Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans

Chauve, Laetitia; Hodge, Francesca; Murdoch, Sharlene; Masoudzadeh, Fatemeh; Mann, Harry-Jack; Lopez-Clavijo, Andrea F.; Okkenhaug, Hanneke; West, Greg; Sousa, Bebiana C.; Segonds‐Pichon, Anne; Li, Cheryl; Wingett, Steven; Kienberger, Hermine; Kleigrewe, Karin; Bono, Mario de; Wakelam, Michael J.O.; Casanueva, Olivia

doi:10.1371/journal.pbio.3001431

Cited by 17 publications

(29 citation statements)

References 78 publications

(99 reference statements)

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“…Pioneering work by Lee and Kenyon showed that a reduction in HSF-1 function further shortened lifespan at 22.5°C. Consistent with this, recent data show that overexpression of hsf-1 in neurons protects animals at 25°C and extends their lifespan ( Chauve et al, 2021 ). Overexpression of the proteasomal subunit rpn-6.1 extends lifespan independently of HSF-1 in a DAF-16-dependent manner at 25°C ( Vilchez et al, 2012 ).…”

Section: Modulation Of Organismal Longevity By Temperaturesupporting

confidence: 64%

Temperature-Dependent Regulation of Proteostasis and Longevity

Vakkayil

Hoppe

2022

Front. Aging

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Temperature is an important environmental condition that determines the physiology and behavior of all organisms. Animals use different response strategies to adapt and survive fluctuations in ambient temperature. The hermaphrodite Caenorhabditis elegans has a well-studied neuronal network consisting of 302 neurons. The bilateral AFD neurons are the primary thermosensory neurons in the nematode. In addition to regulating thermosensitivity, AFD neurons also coordinate cellular stress responses through systemic mechanisms involving neuroendocrine signaling. Recent studies have examined the effects of temperature on altering various signaling pathways through specific gene expression programs that promote stress resistance and longevity. These studies challenge the proposed theories of temperature-dependent regulation of aging as a passive thermodynamic process. Instead, they provide evidence that aging is a well-defined genetic program. Loss of protein homeostasis (proteostasis) is one of the key hallmarks of aging. Indeed, proteostasis pathways, such as the heat shock response and aggregation of metastable proteins, are also controlled by thermosensory neurons in C. elegans. Prolonged heat stress is thought to play a critical role in the development of neurodegenerative protein misfolding diseases in humans. This review presents the latest evidence on how temperature coordinates proteostasis and aging. It also discusses how studies of poikilothermic organisms can be applied to vertebrates and provides new therapeutic strategies for human disease.

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Section: Modulation Of Organismal Longevity By Temperaturesupporting

confidence: 64%

Temperature-Dependent Regulation of Proteostasis and Longevity

Vakkayil

Hoppe

2022

Front. Aging

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“…For qPCR reactions, cDNA (~1200 ng/μl) was diluted fivefold and prepared for amplification using a BioRad SYBR Green Supermix Kit with the primers for nucleoporin genes listed in key resource table as well as pmp-3 primers from Chauve et al, 2021 . For each biological replicate (two wild type and two ndc1Δ ), four technical replicates were performed.…”

Section: Methodsmentioning

confidence: 99%

Ndc1 drives nuclear pore complex assembly independent of membrane biogenesis to promote nuclear formation and growth

Mauro

Celma

Zimyanin

et al. 2022

eLife

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The nuclear envelope (NE) assembles and grows from bilayer lipids produced at the endoplasmic reticulum (ER). How ER membrane incorporation coordinates with assembly of nuclear pore complexes (NPCs) to generate a functional NE is not well understood. Here, we use the stereotypical first division of the early C. elegans embryo to test the role of the membrane-associated nucleoporin Ndc1 in coupling NPC assembly to NE formation and growth. 3D-EM tomography of reforming and expanded NEs establishes that Ndc1 determines NPC density. Loss of ndc1 results in faster turnover of the outer scaffold nucleoporin Nup160 at the NE, providing an explanation for how Ndc1 controls NPC number. NE formation fails in the absence of both Ndc1 and the inner ring component Nup53, suggesting partially redundant roles in NPC assembly. Importantly, upregulation of membrane synthesis restored the slow rate of nuclear growth resulting from loss of ndc1 but not from loss of nup53. Thus, membrane biogenesis can be decoupled from Ndc1-mediated NPC assembly to promote nuclear growth. Together, our data suggest that Ndc1 functions in parallel with Nup53 and membrane biogenesis to control NPC density and nuclear size.

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“…Hsf-1 is an important long-lived transcription factor that acts downstream of the IIS and is widely studied. It has been reported that downregulation of the IIS pathway, along with coactivation of Hsf-1, is necessary for the prolongation of life ( Chauve et al, 2021 ). To investigate whether Hsf-1 is required for SVHRSP-mediated life extension, we tested the effects of 20- and 40-μM SVHRSP on Hsf-1 (SY441) mutant worms PS3551.…”

Section: Resultsmentioning

confidence: 99%

Scorpion Venom Heat–Resistant Synthesized Peptide Increases Stress Resistance and Extends the Lifespan of Caenorhabditis elegans via the Insulin/IGF-1-Like Signal Pathway

et al. 2022

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Improving healthy life expectancy by targeting aging-related pathological changes has been the spotlight of geroscience. Scorpions have been used in traditional medicine in Asia and Africa for a long time. We have isolated heat-resistant peptides from scorpion venom of Buthusmartensii Karsch (SVHRP) and found that SVHRP can attenuate microglia activation and protect Caenorhabditis elegans (C. elegans) against β-amyloid toxicity. Based on the amino acid sequence of these peptides, scorpion venom heat–resistant synthesized peptide (SVHRSP) was prepared using polypeptide synthesis technology. In the present study, we used C. elegans as a model organism to assess the longevity-related effects and underlying molecular mechanisms of SVHRSP in vivo. The results showed that SVHRSP could prolong the lifespan of worms and significantly improve the age-related physiological functions of worms. SVHRSP increases the survival rate of larvae under oxidative and heat stress and decreases the level of reactive oxygen species and fat accumulation in vivo. Using gene-specific mutation of C. elegans, we found that SVHRSP-mediated prolongation of life depends on Daf-2, Daf-16, Skn-1, and Hsf-1 genes. These results indicate that the antiaging mechanism of SVHRSP in nematodes might be mediated by the insulin/insulin-like growth factor-1 signaling pathway. Meanwhile, SVHRSP could also up-regulate the expression of stress-inducing genes Hsp-16.2, Sod-3, Gei-7, and Ctl-1 associated with aging. In general, our study may have important implications for SVHRSP to promote healthy aging and provide strategies for research and development of drugs to treat age-related diseases.

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Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans

Cited by 17 publications

References 78 publications

Temperature-Dependent Regulation of Proteostasis and Longevity

Temperature-Dependent Regulation of Proteostasis and Longevity

Ndc1 drives nuclear pore complex assembly independent of membrane biogenesis to promote nuclear formation and growth

Scorpion Venom Heat–Resistant Synthesized Peptide Increases Stress Resistance and Extends the Lifespan of Caenorhabditis elegans via the Insulin/IGF-1-Like Signal Pathway

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