Differential effects of GH and GH-releasing peptide-6 on astrocytes

Journal of Endocrinology

Volumn 218, Issue 3, 2013, Pages 263-274

  Baquedano, Eva ^a,c   Chowen, Julie A ^b,c   Argente, Jesús ^a,b,c   Frago, Laura M ^a,c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

^c Instituto de Salud Carlos III   (Spain)

Author keywords

Differentiation; GH; GHRP 6; Hippocampus; Hypothalamus; Proliferation

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; GLIAL FIBRILLARY ACIDIC PROTEIN; GROWTH HORMONE; HISTIDYL DEXTRO TRYPTOPHYLALANYLTRYPTOPHYL DEXTRO PHENYLALANYLLYSINAMIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOMA CELL; BRAIN LEVEL; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLUM; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; HORMONE ACTION; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

DIFFERENTIATION; GH; GHRP-6; HIPPOCAMPUS; HYPOTHALAMUS; PROLIFERATION;

ANIMALS; ASTROCYTES; CELL LINE; CELL PROLIFERATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GROWTH HORMONE; HIPPOCAMPUS; HYPOTHALAMUS; MALE; OLIGOPEPTIDES; RATS; RATS, WISTAR; VIMENTIN;

EID: 84884173876     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0053     Document Type: Article

References (76)

1. Åberg MA, Åberg ND, Hedbäcker H, Oscarsson J & Eriksson PS 2000 Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. Journal of Neuroscience 20 2896-2903.
2. Ajo R, Cacicedo L, Navarro C, & Sánchez-Franco F 2003 Growth hormone action on proliferation and differentiation of cerebral cortical cells from fetal rat. Endocrinology 144 1086-1097. (doi:10.1210/en.2002-220667)
3. Andrews ZB 2011 The extra-hypothalamic actions of ghrelin on neuronal function. Trends in Neuroscience 34 31-40. (doi:10.1016/j.tins.2010. 10.001)
4. Barres BA 1991 New roles for glia. Journal of Neuroscience 11 3685-3694.
5. Bennett PA, Levy A, Carmignac DF, Robinson IC, & Lightman SL 1996 Differential regulation of the growth hormone receptor gene: effects of dexamethasone and estradiol. Endocrinology 137 3891-3896. (doi:10.1210/en.137.9.3891)
6. Blackmore DG, Reynolds BA, Golmohammadi MG, Large B, Aguilar RM, Haro L, Waters MJ, & Rietze RL 2012 Growth hormone responsive neural precursor cells reside within the adult mammalian brain. Scientific Reports 2 250. (doi:10.1038/srep00250)
7. Brooks AJ, Wooh JW, Tunny KA, & Waters MJ 2008 Growth hormone receptor; mechanism of action. International Journal of Biochemistry, & Cell Biology 40 1984-1989. (doi:10.1016/j.biocel.2007.07.008)
8. Burman P, & Deijen J 1998 Quality of life and cognitive function in patients with pituitary insufficiency. Psychotherapy and Psychosomatics 67 154-167. (doi:10.1159/000012276)
9. Camiña JP, Carreira MC, Micic D, Pombo M, Kalestimur F, Dieguez C, & Casanueva FF 2003 Regulation of ghrelin secretion and action. Endocrine 22 5-12. (doi:10.1385/ENDO:22:1:5)
10. Chan CB, Tse MC, & Cheng CH 2006 Regulation and mechanism of growth hormone and insulin-like growth factor-I biosynthesis and secretion. In The Somatotrophic Axis in Brain Function, pp 7-23. Ed. Fred Nyberg. Burlington: Elsevier Academic Press.
11. Chen JH, Huang SM, Chen CC, Tsai CF, Yeh WL, Chou SJ, Hsieh WT, & Lu DY 2011 Ghrelin induces cell migration through GHS-R, CaMKII, AMPK and NF-kB signaling pathway in glioma cells. Journal of Cellular Biochemistry 112 2931-2941. (doi:10.1002/jcb.23209)
12. Chung H, Kim E, Lee DH, Seo S, Ju S, Lee D, Kim H, & Park S 2007 Ghrelin inhibits apoptosis in hypothalamic neuronal cells during oxygen-glucose deprivation. Endocrinology 148 148-159. (doi:10.1210/ en.2006-0991)
13. Clark RG, Carlsson LMS, & Robinson ICAF 1988 Growth hormone (GH) secretion in the conscious rat: negative feedback of GH on its own release. Journal of Endocrinology 119 201-209. (doi:10.1677/joe.0. 1190201)
14. Conway-Campbell BL, Wooh JW, Brooks AJ, Gordon D, Brown RJ, Lichanska AM, Chin HS, Barton CL, Boyle GM, Parsons PG et al. 2007 Nuclear targeting of the growth hormone receptor results in dysregulation of cell proliferation and tumorigenesis. PNAS 104 13331-13336. (doi:10.1073/pnas.0600181104)
15. Cuellar JN, & Isokawa M 2011 Ghrelin-induced activation of cAMP signal transduction and its negative regulation by endocannabinoids in the hippocampus. Neuropharmacology 60 842-851. (doi:10.1016/j.neuropharm. 2010.12.024)
16. Davenport AP, Bonner TI, Foord SM, Harmar AJ, Neubig RR, Pin JP, Spedding M, Kojima M, & Kangawa K 2005 International Union of Pharmacology. LVI: ghrelin receptor nomenclature, distribution, and function. Pharmacological Reviews 57 541-546. (doi:10.1124/pr.57.4.1)
17. Deijen B, Arwert LI, & Drent ML 2011 The GH/IGF-I axis and cognitive changes across a 4-year period in healthy adults. ISRN Endocrinology 2011 249421. (doi:10.5402/2011/249421)
18. Delgado-Rubin A, Chowen JA, Argente J, & Frago LM 2009 Growth hormone releasing peptide-6 protection of hypothalamic neurons from glutamate excitotoxicity is caspase independent and mediated by insulin-like growth factor I. European Journal of Neuroscience 29 2115-2124. (doi:10.1111/j.1460-9568.2009.06770.x)
19. Delgado-Rubin de Célix A, Chowen JA, Argente J, & Frago LM 2006 Growth hormone releasing peptide-6 acts as a survival factor in glutamateinduced excitotoxicity. Journal of Neurochemistry 99 839-849. (doi:10.1111/j.1471-4159.2006.04122.x)
20. Diano S, Farr SA, Benoit S, McNay EC, da Silva I, Horvath B, Gaskin FS, Nonaka N, Jaeger LB, Banks WA, et al. 2006 Ghrelin controls hippocampal spine synapse density and memory performance. Nature Neuroscience 9 381-388. (doi:10.1038/nn1656)
21. Dieguez C, & Casanueva FF 2000 Ghrelin: a step forward in the understanding of somatroph cell function and growth regulation. European Journal of Endocrinology 142 413-417. (doi:10.1530/eje.0.1420413)
22. Dixit VD, Weeraratna AT, Tang H, Bertak D, Cooper-Jenkins A, Riggins GJ, Eberhart CG, & Taub DD 2006 Ghrelin and the growth hormone secretagogue receptor constitute a novel autocrine pathway in astrocytoma motility. Journal of Biological Chemistry 24 16681-16690. (doi:10.1074/jbc.M600223200)
23. Donahue CP, Kosik KS, & Shors TJ 2006 Growth hormone is produced within the hippocampus where it responds to age, sex and stress. PNAS 103 6031-6036. (doi:10.1073/pnas.0507776103)
24. Frago LM, Pañeda C, Dickson SL, Hewson AK, Argente J, & Chowen JA 2002 Growth hormone (GH) and GH-releasing peptide-6 increase brain insulin-like growth factor-I expression and activate intracellular signaling pathways involved in neuroprotection. Endocrinology 143 4113-4122. (doi:10.1210/en.2002-220261)
25. Frago LM, Baquedano E, Argente J, & Chowen JA 2011 Neuroprotective actions of ghrelin and growth hormone secretagogues. Frontiers in Molecular Neuroscience 4 23. (doi:10.3389/fnmol.2011.00023)
26. Fraser RA, Attardo D, & Harvey S 1990 Growth hormone receptors in hypothalamic and extra-hypothalamic tissues. Journal of Molecular Endocrinology 5 231-238. (doi:10.1677/jme.0.0050231)
27. Freeman MR 2010 Specification and morphogenesis of astrocytes. Science 330 774-778. (doi:10.1126/science.1190928)
28. Galou M, Colucci-Guyon E, Ensergueix D, Ridet JL, Gimenez y Ribotta M, Privat A, Babinet C, & Dupouey P 1996 Disrupted glial fibrillary acidic protein network in astrocytes from vimentin knockout mice. Journal of Cell Biology 133 853-863. (doi:10.1083/jcb.133.4.853)
29. García-Segura LM, & McCarthy MM 2004 Minireview: role of glia in neuroendocrine function. Endocrinology 145 1082-1086. (doi:10.1210/ en.2003-1383)
30. Ghigo E, Arvat E, Giordano R, Broglio F, Gianotti L, Maccario M, Bisi G, Graziani A, Papotti M, Muccioli G, et al. 2001 Biological activities of growth hormone secretagogues in humans. Endocrine 14 87-93. (doi:10.1385/ENDO:14:1:087)
31. Ghosh M, Gharami K, Paul S, & Das S 2005 Thyroid hormone-induced morphological differentation and maturation of astrocytes involves activation of protein kinase A and ERK signaling pathway. European Journal of Neuroscience 22 1609-1617. (doi:10.1111/j.1460-9568.2005. 04351.x)
32. Gomes FCA, Paulin D, & Moura-Neto V 1999a Glial fibrilary acidic protein (GFAP): modulation by growth factors and its implication in astrocyte differentiation. Brazilian Journal of Medical and Biological Research 32 619-631. (doi:10.1590/S0100-879X1999000500016)
33. Gomes FCA, Garcia-Abreu J, Galou M, Paulin D, & Moura Neto V 1999b Neurons induce GFAP gene promoter of cultured astrocytes from transgenic mice. Glia 26 97-108. (doi:10.1002/(SICI)1098- 1136(199904)26:2!97::AID-GLIA1O3.0.CO;2-Z)
34. Gould E, Frankfurt M, Westlind-Danieldsson A, & McEwen BS 1990 Developing forebrain astrocytes are sensitive to thyroid hormone. Glia 3 283-292. (doi:10.1002/glia.440030408)
35. Harvey S, Hull KL, & Fraser RA 1993 Growth hormone: neurocrine and neuroendocrine perspectives. Growth Regulation 3 161-171.
36. Inagaki M, Gonda Y, Nishizawa K, Kitamura S, Sato C, Ando S, Tanabe K, Kikuchi K, Tsuiki S, & Nishi Y 1990 Phosphorylation sites linked to glial filament disassembly in vitro locate in a non-alpha-helical head domain. Journal of Biological Chemistry 265 4722-4729.
37. InagakiM, ImakamuraY,TakedaM,NishimuraT&InagakiN2008Glialfibrilary acidic protein: dynamic property and regulation by phosphorylation. Brain Pathology 4 239-243. (doi:10.1111/j.1750-3639.1994.tb00839.x)
38. Järlestedt K, Rousset CI, Faiz M, Wilhelmsson U, StÅhlberg A, Sourkova H, Pekna M, Mallard C, Hagberg H, & Pekny M 2010 Attenuation of reactive gliosis does not affect infarct volume in neonatal hypoxic- ischemic brain injury in mice. PLoS ONE 5 e10397. (doi:10.1371/ journal.pone.0010397)
39. Kim SW, Her SJ, Park SJ, Kim D, Park KS, Lee HK, Han BH, Kim MS, Shin CS, & Kim SY 2005 Ghrelin stimulates proliferation and differentiation and inhibits apoptosis in osteoblastic MC3T3-E1 cells. Bone 37 359-369. (doi:10.1016/j.bone.2005.04.020)
40. Kulik G, & Weber MJ 1998 Akt-dependent and independent survival signalling pathways utilized by insulin-like growth factor. Molecular and Cellular Biology 18 6711-6718.
41. Lanning NJ, & Carter-Su C 2006 Recent advances in growth hormone signalling. Reviews in Endocrine, & Metabolic Disorders 7 225-235. (doi:10.1007/s11154-007-9025-5)
42. Laping NJ, Teter B, Nichols NR, Rozovsky I, & Finch CE 1994 Glial fibrillary acidic protein: regulation by hormones, cytokines and growth factors. Brain Pathology 4 259-275. (doi:10.1111/j.1750-3639.1994.tb00841.x)
43. Le Greves M, Le Greves P, & Nyberg F 2005 Age-related effects of IGF-1 on the NMDA-, GH- and IGF-1-receptor mRNA transcript in the rat hippocampus. Brain Research Bulletin 15 369-374. (doi:10.1016/ j.brainresbull.2005.01.012)
44. Lichanska AM, & Waters MJ 2008 New insights into growth hormone receptor function and clinical implications. Hormone Research 69 138-145. (doi:10.1159/000112586)
45. Lima FRS, Trentin AG, Rosenthal D, Chagas C, & Moura Neto V 1997 Thyroid hormone induces protein secretion and morphological changes in astroglial cells with an increase in expression of glial fibrillary acidic protein. Journal of Endocrinology 154 167-175. (doi:10.1677/joe.0.1540167)
46. List EO, Sackmann-Sala L, Berryman DE, Funk K, Kelder B, Gosney ES, Okada S, Ding J, Cruz-Topete D, & Kopchick JJ 2011 Endocrine parameters and phenotypes of the growth hormone receptor gene disrupted (GHRK/K) mouse. Endocrine Reviews 32 356-386. (doi:10.1210/er.2010-0009)
47. Lobie PE, García-Aragón J, Lincoln DT, Barnard R, Wilcox JN, & Waters MJ 1993 Localization and ontogeny of growth hormone receptor gene expression in the central nervous system. Developmental Brain Research 74 225-233. (doi:10.1016/0165-3806(93)90008-X)
48. Lobie PE, Zhu T, Graichen R, & Goh ELK 2000 Growth hormone, insulinlike growth factor I and the CNS: localization, function and mechanism of action. Growth Hormone, & IGF Research 10 S51-S56. (doi:10.1016/ S1096-6374(00)80010-6)
49. Lyuh E, Kim HJ, Kim M, Lee JK, Park KS, Yoo KY, Lee KW, & Ahn YO 2007 Dose-specific or dose-dependent effect of growth hormone treatment on the proliferation and differentiation of cultured neuronal cells. Growth Hormone, & IGF Research 17 315-322. (doi:10.1016/j.ghir.2007.03.002)
50. McLenachan S, Gum M-G, Waters MJ, & Turnley AM 2009 Growth hormone promotes proliferation of adult neurosphere cultures. Growth Hormone, & IGF Research 19 212-218. (doi:10.1016/j.ghir.2008.09.003)
51. Miller DB, Bartke A, & O'Callaghan JP 1995 Increased glial fibrillary acidic protein (GFAP) levels in the brains of transgenic mice expressing the bovine growth hormone (bGH) gene. Experimental Gerontology 30 383-400. (doi:10.1016/0531-5565(94)00064-A)
52. Minami S, Kamegai J, Hasegawa O, Sugihara H, Okada K, & Wakabayashi I 2006 Expression of growth hormone receptor gene in rat hypothalamus. Journal of Neurochemistry 5 691-696.
53. Mong JA, & Blutstein T 2006 Estradiol modulation of astrocytic form and function: implication for hormonal control of synaptic communication. Neuroscience 138 967-975. (doi:10.1016/j.neuroscience.2005. 10.017)
54. Muccioli G, Baragli A, Granata A, Papotti M, & Ghigho E 2007 Heterogeneity of ghrelin/growth hormone secretagogue receptors. Neuroendocrinology 86 147-164. (doi:10.1159/000105141)
55. Mucha S, & Stepien H 2002 Modulation of ghrelin axis influences the growth of colonic and prostatic cancer cells in vitro. Pharmacological Reports 64 951-959.
56. Mukhina S, Mertani HC, Guo K, Lee KO, Gluckman PD, & Lobie PE 2004 Phenotypic conversion of human mammary carcinoma cells by autocrine human growth hormone. PNAS 101 15166-15171. (doi:10.1073/pnas.0405881101)
57. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, & Matsukura S 2001 A role for ghrelin in the central regulation of feeding. Nature 409 194-198. (doi:10.1038/35051587)
58. Nyberg F 2000 Growth hormone in the brain: characteristics of specific brain targets for the hormone and their functional significance. Frontiers in Neuroendocrinology 21 330-348. (doi:10.1006/frne.2000. 0200)
59. Pascual M, & Guerri C 2007 The peptide NAP promotes neuronal growth and differentiation through extracellular signal-regulated protein kinase and Akt pathways, and protects neurons co-cultured with astrocytes damaged by ethanol. Journal of Neurochemistry 103 557-568. (doi:10.1111/j.1471-4159.2007.04761.x)
60. Perea G, & Araque A 2005 Synaptic regulation of the astrocyte calcium signal. Journal of Neural Transmission 112 127-135. (doi:10.1007/ s00702-004-0170-7)
61. Petersen PS, Woldbye DP, Madsen AN, Egerod KL, Jin C, Lang M, & Holst B 2009 In vivo characterization of high basal signalling from the ghrelin receptor. Endocrinology 150 4920-4930. (doi:10.1210/en.2008-1638)
62. Petersenn S 2002 Structure and regulation of the growth hormone secretagogue receptor. Minerva Endocrinologica 27 243-256.
63. Pettersson I, Muccioli G, Granata R, Deghenghi R, Ghigo E, Ohlsson C, & Isgaard J 2002 Natural (ghrelin) and synthetic (hexalerin) GH secretagogues stimulate H9c2 cardiomyocyte cell proliferation. Journal of Endocrinology 175 201-209. (doi:10.1677/joe.0.1750201)
64. Reilly JF, Maher PA, & Kumari VG 1998 Regulation of astrocyte GFAP expression by TGF-b1 and FGF-2. Glia 22 202-210. (doi:10.1002/ (SICI)1098-1136(199802)22:2!202::AID-GLIA11O3.0.CO;2-1)
65. Rossi F, Castelli A, Bianco MJ, Bertone C, Brama M, & Santiemma V 2009 Ghrelin inhibits contraction and proliferation of human aortic smooth muscle cells by cAMP/PKA pathway activation. Atherosclerosis 203 97-104. (doi:10.1016/j.atherosclerosis.2008.06.015)
66. Scheepens A, Sirimanne E, Beilharz E, Breier BH, Waters MJ, Gluckman PD, & Williams CE 1999 Alterations in the neural growth hormone axis following hypoxic-ischemic brain injury. Molecular Brain Research 68 88-110. (doi:10.1016/S0169-328X(99)00051-0)
67. Sousa V de O, Romao L, Neto VM, & Gomes FC 2004 Glial fibrillary acidic protein gene promoter is differently modulated by transforming growth factor-b1 in astrocytes from distinct brain regions. European Journal of Neuroscience 19 1721-1730. (doi:10.1111/j.1460-9568.2004. 03249.x)
68. Stoving RK, Veldhuis JD, Flyvgjerg A, Vinten J, Hangaard J, Koldjaer OG, Kristiansen J, & Hagen C 1999 Jointly amplified basal and pulsatile growth hormone secretion and increased process irregularity in women within the GH-insulin-like growth factor I axis. Journal of Clinical Endocrinology and Metabolism 84 2056-2063. (doi:10.1210/ jc.84.6.2056)
69. Sullivan SM, Sullivan RKP, Miller SM, Ireland Z, Björkman T, Pow DV, & Colditz PB 2012 Phosphorylation of GFAP is associated with injury in the neonatal pig hypoxic-ischemic brain. Neurochemical Research 37 2364-2378. (doi:10.1007/s11064-012-0774-5)
70. Takemura M, Gomi H, Colucci-Guyon E, & Itohara S 2002 Protective role of phosphorylation in turnover of glial fibrillary acidic protein in mice. Journal of Neuroscience 22 6972-6979.
71. Thompson NM, Davies JS, Mode A, Houston PA, & Wells T 2003 Patterndependent suppression of growth hormone (GH) pulsatility by ghrelin and GH-releasing peptide-6 in moderately GH-deficient rats. Endocrinology 144 4859-4867. (doi:10.1210/en.2003-0423)
72. Thompson NM, Gill DAS, Davies R, Loveridge N, Houston PA, Robinson LCAF, & Wells T 2004 Ghrelin and des-octanoyl ghrelin promote adipogenesis directly in vivo by a mechanism independent of the type 1a growth hormone secretagogue receptor. Endocrinology 145 234-242. (doi:10.1210/en.2003-0899)
73. Torres-Aleman I, Rejas MT, Pons S, & Garcica-Segura LM 1992 Estradiol promotes cell shape changes and glial fibrillary acidic protein redistribution in hypothalamic astrocytes in vitro: a neuronal-mediated effect. Glia 6 180-187. (doi:10.1002/glia.440060305)
74. Yarwood SJ, Kilgour E, & Anderson NG 1998 Cyclic AMP potentiates growth hormone-dependent differentiation of 3T3-F442A preadipocytes: possible involvement of the transcription factor CREB. Molecular and Cellular Endocrinology 138 41. (doi:10.1016/S0303-7207(98)00049-5)
75. Zhu T, Goh EL, Graichen R, Ling L, & Lobie PE 2001 Signal transduction via the growth hormone receptor. Cellular Signalling 13 599-616. (doi:10.1016/S0898-6568(01)00186-3)
76. Zigman JM, Jones JE, Lee CE, Saper CB, & Elmquist JK 2006 Expression of ghrelin receptor mRNA in the rat and the mouse brain. Journal of Comparative Neurology 494 528-548. (doi:10.1002/cne.20823)