ZFIN ID: ZDB-LAB-060628-2
Rawls Lab
PI/Director: Rawls, John F.
Contact Person: Rawls, John F.
Email: john.rawls@duke.edu
URL: http://sites.duke.edu/rawlslab/
Address: Department of Molecular Genetics & Microbiology Duke Microbiome Center Duke University School of Medicine 213 Research Drive 327 CARL Building, Box 3580 Durham, NC 27710
Country: United States
Phone: (919) 660-0894; (919) 660-0893
Fax: (919) 684-2790
Line Designation: rdu

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We seek to understand how the intestinal microbiome contributes to vertebrate physiology and disease. To that end, we leverage complementary zebrafish and mouse models to study the integrative physiology of host-microbiome interactions. This work has identified novel and conserved mechanisms by which intestinal bacteria regulate dietary fat metabolism and systemic innate immunity. We also apply genomic approaches in these animal models to understand the transcriptional regulatory pathways utilized by the intestinal epithelium to mediate host responses to the microbiome. Using this approach, we have identified mechanisms of transcriptional and chromatin regulation that have been conserved during vertebrate evolution and also contribute to modern human diseases such as the inflammatory bowel diseases, obesity, and diabetes. To further advance our understanding of obesity pathophysiology, we developed the zebrafish as a model system for studying adipose tissues and identifying new environmental and genetic regulators of adiposity. We are also engaged in translational research in humans and animal models to define microbial and metabolic determinants of obesity and efficacy of weight loss intervention. Grounded in comparative and integrative physiology, our research program has been effective in discovering ancient mechanisms of host-microbiome interaction that are conserved across animal taxa and contribute to the etiology of modern human diseases. These insights are advancing our understanding of host-microbiome relationships in vertebrate physiology and identifying novel therapeutic targets for human diseases ranging from inflammatory bowel disease to obesity to neurological disorders.

Tillman, Matthew Post-Doc Wen, Jia Post-Doc Davis, Briana Graduate Student
Jawahar, Jay Graduate Student Kelly, Cecelia Graduate Student Mercado, Gilberto Padilla Graduate Student
Morash, Maggie Graduate Student Lickwar, Colin Research Staff McCann, Jessica Research Staff
Godwin, Julia Technical Staff

Heppert, J.K., Lickwar, C.R., Tillman, M.C., Davis, B.R., Davison, J.M., Lu, H.Y., Chen, W., Busch-Nentwich, E.M., Corcoran, D.L., Rawls, J.F. (2022) Conserved roles for Hnf4 family transcription factors in zebrafish development and intestinal function. Genetics. 222(4):
Jawahar, J., McCumber, A.W., Lickwar, C.R., Amoroso, C.R., de la Torre Canny, S.G., Wong, S., Morash, M., Thierer, J.H., Farber, S.A., Bohannan, B.J.M., Guillemin, K., Rawls, J.F. (2022) Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding. BMC Genomics. 23:225
Yan, C., Yang, Q., Zhang, S., Millar, D.G., Alpert, E.J., Do, D., Veloso, A., Brunson, D.C., Drapkin, B.J., Stanzione, M., Scarfò, I., Moore, J.C., Iyer, S., Qin, Q., Wei, Y., McCarthy, K.M., Rawls, J.F., Dyson, N.J., Cobbold, M., Maus, M.V., Langenau, D.M. (2021) Single-cell imaging of T cell immunotherapy responses in vivo. The Journal of experimental medicine. 218(10):
