The type 2 diabetes drug liraglutide reduces chronic inflammation induced by irradiation in the mouse brain

European Journal of Pharmacology

Volumn 700, Issue 1-3, 2013, Pages 42-50

  Parthsarathy, Vadivel ^a   Hölscher, Christian ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

Alzheimer's disease; GLP 1; Incretins; Infection; Liraglutide; Neurodegenerative diseases; Parkinson's disease

Indexed keywords

CYTOKINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12P70; INTERLEUKIN 6; LIRAGLUTIDE; NITRIC OXIDE; NITRITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN RADIATION; CELL ACTIVATION; CHRONIC INFLAMMATION; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFICACY; ENCEPHALITIS; FOOD INTAKE; HIPPOCAMPUS; MALE; MICROGLIA; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION DOSE; TREATMENT RESPONSE; UPREGULATION; WEIGHT REDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ASTROCYTES; BODY WEIGHT; BRAIN; CYTOKINES; DIABETES MELLITUS, TYPE 2; EATING; GLUCAGON-LIKE PEPTIDE 1; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; RADIATION INJURIES, EXPERIMENTAL;

EID: 84874085243     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2012.12.012     Document Type: Article

References (55)

1. H. Agersø, and P. Vicini Pharmacodynamics of NN2211, a novel long acting GLP-1 derivative Eur. J. Pharmacol. 19 2003 141 150 (Pubitemid 36668041)
2. M. Arakawa, T. Mita, K. Azuma, C. Ebato, H. Goto, T. Nomiyama, Y. Fujitani, T. Hirose, R. Kawamori, and H. Watada Inhibition of monocyte adhesion to endothelial cells and attenuation of atherosclerotic lesion by a glucagon-like peptide-1 receptor agonist, exendin-4 Diabetes 59 2010 1030 1037
3. K. Ayasolla, M. Khan, A.K. Singh, and I. Singh Inflammatory mediator and beta-amyloid (25-35)-induced ceramide generation and iNOS expression are inhibited by vitamin E Free Radic. Biol. Med. 37 2004 325 338 (Pubitemid 38833999)
4. M. Blandino, G. Perez, and M. Mellado Anti-proliferative effect of proinflammatory cytokines in cultured beta cells is associated with extracellular signal-regulated kinase1/2 pathway inhibition: protective role of GLP-1 J. Mol. Endicrinol. 1 2008 35 44
5. L. Bondolfi, M. Calhoun, F. Ermini, H.G. Kuhn, K.H. Wiederhold, L. Walker, M. Staufenbiel, and M. Jucker Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice J. Neurosci. 22 2002 515 522 (Pubitemid 34049090)
6. W. Burger, and M. Burge Digital Imaging Processing - An Algorhythmic Introduction Using Java 2009 Springer Verlag Berlin
7. M.D. Burton, and R.W. Johnson Interleukin-6 trans-signaling in the senescent mouse brain is involved in infection-related deficits in contextual fear conditioning Brain Behav. Immun. 26 2012 732 738
8. S.Y. Chen, T.F. Chen, L.C. Lai, J.H. Chen, Y. Sun, L.L. Wen, P.K. Yip, Y.M. Chu, and Y.C. Chen Sequence variants of interleukin 6 (IL-6) are significantly associated with a decreased risk of late-onset Alzheimer's disease J. Neuroinflammation 9 2012 21
9. G.M. Cole, T. Morihara, G.P. Lim, F. Yang, A. Begum, and S.A. Frautschy NSAID and antioxidant prevention of Alzheimer's disease: lessons from in vitro and animal models Ann. NY Acad. Sci. 1035 2004 68 84 (Pubitemid 40362327)
10. C. Cunningham, and D.T. Skelly Non-steroidal anti-inflammatory drugs and cognitive function: are prostaglandins at the heart of cognitive impairment in dementia and delirium? J. Neuroimmune Pharmacol. 7 2012 60 73
11. R. Delgado, A. Carlin, L. Airaghi, M.T. Demitri, L. Meda, D. Galimberti, P. Baron, J.M. Lipton, and A. Catania Melanocortin peptides inhibit production of proinflammatory cytokines and nitric oxide by activated microglia J. Leukoc. Biol. 63 6 1998 740 745 (Pubitemid 28274836)
12. K.C. Dozier, E.L. Cureton, R.O. Kwan, B. Curran, J. Sadjadi, and G.P. Victorino Glucagon-like peptide-1 protects mesenteric endothelium from injury during inflammation Peptides 30 2009 1735 1741
13. A. Fukuda, H. Fukuda, M. Jonsson, J. Swanpalmer, S. Hertzman, B. Lannering, T. Bjork-Eriksson, I. Marky, and K. Blomgren Progenitor cell injury after irradiation to the developing brain can be modulated by mild hypothermia or hyperthermia J. Neurochem. 94 2005 1604 1619 (Pubitemid 41324642)
14. F. Garcia-Oscos, H. Salgado, S. Hall, F. Thomas, G.E. Farmer, J. Bermeo, L.C. Galindo, R.D. Ramirez, S. D'Mello, S. Rose-John, and M. Atzori The stress-induced cytokine interleukin-6 decreases the inhibition/excitation ratio in the rat temporal cortex via trans-signaling Biol. Psychiatry 71 2012 574 582
15. R. Goke, P.J. Larsen, J.D. Mikkelsen, and S.P. Sheikh 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. 7 1995 2294 2300
16. N.H. Greig, M.P. Mattson, T. Perry, S.L. Chan, T. Giordano, K. Sambamurti, J.T. Rogers, H. Ovadia, and D.K. Lahiri New Therapeutic Strategies and Drug Candidates for Neurodegenerative Diseases: p53 and TNF-{alpha} Inhibitors, and GLP-1 Receptor Agonists Ann. NY Acad. Sci. 1035 2004 290 315 (Pubitemid 40362340)
17. A. Hamilton, and C. Holscher Receptors for the insulin-like peptide GLP-1 are expressed on neurons in the CNS Neuroreport 20 2009 1161 1166
18. A. Hamilton, S. Patterson, D. Porter, V.A. Gault, and C. Holscher Novel GLP-1 mimetics developed to treat type 2 diabetes promote progenitor cell proliferation in the brain J. Neurosci. Res. 89 2011 481 489
19. A. Harkavyi, A. Abuirmeileh, R. Lever, A.E. Kingsbury, C.S. Biggs, and P.S. Whitton Glucagon-like peptide 1 receptor stimulation reverses key deficits in distinct rodent models of Parkinson's disease J. Neuroinflammation 5 2008 19
20. C. Holmes, C. Cunningham, E. Zotova, D. Culliford, and V.H. Perry Proinflammatory cytokines, sickness behavior, and Alzheimer disease Neurology 77 2011 212 218
21. C. Holscher Incretin analogues that have been developed to treat type 2 diabetes hold promise as a novel treatment strategy for Alzheimer's disease Recent Pat. CNS Drug Discov. 5 2010 109 117
22. C. Hölscher Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity Trends Neurosci. 20 1997 298 303 (Pubitemid 27348739)
23. Y. Huang, D.E. Smith, O. Ibanez-Sandoval, J.E. Sims, and W.J. Friedman Neuron-specific effects of interleukin-1beta are mediated by a novel isoform of the IL-1 receptor accessory protein J. Neurosci. 31 2011 18048 18059
24. M. Huell, S. Strauss, B. Volk, M. Berger, and J. Bauer Interleukin-6 is present in early stages of plaque formation and is restricted to the brains of Alzheimer's disease patients Acta Neuropathol. 89 1995 544 551
25. K. Hunter, and C. Holscher Drugs developed to treat diabetes, liraglutide and lixisenatide, cross the blood brain barrier and enhance neurogenesis BMC Neurosci. 13 2012 33 38
26. T. Iwai, S. Ito, K. Tanimitsu, S. Udagawa, and J. Oka Glucagon-like peptide-1 inhibits LPS-induced IL-1beta production in cultured rat astrocytes Neurosci. Res. 55 2006 352 360 (Pubitemid 43866249)
27. M. Kalm, B. Lannering, T. Bjork-Eriksson, and K. Blomgren Irradiation-induced loss of microglia in the young brain J. Neuroimmunol. 206 2009 70 75
28. A.J. Kastin, V. Akerstrom, and W. Pan Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier J. Mol. Neurosci. MN 18 2002 7 14 (Pubitemid 34252619)
29. L.A. Kotilinek, M.A. Westerman, Q. Wang, K. Panizzon, G.P. Lim, A. Simonyi, S. Lesne, A. Falinska, L.H. Younkin, S.G. Younkin, M. Rowan, J. Cleary, R.A. Wallis, G.Y. Sun, G. Cole, S. Frautschy, R. Anwyl, and K.H. Ashe Cyclooxygenase-2 inhibition improves amyloid-beta-mediated suppression of memory and synaptic plasticity Brain 131 2008 651 664 (Pubitemid 351294724)
30. F. Lazarini, M.A. Mouthon, G. Gheusi, F. de Chaumont, J.C. Olivo-Marin, S. Lamarque, D.N. Abrous, F.D. Boussin, and P.M. Lledo Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice PLoS One 4 2009 e7017
31. Y.J. Lee, S.B. Han, S.Y. Nam, K.W. Oh, and J.T. Hong Inflammation and Alzheimer's disease Arch Pharm. Res. 33 2010 1539 1556
32. H. Li, C.H. Lee, K.Y. Yoo, J.H. Choi, O.K. Park, B.C. Yan, K. Byun, B. Lee, I.K. Hwang, and M.H. Won Chronic treatment of exendin-4 affects cell proliferation and neuroblast differentiation in the adult mouse hippocampal dentate gyrus Neurosci. Lett. 19 2010 1205 1219
33. Y. Li, T. Perry, M.S. Kindy, B.K. Harvey, D. Tweedie, H.W. Holloway, K. Powers, H. Shen, J.M. Egan, K. Sambamurti, A. Brossi, D.K. Lahiri, M.P. Mattson, B.J. Hoffer, Y. Wang, and N.H. Greig 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 2009 1285 1290
34. C.L. Limoli, E. Giedzinski, R. Rola, S. Otsuka, T.D. Palmer, and J.R. Fike Radiation response of neural precursor cells: linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress Radiat. Res. 161 2004 17 27 (Pubitemid 38018720)
35. N.M. Luheshi, K.J. Kovacs, G. Lopez-Castejon, D. Brough, and A. Denes Interleukin-1alpha expression precedes IL-1beta after ischemic brain injury and is localised to areas of focal neuronal loss and penumbral tissues J. Neuroinflammation 8 2011 186
36. M.E. Lull, and M.L. Block Microglial activation and chronic neurodegeneration Neurotherapeutics 7 2010 354 365
37. S.B. Matousek, S. Ghosh, S.S. Shaftel, S. Kyrkanides, J.A. Olschowka, and M.K. O'Banion Chronic IL-1beta-mediated neuroinflammation mitigates amyloid pathology in a mouse model of Alzheimer's disease without inducing overt neurodegeneration J. Neuroimmune Pharmacol. 7 2012 156 164
38. P. McClean, V. Parthsarathy, E. Faivre, and C. Hölscher The diabetes drug Liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease J. Neurosci. 31 2011 6587 6594
39. S. Mizumatsu, M.L. Monje, D.R. Morhardt, R. Rola, T.D. Palmer, and J.R. Fike Extreme sensitivity of adult neurogenesis to low doses of X-irradiation Cancer Res. 63 2003 4021 4027 (Pubitemid 36917922)
40. M.L. Monje, H. Toda, and T.D. Palmer Inflammatory blockade restores adult hippocampal neurogenesis Science 302 2003 1760 1765 (Pubitemid 37505739)
41. A.S. Naylor, C. Bull, M.K. Nilsson, C. Zhu, T. Bjork-Eriksson, P.S. Eriksson, K. Blomgren, and H.G. Kuhn Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain Proc. Natl. Acad. Sci. USA 105 2008 14632 14637
42. D.M. Paresce, H. Chung, and F.R. Maxfield Slow degradation of aggregates of the Alzheimer's disease amyloid beta-protein by microglial cells J. Biol. Chem. 272 1997 29390 29397 (Pubitemid 27498234)
43. R.L. Perez, J.D. Ritzenthaler, and J. Roman Transcriptional regulation of the interleukin-1beta promoter via fibrinogen engagement of the CD18 integrin receptor Am. J. Respir. Cell Mol. Biol. 20 5 1999 1059 1066 (Pubitemid 129540865)
44. R. Perfetti, J. Zhou, M.E. Doyle, and J.M. Egan 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 141 2000 4600 4605 (Pubitemid 32055138)
45. T. Perry, and N.H. Greig Enhancing central nervous system endogenous GLP-1 receptor pathways for intervention in Alzheimer's disease Curr. Alzheimer Res. 2 2005 377 385 (Pubitemid 40980196)
46. W.D. Porter, B.D. Kerr, P.R. Flatt, C. Holscher, and V.A. Gault Four weeks administration of Liraglutide improves memory and learning as well as glycaemic control in mice with high fat dietary-induced obesity and insulin resistance Diabetes Obes. Metab. 12 10 2010 891 899
47. L. Radenovic, I. Vasiljevic, V. Selakovic, and M. Jovanovic 7-nitroindazole reduces nitrite concentration in rat brain after intrahippocampal kainate-induced seizure Comp. Biochem. Physiol. Toxicol. Pharmacol. CBP 135 2003 443 450 (Pubitemid 38367468)
48. S. Rossi, R. Furlan, V. De Chiara, C. Motta, V. Studer, F. Mori, A. Musella, A. Bergami, L. Muzio, G. Bernardi, L. Battistini, G. Martino, and D. Centonze Interleukin-1beta causes synaptic hyperexcitability in multiple sclerosis Ann. Neurol. 71 2012 76 83
49. P.L. Sandow, M. Hejrat-Yazdi, and M.W. Heft Taste loss and recovery following radiation therapy J. Dent. Res. 85 2006 608 611 (Pubitemid 44085949)
50. M. Smith, and G. Perry Free radical damage, iron, and Alzheimer's disease J. Neurol. Sci. 134 1995 92 94
51. A.R. Vaz, S.L. Silva, A. Barateiro, A. Fernandes, A.S. Falcao, M.A. Brito, and D. Brites Pro-inflammatory cytokines intensify the activation of NO/NOS, JNK1/2 and caspase cascades in immature neurons exposed to elevated levels of unconjugated bilirubin Exp. Neurol. 229 2011 381 390
52. A. Vella, P. Shah, A.S. Reed, A.S. Adkins, R. Basu, and R.A. Rizza Lack of effect of exendin-4 and glucagon-like peptide-1-(7,36)-amide on insulin action in non-diabetic humans Diabetologia 45 2002 1410 1415 (Pubitemid 35244894)
53. J.M. Wojtowicz Irradiation as an experimental tool in studies of adult neurogenesis Hippocampus 16 2006 261 266
54. M. Yaguchi, S. Ohta, Y. Toyama, Y. Kawakami, and M. Toda Functional recovery after spinal cord injury in mice through activation of microglia and dendritic cells after IL-12 administration J. Neurosci. Res. 86 2008 1972 1980
55. M. Zandian, K.R. Mott, S.J. Allen, S. Chen, M. Arditi, and H. Ghiasi IL-2 suppression of IL-12p70 by a recombinant HSV-1 expressing IL-2 induces T-cell auto-reactivity and CNS demyelination PLoS One 6 2011 e16820