Dataset Information

O-GlcNAc reports ambient temperature and confers heat resistance on ectotherm development.

ABSTRACT: Effects of temperature on biological processes are complex. Diffusion is less affected than the diverse enzymatic reactions that have distinct individual temperature profiles. Hence thermal fluctuations pose a formidable challenge to ectothermic organisms in which body temperature is largely dictated by the ambient temperature. How cells in ectotherms cope with the myriad disruptive effects of temperature variation is poorly understood at the molecular level. Here we show that nucleocytoplasmic posttranslational modification of proteins with O-linked GlcNAc (O-GlcNAc) is closely correlated with ambient temperature during development of distantly related ectotherms ranging from the insect Drosophila melanogaster to the nematode Caenorhabditis elegans to the fish Danio rerio. Regulation seems to occur at the level of activity of the only two enzymes, O-GlcNAc transferase and O-GlcNAcase, that add and remove, respectively, this posttranslational modification in nucleus and cytoplasm. With genetic approaches in D. melanogaster and C. elegans, we demonstrate the importance of high levels of this posttranslational modification for successful development at elevated temperatures. Because many cytoplasmic and nuclear proteins in diverse pathways are O-GlcNAc targets, temperature-dependent regulation of this modification might contribute to an efficient coordinate adjustment of cellular processes in response to thermal change.

SUBMITTER: Radermacher PT

PROVIDER: S-EPMC3992692 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

O-GlcNAc reports ambient temperature and confers heat resistance on ectotherm development.

Radermacher Pablo T PT Myachina Faina F Bosshardt Fritz F Pandey Rahul R Mariappa Daniel D Müller H-Arno J HA Lehner Christian F CF

Proceedings of the National Academy of Sciences of the United States of America 20140331 15

Effects of temperature on biological processes are complex. Diffusion is less affected than the diverse enzymatic reactions that have distinct individual temperature profiles. Hence thermal fluctuations pose a formidable challenge to ectothermic organisms in which body temperature is largely dictated by the ambient temperature. How cells in ectotherms cope with the myriad disruptive effects of temperature variation is poorly understood at the molecular level. Here we show that nucleocytoplasmic ...[more]

PMID: 24706800

Similar Datasets

Project description:This study aimed to investigate the effects of different acute high ambient temperatures on redox status in liver of broilers. A total of 144 35-day-old Arbor Acres broilers were randomly divided into 4 groups with 6 replicates of 6 birds each and subsequently distributed in different environment chambers for acute heat stress. The temperature of 4 environment chambers were set to 26°C (control), 29°C, 32°C, 35°C for 6 h, respectively. Various indicators were tested to evaluate hepatic redox status. Then, the hallmarks of hepatocellular antioxidant and apoptosis were measured by qRT-PCR and Western Blot. The results showed that with the ambient temperature increase (i) the content of hydrogen peroxide (H2O2) and protein carbonyl (PC) in the liver of broilers increased significantly (P < 0.05), but the content of malondialdehyde (MDA) and 8-hydroxyguanosine (8-OHdG) was not affected; (ii) the activity of catalase (CAT) and glutathione reductase (GR) increased significantly (P < 0.05). Similarly, the superoxide dismutase (SOD) had an increasing tendency (P = 0.07), and the content of the reduced glutathione (GSH) was also significantly increased (P < 0.05) under high temperature; (iii) the heat shock protein (HSP70), nuclear factor erythroid-2-related factor 2 (Nrf2), and other antioxidant gene (HO-1, NQO1, GCLc, GST, SOD1, SOD2, CAT, Prx3) were upregulated in broilers liver. Moreover, the protein level of HSP70, Nrf2, and Prx3 were also upregulated; (iv) high temperature upregulated the antiapoptotic gene expression (BCL-2); however, the proapoptotic genes (BAK1, caspase-3, and caspase-9) did not change significantly; meanwhile, there was no significant changes in the protein level of caspase-3 and caspase-9. The results of this study indicated that 35-day-old Arbor Acres broilers have a certain tolerance to oxidative stress induced by high ambient temperature. Six hours of acute heat stress-activated Nrf2 signaling pathway. Meanwhile, the expression of related antioxidant genes and proteins is upregulated, consequently resulted in increased antioxidant enzymes activity and GSH. These effects enable the body to scavenge large amounts of reactive oxygen species produced by high temperature and prevent the occurrence of apoptosis.

Project description:Some chlorine-resistant Escherichia coli isolates harbor the locus of heat resistance (LHR), a genomic island conferring heat resistance. In this study, the protective effect of the LHR for cells challenged by chlorine and oxidative stress was quantified. Cloning of the LHR protected against NaClO (32 mM; 5 min), H2O2 (120 mM; 5 min), and peroxyacetic acid (105 mg/liter; 5 min) but not against 5.8 mM KIO4, 10 mM acrolein, or 75 mg/liter allyl isothiocyanate. The lethality of oxidizing treatments for LHR-negative strains of E. coli was about 2 log10 CFU/ml higher than that for LHR-positive strains of E. coli The oxidation of cytoplasmic proteins and membrane lipids was quantified with the fusion probe roGFP2-Orp1 and the fluorescent probe BODIPY581/591, respectively. The fragment of the LHR coding for heat shock proteins protected cytoplasmic proteins but not membrane lipids against oxidation. The middle fragment of the LHR protected against the oxidation of membrane lipids but not of cytoplasmic proteins. The addition of H2O2, NaClO, and peroxyacetic acid also induced green fluorescent protein (GFP) expression in the oxidation-sensitive reporter strain E. coli O104:H4 Δstx2::gfp::amp Cloning of pLHR reduced phage induction in E. coli O104:H4 Δstx2::gfp::amp after treatment with oxidizing chemicals. Screening of 160 strains of Shiga toxin-producing E. coli (STEC) revealed that none of them harbors the LHR, additionally suggesting that the LHR and Stx prophages are mutually exclusive. Taking our findings together, the contribution of the LHR to resistance to chlorine and oxidative stress is based on the protection of multiple cellular targets by different proteins encoded by the genetic island.IMPORTANCE Chlorine treatments are used in water and wastewater sanitation; the resistance of Escherichia coli to chlorine is thus of concern to public health. We show that a genetic island termed the locus of heat resistance (LHR) protects E. coli not only against heat but also against chlorine and other oxidizing chemicals, adding to our knowledge of the tools used by E. coli to resist stress. Specific detection of the oxidation of different cellular targets in combination with the cloning of fragments of the LHR provided insight into mechanisms of protection and demonstrated that different fragments of the LHR protect different cellular targets. In E. coli, the presence of the LHR virtually always excluded other virulence factors. It is tempting to speculate that the LHR is maintained by strains of E. coli with an environmental lifestyle but is excluded by pathogenic strains that adapted to interact with vertebrate hosts.

Dataset Information

O-GlcNAc reports ambient temperature and confers heat resistance on ectotherm development.

Publications

O-GlcNAc reports ambient temperature and confers heat resistance on ectotherm development.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets