Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-24T05:56:01.346Z Has data issue: false hasContentIssue false

Insulin-like growth factor-I feedback regulation of growth hormone and luteinizing hormone secretion in the pig: evidence for a pituitary site of action

Published online by Cambridge University Press:  01 June 2009

C. R. Barb*
Affiliation:
USDA-ARS, Russell Research Center, PO Box 5677, Athens, GA 30604, USA
G. J. Hausman
Affiliation:
USDA-ARS, Russell Research Center, PO Box 5677, Athens, GA 30604, USA
Get access

Abstract

Three experiments (EXP) were conducted to determine the role of insulin-like growth factor-I (IGF-I) in the control of growth hormone (GH) and LH secretion. In EXP I, prepuberal gilts, 65 ± 6 kg body weight and 140 days of age received intracerebroventricular (ICV) injections of saline (n = 4), 25 μg (n = 4) or 75 μg (n = 4) IGF-I and jugular blood samples were collected. In EXP II, anterior pituitary cells in culture collected from 150-day-old prepuberal gilts (n = 6) were challenged with 0.1, 10 or 1000 nM [Ala15]-h growth hormone-releasing hormone-(1-29)NH2 (GHRH), or 0.01, 0.1, 1, 10, 30 nM IGF-I individually or in combinations with 1000 nM GHRH. Secreted GH was measured at 4 and 24 h after treatment. In EXP III, anterior pituitary cells in culture collected from 150-day-old barrows (n = 5) were challenged with 10, 100 or 1000 nM gonadotropin-releasing hormone (GnRH) or 0.01, 0.1, 1, 10, 30 nM IGF-I individually or in combinations with 100 nM GnRH. Secreted LH was measured at 4 h after treatment. In EXP I, serum GH and LH concentrations were unaffected by ICV IGF-I treatment. In EXP II, relative to control all doses of GHRH increased (P < 0.01) GH secretion. Only 1, 10, 30 nM IGF-I enhanced (P < 0.02) basal GH secretion at 4 h, whereas by 24 h all doses except for 30 nM IGF-I suppressed (P < 0.02) basal GH secretion compared to control wells. All doses of IGF-I in combination with 1000 nM GHRH increased (P < 0.04) the GH response to GHRH compared to GHRH alone at 4 h, whereas by 24 h all doses of IGF-I suppressed (P < 0.04) the GH response to GHRH. In EXP III, all doses of IGF-I increased (P < 0.01) basal LH levels while the LH response to GnRH was unaffected by IGF-I (P > 0.1). In conclusion, under these experimental conditions the results suggest that the pituitary is the putative site for IGF-I modulation of GH and LH secretion. Further examination of the role of IGF-I on GH and LH secretion is needed to understand the inhibitory and stimulatory action of IGF-I on GH and LH secretion.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abe, H, Molitch, ME, Van Wyk, JJ, Underwood, LE 1983. Human growth hormone and somatomedin-C suppress the spontaneous release of growth hormone in unanesthetized rats. Endocrinology 113, 13191324.CrossRefGoogle ScholarPubMed
Adam, CL, Findlay, PA, Moore, AH 1998. Effects of insulin-like growth factor-1 on luteinizing hormone secretion in sheep. Animal Reproduction Science 50, 4556.CrossRefGoogle ScholarPubMed
Adam, CL, Gadd, TS, Findlay, PA, Wathes, DC 2000. IGF-I stimulation of luteinizing hormone secretion, IGF-binding proteins (IGFBPs) and expression of mRNAs for IGFs, IGF receptors and IGFBPs in the ovine pituitary gland. Journal of Endocrinology 166, 247254.CrossRefGoogle ScholarPubMed
Barb, CR, Kraeling, RR, Rampacek, GB, Fonda, ES, Kiser, TE 1982. Inhibition of ovulation and LH secretion in the gilt after treatment with ACTH or hydrocortisone. Journal of Reproduction and Fertility 64, 8592.CrossRefGoogle ScholarPubMed
Barb, CR, Estienne, MJ, Kraeling, RR, Marple, DN, Rampacek, GB, Rahe, CH, Sartin, JL 1991. Endocrine changes in sows exposed to elevated ambient temperature during lactation. Domestic Animal Endocrinology 8, 117127.CrossRefGoogle ScholarPubMed
Barb, CR, Kraeling, RR, Rampacek, GB 1995. Glucose and free fatty acid modulation of growth hormone and luteinizing hormone secretion by cultured porcine pituitary cells. Journal of Animal Science 73, 14161423.CrossRefGoogle ScholarPubMed
Barb, CR, Barrett, JB, Kraeling, RR, Rampacek, GB 2001. Serum leptin concentrations, luteinizing hormone and growth hormone secretion during feed and metabolic fuel restriction in the prepuberal gilt. Domestic Animal Endocrinology 20, 4763.CrossRefGoogle ScholarPubMed
