Highly pathogenic Alzheimer's disease presenilin 1 P117R mutation causes a specific increase in p53 and p21 protein levels and cell cycle dysregulation in human lymphocytes

Journal of Alzheimer's Disease

Volumn 32, Issue 2, 2012, Pages 397-415

  Bialopiotrowicz, Emilia ^a   Szybinska, Aleksandra ^a   Kuzniewska, Bozena ^a   Buizza, Laura ^b   Uberti, Daniela ^b   Kuznicki, Jacek ^a,c   Wojda, Urszula ^a  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^b UNIVERSITY OF BRESCIA   (Italy)

^c NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Amyloid ; cell cycle; familial Alzheimer's disease; human lymphocytes; p21; p53; presenilin 1

Indexed keywords

CYCLIN D1; GAMMA SECRETASE; PRESENILIN 1; PROTEIN P21; PROTEIN P53;

ADULT; ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL TYPE; CLINICAL ARTICLE; DISEASE COURSE; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; LYMPHOBLAST; LYMPHOCYTE; MALE; MUTATIONAL ANALYSIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

EID: 84867567270     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-121129     Document Type: Article

References (60)

1. Hass MR, Sato C, Kopan R, Zhao G (2009) Presenilin: RIP and beyond. Semin. Cell Dev Biol 20, 201-210.
2. Tagami S, Okochi M, Fukumori A, Jiang J, Yanagida K, Nakayama T, Morihara T, Tanaka T,Kudo T, TakedaM(2008) Processes of -amyloid and intracellular cytoplasmic domain generation by presenilin/(γ-secretase. Neurodegener Dis 5, 160-162.
3. Herrup K (2010) The involvement of cell cycle events in the pathogenesis of Alzheimer's disease. Alzheimers Res Ther 2, 13.
4. Malik B, Currais A, Andres A, Towlson C, Pitsi D, Nunes A, Niblock M, Cooper J, Hortobagyi T, Soriano S (2008) Loss of neuronal cell cycle control as a mechanism of eurodegeneration in the presenilin-1 Alzheimer's disease brain. Cell Cycle 7, 637-646.
5. Chevallier NL, Soriano S, Kang DE, Masliah E, Hu G, Koo EH (2005) Perturbed neurogenesis in the adult hippocampus associated with presenilin-1 A246E mutation. Am J Pathol 167, 151-159.
6. Prager K, Wang-Ecklhardt L, Fluhrer R, Kilick R, Barth E, Hampel H, Haass C, Walter J (2007) A structural switch of presenilin 1 by glycogen synthase kinase 3beta-mediated phosphorylation regulates the interaction with beta-catenin and its nuclear signaling. J Biol Chem 282, 14083- 14093.
7. Baki L, Shioi J, Wen P, Shao Z, Schwarzman A, Gama- Sosa M, Neve R, Robakis NK (2004) PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: Effects of FAD mutations. EMBO J 23, 2586-2596.
8. Ryan NS, RossorMN(2010) Correlating familial Alzheimer's disease gene mutations with clinical phenotype. Biomark Med 4, 99-112.
9. Larner A, DoranM(2009) Genotype-phenotype relationships of presenilin-1 mutations in Alzheimer's disease: An update. J Alzheimers Dis 17, 259-265.
10. Bonda DJ, Lee HP, Kudo W, Zhu X, Smith MA, Lee HG (2010) Pathological implications of cell cycle re-entry in Alzheimer disease. Expert Rev Mol Med 12, e19.
11. Arendt T (2003) Synaptic plasticity and CC activation in neurons are alternative effector pathways: The 'Dr. Jekyll and Mr. Hyde concept' of Alzheimer's disease or the yin and yang of neuroplasticity. Prog Neurobiol 71, 83-248.
12. Demir O, Singh S, Klimaschewski L, Kurnaz IA (2009) From birth till death: Neurogenesis, cell cycle, and neurodegeneration. Anat Rec (Hoboken) 292, 1953-1961.
