Regulatory region genetic variation is associated with FYN expression in Alzheimer's disease

Neurobiology of Aging

Volumn 51, Issue , 2017, Pages 43-53

  Zahratka, Jeffrey A ^a   Shao, Yvonne ^a   Shaw, McKenzie ^a   Todd, Kaitlin ^a   Formica, Shane V ^a   Khrestian, Maria ^a   Montine, Thomas ^b   Leverenz, James B ^a   Bekris, Lynn M ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Cerebellum; Fyn; Hippocampus; Reporter assay; SNP

Indexed keywords

MESSENGER RNA; PROTEIN KINASE FYN; 3' UNTRANSLATED REGION; FYN PROTEIN, HUMAN; TAU PROTEIN;

3' UNTRANSLATED REGION; AGED; ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; FEMALE; FYN GENE; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENETIC VARIATION; GENOTYPE; HAPLOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNODETECTION; IMMUNOHISTOCHEMISTRY; MALE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; VERY ELDERLY; WESTERN BLOTTING; BRAIN; CELL LINE; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; PHOSPHORYLATION; REGULATORY SEQUENCE;

3' UNTRANSLATED REGIONS; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BRAIN; CELL LINE; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; HAPLOTYPES; HUMANS; MALE; PHOSPHORYLATION; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEINS C-FYN; REGULATORY SEQUENCES, NUCLEIC ACID; TAU PROTEINS;

EID: 85007043459     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2016.11.001     Document Type: Article

References (56)

