2023

Gipson, G. R., Nolan, K., Kattamuri, C., Kenny, A. P., Agricola, Z., Edwards, N. A., Zinski, J., Czepnik, M., Mullins, M. C., Zorn, A. M. & Thompson, T. B. Formation and characterization of BMP2/GDF5 and BMP4/GDF5 heterodimers. BMC Biol 21, 16 (2023). PDB: 8E3G

Kappes, E. C., Kattamuri, C., Czepnik, M., Yarawsky, A. E., Brûlé, E., Wang, Y., Ongaro, L., Herr, A. B., Walton, K. L., Bernard, D. J. & Thompson, T. B. Follistatin Forms a Stable Complex With Inhibin A That Does Not Interfere With Activin A Antagonism. Endocrinology 164, bqad017 (2023).

2022

Goebel, E. J., Ongaro, L., Kappes, E. C., Vestal, K., Belcheva, E., Castonguay, R., Kumar, R., Bernard, D. J. & Thompson, T. B. The orphan ligand, activin C, signals through activin receptor-like kinase 7. eLife 11, e78197 (2022).

Howard, J. A., Hart, K. N. & Thompson, T. B. Molecular Mechanisms of AMH Signaling. Front Endocrinol (Lausanne) 13, 927824 (2022).

Goebel, E. J., Kattamuri, C., Gipson, G. R., Krishnan, L., Chavez, M., Czepnik, M., Maguire, M. C., Grenha, R., Håkansson, M., Logan, D. T., Grinberg, A. V., Sako, D., Castonguay, R., Kumar, R. & Thompson, T. B. Structures of activin ligand traps using natural sets of type I and type II TGFβ receptors. iScience 25, 103590 (2022). PDB: 7MRZ

2021

Rydze, R. T., Patton, B. K., Briley, S. M., Salazar Torralba, H., Gipson, G., James, R., Rajkovic, A., Thompson, T. & Pangas, S. A. Deletion of Gremlin-2 alters estrous cyclicity and disrupts female fertility in mice†. Biol Reprod 105, 1205–1220 (2021).

Brown, M. L., Lopez, A., Meyer, N., Richter, A. & Thompson, T. B. FSTL3-Neutralizing Antibodies Enhance Glucose-Responsive Insulin Secretion in Dysfunctional Male Mouse and Human Islets. Endocrinology 162, bqab019 (2021).

Hart, K. N., Stocker, W. A., Nagykery, N. G., Walton, K. L., Harrison, C. A., Donahoe, P. K., Pépin, D. & Thompson, T. B. Structure of AMH bound to AMHR2 provides insight into a unique signaling pair in the TGF-β family. PNAS 118, (2021). PDB: 7L0J

McCoy, J. C., Goebel, E. J. & Thompson, T. B. Characterization of tolloid-mediated cleavage of the GDF8 procomplex. Biochem J (2021).

Walker, R. G., Kattamuri, C., Goebel, E. J., Zhang, F., Hammel, M., Tainer, J. A., Linhardt, R. J. & Thompson, T. B. Heparin-mediated dimerization of follistatin. Exp Biol Med (Maywood) 246, 467–482 (2021).

2020

Gipson, G. R., Goebel, E. J., Hart, K. N., Kappes, E. C., Kattamuri, C., McCoy, J. C. & Thompson, T. B. Structural perspective of BMP ligands and signaling. Bone 140, 115549 (2020).

Gipson, G. R., Kattamuri, C., Czepnik, M. & Thompson, T. B. Characterization of the different oligomeric states of the DAN family antagonists SOSTDC1 and SOST. Biochem J 477, 3167–3182 (2020).

Hart, K. N., Pépin, D., Czepnik, M., Donahoe, P. K. & Thompson, T. B. Mutational Analysis of the Putative Anti-Müllerian Hormone (AMH) Binding Interface on its Type II Receptor, AMHR2. Endocrinology 161, (2020).

Aykul, S., Corpina, R. A., Goebel, E. J., Cunanan, C. J., Dimitriou, A., Kim, H. J., Zhang, Q., Rafique, A., Leidich, R., Wang, X., McClain, J., Jimenez, J., Nannuru, K. C., Rothman, N. J., Lees-Shepard, J. B., Martinez-Hackert, E., Murphy, A. J., Thompson, T. B., Economides, A. N. & Idone, V. Activin A forms a non-signaling complex with ACVR1 and type II Activin/BMP receptors via its finger 2 tip loop. Elife 9, (2020).

Castleberry, M., Davis, X., Liu, M., Thompson, T. B., Tso, P. & Davidson, W. S. Functional recombinant apolipoprotein A5 that is stable at high concentrations at physiological pH. J Lipid Res 61, 244–251 (2020).

2019

Thompson, T. B. & Kovall, R. A. Structural biology: Gaining atomic level insight into the biological function of macromolecules. Exp Biol Med (Maywood) 244, 1507–1509 (2019).

Goebel, E. J., Hart, K. N., McCoy, J. C. & Thompson, T. B. Structural biology of the TGFβ family. Exp. Biol. Med. (Maywood) 244, 1530–1546 (2019).

Cox, T. C., Lidral, A. C., McCoy, J. C., Liu, H., Cox, L. L., Zhu, Y., Anderson, R. D., Moreno Uribe, L. M., Anand, D., Deng, M., Richter, C. T., Nidey, N. L., Standley, J. M., Blue, E. E., Chong, J. X., Smith, J. D., Kirk, E. P., Venselaar, H., Krahn, K. N., van Bokhoven, H., Zhou, H., Cornell, R. A., Glass, I. A., Bamshad, M. J., Nickerson, D. A., Murray, J. C., Lachke, S. A., Thompson, T. B., Buckley, M. F. & Roscioli, T. Mutations in GDF11 and the extracellular antagonist, Follistatin, as a likely cause of Mendelian forms of orofacial clefting in humans. Hum Mutat 40, 1813–1825 (2019).

Goebel, E. J., Corpina, R. A., Hinck, C. S., Czepnik, M., Castonguay, R., Grenha, R., Boisvert, A., Miklossy, G., Fullerton, P. T., Matzuk, M. M., Idone, V. J., Economides, A. N., Kumar, R., Hinck, A. P. & Thompson, T. B. Structural characterization of an activin class ternary receptor complex reveals a third paradigm for receptor specificity. Proc. Natl. Acad. Sci. U.S.A. 116, 15505–15513 (2019). PDB: 6MAC

Czaja, W., Nakamura, Y. K., Li, N., Eldridge, J. A., DeAvila, D. M., Thompson, T. B. & Rodgers, B. D. Myostatin regulates pituitary development and hepatic IGF1. Am J Physiol Endocrinol Metab 316, E1036–E1049 (2019).

McCoy, J. C., Walker, R. G., Murray, N. H. & Thompson, T. B. Crystal structure of the WFIKKN2 follistatin domain reveals insight into how it inhibits growth differentiation factor 8 (GDF8) and GDF11. J. Biol. Chem. 294, 6333–6343 (2019). PDB: 6MAA

Panmanee, W., Su, S., Schurr, M. J., Lau, G. W., Zhu, X., Ren, Z., McDaniel, C. T., Lu, L. J., Ohman, D. E., Muruve, D. A., Panos, R. J., Yu, H. D., Thompson, T. B., Tseng, B. S. & Hassett, D. J. The anti-sigma factor MucA of Pseudomonas aeruginosa: Dramatic differences of a mucA22 vs. a ΔmucA mutant in anaerobic acidified nitrite sensitivity of planktonic and biofilm bacteria in vitro and during chronic murine lung infection. PLoS One 14, e0216401 (2019).

2018

Walker, R. G. & Thompson, T. B. New Insight Into Hyperemesis Gravidarum and a Potential Role for GDF15. Endocrinology 159, 2698–2700 (2018).

Cooke, A. L., Morris, J., Melchior, J. T., Street, S. E., Jerome, W. G., Huang, R., Herr, A. B., Smith, L. E., Segrest, J. P., Remaley, A. T., Shah, A. S., Thompson, T. B. & Davidson, W. S. A thumbwheel mechanism for APOA1 activation of LCAT activity in HDL. J. Lipid Res. 59, 1244–1255 (2018).

