Exendin-4 protects dopaminergic neurons by inhibition of microglial activation and matrix metalloproteinase-3 expression in an animal model of Parkinson's disease

Kim, Sehee; Moon, Minho; Park, Seungjoon

doi:10.1677/joe-09-0132

Cited by 263Parkinson's Disease Mechanisms and TreatmentsNeuroinflammation and Neurodegeneration MechanismsNuclear Receptors and Signaling

Exendin-4 protects dopaminergic neurons by inhibition of microglial activation and matrix metalloproteinase-3 expression in an animal model of Parkinson's disease

Kim, Sehee, Moon, Minho, Park, Seungjoon·2009·Journal of Endocrinology

DOI 10.1677/joe-09-0132

Open this paper in CoChat — free account

Abstract

Exendin-4 is a naturally occurring more potent and stable analog of glucagon-like peptide-1 (GLP-1) that selectively binds at the GLP-1 receptor. It has been recently demonstrated that GLP-1 receptor stimulation preserves dopaminergic neurons in cellular and rodent models of Parkinson's disease (PD). 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) causes nigrostriatal dopaminergic neurotoxicity in rodents; previous studies suggest that activated microglia actively participate in the pathogenesis of PD neurodegeneration. However, the role of microglia in the neuroprotective properties of exendin-4 is still unknown. Here, we show that, in the mouse MPTP PD model, systemic administration of exendin-4 significantly attenuates the loss of substantia nigra pars compacta (SNpc) neurons and the striatal dopaminergic fibers. Exendin-4 prevents MPTP-induced microglial activation in the SNpc and striatum, and the expression of matrix metalloproteinase-3. In addition, exendin-4 also suppressed MPTP-induced expression of pro-inflammatory molecules and tumor necrosis factor α and interleukin-1β. Our data indicate that exendin-4 may act as a survival factor for dopaminergic neurons by functioning as a microglia-deactivating factor and suggest that exendin-4 may be a valuable therapeutic agent for neurodegenerative diseases such as PD.

Integrity signals

Registry

Crossref · 10.1677/joe-09-0132

Cites

55 of 55 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Exendin-4 (10 μg/kg) treatment significantly decreased MPTP-induced microglial activation and suppressed MPTP-induced expression of TNF-α and IL-1β.
“Exendin-4 (10 μg/kg) treatment significantly decreased MPTP-induced microglial activation and suppressed MPTP-induced expression of TNF-α and IL-1β [94].”
From Anti-Inflammatory Effects of GLP-1-Based Therapies beyond Glucose Control (2016) · cites this paper as [94]

