Measures of striatal insulin resistance in a 6-hydroxydopamine model of Parkinson's disease

Brain Research

Volumn 1240, Issue , 2008, Pages 185-195

  Morris, J K ^a,b   Zhang, H ^a,b   Gupte, A A ^a,b   Bomhoff, G L ^a,b   Stanford, J A ^a,b   Geiger, P C ^a,b  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Animal model; Basal ganglia; Diabetes; Glucose; Insulin signaling; IRS2; Parkinson's disease; Striatum

Indexed keywords

ACTIN; DOPAMINE; GLUCOSE; GLUCOSE TRANSPORTER 4; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; HEAT SHOCK PROTEIN 25; INSULIN RECEPTOR SUBSTRATE 2; OXIDOPAMINE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GLUCOSE TRANSPORT; INSULIN RESISTANCE; MALE; NERVE DEGENERATION; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ADRENERGIC AGENTS; ANIMALS; BASAL GANGLIA; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GLYCOGEN SYNTHASE KINASE 3; HSP27 HEAT-SHOCK PROTEINS; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; MALE; OXIDOPAMINE; PARKINSONIAN DISORDERS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, INBRED F344; SERINE;

ANIMALIA; RATTUS;

EID: 54549097933     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.08.089     Document Type: Article

References (67)

