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Pulsatile growth hormone secretion, circulating insulin-like growth factor-1 concentration and cellular density of somatotrophs differ between Wagyu and Holstein steers

Published online by Cambridge University Press:  18 August 2016

M. Matsuzaki ,
T. Sato ,
S. Morita ,
N. Shiba ,
E. Tsuneishi ,
S. Hara ,
K. Ozutsumi  and
T. Yamaguchi
M. Matsuzaki*
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Center for Kyushu Okinawa Region, Kumamoto 861-1192, Japan
T. Sato
Affiliation:
Department of Animal Production Science, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan
S. Morita
Affiliation:
Animal Husbandry Institute, Kumamoto Agricultural Research Centre, Kumamoto 861-1113, Japan
N. Shiba
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Center for Kyushu Okinawa Region, Kumamoto 861-1192, Japan
E. Tsuneishi
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Center for Kyushu Okinawa Region, Kumamoto 861-1192, Japan
S. Hara
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Center for Kyushu Okinawa Region, Kumamoto 861-1192, Japan
K. Ozutsumi
Affiliation:
Department of Animal and Grassland Research, National Agricultural Research Center for Kyushu Okinawa Region, Kumamoto 861-1192, Japan
T. Yamaguchi
Affiliation:
Department of Animal Production Science, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan
*
†Email :[email protected]
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Abstract

Japanese Black cattle (Wagyu), deposit much higher amounts of intramuscular fat, known as marbling, than other breeds of cattle. To determine whether this unique fat deposition is attributable to the somatotropic axis, we compared pulsatile growth hormone (GH) secretion, plasma levels of insulin-like growth factor-1 (IGF-1) and cellular density of somatotrophs (GH-expressing cells) in the anterior pituitary glands of Japanese Black and Holstein steers. Blood samples were withdrawn every 15 min for 6 h from 14 Japanese Black and 12 Holstein steers at about 17 months of age, and GH and IGF-1 concentrations were determined. The distribution and proportion of GH-expressing cells were analysed by immunohistochemistry combined with point-count morphometry in pituitaries from six steers from each breed aged about 18 to 21 months. Overall mean and baseline plasma GH concentrations were lower (P < 0·001) in Japanese Black than Holstein steers. In addition, Japanese Black had smaller (P < 0·05) amplitudes of GH secretory pulses than Holstein steers, whereas the GH pulse frequency did not differ between the breeds. Japanese Black steers also had lower (P < 0·001) plasma levels of IGF-1 than Holstein steers. The marbling score of Japanese Black steers was higher (P < 0·001) than that of Holsteins at the same carcass weight. The proportion of GH-expressing cells was smaller (P < 0·05) in Japanese Black than Holstein steers at the hind dorsal and hind ventral regions of the adenohypophysis. Thus, in Japanese Black and Holstein steers, the breed difference in the relative density of GH-expressing cells corresponded to that in profiles of pulsatile GH secretion. These results suggest that the features of the somatotropic axis intrinsically differ between Japanese Black and Holstein cattle and that these features may be partly responsible for the genetic ability of the former to deposit greater amounts of marbling fat and for the smaller frame of Wagyu cattle.

Keywords

cattle breedsinsulin-like growth factor -1somatotropin.
Type
Growth, development and meat science
Information
Animal Science , Volume 73 , Issue 3 , December 2001 , pp. 425 - 432
Copyright
Copyright © British Society of Animal Science 2001

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References

Agriculture, Forestry and Fisheries Research Council Secretariat. 1995. Japanese feeding standard for beef cattle. Central Association of Livestock Industry, Tokyo, Japan.Google Scholar
Bick, T., Hochberg, Z., Amit, T., Isaksson, O. G. P. and Jansson, J. O. 1992. Roles of pulsatility and continuity of growth hormone (GH) administration in the regulation of hepatic GH-receptors, and circulating GH-binding protein and insulin-like growth factor-I. Endocrinology 131: 423–429.CrossRefGoogle ScholarPubMed
Breier, B. H., Gallaher, B. W. and Gluckman, P. D. 1991. Radioimmunoassay for insulin-like growth factor-I: solutions to some potential problems and pitfalls. Journal of Endocrinology 128: 347–357.CrossRefGoogle ScholarPubMed
Clark, R. G., Jansson, J. O., Isaksson, O. and Robinson, I. C. A. F. 1985. Intravenous growth hormone: growth responses to patterned infusions in hypophysectomized rats. Journal of Endocrinology 104: 53–61.Google Scholar
Gatford, K. L., Fletcher, T. P., Clarke, I. J., Owens, P. C., Quinn, K. J., Walton, P. E., Grant, P. A., Hosking, B. J., Egan, A. R. and Ponnampalam, E. N. 1996. Sexual dimorphism of circulating somatotropin, insulin-like growth factor I and II, insulin-like growth factor binding proteins, and insulin: relationships to growth rate and carcass characteristics in growing lambs. Journal of Animal Science 74: 1314–1325.CrossRefGoogle ScholarPubMed
Gatford, K. L., Fletcher, T. P., Rao, A., Egan, A. R., Hosking, B. J. and Clarke, I. J. 1997. GH, GH-releasing factor and somatostatin in the growing lamb: sex differences and mechanisms for sex differences. Journal of Endocrinology 152: 19–27.CrossRefGoogle ScholarPubMed
Gluckman, P. D., Breier, B. H. and Davis, S. R. 1987. Physiology of the somatotropic axis with particular reference to the ruminant. Journal of Dairy Science 70: 442–466.Google Scholar
Grigsby, M. E. and Trenkle, A. 1986. Plasma growth hormone, insulin, glucocorticoids and thyroid hormones in large, medium and small breeds of steers with and without an estradiol implant. Domestic Animal Endocrinology 3: 261–267.Google Scholar
Hannon, K., Gronowski, A. and Trenkle, A. 1991. Relationship of liver and skeletal muscle IGF-1 mRNA to plasma GH profile, production of IGF-1 by liver, plasma IGF-I concentrations, and growth rates of cattle. Proceedings of the Society for Experimental Biology and Medicine 196: 155–163.CrossRefGoogle ScholarPubMed
Isgaard, J., Carlsson, L., Isaksson, O. G. P. and Jansson, J. O. 1988. Pulsatile intravenous growth hormone (GH) infusion to hypophysectomized rats increases insulin-like growth factor I messenger ribonucleic acid in skeletal tissues more effectively than continuous GH infusion. Endocrinology 123: 2605–2610.CrossRefGoogle ScholarPubMed
Japan Meat Grading Association. 1989. New beef carcass grading standards. Japan Meat Grading Association, Tokyo, Japan.Google Scholar
Kineman, R. D., Faught, W. J. and Frawley, L. S. 1990. Bovine pituitary cells exhibit a unique form of somatotrope secretory heterogeneity. Endocrinology 127: 2229–2235.Google Scholar
Kineman, R. D., Faught, W. J. and Frawley, L. S. 1991a. Mammosomatotropes are abundant in bovine pituitaries: influence of gonadal status. Endocrinology 128: 2229–2233.Google Scholar
Kineman, R. D., Faught, W. J. and Frawley, L. S. 1992. The ontogenic and functional relationships between growth hormone- and prolactin-releasing cells during the development of the bovine pituitary. Journal of Endocrinology 134: 91–96.Google Scholar
Kineman, R. D., Henricks, D. M., Faught, W. J. and Frawley, L. S. 1991b. Fluctuations in the proportions of growth hormone- and prolactin-secreting cells during the bovine estrus cycle. Endocrinology 129: 1221–1225.Google Scholar
