Impact of heat shock transcription factor 1 on global gene expression profiles in cells which induce either cytoprotective or pro-apoptotic response following hyperthermia

Kus‐Liśkiewicz, Małgorzata; Polańska, Joanna; Korfanty, Joanna; Olbryt, Magdalena; Vydra, Natalia; Toma, Agnieszka; Widłak, Wiesława

doi:10.1186/1471-2164-14-456

Cited by 31 publications

(38 citation statements)

References 96 publications

(110 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Adult (10-16-week-old), inbred FVB/N male mice were used for spermatocytes isolation (20 males per one isolation) by unit gravity sedimentation in linear BSA gradient as described earlier (Kus-Liśkiewicz et al, 2013). Isolated fraction contained up to 80% of spermatocytes and was contaminated mainly by round spermatids.…”

Section: Isolation Of Spermatocytesmentioning

confidence: 99%

“…For ChIP experiments heat shock was performed as described in details elsewhere (Kus-Liśkiewicz et al, 2013): an equal volume (10 ml) of CO 2 saturated, pre-heated media (to 53 • C or 60 • C) were added to the cell suspension, which immediately raised the temperature of the media from 32 • C to 38 • C or 43 • C, respectively. The tubes were submerged in a water bath at the appropriate temperature for an additional 5, 10, or 20 min (these samples were pooled and treated as heat shocked sample).…”

Section: Hyperthermia Treatmentmentioning

confidence: 99%

“…We used the ChIP-Seq approach to characterize actual binding sites for HSF1 and HSF2 in isolated mouse spermatocytes that were either untreated or heat-shocked for 5-20 min at 38 • C or at 43 • C. Duration of the heat shock was previously established as optimal for HSF1 activation (Kus-Liśkiewicz et al, 2013). We used a spermatocyte-enriched fraction of testicular cells because these cells are the most sensitive to damage at elevated temperatures (Yin et al, 1997); this approach also allows the avoiding of possible interference of somatic testicular cells (Kus-Liśkiewicz et al, 2013).…”

Section: Genome-wide Identification Of Hsf1 and Hsf2 Chromatin Bindinmentioning

confidence: 99%

“…We used a spermatocyte-enriched fraction of testicular cells because these cells are the most sensitive to damage at elevated temperatures (Yin et al, 1997); this approach also allows the avoiding of possible interference of somatic testicular cells (Kus-Liśkiewicz et al, 2013). The ChIP-Seq provided high-resolution maps of HSF1 and HSF2 target sites in the mouse genome (Suppl.…”

Section: Genome-wide Identification Of Hsf1 and Hsf2 Chromatin Bindinmentioning

confidence: 99%

“…Increasing the temperature of testis up to the body temperature (or above it) leads to the activation of HSF1. However, inducible Hspa1 (Hsp70i) genes expression is blocked in heat shocked murine spermatocytes (Izu et al, 2004;Vydra et al, 2006), although HSF1 binds to their promoters (Kus-Liśkiewicz et al, 2013). Moreover, the constitutively expressed testis-specific variant of HSP70 (HSPA2) is depleted after HSF1 activation (Widlak et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Crosstalk between HSF1 and HSF2 during the heat shock response in mouse testes

Korfanty

Stokowy

Widłak

et al. 2014

The International Journal of Biochemistry & Cell Biology

Self Cite

View full text Add to dashboard Cite

Heat Shock Factor 1 (HSF1) is the primary transcription factor responsible for the response to cellular stress, while HSF2 becomes activated during development and differentiation, including spermatogenesis. Although both factors are indispensable for proper spermatogenesis, activation of HSF1 by heat shock initiates apoptosis of spermatogenic cells leading to infertility of males. To characterize mechanisms assisting such heat induced apoptosis we studied how HSF1 and HSF2 cooperate during the heat shock response. For this purpose we used chromatin immunoprecipitation and the proximity ligation approaches. We looked for co-occupation of binding sites by HSF1 and HSF2 in untreated (32 °C) or heat shocked (at 38 °C or 43 °C) spermatocytes, which are cells the most sensitive to hyperthermia. At the physiological temperature or after mild hyperthermia at 38 °C, the sharing of binding sites for both HSFs was observed mainly in promoters of Hsp genes and other stress-related genes. Strong hyperthermia at 43 °C resulted in an increased binding of HSF1 and releasing of HSF2, hence co-occupation of promoter regions was not detected any more. The close proximity of HSF1 and HSF2 (and/or existence of HSF1/HSF2 complexes) was frequent at the physiological temperature. Temperature elevation resulted in a decreased number of such complexes and they were barely detected after strong hyperthermia at 43 °C. We have concluded that at the physiological temperature HSF1 and HSF2 cooperate in spermatogenic cells. However, temperature elevation causes remodeling of chromatin binding and interactions between HSFs are disrupted. This potentially affects the regulation of stress response and contributes to the heat sensitivity of these cells.

show abstract

Section: Isolation Of Spermatocytesmentioning

confidence: 99%

Section: Hyperthermia Treatmentmentioning

confidence: 99%

Section: Genome-wide Identification Of Hsf1 and Hsf2 Chromatin Bindinmentioning

confidence: 99%

Section: Genome-wide Identification Of Hsf1 and Hsf2 Chromatin Bindinmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Crosstalk between HSF1 and HSF2 during the heat shock response in mouse testes

Korfanty

Stokowy

Widłak

et al. 2014

The International Journal of Biochemistry & Cell Biology

Self Cite

View full text Add to dashboard Cite

show abstract

The Role of Heat Shock Factors in Mammalian Spermatogenesis

Widłak

Vydra

2017

Advances in Anatomy, Embryology and Cell Biology

View full text Add to dashboard Cite

Heat shock transcription factors (HSFs), as regulators of heat shock proteins (HSPs) expression, are well known for their cytoprotective functions during cellular stress. They also play important yet less recognized roles in gametogenesis. All HSF family members are expressed during mammalian spermatogenesis, mainly in spermatocytes and round spermatids which are characterized by extensive chromatin remodeling. Different HSFs could cooperate to maintain proper spermatogenesis. Cooperation of HSF1 and HSF2 is especially well established since their double knockout results in meiosis arrest, spermatocyte apoptosis, and male infertility. Both factors are also involved in the repackaging of the DNA during spermatid differentiation. They can form heterotrimers regulating the basal level of transcription of target genes. Moreover, HSF1/HSF2 interactions are lost in elevated temperatures which can impair the transcription of genes essential for spermatogenesis. In most mammals, spermatogenesis occurs a few degrees below the body temperature and spermatogenic cells are extremely heat-sensitive. Pro-survival pathways are not induced by heat stress (e.g., cryptorchidism) in meiotic and postmeiotic cells. Instead, male germ cells are actively eliminated by apoptosis, which prevents transition of the potentially damaged genetic material to the next generation. Such a response depends on the transcriptional activity of HSF1 which in contrary to most somatic cells, acts as a proapoptotic factor in spermatogenic cells. HSF1 activation could be the main trigger of impaired spermatogenesis related not only to elevated temperature but also to other stress conditions; therefore, HSF1 has been proposed to be the quality control factor in male germ cells.

show abstract

Cross talk between cytokine and hyperthermia-induced pathways: identification of different subsets of NF-κB-dependent genes regulated by TNFα and heat shock

et al. 2015

View full text Add to dashboard Cite

Heat shock inhibits NF-κB signaling, yet the knowledge about its influence on the regulation of NF-κB-dependent genes is limited. Using genomic approaches, i.e., expression microarrays and ChIP-Seq, we aimed to establish a global picture for heat shock-mediated impact on the expression of genes regulated by TNFα cytokine. We found that 193 genes changed expression in human U-2 osteosarcoma cells stimulated with cytokine (including 77 genes with the κB motif in the proximal promoters). A large overlap between sets of genes modulated by cytokine or by heat shock was revealed (86 genes were similarly affected by both stimuli). Binding sites for heat shock-induced HSF1 were detected in regulatory regions of 1/3 of these genes. Furthermore, pre-treatment with heat shock affected the expression of 2/3 of cytokine-modulated genes. In the largest subset of co-affected genes, heat shock suppressed the cytokine-mediated activation (antagonistic effect, 83 genes), which genes were associated with the canonical functions of NF-κB signaling. However, subsets of co-activated and co-repressed genes were also revealed. Importantly, pre-treatment with heat shock resulted in the suppression of NF-κB binding in the promoters of the cytokine-upregulated genes, either antagonized or co-activated by both stimuli. In conclusion, we confirmed that heat shock inhibited activation of genes involved in the classical cytokine-mediated functions of NF-κB. On the other hand, genes involved in transcription regulation were over-represented in the subset of genes upregulated by both stimuli. This suggests the replacement of NF-κB-mediated regulation by heat shock-mediated regulation in the latter subset of genes, which may contribute to the robust response of cells to both stress conditions.Electronic supplementary materialThe online version of this article (doi:10.1007/s00438-015-1055-1) contains supplementary material, which is available to authorized users.

show abstract

Impact of heat shock transcription factor 1 on global gene expression profiles in cells which induce either cytoprotective or pro-apoptotic response following hyperthermia

Cited by 31 publications

References 96 publications

Crosstalk between HSF1 and HSF2 during the heat shock response in mouse testes

Crosstalk between HSF1 and HSF2 during the heat shock response in mouse testes

The Role of Heat Shock Factors in Mammalian Spermatogenesis

Cross talk between cytokine and hyperthermia-induced pathways: identification of different subsets of NF-κB-dependent genes regulated by TNFα and heat shock

Contact Info

Product

Resources

About