1. Abràmoff, M.D., Magalhães, P.J., Ram, S.J., Image processing with imageJ. Biophotonics Int. 11 (2004), 36–41.
2. Allen, M., Kachadoorian, M., Quicksall, Z., Zou, F., Chai, H.S., Younkin, C., Crook, J.E., Pankratz, V.S., Carrasquillo, M.M., Krishnan, S., Nguyen, T., Li, M., Malphrus, K., Lincoln, S., Bisceglio, G., Kolbert, C.P., Jin, J., Mukherjee, S., Kauwe, J.K., Crane, P.K., Haines, J.L., Mayeux., Pericak-Vance, M.A., Farrer, L.A., Schellenberg, G.D., Alzheimer's Disease Genetics Consortium, Parisi, J.E., Petersen, R.C., Graff-Radford, N.R., Dickson, D.W., Younkin, S.G., Ertekin-Taner, N., Association of MAPT haplotypes with Alzheimer's disease risk and MAPT brain gene expression levels. Alzheimers Res. Ther., 6, 2014, 39.
3. Ash, P.E.A., Vanderweyde, T.E., Youmans, K.L., Apicco, D.J., Wolozin, B., Pathological stress granules in Alzheimer's disease. Brain Res. 1584 (2014), 1–7.
4. Bekris, L.M., Lutz, F., Li, G., Galasko, D.R., Farlow, M.R., Quinn, J.F., Kaye, J.A., Leverenz, J.B., Tsuang, D.W., Montine, T.J., Peskind, E.R., Yu, C-E., ADAM10 expression and promoter haplotype in Alzheimer's disease. Neurobiol. Aging 33 (2012), 2229.e1–2229.e9.
5. Bekris, L.M., Millard, S., Lutz, F., Li, G., Galasko, D.R., Farlow, M.R., Quinn, J.F., Kaye, J.A., Leverenz, J.B., Tsuang, D.W., Yu, C.-E., Peskind, E.R., Tau phosphorylation pathway genes and cerebrospinal fluid tau levels in Alzheimer's disease. Am. J. Med. Genet. B Neuropsychiatr. Genet. 159B (2012), 874–883.
6. Bekris, L.M., Millard, S.P., Galloway, N.M., Vuletic, S., Albers, J.J., Li, G., Galasko, D.R., DeCarli, C., Farlow, M.R., Clark, C.M., Quinn, J.F., Kaye, J.A., Schellenberg, G.D., Tsuang, D.W., Peskind, E.R., Yu, C.-E., Multiple SNPs within and surrounding the apolipoprotein E gene influence cerebrospinal fluid apolipoprotein E protein levels. J. Alzheimers Dis. 13 (2008), 255–266.
7. Bekris, L.M., Yu, C.-E., Bird, T.D., Tsuang, D.W., Genetics of Alzheimer disease. J. Geriatr. Psychiatry Neurol. 23 (2010), 213–227.
8. Boehm, J., A “danse macabre”: tau and Fyn in STEP with amyloid beta to facilitate induction of synaptic depression and excitotoxicity. Eur. J. Neurosci. 37 (2013), 1925–1930.
9. Braak, H., Braak, E., Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82 (1991), 239–259.
10. Challenor, M., O'Hare Doig, R., Fuller, P., Giacci, M., Bartlett, C., Wale, C.H., Cozens, G.S., Hool, L., Dunlop, S., Swaminathan Iyer, K., Rodger, J., Fitzgerald, M., Prolonged glutamate excitotoxicity increases GluR1 immunoreactivity but decreases mRNA of GluR1 and associated regulatory proteins in dissociated rat retinae in vitro. Biochimie 112 (2015), 160–171.
11. Chin, J., Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer's disease. J. Neurosci. 25 (2005), 9694–9703.
12. Chun, J.T., Crispino, M., Tocco, G., The dual response of protein kinase Fyn to neural trauma: early induction in neurons and delayed induction in reactive astrocytes. Exp. Neurol. 185 (2004), 109–119.
13. Davidson, D., Chow, L.M., Fournel, M., Veillette, A., Differential regulation of T cell antigen responsiveness by isoforms of the src-related tyrosine protein kinase p59fyn. J. Exp. Med. 175 (1992), 1483–1492.
14. Davidson, D., Viallet, J., Veillette, A., Unique catalytic properties dictate the enhanced function of p59fynT, the hemopoietic cell-specific isoform of the Fyn tyrosine protein kinase, in T cells. Mol. Cell Biol. 14 (1994), 4554–4564.
15. Delay, C., Calon, F., Mathews, P., Hébert, S.S., Alzheimer-specific variants in the 3′UTR of amyloid precursor protein affect microRNA function. Mol. Neurodegener., 6, 2011, 70.
16. Du, C.-P., Tan, R., Hou, X.-Y., Fyn kinases play a critical role in neuronal apoptosis induced by oxygen and glucose deprivation or amyloid-β peptide treatment. CNS Neurosci. Ther. 18 (2012), 754–761.
17. Duka, V., Lee, J.H., Credle, J., Wills, J., Oaks, A., Smolinsky, C., Shah, K., Mash, D.C., Masliah, E., Sidhu, A., Identification of the sites of tau hyperphosphorylation and activation of tau kinases in synucleinopathies and Alzheimer's diseases. PLoS One, 8, 2013, e75025.