Cotton, T. R., Fischer, G., Wang, X., McCoy, J. C., Czepnik, M., Thompson, T. B. & Hyvönen, M. Structure of the human myostatin precursor and determinants of growth factor latency. EMBO J. 37, 367–383 (2018).

Walker, R. G., McCoy, J. C., Czepnik, M., Mills, M. J., Hagg, A., Walton, K. L., Cotton, T. R., Hyvönen, M., Lee, R. T., Gregorevic, P., Harrison, C. A. & Thompson, T. B. Molecular characterization of latent GDF8 reveals mechanisms of activation. Proc. Natl. Acad. Sci. U.S.A. 115, E866–E875 (2018).

Bernard, D. J., Schang, G., Li, Y., Ongaro, L. & Thompson, T. B. Activins and Inhibins in Female Reproduction. in Encyclopedia of Reproduction (Second Edition) (ed. Skinner, M. K.) 202–210 (Academic Press, 2018).

2017

Melchior, J. T., Walker, R. G., Cooke, A. L., Morris, J., Castleberry, M., Thompson, T. B., Jones, M. K., Song, H. D., Rye, K.-A., Oda, M. N., Sorci-Thomas, M. G., Thomas, M. J., Heinecke, J. W., Mei, X., Atkinson, D., Segrest, J. P., Lund-Katz, S., Phillips, M. C. & Davidson, W. S. A consensus model of human apolipoprotein A-I in its monomeric and lipid-free state. Nat. Struct. Mol. Biol. 24, 1093–1099 (2017).

Bylund, J. B., Trinh, L. T., Awgulewitsch, C. P., Paik, D. T., Jetter, C., Jha, R., Zhang, J., Nolan, K., Xu, C., Thompson, T. B., Kamp, T. J. & Hatzopoulos, A. K. Coordinated Proliferation and Differentiation of Human-Induced Pluripotent Stem Cell-Derived Cardiac Progenitor Cells Depend on Bone Morphogenetic Protein Signaling Regulation by GREMLIN 2. Stem Cells Dev. 26, 678–693 (2017).

Kattamuri, C., Nolan, K. & Thompson, T. B. Analysis and identification of the Grem2 heparin/heparan sulfate-binding motif. Biochem. J. 474, 1093–1107 (2017).

Walker, R. G., Czepnik, M., Goebel, E. J., McCoy, J. C., Vujic, A., Cho, M., Oh, J., Aykul, S., Walton, K. L., Schang, G., Bernard, D. J., Hinck, A. P., Harrison, C. A., Martinez-Hackert, E., Wagers, A. J., Lee, R. T. & Thompson, T. B. Structural basis for potency differences between GDF8 and GDF11. BMC Biol. 15, 19 (2017). PDBs: 5JI1 5JHW 5UHM

2016

Yilmaz, A., Kattamuri, C., Ozdeslik, R. N., Schmiedel, C., Mentzer, S., Schorl, C., Oancea, E., Thompson, T. B. & Fallon, J. R. MuSK is a BMP co-receptor that shapes BMP responses and calcium signaling in muscle cells. Sci Signal 9, ra87 (2016).

Nolan, K., Kattamuri, C., Rankin, S. A., Read, R. J., Zorn, A. M. & Thompson, T. B. Structure of Gremlin-2 in Complex with GDF5 Gives Insight into DAN-Family-Mediated BMP Antagonism. Cell Rep 16, 2077–2086 (2016). PDB: 5HK5

Sanders, L. N., Schoenhard, J. A., Saleh, M. A., Mukherjee, A., Ryzhov, S., McMaster, W. G., Nolan, K., Gumina, R. J., Thompson, T. B., Magnuson, M. A., Harrison, D. G. & Hatzopoulos, A. K. BMP Antagonist Gremlin 2 Limits Inflammation After Myocardial Infarction. Circ. Res. 119, 434–449 (2016).

Walker, R. G., Poggioli, T., Katsimpardi, L., Buchanan, S. M., Oh, J., Wattrus, S., Heidecker, B., Fong, Y. W., Rubin, L. L., Ganz, P., Thompson, T. B., Wagers, A. J. & Lee, R. T. Biochemistry and Biology of GDF11 and Myostatin: Similarities, Differences, and Questions for Future Investigation. Circ. Res. 118, 1125–1141; discussion 1142 (2016).

