The amyloid precursor protein (APP) family members are key players in S-adenosylmethionine formation by MAT2A and modify BACE1 and PSEN1 gene expression-relevance for Alzheimer's disease

Molecular and Cellular Proteomics

Volumn 11, Issue 11, 2012, Pages 1274-1288

  Schrötter, Andreas ^a   Pfeiffer, Kathy ^a   El Magraoui, Fouzi ^b   Platta, Harald W ^b   Erdmann, Ralf ^b   Meyer, Helmut E ^a   Egensperger, Rupert ^c   Marcus, Katrin ^a   Mul̈ler, Thorsten ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; AMYLOID PRECURSOR PROTEIN; APLP1 PROTEIN; APLP2 PROTEIN; BETA SECRETASE 1; CALCYCLIN BINDING PROTEIN; COILED COIL DOMAIN CONTAINING PROTEIN 56; DREBRIN LIKE PROTEIN; DYNACTIN; IRON REGULATORY PROTEIN 1; ISOLEUCINE TRANSFER RNA LIGASE; MESSENGER RNA; METHIONINE; METHIONINE ADENOSYLTRANSFERASE II ALPHA; NUCLEOSIDE TRIPHOSPHATE PHOSPHOHYDROLASE; PEROXIREDOXIN 4; PHOSPHOHISTIDINE PHOSPHATASE 1; PROTEIN; PROTEIN BAX; PROTEIN DNAJ; PSEN1 PROTEIN; RNA BINDING PROTEIN 25; S ADENOSYLMETHIONINE; SIDEROFLEXIN 1; SMALL NUCLEAR RIBONUCLEOPROTEIN SM D1; SUPERKILLER VIRALICIDIC ACTIVITY 2 LIKE 2; TREACLE PROTEIN; TRUNCATED BETA GLOBIN; UBIQUILIN 2; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; METHYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ACID ENDOPEPTIDASES; CEREBRAL CORTEX; DOWN-REGULATION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; METHIONINE ADENOSYLTRANSFERASE; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PEROXIREDOXINS; PRESENILIN-1; PROTEOME; REPRODUCIBILITY OF RESULTS; S-ADENOSYLMETHIONINE; STAINING AND LABELING;

EID: 84869223239     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.019364     Document Type: Article

References (53)

1. Zheng, H., and Koo, E. H. (2006) The amyloid precursor protein: beyond amyloid. Mol. Neurodegener. 1, 5
2. Müller, T., Meyer, H. E., Egensperger, R., and Marcus, K. (2008) The amyloid precursor protein intracellular domain (AICD) as modulator of gene expression, apoptosis, and cytoskeletal dynamics-Relevance for Alzheimer's disease. Prog. Neurobiol. 85, 393-406
3. Nikolaev, A., McLaughlin, T., O'Leary, D. D., and Tessier-Lavigne, M. (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457, 981-989
4. Müller, T., Concannon, C. G., Ward, M. W., Walsh, C. M., Tirniceriu, A. L., Tribl, F., Kogel, D., Prehn, J. H., and Egensperger, R. (2007) Modulation of Gene Expression and Cytoskeletal Dynamics by the Amyloid Precursor Protein Intracellular Domain (AICD). Mol. Biol. Cell 18, 201-210 (Pubitemid 46066721)
5. Furukawa, K., Sopher, B. L., Rydel, R. E., Begley, J. G., Pham, D. G., Martin, G. M., Fox, M., and Mattson, M. P. (1996) Increased activity-regulating and neuroprotective efficacy of alpha-secretase-derived secreted amyloid precursor protein conferred by a C-terminal heparin-binding domain. J. Neurochem. 67, 1882-1896 (Pubitemid 26349661)
6. Eggert, S., Paliga, K., Soba, P., Evin, G., Masters, C. L., Weidemann, A., and Beyreuther, K. (2004) The proteolytic processing of the amyloid precursor protein gene family members APLP-1 and APLP-2 involves alpha-, beta-, gamma-, and epsilon-like cleavages: modulation of APLP-1 processing by n-glycosylation. J. Biol. Chem. 279, 18146-18156 (Pubitemid 38623227)
7. Herms, J., Anliker, B., Heber, S., Ring, S., Fuhrmann, M., Kretzschmar, H., Sisodia, S., and Müller, U. (2004) Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J. 23, 4106-4115 (Pubitemid 39472431)
8. Ring, S., Weyer, S. W., Kilian, S. B., Waldron, E., Pietrzik, C. U., Filippov, M. A., Herms, J., Buchholz, C., Eckman, C. B., Korte, M., Wolfer, D. P., and Müller, U. C. (2007) The secreted beta-amyloid precursor protein ectodomain APPs alpha is sufficient to rescue the anatomical, behavioral, and electrophysiological abnormalities of APP-deficient mice. J. Neurosci. 27, 7817-7826 (Pubitemid 47093823)
9. Wang, P., Yang, G., Mosier, D. R., Chang, P., Zaidi, T., Gong, Y. D., Zhao, N. M., Dominguez, B., Lee, K. F., Gan, W. B., and Zheng, H. (2005) Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-Like protein 2. J. Neurosci. 25, 1219-1225 (Pubitemid 40268964)
10. Bergmans, B. A., Shariati, S. A., Habets, R. L., Verstreken, P., Schoonjans, L., Müller, U., Dotti, C. G., and De, S. B. (2010) Neurons generated from APP/APLP1/APLP2 triple knockout embryonic stem cells behave normally in vitro and in vivo: lack of evidence for a cell autonomous role of the amyloid precursor protein in neuronal differentiation. Stem Cells 28, 399-406
11. Schrenk-Siemens, K., Perez-Alcala, S., Richter, J., Lacroix, E., Rahuel, J., Korte, M., Müller, U., Barde, Y. A., and Bibel, M. (2008) Embryonic stem cell-derived neurons as a cellular system to study gene function: lack of amyloid precursor proteins APP and APLP2 leads to defective synaptic transmission. Stem Cells 26, 2153-2163
12. Lannfelt, L., Basun, H., Wahlund, L. O., Rowe, B. A., and Wagner, S. L. (1995) Decreased alpha-secretase-cleaved amyloid precursor protein as a diagnostic marker for Alzheimer's disease. Nat. Med. 1, 829-832
13. Nakaya, T., and Suzuki, T. (2006) Role of APP phosphorylation in FE65-dependent gene transactivation mediated by AICD. Genes Cells 11, 633-645 (Pubitemid 43744814)
14. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408 (Pubitemid 34164012)
15. Müller, T., Loosse, C., Schrötter, A., Schnabel, A., Helling, S., Egensperger, R., and Marcus, K. (2011) The AICD interacting protein DAB1 is upregulated in Alzheimer frontal cortex brain samples and causes deregulation of proteins involved in gene expression changes. Curr. AlzheimerRes. 8, 573-582
16. Spitzer, P., Klafki, H. W., Blennow, K., Buee, L., Esselmann, H., Herruka, S. K., Jimenez, C., Klivenyi, P., Lewczuk, P., Maler, J. M., Markus, K., Meyer, H. E., Morris, C., Muller, T., Otto, M., Parnetti, L., Soininen, H., Schraen, S., Teunissen, C., Vecsei, L., Zetterberg, H., and Wiltfang, J. (2010) cNEUPRO: novel biomarkers for neurodegenerative diseases. Int.J. Alzheimers. Dis. pii, 548145
17. Reidegeld, K. A., Eisenacher, M., Kohl, M., Chamrad, D., Korting, G., Blüggel, M., Meyer, H. E., and Stephan, C. (2008) An easy-to-use Decoy Database Builder software tool, implementing different decoy strategies for false discovery rate calculation in automated MS/MS protein identifications. Proteomics. 8, 1129-1137 (Pubitemid 351462918)
18. Müller, T., Schrötter, A., Loosse, C., Helling, S., Stephan, C., Ahrens, M., Uszkoreit, J., Eisenacher, M., Meyer, H. E., and Marcus, K. (2011) Sense and nonsense of pathway analysis software in proteomics. J. Proteome.Res. 10, 5398-5408
19. Benjamni, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc.B 57, 289-300
20. Braak, H., and Braak, E. (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82, 239-259
21. Mirra, S. S., Heyman, A., McKeel, D., Sumi, S. M., Crain, B. J., Brownlee, L. M., Vogel, F. S., Hughes, J. P., van Belle, G., and Berg, L. (1991) The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41, 479-486
