Intrafetal insulin-like growth factor-I infusion stimulates adrenal growth but not steroidogenesis in the sheep fetus during late gestation

Endocrinology

Volumn 148, Issue 11, 2007, Pages 5424-5432

  Ross, J T ^a   McMillen, I C ^a,c   Lok, F ^a   Thiel, A G ^a   Owens, J A ^a   Coulter, C L ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CATECHOLAMINE; HYDROCORTISONE; SODIUM CHLORIDE; SOMATOMEDIN C;

ADRENAL CORTEX; ADRENAL GLAND; ADRENAL MEDULLA; ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CELL NUCLEUS; CONTROLLED STUDY; DRUG EFFECT; FETUS; FETUS GROWTH; FETUS WEIGHT; GESTATION PERIOD; IMMUNOCYTOCHEMISTRY; MORPHOMETRICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEEP; STEROIDOGENESIS; ZONA FASCICULATA; ZONA GLOMERULOSA;

ADRENAL GLANDS; ANIMALS; FEMALE; FETAL BLOOD; FETAL DEVELOPMENT; FETAL WEIGHT; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GESTATIONAL AGE; HYDROCORTISONE; INSULIN-LIKE GROWTH FACTOR I; ORGAN SIZE; PREGNANCY; SHEEP; STEROIDS;

EID: 35548953244     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2006-1573     Document Type: Article

References (55)

