Skip to main content
Top
Published in: Tumor Biology 9/2016

01-09-2016 | Review

Complex roles of NRAGE on tumor

Authors: Ge Zhang, Huandi Zhou, Xiaoying Xue

Published in: Tumor Biology | Issue 9/2016

Login to get access

Abstract

NRAGE, also known as Dlxin-1or MAGE-D1, is a member of type II melanoma-associated antigen (MAGE) and plays an essential role in life activities, including differentiation, apoptosis, and cell cycle. Studies increasingly found that NRAGE is closely related to the tumor events, such as tumor occurrence, invasion, and metastasis. However, complex and contradictory functions of NRAGE in different circumstances are observed, suggesting that NRAGE is unique from other MAGE gene family members. This review summarizes recent findings concerning the structure and biological functions of NRAGE, which may provide a basis for a more comprehensive understanding of and further research on NRAGE.
Literature
1.
go back to reference Chomez P, De Backer O, Bertrand M, De Plaen E, Boon T, Lucas S. An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res. 2001;61(14):5544–51.PubMed Chomez P, De Backer O, Bertrand M, De Plaen E, Boon T, Lucas S. An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res. 2001;61(14):5544–51.PubMed
2.
go back to reference Clotman F, De Backer O, De Plaen E, Boon T, Picard J. Cell- and stage-specific expression of mage genes during mouse spermatogenesis. Mamm Genome. 2000;11(8):696–9.CrossRefPubMed Clotman F, De Backer O, De Plaen E, Boon T, Picard J. Cell- and stage-specific expression of mage genes during mouse spermatogenesis. Mamm Genome. 2000;11(8):696–9.CrossRefPubMed
3.
go back to reference Lucas S, Brasseur F, Boon T. A new MAGE gene with ubiquitous expression does not code for known MAGE antigens recognized by T cells. Cancer Res. 1999;59(16):4100–3.PubMed Lucas S, Brasseur F, Boon T. A new MAGE gene with ubiquitous expression does not code for known MAGE antigens recognized by T cells. Cancer Res. 1999;59(16):4100–3.PubMed
4.
go back to reference Barker PA, Salehi A. The MAGE proteins: emerging roles in cell cycle progression, apoptosis, and neurogenetic disease. J Neurosci Res. 2002;67(6):705–12.CrossRefPubMed Barker PA, Salehi A. The MAGE proteins: emerging roles in cell cycle progression, apoptosis, and neurogenetic disease. J Neurosci Res. 2002;67(6):705–12.CrossRefPubMed
5.
go back to reference Hennuy B, Reiter E, Cornet A, Bruyninx M, Daukandt M, Houssa P, et al. A novel messenger ribonucleic acid homologous to human MAGE-D is strongly expressed in rat Sertoli cells and weakly in Leydig cells and is regulated by Follitropin, lutropin, and prolactin1. Endocrinology. 2000;141(10):3821–31.PubMed Hennuy B, Reiter E, Cornet A, Bruyninx M, Daukandt M, Houssa P, et al. A novel messenger ribonucleic acid homologous to human MAGE-D is strongly expressed in rat Sertoli cells and weakly in Leydig cells and is regulated by Follitropin, lutropin, and prolactin1. Endocrinology. 2000;141(10):3821–31.PubMed
6.
go back to reference Põld M, Zhou J, Chen GL, Hall JM, Vescio RA, Berenson JR. Identification of a new, unorthodox member of the MAGE gene family. Genomics. 1999;59(2):161–7.CrossRefPubMed Põld M, Zhou J, Chen GL, Hall JM, Vescio RA, Berenson JR. Identification of a new, unorthodox member of the MAGE gene family. Genomics. 1999;59(2):161–7.CrossRefPubMed
7.