1. Aguirre V., Werner E.D., Giraud J., Lee Y.H., Shoelson S.E., and White M.F. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J. Biol. Chem. 277 (2002) 1531-1537
2. Barbeau A., and Pourcher E. New data on the genetics of Parkinson's disease. Can. J. Neurol. Sci. 9 (1982) 53-60
3. Baum L., Hansen L., Masliah E., and Saitoh T. Glycogen synthase kinase 3 alteration in Alzheimer disease is related to neurofibrillary tangle formation. Mol. Chem. Neuropathol. 29 (1996) 253-261
4. Bennett B.D., and Wilson C.J. Synaptology and physiology of neostriatal neurones. In: Miller R., and Wickens J.R. (Eds). Brain Dynamics and the Striatal Complex (2000), Harwood Academic Publishers, Australia 11-140
5. Beal M.F. Mitochondria, oxidative damage, and inflammation in Parkinson's disease. Ann. N. Y. Acad. Sci. 991 (2003) 120-131
6. Bloch-Damti A., and Bashan N. Proposed mechanisms for the induction of insulin resistance by oxidative stress. Antioxid. Redox. Signal. 7 (2005) 1553-1567
7. Bloch-Damti A., Potashnik R., Gual P., Le Marchand-Brustel Y., Tanti J.F., Rudich A., and Bashan N. Differential effects of IRS1 phosphorylated on Ser307 or Ser632 in the induction of insulin resistance by oxidative stress. Diabetologia 49 (2006) 2463-2473
8. Boyd III A.E., Lebovitz H.E., and Feldman J.M. Endocrine function and glucose metabolism in patients with Parkinson's disease and their alternation by L-Dopa. J. Clin. Endocrinol. Metab. 33 (1971) 829-837
9. Cadet J.L., Kujirai K., and Przedborski S. Bilateral modulation of [3H]neurotensin binding by unilateral intrastriatal 6-hydroxydopamine injections: evidence from a receptor autoradiographic study. Brain Res. 564 (1991) 37-44
10. Chen G., Bower K.A., Ma C., Fang S., Thiele C.J., and Luo J. Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. Faseb J. 18 (2004) 1162-1164
11. Dong X., Park S., Lin X., Copps K., Yi X., and White M.F. Irs1 and Irs2 signaling is essential for hepatic glucose homeostasis and systemic growth. J. Clin. Invest. 116 (2006) 101-114
12. Downs C.A., Jones L.R., and Heckathorn S.A. Evidence for a novel set of small heat-shock proteins that associates with the mitochondria of murine PC12 cells and protects NADH:ubiquinone oxidoreductase from heat and oxidative stress. Arch. Biochem. Biophys. 365 (1999) 344-350
13. El Messari S., Leloup C., Quignon M., Brisorgueil M.J., Penicaud L., and Arluison M. Immunocytochemical localization of the insulin-responsive glucose transporter 4 (Glut4) in the rat central nervous system. J. Comp. Neurol. 399 (1998) 492-512
14. Enna S.J., Reisman S.A., and Stanford J.A. CGP 56999A, a GABA(B) receptor antagonist, enhances expression of brain-derived neurotrophic factor and attenuates dopamine depletion in the rat corpus striatum following a 6-hydroxydopamine lesion of the nigrostriatal pathway. Neurosci. Lett. 406 (2006) 102-106
15. Escobedo J., Pucci A.M., and Koh T.J. HSP25 protects skeletal muscle cells against oxidative stress. Free Radic. Biol. Med. 37 (2004) 1455-1462
16. Figlewicz D.P., Evans S.B., Murphy J., Hoen M., and Baskin D.G. Expression of receptors for insulin and leptin in the ventral tegmental area/substantia nigra (VTA/SN) of the rat. Brain Res. 964 (2003) 107-115
17. Fink R.I., Kolterman O.G., Griffin J., and Olefsky J.M. Mechanisms of insulin resistance in aging. J. Clin. Invest. 71 (1983) 1523-1535
18. Garcia-Segura L.M., Diz-Chaves Y., Perez-Martin M., and Darnaudery M. Estradiol, insulin-like growth factor-I and brain aging. Psychoneuroendocrinology 32 Suppl 1 (2007) S57-61
19. Garcia B.G., Wei Y., Moron J.A., Lin R.Z., Javitch J.A., and Galli A. Akt is essential for insulin modulation of amphetamine-induced human dopamine transporter cell-surface redistribution. Mol. Pharmacol. 68 (2005) 102-109
20. Geiger P.C., Hancock C., Wright D.C., Han D.H., and Holloszy J.O. IL-6 increases muscle insulin sensitivity only at superphysiological levels. Am. J. Physiol. Endocrinol. Metab. 292 (2007) E1842-1846
21. Gupte A.A., Bomhoff G.L., and Geiger P.C. Age-related differences in skeletal muscle insulin signaling: the role of stress kinases and heat shock proteins. J. Appl. Physiol. (2008)
22. Henriksen E.J., Kinnick T.R., Teachey M.K., O'Keefe M.P., Ring D., Johnson K.W., and Harrison S.D. Modulation of muscle insulin resistance by selective inhibition of GSK-3 in Zucker diabetic fatty rats. Am. J. Physiol. Endocrinol. Metab. 284 (2003) E892-900
23. Hudson J.L., van Horne C.G., Stromberg I., Brock S., Clayton J., Masserano J., Hoffer B.J., and Gerhardt G.A. Correlation of apomorphine- and amphetamine-induced turning with nigrostriatal dopamine content in unilateral 6-hydroxydopamine lesioned rats. Brain Res. 626 (1993) 167-174
24. Kim B., van Golen C.M., and Feldman E.L. Insulin-like growth factor I induces preferential degradation of insulin receptor substrate-2 through the phosphatidylinositol 3-kinase pathway in human neuroblastoma cells. Endocrinology 146 (2005) 5350-5357
25. Klintworth H., Newhouse K., Li T., Choi W.S., Faigle R., and Xia Z. Activation of c-Jun N-terminal protein kinase is a common mechanism underlying paraquat- and rotenone-induced dopaminergic cell apoptosis. Toxicol. Sci. 97 (2007) 149-162
26. Lawler C.P., Gilmore J.H., Watts V.J., Walker Q.D., Southerland S.B., Cook L.L., Mathis C.A., and Mailman R.B. Interhemispheric modulation of dopamine receptor interactions in unilateral 6-OHDA rodent model. Synapse 21 (1995) 299-311
27. Lee J., and Kim M.S. The role of GSK3 in glucose homeostasis and the development of insulin resistance. Diabetes Res. Clin. Pract. 77 Suppl 1 (2007) S49-57
28. Leroy K., and Brion J.P. Developmental expression and localization of glycogen synthase kinase-3beta in rat brain. J. Chem. Neuroanat. 16 (1999) 279-293
29. Liberman Z., Plotkin B., Tennenbaum T., and Eldar-Finkelman H. Coordinated phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 and protein kinase C betaII in the diabetic fat tissue. Am. J. Physiol. Endocrinol. Metab. 294 (2008) E1169-1177
30. Lin X., Taguchi A., Park S., Kushner J.A., Li F., Li Y., and White M.F. Dysregulation of insulin receptor substrate 2 in beta cells and brain causes obesity and diabetes. J. Clin. Invest. 114 (2004) 908-916
31. Lipman I.J., Boykin M.E., and Flora R.E. Glucose intolerance in Parkinson's disease. J. Chronic. Dis. 27 (1974) 573-579
32. Moroo I., Yamada T., Makino H., Tooyama I., McGeer P.L., McGeer E.G., and Hirayama K. Loss of insulin receptor immunoreactivity from the substantia nigra pars compacta neurons in Parkinson's disease. Acta Neuropathol. 87 (1994) 343-348
33. Morton J.P., Maclaren D.P., Cable N.T., Campbell I.T., Evans L., Bongers T., Griffiths R.D., Kayani A.C., McArdle A., and Drust B. Elevated core and muscle temperature to levels comparable to exercise do not increase heat shock protein content of skeletal muscle of physically active men. Acta Physiol. (Oxf.) 190 (2007) 319-327
34. Nikolaus S., Larisch R., Beu M., Forutan F., Vosberg H., and Muller-Gartner H.W. Bilateral increase in striatal dopamine D2 receptor density in the 6-hydroxydopamine-lesioned rat: a serial in vivo investigation with small animal PET. Eur. J. Nucl. Med. Mol. Imaging 30 (2003) 390-395
35. Papapetropoulos S., Ellul J., Argyriou A.A., Talelli P., Chroni E., and Papapetropoulos T. The effect of vascular disease on late onset Parkinson's disease. Eur. J. Neurol. 11 (2004) 231-235
36. Pardini A.W., Nguyen H.T., Figlewicz D.P., Baskin D.G., Williams D.L., Kim F., and Schwartz M.W. Distribution of insulin receptor substrate-2 in brain areas involved in energy homeostasis. Brain Res. 1112 (2006) 169-178
37. Park K.J., Gaynor R.B., and Kwak Y.T. Heat shock protein 27 association with the I kappa B kinase complex regulates tumor necrosis factor alpha-induced NF-kappa B activation. J. Biol. Chem. 278 (2003) 35272-35278
38. Paz K., Hemi R., LeRoith D., Karasik A., Elhanany E., Kanety H., and Zick Y. A molecular basis for insulin resistance. Elevated serine/threonine phosphorylation of IRS-1 and IRS-2 inhibits their binding to the juxtamembrane region of the insulin receptor and impairs their ability to undergo insulin-induced tyrosine phosphorylation. J. Biol. Chem. 272 (1997) 29911-29918
39. Pederson T.M., Kramer D.L., and Rondinone C.M. Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes 50 (2001) 24-31
40. Peng J., and Andersen J.K. The role of c-Jun N-terminal kinase (JNK) in Parkinson's disease. IUBMB Life 55 (2003) 267-271
41. Porte Jr. D., Baskin D.G., and Schwartz M.W. Insulin signaling in the central nervous system: a critical role in metabolic homeostasis and disease from C. elegans to humans. Diabetes 54 (2005) 1264-1276
42. Pressley J.C., Louis E.D., Tang M.X., Cote L., Cohen P.D., Glied S., and Mayeux R. The impact of comorbid disease and injuries on resource use and expenditures in parkinsonism. Neurology 60 (2003) 87-93
43. Rawal N., Parish C., Castelo-Branco G., and Arenas E. Inhibition of JNK increases survival of transplanted dopamine neurons in Parkinsonian rats. Cell Death Differ. 14 (2007) 381-383
44. Reagan L.P. Neuronal insulin signal transduction mechanisms in diabetes phenotypes. Neurobiol. Aging 26 Suppl 1 (2005) 56-59
45. Rui L., Fisher T.L., Thomas J., and White M.F. Regulation of insulin/insulin-like growth factor-1 signaling by proteasome-mediated degradation of insulin receptor substrate-2. J. Biol. Chem. 276 (2001) 40362-40367
46. Rui L., Yuan M., Frantz D., Shoelson S., and White M.F. SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J. Biol. Chem. 277 (2002) 42394-42398
47. Sanchez-Iglesias S., Rey P., Mendez-Alvarez E., Labandeira-Garcia J.L., and Soto-Otero R. Time-course of brain oxidative damage caused by intrastriatal administration of 6-hydroxydopamine in a rat model of Parkinson's disease. Neurochem. Res. 32 (2007) 99-105
48. Sandyk R. The relationship between diabetes mellitus and Parkinson's disease. Int. J. Neurosci. 69 (1993) 125-130
49. Sawka-Verhelle D., Baron V., Mothe I., Filloux C., White M.F., and Van Obberghen E. Tyr624 and Tyr628 in insulin receptor substrate-2 mediate its association with the insulin receptor. J. Biol. Chem. 272 (1997) 16414-16420
50. Schober A. Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell Tissue Res. 318 (2004) 215-224
51. Sharfi H., and Eldar-Finkelman H. Sequential phosphorylation of insulin receptor substrate-2 by glycogen synthase kinase-3 and c-Jun NH2-terminal kinase plays a role in hepatic insulin signaling. Am. J. Physiol. Endocrinol. Metab. 294 (2008) E307-315
52. Sirtori C.R., Bolme P., and Azarnoff D.L. Metabolic responses to acute and chronic L-dopa administration in patients with parkinsonism. N. Engl. J. Med. 287 (1972) 729-733
53. Skitek E.B., Fowler S.C., and Tessel R.E. Effects of unilateral striatal dopamine depletion on tongue force and rhythm during licking in rats. Behav. Neurosci. 113 (1999) 567-573
54. Smiley D., and Umpierrez G. Metformin/rosiglitazone combination pill (Avandamet) for the treatment of patients with Type 2 diabetes. Expert Opin. Pharmacother. 8 (2007) 1353-1364
55. Smith J.L., Ju J.S., Saha B.M., Racette B.A., and Fisher J.S. Levodopa with carbidopa diminishes glycogen concentration, glycogen synthase activity, and insulin-stimulated glucose transport in rat skeletal muscle. J. Appl. Physiol. 97 (2004) 2339-2346
56. Sykiotis G.P., and Papavassiliou A.G. Serine phosphorylation of insulin receptor substrate-1: a novel target for the reversal of insulin resistance. Mol. Endocrinol. 15 (2001) 1864-1869
57. Taguchi A., Wartschow L.M., and White M.F. Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 317 (2007) 369-372
58. Takahashi M., Yamada T., Tooyama I., Moroo I., Kimura H., Yamamoto T., and Okada H. Insulin receptor mRNA in the substantia nigra in Parkinson's disease. Neurosci. Lett. 204 (1996) 201-204
59. Uyama N., Geerts A., and Reynaert H. Neural connections between the hypothalamus and the liver. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280 (2004) 808-820
60. van der Heide L.P., Ramakers G.M., and Smidt M.P. Insulin signaling in the central nervous system: learning to survive. Prog. Neurobiol. 79 (2006) 205-221
61. Wang Q., Somwar R., Bilan P.J., Liu Z., Jin J., Woodgett J.R., and Klip A. Protein kinase B/Akt participates in GLUT4 translocation by insulin in L6 myoblasts. Mol. Cell. Biol. 19 (1999) 4008-4018
62. Werner E.D., Lee J., Hansen L., Yuan M., and Shoelson S.E. Insulin resistance due to phosphorylation of insulin receptor substrate-1 at serine 302. J. Biol. Chem. 279 (2004) 35298-35305
63. White M.F. The IRS-signalling system: a network of docking proteins that mediate insulin action. Mol. Cell. Biochem. 182 (1998) 3-11
64. White M.F. IRS proteins and the common path to diabetes. Am. J. Physiol. Endocrinol. Metab. 283 (2002) E413-E422
65. Wilhelm K.R., Yanamandra K., Gruden M.A., Zamotin V., Malisauskas M., Casaite V., Darinskas A., Forsgren L., and Morozova-Roche L.A. Immune reactivity towards insulin, its amyloid and protein S100B in blood sera of Parkinson's disease patients. Eur. J. Neurol. 14 (2007) 327-334
66. Yuan H., Sarre S., Ebinger G., and Michotte Y. Histological, behavioural and neurochemical evaluation of medial forebrain bundle and striatal 6-OHDA lesions as rat models of Parkinson's disease. J. Neurosci. Methods 144 (2005) 35-45
67. Zhande R., Mitchell J.J., Wu J., and Sun X.J. Molecular mechanism of insulin-induced degradation of insulin receptor substrate 1. Mol. Cell. Biol. 22 (2002) 1016-1026