Constitutively active Akt inhibits trafficking of amyloid precursor protein and amyloid precursor protein metabolites through feedback inhibition of phosphoinositide 3-kinase

Biochemistry

Volumn 48, Issue 17, 2009, Pages 3787-3794

  Shineman, Diana W ^a   Dain, Aleksandra S ^a   Kim, Minkyu L ^a   Lee, Virginia M Y ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; AMYLOID PLAQUES; AMYLOID PRECURSOR PROTEINS; CELLULAR SECRETION; CONSTITUTIVELY ACTIVES; DOWNSTREAM COMPONENTS; FEEDBACK INHIBITION; GROWTH FACTOR; INSULIN RECEPTOR SUBSTRATE-1; MOLECULAR TARGETS; MULTIPLE CELLS; OVER-EXPRESSION; PATHOPHYSIOLOGY; PHOSPHOINOSITIDE 3-KINASE; PROTEIN LEVEL; PROTEIN STABILITY; PROTEOLYTIC CLEAVAGE; SIGNALING PATHWAYS;

AMINES; CELL CULTURE; GLYCOPROTEINS; INSULIN; METABOLISM; METABOLITES; PEPTIDES; SIGNALING;

PUMPING PLANTS;

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SOMATOMEDIN C;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; METABOLITE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL LINE; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; CRICETULUS; FEEDBACK, BIOCHEMICAL; HUMANS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MICE; MYRISTIC ACID; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 66049094854     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi802070j     Document Type: Article

References (40)

1. Koo, E. H., and Squazzo, S. L. (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J. Biol. Chem. 269, 17386-17389. (Pubitemid 24218009)
2. Mattson, M. P. (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631-639. (Pubitemid 39061671)
3. Vetrivel, K. S., and Thinakaran, G. (2005) Amyloidogenic processing of {beta}-amyloid precursor protein in intracellular compartments. Neurology XX.
4. Ling, Y., Morgan, K., and Kalsheker, N. (2003) Amyloid precursor protein (APP) and the biology of proteolytic processing: relevance to Alzheimer's disease. Int. J. Biochem. Cell Biol. 35, 1505-1535. (Pubitemid 36724946)
5. Hardy, J. (2006) A hundred years of Alzheimer's disease research. Neuron 52, 3-13. (Pubitemid 44472602)
6. Sisodia, S. S. (1992) Beta-amyloid precursor protein cleavage by a membrane-bound protease. Proc. Natl. Acad. Sci. U S.A. 89, 6075-6079.
7. Yan, R., Han, P., Miao, H., Greengard, P., and Xu, H. (2001) The transmembrane domain of the Alzheimer's beta-secretase (BACE1) determines its late Golgi localization and access to beta -amyloid precursor protein (APP) substrate. J. Biol. Chem. 276, 36788-36796. (Pubitemid 37384295)
8. Kinoshita, A., Fukumoto, H., Shah, T., Whelan, C. M., Irizarry, M. C., and Hyman, B. T. (2003) Demonstration by FRET of BACE interaction with the amyloid precursor protein at the cell surface and in early endosomes. J. Cell Sci. 116, 3339-3346. (Pubitemid 37038982)
9. Chyung, J. H., Raper, D. M., and Selkoe, D. J. (2005) Gamma-secretase exists on the plasma membrane as an intact complex that accepts substrates and effects intramembrane cleavage. J. Biol. Chem. 280, 4383-4392. (Pubitemid 40288602)
10. Annaert, W. G., Levesque, L., Craessaerts, K., Dierinck, I., Snellings, G., Westaway, D., George-Hyslop, P. S., Cordell, B., Fraser, P., and De Strooper, B. (1999) Presenilin 1 controls gamma-secretase processing of amyloid precursor protein in pre-Golgi compartments of hippocampal neurons. J. Cell Biol. 147, 277-294. (Pubitemid 29496338)
11. Chyung, A. S., Greenberg, B. D., Cook, D. G., Doms, R. W., and Lee, V. M. Y. (1997) Novel beta-secretase cleavage of beta-amyloid precursor protein in the endoplasmic reticulum/intermediate compartment of NT2N cells. J. Cell Biol. 138, 671-680. (Pubitemid 27349846)
12. Taniguchi, C. M., Emanuelli, B., and Kahn, C. R. (2006) Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 7, 85-96. (Pubitemid 43278292)
13. Farese, R. V., Sajan, M. P., and Standaert, M. L. (2005) Atypical protein kinase C in insulin action and insulin resistance. Biochem. Soc. Trans. 33, 350-353.
14. Welsh, G. I., Hers, I., Berwick, D. C., Dell, G., Wherlock, M., Birkin, R., Leney, S., and Tavare, J. M. (2005) Role of protein kinase B in insulin-regulated glucose uptake. Biochem. Soc. Trans. 33, 346-349. (Pubitemid 40604369)
15. Gasparini, L., Gouras, G. K., Wang, R., Gross, R. S., Beal, M. F., Greengard, P., and Xu, H. (2001) Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. J. Neurosci. 21, 2561-2570. (Pubitemid 32298198)
16. Solano, D. C., Sironi, M., Bonfini, C., Solerte, S. B., Govoni, S., and Racchi, M. (2000) Insulin regulates soluble amyloid precursor protein release via phosphatidyl inositol 3 kinase-dependent pathway. FASEB J. 14, 1015-1022. (Pubitemid 30241680)
17. Adlerz, L., Holback, S., Multhaup, G., and Iverfeldt, K. (2007) IGF-1-induced processing of the amyloid precursor protein family is mediated by different signaling pathways. J. Biol. Chem. 282, 10203-10209. (Pubitemid 47093446)
18. Petanceska, S. S., and Gandy, S. (1999) The phosphatidylinositol 3-kinase inhibitor wortmannin alters the metabolism of the Alzheimer's amyloid precursor protein. J. Neurochem. 73, 2316-2320.
19. Forman, M. S., Cook, D. G., Leight, S., Doms, R. W., and Lee, V. M. Y. (1997) Differential effects of the swedish mutant amyloid precursor protein on beta-amyloid accumulation and secretion in neurons and nonneuronal cells. J. Biol. Chem. 272, 32247-32253. (Pubitemid 28011902)
20. Gravina, S. A., Ho, L., Eckman, C. B., Long, K. E., Otvos, L., Jr., Younkin, L. H., Suzuki, N., and Younkin, S. G. (1995) Amyloid beta protein (A beta) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at A beta 40 or A beta 42(43). J. Biol. Chem. 270, 7013-7016.
21. Wertkin, A. M., Turner, R. S., Pleasure, S. J., Golde, T. E., Younkin, S. G., Trojanowski, J. Q., and Lee, V. M. Y. (1993) Human neurons derived from a teratocarcinoma cell line express solely the 695-amino acid amyloid precursor protein and produce intracellular beta-amyloid or A4 peptides. Proc. Natl. Acad. Sci. U.S.A. 90, 9513-9517. (Pubitemid 23315815)
22. Turner, R. S., Suzuki, N., Chyung, A. S., Younkin, S. G., and Lee, V. M. Y. (1996) Amyloids beta40 and beta42 are generated intracellularly in cultured human neurons and their secretion increases with maturation. J. Biol. Chem. 271, 8966-8970. (Pubitemid 26123324)
23. Lee, E. B., Zhang, B., Liu, K., Greenbaum, E. A., Doms, R. W., Trojanowski, J. Q., and Lee, V. M. Y. (2005) BACE overexpression alters the subcellular processing of APP and inhibits Abeta deposition in vivo. J. Cell Biol. 168, 291-302. (Pubitemid 40248226)
24. Nagoshi, T., Matsui, T., Aoyama, T., Leri, A., Anversa, P., Li, L., Ogawa, W., del Monte, F., Gwathmey, J. K., Grazette, L., Hemmings, B. A., Kass, D. A., Champion, H. C., and Rosenzweig, A. (2005) PI3K rescues the detrimental effects of chronic Akt activation in the heart during ischemia/reperfusion injury. J Clin. Invest. 115, 2128-2138. (Pubitemid 41134154)
25. Gual, P., Marchand-Brustel, Y., and Tanti, J. F. (2005) Positive and negative regulation of insulin signaling through IRS-1 phosphorylation. Biochimie 87, 99-109. (Pubitemid 40298772)
26. Hers, I., and Tavare, J. M. (2005) Mechanism of feedback regulation of insulin receptor substrate-1 phosphorylation in primary adipocytes. Biochem. J. 388, 713-720. (Pubitemid 40839949)
27. Harrington, L. S., Findlay, G. M., and Lamb, R. F. (2005) Restraining PI3K: mTOR signalling goes back to the membrane Trends. Biochem. Sci. 30, 35-42. (Pubitemid 40093739)
28. Aguirre, V., Uchida, T., Yenush, L., Davis, R., and White, M. F. (2000) The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J. Biol. Chem. 275, 9047-9054. (Pubitemid 30180265)
29. Li, Y., Soos, T. J., Li, X., Wu, J., Degennaro, M., Sun, X., Littman, D. R., Birnbaum, M. J., and Polakiewicz, R. D. (2004) Protein kinase C Theta inhibits insulin signaling by phosphorylating IRS1 at Ser(1101). J. Biol. Chem. 279, 45304-45307. (Pubitemid 39491511)
30. Gao, Z., Hwang, D., Bataille, F., Lefevre, M., York, D., Quon, M. J., and Ye, J. (2002) Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J. Biol. Chem. 277, 48115-48121. (Pubitemid 35470759)
31. Mothe, I., and Van Obberghen, E. (1996) Phosphorylation of insulin receptor substrate-1 on multiple serine residues, 612, 632, 662, and 731, modulates insulin action. J. Biol. Chem. 271, 11222-11227. (Pubitemid 26155955)
32. Ravichandran, L. V., Esposito, D. L., Chen, J., and Quon, M. J. (2001) Protein kinase C-zeta phosphorylates insulin receptor substrate-1 and impairs its ability to activate phosphatidylinositol 3-kinase in response to insulin. J. Biol. Chem. 276, 3543-3549. (Pubitemid 37411655)
33. Chang, Q., Li, Y., White, M. F., Fletcher, J. A., and Xiao, S. (2002) Constitutive activation of insulin receptor substrate 1 is a frequent event in human tumors: therapeutic implications. Cancer Res. 62, 6035-6038. (Pubitemid 35244449)
34. Bellacosa, A., Testa, J. R., Staal, S. P., and Tsichlis, P. N. (1991) A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science 254, 274-277. (Pubitemid 21917339)
35. Imamura, T., Huang, J., Usui, I., Satoh, H., Bever, J., and Olefsky, J. M. (2003) Insulin-induced GLUT4 translocation involves protein kinase C-lambda-mediated functional coupling between Rab4 and the motor protein kinesin. Mol. Cell. Biol. 23, 4892-4900. (Pubitemid 36793335)
36. 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)
37. Stein, T. D., Anders, N. J., DeCarli, C., Chan, S. L., Mattson, M. P., and Johnson, J. A. (2004) Neutralization of transthyretin reverses the neuroprotective effects of secreted amyloid precursor protein (APP) in APPSW mice resulting in tau phosphorylation and loss of hippocampal neurons: support for the amyloid hypothesis. J. Neurosci. 24, 7707-7717. (Pubitemid 39186826)
38. Caille, I., Allinquant, B., Dupont, E., Bouillot, C., Langer, A., Muller, U., and Prochiantz, A. (2004) Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development 131, 2173-2181. (Pubitemid 38702048)
39. Echeverria, V., and Cuello, A. C. (2002) Intracellular A-beta amyloid, a sign for worse things to come? Mol. Neurobiol. 26, 299-316. (Pubitemid 35239806)
40. Skovronsky, D. M., Doms, R. W., and Lee, V. M. Y. (1998) Detection of a novel intraneuronal pool of insoluble amyloid beta protein that accumulates with time in culture. J. Cell Biol. 141, 1031-1039. (Pubitemid 28243969)