Neuronal protection from glucose deprivation via modulation of glucose transport and inhibition of apoptosis: A role for the insulin-like growth factor system

Brain Research

Volumn 1009, Issue 1-2, 2004, Pages 40-53

  Russo, V C ^a,b   Kobayashi, K ^a   Najdovska, S ^a   Baker, N L ^b   Werther, G A ^a,b  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Bcl 2, cell death, apoptosis; Development and regeneration; Diabetes, glucopenia; Glucose transport, GLUT1; Insulin like growth factor system, IGF I; Neuroblastoma cell, neuronal cell; Neuroprotection; Neurotrophic factors: biological effects

Indexed keywords

FAS ANTIGEN; GLUCOSE; GLUCOSE TRANSPORTER 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; PROTEIN BCL 2; RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; BRAIN INJURY; BRAIN MITOCHONDRION; CELL GROWTH; CELL LOSS; CELL MEMBRANE; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE TRANSLOCATION; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; HYPOGLYCEMIA; NERVE CELL LESION; NEUROBLASTOMA CELL; NEUROPROTECTION; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; APOPTOSIS; BIOLOGICAL TRANSPORT; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL COUNT; CELL DIVISION; CELL LINE, TUMOR; CELL SURVIVAL; CULTURE MEDIA, SERUM-FREE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; INSULIN-LIKE GROWTH FACTOR I; IODINE ISOTOPES; MITOCHONDRIA; MONOSACCHARIDE TRANSPORT PROTEINS; NEUROBLASTOMA; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSLOCATION, GENETIC;

EID: 2142697164     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.02.042     Document Type: Article

References (81)

1. Abcouwer S.F., Schwarz C., Meguid R.A. Glutamine deprivation induces the expression of GADD45 and GADD153 primarily by mRNA stabilization. J. Biol. Chem. 274:1999;28645-28651
2. Aller C.B., Ehmann S., Gilman-Sachs A., Snyder A.K. Flow cytometric analysis of glucose transport by rat brain cells. Cytometry. 27:1997;262-268
3. Asada T., Ogawa T., Iwai M., Shimomura K., Kobayashi M. Recombinant insulin-like growth factor I normalizes expression of renal glucose transporters in diabetic rats. Am. J. Physiol. 273:1997;F27-F37
4. Baker N.L., Russo V.C., Bernard O., D'Ercole A.J., Werther G.A. Interactions between bcl-2 and the IGF system control apoptosis in the developing mouse brain. Brain Res. Dev. Brain Res. 118:1999;109-118
5. Barthel A., Okino S.T., Liao J., Nakatani K., Li J., Whitlock J.P. Jr., Roth R.A. Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1. J. Biol. Chem. 274:1999;20281-20286
6. Baserga R., Hongo A., Rubini M., Prisco M., Valentinis B. The IGF-I receptor in cell growth, transformation and apoptosis. Biochim. Biophys. Acta. 1332:1997;F105-F126
7. Beilharz E.J., Russo V.C., Butler G., Baker N.L., Connor B., Sirimanne E.S., Dragunow M., Werther G.A., Gluckman P.D., Williams C.E., Scheepens A. Co-ordinated and cellular specific induction of the components of the IGF / IGFBP axis in the rat brain following hypoxic-ischemic injury. Brain Res. 59:1998;119-134
8. Bilan P.J., Mitsumoto Y., Ramlal T., Klip A. Acute and long-term effects of insulin-like growth factor I on glucose transporters in muscle cells. Translocation and biosynthesis. FEBS Lett. 298:1992;285-290
9. Boado R.J. Amplification of blood-brain barrier GLUT1 glucose transporter gene expression by brain-derived peptides. Neurosci. Res. 40:2001;337-342
10. Boado R.J., Pardridge W.M. Glucose deprivation causes posttranscriptional enhancement of brain capillary endothelial glucose transporter gene expression via GLUT1 mRNA stabilization. J. Neurochem. 60:1993;2290-2296
11. Bondy C.A., Cheng C.M. Insulin-like growth factor-1 promotes neuronal glucose utilization during brain development and repair processes. Int. Rev. Neurobiol. 51:2002;189-217
12. Bruckner B.A., Ammini C.V., Otal M.P., Raizada M.K., Stacpoole P.W. Regulation of brain glucose transporters by glucose and oxygen deprivation. Metabolism. 48:1999;422-431
13. Cheng C.M., Reinhardt R.R., Lee W.H., Joncas G., Patel S.C., Bondy C.A. Insulin-like growth factor 1 regulates developing brain glucose metabolism. Proc. Natl. Acad. Sci. U. S. A. 97:2000;10236-10241
14. Chrysis D., Calikoglu A.S., Ye P., D'Ercole A.J. Insulin-like growth factor-I overexpression attenuates cerebellar apoptosis by altering the expression of Bcl family proteins in a developmentally specific manner. J. Neurosci. 21:2001;1481-1489
15. Costantini P., Bruey J.M., Castedo M., Metivier D., Loeffler M., Susin S.A., Ravagnan L., Zamzami N., Garrido C., Kroemer G. Pre-processed caspase-9 contained in mitochondria participates in apoptosis. Cell Death Differ. 9:2002;82-88
16. DeBosch B.J., Baur E., Deo B.K., Hiraoka M., Kumagai A.K. Effects of insulin-like growth factor-1 on retinal endothelial cell glucose transport and proliferation. J. Neurochem. 77:2001;1157-1167
17. DeBosch B.J., Deo B.K., Kumagai A.K. Insulin-like growth factor-1 effects on bovine retinal endothelial cell glucose transport: role of MAP kinase. J. Neurochem. 81:2002;728-734
18. D'Ercole A.J., Ye P., Calikoglu A.S., Gutierrez-Ospina G. The role of the insulin-like growth factors in the central nervous system. [Review 190 refs.] Mol. Neurobiol. 13:1996;227-255
19. Diabetes Control and Complications Trial (DCCT): results of feasibility study. The DCCT Research Group. Diabetes Care. 10:1987;1-19
20. Duelli R., Staudt R., Duembgen L., Kuschinsky W. Increase in glucose transporter densities of Glut3 and decrease of glucose utilization in rat brain after one week of hypoglycemia. Brain Res. 831:1999;254-262
21. Dwyer K.J., Pardridge W.M. Developmental modulation of blood-brain barrier and choroid plexus GLUT1 glucose transporter messenger ribonucleic acid and immunoreactive protein in rabbits. Endocrinology. 132:1993;558-565
22. Dwyer K.J., Boado R.J., Pardridge W.M. Cis-element/cytoplasmic protein interaction within the 3′-untranslated region of the GLUT1 glucose transporter mRNA. J. Neurochem. 66:1996;449-458
23. Dwyer D.S., Vannucci S.J., Simpson I.A. Expression, regulation, and functional role of glucose transporters (GLUTs) in brain. Int. Rev. Neurobiol. 51:2002;159-188
24. Farlie P.G., Dringen R., Rees S.M., Kannourakis G., Bernard O. bcl-2 transgene expression can protect neurons against developmental and induced cell death. Proc. Natl. Acad. Sci. U. S. A. 92:1995;4397-4401
25. Federici M., Hribal M., Perego L., Ranalli M., Caradonna Z., Perego C., Usellini L., Nano R., Bonini P., Bertuzzi F., Marlier L.N., Davalli A.M., Carandente O., Pontiroli A.E., Melino G., Marchetti P., Lauro R., Sesti G., Folli F. High glucose causes apoptosis in cultured human pancreatic islets of Langerhans: a potential role for regulation of specific Bcl family genes toward an apoptotic cell death program. Diabetes. 50:2001;1290-1301
26. Fiordaliso F., Leri A., Cesselli D., Limana F., Safai B., Nadal-Ginard B., Anversa P., Kajstura J. Hyperglycemia activates p53 and p53-regulated genes leading to myocyte cell death. Diabetes. 50:2001;2363-2375
27. Fladeby C., Bjonness B., Serck-Hanssen G. GLUT1-mediated glucose transport and its regulation by IGF-I in cultured bovine chromaffin cells. J. Cell. Physiol. 169:1996;242-247
28. Fladeby C., Skar R., Serck-Hanssen G. Distinct regulation of glucose transport and GLUT1/GLUT3 transporters by glucose deprivation and IGF-I in chromaffin cells. Biochim. Biophys. Acta. 1593:2003;201-208
29. Gallaher B.W., Hille R., Raile K., Kiess W. Apoptosis: live or die-hard work either way! Horm. Metab. Res. 33:2001;511-519
30. Guan J., Williams C.E., Skinner S.J., Mallard E.C., Gluckman P.D. The effects of insulin-like growth factor (IGF)-1, IGF-2, and des-IGF-1 on neuronal loss after hypoxic-ischemic brain injury in adult rats: evidence for a role for IGF binding proteins. Endocrinology. 137:1996;893-898
31. Hansen M.B., Nielsen S.E., Berg K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods. 119:1989;203-210
32. Heck S., Lezoualc'h F., Engert S., Behl C. Insulin-like growth factor-1-mediated neuroprotection against oxidative stress is associated with activation of nuclear factor kappaB. J. Biol. Chem. 274:1999;9828-9835
33. Hueber A.O., Zornig M., Lyon D., Suda T., Nagata S., Evan G.I. Requirement for the CD95 receptor-ligand pathway in c-Myc-induced apoptosis [see comments]. Science. 278:1997;1305-1309
34. Hurtado O., Lizasoain I., Fernandez-Tome P., Alvarez-Barrientos A., Leza J.C., Lorenzo P., Moro M.A. TACE/ADAM17-TNF-alpha pathway in rat cortical cultures after exposure to oxygen-glucose deprivation or glutamate. J. Cereb. Blood Flow Metab. 22:2002;576-585
35. Janet T., Ludecke G., Otten U., Unsicker K. Heterogeneity of human neuroblastoma cell lines in their proliferative responses to basic FGF, NGF, and EGF: correlation with expression of growth factors and growth factor receptors. J. Neurosci. Res. 40:1995;707-715
36. Jung Y., Miura M., Yuan J. Suppression of interleukin-1 beta-converting enzyme-mediated cell death by insulin-like growth factor. J. Biol. Chem. 271:1996;5112-5117
37. Kim B., Leventhal P.S., Saltiel A.R., Feldman E.L. Insulin-like growth factor-I-mediated neurite outgrowth in vitro requires mitogen-activated protein kinase activation. J. Biol. Chem. 272:1997;21268-21273
38. Klip A., Tsakiridis T., Marette A., Ortiz P.A. Regulation of expression of glucose transporters by glucose: a review of studies in vivo and in cell cultures. FASEB J. 8:1994;43-53
39. Lee D.H., Chung M.Y., Lee J.U., Kang D.G., Paek Y.W. Changes of glucose transporters in the cerebral adaptation to hypoglycemia. Diabetes Res. Clin. Pract. 47(1):2000 (Jan.);15-23
40. Leventhal P.S., Randolph A.E., Vesbit T.E., Schenone A., Windebank A., Feldman E.L. Insulin-like growth factor-II as a paracrine growth factor in human neuroblastoma cells. Exp. Cell Res. 221:1995;179-186
41. Leventhal P.S., Russel J.W., Feldman E.L. IGF and the nervous system. Rosenfeld R.G., Roberts C.T.J. The IGF System. 1999;425-455 Human Press, Totowa, NJ
42. Linseman D.A., McClure M.L., Bouchard R.J., Laessig T.A., Ahmadi F.A., Heidenreich K.A. Suppression of death receptor signaling in cerebellar purkinje neurons protects neighboring granule neurons from apoptosis via an insulin-like growth factor-I dependent mechanism. J. Biol. Chem. 8:2002;24546-24553
43. Maedler K., Spinas G.A., Lehmann R., Sergeev P., Weber M., Fontana A., Kaiser N., Donath M.Y. Glucose induces beta-cell apoptosis via upregulation of the Fas receptor in human islets. Diabetes. 50:2001;1683-1690
44. Maher F., Harrison L.C. Stabilization of glucose transporter mRNA by insulin/IGF-1 and glucose deprivation. Biochem. Biophys. Res. Commun. 171:1990;210-215
