Growth hormone receptor immunoreactivity is increased in the subventricular zone of juvenile rat brain after focal ischemia: A potential role for growth hormone in injury-induced neurogenesis

Growth Hormone and IGF Research

Volumn 19, Issue 6, 2009, Pages 497-506

  Christophidis, Larissa Joy ^a,b   Gorba, Thorsten ^a   Gustavsson, Malin ^a   Williams, Chris Edward ^a   Werther, George Arthur ^b,c   Russo, Vincenzo Carlo ^b,c   Scheepens, Arjan ^d  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b ROYAL CHILDREN'S HOSPITAL   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

Author keywords

Brain; Growth hormone; Hypoxia; Ischemia; Neural stem cell; Neurogenesis

Indexed keywords

BROXURIDINE; DOUBLECORTIN; GROWTH HORMONE; GROWTH HORMONE RECEPTOR; KI 67 ANTIGEN; NESTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FEMALE; JUVENILE ANIMAL; MALE; MOUSE; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SUBVENTRICULAR ZONE;

ANIMALS; ANOXIA; BRAIN; BRAIN INJURIES; BRAIN ISCHEMIA; CELL PROLIFERATION; EMBRYONIC STEM CELLS; GROWTH HORMONE; ISCHEMIA; MICE; NEUROGENESIS; NEURONS; RATS; RATS, WISTAR; RECEPTORS, SOMATOTROPIN;

EID: 72049122655     PISSN: 10966374     EISSN: 15322238     Source Type: Journal    
DOI: 10.1016/j.ghir.2009.05.001     Document Type: Article

References (62)

