International Journal of Stem Cells

Korean Society for Stem Cell Research (한국줄기세포학회)
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Host-Microbe Interactions Regulate Intestinal Stem Cells and Tissue Turnover in Drosophila

  • Ji-Hoon Lee (National Creative Research Initiative Center for Hologenomics and School of Biological Sciences, Seoul National University)
  • Received : 2023.10.30
  • Accepted : 2023.11.22
  • Published : 2024.02.28
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Abstract

With the activity of intestinal stem cells and continuous turnover, the gut epithelium is one of the most dynamic tissues in animals. Due to its simple yet conserved tissue structure and enteric cell composition as well as advanced genetic and histologic techniques, Drosophila serves as a valuable model system for investigating the regulation of intestinal stem cells. The Drosophila gut epithelium is in constant contact with indigenous microbiota and encounters externally introduced "non-self" substances, including foodborne pathogens. Therefore, in addition to its role in digestion and nutrient absorption, another essential function of the gut epithelium is to control the expansion of microbes while maintaining its structural integrity, necessitating a tissue turnover process involving intestinal stem cell activity. As a result, the microbiome and pathogens serve as important factors in regulating intestinal tissue turnover. In this manuscript, I discuss crucial discoveries revealing the interaction between gut microbes and the host's innate immune system, closely associated with the regulation of intestinal stem cell proliferation and differentiation, ultimately contributing to epithelial homeostasis.

Keywords

Acknowledgement

I thank Dr. Won-Jae Lee (Seoul National University) for critical reading of the manuscript.

