Type 2 diabetes-induced neuronal pathology in the piriform cortex of the rat is reversed by the GLP-1 receptor agonist Exendin-4

Oncotarget

Volumn 7, Issue 5, 2016, Pages 5865-5876

  Lietzau, Grazyna ^a,b   Nyström, Thomas ^a   Östenson, Claes Göran ^a   Darsalia, Vladimer ^a   Patrone, Cesare ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MEDICAL UNIVERSITY OF GDANSK   (Poland)

Author keywords

Diabetes; GLP 1R; Goto Kakizaki rats; Olfaction; Piriform cortex

Indexed keywords

CALBINDIN 1; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCAGON LIKE PEPTIDE 1 RECEPTOR AGONIST; NEURON SPECIFIC NUCLEAR PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; ANTIDIABETIC AGENT; INSULIN; PEPTIDE; VENOM;

ADULT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DISEASE; CELL STRESS; CELL STRUCTURE; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GOTO KAKIZAKI RAT; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INTERNEURON; LONG TERM CARE; MALE; MIDDLE AGED; NEUROPATHOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PYRIFORM CORTEX; RAT; SIGNAL TRANSDUCTION; SMELLING; STEREOLOGY; TREATMENT DURATION; TUNEL ASSAY; WISTAR RAT; YOUNG ADULT; AGONISTS; ANIMAL; CELL CULTURE; DRUG EFFECTS; ENZYME IMMUNOASSAY; EXPERIMENTAL DIABETES MELLITUS; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; HYPOGLYCEMIC AGENTS; IMMUNOENZYME TECHNIQUES; INSULIN; MALE; NEURONS; PEPTIDES; PIRIFORM CORTEX; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; VENOMS;

EID: 84958064165     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6823     Document Type: Article

References (59)

