Neuroprotective effects of an oxyntomodulin analogue in the MPTP mouse model of Parkinson's disease

European Journal of Pharmacology

Volumn 765, Issue , 2015, Pages 284-290

  Liu, WeiZhen ^b   Li, Yanwei ^b   Jalewa, Jaishree ^a   Saunders Wood, Taylor ^a   Li, Lin ^b   Hölscher, Christian ^a,b  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b SHANXI MEDICAL UNIVERSITY   (China)

Author keywords

GLP 1; Glucagon; Growth factor; Incretin; Insulin; Mice; Neurodegeneration

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; OXYNTOMODULIN; PROTEIN BCL 2; PROTEIN KINASE B; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA; TYROSINE 3 MONOOXYGENASE; D-SER2-OXYNTOMODULIN; GLUCAGON LIKE PEPTIDE 1; NEUROPROTECTIVE AGENT;

ADULT; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; DOPAMINE METABOLISM; HYPOKINESIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LOCOMOTION; MALE; MOUSE; MUSCLE STRENGTH; NEUROPROTECTION; NONHUMAN; OPEN FIELD TEST; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ROTAROD TEST; SUBSTANTIA NIGRA; SWIMMING; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; PARKINSONIAN DISORDERS; PATHOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DOPAMINERGIC NEURONS; GLUCAGON-LIKE PEPTIDE 1; MALE; MICE, INBRED C57BL; MUSCLE STRENGTH; NEUROPROTECTIVE AGENTS; OXYNTOMODULIN; PARKINSONIAN DISORDERS; SUBSTANTIA NIGRA; SWIMMING; TYROSINE 3-MONOOXYGENASE;

EID: 84940650550     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2015.08.038     Document Type: Article

References (48)

