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Morpho-functional changes of fat body in bacteria fed Drosophila melanogaster strains

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Abstract

We have examined the addition of Escherichia coli to the diet at day 0 of adult life of females from two Oregon R Drosophila melanogaster strains, selected for different longevities: a short-life with an average adult life span of 10 days and a long-life standard R strain with an average adult life span of 50 days. The addition of bacteria to the diet significantly prolonged the fly longevity in both strains and affected the structure and histochemical reactivity of the fat body. The increased survival was characterized by great amount of glycogen accumulated in fat body cells from both strains. In aged control animals, fed with standard diet, lipid droplets were seen to be stored in fat body of short-lived, but not long-lived, flies. On the whole, our data indicate that exogenous bacteria are able to extend the survival of Drosophila females, and suggest that such a beneficial effect can be mediated, at least in part, by the fat body cells that likely play a role in modulating the accumulation and mobilization of reserve stores to ensure lifelong energy homeostasis.

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References

  • Arking R, Force AG, Dudas SP, Buck S, Baker GT 3rd (1996) Factors contributing to the plasticity of the extended longevity phenotypes of Drosophila. Exp Gerontol 31:623–643

    Article  PubMed  CAS  Google Scholar 

  • Arking R, Buck S, Novoseltev VN, Hwangbo DS, Lane M (2002) Genomic plasticity, energy allocations, and the extended longevity phenotypes of Drosophila. Ageing Res Rev 1:209–228

    Article  PubMed  CAS  Google Scholar 

  • Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225

    Article  PubMed  CAS  Google Scholar 

  • Bancroft JD, Gamble M (2002) Theory and practice of histological techniques, 5th edn. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Behar A, Yuval B, Jurkevitch E (2008) Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. J Insect Physiol 54:1377–1383

    Article  PubMed  CAS  Google Scholar 

  • Bignell DE (1984) The arthropod gut as an environment for microorganisms. In: Anderson JM, Raynon ADM, Walton DWA (eds) Invertebrate-microbial interactions. Cambridge University Press, Cambridge, pp 205–227

    Google Scholar 

  • Bland JM, Altman DG (2004) The logrank test. BMJ 328 doi:10.1136/bmj.328.7447.1073

  • Blüher M (2008) Fat tissue and long life. Obes Facts 1:176–182

    Article  PubMed  Google Scholar 

  • Bonafè M, Barbieri M, Marchegiani F, Olivieri F, Ragno E, Giampieri C, Mugianesi E, Centurelli M, Franceschi C, Paolisso G (2003) Polymorphic variants of insulin-like growth factor I (IGF-I) receptor and phosphoinositide 3-kinase genes affect IGF-I plasma levels and human longevity: cues for an evolutionarily conserved mechanism of life span control. J Clin Endocrinol Metab 88:3299–3304

    Article  PubMed  Google Scholar 

  • Brauman A, Doré J, Eggleton P, Bignell D, Breznak JA, Kane MD (2001) Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol Ecol 35:27–36

    Article  PubMed  CAS  Google Scholar 

  • Breznak JA, Panratz HS (1977) In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki]. Appl Environ Microbiol 33:406–426

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Campbell BC, Bernays EA (1990) On the role of microbial symbiotes in herbivorous insects. In: Insect-plant interactions. CRC press, Boca Raton; pp 1–45

  • Canavoso LE, Jouni ZE, Karnas KJ, Pennington JE, Wells MA (2001) Fat metabolism in insects. Annu Rev Nutr 21:23–46

    Article  PubMed  CAS  Google Scholar 

  • Charroux B, Royet J (2010) Drosophila immune response: from systemic antimicrobial peptide production in fat body cells to local defense in the intestinal tract. Fly (Austin) 4:40–47

    CAS  Google Scholar 

  • Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Léopold P (2003) A nutrient sensor mechanism controls Drosophila growth. Cell 114:739–749

    Article  PubMed  CAS  Google Scholar 

  • De Vries EJ, van der Wurff AW, Jacobs G, Breeuwer JA (2008) Onion thrips, Thrips tabaci, have gut bacteria that are closely related to the symbionts of the western flower thrips, Frankliniella occidentalis. J Insect Sci 8:1–11

