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Intestinal Homeostasis and Longevity: Drosophila Gut Feeling

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Aging and Aging-Related Diseases

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1086))

Abstract

The association between intestinal homeostasis and life span has caught the attention of the research community worldwide. There have been multiple evidences which support the role of gut homeostasis in aging. The Drosophila gastrointestinal tract is very similar to the mammalian gut, and therefore it can directly be used as a model to understand the association between gut microbiota, immune system, and aging in humans. In current review we have discussed the importance of gut microbiota in aging. Also we have highlighted the importance of host immune system and gut aging. Since the increased microbial load in the gut activates the host immune system, the dysregulated microbiota can have direct implications in gut aging. The proliferation and renewal of intestinal stem cells can also affect gut aging. Another important aspect that we have discussed is the communication between the gut and the other organ systems which affect the overall aging process. Altogether we propose that the Drosophila gut can be a good model to improve our understanding of human gut aging.

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References

  • Amcheslavsky A, Ip YT (2012) Be a good neighbor: organ-to-organ communication during the innate immune response. Cell Host Microbe 11:323–324

    Article  CAS  PubMed  Google Scholar 

  • Amcheslavsky A, Jiang J, Ip YT (2009) Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 4:49–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amcheslavsky A, Song W, Li Q, Nie Y, Bragatto I, Ferrandon D, Perrimon N, Ip YT (2014) Enteroendocrine cells support intestinal stem-cell-mediated homeostasis in Drosophila. Cell Rep 9:32–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayyaz A, Jasper H (2013) Intestinal inflammation and stem cell homeostasis in aging Drosophila melanogaster. Front Cell Infect Microbiol 3:98

    Article  PubMed  PubMed Central  Google Scholar 

  • Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, Royet J (2006) Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog 2:e14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Biteau B, Hochmuth CE, Jasper H (2008) JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3:442–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biteau B, Hochmuth CE, Jasper H (2011) Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. Cell Stem Cell 9:402–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broderick NA, Buchon N, Lemaitre B (2014) Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. MBio 5:e01117–e01114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brummel T, Ching A, Seroude L, Simon AF, Benzer S (2004) Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci U S A 101:12974–12979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B (2009) Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5:200–211

    Article  CAS  PubMed  Google Scholar 

  • Buchon N, Broderick NA, Lemaitre B (2013) Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat Rev Microbiol 11:615–626

    Article  CAS  PubMed  Google Scholar 

  • Chakrabarti S, Poidevin M, Lemaitre B (2014) The Drosophila MAPK p38c regulates oxidative stress and lipid homeostasis in the intestine. PLoS Genet 10:e1004659

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen H, Zheng X, Zheng Y (2014) Age-associated loss of lamin-B leads to systemic inflammation and gut hyperplasia. Cell 159:829–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Zheng X, Zheng Y (2015) Lamin-B in systemic inflammation, tissue homeostasis, and aging. Nucleus 6:183–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark RI, Salazar A, Yamada R, Fitz-Gibbon S, Morselli M, Alcaraz J, Rana A, Rera M, Pellegrini M, William WJ (2015) Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Rep 12:1656–1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costechareyre D, Capo F, Fabre A, Chaduli D, Kellenberger C, Roussel A, Charroux B, Royet J (2016) Tissue-specific regulation of Drosophila NF-x03BA; B pathway activation by peptidoglycan recognition protein SC. J Innate Immun 8:67–80

    Article  CAS  PubMed  Google Scholar 

  • Dobson AJ, Chaston JM, Newell PD, Donahue L, Hermann SL, Sannino DR, Westmiller S, Wong AC, Clark AG, Lazzaro BP et al (2015) Host genetic determinants of microbiota-dependent nutrition revealed by genome-wide analysis of Drosophila melanogaster. Nat Commun 6:6312

    Article  CAS  PubMed  Google Scholar 

  • Dutta D, Dobson AJ, Houtz PL, Glasser C, Revah J, Korzelius J, Patel PH, Edgar BA, Buchon N (2015) Regional cell-specific transcriptome mapping reveals regulatory complexity in the adult Drosophila midgut. Cell Rep 12:346–358

    Article  CAS  PubMed  Google Scholar 

  • Fan X, Liang Q, Lian T, Wu Q, Gaur U, Li D, Yang D, Mao X, Jin Z, Li Y et al (2015) Rapamycin preserves gut homeostasis during Drosophila aging. Oncotarget 6:35274–35283

    Article  PubMed  PubMed Central  Google Scholar 

  • Fink C, Hoffmann J, Knop M, Li Y, Isermann K, Roeder T (2016) Intestinal FoxO signaling is required to survive oral infection in Drosophila. Mucosal Immunol 9:927

    Article  CAS  PubMed  Google Scholar 

  • Fontana L, Partridge L (2015) Promoting health and longevity through diet: from model organisms to humans. Cell 161:106–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaur U, Fan X, Yang M (2016) Rapamycin slows down gut aging. Aging 8:833–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gems D, Partridge L (2013) Genetics of longevity in model organisms: debates and paradigm shifts. Annu Rev Physiol 75:621–644

    Article  CAS  PubMed  Google Scholar 

  • Gervais L, Bardin AJ (2017) Tissue homeostasis and aging: new insight from the fly intestine. Curr Opin Cell Biol 48:97–105

