The acetate switch of an intestinal pathogen disrupts host insulin signaling and lipid metabolism

Cell Host and Microbe

Volumn 16, Issue 5, 2014, Pages 592-604

  Hang, Saiyu ^a   Purdy, Alexandra E ^a,d   Robins, William P ^b   Wang, Zhipeng ^a,e   Mandal, Manabendra ^a,c   Chang, Sarah ^a   Mekalanos, John J ^b   Watnick, Paula I ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TEZPUR UNIVERSITY   (India)

^d AMHERST COLLEGE   (United States)

^e RENMIN UNIVERSITY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ACETYL COENZYME A SYNTHASE 1; ACETYL COENZYME A SYNTHETASE; BACTERIAL PROTEIN; CHOLERA TOXIN; INSULIN; LIPID; PROTEIN CRBRS; SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG; ACETIC ACID DERIVATIVE; COENZYME A LIGASE; FACL2 PROTEIN, RAT; INSULIN DERIVATIVE; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; BIOACCUMULATION; CHOLERA; COMMENSAL; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; HOST PATHOGEN INTERACTION; INTESTINE CELL; LETHALITY; LIPID METABOLISM; NONHUMAN; SIGNAL TRANSDUCTION; STEATOSIS; TRANSCRIPTION INITIATION; VIBRIO CHOLERAE; ANIMAL; GENETICS; INNATE IMMUNITY; INTESTINE; METABOLISM; MICROBIOLOGY; MICROFLORA; PATHOGENICITY;

ACETATES; ANIMALS; BACTERIAL PROTEINS; CHOLERA TOXIN; COENZYME A LIGASES; DROSOPHILA MELANOGASTER; ENTEROCYTES; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INSULINS; INTESTINES; LIPID METABOLISM; MICROBIOTA; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE; VIRULENCE FACTORS;

EID: 84910623900     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.10.006     Document Type: Article

References (44)

