Targeting amyloid-beta by glucagon-like peptide -1 (GLP-1) in Alzheimer's disease and diabetes

Expert Opinion on Therapeutic Targets

Volumn 15, Issue 10, 2011, Pages 1153-1162

  Bak, Ann Mosegaard ^a   Egefjord, Lærke ^b   Gejl, Michael ^b   Steffensen, Charlotte ^a   Stecher, Chalotte Willemann ^a   Smidt, Kamille ^b   Brock, Birgitte ^a   Rungby, Jørgen ^b  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Alzheimer's disease; amyloid; beta amyloid; diabetes; GLP 1; IAPP

Indexed keywords

AMYLOID BETA PROTEIN; GLUCAGON LIKE PEPTIDE 1;

ALZHEIMER DISEASE; DIABETES MELLITUS; DIET RESTRICTION; HUMAN; HYPERCHOLESTEROLEMIA; HYPERGLYCEMIA; HYPERINSULINEMIA; LANGERHANS CELL; NEUROPROTECTION; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; RISK FACTOR;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; COGNITION; DIABETES MELLITUS, TYPE 2; GLUCAGON-LIKE PEPTIDE 1; HUMANS; LEARNING; MEMORY; NEUROPROTECTIVE AGENTS; RATS;

EID: 80052905545     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2011.600691     Document Type: Review

References (88)

1. Haan MN. Therapy Insight: type 2 diabetes mellitus and the risk of late-onset Alzheimer's disease. Nat Clin Pract Neurol 2006;2:159-66
2. Luchsinger JA, Reitz C, Honig LS, et al. Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology 2005;65:545-51 (Pubitemid 41170713)
3. Xu WL, Qiu CX, Wahlin A, et al. Diabetes mellitus and risk of dementia in the Kungsholmen project: a 6-year follow-up study. Neurology 2004;63:1181-6 (Pubitemid 39350014)
4. Xu WL, Von SE, Qiu CX, et al. Uncontrolled diabetes increases the risk of Alzheimer's disease: a population-based cohort study. Diabetologia 2009;52:1031-9
5. Luchsinger JA, Tang MX, Shea S, et al. Hyperinsulinemia and risk of Alzheimer disease. Neurology 2004;63:1187-92 (Pubitemid 39350015)
6. Grossman H. Does diabetes protect or provoke Alzheimer's disease? Insights into the pathobiology and future treatment of Alzheimer's disease. CNS Spectr 2003;8:815-23
7. Yaffe K, Blackwell T, Kanaya AM, et al. Diabetes, impaired fasting glucose, and development of cognitive impairment in older women. Neurology 2004;63:658-63 (Pubitemid 39100821)
8. Cukierman T, Gerstein HC, Williamson JD. Cognitive decline and dementia in diabetes-systematic overview of prospective observational studies. Diabetologia 2005;48:2460-9 (Pubitemid 41738208)
9. Janson J, Laedtke T, Parisi JE, et al. Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 2004;53:474-81 (Pubitemid 38174565)
10. Craft S, Asthana S, Cook DG, et al. Insulin dose-response effects on memory and plasma amyloid precursor protein in Alzheimer's disease: interactions with apolipoprotein E genotype. Psychoneuroendocrinology 2003;28:809-22 (Pubitemid 36695035)
11. Peila R, Rodriguez BL, Launer LJ. Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: the Honolulu-Asia Aging Study. Diabetes 2002;51:1256-62 (Pubitemid 34438377)
12. Clark A, Nilsson MR. Islet amyloid: a complication of islet dysfunction or an aetiological factor in Type 2 diabetes? Diabetologia 2004;47:157-69 (Pubitemid 38315352)
13. Kompoti M, Mariolis A, Alevizos A, et al. Elevated serum triglycerides is the strongest single indicator for the presence of metabolic syndrome in patients with type 2 diabetes. Cardiovasc Diabetol 2006;5:21
14. Cole SL, Grudzien A, Manhart IO, et al. Statins cause intracellular accumulation of amyloid precursor protein, beta-secretase-cleaved fragments, and amyloid beta-peptide via an isoprenoid-dependent mechanism. J Biol Chem 2005;280:18755-70 (Pubitemid 41379577)
15. Craft S. Insulin resistance and Alzheimer's disease pathogenesis: potential mechanisms and implicationsfor treatment. Curr Alzheimer Res 2007;4:147-52 (Pubitemid 46557503)
16. Holscher C. The role of GLP-1 in neuronal activity and neurodegeneration. Vitam Horm 2010;84:331-54
17. Kaiyala KJ, Prigeon RL, Kahn SE, et al. Obesity induced by a high-fat diet is associated with reduced brain insulin transport in dogs. Diabetes 2000;49:1525-33
18. Zhao WQ, Chen H, Quon MJ, et al. Insulin and the insulin receptor in experimental models of learning and memory. Eur J Pharmacol 2004;490:71-81 (Pubitemid 38482161)
19. Steen E, Terry BM, Rivera EJ, et al. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes? J Alzheimers Dis 2005;7:63-80 (Pubitemid 40387185)
20. Park CR, Seeley RJ, Craft S, et al. Intracerebroventricular insulin enhances memory in a passive-avoidance task. Physiol Behav 2000;68:509-14 (Pubitemid 30129236)
21. Reger MA, Watson GS, Frey WH, et al. Effects of intranasal insulin on cognition in memory-impaired older adults: modulation by APOE genotype. Neurobiol Aging 2006;27:451-8 (Pubitemid 43185331)
22. Kulstad JJ, Green PS, Cook DG, et al. Differential modulation of plasma beta-amyloid by insulin in patients with Alzheimer disease. Neurology 2006;66:1506-10 (Pubitemid 43958544)
23. Watson GS, Peskind ER, Asthana S, et al. Insulin increases CSF Abeta42 levels in normal older adults. Neurology 2003;60:1899-903 (Pubitemid 36736003)
24. Qiu WQ, Walsh DM, Ye Z, et al. Insulin-degrading enzyme regulates extracellular levels of amyloid beta-protein by degradation. J Biol Chem 1998;273:32730-8 (Pubitemid 28557658)
25. Cole AR, Astell A, Green C, et al. Molecular connexions between dementia and diabetes. Neurosci Biobehav Rev 2007;31:1046-63 (Pubitemid 47332620)
26. Freude S, Plum L, Schnitker J, et al. Peripheral hyperinsulinemia promotes tau phosphorylation in vivo. Diabetes 2005;54:3343-8 (Pubitemid 43334322)
27. Leahy JL, Cooper HE, Deal DA, et al. Chronic hyperglycemia is associated with impaired glucose influence on insulin secretion. A study in normal rats using chronic in vivo glucose infusions. J Clin Invest 1986;77:908-15 (Pubitemid 16067964)
28. O'Donnell N, Zachara NE, Hart GW, et al. Ogt-dependent X-chromosome-linked protein glycosylation is a requisite modification in somatic cell function and embryo viability. Mol Cell Biol 2004;24:1680-90 (Pubitemid 38167089)
29. Li L, Holscher C. Common pathological processes in Alzheimer disease and type 2 diabetes: a review. Brain Res Rev 2007;56:384-402 (Pubitemid 350166529)
30. Drucker DJ. Biological actions and therapeutic potential of the glucagon-like peptides. Gastroenterology 2002;122:531-44 (Pubitemid 34117003)
31. Schmidt WE, Siegel EG, Creutzfeldt W. Glucagon-like peptide-1 but not glucagon-like peptide-2 stimulates insulin release from isolated rat pancreatic islets. Diabetologia 1985;28:704-7 (Pubitemid 16226411)
32. + channel activity. Endocrinology 1993;133:1685-92 (Pubitemid 23295196)
33. Mingrone G, Nolfe G, Castagneto GG, et al. Circadian rhythms of GIP and GLP1 in glucose-tolerant and in type 2 diabetic patients after biliopancreatic diversion. Diabetologia 2009;52:873-81
34. Balks HJ, Holst JJ, Von zur MA, et al. Rapid oscillations in plasma glucagon-like peptide-1 (GLP-1) in humans: cholinergic control of GLP-1 secretion via muscarinic receptors. J Clin Endocrinol Metab 1997;82:786-90 (Pubitemid 27106588)
35. Elliott RM, Morgan LM, Tredger JA, et al. Glucagon-like peptide-1(7-36) amide and glucose-dependent insulinotropic polypeptide secretion in response to nutrient ingestion in man: acute post-prandial and 24-h secretion patterns. J Endocrinol 1993;138:159-66 (Pubitemid 23266831)
36. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev 2007;87:1409-39 (Pubitemid 350041474)
37. Ahren B. GLP-1 and extra-islet effects. Horm Metab Res 2004;36:842-5 (Pubitemid 40115908)
38. Hui H, Zhao X, Perfetti R. Structure and function studies of glucagon-like peptide-1 (GLP-1): the designing of a novel pharmacological agent for the treatment of diabetes. Diabetes Metab Res Rev 2005;21:313-31 (Pubitemid 40945953)
39. Nauck MA. Glucagon-like peptide 1 (GLP-1): a potent gut hormone with a possible therapeutic perspective. Acta Diabetol 1998;35:117-29
40. Goke R, Larsen PJ, Mikkelsen JD, et al. Distribution of GLP-1 binding sites in the rat brain: evidence that exendin-4 is a ligand of brain GLP-1 binding sites. Eur J Neurosci 1995;7:2294-300
41. Shughrue PJ, Lane MV, Merchenthaler I. Glucagon-like peptide-1 receptor (GLP1-R) mRNA in the rat hypothalamus. Endocrinology 1996;137:5159-62 (Pubitemid 26403362)
42. Wei Y, Mojsov S. Tissue-specific expression of the human receptor for glucagon-like peptide-I: brain, heart and pancreatic forms have the same deduced amino acid sequences. FEBS Lett 1995;358:219-24
43. Kastin AJ, Akerstrom V, Pan W. Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier. J Mol Neurosci 2002;18:7-14 (Pubitemid 34252619)
44. Banks WA. The source of cerebral insulin. Eur J Pharmacol 2004;490:5-12 (Pubitemid 38482157)
45. Lerche S, Brock B, Rungby J, et al. Glucagon-like peptide-1 inhibits blood-brain glucose transfer in humans. Diabetes 2008;57:325-31
46. Perfetti R, Zhou J, Doyle ME, et al. Glucagon-like peptide-1 induces cell proliferation and pancreatic-duodenum homeobox-1 expression and increases endocrine cell mass in the pancreas of old, glucose-intolerant rats. Endocrinology 2000;141:4600-5 (Pubitemid 32055138)
47. During MJ, Cao L, Zuzga DS, et al. Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat Med 2003;9:1173-9 (Pubitemid 37173702)
48. Perry T, Lahiri DK, Chen D, et al. A novel neurotrophic property of glucagon-like peptide 1: a promoter of nerve growth factor-mediated differentiation in PC12 cells. J Pharmacol Exp Ther 2002;300:958-66 (Pubitemid 34165002)
49. Perry T, Haughey NJ, Mattson MP, et al. Protection and reversal of excitotoxic neuronal damage by glucagon-like peptide-1 and exendin-4. J Pharmacol Exp Ther 2002;302:881-8 (Pubitemid 34920207)
50. Perry T, Holloway HW, Weerasuriya A, et al. Evidence of GLP-1-mediated neuroprotection in an animal model of pyridoxine-induced peripheral sensory neuropathy. Exp Neurol 2007;203:293-301 (Pubitemid 46157226)
51. Harkavyi A, Abuirmeileh A, Lever R, et al. Glucagon-like peptide 1 receptor stimulation reverses key deficits in distinct rodent models of Parkinson's disease. J Neuroinflammation 2008;5:19
52. Bertilsson G, Patrone C, Zachrisson O, et al. Peptide hormone exendin-4 stimulates subventricular zone neurogenesis in the adult rodent brain and induces recovery in an animal model of Parkinson's disease. J Neurosci Res 2008;86:326-38 (Pubitemid 351196738)
53. Li Y, Perry T, Kindy MS, et al. GLP-1 receptor stimulation preserves primary cortical and dopaminergic neurons in cellular and rodent models of stroke and Parkinsonism. Proc Natl Acad Sci USA 2009;106:1285-90
54. Mora F, Exposito I, Sanz B, et al. Selective release of glutamine and glutamic acid produced by perfusion of GLP-1 (7-36) amide in the basal ganglia of the conscious rat. Brain Res Bull 1992;29:359-61
55. Calvo JC, Gisolfi CV, Blazquez E, et al. Glucagon-like peptide-1(7-36) amide induces the release of aspartic acid and glutamine by the ventromedial hypothalamus of the conscious rat. Brain Res Bull 1995;38:435-9
56. Oka JI, Goto N, Kameyama T. Glucagon-like peptide-1 modulates neuronal activity in the rat's hippocampus. Neuroreport 1999;10:1643-6 (Pubitemid 29354286)
57. Abbas T, Faivre E, Holscher C. Impairment of synaptic plasticity and memory formation in GLP-1 receptor KO mice: Interaction between type 2 diabetes and Alzheimer's disease. Behav Brain Res 2009;205:265-71
58. Gault VA, Porter WD, Flatt PR, et al. Actions of exendin-4 therapy on cognitive function and hippocampal synaptic plasticity in mice fed a high-fat diet. Int J Obes (Lond) 2010;34:1341-4
59. Sipe JD, Cohen AS. Review: history of the amyloid fibril. J Struct Biol 2000;130:88-98
60. Hoppener JW, Ahren B, Lips CJ. Islet amyloid and type 2 diabetes mellitus. N Engl J Med 2000;343:411-19 (Pubitemid 30626125)
61. Kahn SE, D'Alessio DA, Schwartz MW, et al. Evidence of cosecretion of islet amyloid polypeptide and insulin by beta-cells. Diabetes 1990;39:634-8 (Pubitemid 20223792)
62. Opie EL. The relation of diabetes mellitus to lesions of the pancreas. hyaline degeneration of the islands of Langerhans. J Exp Med 1901;5:527-40
63. Wajchenberg BL. beta-cell failure in diabetes and preservation by clinical treatment. Endocr Rev 2007;28:187-218 (Pubitemid 46984834)
64. Haataja L, Gurlo T, Huang CJ, et al. Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr Rev 2008;29:303-16 (Pubitemid 351679701)
65. Tanzi RE, Bertram L. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 2005;120:545-55 (Pubitemid 40269768)
66. Chiang PK, Lam MA, Luo Y. The many faces of amyloid beta in Alzheimer's disease. Curr Mol Med 2008;8:580-4
67. Nitta A, Fukuta T, Hasegawa T, et al. Continuous infusion of beta-amyloid protein into the rat cerebral ventricle induces learning impairment and neuronal and morphological degeneration. Jpn J Pharmacol 1997;73:51-7 (Pubitemid 27078010)
68. Nitta A, Itoh A, Hasegawa T, et al. beta. amyloid protein-induced Alzheimer's disease animal model. Neurosci Lett 1994;170:63-6
69. Miklossy J, Qing H, Radenovic A, et al. Beta amyloid and hyperphosphorylated tau deposits in the pancreas in type 2 diabetes. Neurobiol Aging 2010;31:1503-15
70. Stoltenberg M, Bush AI, Bach G, et al. Amyloid plaques arise from zinc-enriched cortical layers in APP/PS1 transgenic mice and are paradoxically enlarged with dietary zinc deficiency. Neuroscience 2007;150:357-69 (Pubitemid 350198720)
71. Smidt K, Jessen N, Petersen AB, et al. SLC30A3 responds to glucose-and zinc variantions in beta-cells and is critical for insulin production and in vivo glucose-metabolism during beta-cell stress. PLoS One 2009;4:1-12
72. Petersen AB, Smidt K, Magnusson N, et al. Apoptosis in INS-1E cells after ZnT-3 and ZnT-8 knock-out. Diabetologia 2009;52:s152-3
73. Oka J, Suzuki E, Goto N, et al. Endogenous GLP-1 modulates hippocampal activity in beta-amyloid protein-treated rats. Neuroreport 1999;10:2961-4 (Pubitemid 29507761)
74. Oka J, Suzuki E, Kondo Y. Endogenous GLP-1 is involved in beta-amyloid protein-induced memory impairment and hippocampal neuronal death in rats. Brain Res 2000;878:194-8
75. Perry T, Lahiri DK, Sambamurti K, et al. Glucagon-like peptide-1 decreases endogenous amyloid-beta peptide (Abeta) levels and protects hippocampal neurons from death induced by Abeta and iron. J Neurosci Res 2003;72:603-12 (Pubitemid 36578646)
76. Liu J, Yin F, Zheng X, et al. Geniposide, a novel agonist for GLP-1 receptor, prevents PC12 cells from oxidative damage via MAP kinase pathway. Neurochem Int 2007;51:361-9 (Pubitemid 47503463)
77. Liu J, Zheng X, Yin F, et al. Neurotrophic property of geniposide for inducing the neuronal differentiation of PC12 cells. Int J Dev Neurosci 2006;24:419-24 (Pubitemid 44584607)
78. Liu JH, Yin F, Guo LX, et al. Neuroprotection of geniposide against hydrogen peroxide induced PC12 cells injury: involvement of PI3 kinase signal pathway. Acta Pharmacol Sin 2009;30:159-65
79. Qin Z, Sun Z, Huang J, et al. Mutated recombinant human glucagon-like peptide-1 protects SH-SY5Y cells from apoptosis induced by amyloid-beta peptide (1-42). Neurosci Lett 2008;444:217-21
80. Gault VA, Holscher C. GLP-1 agonists facilitate hippocampal LTP and reverse the impairment of LTP induced by beta-amyloid. Eur J Pharmacol 2008;587:112-17
81. McClean PL, Gault VA, Harriott P, et al. Glucagon-like peptide-1 analogues enhance synaptic plasticity in the brain: a link between diabetes and Alzheimer's disease. Eur J Pharmacol 2010;630:158-62
82. Gengler S, McClean PL, McCurtin R, et al. Val(8)GLP-1 rescues synaptic plasticity and reduces dense core plaques in APP/PS1 mice. Neurobiol Aging 2010;punblished online 31 March 2010; doi:10.1016/j.neurobiolaging. 2010.02.014
83. Li Y, Duffy KB, Ottinger MA, et al. GLP-1 receptor stimulation reduces amyloid-beta peptide accumulation and cytotoxicity in cellular and animal models of Alzheimer's disease. J Alzheimers Dis 2010;19:1205-19
84. D'Amico M, Di FC, Marfella R, et al. Long-term inhibition of dipeptidyl peptidase-4 in Alzheimer's prone mice. Exp Gerontol 2010;45:202-7
85. Perry TA, Greig NH. A new Alzheimer's disease interventive strategy: GLP-1. Curr Drug Targets 2004;5:565-71 (Pubitemid 39004431)
86. Holst JJ, Burcelin R, Nathanson E. Neuroprotective properties of GLP-1: theoretical and practical applications. Curr Med Res Opin 2011;27:547-58
87. Rossor MN. Neurotransmitters and CNS disease. Dementia. Lancet 1982;2:1200-4
88. Moreira PI, Zhu X, Nunomura A, et al. Therapeutic options in Alzheimer's disease. Expert Rev Neurother 2006;6:897-910