45. Malhotra R., Lin Z., Vincenz C., Brosius F.C. 3rd Hypoxia induces apoptosis via two independent pathways in Jurkat cells: differential regulation by glucose. Am. J. Physiol., Cell Physiol. 281:2001;C1596-C1603
46. Matthews C.C., Feldman E.L. Insulin-like growth factor I rescues SH-SY5Y human neuroblastoma cells from hyperosmotic induced programmed cell death. J. Cell. Physiol. 166:1996;323-331
47. McGowan K.M., Police S., Winslow J.B., Pekala P.H. Tumor necrosis factor-alpha regulation of glucose transporter (GLUT1) mRNA turnover. Contribution of the 3′-untranslated region of the GLUT1 message. J. Biol. Chem. 272:1997;1331-1337
48. Meyer G.E., Shelden E., Kim B., Feldman E.L. Insulin-like growth factor I stimulates motility in human neuroblastoma cells. Oncogene. 20:2001;7542-7550
49. Moley K.H., Mueckler M.M. Glucose transport and apoptosis. Apoptosis. 5:2000;99-105
50. Mooradian A.D. Pathophysiology of central nervous system complications in diabetes mellitus. Clin. Neurosci. 4:1997;322-326
51. Nakamura M., Raghupathi R., Merry D.E., Scherbel U., Saatman K.E., McIntosh T.K. Overexpression of Bcl-2 is neuroprotective after experimental brain injury in transgenic mice. J. Comp. Neurol. 412:1999;681-692
52. Newcomb-Fernandez J.K., Zhao X., Pike B.R., Wang K.K., Kampfl A., Beer R., DeFord S.M., Hayes R.L. Concurrent assessment of calpain and caspase-3 activation after oxygen-glucose deprivation in primary septo-hippocampal cultures. J. Cereb. Blood Flow Metab. 21:2001;1281-1294
53. Ngarmukos C., Baur E.L., Kumagai A.K. Co-localization of GLUT1 and GLUT4 in the blood-brain barrier of the rat ventromedial hypothalamus. Brain Res. 900:2001;1-8
54. Northam E.A., Anderson P.J., Werther G.A., Warne G.L., Adler R.G., Andrewes D. Neuropsychological complications of IDDM in children 2 years after disease onset. Diabetes Care. 21:1998;379-384
55. Northam E.A., Anderson P.J., Jacobs R., Hughes M., Warne G.L., Werther G.A. Neuropsychological profiles of children with type 1 diabetes 6 years after disease onset. Diabetes Care. 24:2001;1541-1546
56. Parrizas M., Saltiel A.R., LeRoith D. Insulin-like growth factor I inhibits apoptosis using the phosphatidylinositol 3′-kinase and mitogen-activated protein kinase pathways. J. Biol. Chem. 272:1997;154-161
57. Peruzzi F., Prisco M., Dews M., Salomoni P., Grassilli E., Romano G., Calabretta B., Baserga R. Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol. Cell. Biol. 19:1999;7203-7215
58. Peruzzi F., Prisco M., Morrione A., Valentinis B., Baserga R. Anti-apoptotic signaling of the insulin-like growth factor-I receptor through mitochondrial translocation of c-Raf and Nedd4. J. Biol. Chem. 276:2001;25990-25996
59. Rovet J.F., Ehrlich R.M., Hoppe M. Intellectual deficits associated with early onset of insulin-dependent diabetes mellitus in children. Diabetes Care. 10:1987;510-515
60. Russell J.W., Windebank A.J., Schenone A., Feldman E.L. Insulin-like growth factor-I prevents apoptosis in neurons after nerve growth factor withdrawal. J. Neurobiol. 36:1998;455-467
61. Russo V.C., Cheesman H., Werther G.A. Organ culture: an in vitro system for the sustained growth of neonatal olfactory bulb. Neurosci. Prot. 3:1994;1-11
62. Russo V.C., Bach L.A., Fosang A.J., Baker N.L., Werther G.A. Insulin-like growth factor binding protein-2 binds to cell surface proteoglycans in the rat brain olfactory bulb. Endocrinology. 138:1997;4858-4867
63. Russo V.C., Rekaris G., Baker N.L., Bach L.A., Werther G.A. Basic fibroblast growth factor induces proteolysis of secreted and cell membrane-associated insulin-like growth factor binding protein-2 in human neuroblastoma cells. Endocrinology. 140:1999;3082-3090
64. Saeki M., Maeda S., Wada K., Kamisaki Y. Insulin-like growth factor-1 protects peroxynitrite-induced cell death by preventing cytochrome c-induced caspase-3 activation. J. Cell. Biochem. 84:2002;708-716
65. Sharif S., Arreaza G.A., Zucker P., Mi Q.S., Sondhi J., Naidenko O.V., Kronenberg M., Koezuka Y., Delovitch T.L., Gombert J.M., Leite-De-Moraes M., Gouarin C., Zhu R., Hameg A., Nakayama T., Taniguchi M., Lepault F., Lehuen A., Bach J.F., Herbelin A. Activation of natural killer T cells by alpha-galactosylceramide treatment prevents the onset and recurrence of autoimmune Type 1 diabetes. Nat. Med. 7:2001;1057-1062
66. Singh G., Lakkis C.L., Laucirica R., Epner D.E. Regulation of prostate cancer cell division by glucose. J. Cell. Physiol. 180:1999;431-438
67. Singleton J.R., Dixit V.M., Feldman E.L. Type I insulin-like growth factor receptor activation regulates apoptotic proteins. J. Biol. Chem. 271:1996;31791-31794
68. Singleton J.R., Randolph A.E., Feldman E.L. Insulin-like growth factor I receptor prevents apoptosis and enhances neuroblastoma tumorigenesis. Cancer Res. 56:1996;4522-4529
69. Tafuri S.R. Troglitazone enhances differentiation, basal glucose uptake, and Glut1 protein levels in 3T3-L1 adipocytes. Endocrinology. 137:1996;4706-4712
70. Taha C., Liu Z., Jin J., Al-Hasani H., Sonenberg N., Klip A. Opposite translational control of GLUT1 and GLUT4 glucose transporter mRNAs in response to insulin. Role of mammalian target of rapamycin, protein kinase b, and phosphatidylinositol 3-kinase in GLUT1 mRNA translation. J. Biol. Chem. 274:1999;33085-33091
71. Tilly J.L., Hsueh A.J. Microscale autoradiographic method for the qualitative and quantitative analysis of apoptotic DNA fragmentation. J. Cell. Physiol. 154:1993;519-526
72. van Golen C.M., Castle V.P., Feldman E.L. IGF-I receptor activation and BCL-2 overexpression prevent early apoptotic events in human neuroblastoma. Cell Death Differ. 7:2000;654-665
73. Vannucci S.J., Gibbs E.M., Simpson I.A. Glucose utilization and glucose transporter proteins GLUT-1 and GLUT-3 in brains of diabetic (db/db) mice. Am. J. Physiol. 272(Pt 1):1997;E267-E274
74. Vannucci S.J., Maher F., Simpson I.A. Glucose transporter proteins in brain: delivery of glucose to neurons and glia. GLIA. 21:1997;2-21
75. Vannucci S.J., Reinhart R., Maher F., Bondy C.A., Lee W.H., Vannucci R.C., Simpson I.A. Alterations in GLUT1 and GLUT3 glucose transporter gene expression following unilateral hypoxia-ischemia in the immature rat brain. Brain Res. Dev. Brain Res. 107:1998;255-264
76. Velthuis J.H., Rouschop K.M., De Bont H.J., Mulder G.J., Nagelkerke J.F. Distinct intracellular signaling in TRAIL- and CD95L-mediated apoptosis. J. Biol. Chem. 2002;24631-24637
77. von der Crone S., Deppe C., Barthel A., Sasson S., Joost H.G., Schurmann A. Glucose deprivation induces Akt-dependent synthesis and incorporation of GLUT1, but not of GLUT4, into the plasma membrane of 3T3-L1 adipocytes. Eur. J. Cell Biol. 79:2000;943-949
78. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 292:2001;727-730
79. Werther G.A., Cheesman H., Russo V. Olfactory bulb organ culture is supported by combined insulin-like growth factor-I and basic fibroblast growth factor. Brain Res. 617:1993;339-342
80. Wilson C.M., Mitsumoto Y., Maher F., Klip A. Regulation of cell surface GLUT1, GLUT3, and GLUT4 by insulin and IGF-I in L6 myotubes. FEBS Lett. 368:1995;19-22
81. Zhou J., Bievre M., Bondy C.A. Reduced GLUT1 expression in Igf1-/- null oocytes and follicles. Growth Horm. IGF Res. 10:2000;111-117