    Article  CAS  PubMed  Google Scholar 

  • Guo L, Karpac J, Tran SL, Jasper H (2014) PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell 156:109–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ha EM, Oh CT, Bae YS, Lee WJ (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310:847–850

    Article  CAS  PubMed  Google Scholar 

  • Han M, Qin S, Song X, Li Y, Jin P, Chen L, Ma F (2013) Evolutionary rate patterns of genes involved in the Drosophila Toll and Imd signaling pathway. BMC Evol Biol 13:245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jiang H, Edgar BA (2012) Intestinal stem cell function in Drosophila and mice. Curr Opin Genet Dev 22:354–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA (2009) Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137:1343–1355

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim SH, Lee WJ (2014) Role of DUOX in gut inflammation: lessons from Drosophila model of gut-microbiota interactions. Front Cell Infect Microbiol 3:116

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee WJ, Hase K (2014) Gut microbiota-generated metabolites in animal health and disease. Nat Chem Biol 10:416–424

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743

    Article  CAS  PubMed  Google Scholar 

  • Li H, Qi Y, Jasper H (2016) Preventing age-related decline of gut compartmentalization limits microbiota dysbiosis and extends lifespan. Cell Host Microbe 19:240–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayer EA (2011) Gut feelings: the emerging biology of gut-brain communication. Nat Rev Neurosci 12:453–466

    Article  CAS  PubMed  Google Scholar 

  • Myllymaki H, Valanne S, Ramet M (2014) The Drosophila imd signaling pathway. J Immunol 192:3455–3462

    Article  PubMed  CAS  Google Scholar 

  • Nässel DR, Kubrak OI, Liu Y, Luo J, Lushchak OV (2013) Factors that regulate insulin producing cells and their output in Drosophila. Front Physiol 4:252

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470–474

    Article  CAS  PubMed  Google Scholar 

  • Paredes JC, Welchman DP, Poidevin M, Lemaitre B (2011) Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection. Immunity 35:770–779

    Article  CAS  PubMed  Google Scholar 

  • Piper MDW, Partridge L (2017) Drosophila as a model for ageing. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease. https://doi.org/10.1016/j.bbadis.2017.09.016

    Article  CAS  Google Scholar 

  • Regan JC, Khericha M, Dobson AJ, Bolukbasi E, Rattanavirotkul N, Partridge L (2016) Sex difference in pathology of the ageing gut mediates the greater response of female lifespan to dietary restriction. elife 5:e10956

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rera M, Bahadorani S, Cho J, Koehler CL, Ulgherait M, Hur JH, Ansari WS, Lo T Jr, Jones DL, Walker DW (2011) Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell Metab 14:623–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW, Lee DG, Shin SC, Ha EM, Lee WJ (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319:777–782

    Article  CAS  PubMed  Google Scholar 

  • Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904

    Article  CAS  PubMed  Google Scholar 

  • Shen R, Wang B, Giribaldi MG, Ayres J, Thomas JB, Montminy M (2016) Neuronal energy-sensing pathway promotes energy balance by modulating disease tolerance. Proc Natl Acad Sci U S A 113:E3307–E3314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shin SC, Kim SH, You H, Kim B, Kim AC, Lee KA, Yoon JH, Ryu JH, Lee WJ (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334:670–674

    Article  CAS  PubMed  Google Scholar 

  • Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14:403–414

    Article  CAS  PubMed  Google Scholar 

  • Tang WH, Kitai T, Hazen SL (2017) Gut microbiota in cardiovascular health and disease. Circ Res 120:1183–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulgherait M, Rana A, Rera M, Graniel J, Walker DW (2014) AMPK modulates tissue and organismal aging in a non-cell-autonomous manner. Cell Rep 8:1767–1780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaiserman AM, Koliada AK, Marotta F (2017) Gut microbiota: a player in aging and a target for anti-aging intervention. Ageing Res Rev 35:36–45

    Article  CAS  PubMed  Google Scholar 

  • Villanueva-Millan MJ, Perez-Matute P, Oteo JA (2015) Gut microbiota: a key player in health and disease. A review focused on obesity. J Physiol Biochem 71:509–525

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Karpac J, Jasper H (2014) Promoting longevity by maintaining metabolic and proliferative homeostasis. J Exp Biol 217:109–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Esteve E, Tremaroli V, Khan MT, Caesar R, Manneras-Holm L, Stahlman M, Olsson LM, Serino M, Planas-Felix M et al (2017) Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat Med 7:850–858

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Natural Science Foundation of China (No. 31771338 and No 81701392).

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Authors and Affiliations

  1. Institute of Animal Genetics and Breeding, Sichuan Agricultural University, Chengdu, China

    Xiaolan Fan & Mingyao Yang

  2. Faculty of Health Sciences, University of Macau, Beijing, China

    Uma Gaur

Authors
  1. Xiaolan Fan
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  2. Uma Gaur
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  3. Mingyao Yang
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Corresponding author

Correspondence to Mingyao Yang .

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Editors and Affiliations

  1. School of Pharmaceutical Sciences, Tsinghua University, Beijing, China

    Zhao Wang

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Fan, X., Gaur, U., Yang, M. (2018). Intestinal Homeostasis and Longevity: Drosophila Gut Feeling. In: Wang, Z. (eds) Aging and Aging-Related Diseases. Advances in Experimental Medicine and Biology, vol 1086. Springer, Singapore. https://doi.org/10.1007/978-981-13-1117-8_10

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