18. Gao, Y., Howard, A., Ban, K., Chandra, J., Oxidative stress promotes transcriptional up-regulation of Fyn in BCR-ABL1-expressing cells. J. Biol. Chem. 284 (2009), 7114–7125.
19. Goldsmith, J.F., Hall, C.G., Atkinson, T.P., Identification of an alternatively spliced isoform of the fyn tyrosine kinase. Biochem. Biophys. Res. Commun. 298 (2002), 501–504.
20. Grossman, H., Chuderland, D., Ninio-Many, L., Hasky, N., Kaplan-Kraicer, R., Shalgi, R., A novel regulatory pathway in granulosa cells, the LH/human chorionic gonadotropin-microRNA-125a-3p-Fyn pathway, is required for ovulation. FASEB J. 29 (2015), 3206–3216.
21. Haas, L.T., Strittmatter, S.M., Oligomers of amyloid-beta prevent physiological activation of the cellular prion protein-metabotropic glutamate receptor 5 complex by glutamate in Alzheimer′s disease. J. Biol. Chem. 291 (2016), 17112–171121.
22. Huang, Y., Wu, Z., Zhou, B., Behind the curtain of tauopathy: a show of multiple players orchestrating tau toxicity. Cell Mol. Life Sci. 73 (2016), 1–21.
23. Hughes, R., Gilley, J., Kristiansen, M., Ham, J., The MEK-ERK pathway negatively regulates bim expression through the 3′UTR in sympathetic neurons. BMC Neurosci., 12, 2011, 69.
24. Iqbal, K., Liu, F., Gong, C.-X., Tau and neurodegenerative disease: the story so far. Nat. Rev. Neurol. 12 (2015), 1–14.
25. Jayapalan, S., Natarajan, J., The role of CDK5 and GSK3B kinases in hyperphosphorylation of microtubule associated protein tau (MAPT) in Alzheimer's disease. Bioinformation 9 (2013), 1023–1030.
26. Kaufman, A.C., Salazar, S.V., Haas, L.T., Yang, J., Kostylev, M.A., Jeng, A.T., Robinson, S.A., Gunther, E.C., van Dyck, C.H., Nygaard, H.B., Strittmatter, S.M., Fyn inhibition rescues established memory and synapse loss in Alzheimer mice. Ann. Neurol. 77 (2015), 953–971.
27. Ko, H.M., Lee, S.H., Kim, K.C., Joo, S.H., Choi, W.S., Shin, C.Y., The role of TLR4 and fyn interaction on lipopolysaccharide-stimulated PAI-1 expression in astrocytes. Mol. Neurobiol. 52 (2015), 8–25.
28. Krüger, L., Mandelkow, E.M., Tau neurotoxicity and rescue in animal models of human tauopathies. Curr. Opin. Neurobiol. 36 (2016), 52–58.
29. Larson, M., Sherman, M.A., Amar, F., Nuvolone, M., Schneider, J.A., Bennett, D.A., Aguzzi, A., Lesné, S.E., The complex PrP(c)-Fyn couples human oligomeric Aβ with pathological tau changes in Alzheimer's disease. J. Neurosci. 32 (2012), 16857–16871a.
30. Le Cam, A., Legraverend, C., Transcriptional repression, a novel function for 3' untranslated regions. Eur. J. Biochem. 231 (1995), 620–627.
31. Lee, C., Kim, M.G., Jeon, S.H., Park, D.E., Park, S.D., Seong, R.H., Two species of mRNAs for the fyn proto-oncogene are produced by an alternative polyadenylation. Mol. Cells 8 (1998), 746–749.
32. Lee, C., Low, C.Y.B., Francis, P.T., Attems, J., Wong, P.T.H., Lai, M.K.P., Tan, M.G.K., An isoform-specific role of FynT tyrosine kinase in Alzheimer's disease. J. Neurochem. 136 (2016), 637–650.
33. Lee, G., Thangavel, R., Sharma, V.M., Litersky, J.M., Bhaskar, K., Fang, S.M., Do, L.H., Andreadis, A., Van Hoesen, G., Ksiezak-Reding, H., Phosphorylation of tau by fyn: implications for Alzheimer's disease. J. Neurosci. 24 (2004), 2304–2312.
34. Liao, J., Yang, T.T., Weng, R.R., Kuo, C., Chang, C., TTBK2: a tau protein kinase beyond tau phosphorylation. Biomed. Res. Int. 2015 (2015), 1–10.
35. Mandelkow, E.-M., MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J. Cell Biol. 167 (2004), 99–110.
36. Matthews, A.G., Haynes, C., Liu, C., Ott, J., Collapsing SNP genotypes in case-control genome-wide association studies increases the type I error rate and power. Stat. Appl. Genet. Mol. Biol., 7, 2008, 1325.
37. Ninio-Many, L., Grossman, H., Shomron, N., Chuderland, D., Shalgi, R., microRNA-125a-3p reduces cell proliferation and migration by targeting Fyn. J. Cell Sci. 126 (2013), 2867–2876.
38. Nisbet, R.M., Polanco, J.-C., Ittner, L.M., Götz, J., Tau aggregation and its interplay with amyloid-β. Acta Neuropathol. 129 (2014), 207–220.
39. Nygaard, H.B., van Dyck, C.H., Strittmatter, S.M., Fyn kinase inhibition as a novel therapy for Alzheimer's disease. Alzheimers Res. Ther., 6, 2014, 8.
40. Ogbourne, S., Antalis, T.M., Transcriptional control and the role of silencers in transcriptional regulation in eukaryotes. Biochem. J. 331 (1998), 1–14.
41. Peckham, H., Giuffrida, L., Wood, R., Gonsalvez, D., Ferner, A., Kilpatrick, T.J., Murray, S.S., Xiao, J., Fyn is an intermediate kinase that BDNF utilizes to promote oligodendrocyte myelination. Glia 64 (2016), 255–269.
42. Resh, M.D., Fyn, a Src family tyrosine kinase. Int. J. Biochem. Cell Biol. 30 (1998), 1159–1162.
43. Roberson, E.D., Halabisky, B., Yoo, J.W., Yao, J., Chin, J., Yan, F., Wu, T., Hamto, P., Devidze, N., Yu, G.-Q., Palop, J.J., Noebels, J.L., Mucke, L., Amyloid-β/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. J. Neurosci. 31 (2011), 700–711.
44. Rosenbloom, K.R., Armstrong, J., Barber, G.P., Casper, J., Clawson, H., Diekhans, M., Dreszer, T.R., Fujita, P.A., Guruvadoo, L., Haeussler, M., Harte, R.A., Heitner, S., Hickey, G., Hinrichs, A.S., Hubley, R., Karolchik, D., Learned, K., Lee, B.T., Li, C.H., Miga, K.H., Nguyen, N., Paten, B., Raney, B.J., Smit, A.F.A., Speir, M.L., Zweig, A.S., Haussler, D., Kuhn, R.M., Kent, W.J., The UCSC Genome Browser database: 2015 update. Nucleic Acids Res. 43 (2015), D670–D681.
45. Rosenbloom, K.R., Sloan, C.A., Malladi, V.S., Dreszer, T.R., Learned, K., Kirkup, V.M., Wong, M.C., Maddren, M., Fang, R., Heitner, S.G., Lee, B.T., Barber, G.P., Harte, R.A., Diekhans, M., Long, J.C., Wilder, S.P., Zweig, A.S., Karolchik, D., Kuhn, R.M., Haussler, D., Kent, W.J., ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res. 41 (2013), D56–D63.
46. Sato-Harada, R., Okabe, S., Umeyama, T., Kanai, Y., Hirokawa, N., Microtubule-associated proteins regulate microtubule function as the track for intracellular membrane organelle transports. Cell Struct. Funct. 21 (1996), 283–295.
47. Shanley, M.R., Hawley, D., Leung, S., Zaidi, N.F., Dave, R., Schlosser, K.A., Bandopadhyay, R., Gerber, S.A., Liu, M., LRRK2 facilitates tau phosphorylation through strong interaction with tau and cdk5. Biochemistry 54 (2015), 5198–5208.
48. Sontag, J.M., Nunbhakdi-Craig, V., White, C.L., Halpain, S., Sontag, E., The protein phosphatase PP2A/Bα binds to the microtubule-associated proteins Tau and MAP2 at a motif also recognized by the kinase Fyn: implications for tauopathies. J. Biol. Chem. 287 (2012), 14984–14993.
49. Tenreiro, S., Eckermann, K., Outeiro, T.F., Protein phosphorylation in neurodegeneration: friend or foe?. Front. Mol. Neurosci. 7 (2014), 1–30.
50. Trepanier, C.H., Jackson, M.F., MacDonald, J.F., Regulation of NMDA receptors by the tyrosine kinase Fyn. FEBS J. 279 (2012), 12–19.
51. Um, J.W., Kaufman, A.C., Kostylev, M., Heiss, J.K., Stagi, M., Takahashi, H., Kerrisk, M.E., Vortmeyer, A., Wisniewski, T., Koleske, A.J., Gunther, E.C., Nygaard, H.B., Strittmatter, S.M., Metabotropic glutamate receptor 5 is a coreceptor for alzheimer Aβ oligomer bound to cellular prion protein. Neuron 79 (2013), 887–902.
52. Um, J.W., Nygaard, H.B., Heiss, J.K., Kostylev, M.A., Stagi, M., Vortmeyer, A., Wisniewski, T., Gunther, E.C., Strittmatter, S.M., Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat. Neurosci. 15 (2012), 1227–1235.
53. Vanderweyde, T., Yu, H., Varnum, M., Liu-Yesucevitz, L., Citro, A., Ikezu, T., Duff, K., Wolozin, B., Contrasting pathology of the stress granule proteins TIA-1 and G3BP in tauopathies. J. Neurosci. 32 (2012), 8270–8283.
54. Xia, D., Li, C., Götz, J., Pseudophosphorylation of Tau at distinct epitopes or the presence of the P301L mutation targets the microtubule-associated protein Tau to dendritic spines. Biochim. Biophys. Acta 1852 (2015), 913–924.
55. Xu, J., Chatterjee, M., Baguley, T.D., Brouillette, J., Kurup, P., Ghosh, D., Kanyo, J., Zhang, Y., Seyb, K., Ononenyi, C., Foscue, E., Anderson, G.M., Gresack, J., Cuny, G.D., Glicksman, M.A., Greengard, P., Lam, T.T., Tautz, L., Nairn, A.C., Ellman, J.A., Lombroso, P.J., Inhibitor of the tyrosine phosphatase step reverses cognitive deficits in a mouse model of Alzheimer's disease. PLoS Biol., 12, 2014, e1001923.
56. Yang, K., Belrose, J., Trepanier, C.H., Lei, G., Jackson, M.F., MacDonald, J.F., Fyn, a potential target for Alzheimer's disease. J. Alzheimers Dis. 27 (2011), 243–252.