Fyn kinase regulates the association between amyloid precursor protein and Dab1 by promoting their localization to detergent-resistant membranes

Journal of Neurochemistry

Volumn 118, Issue 5, 2011, Pages 879-890

  Minami, S Sakura ^a,b   Hoe, Hyang Sook ^a   Rebeck, G William ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

adaptor protein; amyloid; lipid raft; reelin; tyrosine kinase

Indexed keywords

ADAPTOR PROTEIN; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E2; DETERGENT; DISABLED 1; PROTEIN KINASE FYN; PROTEIN TYROSINE KINASE; REELIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FRACTIONATION; CELL MEMBRANE; CONTROLLED STUDY; ENZYME REGULATION; IMMUNOPRECIPITATION; LIPID RAFT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; WESTERN BLOTTING;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL MEMBRANE; CELLS, CULTURED; CEREBRAL CORTEX; DETERGENTS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX PROTEINS; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FYN; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; TYROSINE;

MUS;

EID: 80051776265     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07296.x     Document Type: Article

References (54)

1. Arnaud L., Ballif B. A., and, Cooper J. A., (2003) Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell. Biol. 23, 9293-9302. (Pubitemid 37499816)
2. Bock H. H., Jossin Y., May P., Bergner O., and, Herz J., (2004) Apolipoprotein E receptors are required for reelin-induced proteasomal degradation of the neuronal adaptor protein Disabled-1. J. Biol. Chem. 279, 33471-33479. (Pubitemid 39062996)
3. Borg J. P., Ooi J., Levy E., and, Margolis B., (1996) The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein. Mol. Cell. Biol. 16, 6229-6241. (Pubitemid 26360983)
4. Borg J. P., Straight S. W., Kaech S. M., de Taddeo-Borg M., Kroon D. E., Karnak D., Turner R. S., Kim S. K., and, Margolis B., (1998) Identification of an evolutionarily conserved heterotrimeric protein complex involved in protein targeting. J. Biol. Chem. 273, 31633-31636. (Pubitemid 29177088)
5. Brown D. A., and, Rose J. K., (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544.
6. Delint-Ramirez I., Fernandez E., Bayes A., Kicsi E., Komiyama N. H., and, Grant S. G., (2010) In vivo composition of NMDA receptor signaling complexes differs between membrane subdomains and is modulated by PSD-95 and PSD-93. J. Neurosci. 30, 8162-8170.
7. Filipp D., Zhang J., Leung B. L., Shaw A., Levin S. D., Veillette A., and, Julius M., (2003) Regulation of Fyn through translocation of activated Lck into lipid rafts. J. Exp. Med. 197, 1221-1227. (Pubitemid 36570078)
8. Frears E. R., Stephens D. J., Walters C. E., Davies H., and, Austen B. M., (1999) The role of cholesterol in the biosynthesis of beta-amyloid. Neuroreport 10, 1699-1705.
9. Gallagher E., Howell B. W., Soriano P., Cooper J. A., and, Hawkes R., (1998) Cerebellar abnormalities in the disabled (mdab1-1) mouse. J. Comp. Neurol. 402, 238-251. (Pubitemid 28533321)
10. Goffinet A. M., (1979) An early development defect in the cerebral cortex of the reeler mouse. A morphological study leading to a hypothesis concerning the action of the mutant gene. Anat. Embryol. (Berl) 157, 205-216. (Pubitemid 10192068)
11. Gotthardt M., Trommsdorff M., Nevitt M. F., Shelton J., Richardson J. A., Stockinger W., Nimpf J., and, Herz J., (2000) Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J. Biol. Chem. 275, 25616-25624.
12. Guenette S. Y., Chen J., Jondro P. D., and, Tanzi R. E., (1996) Association of a novel human FE65-like protein with the cytoplasmic domain of the beta-amyloid precursor protein. Proc. Natl. Acad. Sci. U S A 93, 10832-10837. (Pubitemid 26333075)
13. He X., Cooley K., Chung C. H., Dashti N., and, Tang J., (2007) Apolipoprotein receptor 2 and X11 alpha/beta mediate apolipoprotein E-induced endocytosis of amyloid-beta precursor protein and beta-secretase, leading to amyloid-beta production. J. Neurosci. 27, 4052-4060. (Pubitemid 46597171)
14. Herz J., and, Beffert U., (2000) Apolipoprotein E receptors: linking brain development and Alzheimer's disease. Nat. Rev. Neurosci. 1, 51-58.
15. Hiesberger T., Trommsdorff M., Howell B. W., Goffinet A., Mumby M. C., Cooper J. A., and, Herz J., (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24, 481-489. (Pubitemid 29508421)
16. Ho G. J., Hashimoto M., Adame A., Izu M., Alford M. F., Thal L. J., Hansen L. A., and, Maslish E., (2005) Altered p59Fyn kinase expression accompanies disease progression in Alzheimer's disease: implications for its functional role. Neurobiol. Aging 26, 625-635. (Pubitemid 40228754)
17. Hoe H. S., Magill L. A., Fu Z., Vicini S., and, Rebeck G. W., (2006a) FE65 interaction with the apoE receptor ApoEr2. J. Biol. Chem. 281, 24521-24530. (Pubitemid 44274227)
18. Hoe H. S., Tran T. S., Matsuoka Y., Howell B. W., and, Rebeck G. W., (2006b) Dab1 and Reelin effects on APP and ApoEr2 trafficking and processing. J. Biol. Chem. 281, 35176-35185. (Pubitemid 46036557)
19. Hoe H. S., Minami S. S., Makarova A., Lee J., Hyman B. T., Matsuoka Y., and, Rebeck G. W., (2008) Fyn modulation of Dab1 effects on amyloid precursor protein and ApoE receptor 2 processing. J. Biol. Chem. 283, 6288-6299.
20. Hoe H. S., Fu Z., Makarova A., et al. (2009a) The effects of amyloid precursor protein on postsynaptic composition and activity. J. Biol. Chem. 284, 8495-8506.
21. Hoe H. S., Lee K. J., Carney R. S., et al. (2009b) Interaction of reelin with amyloid precursor protein promotes neurite outgrowth. J. Neurosci. 29, 7459-7473.
22. Howell B. W., Herrick T. M., and, Cooper J. A., (1999) Reelin-induced tyrosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev. 13, 643-648. (Pubitemid 29155970)
23. Huse J. T., Pijak D. S., Leslie G. J., Lee V. M., and, Doms R. W., (2000) Maturation and endosomal targeting of beta-site amyloid precursor protein-cleaving enzyme. The Alzheimer's disease beta-secretase. J. Biol. Chem. 275, 33729-33737.
24. Inomata M., Takayama Y., Kiyama H., Nada S., Okada M., and, Nakagawa H., (1994) Regulation of Src family kinases in the developing rat brain: correlation with their regulator kinase, Csk. J. Biochem. 116, 386-392. (Pubitemid 24265614)
25. Ittner L. M., Ke Y. D., Delerue F., et al. (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 142, 387-397.
26. Kivipelto M., Helkala E. L., Laakso M. P., Hanninen T., Hallikainen M., Alhainen K., Soininen H., Tuomilehto J., and, Nissinen A., (2001) Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study. Br. Med. J. 322, 1447-1451. (Pubitemid 32575406)
27. Kramer E. M., Klein C., Koch T., Boytinck M., and, Trotter J., (1999) Compartmentation of Fyn kinase with glycosylphosphatidylinositol-anchored molecules in oligodendrocytes facilitates kinase activation during myelination. J. Biol. Chem. 274, 29042-29049.
28. Lau K. F., McLoughlin D. M., Standen C. L., Irving N. G., and, Miller C. C., (2000) Fe65 and X11beta co-localize with and compete for binding to the amyloid precursor protein. Neuroreport 11, 3607-3610.
29. Lee J., Retamal C., Cuitino L., Caruano-Yzermans A., Shin J. E., van Kerkhof P., Marzolo M. P., and, Bu G., (2008) Adaptor protein sorting nexin 17 regulates amyloid precursor protein trafficking and processing in the early endosomes. J. Biol. Chem. 283, 11501-11508.
30. Marengere L. E., and, Pawson T., (1994) Structure and function of SH2 domains. J. Cell Sci. Suppl. 18, 97-104.
31. Minami S. S., Sung Y. M., Dumanis S. B., et al. (2009) The cytoplasmic adaptor protein X11{alpha} and extracellular matrix protein Reelin regulate ApoE receptor 2 trafficking and cell movement. FASEB J. 24, 58-69.
32. Nishitomi K., Sakaguchi G., Horikoshi Y., et al. (2006) BACE1 inhibition reduces endogenous Abeta and alters APP processing in wild-type mice. J. Neurochem. 99, 1553-1563.
33. Pappolla M. A., Bryant-Thomas T. K., Herbert D., et al. (2003) Mild hypercholesterolemia is an early risk factor for the development of Alzheimer amyloid pathology. Neurology 61, 199-205. (Pubitemid 36875301)
34. Parisiadou L., and, Efthimiopoulos S., (2007) Expression of mDab1 promotes the stability and processing of amyloid precursor protein and this effect is counteracted by X11alpha. Neurobiol. Aging 28, 377-388. (Pubitemid 46188492)
35. Parkin E. T., Hussain I., Karran E. H., Turner A. J., and, Hooper N. M., (1999) Characterization of detergent-insoluble complexes containing the familial Alzheimer's disease-associated presenilins. J. Neurochem. 72, 1534-1543. (Pubitemid 29140826)
36. Parvathy S., Hussain I., Karran E. H., Turner A. J., and, Hooper N. M., (1999) Cleavage of Alzheimer's amyloid precursor protein by alpha-secretase occurs at the surface of neuronal cells. Biochemistry 38, 9728-9734.
37. Peterziel H., Sackmann T., Strelau J., Kuhn P. H., Lichtenthaler S. F., Marom K., Klar A., and, Unsicker K., (2011) F-spondin regulates neuronal survival through activation of disabled-1 in the chicken ciliary ganglion. Mol. Cell. Neurosci. 46, 483-497.
38. Pramatarova A., Chen K., and, Howell B. W., (2008) A genetic interaction between the APP and Dab1 genes influences brain development. Mol. Cell. Neurosci. 37, 178-186. (Pubitemid 350300003)
39. Qiu Z., Hyman B. T., and, Rebeck G. W., (2004) Apolipoprotein E receptors mediate neurite outgrowth through activation of p44/42 mitogen-activated protein kinase in primary neurons. J. Biol. Chem. 279, 34948-34956. (Pubitemid 39318131)
40. Qiu S., Korwek K. M., Pratt-Davis A. R., Peters M., Bergman M. Y., and, Weeber E. J., (2006) Cognitive disruption and altered hippocampus synaptic function in Reelin haploinsufficient mice. Neurobiol. Learn. Mem. 85, 228-242.
41. Refolo L. M., Malester B., LaFrancois J., Bryant-Thomas T., Wang R., Tint G. S., Sambamurti K., Duff K., and, Pappolla M. A., (2000) Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol. Dis. 7, 321-331.
42. Riddell D. R., Christie G., Hussain I., and, Dingwall C., (2001) Compartmentalization of beta-secretase (Asp2) into low-buoyant density, noncaveolar lipid rafts. Curr. Biol. 11, 1288-1293. (Pubitemid 32774087)
43. Sastre M., Turner R. S., and, Levy E., (1998) X11 interaction with beta-amyloid precursor protein modulates its cellular stabilization and reduces amyloid beta-protein secretion. J. Biol. Chem. 273, 22351-22357. (Pubitemid 28399796)
44. Shirazi S. K., and, Wood J. G., (1993) The protein tyrosine kinase, fyn, in Alzheimer's disease pathology. Neuroreport 4, 435-437. (Pubitemid 23116742)
45. Simons K., and, Toomre D., (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
46. Stolt P. C., and, Bock H. H., (2006) Modulation of lipoprotein receptor functions by intracellular adaptor proteins. Cell. Signal. 18, 1560-1571. (Pubitemid 44216137)
47. Tomita S., Ozaki T., Taru H., Oguchi S., Takeda S., Yagi Y., Sakiyama S., Kirino Y., and, Suzuki T., (1999) Interaction of a neuron-specific protein containing PDZ domains with Alzheimer's amyloid precursor protein. J. Biol. Chem. 274, 2243-2254.
48. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., Hammer R. E., Richardson J. A., and, Herz J., (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689-701. (Pubitemid 29278044)
49. Umemori H., Wanaka A., Kato H., Takeuchi M., Tohyama M., and, Yamamoto T., (1992) Specific expressions of Fyn and Lyn, lymphocyte antigen receptor-associated tyrosine kinases, in the central nervous system. Brain Res. Mol. Brain Res. 16, 303-310. (Pubitemid 23035974)
50. Vetrivel K. S., Cheng H., Lin W., Sakurai T., Li T., Nukina N., Wong P. C., Xu H., and, Thinakaran G., (2004) Association of gamma-secretase with lipid rafts in post-Golgi and endosome membranes. J. Biol. Chem. 279, 44945-44954. (Pubitemid 39430908)
51. Vetrivel K. S., Cheng H., Kim S. H., Chen Y., Barnes N. Y., Parent A. T., Sisodia S. S., and, Thinakaran G., (2005) Spatial segregation of gamma-secretase and substrates in distinct membrane domains. J. Biol. Chem. 280, 25892-25900. (Pubitemid 40962301)
52. Wang Z., Wang B., Yang L., Guo Q., Aithmitti N., Songyang Z., and, Zheng H., (2009) Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis. J. Neurosci. 29, 10788-10801.
53. Wellington C. L., (2004) Cholesterol at the crossroads: Alzheimer's disease and lipid metabolism. Clin. Genet. 66, 1-16. (Pubitemid 38960816)
54. Young-Pearse T. L., Bai J., Chang R., Zheng J. B., LoTurco J. J., and, Selkoe D. J., (2007) A critical function for beta-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. J. Neurosci. 27, 14459-14469.