    Article  PubMed  Google Scholar 

  • DeVeale B, Brummel T, Seroude L (2004) Immunity and aging: the enemy within? Aging Cell 3:195–208

    Article  PubMed  CAS  Google Scholar 

  • DiAngelo JR, Birnbaum MJ (2009) Regulation of fat cell mass by insulin in Drosophila melanogaster. Mol Cell Biol 29:6341–6352

    Article  PubMed  CAS  Google Scholar 

  • Dillon FJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92

    Article  PubMed  CAS  Google Scholar 

  • Dillon RJ, Webster G, Weightman AJ, Keith Charnley A (2010) Diversity of gut microbiota increases with aging and starvation in the desert locust. Antonie Van Leeuwenhoek 97:69–77

    Article  PubMed  CAS  Google Scholar 

  • Fontana L, Partridge L, Longo VD (2010) Extending healthy life span from yeast to humans. Science 328:321–326

    Article  PubMed  CAS  Google Scholar 

  • Franchini A, Peruzzi E, Ottaviani E (2003) Morphochemical age-related changes in the nematode Caenorhabditis elegans: immunoperoxidase localization of cytokine- and growth factor-like molecules. Eur J Histochem 47:75–80

    PubMed  CAS  Google Scholar 

  • Fry AJ, Rand DM (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56:1976–1981

    PubMed  Google Scholar 

  • Géminard C, Rulifson EJ, Léopold P (2009) Remote control of insulin secretion by fat cells in Drosophila. Cell Metab 10:199–207

    Article  PubMed  Google Scholar 

  • Giannakou ME, Partridge L (2007) Role of insulin-like signalling in Drosophila lifespan. Trends Biochem Sci 32:180–188

    Article  PubMed  CAS  Google Scholar 

  • Giannakou ME, Goss M, Jünger MA, Hafen E, Leevers SJ, Partridge L (2004) Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305:361

    Article  PubMed  CAS  Google Scholar 

  • Graves JL, Toolson EC, Jeong C, Vu LN, Rose MR (1992) Dessication, flight, glycogen, and postponed senescence in Drosophila melanogaster. Physiol Zool 65:268–286

    CAS  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  PubMed  CAS  Google Scholar 

  • Haselton A, Sharmin E, Schrader J, Sah M, Poon P, Fridell YW (2010) Partial ablation of adult Drosophila insulin-producing neurons modulates glucose homeostasis and extends life span without insulin resistance. Cell Cycle 9:3063–3071

    Article  PubMed  CAS  Google Scholar 

  • Huffman DM, Barzilai N (2010) Contribution of adipose tissue to health span and longevity. Interdiscip Top Gerontol 37:1–19

    Article  PubMed  Google Scholar 

  • Hwangbo DS, Gershman B, Tu MP, Palmer M, Tatar M (2004) Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429:562–566

    Article  PubMed  CAS  Google Scholar 

  • Katic M, Kahn CR (2005) The role of insulin and IGF-1 signaling in longevity. Cell Mol Life Sci 62:320–343

    Article  PubMed  CAS  Google Scholar 

  • Klöting N, Blüher M (2005) Extended longevity and insulin signaling in adipose tissue. Exp Gerontol 40:878–883

    Article  PubMed  Google Scholar 

  • Landis GN, Abdueva D, Skvortsov D, Yang J, Rabin BE, Carrick J, Tavaré S, Tower J (2004) Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci USA 101:7663–7668

    Article  PubMed  CAS  Google Scholar 

  • Lee A (1980) Normal flora of animal intestinal surface. In: Bitton G, Marshall KC (eds) Absorption of microorganisms to surface. John Wiley and Sons, New York, pp 145–173

    Google Scholar 

  • Lee A (1985) Neglected niches. The microbial ecology of the gastrointestinal tract. Adv Microb Ecol 8:115–162

    Article  Google Scholar 

  • Lee WJ (2008) How do flies tolerate microorganisms in the gut? Cell Host Microbe 4:91–93

    Article  PubMed  CAS  Google Scholar 

  • Lints FA, Lints CV, Bullens P, Bourgois M, Delincé J (1989) Unexplained variations in life span of the Oregon-R strain of Drosophila melanogaster over a four-year period. Exp Gerontol 24:265–271

