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Microbes control Drosophila germline stem cell increase and egg maturation through hormonal pathways – Communications Biology

  • Yoshinari, Y., Kurogi, Y., Ameku, T. & Niwa, R. Endocrine regulation of female germline stem cells in the fruit fly Drosophila melanogaster. Curr. Opin. Insect Sci. 31, 14–19 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Armstrong, A. R. Ovarian function. Reproduction, 159, R69–R82 (2020).

  • Leitão-Gonçalves, R. et al. Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLoS Biol. 15, 1–29 (2017).

    Article 

    Google Scholar
     

  • Wong, A. C. N., Dobson, A. J. & Douglas, A. E. Gut microbiota dictates the metabolic response of Drosophila to diet. J. Exp. Biol. 217, 1894–1901 (2014).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gnainsky, Y. et al. Systemic regulation of host energy and oogenesis by microbiome-derived mitochondrial coenzymes. Cell Rep. 34, 108583 (2021).

  • Wong, A. C. N. et al. The host as the driver of the microbiota in the gut and external environment of Drosophila melanogaster. Appl. Environ. Microbiol. 81, 6232–6240 (2015).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Gould, A. L. et al. Microbiome interactions shape host fitness. Proc. Natl Acad. Sci. USA 115, E11951–E11960 (2018).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260–270 (2012).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Leulier, F. et al. Integrative physiology: at the crossroads of nutrition, microbiota, animal physiology, and human health. Cell Metab. 25, 522–534 (2017).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Gleason, R. J., Anand, A., Kai, T. & Chen, X. Protecting and diversifying the germline. Genetics 208, 435–471 (2018).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • He, L., Wang, X. & Montell, D. J. Shining light on Drosophila oogenesis: live imaging of egg development. Curr. Opin. Genet. Dev. 21, 612–619 (2011).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Lehmann, R. Germline stem cells: origin and destiny. Cell Stem Cell 10, 729–739 (2012).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Pritchett, T. L., Tanner, E. A. & McCall, K. Cracking open cell death in the Drosophila ovary. Apoptosis 14, 969–979 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Armstrong, A. R. & Drummond-Barbosa, D. Insulin signaling acts in adult adipocytes via GSK-3β and independently of FOXO to control Drosophila female germline stem cell numbers. Dev. Biol. 440, 31–39 (2018).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Carney, G. E. & Bender, M. The Drosophila ecdysone receptor (EcR) gene is required maternally for normal oogenesis. Genetics 154, 1203–1211 (2000).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Baumann, A. A. et al. Genetic tools to study juvenile hormone action in Drosophila. Sci. Rep. 7, 1–15 (2017).

    Article 

    Google Scholar
     

  • Andreenkova, O. V., Adonyeva, N. V., Eremina, M. A., Gruntenko, N. E. & Rauschenbach, I. Y. The insulin-like receptor gene expression in the tissues synthesizing gonadotropic hormones at sexual maturation of Drosophila melanogaster females. Russ. J. Genet. 52, 1214–1217 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Garofalo, R. S. & Rosen, O. M. Tissue localization of Drosophila melanogaster insulin receptor transcripts during development. Mol. Cell. Biol. 8, 1638–1647 (1988).

    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Hsu, H. J. & Drummond-Barbosa, D. Insulin levels control female germline stem cell maintenance via the niche in Drosophila. Proc. Natl Acad. Sci. USA 106, 1117–1121 (2009).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Drummond-Barbosa, D. & Spradling, A. C. Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev. Biol. 231, 265–278 (2001).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Mirth, C. K. et al. Juvenile hormone regulates body size and perturbs insulin signaling in Drosophila. Proc. Natl Acad. Sci. USA 111, 7018–7023 (2014).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Sieber, M. H. & Spradling, A. C. Steroid signaling establishes a female metabolic state and regulates SREBP to control oocyte lipid accumulation. Curr. Biol. 25, 993–1004 (2015).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • LaFever, L. & Drummond-Barbosa, D. Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309, 1071–1073 (2005).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Ameku, T. & Niwa, R. Mating-induced increase in germline stem cells via the neuroendocrine system in female Drosophila. PLoS Genet. 12, e1006123 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yoshinari, Y. et al. Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster. Elife 9, 1–35 (2020).

    Article 

    Google Scholar
     

  • Belles, X. & Piulachs, M. D. Ecdysone signalling and ovarian development in insects: from stem cells to ovarian follicle formation. Biochim. Biophys. Acta – Gene Regul. Mech. 1849, 181–186 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Terashima, J., Takaki, K., Sakurai, S. & Bownes, M. Nutritional status affects 20-hydroxyecdysone concentration and progression of oogenesis in Drosophila melanogaster. J. Endocrinol. 187, 69–79 (2005).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Schwedes, C. C. & Carney, G. E. Ecdysone signaling in adult Drosophila melanogaster. J. Insect Physiol. 58, 293–302 (2012).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Ables, E. T., Bois, K. E., Garcia, C. A. & Drummond-Barbosa, D. Ecdysone response gene E78 controls ovarian germline stem cell niche formation and follicle survival in Drosophila. Dev. Biol. 400, 33–42 (2015).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Ables, E. T. & Drummond-Barbosa, D. The steroid hormone ecdysone functions with intrinsic chromatin remodeling factors to control female germline stem cells in Drosophila. Cell Stem Cell 7, 581–592 (2010).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Buszczak, M. et al. Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development 126, 4581–4589 (1999).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Terashima, J. & Bownes, M. E75A and E75B have opposite effects on the apoptosis/development choice of the Drosophila egg chamber. Cell Death Differ. 13, 454–464 (2006).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Riddiford, L. M., Cherbas, P. & Truman, J. W. Ecdysone receptors and their biological actions. Vitam. Horm. 60, 1–73 (2000).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Soller, M., Bownes, M. & Kubli, E. Control of oocyte maturation in sexually mature Drosophila females. Dev. Biol. 208, 337–351 (1999).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Gruntenko, N. E. & Rauschenbach, I. Y. Interplay of JH, 20E and biogenic amines under normal and stress conditions and its effect on reproduction. J. Insect Physiol. 54, 902–908 (2008).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Shin, S. C. et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334, 670–674 (2011).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Lee, I. P. A., Eldakar, O. T., Gogarten, J. P. & Andam, C. P. Bacterial cooperation through horizontal gene transfer. Trends Ecol. Evol. 37, 223–232 (2022).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Craddock, E. M. & Boake, C. Onset of vitellogenesis in female Drosophila silvestrls is accelerated in the presence of sexually mature males. Endocrinology 38, 643–650 (1992).


    Google Scholar
     

  • Lieber, T., Kidd, S. & Struhl, G. DSL-notch signaling in the Drosophila brain in response to olfactory stimulation. Neuron 69, 468–481 (2011).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Balakireva, M., Stocker, R. F., Gendre, N. & Ferveur, J. F. Voila, a new Drosophila courtship variant that affects the nervous system: Behavioral, neural, and genetic characterization. J. Neurosci. 18, 4335–4343 (1998).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Koyle, M. L. et al. Rearing the fruit fly drosophila melanogaster under axenic and gnotobiotic conditions. J. Vis. Exp. 113, e54219 (2016).