1. Zhao C., Deng W., and Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 132 (2008) 645-660
2. Parent J.M. Injury-induced neurogenesis in the adult mammalian brain. Neuroscientist 9 (2003) 261-272
3. Jin K., Wang X., Xie L., et al. Evidence for stroke-induced neurogenesis in the human brain. Proc. Natl. Acad. Sci. USA 103 (2006) 13198-13202
4. Arvidsson A., Collin T., Kirik D., Kokaia Z., and Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8 (2002) 963-970
5. Parent J.M., Vexler Z.S., Gong C., Derugin N., and Ferriero D.M. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52 (2002) 802-813
6. Thored P., Arvidsson A., Cacci E., et al. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24 (2006) 739-747
7. Yamashita T., Ninomiya M., Hernandez Acosta P., et al. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J. Neurosci. 26 (2006) 6627-6636
8. Wiltrout C., Lang B., Yan Y., Dempsey R.J., and Vemuganti R. Repairing brain after stroke: a review on post-ischemic neurogenesis. Neurochem. Int. 50 (2007) 1028-1041
9. Dempsey R.J., and Kalluri H.S. Ischemia-induced neurogenesis: role of growth factors. Neurosurg. Clin. N. Am. 18 (2007) 183-190
10. Greenberg D.A., and Jin K. Growth factors and stroke. NeuroRx 3 (2006) 458-465
11. Scheepens A., Sirimanne E., Beilharz E., et al. Alterations in the neural growth hormone axis following hypoxic-ischemic brain injury. Brain Res. Mol. Brain Res. 68 (1999) 88-100
12. Scheepens A., Sirimanne E.S., Breier B.H., Clark R.G., Gluckman P.D., and Williams C.E. Growth hormone as a neuronal rescue factor during recovery from CNS injury. Neuroscience 104 (2001) 677-687
13. Möderscheim T.A., Christophidis L.J., Williams C.E., and Scheepens A. Distinct neuronal growth hormone receptor ligand specificity in the rat brain. Brain Res. 1137 (2007) 29-34
14. Shin D.H., Lee E., Kim J.W., et al. Protective effect of growth hormone on neuronal apoptosis after hypoxia-ischemia in the neonatal rat brain. Neurosci. Lett. 354 (2004) 64-68
15. Gustafson K., Hagberg H., Bengtsson B.A., Brantsing C., and Isgaard J. Possible protective role of growth hormone in hypoxia-ischemia in neonatal rats. Pediatr. Res. 45 (1999) 318-323
16. García-Aragón J., Lobie P.E., Muscat G.E., Gobius K.S., Norstedt G., and Waters M.J. Prenatal expression of the growth hormone (GH) receptor/binding protein in the rat: a role for GH in embryonic and fetal development?. Development 114 (1992) 869-876
17. Turnley A.M., Faux C.H., Rietze R.L., Coonan J.R., and Bartlett P.F. Suppressor of cytokine signaling 2 regulates neuronal differentiation by inhibiting growth hormone signaling. Nat. Neurosci. 5 (2002) 1155-1162
18. Lobie P.E., García-Aragón J., Lincoln D.T., Barnard R., Wilcox J.N., and Waters M.J. Localization and ontogeny of growth hormone receptor gene expression in the central nervous system. Brain Res. Dev. Brain Res. 74 (1993) 225-233
19. Donahue C.P., Jensen R.V., Ochiishi T., et al. Transcriptional profiling reveals regulated genes in the hippocampus during memory formation. Hippocampus 12 (2002) 821-833
20. Donahue C.P., Kosik K.S., and Shors T.J. Growth hormone is produced within the hippocampus where it responds to age, sex, and stress. Proc. Natl. Acad. Sci. USA 103 (2006) 6031-6036
21. Sun L.Y., Evans M.S., Hsieh J., Panici J., and Bartke A. Increased neurogenesis in dentate gyrus of long-lived Ames dwarf mice. Endocrinology 146 (2005) 1138-1144
22. Sun L.Y., Al-Regaiey K., Masternak M.M., Wang J., and Bartke A. Local expression of GH and IGF-1 in the hippocampus of GH-deficient long-lived mice. Neurobiol. Aging 26 (2005) 929-937
23. Sun L.Y., and Bartke A. Adult neurogenesis in the hippocampus of long-lived mice during aging. J. Gerontol. A - Biol. Sci. Med. Sci. 62 (2007) 117-125
24. Lichtenwalner R.J., Forbes M.E., Sonntag W.E., and Riddle D.R. Adult-onset deficiency in growth hormone and insulin-like growth factor-I decreases survival of dentate granule neurons: insights into the regulation of adult hippocampal neurogenesis. J. Neurosci. Res. 83 (2006) 199-210
25. Ajo R., Cacicedo L., Navarro C., and Sanchez-Franco F. Growth hormone action on proliferation and differentiation of cerebral cortical cells from fetal rat. Endocrinology 144 (2003) 1086-1097
26. Byts N., Samoylenko A., Fasshauer T., et al. Essential role for Stat5 in the neurotrophic but not in the neuroprotective effect of erythropoietin. Cell Death Differ. 15 (2008) 783-792
27. Sirimanne E.S., Guan J., Williams C.E., and Gluckman P.D. Two models for determining the mechanisms of damage and repair after hypoxic-ischaemic injury in the developing rat brain. J. Neurosci. Meth. 55 (1994) 7-14
28. Möderscheim T.A., Gorba T., Pathipati P., et al. Prolactin is involved in glial responses following a focal injury to the juvenile rat brain. Neuroscience 145 (2007) 963-973
29. Beilharz E.J., Russo V.C., Butler G., et al. Co-ordinated and cellular specific induction of the components of the IGF/IGFBP axis in the rat brain following hypoxic-ischemic injury. Brain Res. Mol. Brain Res. 59 (1998) 119-134
30. Beilharz E.J., Bassett N.S., Sirimanne E.S., Williams C.E., and Gluckman P.D. Insulin-like growth factor II is induced during wound repair following hypoxic-ischemic injury in the developing rat brain. Brain Res. Mol. Brain Res. 29 (1995) 81-91
31. Russo V., and Werther G.A. Growth hormone and insulin-like growth factors in the central nervous system: localization in mammalian species. In: Nyberg F. (Ed). The Somatotrophic Axis in Brain Function (2005), Elsevier Academic Press, Amsterdam 81-90
32. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates - The New Coronal Set. fifth ed. (2005), Elsevier Academic Press, San Diego 209pp