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Liu H, Liu S, Wang S, Jiang RJ, Li S (2009) Hormonal and nutritional regulation of insect fat body development and function. Arch Insect Biochem Physiol 71:16–30

    Article  PubMed  CAS  Google Scholar 

  • Longo VD, Finch CE (2003) Evolutionary medicine: from dwarf model systems to healthy centenarians? Science 299:1342–1346

    Article  PubMed  Google Scholar 

  • Muzumdar R, Allison DB, Huffman DM, Ma X, Atzmon G, Einstein FH, Fishman S, Poduval AD, McVei T, Keith SW, Barzilai N (2008) Visceral adipose tissue modulates mammalian longevity. Aging Cell 7:438–440

    Article  PubMed  CAS  Google Scholar 

  • Ottaviani E, Ventura N, Mandrioli M, Candela M, Franchini A, Franceschi C (2011) Gut microbiota as a candidate for lifespan extension: an ecological/evolutionary perspective targeted on living organisms as metaorganisms. Biogerontology 12:599–609

    Article  PubMed  CAS  Google Scholar 

  • Paolisso G, Barbieri M, Rizzo MR, Carella C, Rotondi M, Bonafè M, Franceschi C, Rose G, De Benedictis G (2001) Low insulin resistance and preserved beta-cell function contribute to human longevity but are not associated with TH-INS genes. Exp Gerontol 37:149–156

    Article  PubMed  CAS  Google Scholar 

  • Partridge L, Alic N, Bjedov I, Piper MD (2010) Ageing in Drosophila: the role of the insulin/Igf and TOR signalling network. Exp Gerontol 46:376–381

    Article  PubMed  Google Scholar 

  • Pletcher SD, Macdonald SJ, Marguerie R, Certa U, Stearns SC, Goldstein DB, Partridge L (2002) Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Curr Biol 12:712–723

    Article  PubMed  CAS  Google Scholar 

  • Rajagopal R (2009) Beneficial interactions between insects and gut bacteria. Indian J Microbiol 49:114–119

    Article  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  PubMed  CAS  Google Scholar 

  • Roma GC, Bueno OC, Camargo-Mathias MI (2010) Morpho-physiological analysis of the insect fat body: a review. Micron 41:395–401

    Article  PubMed  CAS  Google Scholar 

  • Ryu JH, Ha EM, Lee WJ (2010) Innate immunity and gut-microbe mutualism in Drosophila. Dev Comp Immunol 34:369–376

    Article  PubMed  CAS  Google Scholar 

  • Seroude L, Brummel T, Kapahi P, Benzer S (2002) Spatio-temporal analysis of gene expression during aging in Drosophila melanogaster. Aging Cell 1:47–56

    Article  PubMed  CAS  Google Scholar 

  • Service PM (1987) Physiological mechanisms of increased stress resistance in Drosophila melanogaster selected for postponed senescence. Physiol Zool 60:321–326

    Google Scholar 

  • Service PM, Hutchinson HW, MacKinley MD, Rose MR (1985) Resistance to environmental stress in Drosophila melanogaster selected for postponed senescence. Physiol Zool 58:380–389

    Google Scholar 

  • Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107–110

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Gordon JI (2003) Honor thy symbionts. Proc Natl Acad Sci USA 100:10452–10459

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was partly supported by a MIUR (Italy) grant and by the EU projects “IDEAL” (FP7, contract 259679) and NU-AGE (FP7 contract n. 266486).

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Authors and Affiliations

  1. Department of Biology, University of Modena and Reggio Emilia, Via Campi 213/D, 41125, Modena, Italy

    Antonella Franchini, Mauro Mandrioli & Enzo Ottaviani

  2. Department of Experimental Pathology and CIG, Interdipartimental Center L. Galvani, University of Bologna, Bologna, Italy

    Claudio Franceschi

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  1. Antonella Franchini
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  2. Mauro Mandrioli
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  4. Enzo Ottaviani
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Correspondence to Enzo Ottaviani.

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Franchini, A., Mandrioli, M., Franceschi, C. et al. Morpho-functional changes of fat body in bacteria fed Drosophila melanogaster strains. J Mol Hist 43, 243–251 (2012). https://doi.org/10.1007/s10735-011-9382-y

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  • DOI: https://doi.org/10.1007/s10735-011-9382-y

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