Neurological changes induced by stress in streptozotocin diabetic rats

Annals of the New York Academy of Sciences

Volumn 893, Issue , 1999, Pages 126-137

  Reagan, Lawrence P ^a   Magariños, Ana Maria ^a   McEwen, Bruce S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER; MESSENGER RNA; SOMATOMEDIN RECEPTOR;

ATROPHY; CONFERENCE PAPER; DENDRITE; HIPPOCAMPUS; HOMEOSTASIS; HYPERGLYCEMIA; IMMOBILIZATION STRESS; NEUROENDOCRINE DISEASE; NEUROLOGIC DISEASE; NONHUMAN; OXIDATION; POLYDIPSIA; POLYURIA; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; STREPTOZOCIN DIABETES; WEIGHT REDUCTION;

EID: 0033380583     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.1999.tb07822.x     Document Type: Conference Paper

References (80)

1. 1. Mandrup-Poulsen, T. 1998. Diabetes. Br. Med. J. 316: 1221-1225.
2. 2. Brown, M.J. & A.K. Asbury. 1983. Diabetic neuropathy. Ann. Neurol. 15: 2-12.
3. 3. Mooradian, A.D. 1988. Diabetic complications of the central nervous system. Endocr. Rev. 9: 346-356.
4. 4. McCall, A.L. 1992. The impact of diabetes on the CNS. Diabetes 41: 557-570.
5. 5. Ryan, C.M. 1988. Neurobehavioral complications of type I diabetes. Examination of possible risk factors. Diabetes Care 11: 86-93.
6. 6. Gradman, T.J., A. Laws, L.W. Thompson & G.M. Reaven. 1993. Verbal learning and/or memory improves with glycemic control in older subjects with non-insulin-dependent diabetes mellitus. J. Am. Geriatr. Soc. 41: 1305-1312.
7. 7. Meneilly, G.S., E. Cheung, D. Tessier, C. Yakura & H. Tuokko. 1993. The effect of improved glycemic control on cognitive functions in the elderly patient with diabetes. J. Gerontol. 48: M117-M121.
8. 8. Couch, R.M. 1992. Dissociation of cortisol and adrenal androgen secretion in poorly controlled insulin-dependent diabetes mellitus. Acta Endocrinol. 127: 115-117.
9. 9. McEwen, B.S. & R.M. Sapolsky. 1995. Stress and cognitive function. Curr. Opin. Neurobiol. 5: 205-216.
10. 10. Woolley, C.S., E. Gould & B.S. McEwen. 1990. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531: 225-231.
11. 11. Watanabe, Y., E. Gould & B.S. McEwen. 1992. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588: 341-345.
12. 12. Conrad, C.D., L.A. Galea, Y. Kuroda & B.S. McEwen. 1996. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 110: 1321-1334.
13. 13. Sapolsky, R.M., L.C. Krey & B.S. McEwen. 1985. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J. Neurosci. 5: 1222-1227.
14. 14. Kerr, D.S., L.W. Campbell, M.D. Applegate, A. Brodish & P.W. Landfield. 1991. Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J. Neurosci. 11: 1316-1324.
15. 15. Uno, H., R. Tarara, J.G. Else, M.A. Suleman & R.M. Sapolsky. 1989. Hippocampal damage associated with prolonged and fatal stress in primates. J. Neurosci. 9: 1705-1711.
16. 16. Sapolsky, R.M., H. Uno, C.S. Rebert & C.E. Finch. 1990. Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J. Neurosci. 10: 2897-2902.
17. 17. Reagan, L.P. & B.S. McEwen. 1997. Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. J. Chem. Neuroanat. 13: 149-167.
18. 18. Kadekaro, M., M. Ito & P.M. Gross. 1988. Local cerebral glucose utilization is increased in acutely adrenalectomized rats. Neuroendocrinology 47: 329-334.
19. 19. Horner, H.C., D.R. Packan & R.M. Sapolsky. 1990. Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia. Neuroendocrinology 52: 57-64.
20. 20. De Leon, M.J., T. McRae, H. Rusinek, A. Convit, S. De Santi, C. Tarshish, J. Golomb, N. Volkow, K. Daisley, N. Orentreich & B.S. McEwen. 1997. Cortisol reduces hippocampal glucose metabolism in normal elderly, but not in Alzheimer's disease. J. Clin. Endocrinol. Metab. 82: 3251-3259.
21. 21. McEwen, B.S. 1998. Protective and damaging effects of stress mediators. N. Engl. J. Med. 338: 171-179.
22. 22. Niakan, E., Y. Harati & J.P. Comstock. 1986. Diabetic autonomic neuropathy. Metabolism 35: 224-234.