1. I. Aviles-Olmos, J. Dickson, Z. Kefalopoulou, A. Djamshidian, P. Ell, T. Soderlund, P. Whitton, R. Wyse, T. Isaacs, A. Lees, P. Limousin, and T. Foltynie Exenatide and the treatment of patients with Parkinson's disease J. Clin. Investig. 123 2013 2730 2736
2. I. Aviles-Olmos, J. Dickson, Z. Kefalopoulou, A. Djamshidian, J. Kahan, P.E. Fmedsci, P. Whitton, R. Wyse, T. Isaacs, A. Lees, P. Limousin, and T. Foltynie Motor and cognitive advantages persist 12 months after exenatide exposure in Parkinson's disease J. Parkinson's Dis. 4 2014 337 344
3. W.A. Banks, J.B. Jaspan, and A.J. Kastin Selective, physiological transport of insulin across the blood-brain barrier: novel demonstration by species-specific radioimmunoassays Peptides 18 1997 1257 1262
4. W.A. Banks, A.J. Kastin, W. Huang, J.B. Jaspan, and L.M. Maness Leptin enters the brain by a saturable system independent of insulin Peptides 17 1996 305 311
5. G. Bertilsson, C. Patrone, O. Zachrisson, A. Andersson, K. Dannaeus, J. Heidrich, J. Kortesmaa, A. Mercer, E. Nielsen, H. Ronnholm, and L. Wikstrom 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. 86 2008 326 338
6. W. Bobela, L. Zheng, and B.L. Schneider Overview of mouse models of Parkinson's disease Curr. Protoc. Mouse Biol. 4 2014 121 139
7. 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.: Off. J. Soc. Neurosci. 22 2002 515 522
8. C. Clemmensen, J. Chabenne, B. Finan, L. Sullivan, K. Fischer, D. Kuchler, L. Sehrer, T. Ograjsek, S. Hofmann, S.S. Schriever, P.T. Pfluger, J. Pinkstaff, M.H. Tschop, R. Dimarchi, and T.D. Muller GLP-1/glucagon co-agonism restores leptin responsiveness in obese mice chronically maintained on an obesogenic diet Diabetes 63 2013 1422 1427
9. V. Darsalia, S. Mansouri, H. Ortsater, A. Olverling, N. Nozadze, C. Kappe, K. Iverfeldt, L.M. Tracy, N. Grankvist, A. Sjoholm, and C. Patrone Glucagon-like peptide-1 receptor activation reduces ischaemic brain damage following stroke in Type 2 diabetic rats Clin. Sci. (Lond.) 122 2012 473 483
10. J.L. Estall, and D.J. Drucker Glucagon and glucagon-like peptide receptors as drug targets Curr. Pharm. Des. 12 2006 1731 1750
11. M. Gerlach, P. Riederer, H. Przuntek, and M.B. Youdim MPTP mechanisms of neurotoxicity and their implications for Parkinson's disease Eur. J. Pharmacol. 208 1991 273 286
12. R. Giraldez-Perez, M. Antolin-Vallespin, M. Munoz, and A. Sanchez-Capelo Models of alpha-synuclein aggregation in Parkinson's disease Acta Neuropathol. Commun. 2 2014 176
13. V. Glover, C. Gibb, and M. Sandler The role of MAO in MPTP toxicity - a review J. Neural Transm. Suppl. 20 1986 S65 S76
14. 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. N. Y. Acad. Sci. 1035 2004 290 315
15. 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 19 2008 11 19
16. C. Holscher Central effects of GLP-1: new opportunities for treatments of neurodegenerative diseases J. Endocrinol. 221 2013 31 41
17. C. Holscher Insulin, incretins and other growth factors as potential novel treatments for Alzheimer's and Parkinson's diseases Biochem. Soc. Trans. 42 2014 593 599
18. J.J. Holst Treatment of type 2 diabetes mellitus with agonists of the GLP-1 receptor or DPP-IV inhibitors Expert Opin. Emerg. Drugs 9 2004 155 166
19. 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
20. A.J. Kastin, and V. Akerstrom Entry of exendin-4 into brain is rapid but may be limited at high doses Int. J. Obes. Relat. Metab. Disord.: J. Int. Assoc. Study Obes. 27 2003 313 318
21. 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
22. B.D. Kerr, P.R. Flatt, and V.A. Gault (d-Ser2)Oxm[mPEG-PAL]: a novel chemically modified analogue of oxyntomodulin with antihyperglycaemic, insulinotropic and anorexigenic actions Biochem. Pharmacol. 80 2010 1727 1735
23. S. Kim, M. Moon, and S. Park 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 2009 431 439
24. H. Kinemuchi, C.J. Fowler, and K.F. Tipton The neurotoxicity of 1-methyl-4-phenyl-1,2,3,6,-tetrahydropyridine (mptp) and its relevance to parkinson's disease Neurochem. Int. 11 1987 359 373
25. I.J. Kopin, and S.P. Markey MPTP toxicity: implications for research in Parkinson's disease Annu. Rev. Neurosci. 11 1988 81 96
26. J.W. Langston Parkinson's disease: current and future challenges Neurotoxicology 23 2002 443 450
27. 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. U. S. A. 106 2009 1285 1290
28. Y. Li, D. Tweedie, M.P. Mattson, H.W. Holloway, and N.H. Greig Enhancing the GLP-1 receptor signaling pathway leads to proliferation and neuroprotection in human neuroblastoma cells J. Neurochem. 113 2010 1621 1631
29. W. Liu, J. Jalewa, M. Sharma, G. Li, L. Li, and C. Hölscher Neuroprotective effects of lixisenatide and liraglutide in the MPTP mouse model of Parkinson's disease Neuroscience 303 2015 42 50
30. Y.L. Liu, H.E. Ford, M.R. Druce, J.S. Minnion, B.C. Field, J.C. Shillito, J. Baxter, K.G. Murphy, M.A. Ghatei, and S.R. Bloom Subcutaneous oxyntomodulin analogue administration reduces body weight in lean and obese rodents Int. J. Obes. (Lond.) 34 2010 1715 1725
31. F.C. Luo, S.D. Wang, L. Qi, J.Y. Song, T. Lv, and J. Bai Protective effect of panaxatriol saponins extracted from Panax notoginseng against MPTP-induced neurotoxicity in vivo J. Ethnopharmacol. 133 2011 448 453
32. 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.: Off. J. Soc. Neurosci. 31 2011 6587 6594
33. P.L. McClean, and C. Holscher Lixisenatide, a drug developed to treat type 2 diabetes, shows neuroprotective effects in a mouse model of Alzheimer's disease Neuropharmacology 86C 2014 241 258
34. A.L. Mickiewicz, and J.H. Kordower GDNF family ligands: a potential future for Parkinson's disease therapy CNS Neurol. Disord. Drug Targets 10 2011 703 711
35. T. Nagatsu, M. Mogi, H. Ichinose, and A. Togari Changes in cytokines and neurotrophins in Parkinson's disease J. Neural Transm. Suppl. 60 2000 S277 S290
36. S. Nakamura, and S.R. Vincent Histochemistry of MPTP oxidation in the rat brain: sites of synthesis of the parkinsonism-inducing toxin MPP+ Neurosci. Lett. 65 1986 321 325
37. T.A. Perry, and N.H. Greig A new Alzheimer's disease interventive strategy: GLP-1 Curr. Drug Targets 5 2004 565 571
38. A. Pocai Action and therapeutic potential of oxyntomodulin Mol. Metab. 3 2014 241 251
39. A. Santoprete, E. Capito, P.E. Carrington, A. Pocai, M. Finotto, A. Langella, P. Ingallinella, K. Zytko, S. Bufali, S. Cianetti, M. Veneziano, F. Bonelli, L. Zhu, E. Monteagudo, D.J. Marsh, R. Sinharoy, E. Bianchi, and A. Pessi DPP-IV-resistant, long-acting oxyntomodulin derivatives J. Pept. Sci. 17 2011 270 280
40. K. Sato, M. Kameda, T. Yasuhara, T. Agari, T. Baba, F. Wang, A. Shinko, T. Wakamori, A. Toyoshima, H. Takeuchi, T. Sasaki, S. Sasada, A. Kondo, C.V. Borlongan, M. Matsumae, and I. Date Neuroprotective effects of liraglutide for stroke model of rats Int. J. Mol. Sci. 14 2013 21513 21524
41. B.T. Schjoldager, F.G. Baldissera, P.E. Mortensen, J.J. Holst, and J. Christiansen Oxyntomodulin: a potential hormone from the distal gut. Pharmacokinetics and effects on gastric acid and insulin secretion in man Eur. J. Clin. Investig. 18 1988 499 503
42. M. Sharma, and C. Hölscher The neurophysiological and neuroprotective effects of leptin JSM Alzheimer's Dis. Relat. Dement. 1 2014 1009
43. T.S. Smith, and J.P. Bennett Jr. Mitochondrial toxins in models of neurodegenerative diseases. I: in vivo brain hydroxyl radical production during systemic MPTP treatment or following microdialysis infusion of methylpyridinium or azide ions Brain Res. 765 1997 183 188
44. T. Tan, and S. Bloom Gut hormones as therapeutic agents in treatment of diabetes and obesity Curr. Opin. Pharmacol. 13 2013 996 1001
45. D. Tweedie, L. Rachmany, V. Rubovitch, E. Lehrmann, Y. Zhang, K.G. Becker, E. Perez, J. Miller, B.J. Hoffer, N.H. Greig, and C.G. Pick Exendin-4, a glucagon-like peptide-1 receptor agonist prevents mTBI-induced changes in hippocampus gene expression and memory deficits in mice Exp. Neurol. 239 2013 170 182
46. N. Vrang, and P.J. Larsen Preproglucagon derived peptides GLP-1, GLP-2 and oxyntomodulin in the CNS: role of peripherally secreted and centrally produced peptides Prog. Neurobiol. 92 2010 442 462
47. D.C. Wu, V. Jackson-Lewis, M. Vila, K. Tieu, P. Teismann, C. Vadseth, D.K. Choi, H. Ischiropoulos, and S. Przedborski Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease J. Neurosci.: Off. J. Soc. Neurosci. 22 2002 1763 1771
48. Y.F. Zhang, Y.M. Chen, L. LI, and C. Hölscher Neuroprotective effects of (Val8)GLP-1-Glu-PAL in the MPTP Parkinson's disease mouse model Behav. Brain Res. 293 2015 107 113