Melchior, J. T., Walker, R. G., Morris, J., Jones, M. K., Segrest, J. P., Lima, D. B., Carvalho, P. C., Gozzo, F. C., Castleberry, M., Thompson, T. B. & Davidson, W. S. An Evaluation of the Crystal Structure of C-terminal Truncated Apolipoprotein A-I in Solution Reveals Structural Dynamics Related to Lipid Binding. J. Biol. Chem. 291, 5439–5451 (2016).

Poggioli, T., Vujic, A., Yang, P., Macias-Trevino, C., Uygur, A., Loffredo, F. S., Pancoast, J. R., Cho, M., Goldstein, J., Tandias, R. M., Gonzalez, E., Walker, R. G., Thompson, T. B., Wagers, A. J., Fong, Y. W. & Lee, R. T. Circulating Growth Differentiation Factor 11/8 Levels Decline With Age. Circ. Res. 118, 29–37 (2016).

Li, N., Yang, Q., Walker, R. G., Thompson, T. B., Du, M. & Rodgers, B. D. Myostatin Attenuation In Vivo Reduces Adiposity, but Activates Adipogenesis. Endocrinology 157, 282–291 (2016).

2015

Walker, R. G. & Thompson, T. B. Fibronectin-based scaffold domain proteins that bind myostatin: a patent evaluation of WO2014043344. Expert Opin Ther Pat 25, 619–624 (2015).

Deng, X., Walker, R. G., Morris, J., Davidson, W. S. & Thompson, T. B. Role of Conserved Proline Residues in Human Apolipoprotein A-IV Structure and Function. J. Biol. Chem. 290, 10689–10702 (2015).

Walker, R. G., Angerman, E. B., Kattamuri, C., Lee, Y.-S., Lee, S.-J. & Thompson, T. B. Alternative binding modes identified for growth and differentiation factor-associated serum protein (GASP) family antagonism of myostatin. J. Biol. Chem. 290, 7506–7516 (2015).

Nolan, K., Kattamuri, C., Luedeke, D. M., Angerman, E. B., Rankin, S. A., Stevens, M. L., Zorn, A. M. & Thompson, T. B. Structure of neuroblastoma suppressor of tumorigenicity 1 (NBL1): insights for the functional variability across bone morphogenetic protein (BMP) antagonists. J. Biol. Chem. 290, 4759–4771 (2015). PDB: 4X1J

2014

Peng, J., Wigglesworth, K., Rangarajan, A., Eppig, J. J., Thompson, T. B. & Matzuk, M. M. Amino acid 72 of mouse and human GDF9 mature domain is responsible for altered homodimer bioactivities but has subtle effects on GDF9:BMP15 heterodimer activities. Biol. Reprod. 91, 142 (2014).

Nolan, K. & Thompson, T. B. The DAN family: modulators of TGF-β signaling and beyond. Protein Sci. 23, 999–1012 (2014).

Rodgers, B. D., Wiedeback, B. D., Hoversten, K. E., Jackson, M. F., Walker, R. G. & Thompson, T. B. Myostatin stimulates, not inhibits, C2C12 myoblast proliferation. Endocrinology 155, 670–675 (2014).

Walker, R. G., Deng, X., Melchior, J. T., Morris, J., Tso, P., Jones, M. K., Segrest, J. P., Thompson, T. B. & Davidson, W. S. The structure of human apolipoprotein A-IV as revealed by stable isotope-assisted cross-linking, molecular dynamics, and small angle x-ray scattering. J. Biol. Chem. 289, 5596–5608 (2014).

2013

Rejon, C. A., Hancock, M. A., Li, Y. N., Thompson, T. B., Hébert, T. E. & Bernard, D. J. Activins bind and signal via bone morphogenetic protein receptor type II (BMPR2) in immortalized gonadotrope-like cells. Cell. Signal. 25, 2717–2726 (2013).

Nolan, K., Kattamuri, C., Luedeke, D. M., Deng, X., Jagpal, A., Zhang, F., Linhardt, R. J., Kenny, A. P., Zorn, A. M. & Thompson, T. B. Structure of protein related to Dan and Cerberus: insights into the mechanism of bone morphogenetic protein antagonism. Structure 21, 1417–1429 (2013). PDB: 4JPH

Cash, J. N., Angerman, E. B., Kirby, R. J., Merck, L., Seibel, W. L., Wortman, M. D., Papoian, R., Nelson, S. & Thompson, T. B. Development of a small-molecule screening method for inhibitors of cellular response to myostatin and activin A. J Biomol Screen 18, 837–844 (2013).

Peng, J., Li, Q., Wigglesworth, K., Rangarajan, A., Kattamuri, C., Peterson, R. T., Eppig, J. J., Thompson, T. B. & Matzuk, M. M. Reply to Mottershead et al.: GDF9:BMP15 heterodimers are potent regulators of ovarian functions. Proc Natl Acad Sci U S A 110, E2258 (2013).

Peng, J., Li, Q., Wigglesworth, K., Rangarajan, A., Kattamuri, C., Peterson, R. T., Eppig, J. J., Thompson, T. B. & Matzuk, M. M. Growth differentiation factor 9:bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc. Natl. Acad. Sci. U.S.A. 110, E776-785 (2013).

Deng, X., Morris, J., Chaton, C., Schröder, G. F., Davidson, W. S. & Thompson, T. B. Small-angle X-ray scattering of apolipoprotein A-IV reveals the importance of its termini for structural stability. J. Biol. Chem. 288, 4854–4866 (2013).

2012

Kattamuri, C., Luedeke, D. M., Nolan, K., Rankin, S. A., Greis, K. D., Zorn, A. M. & Thompson, T. B. Members of the DAN family are BMP antagonists that form highly stable noncovalent dimers. J. Mol. Biol. 424, 313–327 (2012).

Zhang, F., Beaudet, J. M., Luedeke, D. M., Walker, R. G., Thompson, T. B. & Linhardt, R. J. Analysis of the interaction between heparin and follistatin and heparin and follistatin-ligand complexes using surface plasmon resonance. Biochemistry 51, 6797–6803 (2012).

Cash, J. N., Angerman, E. B., Keutmann, H. T. & Thompson, T. B. Characterization of follistatin-type domains and their contribution to myostatin and activin A antagonism. Mol. Endocrinol. 26, 1167–1178 (2012).

Deng, X., Morris, J., Dressmen, J., Tubb, M. R., Tso, P., Jerome, W. G., Davidson, W. S. & Thompson, T. B. The structure of dimeric apolipoprotein A-IV and its mechanism of self-association. Structure 20, 767–779 (2012). PDB: 3S84

Kattamuri, C., Luedeke, D. M. & Thompson, T. B. Expression and purification of recombinant protein related to DAN and cerberus (PRDC). Protein Expr. Purif. 82, 389–395 (2012).

Cash, J. N., Angerman, E. B., Kattamuri, C., Nolan, K., Zhao, H., Sidis, Y., Keutmann, H. T. & Thompson, T. B. Structure of myostatin·follistatin-like 3: N-terminal domains of follistatin-type molecules exhibit alternate modes of binding. J. Biol. Chem. 287, 1043–1053 (2012). PDB: 3SEK

Deng, X., Davidson, W. S. & Thompson, T. B. Improving the diffraction of apoA-IV crystals through extreme dehydration. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68, 105–110 (2012).

2011

Syed, K., Kattamuri, C., Thompson, T. B. & Yadav, J. S. Cytochrome b₅ reductase-cytochrome b₅ as an active P450 redox enzyme system in Phanerochaete chrysosporium: atypical properties and in vivo evidence of electron transfer capability to CYP63A2. Arch Biochem Biophys 509, 26–32 (2011).

2009

Cash, J. N., Rejon, C. A., McPherron, A. C., Bernard, D. J. & Thompson, T. B. The structure of myostatin:follistatin 288: insights into receptor utilization and heparin binding. EMBO J. 28, 2662–2676 (2009). PDB: 3HH2

2008

Stamler, R., Keutmann, H. T., Sidis, Y., Kattamuri, C., Schneyer, A. & Thompson, T. B. The structure of FSTL3.activin A complex. Differential binding of N-terminal domains influences follistatin-type antagonist specificity. J. Biol. Chem. 283, 32831–32838 (2008). PDB: 3B4V

2007

Davidson, W. S. & Thompson, T. B. The structure of apolipoprotein A-I in high density lipoproteins. J. Biol. Chem. 282, 22249–22253 (2007).