The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
A JOURNAL OF PHARMACOLOGY AND EXPERIMENTAL THERAPEUTICS
Lindemann, L., Jaeschke, G., Michalon, A., Vieira, E., Honer, M., Spooren, W., Porter, R., Hartung, T., Kolczewski, S., Büttelmann, B., et al. (1909) · JAMA · doi:10.1001/jama.1909.02550020033007 · Cited by 7,865 · see citing works
Microglia-mediated neurotoxicity: uncovering the molecular mechanisms
Block, M. L., Zecca, L., & Hong, J.-S. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2038 · Cited by 4,110 · see citing works
Biology of Incretins: GLP-1 and GIP
Baggio, L. L., & Drucker, D. J. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.03.054 · Cited by 3,639 · see citing works
Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · see citing works
Blockade of Microglial Activation Is Neuroprotective in the 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine Mouse Model of Parkinson Disease
Wu, D. C., Jackson-Lewis, V., Vila, M., Tieu, K., Teismann, P., Vadseth, C., Choi, D.-K., Ischiropoulos, H., & Przedborski, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01763.2002 · Cited by 1,183 · see citing works
Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease
Liberatore, G. T., Jackson-Lewis, V., Vukosavic, S., Mandir, A. S., Vila, M., McAuliffe, W. G., Dawson, V. L., Dawson, T. M., & Przedborski, S. (1999) · Nature Medicine · doi:10.1038/70978 · Cited by 1,046 · cited 4× · see citing works
“Microglia-derived NO-mediated nitrate stress plays a pivotal role in the pathogenesis of PD, which is supported by the demonstration that MPTP-induced SNpc dopaminergic neuron loss and the production of ventral midbrain nitrotyrosine are attenuated in mice lacking the iNOS gene (Liberatore et al. 1999).”
Influential
Cytotoxicity of microglia
Banati, R. B., Gehrmann, J., Schubert, P., & Kreutzberg, G. W. (1993) · Glia · doi:10.1002/glia.440070117 · Cited by 1,020 · see citing works
MICROGLIA AS MEDIATORS OF INFLAMMATORY AND DEGENERATIVE DISEASES
González-Scarano, F., & Baltuch, G. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.219 · Cited by 984 · see citing works
Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP.
D'Mello, S. R., Galli, C., Ciotti, T., & Calissano, P. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.23.10989 · Cited by 892 · see citing works
Interleukin-1β, interleukin-6, epidermal growth factor and transforming growth factor-α are elevated in the brain from parkinsonian patients
Mogi, M., Harada, M., Kondo, T., Riederer, P., Inagaki, H., Minami, M., & Nagatsu, T. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90508-8 · Cited by 855 · see citing works
Glucagon-like peptide-1 receptor is involved in learning and neuroprotection
During, M. J., Cao, L., Zuzga, D. S., Francis, J. S., Fitzsimons, H. L., Jiao, X., Bland, R. J., Klugmann, M., Banks, W. A., Drucker, D. J., et al. (2003) · Nature Medicine · doi:10.1038/nm919 · Cited by 851 · see citing works
Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease
Kim, Y. S., & Joh, T. H. (2006) · Experimental & Molecular Medicine · doi:10.1038/emm.2006.40 · Cited by 655 · see citing works
Nitric oxide synthase and neuronal vulnerability in parkinson's disease
Hunot, S., Boissière, F., Faucheux, B., Brugg, B., Mouatt-Prigent, A., Agid, Y., & Hirsch, E. C. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00578-1 · Cited by 595 · see citing works
GLP-1 receptor stimulation preserves primary cortical and dopaminergic neurons in cellular and rodent models of stroke and Parkinsonism
Li, Y., Perry, T., Kindy, M. S., Harvey, B. K., Tweedie, D., Holloway, H. W., Powers, K., Shen, H., Egan, J. M., Sambamurti, K., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806720106 · Cited by 589 · see citing works
Glucagon-like Peptide-1 Receptor Signaling Modulates β Cell Apoptosis
Li, Y., Hansotia, T., Yusta, B., Ris, F., Halban, P. A., & Drucker, D. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209423200 · Cited by 589 · see citing works
Minireview: Glucagon-Like Peptides Regulate Cell Proliferation and Apoptosis in the Pancreas, Gut, and Central Nervous System
Brubaker, P. L., & Drucker, D. J. (2004) · Endocrinology · doi:10.1210/en.2004-0015 · Cited by 539 · see citing works
Distribution of GLP‐1 Binding Sites in the Rat Brain: Evidence that Exendin‐4 is a Ligand of Brain GLP‐1 Binding Sites
Göke, R., Larsen, P. J., Mikkelsen, J. D., & Sheikh, S. P. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb00650.x · Cited by 474 · see citing works
Protection and Reversal of Excitotoxic Neuronal Damage by Glucagon-Like Peptide-1 and Exendin-4
Perry, T., Haughey, N. J., Mattson, M. P., Egan, J. M., & Greig, N. H. (2002) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.037481 · Cited by 380 · see citing works
Mice deficient in TNF receptors are protected against dopaminergic neurotoxicity: Implications for Parkinson's disease
Sriram, K., Matheson, J. M., Benkovic, S. A., Miller, D. B., Luster, M. I., & O'Callaghan, J. P. (2002) · The FASEB Journal · doi:10.1096/fj.02-0216fje · Cited by 364 · see citing works
Cellular pathology of Parkinson?s disease: astrocytes, microglia and inflammation
Teismann, P., & Schulz, J. B. (2004) · Cell and Tissue Research · doi:10.1007/s00441-004-0944-0 · Cited by 363 · see citing works
Entry of exendin-4 into brain is rapid but may be limited at high doses
Kastin, A., & Akerstrom, V. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802206 · Cited by 362 · see citing works
Naloxone Protects Rat Dopaminergic Neurons against Inflammatory Damage through Inhibition of Microglia Activation and Superoxide Generation
Liu, B., Du, L., & Hong, J.-S. (2000) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)39275-4 · Cited by 347 · cited 1× · see citing works
“In fact, it has been demonstrated that several agents have neuroprotective effects due to their ability to suppress the microglial activation in several PD models (Liu et al. 2000, 2003, Wu et al. 2002, Delgado & Ganea 2003).”
Glucagon‐like peptide‐1 decreases endogenous amyloid‐β peptide (Aβ) levels and protects hippocampal neurons from death induced by Aβ and iron
Perry, T., Lahiri, D. K., Sambamurti, K., Chen, D., Mattson, M. P., Egan, J. M., & Greig, N. H. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10611 · Cited by 347 · see citing works
Peptide hormone exendin‐4 stimulates subventricular zone neurogenesis in the adult rodent brain and induces recovery in an animal model of parkinson's disease
Bertilsson, G., Patrone, C., Zachrisson, O., Andersson, A., Dannaeus, K., Heidrich, J., Kortesmaa, J., Mercer, A., Nielsen, E., Rönnholm, H., et al. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21483 · Cited by 345 · see citing works
Deficiency of Inducible Nitric Oxide Synthase Protects Against MPTP Toxicity In Vivo
Dehmer, T., Lindenau, J. H., Haid, S., DICHGANS, J., & Schulz, J. B. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0742213.x · Cited by 337 · see citing works
Glial cells and inflammation in parkinson's disease: A role in neurodegeneration?
Hirsch, É. C., Hunot, S., Damier, P., & Faucheux, B. A. (1998) · Annals of Neurology · doi:10.1002/ana.410440717 · Cited by 334 · see citing works
Cytokines in Parkinson’s disease
Nagatsu, T., Mogi, M., Ichinose, H., & Togari, A. (2000) · Springer eBooks · doi:10.1007/978-3-7091-6284-2_12 · Cited by 327 · see citing works
The role of glial cells in Parkinsonʼs disease
Vila, M., Jackson-Lewis, V., Guégan, C., Chu Wu, D., Teismann, P., Choi, D.-K., Tieu, K., & Przedborski, S. (2001) · Current Opinion in Neurology · doi:10.1097/00019052-200108000-00009 · Cited by 326 · see citing works
A novel neurotrophic property of glucagon-like peptide 1: a promoter of nerve growth factor-mediated differentiation in PC12 cells.
Perry, T., Lahiri, D., Chen, D., Zhou, J., Shaw, K., Egan, J., & Greig, N. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.300.3.958 · Cited by 306 · see citing works
Glucagon-like peptide 1 receptor stimulation reverses key deficits in distinct rodent models of Parkinson's disease
Harkavyi, A., Abuirmeileh, A. N., Lever, R., Kingsbury, A. E., Biggs, C. S., & Whitton, P. S. (2008) · Journal of Neuroinflammation · doi:10.1186/1742-2094-5-19 · Cited by 290 · see citing works
Pathogenic role of glial cells in Parkinson's disease
Teismann, P., Tieu, K., Cohen, O. S., Choi, D., Wu, D. C., Marks, D., Vila, M., Jackson-Lewis, V. R., & Przedborski, S. (2002) · Movement Disorders · doi:10.1002/mds.10332 · Cited by 272 · see citing works
Matrix Metalloproteinase-3: A Novel Signaling Proteinase from Apoptotic Neuronal Cells That Activates Microglia
Kim, Y.-S., Kim, S. S., Cho, J., Choi, D.-H., Hwang, O., Shin, D., Hong, S.-C., Beal, M., & Joh, T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4346-04.2005 · Cited by 272 · see citing works
Self-citation
Cyclic AMP Elevation Is Sufficient to Promote the Survival of Spinal Motor NeuronsIn Vitro
Hanson, M. G., Shen, S., Wiemelt, A. P., McMorris, F. A., & Barres, B. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07361.1998 · Cited by 216 · see citing works
Glucagon-like peptide-1 inhibits LPS-induced IL-1β production in cultured rat astrocytes
Iwai, T., Ito, S., Tanimitsu, K., Udagawa, S., & Oka, J.-I. (2006) · Neuroscience Research · doi:10.1016/j.neures.2006.04.008 · Cited by 207 · see citing works
Dextromethorphan Protects Dopaminergic Neurons against Inflammation-Mediated Degeneration through Inhibition of Microglial Activation
Liu, Y., Qin, L., Li, G., Zhang, W., An, L., Liu, B., & Hong, J. (2003) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.043166 · Cited by 205 · see citing works
A pivotal role of matrix metalloproteinase‐3 activity in dopaminergic neuronal degeneration via microglial activation
Kim, Y. S., Choi, D. H., Block, M. L., Lorenzl, S., Yang, L., Kim, Y., Sugama, S., Cho, B. P., Hwang, O., Browne, S. E., et al. (2006) · The FASEB Journal · doi:10.1096/fj.06-5865com · Cited by 199 · see citing works
Self-citation
Evidence of GLP-1-mediated neuroprotection in an animal model of pyridoxine-induced peripheral sensory neuropathy
Perry, T., Holloway, H. W., Weerasuriya, A., Mouton, P. R., Duffy, K. B., Mattison, J. A., & Greig, N. H. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.09.028 · Cited by 183 · see citing works
Neuroprotective effect of vasoactive intestinal peptide (VIP) in a mouse model of Parkinson's disease by blocking microglial activation
Delgado, M., & Ganea, D. (2003) · The FASEB Journal · doi:10.1096/fj.02-0799fje · Cited by 166 · see citing works
Glucagon-Like Peptide-1
Doyle, M. E. (2001) · Recent Progress in Hormone Research · doi:10.1210/rp.56.1.377 · Cited by 156 · see citing works
Glucagon-like peptide-1: a major regulator of pancreatic beta-cell function
Perfetti, R., & Merkel, P. A. (2000) · European Journal of Endocrinology · doi:10.1530/eje.0.1430717 · Cited by 143 · see citing works
IL-1β, IL-2, IL-6 and TNF-α production by peripheral blood mononuclear cells from patients with Parkinson's disease
Bessler, H., Djaldetti, R., Salman, H., Bergman, M., & Djaldetti, M. (1999) · Biomedicine & Pharmacotherapy · doi:10.1016/s0753-3322(99)80079-1 · Cited by 135 · see citing works
Enhancing Central Nervous System Endogenous GLP-1 Receptor Pathways for Intervention in Alzheimers Disease
Perry, T., & Greig, N. (2005) · Current Alzheimer Research · doi:10.2174/1567205054367892 · Cited by 127 · see citing works
A novel intracellular role of matrix metalloproteinase‐3 during apoptosis of dopaminergic cells
Choi, D. H., Kim, E., Son, H. J., JOH, T. H., Kim, Y. S., Kim, D., Beal, M. F., & Hwang, O. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05399.x · Cited by 124 · see citing works
The glucagon-like peptides: a double-edged therapeutic sword?
Perry, T., & Greig, N. H. (2003) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(03)00160-3 · Cited by 114 · see citing works
Parkinson’s Disease: Current and Future Challenges
Langston, J. W. (2002) · NeuroToxicology · doi:10.1016/s0161-813x(02)00098-0 · Cited by 109 · see citing works
Modulation of microglial pro-inflammatory and neurotoxic activity for the treatment of Parkinson’s disease
Liu, B. (2006) · The AAPS Journal · doi:10.1208/aapsj080369 · Cited by 100 · see citing works
Colocalization of calbindin D-28k, calretinin, and GABA immunoreactivities in neurons of the human temporal cortex
del R�o, M. R., & DeFelipe, J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960603)369:3 · Cited by 97 · see citing works
Hypothalamic/Pituitary-Axis of the Spontaneous Dwarf Rat: Autofeedback Regulation of Growth Hormone (GH) Includes Suppression of GH Releasing-Hormone Receptor Messenger Ribonucleic Acid
Kamegai, J., Unterman, T. G., Frohman, L. A., & Kineman, R. D. (1998) · Endocrinology · doi:10.1210/endo.139.8.6136 · Cited by 70 · see citing works
Effects of Dibutyryl Cyclic AMP and Retinoic Acid on the Differentiation of Dopamine Neurons: Prevention of Cell Death by Dibutyryl Cyclic AMP
Mena, M. A., Casarejos, M. J., Bonnin, A., Ramos, J. A., & de Yébenes, J. G. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.65062612.x · Cited by 55 · see citing works
Cytokines in Parkinson’s Disease
Nagatsu, T., & Mogi, M. (1998) · Advances in behavioral biology · doi:10.1007/978-1-4615-5337-3_58 · Cited by 53 · see citing works
Fasting-induced changes in the hypothalamic-pituitary-GH axis in the absence of GH expression: lessons from the spontaneous dwarf rat
Park, S., Sohn, S., & Kineman, R. D. (2004) · Journal of Endocrinology · doi:10.1677/joe.0.1800369 · Cited by 48 · see citing works
Self-citation
Art and artifice in the science of histology
RIO‐HORTEGA, P. D. (1993) · Histopathology · doi:10.1111/j.1365-2559.1993.tb00171.x · Cited by 27 · see citing works
Pathogenic role of glial cells in Parkinson's disease
Przedborski, S., & Goldman, J. E. (2003) · Advances in molecular and cell biology · doi:10.1016/s1569-2558(03)31043-4 · Cited by 15 · see citing works
Cytotoxicity of microglia
Banati, R. B., & Kreutzberg, G. W. (1992) · Journal of Neuroimmunology · doi:10.1016/0165-5728(92)90227-c · Cited by 10 · see citing works

Flagged first, then by citations

Sorted by citations

Glucagon-like peptide 1 (GLP-1)
Müller, T. D., Finan, B., Bloom, S. R., D'Alessio, D., Drucker, D. J., Flatt, P. R., Fritsche, A., Gribble, F., Grill, H. J., Habener, J. F., et al. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.09.010 · Cited by 1,868 · see citing works
Pharmacology, physiology, and mechanisms of incretin hormone action.
Campbell, J. E., & Drucker, D. J. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.04.008 · Cited by 1,500 · see citing works
Block of A1 astrocyte conversion by microglia is neuroprotective in models of Parkinson’s disease
Yun, S. P., Kam, T.-I., Panicker, N., Kim, S., Oh, Y., Park, J.-S., Kwon, S.-H., Park, Y. J., Karuppagounder, S. S., Park, H., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0051-5 · Cited by 1,123 · see citing works
Self-citation
Exenatide once weekly versus placebo in Parkinson's disease: a randomised, double-blind, placebo-controlled trial
Athauda, D., Maclagan, K., Skene, S. S., Bajwa-Joseph, M., Letchford, D., Chowdhury, K., Hibbert, S., Budnik, N., Zampedri, L., Dickson, J., et al. (2017) · The Lancet · doi:10.1016/s0140-6736(17)31585-4 · Cited by 889 · see citing works
Exenatide and the treatment of patients with Parkinson's disease
Aviles-Olmos, I., Dickson, J., Kefalopoulou, Z., Djamshidian, A., Ell, P., Soderlund, T., Whitton, P., Wyse, R., Isaacs, T., Lees, A., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci68295 · Cited by 529 · see citing works
Anti-Inflammatory Effects of GLP-1-Based Therapies beyond Glucose Control
Lee, Y.-S., & Jun, H.-S. (2016) · Mediators of Inflammation · doi:10.1155/2016/3094642 · Cited by 503 · see citing works
“Sitagliptin (10mg/kg/day) treatment decreased the expression of proinflammatory cytokine genes IL-1𝛽 and TNF-𝛼 in kidney of diabetic ZDF rat [25].”
BackgroundInfluential
GLP-1 Receptor Agonists: Beyond Their Pancreatic Effects
Zhao, X., Wang, M., Wen, Z., Lu, Z., Cui, L., Fu, C., Xue, H., Liu, Y., & Zhang, Y. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.721135 · Cited by 463 · see citing works
Glucagon-Like Peptide-1 and Its Class B G Protein–Coupled Receptors: A Long March to Therapeutic Successes
Graaf, C. D., Donnelly, D., Wootten, D., Lau, J., Sexton, P. M., Miller, L. J., Ahn, J.-M., Liao, J., Fletcher, M. M., Yang, D., et al. (2016) · Pharmacological Reviews · doi:10.1124/pr.115.011395 · Cited by 403 · see citing works
The glucagon-like peptide 1 (GLP) receptor as a therapeutic target in Parkinson's disease: mechanisms of action
Athauda, D., & Foltynie, T. (2016) · Drug Discovery Today · doi:10.1016/j.drudis.2016.01.013 · Cited by 383 · see citing works
Insulin resistance and Parkinson’s disease: A new target for disease modification?
Athauda, D. S., & Foltynie, T. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.10.001 · Cited by 333 · see citing works
Insulin, IGF-1 and GLP-1 signaling in neurodegenerative disorders: Targets for disease modification?
Bassil, F., Fernagut, P., Bézard, E., & Meissner, W. G. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.02.005 · Cited by 313 · see citing works
Motor and Cognitive Advantages Persist 12 Months After Exenatide Exposure in Parkinson’s Disease
Avilés-Olmos, I., Dickson, J. C., Kefalopoulou, Z. M., Djamshidian, A., Kahan, J., Ell, P. J., Whitton, P. S., Wyse, R. K. H., Isaacs, T., Lees, A. J., et al. (2014) · Journal of Parkinson s Disease · doi:10.3233/jpd-140364 · Cited by 300 · see citing works
Microglial phenotypes in Parkinson’s disease and animal models of the disease
Joers, V., Tansey, M. G., Mulas, G., & Carta, A. R. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.04.006 · Cited by 285 · see citing works
Parkinson's disease, insulin resistance and novel agents of neuroprotection
Avilés-Olmos, I., Limousin, P. D., Lees, A. J., & Foltynie, T. (2012) · Brain · doi:10.1093/brain/aws009 · Cited by 284 · see citing works
The ongoing pursuit of neuroprotective therapies in Parkinson disease
Athauda, D. S., & Foltynie, T. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.226 · Cited by 267 · see citing works
Hormones and diet, but not body weight, control hypothalamic microglial activity
Gao, Y., Ottaway, N., Schriever, S. C., Legutko, B., García‐Cáceres, C., de la Fuente, E., Mergen, C., Bour, S., Thaler, J. P., Seeley, R. J., et al. (2013) · Glia · doi:10.1002/glia.22580 · Cited by 265 · see citing works
Neuroprotective and neurotrophic actions of glucagon‐like peptide‐1: an emerging opportunity to treat neurodegenerative and cerebrovascular disorders
Salcedo, I., Tweedie, D., Li, Y., & Greig, N. H. (2012) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2012.01971.x · Cited by 263 · see citing works
The neuroprotective effects of glucagon-like peptide 1 in Alzheimer’s and Parkinson’s disease: An in-depth review
Reich, N., & Hölscher, C. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.970925 · Cited by 248 · see citing works
Neuroprotective effects of lixisenatide and liraglutide in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson’s disease
Liu, W., Jalewa, J., Sharma, M., Li, G., Li, L., & Hölscher, C. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.06.054 · Cited by 246 · see citing works
Neuroprotective effects of vildagliptin in rat rotenone Parkinson's disease model: role of RAGE ‐ NF κB and Nrf2‐antioxidant signaling pathways
Abdelsalam, R. M., & Safar, M. M. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13087 · Cited by 222 · see citing works
Brain uptake pharmacokinetics of incretin receptor agonists showing promise as Alzheimer’s and Parkinson’s disease therapeutics
Salameh, T. S., Rhea, E. M., Talbot, K., & Banks, W. A. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.114187 · Cited by 188 · see citing works
The central GLP-1: implications for food and drug reward
Skibicka, K. P. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00181 · Cited by 188 · see citing works
Antidiabetic agents as a novel treatment for Alzheimer’s and Parkinson’s disease
Nowell, J., Blunt, E., Gupta, D., & Edison, P. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.101979 · Cited by 179 · see citing works
Semaglutide is Neuroprotective and Reduces α-Synuclein Levels in the Chronic MPTP Mouse Model of Parkinson’s Disease
Zhang, L., Zhang, L., Li, L., & Hölscher, C. (2019) · Journal of Parkinson's Disease · doi:10.3233/jpd-181503 · Cited by 173 · see citing works
The Diabetes Drug Liraglutide Ameliorates Aberrant Insulin Receptor Localisation and Signalling in Parallel with Decreasing Both Amyloid-β Plaque and Glial Pathology in a Mouse Model of Alzheimer’s Disease
Long-Smith, C. M., Manning, S., McClean, P. L., Coakley, M. F., O’Halloran, D., Hölscher, C., & O’Neill, C. (2012) · NeuroMolecular Medicine · doi:10.1007/s12017-012-8199-5 · Cited by 156 · see citing works
