Chronic Treatment with the GLP1 Analogue Liraglutide Increases Cell Proliferation and Differentiation into Neurons in an AD Mouse Model

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Parthsarathy, Vadivel ^a   Hölscher, Christian ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CELL MARKER; KI 67 ANTIGEN; LIRAGLUTIDE; NEURON SPECIFIC NUCLEAR PROTEIN;

ACUTE DRUG ADMINISTRATION; AGE; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DENTATE GYRUS; DISEASE MODEL; DRUG EFFECT; FEMALE; MOUSE; MOUSE STRAIN; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PHENOTYPE; WILD TYPE;

AGE FACTORS; ALZHEIMER DISEASE; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; FEMALE; GLUCAGON-LIKE PEPTIDE 1; MICE; NEUROGENESIS; NEURONS;

EID: 84874924233     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058784     Document Type: Article

References (67)

1. Emsley JG, Mitchell BD, Kempermann G, Macklis JD, (2005) Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 75: 321-341.
2. Altman J, (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J comp Neurol Neurol 137: 433-457.
3. Cameron H, McKay R, (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435: 406-417.
4. Abrous DN, Koehl M, Le Moal M, (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85: 523-569.
5. Bruel-Jungerman E, Davis S, Rampon C, Laroche S, (2006) Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J Neurosci 26: 5888-5893.
6. Tanapat P, Hastings NB, Reeves AJ, Gould E, (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19: 5792-5801.
7. Bain MJ, Dwyer SM, Rusak B, (2004) Restraint stress affects hippocampal cell proliferation differently in rats and mice. Neurosci Lett 368: 7-10.
8. Yagita Y, Kitagawa K, Sasaki T, Terasaki Y, Todo K, et al. (2006) Postischemic exercise decreases neurogenesis in the adult rat dentate gyrus. Neurosci Lett 409: 24-29.
9. Li H, Lee CH, Yoo KY, Choi JH, Park OK, et al. (2010) Chronic treatment of exendin-4 affects cell proliferation and neuroblast differentiation in the adult mouse hippocampal dentate gyrus. Neurosci Lett 19: 1205-1219.
10. van Praag H, Shubert T, Zhao C, Gage FH, (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25: 8680-8685.
11. Kuhn HG, Dickinson-Anson H, Gage FH, (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-2033.
12. Harkavyi A, Abuirmeileh A, Lever R, Kingsbury AE, Biggs CS, et al. (2008) Glucagon-like peptide 1 receptor stimulation reverses key deficits in distinct rodent models of Parkinson's disease. J Neuroinflammation 5: 19.
13. Hamilton A, Patterson S, Porter D, Gault VA, Holscher C, (2011) Novel GLP-1 mimetics developed to treat type 2 diabetes promote progenitor cell proliferation in the brain. J Neurosci Res 89: 481-489.
14. Brinton RD, Wang JM, (2006) Therapeutic potential of neurogenesis for prevention and recovery from Alzheimer's disease: allopregnanolone as a proof of concept neurogenic agent. Curr Alzheimer Res 3: 185-190.
15. Demars M, Hu YS, Gadadhar A, Lazarov O, (2010) Impaired neurogenesis is an early event in the etiology of familial Alzheimer's disease in transgenic mice. J Neurosci Res 88: 2103-2117.
16. Greenberg DA, Jin K, (2006) Neurodegeneration and neurogenesis: focus on Alzheimer's disease. Curr Alzheimer Res 3: 25-28.
17. Heese K, Low JW, Inoue N, (2006) Nerve growth factor, neural stem cells and Alzheimer's disease. Neurosignals 15: 1-12.
18. Haughey NJ, Nath A, Chan SL, Borchard AC, Rao MS, et al. (2002) Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J Neurochem 83: 1509-1524.
19. Faure A, Verret L, Bozon B, El Tannir El Tayara N, Ly M, et al. (2011) Impaired neurogenesis, neuronal loss, and brain functional deficits in the APPxPS1-Ki mouse model of Alzheimer's disease. Neurobiol Aging 32: 407-418.
20. Holmes C, Cunningham C, Zotova E, Culliford D, Perry VH, (2011) Proinflammatory cytokines, sickness behavior, and Alzheimer disease. Neurology 77: 212-218.
21. Monje ML, Toda H, Palmer TD, (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765.
22. Holscher C, (2011) Diabetes as a risk factor for Alzheimer's disease: insulin signalling impairment in the brain as an alternative model of Alzheimer's disease. Biochem Soc Trans 39: 891-897.
23. Talbot K, Wang HY, Kazi H, Han LY, Bakshi KP, et al. (2012) Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest 122: 1316-1338.
24. Bomfim TR, Forny-Germano L, Sathler LB, Brito-Moreira J, Houzel JC, et al. (2012) An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer's disease- associated Abeta oligomers. J Clin Invest 122: 1339-1353.
25. Steen E, Terry BM, Rivera E, Cannon JL, Neely TR, et al. (2005) Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease - is this type 3 diabetes? J Alzheimers Dis 7: 63-80.
26. Hoyer S, (2004) Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. Eur J Pharmacol 490: 115-125.
27. Craft S, (2007) Insulin resistance and Alzheimer's disease pathogenesis: potential mechanisms and implications for treatment. Curr Alzheimer Res 4: 147-152.
28. Baggio LL, Drucker DJ, (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132: 2131-2157.
29. Lovshin JA, Drucker DJ, (2009) Incretin-based therapies for type 2 diabetes mellitus. Nat Rev Endocrinol 5: 262-269.
30. Vella A, Shah P, Reed AS, Adkins AS, Basu R, et al. (2002) Lack of effect of exendin-4 and glucagon-like peptide-1-(7,36)-amide on insulin action in non-diabetic humans. Diabetologia 45: 1410-1415.
31. Vilsboll T, (2009) The effects of glucagon-like peptide-1 on the beta cell. Diabetes Obes Metab 11Suppl 3: 11-18.
32. Abbas T, Faivre E, Hölscher C, (2009) 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: 265-271.
33. Hamilton A, Holscher C, (2009) Receptors for the insulin-like peptide GLP-1 are expressed on neurons in the CNS. Neuroreport 20: 1161-1166.
34. Kastin AJ, Akerstrom V, Pan W, (2002) Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier. J Mol Neurosci 18: 7-14.
35. McClean P, Parthsarathy V, Faivre E, Hölscher C, (2011) The diabetes drug Liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease. J Neurosci 31: 6587-6594.
36. Hunter K, Holscher C, (2012) Drugs developed to treat diabetes, liraglutide and lixisenatide, cross the blood brain barrier and enhance neurogenesis. BMC Neurosci 13: 33-38.
37. Li Y, Perry T, Kindy MS, Harvey BK, Tweedie D, et al. (2009) 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: 1285-1290.
38. During MJ, Cao L, Zuzga DS, Francis JS, Fitzsimons HL, et al. (2003) Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat Med 9: 1173-1179.
39. Gault V, Holscher C, (2008) GLP-1 agonists facilitate hippocampal LTP and reverse the impairment of LTP induced by beta-amyloid. Eur J Pharmacol 587: 112-117.
40. McClean PL, Gault VA, Harriott P, Holscher C, (2010) Glucagon-like peptide-1 analogues enhance synaptic plasticity in the brain: A link between diabetes and Alzheimer's disease. Eur J Pharmacol 630: 158-162.
41. Porter DW, Kerr BD, Flatt PR, Holscher C, Gault VA, (2010) 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: 891-899.
42. Hamilton A, Holscher C, (2012) The effect of ageing on neurogenesis and oxidative stress in the APP(swe)/PS1(deltaE9) mouse model of Alzheimer's disease. Brain Res 1449: 83-93.
43. Franklin K, Paxinos G (2004) The Mouse Brain in Stereotaxic Coordinates. Amsterdam: Elsevier Academic Press.
44. Bondolfi L, Calhoun M, Ermini F, Kuhn HG, Wiederhold KH, et al. (2002) Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J Neurosci 22: 515-522.
45. Gengler S, McClean P, McCurtin R, Gault V, Holscher C, (2012) Val(8)GLP-1 rescues synaptic plasticity and reduces dense core plaques in APP/PS1 mice. Neurobiol Aging 33: 265-276.
46. Stanfield BB, Trice JE, (1988) Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp Brain Res 72: 399-406.
47. Wen PH, Hof PR, Chen X, Gluck K, Austin G, et al. (2004) The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp Neurol 188: 224-237.
48. Kronenberg G, Bick-Sander A, Bunk E, Wolf C, Ehninger D, et al. (2006) Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol Aging 27: 1505-1513.
49. Taupin P, (2007) BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 53: 198-214.
50. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, et al. (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110: 429-441.
51. Kobayashi T, Ahlenius H, Thored P, Kobayashi R, Kokaia Z, et al. (2006) Intracerebral infusion of glial cell line-derived neurotrophic factor promotes striatal neurogenesis after stroke in adult rats. Stroke 37: 2361-2367.
52. Schulte-Herbruggen O, Braun A, Rochlitzer S, Jockers-Scherubl MC, Hellweg R, (2007) Neurotrophic factors - a tool for therapeutic strategies in neurological, neuropsychiatric and neuroimmunological diseases? Curr Med Chem 14: 2318-2329.
53. Zuccato C, Cattaneo E, (2009) Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol 5: 311-322.
54. Covaceuszach S, Capsoni S, Ugolini G, Spirito F, Vignone D, et al. (2009) Development of a non invasive NGF-based therapy for Alzheimer's disease. Curr Alzheimer Res 6: 158-170.
55. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, et al. (2001) Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng 17: 157-165.
56. De Felice FG, Vieira MN, Bomfim TR, Decker H, Velasco PT, et al. (2009) Protection of synapses against Alzheimer's-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc Natl Acad Sci U S A 106: 1971-1976.
57. Adamo M, Raizada MK, LeRoith D, (1989) Insulin and insulin-like growth factor receptors in the nervous system. Mol Neurobiol 3: 71-100.
58. Carro E, Torres AI, (2004) The role of insulin and insulin-like growth factor I in the molecular and cellular mechanisms underlying the pathology of Alzheimer's disease. Eur J Pharmacol 490: 127-133.
59. Perry T, Lahiri DK, Chen D, Zhou J, Shaw KT, et al. (2002) 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: 958-966.
60. Bertilsson G, Patrone C, Zachrisson O, Andersson A, Dannaeus K, et al. (2008) 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: 326-338.
61. Drucker DJ, (2003) Glucagon-like peptides: regulators of cell proliferation, differentiation, and apoptosis. Mol Endocrinol 17: 161-171.
62. Oka J, Suzuki E, Kondo Y, (2000) Endogenous GLP-1 is involved in beta-amyloid protein-induced memory impairment and hippocampal neuronal death in rats. Brain Res 878: 194-198.
63. Perry TA, Greig NH, (2004) A new Alzheimer's disease interventive strategy: GLP-1. Curr Drug Targets 5: 565-571.
64. Raber J, Rola R, LeFevour A, Morhardt D, Curley J, et al. (2004) Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162: 39-47.
65. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM, (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130: 843-852.
66. Bonner-Weir S, Weir GC, (2005) New sources of pancreatic beta-cells. Nat Biotechnol 23: 857-861.
67. Porter WD, Flatt PR, Holscher C, Gault VA (2012) Liraglutide improves hippocampal synaptic plasticity associated with increased expression of Mash1 in ob/ob mice. Int J Obes (Lond). DOI:10.1038/ijo.2012.91.