1. Challis JRG, Matthews SG, Gibb W, Lye SJ 2000 Endocrine and paracrine regulation of birth at term and preterm. Endocr Rev 21:514-550
2. Coulter CL, Ross JT, Owens JA, Bennett HP, McMillen IC 2002 Role of pituitary POMC-peptides and insulin-like growth factor II in the developmental biology of the adrenal gland. Arch Physiol Biochem 110:99-105
3. Mesiano S, Jaffe RB 1997 Developmental and functional biology of the primate fetal adrenal cortex. Endocr Rev 18:378-403
4. Liggins GC 1994 The role of cortisol in preparing the fetus for birth. Reprod Fertil Dev 6:141-150
5. Challis JR, Brooks AN 1989 Maturation and activation of hypothalamic-pituitary adrenal function in fetal sheep. Endocr Rev 10:182-204
6. Antolovich GC, Clarke IJ, McMillen IC, Perry RA, Robinson PM, Silver M, Young R 1990 Hypothalamo-pituitary disconnection in the fetal sheep. Neuroendocrinol 51:1-9
7. Barnes RJ, Comline RS, Silver M 1977 The effects of bilateral adrenalectomy or hypophysectomy of the foetal lamb in utero. J Physiol (Lond) 264:429-447
8. Liggins GC, Kennedy PC, Holm LW 1967 Failure of initiation of parturition after electrocoagulation of the pituitary of the fetal lamb. Am J Obstet Gynecol 98:1080-1086
9. Phillips ID, Ross JT, Owens JA, Young IR, McMillen IC 1996 The peptide ACTH (1-39), adrenal growth and steroidogenesis in the sheep fetus after disconnection of the hypothalamus and pituitary. J Physiol (Lond) 491:871-879
10. Liggins GC 1968 Premature parturition after infusion of corticotrophin or cortisol into foetal lambs. J Endocrinol 42:323-329
11. Hornsby PJ, Gill GN 1977 Hormonal control of adrenocortical cell proliferation. Desensitization to ACTH and interaction between ACTH and fibroblast growth factor in bovine adrenocortical cell cultures. J Clin Invest 60:342-352
12. Naaman E, Chatelain P, Saez JM, Durand P 1989 In vitro effect of insulin and insulin-like growth factor-I on cell multiplication and adrenocorticotropin responsiveness of fetal adrenal cells. Biol Reprod 40:570-577
13. Wolf E, Lahm H, Wu M, Wanke R, Hoeflich A 2000 Effects of IGFBP-2 overexpression in vitro and in vivo. Pediatr Nephrol 14:572-578
14. Coulter CL, Goldsmith PC, Mesiano S, Voytek CC, Martin MC, Han VK, Jaffe RB 1996 Functional maturation of the primate fetal adrenal in vivo. I. Role of insulin-like growth factors (IGFs), IGF-I receptor, and IGF binding proteins in growth regulation. Endocrinology 137:4487-4498
15. Mesiano S, Katz SL, Lee JY, Jaffe RB 1997 Insulin-like growth factors augment steroid production and expression of steroidogenic enzymes in human fetal adrenal cortical cells: implications for adrenal androgen regulation. J Clin Endocrinol Metab 82:1390-1396
16. Mesiano S, Mellon SH, Jaffe RB 1993 Mitogenic action, regulation and localization of insulin-like growth factors in the human fetal adrenal gland. J Clin Endocrinol Metab 76:968-976
17. Penhoat A, Leduque P, Jaillard C, Chatelain PG, Dubois PM, Saez JM 1991 ACTH and angiotensin II regulation of insulin-like growth factor-I and its binding proteins in cultured bovine adrenal cells. J Mol Endocrinol 7:223-232
18. Han VK, Lu F, Bassett N, Yang KP, Delhanty PJ, Challis JR 1992 Insulin-like growth factor-II (IGF-II) messenger ribonucleic acid is expressed in steroidogenic cells of the developing ovine adrenal gland: evidence of an autocrine/paracrine role for IGF-II. Endocrinology 131:3100-3109
19. Dahmer MK, Hart PM, Perlman RL 1991 Insulin-like growth factor-I enhances tyrosine hydroxylase activation in bovine chromaffin cells. J Neurochem 57:1347-1353
20. Dahmer MK, Hart PM, Perlman RL 1990 Studies on the effect of insulin-like growth factor-I on catecholamine secretion from chromaffin cells. J Neurochem 54:931-936
21. Dahmer MK, Perlman RL 1988 Bovine chromaffin cells have insulin-like growth factor-I (IGF-I) receptors: IGF-I enhances catecholamine secretion. J Neurochem 51:321-323
22. Owens JA, Kind KL, Smeaton TC, Lord APD, Robinson JS, Owens PC, Circulating insulin-like growth factors (IGF) and IGF binding protein 1 are acutely regulated by glucose in fetal sheep in late gestation. Proc 10th International Congress of Endocrinology, San Francisco, CA, June 12-15, 1996 (Abstract P1-542)
23. Lok F, Owens JA, Mundy L, Robinson JS, Owens PC 1996 Insulin-like growth factor I promotes growth selectively in fetal sheep in late gestation. Am J Physiol 270:R1148-R1155
24. Owens JA, Kind KL, Carbone F, Robinson JS, Owens PC 1994 Circulating insulin-like growth factors-I and -II and substrates in fetal sheep following restriction of placental growth. J Endocrinol 140:5-13
25. Carr JM, Owens JA, Grant PA, Walton PE, Owens PC, Wallace JC 1995 Circulating insulin-like growth factors (IGFs), IGF-binding proteins (IGFBPs) and tissue mRNA levels of IGFBP-2 and IGFBP-4 in the ovine fetus. J Endocrinol 145:545-557
26. Edwards LJ, Simonetta G, Owens JA, Robinson JS, McMillen IC 1999 Restriction of placental and fetal growth in sheep alters fetal blood pressure responses to angiotensin II and captopril. J Physiol (Lond) 515:897-904
27. Francis GL, McNeil KA, Wallace JC, Ballard FJ, Owens PC 1989 Sheep insulin-like growth factors I and II: sequences, activities and assays. Endocrinology 124:1173-1183
28. Coulter CL, Read LC, Carr BR, Tarantal AF, Barry S, Styne DM 1996 A role for epidermal growth factor in the morphological and functional maturation of the adrenal gland in the fetal rhesus monkey in vivo. J Clin Endocrinol Metab 81:1254-1260
29. Coulter CL, Mulvogue HM, Young IR, Browne CA, McMillen IC 1989 Effect of fetal hypophysectomy on the localization of the catecholamine biosynthetic enzymes and enkephalins in the adrenal medulla of the fetal sheep. J Endocrinol 121:425-430
30. Coulter CL, Young IR, Browne CA, McMillen IC 1989 Effect of hypophysectomy on the growth and development of the sheep adrenal gland: a morphometric study. Acta Endocrinol (Copenh) 120:301-307
31. McMillen IC, Mulvogue HM, Coulter CL, Browne CA, Howe PR 1988 Ontogeny of catecholamine-synthesizing enzymes and enkephalins in the sheep adrenal medulla: an immunocytochemical study. J Endocrinol 118:221-226
32. Doody KM, Carr BR, Rainey WE, Byrd W, Murray BA, Strickler RC, Thomas JL, Mason JI 1990 3β-Hydroxysteroid dehydrogenase/isomerase in the fetal zone and neocortex of the human fetal adrenal gland. Endocrinology 126:2487-2492
33. Warnes KE, McMillen IC, Robinson JS, Coulter CL 2004 Differential actions of metyrapone on the fetal pituitary-adrenal axis in the sheep fetus in late gestation. Biol Reprod 71:620-628
34. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H 1984 Cell-cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal-antibody Ki-67. J Immunol 133:1710-1715
35. McMillen IC, Mercer JE, Thorburn GD 1988 Pro-opiomelanocortin mRNA levels fall in the fetal sheep pituitary before birth. J Mol Endocrinol 1:141-145
36. Phillips ID, Simonetta G, Owens JA, Robinson JS, Clarke IJ, McMillen IC 1996 Placental restriction alters the functional development of the pituitary-adrenal axis in the sheep fetus during late gestation. Pediatr Res 40:861-866
37. D'Mello SR, Weisberg EP, Stachowiak MK, Turzai LM, Gioio AE, Kaplan BB 1988 Isolation and nucleotide sequence of a cDNA clone encoding bovine adrenal tyrosine hydroxylase: comparative analysis of tyrosine hydroxylase gene products. J Neurosci Res 19:440-449
38. Wan DC, Scanlon D, Choi CL, Bunn SJ, Howe PR, Livett BG 1989 Colocalization of RNAs coding for phenylethanolamine N-methyltransferase and proenkephalin A in bovine and ovine adrenals. J Auton Nerv Syst 26:231-240
39. Adams MB, McMillen IC 2000 Actions of hypoxia on catecholamine synthetic enzyme mRNA expression before and after development of adrenal innervation in the sheep fetus. J Physiol (Lond) 529:519-531
40. Mesiano S, Young IR, Hey AW, Browne CA, Thorburn GD 1989 Hypophysectomy of the fetal lamb leads to a fall in the plasma concentration of insulin-like growth factor-I (IGF-I), but not IGF-II. Endocrinology 124:1485-1491
41. Hoeflich A, Weber MM, Fisch T, Nedbal S, Fottner C, Elmlinger MW, Wanke R, Wolf E 2002 Insulin-like growth factor binding protein 2 (IGFBP-2) separates hypertrophic and hyperplastic effects of growth hormone (GH)/IGF-I excess on adrenocortical cells in vivo. FASEB J 16:1721-1731
42. van Dijk JP, Tanswell AK, Challis JR 1988 Insulin-like growth factor (IGF)-II and insulin, but not IGF-I, are mitogenic for fetal rat adrenal cells in vitro. J Endocrinol 119:509-516
43. Frodin M, Gammeltoft S 1994 Insulin-like growth factors act synergistically with basic fibroblast growth factor and nerve growth factor to promote chromaffin cell proliferation. Proc Natl Acad Sci USA 91:1771-1775
44. Chatelain P, Penhoat A, Perrard-Sapori MH, Jaillard C, Naville D, Saez J 1988 Maturation of steroidogenic cells: a target for IGF-I. Acta Paediatr Scand Suppl 347:104-109
45. Penhoat A, Chatelain PG, Jaillard C, Saez JM 1988 Characterization of insulin-like growth factor I and insulin receptors on cultured bovine adrenal fasciculata cells. Role of these peptides on adrenal cell function. Endocrinology 122:2518-2526
46. Begeot M, Langlois D, Saez JM 1989 Insulin-like growth factor-I and insulin increase the stimulatory guanine nucleotide binding protein (Gs) in cultured bovine adrenal cells. Mol Cell Endocrinol 66:53-57
47. Penhoat A, Jaillard C, Saez JM 1989 Corticotropin positively regulates its own receptors and cAMP response in cultured bovine adrenal cells. Proc Natl Acad Sci USA 86:4978-4981
48. Singleton JR, Feldman EL 2001 Insulin-like growth factor-I in muscle metabolism and myotherapies. Neurobiol Dis 8:541-554
49. Rose A, Froment P, Perrot V, Quon MJ, LeRoith D, Dupont J 2004 The luteinizing hormone-releasing hormone inhibits the anti-apoptotic activity of insulin-like growth factor-1 in pituitary αT3 cells by protein kinase Cα-mediated negative regulation of Akt. J Biol Chem 279:52500-52516
50. Saphier PW, Glynn BP, Woods RJ, Shepherd DA, Jeacock MK, Lowry PJ 1993 Elevated levels of N-terminal pro-opiomelanocortin peptides in fetal sheep plasma may contribute to fetal adrenal gland development and the pre-parturient cortisol surge. Endocrinology 133:1459-1461
51. Lowry PJ, Silas L, McLean C, Linton EA, Estivariz FE 1983 Pro-γ-melanocyte-stimulating hormone cleavage in adrenal gland undergoing compensatory growth. Nature 306:70-73
52. Estivariz FE, Carino M, Lowry PJ, Jackson S 1988 Further evidence that N-terminal pro-opiomelanocortin peptides are involved in adrenal mitogenesis. J Endocrinol 116:201-206
53. Estivariz FE, Iturriza F, McLean C, Hope J, Lowry PJ 1982 Stimulation of adrenal mitogenesis by N-terminal proopiocortin peptides. Nature 297:419-422
54. Ross JT, Bennett HP, James S, McMillen IC 2000 Infusion of N-proopiomelanocortin-(1-77) increases adrenal weight and messenger ribonucleic acid levels of cytochrome P450 17α-hydroxylase in the sheep fetus during late gestation. Endocrinology 141:2153-2158
55. Lu F, Yang K, Han VK, Challis JR 1995 Expression, distribution, regulation and function of IGFs in the ovine fetal pituitary. J Mol Endocrinol 14:323-336