Ethanol inhibits insulin expression and actions in the developing brain

Cellular and Molecular Life Sciences

Volumn 62, Issue 10, 2005, Pages 1131-1145

  De La Monte, S M ^a   Xu, X J ^a   Wands, J R ^a  

^a RHODE ISLAND HOSPITAL   (United States)

Author keywords

Central nervous system; Ethanol; Fetal alcohol syndrome; Insulin receptor tyrosine kinase; Insulin like growth factor, type I; Protein tyrosine phosphatase

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALCOHOL; GLUCOSE TRANSPORTER; INSULIN; PROTEIN TYROSINE KINASE; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CEREBELLUM; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; FETAL ALCOHOL SYNDROME; GENE EXPRESSION; GLUCOSE TRANSPORT; NERVE CELL CULTURE; NONHUMAN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; STEADY STATE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; BRAIN; CEREBELLUM; ETHANOL; FEMALE; FETAL ALCOHOL SYNDROME; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOSE; INSULIN; MODELS, ANIMAL; MONOSACCHARIDE TRANSPORT PROTEINS; NEURONS; PREGNANCY; PROTEIN-TYROSINE KINASES; RATS; RATS, LONG-EVANS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, INSULIN; RECEPTORS, SOMATOMEDIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOMATOMEDINS;

EPICOCCUM;

EID: 20944441349     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-005-4571-z     Document Type: Article

References (76)

1. Clarren S. K., Alvord E. J., Sumi S. M., Streissguth A. P. and Smith D. W. (1978) Brain malformations related to prenatal exposure to ethanol. J. Pediatr. 92: 64-67
2. Maier S. E. and West J. R. (2001) Regional differences in cell loss associated with binge-like alcohol exposure during the first two trimesters equivalent in the rat. Alcohol 23: 49-57
3. Minana R., Climent E., Barettino D., Segui J. M., Renau-Piqueras J. and Guerri C. (2000) Alcohol exposure alters the expression pattern of neural cell adhesion molecules during brain development. J. Neurochem. 75: 954-964
4. Olney J. W., Ishimaru M. J., Bittigau P. and Ikonomidou C. (2000) Ethanol-induced apoptotic neurodegeneration in the developing brain. Apoptosis 5: 515-521
5. Swanson D. J., King M. A. Walker D. W., and Heaton, M. B. (1995) Chronic prenatal ethanol exposure alters the normal ontogeny of choline acetyltransferase activity in the rat septohippocampal system. Alcohol Clin. Exp. Res. 19: 1252-1260
6. Yanni P. A. and Lindsley T. A. (2000) Ethanol inhibits development of dendrites and synapses in rat hippocampal pyramidal neuron cultures. Brain Res. Dev. Brain Res. 120: 233-243
7. Liesi P. (1997) Ethanol-exposed central neurons fail to migrate and undergo apoptosis. J. Neurosci. Res. 48: 439-448
8. Ikonomidou C., Bittigau P., Ishimaru M. J., Wozniak D. F., Koch C., Genz K. et al. (2000) Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 287: 1056-1060
9. Zhang F. X., Rubin R. and Rooney T. A. (1998) Ethanol induces apoptosis in cerebellar granule neurons by inhibiting insulin-like growth factor 1 signaling. J. Neurochem. 71: 196-204
10. de la Monte S. M., Neely T. R., Cannon J. and Wands J. R. (2001) Ethanol impairs insulin-stimulated mitochondrial function in cerebellar granule neurons. Cell. Mol. Life Sci. 58: 1950-1960
11. de la Monte S. M. and Wands J. R. (2002) Chronic gestational exposure to ethanol impairs insulin-stimulated survival and mitochondrial function in cerebellar neurons. Cell. Mol. Life Sci. 59: 882-893
12. Ramachandran V., Perez A., Chen J., Senthil D., Schenker S. and Henderson G. I. (2001) In utero ethanol exposure causes mitochondrial dysfunction, which can result in apoptotic cell death in fetal brain: a potential role for 4-hydroxynonenal. Alcohol Clin. Exp. Res. 25: 862-871
13. de la Monte S. M. and Wands J. R. (2001) Mitochondrial DNA damage and impaired mitochondrial function contribute to apoptosis of insulin-stimulated ethanol-exposed neuronal cells. Alcohol Clin. Exp. Res. 25: 898-906
14. Goodyer C. G., De S. L., Lai W. H., Guyda H. J. and Posner B. I. (1984) Characterization of insulin-like growth factor receptors in rat anterior pituitary, hypothalamus, and brain. Endocrinology 114: 1187-1195
15. Gammeltoft S., Fehlmann M. and Van O. E. (1985) Insulin receptors in the mammalian central nervous system: binding characteristics and subunit structure. Biochimie 67: 1147-1153
16. Hill J. M., Lesniak M. A., Pert C. B. and Roth J. (1986) Autoradiographic localization of insulin receptors in rat brain: prominence in olfactory and limbic areas. Neuroscience 17: 1127-1138
17. de la Monte S. M., Ganju N., Banerjee K., Brown N. V., Luong T. and Wands J. R. (2000) Partial rescue of ethanol-induced neuronal apoptosis by growth factor activation of phosphoinositol-3-kinase. Alcohol Clin. Exp. Res. 24: 716-726
18. Hallak H., Seiler A. E., Green J. S., Henderson A., Ross B. N. and Rubin R. (2001) Inhibition of insulin-like growth factor-I signaling by ethanol in neuronal cells. Alcohol Clin. Exp. Res. 25: 1058-1064
19. Ullrich A., Bell J. R., Chen E. Y., Herrera R., Petruzzelli L. M., Dull T. J. et al. (1985) Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes. Nature 313: 756-761
20. O'Hare T. and Pilch P. F. (1990) Intrinsic kinase activity of the insulin receptor. Int. J. Biochem. 22: 315-324
21. Myers M. G., Sun X. J. and White M. F. (1994) The IRS-1 signaling system. Trends Biochem. Sci. 19: 289-293
22. Shpakov A. O. and Pertseva M. N. (2000) Structural and functional characterization of insulin receptor substrate proteins and the molecular mechanisms of their interaction with insulin superfamily tyrosine kinase receptors and effector proteins. Membr. Cell Biol. 13: 455-484
23. Skolnik E. Y., Batzer A., Li N., Lee C. H., Lowenstein E., Mohammadi M. et al. (1993) The function of GRB2 in linking the insulin receptor to Ras signaling pathways. Science 260: 1953-1955
24. Baltensperger K., Kozma L. M., Cherniack A. D., Klarlund J. K., Chawla A., Banerjee U. et al. (1993) Binding of the Ras activator son of sevenless to insulin receptor substrate-1 signaling complexes. Science 260: 1950-1952
