Focal adhesions regulate Aβ signaling and cell death in Alzheimer's disease

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1772, Issue 4, 2007, Pages 438-445

  Caltagarone, John ^a   Jing, Zheng ^b   Bowser, Robert ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Alzheimer's disease; Cell cycle; Cyclin D1; FAK; Integrin; Paxillin

Indexed keywords

AMYLOID BETA PROTEIN; FOCAL ADHESION KINASE 1; INTEGRIN;

ALZHEIMER DISEASE; CELL ACTIVATION; CELL COMMUNICATION; CELL CYCLE; CELL DEATH; CELL FUNCTION; CYTOSKELETON; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; NERVE CELL MEMBRANE; NONHUMAN; PATHOGENESIS; PHOSPHORYLATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; CELL ADHESION; CELL CYCLE; CELL DEATH; CELL SURVIVAL; HUMANS; INTEGRINS; NEURONS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 33947164895     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2006.11.007     Document Type: Review

References (73)

1. Gilmore A.P. Anoikis. Cell Death Differ. 12 Suppl. 2 (2005) 1473-1477
2. Howe A., Aplin A.E., Alahari S.K., and Juliano R.L. Integrin signaling and cell growth control. Curr. Opin. Cell Biol. 10 (1998) 220-231
3. Reddig P.J., and Juliano R.L. Clinging to life: cell to matrix adhesion and cell survival. Cancer Metastasis Rev. 24 (2005) 425-439
4. Cordes N., and Meineke V. Integrin signalling and the cellular response to ionizing radiation. J. Mol. Histol. 35 (2004) 327-337
5. Giancotti F.G., and Ruoslahti E. Integrin signaling. Science 285 (1999) 1028-1032
6. Verdier Y., and Penke B. Binding sites of amyloid beta-peptide in cell plasma membrane and implications for Alzheimer's disease. Curr. Protein Pept. Sci. 5 (2004) 19-31
7. Cary L.A., and Guan J.L. Focal adhesion kinase in integrin-mediated signaling. Front. Biosci. 4 (1999) D102-D113
8. Sonoda Y., Watanabe S., Matsumoto Y., Aizu-Yokota E., and Kasahara T. FAK is the upstream signal protein of the phosphatidylinositol 3-kinase-Akt survival pathway in hydrogen peroxide-induced apoptosis of a human glioblastoma cell line. J. Biol. Chem. 274 (1999) 10566-10570
9. Williamson R., Scales T., Clark B.R., Gibb G., Reynolds C.H., Kellie S., Bird I.N., Varndell I.M., Sheppard P.W., Everall I., and Anderton B.H. Rapid tyrosine phosphorylation of neuronal proteins including tau and focal adhesion kinase in response to amyloid-beta peptide exposure: involvement of Src family protein kinases. J. Neurosci. 22 (2002) 10-20
10. Leventhal P.S., and Feldman E.L. Tyrosine phosphorylation and enhanced expression of paxillin during neuronal differentiation in vitro. J. Biol. Chem. 271 (1996) 5957-5960
11. de Curtis I., and Malanchini B. Integrin-mediated tyrosine phosphorylation and redistribution of paxillin during neuronal adhesion. Exp. Cell Res. 230 (1997) 233-243
12. Huang C., Borchers C.H., Schaller M.D., and Jacobson K. Phosphorylation of paxillin by p38MAPK is involved in the neurite extension of PC-12 cells. J. Cell Biol. 164 (2004) 593-602
13. Zhang C., Lambert M.P., Bunch C., Barber K., Wade W.S., Krafft G.A., and Klein W.L. Focal adhesion kinase expressed by nerve cell lines shows increased tyrosine phosphorylation in response to Alzheimer's A beta peptide. J. Biol. Chem. 269 (1994) 25247-25250
14. Berg M.M., Krafft G.A., and Klein W.L. Rapid impact of beta-amyloid on paxillin in a neural cell line. J. Neurosci. Res. 50 (1997) 979-989
15. Grace E.A., and Busciglio J. Aberrant activation of focal adhesion proteins mediates fibrillar amyloid beta-induced neuronal dystrophy. J. Neurosci. 23 (2003) 493-502
16. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., and Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 343-347
17. 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., and Rakic P. Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J. Neurosci. 24 (2004) 10763-10772
18. Jordan-Sciutto K., Rhodes J., and Bowser R. Altered subcellular distribution of transcriptional regulators in response to Abeta peptide and during Alzheimer's disease. Mech. Ageing Dev. 123 (2001) 11-20
19. Herrup K., Neve R., Ackerman S.L., and Copani A. Divide and die: cell cycle events as triggers of nerve cell death. J. Neurosci. 24 (2004) 9232-9239
20. Smith D.S., Leone G., DeGregori J., Ahmed M.N., Qumsiyeh M.B., and Nevins J.R. Induction of DNA replication in adult rat neurons by deregulation of the retinoblastoma/E2F G1 cell cycle pathway. Cell Growth Differ. 11 (2000) 625-633
21. Yang Y., Geldmacher D.S., and Herrup K. DNA replication precedes neuronal cell death in Alzheimer's disease. J. Neurosci. 21 (2001) 2661-2668
22. Aplin A.E. Cell adhesion molecule regulation of nucleocytoplasmic trafficking. FEBS Lett. 534 (2003) 11-14
23. Schwartz M.A., and Assoian R.K. Integrins and cell proliferation: regulation of cyclin-dependent kinases via cytoplasmic signaling pathways. J. Cell Sci. 114 (2001) 2553-2560
24. Nishiya N., Tachibana K., Shibanuma M., Mashimo J.I., and Nose K. Hic-5-reduced cell spreading on fibronectin: competitive effects between paxillin and Hic-5 through interaction with focal adhesion kinase. Mol. Cell. Biol. 21 (2001) 5332-5345
25. Brown M.C., and Turner C.E. Paxillin: adapting to change. Physiol. Rev. 84 (2004) 1315-1339
26. Wehrle-Haller B., and Imhof B. The inner lives of focal adhesions. Trends Cell Biol. 12 (2002) 382-389
27. Lambert M.P., Stevens G., Sabo S., Barber K., Wang G., Wade W., Krafft G., Snyder S., Holzman T.F., and Klein W.L. Beta/A4-evoked degeneration of differentiated SH-SY5Y human neuroblastoma cells. J. Neurosci. Res. 39 (1994) 377-385
28. Zhao J.H., Reiske H., and Guan J.L. Regulation of the cell cycle by focal adhesion kinase. J. Cell Biol. 143 (1998) 1997-2008
29. Zhao J., Pestell R., and Guan J.L. Transcriptional activation of cyclin D1 promoter by FAK contributes to cell cycle progression. Mol. Biol. Cell 12 (2001) 4066-4077
30. Kasahara T., Koguchi E., Funakoshi M., Aizu-Yokota E., and Sonoda Y. Antiapoptotic action of focal adhesion kinase (FAK) against ionizing radiation. Antioxid. Redox Signal. 4 (2002) 491-499
31. Calalb M.B., Polte T.R., and Hanks S.K. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol. Cell. Biol. 15 (1995) 954-963
32. Golubovskaya V., Kaur A., and Cance W. Cloning and characterization of the promoter region of human focal adhesion kinase gene: nuclear factor kappa B and p53 binding sites. Biochim. Biophys. Acta 1678 (2004) 111-125
33. Golubovskaya V.M., Finch R., and Cance W.G. Direct interaction of the N-terminal domain of focal adhesion kinase with the N-terminal transactivation domain of p53. J. Biol. Chem. 280 (2005) 25008-25021
34. Ivankovic-Dikic I., Gronroos E., Blaukat A., Barth B.U., and Dikic I. Pyk2 and FAK regulate neurite outgrowth induced by growth factors and integrins. Nat. Cell Biol. 2 (2000) 574-581
35. Huang C., Rajfur Z., Borchers C., Schaller M.D., and Jacobson K. JNK phosphorylates paxillin and regulates cell migration. Nature 424 (2003) 219-223
36. Bowser R., and Smith M.A. Cell cycle proteins in Alzheimer's disease: plenty of wheels but no cycle. J. Alzheimer's Dis. 4 (2002) 249-254
37. Yu X., Caltagarone J., Smith M.A., and Bowser R. DNA damage induces cdk2 protein levels and histone H2B phosphorylation in SH-SY5Y neuroblastoma cells. J. Alzheimer's Dis. 8 (2005) 7-21
38. Ogawa O., Lee H.G., Zhu X., Raina A., Harris P.L., Castellani R.J., Perry G., and Smith M.A. Increased p27, an essential component of cell cycle control, in Alzheimer's disease. Aging Cell 2 (2003) 105-110
39. Busser J., Geldmacher D.S., and Herrup K. Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J. Neurosci. 18 (1998) 2801-2807
40. Jordan-Sciutto K.L., Malaiyandi L.M., and Bowser R. Altered distribution of cell cycle transcriptional regulators during Alzheimer disease. J. Neuropathol. Exp. Neurol. 61 (2002) 358-367
41. Hoozemans J.J., Stieler J., van Haastert E.S., Veerhuis R., Rozemuller A.J., Baas F., Eikelenboom P., Arendt T., and Scheper W. The unfolded protein response affects neuronal cell cycle protein expression: implications for Alzheimer's disease pathogenesis. Exp. Gerontol. 41 (2006) 380-386
42. Arendt T., Holzer M., Grossmann A., Zedlick D., and Bruckner M.K. Increased expression and subcellular translocation of the mitogen activated protein kinase kinase and mitogen-activated protein kinase in Alzheimer's disease. Neuroscience 68 (1995) 5-18
43. Haddad J.J. Mitogen-activated protein kinases and the evolution of Alzheimer's: a revolutionary neurogenetic axis for therapeutic intervention?. Prog. Neurobiol. 73 (2004) 359-377
44. Webster B., Hansen L., Adame A., Crews L., Torrance M., Thal L., and Masliah E. Astroglial activation of extracellular-regulated kinase in early stages of Alzheimer disease. J. Neuropathol. Exp. Neurol. 65 (2006) 142-151
45. Guan J.L. Focal adhesion kinase in integrin signaling. Matrix Biol. 16 (1997) 195-200
46. Zalewska T., Makarewicz D., Janik B., and Ziemka-Nalecz M. Neonatal cerebral hypoxia-ischemia: involvement of FAK-dependent pathway. Int. J. Dev. Neurosci. 23 (2005) 657-662
47. Schlaepfer D.D., and Hunter T. Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src. J. Biol. Chem. 272 (1997) 13189-13195
48. Kacimi R., and Gerdes A.M. Alterations in G protein and MAP kinase signaling pathways during cardiac remodeling in hypertension and heart failure. Hypertension 41 (2003) 968-977
49. Yamamoto D., Sonoda Y., Hasegawa M., Funakoshi-Tago M., Aizu-Yokota E., and Kasahara T. FAK overexpression upregulates cyclin D3 and enhances cell proliferation via the PKC and PI3-kinase-Akt pathways. Cell Signal. 15 (2003) 575-583
50. Koyama Y., Yoshioka Y., Shinde M., Matsuda T., and Baba A. Focal adhesion kinase mediates endothelin-induced cyclin D3 expression in rat cultured astrocytes. J. Neurochem. 90 (2004) 904-912
51. Reiske H.R., Zhao J., Han D.C., Cooper L.A., and Guan J.L. Analysis of FAK-associated signaling pathways in the regulation of cell cycle progression. FEBS Lett. 486 (2000) 275-280
52. Russo C., Dolcini V., Salis S., Venezia V., Violani E., Carlo P., Zambrano N., Russo T., and Schettini G. Signal transduction through tyrosine-phosphorylated carboxy-terminal fragments of APP via an enhanced interaction with Shc/Grb2 adaptor proteins in reactive astrocytes of Alzheimer's disease brain. Ann. N. Y. Acad. Sci. 973 (2002) 323-333
53. Russo C., Venezia V., Repetto E., Nizzari M., Violani E., Carlo P., and Schettini G. The amyloid precursor protein and its network of interacting proteins: physiological and pathological implications. Brain Res. Brain Res. Rev. 48 (2005) 257-264
54. Cheng M., Sexl V., Sherr C.J., and Roussel M.F. Assembly of cyclin D-dependent kinase and titration of p27Kip1 regulated by mitogen-activated protein kinase kinase (MEK1). Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 1091-1096
55. Walker J.L., and Assoian R.K. Integrin-dependent signal transduction regulating cyclin D1 expression and G1 phase cell cycle progression. Cancer Metastasis Rev. 24 (2005) 383-393
56. Zhao J., Bian Z.C., Yee K., Chen B.P., Chien S., and Guan J.L. Identification of transcription factor KLF8 as a downstream target of focal adhesion kinase in its regulation of cyclin D1 and cell cycle progression. Mol. Cell 11 (2003) 1503-1515
57. Suske G., Bruford E., and Philipsen S. Mammalian SP/KLF transcription factors: bring in the family. Genomics 85 (2005) 551-556
58. Wang X., and Zhao J. KLF8 transcription factor participates in oncogenic transformation. Oncogene (2006)
59. Chen Y., Wang S.M., Wu J.C., and Huang S.H. Effects of PPARgamma agonists on cell survival and focal adhesions in a Chinese thyroid carcinoma cell line. J. Cell. Biochem. 98 (2006) 1021-1035
60. Micsenyi A., Tan X., Sneddon T., Luo J.H., Michalopoulos G.K., and Monga S.P. Beta-catenin is temporally regulated during normal liver development. Gastroenterology 126 (2004) 1134-1146
61. Fuentealba R.A., Farias G., Scheu J., Bronfman M., Marzolo M.P., and Inestrosa N.C. Signal transduction during amyloid-beta-peptide neurotoxicity: role in Alzheimer disease. Brain Res. Brain Res. Rev. 47 (2004) 275-289
62. Essers M.A., de Vries-Smits L.M., Barker N., Polderman P.E., Burgering B.M., and Korswagen H.C. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308 (2005) 1181-1184
63. Alvarez A.R., Godoy J.A., Mullendorff K., Olivares G.H., Bronfman M., and Inestrosa N.C. Wnt-3a overcomes beta-amyloid toxicity in rat hippocampal neurons. Exp. Cell Res. 297 (2004) 186-196
64. Garrido J.L., Godoy J.A., Alvarez A., Bronfman M., and Inestrosa N.C. Protein kinase C inhibits amyloid beta peptide neurotoxicity by acting on members of the Wnt pathway. FASEB J. 16 (2002) 1982-1984
65. Greer E.L., and Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24 (2005) 7410-7425
66. Hosaka T., Biggs III W.H., Tieu D., Boyer A.D., Varki N.M., Cavenee W.K., and Arden K.C. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 2975-2980
67. Strachan G.D., Morgan K.L., Otis L.L., Caltagarone J., Gittis A., Bowser R., and Jordan-Sciutto K.L. Fetal Alz-50 clone 1 interacts with the human orthologue of the Kelch-like Ech-associated protein. Biochemistry 43 (2004) 12113-12122
68. Velichkova M., and Hasson T. Keap1 in adhesion complexes. Cell Motil. Cytoskeleton 56 (2003) 109-119
69. Velichkova M., and Hasson T. Keap1 regulates the oxidation-sensitive shuttling of Nrf2 into and out of the nucleus via a Crm1-dependent nuclear export mechanism. Mol. Cell. Biol. 25 (2005) 4501-4513
70. Lee J.M., Li J., Johnson D.A., Stein T.D., Kraft A.D., Calkins M.J., Jakel R.J., and Johnson J.A. Nrf2, a multi-organ protector?. FASEB J. 19 (2005) 1061-1066
71. Jordan-Sciutto K.L., Dragich J.M., Rhodes J.L., and Bowser R. Fetal Alz-50 clone 1, a novel zinc finger protein, binds a specific DNA sequence and acts as a transcriptional regulator. J. Biol. Chem. 274 (1999) 35262-35268
72. Barak O., Lazzaro M.A., Lane W.S., Speicher D.W., Picketts D.J., and Shiekhattar R. Isolation of human NURF: a regulator of Engrailed gene expression. EMBO J. 22 (2003) 6089-6100
73. Herrup K., and Busser J.C. The induction of multiple cell cycle events precedes target-related neuronal death. Development 121 (1995) 2385-2395