Publications


Bhar, S.*, Yoon, C.-S.*, Mai, K., Han, J., Prajapati, D.V., Wang, Y., Steffen, C.L., Bailey, L.S., Basso, K.B., Butcher, R.A., An acyl-CoA thioesterase is essential for the biosynthesis of the dauer pheromone in C. elegansCell Chem. Biol. (2024) doi: 10.1016/j.chembiol.2023.12.006. 


Wu, T., Ge, M., Wu, M., Duan, F., Liang, J., Chen., M., Gracida, X., Liu, H., Yang, W., Dar, A.R., Butcher, R.A., Saltzman, A.L., Zhang, Y., Pathogenic bacteria modulate pheromone response to promote mating. Nature (2023) 613: 324-331.


Abraham, E., Butcher, R.A., Warhead assembly in a lethal pathogen.  Nat. Chem. (2022) 14:848850.


Shimizu, T., Sugiura, K., Sakai, Y., Dar, A.R., Butcher, R.A., Matsumoto, K., Hisamoto, N., Chemical signaling regulates axon regeneration via the GPCR-Gqa pathway in Caenorhabditis elegansJ. Neurosci. (2022) 42:720-730. 


Wasson, J.A., Harris, G., Keppler-Ross, S., Centko, R.M., Brock, T.J., Dar, A.R., Butcher, R.A., Fischer, S.E.J., Kagias, K., Clardy, J., Zhang, Y., Mango, S., Neuronal control of maternal provisioning in response to social cues.  Sci. Adv. (2021) 7:eabf8782. doi: 10.1126/sciadv.abf8782. 


Feng, L., Gordon, M.T., Liu, Y., Basso, K.B., Butcher, R.A., Mapping the biosynthetic pathway of a hybrid polyketide-nonribosomal peptide in a metazoan. Nat. Commun. (2021) 12:4912. doi: 10.1038/s41467-021-24682-9.


Park, J., Oh, H., Kim, D.-Y., Cheon, Y., Park, Y.-J., Neal, S.J., Dar., A.R., Butcher, R.A., Sengupta, P., Kim, D., Kim, K., CREB mediates the C. elegans dauer polyphenism through direct and cell-autonomous regulation of TGF-β expression. PLoS Genetics. (2021) 17:e1009678.  doi: 10.1371/journal.pgen.1009678.


Faghih, N.*, Bhar, S.*, Zhou, Y., Dar, A.R., Mai, K., Bailey, L.S., Basso, K.B., Butcher, R.A., A large family of enzymes responsible for the modular architecture of nematode pheromones. J. Am. Chem. Soc. (2020) doi: 10.1021/jacs.0c04223.


Butcher, R.A., Natural products as chemical tools to dissect complex biology in C. elegans. Curr. Opin. Chem. Biol. (2019) 50:138-144.


Roder, A.C., Wang, Y., Butcher, R.A., Stock, S.P., Influence of symbiotic and non-symbiotic bacteria on pheromone production in Steinernema nematodes (Nematoda, Steinernematidae). J. Exp. Biol. (2019) 222:jeb212068. doi:10.1242/jeb.212068.


Wu, T., Duan, F., Yang, W., Liu, H., Caballero, A., Fernandes de Abreu, D.A., Dar, A.R., Alcedo, J., Ch’ng, Q., Butcher, R.A., Zhang, Y., Pheromones modulate learning by regulating the balanced signals of two insulin-like peptides. Neuron (2019) 104:1095-1109.


Zhou, Y., Zhang, X., Butcher, R.A., Tryptophan metabolism in Caenorhabditis elegans links aggregation behavior to nutritional status. ACS Chem. Biol. (2019) 14:50-57.

Trp


Park, J., Choi, W., Dar, A.R., Butcher, R.A., Kim, K., Neuropeptide signaling regulates pheromone-mediated gene expression of a chemoreceptor gene in C. elegans. Mol. Cells (2018) doi: 10.14348/molcells.2018.0380.


Ryu, L., Cheon, Y., Huh, Y.H., Pyo, S., Chinta, S., Butcher, R.A., Kim, K., Feeding state regulates pheromone-mediated avoidance behavior via the insulin signaling pathway in Caenorhabditis elegans. EMBO J. (2018) 37(15). pii: e98402. doi: 10.15252/embj.201798402.


Zhou, Y.*, Wang, Y.*, Zhang, X., Bhar, S., Jones Lipinski, R.A., Han, J., Feng, L., Butcher, R.A., Biosynthetic tailoring of existing ascarosides alters their biological function in C. elegans. Elife (2018) 7. pii: e33286. doi: 10.7554/eLife.33286.


Zhang, X.*, Wang, Y.*, Perez, D.H., Jones Lipinski, R.A., Butcher, R.A., Acyl-CoA oxidases fine-tune the production of ascaroside pheromones with specific side chain lengths. ACS Chem. Biol. (2018) 13:1048-56.


Hong, M., Ryu, L., Ow, M.C., Kim, J., Je, A.R., Chinta, S., Huh, Y.H., Lee, K.J., Butcher, R.A., Choi, H., Sengupta, P., Hall, S.E., Kim, K., Early pheromone experience modifies a synaptic activity to influence adult pheromone responses of C. elegans. Curr. Biol. (2017) 27:3168-77.


Butcher, R.A., Small-molecule signals controlling nematode development. Nat. Chem. Biol. (2017) 13:577-86.


Zhou, Y., Loeza-Cabrera, M., Liu, Z., Aleman-Meza, B., Nguyen, J.K., Jung, S.K., Choi, Y., Shou, Q., Butcher, R.A., Zhong, W., Potential nematode alarm pheromone induces acute avoidance in Caenorhabditis elegans. Genetics (2017) 206:1469-78.


Butcher, R.A., Decoding chemical communication in nematodes. Nat. Prod. Rep. (2017) 34:472-77.


Chen, C., Itakura, E., Nelson, G.M., Sheng, M., Laurent, P., Fenk, L.A., Butcher, R.A., Hegde, R.S., de Bono, M., IL-17 is a neuromodulator of Caenorhabditis elegans sensory responses. Nature (2017) 542:43-48.


Greene, J.S., Dobosiewicz, M., Butcher, R.A., McGrath, P.T., Bargmann, C.I., Regulatory changes in two chemoreceptor genes contribute to a Caenorhabditis elegans QTL for foraging behavior. Elife (2016) 5. pii: e21454. doi: 10.7554/eLife.21454.


Greene, J.S., Brown, M., Dobosiewicz, M., Ishida, I.G., Macosko, E.Z., Zhang, X., Butcher, R.A., Cline, D.J., McGrath, P.T., Bargmann, C.I., Balancing selection shapes density-dependent foraging behavior. Nature (2016) 539:254-8.


Zhang, X., Li, K., Jones, R.A., Bruner, S.D., Butcher, R.A., Structural characterization of acyl-CoA oxidases reveals a direct link between pheromone biosynthesis and metabolic state in C. elegans. Proc. Natl. Acad. Sci. U S A (2016) 113: 10055-10060.


Shou, Q.*, Feng, L.*, Long, Y., Han, J., Nunnery, J.K., Powell, D.H., Butcher, R.A., A hybrid polyketide-nonribosomal peptide in nematodes that promotes larval survival. Nat. Chem. Biol. (2016) 12:770-2.


Zhao, L., Zhang, X., Wei, Y., Zhou, J., Zhang, W., Qin, P., Chinta, S., Kong, X., Liu, Y., Yu, H., Hu, S., Zou, Z., Butcher, R.A., Sun, J., Ascarosides coordinate the dispersal of a plant-parasitic nematode with the metamorphosis of its vector beetle. Nat. Commun. (2016) 7:12341.


Large, E.E., Xu, W., Zhao, Y., Brady, S.C., Long, L., Butcher, R.A., Andersen, E.C., McGrath, P.T., Selection on a subunit of the NURF chromatin remodeler modifies life history traits in C. elegans. PLOS Genet. (2016) 12(7):e1006219. doi: 10.1371/journal.pgen.1006219.


Feng, L., Shou, Q., Butcher, R.A., Identification of a dTDP-rhamnose biosynthetic pathway that oscillates with the molting cycle in the nematode Caenorhabditis elegans. Biochem. J. (2016) 473:1507-21.


Neal, S.J., Takeishi, A., O’Donnell, M.P., Park, J., Hong, M., Butcher, R.A., Kim, K., Sengupta, P., Feeding state-dependent regulation of developmental plasticity via CaMKI and neuroendocrine signaling. Elife (2015) e10110.


Zhang, X., Feng, L., Chinta, S., Singh, P., Wang, Y., Nunnery, J.K., Butcher, R.A., Acyl-CoA oxidase complexes control the chemical message produced by C. elegans. Proc. Natl. Acad. Sci. U S A (2015) 112:3955-60.


Zhao, L., Mota, M., Vieira, P., Butcher, R.A., Sun, J., Interspecific communication between pinewood nematode, its insect vector, and associated microbes. Trends Parasitol. (2014) 30:299-308.


Zhao, L., Zhang, S., Wei, W., Hao, H., Zhang, B., Butcher, R.A., Sun, J., Chemical signals synchronize the life cycles of a plant-parasitic nematode and its vector beetle. Curr. Biol. (2013) 23:2038-43.


Zhang, X., Noguez, J., Zhou, Y., Butcher, R.A., Analysis of ascarosides from Caenorhabditis elegans using mass spectrometry and NMR spectroscopy, in Pheromone Signaling: Methods and Protocols, (Methods in Molecular Biology series), K. Touhara (ed.), New York: Springer, (2013) 1068:71-92.


Hollister, K., Conner, E.S., Zhang, X., Butcher, R.A., Ragains, J.R., Ascaroside activity in Caenorhabditis elegans is highly dependent on chemical structure. Bioorg. Med. Chem. (2013) 21:5754-69.


Jang, H., Kim, K., Neal, S.J., Macosko, E., Kim, D., Butcher, R.A., Zeiger, D.M., Bargmann, C.I., Sengupta, P., Neuromodulatory state and sex specific alternative behaviors through antagonistic synaptic pathways in C. elegans. Neuron (2012) 75:585-92.


Noguez, J.H., Conner, E.S., Zhou, Y., Ciche, T.A., Ragains, J.R., Butcher, R.A., A novel ascaroside controls the parasitic life cycle of the entomopathogenic nematode Heterorhabditis bacteriophora. ACS Chem. Biol. (2012) 7:961-6.


McGrath, P.T., Xu, Y., Ailion, M., Garrison, J.L., Butcher, R.A., Bargmann, C.I., Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature (2011) 477:321-5.


Postdoctoral and Graduate Work

Sakai, N., Iwata, R., Yokoi, S., Butcher, R.A., Clardy, J., Tomioka, M., Iino, Y., A sexually conditioned switch of chemosensory behavior in C. elegans. Plos One (2013) 8:e68676.


Yamada K., Hirotsu T., Matsuki M., Butcher R.A., Tomioka M., Ishihara T., Clardy J., Kunitomo H., Iino Y., Olfactory plasticity is regulated by pheromonal signaling in Caenorhabditis elegans. Science (2010) 329:1647-50.


Kim, K., Sato, K., Shibuya, M., Zeiger, D.M., Butcher, R.A., Ragains, J.R., Clardy, J., Touhara, K., Sengupta, P., Two chemoreceptors mediate developmental effects of dauer pheromone in C. elegans. Science (2009) 13:994-8.


Butcher, R.A., Ragains, J.R., Clardy, J., An indole-containing dauer pheromone component with unusual dauer inhibitory activity at higher concentrations. Org. Lett. (2009) 11:3100-3.


Butcher, R.A., Ragains, J.R., Li, W., Ruvkun, G., Clardy, J., Mak, H.Y., Biosynthesis of the C. elegans dauer pheromone. Proc. Natl. Acad. Sci. U S A (2009) 106: 1875-9.


Macosko, E.Z., Pokala, N., Feinberg, E.H., Chalasani, S.H., Butcher, R.A., Clardy, J., Bargmann, C.I., A hub-and-spoke circuit drives pheromone attraction and social behavior in C. elegans. Nature (2009) 458: 1171-5.


Butcher, R.A., Ragains, J.R., Kim, E., Clardy, J., A potent dauer pheromone component in C. elegans that acts synergistically with other components. Proc. Natl. Acad. Sci. U S A (2008) 105: 14288-92.


Kontnik, R.*, Bosak, T.*, Butcher, R.A., Brocks, J.J., Losick, R., Clardy, J., Pearson, A., Sporulenes, heptaprenyl metabolites from Bacillus subtilis spores. Org. Lett. (2008) 10:3551-4.


Butcher, R.A.*, Fujita, M.*, Schroeder, F.C., Clardy, J., Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat. Chem. Biol. (2007) 3:420-2.


Butcher, R.A., Schroeder, F.C., Fischbach, M.A., Straight, P.D., Kolter, R., Walsh, C.T., Clardy, J., The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis. Proc. Natl. Acad. Sci. U S A (2007) 104:1506-9.


Butcher, R.A., Schreiber, S.L., A microarray-based protocol for monitoring the growth of yeast overexpression strains. Nat. Protocols (2006) 1:569-76.


Butcher, R.A., Bhullar, B.S., Perlstein, E.O., Marsischky, G., LaBaer, J., Schreiber, S.L., Microarray-based method for monitoring yeast overexpression strains reveals small-molecule targets in TOR pathway. Nat. Chem. Biol. (2006) 2:103-9.


Butcher, R.A., Schreiber, S.L., Using genome-wide transcriptional profiling to elucidate small-molecule mechanism. Curr. Opin. Chem. Biol. (2005) 9:25-30.


Butcher, R.A., Schreiber, S.L., Identification of Ald6p as the target of a class of small-molecule suppressors of FK506 and their use in network dissection. Proc. Natl. Acad. Sci. U S A (2004) 101:7868-73.


Butcher, R.A., Schreiber, S.L., A small molecule suppressor of FK506 that targets the mitochondria and modulates ionic balance in Saccharomyces cerevisiae. Chem. Biol. (2003) 10:521-31.


Haggarty, S.J., Koeller, K.M., Wong, J.C., Butcher, R.A., Schreiber, S.L., Multidimensional chemical genetic analysis of diversity-oriented synthesis-derived deacetylase inhibitors using cell-based assays. Chem. Biol. (2003) 10:383-96.