22. Katoh, Y., Ikura, T., Hoshikawa, Y., Tashiro, S., Ito, T., Ohta, M., Kera, Y., Noda, T., and Igarashi, K. (2011) Methionine adenosyltransferase II serves as a transcriptional corepressor of Maf oncoprotein. Mol. Cell 41, 554-566
23. Panza, F., Frisardi, V., Capurso, C., D'Introno, A., Colacicco, A. M., Vendemiale, G., Capurso, A., and Solfrizzi, V. (2009) Possible role of Sadenosylmethionine, S-adenosylhomocysteine, and polyunsaturated fatty acids in predementia syndromes and Alzheimer's disease. J. Alzheimers.Dis. 16, 467-470
24. Kim, S. H., Fountoulakis, M., Cairns, N., and Lubec, G. (2001) Protein levels of human peroxiredoxin subtypes in brains of patients with Alzheimer's disease and Down syndrome. J. Neural Transm. 61, 223-235 (Pubitemid 38085085)
25. Morrison, L. D., Smith, D. D., and Kish, S. J. (1996) Brain S-adenosylmethionine levels are severely decreased in Alzheimer's disease. J. Neurochem.67, 1328-1331 (Pubitemid 26277949)
26. Gomes, Trolin, C., Regland, B., and Oreland, L. (1995) Decreased methionine adenosyltransferase activity in erythrocytes of patients with dementia disorders. Eur. Neuropsychopharmacol. 5, 107-114
27. Trolin, C. G., Löfberg, C., Trolin, G., and Oreland, L. (1994) Brain ATP:L-methionine S-adenosyltransferase (MAT), S-adenosylmethionine (SAM) and S-adenosylhomocysteine (SAH): regional distribution and age-related changes. Eur. Neuropsychopharmacol. 4, 469-477
28. Bottiglieri, T., Godfrey, P., Flynn, T., Carney, M. W., Toone, B. K., and Reynolds, E. H. (1990) Cerebrospinal fluid S-adenosylmethionine in depression and dementia: effects of treatment with parenteral and oral S- adenosylmethionine. J. Neurol. Neurosurg. Psychiatry 53, 1096-1098
29. Fuso, A., Seminara, L., Cavallaro, R. A., D'Anselmi, F., and Scarpa, S. (2005) S-adenosylmethionine/homocysteine cycle alterations modify DNA methylation status with consequent deregulation of PS1 and BACE and beta-amyloid production. Mol. Cell Neurosci. 28, 195-204 (Pubitemid 39656023)
30. Jackson, A. L., Bartz, S. R., Schelter, J., Kobayashi, S. V., Burchard, J., Mao, M., Li, B., Cavet, G., and Linsley, P. S. (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21, 635-637
31. von Koch, C. S., Zheng, H., Chen, H., Trumbauer, M., Thinakaran, G., van der Ploeg, L. H., Price, D. L., and Sisodia, S. S. (1997) Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol. Aging 18, 661-669
32. Heber, S., Herms, J., Gajic, V., Hainfellner, J., Aguzzi, A., Rülicke, T., von Kretzschmar, H., von Koch, C., Sisodia, S., Tremml, P., Lipp, H. P., Wolfer, D. P., and Muller, U. (2000) Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J. Neurosci. 20, 7951-7963
33. Sannerud, R., and Annaert, W. (2009) Trafficking, a key player in regulated intramembrane proteolysis. Semin. Cell Dev. Biol. 20, 183-190
34. Miller, A. L. (2008) The methylation, neurotransmitter, and antioxidant connections between folate and depression. Altern. Med. Rev. 13, 216-226
35. Martinez-Chantar, M. L., Latasa, M. U., Varela-Rey, M., Lu, S. C., Garcia-Trevijano, E. R., Mato, J. M., and Avila, M. A. (2003) L-methionine availability regulates expression of the methionine adenosyltransferase 2A gene in human hepatocarcinoma cells: role of S-adenosylmethionine. J. Biol. Chem. 278, 19885-19890 (Pubitemid 36799177)
36. Martinez-Chantar, M. L., Garcia-Trevijano, E. R., Latasa, M. U., Martin-Duce, A., Fortes, P., Caballeria, J., Avila, M. A., and Mato, J. M. (2003) Methionine adenosyltransferase II beta subunit gene expression provides a proliferative advantage in human hepatoma. Gastroenterology124, 940-948 (Pubitemid 36389797)
