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Published in: European Archives of Oto-Rhino-Laryngology 1/2024

01-09-2023 | Head and Neck

A novel and independent survival prognostic model for OSCC: the functions and prognostic values of RNA-binding proteins

Authors: Shanshan Wang, Shuang Liu, Yaomin Zhu, Baorong Zhang, Yongtao Yang, Limei Li, Yingying Sun, Long Zhang, Lina Fan, Xuegang Hu, Chunyu Huang

Published in: European Archives of Oto-Rhino-Laryngology | Issue 1/2024

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Abstract

Background

Oral squamous cell carcinoma (OSCC), exhibiting high morbidity and malignancy, is the most common type of oral cancer. The abnormal expression of RNA-binding proteins (RBPs) plays important roles in the occurrence and progression of cancer. The objective of the present study was to establish a prognostic assessment model of RBPs and to evaluate the prognosis of OSCC patients.

Methods

Gene expression data in The Cancer Genome Atlas (TCGA) were analyzed by univariate Cox regression analysis model that established a novel nine RBPs, which were used to build a prognostic risk model. A multivariate Cox proportional regression model and the survival analysis were used to evaluate the prognostic risk model. Moreover, the receive operator curve (ROC) analysis was tested further the efficiency of prognostic risk model based on data from TCGA database and Gene Expression Omnibus (GEO).

Results

Nine RBPs’ signatures (ACO1, G3BP1, NMD3, RNGTT, ZNF385A, SARS, CARS2, YARS and SMAD6) with prognostic value were identified in OSCC patients. Subsequently, the patients were further categorized into high-risk group and low-risk in the overall survival (OS) and disease-free survival (DFS), and external validation dataset. ROC analysis was significant for both the TCGA and GEO. Moreover, GSEA revealed that patients in the high-risk group significantly enriched in many critical pathways correlated with tumorigenesis than the low, including cell cycle, adheres junctions, oocyte meiosis, spliceosome, ERBB signaling pathway and ubiquitin-mediated proteolysis.

