Neuronal human BACE1 knockin induces systemic diabetes in mice

Diabetologia

Volumn 59, Issue 7, 2016, Pages 1513-1523

  Plucińska, Kaja ^a   Dekeryte, Ruta ^a   Koss, David ^a   Shearer, Kirsty ^a   Mody, Nimesh ^a   Whitfield, Phillip D ^b   Doherty, Mary K ^b   Mingarelli, Marco ^a   Welch, Andy ^a   Riedel, Gernot ^a   Delibegovic, Mirela ^a   Platt, Bettina ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF THE HIGHLANDS AND ISLANDS   (United Kingdom)

Author keywords

18FDG PET; Ceramide; ER stress; Glucose homeostasis; Insulin signalling; Neuronal BACE1

Indexed keywords

BETA SECRETASE 1; CERAMIDE; DIACYLGLYCEROL; FLUORODEOXYGLUCOSE F 18; GLUCOSE; GLYCEROPHOSPHOLIPID; GLYCOGEN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; INSULIN; LIPID; LYSOPHOSPHATIDYLETHANOLAMINE; MELANOCORTIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; PHOSPHOLIPID; PROTEIN TYROSINE PHOSPHATASE 1B; RETINOL BINDING PROTEIN 4; RIBOSOME PROTEIN; SPHINGOLIPID; SPHINGOMYELIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; AMYLOID PRECURSOR PROTEIN; ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; BACE1 PROTEIN, MOUSE; SECRETASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL COMPOSITION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL DIABETES MELLITUS; FATTY LIVER; FEMALE; FOREBRAIN; GLUCOSE BRAIN LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; GLYCOGEN LIVER LEVEL; HUMAN; HYPOTHALAMUS DISEASE; INSULIN RESISTANCE; LIPID BLOOD LEVEL; LIPIDOMICS; MALE; MOLECULAR BIOLOGY; MOUSE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PHOSPHOLIPID BLOOD LEVEL; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYSTEMIC DISEASE; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; WESTERN BLOTTING; ALZHEIMER DISEASE; ANIMAL; DIABETES MELLITUS; DISEASE MODEL; GENETICS; HOMEOSTASIS; METABOLISM; NERVE CELL; OBESITY; PATHOPHYSIOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; DIABETES MELLITUS; DISEASE MODELS, ANIMAL; GLUCOSE; GLUCOSE INTOLERANCE; HOMEOSTASIS; HUMANS; MICE; NEURONS; OBESITY; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1;

EID: 84965020773     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-016-3960-1     Document Type: Article

References (49)

