Secreted Aeromonas GlcNAc binding protein GbpA stimulates epithelial cell proliferation in the zebrafish intestine

References

• Bosch TCG, McFall-Ngai M. Animal development in the microbial world: re-thinking the conceptual framework. Curr Top Dev Biol. 2021;141:399–15.
   PubMed Web of Science ®Google Scholar
• Walsh KT, Guillemin K. The impacts of microbiota on animal development and physiology. In: Rook GAW, Lowry CA, editors. Evolution, biodiversity, and a reassessment of the hygiene hypothesis. 2022. p. 177–196. doi:10.1007/978-3-030-91051-8_6.
   Google Scholar
• Massaquoi MS, Kong G, Chillin D, Hamilton MK, Melancon E, Eisen JS, Guillemin K. Global host responses to the microbiota at single cell resolution in gnotobiotic zebrafish. BioRXiv. 2022. doi:10.1101/2022.03.28.486083.
   Google Scholar
• Wang G, Sweren E, Liu H, Wier E, Alphonse MP, Chen R, Islam N, Li A, Xue Y, Chen J, et al. Bacteria induce skin regeneration via IL-1β signaling. Cell Host Microbe. 2021;29(5):777–791.e6. doi:10.1016/j.chom.2021.03.003.
   PubMed Web of Science ®Google Scholar
• Abo H, Chassaing B, Harusato A, Quiros M, Brazil JC, Ngo VL, Viennois E, Merlin D, Gewirtz AT, Nusrat A, et al. Erythroid differentiation regulator-1 induced by microbiota in early life drives intestinal stem cell proliferation and regeneration. Nat Commun. 2020;11(1):513. doi:10.1038/s41467-019-14258-z.
   PubMed Web of Science ®Google Scholar
• Abrams GD, Bauer H, Sprinz H. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab Invest. 1963;12:355–364.
   PubMed Web of Science ®Google Scholar
• Cheesman SE, Neal JT, Mittge E, Seredick BM, Guillemin K. Epithelial cell proliferation in the developing zebrafish intestine is regulated by the Wnt pathway and microbial signaling via Myd88. Proc Natl Acad Sci U S A. 2011;108(supplement_1):4570–4577. doi:10.1073/pnas.1000072107.
   PubMedGoogle Scholar
• Rawls JF, Samuel BS, Gordon JI. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. PNAS. 2004;101(13):4596–4601. doi:10.1073/pnas.0400706101.
   PubMed Web of Science ®Google Scholar
• Rawls JF, Mahowald MA, Ley RE, Gordon JI. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell. 2016;127(2):423–433. doi:10.1016/j.cell.2006.08.043.
   Google Scholar
• Broderick NA, Buchon N, Lemaitre B, McFall-Ngai MJ. Microbiota-induced changes in drosophila melanogaster host gene expression and gut morphology. mBio. 2014;5(3):1–13. doi:10.1128/mBio.01117-14.
   Web of Science ®Google Scholar
• Jones RM, Luo L, Ardita CS, Richardson AN, Kwon YM, Mercante JW, Alam A, Gates CL, Wu H, Swanson PA, et al. Symbiotic Lactobacilli stimulate gut epithelial proliferation via Nox-mediated generation of reactive oxygen species. Embo J. 2013;32(23):3017–3028. doi:10.1038/emboj.2013.224.
   PubMed Web of Science ®Google Scholar
• Jones TA, Guillemin K. Racing to stay put: how resident microbiota stimulate intestinal epithelial cell proliferation. Curr Pathobiol Rep. 2018;6(1):23–28. doi:10.1007/s40139-018-0163-0.
   Google Scholar
• Hill JH, Franzosa EA, Huttenhower C, Guillemin K. A conserved bacterial protein induces pancreatic beta cell expansion during zebrafish development. Elife. 2016;5:18. doi:10.7554/eLife.20145.
   Web of Science ®Google Scholar
• Melancon E, Gomez De La Torre Cann S, Sichel S, Kelly M, Wiles TJ, Rawls JF, Eisen JS, Guillemin K. Best practices for germ-free derivation and gnotobiotic zebrafish husbandry. Methods Cell Biology. 2015;155:1683–1695. doi:10.1016/bs.mcb.2016.11.005.
   Google Scholar
• Wiles TJ, Wall ES, Schlomann BH, Hay EA, Parthasarathy R, Guillemin K. Modernized tools for streamlined genetic manipulation and comparative study of wild and diverse proteobacterial lineages. mBio. 2018;9(5). doi:10.1128/mBio.01877-18.
   PubMed Web of Science ®Google Scholar
• Rolig AS, Sweeney EG, Kaye LE, DeSantis MD, Perkins A, Banse AV, Hamilton MK, Guillemin K. A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish. Elife. 2018;7. doi:10.7554/eLife.37172.
   PubMed Web of Science ®Google Scholar
• Kirn TJ, Jude BA, Taylor RK. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature. 2005;438(7069):863–866. doi:10.1038/nature04249.
   PubMed Web of Science ®Google Scholar
• Bhowmick R, Ghosal A, Das B, Koley H, Saha DR, Ganguly S, Nandy RK, Bhadra RK, Chatterjee NS. Intestinal adherence of Vibrio cholerae involves a coordinated interaction between colonization factor GbpA and mucin. Infect Immun. 2008;76(11):4968–4977. doi:10.1128/IAI.01615-07.
   PubMed Web of Science ®Google Scholar
• Wong E, Vaaje-Kolstad G, Ghosh A, Hurtado-Guerrero R, Konarev PV, Ibrahim AFM, Svergun DI, Eijsink VGH, Chatterjee NS, van Aalten DMF, et al. The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces. PLoS Pathog. 2012;8(1):e1002373. doi:10.1371/journal.ppat.1002373.
   PubMed Web of Science ®Google Scholar
• Book AJ, Yennamalli RM, Takasuka TE, Currie CR, Phillips GN, Fox BG. Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases. Biotechnol Biofuels. 2014;7(1):109. doi:10.1186/1754-6834-7-109.
   PubMedGoogle Scholar
• Loose JSM, Forsberg Z, Fraaije MW, Eijsink VGH, Vaaje-Kolstad G. A rapid quantitative activity assay shows that the Vibrio cholerae colonization factor GbpA is an active lytic polysaccharide monooxygenase. FEBS Lett. 2014;588(18):3435–3440. doi:10.1016/j.febslet.2014.07.036.
   PubMed Web of Science ®Google Scholar
• Vandhana TM, Reyre J-L, Sushmaa D, Berrin J-G, Bissaro B, Madhuprakash J. On the expansion of biological functions of lytic polysaccharide monooxygenases. New Phytol. 2022;233(6):2380–2396. doi:10.1111/nph.17921.
   PubMed Web of Science ®Google Scholar
• The Zebrafish Book. A guide for the laboratory use of zebrafish (Danio rerio). 5th ed. Eugene: University of Oregon Press. https://zfin.org/cgi-bin/webdriver.
   Google Scholar
• Bates JM, Akerlund J, Mittge E, Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe. 2007;2(6):371–382. doi:10.1016/j.chom.2007.10.010.
   PubMed Web of Science ®Google Scholar
• Graf J, Nelson MC, Colston SM, Dunning Hotopp JC. Closed genome sequence of Aeromonas veronii strain Hm21, an isolate from the medicinal leech Hirudo verbana. Microbiol Resour Announc. 2020;9(42):20–21. doi:10.1128/MRA.00922-20.
   Web of Science ®Google Scholar
• Choi K-H, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, Schweizer HP. A Tn7-based broad-range bacterial cloning and expression system. Nat Methods. 2005;2(6):443–448. doi:10.1038/NMETH765.
   PubMed Web of Science ®Google Scholar
• Maltz M, Graf J. The Type II Secretion System is essential for erythrocyte lysis and gut colonization by the leech digestive tract symbiont Aeromonas veronii. Appl Environ Microbiol. 2011;77(2):597–603. doi:10.1128/AEM.01621-10.
   PubMed Web of Science ®Google Scholar
• Graf J. Symbiosis of Aeromonas veronii biovar sobria and Hirudo medicinalis, the medicinal leech: a novel model for digestive tract associations. Infect Immun. 1999;67(1):1–7. doi:10.1128/IAI.67.1.1-7.1999.
   PubMed Web of Science ®Google Scholar
• Milligan-Myhre K, Charette JR, Phennicie RT, Stephens WZ, Rawls JF, Guillemin K, Kim CH. Methods Cell Biology. 2011;105:87–116. doi:10.1016/B978-0-12-381320-6.00004-7.
   PubMed Web of Science ®Google Scholar
• Jemielita M, Taormina MJ, Burns AR, Hampton JS, Rolig AS, Guillemin K, Parthasarathy R. Spatial and temporal features of the growth of a bacterial species colonizing the zebrafish gut. mBio. 2014;5(6). doi:10.1128/mBio.01751-14.
   PubMed Web of Science ®Google Scholar
• Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EHK. Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science. 2008;322(5904):1065–1069. doi:10.1126/science.1162493.
   PubMed Web of Science ®Google Scholar
• Logan SL, Thomas J, Yan J, Baker RP, Shields DS, Xavier JB, Hammer BK, Parthasarathy R. The Vibrio cholerae type VI secretion system can modulate host intestinal mechanics to displace gut bacterial symbionts. Proc Natl Acad Sci U S A. 2018;115(16):E3779–3787. doi:10.1073/pnas.1720133115.
   PubMed Web of Science ®Google Scholar
• Runft DL, Mitchell KC, Abuaita BH, Allen JP, Bajer S, Ginsburg K, Neely MN, Withey JH. Zebrafish as a natural host model for Vibrio cholerae colonization and transmission. Appl Environ Microbiol. 2014;80(5):1710–1717. doi:10.1128/AEM.03580-13.
   PubMed Web of Science ®Google Scholar
• Taormina MJ, Jemielita M, Stephens WZ, Burns AR, Troll JV, Parthasarathy R, Guillemin K. Investigating bacterial-animal symbioses with light sheet microscopy. Biol Bull. 2012;223(1):7–20. doi:10.1086/BBLv223n1p7.
   PubMed Web of Science ®Google Scholar
• Wiles TJ, Jemielita M, Baker RP, Schlomann BH, Logan SL, Ganz J, Melancon E, Eisen JS, Guillemin K, Parthasarathy R, et al. Host gut motility promotes competitive exclusion within a model intestinal microbiota. PLoS Biol. 2016;14(7):e1002517. doi:10.1371/journal.pbio.1002517.
   PubMed Web of Science ®Google Scholar
• Reedy AR, Luo L, Neish AS, Jones RM. Commensal microbiota-induced redox signaling activates proliferative signals in the intestinal stem cell microenvironment. Development. 2019;146:dev171520. doi:10.1242/dev.171520.
   PubMed Web of Science ®Google Scholar
• Powell DN, Swimm A, Sonowal R, Bretin A, Gewirtz AT, Jones RM, Kalman D. Indoles from the commensal microbiota act via the AHR and IL-10 to tune the cellular composition of the colonic epithelium during aging. Proc Natl Acad Sci U S A. 2020;117(35):21519–21526. doi:10.1073/pnas.2003004117.
   PubMed Web of Science ®Google Scholar
• Nakamura A, Kurihara S, Takahashi D, Ohashi W, Nakamura Y, Kimura S, Onuki M, Kume A, Sasazawa Y, Furusawa Y, et al. Symbiotic polyamine metabolism regulates epithelial proliferation and macrophage differentiation in the colon. Nat Commun. 2021;12(1). doi:10.1038/s41467-021-22212-1.
   Web of Science ®Google Scholar
• Sigal M, Rothenberg ME, Logan CY, Lee JY, Honaker RW, Cooper RL, Passarelli B, Camorlinga M, Bouley DM, Alvarez G, et al. Helicobacter pylori activates and expands Lgr5(+) stem cells through direct colonization of the gastric glands. Gastroenterology. 2015;148(7):1392–404.e21. doi:10.1053/j.gastro.2015.02.049.
   PubMed Web of Science ®Google Scholar
• Neal JT, Peterson TS, Kent ML, Guillemin K. H. pylori virulence factor CagA increases intestinal cell proliferation by Wnt pathway activation in a transgenic zebrafish model. Dis Model Mech. 2013;6:802–810. doi:10.1242/dmm.011163.
   PubMed Web of Science ®Google Scholar
• Jones TA, Hernandez DZ, Wong ZC, Wandler AM, Guillemin K, Monack DM. The bacterial virulence factor CagA induces microbial dysbiosis that contributes to excessive epithelial cell proliferation in the Drosophila gut. PLoS Pathog. 2017;13(10):1–20. doi:10.1371/journal.ppat.1006631.
   Web of Science ®Google Scholar
• Rolig AS, Mittge EK, Ganz J, Troll JV, Melancon E, Wiles TJ, Alligood K, Stephens WZ, Eisen JS, Guillemin K, et al. The enteric nervous system promotes intestinal health by constraining microbiota composition. PLoS Biol. 2017;15(2):e2000689. doi:10.1371/journal.pbio.2000689.
   PubMed Web of Science ®Google Scholar
• Kitts G, Giglio KM, Zamorano-Sánchez D, Park JH, Townsley L, Cooley RB, Wucher BR, Klose KE, Nadell CD, Yildiz FH, et al. A conserved regulatory circuit controls large adhesins in Vibrio cholerae. mBio. 2019;10(6). doi:10.1128/mBio.02822-19.
   PubMed Web of Science ®Google Scholar
• Syed KA, Beyhan S, Correa N, Queen J, Liu J, Peng F, Satchell KJF, Yildiz F, Klose KE. The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J Bacteriol. 2009;191(21):6555–6570. doi:10.1128/JB.00949-09.
   PubMed Web of Science ®Google Scholar
• Meibom KL, Li XB, Nielsen AT, Wu C-Y, Roseman S, Schoolnik GK. The Vibrio cholerae chitin utilization program. Proceedings of the National Academy of Sciences. 2004;101(8):2524–2529. doi:10.1073/pnas.0308707101.
   PubMed Web of Science ®Google Scholar
• Askarian F, Uchiyama S, Masson H, Sørensen HV, Golten O, Bunæs AC, Mekasha S, Røhr ÅK, Kommedal E, Ludviksen JA, et al. The lytic polysaccharide monooxygenase CbpD promotes Pseudomonas aeruginosa virulence in systemic infection. Nat Commun. 2021;12(1). doi:10.1038/s41467-021-21473-0.
   PubMed Web of Science ®Google Scholar
• Tang JW, Fernandez J, Sohn JJ, Amemiya CT. Chitin is endogenously produced in vertebrates. Current Biology. 2015;25(7):897–900. doi:10.1016/j.cub.2015.01.058.
   PubMed Web of Science ®Google Scholar
• Nakashima K, Kimura S, Ogawa Y, Watanabe S, Soma S, Kaneko T, Yamada L, Sawada H, Tung C-H, Lu T-M, et al. Chitin-based barrier immunity and its loss predated mucus-colonization by indigenous gut microbiota. Nat Commun. 2018;24(1). doi:10.1038/s41467-018-05884-0.
   Google Scholar
• Wiles TJ, Guillemin K. Patterns of partnership: surveillance and mimicry in host-microbiota mutualisms. Curr Opin Microbiol. 2020;54:87–94. doi:10.1016/j.mib.2020.01.012.
   PubMed Web of Science ®Google Scholar