Publications

Baliga N.S., Bjorkegren J.L., Boeke J.D., Boutros M., Crawford N.P., Dudley A.M., Farber C.R., Jones A., Levey A.I., Lusis A.J., Mak H.C., Nadeau J.H., Noyes M.B., Petretto E., Seyfried N.T., Steinmetz L.M. and Vonesch S.C. (2017). The State of Systems Genetics in 2017. Cell Syst 4: 7-15.

Rangaraju S., Raza S.A., Pennati A., Deng Q., Dammer E.B., Duong D., Pennington M.W., Tansey M.G., Lah J.J., Betarbet R., Seyfried N.T. and Levey A.I. (2017). A systems pharmacology-based approach to identify novel Kv1.3 channel-dependent mechanisms in microglial activation. J Neuroinflammation 14: 128.

Rha J., Jones S.K., Fidler J., Banerjee A., Leung S.W., Morris K.J., Wong J.C., Inglis G.A.S., Shapiro L., Deng Q., Cutler A.A., Hanif A.M., Pardue M.T., Schaffer A., Seyfried N.T., Moberg K.H., Bassell G.J., Escayg A., Garcia P.S. and Corbett A.H. (2017). The RNA-binding Protein, ZC3H14, is Required for Proper Poly(A) Tail Length Control, Expression of Synaptic Proteins, and Brain Function in Mice. Hum Mol Genet.

Zhang Z., Kang S.S., Liu X., Ahn E.H., Zhang Z., He L., Iuvone P.M., Duong D.M., Seyfried N.T., Benskey M.J., Manfredsson F.P., Jin L., Sun Y.E., Wang J.Z. and Ye K. (2017). Asparagine endopeptidase cleaves alpha-synuclein and mediates pathologic activities in Parkinson's disease. Nat Struct Mol Biol.

Wingo T.S., Duong D.M., Zhou M., Dammer E.B., Wu H., Cutler D.J., Lah J.J., Levey A.I., and Seyfried N.T. (2017). Integrating next-generation genomic sequencing and mass spectrometry to identify variant peptides in human brain. Accepted at J. Proteome Res.

Diner I., Nguyen T., and Seyfried N.T. (2017). Enrichment of Detergent-insoluble Protein Aggregates from Human Postmortem Brain. Accepted to Journal of Visual Experimentation (JoVE).

Ivanova A.A., Caspary T., Seyfried N.T., Duong D.M., West A.B., Liu Z. and Kahn R.A. (2017). Biochemical characterization of purified mammalian ARL13B indicate that it is an atypical GTPase and ARL3 guanine nucleotide exchange factor (GEF). J Biol Chem.

Li Y., Dammer E.B., Zhang-Brotzge X., Chen S., Duong D.M., Seyfried N.T., Kuan C.Y. and Sun Y.Y. (2017). Osteopontin Is a Blood Biomarker for Microglial Activation and Brain Injury in Experimental Hypoxic-Ischemic Encephalopathy. eNeuro 4.

Seyfried N.T.*, Dammer E.B., Swarup V., Nandakumar D., Duong D.M., Yin L., Deng Q., Nguyen T., Hales C.M., Wingo T., Glass J., Gearing M., Thambisetty M., Troncoso J.C., Geschwind D.H., Lah J.J. and Levey A.I. (2017). A Multi-network Approach Identifies Protein-Specific Co-expression in Asymptomatic and Symptomatic Alzheimer's Disease. Cell Syst 4: 60-72 e64. * co-corresponding author and lead contact author.

Varma V.R., Varma S., An Y., Hohman T.J., Seddighi S., Casanova R., Beri A., Dammer E.B., Seyfried N.T., Pletnikova O., Moghekar A., Wilson M.R., Lah J.J., O'Brien R.J., Levey A.I., Troncoso J.C., Albert M.S. and Thambisetty M. (2017). Alpha-2 macroglobulin in Alzheimer's disease: a marker of neuronal injury through the RCAN1 pathway. Mol Psychiatry 22: 13-23.

Cutler AA, Dammer EB, Doung DM, Seyfried NT, Corbett AH, Pavlath GK. (2017). Biochemical isolation of myonuclei employed to define changes to the myonuclear proteome that occur with aging. Aging Cell. May 23. doi: 10.1111/acel.12604.

