Advanced glycation end products are mitogenic signals and trigger cell cycle reentry of neurons in Alzheimer's disease brain

Neurobiology of Aging

Volumn 36, Issue 2, 2015, Pages 753-761

  Kuhla, Angela ^a   Ludwig, Sophie C ^a   Kuhla, Björn ^b   Münch, Gerald ^c   Vollmar, Brigitte ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^c UNIVERSITY OF WESTERN SYDNEY   (Australia)

Author keywords

Advanced glycation end products; Alzheimer's disease; Cell cycle reentry; Mitogenic signaling

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; APOLIPOPROTEIN E; CYCLIN D1; MITOGEN ACTIVATED PROTEIN KINASE; THIOCTIC ACID; CCND1 PROTEIN, MOUSE; STK30 PROTEIN, MOUSE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CASE REPORT; CELL CYCLE PARAMETERS; CELL CYCLE REENTRY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVATION; FLUORESCENCE IN SITU HYBRIDIZATION; GLYCATION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MALE; MITOGENESIS; MOUSE; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; ASTROCYTE; BRAIN; C57BL MOUSE; CELL CULTURE; CELL CYCLE; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; MICROGLIA; NERVE DEGENERATION; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; ANIMALS; ASTROCYTES; BRAIN; CELL CYCLE; CELLS, CULTURED; CYCLIN D1; DISEASE MODELS, ANIMAL; DNA REPLICATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MITOGEN-ACTIVATED PROTEIN KINASES; NERVE DEGENERATION; NEURONS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; THIOCTIC ACID;

EID: 84922765522     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.09.025     Document Type: Article

References (40)