go back to reference Masuda Y, Sasaki A, Shibuya H, Ueno N, Ikeda K, Watanabe K. Dlxin-1, a novel protein that binds Dlx5 and regulates its transcriptional function. J Biol Chem. 2001;276(7):5331–8.CrossRefPubMed Masuda Y, Sasaki A, Shibuya H, Ueno N, Ikeda K, Watanabe K. Dlxin-1, a novel protein that binds Dlx5 and regulates its transcriptional function. J Biol Chem. 2001;276(7):5331–8.CrossRefPubMed
8.
go back to reference Salehi AH, Roux PP, Kubu CJ, Zeindler C, Bhakar A, Tannis LL, et al. NRAGE, a novel MAGE protein, interacts with the p75 neurotrophin receptor and facilitates nerve growth factor-dependent apoptosis. Neuron. 2000;27(2):279–88.CrossRefPubMed Salehi AH, Roux PP, Kubu CJ, Zeindler C, Bhakar A, Tannis LL, et al. NRAGE, a novel MAGE protein, interacts with the p75 neurotrophin receptor and facilitates nerve growth factor-dependent apoptosis. Neuron. 2000;27(2):279–88.CrossRefPubMed
9.
go back to reference Rochira JA, Matluk NN, Adams TL, Karaczyn AA, Oxburgh L, Hess ST, et al. A small peptide modeled after the NRAGE repeat domain inhibits XIAP-TAB1-TAK1 signaling for NF-kB activation and apoptosis in P19 cells. PLoS ONE. 2011;6(7), e20659.CrossRefPubMedPubMedCentral Rochira JA, Matluk NN, Adams TL, Karaczyn AA, Oxburgh L, Hess ST, et al. A small peptide modeled after the NRAGE repeat domain inhibits XIAP-TAB1-TAK1 signaling for NF-kB activation and apoptosis in P19 cells. PLoS ONE. 2011;6(7), e20659.CrossRefPubMedPubMedCentral
10.
go back to reference Matluk N, Rochira JA, Karaczyn A, Adams T, Verdi JM. A role for NRAGE in NF-kB activation through the non-canonical BMP pathway. BMC Biol. 2010;8(1):7.CrossRefPubMedPubMedCentral Matluk N, Rochira JA, Karaczyn A, Adams T, Verdi JM. A role for NRAGE in NF-kB activation through the non-canonical BMP pathway. BMC Biol. 2010;8(1):7.CrossRefPubMedPubMedCentral
11.
go back to reference Rochira JA, Cowling RA, Himmelfarb JS, Adams TL, Verdi JM. Mapping of NRAGE domains reveals clues to cell viability in BMP signaling. Apoptosis. 2010;15(1):63–70.CrossRefPubMedPubMedCentral Rochira JA, Cowling RA, Himmelfarb JS, Adams TL, Verdi JM. Mapping of NRAGE domains reveals clues to cell viability in BMP signaling. Apoptosis. 2010;15(1):63–70.CrossRefPubMedPubMedCentral
12.
go back to reference Lebrun-Julien F, Bertrand MJ, De Backer O, Stellwagen D, Morales CR, Di Polo A, et al. ProNGF induces TNF -dependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway. Proc Nat Acad Sci. 2010;107(8):3817–22.CrossRefPubMedPubMedCentral Lebrun-Julien F, Bertrand MJ, De Backer O, Stellwagen D, Morales CR, Di Polo A, et al. ProNGF induces TNF -dependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway. Proc Nat Acad Sci. 2010;107(8):3817–22.CrossRefPubMedPubMedCentral
13.
go back to reference Nikopoulos GN, Martins JF, Adams TL, Karaczyn A, Adams D, Vary C, et al. NRAGE: a potential rheostat during branching morphogenesis. Mech Dev. 2009;126(5-6):337–49.CrossRefPubMedPubMedCentral Nikopoulos GN, Martins JF, Adams TL, Karaczyn A, Adams D, Vary C, et al. NRAGE: a potential rheostat during branching morphogenesis. Mech Dev. 2009;126(5-6):337–49.CrossRefPubMedPubMedCentral
14.
