Promoter DNA methylation regulates progranulin expression and is altered in FTLD

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Banzhaf Strathmann, Julia ^a   Claus, Rainer ^b,c   Mücke, Oliver ^b   Rentzsch, Kristin ^a   van der Zee, Julie ^d,e   Engelborghs, Sebastiaan ^e,f   De Deyn, Peter P ^e,f   Cruts, Marc ^d,e   van Broeckhoven, Christine ^d,e   Plass, Christoph ^b   Edbauer, Dieter ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e UNIVERSITY OF ANTWERP   (Belgium)

^f Hospital Network Antwerp Middelheim and Hoge Beuken   (Belgium)

Author keywords

5 aza 2, deoxycytidine; DNA methylation; Epigenetics; FTLD; Progranulin

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; AZACITIDINE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3A; ENZYME INHIBITOR; GRN PROTEIN, HUMAN; MESSENGER RNA; SIGNAL PEPTIDE;

AGED; ALZHEIMER DISEASE; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; CELL LINE; COMPARATIVE STUDY; CPG ISLAND; DNA METHYLATION; DRUG EFFECTS; FEMALE; FRONTOTEMPORAL DEMENTIA; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; MALE; METABOLISM; MIDDLE AGED; MOUSE; PARKINSON DISEASE; PROMOTER REGION; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; AZACITIDINE; BRAIN; CELL LINE; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ENZYME INHIBITORS; FEMALE; FRONTOTEMPORAL LOBAR DEGENERATION; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MIDDLE AGED; PARKINSON DISEASE; PROMOTER REGIONS, GENETIC; RNA, MESSENGER;

EID: 85005929986     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/20515960116     Document Type: Article

References (60)

1. Graff-Radford NR, Woodruff BK: Frontotemporal dementia. Semin Neurol 2007, 27: 048-057. 10.1055/s-2006-956755
2. Premi E, Padovani A, Borroni B: Frontotemporal lobar degeneration. Adv Exp Med Biol 2012, 724: 114-127. 10.1007/978-1-4614-0653-2_9
3. Mackenzie I, Baborie A, Pickering-Brown S, Plessis D, Jaros E, Perry R, Neary D, Snowden J, Mann D: Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration: classification and relation to clinical phenotype. Acta Neuropathol 2006, 112: 539-549. 10.1007/s00401-006-0138-9
4. Sampathu DM, Neumann M, Kwong LK, Chou TT, Micsenyi M, Truax A, Bruce J, Grossman M, Trojanowski JQ, Lee VMY: Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohistochemistry and novel monoclonal antibodies. Am J Pathol 2006, 169: 1343-1352. 10.2353/ajpath.2006.060438
5. DeJesus-Hernandez M, Mackenzie Ian R, Boeve Bradley F, Boxer Adam L, Baker M, Rutherford Nicola J, Nicholson Alexandra M, Finch NiCole A, Flynn H, Adamson J: Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72: 245-256. 10.1016/j.neuron.2011.09.011
6. Gijselinck I, Van Langenhove T, van der Zee J, Sleegers K, Philtjens S, Kleinberger G, Janssens J, Bettens K, Van Cauwenberghe C, Pereson S: A C9orf72 promoter repeat expansion in a Flanders-Belgian cohort with disorders of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum: a gene identification study. Lancet Neurol 2012, 11: 54-65. 10.1016/S1474-4422(11)70261-7
7. Renton Alan E, Majounie E, Waite A, Simón-Sánchez J, Rollinson S, Gibbs JR, Schymick Jennifer C, Laaksovirta H, Van Swieten JC, Myllykangas L: A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72: 257-268. 10.1016/j.neuron.2011.09.010
8. Borroni B, Archetti S, Del Bo R, Papetti A, Buratti E, Bonvicini C, Agosti C, Cosseddu M, Turla M, Di Lorenzo D: TARDBP mutations in frontotemporal lobar degeneration: frequency, clinical features, and disease course. Rejuvenation Res 2010, 13: 509-517. 10.1089/rej.2010.1017
9. Forman MS, Mackenzie IR, Cairns NJ, Swanson E, Boyer PJ, Drachman DA, Jhaveri BS, Karlawish JH, Pestronk A, Smith TW: Novel ubiquitin neuropathology in frontotemporal dementia with valosin-containing protein gene mutations. J Neuropathol Exp Neurol 2006, 65: 571-581. 10.1097/00005072-200606000-00005
10. Cruts M, Gijselinck I, van der Zee J, Engelborghs S, Wils H, Pirici D, Rademakers R, Vandenberghe R, Dermaut B, Martin J-J: Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 2006, 442: 920-924. 10.1038/nature05017
11. Baker M, Mackenzie IR, Pickering-Brown SM, Gass J, Rademakers R, Lindholm C, Snowden J, Adamson J, Sadovnick AD, Rollinson S: Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 2006, 442: 916-919. 10.1038/nature05016
12. Gijselinck I, Van Broeckhoven C, Cruts M: Granulin mutations associated with frontotemporal lobar degeneration and related disorders: An update. Hum Mutat 2008, 29: 1373-1386. 10.1002/humu.20785
13. Ryan CL, Baranowski DC, Chitramuthu BP, Malik S, Li Z, Cao M, Minotti S, Durham HD, Kay DG, Shaw CA: Progranulin is expressed within motor neurons and promotes neuronal cell survival. BMC Neurosci 2009, 10: 130. 10.1186/1471-2202-10-130
14. Finch N, Baker M, Crook R, Swanson K, Kuntz K, Surtees R, Bisceglio G, Rovelet-Lecrux A, Boeve B, Petersen RC: Plasma progranulin levels predict progranulin mutation status in frontotemporal dementia patients and asymptomatic family members. Brain 2009, 132: 583-591. 10.1093/brain/awn352
15. Sleegers K, Brouwers N, Van Damme P, Engelborghs S, Gijselinck I, van derZee J, Peeters K, Mattheijssens M, Cruts M, Vandenberghe R: Serum biomarker for progranulin-associated frontotemporal lobar degeneration. Ann Neurol 2009, 65: 603-609. 10.1002/ana.21621
16. Ghidoni R, Benussi L, Glionna M, Franzoni M, Binetti G: Low plasma progranulin levels predict progranulin mutations in frontotemporal lobar degeneration. Neurology 2008, 71: 1235-1239. 10.1212/01.wnl.0000325058.10218.fc
17. Beck J, Rohrer JD, Campbell T, Isaacs A, Morrison KE, Goodall EF, Warrington EK, Stevens J, Revesz T, Holton J: A distinct clinical, neuropsychological and radiological phenotype is associated with progranulin gene mutations in a large UK series. Brain 2008, 131: 706-720. 10.1093/brain/awm320
18. Whitwell JL, Weigand SD, Boeve BF, Senjem ML, Gunter JL, DeJesus-Hernandez M, Rutherford NJ, Baker M, Knopman DS, Wszolek ZK: Neuroimaging signatures of frontotemporal dementia genetics: C9ORF72, tau, progranulin and sporadics. Brain 2012, 135: 794-806. 10.1093/brain/aws001
19. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suñer D, Cigudosa JC, Urioste M, Benitez J: Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 2005, 102: 10604-10609. 10.1073/pnas.0500398102
20. Cenik B, Sephton CF, Dewey CM, Xian X, Wei S, Yu K, Niu W, Coppola G, Coughlin SE, Lee SE: SAHA (VORINOSTAT) upregulates progranulin transcription: a rational therapeutic approach to frontotemporal dementia. J Biol Chem 2011, 286: 16101-16108. 10.1074/jbc.M110.193433
21. Herman JG, Baylin SB: Gene silencing in cancer in association with promoter hypermethylation. NEnglJMed 2003, 349: 2042-2054. 10.1056/NEJMra023075
22. Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G, Cantor CR, Field JK, van den Boom D: Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci USA 2005, 102: 15785-15790. 10.1073/pnas.0507816102
23. Finch N, Carrasquillo MM, Baker M, Rutherford NJ, Coppola G, DeJesus-Hernandez M, Crook R, Hunter T, Ghidoni R, Benussi L: TMEM106B regulates progranulin levels and the penetrance of FTLD in GRN mutation carriers. Neurology 2011, 76: 467-474. 10.1212/WNL.0b013e31820a0e3b
24. Querfurth HW, LaFerla FM: Alzheimer's Disease. N Engl J Med 2010, 362: 329-344. 10.1056/NEJMra0909142
25. Abe M, Bonini NM: MicroRNAs and neurodegeneration: role and impact. Trends Cell Biol 2013, 23: 30-36. 10.1016/j.tcb.2012.08.013
26. Claus R, Almstedt M, Lubbert M: Epigenetic treatment of hematopoietic malignancies: in vivo targets of demethylating agents. SeminOncol 2005, 32: 511-520.
27. Klug M, Rehli M: Functional analysis of promoter CPG-methylation using a CpG-free luciferase reporter vector. Epigenetics 2006, 1: 127-130. 10.4161/epi.1.3.3327
28. Mackenzie I, Neumann M, Baborie A, Sampathu D, Du Plessis D, Jaros E, Perry R, Trojanowski J, Mann D, Lee V: A harmonized classification system for FTLD-TDP pathology. Acta Neuropathol 2011, 122: 111-113. 10.1007/s00401-011-0845-8
29. Van Langenhove T, van der Zee J, Gijselinck I, Engelborghs S, Vandenberghe R, Vandenbulcke M, De Bleecker J, Sieben A, Versijpt J, Ivanoiu A: Distinct clinical characteristics of C9orf72 expansion carriers compared with GRN, MAPT, and nonmutation carriers in a Flanders-Belgian FTLD cohort. JAMA Neurol 2013, 21: 1-9.
30. van der Zee J, Rademakers R, Engelborghs S, Gijselinck I, Bogaerts V, Vandenberghe R, Santens P, Caekebeke J, De Pooter T, Peeters K: A Belgian ancestral haplotype harbours a highly prevalent mutation for 17q21-linked tau-negative FTLD. Brain 2006, 129: 841-852. 10.1093/brain/awl029
31. Rollinson S, Rohrer JD, van der Zee J, Sleegers K, Mead S, Engelborghs S, Collinge J, De Deyn PP, Mann DM, Van Broeckhoven C, Pickering-Brown SM: No association of PGRN 3,UTR rs5848 in frontotemporal lobar degeneration. Neurobiol Aging 2011, 32: 754-755. 10.1016/j.neurobiolaging.2009.04.009
32. van der Zee J, Pirici D, Van Langenhove T, Engelborghs S, Vandenberghe R, Hoffmann M, Pusswald G, Van den Broeck M, Peeters K, Mattheijssens M: Clinical heterogeneity in 3 unrelated families linked to VCP p.Arg159His. Neurology 2009, 73: 626-632. 10.1212/WNL.0b013e3181b389d9
33. Theuns J, Brouwers N, Engelborghs S, Sleegers K, Bogaerts V, Corsmit E, De Pooter T, Van Duijn CM, De Deyn PP, Van Broeckhoven C: Promoter mutations that increase amyloid precursor-protein expression are associated with Alzheimer disease. Am J Hum Genet 2006, 78: 936-946. 10.1086/504044
34. Cruts M, Theuns J, Van Broeckhoven C: Locus-specific mutation databases for neurodegenerative brain diseases. Hum Mutat 2012, 33: 1340-1344. 10.1002/humu.22117
35. Baylin SB, Herman JG: DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet 2000, 16: 168-174. 10.1016/S0168-9525(99)01971-X
36. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M: The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009, 41: 178-186. 10.1038/ng.298
37. Morahan JM, Yu B, Trent RJ, Pamphlett R: A genome-wide analysis of brain DNA methylation identifies new candidate genes for sporadic amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2009, 10: 418-429. 10.3109/17482960802635397
38. Silva PN, Gigek CO, Leal MF, Bertolucci PH, De Labio RW, Payao SL, Smith Mde A: Promoter methylation analysis of SIRT3, SMARCA5, HTERT and CDH1 genes in aging and Alzheimer's disease. J Alzheimers Dis 2008, 13: 173-176.
39. Issa JP: DNA methylation as a clinical marker in oncology. J Clin Oncol 2012, 30: 2566-2568. 10.1200/JCO.2012.42.1016
40. Brettschneider J, Libon DJ, Toledo JB, Xie SX, McCluskey L, Elman L, Geser F, Lee VM, Grossman M, Trojanowski JQ: Microglial activation and TDP-43 pathology correlate with executive dysfunction in amyotrophic lateral sclerosis. Acta Neuropathol 2012, 123: 395-407. 10.1007/s00401-011-0932-x
41. Tanaka Y, Matsuwaki T, Yamanouchi K, Nishihara M: Exacerbated inflammatory responses related to activated microglia after traumatic brain injury in progranulin-deficient mice. Neuroscience 2013, 231: 49-60.
42. Chen-Plotkin A, Xiao J, Geser F, Martinez-Lage M, Grossman M, Unger T, Wood E, Van Deerlin V, Trojanowski J, Lee V: Brain progranulin expression inGRN -associated frontotemporal lobar degeneration. Acta Neuropathol 2010, 119: 111-122. 10.1007/s00401-009-0576-2
43. Galimberti D, D'Addario C, Dell'osso B, Fenoglio C, Marcone A, Cerami C, Cappa SF, Palazzo MC, Arosio B, Mari D: Progranulin gene (GRN) promoter methylation is increased in patients with sporadic frontotemporal lobar degeneration. Neurol Sci 2012, 14: 14.
44. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G, Sun YE: DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 2003, 302: 890-893. 10.1126/science.1090842
45. Martins-Taylor K, Schroeder DI, Lasalle JM, Lalande M, Xu RH: Role of DNMT3B in the regulation of early neural and neural crest specifiers. Epigenetics 2012, 7: 71-82. 10.4161/epi.7.1.18750
46. Feng J, Fan G: Chapter 4 - the role of DNA methylation in the central nervous system and neuropsychiatric disorders. In International Review of Neurobiology. Volume Volume 89. Edited by: Xiao-Hong L. Amsterdam: Academic; 2009:67-84.
47. Bousquet M, Harris MH, Zhou B, Lodish HF: MicroRNA miR-125b causes leukemia. Proc Natl Acad Sci 2010, 107: 21558-21563. 10.1073/pnas.1016611107
48. Yoo CB, Jones PA: Epigenetic therapy of cancer: past, present and future. NatRevDrug Discov 2006, 5: 37-50. 10.1038/nrd1930
49. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH: Recovery of learning and memory is associated with chromatin remodelling. Nature 2007, 447: 178-182. 10.1038/nature05772
50. Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, Agis-Balboa RC, Cota P, Wittnam JL, Gogol-Doering A, Opitz L: Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 2010, 328: 753-756. 10.1126/science.1186088
51. Capell A, Liebscher S, Fellerer K, Brouwers N, Willem M, Lammich S, Gijselinck I, Bittner T, Carlson AM, Sasse F: Rescue of progranulin deficiency associated with frontotemporal lobar degeneration by alkalizing reagents and inhibition of vacuolar ATPase. J Neurosci 2011, 31: 1885-1894. 10.1523/JNEUROSCI.5757-10.2011
52. Lubin FD, Roth TL, Sweatt JD: Epigenetic regulation of bdnf gene transcription in the consolidation of fear memory. J Neurosci 2008, 28: 10576-10586. 10.1523/JNEUROSCI.1786-08.2008
53. Petkau TL, Neal SJ, Orban PC, MacDonald JL, Hill AM, Lu G, Feldman HH, Mackenzie IRA, Leavitt BR: Progranulin expression in the developing and adult murine brain. J Comp Neurol 2010, 518: 3931-3947. 10.1002/cne.22430
54. Kaiser J: Epigenetic drugs take on cancer. Science 2010, 330: 576-578. 10.1126/science.330.6004.576
55. Fischer A, Sananbenesi F, Mungenast A, Tsai LH: Targeting the correct HDAC(s) to treat cognitive disorders. Trends Pharmacol Sci 2010, 31: 605-617. 10.1016/j.tips.2010.09.003
56. Allen B, Ingram E, Takao M, Smith MJ, Jakes R, Virdee K, Yoshida H, Holzer M, Craxton M, Emson PC: Abundant Tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S Tau protein. J Neurosci 2002, 22: 9340-9351.
57. van der Zee J, Van Langenhove T, Kleinberger G, Sleegers K, Engelborghs S, Vandenberghe R, Santens P, Van den Broeck M, Joris G, Brys J: TMEM106B is associated with frontotemporal lobar degeneration in a clinically diagnosed patient cohort. Brain 2011, 134: 808-815. 10.1093/brain/awr007
58. van der Zee J, Gijselinck I, Dillen L, Van Langenhove T, Theuns J, Engelborghs S, Philtjens S, Vandenbulcke M, Sleegers K, Sieben A: A Pan-European study of the C9orf72 repeat associated with FTLD: geographic prevalence, genomic instability, and intermediate repeats. Hum Mutat 2013, 34: 363-373. 10.1002/humu.22244
59. Brouwers N, Nuytemans K, van der Zee J, Gijselinck I, Engelborghs S, Theuns J, Kumar-Singh S, Pickut BA, Pals P, Dermaut B: Alzheimer and Parkinson diagnoses in progranulin null mutation carriers in an extended founder family. Arch Neurol 2007, 64: 1436-1446. 10.1001/archneur.64.10.1436
60. Edbauer D, Neilson JR, Foster KA, Wang C-F, Seeburg DP, Batterton MN, Tada T, Dolan BM, Sharp PA, Sheng M: Regulation of synaptic structure and function by FMRP-associated MicroRNAs miR-125b and miR-132. Neuron 2010, 65: 373-384. 10.1016/j.neuron.2010.01.005