Research Summary

My group has long-standing, extensive expertise and experience in mass spectrometry, proteomics and systems biology, especially focused on sequencing, identification and study of unknown proteins, and the detection, assignment and site-specific dynamics of posttranslational modifications of proteins, particularly OGlcNAcylation, phosphorylation, acetylation, methylation and ubiquitinylation. Over many years we have collaborated with the neurobiological community extensively, including structural characterization of the GPI membrane anchor of the prion protein, structure of the lysyl oxidase co-factor, identification and PTM regulation of proteins in the retrograde signaling complexes in damaged axons, the O-GlcNAc/phosphorylation dynamics at the murine synapse, identification of new proteins involved in the Nodes of Ranvier, etc.

In addition to the work in proteomics and epigenetics above, we have focused significant effort on other studies concerning the architecture of protein complexes and machines for which angstrom resolution structural information has not yet been tractable. For example we have developed a new lysine-lysine cross-linking strategy based on chemical reductive amination that provides comprehensive sequence and cross-link site assignments using electron transfer dissociation (ETD). This information provides accurate distance constraints that complement cryoEM and computer modeling efforts. In parallel software algorithms and scoring strategies have been developed that greatly facilitates the assignment of cross-linked peptides in general. Very recently we have initiated a thrust into development and application of methodology to measure protein complexes directly in the gas phase using a newly acquired high mass Orbitrap Exactive instrument (m/z < 22,000). This effort will complement our long-standing work on chemical cross-linking of protein complexes and machines.

Finally, we have developed a general suite of programs and software tools required for processing large scale mass spectral data sets (HCD, ETD, etc) and stable isotopic labeling experiments (SILAC, iTRAQ, etc) called Protein Prospector.

Research Funding

  • July 1, 1985 - May 31, 2023 - UCSF Liver Center , Co-Investigator . Sponsor: NIH, Sponsor Award ID: P30DK026743
  • August 1, 2002 - April 30, 2020 - Genetic Biochemical Studies of Plant Steroid Signaling , Principal Investigator . Sponsor: NIH, Sponsor Award ID: R01GM066258
  • September 30, 1987 - March 31, 2017 - Toxic Substances in the Environment , Co-Investigator . Sponsor: NIH, Sponsor Award ID: P42ES004705
  • March 15, 1997 - May 31, 2016 - Bio-Organic Biomedical Mass Spectrometry Resource , Principal Investigator . Sponsor: NIH, Sponsor Award ID: P41GM103481

Education

University of Rhode Island, Kingston, RI, B.S. 1959, Chemistry
MIT, Cambridge, MA, Ph.D., 1962, Chemistry, Physics

Honors & Awards

  • 1970-72
    Guggenheim Fellow, Karolinska Institute, Stockholm
  • 1990-
    Elected Fellow, American Association for the Advancement of Science1999-2006
    Deputy Editor, Molecular and Cellular Proteomics
  • 2002-04
    Physiological Chemistry Study Section CSR, NIH
  • 2006-
    Co-editor, Molecular and Cellular Proteomics
  • 2013-
    Editor-in-chief, Molecular and Cellular Proteomics
  • 2012
    International Forum of Proteomics, Achievement Award
  • 2013
    Awarded the MCP lectureship Plenary at the Society for Glycobiology, St Petersburg, FL, November 17-20, 2013
  • 2018
    Albert Nelson Marquis Lifetime Achievement Award

Selected Publications

  1. Alber S, Di Matteo P, Zdradzinski MD, Dalla Costa I, Medzihradszky KF, Kawaguchi R, Di Pizio A, Freund P, Panayotis N, Marvaldi L, Doron-Mandel E, Okladnikov N, Rishal I, Nevo R, Coppola G, Lee SJ, Sahoo PK, Burlingame AL, Twiss JL, Fainzilber M. PTBP1 regulates injury responses and sensory pathways in adult peripheral neurons. Sci Adv. 2023 Jul 28; 9(30):eadi0286.  View on PubMed
  2. Beusch I, Rao B, Studer MK, Luhovska T, Šukyte V, Lei S, Oses-Prieto J, SeGraves E, Burlingame A, Jonas S, Madhani HD. Targeted high-throughput mutagenesis of the human spliceosome reveals its in vivo operating principles. Mol Cell. 2023 07 20; 83(14):2578-2594.e9.  View on PubMed
  3. Tsusaka T, Oses-Prieto JA, Lee C, DeFelice BC, Burlingame AL, Goldberg EL. Non-specific recognition of histone modifications by H3K9bhb antibody. iScience. 2023 Jul 21; 26(7):107235.  View on PubMed
  4. Tsusaka T, Oses-Prieto JA, Lee C, DeFelice BC, Burlingame AL, Goldberg E. Non-specific recognition of histone modifications by H3K9bhb antibody. bioRxiv. 2023 Apr 13.  View on PubMed
  5. Dai S, Liu S, Zhou C, Yu F, Zhu G, Zhang W, Deng H, Burlingame A, Yu W, Wang T, Li N. Capturing the hierarchically assorted modules of protein-protein interactions in the organized nucleome. Mol Plant. 2023 05 01; 16(5):930-961.  View on PubMed
  6. Estevez P, Oses Prieto J, Burlingame A, Gago Martinez A. Characterization of the Ciguatoxin Profile in Fish Samples from the Eastern Atlantic Ocean using Capillary Liquid Chromatography-High Resolution Mass Spectrometry. Food Chem. 2023 Aug 30; 418:135960.  View on PubMed
  7. Kim TW, Park CH, Hsu CC, Kim YW, Ko YW, Zhang Z, Zhu JY, Hsiao YC, Branon T, Kaasik K, Saldivar E, Li K, Pasha A, Provart NJ, Burlingame AL, Xu SL, Ting AY, Wang ZY. Mapping the signaling network of BIN2 kinase using TurboID-mediated biotin labeling and phosphoproteomics. Plant Cell. 2023 03 15; 35(3):975-993.  View on PubMed
  8. Ogawa Y, Lim BC, George S, Oses-Prieto JA, Rasband JM, Eshed-Eisenbach Y, Nair S, Boato F, Peles E, Burlingame AL, Aelst LV, Rasband MN. Antibody-directed extracellular proximity biotinylation reveals Contactin-1 regulates axo-axonic innervation of axon initial segments. bioRxiv. 2023 Mar 06.  View on PubMed
  9. Zhang Z, Huang Z, Awad M, Elsalanty M, Cray J, Ball LE, Maynard JC, Burlingame AL, Zeng H, Mansky KC, Ruan HB. O-GlcNAc glycosylation orchestrates fate decision and niche function of bone marrow stromal progenitors. Elife. 2023 03 02; 12.  View on PubMed
  10. Dugan MP, Ferguson LB, Hertz NT, Chalkley RJ, Burlingame AL, Shokat KM, Parker PJ, Messing RO. Chemical Genetic Identification of PKC Epsilon Substrates in Mouse Brain. Mol Cell Proteomics. 2023 04; 22(4):100522.  View on PubMed
  11. Phillips NJ, Vinaithirthan BM, Oses-Prieto JA, Chalkley RJ, Burlingame AL. Capture, Release, and Identification of Newly Synthesized Proteins for Improved Profiling of Functional Translatomes. Mol Cell Proteomics. 2023 03; 22(3):100497.  View on PubMed
  12. Liu Y, Trnka MJ, He L, Burlingame AL, Correia MA. In-Cell Chemical Crosslinking Identifies Hotspots for SQSTM-1/p62-IκBα Interaction That Underscore a Critical Role of p62 in Limiting NF-κB Activation Through IκBα Stabilization. Mol Cell Proteomics. 2023 02; 22(2):100495.  View on PubMed
  13. Forester CM, Oses-Prieto JA, Phillips NJ, Miglani S, Pang X, Byeon GW, DeMarco R, Burlingame A, Barna M, Ruggero D. Regulation of eIF4E guides a unique translational program to control erythroid maturation. Sci Adv. 2022 Dec 23; 8(51):eadd3942.  View on PubMed
  14. Song DA, Alber S, Doron-Mandel E, Schmid V, Albus CA, Leitner O, Hamawi H, Oses-Prieto JA, Dezorella N, Burlingame AL, Fainzilber M, Rishal I. A New Monoclonal Antibody Enables BAR Analysis of Subcellular Importin β1 Interactomes. Mol Cell Proteomics. 2022 Nov; 21(11):100418.  View on PubMed
  15. Genuth NR, Shi Z, Kunimoto K, Hung V, Xu AF, Kerr CH, Tiu GC, Oses-Prieto JA, Salomon-Shulman REA, Axelrod JD, Burlingame AL, Loh KM, Barna M. A stem cell roadmap of ribosome heterogeneity reveals a function for RPL10A in mesoderm production. Nat Commun. 2022 09 19; 13(1):5491.  View on PubMed
  16. Zhao M, Ren K, Xiong X, Xin Y, Zou Y, Maynard JC, Kim A, Battist AP, Koneripalli N, Wang Y, Chen Q, Xin R, Yang C, Huang R, Yu J, Huang Z, Zhang Z, Wang H, Wang D, Xiao Y, Salgado OC, Jarjour NN, Hogquist KA, Revelo XS, Burlingame AL, Gao X, von Moltke J, Lin Z, Ruan HB. Epithelial STAT6 O-GlcNAcylation drives a concerted anti-helminth alarmin response dependent on tuft cell hyperplasia and Gasdermin C. Immunity. 2022 Jul 12; 55(7):1327.  View on PubMed
  17. Park CH, Bi Y, Youn JH, Kim SH, Kim JG, Xu NY, Shrestha R, Burlingame AL, Xu SL, Mudgett MB, Kim SK, Kim TW, Wang ZY. Deconvoluting signals downstream of growth and immune receptor kinases by phosphocodes of the BSU1 family phosphatases. Nat Plants. 2022 06; 8(6):646-655.  View on PubMed
  18. Patel P, Buchanan CN, Zdradzinski MD, Sahoo PK, Kar AN, Lee SJ, Vaughn LS, Urisman A, Oses-Prieto J, Dell'Orco M, Cassidy DE, Costa ID, Miller S, Thames E, Smith TP, Burlingame AL, Perrone-Bizzozero N, Twiss JL. Intra-axonal translation of Khsrp mRNA slows axon regeneration by destabilizing localized mRNAs. Nucleic Acids Res. 2022 06 10; 50(10):5772-5792.  View on PubMed
  19. Yang T, Cuesta A, Wan X, Craven GB, Hirakawa B, Khamphavong P, May JR, Kath JC, Lapek JD, Niessen S, Burlingame AL, Carelli JD, Taunton J. Reversible lysine-targeted probes reveal residence time-based kinase selectivity. Nat Chem Biol. 2022 09; 18(9):934-941.  View on PubMed
  20. Zhang MY, Yang H, Ortiz G, Trnka MJ, Petronikolou N, Burlingame AL, DeGrado WF, Fujimori DG. Covalent labeling of a chromatin reader domain using proximity-reactive cyclic peptides. Chem Sci. 2022 Jun 07; 13(22):6599-6609.  View on PubMed

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