go back to reference Bertrand MJM, Kenchappa RS, Andrieu D, Leclercq-Smekens M, Nguyen HNT, Carter BD, et al. NRAGE, a p75NTR adaptor protein, is required for developmental apoptosis in vivo. Cell Death Differ. 2008;15(12):1921–9.CrossRefPubMedPubMedCentral Bertrand MJM, Kenchappa RS, Andrieu D, Leclercq-Smekens M, Nguyen HNT, Carter BD, et al. NRAGE, a p75NTR adaptor protein, is required for developmental apoptosis in vivo. Cell Death Differ. 2008;15(12):1921–9.CrossRefPubMedPubMedCentral
15.
go back to reference Di Certo MG, Corbi N, Bruno T, Iezzi S, De Nicola F, Desantis A, et al. NRAGE associates with the anti-apoptotic factor Che-1 and regulates its degradation to induce cell death. J Cell Sci. 2007;120(11):1852–8.CrossRefPubMed Di Certo MG, Corbi N, Bruno T, Iezzi S, De Nicola F, Desantis A, et al. NRAGE associates with the anti-apoptotic factor Che-1 and regulates its degradation to induce cell death. J Cell Sci. 2007;120(11):1852–8.CrossRefPubMed
16.
go back to reference Salehi AH, Morris SJ, Ho W, Dickson KM, Doucet G, Milutinovic S, et al. AEG3482 is an antiapoptotic compound that inhibits Jun kinase activity and cell death through induced expression of heat shock protein 70. Chem Biol. 2006;13(2):213–23.CrossRefPubMed Salehi AH, Morris SJ, Ho W, Dickson KM, Doucet G, Milutinovic S, et al. AEG3482 is an antiapoptotic compound that inhibits Jun kinase activity and cell death through induced expression of heat shock protein 70. Chem Biol. 2006;13(2):213–23.CrossRefPubMed
17.
go back to reference Kendall SE, Battelli C, Irwin S, Mitchell JG, Glackin CA, Verdi JM. NRAGE mediates p38 activation and neural progenitor apoptosis via the bone morphogenetic protein signaling cascade. Mol Cell Biol. 2005;25(17):7711–24.CrossRefPubMedPubMedCentral Kendall SE, Battelli C, Irwin S, Mitchell JG, Glackin CA, Verdi JM. NRAGE mediates p38 activation and neural progenitor apoptosis via the bone morphogenetic protein signaling cascade. Mol Cell Biol. 2005;25(17):7711–24.CrossRefPubMedPubMedCentral
18.
go back to reference Williams ME, Strickland P, Watanabe K, Hinck L. UNC5H1 induces apoptosis via its juxtamembrane region through an interaction with NRAGE. J Biol Chem. 2003;278(19):17483–90.CrossRefPubMed Williams ME, Strickland P, Watanabe K, Hinck L. UNC5H1 induces apoptosis via its juxtamembrane region through an interaction with NRAGE. J Biol Chem. 2003;278(19):17483–90.CrossRefPubMed
19.
go back to reference Salehi AH, Xanthoudakis S, Barker PA. NRAGE, a p75 neurotrophin receptor-interacting protein, induces caspase activation and cell death through a JNK-dependent mitochondrial pathway. J Biol Chem. 2002;277(50):48043–50.CrossRefPubMed Salehi AH, Xanthoudakis S, Barker PA. NRAGE, a p75 neurotrophin receptor-interacting protein, induces caspase activation and cell death through a JNK-dependent mitochondrial pathway. J Biol Chem. 2002;277(50):48043–50.CrossRefPubMed
20.
go back to reference Jordan BWM, Dinev D, LeMellay V, Troppmair J, Gotz R, Wixler L, et al. Neurotrophin receptor-interacting mage homologue is an inducible inhibitor of apoptosis protein-interacting protein that augments cell death. J Biol Chem. 2001;276(43):39985–9.CrossRefPubMed Jordan BWM, Dinev D, LeMellay V, Troppmair J, Gotz R, Wixler L, et al. Neurotrophin receptor-interacting mage homologue is an inducible inhibitor of apoptosis protein-interacting protein that augments cell death. J Biol Chem. 2001;276(43):39985–9.CrossRefPubMed
21.
