Centrally applied somatostatin inhibits the estrogen-induced luteinizing hormone surge via hypothalamic gonadotropin-releasing hormone cell activation in female rats

Biology of Reproduction

Volumn 71, Issue 3, 2004, Pages 813-819

  Van Vugt, Harmke H ^a   Swarts, Hans J M ^a   Van De Heijning, Bert J M ^a   Van Der Beek, Eline M ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b NUMICO RESEARCH   (Netherlands)

Author keywords

Gonadotropin releasing hormone; Growth hormone; Hypothalamus; Luteinizing hormone; Ovulatory cycle

Indexed keywords

ESTROGEN; GONADORELIN; GROWTH HORMONE; LUTEINIZING HORMONE; OCTREOTIDE; PROTEIN C FOS; SODIUM CHLORIDE; SOMATOSTATIN;

ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; GONADOTROPIN SECRETING CELL; GROWTH HORMONE DEFICIENCY; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LUTEINIZING HORMONE RELEASE; MOLECULAR INTERACTION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROESTRUS; RAT; REPRODUCTION; SOMATIC CELL;

ANIMALS; ESTRADIOL; FEMALE; GASTROINTESTINAL AGENTS; GONADOTROPIN-RELEASING HORMONE; GROWTH HORMONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INJECTIONS, INTRAVENTRICULAR; LUTEINIZING HORMONE; OCTREOTIDE; OVARIECTOMY; PITUITARY GLAND; PROESTRUS; RATS; RATS, WISTAR; SOMATOSTATIN;

ANIMALIA;

EID: 4243075352     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.028936     Document Type: Article

References (68)