25. Sun X. J., Crimmins D. L., Myers M. J., Miralpeix M. and White M. F. (1993) Pleiotropic insulin signals are engaged by multisite phosphorylation of IRS-1. Mol. Cell Biol. 13: 7418-7428
26. Lam K., Carpenter C. L., Ruderman N. B., Friel J. C. and Kelly K. L. (1994) The phosphatidylinositol 3-kinase serine kinase phosphorylates IRS-1: stimulation by insulin and inhibition by wortmannin. J. Biol. Chem. 269: 20648-20652
27. Kandel E. S. and Hay N. (1999) The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp. Cell Res. 253: 210-229
28. Burgering B. M. and Coffer P. J. (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599-602
29. Pap M. and Cooper G. M. (1998) Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 273: 19929-19932
30. Weeren P. C. van, Bruyn K. M. de, Vries-Smits A. M. de, Lint J. van and Burgering B. M. (1998) Essential role for protein kinase B (PKB) in insulin-induced glycogen synthase kinase 3 inactivation: characterization of dominant-negative mutant of PKB. J. Biol. Chem. 273: 13150-13156
31. Datta S. R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y. et al. (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241
32. Hetman M., Cavanaugh J. E., Kimelman D. and Xia Z. (2000) Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20: 2567-2574
33. Dudek H., Datta S. R., Franke T. F., Birnbaum M. J., Yao R., Cooper G. M. et al. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275: 661-665
34. Eves E. M., Xiong W., Bellacosa A., Kennedy S. G., Tsichlis P. N., Rosner M. R. et al. (1998) Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol. Cell. Biol. 18: 2143-2152
35. Condorelli F., Salomoni P., Cotteret S., Cesi V., Srinivasula S. M., Alnemri E. S. et al. (2001) Caspase cleavage enhances the apoptosis-inducing effects of BAD. Mol. Cell. Biol. 21: 3025-3036.
36. Halestrap A. P., Doran E., Gillespie J. P. and O'Toole A. (2000) Mitochondria and cell death. Biochem. Soc. Trans. 28: 170-177
37. Hirsch T., Susin S. A., Marzo I., Marchetti P., Zamzami N. and Kroemer G. (1998) Mitochondrial permeability transition in apoptosis and necrosis. Cell Biol. Toxicol. 14: 141-145
38. Xu J., Yeon J. E., Chang H., Tison G., Chen G. J., Wands J. and de la Monte S. M. (2003) Ethanol impairs insulin-stimulated neuronal survival in the developing brain: role of PTEN phosphatase. J. Biol. Chem. 278: 26929-26937
39. Yeon J. E., Califano S., Xu J., Wands J. R. and Monte S. M. de la (2003) Potential role of PTEN phosphatase in ethanol-impaired survival signaling in the liver. Hepatology 38: 703-714
40. Dahia P. L., Aguiar R. C., Alberta J., Kum J. B., Caron S., Sill H. et al. (1999) PTEN is inversely correlated with the cell survival factor Akt/PKB and is inactivated via multiple mechanisms in haematological malignancies. Hum. Mol. Genet. 8: 185-193
41. Urso T., Gavaler J. S. and Van T. D. (1981) Blood ethanol levels in sober alcohol users seen in an emergency room. Life Sci. 28: 1053-1056
42. Mohamed S. A., Nathaniel E. J., Nathaniel D. R. and Snell L. (1987) Altered Purkinje cell maturation in rats exposed prenatally to ethanol. I. Cytology. Exp. Neurol. 97: 35-52
43. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A. et al. (2002) Current Protocols in Molecular Biology, Wiley, New York
44. Banerjee K., Mohr L., Wands J. R. and Monte S. M. de la (1998) Ethanol inhibition of insulin signaling in hepatocellular carcinoma cells. Alcohol Clin. Exp. Res. 22: 2093-2101
45. de la Monte S. M., Ganju N., Tanaka S., Banerjee K., Karl P. J., Brown N. V. et al. (1999) Differential effects of ethanol on insulin-signaling through the insulin receptor substrate-1. Alcohol Clin. Exp. Res. 23: 770-777
46. Nikolic M., Dudek H., Kwon Y. T., Ramos Y. F. and Tsai L. H. (1996) The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10: 816-825
47. Szabo A., Dalmau J., Manley G., Rosenfeld M., Wong E., Henson J. et al. (1991) HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to Elav and Sex-lethal. Cell 67: 325-333
48. Karl P. I. and Fisher S. E. (1993) Ethanol alters hormone production in cultured human placental trophoblasts. Alcohol Clin. Exp. Res. 17: 816-821
49. Karl P. I. and Fisher S. E. (1994) Chronic ethanol exposure inhibits insulin and IGF-1 stimulated amino acid uptake in cultured human placental trophoblasts. Alcohol Clin. Exp. Res. 18: 942-946
50. Dumke C. L., Wetter A. C., Arias E. B., Kahn C. R. and Cartee G. D. (2001) Absence of insulin receptor substrate-1 expression does not alter GLUT1 or GLUT4 abundance or contraction-stimulated glucose uptake by mouse skeletal muscle. Horm. Metab. Res. 33: 696-700
51. Rasmussen S. K., Hansen L., Frevert E. U., Cohen P. T., Kahn B. B. and Pedersen O. (2000) Adenovirus-mediated expression of a naturally occurring Asp905Tyr variant of the glycogen-associated regulatory subunit of protein phosphatase-1 in L6 myotubes. Diabetologia 43: 718-722