The extra‐pancreatic effects of <scp>GLP‐1</scp> receptor agonists: a focus on the cardiovascular, gastrointestinal and central nervous systems
Seufert, J., & Gallwitz, B. (2014) · Diabetes, Obesity and Metabolism · doi:10.1111/dom.12251 · Cited by 156 · see citing works
A Synopsis on the Role of Tyrosine Hydroxylase in Parkinson’s Disease
Tabrez, S. S. M., Jabir, N. R., Shakil, S., Greig, N. H., Alam, Q., Abuzenadah, A. M., Damanhouri, G., & Kamal, M. A. (2012) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152712800792785 · Cited by 152 · see citing works
Neuroprotective properties of GLP-1: theoretical and practical applications
Holst, J. J., Burcelin, R., & Nathanson, E. (2011) · Current Medical Research and Opinion · doi:10.1185/03007995.2010.549466 · Cited by 152 · see citing works
The glucagon-like peptide 1 receptor agonist exendin-4 improves reference memory performance and decreases immobility in the forced swim test
Isacson, R., Nielsen, E. I., Dannaeus, K., Bertilsson, G., Patrone, C., Zachrisson, O., & Wikström, L. (2010) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2010.10.008 · Cited by 150 · see citing works
Neuroprotective effects of the novel GLP-1 long acting analogue semaglutide in the MPTP Parkinson's disease mouse model
Zhang, L., Zhang, L., Li, L., & Hölscher, C. (2018) · Neuropeptides · doi:10.1016/j.npep.2018.07.003 · Cited by 151 · see citing works
Anti-Inflammatory Effects of GLP-1 Receptor Activation in the Brain in Neurodegenerative Diseases
Diz-Chaves, Y., Mastoor, Z., Spuch, C., González-Matías, L. C., & Mallo, F. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23179583 · Cited by 148 · see citing works
The DPP-4 Inhibitor Linagliptin Counteracts Stroke in the Normal and Diabetic Mouse Brain
Darsalia, V., Ortsäter, H., Olverling, A., Darlöf, E., Wolbert, P., Nyström, T., Klein, T., Sjöholm, Å., & Patrone, C. (2012) · Diabetes · doi:10.2337/db12-0988 · Cited by 147 · see citing works
Diet in Parkinson’s Disease: Critical Role for the Microbiome
Jackson, A., Forsyth, C. B., Shaikh, M., Voigt, R. M., Engen, P. A., Ramirez, V., & Keshavarzian, A. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.01245 · Cited by 145 · see citing works
Protective properties of GLP‐1 and associated peptide hormones in neurodegenerative disorders
Hölscher, C. (2021) · British Journal of Pharmacology · doi:10.1111/bph.15508 · Cited by 147 · see citing works
Crosstalk between diabetes and brain: Glucagon-like peptide-1 mimetics as a promising therapy against neurodegeneration
Duarte, A. I., Candeias, E., Correia, S. C., Santos, R. X., Carvalho, C., Cardoso, S., Plácido, A. I., Santos, M. S., Oliveira, C. R., & Moreira, P. I. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.01.008 · Cited by 142 · see citing works
G lycation in P arkinson's disease and Alzheimer's disease
Miranda, H. V., El‐Agnaf, O. M. A., & Outeiro, T. F. (2016) · Movement Disorders · doi:10.1002/mds.26566 · Cited by 142 · see citing works
The Promise of Neuroprotective Agents in Parkinson?s Disease
Seidl, S. E., & Potashkin, J. A. (2011) · Frontiers in Neurology · doi:10.3389/fneur.2011.00068 · Cited by 141 · see citing works
A New Treatment Strategy for Parkinson's Disease through the Gut–Brain Axis: The Glucagon-Like Peptide-1 Receptor Pathway
Kim, D. S., Choi, H.-I., Wang, Y., Luo, Y., Hoffer, B. J., & Greig, N. H. (2017) · Cell Transplantation · doi:10.1177/0963689717721234 · Cited by 136 · see citing works
Incretin and insulin signaling as novel therapeutic targets for Alzheimer’s and Parkinson’s disease
Nowell, J., Blunt, E., & Edison, P. (2023) · Molecular Psychiatry · doi:10.1038/s41380-022-01792-4 · Cited by 136 · see citing works
Exendin-4 Ameliorates Motor Neuron Degeneration in Cellular and Animal Models of Amyotrophic Lateral Sclerosis
Li, Y., Chigurupati, S., Holloway, H. W., Mughal, M. R., Tweedie, D., Bruestle, D. A., Mattson, M. P., Wang, Y., Harvey, B. K., Ray, B., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032008 · Cited by 131 · see citing works
Glucagon-like peptide-1 receptor activation reduces ischaemic brain damage following stroke in Type 2 diabetic rats
Darsalia, V., Mansouri, S., Ortsäter, H., Olverling, A., Nozadze, N., Krizhanovskii, C., Iverfeldt, K., Tracy, L. M., Grankvist, N., Sjöholm, Å., et al. (2011) · Clinical Science · doi:10.1042/cs20110374 · Cited by 129 · see citing works
Emerging Treatment Approaches for Parkinson’s Disease
Stoker, T. B., Torsney, K., & Barker, R. A. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00693 · Cited by 128 · see citing works
GLP-1’s role in neuroprotection: a systematic review
Erbil, D., Eren, C. Y., Demirel, Ç., Küçüker, M. U., Solaroğlu, İ., & Eser, H. Y. (2019) · Brain Injury · doi:10.1080/02699052.2019.1587000 · Cited by 128 · see citing works
Pharmacologically reversible zonation-dependent endothelial cell transcriptomic changes with neurodegenerative disease associations in the aged brain
Zhao, L., Li, Z., Vong, J. S. L., Chen, X., Lai, H. M., Yan, L. Y. C., Huang, J., Sy, S. K. H., Tian, X. Y., Huang, Y., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18249-3 · Cited by 119 · see citing works
Activation of Glucagon-Like Peptide-1 Receptor Promotes Neuroprotection in Experimental Autoimmune Encephalomyelitis by Reducing Neuroinflammatory Responses
Lee, C., Jeon, S. J., Cho, K. S., Moon, E., Sapkota, A., Jun, H., Ryu, J. H., & Choi, J. W. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0550-2 · Cited by 126 · see citing works
Sitagliptin and liraglutide reversed nigrostriatal degeneration of rodent brain in rotenone-induced Parkinson’s disease
Badawi, G. A., Fattah, M. A. A. E., Zaki, H. F., & Sayed, M. I. E. (2017) · Inflammopharmacology · doi:10.1007/s10787-017-0331-6 · Cited by 123 · see citing works
Saxagliptin: A novel antiparkinsonian approach
Nassar, N. N., Al‐Shorbagy, M. Y., Arab, H. H., & Abdallah, D. M. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.10.007 · Cited by 122 · see citing works
Doxycycline restrains glia and confers neuroprotection in a 6‐OHDA Parkinson model
Lazzarini, M., Martin, S., Mitkovski, M., Raisman‐Vozari, R., Stühmer, W., & Bel, E. D. (2013) · Glia · doi:10.1002/glia.22496 · Cited by 119 · see citing works
Ischemia‐induced changes in glucagon‐like peptide‐1 receptor and neuroprotective effect of its agonist, exendin‐4, in experimental transient cerebral ischemia
Lee, C. H., Yan, B., Yoo, K., Choi, J. H., Kwon, S., Her, S., Sohn, Y., Hwang, I. K., Cho, J. H., Kim, Y., et al. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22596 · Cited by 118 · see citing works
Understanding the Links Between Cardiovascular Disease and Parkinson's Disease
Potashkin, J., Huang, X., Becker, C., Chen, H., Foltynie, T., & Marras, C. (2019) · Movement Disorders · doi:10.1002/mds.27836 · Cited by 117 · see citing works
The gut microbiota regulates hypothalamic inflammation and leptin sensitivity in Western diet-fed mice via a GLP-1R-dependent mechanism
Heiss, C. N., Mannerås-Holm, L., Lee, Y. S., Serrano-Lobo, J., Håkansson Gladh, A., Seeley, R. J., Drucker, D. J., Bäckhed, F., & Olofsson, L. E. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109163 · Cited by 114 · see citing works
Role of matrix metalloproteinase-3 in neurodegeneration
Kim, E., & Hwang, O. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07082.x · Cited by 114 · see citing works
Imaging of microglia in patients with neurodegenerative disorders
Politis, M. (2012) · Frontiers in Pharmacology · doi:10.3389/fphar.2012.00096 · Cited by 111 · see citing works
The Relevance of Insulin Action in the Dopaminergic System
Fiory, F., Perruolo, G., Cimmino, I., Cabaro, S., Pignalosa, F. C., Miele, C., Bèguinot, F., Formisano, P., & Oriente, F. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00868 · Cited by 114 · see citing works
Neuroprotective effects of geniposide in the MPTP mouse model of Parkinson's disease
Chen, Y., Zhang, Y., Li, L., & Hölscher, C. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.09.029 · Cited by 111 · see citing works
Gut hormone polyagonists for the treatment of type 2 diabetes
Brandt, S. J., Götz, A., Tschöp, M. H., & Müller, T. D. (2018) · Peptides · doi:10.1016/j.peptides.2017.12.021 · Cited by 108 · see citing works
Exendin-4 and sitagliptin protect kidney from ischemia-reperfusion injury through suppressing oxidative stress and inflammatory reaction
Chen, Y.-T., Tsai, T., Yang, C.-C., Sun, C., Chang, L., Chen, H.-H., Chang, C.-L., Sung, P., Zhen, Y., Leu, S., et al. (2013) · Journal of Translational Medicine · doi:10.1186/1479-5876-11-270 · Cited by 109 · see citing works
Novel targeted therapies for Parkinson’s disease
Ntetsika, T., Papathoma, P.-E., & Markaki, I. (2021) · Molecular Medicine · doi:10.1186/s10020-021-00279-2 · Cited by 112 · see citing works
Effects of glucagon-like peptide-1 receptor agonists on non-alcoholic fatty liver disease and inflammation
Wang, X.-C. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i40.14821 · Cited by 109 · see citing works
A novel dual GLP-1 and GIP receptor agonist is neuroprotective in the MPTP mouse model of Parkinson′s disease by increasing expression of BNDF
Ji, C., Xue, G., Cao, L., Feng, P., Li, D., Li, L., Li, G., & Hölscher, C. (2015) · Brain Research · doi:10.1016/j.brainres.2015.09.035 · Cited by 101 · see citing works
The cardioprotective effect of melatonin and exendin‐4 treatment in a rat model of cardiorenal syndrome
Chua, S. O., Lee, F., Chiang, H., Chen, K., Lu, H., Chen, Y., Yang, C., Lin, K., Chen, Y., Kao, G., et al. (2016) · Journal of Pineal Research · doi:10.1111/jpi.12357 · Cited by 99 · see citing works
Protective effects of the GLP-1 mimetic exendin-4 in Parkinson's disease
Athauda, D. S., & Foltynie, T. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.09.023 · Cited by 97 · see citing works
MMP-3 Contributes to Nigrostriatal Dopaminergic Neuronal Loss, BBB Damage, and Neuroinflammation in an MPTP Mouse Model of Parkinson’s Disease
Chung, Y. C., Kim, Y.-S., Bok, E., Yune, T. Y., Maeng, S., & Jin, B. K. (2013) · Mediators of Inflammation · doi:10.1155/2013/370526 · Cited by 94 · see citing works
Glucagon-like peptide-1 class drugs show clear protective effects in Parkinson's and Alzheimer's disease clinical trials: A revolution in the making?
Hölscher, C. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.109952 · Cited by 94 · see citing works
The Gut Hormones in Appetite Regulation
Suzuki, K., Jayasena, C. N., & Bloom, S. R. (2011) · Journal of Obesity · doi:10.1155/2011/528401 · Cited by 92 · see citing works
A novel dual GLP-1 and GIP incretin receptor agonist is neuroprotective in a mouse model of Parkinson’s disease by reducing chronic inflammation in the brain
Cao, L., Li, D., Feng, P., Li, L., Xue, G., Li, G., & Hölscher, C. (2016) · Neuroreport · doi:10.1097/wnr.0000000000000548 · Cited by 90 · see citing works
Glucose metabolism impairment in Parkinson’s disease
Dai, C., Tan, C., Zhao, L., Liang, Y., Liu, G., Liu, H., Zhong, Y., Liu, Z., Mo, L., Liu, X., et al. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.110672 · Cited by 89 · see citing works
System-based approaches to decode the molecular links in Parkinson's disease and diabetes
Santiago, J. A., & Potashkin, J. A. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.03.019 · Cited by 85 · see citing works
The Role of Glucagon-Like Peptide-1 Receptor Agonists (GLP-1 RA) in Diabetes-Related Neurodegenerative Diseases
Cheng, D., Yang, S., Zhao, X., & Wang, G. (2022) · Drug Design, Development and Therapy · doi:10.2147/dddt.s348055 · Cited by 84 · see citing works
Imaging neuroinflammation in Alzheimer's disease and other dementias: Recent advances and future directions
Varley, J. A., Brooks, D. J., & Edison, P. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2014.08.105 · Cited by 81 · see citing works
Neuroinflammation in Parkinson"s Disease and its Treatment Opportunities
Çınar, E., Tel, B. C., & Şahin, G. (2022) · Balkan Medical Journal · doi:10.4274/balkanmedj.galenos.2022.2022-7-100 · Cited by 82 · see citing works
Neuroprotective effects of a GIP analogue in the MPTP Parkinson's disease mouse model
Li, Y., Liu, W., Li, L., & Hölscher, C. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.10.002 · Cited by 80 · see citing works
Ascorbic acid ameliorates behavioural deficits and neuropathological alterations in rat model of Alzheimer’s disease
Olajide, O. J., Yawson, E. O., Gbadamosi, I. T., Arogundade, T. T., Lambe, E., Obasi, K., Lawal, I. T., Ibrahim, A., & Ogunrinola, K. Y. (2017) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2017.02.010 · Cited by 79 · see citing works
The Novel Dual GLP-1/GIP Receptor Agonist DA-CH5 Is Superior to Single GLP-1 Receptor Agonists in the MPTP Model of Parkinson’s Disease
Zhang, L., Zhang, L., Li, Y., Li, L., Melchiorsen, J. U., ROSENKILDE, M. M., & Hölscher, C. (2020) · Journal of Parkinson s Disease · doi:10.3233/jpd-191768 · Cited by 80 · see citing works
Resveratrol synergizes with low doses of L-DOPA to improve MPTP-induced Parkinson disease in mice
Liu, Q., Zhu, D., Jiang, P.-E., Tang, X., Lang, Q., Yu, Q.-Y., Zhang, S., Che, Y., & Feng, X. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.043 · Cited by 78 · see citing works
Neuroprotective Actions of Glucagon-Like Peptide-1 (GLP-1) Analogues in Alzheimer’s and Parkinson’s Diseases
Batista, A. F., Bodart‐Santos, V., Felice, F. G. D., & Ferreira, S. T. (2018) · CNS Drugs · doi:10.1007/s40263-018-0593-6 · Cited by 77 · see citing works
Novel incretin analogues improve autophagy and protect from mitochondrial stress induced by rotenone in SH ‐ SY 5Y cells
Jalewa, J., Sharma, M. K., & Hölscher, C. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13736 · Cited by 75 · see citing works
Type 2 Diabetes and Parkinson's Disease: A Focused Review of Current Concepts