1. Tannenbaum GS, Painson JC, Lapointe M, Gurd W, McCarthy GF. Interplay of somatostatin and growth hormone-releasing hormone in genesis of episodic growth hormone secretion. Metabolism 1990; 39: 35-39.
2. Muller EE, Locatelli V, Cocchi D. Neuroendocrine control of growth hormone secretion. Physiol Rev 1999; 79:511-607.
3. Naar EM, Bartke A, Majumdar SS, Buonomo FC, Yun JS, Wagner TE. Fertility of transgenic female mice expressing bovine growth hormone or human growth hormone variant genes. Biol Reprod 1991; 45:178-187.
4. Bartke A. Role of growth hormone and prolactin in the control of reproduction: what are we learning from transgenic and knock-out animals? Steroids 1999; 64:598-604.
5. Bartke A, Chandrashekar V, Bailey B, Zaczek D, Turyn D. Consequences of growth hormone (GH) overexpression and GH resistance. Neuropeptides 2002; 36:201-208.
6. Bartke A, Chandrashekar V, Turyn D, Steger RW, Debeljuk L, Winters TA, Mattison JA, Danilovich NA, Croson W, Wernsing DR, Kopchick JJ. Effects of growth hormone overexpression and growth hormone resistance on neuroendocrine and reproductive functions in transgenic and knock-out mice. Proc Soc Exp Biol Med 1999; 222:113-123.
7. Sasaki F, Tojo H, Iwama Y, Miki N, Maeda K, Ono M, Kiso Y, Okada T, Matsumoto Y, Tachi C. Growth hormone-releasing hormone (GHRH)-GH-somatic growth and luteinizing hormone (LH)RH-LH-ovarian axes in adult female transgenic mice expressing human GH gene. J Neuroendocrinol 1997; 9:615-626.
8. Freeman ME. The neuroendocrine control of the ovarian cycle of the rat. In: Knobil E, Neill JD (eds.), The Physiology of Reproduction, vol. 2, 2nd ed. New York: Raven press; 1994:613-658.
9. Tang K, Bartke A, Gardiner CS, Wagner TE, Yun JS. Gonadotropin secretion, synthesis, and gene expression in human growth hormone transgenic mice and in Ames dwarf mice. Endocrinology 1993; 132: 2518-2524.
10. Bartke A, Cecim M, Tang K, Steger RW, Chandrashekar V, Turyn D. Neuroendocrine and reproductive consequences of overexpression of growth hormone in transgenic mice. Proc Soc Exp Biol Med 1994; 206:345-359.
11. Hurley DL, Phelps CJ. Hypothalamic preprosomatostatin messenger ribonucleic acid expression in mice transgenic for excess or deficient endogenous growth hormone. Endocrinology 1992; 130:1809-1815.
12. Yu WH, Kimura M, McCann SM. Effect of somatostatin on the release of gonadotropins in male rats. Proc Soc Exp Biol Med 1997; 214:83-86.
13. Starcevic V, Milosevic V, Brkic B, Severs WB. Somatostatin affects morphology and secretion of pituitary luteinizing hormone (LH) cells in male rats. Life Sci 2003; 70:3019-3027.
14. Lovren M, Sekulic M, Milosevic V, Radulovic N. Effects of somatostatins on gonadotrophic cells in female rats. Acta Histochem 1998; 100:329-335.
15. Nestorovic N, Lovren M, Sekulic M, Sosic-Jurjevic B, Negic N, Milosevic V. Effects of centrally applied octreotide on pituitary gonadotrophic cells in rat females. In: Program of the ENEA; 2002; Munich, Germany. Abstract PB-335.
16. Nestorovic N, Lovren M, Sekulic M, Filipovic B, Milosevic V. Effects of multiple somatostatin treatment on rat gonadotrophic cells and ovaries. Histochem J 2003; 33:695-702.
17. Biermasz NR, Pereira AM, Frolich M, Romijn JA, Veldhuis JD, Roelfsema F. Octreotide represses secretory-burst mass and nonpulsatile secretion but does not restore event frequency or orderly GH secretion in acromegaly. Am J Physiol Endocrinol Metab 2004; 286: E25-E30.
18. Griffioen HA, Van der Beek E, Boer GJ. Gelatin embedding to preserve lesion-damaged hypothalami and intracerebroventricular grafts for vibratome slicing and immunocytochemistry. J Neurosci Methods 1992; 43:43-47.
19. Van der Beek EM, Van Oudheusden HJ, Buijs RM, Van der Donk HA, Van den Hurk R, Wiegant VM. Preferential induction of c-fos immunoreactivity in vasoactive intestinal polypeptide-innervated gonadotropin-releasing hormone neurons during a steroid-induced luteinizing hormone surge in the female rat. Endocrinology 1994; 134: 2636-2644.
20. Palm IF, Van der Beek EM, Wiegant VM, Buijs RM, Kalsbeek A. The stimulatory effect of vasopressin on the luteinizing hormone surge in ovariectomized, estradiol-treated rats is time-dependent. Brain Res 2001; 901:109-116.
21. Hoffman GE, Lee WS, Attardi B, Yann V, Fitzsimmons MD. Luteinizing hormone-releasing hormone neurons express c-fos antigen after steroid activation. Endocrinology 1990; 126:1736-1741.
22. Lee WS, Smith MS, Hoffman GE. Luteinizing hormone-releasing hormone neurons express Fos protein during the proestrous surge of luteinizing hormone. Proc Natl Acad Sci U S A 1990; 87:5163-5167.
23. Van der Beek EM, Swarts HJ, Wiegant VM. Central administration of antiserum to vasoactive intestinal peptide delays and reduces luteinizing hormone and prolactin surges in ovariectomized, estrogen-treated rats. Neuroendocrinology 1999; 69:227-237.