Conclusions

Collectively, we developed and validated a novel robust nine RBPs for OSCC prognosis prediction. The nine RBPs could serve as an independent and reliable prognostic biomarker and guiding clinical therapy for OSCC patients.
Literature
1.
go back to reference Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A, Global cancer statistics (2018) GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(2018):394–424PubMed Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A, Global cancer statistics (2018) GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(2018):394–424PubMed
2.
go back to reference Zhao X, Sun S, Zeng X, Cui L (2018) Expression profiles analysis identifies a novel three-mRNA signature to predict overall survival in oral squamous cell carcinoma. Am J Cancer Res 8:450–461PubMedPubMedCentral Zhao X, Sun S, Zeng X, Cui L (2018) Expression profiles analysis identifies a novel three-mRNA signature to predict overall survival in oral squamous cell carcinoma. Am J Cancer Res 8:450–461PubMedPubMedCentral
3.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359-386PubMed Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359-386PubMed
4.
go back to reference Corley M, Burns MC, Yeo GW (2020) How RNA-binding proteins interact with RNA: molecules and mechanisms. Mol Cell 78:9–29PubMedPubMedCentral Corley M, Burns MC, Yeo GW (2020) How RNA-binding proteins interact with RNA: molecules and mechanisms. Mol Cell 78:9–29PubMedPubMedCentral
5.
go back to reference Hentze MW, Castello A, Schwarzl T, Preiss T (2018) A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol 19:327–341PubMed Hentze MW, Castello A, Schwarzl T, Preiss T (2018) A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol 19:327–341PubMed
6.
go back to reference Qin H, Ni H, Liu Y, Yuan Y, Xi T, Li X, Zheng L (2020) RNA-binding proteins in tumor progression. J Hematol Oncol 13:90PubMedPubMedCentral Qin H, Ni H, Liu Y, Yuan Y, Xi T, Li X, Zheng L (2020) RNA-binding proteins in tumor progression. J Hematol Oncol 13:90PubMedPubMedCentral
7.
go back to reference Chatterji P, Rustgi AK (2018) RNA binding proteins in intestinal epithelial biology and colorectal cancer. Trends Mol Med 24:490–506PubMedPubMedCentral Chatterji P, Rustgi AK (2018) RNA binding proteins in intestinal epithelial biology and colorectal cancer. Trends Mol Med 24:490–506PubMedPubMedCentral
8.
go back to reference Xie M, Ma T, Xue J, Ma H, Sun M, Zhang Z, Liu M, Liu Y, Ju S, Wang Z, De W (2019) The long intergenic non-protein coding RNA 707 promotes proliferation and metastasis of gastric cancer by interacting with mRNA stabilizing protein HuR. Cancer Lett 443:67–79PubMed Xie M, Ma T, Xue J, Ma H, Sun M, Zhang Z, Liu M, Liu Y, Ju S, Wang Z, De W (2019) The long intergenic non-protein coding RNA 707 promotes proliferation and metastasis of gastric cancer by interacting with mRNA stabilizing protein HuR. Cancer Lett 443:67–79PubMed
9.
go back to reference McCullough MJ, Prasad G, Farah CS (2010) Oral mucosal malignancy and potentially malignant lesions: an update on the epidemiology, risk factors, diagnosis and management. Aust Dent J 55(Suppl 1):61–65PubMed McCullough MJ, Prasad G, Farah CS (2010) Oral mucosal malignancy and potentially malignant lesions: an update on the epidemiology, risk factors, diagnosis and management. Aust Dent J 55(Suppl 1):61–65PubMed
10.
go back to reference Kartha VK, Alamoud KA, Sadykov K, Nguyen BC, Laroche F, Feng H, Lee J, Pai SI, Varelas X, Egloff AM, Snyder-Cappione JE, Belkina AC, Bais MV, Monti S, Kukuruzinska MA (2018) Functional and genomic analyses reveal therapeutic potential of targeting β-catenin/CBP activity in head and neck cancer. Genome Med 10:54PubMedPubMedCentral Kartha VK, Alamoud KA, Sadykov K, Nguyen BC, Laroche F, Feng H, Lee J, Pai SI, Varelas X, Egloff AM, Snyder-Cappione JE, Belkina AC, Bais MV, Monti S, Kukuruzinska MA (2018) Functional and genomic analyses reveal therapeutic potential of targeting β-catenin/CBP activity in head and neck cancer. Genome Med 10:54PubMedPubMedCentral
11.
go back to reference Pereira B, Billaud M, Almeida R (2017) RNA-binding proteins in cancer: old players and new actors, trends. Cancer 3:506–528 Pereira B, Billaud M, Almeida R (2017) RNA-binding proteins in cancer: old players and new actors, trends. Cancer 3:506–528
12.
go back to reference Coppin L, Leclerc J, Vincent A, Porchet N, Pigny P (2018) Messenger RNA life-cycle in cancer cells: emerging role of conventional and non-conventional RNA-binding proteins. Int J Mol Sci 19:650PubMedPubMedCentral Coppin L, Leclerc J, Vincent A, Porchet N, Pigny P (2018) Messenger RNA life-cycle in cancer cells: emerging role of conventional and non-conventional RNA-binding proteins. Int J Mol Sci 19:650PubMedPubMedCentral
13.
go back to reference Mucha B, Qie S, Bajpai S, Tarallo V, Diehl JN, Tedeschi F, Zhou G, Gao Z, Flashner S, Klein-Szanto AJ, Hibshoosh H, Masataka S, Chajewski OS, Majsterek I, Pytel D, Hatzoglou M, Der CJ, Nakagawa H, Bass AJ, Wong KK, Fuchs SY, Rustgi AK, Jankowsky E, Diehl JA (2022) Tumor suppressor mediated ubiquitylation of hnRNPK is a barrier to oncogenic translation. Nat Commun 13:6614PubMedPubMedCentral Mucha B, Qie S, Bajpai S, Tarallo V, Diehl JN, Tedeschi F, Zhou G, Gao Z, Flashner S, Klein-Szanto AJ, Hibshoosh H, Masataka S, Chajewski OS, Majsterek I, Pytel D, Hatzoglou M, Der CJ, Nakagawa H, Bass AJ, Wong KK, Fuchs SY, Rustgi AK, Jankowsky E, Diehl JA (2022) Tumor suppressor mediated ubiquitylation of hnRNPK is a barrier to oncogenic translation. Nat Commun 13:6614PubMedPubMedCentral
14.
go back to reference Lu X, Zhong J, Liu L, Zhang W, Zhao S, Chen L, Wei Y, Zhang H, Wu J, Chen W, Ge F (2022) The function and regulatory mechanism of RNA-binding proteins in breast cancer and their future clinical treatment prospects. Front Oncol 12:929037PubMedPubMedCentral Lu X, Zhong J, Liu L, Zhang W, Zhao S, Chen L, Wei Y, Zhang H, Wu J, Chen W, Ge F (2022) The function and regulatory mechanism of RNA-binding proteins in breast cancer and their future clinical treatment prospects. Front Oncol 12:929037PubMedPubMedCentral
15.
go back to reference Evan GI, Vousden KH (2001) Proliferation, cell cycle and apoptosis in cancer. Nature 411:342–348PubMed Evan GI, Vousden KH (2001) Proliferation, cell cycle and apoptosis in cancer. Nature 411:342–348PubMed
16.
go back to reference Syrigos KN, Katirtzoglou N, Kotteas E, Harrington K (2008) Adhesion molecules in lung cancer: implications in the pathogenesis and management. Curr Pharm Des 14:2173–2183PubMed Syrigos KN, Katirtzoglou N, Kotteas E, Harrington K (2008) Adhesion molecules in lung cancer: implications in the pathogenesis and management. Curr Pharm Des 14:2173–2183PubMed
17.
go back to reference Schimmel P, Tao J, Hill J (1998) Aminoacyl tRNA synthetases as targets for new anti-infectives. FASEB J 12:1599–1609PubMed Schimmel P, Tao J, Hill J (1998) Aminoacyl tRNA synthetases as targets for new anti-infectives. FASEB J 12:1599–1609PubMed