33. Ilkbahar Y.N., Thordarson G., Camarillo I.G., and Talamantes F. Differential expression of the growth hormone receptor and growth hormone-binding protein in epithelia and stroma of the mouse mammary gland at various physiological stages. J. Endocrinol. 161 (1999) 77-87
34. Rasband W.S. ImageJ (1997-2006), US National Institutes of Health, Bethesda, MA, USA
35. Gritti A., Galli R., and Vescovi A.L. Cultures of stem cells of the central nervous system. In: Fedoroff S., and Richardson A. (Eds). Protocols for Neural Cell Culture (2001), Humana Press Inc., Totawa, New Jersey 173-197
36. Gorba T., Bradoo P., Antonic A., et al. Neural regeneration protein is a novel chemoattractive and neuronal survival-promoting factor. Exp. Cell Res. 312 (2006) 3060-3074
37. Plane J.M., Liu R., Wang T.W., Silverstein F.S., and Parent J.M. Neonatal hypoxic-ischemic injury increases forebrain subventricular zone neurogenesis in the mouse. Neurobiol. Dis. 16 (2004) 585-595
38. Zhang R., Zhang Z., Zhang C., et al. Stroke transiently increases subventricular zone cell division from asymmetric to symmetric and increases neuronal differentiation in the adult rat. J. Neurosci. 24 (2004) 5810-5815
39. Ong J., Plane J.M., Parent J.M., and Silverstein F.S. Hypoxic-ischemic injury stimulates subventricular zone proliferation and neurogenesis in the neonatal rat. Pediatr. Res. 58 (2005) 600-606
40. Brazel C.Y., Rosti III R.T., Boyce S., Rothstein R.P., and Levison S.W. Perinatal hypoxia/ischemia damages and depletes progenitors from the mouse subventricular zone. Dev. Neurosci. 26 (2004) 266-274
41. Romanko M.J., Rothstein R.P., and Levison S.W. Neural stem cells in the subventricular zone are resilient to hypoxia/ischemia whereas progenitors are vulnerable. J. Cerebr. Blood Flow Metab. 24 (2004) 814-825
42. Levison S.W., Rothstein R.P., Romanko M.J., Snyder M.J., Meyers R.L., and Vannucci S.J. Hypoxia/ischemia depletes the rat perinatal subventricular zone of oligodendrocyte progenitors and neural stem cells. Dev. Neurosci. 23 (2001) 234-247
43. Rao M.S., and Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur. J. Neurosci. 19 (2004) 234-246
44. Couillard-Despres S., Winner B., Schaubeck S., et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21 (2005) 1-14
45. Yang Z., Covey M.V., Bitel C.L., Ni L., Jonakait G.M., and Levison S.W. Sustained neocortical neurogenesis after neonatal hypoxic/ischemic injury. Ann. Neurol. 61 (2007) 199-208
46. Modanlou H.D., Gharraee Z., Hasan J., Waltzman J., Nageotte S., and Beharry K.D. Ontogeny of VEGF, IGF-I, and GH in neonatal rat serum, vitreous fluid, and retina from birth to weaning. Invest. Ophthalmol. Vis. Sci. 47 (2006) 738-744
47. Berry Jr. W.D., Moriarty C.M., and Lau Y.S. Lead attenuation of episodic growth hormone secretion in male rats. Int. J. Toxicol. 21 (2002) 93-98
48. Martin J.B., Durand D., Gurd W., Faille G., Audet J., and Brazeau P. Neuropharmacological regulation of episodic growth hormone and prolactin secretion in the rat. Endocrinology 102 (1978) 106-113
49. Lyuh E., Kim H.J., Kim M., et al. Dose-specific or dose-dependent effect of growth hormone treatment on the proliferation and differentiation of cultured neuronal cells. Growth Horm. IGF Res. 17 (2007) 315-322
50. Russo V.C., Gluckman P.D., Feldman E.L., and Werther G.A. The insulin-like growth factor system and its pleiotropic functions in brain. Endocr. Rev. 26 (2005) 916-943
51. Johansson G.S., and Arnqvist H.J. Insulin and IGF-I action on insulin receptors, IGF-I receptors, and hybrid insulin/IGF-I receptors in vascular smooth muscle cells. Am. J. Physiol. Endocrinol. Metab. 291 (2006) E1124-E1130
52. Li G., Barrett E.J., Wang H., Chai W., and Liu Z. Insulin at physiological concentrations selectively activates insulin but not insulin-like growth factor I (IGF-I) or insulin/IGF-I hybrid receptors in endothelial cells. Endocrinology 146 (2005) 4690-4696
53. Entingh-Pearsall A., and Kahn C.R. Differential roles of the insulin and insulin-like growth factor-I (IGF-I) receptors in response to insulin and IGF-I. J. Biol. Chem. 279 (2004) 38016-38024
54. Ranke M.B., Stanley C.A., Tenore A., Rodbard D., Bongiovanni A.M., and Parks J.S. Characterization of somatogenic and lactogenic binding sites in isolated rat hepatocytes. Endocrinology 99 (1976) 1033-1045
55. Sugino N., Telleria C.M., Tessier C., and Gibori G. Regulation and role of the insulin-like growth factor I system in rat luteal cells. J. Reprod. Fertil. 115 (1999) 349-355
56. Murphy L.J., Tachibana K., and Friesen H.G. Stimulation of hepatic insulin-like growth factor-I gene expression by ovine prolactin: evidence for intrinsic somatogenic activity in the rat. Endocrinology 122 (1988) 2027-2033
57. Shingo T., Gregg C., Enwere E., et al. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299 (2003) 117-120
58. Silva C., Zhang K., Tsutsui S., Holden J.K., Gill M.J., and Power C. Growth hormone prevents human immunodeficiency virus-induced neuronal p53 expression. Ann. Neurol. 54 (2003) 605-614
59. van Marle G., Antony J.M., Silva C., Sullivan A., and Power C. Aberrant cortical neurogenesis in a pediatric neuroAIDS model: neurotrophic effects of growth hormone. AIDS 19 (2005) 1781-1791
60. McLenachan S., Lum M.G., Waters M.J., and Turnley A.M. Growth hormone promotes proliferation of adult neurosphere cultures. Growth Horm. IGF Res. 19 (2009) 212-218
61. Scott H.J., Stebbing M.J., Walters C.E., et al. Differential effects of SOCS2 on neuronal differentiation and morphology. Brain Res. 1067 (2006) 138-145
62. Pan W., Yu Y., Cain C.M., Nyberg F., Couraud P.O., and Kastin A.J. Permeation of growth hormone across the blood-brain barrier. Endocrinology 146 (2005) 4898-4904