Regulatory mechanism of cold-inducible diapause in Caenorhabditis elegans.

Animals Caenorhabditis elegans / genetics Caenorhabditis elegans Proteins / genetics Transcription Factors / metabolism Diapause / genetics Longevity / genetics Cold Temperature DNA-Binding Proteins / genetics Mutation Signal Transduction Forkhead Transcription Factors / metabolism Codon, Nonsense / genetics Neuropeptides / metabolism Carrier Proteins Basic Helix-Loop-Helix Transcription Factors

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
10 Jul 2024
Historique:
received: 07 02 2023
accepted: 28 06 2024
medline: 11 7 2024
pubmed: 11 7 2024
entrez: 10 7 2024
Statut: epublish

Résumé

Temperature is a critical environmental cue that controls the development and lifespan of many animal species; however, mechanisms underlying low-temperature adaptation are poorly understood. Here, we describe cold-inducible diapause (CID), another type of diapause induced by low temperatures in Caenorhabditis elegans. A premature stop codon in heat shock factor 1 (hsf-1) triggers entry into CID at 9 °C, whereas wild-type animals enter CID at 4 °C. Furthermore, both wild-type and hsf-1(sy441) mutant animals undergoing CID can survive for weeks, and resume growth at 20 °C. Using epistasis analysis, we demonstrate that neural signalling pathways, namely tyraminergic and neuromedin U signalling, regulate entry into CID of the hsf-1 mutant. Overexpression of anti-ageing genes, such as hsf-1, XBP1/xbp-1, FOXO/daf-16, Nrf2/skn-1, and TFEB/hlh-30, also inhibits CID entry of the hsf-1 mutant. Based on these findings, we hypothesise that regulators of the hsf-1 mutant CID may impact longevity, and successfully isolate 16 long-lived mutants among 49 non-CID mutants via genetic screening. Furthermore, we demonstrate that the nonsense mutation of MED23/sur-2 prevents CID entry of the hsf-1(sy441) mutant and extends lifespan. Thus, CID is a powerful model to investigate neural networks involving cold acclimation and to explore new ageing mechanisms.

Identifiants

DOI: 10.1038/s41467-024-50111-8 PMID: 38987256
pubmed: 38987256
doi: 10.1038/s41467-024-50111-8
pii: 10.1038/s41467-024-50111-8
doi:

Substances chimiques

Caenorhabditis elegans Proteins 0
heat shock factor-1, C elegans 0
Transcription Factors 0
DNA-Binding Proteins 0
daf-16 protein, C elegans 0
skn-1 protein, C elegans 148733-36-2
HLH-30 protein, C elegans 0
XBP-1 protein, C elegans 0
Forkhead Transcription Factors 0
Codon, Nonsense 0
Neuropeptides 0
Carrier Proteins 0
Basic Helix-Loop-Helix Transcription Factors 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5793

Subventions

Organisme : MEXT | Japan Society for the Promotion of Science (JSPS)
ID : JP22K06596
Organisme : MEXT | Japan Society for the Promotion of Science (JSPS)
ID : JP22H02260
Organisme : Japan Agency for Medical Research and Development (AMED)
ID : 21gm6110017h0004
Organisme : Japan Agency for Medical Research and Development (AMED)
ID : JP22gm6110029

Informations de copyright

© 2024. The Author(s).

Références

Klass, M. R. Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech. Ageing Dev. 6, 413–429 (1977).
pubmed: 926867 doi: 10.1016/0047-6374(77)90043-4
Lee, S.-J. & Kenyon, C. Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans. Curr. Biol. 19, 715–722 (2009).
pubmed: 19375320 pmcid: 2868911 doi: 10.1016/j.cub.2009.03.041
Miquel, J., Lundgren, P. R., Bensch, K. G. & Atlan, H. Effects of temperature on the life span, vitality and fine structure of Drosophila melanogaster. Mech. Ageing Dev. 5, 347–370 (1976).
pubmed: 823384 doi: 10.1016/0047-6374(76)90034-8
Xiao, R. et al. A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152, 806–817 (2013).
pubmed: 23415228 pmcid: 3594097 doi: 10.1016/j.cell.2013.01.020
Horikawa, M., Sural, S., Hsu, A.-L. & Antebi, A. Co-chaperone p23 regulates C. elegans lifespan in response to temperature. PLOS Genet 11, e1005023 (2015).
pubmed: 25830239 pmcid: 4382338 doi: 10.1371/journal.pgen.1005023
Svensk, E. et al. PAQR-2 regulates fatty acid desaturation during cold adaptation in C. elegans. PLoS Genet 9, e1003801 (2013).
pubmed: 24068966 pmcid: 3772066 doi: 10.1371/journal.pgen.1003801
Takagaki, N. et al. The mechanoreceptor DEG‐1 regulates cold tolerance in Caenorhabditis elegans. EMBO Rep. 21, e48671 (2020).
Zhang, B. et al. Environmental temperature differentially modulates C. elegans longevity through a thermosensitive TRP channel. Cell Rep 11, 1414–1424 (2015).
pubmed: 26027928 pmcid: 4758836 doi: 10.1016/j.celrep.2015.04.066
Kuhara, A. et al. Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science 320, 803–807 (2008).
pubmed: 18403676 doi: 10.1126/science.1148922
Mori, I. & Ohshima, Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376, 344–348 (1995).
pubmed: 7630402 doi: 10.1038/376344a0
Takeishi, A. Environmental-temperature and internal-state dependent thermotaxis plasticity of nematodes. Curr. Opin. Neurobiol. 74, 102541 (2022).
pubmed: 35447377 doi: 10.1016/j.conb.2022.102541
Glauser, D. A. Temperature sensing and context-dependent thermal behavior in nematodes. Curr. Opin. Neurobiol. 73, 102525 (2022).
pubmed: 35307612 doi: 10.1016/j.conb.2022.102525
Gong, J. et al. A cold-sensing receptor encoded by a glutamate receptor gene. Cell 178, 1375–1386.e11 (2019).
pubmed: 31474366 pmcid: 6743979 doi: 10.1016/j.cell.2019.07.034
Ohnishi, K. et al. OSM-9 and OCR-2 TRPV channels are accessorial warm receptors in Caenorhabditis elegans temperature acclimatisation. Sci. Rep. 10, 18566 (2020).
pubmed: 33122746 pmcid: 7596061 doi: 10.1038/s41598-020-75302-3
Ohta, A., Ujisawa, T., Sonoda, S. & Kuhara, A. Light and pheromone-sensing neurons regulates cold habituation through insulin signalling in Caenorhabditis elegans. Nat. Commun. 5, 4412 (2014).
pubmed: 25048458 doi: 10.1038/ncomms5412
Ujisawa, T. et al. Endoribonuclease ENDU-2 regulates multiple traits including cold tolerance via cell autonomous and nonautonomous controls in Caenorhabditis elegans. Proc. Natl. Acad. Sci. 115, 8823–8828 (2018).
pubmed: 30104389 pmcid: 6126727 doi: 10.1073/pnas.1808634115
Abdelnour, S. A. et al. Cellular and functional adaptation to thermal stress in ovarian granulosa cells in mammals. J. Therm. Biol. 92, 102688 (2020).
pubmed: 32888576 doi: 10.1016/j.jtherbio.2020.102688
Hazel, J. R. Thermal Adaptation in Biological Membranes: Is Homeoviscous Adaptation the Explanation? Annu. Rev. Physiol. 57, 19–42 (1995).
pubmed: 7778864 doi: 10.1146/annurev.ph.57.030195.000315
Chen, Y.-L. et al. Adiponectin receptor PAQR-2 signaling senses low temperature to promote C. elegans longevity by regulating autophagy. Nat. Commun. 10, 2602 (2019).
pubmed: 31197136 pmcid: 6565724 doi: 10.1038/s41467-019-10475-8
Lee, D. et al. MDT-15/MED15 permits longevity at low temperature via enhancing lipidostasis and proteostasis. PLOS Biol 17, e3000415 (2019).
pubmed: 31408455 pmcid: 6692015 doi: 10.1371/journal.pbio.3000415
Fujita, J. Cold shock response in mammalian cells. J. Mol. Microbiol. Biotechnol. 1, 243–255 (1999).
pubmed: 10943555
King, A. M. & MacRae, T. H. Insect heat shock proteins during stress and diapause. Annu. Rev. Entomol. 60, 59–75 (2015).
pubmed: 25341107 doi: 10.1146/annurev-ento-011613-162107
Lubawy, J., Chowański, S., Adamski, Z. & Słocińska, M. Mitochondria as a target and central hub of energy division during cold stress in insects. Front. Zool. 19, 1 (2022).
pubmed: 34991650 pmcid: 8740437 doi: 10.1186/s12983-021-00448-3
Fielenbach, N. & Antebi, A. C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 22, 2149–2165 (2008).
pubmed: 18708575 pmcid: 2735354 doi: 10.1101/gad.1701508
Geanacopoulos, M. The determinants of lifespan in the nematode Caenorhabditis elegans: a short primer. Sci. Prog. 87, 227–247 (2004).
pubmed: 16028834 pmcid: 10367488 doi: 10.3184/003685004783238472
Kenyon, C., Chang, J., Gensch, E., Rudner, A. & Tabtiang, R. A. C. elegans mutant that lives twice as long as wild type. Nature 366, 461–464 (1993).
pubmed: 8247153 doi: 10.1038/366461a0
Angelo, G. & Van Gilst, M. R. Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326, 954–958 (2009).
pubmed: 19713489 doi: 10.1126/science.1178343
Fukuyama, M., Rougvie, A. E. & Rothman, J. H. C. elegans DAF-18/PTEN Mediates Nutrient-Dependent Arrest of Cell Cycle and Growth in the Germline. Curr. Biol. 16, 773–779 (2006).
pubmed: 16631584 doi: 10.1016/j.cub.2006.02.073
Fukuyama, M. et al. C. elegans AMPKs promote survival and arrest germline development during nutrient stress. Biol. Open 1, 929–936 (2012).
pubmed: 23213370 pmcid: 3507181 doi: 10.1242/bio.2012836
Gerisch, B. et al. HLH-30/TFEB Is a master regulator of reproductive quiescence. Dev. Cell 53, 316–329.e5 (2020).
pubmed: 32302543 doi: 10.1016/j.devcel.2020.03.014
Baugh, L. R. To grow or not to grow: nutritional control of development during Caenorhabditis elegans L1 arrest. Genetics 194, 539–555 (2013).
pubmed: 23824969 pmcid: 3697962 doi: 10.1534/genetics.113.150847
Hu, P. J. Dauer. WormBook https://doi.org/10.1895/wormbook.1.144.1 (2007).
Adjirackor, N. A., Harvey, K. E. & Harvey, S. C. Eukaryotic response to hypothermia in relation to integrated stress responses. Cell Stress Chaperones 25, 833–846 (2020).
pubmed: 32676830 pmcid: 7591648 doi: 10.1007/s12192-020-01135-8
Henis-Korenblit, S. et al. Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proc. Natl. Acad. Sci. 107, 9730–9735 (2010).
pubmed: 20460307 pmcid: 2906894 doi: 10.1073/pnas.1002575107
Karp, X. Working with dauer larvae. WormBook 1–19 https://doi.org/10.1895/wormbook.1.180.1 .(2018).
Fukuyama, M., Kontani, K., Katada, T., Rougvie, A. E. & The, C. Elegans hypodermis couples progenitor cell quiescence to the dietary state. Curr. Biol. 25, 1241–1248 (2015).
pubmed: 25891400 doi: 10.1016/j.cub.2015.03.016
Barna, J. et al. Heat shock factor-1 intertwines insulin/IGF-1, TGF-β and cGMP signaling to control development and aging. BMC Dev. Biol. 12, 32 (2012).
pubmed: 23116063 pmcid: 3558376 doi: 10.1186/1471-213X-12-32
Kaplan, R. E. W. et al. dbl-1/TGF-β and daf-12/NHR Signaling mediate cell-nonautonomous effects of daf-16/FOXO on starvation-induced developmental arrest. PLOS Genet 11, e1005731 (2015).
pubmed: 26656736 pmcid: 4676721 doi: 10.1371/journal.pgen.1005731
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
Zheng, S. et al. A functional study of all 40 Caenorhabditis elegans insulin-like peptides. J. Biol. Chem. 293, 16912–16922 (2018).
pubmed: 30206121 pmcid: 6204898 doi: 10.1074/jbc.RA118.004542
Meiselman, M. R. et al. Recovery from cold-induced reproductive dormancy is regulated by temperature-dependent AstC signaling. Curr. Biol. 32, 1362–1375.e8 (2022).
pubmed: 35176227 pmcid: 8969192 doi: 10.1016/j.cub.2022.01.061
Mizuno, Y. et al. A population of neurons that produce hugin and express the diuretic hormone 44 receptor gene projects to the corpora allata in Drosophila melanogaster. Dev. Growth Differ. 63, 249–261 (2021).
pubmed: 34021588 doi: 10.1111/dgd.12733
Kurogi, Y., Mizuno, Y., Imura, E. & Niwa, R. Neuroendocrine regulation of reproductive dormancy in the fruit fly drosophila melanogaster: a review of juvenile hormone-dependent regulation. Front. Ecol. Evol. 9, 715029 (2021).
doi: 10.3389/fevo.2021.715029
Watteyne, J. et al. Neuromedin U signaling regulates retrieval of learned salt avoidance in a C. elegans gustatory circuit. Nat. Commun. 11, 2076 (2020).
pubmed: 32350283 pmcid: 7190830 doi: 10.1038/s41467-020-15964-9
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).
pubmed: 20520844 pmcid: 2876044 doi: 10.1371/journal.pbio.1000376
Chase, D. & Koelle, M. R. Biogenic amine neurotransmitters in C. elegans. WormBook https://doi.org/10.1895/wormbook.1.132.1 (2007).
Lazaro-Pena, M. I. et al. HSF-1: Guardian of the proteome through integration of longevity signals to the proteostatic network. Front. Aging 3, 861686 (2022).
pubmed: 35874276 pmcid: 9304931 doi: 10.3389/fragi.2022.861686
Morton, E. A. & Lamitina, T. Caenorhabditis elegans HSF-1 is an essential nuclear protein that forms stress granule-like structures following heat shock. Aging Cell 12, 112–120 (2013).
pubmed: 23107491 doi: 10.1111/acel.12024
Hajdu-Cronin, Y. M., Chen, W. J. & Sternberg, P. W. The L-type cyclin CYL-1 and the heat-shock-factor HSF-1 are required for heat-shock-induced protein expression in Caenorhabditis elegans. Genetics 168, 1937–1949 (2004).
pubmed: 15611166 pmcid: 1448743 doi: 10.1534/genetics.104.028423
Sugi, T., Nishida, Y. & Mori, I. Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat. Neurosci. 14, 984–992 (2011).
pubmed: 21706021 doi: 10.1038/nn.2854
Edwards, S. L. et al. Insulin/IGF-1 signaling and heat stress differentially regulate HSF1 activities in germline development. Cell Rep 36, 109623 (2021).
pubmed: 34469721 pmcid: 8442575 doi: 10.1016/j.celrep.2021.109623
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
Miller, H. et al. Genetic interaction with temperature is an important determinant of nematode longevity. Aging Cell 16, 1425–1429 (2017).
pubmed: 28940623 pmcid: 5676069 doi: 10.1111/acel.12658
Tataridas-Pallas, N. et al. Neuronal SKN-1B modulates nutritional signalling pathways and mitochondrial networks to control satiety. PLOS Genet 17, e1009358 (2021).
pubmed: 33661901 pmcid: 7932105 doi: 10.1371/journal.pgen.1009358
Tullet, J. M. A. et al. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132, 1025–1038 (2008).
pubmed: 18358814 pmcid: 2367249 doi: 10.1016/j.cell.2008.01.030
Lapierre, L. R. et al. The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans. Nat. Commun. 4, 2267 (2013).
pubmed: 23925298 doi: 10.1038/ncomms3267
Kutscher, L. M. Forward and reverse mutagenesis in C. elegans. WormBook 1–26 https://doi.org/10.1895/wormbook.1.167.1 (2014).
Abe, A. et al. Genome sequencing reveals agronomically important loci in rice using MutMap. Nat. Biotechnol. 30, 174–178 (2012).
pubmed: 22267009 doi: 10.1038/nbt.2095
Masse, I. et al. A novel role for the SMG-1 kinase in lifespan and oxidative stress resistance in Caenorhabditis elegans. PLoS ONE 3, e3354 (2008).
pubmed: 18836529 pmcid: 2556085 doi: 10.1371/journal.pone.0003354
Sakaki, K. et al. RNA surveillance is required for endoplasmic reticulum homeostasis. Proc. Natl. Acad. Sci. 109, 8079–8084 (2012).
pubmed: 22562797 pmcid: 3361423 doi: 10.1073/pnas.1110589109
Son, H. G. et al. RNA surveillance via nonsense-mediated mRNA decay is crucial for longevity in daf-2/insulin/IGF-1 mutant C. elegans. Nat. Commun. 8, 14749 (2017).
pubmed: 28276441 pmcid: 5347137 doi: 10.1038/ncomms14749
Campos, J. C. et al. Mild mitochondrial impairment enhances innate immunity and longevity through ATFS‐1 and p38 signaling. EMBO Rep. 22, (2021).
Uno, M. et al. A fasting-responsive signaling pathway that extends life span in C. elegans. Cell Rep 3, 79–91 (2013).
pubmed: 23352664 doi: 10.1016/j.celrep.2012.12.018
Kobayashi, K. et al. Single-cell memory regulates a neural circuit for sensory behavior. Cell Rep 14, 11–21 (2016).
pubmed: 26725111 doi: 10.1016/j.celrep.2015.11.064
Howard, R. M. & Sundaram, M. V. C. elegans EOR-1/PLZF and EOR-2 positively regulate Ras and Wnt signaling and function redundantly with LIN-25 and the SUR-2 Mediator component. Genes Dev 16, 1815–1827 (2002).
pubmed: 12130541 pmcid: 186391 doi: 10.1101/gad.998402
Bialas, N. J. et al. Functional interactions between the ciliopathy-associated Meckel syndrome 1 (MKS1) protein and two novel MKS1-related (MKSR) proteins. J. Cell Sci. 122, 611–624 (2009).
pubmed: 19208769 pmcid: 2720918 doi: 10.1242/jcs.028621
Dudkevich, R. et al. Neuronal IRE-1 coordinates an organism-wide cold stress response by regulating fat metabolism. Cell Rep 41, 111739 (2022).
pubmed: 36450261 doi: 10.1016/j.celrep.2022.111739
Zou, J., Guo, Y., Guettouche, T., Smith, D. F. & Voellmy, R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 Complex) that forms a stress-sensitive complex with HSF1. Cell 94, 471–480 (1998).
pubmed: 9727490 doi: 10.1016/S0092-8674(00)81588-3
Karagöz, G. E. & Rüdiger, S. G. D. Hsp90 interaction with clients. Trends Biochem. Sci. 40, 117–125 (2015).
pubmed: 25579468 doi: 10.1016/j.tibs.2014.12.002
Alkema, M. J., Hunter-Ensor, M., Ringstad, N. & Horvitz, H. R. Tyramine functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46, 247–260 (2005).
pubmed: 15848803 doi: 10.1016/j.neuron.2005.02.024
Glover-Cutter, K. M., Lin, S. & Blackwell, T. K. Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet 9, e1003701 (2013).
pubmed: 24068940 pmcid: 3772064 doi: 10.1371/journal.pgen.1003701
Lin, K., Hsin, H., Libina, N. & Kenyon, C. Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat. Genet. 28, 139–145 (2001).
pubmed: 11381260 doi: 10.1038/88850
Mahalak, K. K., Jama, A. M., Billups, S. J., Dawes, A. T. & Chamberlin, H. M. Differing roles for sur-2/MED23 in C. elegans and C. briggsae vulval development. Dev. Genes Evol. 227, 213–218 (2017).
pubmed: 28220250 doi: 10.1007/s00427-017-0577-4
Dias, I. B., Bouma, H. R. & Henning, R. H. Unraveling the big sleep: molecular aspects of stem cell dormancy and hibernation. Front. Physiol. 12, 624950 (2021).
pubmed: 33867999 pmcid: 8047423 doi: 10.3389/fphys.2021.624950
Chiu, C. N. et al. A zebrafish genetic screen identifies neuromedin u as a regulator of sleep/wake states. Neuron 89, 842–856 (2016).
pubmed: 26889812 doi: 10.1016/j.neuron.2016.01.007
Schwarz, J. E., King, A. N., Hsu, C. T., Barber, A. F. & Sehgal, A. Hugin
pubmed: 34782479 pmcid: 8617458 doi: 10.1073/pnas.2111183118
Stiernagle, T. Maintenance of C. elegans. WormBook https://doi.org/10.1895/wormbook.1.101.1 (2006).
Chiyoda, H. et al. Caenorhabditis elegans PTR/PTCHD PTR-18 promotes the clearance of extracellular hedgehog-related protein via endocytosis. PLOS Genet 17, e1009457 (2021).
pubmed: 33872306 pmcid: 8104386 doi: 10.1371/journal.pgen.1009457

Auteurs

Makoto Horikawa (M)

Unit of Biotechnology, Graduate School of Integrated Sciences for Life, Hiroshima University, Higashi-Hiroshima, Japan. mhorikawa0204@hiroshima-u.ac.jp.
ORCID: 0000-0002-5094-7070

Masamitsu Fukuyama (M)

Laboratory of Physiological Chemistry, Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan.
ORCID: 0000-0001-6999-8778

Adam Antebi (A)

Max Planck Institute for Biology of Ageing, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
ORCID: 0000-0002-7241-3029

Masaki Mizunuma (M)

Unit of Biotechnology, Graduate School of Integrated Sciences for Life, Hiroshima University, Higashi-Hiroshima, Japan. mmizu49120@hiroshima-u.ac.jp.
Hiroshima Research Center for Healthy Aging (HiHA), Hiroshima University, Higashi-Hiroshima, Japan. mmizu49120@hiroshima-u.ac.jp.
ORCID: 0000-0002-1531-1763

Articles similaires

Evaluating the efficacy of telesurgery with dual console SSI Mantra Surgical Robotic System: experiment on animal model and clinical trials.

Sudhir Prem Srivastava, Vishwajyoti Pascual Srivastava, Avinesh Singh et al.
1.00
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell

FBXO22 inhibits colitis and colorectal carcinogenesis by regulating the degradation of the S2448-phosphorylated form of mTOR.

Minle Li, Xuan Chen, Pengfei Qu et al.
1.00
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Use of organic material provided by an automatic enrichment device by weaner pigs and its influence on tail lesions.

Philipp Heseker, Jeanette Probst, Stefanie Ammer et al.
1.00
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Eucaryotes › Animaux › Invertébrés › Helminthes › Nematoda › Chromadorea › Rhabditida › Rhabditoidea › Caenorhabditis › Caenorhabditis elegans › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines d'helminthes › Protéines de Caenorhabditis elegans › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Phénomènes physiologiques › Croissance et développement › Morphogenèse › Métamorphose biologique › Étapes du cycle de vie › Diapause › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Phénomènes physiologiques › Longévité › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Environnement et santé publique › Environnement › Concepts météorologiques › Atmosphère › Temps (météorologie) › Température › Basse température › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines de liaison à l'ADN › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Phénomènes génétiques › Variation génétique › Mutation › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Transduction du signal › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Facteurs de transcription à motif hélice ailée › Facteurs de transcription Forkhead › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Phénomènes génétiques › Variation génétique › Mutation › Codon non-sens › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines de tissu nerveux › Neuropeptides › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines de transport › Regulatory mechanism of cold-inducible...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Facteurs de transcription à motif basique hélice-boucle-hélice › Regulatory mechanism of cold-inducible...