Penn State (2013 – present)
*denotes equal contribution, underscore denotes undergraduate author
Larrinaga, W.B.; Jung, J.J.; Lin, C.-Y.; Boal, A.K.; Cotruvo, J.A. “Modulating metal-centered dimerization of a lanthanide chaperone protein for separation of light lanthanides.” Proc Natl Acad Sci USA 2024, 121 (45) e2410926121.
Wenger, E.S.; Martinie, R.J.; Ushimaru, R.; Pollock, C.J.; Sil, D.; Li, A.; Hoang, N.; Palowitch, G.M.; Graham, B.P.; Schaperdoth, I.; Burke, E.J.; Maggiolo, A.O.; Chang, W.-c.; Allen, B.D.; Krebs, C.; Silakov, A.; Boal, A.K.; Bollinger, J.M., Jr. “Optimized Substrate Positioning Enables Switches in the C-H Cleavage Site and Reaction Outcome in the Hydroxylation-Epoxidation Sequence Catalyzed by Hyoscyamine 6β-Hydroxylase.” J. Am. Chem. Soc. 2024, 146, 24271-24287.
Slater, J.W.; Lin, C.-Y.; Neugebauer, M.E.; McBride, M.J.; Sil, D.; Nair, M.A.; Katch, B.J.; Boal, A.K.; Chang, M.C.Y.; Silakov, A.; Krebs, C.; Bollinger, J.M., Jr. “Synergistic Binding of the Halide and Cationic Prime Substrate of l-Lysine 4-Chlorinase, BesD, in Both Ferrous and Ferryl States.” Biochemistry 2023. DOI: 10.1021/acs.biochem.3c00248.
Mattocks, J.A.; Jung, J.J.; Lin, C.-Y.; Dong, Z.; Yennawar, N.H.; Featherston, E.R.; Kang-Yun, C.S.; Hamilton, T.A.; Park, D.M.; Boal, A.K.; Cotruvo, J.A. “Enhanced rare-earth separation with a metal-sensitive lanmodulin dimer.” Nature 2023, 618 (7963), 87-93.
McBride, M.J.; Pope, S.R.; Nair, M.A.; Sil, D.; Salas-Sola, X.E.; Krebs, C.; Bollinger, J.M., Jr.; Boal, A.K. “Methods for Biophysical Characterization of SznF, a Member of the Heme-Oxygenase-Like Diiron Oxidase/Oxygenase Superfamily.” In Oxygen Sensing: Methods and Protocols; Weinert, E.E., Ed.; Methods in Molecular Biology; Springer US: New York, NY, 2023; pp 123–154.
Lloyd, C.T.; Iwig, D.F.; Wang, B.; Cossu, M.; Metcalf, W.W.; Boal, A.K.; Booker, S.J. “Discovery, structure and mechanism of a tetraether lipid synthase.” Nature 2022, 609, 197-203.
Lin, C.-Y.; Muñoz Hernández, A.L.; Laremore, T.N.; Silakov, A.; Krebs, C.; Boal, A.K.; Bollinger, J.M., Jr. “Use of Noncanonical Tyrosine Analogues to Probe Control of Radical Intermediates during Endoperoxide Installation by Verruculogen Synthase (FtmOx1).” ACS Catalysis 2022, 12, 6968-6979.
McBride M.J.; Nair, M.A.; Sil, D.; Slater, J.W.; Neugebauer, M.E.; Chang, M.C.Y.; Boal, A.K.; Krebs, C.; Bollinger, J. M., Jr. “Substrate-Triggered μ-Peroxodiiron(III) Intermediate in the 4-Chloro-l-Lysine-Fragmenting Heme-Oxygenase-like Diiron Oxidase (HDO) BesC: Substrate Dissociation from, and C4 Targeting by, the Intermediate.” Biochemistry 2022,61, 689–702.
Braffman, N.R.*; Ruskoski, T.B.*; Davis, K.M.; Glasser, N.R.; Johnson, C.; Okafor, C.D.; Boal, A.K.; Balskus, E.P. “Structural basis for an unprecedented enzymatic alkylation in cylindrocyclophane biosynthesis.” Elife 2022, 11, e75761.
