Aberrant activation of focal adhesion proteins mediates fibrillar amyloid β-induced neuronal dystrophy

Journal of Neuroscience

Volumn 23, Issue 2, 2003, Pages 493-502

  Grace, Elizabeth A ^a,b   Busciglio, Jorge ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Amyloid ; Focal adhesion; Neurodegeneration; Neuronal dystrophy; Senile plaques

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; FOCAL ADHESION KINASE; FOCAL ADHESION PROTEIN; INTEGRIN; INTEGRIN RECEPTOR; PAXILLIN; PROTEIN TYROSINE PHOSPHATASE; SYNAPTOPHYSIN; TAU PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ADAPTATION; ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; DEGENERATIVE DISEASE; EMBRYO; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RAT; SENILE PLAQUE; SIGNAL TRANSDUCTION; SYNAPSE;

EID: 0037439642     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-02-00493.2003     Document Type: Article

References (78)

1. Akiyama H, Kawamata T, Dedhar S, McGeer PL (1991) Immunohistochemical localization of vitronectin, its receptor and beta-3 integrin in Alzheimer brain tissue. J Neuroimmunol 32:19-28.
2. Angers-Loustau A, Cote JF, Charest A, Dowbenko D, Spencer S, Lasky LA, Tremblay ML (1999) Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J Cell Biol 144:1019-1031.
3. Aplin AE, Howe A, Alahari SK, Juliano RL (1998) Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol Rev 50:197-263.
4. Baumann K, Mandelkow EM, Biernat J, Piwnica-Worms H, Mandelkow E (1993) Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett 336:417-424.
5. Benzing WC, Mufson EJ, Armstrong DM (1993) Alzheimer's disease-like dystrophic neurites characteristically associated with senile plaques are not found within other neurodegenerative diseases unless amyloid beta-protein deposition is present. Brain Res 606:10-18.
6. Berg MM, Krafft GA, Klein WL (1997) Rapid impact of beta-amyloid on paxillin in a neural cell line. J Neurosci Res 50:979-989.
7. Bhat RV, Shanley J, Correll MP, Fieles WE, Keith RA, Scott CW, Lee CM (2000) Regulation and localization of tyrosine 216 phosphorylation of glycogen synthase kinase-3 beta in cellular and animal models of neuronal degeneration. Proc Natl Acad Sci USA 97:11074-11079.
8. Brown MC, Perrotta JA, Turner CE (1996) Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J Cell Biol 135:1109-1123.
9. Busciglio J, Yankner BA (1995) Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature 378:776-779.
10. Busciglio J, Lorenzo A, Yankner BA (1992) Methodological variables in the assessment of beta amyloid neurotoxicity. Neurobiol Aging 13:609-612.
11. Busciglio J, Gabuzda DH, Matsudaira P, Yankner BA (1993) Generation of beta-amyloid in the secretory pathway in neuronal and nonneuronal cells. Proc Natl Acad Sci USA 90:2092-2096.
12. Busciglio J, Lorenzo A, Yeh J, Yankner BA (1995) Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14:879-888.
13. Busciglio J, Hartmann H, Lorenzo A, Wong C, Baumann K, Sommer B, Staufenbiel M, Yankner BA (1997) Neuronal localization of presenilin-1 and association with amyloid plaques and neurofibrillary tangles in Alzheimer's disease. J Neurosci 17:5101-5107.
14. Carson F (1990) Histotechnology: a self-instructional text, pp 167-169. Chicago: American Society for Clinical Pathology.
15. Chen LM, Bailey D, Fernandez-Valle C (2000) Association of beta 1 integrin with focal adhesion kinase and paxillin in differentiating Schwann cells. J Neurosci 20:3776-3784.
16. Cote JF, Turner CE, Tremblay ML (1999) Intact LIM 3 and LIM 4 domains of paxillin are required for the association to a novel polyproline region (Pro 2) of protein-tyrosine phosphatase-PEST. J Biol Chem 274:20550-20560.
17. Cotman CW, Hailer NP, Pfister KK, Soltesz I, Schachner M (1998) Cell adhesion molecules in neural plasticity and pathology: similar mechanisms, distinct organizations? Prog Neurobiol 55:659-669.
18. Cukierman E, Pankov R, Stevens DR, Yamada KM (2001) Taking cell-matrix adhesions to the third dimension. Science 294:1708-1712.
19. Dawid IB, Breen JJ, Toyama R (1998) LIM domains: multiple roles as adapters and functional modifiers in protein interactions. Trends Genet 14:156-162.
20. Delatour B, Mercken L, El Hachimi KH, Colle MA, Pradier L, Duyckaerts C (2001) FE65 in Alzheimer's disease: neuronal distribution and association with neurofibrillary tangles. Am J Pathol 158:1585-1591.
21. Dogic D, Rousselle P, Aumailley M (1998) Cell adhesion to laminin 1 or 5 induces isoform-specific clustering of integrins and other focal adhesion components. J Cell Sci 111:793-802.
22. Eikelenboom P, Zhan SS, Kamphorst W, van der Valk P, Rozemuller JM (1994) Cellular and substrate adhesion molecules (integrins) and their ligands in cerebral amyloid plaques in Alzheimer's disease. Virchows Arch 424:421-427.
23. Flaherty DB, Soria JP, Tomasiewicz HG, Wood JG (2000) Phosphorylation of human tau protein by microtubule-associated kinases: GSK3 beta and cdk5 are key participants. J Neurosci Res 62:463-472.
24. Frohman EM, Frohman TC, Gupta S, de Fougerolles A, van den Noort S (1991) Expression of intercellular adhesion molecule 1 (ICAM-1) in Alzheimer's disease. J Neurol Sci 106:105-111.
25. Geddes JW, Anderson KJ, Cotman CW (1986) Senile plaques as aberrant sprout-stimulating structures. Exp Neurol 94:767-776.
26. Geula C, Wu CK, Saroff D, Lorenzo A, Yuan M, Yankner BA (1998) Aging renders the brain vulnerable to amyloid beta-protein neurotoxicity. Nat Med 4:827-831.
27. Goodwin JL, Kehrli Jr ME, Uemura E (1997) Integrin Mac-1 and beta-amyloid in microglial release of nitric oxide. Brain Res 768:279-286.
28. Grace E, Rabiner AC, Busciglio J (2002) Characterization of neuronal dystrophy induced by fibrillar amyloid β: implications for Alzheimer's disease. Neuroscience 11:265-273.
29. Greenberg SG, Davies P, Schein JD, Binder LI (1992) Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. J Biol Chem 267:564-569.
30. Hildebrand JD, Schaller MD, Parsons JT (1995) Paxillin, a tyrosine phosphorylated focal adhesion-associated protein binds to the carboxyl terminal domain of focal adhesion kinase. Mol Biol Cell 6:637-647.
31. Hu Q, Kukull WA, Bressler SL, Gray MD, Cam JA, Larson EB, Martin GM, Deeb SS (1998) The human FE65 gene: genomic structure and an intronic biallelic polymorphism associated with sporadic dementia of the Alzheimer type. Hum Genet 103:295-303.
32. Hu Q, Cool BH, Wang B, Hearn MG, Martin GM (2002) A candidate molecular mechanism for the association of an intronic polymorphism of FE65 with resistance to very late onset dementia of the Alzheimer type. Hum Mol Genet 11:465-475.
33. Irizarry MC, McNamara M, Fedorchak K, Hsiao K, Hyman BT (1997) APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CA1. J Neuropathol Exp Neurol 56:965-973.
34. Jurata LW, Gill GN (1998) Structure and function of LIM domains. Curr Top Microbiol Immunol 228:75-113.
35. Katoh K, Masuda M, Kano Y, Jinguji Y, Fujiwara K (1995) Focal adhesion proteins associated with apical stress fibers of human fibroblasts. Cell Motil Cytoskeleton 31:177-195.
36. Kowalska MA, Badellino K (1994) Beta-amyloid protein induces platelet aggregation and supports platelet adhesion. Biochem Biophys Res Commun 205:1829-1835.
37. Lambert JC, Mann D, Goumidi L, Harris J, Pasquier F, Frigard B, Cottel D, Lendon C, Iwatsubo T, Amouyel P, Chartier-Harlin MC (2000) A FE65 polymorphism associated with risk of developing sporadic late-onset Alzheimer's disease but not with Abeta loading in brains. Neurosci Lett 293:29-32.
38. Lashuel HA, Hartley D, Petre BM, Walz T, Lansbury PT (2002) Amyloid pores from pathogenic mutations. Nature 418:291.
39. Li BS, Zhang L, Gu J, Amin ND, Pant HC (2000) Integrin α(1)β(1)-mediated activation of cyclin-dependent kinase 5 activity is involved in neurite outgrowth and human neurofilament protein H Lys-Ser-Pro tail domain phosphorylation. J Neurosci 20:6055-6062.
40. Lorenzo A, Yankner BA (1994) Beta-amyloid neurotoxicity requires fibril formation and is inhibited by congo red. Proc Natl Acad Sci USA 91:12243-12247.
41. Lorenzo A, Yuan M, Zhang Z, Paganetti PA, Sturchler-Pierrat C, Staufenbiel M, Mautino J, Vigo FS, Sommer B, Yankner BA (2000) Amyloid beta interacts with the amyloid precursor protein: a potential toxic mechanism in Alzheimer's disease. Nat Neurosci 3:460-464.
42. Mandelkow EM, Drewes G, Biernat J, Gustke N, Van Lint J, Vandenheede JR, Mandelkow E (1992) Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett 314:315-321.
43. Masliah E, Mallory M, Hansen L, Alford M, Albright T, DeTeresa R, Terry R, Baudier J, Saitoh T (1991) Patterns of aberrant sprouting in Alzheimer's disease. Neuron 6:729-739.
44. Mattson MP, DuanW (1999) "Apoptotic" biochemical cascades in synaptic compartments: roles in adaptive plasticity and neurodegenerative disorders. J Neurosci Res 58:152-166.
45. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE (1992) β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:376-389.
46. McKee AC, Kosik KS, Kowall NW (1991) Neuritic pathology and dementia in Alzheimer's disease. Ann Neurol 30:156-165.
47. Mesulam MM (1999) Neuroplasticity failure in Alzheimer's disease: bridging the gap between plaques and tangles. Neuron 24:521-529.
48. Mueller SC, Kelly T, Dai MZ, Dai HN, Chen WT (1989) Dynamic cytoskeleton-integrin associations induced by cell binding to immobilized fibronectin. J Cell Biol 109:3455-3464.
49. Nakamura K, Yano H, Uchida H, Hashimoto S, Schaefer E, Sabe H (2000) Tyrosine phosphorylation of paxillin a is involved in temporospatial regulation of paxillin-containing focal adhesion formation and F-actin organization in motile cells. J Biol Chem 275:27155-27164.
50. Pei JJ, Grundke-Iqbal I, Iqbal K, Bogdanovic N, Winblad B, Cowburn RF (1998) Accumulation of cyclin-dependent kinase 5 (cdk5) in neurons with early stages of Alzheimer's disease neurofibrillary degeneration. Brain Res 797:267-277.
51. Pigino G, Pelsman A, Mori H, Busciglio J (2001) Presenilin-1 mutations reduce cytoskeletal association, deregulate neurite growth, and potentiate neuronal dystrophy and tau phosphorylation. J Neurosci 21:834-842.
52. Pike CJ, Walencewicz AJ, Glabe CG, Cotman CW (1991) Aggregation-related toxicity of synthetic beta-amyloid protein in hippocampal cultures. Eur J Pharmacol 207:367-368.
53. Pike CJ, Cummings BJ, Cotman CW (1992) Beta-amyloid induces neuritic dystrophy in vitro: similarities with Alzheimer pathology. Neuro Report 3:769-772.
54. Sabo S, Lambert MP, Kessey K, Wade W, Krafft G, Klein WL (1995) Interaction of beta-amyloid peptides with integrins in a human nerve cell line. Neurosci Lett 184:25-28.
55. Sabo SL, Ikin AF, Buxbaum JD, Greengard P (2001) The Alzheimer amyloid precursor protein (APP) and FE65, an APP-binding protein, regulate cell movement. J Cell Biol 153:1403-1414.
56. Saitoh T, Horsburgh K, Masliah E (1993) Hyperactivation of signal transduction systems in Alzheimer's disease. Ann NY Acad Sci 695:34-41.
57. Salgia R, Li JL, Lo SH, Brunkhorst B, Kansas GS, Sobhany ES, Sun Y, Pisick E, Hallek M, Ernst T, Tantravahi R, Chen LB, Griffin JD (1995) Molecular cloning of human paxillin, a focal adhesion protein phosphorylated by P210BCR/ABL. J Biol Chem 270:5039-5047.
58. Schaller MD, Parsons JT (1994) Focal adhesion kinase and associated proteins. Curr Opin Cell Biol 6:705-710.
59. Schaller MD, Borgman CA, Parsons JT (1993) Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK. Mol Cell Biol 13:785-791.
60. Schaller MD, Otey CA, Hildebrand JD, Parsons JT (1995) Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J Cell Biol 130:1181-1187.
61. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81:741-766.
62. Sengupta A, Wu Q, Grundke-Iqbal I, Iqbal K, Singh TJ (1997) Potentiation of GSK-3-catalyzed Alzheimer-like phosphorylation of human tau by cdk5. Mol Cell Biochem 167:99-105.
63. Shen Y, Lyons P, Cooley M, Davidson D, Veillette A, Salgia R, Griffin JD, Schaller MD (2000) The noncatalytic domain of protein-tyrosine phosphatase-PEST targets paxillin for dephosphorylation in vivo. J Biol Chem 275:1405-1413.
64. Small DH (1998) The role of the amyloid protein precursor (APP) in Alzheimer's disease: does the normal function of APP explain the topography of neurodegeneration? Neurochem Res 23:795-806.
65. Storey E, Beyreuther K, Masters CL (1996) Alzheimer's disease amyloid precursor protein on the surface of cortical neurons in primary culture colocalizes with adhesion patch components. Brain Res 735:217-231.
66. Thomas JW, Cooley MA, Broome JM, Salgia R, Griffin JD, Lombardo CR, Schaller MD (1999) The role of focal adhesion kinase binding in the regulation of tyrosine phosphorylation of paxillin. J Biol Chem 274:36684-36692.
67. Turner CE (2000) Paxillin interactions. J Cell Sci 113:4139-4140.
68. Turner CE, Miller JT (1994) Primary sequence of paxillin contains putative SH2 and SH3 domain binding motifs and multiple LIM domains: identification of a vinculin and pp125Fak-binding region. J Cell Sci 107:1583-1591.
69. Van Gool D, Carmeliet G, Triau E, Cassiman JJ, Dom R (1994) Appearance of localized immunoreactivity for the alpha 4 integrin subunit and for fibronectin in brains from Alzheimer's, Lewy body dementia patients and aged controls. Neurosci Lett 170:71-73.
70. Williamson R, Scales T, Clark BR, Gibb G, Reynolds CH, Kellie S, Bird IN, Varndell IM, Sheppard PW, Everall I, Anderton BH (2002) 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 22:10-20.
71. Yamaguchi H, Ishiguro K, Uchida T, Takashima A, Lemere CA, Imahori K (1996) Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3 beta and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol (Berl) 92:232-241.
72. Yamazaki T, Koo EH, Selkoe DJ (1997) Cell surface amyloid beta-protein precursor colocalizes with beta 1 integrins at substrate contact sites in neural cells. J Neurosci 17:1004-1010.
73. Yankner BA (1996) Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16:921-932.
74. Yankner BA, Duffy LK, Kirschner DA (1990) Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science 250:279-282.
75. Zhang C, Lambert MP, Bunch C, Barber K, Wade WS, Krafft GA, Klein WL (1994) Focal adhesion kinase expressed by nerve cell lines shows increased tyrosine phosphorylation in response to Alzheimer's Aβ peptide. J Biol Chem 269:25247-25250.
76. Zhang C, Qiu HE, Krafft GA, Klein WL (1996) A beta peptide enhances focal adhesion kinase/Fyn association in a rat CNS nerve cell line. Neurosci Lett 211:187-190.
77. Zheng DQ, Woodard AS, Fornaro M, Tallini G, Languino LR (1999) Prostatic carcinoma cell migration via α(v)β3 integrin is modulated by a focal adhesion kinase pathway. Cancer Res 59:1655-1664.
78. Zukerberg LR, Patrick GN, Nikolic M, Humbert S, Wu CL, Lanier LM, Gertler FB, Vidal M, Van Etten RA, Tsai LH (2000) Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 26:633-646.