Wen, J., Mercado, G.P., Volland, A., Doden, H.L., Lickwar, C.R., Crooks, T., Kakiyama, G., Kelly, C., Cocchiaro, J.L., Ridlon, J.M., Rawls, J.F. (2021) Fxr signaling and microbial metabolism of bile salts in the zebrafish intestine. Science advances. 7(30)
Chen, C., Gu, Y., Philippe, J., Zhang, P., Bachman, H., Zhang, J., Mai, J., Rufo, J., Rawls, J.F., Davis, E.E., Katsanis, N., Huang, T.J. (2021) Acoustofluidic rotational tweezing enables high-speed contactless morphological phenotyping of zebrafish larvae. Nature communications. 12:1118
Heppert, J.K., Davison, J.M., Kelly, C., Mercado, G.P., Lickwar, C.R., Rawls, J.F. (2021) Transcriptional programmes underlying cellular identity and microbial responsiveness in the intestinal epithelium. Nature reviews. Gastroenterology & hepatology. 18:7-23
Ye, L., Bae, M., Cassilly, C.D., Jabba, S.V., Thorpe, D.W., Martin, A.M., Lu, H.Y., Wang, J., Thompson, J.D., Lickwar, C.R., Poss, K.D., Keating, D.J., Jordt, S.E., Clardy, J., Liddle, R.A., Rawls, J.F. (2020) Enteroendocrine cells sense bacterial tryptophan catabolites to activate enteric and vagal neuronal pathways. Cell Host & Microbe. 29(2):179-196.e9
Cholan, P.M., Han, A., Woodie, B.R., Watchon, M., Kurz, A.R., Laird, A.S., Britton, W.J., Ye, L., Holmes, Z.C., McCann, J.R., David, L.A., Rawls, J.F., Oehlers, S.H. (2020) Conserved anti-inflammatory effects and sensing of butyrate in zebrafish. Gut microbes. 12:1-11
Yan, C., Do, D., Yang, Q., Brunson, D.C., Rawls, J.F., Langenau, D.M. (2020) Single-cell imaging of human cancer xenografts using adult immunodeficient zebrafish. Nature Protocols. 15(9):3105-3128
Loh, N.Y., Minchin, J.E.N., Pinnick, K.E., Verma, M., Todorčević, M., Denton, N., Moustafa, J.E., Kemp, J.P., Gregson, C.L., Evans, D.M., Neville, M.J., Small, K.S., McCarthy, M.I., Mahajan, A., Rawls, J.F., Karpe, F., Christodoulides, C. (2020) RSPO3 impacts body fat distribution and regulates adipose cell biology in vitro. Nature communications. 11:2797
Ye, L., Mueller, O., Bagwell, J., Bagnat, M., Liddle, R.A., Rawls, J.F. (2019) High fat diet induces microbiota-dependent silencing of enteroendocrine cells. eLIFE. 8:
Murdoch, C.C., Rawls, J.F. (2019) Commensal Microbiota Regulate Vertebrate Innate Immunity-Insights From the Zebrafish. Frontiers in immunology. 10:2100
Park, J., Levic, D.S., Sumigray, K.D., Bagwell, J., Eroglu, O., Block, C.L., Eroglu, C., Barry, R., Lickwar, C.R., Rawls, J.F., Watts, S.A., Lechler, T., Bagnat, M. (2019) Lysosome-Rich Enterocytes Mediate Protein Absorption in the Vertebrate Gut. Developmental Cell. 51(1):7-20.e6
Casadei, E., Tacchi, L., Lickwar, C.R., Espenschied, S.T., Davison, J.M., Muñoz, P., Rawls, J.F., Salinas, I. (2019) Commensal bacteria regulate gene expression and differentiation in vertebrate olfactory systems through transcription factor REST. Chemical senses. 44(8):615-630
Espenschied, S.T., Cronan, M.R., Matty, M.A., Mueller, O., Redinbo, M.R., Tobin, D.M., Rawls, J.F. (2019) Epithelial delamination is protective during pharmaceutical-induced enteropathy. Proceedings of the National Academy of Sciences of the United States of America. 116(34):16961-16970