Ruskoski, T.B.; Boal, A.K. “The Periodic Table of Ribonucleotide Reductases.” Journal of Biological Chemistry 2021, 297 (4).
Jeyachandran, V.R.; Pendyala, J.V.; McCarthy, E.L.; Boal, A.K.; Booker, S.J. “Biochemical Approaches to Probe the Role of the Auxiliary Iron-Sulfur Cluster of Lipoyl Synthase from Mycobacterium Tuberculosis.” In Fe-S Proteins: Methods and Protocols; Dos Santos, P. C., Ed.; Methods in Molecular Biology; Springer US: New York, NY, 2021; pp 307–332.
McBride, M.J.; Pope, S.R.; Hu, K.; Okafor, C.D.; Balskus, E.P.; Bollinger, J.M., Jr.; Boal, A.K. “Structure and assembly of the diiron cofactor in the heme-oxygenase–like domain of the N-nitrosourea–producing enzyme SznF.” Proc Natl Acad Sci USA 2021,118 (4) e2015931118.
McBride, M.J.; Sil, D.; Ng, T.L.; Crooke, A.M.; Kenney, G.E.; Tysoe, C.R.; Zhang, B.; Balskus, E.P.; Boal, A.K.; Krebs, C.; Bollinger, J.M., Jr. “A Peroxodiiron(III) Intermediate Mediating both N-Hydroxylation Steps in Biosynthesis of the N-Nitrosourea Pharmacophore of Streptozotocin by SznF.” J. Am. Chem. Soc. 2020, 142, 11818-11828.
Rajakovich, L.J.; Zhang, B.; McBride, M.J., Boal, A.K.; Krebs, C.; Bollinger, J.M., Jr. “Emerging Structural and Functional Diversity in Proteins with Dioxygen-Reactive Dinuclear Transition Metal Cofactors.” in “Comprehensive Natural Products III: Chemistry and Biology” edited by Liu, H.-w. and Begley, T. P., Elsevier, Amsterdam, 2020.
Rose, H.R.; Palowitch, G.M.; Hu, K.; Gandhi, A.; Boal, A.K. “Structure-Function Relationships in Assembly of the Radical-Initiating Cofactors of Class Ia–e Ribonucleotide Reductases.” in Comprehensive Natural Products III: Chemistry and Biology” Elsevier, Amsterdam, 2020.
Gumkowski, J.A.; Martinie, R.J.; Corrigan, P.S.; Pan, J.; Bauerle, M.; Almarei, M.; Booker, S.J.; Silakov, A.; Krebs, C.; Boal, A.K. “Analysis of RNA modification by phylogenetically diverse Cfr radical SAM methylases reveals an iron-binding accessory domain in a clostridial enzyme.” Biochemistry 2019 58, 3169-3184.
Dunham, N.P.; Del Río-Pantoja, J.M.; Zhang, B.; Rajakovich, L.J.; Allen, B.D.; Boal, A.K. Krebs, C.; Bollinger, J.M., Jr. “Hydrogen donation but not abstraction by a tyrosine residue (Y68) during installation of the endoperoxide of verroculogen by FtmOx1.” J. Am Chem. Soc. 2019 141, 9964-9979.
Featherston, E.R.; Rose, H.R.; McBride, M.J.; Taylor, E.; Boal, A.K., Cotruvo, J.A., Jr. “Biochemical and structural characterization of XoxG and XoxJ and their roles in activity of the lanthanide-dependent methanol dehydrogenase, XoxF.” Chembiochem 2019, DOI:10.1002/cbic.201900184.
Rose, H.R.; Maggiolo, A.O.; McBride, M.J.; Palowitch, G.M.; Pandelia, M.E.; Davis K.M.; Yennawar N.H.; Boal A.K. “Structures of class Id ribonucleotide reductase catalytic subunits reveal a minimal architecture for deoxynucleotide biosynthesis.” Biochemistry 2019 58,1845-1860.
Rajakovich, L.; Pandelia, M.-E.; Mitchell, A.J.; Chang, W.-c.; Zhang, B.; Boal, A.K.; Krebs, C.; Bollinger, J.M., Jr. “A new microbial pathway for organophosphonate degradation catalyzed by two previously misannotated non-heme-iron oxygenases.” Biochemistry 2019 58,1627-1647.
Ng, T.; Rohac, R.; Mitchell, A.J.; Boal, A.K.; Balskus, E.P. “An N-nitrosating metalloenzyme constructs the pharmacophore of streptozotocin.” Nature 2019 566, 94-99.
Dunham, N.P.; Mitchell, A.J.; Del Río-Pantoja, J.; Krebs, C.; Bollinger, J.M., Jr.; Boal, A.K. “α-Amine desaturation of D-arginine by the iron(II) and 2-(oxo)-glutarate-dependent L-arginine 3-hydroxylase, VioC.” Biochemistry 2018 57, 6479-6488.
Blaesi, E.J.*; Palowitch, G.M.*; Hu, K.*; Kim, A.J.; Rose, H.R.; Alapati, R.B.; Lougee, M.G.; Kee, H.J.; Taguchi, A.T.; Tan, K.O.; Griffin, R.G.; Krebs, C.; Matthews, M.L.; Silakov, A.; Bollinger, J.M., Jr.; Allen, B.D.; Boal, A.K. “Metal-free class Ie ribonucleotide reductase from pathogens initiates catalysis with a tyrosine-derived dihydroxyphenylalanine radical.” Proc. Natl. Acad. Sci. USA 2018 115, 10022-10027.
Parker, M.J.; Maggiolo, A.O.*; Thomas, W.C.*; Kim, A.; Meisburger, S.P.; Ando, N.; Boal, A.K.; Stubbe, J. “An endogenous dAMP ligand in Bacillus subtilis class Ib ribonucleotide reductase promotes assembly of a non-canonical dimer for regulation by dATP.” Proc Natl Acad Sci USA 2018, 115, E4595-E4603.
Dunham, N.P.; Chang, W.-c.; Mitchell, A.J.; Martinie, R.J.; Zhang, B.; Bergman, J.A.; Rajakovich, L.J.; Wang, B.; Silakov, A.; Krebs, C.; Boal, A.K.; Bollinger, J.M., Jr. “Two distinct mechanisms for C-C desaturation by iron(II)- and 2-(oxo)-glutarate-dependent oxygenases: importance of a-heteroatom assistance.” J. Am. Chem. Soc. 2018 140, 7116-7126.
Rose, H.R.*; Ghosh, M.K.*; Maggiolo, A.O.; Pollock, C.J.; Blaesi, E.J.; Hajj, V.; Wei, Y.; Rajakovich, L.J.; Chang, W.-c.; Han, Y.; Hajj, M.; Pandelia, M.-E.; Krebs, C.; Bollinger, J.M., Jr.; Boal, A.K. “Structural basis for superoxide activation of Flavobacterium johnsoniae class I ribonucleotide reductase and for radical initiation by its dimanganese cofactor.” Biochemistry 2018 57, 2679-2693.
Mitchell, A.J.*; Dunham, N.P.*; Martinie, R.J.; Bergman, J.A.; Pollock, C.J.; Hu, K.; Allen, B.D.; Chang, W.-c.; Silakov, A.; Bollinger, J.M., Jr.; Krebs, C.; Boal, A.K. “Visualizing the reaction cycle in an iron(II) and 2-(oxo)-glutarate-dependent hydroxlase.” J. Am. Chem. Soc. 2017 139, 13830-13836.
Liu, Y.; Fares, M.; Dunham, N.P.; Gao, Z.; Miao, K.; Jiang, X.; Bollinger, S.S.; Boal, A.K.; Zhang, X. “AgHalo: a facile fluorogenic proteostasis sensor to detect drug-induced proteome stress.” Angew. Chem. Int. Ed. Engl. 2017 56, 8672-8676.
Badding, E.D.; Grove, T.L.; Gadsby, L.; Boal, A.K.; Booker, S.J. “Rerouting the pathway for the biosynthesis of the dimethylindolic acid moiety of nosiheptide: the roles of NosI, NosJ, and NosK.” J. Am. Chem. Soc. 2017 139, 5896-5905.
Liu, Y.; Miao, K.; Dunham, N.P.; Liu, H.; Fares, M.; Boal, A.K.; Li, X.; Zhang, X. “The cation-pi interaction enables a Halo-tag fluorogenic probe for fast no-wash live cell imaging and gel-free protein quantification.” Biochemistry 2017 56, 1585-1595.
Mitchell, A.J.; Dunham, N.P.; Bergman, J.A.; Wang, B.; Chang, W.-c. Liu, X.; Boal, A.K. “Structure-guided engineering of a small-molecule aliphatic halogenase.” Biochemistry 2017 56, 441-444.
Davis, K.M.; Boal, A.K. “Mechanism-based strategies for structural characterization of radical SAM reaction intermediates.” Methods Enzymol. 2017, 595, 331-359.
Mitchell, A.J.; Zhu, Q.; Maggiolo, A.O.; Ananth, N.; Hillwig, M.L.; Liu, X.; Boal, A.K. “Structural basis for selective chlorination by iron- and 2-oxo-glutarate-dependent WelO5.” Nat. Chem. Biol. 2016, 12, 636-640.
Schwalm, E.L.*; Grove, T.L.*; Booker, S.J.; Boal, A.K. “Crystallographic capture of a radical S-adenosylmethionine enzyme in the act of modifying tRNA.” Science 2016, 352, 309-312.
Boal, A.K.; Bollinger, J.M., Jr.; Chang, W.-c. “Assembly of the unusual oxacycles in the orthomycin antibiotics.” Proc. Natl. Acad. Sci. USA 2015, 112, 11989-11990.
Silakov, A.; Grove, T.L.; Radle, M.I.; Bauerle, M.R.; Green, M.T.; Rosenzweig, A.C.; Boal, A.K.; Booker, S.J. “Characterization of a cross-linked protein-nucleic acid substrate radical in the reaction catalyzed by RlmN.” J. Am. Chem. Soc. 2014, 136, 8221-8228.
Chang, W.-c.; Guo, Y.; Wang, C.; Butch, S.E.; Rosenzweig, A.C.; Boal, A.K.; Krebs, C.; Bollinger, J.M., Jr. “Mechanism of the C5 stereoinversion reaction in the biosynthesis of carbapenem antibiotics.” Science 2014, 343, 1140-1144.
Wörsdörfer, B.; Lingaraju, M.; Yennawar, N.H.; Boal, A.K.; Krebs, C.; Bollinger, J.M., Jr.; Pandelia, M.-E. “Organophosphate-degrading PhnZ reveals an emerging family of HD-domain mixed-valent diiron oxygenases.” Proc. Natl. Acad. Sci. USA 2013, 110, 18874-18879.
Dassama, L.M.K.; Krebs, C.; Bollinger, J.M., Jr.; Rosenzweig, A.C.; Boal, A.K. “Structural basis for assembly of the MnIV/FeIII cofactor in the class Ic ribonucleotide reductase from Chlamydia trachomatis.” Biochemistry 2013, 52, 6424-6436.
Prior to Penn State (2000 – 2013)
Research Articles:
12. Makhlynets, O.; Boal, A.K.; Rhodes, D.; Kitten, T.; Rosenzweig, A.C.; Stubbe, J. “Streptococcus sanguinis class Ib ribonucleotide reductase: high activity with both iron and manganese cofactors and structural insights.” J. Biol. Chem. 2014, 289, 6259-6272.
11. Boal, A.K.; Cotruvo, J.A., Jr.; Stubbe, J.; Rosenzweig, A.C. “The dimanganese(II) site of Bacillus subtilis class Ib ribonucleotide reductase.” Biochemistry 2012, 51, 3861-3871.
10. Dassama, L.M.K.*; Boal, A.K.*; Krebs, C.; Rosenzweig, A.C.; Bollinger, J.M., Jr. “Evidence that the beta subunit of Chlamydia trachomatis ribonucleotide reductase is active with the manganese ion of its manganese(IV)/iron(III) cofactor in site 1.” J. Am. Chem. Soc. 2012, 134, 2520-2523.
9. Boal, A.K.; Grove, T.L.; McLaughlin, M.I.; Yennawar, N.H.; Booker, S.J.; Rosenzweig, A.C. “Structural basis for methyl transfer by a radical SAM enzyme.” Science 2011, 332, 1089-1092.
8. Boal, A.K.; Cotruvo, J.A., Jr.; Stubbe, J.; Rosenzweig, A.C. “Structural basis for activation of class Ib ribonucleotide reductase.” Science 2010, 329, 1526-1530.
7. Boal, A.K.; Rosenzweig, A.C. “Crystal structures of cisplatin bound to a human copper chaperone.” J. Am. Chem. Soc. 2009, 131, 14196-14197.
6. Boal, A.K.; Genereux, J.C.; Sontz, P.A.; Gralnick, J.A.; Newman, D.K.; Barton, J.K. “Redox signaling between DNA repair proteins for efficient lesion detection.” Proc. Natl. Acad. Sci. USA 2009, 106, 15237-15242.
5. Boal, A.K.; Guryanov, I.; Moretto, A.; Crisma, M.; Lanni, E.L.; Toniolo, C.; Grubbs, R.H.; O’Leary, D.J. “Facile and E-selective intramolecular ring-closing metathesis reactions in 310-helical peptides: a 3D structural study.” J. Am. Chem. Soc. 2007, 129, 6986-6987.
4. Gorodetsky, A.A.; Boal, A.K.; Barton, J.K. “Direct electrochemistry of endonuclease III in the presence and absence of DNA.” J. Am. Chem. Soc. 2006, 128, 12082-12083.
3. Boal, A.K.; Yavin, E.; Lukianova, O.A.; O’Shea, V.L.; David, S.S.; Barton, J.K. “DNA-bound redox activity of DNA repair glycosylases containing [4Fe-4S] clusters.” Biochemistry 2005, 44
2. Boal, A.K.; Barton, J.K. “Electrochemical detection of lesions in DNA.” Bioconjug. Chem. 2005, 16, 312-321.
1. Yavin, E.; Boal, A.K.; Stemp, E.D.A.; Boon, E.M.; Livingston, A.L.; O’Shea, V.L.; David, S.S.; Barton, J.K. “Protein-DNA charge transport: redox activation of a DNA repair protein by guanine radical.” Proc. Natl. Acad. Sci. USA 2005, 102, 3546-3551.
Reviews and perspectives:
6. Boal, A.K.; Rosenzweig, A.C. “Response to ‘Crystallography and chemistry should always go together: a cautionary tale of protein complexes with cisplatin and carboplatin.’” Acta Crystallogr. D 2015, 71, 1984-1986.
5. Boal, A.K.; Rosenzweig, A.C. “A radical route for nitrogenase carbide insertion.” Science 2012, 337, 1617-1618.
4. Genereux, J.C.; Boal, A.K.; Barton J.K. “DNA-mediated charge transport in redox sensing and signaling.” J. Am. Chem. Soc. 2010, 109, 891-905.
3. Boal, A.K.; Rosenzweig, A.C. “Structural biology of copper trafficking.” Chem. Rev. 2009, 109, 4760-4779.
2. Merino, E.J.; Boal, A.K.; Barton, J.K. “Biological contexts for DNA charge transport chemistry.” Curr. Opin. Chem. Biol. 2008, 12, 229-237.
1. Boal, A.K.; Yavin, E.; Barton, J.K. “DNA repair glycosylases with a [4Fe-4S] cluster: a redox cofactor for DNA-mediated charge transport?” J. Inorg. Biochem. 2007, 101, 1913-1921.