Cullinane, P. W., Pablo‐Fernández, E. D., König, A., Outeiro, T. F., Jaunmuktane, Z., & Warner, T. T. (2022) · Movement Disorders · doi:10.1002/mds.29298 · Cited by 73 · see citing works
The role of glia in the physiology and pharmacology of glucagon‐like peptide‐1: implications for obesity, diabetes, neurodegeneration and glaucoma
Cui, Q. N., Stein, L. M., Fortin, S. M., & Hayes, M. R. (2021) · British Journal of Pharmacology · doi:10.1111/bph.15683 · Cited by 71 · see citing works
Neurodegenerative disease and obesity: what is the role of weight loss and bariatric interventions?
Ashrafian, H., Harling, L., Darzi, A. W., & Athanasiou, T. (2013) · Metabolic Brain Disease · doi:10.1007/s11011-013-9412-4 · Cited by 71 · see citing works
Repeated administration of exendin-4 reduces focal cerebral ischemia-induced infarction in rats
Briyal, S., Gulati, K., & Gulati, A. (2011) · Brain Research · doi:10.1016/j.brainres.2011.10.026 · Cited by 71 · see citing works
Incretin mimetics as pharmacologic tools to elucidate and as a new drug strategy to treat traumatic brain injury
Greig, N. H., Tweedie, D., Rachmany, L., Li, Y., Rubovitch, V., Schreiber, S., Chiang, Y. H., Hoffer, B. J., Miller, J. P., Lahiri, D. K., et al. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.12.011 · Cited by 71 · see citing works
Glucagon-Like Peptide-1 Receptor Agonist, Exendin-4, Regulates Feeding-Associated Neuropeptides in Hypothalamic Neurons in Vivo and in Vitro
Dalvi, P. S., Nazarians-Armavil, A., Purser, M. J., & Belsham, D. D. (2012) · Endocrinology · doi:10.1210/en.2011-1795 · Cited by 69 · see citing works
Peripheral-Central Neuroimmune Crosstalk in Parkinson's Disease: What Do Patients and Animal Models Tell Us?
Armentero, M., Cerri, S., & Blandini, F. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00232 · Cited by 70 · see citing works
Akt as a Victim, Villain and Potential Hero in Parkinson’s Disease Pathophysiology and Treatment
Greene, L. A., Levy, O., & Malagelada, C. (2011) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-011-9671-8 · Cited by 68 · see citing works
Post-treatment with PT302, a long-acting Exendin-4 sustained release formulation, reduces dopaminergic neurodegeneration in a 6-Hydroxydopamine rat model of Parkinson’s disease
Chen, S., Yu, S., Li, Y., Lecca, D., Glotfelty, E. J., Kim, H. K., Choi, H., Hoffer, B. J., Greig, N. H., Kim, D. S., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-28449-z · Cited by 68 · see citing works
Anti-Inflammatory Properties of Exenatide in Human Pancreatic Islets
Cechin, S. R., Pérez-Álvarez, I., Fenjves, E., Molano, R. D., Pileggi, A., Berggren, P.-O., Ricordi, C., & Pastori, R. L. (2012) · Cell Transplantation · doi:10.3727/096368911x576027 · Cited by 67 · see citing works
GLP-1 receptor agonists downregulate aberrant GnT-III expression in Alzheimer's disease models through the Akt/GSK-3β/β-catenin signaling
Wang, Y., Chen, S., Zheng, X., Chen, S., Yao, W., & Gao, X. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.11.048 · Cited by 67 · see citing works
Exendin-4 protects against post-myocardial infarction remodelling via specific actions on inflammation and the extracellular matrix
Robinson, E., Cassidy, R. S., Tate, M., Zhao, Y., Lockhart, S. M., Calderwood, D., Church, R. H., McGahon, M. K., Brazil, D. P., McDermott, B. J., et al. (2015) · Basic Research in Cardiology · doi:10.1007/s00395-015-0476-7 · Cited by 67 · see citing works
GLP-1 receptor agonist liraglutide reverses long-term atypical antipsychotic treatment associated behavioral depression and metabolic abnormalities in rats
Sharma, A. N., Ligade, S. S., Sharma, J. N., Shukla, P., Elased, K. M., & Lucot, J. B. (2014) · Metabolic Brain Disease · doi:10.1007/s11011-014-9591-7 · Cited by 66 · see citing works
Alternative role of glucagon-like Peptide-1 receptor agonists in neurodegenerative diseases
Chen, S., Chuang, Y., Lin, T., & Yang, J. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175439 · Cited by 66 · see citing works
Protective Effect of a GLP-1 Analog on Ischemia-Reperfusion Induced Blood–Retinal Barrier Breakdown and Inflammation
Gonçalves, A., Lin, C.-M., Muthusamy, A., Ribeiro, C., Ambrósio, A. F., Abcouwer, S. F., Fernandes, R., & Antonetti, D. A. (2016) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-19006 · Cited by 64 · see citing works
Analysis of the Relationship between Type II Diabetes Mellitus and Parkinson’s Disease: A Systematic Review
Maluf, F. C., Feder, D., & Carvalho, A. A. D. S. (2019) · Parkinson s Disease · doi:10.1155/2019/4951379 · Cited by 63 · see citing works
The Molecular Mechanisms of the Relationship between Insulin Resistance and Parkinson’s Disease Pathogenesis
Ruiz-Pozo, V. A., Tamayo-Trujillo, R., Cadena-Ullauri, S., Frias-Toral, E., Guevara-Ramírez, P., Paz-Cruz, E., Chapela, S., Montalván, M., Morales-López, T., Simancas-Racines, D., et al. (2023) · Nutrients · doi:10.3390/nu15163585 · Cited by 63 · see citing works
Sitagliptin attenuated brain damage and cognitive impairment in mice with chronic cerebral hypo-perfusion through suppressing oxidative stress and inflammatory reaction
Tsai, T., Sun, C., Su, C.-H., Sung, P., Chua, S. O., Zhen, Y., Leu, S., Chang, H., Yang, J., & Yip, H. (2015) · Journal of Hypertension · doi:10.1097/hjh.0000000000000529 · Cited by 64 · see citing works
D-Ala2-GIP-glu-PAL is neuroprotective in a chronic Parkinson's disease mouse model and increases BNDF expression while reducing neuroinflammation and lipid peroxidation
Li, Y., Liu, W., Li, L., & Hölscher, C. (2016) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2016.11.050 · Cited by 62 · see citing works
Beneficial effects of dipeptidyl peptidase-4 inhibitors in diabetic Parkinson’s disease
Jeong, S. H., Chung, S. J., Yoo, H. S., Hong, N., Jung, J. H., Baik, K., Lee, Y. H., Sohn, Y. H., & Lee, P. H. (2021) · Brain · doi:10.1093/brain/awab015 · Cited by 62 · see citing works
Anti-inflammatory action of exendin-4 in human islets is enhanced by phosphodiesterase inhibitors: potential therapeutic benefits in diabetic patients
Pugazhenthi, U., Velmurugan, K., Tran, A., Mahaffey, G., & Pugazhenthi, S. (2010) · Diabetologia · doi:10.1007/s00125-010-1849-y · Cited by 61 · see citing works
Intracerebroventricular Injection of Encapsulated Human Mesenchymal Cells Producing Glucagon-Like Peptide 1 Prolongs Survival in a Mouse Model of ALS
Knippenberg, S., Thau, N., Dengler, R., Brinker, T., & Petri, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036857 · Cited by 61 · see citing works
Pharmacologic antagonism of dopamine receptor D3 attenuates neurodegeneration and motor impairment in a mouse model of Parkinson's disease
Elgueta, D., Aymerich, M. S., Contreras, F., Montoya, A., Celorrio, M., Rojo-Bustamante, E., Riquelme, E., González, H., Vásquez, M., Franco, R., et al. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.09.028 · Cited by 61 · see citing works

Exendin-4 protects the dopaminergic neurons by attenuating inflammatory responses of microglial cells via activation of AMPK
Rimal, N., Khanal, S., Bohara, G., & Choi, D. (2025) · Neuropharmacology · doi:10.1016/j.neuropharm.2025.110643 · Cited by 5 · see citing works
Exendin-4 and linagliptin attenuate neuroinflammation in a mouse model of Parkinson′s disease
Yu, H., Sun, T., Wang, Z., Li, H., Xu, D., An, J., Wen, L.-L., Li, J., Li, W., & Feng, J. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.360242 · Cited by 38 · see citing works
Interleukin-4 Protects Dopaminergic Neurons In vitro but Is Dispensable for MPTP-Induced Neurodegeneration In vivo
Hühner, L., Rilka, J., Gilsbach, R., Zhou, X., Machado, V., & Spittau, B. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00062 · Cited by 25 · see citing works
A Research Update on Exendin-4 as a Novel Molecule Against Parkinson’s Disease
Singh, N. K., Singh, A., Varshney, M., & Agrawal, R. (2023) · Current Molecular Medicine · doi:10.2174/1566524023666230529093314 · Cited by 8 · see citing works
Neuroprotective effect of GLP-1 receptor agonist exendin-4 in rat models of Parkinson's disease
Harkavyi, A. (2009) · OpenGrey (Institut de l'Information Scientifique et Technique)

