Olfaction regulates organismal proteostasis and longevity via microRNA-dependent signaling.


Journal

Nature metabolism
ISSN: 2522-5812
Titre abrégé: Nat Metab
Pays: Germany
ID NLM: 101736592

Informations de publication

Date de publication:
03 2019
Historique:
entrez: 20 9 2019
pubmed: 20 9 2019
medline: 20 9 2019
Statut: ppublish

Résumé

The maintenance of proteostasis is crucial for any organism to survive and reproduce in an ever-changing environment, but its efficiency declines with age

Identifiants

pubmed: 31535080
doi: 10.1038/s42255-019-0033-z
pmc: PMC6751085
mid: EMS84347
pii: 10.1038/s42255-019-0033-z
doi:

Substances chimiques

MicroRNAs 0

Types de publication

Letter Research Support, Non-U.S. Gov't

Langues

eng

Pagination

350-359

Subventions

Organisme : European Research Council
ID : 337161
Pays : International
Organisme : European Research Council
ID : 616499
Pays : International
Organisme : Austrian Science Fund FWF
ID : W 1207
Pays : Austria

Commentaires et corrections

Type : ErratumIn

Déclaration de conflit d'intérêts

Competing interests: The authors declare no competing interests.

Références

Taylor, R. C. & Dillin, A. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Biol. 3, a004440 (2011).
Krol, J., Loedige, I. & Filipowicz, W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597–610 (2010).
pubmed: 20661255 doi: 10.1038/nrg2843
de Lencastre, A. et al. MicroRNAs both promote and antagonize longevity in C. elegans. Curr. Biol. 20, 2159–2168 (2010).
pubmed: 21129974 pmcid: 3023310 doi: 10.1016/j.cub.2010.11.015
Mori, M. A. et al. Role of microRNA processing in adipose tissue in stress defense and longevity. Cell Metab. 16, 336–347 (2012).
pubmed: 22958919 pmcid: 3461823 doi: 10.1016/j.cmet.2012.07.017
Segref, A., Torres, S. & Hoppe, T. A screenable in vivo assay to study proteostasis networks in Caenorhabditis elegans. Genetics 187, 1235–1240 (2011).
pubmed: 21288877 pmcid: 3070531 doi: 10.1534/genetics.111.126797
Denzel, M. S. et al. Hexosamine pathway metabolites enhance protein quality control and prolong life. Cell 156, 1167–1178 (2014).
pubmed: 24630720 doi: 10.1016/j.cell.2014.01.061
Ruggiano, A., Foresti, O. & Carvalho, P. Quality control: ER-associated degradation: protein quality control and beyond. J. Cell Biol. 204, 869–879 (2014).
pubmed: 24637321 pmcid: 3998802 doi: 10.1083/jcb.201312042
Vilchez, D. et al. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 489, 263–268 (2012).
pubmed: 22922647 doi: 10.1038/nature11315
Calfon, M. et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92–96 (2002).
pubmed: 11780124 doi: 10.1038/415092a
Boulias, K. & Horvitz, H. R. The C. elegans microRNA mir-71 acts in neurons to promote germline-mediated longevity through regulation of DAF-16/FOXO. Cell Metab. 15, 439–450 (2012).
pubmed: 22482727 pmcid: 3344382 doi: 10.1016/j.cmet.2012.02.014
Hsieh, Y.-W., Chang, C. & Chuang, C.-F. The microRNA mir-71 inhibits calcium signaling by targeting the TIR-1/Sarm1 adaptor protein to control stochastic L/R neuronal asymmetry in C. elegans. PLoS Genet. 8, e1002864 (2012).
pubmed: 22876200 pmcid: 3410857 doi: 10.1371/journal.pgen.1002864
Hobert, O. Terminal selectors of neuronal identity. Curr. Top. Dev. Biol. 116, 455–475 (2016).
pubmed: 26970634 doi: 10.1016/bs.ctdb.2015.12.007
Alcedo, J. & Kenyon, C. Regulation of C. elegans longevity by specific gustatory and olfactory neurons. Neuron 41, 45–55 (2004).
pubmed: 14715134 doi: 10.1016/S0896-6273(03)00816-X
Troemel, E. R., Kimmel, B. E. & Bargmann, C. I. Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell 91, 161–169 (1997).
pubmed: 9346234 doi: 10.1016/S0092-8674(00)80399-2
Jan, C. H., Friedman, R. C., Ruby, J. G. & Bartel, D. P. Formation, regulation and evolution of Caenorhabditis elegans 3′ UTRs. Nature 469, 97–101 (2011).
pubmed: 21085120 doi: 10.1038/nature09616
Chuang, C.-F. & Bargmann, C. I. A Toll–interleukin 1 repeat protein at the synapse specifies asymmetric odorant receptor expression via ASK1 MAPKKK signaling. Genes Dev. 19, 270–281 (2005).
pubmed: 15625192 pmcid: 545892 doi: 10.1101/gad.1276505
Liberati, N. T. et al. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc. Natl Acad. Sci. USA 101, 6593–6598 (2004).
pubmed: 15123841 doi: 10.1073/pnas.0308625101 pmcid: 404090
Xie, Y., Moussaif, M., Choi, S., Xu, L. & Sze, J. Y. RFX transcription factor DAF-19 regulates 5-HT and innate immune responses to pathogenic bacteria in Caenorhabditis elegans. PLoS Genet. 9, e1003324 (2013).
pubmed: 23505381 pmcid: 3591283 doi: 10.1371/journal.pgen.1003324
Taylor, R. C. & Dillin, A. XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153, 1435–1447 (2013).
pubmed: 23791175 pmcid: 4771415 doi: 10.1016/j.cell.2013.05.042
Prahlad, V., Cornelius, T. & Morimoto, R. I. Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320, 811–814 (2008).
pubmed: 18467592 pmcid: 3429343 doi: 10.1126/science.1156093
Madison, J. M., Nurrish, S. & Kaplan, J. M. UNC-13 interaction with syntaxin is required for synaptic transmission. Curr. Biol. 15, 2236–2242 (2005).
pubmed: 16271476 doi: 10.1016/j.cub.2005.10.049
Speese, S. et al. UNC-31 (CAPS) Is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J. Neurosci. 27, 6150–6162 (2007).
pubmed: 17553987 pmcid: 6672138 doi: 10.1523/JNEUROSCI.1466-07.2007
Li, C. The ever-expanding neuropeptide gene families in the nematode Caenorhabditis elegans. Parasitology 131(Suppl.), S109–S127 (2005).
pubmed: 16569285
Chalasani, S. H. et al. Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450, 63–70 (2007).
pubmed: 17972877 doi: 10.1038/nature06292
Hobert, O. et al. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19, 345–357 (1997).
pubmed: 9292724 doi: 10.1016/S0896-6273(00)80944-7
Bargmann, C. I. Chemosensation in C. elegans. in WormBook (ed. The C. elegans Research Community) https://doi.org/10.1895/wormbook.1.123.1 (2006).
Pokala, N., Liu, Q., Gordus, A. & Bargmann, C. I. Inducible and titratable silencing of Caenorhabditis elegans neurons in vivo with histamine-gated chloride channels. Proc. Natl Acad. Sci. USA 111, 2770–2775 (2014).
pubmed: 24550306 doi: 10.1073/pnas.1400615111 pmcid: 3932931
Ward, S. Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants. Proc. Natl Acad. Sci. USA 70, 817–821 (1973).
pubmed: 4351805 doi: 10.1073/pnas.70.3.817 pmcid: 433366
Ben Arous, J., Laffont, S. & Chatenay, D. Molecular and sensory basis of a food related two-state behavior in C. elegans. PLoS One 4, e7584 (2009).
pubmed: 19851507 pmcid: 2762077 doi: 10.1371/journal.pone.0007584
Libert, S. et al. Regulation of Drosophila life span by olfaction and food-derived odors. Science 315, 1133–1137 (2007).
pubmed: 17272684 doi: 10.1126/science.1136610
Maier, W., Adilov, B., Regenass, M. & Alcedo, J. A neuromedin U receptor acts with the sensory system to modulate food type-dependent effects on C. elegans lifespan. PLoS Biol. 8, e1000376 (2010).
Inoue, A. et al. Forgetting in C. elegans is accelerated by neuronal communication via the TIR-1/JNK-1 pathway. Cell Rep. 3, 808–819 (2013).
pubmed: 23523351 doi: 10.1016/j.celrep.2013.02.019
Essuman, K. et al. The SARM1 Toll/interleukin-1 receptor domain possesses intrinsic NAD
pubmed: 28334607 pmcid: 6284238 doi: 10.1016/j.neuron.2017.02.022
Tsvetkov, P. et al. NADH binds and stabilizes the 26S proteasomes independent of ATP. J. Biol. Chem. 289, 11272–11281 (2014).
pubmed: 24596095 pmcid: 4036265 doi: 10.1074/jbc.M113.537175
Summers, D. W., Gibson, D. A., DiAntonio, A. & Milbrandt, J. SARM1-specific motifs in the TIR domain enable NAD
pubmed: 27671644 doi: 10.1073/pnas.1601506113 pmcid: 5068253
Pan, Z.-G. & An, X.-S. SARM1 deletion restrains NAFLD induced by high fat diet (HFD) through reducing inflammation, oxidative stress and lipid accumulation. Biochem. Biophys. Res. Commun. 498, 416–423 (2018).
pubmed: 29454967 doi: 10.1016/j.bbrc.2018.02.115
Lin, C.-W. & Hsueh, Y.-P. Sarm1, a neuronal inflammatory regulator, controls social interaction, associative memory and cognitive flexibility in mice. Brain Behav. Immun. 37, 142–151 (2014).
pubmed: 24321214 doi: 10.1016/j.bbi.2013.12.002
Brooks, K. K., Liang, B. & Watts, J. L. The influence of bacterial diet on fat storage in C. elegans. PLoS One 4, e7545 (2009).
pubmed: 19844570 pmcid: 2760100 doi: 10.1371/journal.pone.0007545
Riera, C. E. et al. The sense of smell impacts metabolic health and obesity. Cell Metab. 26, 198–211 (2017).
pubmed: 28683287 doi: 10.1016/j.cmet.2017.06.015
Teff, K. Nutritional implications of the cephalic-phase reflexes: endocrine responses. Appetite 34, 206–213 (2000).
pubmed: 10744911 doi: 10.1006/appe.1999.0282
Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).
pubmed: 4366476 pmcid: 1213120 doi: 10.1093/genetics/77.1.71
Stiernagle, T. Maintenance of C. elegans.in WormBook (ed. The C. elegans Research Community) https://doi.org/10.1895/wormbook.1.101.1 (2006).
Miedel, M. T. et al. A pro-cathepsin L mutant is a luminal substrate for endoplasmic-reticulum-associated degradation in C. elegans. PLoS One 7, e40145 (2012).
pubmed: 22768338 pmcid: 3388072 doi: 10.1371/journal.pone.0040145
Roayaie, K., Crump, J. G., Sagasti, A. & Bargmann, C. I. The G
pubmed: 9459442 doi: 10.1016/S0896-6273(00)80434-1
Radman, I., Greiss, S. & Chin, J. W. Efficient and rapid C. elegans transgenesis by bombardment and hygromycin B selection. PLoS One 8, e76019 (2013).
Drexel, T., Mahofsky, K., Latham, R., Zimmer, M. & Cochella, L. Neuron type-specific miRNA represses two broadly expressed genes to modulate an avoidance behavior in C. elegans. Genes Dev. 30, 2042–2047 (2016).
pubmed: 27688400 pmcid: 5066611 doi: 10.1101/gad.287904.116
Friedland, A. E. et al. Heritable genome editing in C. elegans via a CRISPR–Cas9 system. Nat. Methods 10, 741–743 (2013).
pubmed: 23817069 pmcid: 3822328 doi: 10.1038/nmeth.2532
Katic, I. & Großhans, H. Targeted heritable mutation and gene conversion by Cas9–CRISPR in Caenorhabditis elegans. Genetics 113, 155754 (2013).
Semple, J. I., Biondini, L. & Lehner, B. Generating transgenic nematodes by bombardment and antibiotic selection. Nat. Methods 9, 118–119 (2012).
pubmed: 22290182 doi: 10.1038/nmeth.1864
Mitchell, D. H., Stiles, J. W., Santelli, J. & Sanadi, D. R. Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine 1. J. Gerontol. 34, 28–36 (1979).
Timmons, L. & Fire, A. Specific interference by ingested dsRNA. Nature 395, 854 (1998).
pubmed: 9804418 doi: 10.1038/27579
Kamath, R. S., Martinez-Campos, M., Zipperlen, P., Fraser, A. G. & Ahringer, J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, RESEARCH0002 (2001).
pubmed: 11178279 doi: 10.1186/gb-2001-2-2-reports0002
Rual, J. F. et al. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 14, 2162–2168 (2004).
pubmed: 15489339 pmcid: 528933 doi: 10.1101/gr.2505604
Jadiya, P. & Nazir, A. A pre- and co-knockdown of RNAseT enzyme, Eri-1, enhances the efficiency of RNAi induced gene silencing in Caenorhabditis elegans. PLoS One 9, e87635 (2014).
pubmed: 24475317 pmcid: 3901743 doi: 10.1371/journal.pone.0087635
Hoogewijs, D., Houthoofd, K., Matthijssens, F., Vandesompele, J. & Vanfleteren, J. R. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol. Biol. 9, 9 (2008).
pubmed: 18211699 pmcid: 2254638 doi: 10.1186/1471-2199-9-9
Potluri, L. et al. Septal and lateral wall localization of PBP5, the major D,D-carboxypeptidase of Escherichia coli, requires substrate recognition and membrane attachment. Mol. Microbiol. 77, 300–323 (2010).
pubmed: 20545860 pmcid: 2909392 doi: 10.1111/j.1365-2958.2010.07205.x
Kitazono, T. et al. Multiple signaling pathways coordinately regulate forgetting of olfactory adaptation through control of sensory responses in Caenorhabditis elegans. J. Neurosci. 37, 10240–10251 (2017).
pubmed: 28924007 pmcid: 6596540 doi: 10.1523/JNEUROSCI.0031-17.2017

Auteurs

Fabian Finger (F)

Institute for Genetics and CECAD Research Center, University of Cologne, Cologne, Germany.

Franziska Ottens (F)

Institute for Genetics and CECAD Research Center, University of Cologne, Cologne, Germany.

Alexander Springhorn (A)

Institute for Genetics and CECAD Research Center, University of Cologne, Cologne, Germany.

Tanja Drexel (T)

Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Vienna, Austria.

Lucie Proksch (L)

Institute for Genetics and CECAD Research Center, University of Cologne, Cologne, Germany.

Sophia Metz (S)

Institute for Genetics and CECAD Research Center, University of Cologne, Cologne, Germany.

Luisa Cochella (L)

Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Vienna, Austria.

Thorsten Hoppe (T)

Institute for Genetics and CECAD Research Center, University of Cologne, Cologne, Germany. thorsten.hoppe@uni-koeln.de.

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