go back to reference Teuber J, Mueller B, Fukabori R, Lang D, Albrecht A, Stork O. The ubiquitin ligase Praja1 reduces NRAGE expression and inhibits neuronal differentiation of PC12 cells. PLoS ONE. 2013;8(5), e63067.CrossRefPubMedPubMedCentral Teuber J, Mueller B, Fukabori R, Lang D, Albrecht A, Stork O. The ubiquitin ligase Praja1 reduces NRAGE expression and inhibits neuronal differentiation of PC12 cells. PLoS ONE. 2013;8(5), e63067.CrossRefPubMedPubMedCentral
22.
go back to reference Nguyen TH, Bertrand MJ, Sterpin C, Achouri Y, De Backer OR. Maged1, a new regulator of skeletal myogenic differentiation and muscle regeneration. BMC Cell Biol. 2010;11(1):57.CrossRefPubMedPubMedCentral Nguyen TH, Bertrand MJ, Sterpin C, Achouri Y, De Backer OR. Maged1, a new regulator of skeletal myogenic differentiation and muscle regeneration. BMC Cell Biol. 2010;11(1):57.CrossRefPubMedPubMedCentral
23.
go back to reference Feng Z, Li K, Liu M, Wen C. NRAGE is a negative regulator of nerve growth factor-stimulated neurite outgrowth in PC12 cells mediated through TrkA-ERK signaling. J Neurosci Res 2010: NA-NA. Feng Z, Li K, Liu M, Wen C. NRAGE is a negative regulator of nerve growth factor-stimulated neurite outgrowth in PC12 cells mediated through TrkA-ERK signaling. J Neurosci Res 2010: NA-NA.
24.
go back to reference Kuwajima T. Necdin promotes GABAergic neuron differentiation in cooperation with Dlx homeodomain proteins. J Neurosci. 2006;26(20):5383–92.CrossRefPubMed Kuwajima T. Necdin promotes GABAergic neuron differentiation in cooperation with Dlx homeodomain proteins. J Neurosci. 2006;26(20):5383–92.CrossRefPubMed
25.
go back to reference Bertrand M, Huijbers I, Chomez P, De Backer O. Comparative expression analysis of theMAGED genes during embryogenesis and brain development. Dev Dyn. 2004;230(2):325–34.CrossRefPubMed Bertrand M, Huijbers I, Chomez P, De Backer O. Comparative expression analysis of theMAGED genes during embryogenesis and brain development. Dev Dyn. 2004;230(2):325–34.CrossRefPubMed
26.
go back to reference Kuwajima T. Necdin interacts with the Msx2 homeodomain protein via MAGE-D1 to promote myogenic differentiation of C2C12 cells. J Biol Chem. 2004;279(39):40484–93.CrossRefPubMed Kuwajima T. Necdin interacts with the Msx2 homeodomain protein via MAGE-D1 to promote myogenic differentiation of C2C12 cells. J Biol Chem. 2004;279(39):40484–93.CrossRefPubMed
27.
go back to reference Sasaki A. A RING finger protein Praja1 regulates Dlx5-dependent transcription through its ubiquitin ligase activity for the Dlx/Msx-interacting MAGE/necdin family protein, dlxin-1. J Biol Chem. 2002;277(25):22541–6.CrossRefPubMed Sasaki A. A RING finger protein Praja1 regulates Dlx5-dependent transcription through its ubiquitin ligase activity for the Dlx/Msx-interacting MAGE/necdin family protein, dlxin-1. J Biol Chem. 2002;277(25):22541–6.CrossRefPubMed
28.
go back to reference Wang X, Tang J, Xing L, Shi G, Ruan H, Gu X, et al. Interaction of MAGED1 with nuclear receptors affects circadian clock function. EMBO J. 2010;29(8):1389–400.CrossRefPubMedPubMedCentral Wang X, Tang J, Xing L, Shi G, Ruan H, Gu X, et al. Interaction of MAGED1 with nuclear receptors affects circadian clock function. EMBO J. 2010;29(8):1389–400.CrossRefPubMedPubMedCentral
29.
go back to reference Mouri A, Sasaki A, Watanabe K, Sogawa C, Kitayama S, Mamiya T, et al. MAGE-D1 regulates expression of depression-like behavior through serotonin transporter ubiquitylation. J Neurosci. 2012;32(13):4562–80.CrossRefPubMed Mouri A, Sasaki A, Watanabe K, Sogawa C, Kitayama S, Mamiya T, et al. MAGE-D1 regulates expression of depression-like behavior through serotonin transporter ubiquitylation. J Neurosci. 2012;32(13):4562–80.CrossRefPubMed
30.
go back to reference Dombret C, Nguyen T, Schakman O, Michaud JL, Hardin-Pouzet H, Bertrand MJM, et al. Loss of Maged1 results in obesity, deficits of social interactions, impaired sexual behavior and severe alteration of mature oxytocin production in the hypothalamus. Hum Mol Genet. 2012;21(21):4703–17.CrossRefPubMed Dombret C, Nguyen T, Schakman O, Michaud JL, Hardin-Pouzet H, Bertrand MJM, et al. Loss of Maged1 results in obesity, deficits of social interactions, impaired sexual behavior and severe alteration of mature oxytocin production in the hypothalamus. Hum Mol Genet. 2012;21(21):4703–17.CrossRefPubMed
31.
go back to reference Silva MMCD, Gil LHVG, Marques Junior ETDA, Calzavara-Silva CE. Potential biomarkers for the clinical prognosis of severe dengue. Memórias do Instituto Oswaldo Cruz. 2013;108(6):755–62.CrossRefPubMedPubMedCentral Silva MMCD, Gil LHVG, Marques Junior ETDA, Calzavara-Silva CE. Potential biomarkers for the clinical prognosis of severe dengue. Memórias do Instituto Oswaldo Cruz. 2013;108(6):755–62.CrossRefPubMedPubMedCentral
32.
go back to reference Yang J, Lai B, Xu A, Liu Y, Li X, Zhao Y, et al. Maged1 co-interacting with CREB through a hexapeptide repeat domain regulates learning and memory in mice. Mol Neurobiol. 2015;51(1):8–18.CrossRefPubMed Yang J, Lai B, Xu A, Liu Y, Li X, Zhao Y, et al. Maged1 co-interacting with CREB through a hexapeptide repeat domain regulates learning and memory in mice. Mol Neurobiol. 2015;51(1):8–18.CrossRefPubMed
33.
go back to reference Shen W, Xue Q, Zhu J, Hu B, Zhang Y, Wu Y, et al. Inhibition of adenovirus-mediated human MAGE-D1 on angiogenesis in vitro and in vivo. Mol Cell Biochem. 2007;300(1-2):89–99.CrossRefPubMed Shen W, Xue Q, Zhu J, Hu B, Zhang Y, Wu Y, et al. Inhibition of adenovirus-mediated human MAGE-D1 on angiogenesis in vitro and in vivo. Mol Cell Biochem. 2007;300(1-2):89–99.CrossRefPubMed
34.
go back to reference Kang J, Chung KC. The F-box protein FBXO7 positively regulates bone morphogenetic protein-mediated signaling through Lys-63-specific ubiquitination of neurotrophin receptor-interacting MAGE (NRAGE). Cell Mol Life Sci. 2015;72(1):181–95.CrossRefPubMed Kang J, Chung KC. The F-box protein FBXO7 positively regulates bone morphogenetic protein-mediated signaling through Lys-63-specific ubiquitination of neurotrophin receptor-interacting MAGE (NRAGE). Cell Mol Life Sci. 2015;72(1):181–95.CrossRefPubMed
35.
go back to reference Yang Q, Ou C, Liu M, Xiao W, Wen C, Sun F. NRAGE promotes cell proliferation by stabilizing PCNA in a ubiquitin-proteasome pathway in esophageal carcinomas. Carcinogenesis. 2014;35(7):1643–51.CrossRefPubMed Yang Q, Ou C, Liu M, Xiao W, Wen C, Sun F. NRAGE promotes cell proliferation by stabilizing PCNA in a ubiquitin-proteasome pathway in esophageal carcinomas. Carcinogenesis. 2014;35(7):1643–51.CrossRefPubMed
36.
go back to reference Lee D, Lee GK, Yoon K, Lee JS. Pathway-based analysis using genome-wide association data from a Korean non-small cell lung cancer study. PloS one. 2013;8(6), e65396.CrossRefPubMedPubMedCentral Lee D, Lee GK, Yoon K, Lee JS. Pathway-based analysis using genome-wide association data from a Korean non-small cell lung cancer study. PloS one. 2013;8(6), e65396.CrossRefPubMedPubMedCentral
37.
go back to reference Lai S, Xue B, Yang Y, Zhao L, Chu C, Hao J, et al. Ror2-Src signaling in metastasis of mouse melanoma cells is inhibited by NRAGE. Cancer Genetics. 2012;205(11):552–62.CrossRefPubMed Lai S, Xue B, Yang Y, Zhao L, Chu C, Hao J, et al. Ror2-Src signaling in metastasis of mouse melanoma cells is inhibited by NRAGE. Cancer Genetics. 2012;205(11):552–62.CrossRefPubMed
38.
go back to reference Kumar S, Park SH, Cieply B, Schupp J, Killiam E, Zhang F, et al. A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol Cell Biol. 2011;31(19):4036–51.CrossRefPubMedPubMedCentral Kumar S, Park SH, Cieply B, Schupp J, Killiam E, Zhang F, et al. A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol Cell Biol. 2011;31(19):4036–51.CrossRefPubMedPubMedCentral
39.
go back to reference Fussbroich B, Wagener N, Macher-Goeppinger S, Benner A, Fälth M, Sültmann H, et al. EZH2 depletion blocks the proliferation of colon cancer cells. PLoS ONE. 2011;6(7), e21651.CrossRefPubMedPubMedCentral Fussbroich B, Wagener N, Macher-Goeppinger S, Benner A, Fälth M, Sültmann H, et al. EZH2 depletion blocks the proliferation of colon cancer cells. PLoS ONE. 2011;6(7), e21651.CrossRefPubMedPubMedCentral
40.
go back to reference Reddy EM, Chettiar ST, Kaur N, Ganeshkumar R, Shepal V, Shanbhag NC, et al. Dlxin-1, a member of MAGE family, inhibits cell proliferation, invasion and tumorigenicity of glioma stem cells. Cancer Gene Ther. 2010;18(3):206–18.CrossRefPubMed Reddy EM, Chettiar ST, Kaur N, Ganeshkumar R, Shepal V, Shanbhag NC, et al. Dlxin-1, a member of MAGE family, inhibits cell proliferation, invasion and tumorigenicity of glioma stem cells. Cancer Gene Ther. 2010;18(3):206–18.CrossRefPubMed
41.
go back to reference Xue XY, Liu ZH, Jing FM, Li YG, Liu HZ, Gao XS. Relationship between NRAGE and the radioresistance of esophageal carcinoma cell line TE13R120. Chin J Cancer. 2010;29(10):900–6.CrossRefPubMed Xue XY, Liu ZH, Jing FM, Li YG, Liu HZ, Gao XS. Relationship between NRAGE and the radioresistance of esophageal carcinoma cell line TE13R120. Chin J Cancer. 2010;29(10):900–6.CrossRefPubMed
42.
go back to reference Du Q, Zhang Y, Tian X, Li Y, Fang W. MAGE-D1 inhibits proliferation, migration and invasion of human breast cancer cells. Oncol Rep. 2009;22(3):659–65.PubMed Du Q, Zhang Y, Tian X, Li Y, Fang W. MAGE-D1 inhibits proliferation, migration and invasion of human breast cancer cells. Oncol Rep. 2009;22(3):659–65.PubMed
43.
go back to reference Shen W, Xue Q, Wu Y, Hu B, Zhu J, Zhang Y, et al. Melanoma-associated antigen family protein-D1 regulation of tumor cell migration, adhesion to endothelium, and actin structures reorganization in response to hypoxic stress. Cell Commun Adhes. 2007;14(1):21–31.CrossRefPubMed Shen W, Xue Q, Wu Y, Hu B, Zhu J, Zhang Y, et al. Melanoma-associated antigen family protein-D1 regulation of tumor cell migration, adhesion to endothelium, and actin structures reorganization in response to hypoxic stress. Cell Commun Adhes. 2007;14(1):21–31.CrossRefPubMed
44.
go back to reference Chu C, Xue B, Tu C, Feng Z, Shi Y, Miao Y, et al. NRAGE suppresses metastasis of melanoma and pancreatic cancer in vitro and in vivo. Cancer Lett. 2007;250(2):268–75.CrossRefPubMed Chu C, Xue B, Tu C, Feng Z, Shi Y, Miao Y, et al. NRAGE suppresses metastasis of melanoma and pancreatic cancer in vitro and in vivo. Cancer Lett. 2007;250(2):268–75.CrossRefPubMed
46.
go back to reference Xue B, Wen C, Shi Y, Zhao D, Li C. Human NRAGE disrupts E-cadherin/β-catenin regulated homotypic cell–cell adhesion. Biochem Biophys Res Commun. 2005;336(1):247–51.CrossRefPubMed Xue B, Wen C, Shi Y, Zhao D, Li C. Human NRAGE disrupts E-cadherin/β-catenin regulated homotypic cell–cell adhesion. Biochem Biophys Res Commun. 2005;336(1):247–51.CrossRefPubMed
47.
go back to reference Wen C, Xue B, Qin W, Yu M, Zhang M, Zhao D, et al. hNRAGE, a human neurotrophin receptor interacting MAGE homologue, regulates p53 transcriptional activity and inhibits cell proliferation. FEBS Lett. 2004;564(1-2):171–6.CrossRefPubMed Wen C, Xue B, Qin W, Yu M, Zhang M, Zhao D, et al. hNRAGE, a human neurotrophin receptor interacting MAGE homologue, regulates p53 transcriptional activity and inhibits cell proliferation. FEBS Lett. 2004;564(1-2):171–6.CrossRefPubMed
48.
go back to reference Reddy EM, Chettiar ST, Kaur N, Shepal V, Shiras A. Dlxin-1, a MAGE family protein, induces accelerated neurite outgrowth and cell survival by enhanced and early activation of MEK and Akt signalling pathways in PC12 cells. Exp Cell Res. 2010;316(14):2220–36.CrossRefPubMed Reddy EM, Chettiar ST, Kaur N, Shepal V, Shiras A. Dlxin-1, a MAGE family protein, induces accelerated neurite outgrowth and cell survival by enhanced and early activation of MEK and Akt signalling pathways in PC12 cells. Exp Cell Res. 2010;316(14):2220–36.CrossRefPubMed
49.
go back to reference Cheng C, Huang X, Ding Y, Zang W, Zhang Q. Effect of shRNA against NRAGE gene on proliferation and apoptosis of SGC7901 cells. J Zhengzhou Univ (Medical Sciences). 2008;43(2):304–6. Cheng C, Huang X, Ding Y, Zang W, Zhang Q. Effect of shRNA against NRAGE gene on proliferation and apoptosis of SGC7901 cells. J Zhengzhou Univ (Medical Sciences). 2008;43(2):304–6.
50.
go back to reference Passananti C, Fanciulli M. The anti-apoptotic factor Che-1/AATF links transcriptional regulation, cell cycle control, and DNA damage response. Cell Div. 2007;2(1):21.CrossRefPubMedPubMedCentral Passananti C, Fanciulli M. The anti-apoptotic factor Che-1/AATF links transcriptional regulation, cell cycle control, and DNA damage response. Cell Div. 2007;2(1):21.CrossRefPubMedPubMedCentral
51.
go back to reference Bragason BT, Palsdottir A. Interaction of PrP with NRAGE, a protein involved in neuronal apoptosis. Mol Cell Neurosci. 2005;29(2):232–44.CrossRefPubMed Bragason BT, Palsdottir A. Interaction of PrP with NRAGE, a protein involved in neuronal apoptosis. Mol Cell Neurosci. 2005;29(2):232–44.CrossRefPubMed
52.
go back to reference Wu Q, Qi S, Ma J, Chen F, Chen J, Li J, et al. The effect of NRAGE on cell cycle and apoptosis of human dental pulp cells and MDPC-23. Int J Clin Exp Med. 2015;8(7):10657–67.PubMedPubMedCentral Wu Q, Qi S, Ma J, Chen F, Chen J, Li J, et al. The effect of NRAGE on cell cycle and apoptosis of human dental pulp cells and MDPC-23. Int J Clin Exp Med. 2015;8(7):10657–67.PubMedPubMedCentral
53.
go back to reference Zhou L, Xue B, Guo S, Shi Y, Wen C, Li C. Construction of recombinant adenovirus vector of hNRAGE gene and its effect on cell cycle of 293 cells. Chin J Cell Mol Immunol. 2006;22(01):18–21. Zhou L, Xue B, Guo S, Shi Y, Wen C, Li C. Construction of recombinant adenovirus vector of hNRAGE gene and its effect on cell cycle of 293 cells. Chin J Cell Mol Immunol. 2006;22(01):18–21.
54.
go back to reference Xue X, Gao X, Zhou Z, Zhang P, Lu F, Duan H. A study of the relationship of the radioresistance of esophageal carcinoma cell line TE13R120 with HDAC3, NF-kB and NRAGE. Chin J Radiol Med Protecion. 2005;25(1):27–30. Xue X, Gao X, Zhou Z, Zhang P, Lu F, Duan H. A study of the relationship of the radioresistance of esophageal carcinoma cell line TE13R120 with HDAC3, NF-kB and NRAGE. Chin J Radiol Med Protecion. 2005;25(1):27–30.
55.
go back to reference Zhang Z, Yan A, Zhang Z, Luo D. Expression of NRAGE gene in gastric carcinoma and its regulation role in apoptosis. J Med Forum. 2007;28(19):17–8. Zhang Z, Yan A, Zhang Z, Luo D. Expression of NRAGE gene in gastric carcinoma and its regulation role in apoptosis. J Med Forum. 2007;28(19):17–8.
56.
go back to reference Matsuda T, Suzuki H, Oishi I, Kani S, Kuroda Y, Komori T, et al. The receptor tyrosine kinase Ror2 associates with the melanoma-associated antigen (MAGE) family protein dlxin-1 and regulates its intracellular distribution. J Biol Chem. 2003;278(31):29057–64.CrossRefPubMed Matsuda T, Suzuki H, Oishi I, Kani S, Kuroda Y, Komori T, et al. The receptor tyrosine kinase Ror2 associates with the melanoma-associated antigen (MAGE) family protein dlxin-1 and regulates its intracellular distribution. J Biol Chem. 2003;278(31):29057–64.CrossRefPubMed
57.
go back to reference Zhou H, Zhang G, Xue X, Yang Y, Yang Y, Chang X, Ge X, Xiao Z, Guo H, Wang Y. Identification of novel NRAGE involved in the radioresistance of esophageal cancer cells. Tumour Biol 2016. Zhou H, Zhang G, Xue X, Yang Y, Yang Y, Chang X, Ge X, Xiao Z, Guo H, Wang Y. Identification of novel NRAGE involved in the radioresistance of esophageal cancer cells. Tumour Biol 2016.
Metadata
Title
Complex roles of NRAGE on tumor
Authors
Ge Zhang
Huandi Zhou
Xiaoying Xue
Publication date
01-09-2016
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 9/2016
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-016-5084-0

Other articles of this Issue 9/2016

Tumor Biology 9/2016 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine