Graduate Student Publications
Schumacher, MA; Choi, KY; Zalkin; H, Brennan, RG. Crystallization and preliminary X-ray studies on the corepressor binding domain of the Escherichia coli purine repressor. J. Mol. Bio. (1992). Schumacher, MA; Macdonald, JR; Bjorkman, J; Mowbray, SL; Brennan, RG. Structural analysis of the purine repressor, an Escherichia coli DNA-binding protein. J. Biol. Chem. (1993). Schumacher, MA; Choi, KY; Zalkin, H; Brennan, RG. Crystallization and Preliminary Xray analysis of an Escherichia coli purine repressor-hypoxanthine-DNA complex. J. Mol. Biol. (1994). Schumacher, MA; Choi, KY; Zalkin, H; Brennan, RG. Crystal structure of the LacI member, PurR, bound to DNA: minor groove binding by alpha-helices. Science. (1994). Schumacher, MA; Dixon, MM; Kluger, R; Jones, RT; Brennan, RG. Allosteric Transition intermediates modelled by crosslinked haemoglobin. Nature. (1995). Schumacher, MA; Choi, KY; Zalkin, H; Brennan, RG. Mechanism of corepressor-mediated specific DNA binding by the purine repressor. Cell (1995). Nagodoi, A; Morikawa, S; Nakamura, H; Enari, M; Kobayashi, K; Yamamoto, H; Sampei, G; Mizobuchi, K; Schumacher, MA; Brennan, RG; Nishimura, Y. Structural comparison of the free and DNA-bound forms of the purine repressor DNA-binding domain. Structure.(1995). Lewis, M; Chang, G; Horton, NC; Kercher, MA; Pace, HC; Schumacher, MA; Brennan,RG; Lu, P. Structure of the Escherichia coli lactose operon repressor and its complexes with DNA and inducer. Science. (1996).
Postdoctoral Publications
Schumacher, MA; Carter, D; Roos, DS; Ullman, B; Brennan, RG. Crystal Structures of Toxoplasma gondii HGXPRTase reveal the catalytic role of a long flexible loop. Nat Struct & Mol Biol (1996). Glasfeld, A; Schumacher, MA; Choi, KY; Zalkin, H; Brennan, RG. A positively charged residue bound in the minor groove does not alter the bending of a DNA duplex. J Amer Chem Soc (1996). Schumacher, MA; Zheleznova, E; Poundstone, KS; Kluger, R; Jones, RT; Brennan, RG. Allosteric intermediates indicate R2 is the liganded hemoglobin end-state. Proc Natl Acad Sci 1997. Schumacher, MA; Glasfeld, A; Zalkin; H, Brennan, RG. The X-ray structure of the purR guanine-purF operator complex reveals the contributions of complementary electrostatic surfaces and a water-mediated hydrogen bond to corepressor specificity and binding affinity. J Biol Chem 1997. Lu, F; Schumacher, MA; Arvidson, DN; Haldimann, A; Warner, BL; Zalkin, H; Brennan,RG. Structure-based redesign of corepressor specificity of the Escherichia coli purine repressor by substitution of residue 190. Biochemistry 1998. Schumacher, MA; Carter, D; Scott, DM; Roos, DS; Ullman, B; Brennan, RG. Crystal structures of Toxoplasma gondii uracil phosphoribosyltransferase reveal the atomic basis of pyrimidine discrimination and prodrug binding. EMBO 1998. Glasfeld, A; Koehler, AN; Schumacher, MA; Brennan, RG. The role of lysine 55 in determining the specificity of the purine repressor for its operators through minor groove interactions. J Mol Biol 1999. Rechtin, TM; Gillaspy, AF; Schumacher, MA; Brennan, RG; Smeltzer, MS; Hurlburt, BK. Characterization of the sarA virulence gene regulator of Staphylococcus aureus. Mol Microbiol 1999. Schumacher, MA; Goodman, RH; Brennan, RG. The crystal structure of a CREB bZIP-CRE complex reveals the basis for CREB family selective dimerization and CRE binding. J Biol Chem 2000. Schumacher, MA; Brown, M; Wiens, GD; Brennan, RG; Rittenberg, MB. The structural basis of repertoire shift in an immune response to phosphocholine. J Exp Med 2000. Schumacher, MA; Carter, D; Scott, DM; Roos, DS; Ullman, B, Brennan, RG. Crystal Structures of Toxoplasma gondii adenosine kinase reveal a novel catalytic mechanism and prodrug binding. J Mol Biol 2000. Craig, JC; Schumacher, MA; Mansoor, SE; Farrens, DL; Brennan, RG; Goodman, RH. Consensus