52. Moyers J. S., Bilan P. J., Reynet C. and Kahn C. R. (1996) Overexpression of Rad inhibits glucose uptake in cultured muscle and fat cells. J. Biol. Chem. 271: 23111-23116
53. Silva A. M. da, Payao S. L., Borsatto B., Bertolucci P. H. and Smith M. A. (2000) Quantitative evaluation of the rRNA in Alzheimer's disease. Mech. Ageing Dev. 120: 57-64
54. Payao S. L., Smith M. A., Winter L. M. and Bertolucci P. H. (1998) Ribosomal RNA in Alzheimer's disease and aging. Mech. Ageing Dev. 105: 265-272
55. Klingler-Hoffmann M., Fodero-Tavoletti M. T., Mishima K., Narita Y., Cavenee W. K., Furnari F. B. et al. (2001) The protein tyrosine phosphatase TCPTP suppresses the tumorigenicity of glioblastoma cells expressing a mutant epidermal growth factor receptor. J. Biol. Chem. 276: 46313-46318
56. Galic S., Klingler-Hoffmann M., Fodero-Tavoletti M. T., Puryer M. A., Meng T. C., Tonks N. K. et al. (2003) Regulation of insulin receptor signaling by the protein tyrosine phosphatase TCPTP. Mol. Cell. Biol. 23: 2096-2108
57. Folli F., Ghidella S., Bonfanti L., Kahn C. R. and Merighi A. (1996) The early intracellular signaling pathway for the insulin/insulin-like growth factor receptor family in the mammalian central nervous system. Mol. Neurobiol. 13: 155-183
58. D'Ercole A. J., Ye P., Calikoglu A. S. and Gutierrez-Ospina G. (1996) The role of the insulin-like growth factors in the central nervous system. Mol. Neurobiol. 13: 227-255
59. Nakae J., Kido Y. and Accili D. (2001) Distinct and overlapping functions of insulin and IGF-I receptors. Endocr. Rev. 22: 818-835
60. Pete G., Fuller C. R., Oldham J. M., Smith D. R., D'Ercole A. J., Kahn C. R. et al. (1999) Postnatal growth responses to insulin-like growth factor I in insulin receptor substrate-1-deficient mice. Endocrinology 140: 5478-5487
61. Schubert M., Brazil D. P., Burks D. J., Kushner J. A., Ye J., Flint C. L. et al. (2003) Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J. Neurosci. 23: 7084-7092
62. Virkamaki A., Ueki K. and Kahn C. R. (1999) Protein-protein interaction in insulin signaling and the molecular mechanisms of insulin resistance. J. Clin. Invest. 103: 931-943
63. Mauvais-Jarvis F., Kulkarni R. N. and Kahn C. R. (2002) Knockout models are useful tools to dissect the pathophysiology and genetics of insulin resistance. Clin. Endocrinol. 57: 1-9
64. Seiler A. E., Ross B. N., Green J. S. and Rubin R. (2000) Differential effects of ethanol on insulin-like growth factor-I receptor signaling. Alcohol Clin. Exp. Res. 24: 140-148
65. Seiler A. E., Ross B. N. and Rubin R. (2001) Inhibition of insulin-like growth factor-1 receptor and IRS-2 signaling by ethanol in SH-SY5Y neuroblastoma cells. J. Neurochem. 76: 573-581
66. Ravichandran L. V., Chen H., Li Y. and Quon M. J. (2001) Phosphorylation of PTP1B at Ser(50) by Akt impairs its ability to dephosphorylate the insulin receptor. Mol. Endocrinol. 15: 1768-1780
67. Ceulemans H. and Bollen M. (2004) Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol. Rev. 84: 1-39
68. Nam J. S., Ino Y., Sakamoto M. and Hirohashi S. (2002) Src family kinase inhibitor PP2 restores the E-cadherin/catenin cell adhesion system in human cancer cells and reduces cancer metastasis. Clin. Cancer Res. 8: 2430-2436
69. Yokoyama N. and Miller W. T. (2001) Inhibition of Src by direct interaction with protein phosphatase 2A. FEBS Lett. 505: 460-464
70. Sontag E., Nunbhakdi-Craig V., Lee G., Bloom G. S. and Mumby M. C. (1996) Regulation of the phosphorylation state and microtubule-binding activity of Tau by protein phosphatase 2A. Neuron 17: 1201-1207
71. Strack S., Westphal R. S., Colbran R. J., Ebner F. F. and Wadzinski B. E. (1997) Protein serine/threonine phosphatase 1 and 2A associate with and dephosphorylate neurofilaments. Brain Res. Mol. Brain Res. 49: 15-28
72. Alexander B. M., Dugast I., Ercolani L., Kong X. F., Giere L. and Nasrin N. (1992) Multiple insulin-responsive elements regulate transcription of the GAPDH gene. Adv. Enzyme Regul. 32: 149-159
73. Mueckler M. (1994) Facilitative glucose transporters. Eur. J. Biochem. 219: 713-725
74. Handa R. K., DeJoseph M. R., Singh L. D., Hawkins R. A. and Singh S. P. (2000) Glucose transporters and glucose utilization in rat brain after acute ethanol administration. Metab. Brain Dis. 15: 211-222
75. Hu I. C., Singh S. P. and Snyder A. K. (1995) Effects of ethanol on glucose transporter expression in cultured hippocampal neurons. Alcohol Clin. Exp. Res. 19: 1398-1402
76. Singh S. P., Srivenugopal K. S., Yuan X. H., Jiang F. and Snyder A. K. (1993) Effects of ethanol ingestion on glucose transporter-1 protein and mRNA levels in rat brain. Life Sci. 53: 1811-1819