24. Harris TG, Dye S, Robinson JE, Skinner DC, Evans NP. Progesterone can block transmission of the estradiol-induced signal for luteinizing hormone surge generation during a specific period of time immediately after activation of the gonadotropin-releasing hormone surge-generating system. Endocrinology 1999; 140:827-834.
25. Knuth, UA, Sikand GS, Casanueva FE, Friesen HG. Changes in somatostatin-like activity in discrete areas of the rat hypothalamus during different stages of proestrus and diestrus and their relation to serum gonadotropin, prolactin, and growth hormone levels. Endocrinology 1983; 112:1506-1511.
26. Zorilla R, Simard J, Labrie F, Pelletier G. Variations of pre-prosomatostatin mRNA levels in the hypothalamic periventricular nucleus during the rat estrous cycle. Mol Cell Neurosci 1991; 2:294-298.
27. Estupina C, Pinter A, Belmar J, Astier H, Arancibia S. Variations in hypothalamic somatostatin release and content during the estrous cycle in the rat. Effects of ovariectomy and estrogen supplementation. Neuroendocrinology 1996; 63:181-187.
28. Lee WS, Smith S, Hoffman GE. cFos activity identifies recruitment of luteinizing hormone-releasing hormone neurons during the ascending phase of the proestrous luteinizing hormone surge. J Neuroendocrinol 1992; 4: 161-166.
29. Le WW, Berghorn KA, Rassnick S, Hoffman GE. Periventricular preoptic area neurons coactivated with luteinizing hormone (LH)-releasing hormone (LHRH) neurons at the time of the LH surge are LHRH afferents. Endocrinology 1999; 140:510-519.
30. Wang HJ, Hoffman GE, Smith MS. Increased GnRH mRNA in the GnRH neurons expressing cFos during the proestrous LH surge. Endocrinology 1995; 136:3673-3676.
31. Rubin BS, Mitchell S, Lee CE, King JC. Reconstructions of populations of luteinizing hormone releasing hormone neurons in young and middle-aged rats reveal progressive increases in subgroups expressing Fos protein on proestrus and age-related deficits. Endocrinology 1995; 136:3823-3830.
32. Levine JE, Ramirez VD. In vivo release of luteinizing hormone-releasing hormone estimated with push-pull cannulae from the mediobasal hypothalami of ovariectomized, steroid-primed rats. Endocrinology 1980; 107:1782-1790.
33. Levine JE, Ramirez VD. Luteinizing hormone-releasing hormone release during the rat estrous cycle and after ovariectomy, as estimated with push-pull cannulae. Endocrinology 1982; 111:1439-1448.
34. Epelbaum J, Willoughby JO, Brazeau P, Martin JB. Effects of brain lesions and hypothalamic deafferentation on somatostatin distribution in the rat brain. Endocrinology 1977; 101:1495-1502.
35. Praputpittaya C, Arita J, Kimura F. Growth hormone secretion after hypothalamic periventricular lesions in the rat. Neuroendocrinology 1987; 46:104-109.
36. Ishikawa K, Taniguchi Y, Kurosumi K, Suzuki M, Shinoda M. Immunohistochemical identification of somatostatin-containing neurons projecting to the median eminence of the rat. Endocrinology 1987; 121:94-97.
37. Kawano H, Daikoku S. Somatostatin-containing neuron systems in the rat hypothalamus: retrograde tracing and immunohistochemical studies. J Comp Neurol 1988; 271:293-299.
38. Merchenthaler I, Setalo G, Csontos C, Petrusz P, Flerko B, Negro-Vilar A. Combined retrograde tracing and immunocytochemical identification of luteinizing hormone-releasing hormone- and somatostatin-containing neurons projecting to the median eminence of the rat. Endocrinology 1989; 125:2812-2821.
39. Katakami H, Downs TR, Frohman LA. Inhibitory effect of hypothalamic medial preoptic area somatostatin on growth hormone-releasing factor in the rat. Endocrinology 1988; 123:1103-1109.
40. Willoughby JO, Brogan M, Kapoor R. Hypothalamic interconnections of somatostatin and growth hormone releasing factor neurons. Neuroendocrinology 1989; 50:584-591.
41. McCarthy GF, Beaudet A, Tannenbaum GS. Colocalization of somatostatin receptors and growth hormone-releasing factor immunoreactivity in neurons of the rat arcuate nucleus. Neuroendocrinology 1992; 56:18-24.
42. Giustina A, Veldhuis JD. Pathophysiology of the neuroregulation of growth hormone secretion in experimental animals and the human. Endocr Rev 1998; 19:717-797.
43. Bluet-Pajot MT, Epelbaum J, Gourdji D, Hammond C, Kordon C. Hypothalamic and hypophyseal regulation of growth hormone secretion. Cell Mol Neurobiol 1998; 18:101-123.
44. Tannenbaum GS, McCarthy GF, Zeitler P, Beaudet A. Cysteamine-induced enhancement of growth hormone-releasing factor (GRF) immunoreactivity in arcuate neurons: morphological evidence for putative somatostatin/GRF interactions within hypothalamus. Endocrinology 1990; 127:2551-2560.
45. Gardi J, Szentirmai E, Hajdu I, Obal F Jr, Krueger JM. The somatostatin analog, octreotide, causes accumulation of growth hormone-releasing hormone and depletion of angiotensin in the rat hypothalamus. Neurosci Lett 2001; 315:37-40.