1. Arendt T., Holzer M., Grossmann A., Zedlick D., Brückner M.K. Increased expression and subcellular translocation of the mitogen activated protein kinase and mitogen activated protein kinase in Alzheimer's disease. Neuroscience 1995, 68:5-18.
2. Arendt T., Holzer M., Stobe A., Gärtner U., Lüth H.J., Brückner M.K., Ueberham U. Activated mitogenic signaling induces a process of dedifferentiation in Alzheimer's disease that eventually results in cell death. Ann. N. Y. Acad. Sci. 2000, 920:249-255.
3. Arendt T. Alzheimer's disease as a loss of differentiation control in a subset of neurons that retain immature features in the adult brain. Neurobiol. Aging 2000, 21:783-796.
4. Baumann K., Mandelkow E.M., Biernat J., Piwnica-Worms H., Mandelkow E. Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett. 1993, 336:417-424.
5. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
6. Dei R., Takeda A., Niwa H., Li M., Nakagomi Y., Watanabe M. Lipid peroxidation and advanced glycation end products in the brain in normal aging and in Alzheimer's disease. Acta Neuropathol. 2002, 104:113-122.
7. Gärtner U., Holzer M., Arendt T. Elevated expression of p21ras is an early event in Alzheimer's disease and precedes neurofibrillary degeneration. Neuroscience 1999, 91:1-5.
8. Geoffroy K., Wiernsperger N., Lagarde M., El Bawab S. Bimodal effect of advanced glycation end products on mesangial cell proliferation is mediated by neutral ceramidase regulation and endogenous sphingolipids. J.Biol. Chem. 2004, 279:34343-34352.
9. Hamilton A., Holscher C. The effect of ageing on neurogenesis and oxidative stress in the APP(swe)/PS1(deltaE9) mouse model of Alzheimer's disease. Brain Res. 2012, 1449:83-93.
10. Hoozemans J.J., Brückner M.K., Rozemuller A.J., Veerhuis R., Eikelenboom P., Arendt T. Cyclin D1 and cyclin E are co-localized with cyclo-oxygenase 2 (COX-2) in pyramidal neurons in Alzheimer disease temporal cortex. J.Neuropathol. Exp. Neurol. 2002, 61:678-688.
11. Iourov I.Y., Vorsanova S.G., Liehr T., Yurov Y.B. Aneuploidy in the normal, Alzheimer's disease and ataxia-telangiectasia brain: differential expression and pathological meaning. Neurobiol. Dis. 2009, 34:212-220.
12. Kruman I.I. Why do neurons enter the cell cycle?. Cell Cycle 2004, 3:769-773.
13. Kuan C.Y., Schloemer A.J., Lu A., Burns K.A., Weng W.L., Williams M.T., Strauss K.I., Vorhees C.V., Flavell R.A., Davis R.J., Sharp F.R., Rakic P. Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J.Neurosci. 2004, 24:10763-10772.
14. Lew J., Wang J.H. Neuronal cdc2-like kinase. Trends Biochem. Sci. 1995, 20:33-37.
15. Li L., Cheung T., Chen J., Herrup K. Acomparative study of five mouse models of Alzheimer's disease: cell cycle events reveal new insights into neurons at risk for death. Int. J. Alzheimers Dis. 2011, 2011:171464.
16. Lüth H.J., Ogunlade V., Kuhla B., Kientsch-Engel R., Stahl P., Webster J., Arendt T., Münch G. Age- and stage-dependent accumulation of advanced glycation end products in intracellular deposits in normal and Alzheimer's disease brains. Cereb. Cortex 2005, 2:211-220.
17. Masliah E., Mallory M., Ge N., Alford M., Veinbergs I., Roses A.D. Neurodegeneration in the central nervous system of apoE-deficient mice. Exp. Neurol. 1995, 136:107-122.
18. McShea A., Harris P.L., Webster K.R., Wahl A.F., Smith M.A. Abnormal expression of the cell cycle regulators p16 and CDK4 in Alzheimer's disease. Am. J. Pathol. 1997, 150:1933-1939.
19. Montine T.J., Phelps C.H., Beach T.G., Bigio E.H., Cairns N.J., Dickson D.W., Duyckaerts C., Frosch M.P., Masliah E., Mirra S.S., Nelson P.T., Schneider J.A., Thal D.R., Trojanowski J.Q., Vinters H.V., Hyman B.T. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: a practical approach. Acta Neuropathol. 2012, 123:1-11. National Institute on Aging, Alzheimer's AssociationAlzheimer's Association.
20. Mosch B., Morawski M., Mittag A., Lenz D., Tarnok A., Arendt T. Aneuploidy and DNA replication in the normal human brain and Alzheimer's disease. J.Neurosci. 2007, 27:6859-6867.
21. Münch G., Gasic-Milenkovic J., Arendt T. Effect of advanced glycation endproducts on cell cycle and their relevance for Alzheimer's disease. J.Neural Transm. Suppl. 2003, 63-71.
22. Nagy Z. Cell cycle regulatory failure in neurones: causes and consequences. Neurobiol. Aging 2000, 21:761-769.
23. Packer L., Tritschler H.J., Wessel K. Neuroprotection by the metabolic antioxidant alpha-lipoic acid. Free Radic. Biol. Med. 1997, 22:359-378.
24. Ramassamy C., Averill D., Beffert U., Bastianetto S., Theroux L., Lussier-Cacan S., Cohn J.S., Christen Y., Davignon J., Quirion R., Poirier J. Oxidative damage and protection by antioxidants in the frontal cortex of Alzheimer's disease is related to the apolipoprotein E genotype. Free Radic. Biol. Med. 1999, 27:544-553.
25. Ramassamy C., Krzywkowski P., Averill D., Lussier-Cacan S., Theroux L., Christen Y., Davignon J., Poirier J. Impact of apoE deficiency on oxidative insults and antioxidant levels in the brain. Brain Res. Mol. Brain Res. 2001, 86:76-83.
26. Rehen S.K., Yung Y.C., McCreight M.P., Kaushal D., Yang A.H., Almeida B.S., Kingsbury M.A., Cabral K.M., McConnell M.J., Anliker B., Fontanoz M., Chun J. Constitutional aneuploidy in the normal human brain. J.Neurosci. 2005, 25:2176-2180.
27. Richter T., Münch G., Lüth H.J., Arendt T., Kientsch-Engel R., Stahl P., Fengler D., Kuhla B. Immunochemical crossreactivity of antibodies specific for "advanced glycation endproducts" with "advanced lipoxidation endproducts". Neurobiol. Aging 2005, 26:465-474.
28. Sajithlal G., Huttunen H., Rauvala H., Munch G. Receptor for advanced glycation end products plays a more important role in cellular survival than in neurite outgrowth during retinoic acid-induced differentiation of neuroblastoma cells. J.Biol. Chem. 2002, 277:6888-6897.
29. Satoh H., Togo M., Hara M., Miyata T., Han K., Maekawa H. Advanced glycation endproducts stimulate mitogen-activated protein kinase and proliferation in rabbit vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 1997, 239:111-115.
30. Schmidt A., Kuhla B., Bigl K., Münch G., Arendt T. Cell cycle related signaling in Neuro2a cells proceeds via the receptor for advanced glycation end products. J.Neural Transm. 2007, 114:1413-1424.
31. Smith M.A., Monnier V.M., Sayre L.M., Perry G. Amyloidosis, advanced glycation end products and Alzheimer disease. Neuroreport 1995, 6:1595-1596.
32. Vincent I., Jicha G., Rosado M., Dickson D.W. Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J.Neurosci. 1997, 17:3588-3598.
33. Vitek M.P., Bhattacharya K., Glendening J.M., Stopa E., Vlassara H., Bucala R., Manogue K., Cerami A. Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:4766-4770.
34. Wen T.C., Rogido M., Genetta T., Sola A. Permanent focal cerebral ischemia activates erythropoietin receptor in the neonatal rat brain. Neurosci. Lett. 2004, 355:165-168.
35. Wong A., Lüth H.J., Deuther-Conrad W., Dukic-Stefanovic S., Gasic-Milenkovic J., Arendt T., Münch G. Advanced glycation endproducts co-localize with inducible nitric oxide synthase in Alzheimer's disease. Brain Res. 2001, 920:32-40.
36. Yang Y., Geldmacher D.S., Herrup K. DNA replication precedes neuronal cell death in Alzheimer's disease. J.Neurosci. 2001, 21:2661-2668.
37. Yang Y., Herrup K. Loss of neuronal cell cycle control in ataxia-telangiectasia: a unified disease mechanism. J.Neurosci. 2005, 25:2522-2529.
38. Yang Y., Herrup K. Cell division in the CNS: protective response or lethal event in post-mitotic neurons?. Biochim. Biophys. Acta 2007, 1772:457-466.
39. Yang Y., Varvel N.H., Lamb B.T., Herrup K. Ectopic cell cycle events link human Alzheimer's disease and amyloid precursor protein transgenic mouse models. J.Neurosci. 2006, 26:775-784.
40. Yurov Y.B., Iourov I.Y., Monakhov V.V., Soloviev I.V., Vostrikov V.M., Vorsanova S.G. The variation of aneuploidy frequency in the developing and adult human brain revealed by an interphase FISH study. J.Histochem. Cytochem. 2005, 53:385-390.