Hypoxia-inducible Factor-1 (HIF-1)-independent Hypoxia Response of the Small Heat Shock Protein hsp-16.1 Gene Regulated by Chromatin-remodeling Factors in the Nematode Caenorhabditis elegans

Lee, Ji‐Hyun; Lee, Jun-Ho

doi:10.1074/jbc.m112.401554

Cited by 19 publications

(21 citation statements)

References 49 publications

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“…In addition, swsn-7(gk1041) mutants were strongly compromised for induction of P hsp-16.1 ::GFP following hypoxia, demonstrating that SWSN-7 is required for ESRE gene expression under multiple stress conditions (see Fig. S5 in the supplemental material) (63).…”

Section: Resultsmentioning

confidence: 99%

The Conserved PBAF Nucleosome-Remodeling Complex Mediates the Response to Stress in Caenorhabditis elegans

Kuzmanov

Karina

Kirienko

et al. 2014

Molecular and Cellular Biology

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To adapt to stress, cells must undergo major changes in their gene expression profiles. We have previously described a largely uncharacterized stress response pathway in Caenorhabditis elegans that acts through an evolutionarily conserved motif, termed ESRE, for ethanol and stress response element. We characterize here the requirements for ESRE gene expression and show that the ESRE network is regulated by a conserved SWI/SNF family nucleosome remodeling complex termed PBAF. Depletion of PBAF subunits SWSN-7/BAF200 and PBRM-1/BAF180 results in decreased expression of ESRE genes and increased sensitivity to thermal stress. When overexpressed, SWSN-7/BAF200 and PBRM-1/BAF180 led to increased ESRE transcription, enhanced thermotolerance, and induction of a nuclear ESRE-binding activity. Our data support a model in which PBAF is recruited by an ESRE-binding protein to genomic ESRE sites. We also show that the closely related SWI/SNF complex, BAF, which regulates stress induction through DAF-16/FOXO, does not contribute to ESRE gene expression or bind directly to ESRE sites. To our knowledge, this is the first report demonstrating direct and specific regulation of a stress response network by the PBAF nucleosome-remodeling complex in vivo in metazoa. In addition, we show that PBAF cooperates with the histone demethylase, JMJC-1/NO66, to promote expression of ESRE genes following stress.

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Section: Resultsmentioning

confidence: 99%

The Conserved PBAF Nucleosome-Remodeling Complex Mediates the Response to Stress in Caenorhabditis elegans

Kuzmanov

Karina

Kirienko

et al. 2014

Molecular and Cellular Biology

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“…Previous studies have demonstrated the necessity and importance of non-HIF pathway-mediated transcriptional responses in hypoxia (Shen et al 2005;Arany et al 2008;Lee and Lee 2013;Li et al 2013). We were interested in further elucidating how, and to what extent, oxygen-sensitive regulation of transcripts occurs independent of HIF-1 in C.…”

Section: Generating a Hypoxia-sensitive Hif-independent Reporter Linementioning

confidence: 99%

“…In spite of the pervasive nature of the HIF pathway, evidence from diverse systems demonstrates that hypoxia-induced transcriptional responses arise from multiple pathways that collectively drive adaptation in low-oxygen conditions, some of which do not require HIF-1 (Shen et al 2005;Lee and Lee 2013;Li et al 2013). While much progress has been made in defining the mechanisms that support HIF-1-mediated hypoxic actions, the nature and influence of HIF-1-independent hypoxic responses remain ill defined.…”

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confidence: 99%

“…Additionally, C. elegans can survive for 24 hr in anoxic conditions and this response does not require hif-1; instead, this "suspended animation" response is mediated by the spindle checkpoint protein SAN-1 in embryos and the ceramide synthase HYL-2 in adults (Padilla et al 2002;Nystul et al 2003;Menuz et al 2009;Miller and Roth 2009). Additionally, Lee and Lee (2013) described the role of the chromatin-remodeling factor NURF-1 in regulating the expression of a novel HIF-1-independent protein, heat shock protein HSP-16.1 (Lee and Lee 2013).…”

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confidence: 99%

“…Not surprisingly, the core components of the HIF-1 pathway (HIF-1a, HIF-1b, PHD, and VHL) are well conserved in the worm, where HIF-1, AHA-1, EGL-9, and VHL-1 fulfill the necessary roles of their respective mammalian counterparts (Bruick and Epstein et al 2001;Jiang et al 2001;McKnight 2001). As in vertebrates, the C. elegans HIF-1 pathway plays a critical role in varied biological processes including aging, neuronal reorganization, and stress responses (Treinin et al 2003;Bretscher et al 2008;Pocock and Hobert 2008;Chen et al 2009;Budde and Roth 2010 In spite of the pervasive nature of the HIF pathway, evidence from diverse systems demonstrates that hypoxia-induced transcriptional responses arise from multiple pathways that collectively drive adaptation in low-oxygen conditions, some of which do not require HIF-1 (Shen et al 2005;Lee and Lee 2013;Li et al 2013). While much progress has been made in defining the mechanisms that support HIF-1-mediated hypoxic actions, the nature and influence of HIF-1-independent hypoxic responses remain ill defined.…”

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confidence: 99%

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A HIF-Independent Mediator of Transcriptional Responses to Oxygen Deprivation in Caenorhabditis elegans

et al. 2014

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The adaptive response to hypoxia is accompanied by widespread transcriptional changes that allow for prolonged survival in low oxygen. Many of these changes are directly regulated by the conserved hypoxia-inducible factor-1 (HIF-1) complex; however, even in its absence, many oxygen-sensitive transcripts in Caenorhabditis elegans are appropriately regulated in hypoxia. To identify mediators of these non-HIF-dependent responses, we established a hif-1 mutant reporter line that expresses GFP in hypoxia or when worms are treated with the hypoxia mimetic cobalt chloride (CoCl 2 ). The reporter is selective and HIF independent, in that it remains insensitive to a number of cellular stresses, but is unaffected by mutation of the prolyl hydroxylase egl-9, suggesting that the regulators of this response pathway are different from those controlling the HIF pathway. We used the HIF-independent reporter to screen a transcription factor RNA interference (RNAi) library and identified genes that are required for hypoxia-sensitive and CoCl 2 -induced GFP expression. We identified the zinc finger protein BLMP-1 as a mediator of the HIF-independent response. We show that mutation of blmp-1 renders animals sensitive to hypoxic exposure and that blmp-1 is required for appropriate hypoxic-induced expression of HIF-independent transcripts. Further, we demonstrate that BLMP-1 is necessary for an increase of hypoxia-dependent histone acetylation within the promoter of a non-HIF-dependent hypoxia response gene.KEYWORDS hypoxia; HIF independent; BLMP-1; C. elegans C ELLS are routinely challenged with low-oxygen conditions that drive compensatory responses. For instance, in development, low-oxygen conditions induce differentiation of placental cells (Dunwoodie 2009), and in diseased states, hypoxia is often a major contributing factor in cardiovascular disease and in the progression of solid tumor growth (Denko 2008;Semenza 2014). These low-oxygen challenges, whether scripted as in development or as consequences of physiologic dysfunction, are confronted by rapid cellular changes and by slower responses such as those mediated by the hypoxiainducible factor-1 (HIF-1) transcription pathway.The conserved HIF-1 complex regulates the expression of a broad set of genes that affect various aspects of metabolism, vascularization, and cell survival across species (Semenza 2011). In normoxia, the HIF-1 pathway is rendered inactive by prolyl hydroxylases (PHDs) that use molecular oxygen to modify conserved proline residues on the HIF-1a subunit of the transcription factor. The proline-hydroxylated HIF-1a is recognized by the von Hippel-Lindau (VHL) tumor suppressor protein, which targets HIF-1a for degradation (Bruick and McKnight 2001;Epstein et al. 2001). In hypoxia, owing to the reduced activity of PHD, unmodified HIF-1a pairs with the oxygen insensitive HIF-1b and the complex is transcriptionally active (Berra et al. 2006).The nematode Caenorhabditis elegans is adept at enduring periods of low oxygen (Powell-Coffman 2010). Not surprisin...

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Angiogenesis Inhibitors in the Treatment of Cancer

Abdel-Wahab

2023

Handbook of Cancer and Immunology

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Hypoxia-inducible Factor-1 (HIF-1)-independent Hypoxia Response of the Small Heat Shock Protein hsp-16.1 Gene Regulated by Chromatin-remodeling Factors in the Nematode Caenorhabditis elegans

Cited by 19 publications

References 49 publications

The Conserved PBAF Nucleosome-Remodeling Complex Mediates the Response to Stress in Caenorhabditis elegans

The Conserved PBAF Nucleosome-Remodeling Complex Mediates the Response to Stress in Caenorhabditis elegans

A HIF-Independent Mediator of Transcriptional Responses to Oxygen Deprivation in Caenorhabditis elegans

Angiogenesis Inhibitors in the Treatment of Cancer

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