References

  1. Leblond CP, Walker BE. Renewal of cell populations. Physiol Rev 1956;36:255-276
  2. Ohlstein B, Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 2006;439:470-474
  3. Micchelli CA, Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 2006;439:475-479
  4. O'Brien LE, Soliman SS, Li X, Bilder D. Altered modes of stem cell division drive adaptive intestinal growth. Cell 2011;147:603-614
  5. Lee JH, Lee KA, Lee WJ. Microbiota, gut physiology, and insect immunity. Adv Insect Physiol 2017;52:111-138
  6. Zwick RK, Ohlstein B, Klein OD. Intestinal renewal across the animal kingdom: comparing stem cell activity in mouse and Drosophila. Am J Physiol Gastrointest Liver Physiol 2019;316:G313-G322
  7. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian theory of the origin of the four epithelial cell types. Am J Anat 1974;141:537-561
  8. Gehart H, Clevers H. Tales from the crypt: new insights into intestinal stem cells. Nat Rev Gastroenterol Hepatol 2019;16:19-34
  9. Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007;449:1003-1007
  10. Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell 2013;154:274-284
  11. Marianes A, Spradling AC. Physiological and stem cell compartmentalization within the Drosophila midgut. Elife 2013;2:e00886
  12. Buchon N, Osman D, David FP, et al. Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep 2013;3:1725-1738 Erratum in: Cell Rep 2013;3:1755
  13. Guo Z, Ohlstein B. Stem cell regulation. Bidirectional Notch signaling regulates Drosophila intestinal stem cell multipotency. Science 2015;350:aab0988
  14. Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet 2011;7:e1002272
  15. Ryu JH, Kim SH, Lee HY, et al. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 2008;319:777-782
  16. Cox CR, Gilmore MS. Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect Immun 2007;75:1565-1576
  17. Ren C, Webster P, Finkel SE, Tower J. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab 2007;6:144-152
  18. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 2011;14:403-414
  19. Clark RI, Walker DW. Role of gut microbiota in aging-related health decline: insights from invertebrate models. Cell Mol Life Sci 2018;75:93-101
  20. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci U S A 2010;107:20051-20056 Erratum in: Proc Natl Acad Sci U S A 2013;110:4853
  21. Shin SC, Kim SH, You H, et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 2011;334:670-674
  22. Lee KA, Kim SH, Kim EK, et al. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 2013;153:797-811
  23. Amcheslavsky A, Jiang J, Ip YT. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 2009;4:49-61
  24. Buchon N, Broderick NA, Chakrabarti S, Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev 2009;23:2333-2344
  25. Lemaitre B, Kromer-Metzger E, Michaut L, et al. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci U S A 1995;92:9465-9469
  26. Choe KM, Werner T, Stoven S, Hultmark D, Anderson KV. Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 2002;296:359-362
  27. Gottar M, Gobert V, Michel T, Belvin M, Duyk G, Hoffmann JA, et al. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 2002;416:640-644
  28. Ramet M, Manfruelli P, Pearson A, Mathey-Prevot B, Ezekowitz RA. Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 2002;416:644-648
  29. Bosco-Drayon V, Poidevin M, Boneca IG, Narbonne-Reveau K, Royet J, Charroux B. Peptidoglycan sensing by the receptor PGRP-LE in the Drosophila gut induces immune responses to infectious bacteria and tolerance to microbiota. Cell Host Microbe 2012;12:153-165
  30. Myllymaki H, Valanne S, Ramet M. The Drosophila imd signaling pathway. J Immunol 2014;192:3455-3462
  31. Wang L, Ryoo HD, Qi Y, Jasper H. PERK limits Drosophila lifespan by promoting intestinal stem cell proliferation in response to ER stress. PLoS Genet 2015;11:e1005220
  32. Guo L, Karpac J, Tran SL, Jasper H. PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell 2014;156:109-122
  33. Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 2009;137:1343-1355
  34. Houtz P, Bonfini A, Liu X, et al. Hippo, TGF-β, and Src-MAPK pathways regulate transcription of the upd3 cytokine in Drosophila enterocytes upon bacterial infection. PLoS Genet 2017;13:e1007091
  35. Iatsenko I, Boquete JP, Lemaitre B. Microbiota-derived lactate activates production of reactive oxygen species by the intestinal NADPH oxidase Nox and shortens Drosophila lifespan. Immunity 2018;49:929-942.e5
  36. Ha EM, Oh CT, Bae YS, Lee WJ. A direct role for dual oxidase in Drosophila gut immunity. Science 2005;310:847-850
  37. Ha EM, Lee KA, Seo YY, et al. Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in drosophila gut. Nat Immunol 2009;10:949-957
  38. Ha EM, Oh CT, Ryu JH, et al. An antioxidant system required for host protection against gut infection in Drosophila. Dev Cell 2005;8:125-132
  39. Kim EK, Lee KA, Hyeon DY, et al. Bacterial nucleoside catabolism controls quorum sensing and commensal-to-pathogen transition in the Drosophila gut. Cell Host Microbe 2020;27:345-357.e6
  40. Lee KA, Cho KC, Kim B, et al. Inflammation-modulated metabolic reprogramming is required for DUOX-dependent gut immunity in Drosophila. Cell Host Microbe 2018; 23:338-352.e5
  41. Ren F, Wang K, Zhang T, Jiang J, Nice EC, Huang C. New insights into redox regulation of stem cell self-renewal and differentiation. Biochim Biophys Acta 2015;1850:1518-1526
  42. Owusu-Ansah E, Banerjee U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 2009;461:537-541
  43. Hochmuth CE, Biteau B, Bohmann D, Jasper H. Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell 2011;8:188-199
  44. Xu C, Luo J, He L, Montell C, Perrimon N. Oxidative stress induces stem cell proliferation via TRPA1/RyR-mediated Ca2+ signaling in the Drosophila midgut. Elife 2017;6:e22441
  45. Basset A, Khush RS, Braun A, et al. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci U S A 2000;97:3376-3381
  46. Basset A, Tzou P, Lemaitre B, Boccard F. A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster. EMBO Rep 2003;4:205-209
  47. Quevillon-Cheruel S, Leulliot N, Muniz CA, et al. Evf, a virulence factor produced by the Drosophila pathogen Erwinia carotovora, is an S-palmitoylated protein with a new fold that binds to lipid vesicles. J Biol Chem 2009;284:3552-3562
  48. Vodovar N, Vinals M, Liehl P, et al. Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc Natl Acad Sci U S A 2005;102:11414-11419
  49. 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 2006;2:e56
  50. Opota O, Vallet-Gely I, Vincentelli R, et al. Monalysin, a novel β-pore-forming toxin from the Drosophila pathogen Pseudomonas entomophila, contributes to host intestinal damage and lethality. PLoS Pathog 2011;7:e1002259
  51. 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 2012;12:60-70
  52. Lyczak JB, Cannon CL, Pier GB. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2000;2:1051-1060
  53. Grimont PA, Grimont F. The genus Serratia. Annu Rev Microbiol 1978;32:221-248
  54. Flyg C, Kenne K, Boman HG. Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J Gen Microbiol 1980;120:173-181
  55. Kurz CL, Chauvet S, Andres E, et al. Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening. EMBO J 2003;22:1451-1460
  56. Lee KZ, Lestradet M, Socha C, et al. Enterocyte purge and rapid recovery is a resilience reaction of the gut epithelium to pore-forming toxin attack. Cell Host Microbe 2016;20:716-730
  57. Apidianakis Y, Pitsouli C, Perrimon N, Rahme L. Synergy between bacterial infection and genetic predisposition in intestinal dysplasia. Proc Natl Acad Sci U S A 2009;106:20883-20888
  58. Cronin SJ, Nehme NT, Limmer S, et al. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 2009;325:340-343
  59. Chatterjee M, Ip YT. Pathogenic stimulation of intestinal stem cell response in Drosophila. J Cell Physiol 2009;220:664-671