Berelowitz, M, Szabo, M, Frohman, LA, Firestone, S, Chu, L 1981. Somatomedin-C mediates growth hormone negative feedback by effects on both the hypothalamus and the pituitary. Science 212, 12791281.CrossRefGoogle ScholarPubMed
Buonomo, FC, Lauterio, TJ, Caile, CA, Campion, DR 1987. Determination of insulin-like growth factor-1 (IGF1) and IGF binding protein levels in swine. Domestic Animal Endocrinology 4, 2331.CrossRefGoogle ScholarPubMed
Crawford, BA, Handelsman, DJ 1996. Androgens regulate circulating levels of insulin-like growth factor (IGF)-I and IGF binding protein-3 during puberty in male baboons. Journal of Clinical Endocrinology and Metabolism 81, 6572.Google ScholarPubMed
Daftary, SS, Gore, AC 2003. Developmental changes in hypothalamic insulin-like growth factor-1: relationship to gonadotropin-releasing hormone neurons. Endocrinology 144, 20342045.CrossRefGoogle ScholarPubMed
Daftary, SS, Gore, AC 2005. IGF-1 in the brain as a regulator of reproductive neuroendocrine function. Proceedings of the Society for Experimental Biology and Medicine (Maywood) 230, 292306.CrossRefGoogle ScholarPubMed
Dubreuil, P, Pelletier, G, Petitclerc, D, Lapierre, H, Couture, Y, Brazeau, P, Gaudreau, P, Morisset, J 1987. Influence of age and sex on basal secretion of growth hormone (GH) and on GH-induced release by porcine GH-releasing factor pGRF (1-29NH2) in growing pigs. Domestic Animal Endocrinology 4, 299307.CrossRefGoogle Scholar
Estienne, MJ, Kesner, JS, Barb, CR, Kraeling, RR, Rampacek, GB, Estienne, CE 1990. Gonadotropin and prolactin secretion following intraventricular administration of morphine in gilts. Proceedings of the Society for Experimental Biology and Medicine 193, 9297.CrossRefGoogle ScholarPubMed
Fletcher, TP, Thomas, GB, Dunshea, FR, Moore, LG, Clarke, IJ 1995. IGF feedback effects on growth hormone secretion in ewes: evidence for action at the pituitary but not the hypothalamic level. Journal of Endocrinology 144, 323331.CrossRefGoogle Scholar
Fruchtman, S, Jackson, L, Borski, R 2000. Insulin-like growth factor I disparately regulates prolactin and growth hormone synthesis and secretion: studies using the teleost pituitary model. Endocrinology 141, 28862894.CrossRefGoogle ScholarPubMed
Gill, JL 1978. Completely randomized design and analysis of variance. In Design and analysis of experiments in the animal and medical sciences (ed. JL Gill). Iowa State University Press, Ames.Google Scholar
Handelsman, DJ, Spaliviero, JA, Scott, CD, Baxter, RC 1987. Hormonal regulation of the peripubertal surge of insulin-like growth factor-I in the rat. Endocrinology 120, 491496.CrossRefGoogle ScholarPubMed
Harel, Z, Tannenbaum, GS 1992a. Centrally administered insulin-like growth factor II fails to alter pulsatile growth hormone secretion or food intake. Neuroendocrinology 56, 161168.CrossRefGoogle ScholarPubMed
Harel, Z, Tannenbaum, GS 1992b. Synergistic interaction between insulin-like growth factors-I and -II in central regulation of pulsatile growth hormone secretion. Endocrinology 131, 758764.Google Scholar
Hiney, JK, Ojeda, SR, Dees, WL 1991. Insulin-like growth factor-I: a possible metabolic signal involved in the regulation of female puberty. Neuroendocrinology 54, 420423.CrossRefGoogle ScholarPubMed
Hiney, JK, Srivastava, V, Nyberg, CL, Ojeda, SR, Dees, WL 1996. Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology 137, 37173728.CrossRefGoogle ScholarPubMed
Huang, YS, Rousseau, K, Le Belle, N, Vidal, B, Burzawa-Ge’rard, E, Marchelidon, J, Dufour, S 1998. Insulin-like growth factor-I stimulates gonadotrophin production from eel pituitary cells: a possible metabolic signal for induction of puberty. Journal of Endocrinology 159, 4352.CrossRefGoogle Scholar
Kanematsu, T, Irahara, M, Miyake, T, Shitsukawa, K, Aono, T 1991. Effect of insulin-like growth factor I on gonadotropin release from the hypothalamus–pituitary axis in vitro. Acta Endocrinologica 125, 227233.Google ScholarPubMed
Kesner, JS, Kraeling, RR, Rampacek, GB, Johnson, B 1987. Absence of an estradiol-induced surge of luteinizing hormone in pigs receiving unvarying pulsatile gonadotropin-releasing hormone stimulation. Endocrinology 121, 18621869.CrossRefGoogle ScholarPubMed
Lee, CY, Chung, CS, Simmen, FA 1993. Ontogeny of the porcine insulin-like growth factor system. Molecular and Cellular Endocrinology 93, 7180.CrossRefGoogle ScholarPubMed
Littell, RC, Milliken, GA, Stroup, WW, Wolfinger, RD 1996. SAS (R) system for mixed models. SAS Institute Inc., Cary, NC, USA.Google Scholar
Mauras, N, Rogol, AD, Haymond, MW, Veldhuis, JD 1996. Sex steroids, growth hormone, insulin-like growth factor-1: neuroendocrine and metabolic regulation in puberty. Hormone Research 45, 7480.CrossRefGoogle ScholarPubMed
Miller, BH, Gore, AC 2001. Alterations in hypothalamic insulin-like growth factor-I and its associations with gonadotropin releasing hormone neurons during reproductive development and ageing. Journal of Neuroendocrinology 13, 728736.CrossRefGoogle ScholarPubMed
Morita, S, Yamashita, S, Melmed, S 1987. Insulin-like growth factor I action on rat anterior pituitary cells: effects of intracellular messengers on growth hormone secretion and messenger ribonucleic acid levels. Endocrinology 121, 20002006.CrossRefGoogle ScholarPubMed
Muller, EE, Locatelli, V, Cocchi, D 1999. Neuroendocrine control of growth hormone secretion. Physiological Review 79, 511607.CrossRefGoogle ScholarPubMed
Niimi, M, Takahara, J, Kawanishi, K, Irino, S 1985. Effects of age on GH responses to growth hormone-releasing factor in rats. Endocrinology Japan 32, 559562.CrossRefGoogle ScholarPubMed
National Research Council 1998. Nutrient requirements in swine, 10th edition(National Academy of Sciences). National Academy Press, Washington, DC, USA.Google Scholar
Prunier, A, Louveau, I 1997. Influence of ovariectomy on metabolic and endocrine parameters during sexual development in the female pig. Journal of Endocrinology 154, 423429.CrossRefGoogle ScholarPubMed
Roberts, CA, McCutcheon, SN, Blair, HT, Gluckman, PD, Breier, BH 1990. Developmental patterns of plasma insulin-like growth factor-1 concentrations in sheep. Domestic Animal Endocrinology 7, 457463.CrossRefGoogle ScholarPubMed
Statistical Analysis Systems Institute 1999. SAS user’s guide (release 8.0). Statistical Analysis Systems Institute, Inc., Cary, NC, USA.Google Scholar
Soldani, R, Cagnacci, A, Paoletti, AM, Yen, SS, Melis, GB 1995. Modulation of anterior pituitary luteinizing hormone response to gonadotropin-releasing hormone by insulin-like growth factor I in vitro. Fertility and Sterility 64, 634637.CrossRefGoogle ScholarPubMed
Soldani, R, Cagnacci, A, Yen, SSC 1994. Insulin, insulin-like growth factor I (IGF-I) and IGF-II enhance basal and gonadotrophin-releasing hormone-stimulated luteinizing hormone release from rat anterior pituitary cells in vitro. European Journal of Endocrinology 131, 641645.CrossRefGoogle ScholarPubMed
Spencer, GSG, Bass, JJ, Hodgkinson, SC, Edgley, WHR, Moore, LG 1991. Effect of intraventricular injection of IGF-I on circulating growth hormone concentrations in the sheep. Domestic Animal Endocrinology 8, 155160.CrossRefGoogle ScholarPubMed
Spencer, GSG, Berry, CJ, Hodgkinson, SC, Bass, JJ 1993. On the neuroendocrine role of insulin-like growth factors 1 and 2 in the regulation of growth hormone secretion. Molecular and Cellular Neurosciences 4, 538542.CrossRefGoogle ScholarPubMed
Tannenbaum, GS, Guyda, HJ, Posner, BI 1983. Insulin-like growth factors: a role in growth hormone negative feedback and body weight regulation via brain. Science 220, 7779.CrossRefGoogle ScholarPubMed
Whitley, NC, Barb, CR, Utley, RV, Popwell, JM, Kraeling, RR, Rampacek, GB 1995. Influence of stage of the estrous cycle on insulin-like growth factor-I modulation of luteinizing hormone secretion in the gilt. Biology of Reproduction 53, 13591364.CrossRefGoogle ScholarPubMed
Yamamoto, H, Prager, D, Yamasaki, H, Melmed, S 1993. Rat pituitary GC cell insulin-like growth factor-I receptor regulation. Endocrinology 133, 14201425.CrossRefGoogle ScholarPubMed
Yamashita, S, Melmed, S 1986. Insulin-like growth factor I action on rat anterior pituitary cells: suppression of growth hormone secretion and messenger ribonucleic acid levels. Endocrinology 118, 176182.CrossRefGoogle ScholarPubMed