BLMP-1/Blimp-1 Regulates the Spatiotemporal Cell Migration Pattern in C. elegans

Huang, Tsai-Fang; Cho, Chun-Yi; Cheng, Yi-Ting; Huang, Jheng-Wei; Wu, Yunzhe; Yeh, Athena Yi-Chun; Nishiwaki, Kiyoji; Chang, Shih‐Chung; Wu, Yih‐Min

doi:10.1371/journal.pgen.1004428

Cited by 27 publications

(64 citation statements)

References 57 publications

(74 reference statements)

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Section: Blmp-1 Is Necessary For Development Processessupporting

confidence: 80%

“…As previously reported, blmp-1 mutations or RNAi of blmp-1 in C. elegans causes gonadal migration defects and molting defect, along with a small body size ( Figure S1, A-D) (Horn et al 2014;Huang et al 2014). Upon examining the expression pattern of BLMP-1 during development by qPCR and Western blot analysis we noted that the messenger RNA (mRNA) and protein levels of BLMP-1 highly increased at the L2 (second larval) stage compared with other developmental stages (Figure 1, A and B).…”

Section: Blmp-1 Is Necessary For Development Processessupporting

confidence: 74%

“…Defects in the gene function are associated with certain type of lymphoma (Mandelbaum et al 2010), demonstrating its critical role in B cell development. Termination of B cell differentiation is controlled by PRDM-1/BLIMP-1 ( Kallies et al 2004) and an abnormal downregulation of PRDM-1/BLIMP-1 may prevent the terminal differentiation process in diffuse large B-cell lymphoma (Nie et al 2010).Recently, Horn et al (2014) and Huang et al (2014) reported that BLMP-1, which encodes a homolog of PRDM-1/ BLIMP-1, regulates the Caenorhabditis elegans developmental process. Both groups showed that blmp-1 is required for cell migration and the molting process via its interaction with DRE-1 (a C. elegans homolog of FBXO11).…”

mentioning

confidence: 99%

“…Recently, Horn et al (2014) and Huang et al (2014) reported that BLMP-1, which encodes a homolog of PRDM-1/ BLIMP-1, regulates the Caenorhabditis elegans developmental process. Both groups showed that blmp-1 is required for cell migration and the molting process via its interaction with DRE-1 (a C. elegans homolog of FBXO11).…”

mentioning

confidence: 99%

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BLIMP-1/BLMP-1 and Metastasis-Associated Protein Regulate Stress Resistant Development in Caenorhabditis elegans

et al. 2016

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Environmental stress triggers multilevel adaptations in animal development that depend in part on epigenetic mechanisms. In response to harsh environmental conditions and pheromone signals, Caenorhabditis elegans larvae become the highly stressresistant and long-lived dauer. Despite extensive studies of dauer formation pathways that integrate specific environmental cues and appear to depend on transcriptional reprogramming, the role of epigenetic regulation in dauer development has remained unclear. Here we report that BLMP-1, the BLIMP-1 ortholog, regulates dauer formation via epigenetic pathways; in the absence of TGF-b signaling (in daf-7 mutants), lack of blmp-1 caused lethality. Using this phenotype, we screened 283 epigenetic factors, and identified lin-40, a homolog of metastasis-associate protein 1 (MTA1) as an interactor of BLMP-1. The interaction between LIN-40 and BLMP-1 is conserved because mammalian homologs for both MTA1 and BLIMP-1 could also interact. From microarray studies, we identified several downstream target genes of blmp-1: npr-3, nhr-23, ptr-4, and sams-1. Among them S-adenosyl methionine synthase (SAMS-1), is the key enzyme for production of SAM used in histone methylation. Indeed, blmp-1 is necessary for controlling histone methylation level in daf-7 mutants, suggesting BLMP-1 regulates the expression of SAMS-1, which in turn may regulate histone methylation and dauer formation. Our results reveal a new interaction between BLMP-1/BLIMP-1 and LIN-40/MTA1, as well as potential epigenetic downstream pathways, whereby these proteins cooperate to regulate stress-specific developmental adaptations.KEYWORDS stress resistant development; BLMP-1; epigenetics; TGF-b; dauer D URING development, epigenetic changes in gene expression are passed on to the daughter cells to dictate cell fate without changing the DNA sequence itself (Hemberger et al. 2009). Epigenetic regulation is critical not only for normal development but also for tumor proliferation (Jones and Baylin 2007). The PRDM (PR domain-containing genes) family regulates many epigenetic events through interactions with histone modification and nucleosome remodeling factors (Hohenauer and Moore 2012;Pinheiro et al. 2012). Within this family, PRDM-1/BLIMP-1 regulates differentiation of various tissues and cell types including germ cells and B cells (Turner et al. 1994;Bikoff et al. 2009;John and Garrett-Sinha 2009). PRDM-1/BLIMP-1 is a transcriptional repressor, interacting with chromatin factors, such as the SET domain protein G9a (Yu et al. 2000), histone deacetylase HDAC1/2 (Gyory et al. 2004), and demethylase LSD1 (Su et al. 2009). Defects in the gene function are associated with certain type of lymphoma (Mandelbaum et al. 2010), demonstrating its critical role in B cell development. Termination of B cell differentiation is controlled by PRDM-1/BLIMP-1 ( Kallies et al. 2004) and an abnormal downregulation of PRDM-1/BLIMP-1 may prevent the terminal differentiation process in diffuse large B-cell lymphoma (Nie et al. 2010).Recentl...

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Section: Blmp-1 Is Necessary For Development Processessupporting

confidence: 80%

Section: Blmp-1 Is Necessary For Development Processessupporting

confidence: 74%

mentioning

confidence: 99%

mentioning

confidence: 99%

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BLIMP-1/BLMP-1 and Metastasis-Associated Protein Regulate Stress Resistant Development in Caenorhabditis elegans

et al. 2016

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“…The blmp-1 (tm548) mutant was generated by the National Bioresource Project in Japan; it contains an 810-bp deletion that has been described elsewhere (Huang et al 2014b). We acquired it from H. R. Horvitz then outcrossed it 10 times against N2 (the strain is called YJ55).…”

Section: Strains and Culture Conditionsmentioning

confidence: 99%

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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Direct and positive regulation of Caenorhabditis elegans bed-3 by PRDM1/BLIMP1 ortholog BLMP-1

Yang

Fong

Xie

et al. 2015

Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanism

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BLMP-1/Blimp-1 Regulates the Spatiotemporal Cell Migration Pattern in C. elegans

Cited by 27 publications

References 57 publications

BLIMP-1/BLMP-1 and Metastasis-Associated Protein Regulate Stress Resistant Development in Caenorhabditis elegans

BLIMP-1/BLMP-1 and Metastasis-Associated Protein Regulate Stress Resistant Development in Caenorhabditis elegans

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

Direct and positive regulation of Caenorhabditis elegans bed-3 by PRDM1/BLIMP1 ortholog BLMP-1

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