13. Yang Y, Varvel NH, Lamb BT, Herrup K (2006) Ectopic cell cycle events link human Alzheimer's disease and amyloid precursor protein transgenic mouse models. J Neurosci 26, 775-784.
14. Jin K, GalvanV, Xie L, Mao XO, Gorostiza OF, Bredesen DE, Greenberg DA (2004) Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice. Proc Natl Acad Sci U S A 101, 13363-13367.
15. Bialopiotrowicz E, Kuzniewska B, Kachamakova- Trojanowska N, Barcikowska M, Kuznicki J, Wojda U (2011) Cell cycle regulation distinguishes lymphocytes from sporadic and familial Alzheimer's disease patients. Neurobiol Aging 32, 2319.e13-26.
16. Munoz U, Bartolome F, Esteras N, Bermejo-Pareja F, Martin-Requero A (2008) Enhanced proteasome-dependent degradation of the CDK inhibitor p27 in immortalized lymphocytes from Alzheimer's dementia patients. Neurobiol Aging 65, 3507-3519.
17. Zhou X, Jia J (2010) P53-mediated G1/S checkpoint in lymphocytes from Alzheimer's disease patients. Neurosci Lett 468, 320-325.
18. Gartner U, Holzer M, Arendt T (1999) Elevated expression of p21ras is an early event in Alzheimer's disease and precedes neurofibrillary degeneration. Neuroscience 91, 1-5.
19. Herrup K (2010) Reimagining Alzheimer's disease-an agebased hypothesis. J Neurosci 30, 16755-16762.
20. Chang JR, Ghafouri M, Mukerjee R, Bagashev A, Chabrashvili T, Sawaya BE (2011) Role of p53 in neurodegenerative diseases. Neurodegener Dis 9, 68-80.
21. Morgan GA, Guo Q, Chan SL, Gary DS, Osborne BA, Mattson MP (2007) Defects of immune regulation in the presenilin-1 mutant knockin mouse. Neuromolecular Med 9, 35-45.
22. Schwartz M, Shechter R (2010) Systemic inflammatory cells fight off neurodegenerative disease. Nat Rev Neurol 6, 405- 410.
23. Bojarski L, Lewandowicz A, Blazejczyk M, Sobczak A, Kuznicki J, Wojda U (2007) Biochemical properties of endogenous presenilin 1 and presenilin 2 in cultured human B-lymphocytes. Clin Chem Lab Med 45, 1273-1276.
24. Gomez-Tortosa E, Barquero S, Baron M, Gil-Neciga E, Castellanos F, Zurdo M, Manzano S, Munoz DG, Jimenez- Huete A, Rabano A, Sainz MJ, Guerrero R, Gobernado I, Perez-Perez J, Jimenez-Escrig A (2010) Clinical-genetic correlations in familial Alzheimer's disease caused by presenilin 1 mutations. J Alzheimers Dis 19, 873-884.
25. DowjatWK,Kuchna I,WisniewskiT,Wegiel J (2004)Anovel highly pathogenic Alzheimer presenilin-1 mutation in codon 117 (Pro117Ser): Comparison of clinical, neuropathological and cell culture phenotypes of Pro117Leu and Pro117Ser mutations. J Alzheimers Dis 6, 31-43.
26. Eder-Colli L, Abad-Estarlich N, Pannetier C, Vallet PG, Walzer C, Elder GA, Robakis NK, Bouras C, Savioz A (2009) The presenilin-1 familial Alzheimer's disease mutation P117L decreases neuronal differentiation of embryonic murine neural progenitor cells. Brain Res Bull 80, 296-301.
27. Dolcetti R, MasucciMG(2003) Epstein-Barr virus: Induction and control of cell transformation. J Cell Physiol 196, 207- 218.
28. Sie L, Loong S, Tan EK (2009) Utility of lymphoblastoid cell lines. J Neurosci Res 87, 1953-1959.
29. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDAWork Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944.
30. Miller G, LipmanM(1973) Comparison of the yield of infectious virus from clones of human and simian lymphoblastoid lines transformed by Epstein-Barr virus. J ExpMed138, 1398- 1412.
31. Begg AC, McNally NJ, Shrieve DC, Karcher H (1985) A method to measure the duration of DNA synthesis and the potential doubling time from a single sample. Cytometry 6, 620-626.
32. Ortenzi V, Meschini R, Berni A, Mancinelli P, Palitti F (2011) Study on X-ray-induced apoptosis and chromosomal damage in G2 human lymphocytes in the presence of pifithrin-, an inhibitor of p53. Mutat Res 726, 29-35.
33. Golan MP, Styczynska M, Jozwiak K, Walecki J, Maruszak A, Pniewski J, Lugiewicz R, Filipek S, Zekanowski C, BarcikowskaM(2007) Early-onset Alzheimer's disease with a de novo mutation in the presenilin 1 gene. Exp Neurol 208, 264-268.
34. Zekanowski C, Golan MP, Krzysko KA, Lipczynska-LojkowskaW, Filipek S, Kowalska A, Rossa G, Peplonska B, Styczynska M, Maruszak A, Religa D,Wender M, Kulczycki J, Barcikowska M, Kuznicki J (2006) Two novel presenilin 1 gene mutations connected with frontotemporal dementia-like clinical phenotype: Genetic and bioinformatic assessment. Exp Neurol 200, 82-88.
35. Zekanowski C, Peplonska B, Styczynska M, ReligaD, Pfeffer A, Czyzewski K, Gabryelewicz T, Szybinska A, Kijanowska- Haladyna B, Kotapka-Minc S, Luczywek E, Barczak A, Wasiak B, Chodakowska-Zebrowska M, Przekop I, Kuznicki J, Barcikowska M (2004) The E318G substitution in PSEN1 gene is not connected with Alzheimer's disease in a large Polish cohort. Neurosci Lett 357, 167-170.
36. Zekanowski C, Styczynska M, Peplonska B, Gabryelewicz T, ReligaD, Ilkowski J, Kijanowska-Haladyna B,Kotapka-Minc S, Mikkelsen S, Pfeffer A, Barczak A, Luczywek E, Wasiak B, Chodakowska-Zebrowska M, Gustaw K, Laczkowski J, Sobow T, Kuznicki J, Barcikowska M (2003) Mutations in presenilin 1, presenilin 2 and amyloid precursor protein genes in patients with early-onset Alzheimer's disease in Poland. Exp Neurol 184, 991-996.
37. Borchelt DR, Thinakaran G, Eckman CB, LeeMK,Davenport F, Ratovitsky T, Prada CM, Kim G, Seekins S, Yager D, Slunt HH,Wang R, Seeger M, Levey AI, Gandy SE, Copeland NG, Jenkins NA, Price DL, Younkin SG, Sisodia SS (1996) Familial Alzheimer's disease-linked presenilin 1 variants elevate A1-42/1-40 ratio in vitro and in vivo. Neuron 17, 1005-1013.
38. Rabe S, Reichwald J, Ammaturo D, De Strooper B, Safting P, Neumann U, Staufenbiel M (2011) The Swedish APP mutation alters the effect of genetically reducedBACE1 expression on the APP processing. J Neurochem 119, 231-239.
39. Gong P, Vetrivel KS, Nguyen PD, Meckler X, Cheng H, Kounnas MZ, Wagner SL, Parent AT, Thinakaran G (2010) Mutation analysis of the presenilin 1 N-terminal domain reveals a broad spectrum of (γ-secretase activity toward amyloid precursor protein and other substrates. J Biol Chem 285, 38042-38052.
40. Bentahir M, Nyabi O, Verhamme J, Tolia A, Horre K, Wiltfang J, Esselmann H, De Strooper B (2006) Presenilin clinical mutations can affect (γ-secretase activity by different mechanisms. J Neurochem 96, 732-742.
41. MoehlmannT,Winkler E, Xia X, Edbauer D, Murrell J, Capell A, Kaether C, Zheng H, Ghetti B, Haass C, Steiner H (2002) Presenilin-1 mutations of leucine 166 equally affect the generation of the Notch and APP intracellular domains independent of their effect on Abeta 42 production. Proc Natl Acad Sci U S A 99, 8025-8030.
42. Checler F, Sunyach C, Pardossi-Piquard R, Sevalle J, Vincent B, Kawarai T, Girardot N, St. George-Hyslop P, da Costa CA (2007) The /η-secretase- derived APP intracellular domain fragments regulate p53. Curr Alzheimer Res 4, 423-426.
43. Zlves de Costa C, Sunyach C, Pardossi-Piquard R, Sevalle J, Vincent B, Boyer N, Kawarai T, Girardot N, George- Hyslop P, Checler F (2006) Presenilin-dependent -secretasemediated control of p53-associated cell death in Alzheimer's disease. J Neurosci 26, 6377-6385.
44. Ma L, OhyagiY, Miyoshi K, Sakae N, Motomura K, Taniwaki T, Furuya H, Takeda K, Tabira T, Kira J (2009) Increase in p53 protein levels by presenilin 1 gene mutations and its inhibition by secretase inhibitors. J Alzheimers Dis 16, 565-575.
45. Coleman ML, Marshall CJ, Olson MF (2003) Ras promotes p21(Waf1/Cip1) protein stability via a cyclin D1-imposed block in proteasome-mediated degradation. EMBO J 22, 2036-2046.
46. Boonen RA, van Tijn P, Zivkovic D (2009) Wnt signaling in Alzheimer's disease: Up or down, that is the question. Ageing Res Rev 8, 71-82.
47. Brown CJ, Lain S, Verma CS, Fersht AR, Lane DP (2009) Awakening guardian angels: Drugging the p53 pathway. Nat Rev Cancer 9, 862-873.
48. Lewine A, OrenM(2009) The first 30 years of p53: Growing ever more complex. Nat Rev Cancer 9, 749-758.
49. Prinz M, Priller J, Sisodia SS, Ransohoff RM (2011) Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat Neurosci 14, 1227-1235.
50. Pellicano M, Bulati M, Buffa S, Barbagallo M, Di Prima A, Misiano G, Picone P, Di Carlo M, Nuzzo D, Candore G, Vasto S, Lio D, Caruso C, Colonna-Romano G (2010) Systemic immune responses in Alzheimer's disease: In vitro mononuclear cell activation and cytokine production. J Alzheimers Dis 21, 181-192.
51. Stieler J, Grimes R,Weber D, GartnerW, Sabbagh M, Arendt T (2012) Multivariate analysis of differential lymphocyte cell cycle activity in Alzheimer's disease. Neurobiol Aging 33, 234-241.
52. Salomoni P, Calegari F (2010) Cell cycle control of mammalian neural stem cells: Putting a speed limit on G1. Trends Cell Biol 20, 233-243.
53. Lange C, Huttner WB, Calegari F (2009) Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5, 320-331.
54. Wen PH, Hof PR, Chen X, Gluck K, Austin G, Younkin SG, Younkin LH, DeGasperi R, Gama Sosa MA, Robakis NK, Haroutunian V, Elder GA (2004) The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp Neurol 188, 224-237.
55. Uberti D, Piccioni L, Cadei M, Grigolato P, Rotter V, Memo M(2001) p53 is dispensable for apoptosis but controls neurogenesis of mouse dentate gyrus cells following (γ-irradiation. Brain Res Mol Brain Res 93, 81-89.
56. Frasca G, Carbonaro V, Merlo S, Copani A, Sortino MA (2008) Integrins mediate beta-amyloid induced cell-cycle activation and neuronal death. J Neurosci Res 86, 350- 355.
57. Majd S, Zarifkar A, Rastegar K, Takhshid MA (2008) Different fibrillarA 1-42 concentrations induce adult hippocampal neurons to reenter various phases of the cell cycle. Brain Res 1218, 224-229.
58. Murayama O, Tomita T, Nihonmatsu N, Murayama M, Sun X, Honda T, Iwatsubo T, Takashima A (1999) Enhancement of amyloid 42 secretion by 28 different presenilin 1 mutations of familial Alzheimer's disease. Neurosci Lett 265, 61-63.
59. Citron M,Westaway D, XiaW, Carlson G, Diehl T, Levesque G, Johnson-Wood K, Lee M, Seubert P, Davis A, Kholodenko D, Motter R, Sherrington R, Perry B, Yao H, Strome R, Lieberburg I, Rommens J, Kim S, Schenk D, Fraser P, St. George Hyslop P, Selkoe DJ (1997) Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nat Med 3, 67-72.
60. Hardy J (2007) Putting presenilins centre stage: Introduction to the Talking Point on the role of presenilin mutations in Alzheimer disease. EMBO Rep 8, 134-135.