1. M.J. Angelichio, J. Spector, M.K. Waldor, and A. Camilli Vibrio cholerae intestinal population dynamics in the suckling mouse model of infection Infect. Immun. 67 1999 3733 3739
2. E.L. Arrese, and J.L. Soulages Insect fat body: energy, metabolism, and regulation Annu. Rev. Entomol. 55 2010 207 225
3. V. Baselski, R. Briggs, and C. Parker Intestinal fluid accumulation induced by oral challenge with Vibrio cholerae or cholera toxin in infant mice Infect. Immun. 15 1977 704 712
4. C.D. Berkey, N. Blow, and P.I. Watnick Genetic analysis of Drosophila melanogaster susceptibility to intestinal Vibrio cholerae infection Cell. Microbiol. 11 2009 461 474
5. N.S. Blow, R.N. Salomon, K. Garrity, I. Reveillaud, A. Kopin, F.R. Jackson, and P.I. Watnick Vibrio cholerae infection of Drosophila melanogaster mimics the human disease cholera PLoS Pathog. 1 2005 e8
6. J.S. Britton, W.K. Lockwood, L. Li, S.M. Cohen, and B.A. Edgar Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions Dev. Cell 2 2002 239 249
7. B. Charroux, and J. Royet Drosophila immune response: From systemic antimicrobial peptide production in fat body cells to local defense in the intestinal tract Fly (Austin) 4 2010 40 47
8. A. Franceschini, D. Szklarczyk, S. Frankild, M. Kuhn, M. Simonovic, A. Roth, J. Lin, P. Minguez, P. Bork, C. von Mering, and L.J. Jensen STRING v9.1: protein-protein interaction networks, with increased coverage and integration Nucleic Acids Res. 41 Database issue 2013 D808 D815
9. R. Gimenez, M.F. Nuñez, J. Badia, J. Aguilar, and L. Baldoma The gene yjcG, cotranscribed with the gene acs, encodes an acetate permease in Escherichia coli J. Bacteriol. 185 2003 6448 6455
10. A. Guichard, B. Cruz-Moreno, B. Aguilar, N.M. van Sorge, J. Kuang, A.A. Kurkciyan, Z. Wang, S. Hang, G.P. Pineton de Chambrun, and D.F. McCole Cholera toxin disrupts barrier function by inhibiting exocyst-mediated trafficking of host proteins to intestinal cell junctions Cell Host Microbe 14 2013 294 305
11. L. Guo, J. Karpac, S.L. Tran, and H. Jasper PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan Cell 156 2014 109 122
12. D. Hegedus, M. Erlandson, C. Gillott, and U. Toprak New insights into peritrophic matrix synthesis, architecture, and function Annu. Rev. Entomol. 54 2009 285 302
13. J.H. Hoekstra, H. Szajewska, M.A. Zikri, D. Micetic-Turk, Z. Weizman, A. Papadopoulou, A. Guarino, J.A. Dias, and B. Oostvogels Oral rehydration solution containing a mixture of non-digestible carbohydrates in the treatment of acute diarrhea: a multicenter randomized placebo controlled study on behalf of the ESPGHAN working group on intestinal infections J. Pediatr. Gastroenterol. Nutr. 39 2004 239 245
14. B. Honegger, M. Galic, K. Köhler, F. Wittwer, W. Brogiolo, E. Hafen, and H. Stocker Imp-L2, a putative homolog of vertebrate IGF-binding protein 7, counteracts insulin signaling in Drosophila and is essential for starvation resistance J. Biol. 7 2008 10
15. X. Huang, J.T. Warren, J. Buchanan, L.I. Gilbert, and M.P. Scott Drosophila Niemann-Pick type C-2 genes control sterol homeostasis and steroid biosynthesis: a model of human neurodegenerative disease Development 134 2007 3733 3742
16. I.H. Jang, N. Chosa, S.H. Kim, H.J. Nam, B. Lemaitre, M. Ochiai, Z. Kambris, S. Brun, C. Hashimoto, and M. Ashida A Spätzle-processing enzyme required for toll signaling activation in Drosophila innate immunity Dev. Cell 10 2006 45 55
17. I. Kaji, S. Karaki, R. Tanaka, and A. Kuwahara Density distribution of free fatty acid receptor 2 (FFA2)-expressing and GLP-1-producing enteroendocrine L cells in human and rat lower intestine, and increased cell numbers after ingestion of fructo-oligosaccharide J. Mol. Histol. 42 2011 27 38
18. K.A. Lee, S.H. Kim, E.K. Kim, E.M. Ha, H. You, B. Kim, M.J. Kim, Y. Kwon, J.H. Ryu, and W.J. Lee Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila Cell 153 2013 797 811
19. M.J. Lehane Peritrophic matrix structure and function Annu. Rev. Entomol. 42 1997 525 550
20. B. Lemaitre, and I. Miguel-Aliaga The digestive tract of Drosophila melanogaster Annu. Rev. Genet. 47 2013 377 404
21. X. Li, and S. Roseman The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase Proc. Natl. Acad. Sci. USA 101 2004 627 631
22. M.J. Lombardo, J. Michalski, H. Martinez-Wilson, C. Morin, T. Hilton, C.G. Osorio, J.P. Nataro, C.O. Tacket, A. Camilli, and J.B. Kaper An in vivo expression technology screen for Vibrio cholerae genes expressed in human volunteers Proc. Natl. Acad. Sci. USA 104 2007 18229 18234
23. M.J. Lowden, K. Skorupski, M. Pellegrini, M.G. Chiorazzo, R.K. Taylor, and F.J. Kull Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes Proc. Natl. Acad. Sci. USA 107 2010 2860 2865
24. A. Mandlik, J. Livny, W.P. Robins, J.M. Ritchie, J.J. Mekalanos, and M.K. Waldor RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression Cell Host Microbe 10 2011 165 174
25. K.L. Meibom, M. Blokesch, N.A. Dolganov, C.Y. Wu, and G.K. Schoolnik Chitin induces natural competence in Vibrio cholerae Science 310 2005 1824 1827
26. S. Monira, M.M. Hoq, A.K. Chowdhury, A. Suau, F. Magne, H.P. Endtz, M. Alam, M. Rahman, P. Pochart, J.F. Desjeux, and N.H. Alam Short-chain fatty acids and commensal microbiota in the faeces of severely malnourished children with cholera rehydrated with three different carbohydrates Eur. J. Clin. Nutr. 64 2010 1116 1124
27. M.K. Nøhr, M.H. Pedersen, A. Gille, K.L. Egerod, M.S. Engelstoft, A.S. Husted, R.M. Sichlau, K.V. Grunddal, S.S. Poulsen, and S. Han GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes Endocrinology 154 2013 3552 3564
28. V. Olivier, N.H. Salzman, and K.J. Satchell Prolonged colonization of mice by Vibrio cholerae El Tor O1 depends on accessory toxins Infect. Immun. 75 2007 5043 5051
29. V. Olivier, J. Queen, and K.J. Satchell Successful small intestine colonization of adult mice by Vibrio cholerae requires ketamine anesthesia and accessory toxins PLoS ONE 4 2009 e7352
30. C.G. Osorio, J.A. Crawford, J. Michalski, H. Martinez-Wilson, J.B. Kaper, and A. Camilli Second-generation recombination-based in vivo expression technology for large-scale screening for Vibrio cholerae genes induced during infection of the mouse small intestine Infect. Immun. 73 2005 972 980
31. W. Palm, J.L. Sampaio, M. Brankatschk, M. Carvalho, A. Mahmoud, A. Shevchenko, and S. Eaton Lipoproteins in Drosophila melanogaster - assembly, function, and influence on tissue lipid composition PLoS Genet. 8 2012 e1002828
32. A.E. Purdy, and P.I. Watnick Spatially selective colonization of the arthropod intestine through activation of Vibrio cholerae biofilm formation Proc. Natl. Acad. Sci. USA 108 2011 19737 19742
33. J.M. Ritchie, H. Rui, R.T. Bronson, and M.K. Waldor Back to the future: studying cholera pathogenesis using infant rabbits MBio 1 2010
34. J. Royet Epithelial homeostasis and the underlying molecular mechanisms in the gut of the insect model Drosophila melanogaster Cell. Mol. Life Sci. 68 2011 3651 3660
35. E.J. Rubin, B.J. Akerley, V.N. Novik, D.J. Lampe, R.N. Husson, and J.J. Mekalanos In vivo transposition of mariner-based elements in enteric bacteria and mycobacteria Proc. Natl. Acad. Sci. USA 96 1999 1645 1650
36. W.R. Russell, L. Hoyles, H.J. Flint, and M.E. Dumas Colonic bacterial metabolites and human health Curr. Opin. Microbiol. 16 2013 246 254
37. J. Sá-Pessoa, S. Paiva, D. Ribas, I.J. Silva, S.C. Viegas, C.M. Arraiano, and M. Casal SATP (YaaH), a succinate-acetate transporter protein in Escherichia coli Biochem. J. 454 2013 585 595
38. S.C. Shin, S.H. Kim, H. You, B. Kim, A.C. Kim, K.A. Lee, J.H. Yoon, J.H. Ryu, and W.J. Lee Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling Science 334 2011 670 674
39. A.M. Stock, V.L. Robinson, and P.N. Goudreau Two-component signal transduction Annu. Rev. Biochem. 69 2000 183 215
40. A.A. Teleman Molecular mechanisms of metabolic regulation by insulin in Drosophila Biochem. J. 425 2010 13 26
41. K.L. Van Dellen, L. Houot, and P.I. Watnick Genetic analysis of Vibrio cholerae monolayer formation reveals a key role for DeltaPsi in the transition to permanent attachment J. Bacteriol. 190 2008 8185 8196
42. Z. Wang, C.D. Berkey, and P.I. Watnick The Drosophila protein mustard tailors the innate immune response activated by the immune deficiency pathway J. Immunol. 188 2012 3993 4000
43. Z. Wang, S. Hang, A.E. Purdy, and P.I. Watnick Mutations in the IMD pathway and mustard counter Vibrio cholerae suppression of intestinal stem cell division in Drosophila MBio 4 2013 e00337-e13
44. A.J. Wolfe The acetate switch Microbiol. Mol. Biol. Rev. 69 2005 12 50