37. Liu, Q., Wu, K., Zhu, Y., He, Y., Wu, J., and Liu, Z. (2007) Silencing MAT2A gene by RNA interference inhibited cell growth and induced apoptosis in human hepatoma cells. Hepatol. Res. 37, 376-388 (Pubitemid 46605423)
38. Cohen, B. M., Satlin, A., and Zubenko, G. S. (1988) S-adenosyl-L- methionine in the treatment of Alzheimer's disease. J. Clin. Psychopharmacol.8, 43-47 (Pubitemid 18053896)
39. Knopman, D., and Patterson, M. (2001) An open-label, 24-week pilot study of the methyl donor betaine in Alzheimer disease patients. Alzheimer Dis.Assoc. Disord. 15, 162-165 (Pubitemid 32807941)
40. Shea, T. B., and Chan, A. (2008) S-adenosyl methionine: a natural therapeutic agent effective against multiple hallmarks and risk factors associated with Alzheimer's disease. J. Alzheimers. Dis. 13, 67-70 (Pubitemid 351365628)
41. Selley, M. L. (2007) A metabolic link between S-adenosylhomocysteine and polyunsaturated fatty acid metabolism in Alzheimer's disease. Neurobiol.Aging 28, 1834-1839
42. Goodger, Z. V., Rajendran, L., Trutzel, A., Kohli, B. M., Nitsch, R. M., and Konietzko, U. (2009) Nuclear signaling by the APP intracellular domain occurs predominantly through the amyloidogenic processing pathway. J. Cell Sci. 122, 3703-3714
43. Cavallaro, R. A., Fuso, A., Nicolia, V., and Scarpa, S. (2010) S-adenosylmethionine prevents oxidative stress and modulates glutathione metabolism in TgCRND8 mice fed a B-vitamin deficient diet. J. Alzheimers. Dis.20, 997-1002
44. Wang, H. Q., Du, Z. X., Liu, B. Q., Gao, Y. Y., Meng, X., Guan, Y., and Zhang, H. Y. (2009) TNF-related apoptosis-inducing ligand suppresses PRDX4 expression. FEBS Lett. 583, 1511-1515
45. Axelsen, P. H., Komatsu, H., and Murray, I. V. (2011) Oxidative stress and cell membranes in the pathogenesis of Alzheimer's disease. Physiology26, 54-69
46. Mattson, M. P., and Pedersen, W. A. (1998) Effects of amyloid precursor protein derivatives and oxidative stress on basal forebrain cholinergic systems in Alzheimer's disease. Int. J. Dev. Neurosci. 16, 737-753 (Pubitemid 29151762)
47. Lee, H. P., Zhu, X., Casadesus, G., Castellani, R. J., Nunomura, A., Smith, M. A., Lee, H. G., and Perry, G. (2010) Antioxidant approaches for the treatment of Alzheimer's disease. Expert. Rev. Neurother. 10, 1201-1208
48. Scarpa, S., Fuso, A., D'Anselmi, F., and Cavallaro, R. A. (2003) Presenilin 1 gene silencing by S-adenosylmethionine: a treatment for Alzheimer disease? FEBS Lett. 541, 145-148 (Pubitemid 36428933)
49. Lichtenthaler, S. F., Haass, C., and Steiner, H. (2011) Regulated intramembrane proteolysis-lessons from amyloid precursor protein processing. J. Neurochem. 117, 779-796
50. Schliebs, R., and Arendt, T. (2011) The cholinergic system in aging and neuronal degeneration. Behav. Brain Res. 221, 555-563
51. Blusztajn, J. K., Liscovitch, M., Mauron, C., Richardson, U. I., and Wurtman, R. J. (1987) Phosphatidylcholine as a precursor of choline for acetylcholine synthesis. J. Neural Transm. Suppl. 24, 247-259
52. Yang, G., Gong, Y. D., Gong, K., Jiang, W. L., Kwon, E., Wang, P., Zheng, H., Zhang, X. F., Gan, W. B., and Zhao, N. M. (2005) Reduced synaptic vesicle density and active zone size in mice lacking amyloid precursor protein (APP) and APP-like protein 2. Neurosci. Lett. 384, 66-71 (Pubitemid 40826619)
53. Martorana, A., Esposito, Z., and Koch, G. (2010) Beyond the cholinergic hypothesis: do current drugs work in Alzheimer's disease? CNS. Neurosci.Ther. 16, 235-245