Yan, C., Brunson, D.C., Tang, Q., Do, D., Iftimia, N.A., Moore, J.C., Hayes, M.N., Welker, A.M., Garcia, E.G., Dubash, T.D., Hong, X., Drapkin, B.J., Myers, D.T., Phat, S., Volorio, A., Marvin, D.L., Ligorio, M., Dershowitz, L., McCarthy, K.M., Karabacak, M.N., Fletcher, J.A., Sgroi, D.C., Iafrate, J.A., Maheswaran, S., Dyson, N.J., Haber, D.A., Rawls, J.F., Langenau, D.M. (2019) Visualizing Engrafted Human Cancer and Therapy Responses in Immunodeficient Zebrafish. Cell. 177(7):1903-1914.e14
Murdoch, C.C., Espenschied, S.T., Matty, M.A., Mueller, O., Tobin, D.M., Rawls, J.F. (2019) Intestinal Serum amyloid A suppresses systemic neutrophil activation and bactericidal activity in response to microbiota colonization. PLoS pathogens. 15:e1007381
Cronan, M.R., Matty, M.A., Rosenberg, A.F., Blanc, L., Pyle, C.J., Espenschied, S.T., Rawls, J.F., Dartois, V., Tobin, D.M. (2018) An explant technique for high-resolution imaging and manipulation of mycobacterial granulomas. Nature Methods. 15:1098-1107
Minchin, J.E.N., Scahill, C.M., Staudt, N., Busch-Nentwich, E.M., Rawls, J.F. (2018) Deep phenotyping in zebrafish reveals genetic and diet-induced adiposity changes that may inform disease risk. Journal of Lipid Research. 59(8):1536-1545
King, J., Foster, J., Davison, J.M., Rawls, J.F., Breton, G. (2017) Zebrafish Transcription Factor ORFeome for Gene Discovery and Regulatory Network Elucidation. Zebrafish. 15(2):202-205
Phelps, D., Brinkman, N.E., Keely, S.P., Anneken, E.M., Catron, T.R., Betancourt, D., Wood, C.E., Espenschied, S.T., Rawls, J.F., Tal, T. (2017) Microbial colonization is required for normal neurobehavioral development in zebrafish. Scientific Reports. 7:11244
Lickwar, C.R., Camp, J.G., Weiser, M., Cocchiaro, J.L., Kingsley, D.M., Furey, T.S., Sheikh, S.Z., Rawls, J.F. (2017) Genomic dissection of conserved transcriptional regulation in intestinal epithelial cells. PLoS Biology. 15:e2002054
Minchin, J.E.N., Rawls, J.F. (2017) Elucidating the role of plexin D1 in body fat distribution and susceptibility to metabolic disease using a zebrafish model system. Adipocyte. 6(4):277-283
Davison, J.M., Lickwar, C.R., Song, L., Breton, G., Crawford, G.E., Rawls, J.F. (2017) Microbiota regulate intestinal epithelial gene expression by suppressing the transcription factor Hepatocyte nuclear factor 4 alpha. Genome research. 27(7):1195-1206
Minchin, J.E., Rawls, J.F. (2017) A classification system for zebrafish adipose tissues. Disease models & mechanisms. 10(6):797-809
Melancon, E., Gomez De La Torre Canny, S., Sichel, S., Kelly, M., Wiles, T.J., Rawls, J.F., Eisen, J.S., Guillemin, K. (2017) Best practices for germ-free derivation and gnotobiotic zebrafish husbandry. Methods in cell biology. 138:61-100
Minchin, J.E., Rawls, J.F. (2017) In vivo imaging and quantification of regional adiposity in zebrafish. Methods in cell biology. 138:3-27
Bae, S., Mueller, O., Wong, S., Rawls, J.F., Valdivia, R.H. (2016) Genomic sequencing-based mutational enrichment analysis identifies motility genes in a genetically intractable gut microbe. Proceedings of the National Academy of Sciences of the United States of America. 113:14127-14132
Burns, A.R., Zac Stephens, W., Stagaman, K., Wong, S., Rawls, J.F., Guillemin, K., Bohannan, B.J. (2016) Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. The ISME Journal. 10(3):655-64
Wong, S., Stephens, W.Z., Burns, A.R., Stagaman, K., David, L.A., Bohannan, B.J., Guillemin, K., Rawls, J.F. (2015) Ontogenetic Differences in Dietary Fat Influence Microbiota Assembly in the Zebrafish Gut. mBio. 6(5):e00687-15
Wang, L., Oehlers, S.H., Espenschied, S.T., Rawls, J.F., Tobin, D.M., Ko, D.C. (2015) CPAG: software for leveraging pleiotropy in GWAS to reveal similarity between human traits links plasma fatty acids and intestinal inflammation. Genome biology. 16:190
Minchin, J.E., Dahlman, I., Harvey, C.J., Mejhert, N., Singh, M.K., Epstein, J.A., Arner, P., Torres-Vazquez, J., Rawls, J.F. (2015) Plexin D1 determines body fat distribution by regulating the type V collagen microenvironment in visceral adipose tissue. Proceedings of the National Academy of Sciences of the United States of America. 112(14):4363-8
Marjoram, L., Alvers, A., Deerhake, M.E., Bagwell, J., Mankiewicz, J., Cocchiaro, J.L., Beerman, R.W., Willer, J., Sumigray, K.D., Katsanis, N., Tobin, D.M., Rawls, J.F., Goll, M.G., Bagnat, M. (2015) Epigenetic control of intestinal barrier function and inflammation in zebrafish. Proceedings of the National Academy of Sciences of the United States of America. 112(9):2770-5
Kanther, M., Tomkovich, S., Xiaolun, S., Grosser, M.R., Koo, J., Flynn, E.J., Jobin, C., and Rawls, J.F. (2014) Commensal microbiota stimulate systemic neutrophil migration through induction of Serum amyloid A. Cellular Microbiology. 16(7):1053-67
Gratacap, R.L., Rawls, J.F., and Wheeler, R.T. (2013) Mucosal candidiasis elicits NF-κB activation, proinflammatory gene expression and localized neutrophilia in zebrafish. Disease models & mechanisms. 6(5):1260-70
Minchin, J.E., Williams, V.C., Hinits, Y., Low, S., Tandon, P., Fan, C.M., Rawls, J.F., and Hughes, S.M. (2013) Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion. Development (Cambridge, England). 140(14):2972-2984
Sadler, K.C., Rawls, J.F., and Farber, S.A. (2013) Getting the inside tract: new frontiers in zebrafish digestive system biology. Zebrafish. 10(2):129-131
McMenamin, S.K., Minchin, J.E., Gordon, T.N., Rawls, J.F., and Parichy, D.M. (2013) Dwarfism and Increased Adiposity in the gh1 Mutant Zebrafish vizzini. Endocrinology. 154(4):1476-87
Onyiah, J.C., Sheikh, S.Z., Maharshak, N., Steinbach, E.C., Russo, S.M., Kobayashi, T., Mackey, L.C., Hansen, J.J., Moeser, A.J., Rawls, J.F., Borst, L.B., Otterbein, L.E., and Plevy, S.E. (2013) Carbon Monoxide and Heme Oxygenase-1 Prevent Intestinal Inflammation in Mice by Promoting Bacterial Clearance. Gastroenterology. 144(4):789-798
Cocchiaro, J.L., and Rawls, J.F. (2013) Microgavage of zebrafish larvae. Journal of visualized experiments : JoVE. (72):e4434
Goldsmith, J.R., Cocchiaro, J.L., Rawls, J.F., and Jobin, C. (2013) Zebrafish glafenine-intestinal injury is ameliorated by mu-opioid signaling via enhancement of Atf6-dependent cellular stress responses. Disease models & mechanisms. 6(1):146-159
Semova, I., Carten, J.D., Stombaugh, J., Mackey, L.C., Knight, R., Farber, S.A., and Rawls, J.F. (2012) Microbiota regulate intestinal absorption and metabolism of Fatty acids in the zebrafish. Cell Host & Microbe. 12(3):277-288
Camp, J.G., Jazwa, A.L., Trent, C.M., and Rawls, J.F. (2012) Intronic Cis-Regulatory Modules Mediate Tissue-Specific and Microbial Control of angptl4/fiaf Transcription. PLoS Genetics. 8(3):e1002585
Roeselers, G., Mittge, E.K., Stephens, W.Z., Parichy, D.M., Cavanaugh, C.M., Guillemin, K., and Rawls, J.F. (2011) Evidence for a core gut microbiota in the zebrafish. The ISME Journal. 5(10):1595-608
Kanther, M., Sun, X., Mühlbauer, M., Mackey, L.C., Flynn, E.J., Bagnat, M., Jobin, C., and Rawls, J.F. (2011) Microbial colonization induces dynamic temporal and spatial patterns of NF-kappaB activation in the zebrafish digestive tract. Gastroenterology. 141(1):197-207
Milligan-Myhre, K., Charette, J.R., Phennicie, R.T., Stephens, W.Z., Rawls, J.F., Guillemin, K., and Kim, C.H. (2011) Study of host-microbe interactions in zebrafish. Methods in cell biology. 105:87-116
Minchin, J.E., and Rawls, J.F. (2011) In vivo Analysis of White Adipose Tissue in Zebrafish. Methods in cell biology. 105:63-86
Kanther, M., and Rawls, J.F. (2010) Host-microbe interactions in the developing zebrafish. Current opinion in immunology. 22(1):10-19
Volkman, H.E., Pozos, T.C., Zheng, J., Davis, J.M., Rawls, J.F., and Ramakrishnan, L. (2010) Tuberculous Granuloma Induction via Interaction of a Bacterial Secreted Protein with Host Epithelium. Science (New York, N.Y.). 327(5964):466-469
Flynn, E.J. 3rd, Trent, C.M., and Rawls, J.F. (2009) Ontogeny and nutritional control of adipogenesis in zebrafish (Danio rerio). Journal of Lipid Research. 50(8):1641-1652
Camp, J.G., Kanther, M., Semova, I., and Rawls, J.F. (2009) Patterns and scales in gastrointestinal microbial ecology. Gastroenterology. 136(6):1989-2002
Pham, L.N., Kanther, M., Semova, I., and Rawls, J.F. (2008) Methods for generating and colonizing gnotobiotic zebrafish. Nature Protocols. 3(12):1862-1875
Rawls, J.F., Mahowald, M.A., Goodman, A.L., Trent, C.M., and Gordon, J.I. (2007) In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proceedings of the National Academy of Sciences of the United States of America. 104(18):7622-7627
Rawls, J.F., Mahowald, M.A., Ley, R.E., and Gordon, J.I. (2006) Reciprocal Gut Microbiota Transplants from Zebrafish and Mice to Germ-free Recipients Reveal Host Habitat Selection. Cell. 127(20:423-433
Rawls, J.F., Samuel, B.S., and Gordon, J.I. (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proceedings of the National Academy of Sciences of the United States of America. 101(13):4596-4601
Rawls, J.F. and Johnson, S.L. (2003) Temporal and molecular separation of the kit receptor tyrosine kinase's roles in zebrafish melanocyte migration and survival. Developmental Biology. 262(1):152-161
Rawls, J.F., Frieda, M.R., McAdow, A.R., Gross, J.P., Clayton, C.M., Heyen, C.K., and Johnson, S.L. (2003) Coupled mutagenesis screens and genetic mapping in zebrafish. Genetics. 163(3):997-1009
Rawls, J.F., Mellgren, E.M., and Johnson, S.L. (2001) How the zebrafish gets its stripes. Developmental Biology. 240(2):301-314
Rawls, J.F. and Johnson, S.L. (2001) Requirements for the kit receptor tyrosine kinase during regeneration of zebrafish fin melanocytes. Development (Cambridge, England). 128(11):1943-1949
Rawls, J.F. (2001) Genetic dissection of kit-dependent melanocyte development in zebrafish, Danio rerio. Ph.D. Thesis.
Parichy, D.M., Mellgren, E.M., Rawls, J.F., Lopes, S.S., Kelsh, R.N., and Johnson, S.L. (2000) Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio. Developmental Biology. 227(2):294-306
Rawls, J.F. and Johnson, S.L. (2000) Zebrafish kit mutation reveals primary and secondary regulation of melanocyte development during fin stripe regeneration. Development (Cambridge, England). 127(17):3715-3724
Parichy, D.M., Rawls, J.F., Pratt, S.J., Whitfield, T.T., and Johnson, S.L. (1999) Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. Development (Cambridge, England). 126(15):3425-3436