Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: Link to brain reductions in acetylcholine

Journal of Alzheimer's Disease

Volumn 8, Issue 3, 2005, Pages 247-268

  Rivera, Enrique J ^a   Goldin, Alison ^a   Fulmer, Noah ^a   Tavares, Rose ^a   Wands, Jack R ^a   De La Monte, Suzanne M ^a  

^a RHODE ISLAND HOSPITAL   (United States)

Author keywords

Alzheimer's disease; Central nervous system; Growth factor receptors; Insulin gene expression; Insulin resistance; Real time RT PCR; Type 3 diabetes

Indexed keywords

ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN; CHOLINE ACETYLTRANSFERASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GROWTH FACTOR RECEPTOR; MESSENGER RNA; POLYPEPTIDE; RNA BINDING PROTEIN; SOMATOMEDIN; SOMATOMEDIN B; SOMATOMEDIN C;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; AUTOPSY; BRAIN FUNCTION; BRAIN REGION; BRAIN TISSUE; CENTRAL NERVOUS SYSTEM; DISEASE COURSE; FRONTAL LOBE; GENE EXPRESSION; HUMAN; INSULIN RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BINDING; RNA ANALYSIS;

EID: 33644591150     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2005-8304     Document Type: Article

References (73)

1. S.M. de la Monte and J.R. Wands, Review of insulin and insulin-like growth factor expression, signaling, and malfunction in the central nervous system: Relevance to Alzheimer's disease, J Alz Dis 7 (2005), 45-62.
2. S. Hoyer, Glucose metabolism and insulin receptor signal transduction in Alzheimer disease, Eur J Pharmacol 490 (2004), 115-125.
3. S. Hoyer, Causes and consequences of disturbances of cerebral glucose metabolism in sporadic Alzheimer disease: therapeutic implications, Adv Exp Med Biol 541 (2004), 135-152.
4. S. Craft, S. Asthana, D.G. Cook, L.D. Baker, M. Cherrier, K. Purganan, C. Wait, A. Petrova, S. Latendresse, G.S. Watson, J.W. Newcomer, G.D. Schellenberg and A. J. Krohn, Insulin dose-response effects on memory and plasma amyloid precursor protein in Alzheimer's disease: interactions with apolipoprotein E genotype, Psychoneuroendocrinology 28 (2003), 809-822.
5. S. Craft, S. Asthana, G. Schellenberg, L. Baker, M. Cherrier, A.A. Boyt, R.N. Martins, M. Raskind, E. Peskind and S. Plymate, Insulin effects on glucose metabolism, memory, and plasma amyloid precursor protein in Alzheimer's disease differ according to apolipoprotein-E genotype, Ann N Y Acad Sci 903 (2000), 222-228.
6. C. Messier, Diabetes, Alzheimer's disease and apolipoprotein genotype, Exp Gerontol 38 (2003), 941-946.
7. S. Hoyer, The brain insulin signal transduction system and sporadic (type II) Alzheimer disease: an update, J Neural Transm 109 (2002), 341-360.
8. J.R. McDermott and A.M. Gibson, Degradation of Alzheimer's beta-amyloid protein by human and rat brain peptidases: involvement of insulin-degrading enzyme, Neurochem Res 22 (1997), 49-56.
9. W.Q. Qiu, D.M. Walsh, Z. Ye, K. Vekrellis, J. Zhang, M.B. Podlisny, M.R. Rosner, A. Safavi, L.B. Hersh and D.J. Selkoe, Insulin-degrading enzyme regulates extracellular levels of amyloid beta-protein by degradation, J Biol Chem 273 (1998), 32730-32738.
10. W. Farris, S. Mansourian, M.A. Leissring, E.A. Eckman, L. Bertram, C.B. Eckman, R.E. Tanzi and D.J. Selkoe, Partial loss-of-function mutations in insulin-degrading enzyme that induce diabetes also impair degradation of amyloid beta-protein, Am J Pathol 164 (2004), 1425-1434.
11. M. Schubert, D.P. Brazil, D.J. Burks, J.A. Kushner, J. Ye, C.L. Flint, J. Farhang-Fallah, P. Dikkes, X.M. Warot, C. Rio, G. Corfas and M.F. White, Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation, J Neurosci 23 (2003), 7084-7092.
12. M. Schubert, D. Gautam, D. Surjo, K. Ueki, S. Baudler, D. Schubert, T. Kondo, J. Alber, N. Galldiks, E. Kustermann, S. Arndt, A.H. Jacobs, W. Krone, C.R. Kahn and J.C. Bruning, Role for neuronal insulin resistance in neurodegenerative diseases, Proc Natl Acad Sci USA 101 (2004), 3100-3105.
