in

Transcriptomic evidence that insulin signalling pathway regulates the ageing of subterranean termite castes

  • 1.

    Jones, O. R. et al. Diversity of ageing across the tree of life. Nature 505(7482), 169–173 (2014).

  • 2.

    Butler, P. G., Wanamaker, J. A. D., Scourse, J. D., Richardson, C. A. & Reynolds, D. J. Variability of marine climate on the North Icelandic Shelf in a 1357-year proxy archive based on growth increments in the bivalve Arctica islandica. Palaeogeo Palaeoclima Palaeoeco 373, 141–151 (2013).

  • 3.

    Tasaki, E., Sakurai, H., Nitao, M., Matsuura, K. & Iuchi, Y. Uric acid, an important antioxidant contributing to survival in termites. PloS One 12, e0179426 (2017).

  • 4.

    Keller, L. & Genoud, M. Extraordinary lifespans in ants: A test of evolutionary theories of ageing. Nature 389, 958 (1997).

  • 5.

    Keller, L. Queen lifespan and colony characteristics in ants and termites. Insec Soci 45, 235–246 (1998).

  • 6.

    Elsner, D., Meusemann, K. & Korb, J. Longevity and transposon defense, the case of termite reproductives. Proc Natl Acad Sci USA 115, 5504–5509 (2018).

  • 7.

    Keller, L. & Jemielity, S. Social insects as a model to study the molecular basis of ageing. Expe Geronto 41, 553–556 (2006).

  • 8.

    Lucanic, M., Lithgow, G. J. & Alavez, S. Pharmacological lifespan extension of invertebrates. Age Res Rev 12, 445–458 (2013).

  • 9.

    Bitto, A., Wang, A. M., Bennett, C. F. & Kaeberlein, M. Biochemical genetic pathways that modulate aging in multiple species. CSH Perspect Med 5, a025114 (2015).

    • Google Scholar
  • 10.

    Kolovou, G. D., Kolovou, V. & Mavrogeni, S. We are ageing. BioMed Rese, Inter 2014, 808307 (2014).

    • Google Scholar
  • 11.

    Corona, M. et al. Vitellogenin, juvenile hormone, insulin signaling, and queen honeybee longevity. Proc Natl Acad Sci 104, 7128–33 (2007).

  • 12.

    Teleman, A. A., Hietakangas, V., Sayadian, A. C. & Cohen, S. M. Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab 7, 21–32 (2008).

  • 13.

    Luong, N. et al. Activated FOXO-mediated insulin resistance is blocked by reduction of TOR activity. Cell metab 4, 133–142 (2006).

  • 14.

    Bartke, A. Insulin and aging. Cell Cycle 7, 3338–3343 (2008).

  • 15.

    Zajitschek, F., Zajitschek, S. & Bonduriansky, R. Senescence in wild insects: Key questions and challenges. Funct Ecol 34, 26–37 (2020).

    • Article
    • Google Scholar
  • 16.

    Nussey, D. H., Coulson, T., Festa‐Bianchet, M. & Gaillard, J. M. Measuring senescence in wild animal populations: towards a longitudinal approach. Funct Ecol 22, 393–406 (2008).

    • Article
    • Google Scholar
  • 17.

    Tatar, M. et al. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107–110 (2001).

  • 18.

    Clancy, D. J. et al. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292, 104–106 (2001).

  • 19.

    Badisco, L., Van, W. P. & Vanden, B. J. Eat to reproduce: a key role for the insulin signaling pathway in adult insects. Front Physio 4, 202 (2013).

    • Article
    • Google Scholar
  • 20.

    Tasaki, E., Matsuura, K. & Iuchi, Y. Hypoxia adaptation in termites: hypoxic conditions enhance survival and reproductive activity in royals. Insect Mole Biol 27, 808–814 (2018).

  • 21.

    Lucas, E. R. & Keller, L. New explanation for the longevity of social insect reproductives: Transposable element activity. Proc Natl Acad Sci USA 115, 5317–5318 (2018).

  • 22.

    Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28, 27–30 (2000).

  • 23.

    Kanehisa, M., Sato, Y., Furumichi, M., Morishima, K. & Tanabe, M. New approach for understanding genome variations in KEGG. Nucleic Acids Res 47, D590–D595 (2018).

  • 24.

    Kanehisa, M. Toward understanding the origin and evolution of cellular organisms. Protein Sci 28, 1947–1951 (2019).

  • 25.

    Xu, C. et al. De novo and comparative transcriptome analysis of cultivated and wild spinach. Scie Rep 5, 17706 (2015).

  • 26.

    Mitaka, Y., Kobayashi, K. & Matsuura, K. Caste-, sex-, and age-dependent expression of immune-related genes in a Japanese subterranean termite, Reticulitermes speratus. PloS one 12, e0175417 (2017).

  • 27.

    Steijger, T. et al. Assessment of transcript reconstruction methods for RNA-seq. Nature Meth 10, 1177 (2013).

  • 28.

    Giannakou, M. E. & Partridge, L. Role of insulin-like signalling in Drosophila lifespan. Trends Bioche Scie 32, 180–188 (2007).

  • 29.

    Rintelen, F., Stocker, H., Thomas, G. & Hafen, E. PDK1 regulates growth through Akt and S6K in Drosophila. Proc Natl Acad Sci USA 98, 15020–15025 (2001).

  • 30.

    Gao, X., Fu, Y., Ajayi, O. E., Guo, D., Zhang, L. & Wu, Q. Identification of genes underlying phenotypic plasticity of wing size via insulin signaling pathway by network-based analysis in Sogatella furcifera. BMC Genomics 20, 01–21 (2019).

    • Article
    • Google Scholar
  • 31.

    Paradis, S., Ailion, M., Toker, A., Thomas, J. H. & Ruvkun, G. A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Devel 13, 1438–1452 (1999).

  • 32.

    Yuan, Q. Z. et al. “Frequent activation of AKT2 and induction of apoptosis by inhibition of phosphoinositide-3-OH kinase/Akt pathway in human ovarian cancer.“. Oncogene 19, 2324 (2000).

  • 33.

    Sun, M. et al. Phosphatidylinositol-3-OH kinase (PI3K)/AKT2, activated in breast cancer, regulates and is induced by estrogen receptor α (ERα) via interaction between ERα and PI3K. Cancer Res 61, 5985–5991 (2001).

  • 34.

    Yoeli-Lerner, M. & Toker, A. Akt/PKB signaling in cancer: a function in cell motility and invasion. Cell Cycle 5, 603–605 (2006).

  • 35.

    Arboleda, M. J. et al. Overexpression of AKT2/protein kinase Bβ leads to up-regulation of β1 integrins, increased invasion, and metastasis of human breast and ovarian cancer cells. Cancer Res 63, 196–206 (2003).

  • 36.

    Potter, C. J. et al. The tuberous sclerosis complex (TSC) pathway and mechanism of size control. Biochemical Society Transactions 31, 584–586 (2003).

  • 37.

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

  • 38.

    Napolioni, V. & Curatolo, P. Genetics and molecular biology of tuberous sclerosis complex. Curr Genomics 9, 475–487 (2008).

  • 39.

    Cornu, M., Albert, V. & Hall, M. N. mTOR in aging, metabolism, and cancer. Curr Opin Genet Dev 23, 53–62 (2013).

  • 40.

    Paul, C. & Robaire, B. Ageing of the male germ line. Nat Rev Urol 10, 227 (2013).

  • 41.

    Pan, J. et al. Insulin and 20-hydroxyecdysone oppose each other in the regulation of phosphoinositide-dependent kinase-1 expression during insect pupation. J Biol Chem 293, 18613–18623 (2018).

  • 42.

    Yoon, M. S. The role of mammalian target of rapamycin (mTOR) in insulin signaling. Nutrients 9, 1176 (2017).

  • 43.

    Zhai, Y. et al. Activation of the TOR signalling pathway by glutamine regulates insect fecundity. Sci Rep 5, 10694 (2015).

  • 44.

    Yecies, J. L. & Manning, B. D. mTOR links oncogenic signaling to tumor cell metabolism. J Mol Med (Berl) 89, 221–228 (2011).

  • 45.

    Simpson, L. & Parsons, R. PTEN: Life as a tumor suppressor. Exp Cell Res 264, 29–41 (2001).

  • 46.

    Graff, J. R. et al. Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J Clin Invest 117, 2638–2648 (2007).

  • 47.

    McDonald, J. M. et al. Elevated phospho-S6 expression is associated with metastasis in adenocarcinoma of the lung. Clin Cancer Res 14, 7832–7837 (2008).

  • 48.

    Mitaka, Y. et al. Caste-specific and sex-specific expression of chemoreceptor genes in a termite. PLoS One 11, e0146125 (2016).

  • 49.

    Tasaki, E. et al. High expression of the breast cancer susceptibility gene BRCA1 in long-lived termite kings. Aging (Albany NY) 10, 2668–2683 (2018).

  • 50.

    Tasaki, E., Kobayashi, K., Matsuura, K. & Iuchi, Y. An efficient antioxidant aystem in a long‐lived termite queen. PLoS One 12, e0167412 (2017).

  • 51.

    Elsnera, D., Meusemanna, K. & Korba, J. Longevity and transposon defense, the case of termite reproductives. Proc Natl Acad Sci USA 115, 5504–9 (2018).

  • 52.

    Tiebe, M. et al. REPTOR and REPTOR-BP regulate organismal metabolism and transcription downstream of TORC1. Dev Cell 4, 272–84 (2015).

  • 53.

    Takats, S., Varga, A., Pircs, K. & Juhasz, G. Loss of Drosophila Vps16A enhances autophagosome formation through reduced TOR activity. Autophagy 3, 1209–15 (2015).

  • 54.

    Yoon, W. H. et al. Loss of nardilysin, a mitochondrial co-chaperone for α-ketoglutarate dehydrogenase, promotes mTORC1 activation and neurodegeneration. Neuron 4, 115–31 (2017).

  • 55.

    Caraa, F. D., Bulowb, M. H., Simmondsa, A. J. & Rachubinskia, R. A. Dysfunctional peroxisomes compromise gut structure and host defense by increased cell death and Tor-dependent autophagy. Mol Biol Cell 1, 2766–83 (2018).

    • Article
    • Google Scholar
  • 56.

    Tang, H. W. et al. The TORC1-regulated CPA complex rewires an RNA processing network to drive autophagy and metabolic reprogramming. Cell Metab 1, 1040–54 (2018).

  • 57.

    Ramanathan, S. P., Krajnc, M. & Gibson, M. C. Cell-size pleomorphism drives aberrant clone dispersal in proliferating epithelia. Dev Cell 7, 49–61 (2019).

  • 58.

    Lee, B., Barretto, E. C. & Grewal, S. S. TORC1 modulation in adipose tissue is required for organismal adaptation to hypoxia in Drosophila. Nat Commu 23, 1878 (2019).

  • 59.

    Kim, A. R. & Choi, K. W. TRiC/CCT chaperonins are essential for organ growth by interacting with insulin/TOR signaling in Drosophila. Oncogene 38(24), 4739 (2019).

  • 60.

    Kimura, K. D., Tissenbaum, H. A., Liu, Y. & Ruvkun, G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 15, 942–6 (1997).

    • Article
    • Google Scholar
  • 61.

    Tatar, M. & Yin, C. M. Slow aging during insect reproductive diapause: why butterflies, grasshoppers and flies are like worms. Exp Geron 36, 723–738 (2001).

  • 62.

    Garofalo, R. S. Genetic analysis of insulin signaling in Drosophila. Trends Endocrinol Metab 13, 156–162 (2002).

  • 63.

    Brogiolo, W. et al. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11, 213–221 (2001).

  • 64.

    Baena-Lopez, L. A., Rodriguez, I. & Baonza, A. The tumor suppressor genes dachsous and fat modulate different signalling pathways by regulating dally and dally-like. Proc Natl Acad Sci USA 105, 9645–9650 (2008).

  • 65.

    Augustin, H. et al. Reduced insulin signaling maintains electrical transmission in a neural circuit in aging flies. PLoS Biol 15, 2001655 (2017).

  • 66.

    Su, X. et al. Characterization of the transcriptomes and cuticular protein gene expression of alate adult, brachypterous neotenic and adultoid reproductives of Reticulitermes labralis. Sci Rep 6, 1–9 (2016).

  • 67.

    Ye, C., Rasheed, H., Ran, Y., Yang, X., Xing, L. & Su, X. Transcriptome changes reveal the genetic mechanisms of the reproductive plasticity of workers in lower termites. BMC Geno 20, 1–13 (2019).

    • Google Scholar
  • 68.

    Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8, 1494 (2013).

  • 69.

    Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29, 644–652 (2011).

  • 70.

    Li, R. et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966–1967 (2009).

  • 71.

    Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).

  • 72.

    Zhang, J. et al. Transcriptome analysis of Cymbidium sinense and its application to the identification of genes associated with floral development. BMC Genomics 14, 1–17 (2013).

    • Article
    • Google Scholar
  • 73.

    Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676 (2005).

  • 74.

    Ye, J. et al. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34, W293–W297 (2006).

  • 75.

    Nicot, N., Hausman, J. F., Hoffmann, L. & Evers, D. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56, 2907–2914 (2005).

  • 76.

    Tong, Z., Gao, Z., Wang, F., Zhou, J. & Zhang, Z. Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Bio 10, 71 (2009).

    • Article
    • Google Scholar
  • 77.

    Ishitani, K. & Maekawa, K. Ovarian development of female-female pairs in the termite, Reticulitermes speratus. J Insect Sci 10, 1–12 (2010).

  • 78.

    Van Hiel, M. B. et al. Identification and validation of housekeeping genes in brains of the desert locust Schistocerca gregaria under different developmental conditions. BMC Mol Biol 10, 1–10 (2009).


  • Source: Ecology - nature.com

    Melting glaciers cool the Southern Ocean

    3 Questions: Energy studies at MIT and the next generation of energy leaders