Tyrosine kinase inhibition increases functional parkin-Beclin-1 interaction and enhances amyloid clearance and cognitive performance

EMBO Molecular Medicine

Volumn 5, Issue 8, 2013, Pages 1247-1262

  Lonskaya, Irina ^a   Hebron, Michaeline L ^a   Desforges, Nicole M ^a   Franjie, Alexander ^a   Moussa, Charbel E H ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

amyloid; Autophagy; Parkin; Tau phosphorylation; Tyrosine kinase

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; BECLIN 1; BOSUTINIB; NILOTINIB; PARKIN; PROTEIN TYROSINE KINASE; SHORT HAIRPIN RNA;

ANIMAL EXPERIMENT; ARTICLE; CELL VACUOLE; COGNITION; ENZYME INHIBITION; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

Β-AMYLOID; AUTOPHAGY; PARKIN; TAU PHOSPHORYLATION; TYROSINE KINASE;

AMYLOID BETA-PEPTIDES; ANILINE COMPOUNDS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; BRAIN; COGNITION; COGNITION DISORDERS; HUMANS; MEMBRANE PROTEINS; MICE; NEURODEGENERATIVE DISEASES; NITRILES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PYRIMIDINES; QUINOLINES; RNA, SMALL INTERFERING; TAU PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84881490638     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201302771     Document Type: Article

References (62)

1. Alvarez AR, Sandoval PC, Leal NR, Castro PU, Kosik KS (2004) Activation of the neuronal c-Abl tyrosine kinase by amyloid-beta-peptide and reactive oxygen species. Neurobiol Dis 17: 326-336.
2. Burns MP, Zhang L, Rebeck GW, Querfurth HW, Moussa CE (2009) Parkin promotes intracellular Abeta1-42 clearance. Hum Mol Genet 18: 3206-3216.
3. Cancino GI, Perez de Arce K, Castro PU, Toledo EM, von Bernhardi R, Alvarez AR (2011) c-Abl tyrosine kinase modulates tau pathology and Cdk5 phosphorylation in AD transgenic mice. Neurobiol Aging 32: 1249-1261.
4. Cancino GI, Toledo EM, Leal NR, Hernandez DE, Yevenes LF, Inestrosa NC, Alvarez AR (2008) STI571 prevents apoptosis, tau phosphorylation and behavioural impairments induced by Alzheimer's beta-amyloid deposits. Brain 131: 2425-2442.
5. Chen D, Gao F, Li B, Wang H, Xu Y, Zhu C, Wang G (2010) Parkin mono-ubiquitinates Bcl-2 and regulates autophagy. J Biol Chem 285: 38214-38223.
6. Cook DG, Forman MS, Sung JC, Leight S, Kolson DL, Iwatsubo T, Lee VM, Doms RW (1997) Alzheimer's A beta(1-42) is generated in the endoplasmic reticulum/intermediate compartment of NT2N cells. Nat Med 3: 1021-1023.
7. Cortes JE, Kantarjian HM, Brummendorf TH, Kim DW, Turkina AG, Shen ZX, Pasquini R, Khoury HJ, Arkin S, Volkert A, et al (2011) Safety and efficacy of bosutinib (SKI-606) in chronic phase Philadelphia chromosome-positive chronic myeloid leukemia patients with resistance or intolerance to imatinib. Blood 118: 4567-4576.
8. D'Andrea MR, Nagele RG, Wang HY, Peterson PA, Lee DH (2001) Evidence that neurones accumulating amyloid can undergo lysis to form amyloid plaques in Alzheimer's disease. Histopathology 38: 120-134.
9. D'Hooge R, De Deyn PP (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36: 60-90.
10. Davis J, Xu F, Deane R, Romanov G, Previti ML, Zeigler K, Zlokovic BV, Van Nostrand WE (2004) Early-onset and robust cerebral microvascular accumulation of amyloid beta-protein in transgenic mice expressing low levels of a vasculotropic Dutch/Iowa mutant form of amyloid beta-protein precursor. J Biol Chem 279: 20296-20306.
11. de Lavallade H, Apperley JF, Khorashad JS, Milojkovic D, Reid AG, Bua M, Szydlo R, Olavarria E, Kaeda J, Goldman JM, et al (2008) Imatinib for newly diagnosed patients with chronic myeloid leukemia: Incidence of sustained responses in an intention-to-treat analysis. J Clin Oncol 26: 3358-3363.
12. Deremer DL, Ustun C, Natarajan K (2008) Nilotinib: A second-generation tyrosine kinase inhibitor for the treatment of chronic myelogenous leukemia. Clin Ther 30: 1956-1975.
13. Derkinderen P, Scales TM, Hanger DP, Leung KY, Byers HL, Ward MA, Lenz C, Price C, Bird IN, Perera T, et al (2005) Tyrosine 394 is phosphorylated in Alzheimer's paired helical filament tau and in fetal tau with c-Abl as the candidate tyrosine kinase. J Neurosci 25: 6584-6593.
14. Dhawan G, Combs CK (2012) Inhibition of Src kinase activity attenuates amyloid associated microgliosis in a murine model of Alzheimer's disease. J Neuroinflammation 9: 117.
15. Geisler S, Holmstrom KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, Springer W (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 12: 119-131.
16. Gonzalez-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquere S, Eskelinen EL, Pierron G, Saftig P, Kroemer G (2005) The apoptosis/autophagy paradox: Autophagic vacuolization before apoptotic death. J Cell Sci 118: 3091-3102.
17. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, et al (2000) Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 156: 15-20.
18. Greenfield JP, Tsai J, Gouras GK, Hai B, Thinakaran G, Checler F, Sisodia SS, Greengard P, Xu H (1999) Endoplasmic reticulum and trans-Golgi network generate distinct populations of Alzheimer beta-amyloid peptides. Proc Natl Acad Sci U S A 96: 742-747.
19. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297: 353-356.
20. He C, Klionsky DJ (2009) Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43: 67-93.
21. Imam SZ, Zhou Q, Yamamoto A, Valente AJ, Ali SF, Bains M, Roberts JL, Kahle PJ, Clark RA, Li S (2011) Novel regulation of parkin function through c-Abl-mediated tyrosine phosphorylation: implications for Parkinson's disease. J Neurosci 31: 157-163.
22. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wolfing H, Chieng BC, Christie MJ, Napier IA, et al (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 142: 387-397.
23. Iwata A, Riley BE, Johnston JA, Kopito RR (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280: 40282-40292.
24. Jing Z, Caltagarone J, Bowser R (2009) Altered subcellular distribution of c-Abl in Alzheimer's disease. J Alzheimers Dis 17: 409-422.
25. Kantarjian HM, Giles F, Gattermann N, Bhalla K, Alimena G, Palandri F, Ossenkoppele GJ, Nicolini FE, O'Brien SG, Litzow M et al (2007) Nilotinib (formerly AMN107), a highly selective BCR-ABL tyrosine kinase inhibitor, is effective in patients with Philadelphia chromosome-positive chronic myelogenous leukemia in chronic phase following imatinib resistance and intolerance. Blood 110: 3540-3546.
26. Kawahara K, Hashimoto M, Bar-On P, Ho GJ, Crews L, Mizuno H, Rockenstein E, Imam SZ, Masliah E (2008) Alpha-Synuclein aggregates interfere with Parkin solubility and distribution: Role in the pathogenesis of Parkinson disease. J Biol Chem 283: 6979-6987.
27. Keller VAG, Brummendorf TH (2012) Novel aspects of therapy with the dual Src and Abl kinase inhibitor bosutinib in chronic myeloid leukemia. Expert Rev Anticancer Ther 12: 1121-1127.
28. Khandelwal PJ, Herman AM, Hoe HS, Rebeck GW, Moussa CE (2011) Parkin mediates beclin-dependent autophagic clearance of defective mitochondria and ubiquitinated Abeta in AD models. Hum Mol Genet 20: 2091-2102.
29. Khoury HJ, Cortes JE, Kantarjian HM, Gambacorti-Passerini C, Baccarani M, Kim DW, Zaritskey A, Countouriotis A, Besson N, Leip E et al (2012) Bosutinib is active in chronic phase chronic myeloid leukemia after imatinib and dasatinib and/or nilotinib therapy failure. Blood 119: 3403-3412.
30. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605-608.
31. Ko HS, Lee Y, Shin JH, Karuppagounder SS, Gadad BS, Koleske AJ, Pletnikova O, Troncoso JC, Dawson VL, Dawson TM (2010) Phosphorylation by the c-Abl protein tyrosine kinase inhibits parkin's ubiquitination and protective function. Proc Natl Acad Sci U S A 107: 16691-16696.
32. Kovács AL, Reith A, Seglen PO (1982) Accumulation of autophagosomes after inhibition of hepatocytic protein degradation by vinblastine, leupeptin or a lysosomotropic amine. Exp Cell Res 137: 191-201.
33. Lee G (2005) Tau and src family tyrosine kinases. Biochim Biophys Acta 1739: 323-330.
34. Li M, Chen L, Lee DH, Yu LC, Zhang Y (2007) The role of intracellular amyloid beta in Alzheimer's disease. Prog Neurobiol 83: 131-139.
35. Lonskaya I, Hebron ML, Algarzae NK, Desforges N, Moussa CE (2012a) Decreased parkin solubility is associated with impairment of autophagy in the nigrostriatum of sporadic Parkinson's disease. Neuroscience 232C: 90.
36. Lonskaya I, Hebron ML, Algarzae NK, Desforges N, Moussa CE (2012b) Decreased parkin solubility is associated with impairment of autophagy in the nigrostriatum of sporadic Parkinson's disease. Neuroscience 232C: 90.
37. Lonskaya I, Shekoyan AR, Hebron ML, Desforges N, Algarzae NK, Moussa CE (2012c) Diminished parkin solubility and co-localization with intraneuronal amyloid-beta are associated with autophagic defects in alzheimer's disease. J Alzheimers Dis.
38. Lonskaya I, Shekoyan AR, Hebron ML, Desforges N, Algarzae NK, Moussa CE (2013) Diminished parkin solubility and co-localization with intraneuronal amyloid-beta are associated with autophagic defects in Alzheimer's disease. J Alzheimers Dis 33: 231-247.
39. Mahon FX, Hayette S, Lagarde V, Belloc F, Turcq B, Nicolini F, Belanger C, Manley PW, Leroy C, Etienne G et al (2008) Evidence that resistance to nilotinib may be due to BCR-ABL, Pgp, or Src kinase overexpression. Cancer Res 68: 9809-9816.
40. Marzella L, Ahlberg J, Glaumann H (1982) Isolation of autophagic vacuoles from rat liver: Morphological and biochemical characterization. J Cell Biol 93: 144-154.
41. Musumeci F, Schenone S, Brullo C, Botta M (2012) An update on dual Src/Abl inhibitors. Future Med Chem 4: 799-822.
42. Narendra D, Tanaka A, Suen DF, Youle RJ (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183: 795-803.
43. Nixon RA, Yang DS (2011) Autophagy failure in Alzheimer's disease-locating the primary defect. Neurobiol Dis 43: 38-45.
44. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24: 1063-1070.
45. Park J, Kim Y, Chung J, (2009) Mitochondrial dysfunction and Parkinson's disease genes: Insights from Drosophila. Dis Model Mech 2: 336-340.
46. Perucho J, Casarejos MJ, Rubio I, Rodriguez-Navarro JA, Gomez A, Ampuero I, Rodal I, Solano RM, Carro E, Garcia de Yebenes J et al (2010) The effects of parkin suppression on the behaviour, amyloid processing, and cell survival in APP mutant transgenic mice. Exp Neurol 221: 54-67.
47. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B et al (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 118: 2190-2199.
48. Puttini M, Coluccia AM, Boschelli F, Cleris L, Marchesi E, Donella-Deana A, Ahmed S, Redaelli S, Piazza R, Magistroni V et al (2006) In vitro and in vivo activity of SKI-606, a novel Src-Abl inhibitor, against imatinib-resistant Bcr-Abl+ neoplastic cells. Cancer Res 66: 11314-11322.
49. Rebeck GW, Hoe HS, Moussa CE (2010) Beta-amyloid 1-42 gene transfer model exhibits intraneuronal amyloid, gliosis, tau phosphorylation, and neuronal loss. J Biol Chem 285: 7440-7446.
50. Reynolds CH, Garwood CJ, Wray S, Price C, Kellie S, Perera T, Zvelebil M, Yang A, Sheppard PW, Varndell IM et al (2008) Phosphorylation regulates tau interactions with Src homology 3 domains of phosphatidylinositol 3-kinase, phospholipase Cgamma1, Grb2, and Src family kinases. J Biol Chem 283: 18177-18186.
51. Rodriguez-Navarro JA, Gomez A, Rodal I, Perucho J, Martinez A, Furio V, Ampuero I, Casarejos MJ, Solano RM, de Yebenes JG et al (2008) Parkin deletion causes cerebral and systemic amyloidosis in human mutated tau over-expressing mice. Hum Mol Genet 17: 3128-3143.
52. Salomoni P, Calabretta B (2009) Targeted therapies and autophagy: New insights from chronic myeloid leukemia. Autophagy 5: 1050-1051.
53. Schlatterer SD, Acker CM, Davies P (2011) c-Abl in neurodegenerative disease. J Mol Neurosci.
54. Skorski T (2011) BCR-ABL1 kinase: Hunting an elusive target with new weapons. Chem Biol 18: 1352-1353.
55. Skovronsky DM, Doms RW, Lee VM, (1998) Detection of a novel intraneuronal pool of insoluble amyloid beta protein that accumulates with time in culture. J Cell Biol 141: 1031-1039.
56. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG et al (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3: 995-1000.
57. Tremblay MA, Acker CM, Davies P (2010) Tau phosphorylated at tyrosine 394 is found in Alzheimer's disease tangles and can be a product of the Abl-related kinase, Arg. J Alzheimers Dis 19: 721-733.
58. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, May J, Tocilescu MA, Liu W, Ko HS et al (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 107: 378-383.
59. Wang C, Ko HS, Thomas B, Tsang F, Chew KC, Tay SP, Ho MW, Lim TM, Soong TW, Pletnikova O et al (2005) Stress-induced alterations in parkin solubility promote parkin aggregation and compromise parkin's protective function. Hum Mol Genet 14: 3885-3897.
60. Wang JY (2000) Regulation of cell death by the Abl tyrosine kinase. Oncogene 19: 5643-5650.
61. Weisberg E, Manley PW, Breitenstein W, Bruggen J, Cowan-Jacob SW, Ray A, Huntly B, Fabbro D, Fendrich G, Hall-Meyers E et al (2005) Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell 7: 129-141.
62. Xu H, Sweeney D, Wang R, Thinakaran G, Lo AC, Sisodia SS, Greengard P, Gandy S (1997) Generation of Alzheimer beta-amyloid protein in the trans-Golgi network in the apparent absence of vesicle formation. Proc Natl Acad Sci U S A 94: 3748-3752.