Advertisement

Journal of Molecular Neuroscience

, Volume 69, Issue 2, pp 343–350 | Cite as

Does SCFD1 rs10139154 Polymorphism Decrease Alzheimer’s Disease Risk?

  • Polyxeni Stamati
  • Vasileios Siokas
  • Athina-Maria Aloizou
  • Emmanouil Karampinis
  • Stylianos Arseniou
  • Valerii N. Rakitskii
  • Aristidis Tsatsakis
  • Demetrios A. Spandidos
  • Illana Gozes
  • Panayiotis D. Mitsias
  • Dimitrios P. Bogdanos
  • Georgios M. Hadjigeorgiou
  • Efthimios DardiotisEmail author
Article

Abstract

Α number of genetic variants have been associated with Alzheimer’s disease (AD) susceptibility. Sec1 family domain-containing protein 1 (SCFD1) gene polymorphism rs10139154 has recently been implicated in the risk of developing amyotrophic lateral sclerosis (ALS). Similarities in the pathogenetic cascade of both diseases have also been described. The present study was designed to evaluate the possible contribution of SCFD1 rs10139154 to AD. A total of 327 patients with AD and an equal number of healthy controls were included in the study and genotyped for rs10139154. With logistic regression analyses, rs10139154 was examined for the association with the risk of developing AD. In the recessive mode, SCFD1 rs10139154 was associated with a decreased risk of developing AD (odds ratio (OR) (95% confidence interval (CI)) = 0.63 (0.40–0.97), p = 0.036). The current study provides preliminary evidence of the involvement of SCFD1 rs10139154 in the risk of developing AD.

Keywords

AD Genetics SNPs Polymorphism SCFD1 

Notes

Funding

This study was supported in part by a research grant from the Research Committee of the University of Thessaly, Greece (code 5287).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 2017 Alzheimer’s disease facts and figures (2017) Alzheimer's & Dementia 13:325–373  https://doi.org/10.1016/j.jalz.2017.02.001
  2. Alonso AD, Cohen LS, Corbo C, Morozova V, ElIdrissi A, Phillips G, Kleiman FE (2018) Hyperphosphorylation of tau associates with changes in its function beyond microtubule stability. Front Cell Neurosci 12:338.  https://doi.org/10.3389/fncel.2018.00338 CrossRefGoogle Scholar
  3. Anastasiou CA, Yannakoulia M, Kosmidis MH, Dardiotis E, Hadjigeorgiou GM, Sakka P, Arampatzi X, Bougea A, Labropoulos I, Scarmeas N (2017) Mediterranean diet and cognitive health: initial results from the Hellenic Longitudinal Investigation of Ageing and Diet. PLoS One 12:e0182048.  https://doi.org/10.1371/journal.pone.0182048 CrossRefGoogle Scholar
  4. Androutsopoulos VP, Kanavouras K, Tsatsakis AM (2011) Role of paraoxonase 1 (PON1) in organophosphate metabolism: implications in neurodegenerative diseases. Toxicol Appl Pharmacol 256:418–424.  https://doi.org/10.1016/j.taap.2011.08.009 CrossRefGoogle Scholar
  5. Aoki Y, Manzano R, Lee Y, Dafinca R, Aoki M, Douglas AGL, Varela MA, Sathyaprakash C, Scaber J, Barbagallo P, Vader P, Mäger I, Ezzat K, Turner MR, Ito N, Gasco S, Ohbayashi N, el Andaloussi S, Takeda S’, Fukuda M, Talbot K, Wood MJA (2017) C9orf72 and RAB7L1 regulate vesicle trafficking in amyotrophic lateral sclerosis and frontotemporal dementia. Brain 140:887–897.  https://doi.org/10.1093/brain/awx024 CrossRefGoogle Scholar
  6. Argentieri MA, Nagarajan S, Seddighzadeh B, Baccarelli AA, Shields AE (2017) Epigenetic pathways in human disease: the impact of DNA methylation on stress-related pathogenesis and current challenges in biomarker development. EBioMedicine 18:327–350.  https://doi.org/10.1016/j.ebiom.2017.03.044 CrossRefGoogle Scholar
  7. Ashraf GM et al (2016) Recent updates on the association between Alzheimer’s disease and vascular dementia medicinal chemistry. Shariqah (United Arab Emirates) 12:226–237CrossRefGoogle Scholar
  8. Ashton NJ, Schöll M, Heurling K, Gkanatsiou E, Portelius E, Höglund K, Brinkmalm G, Hye A, Blennow K, Zetterberg H (2018) Update on biomarkers for amyloid pathology in Alzheimer’s disease. Biomark Med 12:799–812.  https://doi.org/10.2217/bmm-2017-0433 CrossRefGoogle Scholar
  9. Baltazar MT, Dinis-Oliveira RJ, de Lourdes Bastos M, Tsatsakis AM, Duarte JA, Carvalho F (2014) Pesticides exposure as etiological factors of Parkinson’s disease and other neurodegenerative diseases--a mechanistic approach. Toxicol Lett 230:85–103.  https://doi.org/10.1016/j.toxlet.2014.01.039 CrossRefGoogle Scholar
  10. Bando Y, Katayama T, Taniguchi M, Ishibashi T, Matsuo N, Ogawa S, Tohyama M (2005) RA410/Sly1 suppresses MPP+ and 6-hydroxydopamine-induced cell death in SH-SY5Y cells. Neurobiol Dis 18:143–151.  https://doi.org/10.1016/j.nbd.2004.09.008 CrossRefGoogle Scholar
  11. Beharry C, Cohen LS, Di J, Ibrahim K, Briffa-Mirabella S, Alonso Adel C (2014) Tau-induced neurodegeneration: mechanisms and targets. Neurosci Bull 30:346–358.  https://doi.org/10.1007/s12264-013-1414-z CrossRefGoogle Scholar
  12. Bekris LM, Yu C-E, Bird TD, Tsuang DW (2010) Genetics of Alzheimer disease Journal of geriatric psychiatry and neurology 23:213–227 doi: https://doi.org/10.1177/0891988710383571
  13. Bourdenx M, Koulakiotis NS, Sanoudou D, Bezard E, Dehay B, Tsarbopoulos A (2017) Protein aggregation and neurodegeneration in prototypical neurodegenerative diseases: examples of amyloidopathies, tauopathies and synucleinopathies. Prog Neurobiol 155:171–193.  https://doi.org/10.1016/j.pneurobio.2015.07.003 CrossRefGoogle Scholar
  14. Carmona S, Hardy J, Guerreiro R (2018) The genetic landscape of Alzheimer disease. Handb Clin Neurol 148:395–408.  https://doi.org/10.1016/b978-0-444-64076-5.00026-0 CrossRefGoogle Scholar
  15. Carr CM, Rizo J (2010) At the junction of SNARE and SM protein function. Curr Opin Cell Biol 22:488–495.  https://doi.org/10.1016/j.ceb.2010.04.006 CrossRefGoogle Scholar
  16. Chen Y, Zhou Q, Gu X, Wei Q, Cao B, Liu H, Hou Y, Shang H (2018) An association study between SCFD1 rs10139154 variant and amyotrophic lateral sclerosis in a Chinese cohort. Amyotroph Lateral Scler Frontotemporal Degener 19:413–418.  https://doi.org/10.1080/21678421.2017.1418006 CrossRefGoogle Scholar
  17. Conlon EG et al (2018) Unexpected similarities between C9ORF72 and sporadic forms of ALS/FTD suggest a common disease mechanism. eLife 7.  https://doi.org/10.7554/eLife.37754
  18. Corder EH, Saunders A, Strittmatter W, Schmechel D, Gaskell P, Small G, Roses A, Haines J, Pericak-Vance M (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science (New York, NY) 261:921–923CrossRefGoogle Scholar
  19. Costa C, Tsatsakis A, Mamoulakis C, Teodoro M, Briguglio G, Caruso E, Tsoukalas D, Margina D, Dardiotis E, Kouretas D, Fenga C (2017) Current evidence on the effect of dietary polyphenols intake on chronic diseases. Food Chem Toxicol 110:286–299.  https://doi.org/10.1016/j.fct.2017.10.023 CrossRefGoogle Scholar
  20. Cubinkova V, Valachova B, Uhrinova I, Brezovakova V, Smolek T, Jadhav S, Zilka N (2018) Alternative hypotheses related to Alzheimer’s disease. Bratislavske lekarske listy 119:210–216.  https://doi.org/10.4149/bll_2018_039 Google Scholar
  21. Cuyvers E, Sleegers K (2016) Genetic variations underlying Alzheimer’s disease: evidence from genome-wide association studies and beyond. Lancet Neurol 15:857–868.  https://doi.org/10.1016/s1474-4422(16)00127-7 CrossRefGoogle Scholar
  22. Danborg PB, Simonsen AH, Waldemar G, Heegaard NH (2014) The potential of microRNAs as biofluid markers of neurodegenerative diseases--a systematic review. Biomarkers 19:259–268.  https://doi.org/10.3109/1354750x.2014.904001 CrossRefGoogle Scholar
  23. Dardiotis E, Xiromerisiou G, Hadjichristodoulou C, Tsatsakis AM, Wilks MF, Hadjigeorgiou GM (2013) The interplay between environmental and genetic factors in Parkinson’s disease susceptibility: the evidence for pesticides. Toxicology 307:17–23.  https://doi.org/10.1016/j.tox.2012.12.016 CrossRefGoogle Scholar
  24. Dardiotis E, Kosmidis MH, Yannakoulia M, Hadjigeorgiou GM, Scarmeas N (2014a) The Hellenic Longitudinal Investigation of Aging and Diet (HELIAD): rationale, study design, and cohort description. Neuroepidemiology 43:9–14.  https://doi.org/10.1159/000362723 CrossRefGoogle Scholar
  25. Dardiotis E, Paterakis K, Tsivgoulis G, Tsintou M, Hadjigeorgiou GF, Dardioti M, Grigoriadis S, Simeonidou C, Komnos A, Kapsalaki E, Fountas K, Hadjigeorgiou GM (2014b) AQP4 tag single nucleotide polymorphisms in patients with traumatic brain injury. J Neurotrauma 31:1920–1926.  https://doi.org/10.1089/neu.2014.3347 CrossRefGoogle Scholar
  26. Dardiotis E, Siokas V, Zafeiridis T, Paterakis K, Tsivgoulis G, Dardioti M, Grigoriadis S, Simeonidou C, Deretzi G, Zintzaras E, Jagiella J, Hadjigeorgiou GM (2017) Integrins AV and B8 gene polymorphisms and risk for intracerebral hemorrhage in Greek and Polish populations. NeuroMolecular Med 19:69–80.  https://doi.org/10.1007/s12017-016-8429-3 CrossRefGoogle Scholar
  27. Dardiotis E, Siokas V, Garas A, Paraskevaidis E, Kyrgiou M, Xiromerisiou G, Deligeoroglou E, Galazios G, Kontomanolis E, Spandidos D, Tsatsakis A, Daponte A (2018a) Genetic variations in the SULF1 gene alter the risk of cervical cancer and precancerous lesions. Oncol Lett 16:3833–3841.  https://doi.org/10.3892/ol.2018.9104 Google Scholar
  28. Dardiotis E, Siokas V, Sokratous M, Tsouris Z, Michalopoulou A, Andravizou A, Dastamani M, Ralli S, Vinceti M, Tsatsakis A, Hadjigeorgiou GM (2018b) Genetic polymorphisms in amyotrophic lateral sclerosis: evidence for implication in detoxification pathways of environmental toxicants. Environ Int 116:122–135.  https://doi.org/10.1016/j.envint.2018.04.008 CrossRefGoogle Scholar
  29. Dardiotis E, Karampinis E, Siokas V, Aloizou AM, Rikos D, Ralli S, Papadimitriou D, Bogdanos DP, Hadjigeorgiou GM (2019) ERCC6L2 rs591486 polymorphism and risk for amyotrophic lateral sclerosis in Greek population. Neurol Sci 40:1237–1244.  https://doi.org/10.1007/s10072-019-03825-3 CrossRefGoogle Scholar
  30. Dascher C, Balch WE (1996) Mammalian Sly1 regulates syntaxin 5 function in endoplasmic reticulum to Golgi transport. J Biol Chem 271:15866–15869CrossRefGoogle Scholar
  31. Friese MA, Schattling B, Fugger L (2014) Mechanisms of neurodegeneration and axonal dysfunction in multiple sclerosis. Nat Rev Neurol 10:225–238.  https://doi.org/10.1038/nrneurol.2014.37 CrossRefGoogle Scholar
  32. Fyfe I (2018) Epigenetics links ageing with Alzheimer disease. Nat Rev Neurol 14:254.  https://doi.org/10.1038/nrneurol.2018.36 CrossRefGoogle Scholar
  33. Garcia-Gonzalez P, Cabral-Miranda F, Hetz C, Osorio F (2018) Interplay between the unfolded protein response and immune function in the development of neurodegenerative diseases. Front Immunol 9:2541.  https://doi.org/10.3389/fimmu.2018.02541 CrossRefGoogle Scholar
  34. Gerritsen AA, Bakker C, Verhey FR, de Vugt ME, Melis RJ, Koopmans RT (2016) Prevalence of comorbidity in patients with young-onset Alzheimer disease compared with late-onset: a comparative cohort study. J Am Med Dir Assoc 17:318–323.  https://doi.org/10.1016/j.jamda.2015.11.011 CrossRefGoogle Scholar
  35. Goedert M (2015) NEURODEGENERATION. Alzheimer’s and Parkinson’s diseases: the prion concept in relation to assembled Abeta, tau, and alpha-synuclein. Science (New York) 349:1255555.  https://doi.org/10.1126/science.1255555 CrossRefGoogle Scholar
  36. Gubandru M, Margina D, Tsitsimpikou C, Goutzourelas N, Tsarouhas K, Ilie M, Tsatsakis AM, Kouretas D (2013) Alzheimer’s disease treated patients showed different patterns for oxidative stress and inflammation markers. Food Chem Toxicol 61:209–214.  https://doi.org/10.1016/j.fct.2013.07.013 CrossRefGoogle Scholar
  37. Haeusler AR, Donnelly CJ, Periz G, Simko EAJ, Shaw PG, Kim MS, Maragakis NJ, Troncoso JC, Pandey A, Sattler R, Rothstein JD, Wang J (2014) C9orf72 nucleotide repeat structures initiate molecular cascades of disease. Nature 507:195–200.  https://doi.org/10.1038/nature13124 CrossRefGoogle Scholar
  38. Haines JL (2018) Alzheimer disease: perspectives from epidemiology and genetics. J Law Med Ethics 46:694–698.  https://doi.org/10.1177/1073110518804230 CrossRefGoogle Scholar
  39. Hardy J (2017) The discovery of Alzheimer-causing mutations in the APP gene and the formulation of the “amyloid cascade hypothesis”. FEBS J 284:1040–1044.  https://doi.org/10.1111/febs.14004 CrossRefGoogle Scholar
  40. Hou N, Yang Y, Scott IC, Lou X (2017) The Sec domain protein Scfd1 facilitates trafficking of ECM components during chondrogenesis. Dev Biol 421:8–15.  https://doi.org/10.1016/j.ydbio.2016.11.010 CrossRefGoogle Scholar
  41. Jouroukhin Y, Ostritsky R, Assaf Y, Pelled G, Giladi E, Gozes I (2013) NAP (davunetide) modifies disease progression in a mouse model of severe neurodegeneration: protection against impairments in axonal transport. Neurobiol Dis 56:79–94.  https://doi.org/10.1016/j.nbd.2013.04.012 CrossRefGoogle Scholar
  42. Jovičić A, Mertens J, Boeynaems S, Bogaert E, Chai N, Yamada SB, Paul JW, Sun S, Herdy JR, Bieri G, Kramer NJ, Gage FH, van den Bosch L, Robberecht W, Gitler AD (2015) Modifiers of C9orf72 dipeptide repeat toxicity connect nucleocytoplasmic transport defects to FTD/ALS. Nat Neurosci 18:1226–1229.  https://doi.org/10.1038/nn.4085 CrossRefGoogle Scholar
  43. Karch CM, Goate AM (2015) Alzheimer’s disease risk genes and mechanisms of disease pathogenesis. Biol Psychiatry 77:43–51.  https://doi.org/10.1016/j.biopsych.2014.05.006 CrossRefGoogle Scholar
  44. Katsarou MS, Papasavva M, Latsi R, Toliza I, Gkaros AP, Papakonstantinou S, Gatzonis S, Mitsikostas DD, Kovatsi L, Isotov BN, Tsatsakis AM, Drakoulis N (2018) Population-based analysis of cluster headache-associated genetic polymorphisms. J Mol Neurosci 65:367–376.  https://doi.org/10.1007/s12031-018-1103-5 CrossRefGoogle Scholar
  45. Korczyn AD (2008) The amyloid cascade hypothesis. Alzheimer's Dement 4:176–178.  https://doi.org/10.1016/j.jalz.2007.11.008 CrossRefGoogle Scholar
  46. Lipnicki DM, Crawford JD, Dutta R, Thalamuthu A, Kochan NA, Andrews G, Lima-Costa MF, Castro-Costa E, Brayne C, Matthews FE, Stephan BCM, Lipton RB, Katz MJ, Ritchie K, Scali J, Ancelin ML, Scarmeas N, Yannakoulia M, Dardiotis E, Lam LCW, Wong CHY, Fung AWT, Guaita A, Vaccaro R, Davin A, Kim KW, Han JW, Kim TH, Anstey KJ, Cherbuin N, Butterworth P, Scazufca M, Kumagai S, Chen S, Narazaki K, Ng TP, Gao Q, Reppermund S, Brodaty H, Lobo A, Lopez-Anton R, Santabárbara J, Sachdev PS, Cohort Studies of Memory in an International Consortium (COSMIC) (2017) Age-related cognitive decline and associations with sex, education and apolipoprotein E genotype across ethnocultural groups and geographic regions: a collaborative cohort study. PLoS Med 14:e1002261.  https://doi.org/10.1371/journal.pmed.1002261 CrossRefGoogle Scholar
  47. Liu C-C, Liu C-C, Kanekiyo T, Xu H, Bu G (2013) Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat Rev Neurol 9:106–118.  https://doi.org/10.1038/nrneurol.2012.263 CrossRefGoogle Scholar
  48. Luca M, Luca A, Calandra C (2015) The role of oxidative damage in the pathogenesis and progression of Alzheimer’s disease and vascular dementia. Oxidative Med Cell Longev 2015:504678.  https://doi.org/10.1155/2015/504678 CrossRefGoogle Scholar
  49. Lyubartseva G, Lovell MA (2012) A potential role for zinc alterations in the pathogenesis of Alzheimer’s disease. BioFactors (Oxford, England) 38:98–106.  https://doi.org/10.1002/biof.199 CrossRefGoogle Scholar
  50. Magalingam KB, Radhakrishnan A, Ping NS, Haleagrahara N (2018) Current concepts of neurodegenerative mechanisms in Alzheimer’s disease. Biomed Res Int 2018:3740461.  https://doi.org/10.1155/2018/3740461 CrossRefGoogle Scholar
  51. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 34:939–944.  https://doi.org/10.1212/wnl.34.7.939 CrossRefGoogle Scholar
  52. Mietelska-Porowska A, Wasik U, Goras M, Filipek A, Niewiadomska G (2014) Tau protein modifications and interactions: their role in function and dysfunction. Int J Mol Sci 15:4671–4713.  https://doi.org/10.3390/ijms15034671 CrossRefGoogle Scholar
  53. Miller DB, O'Callaghan JP (2008) Do early-life insults contribute to the late-life development of Parkinson and Alzheimer diseases? Metab Clin Exp 57(Suppl 2):S44–S49.  https://doi.org/10.1016/j.metabol.2008.07.011 CrossRefGoogle Scholar
  54. Muresan V, Ladescu Muresan Z (2016) Shared molecular mechanisms in Alzheimer’s disease and amyotrophic lateral sclerosis: neurofilament-dependent transport of sAPP, FUS, TDP-43 and SOD1, with endoplasmic reticulum-like tubules. Neurodegener Dis 16:55–61.  https://doi.org/10.1159/000439256 CrossRefGoogle Scholar
  55. Muresan V, Villegas C, Ladescu Muresan Z (2014) Functional interaction between amyloid-beta precursor protein and peripherin neurofilaments: a shared pathway leading to Alzheimer’s disease and amyotrophic lateral sclerosis? Neurodegener Dis 13:122–125.  https://doi.org/10.1159/000354238 CrossRefGoogle Scholar
  56. Mushtaq G, H. Greig N, Anwar F, A. Zamzami M, Choudhry H, M. Shaik M, A. Tamargo I, A. Kamal M (2016) miRNAs as circulating biomarkers for Alzheimer’s disease and Parkinson’s disease. Med Chem (Shariqah (United Arab Emirates)) 12:217–225CrossRefGoogle Scholar
  57. Negoita SI, Sandesc D, Rogobete A, Dutu M, Bedreag O, Papurica M, Ercisli M, Popovici S, Dumache R, Sandesc M, Dinu A, Sas A, Serban D, Corneci D (2017) miRNAs expressions and interaction with biological systems in patients with Alzheimer’s disease. In: Using miRNAs as a diagnosis and prognosis biomarker clinical laboratory, vol 63, pp 1315–1321.  https://doi.org/10.7754/Clin.Lab.2017.170327 Google Scholar
  58. Nogueira C, Erlmann P, Villeneuve J, Santos AJ, Martinez-Alonso E, Martinez-Menarguez JA, Malhotra V (2014) SLY1 and syntaxin 18 specify a distinct pathway for procollagen VII export from the endoplasmic reticulum eLife 3:e02784 doi: https://doi.org/10.7554/eLife.02784
  59. O'Brien RJ, Wong PC (2011) Amyloid precursor protein processing and Alzheimer’s disease. Annu Rev Neurosci 34:185–204.  https://doi.org/10.1146/annurev-neuro-061010-113613 CrossRefGoogle Scholar
  60. Parihar MS, Hemnani T (2004) Alzheimer’s disease pathogenesis and therapeutic interventions. J Clin Neurosci 11:456–467.  https://doi.org/10.1016/j.jocn.2003.12.007 CrossRefGoogle Scholar
  61. Pietrzak M, Rempala G, Nelson PT, Zheng JJ, Hetman M (2011) Epigenetic silencing of nucleolar rRNA genes in Alzheimer’s disease. PLoS One 6:e22585.  https://doi.org/10.1371/journal.pone.0022585 CrossRefGoogle Scholar
  62. Qiu C, Kivipelto M, von Strauss E (2009) Epidemiology of Alzheimer’s disease: occurrence, determinants, and strategies toward intervention. Dialogues Clin Neurosci 11:111–128Google Scholar
  63. Raghavan N, Tosto G (2017) Genetics of Alzheimer’s disease: the importance of polygenic and epistatic components. Curr Neurol Neurosci Rep 17:78.  https://doi.org/10.1007/s11910-017-0787-1 CrossRefGoogle Scholar
  64. Razgonova MP, Veselov V, Zakharenko A, Golokhvast K, Nosyrev A, Cravotto G, Tsatsakis A, Spandidos D (2019) Panax ginseng components and the pathogenesis of Alzheimer’s disease (review). Mol Med Rep.  https://doi.org/10.3892/mmr.2019.9972
  65. Roubroeks JAY, Smith RG, van den Hove DLA, Lunnon K (2017) Epigenetics and DNA methylomic profiling in Alzheimer’s disease and other neurodegenerative diseases. J Neurochem 143:158–170.  https://doi.org/10.1111/jnc.14148 CrossRefGoogle Scholar
  66. Scheltens P, Blennow K, Breteler MM, de Strooper B, Frisoni GB, Salloway S, Van der Flier WM (2016) Alzheimer’s disease. Lancet (London, England) 388:505–517.  https://doi.org/10.1016/s0140-6736(15)01124-1 CrossRefGoogle Scholar
  67. Sebastian-Serrano A, de Diego-Garcia L, Diaz-Hernandez M (2018) The neurotoxic role of extracellular tau protein. Int J Mol Sci 19.  https://doi.org/10.3390/ijms19040998
  68. Shao W, Peng D, Wang X (2017) Genetics of Alzheimer’s disease: from pathogenesis to clinical usage. J Clin Neurosci 45:1–8.  https://doi.org/10.1016/j.jocn.2017.06.074 CrossRefGoogle Scholar
  69. Sierra-Fonseca JA, Gosselink KL (2018) Tauopathy and neurodegeneration: a role for stress. Neurobiol Stress 9:105–112.  https://doi.org/10.1016/j.ynstr.2018.08.009 CrossRefGoogle Scholar
  70. Singh SK, Srivastav S, Yadav AK, Srikrishna S, Perry G (2016) Overview of Alzheimer’s disease and some therapeutic approaches targeting Aβ by using several synthetic and herbal compounds oxidative medicine and cellular longevity 2016:7361613–7361613  https://doi.org/10.1155/2016/7361613
  71. Siokas V, Kardaras D, Aloizou AM, Asproudis I, Boboridis KG, Papageorgiou E, Hadjigeorgiou GM, Tsironi EE, Dardiotis E (2018) BDNF rs6265 (Val66Met) polymorphism as a risk factor for blepharospasm. NeuroMolecular Med 21:68–74.  https://doi.org/10.1007/s12017-018-8519-5 CrossRefGoogle Scholar
  72. Siokas V et al (2019) Lack of association of the rs11655081 ARSG gene with blepharospasm. J Mol Neurosci.  https://doi.org/10.1007/s12031-018-1255-3
  73. Skol AD, Scott LJ, Abecasis GR, Boehnke M (2006) Joint analysis is more efficient than replication-based analysis for two-stage genome-wide association studies. Nat Genet 38:209–213.  https://doi.org/10.1038/ng1706 CrossRefGoogle Scholar
  74. Sole X, Guino E, Valls J, Iniesta R, Moreno V (2006) SNPStats: a web tool for the analysis of association studies. Bioinformatics (Oxford, England) 22:1928–1929.  https://doi.org/10.1093/bioinformatics/btl268 CrossRefGoogle Scholar
  75. Theuns J, Verstraeten A, Sleegers K, Wauters E, Gijselinck I, Smolders S, Crosiers D, Corsmit E, Elinck E, Sharma M, Kruger R, Lesage S, Brice A, Chung SJ, Kim MJ, Kim YJ, Ross OA, Wszolek ZK, Rogaeva E, Xi Z, Lang AE, Klein C, Weissbach A, Mellick GD, Silburn PA, Hadjigeorgiou GM, Dardiotis E, Hattori N, Ogaki K, Tan EK, Zhao Y, Aasly J, Valente EM, Petrucci S, Annesi G, Quattrone A, Ferrarese C, Brighina L, Deutschlander A, Puschmann A, Nilsson C, Garraux G, LeDoux MS, Pfeiffer RF, Boczarska-Jedynak M, Opala G, Maraganore DM, Engelborghs S, de Deyn PP, Cras P, Cruts M, van Broeckhoven C, on behalf of the GEO-PD Consortium (2014) Global investigation and meta-analysis of the C9orf72 (G4C2)n repeat in Parkinson disease. Neurology 83:1906–1913.  https://doi.org/10.1212/wnl.0000000000001012 CrossRefGoogle Scholar
  76. Tohgi H, Utsugisawa K, Nagane Y, Yoshimura M, Genda Y, Ukitsu M (1999a) Reduction with age in methylcytosine in the promoter region -224 approximately -101 of the amyloid precursor protein gene in autopsy human cortex brain research. Mol Brain Res 70:288–292CrossRefGoogle Scholar
  77. Tohgi H, Utsugisawa K, Nagane Y, Yoshimura M, Ukitsu M, Genda Y (1999b) The methylation status of cytosines in a tau gene promoter region alters with age to downregulate transcriptional activity in human cerebral cortex. Neurosci Lett 275:89–92CrossRefGoogle Scholar
  78. Tosun D, Landau S, Aisen PS, Petersen RC, Mintun M, Jagust W, Weiner MW (2017) Association between tau deposition and antecedent amyloid-beta accumulation rates in normal and early symptomatic individuals. Brain 140:1499–1512.  https://doi.org/10.1093/brain/awx046 CrossRefGoogle Scholar
  79. Van Cauwenberghe C, Van Broeckhoven C, Sleegers K (2016) The genetic landscape of Alzheimer disease: clinical implications and perspectives. Genet Med 18:421–430.  https://doi.org/10.1038/gim.2015.117 CrossRefGoogle Scholar
  80. Wang SC, Oelze B, Schumacher A (2008) Age-specific epigenetic drift in late-onset Alzheimer’s disease. PLoS One 3:e2698.  https://doi.org/10.1371/journal.pone.0002698 CrossRefGoogle Scholar
  81. Wang J, Yu JT, Tan MS, Jiang T, Tan L (2013) Epigenetic mechanisms in Alzheimer’s disease: implications for pathogenesis and therapy. Ageing Res Rev 12:1024–1041.  https://doi.org/10.1016/j.arr.2013.05.003 CrossRefGoogle Scholar
  82. Xie B, Liu Z, Liu W, Jiang L, Zhang R, Cui D, Zhang Q, Xu S (2017) DNA methylation and tag SNPs of the BDNF gene in conversion of amnestic mild cognitive impairment into Alzheimer’s disease: a cross-sectional cohort study. J Alzheimer's Dis 58:263–274.  https://doi.org/10.3233/jad-170007 CrossRefGoogle Scholar
  83. Yamaguchi T, Dulubova I, Min SW, Chen X, Rizo J, Sudhof TC (2002) Sly1 binds to Golgi and ER syntaxins via a conserved N-terminal peptide motif. Dev Cell 2:295–305CrossRefGoogle Scholar
  84. Zaganas I, Kapetanaki S, Mastorodemos V, Kanavouras K, Colosio C, Wilks MF, Tsatsakis AM (2013) Linking pesticide exposure and dementia: what is the evidence? Toxicology 307:3–11.  https://doi.org/10.1016/j.tox.2013.02.002 CrossRefGoogle Scholar
  85. Zhou XW, Gustafsson JA, Tanila H, Bjorkdahl C, Liu R, Winblad B, Pei JJ (2008) Tau hyperphosphorylation correlates with reduced methylation of protein phosphatase 2A. Neurobiol Dis 31:386–394.  https://doi.org/10.1016/j.nbd.2008.05.013 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Polyxeni Stamati
    • 1
  • Vasileios Siokas
    • 1
  • Athina-Maria Aloizou
    • 1
  • Emmanouil Karampinis
    • 1
  • Stylianos Arseniou
    • 1
  • Valerii N. Rakitskii
    • 2
  • Aristidis Tsatsakis
    • 3
  • Demetrios A. Spandidos
    • 4
  • Illana Gozes
    • 5
  • Panayiotis D. Mitsias
    • 6
  • Dimitrios P. Bogdanos
    • 7
    • 8
  • Georgios M. Hadjigeorgiou
    • 1
    • 9
  • Efthimios Dardiotis
    • 1
    Email author
  1. 1.Department of Neurology, Laboratory of Neurogenetics, University of ThessalyUniversity Hospital of LarissaLarissaGreece
  2. 2.The Federal Budgetary Establishment of Science “Federal Scientific Center of Hygiene named after F. F. Erisman” of the Federal Service for Surveillance on Consumer Rights Protection and Human WellbeingMytishchiRussian Federation
  3. 3.Laboratory of Toxicology, School of MedicineUniversity of CreteHeraklionGreece
  4. 4.Laboratory of Clinical Virology, Medical SchoolUniversity of CreteHeraklionGreece
  5. 5.The Lily and Avraham Gildor Chair for the Investigation of Growth Factors, The Elton Laboratory for Molecular Neuroendocrinology, Department of Human Molecular Genetics and Biochemistry, Sackler Faculty of Medicine, Sagol School of Neuroscience and Adams Super Center for Brain StudiesTel Aviv UniversityTel AvivIsrael
  6. 6.Department of Neurology, School of MedicineUniversity of CreteHeraklionGreece
  7. 7.Department of Rheumatology and Clinical Immunology, University General Hospital of Larissa, Faculty of Medicine, School of Health SciencesUniversity of ThessalyLarissaGreece
  8. 8.Cellular Immunotherapy & Molecular Immunodiagnostics, Biomedical SectionCentre for Research and Technology-Hellas (CERTH)-Institute for Research and Technology-Thessaly (IRETETH)LarissaGreece
  9. 9.Department of Neurology, Medical SchoolUniversity of CyprusNicosiaCyprus

Personalised recommendations