Lunt, D. K., Riley, R. R. and Smith, S. B. 1993. Growth and carcass characteristics of Angus and American Wagyu steers. Meat Science 34: 327–334.Google Scholar
Matsuzaki, M., Takizawa, S. and Ogawa, M. 1997. Plasma insulin, metabolite concentrations, and carcass characteristics of Japanese Black, Japanese Brown, and Holstein steers. Journal of Animal Science 75: 3287–3293.Google Scholar
May, S. G., Savell, J. W., Lunt, D. K., Wilson, J. J., Laurenz, J. C. and Smith, S. B. 1994. Evidence for preadipocyte proliferation during culture of subcutaneous and intramuscular adipose tissues from Angus and Wagyu crossbred steers. Journal of Animal Science 72: 3110–3117.CrossRefGoogle ScholarPubMed
Mears, G. J. and Kozub, G. C. 1995. Effect of selection for feedlot gain, breed and age on growth hormone and growth hormone kinetics in bull calves. Canadian Journal of Animal Science 75: 63–69.Google Scholar
Merriam, G. R. and Wachter, K. W. 1982. Algorithms for the study of episodic hormone secretion. American Journal of Physiology 243: E310-E318.Google Scholar
Miyachi, Y., Vaitukaitis, J. L., Nieschlage, E. and Lipsett, M. P. 1972. Enzymatic radioiodination of gonadotropins. Journal of Clinical Endocrinology and Metabolism 34: 23–28.Google Scholar
Ohlson, D. L., Davis, S. L., Ferrell, C. L. and Jenkins, T. G. 1981. Plasma growth hormone, prolactin and thyrotropin secretory patterns in Hereford and Simmental calves. Journal of Animal Science 53: 371–375.Google Scholar
Ohlson, D. L., Koch, R. M., Klindt, J. and Davis, S. L. 1987. Relationship of growth hormone, prolactin and thyrotropin secretion to individual and progeny performance of Hereford bulls. Journal of Animal Science 65: 63–67.CrossRefGoogle ScholarPubMed
Ozutsumi, K., Ikeda, T., Ando, S., Nakai, Y., Yoshitake, M., Ozawa, S., Koishikawa, T. and Chikuni, K. 1984. Body composition and muscle distribution of Japanese Black, Japanese Brown and Holstein cows. Japanese Journal of Zootechnical Science 55: 821–825.Google Scholar
Sato, T., Yamaguchi, T., Matsuzaki, M., Satoh, T. and Suzuki, A. 1999a. Mammosomatotrophs develop within mammotroph clusters in bovine adenohypophysis. Tissue and Cell 31: 499–504.CrossRefGoogle ScholarPubMed
Sato, T., Yamaguchi, T., Matsuzaki, M. and Suzuki, A. 1999b. Somatotrophs and mammotrophs in adenohypophysis of Japanese Black steers: an immunohistochemical and morphological study. Animal Science Journal 70: 329–335.Google Scholar
Satoh, H., Chiba, K., Takeda, M. and Hagino, A. 1998. Comparison of plasma metabolic hormone concentrations in Japanese Black and Holstein cattle. Animal Science and Technology 69: 483–488.Google Scholar
Statistical Analysis Systems Institute. 1988. SAS/STAT user’s guide (release 6·03). SAS Institute Inc., Cary, NC.Google Scholar
Suttie, J. M., Veenvliet, B. A., Littlejohn, R. P., Gluckman, P. D., Corson, I. D. and Fennessy, P. F. 1993. Growth hormone pulsatility in ram lambs of genotypes selected for fatness or leanness. Animal Production 57: 119–125.Google Scholar
Togashi, K., Asakura, Y., Kimura, H., Hiwaki, K., Yokouchi, K., Nishikawa, K., Nunohira, A. and Wada, J. 1984. Effects of breeds, finish period and feeding rate of concentrates on finish of steers raised on range or pasture. Japanese Journal of Zootechnical Science 55: 947–951.Google Scholar
Trenkle, A. and Topel, D. G. 1978. Relationships of some endocrine measurements to growth and carcass composition of cattle. Journal of Animal Science 46: 1604–1609.Google Scholar
Zembayashi, M., Nabeta, H. and Mototsuji, T. 1988. Effects of breeds and nutritional planes on intramuscular lipid deposition of fattening steers. Japanese Journal of Zootechnical Science 59: 39–48.Google Scholar