2005

Cook, R. W., Thompson, T. B., Kurup, S. P., Jardetzky, T. S. & Woodruff, T. K. Structural basis for a functional antagonist in the transforming growth factor beta superfamily. J. Biol. Chem. 280, 40177–40186 (2005).

Thompson, T. B., Lerch, T. F., Cook, R. W., Woodruff, T. K. & Jardetzky, T. S. The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Dev. Cell 9, 535–543 (2005). PDB: 2B0U

Yuan, P., Thompson, T. B., Wurzburg, B. A., Paterson, R. G., Lamb, R. A. & Jardetzky, T. S. Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13, 803–815 (2005).

2004

Thompson, T. B., Cook, R. W., Chapman, S. C., Jardetzky, T. S. & Woodruff, T. K. Beta A versus beta B: is it merely a matter of expression? Mol. Cell. Endocrinol. 225, 9–17 (2004).

Thompson, T. B., Katayama, K., Watanabe, K., Hutchinson, C. R. & Rayment, I. Structural and functional analysis of tetracenomycin F2 cyclase from Streptomyces glaucescens. A type II polyketide cyclase. J. Biol. Chem. 279, 37956–37963 (2004).

Cook, R. W., Thompson, T. B., Jardetzky, T. S. & Woodruff, T. K. Molecular biology of inhibin action. Semin. Reprod. Med. 22, 269–276 (2004).

2003

Thompson, T. B., Woodruff, T. K. & Jardetzky, T. S. Structures of an ActRIIB:activin A complex reveal a novel binding mode for TGF-beta ligand:receptor interactions. EMBO J. 22, 1555–1566 (2003). PDBs: 1NYU 1NYS

2001

Bauer, C. B., Fonseca, M. V., Holden, H. M., Thoden, J. B., Thompson, T. B., Escalante-Semerena, J. C. & Rayment, I. Three-dimensional structure of ATP:corrinoid adenosyltransferase from Salmonella typhimurium in its free state, complexed with MgATP, or complexed with hydroxycobalamin and MgATP. Biochemistry 40, 361–374 (2001).

2000

Thomas, M. G., Thompson, T. B., Rayment, I. & Escalante-Semerena, J. C. Analysis of the adenosylcobinamide kinase/adenosylcobinamide-phosphate guanylyltransferase (CobU) enzyme of Salmonella typhimurium LT2. Identification of residue His-46 as the site of guanylylation. J Biol Chem 275, 27576–27586 (2000).

Thompson, T. B., Garrett, J. B., Taylor, E. A., Meganathan, R., Gerlt, J. A. & Rayment, I. Evolution of enzymatic activity in the enolase superfamily: structure of o-succinylbenzoate synthase from Escherichia coli in complex with Mg2+ and o-succinylbenzoate. Biochemistry 39, 10662–10676 (2000).

1999

Thompson, T. B., Thomas, M. G., Escalante-Semerena, J. C. & Rayment, I. Three-dimensional structure of adenosylcobinamide kinase/adenosylcobinamide phosphate guanylyltransferase (CobU) complexed with GMP: evidence for a substrate-induced transferase active site. Biochemistry 38, 12995–13005 (1999).

1998

Thompson, T. B., Thomas, M. G., Escalante-Semerena, J. C. & Rayment, I. Three-dimensional structure of adenosylcobinamide kinase/adenosylcobinamide phosphate guanylyltransferase from Salmonella typhimurium determined to 2.3 A resolution,. Biochemistry 37, 7686–7695 (1998).

1996

Fisher, A. J., Thompson, T. B., Thoden, J. B., Baldwin, T. O. & Rayment, I. The 1.5-A resolution crystal structure of bacterial luciferase in low salt conditions. J Biol Chem 271, 21956–21968 (1996).

1995

Thompson, T. B., Chou, K. C. & Zheng, C. Neural network prediction of the HIV-1 protease cleavage sites. J Theor Biol 177, 369–379 (1995).

Thompson, T. B., Chou, K. C. & Zheng, C. Analysis of the loop-helix interaction in bundle motif protein structures. J Protein Chem 14, 559–566 (1995).