Glucagon-like peptide-1-mediated modulation of inflammatory pathways in the diabetic brain: Relevance to alzheimer’s disease

Current Alzheimer Research

Volumn 13, Issue 12, 2016, Pages 1346-1355

  Qin, Limei ^a   Chong, Thomas ^a   Rodriguez, Richard ^a   Pugazhenthi, Subbiah ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Brain; Cognitive function and alzheimer s disease; CREB; Diabetes; Dipeptidyl peptidase 4; Glucagon like peptide1; Hippocampus; Inflammation; Insulin; Oxidative stress

Indexed keywords

ALOGLIPTIN; BACULOVIRAL IAP REPEAT CONTAINING PROTEIN 3; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; PROTEIN; PROTEIN BCL 2; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; CYTOKINE; DIPEPTIDYL PEPTIDASE IV; DPP4 PROTEIN, RAT; GLUCOSE BLOOD LEVEL; INDUCIBLE NITRIC OXIDE SYNTHASE; NERVE PROTEIN; PIPERIDINE DERIVATIVE; TRANSCRIPTOME; URACIL;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; COGNITION; CONTROLLED STUDY; DIABETES MELLITUS; DRUG EFFECT; GENE EXPRESSION PROFILING; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; IN VIVO STUDY; INSULIN BLOOD LEVEL; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; BODY WEIGHT; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOPHYSIOLOGY; ZUCKER RAT;

ALZHEIMER DISEASE; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; BRAIN; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIPEPTIDYL PEPTIDASE 4; GENE EXPRESSION REGULATION; GLUCAGON-LIKE PEPTIDE 1; HYPOGLYCEMIC AGENTS; INSULIN; NERVE TISSUE PROTEINS; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PIPERIDINES; RATS; RATS, ZUCKER; SIGNAL TRANSDUCTION; TRANSCRIPTOME; URACIL;

EID: 84995916509     PISSN: 15672050     EISSN: 18755828     Source Type: Journal    
DOI: 10.2174/1567205013666160401114751     Document Type: Article

References (78)

1. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87(1): 4-14 (2010)
2. Gregg EW, Li Y, Wang J, Burrows NR, Ali MK, Rolka D, et al. Changes in diabetes-related complications in the United States, 1990-2010. N Engl J Med 370(16): 1514-23 (2014)
3. Wang J, Imai K, Engelgau MM, Geiss LS, Wen C, Zhang P. Secular trends in diabetes-related preventable hospitalizations in the United States, 1998-2006. Diabetes Care 32(7): 1213-7 (2009)
4. Strachan MW, Reynolds RM, Marioni RE, Price JF. Cognitive function, dementia and type 2 diabetes mellitus in the elderly. Nat Rev Endocrinol 7(2): 108-14 (2011)
5. van Harten B, de Leeuw FE, Weinstein HC, Scheltens P, Biessels GJ. Brain imaging in patients with diabetes: a systematic review. Diabetes Care 29(11): 2539-48 (2006)
6. Cole AR, Astell A, Green C, Sutherland C. Molecular connexions between dementia and diabetes. Neurosci Biobehav Rev 31(7): 1046-63 (2007)
7. Luchsinger JA. Type 2 diabetes, related conditions, in relation and dementia: an opportunity for prevention? J Alzheimers Dis 20(3): 723-36 (2010)
8. Crane PK, Walker R, Hubbard RA, Li G, Nathan DM, Zheng H, et al. Glucose levels and risk of dementia. N Engl J Med 369(6): 540-8 (2013)
9. Wu W, Brickman AM, Luchsinger J, Ferrazzano P, Pichiule P, Yoshita M, et al. The brain in the age of old: the hippocampal formation is targeted differentially by diseases of late life. Ann Neurol 64(6): 698-706 (2008)
10. Carvalho C, Cardoso S, Correia SC, Santos RX, Santos MS, Baldeiras I, et al. Metabolic alterations induced by sucrose intake and Alzheimer’s disease promote similar brain mitochondrial abnormalities. Diabetes 61(5): 1234-42 (2012)
11. Reddy VP, Zhu X, Perry G, Smith MA. Oxidative stress in diabetes and Alzheimer’s disease. J Alzheimers Dis 16(4): 763-74 (2009)
12. Correia SC, Santos RX, Carvalho C, Cardoso S, Candeias E, Santos MS, et al. Insulin signaling, glucose metabolism and mitochondria: major players in Alzheimer’s disease and diabetes interrelation. Brain Res 1441:64-78 (2012)
13. Valente T, Gella A, Fernandez-Busquets X, Unzeta M, Durany N. Immunohistochemical analysis of human brain suggests pathological synergism of Alzheimer’s disease and diabetes mellitus. Neurobiol Dis 37(1): 67-76 (2010)
14. Ramasamy R, Vannucci SJ, Yan SS, Herold K, Yan SF, Schmidt AM. Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. Glycobiology 15(7): 16R-28R (2005)
15. Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med 12(9): 1005-15 (2006)
16. Ray B, Lahiri DK. Neuroinflammation in Alzheimer’s disease: different molecular targets and potential therapeutic agents including curcumin. Curr Opin Pharmacol 9(4): 434-44 (2009)
17. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell 140(6): 918-34 (2010)
18. Tong L, Balazs R, Soiampornkul R, Thangnipon W, Cotman CW. Interleukin-1 beta impairs brain derived neurotrophic factorinduced signal transduction. Neurobiol Aging 29(9): 1380-93 (2008)
19. Janelsins MC, Mastrangelo MA, Park KM, Sudol KL, Narrow WC, Oddo S, et al. Chronic neuron-specific tumor necrosis factor-alpha expression enhances the local inflammatory environment ultimately leading to neuronal death in 3xTg-AD mice. Am J Pathol 173(6): 1768-82 (2008)
20. Pugazhenthi S, Nesterova A, Jambal P, Audesirk G, Kern M, Cabell L, et al. Oxidative stress-mediated down-regulation of bcl-2 promoter in hippocampal neurons. J Neurochem 84(5): 982-96 (2003)
21. Pugazhenthi S, Phansalkar K, Audesirk G, West A, Cabell L. Differential regulation of c-jun and CREB by acrolein and 4-hydroxynonenal. Free Radic Biol Med 40(1): 21-34 (2006)
22. Jambal P, Masterson S, Nesterova A, Bouchard R, Bergman B, Hutton JC, et al. Cytokine-mediated downregulation of the transcription factor CREB in pancreatic beta -cells. J Biol Chem 278: 23055-65 (2003)
23. Shaywitz AJ, Greenberg ME. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Ann Rev Biochem 68: 821-61 (1999)
24. Pugazhenthi S, Boras T, O’Connor D, Meintzer MK, Heidenreich KA, Reusch JE. Insulin-like growth factor I-mediated activation of the transcription factor cAMP response element-binding protein in PC12 cells. Involvement of p38 mitogen-activated protein kinasemediated pathway. J Biol Chem 274(5): 2829-37 (1999)
25. Kitagawa K. CREB and cAMP response element-mediated gene expression in the ischemic brain. FEBS J 274(13): 3210-7 (2007)
26. Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1(7): 595-601 (1998)
27. Bach ME, Barad M, Son H, Zhuo M, Lu YF, Shih R, et al. Agerelated defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc Natl Acad Sci USA 96(9): 5280-5 (1999)
28. Drucker DJ. The biology of incretin hormones. Cell Metab 3(3): 153-65 (2006)
29. Li Y, Duffy KB, Ottinger MA, Ray B, Bailey JA, Holloway HW, 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 19(4): 1205-19 (2010)
30. Kastin AJ, Akerstrom V, Pan W. Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier. J Mol Neurosci 18(1-2): 7-14 (2002)
31. Li Y, Perry T, Kindy MS, Harvey BK, Tweedie D, Holloway HW, 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 106(4): 1285-90 (2009)
32. 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 205(1): 265-71 (2009)
33. Perry T, Lahiri DK, Sambamurti K, Chen D, Mattson MP, Egan JM, et al. Glucagon-like peptide-1 decreases endogenous amyloidbeta peptide (Abeta) levels and protects hippocampal neurons from death induced by Abeta and iron. J Neurosci Res 72(5): 603-12 (2003)
34. Iwai T, Ito S, Tanimitsu K, Udagawa S, Oka J. Glucagon-like peptide-1 inhibits LPS-induced IL-1beta production in cultured rat astrocytes. Neurosci Res 55(4): 352-60 (2006)
35. Kim S, Moon M, Park S. Exendin-4 protects dopaminergic neurons by inhibition of microglial activation and matrix metalloproteinase-3 expression in an animal model of Parkinson’s disease. J Endocrinol 202(3): 431-9 (2009)
36. Pugazhenthi U, Velmurugan K, Tran A, Mahaffey G, Pugazhenthi S. Anti-inflammatory action of exendin-4 in human islets is enhanced by phosphodiesterase inhibitors: potential therapeutic benefits in diabetic patients. Diabetologia 53(11): 2357-68 (2010)
37. Darsalia V, Mansouri S, Ortsater H, Olverling A, Nozadze N, Kappe C, et al. Glucagon-like peptide-1 receptor activation reduces ischaemic brain damage following stroke in Type 2 diabetic rats. Clin Sci (Lond) 122(10): 473-83 (2012)
38. Velmurugan K, Bouchard R, Mahaffey G, Pugazhenthi S. Neuroprotective actions of Glucagon-like peptide-1 in differentiated human neuroprogenitor cells. J Neurochem 123(6): 919-31 (2012)
39. White JR. Alogliptin for the treatment of type 2 diabetes. Drugs Today (Barc) 47(2): 99-107 (2011)
40. Kawashima S, Matsuoka TA, Kaneto H, Tochino Y, Kato K, Yamamoto K, et al. Effect of alogliptin, pioglitazone and glargine on pancreatic beta-cells in diabetic db/db mice. Biochem Biophys Res Commun 404(1): 534-40 (2011)
41. Zhang X, Wang Z, Huang Y, Wang J. Effects of chronic administration of alogliptin on the development of diabetes and beta-cell function in high fat diet/streptozotocin diabetic mice. Diabetes Obes Metab 13(4): 337-47 (2011)
42. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, et al. Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 93(11): 4331-41 (2008)
43. Pugazhenthi S, Qin L, Bouchard R. Dipeptidyl peptidase-4 inhibition in diabetic rats leads to activation of the transcription factor CREB in beta-cells. Eur J Pharmacol 755: 42-9 (2015)
44. Miller AA, Spencer SJ. Obesity and neuroinflammation: a pathway to cognitive impairment. Brain Behav Immun 42: 10-21 (2014)
45. Pugazhenthi S, Miller E, Sable C, Young P, Heidenreich KA, Boxer LM, et al. Insulin-like growth factor-I induces bcl-2 promoter through the transcription factor cAMP-response element binding protein. J Biol Chem 274: 27529-35 (1999)
46. Pugazhenthi S, Nesterova A, Sable C, Heidenreich K, Boxer L, Heasley L, et al. Akt/Protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem 275: 10761-6 (2000)
47. Pugazhenthi S, Wang M, Pham S, Sze CI, Eckman CB. Downregulation of CREB expression in Alzheimer’s brain and in Abeta-treated rat hippocampal neurons. Mol Neurodegener 6(1): 60 (2011)
48. Ammendrup A, Maillard A, Nielsen K, Aabenhus Andersen N, Serup P, Dragsbaek Madsen O, et al. The c-Jun amino-terminal kinase pathway is preferentially activated by interleukin-1 and controls apoptosis in differentiating pancreatic beta-cells. Diabetes 49(9): 1468-76 (2000)
49. Shoji M, Iwakami N, Takeuchi S, Waragai M, Suzuki M, Kanazawa I, et al. JNK activation is associated with intracellular beta-amyloid accumulation. Brain Res Mol Brain Res 5(1-2): 221-33 (2000)
50. Zhu X, Ogawa O, Wang Y, Perry G, Smith MA. JKK1, an upstream activator of JNK/SAPK, is activated in Alzheimer’s disease. J Neurochem 85(1): 87-93 (2003)
51. Scheinfeld MH, Roncarati R, Vito P, Lopez PA, Abdallah M, D’Adamio L. Jun NH2-terminal kinase (JNK) interacting protein 1 (JIP1) binds the cytoplasmic domain of the Alzheimer’s betaamyloid precursor protein (APP). J Biol Chem 277(5): 3767-75 (2002)
52. Perry T, Lahiri DK, Chen D, Zhou J, Shaw KT, Egan JM, 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 300(3): 958-66 (2002)
53. Velmurugan K, Balamurugan AN, Loganathan G, Ahmad A, Hering BJ, Pugazhenthi S. Antiapoptotic Actions of Exendin-4 against Hypoxia and Cytokines Are Augmented by CREB. Endocrinology 1116-28 (2012)
54. Meier JJ. GLP-1 receptor agonists for individualized treatment of type 2 diabetes mellitus. Nat Rev Endocrinol 8(12): 728-42 (2012)
55. Baetta R, Corsini A. Pharmacology of dipeptidyl peptidase-4 inhibitors: similarities and differences. Drugs 71(11): 1441-67 (2011)
56. Kim B, Feldman EL. Insulin resistance in the nervous system. Trends Endocrinol Metab 23(3): 133-41 (2012)
57. Perry T, Greig NH. Enhancing central nervous system endogenous GLP-1 receptor pathways for intervention in Alzheimer’s disease. Curr Alzheimer Res 2(3): 377-85 (2005)
58. De Felice FG, Ferreira ST. Inflammation, defective insulin signaling, and mitochondrial dysfunction as common molecular denominators connecting type 2 diabetes to Alzheimer disease. Diabetes 63(7): 2262-72 (2014).
59. Haorah J, Ramirez SH, Schall K, Smith D, Pandya R, Persidsky Y. Oxidative stress activates protein tyrosine kinase and matrix metalloproteinases leading to blood-brain barrier dysfunction. J Neurochem 101(2): 566-76 (2007)
60. Larochelle C, Alvarez JI, Prat A. How do immune cells overcome the blood-brain barrier in multiple sclerosis? FEBS Lett 585(23): 3770-80 (2011)
61. Cukierman T, Gerstein HC, Williamson JD. Cognitive decline and dementia in diabetes--systematic overview of prospective observational studies. Diabetologia 48(12): 2460-9 (2005)
62. Yaffe K, Blackwell T, Whitmer RA, Krueger K, Barrett Connor E. Glycosylated hemoglobin level and development of mild cognitive impairment or dementia in older women. J NutR, Health Aging 10(4): 293-5 (2006)
63. Ott A, Stolk R, Harskamp FV, Pols H, Hoffman A, Breteler M. Diabetes mellitus and the risk of dementia. The Rotterdam study. Neurology 53: 1937-42 (1999)
64. Kroner Z. The relationship between Alzheimer’s disease and diabetes: Type 3 diabetes? Altern Med Rev 14(4): 373-9 (2009)
65. Akter K, Lanza EA, Martin SA, Myronyuk N, Rua M, Raffa RB. Diabetes mellitus and Alzheimer’s disease: shared pathology and treatment? Br J Clin Pharmacol 71(3): 365-76 (2011)
66. Ho L, Qin W, Pompl PN, Xiang Z, Wang J, Zhao Z, et al. Dietinduced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer’s disease. FASEB J 18(7): 902-4 (2004)
67. Jolivalt CG, Hurford R, Lee CA, Dumaop W, Rockenstein E, Masliah E. Type 1 diabetes exaggerates features of Alzheimer’s disease in APP transgenic mice. Exp Neurol 223(2): 422-31 (2010)
68. Takeda S, Sato N, Uchio-Yamada K, Sawada K, Kunieda T, Takeuchi D, et al. Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes. Proc Natl Acad Sci USA 107(15): 7036-41 (2010)
69. Ham J, Eilers A, Whitfield J, Neame SJ, Shah B. c-Jun and the transcriptional control of neuronal apoptosis. Biochem Pharmacol 60(8): 1015-21 (2000)
70. Hashimoto Y, Tsuji O, Niikura T, Yamagishi Y, Ishizaka M, Kawasumi M, et al. Involvement of c-Jun N-terminal kinase in amyloid precursor protein-mediated neuronal cell death. J Neurochem 84(4): 864-77 (2003)
71. Qin L, Bouchard R, Pugazhenthi S. Regulation of cAMP response element binding protein during neuroglial interactions. J Neurochem 136(5): 918-30 (2016)
72. Wang M, Crager M, Pugazhenthi S. Modulation of apoptosis pathways by oxidative stress and autophagy in beta cells. Exp Diabetes Res 2012: 647914 (2012)
73. Robertson RP. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J Biol Chem 279(41): 42351-4 (2004)
74. Ioacara S, Guja C, Ionescu-Tirgoviste C, Fica S, Sabau S, Radu S, et al. Improvements in life expectancy in adult type 2 diabetes patients in the last six decades. Diabetes Res Clin Pract 92(3): 400-4 (2011)
75. Han W, Li C. Linking type 2 diabetes and Alzheimer’s disease. Proc Natl Acad Sci USA 107(15): 6557-8 (2010)
76. Jack CR, Jr., Knopman DS, Jagust WJ, Shaw LM, Aisen PS, Weiner MW, et al. Hypothetical model of dynamic biomarkers of the Alzheimer’s pathological cascade. Lancet Neurol 9(1): 119-28 (2010)
77. Zahs KR, Ashe KH. ‘Too much good news’ - are Alzheimer mouse models trying to tell us how to prevent, not cure, Alzheimer’s disease? Trends Neurosci 33(8): 381-9 (2010)
78. Greig NH, Mattson MP, Perry T, Chan SL, Giordano T, Sambamurti K, et al. New therapeutic strategies and drug candidates for neurodegenerative diseases: p53 and TNF-alpha inhibitors, and GLP-1 receptor agonists. Ann NY Acad Sci 1035: 290-315 (2004)