13. M.F. Beal, G. Uhl, M.F. Mazurek, N. Kowall and J.B. Martin, Somatostatin: alterations in the central nervous system in neurological diseases, Res Publ Assoc Res Nerv Ment Dis 64 (1986), 215-257.
14. J.C. Reubi and J. Palacios, Somatostatin and Alzheimer's disease: a hypothesis, J Neurol 233 (1986), 370-372.
15. M. Fisman, B. Gordon, V. Feleki, E. Helmes, T. McDonald and J. Dupre, Metabolic changes in Alzheimer's disease, J Am Geriatr Soc 36 (1988), 298-300.
16. S. Hoyer, Somatostatin and Alzheimer's disease, J Neurol 234 (1987), 266-267.
17. A. Tham, K. Sparring, D. Bowen, L. Wetterberg and V.R. Sara, Insulin-like growth factors and somatomedin B in the cerebrospinal fluid of patients with dementia of the Alzheimer type, Acta Psychiatr Scand 77 (1988), 719-723.
18. G. Bucht, R. Adolfsson, F. Lithner and B. Winblad, Changes in blood glucose and insulin secretion in patients with senile dementia of Alzheimer type, Acta Med Scand 213 (1983), 387-392.
19. S.M. de la Monte, T.R. Neely, J. Cannon and J.R. Wands, Ethanol impairs insulin-stimulated mitochondrial function in cerebellar granule neurons, Cell Mol Life Sci 58 (2001), 1950-1960.
20. S.M. de la Monte and J.R. Wands, Chronic gestational exposure to ethanol impairs insulin-stimulated survival and mitochondrial function in cerebellar neurons, CMLS, Cell Mol Life Sci 59 (2002), 882-893.
21. S.M. de la Monte, N. Ganju, K. Banerjee, N.V. Brown, T. Luong and J.R. Wands, Partial rescue of ethanol-induced neuronal apoptosis by growth factor activation of phosphoinositol-3-kinase, Alcohol Clin Exp Res 24 (2000), 716-726.
22. J. Xu, J. Eun Yeon, H. Chang, G. Tison, G. Jun Chen, J.R. Wands and S.M. De La Monte, Ethanol impairs insulin-stimulated neuronal survival in the developing brain: Role of PTEN phosphatase, J Biol Chem (2003).
23. E.J. Steen, B.J. Terry, E.J. Rivera, J.L. Cannon, T.R. Neely, R. Tavares, X.J. Xu, J.R. Wands and S.M. de la Monte, Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease - Is this type 3 diabetes? J Alz Dis 7 (2005), 63-80.
24. H. Braak and E. Braak, Diagnostic criteria for neuropathologic assessment of Alzheimer's disease, Neurobiol Aging 18 (1997), S85-S88.
25. Z. Nagy, D.M. Yilmazer-Hanke, H. Braak, E. Braak, C. Schultz and J. Hanke, Assessment of the pathological stages of Alzheimer's disease in thin paraffin sections: a comparative study, Dement Geriatr Cogn Disord 9 (1998), 140-144.
26. J.E. Yeon, S. Califano, J. Xu, J.R. Wands and S.M. De La Monte, Potential role of PTEN phosphatase in ethanol-impaired survival signaling in the liver, Hepatology 38 (2003), 703-714.
27. K.A. Jellinger and C. Bancher, Neuropathology of Alzheimer's disease: a critical update, J Neural Transm Suppl 54 (1998), 77-95.
28. National Institue on Aging and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease, Neurobiol Aging 18 (1997), S1-S2.
29. S.L. Payao, M.A. Smith, L.M. Winter and P.H. Bertolucci, Ribosomal RNA in Alzheimer's disease and aging, Mech Ageing Dev 105 (1998), 265-272.
30. A.M. da Silva, S.L. Payao, B. Borsatto, P.H. Bertolucci and M.A. Smith, Quantitative evaluation of the rRNA in Alzheimer's disease, Mech Ageing Dev 120 (2000), 57-64.
31. J.G. Hu, S.L. Fu, K.H. Zhang, Y. Li, L. Yin, P.H. Lu and X.M. Xu, Differential gene expression in neural stem cells and oligodendrocyte precursor cells: a cDNA microarray analysis, J Neurosci Res 78 (2004), 637-646.
32. T. Kumagai, Y. Kitagawa, G. Hirose and K. Sakai, Antibody recognition and RNA binding of a neuronal nuclear autoantigen associated with paraneoplastic neurological syndromes and small cell lung carcinoma, J Neuroimmunol 93 (1999), 37-44.
33. A. Szabo, J. Dalmau, G. Manley, M. Rosenfeld, E. Wong, J. Henson, J.B. Posner and H.M. Furneaux, HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to Elav and Sex-lethal, Cell 67 (1991), 325-333.
34. Y. Imai, I. Ibata, D. Ito, K. Ohsawa and S. Kohsaka, A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage, Biochem Biophys Res Commun 224 (1996), 855-862.
35. D. Ito, K. Tanaka, S. Suzuki, T. Dembo and Y. Fukuuchi, Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain, Stroke 32 (2001), 1208-1215.
36. A. Ullrich, J.R. Bell, E.Y. Chen, R. Herrera, L.M. Petruzzelli, T.J. Dull, A. Gray, L. Coussens, Y.C. Liao and M. Tsubokawa, Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes, Nature 313 (1985), 756-761.
37. M.G. Myers, X.J. Sun and M.F. White, The IRS-1 signaling system, Trends Biochem Sci 19 (1994), 289-293.
38. T. O'Hare and P.F. Pilch, Intrinsic kinase activity of the insulin receptor, Int J Biochem 22 (1990), 315-324.
39. X.J. Sun, P. Rothenberg, C.R. Kahn, J.M. Backer, E. Araki, P.A. Wilden, D.A. Cahill, B.J. Goldstein and M.F. White, Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein, Nature 352 (1991), 73-77.
40. M.F. White, R. Maron and C.R. Kahn, Insulin rapidly stimulates tyrosine phosphorylation of a Mr-185,000 protein in intact cells, Nature 318 (1985), 183-186.
41. X.J. Sun, D.L. Crimmins, M.J. Myers, M. Miralpeix, and M.F. White, Pleiotropic insulin signals are engaged by multisite phosphorylation of IRS-1, Mol Cell Biol 13 (1993), 7418-7428.
42. D.G. Puro and E. Agardh, Insulin-mediated regulation of neuronal maturation, Science 225 (1984), 1170-1172.
43. J.F. Mill, M.V. Chao and D.N. Ishii, Insulin, insulin-like growth factor II, and nerve growth factor effects on tubulin mRNA levels and neurite formation, Proc Natl Acad Sci USA 82 (1985), 7126-7130.
44. K. Lam, C.L. Carpenter, N.B. Ruderman, J.C. Friel, and K.L. Kelly, The phosphatidylinositol 3-kinase serine kinase phosphorylates IRS-1. Stimulation by insulin and inhibition by Wortmannin, J Biol Chem 269 (1994), 20648-20652.
45. G. Kulik, A. Klippel and M.J. Weber, Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt, Mol Cell Biol 17 (1997), 1595-1606.
46. H. Dudek, S.R. Datta, T.F. Franke, M.J. Birnbaum, R. Yao, G.M. Cooper, R.A. Segal, D.R. Kaplan and M.E. Greenberg, Regulation of neuronal survival by the serine-threonine protein kinase Akt [see comments], Science 275 (1997), 661-665.
47. B.M. Burgering and P.J. Coffer, Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction, Nature 376 (1995), 599-602.
48. M. Delcommenne, C. Tan, V. Gray, L. Rue, J. Woodgett and S. Dedhar, Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase, Proc Natl Acad Sci USA 95 (1998), 11211-11216.
49. C.H. Cho, C.S. Lee, M. Chang, I.H. Jang, S.J. Kim, I. Hwang, S.H. Ryu, C.O. Lee and G.Y. Koh, Localization of VEGFR-2 and PLD2 in endothelial caveolae is involved in VEGF-induced phosphorylation of MEK and ERK, Am J Physiol Heart Circ Physiol 286 (2004), H1881-H1888.
50. H. Huo, X. Guo, S. Hong, M. Jiang, X. Liu and K. Liao, Lipid rafts/caveolae are essential for insulin-like growth factor-1 receptor signaling during 3T3-L1 preadipocyte differentiation induction, J Biol Chem 278 (2003), 11561-11569.
51. S. Peiro, J.X. Comella, C. Enrich, D. Martin-Zanca, and N. Rocamora, PC12 cells have caveolae that contain TrkA. Caveolae-disrupting drugs inhibit nerve growth factor-induced, but not epidermal growth factor-induced, MAPK phosphorylation, J Biol Chem 275 (2000), 37846-37852.
52. E.J. Meuillet, V. Leray, P. Hubert, C. Leray and G. Cremel, Incorporation of exogenous lipids modulates insulin signaling in the hepatoma cell line, HepG2, Biochim Biophys Acta 1454 (1999), 38-48.
53. S.M. de la Monte and J.R. Wands, Alzheimer-associated neuronal thread protein mediated cell death is linked to impaired insulin signaling, J Alzheimers Dis 6 (2004), 231-242.
54. S.M. de la Monte, N. Ganju and J.R. Wands, Microtiter immunocytochemical ELISA assay, Biotechniques 26 (1999), 1073-1076, 1078.
55. S.M. de la Monte, T. Luong, T.R. Neely, D. Robinson, and J.R. Wands, Mitochondrial DNA damage as a mechanism of cell loss in Alzheimer's disease, Lab Invest 80 (2000), 1323-1335.
56. S. Hoyer, S.K. Lee, T. Loffler and R. Schliebs, Inhibition of the neuronal insulin receptor. An in vivo model for sporadic Alzheimer disease? Ann N Y Acad Sci 920 (2000), 256-258.
57. S. Hoyer and H. Lannert, Inhibition of the neuronal insulin receptor causes Alzheimer-like disturbances in oxidative/energy brain metabolism and in behavior in adult rats, Ann N Y Acad Sci 893 (1999), 301-303.
58. P. Eikelenboom and W.A. van Gool, Neuroinflammatory perspectives on the two faces of Alzheimer's disease, J Neural Transm 111 (2004), 281-294.
59. E.E. Tuppo and H.R. Arias, The role of inflammation in Alzheimer's disease, Int J Biochem Cell Biol 37 (2005), 289-305.
60. I. Blasko, M. Stampfer-Kountchev, P. Robatscher, R. Veerhuis, P. Eikelenboom and B. Grubeck-Loebenstein, How chronic inflammation can affect the brain and support the development of Alzheimer's disease in old age: the role of microglia and astrocytes, Aging Cell 3 (2004), 169-176.
61. S.M. de la Monte, G.J. Chen, E. Rivera and J.R. Wands, Neuronal thread protein regulation and interaction with microtubule-associated proteins in SH-Sy5y neuronal cells, Cell Mol Life Sci 60 (2003), 2679-2691.
62. G.J. Chen, J. Xu, S.A. Lahousse, N.L. Caggiano and S.M. de la Monte, Transient hypoxia causes Alzheimer-type molecular and biochemical abnormalities in cortical neurons: potential strategies for neuroprotection, J Alzheimers Dis 5 (2003), 209-228.
63. A. Lorenzo and B.A. Yankner, Amyloid fibril toxicity in Alzheimer's disease and diabetes, Ann N Y Acad Sci 777 (1996), 89-95.
64. T. Niikura, Y. Hashimoto, H. Tajima and I. Nishimoto, Death and survival of neuronal cells exposed to Alzheimer's insults, J Neurosci Res 70 (2002), 380-391.
65. E. Tsukamoto, Y. Hashimoto, K. Kanekura, T. Niikura, S. Aiso and I. Nishimoto, Characterization of the toxic mechanism triggered by Alzheimer's amyloid-beta peptides via p75 neurotrophin receptor in neuronal hybrid cells, J Neurosci Res 73 (2003), 627-636.
66. J. Finsterer, Mitochondriopathies, Eur J Neurol 11 (2004), 163-186.
67. S. Suzuki, Diabetes mellitus with mitochondrial gene mutations in Japan, Ann N Y Acad Sci 1011 (2004), 185-192.
68. S.M. de la Monte, K. Ghanbari, W.H. Frey, I. Beheshti, P. Averback, S.L. Hauser, H.A. Ghanbari and J.R. Wands, Characterization of the AD7c-NTP cDNA expression in Alzheimer's disease and measurement of the 41-kD protein in cerebrospinal fluid, J Clin Invest 100 (1997), 1-12.
69. S.M. de la Monte and J.R. Wands, Alzheimer-associated neuronal thread protein-induced apoptosis and impaired mitochondrial function in human central nervous system-derived neuronal cells, J Neuropathol Exp Neurol 60 (2001), 195-207.
70. A. Perez, L. Morelli, J.C. Cresto and E.M. Castano, Degradation of soluble amyloid beta-peptides 1-40, 1-42, and the Dutch variant 1-40Q by insulin degrading enzyme from Alzheimer disease and control brains, Neurochem Res 25 (2000), 247-255.
71. L. Bertram, D. Blacker, K. Mullin, D. Keeney, J. Jones, S. Basu, S. Yhu, M.G. McInnis, R.C. Go, K. Vekrellis, D.J. Selkoe, A.J. Saunders and R.E. Tanzi, Evidence for genetic linkage of Alzheimer's disease to chromosome 10q, Science 290 (2000), 2302-2303.
72. M. Boussaha, D. Hannequin, P. Verpillat, A. Brice, T. Frebourg and D. Campion, Polymorphisms of insulin degrading enzyme gene are not associated with Alzheimer's disease, Neurosci Lett 329 (2002), 121-123.
73. L. Xie, E. Helmerhorst, K. Taddei, B. Plewright, W. Van Bronswijk and R. Martins, Alzheimer's beta-amyloid peptides compete for insulin binding to the insulin receptor, J Neurosci 22 (2002), RC221.