Hales C.M., Dammer E.B., Deng Q., Duong D.M., Gearing M., Troncoso J.C., Thambisetty M., Lah J.J., Shulman J.M., Levey A.I. and Seyfried N.T. (2016). Changes in the detergent-insoluble brain proteome linked to amyloid and tau in Alzheimer's Disease progression. Proteomics 16: 3042-3053.

Hu W.T., Watts K.D., Tailor P., Nguyen T.P., Howell J.C., Lee R.C., Seyfried N.T., Gearing M., Hales C.M., Levey A.I., Lah J.J., Lee E.K. and Alzheimer's Disease Neuro-Imaging I. (2016). CSF complement 3 and factor H are staging biomarkers in Alzheimer's disease. Acta Neuropathol Commun 4: 14.

Kudelka M.R., Antonopoulos A., Wang Y., Duong D.M., Song X., Seyfried N.T., Dell A., Haslam S.M., Cummings R.D. and Ju T. (2016). Cellular O-Glycome Reporter/Amplification to explore O-glycans of living cells. Nat Methods 13: 81-86. 

Owings J.P., Kuiper E.G., Prezioso S.M., Meisner J., Varga J.J., Zelinskaya N., Dammer E.B., Duong D.M., Seyfried N.T., Alberti S., Conn G.L. and Goldberg J.B. (2016). Pseudomonas aeruginosa EftM Is a Thermoregulated Methyltransferase. J Biol Chem 291: 3280-3290.

Soucek S., Zeng Y., Bellur D.L., Bergkessel M., Morris K.J., Deng Q., Duong D., Seyfried N.T., Guthrie C., Staley J.P., Fasken M.B. and Corbett A.H. (2016). The Evolutionarily-conserved Polyadenosine RNA Binding Protein, Nab2, Cooperates with Splicing Machinery to Regulate the Fate of pre-mRNA. Mol Cell Biol.

Zhang H., Head P.E., Daddacha W., Park S.H., Li X., Pan Y., Madden M.Z., Duong D.M., Xie M., Yu B., Warren M.D., Liu E.A., Dhere V.R., Li C., Pradilla I., Torres M.A., Wang Y., Dynan W.S., Doetsch P.W., Deng X., Seyfried N.T., Gius D. and Yu D.S. (2016). ATRIP Deacetylation by SIRT2 Drives ATR Checkpoint Activation by Promoting Binding to RPA-ssDNA. Cell Rep 14: 1435-1447.

Zhang Z, Song M, Liu X, Su Kang S, Duong DM, Seyfried NT, Cao X, Cheng L, Sun YE, Ping Yu S, Jia J, Levey AI, Ye K. Delta-secretase cleaves amyloid precursor protein and regulates the pathogenesis in Alzheimer's disease. Nat Commun. 2015 Nov 9;6:8762. doi: 10.1038/ncomms9762. PubMed PMID: 26549211

Dammer EB, Göttle M, Duong DM, Hanfelt J, Seyfried NT, Jinnah HA. Consequences of impaired purine recycling on the proteome in a cellular model of Lesch-Nyhan disease. Mol Genet Metab. 2015 Apr;114(4):570-9. doi: 10.1016/j.ymgme.2015.02.007. Epub 2015 Mar 5. PubMed PMID: 25769394; PubMed Central PMCID: PMC4390545.

Yang Q, Li W, She H, Dou J, Duong DM, Du Y, Yang SH, Seyfried NT, Fu H, Gao G, Mao Z. Stress induces p38 MAPK-mediated phosphorylation and inhibition of Drosha-dependent cell survival. Mol Cell. 2015 Feb 19;57(4):721-34. doi: 10.1016/j.molcel.2015.01.004. PubMed PMID: 25699712

Dammer EB, Lee AK, Duong DM, Gearing M, Lah JJ, Levey AI, Seyfried NT. Quantitative phosphoproteomics of Alzheimer's disease reveals cross-talk between kinases and small heat shock proteins. Proteomics. 2015 Jan;15(2-3):508-19. doi: 10.1002/pmic.201400189. Epub 2014 Dec 17. PubMed PMID: 25332170

Jin L, Li D, Alesi GN, Fan J, Kang HB, Lu Z, Boggon TJ, Jin P, Yi H, Wright ER, Duong D, Seyfried NT, Egnatchik R, DeBerardinis RJ, Magliocca KR, He C, Arellano ML, Khoury HJ, Shin DM, Khuri FR, Kang S. Glutamate dehydrogenase 1 signals through antioxidant glutathione peroxidase 1 to regulate redox homeostasis and tumor growth. Cancer Cell. 2015 Feb 9;27(2):257-70. doi: 10.1016/j.ccell.2014.12.006. PubMed PMID: 25670081

Ren RJ, Dammer EB, Wang G, Seyfried NT, Levey AI. Proteomics of protein post-translational modifications implicated in neurodegeneration. Transl Neurodegener. 2014 Oct 30;3(1):23. doi: 10.1186/2047-9158-3-23. eCollection 2014. PubMed PMID: 25671099

Diner I, Hales CM, Bishof I, Rabenold L, Duong DM, Yi H, Laur O, Gearing M, Troncoso J, Thambisetty M, Lah JJ, Levey AI, Seyfried NT. Aggregation properties of the small nuclear ribonucleoprotein U1-70K in Alzheimer disease. J Biol Chem. 2014 Dec 19;289(51):35296-313. doi: 10.1074/jbc.M114.562959. Epub 2014 Oct 29. PubMed PMID: 25355317

Zhang Z, Song M, Liu X, Kang SS, Kwon IS, Duong DM, Seyfried NT, Hu WT, LiuZ, Wang JZ, Cheng L, Sun YE, Yu SP, Levey AI, Ye K. Cleavage of tau by asparagine endopeptidase mediates the neurofibrillary pathology in Alzheimer's disease. Nat Med. 2014 Nov;20(11):1254-62. doi: 10.1038/nm.3700. Epub 2014 Oct 19. PubMed PMID: 25326800

Ali M, Chernova TA, Newnam GP, Yin L, Shanks J, Karpova TS, Lee A, Laur O, Subramanian S, Kim D, McNally JG, Seyfried NT, Chernoff YO, Wilkinson KD. Stress-dependent proteolytic processing of the actin assembly protein Lsb1 modulates a yeast prion. J Biol Chem. 2014 Oct 3;289(40):27625-39. doi: 10.1074/jbc.M114.582429. Epub 2014 Aug 20. PubMed PMID: 25143386.

Deng Q, Holler CJ, Taylor G, Hudson KF, Watkins W, Gearing M, Ito D, Murray ME, Dickson DW, Seyfried NT, Kukar T. FUS is phosphorylated by DNA-PK and accumulates in the cytoplasm after DNA damage. J Neurosci. 2014 Jun 4;34(23):7802-13. doi: 10.1523/JNEUROSCI.0172-14.2014. PubMed PMID: 24899704

Hales CM, Seyfried NT, Dammer EB, Duong D, Yi H, Gearing M, Troncoso JC, Mufson EJ, Thambisetty M, Levey AI, Lah JJ. U1 small nuclear ribonucleoproteins (snRNPs) aggregate in Alzheimer's disease due to autosomal dominant genetic mutations and trisomy 21. Mol Neurodegener. 2014 Apr 28;9:15. doi: 10.1186/1750-1326-9-15. PubMed PMID: 24773620

Hales CM, Dammer EB, Diner I, Yi H, Seyfried NT, Gearing M, Glass JD, Montine TJ, Levey AI, Lah JJ. Aggregates of small nuclear ribonucleic acids (snRNAs) in Alzheimer's disease. Brain Pathol. 2014 Jul;24(4):344-51. doi: 10.1111/bpa.12133. Epub 2014 Apr 14. PubMed PMID: 24571648

Herskowitz JH, Feng Y, Mattheyses AL, Hales CM, Higginbotham LA, Duong DM, Montine TJ, Troncoso JC, Thambisetty M, Seyfried NT, Levey AI, Lah JJ. Pharmacologic inhibition of ROCK2 suppresses amyloid-β production in an Alzheimer's disease mouse model. J Neurosci. 2013 Dec 4;33(49):19086-98. doi:10.1523/JNEUROSCI.2508-13.2013. PubMed PMID: 24305806.

Hales CM, Rees H, Seyfried NT, Dammer EB, Duong DM, Gearing M, Montine TJ, Troncoso JC, Thambisetty M, Levey AI, Lah JJ, Wingo TS. Abnormal gephyrin immunoreactivity associated with Alzheimer disease pathologic changes. J Neuropathol Exp Neurol. 2013 Nov;72(11):1009-15. doi: 10.1097/01.jnen.0000435847.59828.db. PubMed PMID: 24128675.

Bai B, Hales CM, Chen PC, Gozal Y, Dammer EB, Fritz JJ, Wang X, Xia Q, Duong DM, Street C, Cantero G, Cheng D, Jones DR, Wu Z, Li Y, Diner I, Heilman CJ, Rees HD, Wu H, Lin L, Szulwach KE, Gearing M, Mufson EJ, Bennett DA, Montine TJ, Seyfried NT, Wingo TS, Sun YE, Jin P, Hanfelt J, Willcock DM, Levey A, Lah JJ, Peng J. U1 small nuclear ribonucleoprotein complex and RNA splicing alterations in Alzheimer's disease. Proc Natl Acad Sci U S A. 2013 Oct 8;110(41):16562-7. doi: 10.1073/pnas.1310249110. Epub 2013 Sep 10. PubMed PMID: 24023061

Go YM, Roede JR, Walker DI, Duong DM, Seyfried NT, Orr M, Liang Y, Pennell KD, Jones DP. Selective targeting of the cysteine proteome by thioredoxin and glutathione redox systems. Mol Cell Proteomics. 2013 Nov;12(11):3285-96. doi: 10.1074/mcp.M113.030437. Epub 2013 Aug 14. PubMed PMID: 23946468.

Zhang H, Park SH, Pantazides BG, Karpiuk O, Warren MD, Hardy CW, Duong DM, Park SJ, Kim HS, Vassilopoulos A, Seyfried NT, Johnsen SA, Gius D, Yu DS. SIRT2 directs the replication stress response through CDK9 deacetylation. Proc Natl Acad Sci U S A. 2013 Aug 13;110(33):13546-51. doi: 10.1073/pnas.1301463110. Epub 2013 Jul 29. PubMed PMID: 23898190

Wu F, Nicholson AD, Haile WB, Torre E, An J, Chen C, Lee AK, Duong DM, Dammer EB, Seyfried NT, Tong FC, Votaw JR, Yepes M. Tissue-type plasminogen activator mediates neuronal detection and adaptation to metabolic stress. J Cereb Blood Flow Metab. 2013 Nov;33(11):1761-9. doi: 10.1038/jcbfm.2013.124. Epub 2013 Jul24. PubMed PMID: 23881246

Dammer EB, Duong DM, Diner I, Gearing M, Feng Y, Lah JJ, Levey AI, Seyfried NT. Neuron enriched nuclear proteome isolated from human brain. J Proteome Res. 2013 Jul 5;12(7):3193-206. doi: 10.1021/pr400246t. Epub 2013 Jun 17. PubMed PMID: 23768213

Donovan LE, Dammer EB, Duong DM, Hanfelt JJ, Levey AI, Seyfried NT, Lah JJ. Exploring the potential of the platelet membrane proteome as a source of peripheral biomarkers for Alzheimer's disease. Alzheimers Res Ther. 2013 Jun 13;5(3):32. doi: 10.1186/alzrt186. eCollection 2013. PubMed PMID: 23764030

Kallappagoudar S, Dammer EB, Duong DM, Seyfried NT, Lucchesi JC. Expression, purification and proteomic analysis of recombinant histone H4 acetylated at lysine 16. Proteomics. 2013 May;13(10-11):1687-91. doi: 10.1002/pmic.201300025.Epub 2013 Apr 26. PubMed PMID: 23554095

Wu F, Wu J, Nicholson AD, Echeverry R, Haile WB, Catano M, An J, Lee AK, Duong D, Dammer EB, Seyfried NT, Tong FC, Votaw JR, Medcalf RL, Yepes M. Tissue-type plasminogen activator regulates the neuronal uptake of glucose in the ischemic brain. J Neurosci. 2012 Jul 18;32(29):9848-58. PubMed PMID: 22815500

Dammer EB, Fallini C, Gozal YM, Duong DM, Rossoll W, Xu P, Lah JJ, Levey AI, Peng J, Bassell GJ, Seyfried NT. Coaggregation of RNA-binding proteins in a model of TDP-43 proteinopathy with selective RGG motif methylation and a role for RRM1 ubiquitination. PLoS One. 2012;7(6):e38658. doi: 10.1371/journal.pone.0038658. Epub 2012 Jun 21. PubMed PMID: 22761693

Herskowitz JH, Gozal YM, Duong DM, Dammer EB, Gearing M, Ye K, Lah JJ, Peng J, Levey AI, Seyfried NT. Asparaginyl endopeptidase cleaves TDP-43 in brain. Proteomics. 2012 Aug;12(15-16):2455-63. doi: 10.1002/pmic.201200006. PubMed PMID:22718532

Donovan LE, Higginbotham L, Dammer EB, Gearing M, Rees HD, Xia Q, Duong DM, Seyfried NT, Lah JJ, Levey AI. Analysis of a membrane-enriched proteome from postmortem human brain tissue in Alzheimer's disease. Proteomics Clin Appl. 2012 Apr;6(3-4):201-11. doi: 10.1002/prca.201100068. PubMed PMID: 22532456

Seyfried NT, Gozal YM, Donovan LE, Herskowitz JH, Dammer EB, Xia Q, Ku L, Chang J, Duong DM, Rees HD, Cooper DS, Glass JD, Gearing M, Tansey MG, Lah JJ, Feng Y, Levey AI, Peng J. Quantitative analysis of the detergent-insoluble brain proteome in frontotemporal lobar degeneration using SILAC internal standards. J Proteome Res. 2012 May 4;11(5):2721-38. doi: 10.1021/pr2010814. Epub 2012 Apr 4. PubMed PMID: 22416763

Gozal YM, Seyfried NT, Gearing M, Glass JD, Heilman CJ, Wuu J, Duong DM, Cheng D, Xia Q, Rees HD, Fritz JJ, Cooper DS, Peng J, Levey AI, Lah JJ. Aberrant septin 11 is associated with sporadic frontotemporal lobar degeneration. Mol Neurodegener. 2011 Nov 29;6:82. doi: 10.1186/1750-1326-6-82. PubMed PMID: 22126117

Dammer EB, Na CH, Xu P, Seyfried NT, Duong DM, Cheng D, Gearing M, Rees H, Lah JJ, Levey AI, Rush J, Peng J. Polyubiquitin linkage profiles in three models of proteolytic stress suggest the etiology of Alzheimer disease. J Biol Chem. 2011 Mar 25;286(12):10457-65. doi: 10.1074/jbc.M110.149633. Epub 2011 Jan 28. PubMed PMID: 21278249

Herskowitz JH, Seyfried NT, Gearing M, Kahn RA, Peng J, Levey AI, Lah JJ. Rho kinase II phosphorylation of the lipoprotein receptor LR11/SORLA alters amyloid-beta production. J Biol Chem. 2011 Feb 25;286(8):6117-27. doi: 10.1074/jbc.M110.167239. Epub 2010 Dec 8. PubMed PMID: 21147781.

Herskowitz JH, Seyfried NT, Duong DM, Xia Q, Rees HD, Gearing M, Peng J, Lah  JJ, Levey AI. Phosphoproteomic analysis reveals site-specific changes in GFAP and NDRG2 phosphorylation in frontotemporal lobar degeneration. J Proteome Res. 2010 Dec 3;9(12):6368-79. doi: 10.1021/pr100666c. Epub 2010 Oct 22. PubMed PMID: 20886841; PubMed Central PMCID: PMC2997170.

Franco M, Seyfried NT, Brand AH, Peng J, Mayor U. A novel strategy to isolate ubiquitin conjugates reveals wide role for ubiquitination during neural development. Mol Cell Proteomics. 2011 May;10(5):M110.002188. doi: 10.1074/mcp.M110.002188. Epub 2010 Sep 22. PubMed PMID: 20861518.

Seyfried NT, Gozal YM, Dammer EB, Xia Q, Duong DM, Cheng D, Lah JJ, Levey AI, Peng J. Multiplex SILAC analysis of a cellular TDP-43 proteinopathy model reveals protein inclusions associated with SUMOylation and diverse polyubiquitin chains. Mol Cell Proteomics. 2010 Apr;9(4):705-18. doi: 10.1074/mcp.M800390-MCP200. Epub  2010 Jan 4. PubMed PMID: 20047951.

2009

Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, Robert J, Rush J, Hochstrasser M, Finley D, Peng J. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell. 2009 Apr 3;137(1):133-45. doi: 10.1016/j.cell.2009.01.041. PubMed PMID: 19345192.

2008

Seyfried NT, Xu P, Duong DM, Cheng D, Hanfelt J, Peng J. Systematic approach for validating the ubiquitinated proteome. Anal Chem. 2008 Jun 1;80(11):4161-9. doi: 10.1021/ac702516a. Epub 2008 Apr 24. PubMed PMID: 18433149

Seyfried NT, Huysentruyt LC, Atwood JA 3rd, Xia Q, Seyfried TN, Orlando R. Up-regulation of NG2 proteoglycan and interferon-induced transmembrane proteins 1 and 3 in mouse astrocytoma: a membrane proteomics approach. Cancer Lett. 2008 May 18;263(2):243-52. doi: 10.1016/j.canlet.2008.01.007. Epub 2008 Feb 20. PubMed PMID: 18281150; PubMed Central PMCID: PMC2726046.

Baker DL, Seyfried NT, Li H, Orlando R, Terns RM, Terns MP. Determination of protein-RNA interaction sites in the Cbf5-H/ACA guide RNA complex by mass spectrometric protein footprinting. Biochemistry. 2008 Feb 12;47(6):1500-10. doi: 10.1021/bi701606m. Epub 2008 Jan 19. PubMed PMID: 18205399.

2007

Seyfried NT, Atwood JA 3rd, Yongye A, Almond A, Day AJ, Orlando R, Woods RJ. Fourier transform mass spectrometry to monitor hyaluronan-protein interactions: use of hydrogen/deuterium amide exchange. Rapid Commun Mass Spectrom. 2007;21(2):121-31. PubMed PMID: 17154353

2006

Kuznetsova SA, Issa P, Perruccio EM, Zeng B, Sipes JM, Ward Y, Seyfried NT, Fielder HL, Day AJ, Wight TN, Roberts DD. Versican-thrombospondin-1 binding in vitro and colocalization in microfibrils induced by inflammation on vascular smooth muscle cells. J Cell Sci. 2006 Nov 1;119(Pt 21):4499-509. Epub 2006 Oct 17. PubMed PMID: 17046999.

2005

Seyfried NT, Day AJ, Almond A. Experimental evidence for all-or-none cooperative interactions between the G1-domain of versican and multivalent hyaluronan oligosaccharides. Matrix Biol. 2006 Jan;25(1):14-9. Epub 2005 Sep 26. PubMed PMID: 16185858.

Seyfried NT, McVey GF, Almond A, Mahoney DJ, Dudhia J, Day AJ. Expression and purification of functionally active hyaluronan-binding domains from human cartilage link protein, aggrecan and versican: formation of ternary complexes with defined hyaluronan oligosaccharides. J Biol Chem. 2005 Feb 18;280(7):5435-48. Epub 2004 Dec 8. PubMed PMID: 15590670.

Seyfried NT, Blundell CD, Day AJ, Almond A. Preparation and application of biologically active fluorescent hyaluronan oligosaccharides. Glycobiology. 2005 Mar;15(3):303-12. Epub 2004 Oct 20. PubMed PMID: 15496500.

Joki T, Machluf M, Atala A, Zhu J, Seyfried NT, Dunn IF, Abe T, Carroll RS, Black PM. Continuous release of endostatin from microencapsulated engineered cells for tumor therapy. Nat Biotechnol. 2001 Jan;19(1):35-9. PubMed PMID: 11135549.

Joki T, Heese O, Nikas DC, Bello L, Zhang J, Kraeft SK, Seyfried NT, Abe T, Chen LB, Carroll RS, Black PM. Expression of cyclooxygenase 2 (COX-2) in human glioma and in vitro inhibition by a specific COX-2 inhibitor, NS-398. Cancer Res. 2000 Sep 1;60(17):4926-31. PubMed PMID: 10987308.