Gut homeostasis in a microbial world: Insights from Drosophila melanogaster

Nature Reviews Microbiology

Volumn 11, Issue 9, 2013, Pages 615-626

  Buchon, Nicolas ^a   Broderick, Nichole A ^b   Lemaitre, Bruno ^b  

^a Department of Obstetrics Gynecology   (United States)

^b EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ADENOSINE PHOSPHATE; BACILLUS THURINGIENSIS TOXIN; CHITIN; CRYSTALLIN; DIAMINOPIMELIC ACID; PEPTIDOGLYCAN RECOGNITION PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; RNA 16S;

BACTERICIDAL ACTIVITY; CANDIDA ALBICANS; CELL PROLIFERATION; CYTOKINE RELEASE; DEFENSE MECHANISM; DIETARY INTAKE; DROSOPHILA MELANOGASTER; ENTOMOPATHOGENIC BACTERIUM; GASTROINTESTINAL INFECTION; GLUCONOBACTER; HEMOLYMPH; HOMEOSTASIS; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOREACTIVITY; INTESTINE BRUSH BORDER; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE FLORA; MICROFLORA; MICROVILLUS; MUCUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REGENERATION; REGULATORY MECHANISM; REVIEW; RNA ANALYSIS; STARVATION; STRESS;

ANIMALS; DROSOPHILA MELANOGASTER; GASTROINTESTINAL TRACT; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; MICROBIOTA;

BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER;

EID: 84882709450     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3074     Document Type: Review

References (116)

1. Lemaitre, B. & Hoffmann, J. A. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697-743 (2007).
2. Ferrandon, D. The complementary facets of epithelial host defenses in the genetic model organism Drosophila melanogaster: from resistance to resilience. Curr. Opin. Immunol. 25, 59-70 (2012).
3. Charroux, B. & Royet, J. Gut-microbiota interactions in non-mammals: what can we learn from Drosophila? Semin. Immunol. 24, 17-24 (2012).
4. Apidianakis, Y. & Rahme, L. Drosophila melanogaster as a model for human intestinal infection and pathology. Dis. Model. Mech. 4, 21-30 (2011).
5. Sang, J. H. The quantitative nutritional requirements of Drosophila melanogaster. J. Exp. Biol. 33, 45-72 (1956).
6. Baumberger, J. P. The food of Drosophila melanogaster Meigen. Proc. Natl Acad. Sci. USA 3, 122-126 (1917).
7. Begon, M. The role of yeast in the nutrition of an insect (Drosophila). J. Biol. Chem. 30, 122-126 (1917).
8. Starmer, W. T. A comparison of Drosophila habitats according to the physiological attributes of the associated yeast communities. Evolution 35, 38-52 (1981).
9. Oakeshott, J. G., Vacek, D. C. & Anderson, P. R. Effects of microbial floras on the distributions of five domestic Drosophila species across fruit resources. Oecologia 78, 533-541 (1989).
10. Starmer, W. T. & Fogleman, J. C. Coadaptation of Drosophila and yeasts in their natural habitat. J. Chem. Ecol. 12, 1037-1055 (1986).
11. McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229-3236 (2013).
12. Vodovar, N. et al. Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc. Natl Acad. Sci. USA 102, 11414-11419 (2005).
13. Nehme, N. T. et al. A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog. 3, e173 (2007).
14. Buchon, N. et al. Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep. 3, 1725-1738 (2013).
15. Basset, A. et al. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc. Natl Acad. Sci. USA 97, 3376-3381 (2000).
16. Buchon, N., Broderick, N. A., Chakrabarti, S. & Lemaitre, B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 23, 2333-2344 (2009).
17. Ryu, J.-H. et al. Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319, 777-782 (2008).
18. Ren, C., Webster, P., Finkel, S. & Tower, J. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab. 6, 144-152 (2007).
19. Cox, C. R. & Gilmore, M. S. Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect. Immun. 75, 1565-1576 (2007).
20. Corby-Harris, V. et al. Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl. Environ. Microbiol. 73, 3470-3479 (2007).
21. Chandler, J., Lang, J., Bhatnagar, S. & Eisen, J. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet. 7, e1002272 (2011).
22. Wong, C. N. A., Ng, P. & Douglas, A. E. Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ. Microbiol. 13, 1889-1900 (2011).
23. Broderick, N. A. & Lemaitre, B. Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3, 307-321 (2012).
24. Bakula, M. The persistence of a microbial flora during postembryogenesis of Drosophila melanogaster. J. Invertebr. Pathol. 14, 365-374 (1969).
25. Shin, S. C. et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334, 670-674 (2011).
26. Sharon, G. et al. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 107, 20051-20056 (2010).
27. Glittenberg, M. et al. Pathogen and host factors are needed to provoke a systemic host response to gastrointestinal infection of Drosophila larvae by Candida albicans. Dis. Model. Mech. 4, 515-525 (2011).
28. Stamps, J. A., Yang, L. H., Morales, V. M. & Boundy-Mills, K. L. Drosophila regulate yeast density and increase yeast community similarity in a natural substrate. PLoS ONE 7, e42238 (2012).
29. Rohlfs, M. Clash of kingdoms or why Drosophila larvae positively respond to fungal competitors. Front. Zool. 2, 2 (2005).
30. Storelli, G. et al. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab. 14, 403-414 (2011).
31. Ridley, E. V., Wong, A. C.-N., Westmiller, S. & Douglas, A. E. Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS ONE 7, e36765 (2012).
32. Amcheslavsky, A., Jiang, J. & Ip, Y. T. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 4, 49-61 (2009).
33. O'Brien, L. E., Soliman, S. S., Li, X. & Bilder, D. Altered modes of stem cell division drive adaptive intestinal growth. Cell 147, 603-614 (2011).
34. Choi, N.-H., Lucchetta, E. & Ohlstein, B. Nonautonomous regulation of Drosophila midgut stem cell proliferation by the insulin-signaling pathway. Proc. Natl Acad. Sci. USA 108, 18702-18707 (2011).
35. Lehane, M. J. Peritrophic matrix structure and function. Annu. Rev. Entomol. 42, 525-550 (1997).
36. Hegedus, D., Erlandson, M., Gillott, C. & Toprak, U. New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol. 54, 285-302 (2009).
37. Vossenkämper, A., Macdonald, T. T. & Marchès, O. Always one step ahead: how pathogenic bacteria use the type III secretion system to manipulate the intestinal mucosal immune system. J. Inflamm. (Lond.) 8, 11 (2011).
38. Kuraishi, T., Binggeli, O., Opota, O., Buchon, N. & Lemaitre, B. Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 108, 15966-15971 (2011).
39. Syed, Z. A., Härd, T., Uv, A. & van Dijk-Härd, I. F. A potential role for Drosophila mucins in development and physiology. PLoS ONE 3, e3041 (2008).
40. Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S. & Lemaitre, B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5, 200-211 (2009).
41. Bonnay, F. et al. big bang gene modulates gut immune tolerance in Drosophila. Proc. Natl Acad. Sci. USA 110, 2957-2962 (2013).
42. Hegan, P. S., Mermall, V., Tilney, L. G. & Mooseker, M. S. Roles for Drosophila melanogaster myosin IB in maintenance of enterocyte brush-border structure and resistance to the bacterial pathogen Pseudomonas entomophila. Mol. Biol. Cell 18, 4625-4636 (2007).
43. Tzou, P. et al. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13, 737-748 (2000).
44. Ryu, J.-H. et al. An essential complementary role of NF-κB pathway to microbicidal oxidants in Drosophila gut immunity. EMBO J. 25, 3693-3701 (2006).
45. Liehl, P., Blight, M., Vodovar, N., Boccard, F. & Lemaitre, B. Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. PLoS Pathog. 2, e56 (2006).
46. Bosco-Drayon, V. et al. Peptidoglycan sensing by the receptor PGRP-LE in the Drosophila gut induces immune responses to infectious bacteria and tolerance to microbiota. Cell Host Microbe 12, 153-165 (2012).
47. Neyen, C., Poidevin, M., Roussel, A. & Lemaitre, B. Tissue-and ligand-specific sensing of Gram-negative infection in Drosophila by PGRP-LC isoforms and PGRP-LE. J. Immunol. 189, 1886-1897 (2012).
48. Takehana, A. et al. Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae. Proc. Natl Acad. Sci. USA 99, 13705-13710 (2002).
49. Leulier, F. et al. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nature Immunol. 4, 478-484 (2003).
50. Kaneko, T. et al. Monomeric and polymeric gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 20, 637-649 (2004).
51. Zaidmanremy, A. et al. The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24, 463-473 (2006).
52. Lhocine, N. et al. PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 4, 147-158 (2008).
53. Johnson, J. W., Fisher, J. F. & Mobashery, S. Bacterial cell-wall recycling. Ann. NY Acad. Sci. 1277, 54-75 (2013).
54. Buchon, N., Broderick, N. A., Kuraishi, T. & Lemaitre, B. Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biol. 8, 152 (2010).
55. Mellroth, P. & Steiner, H. PGRP-SB1: an N-acetylmuramoyl l-alanine amidase with antibacterial activity. Biochem. Biophys. Res. Commun. 350, 994-999 (2006).
56. Bischoff, V. et al. Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog. 2, e14 (2006).
57. Zaidmanremy, A. et al. Drosophila immunity: analysis of PGRP-SB1 expression, enzymatic activity and function. PLoS ONE 6, e17231 (2011).
58. Paredes, J. C., Welchman, D. P., Poidevin, M. & Lemaitre, B. Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection. Immunity 35, 770-779 (2011).
59. Kleino, A. et al. Pirk is a negative regulator of the Drosophila Imd pathway. J. Immunol. 180, 5413-5422 (2008).
60. Aggarwal, K. et al. Rudra interrupts receptor signaling complexes to negatively regulate the IMD pathway. PLoS Pathog. 4, e1000120 (2008).
61. Maillet, F., Bischoff, V., Vignal, C., Hoffmann, J. & Royet, J. The Drosophila peptidoglycan recognition protein PGRP-LF blocks PGRP-LC and IMD/JNK pathway activation. Cell Host Microbe 3, 293-303 (2008).
62. Basbous, N. et al. The Drosophila peptidoglycan-recognition protein LF interacts with peptidoglycan-recognition protein LC to downregulate the Imd pathway. EMBO Rep. 12, 327-333 (2011).
63. Lee, K.-Z. & Ferrandon, D. Negative regulation of immune responses on the fly. EMBO J. 30, 988-990 (2011).
64. Aggarwal, K. & Silverman, N. Positive and negative regulation of the Drosophila immune response. BMB Rep. 41, 267-277 (2008).
65. Ha, E.-M., Oh, C.-T., Bae, Y. S. & Lee, W.-J. A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847-850 (2005).
66. Bae, Y. S., Choi, M. K. & Lee, W.-J. Dual oxidase in mucosal immunity and host-microbe homeostasis. Trends Immunol. 31, 278-287 (2010).
67. Kumar, S., Molina-Cruz, A., Gupta, L., Rodrigues, J. & Barillas-Mury, C. A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327, 1644-1648 (2010).
68. Anh, N. T. T., Nishitani, M., Harada, S., Yamaguchi, M. & Kamei, K. Essential role of Duox in stabilization of Drosophila wing. J. Biol. Chem. 286, 33244-33251 (2011).
69. Juarez, M. T., Patterson, R. A., Sandoval-Guillen, E. & McGinnis, W. Duox, Flotillin-2, and Src42A are required to activate or delimit the spread of the transcriptional response to epidermal wounds in Drosophila. PLoS Genet. 7, e1002424 (2011).
70. Razzell, W., Evans, I. R., Martin, P. & Wood, W. Calcium flashes orchestrate the wound inflammatory response through DUOX activation and hydrogen peroxide release. Curr. Biol. 23, 424-429 (2013).
71. 2+ pathway in Drosophila gut immunity. Dev. Cell 16, 386-397 (2009).
72. Ha, E.-M. et al. Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in Drosophila gut. Nature Immunol. 10, 949-957 (2009).
73. Chen, J. et al. Participation of the p38 pathway in Drosophila host defense against pathogenic bacteria and fungi. Proc. Natl Acad. Sci. USA 170, 20774-20779 (2010).
74. Lee, K.-A. et al. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153, 797-811 (2013).
75. Osman, D. et al. Autocrine and paracrine unpaired signalling regulate intestinal stem cell maintenance and division. J. Cell Sci. 125, 5944-5949 (2012).
76. Michaut, L. et al. Determination of the disulfide array of the first inducible antifungal peptide from insects: drosomycin from Drosophila melanogaster. FEBS Lett. 395, 6-10 (1996).
77. Zhang, Z.-T. & Zhu, S.-Y. Drosomycin, an essential component of antifungal defence in Drosophila. Insect Mol. Biol. 18, 549-556 (2009).
78. Zaidmanremy, A., Regan, J. C., Brandão, A. S. & Jacinto, A. The Drosophila larva as a tool to study gut-associated macrophages: PI3K regulates a discrete hemocyte population at the proventriculus. Dev. Comp. Immunol. 36, 638-647 (2012).
79. Cronin, S. J. F. et al. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 325, 340-343 (2009).
80. Jiang, H. et al. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137, 1343-1355 (2009).
81. Chatterjee, M. & Ip, Y. T. Pathogenic stimulation of intestinal stem cell response in Drosophila. J. Cell. Physiol. 220, 664-671 (2009).
82. Schneider, D. S. & Ayres, J. S. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nature Rev. Immunol. 8, 889-895 (2008).
83. Apidianakis, Y., Pitsouli, C., Perrimon, N. & Rahme, L. Synergy between bacterial infection and genetic predisposition in intestinal dysplasia. Proc. Natl Acad. Sci. USA 106, 20883-20888 (2009).
84. Jiang, H., Grenley, M. O., Bravo, M.-J., Blumhagen, R. Z. & Edgar, B. A. EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell 8, 84-95 (2011).
85. Zhou, F., Rasmussen, A., Lee, S. & Agaisse, H. The UPD3 cytokine couples environmental challenge and intestinal stem cell division through modulation of JAK/STAT signaling in the stem cell microenvironment. Dev. Biol. 373, 383-393 (2012).
86. Cordero, J. B., Stefanatos, R. K., Scopelliti, A., Vidal, M. & Sansom, O. J. Inducible progenitor-derived Wingless regulates adult midgut regeneration in Drosophila. EMBO J. 31, 3901-3917 (2012).
87. Biteau, B. & Jasper, H. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 138, 1045-1055 (2011).
88. Ren, F. et al. Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc. Natl Acad. Sci. USA 107, 21064-21069 (2010).
89. Karpowicz, P., Perez, J. & Perrimon, N. The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137, 4135-4145 (2010).
90. Shaw, R. L. et al. The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137, 4147-4158 (2010).
91. Staley, B. K. & Irvine, K. D. Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr. Biol. 20, 1580-1587 (2010).
92. Choi, N.-H., Kim, J.-G., Yang, D.-J., Kim, Y.-S. & Yoo, M.-A. Age-related changes in Drosophila midgut are associated with PVF2, a PDGF/VEGF-like growth factor. Aging Cell 7, 318-334 (2008).
93. Biteau, B., Hochmuth, C. E. & Jasper, H. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3, 442-455 (2008).
94. Rera, M., Clark, R. I. & Walker, D. W. Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proc. Natl Acad. Sci. USA 109, 21528-21533 (2012).
95. Mulet, M., Gomila, M., Lemaitre, B., Lalucat, J. & García-Valdés, E. Taxonomic characterisation of Pseudomonas strain L48 and formal proposal of Pseudomonas entomophila sp. nov. Syst. Appl. Microbiol. 35, 145-149 (2012).
96. Chakrabarti, S., Liehl, P., Buchon, N. & Lemaitre, B. Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe 12, 60-70 (2012).
97. Gonzalez, M. R., Bischofberger, M., Pernot, L., van der Goot, F.-G. G. & Frêche, B. Bacterial pore-forming toxins: the (w)hole story? Cell. Mol. Life Sci. 65, 493-507 (2008).
98. Gonzalez, M. R. et al. Pore-forming toxins induce multiple cellular responses promoting survival. Cell. Microbiol. 13, 1026-1043 (2011).
99. Opota, O. et al. Monalysin, a novel ß-pore-forming toxin from the Drosophila pathogen Pseudomonas entomophila, contributes to host intestinal damage and lethality. PLoS Pathog. 7, e1002259 (2011).
100. Kocks, C. et al. Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123, 335-346 (2005).
101. Chung, Y.-S. A. & Kocks, C. Recognition of pathogenic microbes by the Drosophila phagocytic pattern recognition receptor eater. J. Biol. Chem. 286, 26524-26532 (2011).
102. Limmer, S. et al. Pseudomonas aeruginosa RhlR is required to neutralize the cellular immune response in a Drosophila melanogaster oral infection model. Proc. Natl Acad. Sci. USA 108, 17378-17383 (2011).
103. Berkey, C. D., Blow, N. & Watnick, P. I. Genetic analysis of Drosophila melanogaster susceptibility to intestinal Vibrio cholerae infection. Cell. Microbiol. 11, 461-474 (2009).
104. Purdy, A. E. & Watnick, P. I. Spatially selective colonization of the arthropod intestine through activation of Vibrio cholerae biofilm formation. Proc. Natl Acad. Sci. USA 108, 19737-19742 (2011).
105. Vallet-Gely, I., Lemaitre, B. & Boccard, F. Bacterial strategies to overcome insect defences. Nature Rev. Microbiol. 6, 302-313 (2008).
106. Stensmyr, M. C. et al. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151, 1345-1357 (2012).
107. Shivers, R. P., Kooistra, T., Chu, S. W., Pagano, D. J. & Kim, D. Tissue-specific activities of an immune signaling module regulate physiological responses to pathogenic and nutritional bacteria in C. elegans. Cell Host Microbe 6, 321-330 (2009).
108. van Frankenhuyzen, K. Insecticidal activity of Bacillus thuringiensis crystal proteins. J. Invertebr. Pathol. 101, 1-16 (2009).
109. Muniz, L. R., Knosp, C. & Yeretssian, G. Intestinal antimicrobial peptides during homeostasis, infection, and disease. Front. Immunol. 3, 310 (2012).
110. Liu, X., Lu, R., Wu, S. & Sun, J. Salmonella regulation of intestinal stem cells through the Wnt/β-catenin pathway. FEBS Lett. 584, 911-916 (2010).
111. Abreu, M. T. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nature Rev. Immunol. 10, 131-144 (2010).
112. Demerec, M. Biology of Drosophila (Cold Spring Harbor Lab. Press, 1994).
113. Micchelli, C. A. & Perrimon, N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439, 475-479 (2006).
114. Ohlstein, B. & Spradling, A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439, 470-474 (2006).
115. Ohlstein, B. & Spradling, A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential Notch signaling. Science 315, 988-992 (2007).
116. Khush, R. S. & Lemaitre, B. Genes that fight infection: what the Drosophila genome says about animal immunity. Trends Genet. 16, 442-449 (2000).