Novel marker for the onset of frontotemporal dementia: Early increase in Activity-Dependent Neuroprotective Protein (ADNP) in the face of tau mutation

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Schirer, Yulie ^a   Malishkevich, Anna ^a   Ophir, Yotam ^a   Lewis, Jada ^b   Giladi, Eliezer ^a   Gozes, Illana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIVITY DEPENDENT NEUROPROTECTIVE PROTEIN; MEMBRANE PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN CORTEX; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DENSITOMETRY; FEMALE; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; GENETIC TRANSCRIPTION; HOMEOSTASIS; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; RNA SPLICING; TRANSGENE;

ALZHEIMER DISEASE; ANIMALS; BIOLOGICAL MARKERS; CEREBELLUM; CEREBRAL CORTEX; FEMALE; HOMEODOMAIN PROTEINS; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; RNA-BINDING PROTEINS; TAU PROTEINS; TRANSCRIPTION FACTORS;

EID: 84900460752     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087383     Document Type: Article

References (55)

1. Bassan M, Zamostiano R, Davidson A, Pinhasov A, Giladi E, et al. (1999) Complete sequence of a novel protein containing a femtomolar-activity-dependent neuroprotective peptide. J Neurochem 72: 1283-1293. (Pubitemid 29085045)
2. Zamostiano R, Pinhasov A, Gelber E, Steingart RA, Seroussi E, et al. (2001) Cloning and characterization of the human activity-dependent neuroprotective protein. J Biol Chem 276: 708-714. (Pubitemid 32050368)
3. Gozes I (2008) VIP, From Gene to Behavior and Back: Summarizing my 25 Years of Research. J Mol Neurosci 36: 115-124.
4. Gozes I, Zaltzman R, Hauser J, Brenneman DE, Shohami E, et al. (2005) The expression of activity-dependent neuroprotective protein (ADNP) is regulated by brain damage and treatment of mice with the ADNP derived peptide, NAP, reduces the severity of traumatic head injury. Curr Alzheimer Res 2: 149-153. (Pubitemid 40862875)
5. Gozes I (2007) Activity-dependent neuroprotective protein: From gene to drug candidate. Pharmacol Ther 114: 146-154.
6. Cosgrave AS, McKay JS, Morris R, Quinn JP, Thippeswamy T (2009) Nitric oxide regulates activity-dependent neuroprotective protein (ADNP) in the dentate gyrus of the rodent model of kainic acid-induced seizure. J Mol Neurosci 39: 9-21.
7. Pinhasov A, Mandel S, Torchinsky A, Giladi E, Pittel Z, et al. (2003) Activity-dependent neuroprotective protein: a novel gene essential for brain formation. Brain Res Dev Brain Res 144: 83-90. (Pubitemid 36897699)
8. Mandel S, Rechavi G, Gozes I (2007) Activity-dependent neuroprotective protein (ADNP) differentially interacts with chromatin to regulate genes essential for embryogenesis. Dev Biol 303: 814-824. (Pubitemid 46341287)
9. Mosch K, Franz H, Soeroes S, Singh PB, Fischle W (2011) HP1 recruits activity-dependent neuroprotective protein to H3K9me3 marked pericentromeric heterochromatin for silencing of major satellite repeats. PLoS One 6: e15894.
10. Mandel S, Gozes I (2007) Activity-dependent neuroprotective protein constitutes a novel element in the SWI/SNF chromatin remodeling complex. J Biol Chem 282: 34448-34456. (Pubitemid 350159432)
11. Batsche E, Yaniv M, Muchardt C (2006) The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat Struct Mol Biol 13: 22-29. (Pubitemid 43049398)
12. Vulih-Shultzman I, Pinhasov A, Mandel S, Grigoriadis N, Touloumi O, et al. (2007) Activity-dependent neuroprotective protein snippet NAP reduces tau hyperphosphorylation and enhances learning in a novel transgenic mouse model. J Pharmacol Exp Ther 323: 438-449. (Pubitemid 350005131)
13. Cleveland DW, Hwo SY, Kirschner MW (1977) Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J Mol Biol 116: 207-225. (Pubitemid 8215104)
14. Cleveland DW, Hwo SY, Kirschner MW (1977) Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J Mol Biol 116: 227-247. (Pubitemid 8215105)
15. Andreadis A (2005) Tau gene alternative splicing: expression patterns, regulation and modulation of function in normal brain and neurodegenerative diseases. Biochim Biophys Acta 1739: 91-103.
16. Goedert M, Jakes R (1990) Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. Embo J 9: 4225-4230. (Pubitemid 120025977)
17. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3: 519-526.
18. Kalbfuss B, Mabon SA, Misteli T (2001) Correction of alternative splicing of tau in frontotemporal dementia and parkinsonism linked to chromosome 17. J Biol Chem 276: 42986-42993.
19. Sultan A, Nesslany F, Violet M, Begard S, Loyens A, et al. (2011) Nuclear tau, a key player in neuronal DNA protection. J Biol Chem 286: 4566-4575.
20. Monroy-Ramirez HC, Basurto-Islas G, Mena R, Cisneros B, Binder LI, et al. (2013) Alterations in the nuclear architecture produced by the overexpression of tau protein in neuroblastoma cells. J Alzheimers Dis 36: 503-520.
21. Ke YD, Dramiga J, Schutz U, Kril JJ, Ittner LM, et al. (2012) Tau-mediated nuclear depletion and cytoplasmic accumulation of SFPQ in Alzheimer's and Pick's disease. PLoS One 7: e35678.
22. Bramblett GT, Goedert M, Jakes R, Merrick SE, Trojanowski JQ, et al. (1993) Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10: 1089-1099. (Pubitemid 23194399)
23. Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, et al. (1997) Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann Neurol 41: 17-24. (Pubitemid 27057088)
24. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, et al. (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282: 1914-1917. (Pubitemid 28555275)
25. Gozes I (2010) Tau pathology and future therapeutics. Curr Alzheimer Res 7: 685-696.
26. Dickey C, Kraft C, Jinwal U, Koren J, Johnson A, et al. (2009) Aging analysis reveals slowed tau turnover and enhanced stress response in a mouse model of tauopathy. Am J Pathol 174: 228-238.
27. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, et al. (2005) Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 25: 10637-10647. (Pubitemid 41681911)
28. Divinski I, Mittelman L, Gozes I (2004) A femtomolar acting octapeptide interacts with tubulin and protects astrocytes against zinc intoxication. J Biol Chem 279: 28531-28538. (Pubitemid 38900136)
29. Shiryaev N, Pickman R, Giladi E, Gozes I (2011) Protection against Tauopathy by the Drug Candidates NAP (Davunetide) and D-SAL: Biochemical, Cellular and Behavioral Aspects. Curr Pharm Des.
30. Cohen-Armon M, Visochek L, Priel E, Ishay JS (2006) A fatal effect of hornet venom on rat-brain cortical neurons. Chem Biodivers 3: 535-543. (Pubitemid 43871410)
31. Ray P, Kar A, Fushimi K, Havlioglu N, Chen X, et al. (2011) PSF suppresses tau exon 10 inclusion by interacting with a stem-loop structure downstream of exon 10. J Mol Neurosci 45: 453-466.
32. Ito T, Watanabe H, Yamamichi N, Kondo S, Tando T, et al. (2008) Brm transactivates the telomerase reverse transcriptase (TERT) gene and modulates the splicing patterns of its transcripts in concert with p54(nrb). Biochem J 411: 201-209. (Pubitemid 351482362)
33. Lee BC, Shav-Tal Y, Peled A, Gothelf Y, Jiang W, et al. (1996) A hematopoietic organ-specific 49-kD nuclear antigen: predominance in immature normal and tumor granulocytes and detection in hematopoietic precursor cells. Blood 87: 2283-2291. (Pubitemid 26086868)
34. Shav-Tal Y, Lee B, Bar-Haim S, Vandekerckhove J, Zipori D (2000) Enhanced proteolysis of pre-mRNA splicing factors in myeloid cells. Exp Hematol 28: 1029-1038.
35. Fernandez-Montesinos R, Torres M, Baglietto-Vargas D, Gutierrez A, Gozes I, et al. (2010) Activity-dependent neuroprotective protein (ADNP) expression in the amyloid precursor protein/presenilin 1 mouse model of Alzheimer's disease. J Mol Neurosci 41: 114-120.
36. Sato A, Sekine Y, Saruta C, Nishibe H, Morita N, et al. (2008) Cerebellar development transcriptome database (CDT-DB): profiling of spatio-temporal gene expression during the postnatal development of mouse cerebellum. Neural Netw 21: 1056-1069.
37. Mandel S, Spivak-Pohis I, Gozes I (2008) ADNP Differential Nucleus/Cytoplasm Localization in Neurons Suggests Multiple Roles in Neuronal Differentiation and Maintenance. J Mol Neurosci 35: 127-141.
38. Dellaire G, Makarov EM, Cowger JJ, Longman D, Sutherland HG, et al. (2002)Mammalian PRP4 kinase copurifies and interacts with components of both the U5 snRNP and the N-CoR deacetylase complexes. Mol Cell Biol 22: 5141-5156. (Pubitemid 34700704)
39. de Barreda EG, Dawson HN, Vitek MP, Avila J (2010) Tau deficiency leads to the upregulation of BAF-57, a protein involved in neuron-specific gene repression. FEBS Lett 584: 2265-2270.
40. Antunes-Martins A, Mizuno K, Irvine EE, Lepicard EM, Giese KP (2007) Sex-dependent up-regulation of two splicing factors, Psf and Srp20, during hippocampal memory formation. Learn Mem 14: 693-702. (Pubitemid 350036776)
41. Borozdin W, Graham JM, Jr., Bohm D, Bamshad MJ, Spranger S, et al. (2007) Multigene deletions on chromosome 20q13.13-q13.2 including SALL4 result in an expanded phenotype of Okihiro syndrome plus developmental delay. Hum Mutat 28: 830.
42. O'Roak BJ, Vives L, Fu W, Egertson JD, Stanaway IB, et al. (2012) Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science 338: 1619-1622.
43. O'Roak BJ, Vives L, Girirajan S, Karakoc E, Krumm N, et al. (2012) Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 485: 246-250.
44. Dresner E, Agam G, Gozes I (2011) Activity-dependent neuroprotective protein (ADNP) expression level is correlated with the expression of the sister protein ADNP2: deregulation in schizophrenia. Eur Neuropsychopharmacol 21: 355-361.
45. Braitch M, Kawabe K, Nyirenda M, Gilles LJ, Robins RA, et al. (2009)Expression of Activity-Dependent Neuroprotective Protein in the Immune System: Possible Functions and Relevance to Multiple Sclerosis. Neuroimmunomodulation 17: 120-125.
46. Yang MH, Yang YH, Lu CY, Jong SB, Chen LJ, et al. (2012) Activity-dependent neuroprotector homeobox protein: A candidate protein identified in serum as diagnostic biomarker for Alzheimer's disease. J Proteomics 75: 3617-3629.
47. Oz S, Ivashko-Pachima Y, Gozes I (2012) The ADNP Derived Peptide, NAP Modulates the Tubulin Pool: Implication for Neurotrophic and Neuroprotective Activities. PLoS One 7: e51458.
48. Quraishe S, Cowan CM, Mudher A (2013) NAP (davunetide) rescues neuronal dysfunction in a Drosophila model of tauopathy. Mol Psychiatry 18: 834-842.
49. Tsukahara T, Haniu H, Matsuda Y (2013) PTB-associated splicing factor (PSF) is a PPARgamma-binding protein and growth regulator of colon cancer cells. PLoS One 8: e58749.
50. Lourenco MV, Ledo JH (2013) Targeting Alzheimer's pathology through PPARgamma signaling: modulation of microglial function. J Neurosci 33: 5083-5084.
51. Roses AD, Lutz MW, Crenshaw DG, Grossman I, Saunders AM, et al. (2013) TOMM40 and APOE: Requirements for replication studies of association with age of disease onset and enrichment of a clinical trial. Alzheimers Dement 9: 132-136.
52. Aboonq MS, Vasiliou SA, Haddley K, Quinn JP, Bubb VJ (2012) Activity-dependent neuroprotective protein modulates its own gene expression. J Mol Neurosci 46: 33-39.
53. Jouroukhin Y, Ostritsky R, Assaf Y, Pelled G, Giladi E, et al. (2013) NAP (davunetide) modifies disease progression in a mouse model of severe neurodegeneration: Protection against impairments in axonal transport. Neurobiol Dis.
54. Gozes I, Iram T, Maryanovsky E, Arviv C, Rozenberg L, et al. (2013) Novel tubulin and tau neuroprotective fragments sharing structural similarities with the drug candidate NAP (davuentide). J Alzheimers Dis In Press.
55. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108. (Pubitemid 351818697)