1. Shaw JE, Sicree RA and Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes research and clinical practice. 2010; 87:4-14.
2. Patterson DS, Turner P and Smart JV. Smell threshold in diabetes mellitus. Nature. 1966; 209:625.
3. Le Floch JP, Le Lievre G, Labroue M, Paul M, Peynegre R and Perlemuter L. Smell dysfunction and related factors in diabetic patients. Diabetes Care. 1993; 16:934-937.
4. Naka A, Riedl M, Luger A, Hummel T and Mueller CA. Clinical significance of smell and taste disorders in patients with diabetes mellitus. Eur Arch Otorhinolaryngol. 2010; 267:547-550.
5. Bramerson A, Johansson L, Ek L, Nordin S and Bende M. Prevalence of olfactory dysfunction: the skovde populationbased study. The Laryngoscope. 2004; 114:733-737.
6. Brady S, Lalli P, Midha N, Chan A, Garven A, Chan C and Toth C. Presence of neuropathic pain may explain poor performances on olfactory testing in diabetes mellitus patients. Chemical senses. 2013; 38:497-507.
7. Gouveri E, Katotomichelakis M, Gouveris H, Danielides V, Maltezos E and Papanas N. Olfactory dysfunction in type 2 diabetes mellitus: an additional manifestation of microvascular disease? Angiology. 2014; 65:869-876.
8. Thiebaud N, Johnson MC, Butler JL, Bell GA, Ferguson KL, Fadool AR, Fadool JC, Gale AM, Gale DS and Fadool DA. Hyperlipidemic diet causes loss of olfactory sensory neurons, reduces olfactory discrimination, and disrupts odor-reversal learning. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2014; 34:6970-6984.
9. Marfaing-Jallat P, Portha B and Penicaud L. Altered conditioned taste aversion and glucose utilization in related brain nuclei of diabetic GK rats. Brain research bulletin. 1995; 37:639-643.
10. Ader R and Peck JH. Early learning and retention of a conditioned taste aversion. Dev Psychobiol. 1977; 10:213-218.
11. Palouzier-Paulignan B, Lacroix MC, Aime P, Baly C, Caillol M, Congar P, Julliard AK, Tucker K and Fadool DA. Olfaction under metabolic influences. Chemical senses. 2012; 37:769-797.
12. Livingston JN, Unger JW, Moxley RT and Moss A. Phosphotyrosine-containing proteins in the CNS of obese Zucker rats are decreased in the absence of changes in the insulin receptor. Neuroendocrinology. 1993; 57:481-488.
13. Baskin DG, Stein LJ, Ikeda H, Woods SC, Figlewicz DP, Porte D, Jr., Greenwood MR and Dorsa DM. Genetically obese Zucker rats have abnormally low brain insulin content. Life sciences. 1985; 36:627-633.
14. Bekkers JM and Suzuki N. Neurons and circuits for odor processing in the piriform cortex. Trends in neurosciences. 2013; 36:429-438.
15. Gottfried JA. Central mechanisms of odour object perception. Nat Rev Neurosci. 2010; 11:628-641.
16. Poo C and Isaacson JS. Odor representations in olfactory cortex: "sparse" coding, global inhibition, and oscillations. Neuron. 2009; 62:850-861.
17. Zhan C and Luo M. Diverse patterns of odor representation by neurons in the anterior piriform cortex of awake mice. J Neurosci. 2010; 30:16662-16672.
18. Drucker DJ and Nauck MA. The incretin system: glucagonlike peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet. 2006; 368:1696-1705.
19. Heppner KM and Perez-Tilve D. GLP-1 based therapeutics: simultaneously combating T2DM and obesity. Front Neurosci. 2015; 9:92.
20. Heppner KM and Perez-Tilve D. GLP-1 based therapeutics: simultaneously combating T2DM and obesity. Front Neurosci-Switz. 2015; 9.
21. Kastin AJ and Akerstrom V. Entry of exendin-4 into brain is rapid but may be limited at high doses. Int J Obes Relat Metab Disord. 2003; 27:313-318.
22. Holscher C. 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. 2010; 5:109-117.
23. Patrone C, Eriksson O and Lindholm D. Diabetes drugs and neurological disorders: new views and therapeutic possibilities. The lancet Diabetes & endocrinology. 2014; 2:256-262.
24. Candeias EM, Sebastiao IC, Cardoso SM, Correia SC, Carvalho CI, Placido AI, Santos MS, Oliveira CR, Moreira PI and Duarte AI. Gut-brain connection: The neuroprotective effects of the anti-diabetic drug liraglutide. World J Diabetes. 2015; 6:807-827.
25. Hussain S, Mansouri S, Sjoholm A, Patrone C and Darsalia V. Evidence for cortical neuronal loss in male type 2 diabetic Goto-Kakizaki rats. Journal of Alzheimer's disease. 2014; 41:551-560.
26. Gavrilovici C, D'Alfonso S and Poulter MO. Diverse Interneuron Populations Have Highly Specific Interconnectivity in the Rat Piriform Cortex. Journal of Comparative Neurology. 2010; 518:1570-1588.
27. Verret L, Mann EO, Hang GB, Barth AM, Cobos I, Ho K, Devidze N, Masliah E, Kreitzer AC, Mody I, Mucke L and Palop JJ. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell. 2012; 149:708-721.
28. Kook SY, Jeong H, Kang MJ, Park R, Shin HJ, Han SH, Son SM, Song H, Baik SH, Moon M, Yi EC, Hwang D and Mook-Jung I. Crucial role of calbindin-D28k in the pathogenesis of Alzheimer's disease mouse model. Cell Death Differ. 2014; 21:1575-1587.
29. Sharma MK, Jalewa J and Holscher C. Neuroprotective and anti-apoptotic effects of liraglutide on SH-SY5Y cells exposed to methylglyoxal stress. J Neurochem. 2014; 128:459-471.
30. Xu W, Yang Y, Yuan G, Zhu W, Ma D and Hu S. Exendin-4, a glucagon-like peptide-1 receptor agonist, reduces Alzheimer disease-associated tau hyperphosphorylation in the hippocampus of rats with type 2 diabetes. Journal of investigative medicine: the official publication of the American Federation for Clinical Research. 2015; 63:267-272.
31. Dent MA, Segura-Anaya E, Alva-Medina J and Aranda-Anzaldo A. NeuN/Fox-3 is an intrinsic component of the neuronal nuclear matrix. FEBS letters. 2010; 584:2767-2771.
32. Foster TC and Kumar A. Calcium dysregulation in the aging brain. The Neuroscientist. 2002; 8:297-301.
33. Yenari MA, Minami M, Sun GH, Meier TJ, Kunis DM, McLaughlin JR, Ho DY, Sapolsky RM and Steinberg GK. Calbindin d28k overexpression protects striatal neurons from transient focal cerebral ischemia. Stroke. 2001; 32:1028-1035.
34. Saiz-Sanchez D, De la Rosa-Prieto C, Ubeda-Banon I and Martinez-Marcos A. Interneurons, tau and amyloid-beta in the piriform cortex in Alzheimer's disease. Brain structure & function. 2015; 220:2011-2025.
35. De Felice FG and Ferreira ST. Inflammation, defective insulin signaling, and mitochondrial dysfunction as common molecular denominators connecting type 2 diabetes to Alzheimer disease. Diabetes. 2014; 63:2262-2272.
36. Darsalia V, Larsson M, Nathanson D, Klein T, Nystrom T and Patrone C. Glucagon-like receptor 1 agonists and DPP-4 inhibitors: potential therapies for the treatment of stroke. J Cerebr Blood F Met. 2015; 35:718-723.
37. Korol SV, Jin Z, Babateen O and Birnir B. GLP-1 and exendin-4 transiently enhance GABAA receptor-mediated synaptic and tonic currents in rat hippocampal CA3 pyramidal neurons. Diabetes. 2015; 64:79-89.
38. Perry T, Lahiri DK, Chen D, Zhou J, Shaw KT, Egan JM and Greig NH. A novel neurotrophic property of glucagonlike peptide 1: a promoter of nerve growth factor-mediated differentiation in PC12 cells. The Journal of pharmacology and experimental therapeutics. 2002; 300:958-966.
39. Lovshin JA and Drucker DJ. Incretin-based therapies for type 2 diabetes mellitus. Nature reviews Endocrinology. 2009; 5:262-269.
40. Ahren B. GLP-1 for type 2 diabetes. Experimental cell research. 2011; 317:1239-1245.
41. Ma DL, Chen FQ, Xu WJ, Yue WZ, Yuan G and Yang Y. Early intervention with glucagon-like peptide 1 analog liraglutide prevents tau hyperphosphorylation in diabetic db/db mice. Journal of neurochemistry. 2015; 135:301-8. doi: 10.1111/jnc.13248.
42. Merchenthaler I, Lane M and Shughrue P. Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol. 1999; 403:261-280.
43. Pyke C and Knudsen LB. The glucagon-like peptide-1 receptor-or not? Endocrinology. 2013; 154:4-8.
44. Llewellyn-Smith IJ, Reimann F, Gribble FM and Trapp S. Preproglucagon neurons project widely to autonomic control areas in the mouse brain. Neuroscience. 2011; 180:111-121.
45. Ban K, Noyan-Ashraf MH, Hoefer J, Bolz SS, Drucker DJ and Husain M. Cardioprotective and vasodilatory actions of glucagon-like peptide 1 receptor are mediated through both glucagon-like peptide 1 receptor-dependent and-independent pathways. Circulation. 2008; 117:2340-2350.
46. Darsalia V, Mansouri S, Ortsater H, Olverling A, Nozadze N, Kappe C, Iverfeldt K, Tracy LM, Grankvist N, Sjoholm A and Patrone C. Glucagon-like peptide-1 receptor activation reduces ischaemic brain damage following stroke in Type 2 diabetic rats. Clin Sci (Lond). 2012; 122:473-483.
47. Kalaria RN. Neurodegenerative disease: Diabetes, microvascular pathology and Alzheimer disease. Nature reviews Neurology. 2009; 5:305-306.
48. Verdile G, Fuller SJ and Martins RN. The role of type 2 diabetes in neurodegeneration. Neurobiology of disease. 2015; 84:22-38. doi: 10.1016/j.nbd.2015.04.008.
49. Biessels GJ, Staekenborg S, Brunner E, Brayne C and Scheltens P. Risk of dementia in diabetes mellitus: a systematic review. The Lancet Neurology. 2006; 5:64-74.
50. Cukierman T, Gerstein HC and Williamson JD. Cognitive decline and dementia in diabetes-systematic overview of prospective observational studies. Diabetologia. 2005; 48:2460-2469.
51. Doty RL. Olfaction in Parkinson's disease and related disorders. Neurobiology of disease. 2012; 46:527-552.
52. Djordjevic J, Jones-Gotman M, De Sousa K and Chertkow H. Olfaction in patients with mild cognitive impairment and Alzheimer's disease. Neurobiology of aging. 2008; 29:693-706.
53. Barresi M, Ciurleo R, Giacoppo S, Foti Cuzzola V, Celi D, Bramanti P and Marino S. Evaluation of olfactory dysfunction in neurodegenerative diseases. Journal of the neurological sciences. 2012; 323:16-24.
54. Sanke H, Mita T, Yoshii H, Yokota A, Yamashiro K, Ingaki N, Onuma T, Someya Y, Komiya K, Tamura Y, Shimizu T, Ohmura C, Kanazawa A, Fujitani Y and Watada H. Relationship between olfactory dysfunction and cognitive impairment in elderly patients with type 2 diabetes mellitus. Diabetes research and clinical practice. 2014; 106:465-473.
55. Goto Y, Kakizaki M and Masaki N. Production of spontaneous diabetic rats by repetition of selective breeding. The Tohoku journal of experimental medicine. 1976; 119:85-90.
56. Murakawa Y, Zhang W, Pierson CR, Brismar T, Ostenson CG, Efendic S and Sima AA. Impaired glucose tolerance and insulinopenia in the GK-rat causes peripheral neuropathy. Diabetes/metabolism research and reviews. 2002; 18:473-483.
57. Moreira T, Malec E, Ostenson CG, Efendic S and Liljequist S. Diabetic type II Goto-Kakizaki rats show progressively decreasing exploratory activity and learning impairments in fixed and progressive ratios of a lever-press task. Behavioural brain research. 2007; 180:28-41.
58. Ostenson CG and Efendic S. Islet gene expression and function in type 2 diabetes; studies in the Goto-Kakizaki rat and humans. Diabetes Obes Metab. 2007; 9 Suppl 2:180-186.
59. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B and et al. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS. 1988; 96:857-881.