and variant cAMP-regulated enhancers have distinct CREB-binding properties. J Biol Chem 2001. Grkovic, S; Brown, MH; Schumacher, MA; Brennan, RG; Skurray, RA. The staphylococcal QacR multidrug regulator binds a correctly spaced operator as a pair of dimers. J Bacteriol 2001. Schumacher, MA; Miller, MC; Grkovic, S; Brown, MH; Skurray, RA; Brennan,RG. Structural mechanisms of QacR induction and multidrug recognition. Science 2001. Schumacher, MA; Bashor, CJ, Hong Song, M, Otsu, K, Shu, S, Parry, RJ, Ullman,B, Brennan, RG. The structural mechanism of GTP stabilized oligomerization and catalytic activation of the Toxoplasma gondii uracil phosphoribosyltransferase. Proc Natl Acad Sci USA 2002. Schumacher, MA; Pearson, RF, Møller, T, Valentin-Hansen, P, Brennan, RG. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex; a bacterial Sm-like protein. EMBO J 2002. Schumacher, MA; Miller, MC; Grkovic, S; Brown, MH; Skurray, RA; Brennan, RG. Structural basis for cooperative DNA binding by two dimers of the multidrug-binding protein QacR. EMBO J 2002. Murray, DS#; Schumacher, MA#, Brennan, RG (#These authors contributed equally). Crystal structures of QacR diamidine complexes reveal additional multidrug binding modes and a novel mechanism of drug charge neutralization. J Biol Chem 2004. Schumacher, MA*; Miller, MC; Brennan, RG. Structural mechanism of simultaneous binding of two drugs to a multidrug binding protein. EMBO J 2004.
Independent Publications
Schumacher, MA*; Rivard, AF; Bachinger, HP; Adelman, JP. Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin. Nature 2001. Schumacher, MA*; Todd, JL; Rice, AE; Tanner, KG; Denu, JM. Structural basis for the recognition of a bisphosphorylated MAP kinase peptide by human VHR phosphatase. Biochemistry 2002. Bruening-Wright, A; Schumacher, MA; Adelman, JP; Maylie, J. Localization of the activation gate for small conductance Ca2+-activated K+ channels. J Neurosci 2002. Schumacher, MA; Adelman, JP. Ion channels: An open and shut case. Nature 2002. Schumacher, MA; Brennan, RG. Structural mechanisms of multidrug recognition and regulation by bacterial multidrug transcription factors. Mol Microbiol 2002. Schumacher, MA; Brennan, RG. Deciphering the molecular basis of multidrug recognition: Crystal structures of the Staphylococcus aureus multidrug binding transcription. Res Microbiol 2003. Schumacher, MA*; Lau, AOT; Johnson, PJ. Structural basis of core promoter recognition in a primitive Eukaryote. Cell 2003. Schumacher, MA, Gating domain of calcium-activated potassium channel with calcium and calmodulin. Vol.3 of "the Handbook of Metalloproteins". 2003. Book chapter Schumacher, MA*; Crum, M; Miller, M. Crystal structures of apocalmodulin and an apocalmodulin/SK2 CaMBD complex: mechanism of Ca2+-activated SK channel gating. Structure 2004. Schumacher, MA*; Allen, GS; Diel, M; Seidel, G; Hillen, W; Brennan, RG. Structural basis for allosteric control of the transcription regulator CcpA by the Phosphoprotein HPr-Ser46-P. Cell 2004. Schumacher, MA*; Mizuno, K; Bachinger, HP. The crystal structure of the collagen like polypeptide (glycl-4(R)-hydroxyprolyl-4(R)-hydroxyproyl)9 at 1.5 Å resolution shows up-puckering of the proline ring in the Xaa position. J Biol Chem 2005. Schumacher, MA*; Funnell, BE. ParB-DNA structures reveal mechanism of partition complex formation. Nature 2005. Schumacher, MA*; Seidel, G, Hillen, W, Brennan, RG. Phosphoprotein Crh-Ser46 P displays altered binding to CcpA to effect carbon catabolite represson. J Biol Chem 2006. Schumacher, MA*; Mizuno, K; Bachinger, HP. The crystal structure of the collagen like polypeptide with 3(S)-hydroxyproline residues in the Xaa position forms a standard 72 collagen triple helix. J Biol Chem 2006. Schumacher, MA*; Karamooz, E; Zikova, A; Trantirek, L; Lukes, J. Crystals structures of T. brucei MRP1/MRP2 guide-RNA-binding complex reveals RNA matchmaking mechanism. Cell 2006. Schumacher, MA*; Mansoor, A.; Funnell, BE. Structure of a four-way bridged ParB DNA complex provides insight into P1 segrosome assembly. J Biol Chem 2007. Vecchiarelli, AG; Schumacher, MA; Funnell, BE. P1 partition complex assembly involves several modes of protein-DNA recognition. J Biol Chem 2007. Schumacher, MA*; Seidel, G; Hillen, W; Brennan, RG. Structural mechanisms for the fine tuning of CcpA function by the small molecule effectors glucose-6-phosphate and fructose 1,6 bisphosphate. J Mol Biol 2007. Schumacher, MA*; Glover, TC; Brzoska, AJ; Jensen, SO; Dunham, TD; Skurray, RA; Firth N. Segrosome structure revealed by a complex of ParR with centromere DNA. Nature 2007. Schumacher, MA; Structural biology of plasmid segregation proteins. Curr Opin Struct Biol 2007. Schumacher, MA; Structural biology of plasmid partition: uncovering the molecular mechanisms of DNA segregation. Biochem J 2008. Wilkinson, DS; Tsai, WW; Schumacher, MA; Barton, MC. Chromatin-bound p53 anchors activated Smads and the mSin3A corepressor to confer TGF{beta}-mediated transcription regulation. Mol Cell Biol 2008. Zikova, A; Kopecna, J; Schumacher, MA; Stuart, K; Trantirek, L; Lukes, J. Structure and function of the native and recombinant mitochondrial MRP1/MRP2 complex from Trypanosoma brucei. Int J Parasitol 2008. Peters, KM; Schuman, JT; Skurray, RH; Brown, MH; Brennan, RG; Schumacher, MA*. QacR-cation recognition is mediated by a redundancy of residues capable of charge neutralization. Biochemistry 2008. Boudko, SP; Engel, J; Okuyama, K; Mizuno, K; Bachinger, HP; Schumacher, MA*. Crystal structure of human type III collagen G991-G1032 cystine knot containing peptide shows both 7/2 and 10/3 triple helical symmetries. J Biol Chem 2008. Schumacher, MA*; Piro, KM; Xu, W; Hansen, S; Lewis, K; Brennan, RG. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 2009. Dunham, TD; Xu, W; Funnell, BE; Schumacher, MA*. The ATP-ADP switch mechanism controlling the dual roles of DNA partition and transcription autoregulation by ParA. EMBO J 2009. Ni, L; Jensen, SO; Tonthat, N; Berg, T; Kwong, SA; Guan, FH; Brown, MH; Skurray, RA; Firth, N; Schumacher, MA*. The Staphylococcus aureus pSK41 plasmid encoded ArtA protein is a master regulator or plasmid transmission genes and contains a RHH motif used in alternative DNA-binding modes. Nucl Acids Res 2009. Popp, D; Xu, W; Narita, A; Brzoska, AJ; Skurray, RA; Firth, N; Ghoshdastider, U; Maéda, Y; Robinson, RC; Schumacher, MA*. Structure and filament dynamics of the pSK41 actin-like ParM protein: implications for plasmid DNA segregation. J Biol Chem 2010. Schumacher, MA*; Piro, KM; Xu, W. Insight into F plasmid DNA segregation revealed by structures of SopB and SopB-DNA complexes. Nucl Acids Res 2010. Sprehe, M; Fisk, JC; McEvoy, SM; Read, LK; Schumacher, MA*. Structure of the Trypanosoma brucei p22 protein, a cytochrome oxidase subunit II-specific RNA editing accessory factor. J Biol Chem 2010. Ni, L; Xu, X; Kumaraswami, M; Schumacher, MA*.Plasmid protein TubR uses a distinct mode of HTH DNA binding and recruits the prokaryotic tubulin homolog TubZ to effect DNA partition. Proc Natl Acad Sci USA 2010. Schumacher, MA*; Sprehe, M; Bartholomae, M; Hillen, W; Brennan, RG*. Structures of carbon catabolite protein A (HPr-Ser46-P) bound to diverse catabolite response element sites reveal the basis for high-affinity binding to degenerate DNA operators. Nucl Acids Res 2011. Tonthat, NK; Arold, ST; Pickering, BF; Van Dyke, MW; Liang, S; Lu, Y; Beuria, TK; Margolin, W; Schumacher, MA*. Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 2011. Peters, KM; Brooks, BE; Schumacher, MA; Skurray, RA; Brennan, RG; Brown, MH. A single acidic residue can guide binding site selection but does not govern QacR cationic-drug affinity. PLOS One 2011. Gu, D; Tonthat, NK; Lee, M; Ji, H; Bhat, KP; Hollingsworth, F; Aldape, KD; Schumacher, MA; Zwaka, TP; McCrea, PB. Caspase-3 cleavage links delta-catenin to the novel nuclear protein ZIFCAT. J Biol Chem 2011. Le, TB; Schumacher, MA; Lawson, DM; Brennan, RG; Buttner, MJ. The crystal structure of the TetR family transcriptional repressor SimR bound to DNA and the role of a flexible N-terminal extension in minor groove binding. Nucl Acids Res 2011. Schumacher, MA. Plasmid partition machinery: a minimalist approach to survival. Curr Opin Struct Biol 2012. Takeda, Kp Tonthat, NKp Glover, Tp Xu, Wp Koonin, EVp Yanagida, Mp Schumacher, MA*. Implications for proteasome nuclear localization revealed by the structure of the nuclear proteasome tether protein Cut8. Proc Natl Acad Sci USA 2012. Hansen, S; Vulic, M; Min, J; Yen, TJ; Schumacher, MA; Brennan, RG; Lewis, K. Regulation of the Escherichia coli hipBA toxin-antitoxin system by proteolysis. PLOS One 2012. Schumacher, MA*; Ye, Q; Barge, M; Zampini, M; Barilla, D; Hayes, F. Structural mechanism of ATP induced polymerization of the partition factor ParF: implications for DNA segregation. J Biol Chem 2012. Schumacher, MA*; Link, TM; Guan, Z; Xu, W; Ahn, Y-H; Min, JM; Soderblum EJ; Kurie, JM; Evdokimov, A; Moseley, MA; Lewis, K; Brennan, RG*. Role of unusual P-loop motif ejection and autophosphorylation in the development of HipA-mediated multidrug tolerance. Cell Rep 2012. Dupaigne, P; Tonthat; NK, Espeli, O; Whitfill, T; Boccard, F; Schumacher, MA*. Structural basis for a protein-mediated DNA looping mechanism that functions in long-range organization of the E. coli chromosome. Mol Cell 2012. Highlighted in Science, Editor's Choice. Dobruk-Serkowska, A; Caccamo, M; Wu, M; Bryce, K; Schumacher, MA; Barilla, D; Hayes, F. Uncoupling of nucleotide hydrolysis and polymerization in the ParA superfamily disrupts DNA segregation dynamics. J Biol Chem 2012. Ni, L; Tonthat, NK; Chinnam, N, Schumacher, MA*. Structures of the Escherichia coli transcription activator and regulator of diauxie, XylR: an AraC DNA-binding family member with a LacI/GalR ligand-binding domain. Nucl Acids Res 2013. Tonthat, NK; Milam, SL; Chinnam, N; Whitfill, T; Margolin, W; Schumacher, MA*. SlmA forms a higher order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Proc Natl Acad Sci USA 2013. Schumacher, MA*; Ohashi, T; Shah, R; Chinnam, N; Erickson, H. Structure of exercise induced myokine irisin suggests new paradigm for ligand-mediated signaling. J Biol Chem 2013. Murray, D; Tonthat, NK; Chinnam, N; Fisher, S; Schumacher, MA*. B. subtilis glutamine synthetase structures reveal dramatic intersubunit catalytic changes linked to isoenzyme specific regulation. J Biol Chem 2013. Daniels, KG; Tonthat, NK; McClure, DR; Chang, YC; Liu, X; Schumacher, MA; Fierke, CA; Schmidler, SC; Oas, TG. Ligand concentration regulates the pathways of coupled protein folding and binding. J Am Chem Soc 2013. Schumacher MA*, Tonthat NK, Kwong SM, Chinnam NB, Liu MA, Skurray RA, Firth N. Mechanism of staphylococcal multiresistance plasmid replication origin assembly by the RepA protein. Proc Natl Acad Sci USA 2014. Emptage RP, Tonthat NK, York JD, Schumacher MA, Zhou P*. Structural basis of lipid binding for the membrane-embedded tetraacyldisaccharide-1-phosphate 4'-kinase LpxK. J Biol Chem 2014. Tschowri N#, Schumacher MA#, Schlimpert S, Chinnam NB, Findlay KC, Brennan RG, Buttner MJ.*Tetrameric c-di-GMP mediates effective transcription factor dimerization to control Streptomyces development. Cell 2014. Schumacher, MA*, Chinnam NB, Cuthbert B, Tonthat NK, Whitfill T. Structures of regulatory machinery reveal novel molecular mechanisms controlling B. subtilis nitrogen homeostasis. Genes Dev 2015. Hover BM, Tonthat NK, Schumacher MA*,Yokoyama K*. Mechanism of pyranopterin ring formation in molybdenum cofactor biosynthesis. Proc Natl Acad Sci USA 2015. Lee SC, Li A, Calo S, Inoue M, Tonthat NK, Bain JM, Louw J, Shinohara ML, Erwig LP, Schumacher MA, Ko DC, Heitman J.*. Calcineurin orchestrates dimorphic transitions, antifungal drug responses and host-pathogen interactions of the pathogenic mucoralean fungus Mucor circinelloides. Mol Microbiol 2015. Shaw PL, McAdams NM, Hast MA, Ammerman ML, Read LK,Schumacher, MA*. Structures of the T. brucei kRNA editing factor MRB1590 reveal unique RNA-binding pore motif contained within an ABC-ATPase fold. Nucleic Acids Res 2015. Cuthbert BJ, Brennan RG*, Schumacher, MA*. Structural and Biochemical Characterization of the Francisella tularensis Pathogenicity Regulator, Macrophage Locus Protein A (MglA). PLoS One 2015. Schumacher, MA*; Balani, P; Min, J; Chinnam, NB; Hansen, S; Vulić, M; Lewis, K*; Brennan, RG*. HipBA-promoter structures reveal the basis of heritable multidrug tolerance. Nature. 2015. Schumacher, MA*; Tonthat, NK; Lee, J; Rodriguez-Castaneda FA; Chinnam, NB; Kalliomaa-Sanford, AK; Ng IW; Barge, MT; Shaw, PL; Barilla, D*. Structures of archaeal DNA segregation machinery reveal bacterial and eukaryotic linkages. Science 2015. Schumacher, MA*; Zeng, W; Huang, KH, Tchorzewski; L Janakiraman, A*. Structural and functional analyses reveal insights into the molecular properties of the Escherichia coli Z ring stabilizing protein, ZapC. J Biol Chem 2016. Tonthat, NK; Juvvadi, PR; Zhang, H; Lee SC; Venters, R; Spicer, L; Steinbach, WJ; Heitman, J; Schumacher, MA*. Structures of pathogenic fungal FKBP12s reveal possible self-catalysis function. mBio 2016. Schumacher, MA*; Zeng, W. Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ. Proc Natl Acad Sci USA 2016. Schumacher, MA*; Lee, J; Zeng, W. Molecular insights into DNA binding and anchoring by the Bacillus subtilis sporulation kinetochore-like RacA protein. Nucleic Acids Res 2016. Miao, Y; Tenor, JL; Toffaletti, DL; Washington, EJ; Liu, J; Shadrick, WR; Schumacher, MA, Lee, RE; Perfect, JR; Brennan, RG*. Structures of trehalose-6-phosphate phosphatase from pathogenic fungi reveal the mechanisms of substrate recognition and catalysis. Proc Natl Acad Sci USA 2016. Schumacher, MA*; Zeng, W. Structures of K. pneumonia MrkH reveal dual utilization of the PilZ fold for c-di-GMP and DNA binding by a novel activator of biofilm genes. Proc Natl Acad Sci USA 2016. McLeod, BN, Allison-Gamble, GE, Barge, MT, Tonthat, NK, Schumacher, MA, Hayes, F, Barilla, D.*. A three-dimensional ParF meshwork assembles through the nucleoid to mediate plasmid segregation. Nucleic Acids Res 2017. Schumacher, MA*; Huang, K-H; Zeng, W; Janakiraman, A*. Structure of the Z ring associated protein, ZapD, bound to the C-terminal domain of the tubulin-like protein, FtsZ, suggests mechanism of Z ring stabilization through FtsZ crosslinking. J. Biol. Chem 2017. Zhang, H; Schumacher, MA*. Structures of partition protein ParA with nonspecific DNA and ParB effector reveal molecular insights into principles governing Walker-box DNA segregation. Genes Dev 2017. Schumacher, MA*; Zheng, W; Findlay, K.C.; Buttner, M.J.; Brennan, R.G.; Tschowri, N. The Streptomyces master regulator BldD binds c-dGMP sequentially to create a functional BldD2-(c-di-GMP)4 complex. Nucleic Acids Res 2017. Schumacher, MA*. Bacterial nucleoid occlusion: Multiple mechanism for preventing chromosome bisection during cell division. Subcell Biochem 2017. Cuthbert, B.J.; Ross, W.; Rohlfing, A. E.;, Dove, S.L.; Gourse, R.L.; Brennan, R.G.*; Schumacher, MA*. Dissection of the molecular circuitry controlling virulence in Francisella tularensis. Genes Dev 2017. In press