The developing story of Sprouty and cancer

Masoumi-Moghaddam, Samar; Amini, Afshin; Morris, David L.

doi:10.1007/s10555-014-9497-1

Cited by 139 publications

(192 citation statements)

References 174 publications

(262 reference statements)

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“…Consistent with our results, SCD1, the main enzyme involved in the synthesis of monounsaturated fatty acids, has been shown to be required for cancer cell proliferation, survival, transformation to cancer (32), and cancer spheroids propagation (33). The Sprouty family of proteins, key regulators of ERK signaling, has been shown to be able to function as negative or positive regulators of tumor development and/or progression in a cell type-dependent manner (34). PGM1 is known to be induced under hypoxic conditions and promotes cancer cell survival (35).…”

Section: Discussionsupporting

confidence: 89%

Long noncoding RNA UPAT promotes colon tumorigenesis by inhibiting degradation of UHRF1

Taniue

Kurimoto

Sugimasa

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

135

127

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Many long noncoding RNAs (lncRNAs) are reported to be dysregulated in human cancers and play critical roles in tumor development and progression. Furthermore, it has been reported that many lncRNAs regulate gene expression by recruiting chromatin remodeling complexes to specific genomic loci or by controlling transcriptional or posttranscriptional processes. Here we show that an lncRNA termed UPAT [ubiquitin-like plant homeodomain (PHD) and really interesting new gene (RING) finger domaincontaining protein 1 (UHRF1) Protein Associated Transcript] is required for the survival and tumorigenicity of colorectal cancer cells. UPAT interacts with and stabilizes the epigenetic factor UHRF1 by interfering with its β-transducin repeat-containing protein (TrCP)-mediated ubiquitination. Furthermore, we demonstrate that UHRF1 up-regulates Stearoyl-CoA desaturase 1 and Sprouty 4, which are required for the survival of colon tumor cells. Our study provides evidence for an lncRNA that regulates protein ubiquitination and degradation and thereby plays a critical role in the survival and tumorigenicity of tumor cells. Our results suggest that UPAT and UHRF1 may be promising molecular targets for the therapy of colon cancer.A mong the RNA products transcribed from the mammalian genome are numerous long noncoding RNAs (lncRNAs)-that is, RNAs longer than 200 nucleotides with little or no protein-coding potential (1, 2). Many lncRNAs are expressed in a developmentally regulated and cell type-dependent manner (3, 4). Increasing evidence suggests that lncRNAs play critical roles in a diverse set of biological processes, including proliferation, differentiation, embryogenesis, neurogenesis, and stem cell pluripotency (5, 6).It has been reported that many lncRNAs regulate gene expression by recruiting chromatin remodeling complexes to specific genomic regions (2). It has also been shown that many lncRNAs regulate transcription by modulating the activity of transcriptional regulators (1, 6-8). lncRNAs also regulate various posttranscriptional processes, including splicing, transport, translation, and degradation of mRNA. Furthermore, recent studies have shown that a number of lncRNAs play critical roles in tumor development and progression.UHRF1 [ubiquitin-like plant homeodomain (PHD) and really interesting new gene (RING) finger domain-containing protein 1] is an epigenetic factor that consists of multiple domains (9). UHRF1 regulates transcription by regulating DNA methylation and histone modification. UHRF1 also possesses E3 ubiquitin ligase activity and ubiquitinates histones and DNA methyltransferase 1 (DNMT1), thereby regulating the chromatin structure and stability of DNMT1 (10, 11). UHRF1 plays key roles in multiple biological processes, including proliferation and development. Furthermore, UHRF1 is overexpressed in various tumors, including colon, breast, bladder, prostate, and lung cancers, and plays a critical role in the proliferation and survival of tumor cells (9).In the present study, we attempted to identify lncRNAs criti...

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Section: Discussionsupporting

confidence: 89%

Long noncoding RNA UPAT promotes colon tumorigenesis by inhibiting degradation of UHRF1

Taniue

Kurimoto

Sugimasa

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

135

127

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“…However, the role of SPRY2 in cancer remains unclear. 2 In colon cancer, we have previously reported SPRY2 upregulation in high-grade tumors and at the invasion front of low-grade tumors. 7 Likewise, SPRY2 RNA and protein levels are higher in colon adenocarcinomas than in normal adjacent mucosa.…”

Section: Introductionmentioning

confidence: 96%

“…[15][16][17][18][19] These opposite effects are indicative of cell-type-dependent activities of SPRY2. 2 To dissect the action of SPRY2 in colon cancer, we analyzed its effects on gene expression and phenotype of SW480-ADH cells. Transcriptomic analyses revealed the repression by SPRY2 of genes encoding proteins involved in cell-to-cell and cell-tomatrix adhesion or regulating epithelial cell polarity such as ST14, which codes for the membrane-anchored serine protease matriptase that is essential for the integrity of the intestinal epithelial barrier.…”

Section: Introductionmentioning

confidence: 99%

SPROUTY-2 represses the epithelial phenotype of colon carcinoma cells via upregulation of ZEB1 mediated by ETS1 and miR-200/miR-150

et al. 2015

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“…In contrast to Drosophila, in mammalian systems, signalling activated by epidermal growth factor is increased with augmented Spry expression. Therefore, the Spry proteins in humans are generally considered as modulators of signal transduction (12). Accordingly, dependent on the tumour type, Spry proteins are found to fulfil multiple roles in cancer.…”

Section: Introductionmentioning

confidence: 99%

“…For example, Spry2 has been indicated to function as an oncogene in colon cancer (13,14) and Spry1 has a tumour promoting role in rhabdomyosarcoma (15). However, Spry proteins have been primarily shown to suppress the tumorigenic process (12). Spry2 is a tumour-suppressor in lung (16), prostate (17,18), breast (19), liver (20) and ovarian cancer (21).…”

Section: Introductionmentioning

confidence: 99%

Sprouty4 mRNA variants and protein expressions in breast and lung-derived cells

2016

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Ab st rac t . Sp rout y p rot ei ns a r e mo du lat or s of mitogen-induced signalling processes and are therefore hypothesized to affect malignant diseases. As a member of the Sprouty family, Sprouty4 has been previously shown to function as a tumour suppressor in lung and breast cancer. The present study analysed the expression of two known Sprouty4 splice variants in cells established from malignant and normal lung and breast tissues using semi-quantitative reverse transcription-polymerase chain reaction and immunoblotting. The results indicated that the expression of the two messenger RNA (mRNA) variants was reduced in the cells derived from malignant tissue in comparison to the normal counterparts. Although the expression of the two splice variants were associated in both tissue types, on average, the relative expression of the longer variant was slightly increased in malignant cells compared with normal tissues. Notably, the protein levels reflected the expression observed at the mRNA level only in breast-derived cells. Contrarily, with regards to the measured mRNA levels, Sprouty4 protein was disproportional augmented in lung cells known to harbour the mutated K-Ras gene. IntroductionThe alteration of important molecules involved in signal transduction is a common characteristic of all malignant cells (1). The mitogen activated protein kinase (MAPK) pathway, which is crucially involved in balancing cell death and differentiation on one side and proliferation and migration on the other, is one of the best described signalling routes that is deregulated in cancer (2). Due to the vital role of the MAPK pathway, numerous feedback loops are present to allow a fine-tuning of signal intensity and duration (3). Certain molecules acting in such a regulatory loop are the members of the Sprouty (Spry) protein family. First discovered in Drosophila (4,5), the Spry proteins counteract processes induced by the presence of various growth factors. In humans, 4 Spry family members are known; all of which share a conserved Spry domain at the C-terminus and 2 homolog N-terminal boxes (6). As indicated by knockout studies in mice, the functions of Sprouty proteins overlap but are not redundant (7-10). Although Spry1, Spry2 and Spry4 can be detected in all organs, their expression pattern in the various cell types is clearly distinguishable (11). Like in Drosophila, mammalian Spry proteins interfere with signal transduction, particularly in the MAPK pathway, in response to various mitogens, such as the members of the fibroblast growth factors (6). In contrast to Drosophila, in mammalian systems, signalling activated by epidermal growth factor is increased with augmented Spry expression. Therefore, the Spry proteins in humans are generally considered as modulators of signal transduction (12). Accordingly, dependent on the tumour type, Spry proteins are found to fulfil multiple roles in cancer. For example, Spry2 has been indicated to function as an oncogene in colon cancer (13,14) and Spry1 has a tumour promoting role in rhabd...

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The developing story of Sprouty and cancer

Cited by 139 publications

References 174 publications

Long noncoding RNA UPAT promotes colon tumorigenesis by inhibiting degradation of UHRF1

Long noncoding RNA UPAT promotes colon tumorigenesis by inhibiting degradation of UHRF1

SPROUTY-2 represses the epithelial phenotype of colon carcinoma cells via upregulation of ZEB1 mediated by ETS1 and miR-200/miR-150

Sprouty4 mRNA variants and protein expressions in breast and lung-derived cells

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