  • Obata, F., Fons, C. O. & Gould, A. P. Early-life exposure to low-dose oxidants can increase longevity via microbiome remodelling in Drosophila. Nat. Commun. 9, 975 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jenkins, V. K., Timmons, A. K. & McCall, K. Diversity of cell death pathways: Insight from the fly ovary. Trends Cell Biol. 23, 567–574 (2013).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Steller, H. Regulation of apoptosis in Drosophila. Cell Death Differ. 15, 1132–1138 (2008).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Ryoo, H. D. & Baehrecke, E. H. Distinct death mechanisms in Drosophila development. Curr. Opin. Cell Biol. 22, 889–895 (2010).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Margolis, J. & Spradling, A. Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121, 3797–3807 (1995).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Dubrovsky, E. B. Hormonal cross talk in insect development. Trends Endocrinol. Metab. 16, 6–11 (2005).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Niwa, Y. S. & Niwa, R. Transcriptional regulation of insect steroid hormone biosynthesis and its role in controlling timing of molting and metamorphosis. Dev. Growth Differ. 58, 94–105 (2016).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Santos, C. G., Humann, F. C. & Hartfelder, K. Juvenile hormone signaling in insect oogenesis. Curr. Opin. Insect Sci. 31, 43–48 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Das, D. & Arur, S. Conserved insulin signaling in the regulation of oocyte growth, development, and maturation. Mol. Reprod. Dev. 84, 444–459 (2017).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Weaver, L. N., Ma, T. & Drummond-Barbosa, D. Analysis of Gal4 expression patterns in adult Drosophila females. G3 Genes Genomes Genet. 10, 4147–4158 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Luo, W. et al. Dual roles of juvenile hormone signaling during early oogenesis in Drosophila. Insect Sci. 27, 665–674 (2020).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Ramos, F. O. et al. Juvenile hormone mediates lipid storage in the oocytes of Dipetalogaster maxima. Insect Biochem. Mol. Biol. 133, 103499 (2021).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Abdou, M. A. et al. Drosophila Met and Gce are partially redundant in transducing juvenile hormone action. Insect Biochem. Mol. Biol. 41, 938–945 (2011).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Niwa, R. & Niwa, Y. S. Enzymes for ecdysteroid biosynthesis: Their biological functions in insects and beyond. Biosci. Biotechnol. Biochem. 78, 1283–1292 (2014).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Wen, D. et al. Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis. PLoS Genet. 11, 1–19 (2015).

    Article 

    Google Scholar
     

  • de A Camargo, R. et al. De novo transcriptome assembly and analysis to identify potential gene targets for RNAi-mediated control of the tomato leafminer (Tuta absoluta). BMC Genom. 16, 635 (2015).

    Article 

    Google Scholar
     

  • Niwa, Y. S. & Niwa, R. Neural control of steroid hormone biosynthesis during development in the fruit fly Drosophila melanogaster. Genes Genet. Syst. 89, 27–34 (2014).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Rewitz, K. F., Yamanaka, N. & O’Connor, M. B. Steroid hormone inactivation is required during the juvenile-adult transition in Drosophila. Dev. Cell 19, 895–902 (2010).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Guittard, E. et al. CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Dev. Biol. 349, 35–45 (2011).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Petryk, A. et al. Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proc. Natl Acad. Sci. USA 100, 13773–13778 (2003).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Niwa, R. et al. Juvenile hormone acid O-methyltransferase in Drosophila melanogaster. Insect Biochem. Mol. Biol. 38, 714–720 (2008).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Bendena, W. G., Zhang, J., Burtenshaw, S. M. & Tobe, S. S. Evidence for differential biosynthesis of juvenile hormone (and related) sesquiterpenoids in Drosophila melanogaster. Gen. Comp. Endocrinol. 172, 56–61 (2011).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Hackney, J. F., Pucci, C., Naes, E. & Dobens, L. L. Ras signaling modulates activity of the Ecdysone Receptor EcR during cell migration in the Drosophila ovary. Dev. Dyn. 236, 1213–1226 (2007).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Kozlova, T. & Thummel, C. S. Spatial patterns of ecdysteroid receptor activation during the onset of Drosophila metamorphosis. Development 129, 1739–1750 (2002).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Grandison, R. C., Piper, M. D. W. & Partridge, L. Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462, 1061–1064 (2009).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Weiss, I. M., Muth, C., Drumm, R. & Kirchner, H. O. K. Thermal decomposition of the amino acids glycine, cysteine, aspartic acid, asparagine, glutamic acid, glutamine, arginine and histidine. BMC Biophys. 11, 1–15 (2018).

    Article 

    Google Scholar
     

  • 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).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Broderick, N. A. & Lemaitre, B. Gut-associated microbes of Drosophila melanogaster. Landes Biosci. 3, 307–321 (2012).


    Google Scholar
     

  • Wong, A. C. N., Chaston, J. M. & Douglas, A. E. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 7, 1922–1932 (2013).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Martino, M. E. et al. Bacterial adaptation to the host’s diet is a key evolutionary force shaping Drosophila-Lactobacillus symbiosis. Cell Host Microbe 24, 109–119.e6 (2018).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Henry, L. P., Bruijning, M., Forsberg, S. K. G. & Ayroles, J. F. The microbiome extends host evolutionary potential. Nat. Commun. 12, 1–13 (2021).

    Article 

    Google Scholar
     

  • Ameku, T. et al. Midgut-derived neuropeptide F controls germline stem cell proliferation in a mating-dependent manner. PLoS Biol. 16, 1–27 (2018).

    Article 

    Google Scholar
     

  • Hou, Y. C. C., Chittaranjan, S., Barbosa, S. G., McCall, K. & Gorski, S. M. Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J. Cell Biol. 182, 1127–1139 (2008).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Nezis, L. P. et al. Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy. Autophagy 5, 298–302 (2009).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Armstrong, A. R., Laws, K. M. & Drummond-Barbosa, D. Adipocyte amino acid sensing controls adult germline stem cell number via the amino acid response pathway and independently of Target of Rapamycin signaling in Drosophila. Development 141, 4479–4488 (2014).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Mattila, J. & Hietakangas, V. Regulation of carbohydrate energy metabolism in Drosophila melanogaster. Genetics 207, 1231–1253 (2017).

    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Cakouros, D., Daish, T. J. & Kumar, S. Ecdysone receptor directly binds the promoter of the Drosophila caspase dronc, regulating its expression in specific tissues. J. Cell Biol. 165, 631–640 (2004).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Jiang, C., Lamblin, J., Steller, H., Thummel, C. S. & Hughes, H. A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol. Cell 5, 445–455 (2000).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Morris, L. X. & Spradling, A. C. Steroid signaling within Drosophila ovarian epithelial cells sex-specifically modulates early germ cell development and meiotic entry. PLoS One 7, 1–11 (2012).

    Article 

    Google Scholar
     

  • König, A., Yatsenko, A. S., Weiss, M. & Shcherbata, H. R. Ecdysteroids affect Drosophila ovarian stem cell niche formation and early germline differentiation. EMBO J. 30, 1549–1562 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reiff, T. et al. Endocrine remodelling of the adult intestine sustains reproduction in Drosophila. Elife 4, 1–19 (2015).

    Article 

    Google Scholar
     

  • Henriques, S. F. et al. Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour. Nat. Commun. 11, 1–15 (2020).

    Article 

    Google Scholar
     

  • Lebo, D. P. V. & McCall, K. Murder on the ovarian express: a tale of non-autonomous cell death in the Drosophila ovary. Cells 10, 1454 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hudry, B. et al. Sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation. Cell 178, 901–918.e16 (2019).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Ahmed, S. M. H. et al. Fitness trade-offs incurred by ovary-to-gut steroid signalling in Drosophila. Nature 584, 415–419 (2020).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Arisdakessian, C., Cleveland, S. B. & Belcaid, M. MetaFlow|mics: scalable and reproducible nextflow pipelines for the analysis of microbiome marker data. ACM Int. Conf. Proc. Ser. 120–124 (2020).

  • Frøslev, T. G. et al. Algorithm for post-clustering curation of DNA amplicon data yields reliable biodiversity estimates. Nat. Commun. 8, 1188 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schloss, P. D. et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Sabat, D. & Johnson, E. M. A protocol to generate germ free drosophila for microbial interaction studies. Adv. Tech. Biol. Med. s1, 001 (2015).

    Article 

    Google Scholar
     

  • Kai, T. & Spradling, A. An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proc. Natl Acad. Sci. USA 100, 4633–4638 (2003).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Harrison, D. A. & Perrimon, N. Simple and efficient generation of marked clones in Drosophila. Curr. Biol. 3, 424–433 (1993).

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Cetraro, N. & Yew, J. Y. In situ lipid profiling of insect pheromone glands by direct analysis in real time mass spectrometry. Analyst 147, 3276–3284 (2022).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Navare, A. T., Mayoral, J. G., Nouzova, M., Noriega, F. G. & Fernández, F. M. Rapid direct analysis in real time (DART) mass spectrometric detection of juvenile hormone III and its terpene precursors. Anal. Bioanal. Chem. 398, 3005–3013 (2010).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar