Similar results have been also obtained in Japanese Black heifers at 22 mo of age ŽSatou et al., 1998a,b. and in steers ŽMatsuzaki et al., 1997.. These differences in insulin secretory function may depend on the native physiological characteristics of cattle breeds. Since Japanese Black cattle have been selected and improved to accelerate anabolic processes, such as the synthesis of muscular protein contributing to muscle development, and the synthesis and deposition of fat, the anabolic action of insulin is likely to be important in Japanese Black cattle. Holstein cattle have been selected and improved to increase catabolic processes, such as milk production. Therefore, the secretion of insulin might

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

267

Fig. 6. Changes in plasma glucose concentration in response to insulin Ž0.2-Urkg BW. at various stages of growth in Japanese Black ŽB, 䢇. and Holstein ŽD, `. heifers. The arrows indicate the time of insulin injection. Asterisks indicate significant differences: U P- 0.05; and UU P- 0.01 compared with the corresponding values for D heifers.

be higher in Japanese Black heifers than in Holstein heifers. Japanese Black heifers had higher plasma insulin level at 18 mo of age than at or before 12 mo of age, whilst Holstein heifers had very similar values at all stages. These results partially contradict those of a previous report showing that plasma insulin levels did not differ depending on age ŽIrvin and Trenkle, 1971.. However, our results are in agreement with those of other reports demonstrating that the basal insulin level in-

creases with increasing age ŽStern et al., 1970; Martin et al., 1979; Roy et al., 1983; Gray et al., 1986; Beeby et al., 1988., and that larger-framed cattle have a lower basal insulin level than smallframed cattle ŽGrigsby and Trenkle, 1986; Beeby et al., 1988.. Both breeds had similar glucose dAUCs following the insulin injection at any stage, as shown in Fig. 7. This finding suggests that the whole body in both breeds may have similar responsiveness to insulin. However, since the plasma glu-

268

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

Fig. 7. Comparison of decreased glucose AUC ŽdAUC. after the injection of insulin Ž0.2-Urkg BW. at various stages of growth in Japanese Black ŽB, closed columns. and Holstein ŽD, open columns. heifers. Within a given breed, different letters indicate values, which differ with P- 0.05.

cose concentration results from the balance between the rate of utilization and the rate of production, especially from the liver, the changes in glucose concentration following the insulin injection should be understood to reflect both utilization and production rate changes. Therefore, further investigations of glucose kinetics are needed to determine the differences of the respective rates between the breeds. In the present study, we also demonstrated that the glucose-induced insulin secretion was increased with increasing age, regardless of the breed, whilst the glucose dAUCs tended to be smaller at and after 3 mo of age. These results reflect that the response of glucose to insulin declines with the development of rumen function after the suckling period, suggesting age-related insulin resistance. Similar results have also been obtained in sheep ŽStern et al., 1970; Sano et al., 1996. and goats ŽStern et al., 1970.. These findings suggest that the differences in GH and insulin secretory functions between the breeds affect their growth rates, body frame and weights, and the degree of marbling during the growth periods. Based on the actions of GH and insulin, in Japanese Black heifers after sexual maturation, it is possible that lower GH secretion results in a smaller body frame, lower BW and DG, lower growth rate, and greater muscle:bone

ratio, and that higher insulin secretion contributes to the development of higher marbling compared with Holstein heifers. However, it remains to be clarified that the changes in other hormones and metabolites Žex. basal plasma IGF1 and NEFA. with advancing age are investigated, since these factors may partially contribute to the specific differences between the breeds. With respect to climatic conditions during the experimental period, the ambient temperature in Morioka city, located in the northeastern part of Japan, seldom exceeds 30⬚C even in summer, and its average is 18.9⬚C in summer, 0.1⬚C in winter. Seasonal changes of glucose metabolism and insulin sensitivity have been reported ŽDenbow et al., 1986.. However, the basal plasma GH levels and the GH responses to secretagogues are not affected significantly by season or ambient temperature in heifers ŽTucker and Wettemann, 1976; Johke, 1978; Gluckman et al., 1987.. Moreover, glucose-induced insulin and insulin-induced glucose responses in heifers were not affected by cold Ž0⬚C. or heat Ž30⬚C. exposure ŽItoh et al., 1997, 1998b.. Based on both the results of these reports and the climatic conditions in the present locality, the hormone secretory functions were investigated without considering the seasonal factor in the present study. From the results obtained in the present study,

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

it is concluded that Japanese Black heifers have lower GH secretory function, and, especially after sexual maturation, higher insulin secretory function than Holstein heifers. In addition, it is possible that the two breeds may have similar responsiveness of tissues to insulin after the suckling period under the present experiment condition.

Acknowledgements The authors thank Dr Shinichi Ohashi for providing bovine GRF. We are also deeply grateful to numerous colleagues at Field Management Section 2, Department of Research Planning and Co-ordination in the National Agricultural Research Center for Tohoku Region for technical assistance and animal management, and to Ms Sachiko Osaki for laboratory assistance during the present study. References Bauman, D.E., McCutcheon, S.N., 1986. The effects of growth hormone and prolactin on metabolism. In: Milligan, L.P., Grovum, W.L., Dobson, A. ŽEds.., Control of Digestion and Metabolism in Ruminants, section 23. Prentice-Hall, Englewood Cliffs, NJ, pp. 436᎐455. Beeby, J.M., Haresign, W., Swan, H., 1988. Endogenous hormone and metabolite concentrations in different breeds of beef steer on two systems of production. Anim. Prod. 47, 231᎐244. Consortium, 1988. Guide for the Care and Use of Agricultural Animals in Agricultural Research and Teaching. Consortium for Developing a Guide for the Care and Use of Agricultural Animals in Agricultural Research and Teaching, Champaign, IL, USA. Denbow, C.J., Perera, K.S., Gwazdauskas, F.C., Akers, R.M., Pearson, R.E., McGilliard, M.L., 1986. Effect of season and stage of lactation on plasma insulin and glucose following glucose injection in Holstein cattle. J. Dairy Sci. 69, 211᎐216. Gluckman, P.D., Breier, B.H., Davis, S.R., 1987. Physiology of the somatotropic axis with particular reference to the ruminant. J. Dairy Sci. 70, 442᎐466. Gray, D.G., Unruh, J.A., Dikeman, M.E., Stevenson, J.S., 1986. Implanting young bulls with zeranol from birth to four slaughter ages: III. Growth performance and endocrine aspects. J. Anim. Sci. 63, 747᎐756. Grigsby, M.E., Trenkle, A., 1986. Plasma growth hormone, insulin, glucocorticoids and thyroid hormones

269

in large, medium and small breeds of steers with and without an estradiol implant. Domest. Anim. Endocrinol. 3, 261᎐267. Irvin, R., Trenkle, A., 1971. Influences of age, breed and sex on plasma hormones in cattle. J. Anim. Sci. 32, 292᎐295. Itoh, F., Obara, Y., Fuse, H., Rose, M.T., Osaka, I., Takahashi, H., 1997. Effects of cold exposure on responses of plasma insulin, glucagon, and metabolites in heifers. J. Anim. Physiol. A. Anim. Nutr. 78, 31᎐41. Itoh, F., Obara, Y., Rose, M.T., Fuse, H., Hashimoto, H., 1998a. Insulin and glucagon secretion in lactating cows during heat exposure. J. Anim. Sci. 76, 2182᎐2189. Itoh, F., Obara, Y., Fuse, H., Rose, M.T., Osaka, I., Takahashi, H., 1998b. Effects of heat exposure on plasma insulin, glucagon and metabolites in response to nutrient injection in heifers. Comp. Biochem. Physiol. 119C, 157᎐164. Japanese Feeding Standard, 1995. Agriculture, Forestry and Fisheries Research Council Secretariat, Tokyo, Japan, Žin Japanese.. Johke, T., 1978. Effects of TRH on circulating growth hormone, prolactin and triiodothyronine levels in the bovine. Endocrinol. Jpn. 25, 19᎐26. Lunt, D.K., Reily, R.R., Smith, S.B., 1993. Growth and carcass characteristics of Angus and American Wagyu steers. Meat Sci. 34, 327᎐334. Martin, T.G., Mollett, T.A., Stewart, T.S., Erb, R.E., Malven, P.V., Veenhuizen, E.L., 1979. Comparison of four levels of protein supplementation with and without oral diethylstilbestrol on blood plasma concentrations of testosterone, growth hormone and insulin in young bulls. J. Anim. Sci. 49, 1489᎐1496. Martin, R.J., Ramsay, T.G., Harris, R.B.S., 1984. Central role of insulin in growth and development. Domest. Anim. Endocrinol. 1, 89᎐104. Matsuzaki, M., Takizawa, S., Ogawa, M., 1997. Plasma insulin, metabolite concentrations, and carcass characteristics of Japanese Black, Japanese Brown, and Holstein steers. J. Anim. Sci. 75, 3287᎐3293. Matsuzaki, M., Sato, T., Morita, S. et al., 1998. Characteristics of somatotropic axis in Wagyu. Biotechnol. Agron. Soc. Environ. 2, 26. Mir, P.S., Bailey, D.R.C., Mir, Z. et al., 1997. Effect of feeding barley-based diets on animal performance, carcass characteristics and meat quality of crossbred beef cattle with and without Wagyu genetics. Can. J. Anim. Sci. 77, 655᎐662. Ohlson, D.L., Davis, S.L., Ferrell, C.L., Jenkins, T.G., 1981. Plasma glucose hormone, prolactin and thyrotropin secretory patterns in Hereford and Simmental calves. J. Anim. Sci. 53, 371᎐375.

270

H. Shingu et al. r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 259᎐270

Ozutsumi, K., Ikeda, T., Ando, S. et al., 1984. Muscle distribution and carcass composition in Japanese Black, Japanese Brown and Holstein cows. Jpn. J. Zootech. Sci. 55, 821᎐825. Žin Japanese with English abstract .. Roy, J.H.B., Hart, I.C., Gillies, C.M., Stobo, I.J.F., Ganderton, P., Perfitt, M.W., 1983. A comparison of preruminant bull calves of the Hereford= Friesian, Aberdeen Angus = Friesian and Friesian breeds. Plasma metabolic hormones in relation to age, and the relationship of metabolic hormone concentration with dry matter intake and heart rate. Anim. Prod. 36, 237᎐251. Sano, H., Asano, K., Noguchi, Y., Yoshimura, K., Senshu, T., Terashima, Y., 1996. Insulin responsiveness, action and sensitivity in growing lambs and mature rams. Can. J. Anim. Sci. 76, 203᎐208. Sato, T., Yamaguchi, T., Matsuzaki, M., Suzuki, A., 1999. Somatotrophs and mammotrophs in adenohypophysis of Japanese Black steers: an immunohistochemical and morphological study. Anim. Sci. J. 70, 329᎐335. Satou, H., Chiba, K., Takeda, M., Hagino, A., 1998a. Hormone responses to glucose injection in Japanese Black cattle and Holstein cattle. Anim. Sci. Technol. 69, 475᎐482. Žin Japanese with English abstract ..

Satou, H., Chiba, K., Takeda, M., Hagino, A., 1998b. Comparison of plasma metabolic hormones concentrations in Japanese Black cattle and Holstein cattle. Anim. Sci. Technol. 69, 483᎐488. Žin Japanese with English abstract .. Shingu, H., Hodate, K., Kushibiki, S. et al., 1998. Comparison of secretory functions of growth hormone and insulin between Japanese Black and Holstein male calves. Tohoku J. Anim. Sci. Technol. 48, 7᎐13. Žin Japanese, with English abstract .. Spencer, G.S.G., 1985. Hormonal systems regulating growth. A review. Livest. Prod. Sci. 12, 31᎐46. Stern, J.S., Baile, C.A., Mayer, J., 1970. Growth hormone, insulin, and glucose in suckling, weanling, and mature ruminants. J. Dairy Sci. 54, 1052᎐1059. Tucker, H.A., Wettemann, R.P., 1976. Effects of ambient temperature and relative humidity on serum prolactin and growth hormone in heifers. Proc. Soc. Exp. Biol. Med. 151, 623᎐626. Zembayashi, M., 1987. Differences of growth patterns of carcass tissues and carcass composition among Japanese Black, Japanese Shorthorn and Holstein steers. Jpn. J. Zootech. Sci. 58, 301᎐308. Žin Japanese with English abstract ..