46. Banks WA, Schally AV, Barrera CM, Fasold MB, Durham DA, Csernus VJ, Groot K, Kastin AJ. Permeability of the murine blood-brain barrier to some octapeptide analogs of somatostatin. Proc Natl Acad Sci U S A 1990; 87:6762-6766.
47. O'Carroll AM, Krempels K. Widespread distribution of somatostatin receptor messenger ribonucleic acids in rat pituitary. Endocrinology 1995; 136:5224-5227.
48. Kimura N, Hayafuji C. Characterization of 17-beta-estradiol-dependent and -independent somatostatin receptor subtypes in rat anterior pituitary. J Biol Chem 1989; 264:7033-7040.
49. Djordjijevic D, Zhang J, Priam M, Viollet C, Gourdji D, Kordon C, Epelbaum J. Effect of 17beta-estradiol on somatostatin receptor expression and inhibitory effects on growth hormone and prolactin release in rat pituitary cell cultures. Endocrinology 1998; 139:2272-2277.
50. Patel YC. Somatostatin and its receptor family. Front Neuroendocrinol 1999; 20:157-198.
51. Schindler M, Humphrey PP, Emson PC. Somatostatin receptors in the central nervous system. Prog Neurobiol 1996; 50:9-47.
52. Childs GV, Unabia G, Wu P. Differential expression of growth hormone messenger ribonucleic acid by somatotropes and gonadotropes in male and cycling female rats. Endocrinology 2000; 141:1560-1570.
53. Childs GV. Growth hormone cells as co-gonadotropes: partners in the regulation of the reproductive system. Trends Endocrinol Metab 2000; 11:168-175.
54. Childs GV, Unabia G, Rougeau D. Cells that express luteinizing hormone (LH) and follicle-stimulating hormone (FSH) beta-subunit messenger ribonucleic acids during the estrous cycle: the major contributors contain LH beta, FSH beta, and/or growth hormone. Endocrinology 1994; 134:990-997.
55. Childs GV, Unabia G, Miller BT. Cytochemical detection of gonadotropin-releasing hormone-binding sites on rat pituitary cells with luteinizing hormone, follicle-stimulating hormone, and growth hormone antigens during diestrous up-regulation. Endocrinology 1994; 134: 1943-1951.
56. Bruno JF, Xu Y, Song J, Berelowitz M. Tissue distribution of somatostatin receptor subtype messenger ribonucleic acid in the rat. Endocrinology 1993; 133:2561-2567.
57. Helboe L, Stidsen CE, Moller M. Immunohistochemical and cytochemical localization of the somatostatin receptor subtype sst1 in the somatostatinergic parvocellular neuronal system of the rat hypothalamus. J Neurosci 1998; 18:4938-4945.
58. Lanneau C, Bluet-Pajot MT, Zizzari P, Csaba Z, Doumaud P, Helboe L, Hoyer D, Pellegrini E, Tannenbaum GS, Epelbaum J, Gardette R. Involvement of the Sst1 somatostatin receptor subtype in the intrahypothalamic neuronal network regulating growth hormone secretion: an in vitro and in vivo antisense study. Endocrinology 2001; 141: 967-979.
59. Hervieu G, Emson PC. Visualisation of somatostatin receptor sst(3) in the rat central nervous system. Brain Res Mol Brain Res 1999; 71: 290-303.
60. Selmer IS, Schindler M, Humphrey PP, Emson PC. Immunohistochemical localization of the somatostatin sst(4) receptor in rat brain. Neuroscience 2001; 98:523-533.
61. Zhang WH, Beaudet A, Tannenbaum GS. Sexually dimorphic expression of sst1 and sst2 somatostatin receptor subtypes in the arcuate nucleus and anterior pituitary of adult rats. J Neuroendocrinol 1999; 11:129-136.
62. Tannenbaum GS, Zhang WH, Lapointe M, Zeitler P, Beaudet A. Growth hormone-releasing hormone neurons in the arcuate nucleus express both Sst1 and Sst2 somatostatin receptor genes. Endocrinology 1998; 139:1450-1453.
63. Beaudet A, Greenspun D, Raelson J, Tannenbaum GS. Patterns of expression of SSTR1 and SSTR2 somatostatin receptor subtypes in the hypothalamus of the adult rat: relationship to neuroendocrine function. Neuroscience 1995; 65:551-561.
64. Goubillon ML, Caraty A, Herbison AE. Evidence in favour of a direct input from the ventromedial nucleus to gonadotropin-releasing hormone neurones in the ewe: an anterograde tracing study. J Neuroendocrinol 2002; 14:95-100.
65. Hoffman GE, Dohanics J, Watson RE Jr, Wiegand SJ. The hypothalamic ventromedial nucleus sends a met-enkephalin projection to the preoptic area's periventricular zone in the female rat. Brain Res Mol Brain Res 1996; 36:201-210.
66. Le WW, Attardi B, Berghorn KA, Blaustein J, Hoffman GE. Progesterone blockade of a luteinizing hormone surge blocks luteinizing hormone-releasing hormone Fos activation and activation of its preoptic area afferents. Brain Res 1997; 778:272-280.
67. Le WW, Wise PM, Murphy AZ, Coolen LM, Hoffman GE. Parallel declines in Fos activation of the medial anteroventral periventricular nucleus and LHRH neurons in middle-aged rats. Endocrinology 2001; 142:4976-4982.
68. Smith MJ, Jennes L. Neural signals that regulate GnRH neurones directly during the oestrous cycle. Reproduction 2003; 122:1-10.