18.
go back to reference Nowaczyk MJ, Huang L, Tarnopolsky M, Schwartzentruber J, Majewski J, Bulman DE, Hartley T, Boycott KM (2017) A novel multisystem disease associated with recessive mutations in the tyrosyl-tRNA synthetase (YARS) gene. Am J Med Genet A 173:126–134PubMed Nowaczyk MJ, Huang L, Tarnopolsky M, Schwartzentruber J, Majewski J, Bulman DE, Hartley T, Boycott KM (2017) A novel multisystem disease associated with recessive mutations in the tyrosyl-tRNA synthetase (YARS) gene. Am J Med Genet A 173:126–134PubMed
19.
20.
go back to reference Fuchs SA, Schene IF, Kok G, Jansen JM, Nikkels P, van Gassen K, Terheggen-Lagro S, van der Crabben SN, Hoeks SE, Niers L, Wolf NI, de Vries MC, Koolen DA, Houwen R, Mulder MF, van Hasselt PM (2019) Aminoacyl-tRNA synthetase deficiencies in search of common themes. Genet Med 21:319–330PubMed Fuchs SA, Schene IF, Kok G, Jansen JM, Nikkels P, van Gassen K, Terheggen-Lagro S, van der Crabben SN, Hoeks SE, Niers L, Wolf NI, de Vries MC, Koolen DA, Houwen R, Mulder MF, van Hasselt PM (2019) Aminoacyl-tRNA synthetase deficiencies in search of common themes. Genet Med 21:319–330PubMed
21.
go back to reference Zhang C, Lin X, Zhao Q, Wang Y, Jiang F, Ji C, Li Y, Gao J, Li J, Shen L (2020) YARS as an oncogenic protein that promotes gastric cancer progression through activating PI3K-Akt signaling. J Cancer Res Clin Oncol 146:329–342PubMedPubMedCentral Zhang C, Lin X, Zhao Q, Wang Y, Jiang F, Ji C, Li Y, Gao J, Li J, Shen L (2020) YARS as an oncogenic protein that promotes gastric cancer progression through activating PI3K-Akt signaling. J Cancer Res Clin Oncol 146:329–342PubMedPubMedCentral
22.
go back to reference Hsu CW, Chang KP, Huang Y, Liu HP, Hsueh PC, Gu PW, Yen WC, Wu CC (2019) Proteomic profiling of paired interstitial fluids reveals dysregulated pathways and salivary NID1 as a biomarker of oral cavity squamous cell carcinoma. Mol Cell Proteomics 18:1939–1949PubMedPubMedCentral Hsu CW, Chang KP, Huang Y, Liu HP, Hsueh PC, Gu PW, Yen WC, Wu CC (2019) Proteomic profiling of paired interstitial fluids reveals dysregulated pathways and salivary NID1 as a biomarker of oral cavity squamous cell carcinoma. Mol Cell Proteomics 18:1939–1949PubMedPubMedCentral
23.
go back to reference Fukui H, Hanaoka R, Kawahara A (2009) Noncanonical activity of seryl-tRNA synthetase is involved in vascular development. Circ Res 104:1253–1259PubMed Fukui H, Hanaoka R, Kawahara A (2009) Noncanonical activity of seryl-tRNA synthetase is involved in vascular development. Circ Res 104:1253–1259PubMed
24.
go back to reference Herzog W, Müller K, Huisken J, Stainier DY (2009) Genetic evidence for a noncanonical function of seryl-tRNA synthetase in vascular development. Circ Res 104:1260–1266PubMedPubMedCentral Herzog W, Müller K, Huisken J, Stainier DY (2009) Genetic evidence for a noncanonical function of seryl-tRNA synthetase in vascular development. Circ Res 104:1260–1266PubMedPubMedCentral
25.
go back to reference Shi Y, Xu X, Zhang Q, Fu G, Mo Z, Wang GS, Kishi S, Yang XL (2014) tRNA synthetase counteracts c-Myc to develop functional vasculature. Elife 3:e02349PubMedPubMedCentral Shi Y, Xu X, Zhang Q, Fu G, Mo Z, Wang GS, Kishi S, Yang XL (2014) tRNA synthetase counteracts c-Myc to develop functional vasculature. Elife 3:e02349PubMedPubMedCentral
26.
go back to reference Zou G, Zhang X, Wang L, Li X, Xie T, Zhao J, Yan J, Wang L, Ye H, Jiao S, Xiang R, Shi Y (2020) Herb-sourced emodin inhibits angiogenesis of breast cancer by targeting VEGFA transcription. Theranostics 10:6839–6853PubMedPubMedCentral Zou G, Zhang X, Wang L, Li X, Xie T, Zhao J, Yan J, Wang L, Ye H, Jiao S, Xiang R, Shi Y (2020) Herb-sourced emodin inhibits angiogenesis of breast cancer by targeting VEGFA transcription. Theranostics 10:6839–6853PubMedPubMedCentral
27.
go back to reference Panse VG, Johnson AW (2010) Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem Sci 35:260–266PubMedPubMedCentral Panse VG, Johnson AW (2010) Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem Sci 35:260–266PubMedPubMedCentral
28.
go back to reference Sengupta J, Bussiere C, Pallesen J, West M, Johnson AW, Frank J (2010) Characterization of the nuclear export adaptor protein Nmd3 in association with the 60S ribosomal subunit. J Cell Biol 189:1079–1086PubMedPubMedCentral Sengupta J, Bussiere C, Pallesen J, West M, Johnson AW, Frank J (2010) Characterization of the nuclear export adaptor protein Nmd3 in association with the 60S ribosomal subunit. J Cell Biol 189:1079–1086PubMedPubMedCentral
29.
go back to reference Bai B, Moore HM, Laiho M (2013) CRM1 and its ribosome export adaptor NMD3 localize to the nucleolus and affect rRNA synthesis. Nucleus 4:315–325PubMedPubMedCentral Bai B, Moore HM, Laiho M (2013) CRM1 and its ribosome export adaptor NMD3 localize to the nucleolus and affect rRNA synthesis. Nucleus 4:315–325PubMedPubMedCentral
30.
go back to reference Chen C, Wang B (2018) Brucea javanica oil emulsion alleviates cachexia induced by Lewis lung cancer cells in mice. J Drug Target 26:222–230PubMed Chen C, Wang B (2018) Brucea javanica oil emulsion alleviates cachexia induced by Lewis lung cancer cells in mice. J Drug Target 26:222–230PubMed
31.
go back to reference Ge Y, Jin J, Li J, Ye M, Jin X (2022) The roles of G3BP1 in human diseases (review). Gene 821:146294PubMed Ge Y, Jin J, Li J, Ye M, Jin X (2022) The roles of G3BP1 in human diseases (review). Gene 821:146294PubMed
32.
go back to reference Zhang LN, Zhao L, Yan XL, Huang YH (2019) Loss of G3BP1 suppresses proliferation, migration, and invasion of esophageal cancer cells via Wnt/β-catenin and PI3K/AKT signaling pathways. J Cell Physiol 234:20469–20484PubMed Zhang LN, Zhao L, Yan XL, Huang YH (2019) Loss of G3BP1 suppresses proliferation, migration, and invasion of esophageal cancer cells via Wnt/β-catenin and PI3K/AKT signaling pathways. J Cell Physiol 234:20469–20484PubMed
33.
go back to reference Hu X, Xia K, Xiong H, Su T (2021) G3BP1 may serve as a potential biomarker of proliferation, apoptosis, and prognosis in oral squamous cell carcinoma. J Oral Pathol Med 50:995–1004PubMed Hu X, Xia K, Xiong H, Su T (2021) G3BP1 may serve as a potential biomarker of proliferation, apoptosis, and prognosis in oral squamous cell carcinoma. J Oral Pathol Med 50:995–1004PubMed
34.
go back to reference Hata A, Lagna G, Massagué J, Hemmati-Brivanlou A (1998) Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 12:186–197PubMedPubMedCentral Hata A, Lagna G, Massagué J, Hemmati-Brivanlou A (1998) Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 12:186–197PubMedPubMedCentral
35.
go back to reference Verschueren K, Huylebroeck D (1999) Remarkable versatility of Smad proteins in the nucleus of transforming growth factor-beta activated cells. Cytokine Growth Factor Rev 10:187–199PubMed Verschueren K, Huylebroeck D (1999) Remarkable versatility of Smad proteins in the nucleus of transforming growth factor-beta activated cells. Cytokine Growth Factor Rev 10:187–199PubMed
36.
go back to reference Miyazono K (2000) TGF-beta signaling by Smad proteins. Cytokine Growth Factor Rev 11:15–22PubMed Miyazono K (2000) TGF-beta signaling by Smad proteins. Cytokine Growth Factor Rev 11:15–22PubMed
37.
go back to reference Park JE, Park JS, Jang SY, Park SH, Kim JW, Ki CS, Kim DK (2019) A novel SMAD6 variant in a patient with severely calcified bicuspid aortic valve and thoracic aortic aneurysm. Mol Genet Genomic Med 7:e620PubMedPubMedCentral Park JE, Park JS, Jang SY, Park SH, Kim JW, Ki CS, Kim DK (2019) A novel SMAD6 variant in a patient with severely calcified bicuspid aortic valve and thoracic aortic aneurysm. Mol Genet Genomic Med 7:e620PubMedPubMedCentral
38.
go back to reference Jeon HS, Dracheva T, Yang SH, Meerzaman D, Fukuoka J, Shakoori A, Shilo K, Travis WD, Jen J (2008) SMAD6 contributes to patient survival in non-small cell lung cancer and its knockdown reestablishes TGF-beta homeostasis in lung cancer cells. Cancer Res 68:9686–9692PubMedPubMedCentral Jeon HS, Dracheva T, Yang SH, Meerzaman D, Fukuoka J, Shakoori A, Shilo K, Travis WD, Jen J (2008) SMAD6 contributes to patient survival in non-small cell lung cancer and its knockdown reestablishes TGF-beta homeostasis in lung cancer cells. Cancer Res 68:9686–9692PubMedPubMedCentral
39.
go back to reference Choi KC, Lee YS, Lim S, Choi HK, Lee CH, Lee EK, Hong S, Kim IH, Kim SJ, Park SH (2006) Smad6 negatively regulates interleukin 1-receptor-Toll-like receptor signaling through direct interaction with the adaptor Pellino-1. Nat Immunol 7:1057–1065PubMed Choi KC, Lee YS, Lim S, Choi HK, Lee CH, Lee EK, Hong S, Kim IH, Kim SJ, Park SH (2006) Smad6 negatively regulates interleukin 1-receptor-Toll-like receptor signaling through direct interaction with the adaptor Pellino-1. Nat Immunol 7:1057–1065PubMed
40.
go back to reference Lönn P, Morén A, Raja E, Dahl M, Moustakas A (2009) Regulating the stability of TGFbeta receptors and Smads. Cell Res 19:21–35PubMed Lönn P, Morén A, Raja E, Dahl M, Moustakas A (2009) Regulating the stability of TGFbeta receptors and Smads. Cell Res 19:21–35PubMed
41.
go back to reference Tan HL, Glen E, Töpf A, Hall D, O’Sullivan JJ, Sneddon L, Wren C, Avery P, Lewis RJ, ten Dijke P, Arthur HM, Goodship JA, Keavney BD (2012) Nonsynonymous variants in the SMAD6 gene predispose to congenital cardiovascular malformation. Hum Mutat 33:720–727PubMedPubMedCentral Tan HL, Glen E, Töpf A, Hall D, O’Sullivan JJ, Sneddon L, Wren C, Avery P, Lewis RJ, ten Dijke P, Arthur HM, Goodship JA, Keavney BD (2012) Nonsynonymous variants in the SMAD6 gene predispose to congenital cardiovascular malformation. Hum Mutat 33:720–727PubMedPubMedCentral
42.
go back to reference Lu W, Sun J, Zhou H, Wang F, Zhao C, Li K, Fan C, Ding G, Wang J (2020) HNF1B inhibits cell proliferation via repression of SMAD6 expression in prostate cancer. J Cell Mol Med 24:14539–14548PubMedPubMedCentral Lu W, Sun J, Zhou H, Wang F, Zhao C, Li K, Fan C, Ding G, Wang J (2020) HNF1B inhibits cell proliferation via repression of SMAD6 expression in prostate cancer. J Cell Mol Med 24:14539–14548PubMedPubMedCentral
43.
go back to reference Bayat Z, Ghaemi Z, Behmanesh M, Soltani BM (2021) Hsa-miR-186-5p regulates TGFβ signaling pathway through expression suppression of SMAD6 and SMAD7 genes in colorectal cancer. Biol Chem 402:469–480PubMed Bayat Z, Ghaemi Z, Behmanesh M, Soltani BM (2021) Hsa-miR-186-5p regulates TGFβ signaling pathway through expression suppression of SMAD6 and SMAD7 genes in colorectal cancer. Biol Chem 402:469–480PubMed
44.
go back to reference Liu L, Zhang C, Wang J, Liu X, Qu H, Zhang G, Liang T, Wang J, Zhang J (2021) A high level of lncFGD5-AS1 inhibits epithelial-to-Mesenchymal transition by regulating the miR-196a-5p/SMAD6/BMP axis in gastric Cancer. BMC Cancer 21:453PubMedPubMedCentral Liu L, Zhang C, Wang J, Liu X, Qu H, Zhang G, Liang T, Wang J, Zhang J (2021) A high level of lncFGD5-AS1 inhibits epithelial-to-Mesenchymal transition by regulating the miR-196a-5p/SMAD6/BMP axis in gastric Cancer. BMC Cancer 21:453PubMedPubMedCentral
45.
go back to reference Park JH, Ameri AH, Dempsey KE, Conrad DN, Kem M, Mino-Kenudson M, Demehri S (2021) Nuclear IL-33/SMAD signaling axis promotes cancer development in chronic inflammation. EMBO J 40:e106151PubMedPubMedCentral Park JH, Ameri AH, Dempsey KE, Conrad DN, Kem M, Mino-Kenudson M, Demehri S (2021) Nuclear IL-33/SMAD signaling axis promotes cancer development in chronic inflammation. EMBO J 40:e106151PubMedPubMedCentral
46.
go back to reference Mi W, Zheng Z, Lu JD, Duan SQ, Zhang J, Zhang HQ, Ding YX, Yin J, Cao F, Zhang J, Li F (2022) KLF16 promotes pancreatic adenocarcinoma cell proliferation and migration by positively regulating SMAD6. World J Gastrointest Oncol 14:2157–2169PubMedPubMedCentral Mi W, Zheng Z, Lu JD, Duan SQ, Zhang J, Zhang HQ, Ding YX, Yin J, Cao F, Zhang J, Li F (2022) KLF16 promotes pancreatic adenocarcinoma cell proliferation and migration by positively regulating SMAD6. World J Gastrointest Oncol 14:2157–2169PubMedPubMedCentral
47.
go back to reference Miyazono K (2000) Positive and negative regulation of TGF-beta signaling. J Cell Sci 113(Pt 7):1101–1109PubMed Miyazono K (2000) Positive and negative regulation of TGF-beta signaling. J Cell Sci 113(Pt 7):1101–1109PubMed
48.
go back to reference Osawa H, Nakajima M, Kato H, Fukuchi M, Kuwano H (2004) Prognostic value of the expression of Smad6 and Smad7, as inhibitory Smads of the TGF-beta superfamily, in esophageal squamous cell carcinoma. Anticancer Res 24:3703–3709PubMed Osawa H, Nakajima M, Kato H, Fukuchi M, Kuwano H (2004) Prognostic value of the expression of Smad6 and Smad7, as inhibitory Smads of the TGF-beta superfamily, in esophageal squamous cell carcinoma. Anticancer Res 24:3703–3709PubMed
49.
go back to reference Mangone FR, Walder F, Maistro S, Pasini FS, Lehn CN, Carvalho MB, Brentani MM, Snitcovsky I, Federico MH (2010) Smad2 and Smad6 as predictors of overall survival in oral squamous cell carcinoma patients. Mol Cancer 9:106PubMedPubMedCentral Mangone FR, Walder F, Maistro S, Pasini FS, Lehn CN, Carvalho MB, Brentani MM, Snitcovsky I, Federico MH (2010) Smad2 and Smad6 as predictors of overall survival in oral squamous cell carcinoma patients. Mol Cancer 9:106PubMedPubMedCentral
Metadata
Title
A novel and independent survival prognostic model for OSCC: the functions and prognostic values of RNA-binding proteins
Authors
Shanshan Wang
Shuang Liu
Yaomin Zhu
Baorong Zhang
Yongtao Yang
Limei Li
Yingying Sun
Long Zhang
Lina Fan
Xuegang Hu
Chunyu Huang
Publication date
01-09-2023
Publisher
Springer Berlin Heidelberg
Published in
European Archives of Oto-Rhino-Laryngology / Issue 1/2024
Print ISSN: 0937-4477
Electronic ISSN: 1434-4726
DOI
https://doi.org/10.1007/s00405-023-08200-9

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