23. 23. DeJong, R.N. 1977. CNS manifestations of diabetes mellitus. Postgrad. Med. 61: 101-107.
24. 24. Reske-Nielsen, E. & K. Lundbaek. 1963. Diabetic encephalopathy: diffuse and focal lesions of the brain in long-term diabetes. Acta Neurol. Scand. 39: 273-290.
25. 25. Reske-Nielsen, E., K. Lundbaek & O.U. Rafaelsen. 1965. Pathological changes in the central and peripheral nervous systems of young long-term diabetics. 1. Diabetic encephalopathy. Diabetologia 1: 233-241.
26. 26. Olsson, Y., J. Save-Soderbergh, P. Sourander & L. Angervall. 1968. A pathoanatomical study of the central and peripheral nervous system in diabetes of early onset and long duration. Pathol. Eur. 3: 62-79.
27. 27. Dejgaard, A., A. Gade, H. Larsson, V. Balle, A. Parving & H.-H. Parving. 1990. Evidence for diabetic encephalopathy. Diabetic Med. 8: 162-167.
28. 28. Bestetti, G.E., M.J. Reymond, C.E. Boujon, T. Lemarchand-Béraud & G.L. Rossi. 1989. Functional and morphological aspects of impaired TRH release by mediobasal hypothalamus of STZ-induced diabetic rats. Diabetes 38: 1351-1356.
29. 29. Bestetti, G., V. Locatelli, F. Tirone, G.L. Rossi & E.E. Müller. 1985. One month of streptozotocin-diabetes induces different neuroendocrine and morphological alterations in the pituitary axis of male and female rats. Endocrinology 117: 208-216.
30. 30. Jakobsen, J., P. Sidenius, H.J.G. Gundersen & R. Osterby. 1987. Quantitative changes of cerebral neocortical structure in insulin-treated long-term streptozotocin-induced diabetes in rats. Diabetes 36: 597-601.
31. 31. Tay, S.S.W. & W.C. Wong 1991. Gracile nucleus of streptozotocin-induced diabetic rats. J. Neurocytol. 20: 356-364.
32. 32. Magariños, A.M. & B.S. McEwen. 1998. The hippocampal morphology of diabetic rats shows an increased vulnerability to repeated stress. Soc. Neurosci. Abstr. 24: 1921.
33. 33. Maher, F., S.J. Vannucci & I.A. Simpson. 1994. Glucose transporter proteins in brain. FASEB J. 8: 1003-1011.
34. 34. Lund-Anderen, H. 1979. Transport of glucose from blood to brain. Physiol. Rev. 59:305-310.
35. 35. Pardridge, W.M. 1983. Brain metabolism: a perspective from the blood-brain barrier. Physiol. Rev. 63: 1481-1535.
36. 36. LeLoup, C., M. Arluison, N. Kassis, N. Lepetit, N. Cartier, P. Ferré & L. Pénicaud. 1996. Discrete brain areas express the insulin-responsive glucose transporter GLUT4. Mol. Brain Res. 38: 45-53.
37. 37. Nagamatsu, S., J.M. Kornhauser, C.F. Burant, S. Seino, K.E. Mayo & G.I. Bell. 1992. Glucose transporter expression in brain. J. Biol. Chem. 267: 467-472.
38. 38. McCall, A.L., A.M. Van Bueren, M. Moholt-Siebert, N.J. Cherry & W.R. Woodward. 1994. Immunohistochemical localization of the neuron-specific glucose transporter (GLUT3) to neuropil in adult rat brain. Brain Res. 659: 292-297.
39. 39. Choi, T.B., R.J. Boado & W.M. Pardridge. 1989. Blood-brain barrier glucose transporter mRNA is increased in experimental diabetes mellitus. Biochem. Biophys. Res. Commun. 164: 375-380.
40. 40. Lutz, A.J. & W.M. Pardridge. 1993. Insulin therapy normalizes GLUT1 glucose transporter mRNA but not immunoreactive transporter protein in streptozotocin-diabetic rats. Metabolism 42: 939-944.
41. 41. Vannucci, S.J., E.M. Gibbs & I.A. Simpson. 1997. Glucose utilization and glucose transporter proteins GLUT-1 and GLUT-3 in brains of diabetic (db/db) mice. Am. J. Physiol. 272: E267-E274.
42. 42. Kainulainen, H., A. Schurmann, P. Vilja & H.G. Joost. 1993. In-vivo glucose uptake and glucose transporter proteins GLUT1 and GLUT3 in brain tissue from streptozotocin-diabetic rats. Acta Physiol. Scand. 149: 221-225.
43. 43. Nagamatsu, S., H. Sawa, N. Inoue, Y. Nakamichi, H. Takeshima & T. Hoshino. 1994. Gene expression of GLUT3 glucose transporter regulated by glucose in vivo in mouse brain and in vitro in neuronal cell cultures from rat embryos. Biochem. J. 300: 125-131.
44. 44. Reagan, L.P., A.M. Magariños, L.R. Lucas, A. Van Bueren, A.L. McCall & B.S. McEwen. 1999. Regulation of GLUT3 glucose transporter in the hippocampus of diabetic rats subjected to stress. Am. J. Physiol. 276: E879-E886.
45. 45. Baynes, J.W. 1991. Role of oxidative stress in development of complications in diabetes. Diabetes 40: 405-412.
46. 46. Wolfe, S.P. 1993. Diabetes mellitus and free radicals. Brit. Med. Bull. 49: 642-652.
47. 47. Liu, J., X. Wang, M.K. Shigenaga, H.C. Yeo, A. Mori & B.N. Ames. 1996. Immobilization stress causes oxidative damage to lipid, protein, and DNA in the brain of rats. FASEB J. 10: 1532-1538.
48. 48. Ceriello, A., D. Giugliano, A. Quatraro, P. Dello Russo & P.J. Lefèbvre. 1991. Metabolic control may influence the increased superoxide generation in diabetic serum. Diabetic Med. 8: 540-542.
49. 49. Aragno, M., E. Brignardello, E. Tamagno, O. Danni & G. Boccuzzi. 1997. Dehydroepiandrosterone administration prevents the oxidative damage induced by acute hyperglycemia in rats. J. Endocrinol. 155: 233-240.
50. 50. Kumar, J.S.S. & V.P. Menon. 1993. Effect of diabetes on levels of lipid peroxides and glycolipids in rat brain. Metabolism 42: 1435-1439.
51. 51. Makar, T.K., K. Rimpel-Lamhaouar, D.G. Abraham, V.S. Gokhale & A.J.L. Cooper. 1995. Antioxidant defense systems in the brains of type II diabetic mice. J. Neurochem. 65: 287-291.
52. 52. Mattson, M.P. 1998. Modification of ion homeostasis by lipid peroxidation: roles in neuronal degeneration and adaptive plasticity. Trends Neurosci. 21: 53-57.
53. 53. Keller, J.N., Z. Pang, J.W. Geddes, J.G. Begley, A. Germeyer, G. Waeg & M.P. Mattson. 1997. Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid β-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J. Neurochem. 69: 273-284.
54. 54. Humphries, K.M., Y. Yoo & L.I. Szweda. 1998. Inhibition of NADH-linked mitochondrial respiration by 4-hydroxy-2-nonenal. Biochemistry 37: 552-557.
55. 55. Humphries, K.M. & L.I. Szweda. 1998. Selective inactivation of α-ketoglutarate dehydrogenase and pyruvate dehydrogenase: reaction of lipoic acid with 4-hydroxy-2-nonenal. Biochemistry 37: 15835-15841.
56. 56. Makar, T.K., B.L. Hungund, G.A. Cook, K. Kashfi & A.J.L. Cooper. 1995. Lipid metabolism and membrane composition are altered in the brains of type II diabetic mice. J. Neurochem. 64: 2159-2168.
57. 57. Uchida, K., L.I. Szweda, H.-Z. Chae & E.R. Stadtman. 1993. Immunochemical detection of 4-hydroxynonenal protein adducts in oxidized hepatocytes. Proc. Natl. Acad. Sci. USA 90: 8742-8746.
58. 58. Reagan, L.P., A.M. Magariños & B.S. McEwen. 1999. Oxidative stress is specifically increased in the hippocampus of diabetic rats subjected to stress. Soc. Neurosci. Abstr. In press.
59. 59. Jones, J.I. & D.R. Clemmons. 1995. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16: 3-34.
60. 60. LeRoith, D., M. Adamo, H. Werner & Roberts, Jr. 1991. Insulinlike growth factors and their receptors as growth regulators in normal physiology and pathologic states. Trends Endocrinol. Metab. 2: 134-139.
61. 61. Wuarin, L., R. Namdev, J.G. Burns, Z. Fei & D.N. Ishii. 1996. Brain insulin-like growth factor-II mRNA content is reduced in insulin-dependent and non-insulin-dependent diabetes mellitus. J. Neurochem. 67: 742-751.
62. 62. Busiguina, S., J.A. Chowen, J. Argente & I. Torres-Aleman. 1996. Specific alterations of the insulin-like growth factor I system in the cerebellum of diabetic rats. Endocrinology 137: 4980-4987.
63. 63. Zhuang, H.-X., L. Wuarin, Z. Fei & D.N. Ishii. 1997. Insulin-like growth factor (IGF) gene expression is reduced in neural tissues and liver from rats with non-insulin-dependent diabetes mellitus, and IGF treatment ameliorates diabetic neuropathy. J. Pharmacol. Exp. Ther. 283: 366-374.
64. 64. Unterman, T.G., J.J. Jentel, D.T. Oehler, R.G. Lacson & J.F. Hofert. 1993. Effects of glucocorticoids on circulating levels and hepatic expression of insulin-like growth factor (IGF)-binding proteins and IGF-I in the adrenalectomized streptozotocin-diabetic rat. Endocrinology 133: 2531-2539.
65. 65. Rodgers, B.D., A.M. Strack, M.F. Dallman, L. Hwa & C.S. Nicholl. 1995. Corticosterone regulation of insulin-like growth factor I, IGF-binding proteins, and growth in streptozotocin-induced diabetic rats. Diabetes 44: 1420-1425.
66. 66. Rodgers, B.D., R.M. Bautista & C.S. Nicholl. 1995. Regulation of insulin-like growth factor binding proteins in rats with insulin-dependent diabetes mellitus. Proc. Soc. Exp. Biol. Med. 210: 234-241.
67. 67. Adamo, M., H. Werner, W. Farnsworth, Roberts, Jr., M. Raizada & D. LeRoith. 1988. Dexamethasone reduces steady state insulin-like growth factor I messenger ribonucleic acid levels in rat neuronal and glial cells in primary culture. Endocrinology 123: 2526-2570.
68. 68. Ohyama, T., M. Sato, M. Niimi, N. Hizuka & J. Takahara. 1997. Effects of short-and long-term dexamethasone treatment on growth and growth hormone (GH)-releasing hormone (GRH)-GH-insulin-like growth factor-I axis in conscious rats. Endocr. J. 44: 827-835.
69. 69. Bernton, E., D. Hoover, R. Galloway & K. Popp. 1995. Adaptation to chronic stress in military trainees. Adrenal androgens, testosterone, glucocorticoids, IGF-I, and immune function. Ann. N. Y. Acad. Sci. 774: 217-231.
70. 70. Islam, A., C. Ayer-LeLievre, C. Heigensköld, N. Boganovic, B. Winblad & A. Adem. 1998. Changes in IGF-1 receptors in the hippocampus of adult rats after long-term adrenalectomy: receptor autoradiography and in situ hybridization histochemistry. Brain Res. 797: 342-346.
71. 71. Craft, S., S.E. Dagogo-Jack, B.V. Wiethop, C. Murphy, R.T. Nevins, S. Fleischman, V. Rice, J.W. Newcomer & P.E. Cryer. 1993. Effects of hyperglycemia on memory and hormone levels in dementia of the Alzheimer type: a longitudinal study. Behav. Neurosci. 6: 926-940.
72. 72. Craft, S., J. Newcomer, S. Kanne, S.E. Dagogo-Jack, P. Cryer, Y. Sheline, J. Luby, A. Dagogo-Jack & A. Anderson. 1996. Memory improvement following induced hyperinsulinaemia in Alzheimer's Disease. Neurobiol. Aging 17: 123-130.
73. 73. Piert, M., R.A. Koeppe, B. Giordani, S. Berent & D.E. Kuhl. 1996. Diminished glucose transport and phosphorylation in Alzheimer's Disease determined by dynamic FDG-PET. J. Nucl. Med. 37: 201-208.
74. 74. Conrad, C.D., A.M. Magariños, J.E. LeDoux & B.S. McEwen. 1999. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. In press.
75. 75. De Leon, M.J., A.E. George, J. Golomb, C. Tarshish, A. Convit, A. Kluger, S. De Santi, T. McRae, S.H. Ferris, B. Reisberg, C. Ince, H. Rusinek, M. Bobinski, B. Quinn, D.C. Miller & H.M. Wisniewski. 1997. Frequency of hippocampal formation atrophy in normal aging and Alzheimer's disease. Neurobiol. Aging 18: 1-11.
76. 76. De Leon, M.J., A.E. George, L.A. Stylopoulos, G. Smith & D.C. Miller. 1989. Early marker for Alzheimer's disease: the atrophic hippocampus. Lancet 2: 672-673.
77. 77. Trojanowski, J.Q., C.M. Clark, M.L. Schmidt, S.E. Arnold & V.M.-Y. Lee. 1997. Strategies for improving the postmortem neuropathological diagnosis of Alzheimer's disease. Neurobiol. Aging 18: S75-S79.
78. 78. Smyth, M.D., J.P. Kesslak, B.J. Cummings & C.W. Cotman. 1994. Analysis of brain injury following intrahippocampal administration of beta-amyloid in streptozotocin-treated rats. Neurobiol. Aging 15: 153-159.
79. 79. Messier, C. & M. Gagnon. 1996. Glucose regulation and cognitive functions: relation to Alzheimer's disease and diabetes. Behav. Brain Res. 75: 1-11.
80. 80. Finch, C.E. & D.M. Cohen. 1997. Aging, metabolism, and Alzheimer disease: review and hypothesis. Exp. Neurol. 143: 82-102.