Authors: Kim, S., Moon, M., & Park, S.
Affiliations: Kyung Hee University (KR)
Corresponding author: Park, Seungjoon
ORCID: Kim, Sehee
Moon, Minho
Venue: Journal of Endocrinology
Publisher: Bioscientifica
Published: 2009-06-29
Volume: 202
Issue: 3
Pages: 431-439
ISSN: 0022-0795 (ISSN-L)
1479-6805
DOI: 10.1677/joe-09-0132
OpenAlex: W2164948885
Cited by: 263
References: 55
Citations by year: 2026: 6 · 2025: 17 · 2024: 14 · 2023: 12 · 2022: 21 · 2021: 22 · 2020: 12 · 2019: 18 · 2018: 20 · 2017: 17 · 2016: 22 · 2015: 19 · 2014: 17 · 2013: 17 · 2012: 15
FWCI: 6.18
Type: journal article
Language: en
Open access: closed
Locations: Journal of Endocrinology (publishedVersion)
PubMed (publishedVersion)
Funders: Korea Science and Engineering Foundation
Ministry of Education and Human Resources Development
Topics: Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
Keywords: exendin-4, Parkinson's disease, dopaminergic neurons, microglial activation, matrix metalloproteinase-3, MPTP-induced neurotoxicity, substantia nigra pars compacta, neuroprotection, GLP-1 receptor, neuroinflammation, TNF-α, IL-1β, nigrostriatal degeneration
MeSH terms: Exenatide, Animals, Corpus Striatum, Disease Models, Animal, Dopamine, Gliosis, Hypoglycemic Agents, Male, Mice, Inbred C57BL, Peptides, Substantia Nigra, Venoms, Gene Expression Regulation, Enzymologic, Microglia, Neuroprotective Agents, Inflammation Mediators, Matrix Metalloproteinase 3, Parkinsonian Disorders, Mice, Matrix Metalloproteinase Inhibitors

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Exendin-4 protects dopaminergic neurons by inhibition of microglial activation and matrix metalloproteinase-3 expression in an animal model of Parkinson's disease

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks