Host-microbe interactions in the gut of Drosophila melanogaster

Frontiers in Physiology

Volumn 4 DEC, Issue , 2013, Pages

  Kuraishi, Takayuki ^a,b   Hori, Aki ^a   Kurata, Shoichiro ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Antimicrobial peptide; Drosophila; Gut flora; Innate immunity; Intestinal stem cell; Peritrophic matrix; Reactive oxygen species

Indexed keywords

POLYPEPTIDE ANTIBIOTIC AGENT; REACTIVE OXYGEN METABOLITE;

ACETOBACTER; CANDIDA ALBICANS; CELL DIFFERENTIATION; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; EPITHELIUM CELL; EXPOSURE; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INTESTINE; INTESTINE EPITHELIUM; LACTOBACILLUS; MOLECULAR MECHANICS; MOUTH INFECTION; NONHUMAN; ORGANISMAL INTERACTION; PLASMODIUM; REVIEW; STEM CELL;

EID: 84891683137     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00375     Document Type: Review

References (86)

1. Abraham, E. G., and Jacobs-Lorena, M. (2004). Mosquito midgut barriers to malaria parasite development. Insect. Biochem. Mol. Biol. 34, 667-671. doi: 10.1016/j.ibmb.2004.03.019.
2. Aggarwal, K., Rus, F., Vriesema-Magnuson, C., Ertürk-Hasdemir, D., Paquette, N., and Silverman, N. (2008). Rudra interrupts receptor signaling complexes to negatively regulate the IMD pathway. PLoS Pathog. 4:e1000120. doi: 10.1371/journal.ppat.1000120.
3. Apidianakis, Y., Pitsouli, C., Perrimon, N., and Rahme, L. (2009). Synergy between bacterial infection and genetic predisposition in intestinal dysplasia. Proc. Natl. Acad. Sci. U.S.A. 106, 20883-20888. doi: 10.1073/pnas.0911797106.
4. Ayres, J. S., and Schneider, D. S. (2012). Tolerance of infections. Annu. Rev. Immunol. 30, 271-294. doi: 10.1146/annurev-immunol-020711-075030.
5. Babior, B. M. (1999). NADPH oxidase: an update. Blood 93, 1464-1476.
6. Bae, Y. S., Choi, M. K., and Lee, W. J. (2010). Dual oxidase in mucosal immunity and host-microbe homeostasis. Trends Immunol. 31, 278-287. doi: 10.1016/j.it.2010.05.003.
7. Basbous, N., Coste, F., Leone, P., Vincentelli, R., Royet, J., Kellenberger, C., et al. (2011). The Drosophila peptidoglycan-recognition protein LF interacts with peptidoglycan-recognition protein LC to downregulate the Imd pathway. EMBO Rep. 12, 327-333. doi: 10.1038/embor.2011.19.
8. Bischoff, V., Vignal, C., Duvic, B., Boneca, I. G., Hoffmann, J. A., and Royet, J. (2006). Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog. 2:e14. doi: 10.1371/journal.ppat.0020014.
9. Biteau, B., and Jasper, H. (2011). EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 138, 1045-1055. doi: 10.1242/dev.056671.
10. Blemont, M., Vincentelli, R., Kellenberger, C., Opota, O., Lemaitre, B., Roussel, A., et al. (2013). Crystallization and preliminary X-ray analysis of monalysin, a novel-pore-forming toxin from the entomopathogen Pseudomonas entomophila. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 69, 930-933. doi: 10.1107/S174430911301885X.
11. Bond, D., and Foley, E. (2012). Autocrine PDGF-VEGF receptor-related (Pvr) pathway activity controls intestinal stem cell proliferation in the adult Drosophila midgut. J. Biol. Chem. 287, 27359-27370. doi: 10.1074/jbc.M112.378018.
12. Bonnay, F., Cohen-Berros, E., Hoffmann, M., Kim, S. Y., Boulianne, G. L., Hoffmann, J. A., et al. (2013). big bang gene modulates gut immune tolerance in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 110, 2957-2962. doi: 10.1073/pnas.1221910110.
13. Bosco-Drayon, V., Poidevin, M., Boneca, I. G., Narbonne-Reveau, K., Royet, J., and Charroux, B. (2012). 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. doi: 10.1016/j.chom.2012.06.002.
14. Broderick, N. A., and Lemaitre, B. (2012). Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3, 307-321. doi: 10.4161/gmic.19896.
15. Buchon, N., Broderick, N. A., Chakrabarti, S., and Lemaitre, B. (2009a). Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 23, 2333-2344. doi: 10.1101/gad.1827009.
16. Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S., and Lemaitre, B. (2009b). Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5, 200-211. doi: 10.1016/j.chom.2009.01.003.
17. Buchon, N., Broderick, N. A., Kuraishi, T., and Lemaitre, B. (2010). Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biol. 8:152. doi: 10.1186/1741-7007-8-152.
18. Buchon, N., Broderick, N. A., and Lemaitre, B. (2013a). Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat. Rev. Microbiol. 11, 615-626. doi: 10.1038/nrmicro3074.
19. Buchon, N., Osman, D., David, F. P. A., Boquete, J. P., Deplancke, B., and Lemaitre, B. (2013b). Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep. 3, 1725-1738. doi: 10.1016/j.celrep.2013.04.001.
20. Chakrabarti, S., Liehl, P., Buchon, N., and Lemaitre, B. (2012). Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe 12, 60-70. doi: 10.1016/j.chom.2012.06.001.
21. Chatterjee, M., and Ip, Y. T. (2009). Pathogenic stimulation of intestinal stem cell response in Drosophila. J. Cell. Physiol. 220, 664-671. doi: 10.1002/jcp.21808.
22. Cirimotich, C. M., Dong, Y., Garver, L. S., Sim, S., and Dimopoulos, G. (2010). Mosquito immune defenses against Plasmodium infection. Dev. Comp. Immunol. 34, 387-395. doi: 10.1002/jcp.21808.
23. Cognigni, P., Bailey, A. P., and Miguel-Aliaga, I. (2011). Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab. 13, 92-104. doi: 10.1016/j.cmet.2010.12.010.
24. Cordero, J. B., Stefanatos, R. K., Scopelliti, A., Vidal, M., and Sansom, O. J. (2012). Inducible progenitor-derived Wingless regulates adult midgut regeneration in Drosophila. EMBO J. 31, 3901-3917. doi: 10.1038/emboj.2012.248.
25. Cronin, S. J., Nehme, N. T., Limmer, S., Liegeois, S., Pospisilik, J. A., Schramek, D., et al. (2009). Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 325, 340-343. doi: 10.1126/science.1173164.
26. Cummings, J. H., and MacFarlane, G. T. (1997). Role of intestinal bacteria in nutrient metabolism. JPEN J. Parenter. Enteral Nutr. 21, 357-365. doi: 10.1177/0148607197021006357.
27. Ferrandon, D. (2013). The complementary facets of epithelial host defenses in the genetic model organism Drosophila melanogaster: from resistance to resilience. Curr. Opin. Immunol. 25, 59-70. doi: 10.1016/j.coi.2012.11.008.
28. Glittenberg, M. T., Kounatidis, I., Christensen, D., Kostov, M., Kimber, S., Roberts, I., et al. (2011). 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. doi: 10.1242/dmm.006627.
29. Ha, E. M., Lee, K. A., Park, S. H., Kim, S. H., Nam, H. J., Lee, H. Y., et al. (2009a). Regulation of DUOX by the Gaq-phospholipase Cβ-Ca2+ pathway in Drosophila gut immunity. Dev. Cell 16, 386-397. doi: 10.1016/j.devcel.2008.12.015.
30. Ha, E. M., Lee, K. A., Seo, Y. Y., Kim, S. H., Lim, J. H., Oh, B. H., et al. (2009b). Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in drosophila gut. Nat. Immunol. 10, 949-957. doi: 10.1038/ni.1765.
31. Ha, E. M., Oh, C. T., Bae, Y. S., and Lee, W. J. (2005). A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847-850. doi: 10.1126/science.1117311.
32. Hashimoto, T., Perlot, T., Rehman, A., Trichereau, J., Ishiguro, H., Paolino, M., et al. (2012). ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature 487, 477-481. doi: 10.1038/nature11228.
33. Hayakawa, T., Shitomi, Y., Miyamoto, K., and Hori, H. (2004). GalNAc pretreatment inhibits trapping of Bacillus thuringiensis Cry1Ac on the peritrophic membrane of Bombyx mori. FEBS Lett. 576, 331-335. doi: 10.1016/j.febslet.2004.09.029.
34. Hegan, P. S., Mermall, V., Tilney, L. G., and Mooseker, M. S. (2007). 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. doi: 10.1091/mbc.E07-02-0191.
35. Hegedus, D., Erlandson, M., Gillott, C., and Toprak, U. (2009). New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol. 54, 285-302. doi: 10.1146/annurev.ento.54.110807.090559.
36. Iwasaki, A., and Medzhitov, R. (2010). Regulation of adaptive immunity by the innate immune system. Science 327, 291-295. doi: 10.1126/science.1183021.
37. Jiang, H., Grenley, M. O., Bravo, M. J., Blumhagen, R. Z., and Edgar, B. A. (2011). EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell 8, 84-95. doi: 10.1016/j.stem.2010.11.026.
38. Jiang, H., Patel, P. H., Kohlmaier, A., Grenley, M. O., Mcewen, D. G., and Edgar, B. A. (2009). Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137, 1343-1355. doi: 10.1016/j.cell.2009.05.014.
39. Karpowicz, P., Perez, J., and Perrimon, N. (2010). The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 138, 4135-4145. doi: 10.1242/dev.060483.
40. Kleino, A., Myllymäki, H., Kallio, J., Vanha-Aho, L. M., Oksanen, K., Ulvila, J., et al. (2008). Pirk is a negative regulator of the Drosophila Imd pathway. J. Immunol. 180, 5413-5422.
41. Kleino, A., and Silverman, N. (2013). The Drosophila IMD pathway in the activation of the humoral immune response. Dev. Comp. Immunol. 42, 25-35. doi: 10.1016/j.dci.2013.05.014.
42. Kumar, S., Molina-Cruz, A., Gupta, L., Rodrigues, J., and Barillas-Mury, C. (2010). A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327, 1644-1648. doi: 10.1126/science.1184008.
43. Kuraishi, T., Binggeli, O., Opota, O., Buchon, N., and Lemaitre, B. (2011). Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 108, 15966-15971. doi: 10.1073/pnas.1105994108.
44. Kurata, S. (2004). Recognition of infectious non-self and activation of immune responses by peptidoglycan recognition protein (PGRP)-family members in Drosophila. Dev. Comp. Immunol. 28, 89-95. doi: 10.1016/S0145-305X(03)00121-6.
45. Kurata, S. (2010). Extracellular and intracellular pathogen recognition by Drosophila PGRP-LE and PGRP-LC. Int. Immunol. 22, 143-148. doi: 10.1093/intimm/dxp128.
46. Lambrechts, L., Scott, T. W., and Gubler, D. J. (2010). Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission. PLoS Negl. Trop. Dis. 4:e646. doi: 10.1371/journal.pntd.0000646.
47. Lee, K. A., Kim, S. H., Kim, E. K., Ha, E. M., You, H., Kim, B., et al. (2013). Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153, 797-811. doi: 10.1016/J.Cell.2013.04.009.
48. Lee, K. Z., and Ferrandon, D. (2011). Negative regulation of immune responses on the fly. EMBO J. 30, 988-990. doi: 10.1038/emboj.2011.47.
49. Lehane, M. J. (1997). Peritrophic matrix structure and function. Annu. Rev. Entomol. 42, 525-550. doi: 10.1146/annurev.ento.42.1.525.
50. Lemaitre, B., and Hoffmann, J. (2007). The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697-743. doi: 10.1146/annurev.immunol.25.022106.141615.
51. Lemaitre, B., and Miguel-Aliaga, I. (2013). The digestive tract of Drosophila melanogaster. Annu. Rev. Genet. 47, 395-422. doi: 10.1146/annurev.genet.111212-133343.
52. Lhocine, N., Ribeiro, P. S., Buchon, N., Wepf, A., Wilson, R., Tenev, T., et al. (2008). PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 4, 147-158. doi: 10.1016/j.chom.2008.07.004.
53. Liehl, P., Blight, M., Vodovar, N., Boccard, F., and Lemaitre, B. (2006). Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. PLoS Pathog. 2:e56. doi: 10.1371/journal.ppat.0020056.
54. Lin, G., Xu, N., and Xi, R. (2008). Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 455, 1119-1123. doi: 10.1038/nature07329.
55. Maillet, F., Bischoff, V., Vignal, C., Hoffmann, J., and Royet, J. (2008). The Drosophila peptidoglycan recognition protein PGRP-LF blocks PGRP-LC and IMD/JNK pathway activation. Cell Host Microbe 3, 293-303. doi: 10.1016/j.chom.2008.04.002.
56. Marianes, A., and Spradling, A. C. (2013). Physiological and stem cell compartmentalization within the Drosophila midgut. eLife 2, e00886. doi: 10.7554/eLife.00886.
57. Micchelli, C. A., and Perrimon, N. (2006). Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439, 475-479. doi: 10.1038/nature04371.
58. Nehme, N. T., Liégeois, S., Kele, B., Giammarinaro, P., Pradel, E., Hoffmann, J. A., et al. (2007). A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog. 3:e173. doi: 10.1371/journal.ppat.0030173.
59. Neyen, C., Poidevin, M., Roussel, A., and Lemaitre, B. (2012). Tissue-and ligand-specific sensing of Gram-negative infection in Drosophila by PGRP-LC isoforms and PGRP-LE. J. Immunol. 189, 1886-1897. doi: 10.4049/jimmunol.1201022.
60. Ohlstein, B., and Spradling, A. (2006). The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439, 470-474. doi: 10.1038/nature04333.
61. O'Neill, L. A., Golenbock, D., and Bowie, A. G. (2013). The history of Toll-like receptors-redefining innate immunity. Nat. Rev. Immunol. 13, 453-460. doi: 10.1038/nri3446.
62. Opota, O., Vallet-Gely, I., Vincentelli, R., Kellenberger, C., Iacovache, I., Gonzalez, M. R., et al. (2011). Monalysin, a novel β-pore-forming toxin from the Drosophila pathogen Pseudomonas entomophila, contributes to host intestinal damage and lethality. PLoS Pathog. 7:e1002259. doi: 10.1371/journal.ppat.1002259.
63. Osman, D., Buchon, N., Chakrabarti, S., Huang, Y. T., Su, W. C., Poidevin, M., et al. (2012). Autocrine and paracrine unpaired signaling regulate intestinal stem cell maintenance and division. J. Cell Sci. 125, 5944-5949. doi: 10.1242/jcs.113100.
64. Paredes, J. C., Welchman, D. P., Poidevin, M., and Lemaitre, B. (2011). Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection. Immunity 35, 770-779. doi: 10.1016/j.immuni.2011.09.018.
65. Ridley, E. V., Wong, A. C., Westmiller, S., and Douglas, A. E. (2012). Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS ONE 7:e36765. doi: 10.1371/journal.pone.0036765.
66. Round, J. L., and Mazmanian, S. K. (2009). The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313-323. doi: 10.1038/nri2515.
67. Royet, J. (2011). Epithelial homeostasis and the underlying molecular mechanisms in the gut of the insect model Drosophila melanogaster. Cell. Mol. Life Sci. 68, 3651-3660. doi: 10.1007/s00018-011-0828-x.
68. Ryu, J. H., Ha, E. M., Oh, C. T., Seol, J. H., Brey, P. T., Jin, I., et al. (2006). An essential complementary role of NF-κB pathway to microbicidal oxidants in Drosophila gut immunity. EMBO J 25, 3693-3701. doi: 10.1038/sj.emboj.7601233.
69. Ryu, J. H., Kim, S. H., Lee, H. Y., Bai, J. Y., Nam, Y. D., Bae, J. W., et al. (2008). Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319, 777-782. doi: 10.1126/science.1149357.
70. Saha, S., Jing, X., Park, S. Y., Wang, S., Li, X., Gupta, D., et al. (2010). Peptidoglycan recognition proteins protect mice from experimental colitis by promoting normal gut flora and preventing induction of interferon-γ. Cell Host Microbe 8, 147-162. doi: 10.1016/j.chom.2010.07.005.
71. Sartor, R. B. (2004). Microbial influences in inflammatory bowel diseases. Gastroenterology 134, 577-594. doi: 10.1053/j.gastro.2007.11.059.
72. Shaw, R. L., Kohlmaier, A., Polesello, C., Veelken, C., Edgar, B. A., and Tapon, N. (2010). The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137, 4147-4158. doi: 10.1242/dev.052506.
73. Shibata, T., Sekihara, S., Fujikawa, T., Miyaji, R., Maki, K., Ishihara, T., et al. (2013). Transglutaminase-catalyzed protein-protein cross-linking suppresses the activity of the NF-κB-like transcription factor Relish. Sci. Signal. 6, ra61. doi: 10.1126/scisignal.2003970.
74. Shin, S. C., Kim, S. H., You, H., Kim, B., Kim, A. C., Lee, K. A., et al. (2011). Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334, 670-674. doi: 10.1126/science.1212782.
75. Staley, B. K., and Irvine, K. D. (2010). Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr. Biol. 20, 1580-1587. doi: 10.1016/j.cub.2010.07.041.
76. Storelli, G., Defaye, A., Erkosar, B., Hols, P., Royet, J., and Leulier, F. (2011). Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab. 14, 403-414. doi: 10.1016/j.cmet.2011.07.012.
77. Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820. doi: 10.1016/j.cell.2010.01.022.
78. Tellam, R. L. (1996). "The peritrophic matrix," in Biology of the Insect Midgut, ed M. J. Lehane and P. F. Billingsley (Cambridge: Chapman and Hall), 86-114.
79. Tzou, P., Ohresser, S., Ferrandon, D., Capovilla, M., Reichhart, J. M., Lemaitre, B., et al. (2000). Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13, 737-748. doi: 10.1016/S1074-7613(00)00072-8.
80. Vodovar, N., Vinals, M., Liehl, P., Basset, A., Degrouard, J., Spellman, P., et al. (2005). Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc. Natl. Acad. Sci. U.S.A. 102, 11414-11419. doi: 10.1073/pnas.0502240102.
81. Wong, C. N. A., Ng, P., and Douglas, A. E. (2011). Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ. Microbiol. 13, 1889-1900. doi: 10.1111/j.1462-2920.2011.02511.x.
82. Yassine, H., and Osta, M. A. (2010). Anopheles gambiae innate immunity. Cell. Microbiol. 12, 1-9. doi: 10.1111/j.1462-5822.2009.01388.x.
83. Yoshimoto, S., Loo, T. M., Atarashi, K., Kanda, H., Sato, S., Oyadomari, S., et al. (2013). Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499, 97-101. doi: 10.1038/nature12347.
84. Zaidman-Rémy, A., Hervé, M., Poidevin, M., Pili-Floury, S., Kim, M. S., Blanot, D., et al. (2006). The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24, 463-473. doi: 10.1016/j.immuni.2006.02.012.
85. Zasloff, M. (2002). Antimicrobial peptides of multicellular organisms. Nature 415, 389-395. doi: 10.1038/415389a.
86. Zhou, F., Rasmussen, A., Lee, S., and Agaisse, H. (2013). 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. doi: 10.1016/j.ydbio.2012.10.023.