1. Xu W, Von Strauss E, Cx Q, Winblad B, Fratiglioni L (2009) Uncontrolled diabetes increases the risk of Alzheimer’s disease: a population-based cohort study. Diabetologia 52:1031–1039
2. Janson J, Laedtke T, Parisi JE, O’Brien P, Petersen RC, Butler PC (2004) Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53:474–481
3. Talbot K, Wang HY, Kazi H 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
4. Prestia A, Caroli A, Wade SK et al (2015) Prediction of AD dementia by biomarkers following the NIA-AA and IWG diagnostic criteria in MCI patients from three European memory clinics. Alzheimer’s Dement 11:1191–1201
5. Carvalho C, Machado N, Mota PC et al (2013) Type 2 diabetic and Alzheimer’s disease mice present similar behavioral, cognitive, and vascular anomalies. J Alzheimer’s Dis 35:623–635
6. Mody N, Agouni A, McIlroy GD, Platt B, Delibegovic M (2011) Susceptibility to diet-induced obesity and glucose intolerance in the APP (SWE)/PSEN1 (A246E) mouse model of Alzheimer’s disease is associated with increased brain levels of protein tyrosine phosphatase 1B (PTP1B) and retinol-binding protein 4 (RBP4), and basal phosphorylation of S6 ribosomal protein. Diabetologia 54:2143–2151
7. Vassar R, Bennett BD, Babu-Khan S et al (1999) β-Secretase cleavage of Alzheimer’s amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286:735–741
8. Fukumoto H, Cheung BS, Hyman BT, Irizarry MC (2002) β-Secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 59:1381–1389
9. Holsinger RMD, McLean CA, Beyreuther K, Masters CL, Evin G (2002) Increased expression of the amyloid precursor β-secretase in Alzheimer’s disease. Ann Neurol 51:783–786
10. Zhang X, Zhou K, Wang R et al (2007) Hypoxia-inducible factor 1α (HIF-1α)-mediated hypoxia increases BACE1 Expression and β-amyloid generation. J Biol Chem 282:10873–10880
11. Walker KR, Kang EL, Whalen MJ, Shen Y, Tesco G (2012) Depletion of GGA1 and GGA3 mediates postinjury elevation of BACE1. J Neurosci 32:10423–10437
12. Laird FM, Cai H, Savonenko AV et al (2005) BACE1, a major determinant of selective vulnerability of the brain to amyloid-β amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J Neurosci 25:11693–11709
13. Plucinska K, Crouch B, Koss D et al (2014) Knock-in of human BACE1 cleaves murine APP and reiterates Alzheimer-like phenotypes. J Neurosci 34:10710–10728
14. Hemming ML, Elias JE, Gygi SP, Selkoe DJ (2009) Identification of beta-secretase (BACE1) substrates using quantitative proteomics. PLoS One 4(12), E8477
15. Huse JT, Byant D, Yang Y et al (2003) Endoproteolysis of β-secretase (β-site amyloid precursor protein-cleaving enzyme) within its catalytic domain: a potential mechanism for regulation. J Biol Chem 278:17141–17149
16. Sinha S, Anderson JP, Barbour R et al (1999) Purification and cloning of amyloid precursor protein β-secretase from human brain. Nature 402:537–540
17. Meakin PJ, Harper AJ, Hamilton DL et al (2012) Reduction in BACE1 decreases body weight, protects against diet-induced obesity and enhances insulin sensitivity in mice. Biochem J 441:285–295
18. Guglielmotto M, Aragno M, Tamagno E et al (2012) AGEs/RAGE complex upregulates BACE1 via Nf-κB pathway activation. Neurobiol Aging 33:196.e13–196.e27
19. Devi L, Alldred MJ, Ginsberg SD, Ohno M (2012) Mechanisms underlying insulin deficiency-induced acceleration of β-amyloidosis in a mouse model of Alzheimer’s disease. PLoS One 7, e32792
20. Owen C, Lees EK, Grant L et al (2013) Inducible liver-specific knockdown of protein tyrosine phosphatase 1B improves glucose and lipid homeostasis in adult mice. Diabetologia 56:2286–2296
21. Platt B, Drever B, Koss D et al (2011) Abnormal cognition, sleep, EEG and brain metabolism in a novel knock-in Alzheimer mouse, PLB1. PLoS One 6, e27068
22. Welinder C, Ekblad L (2011) Coomassie staining as loading control in western blot analysis. J Proteome Res 10:1416–1419
23. McIlroy GD, Delibegovic M, Owen C et al (2013) Fenretinide treatment prevents diet-induced obesity in association with major alterations in retinoid homeostatic gene expression in adipose, liver, and hypothalamus. Diabetes 62:825–836
24. Bence KK, Delibegovic M, Xue B et al (2006) Neuronal PTP1B regulates body weight, adiposity and leptin action. Nat Med 12:917–924
25. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661–671
26. Taskinen MR, Borén J (2015) New insights into the pathophysiology of dyslipidemia in type 2 diabetes. Atherosclerosis 239:483–495
27. Mapstone M, Cheema AK, Fiandaca MS et al (2014) Plasma phospholipids identify antecedent memory impairment in older adults. Nat Med 20:415–418
28. Wang GX, Zhao XY, Lin JD (2015) The Brown fat secretome: metabolic functions beyond thermogenesis. Trends Endocrinol Metab 26:231–237
29. Norseen J, Hosooka T, Hammarstedt A et al (2012) Retinol-binding protein 4 inhibits insulin signaling in adipocytes by inducing proinflammatory cytokines in macrophages through a c-Jun N-terminal kinase- and Toll-like receptor 4-dependent and retinol-independent mechanism. Mol Cell Biol 32:2010–2019
30. Hoffmeister A, Tuennemann J, Sommerer I et al (2013) Genetic and biochemical evidence for a functional role of BACE1 in the regulation of insulin mRNA expression. Obesity 21:E626–E633
31. Denroche HC, Huynh FK, Kieffer TJ (2012) The role of leptin in glucose homeostasis. J Diabetes Investig 3:115–129
32. Mells JE, Anannia FA (2013) The role of gastrointestinal hormones in hepatic liver metabolism. Semin Liver Dis 33:343–357
33. González-Domínguez R, García-Barrera T, Gómez-Ariza JL (2014) Metabolomic study of lipids in serum for biomarker discovery in Alzheimer’s disease using direct infusion mass spectrometry. J Pharm Biomed Anal 98:321–326
34. Proitsi P, Kim M, Whiley L et al (2015) Plasma lipidomics analysis finds long chain cholesteryl esters to be associated with Alzheimer’s disease. Transl Psychiatry 5, E494
35. Wood PL, Barnette BL, Kaye JA, Quinn JF, Woltjer RL (2015) Non-targeted lipidomics of CSF and frontal cortex grey and white matter in control, mild cognitive impairment, and Alzheimer’s disease subjects. Acta Neuropsychiatr 27:270–278
36. Bennett SAL, Valenzuela N, Xu H, Franko B, Fai S, Figeys D (2013) Using neurolipidomics to identify phospholipid mediators of synaptic (dys)function in Alzheimer’s disease. Front Physiol 4:168
37. Yadav RS, Tiwari NK (2014) Lipid integration in neurodegeneration: an overview of Alzheimer’s disease. Mol Neurobiol 50:168–176
38. Cutler RG, Kelly J, Storie K et al (2004) Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer’s disease. Proc Natl Acad Sci U S A 101:2070–2075
39. Han X, Holtzman DM, McKeel DW Jr, Kelley J, Morris JC (2002) Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer’s disease: potential role in disease pathogenesis. J Neurochem 82:809–818
40. Puglielli L, Ellis BC, Saunders AJ, Kovacs DM (2003) Ceramide stabilizes β-site amyloid precursor protein-cleaving enzyme 1 and promotes amyloid β-peptide biogenesis. J Biol Chem 278:19777–19783
41. Jana A, Pahan K (2004) Fibrillar amyloid-β peptides kill human primary neurons via NADPH oxidase-mediated activation of neutral sphingomyelinase: implications for Alzheimer’s disease. J Biol Chem 279:51451–51459
42. Contreras C, González-García I, Martínez-Sánchez N et al (2014) Central ceramide-induced hypothalamic lipotoxicity and ER stress regulate energy balance. Cell Rep 9:366–377
43. Roberts RO, Knopman DS, Cha RH et al (2014) Diabetes and elevated hemoglobin a1c levels are associated with brain hypometabolism but not amyloid accumulation. J Nucl Med 55:759–764
44. Kazemi S, Mounir Z, Baltzis D et al (2007) A novel function of EIF2α kinases as inducers of the phosphoinositide-3 kinase signaling pathway. Mol Biol Cell 18:3635–3644
45. Loskutova N, Honea RA, Brooks WM, Burns JM (2010) Reduced limbic and hypothalamic volumes correlate with bone density in early Alzheimer’s disease. J Alzheimer’s Dis 20:313–322
46. Fronczek R, Van Geest S, Frölich M, Overeem S, Roelandse FWC, Lammers GJ et al (2012) Hypocretin (orexin) loss in Alzheimer’s disease. Neurobiol Aging 33:1642–1650
47. Clarke JR, Lyra E, Silva NM, Figueiredo CP et al (2015) Alzheimer-associated αβ oligomers impact the central nervous system to induce peripheral metabolic deregulation. EMBO Mol Med 7:190–210
48. Çakir I, Cyr NE, Perello M, Litvinov BP, Romero A, Stuart RC et al (2013) Obesity induces hypothalamic endoplasmic reticulum stress and impairs proopiomelanocortin (POMC) post-translational processing. J Biol Chem 288:17675–17688
49. Purkayastha S, Zhang H, Zhang G, Ahmed Z, Wang Y, Cai D (2011) Neural dysregulation of peripheral insulin action and blood pressure by brain endoplasmic reticulum stress. Proc Natl Acad Sci U S A 108:2939–2944