Low cytoplasmic NUB1 protein exerts hypoxic cell death with poorer prognosis in oestrogen receptor negative breast cancer patients

•1) The study identified that downregulated AIPL1 leads to the deactivation of NUB1 under hypoxic conditions, resulting in cell cycle arrest in breast cancer cells. 2) Low cytoplasmic NUB1 expression is significantly associated with poorer overall survival, particularly in ER-negative breast cancer...

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Veröffentlicht in:Translational oncology Jg. 49; S. 102106
Hauptverfasser: Tan, Ka-Liong, Haider, Syed, Zois, Christos E., Hu, Jianting, Turley, Helen, Leek, Russell, Buffa, Francesca, Acuto, Oreste, Harris, Adrian L., Pezzella, Francesco
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Sprache:Englisch
Veröffentlicht: United States Elsevier Inc 01.11.2024
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ISSN:1936-5233, 1936-5233
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Abstract •1) The study identified that downregulated AIPL1 leads to the deactivation of NUB1 under hypoxic conditions, resulting in cell cycle arrest in breast cancer cells. 2) Low cytoplasmic NUB1 expression is significantly associated with poorer overall survival, particularly in ER-negative breast cancer patients, indicating its potential as a prognostic biomarker. 3) NUB1’s role in preventing cell cycle arrest is crucial, with its absence linked to the upregulation of p21 and p27 and poorer survival outcomes in breast cancer. Current prognostic biomarkers fall short in stratifying Oestrogen receptor (ER)-negative breast cancer patients regarding tumour progression risk at diagnosis. The role of AIPL1 in activating its tumour suppressor client protein, NEDD8 Ultimate Buster-1 (NUB1) remains unknown in cancer. Our study demonstrated how downregulated AIPL1 results in the deactivated NUB1 protein under hypoxic conditions. We examined the AIPL1-NUB1 pathwayin vitro using cell lines i.e. MCF-7, MDA-MB-231, RCC4 etc. NUB1 expression was assessed using Oncomine, and cBioPortal was performed to assess NUB1′s prognostic significance in human cancers. In the John Radcliffe Hospital cohort (n = 122), immunohistochemistry analysis revealed downregulated AIPL1 (Log2 fold change=-0.28; p < 0.001) and upregulated NUB1 transcripts (Log2 fold change=0.59; p < 0.001) compared to adjacent normal tissues. In severe chronic hypoxia, multimerised AIPL1 localisedin the cytoplasm while NUB1 protein migrated to the nucleus, where the absence of NUB1 nuclear localisation led to cell cycle arrest. Biopsies showed that patients with lower cytoplasmic NUB1 expression (n = 57) had poorer overall survival compared to those with higher cytoplasmic expression (n = 57), HR=1.78; 95 % CI=1.01–3.35, p = 0.048. Low NUB1 protein levels in both normoxic and hypoxic conditions were associated with cell cycle arrest and upregulation ofp21 and p27 in breast cancer cell lines, correlating significantly withpoorer survival outcomes in all breast cancer and ER-negative breast cancer patients. [Display omitted]
AbstractList Current prognostic biomarkers fall short in stratifying Oestrogen receptor (ER)-negative breast cancer patients regarding tumour progression risk at diagnosis. The role of AIPL1 in activating its tumour suppressor client protein, NEDD8 Ultimate Buster-1 (NUB1) remains unknown in cancer. Our study demonstrated how downregulated AIPL1 results in the deactivated NUB1 protein under hypoxic conditions. We examined the AIPL1-NUB1 pathwayin vitro using cell lines i.e. MCF-7, MDA-MB-231, RCC4 etc. NUB1 expression was assessed using Oncomine, and cBioPortal was performed to assess NUB1's prognostic significance in human cancers. In the John Radcliffe Hospital cohort (n = 122), immunohistochemistry analysis revealed downregulated AIPL1 (Log2 fold change=-0.28; p < 0.001) and upregulated NUB1 transcripts (Log2 fold change=0.59; p < 0.001) compared to adjacent normal tissues. In severe chronic hypoxia, multimerised AIPL1 localisedin the cytoplasm while NUB1 protein migrated to the nucleus, where the absence of NUB1 nuclear localisation led to cell cycle arrest. Biopsies showed that patients with lower cytoplasmic NUB1 expression (n = 57) had poorer overall survival compared to those with higher cytoplasmic expression (n = 57), HR=1.78; 95 % CI=1.01-3.35, p = 0.048. Low NUB1 protein levels in both normoxic and hypoxic conditions were associated with cell cycle arrest and upregulation ofp21 and p27 in breast cancer cell lines, correlating significantly withpoorer survival outcomes in all breast cancer and ER-negative breast cancer patients.
•1) The study identified that downregulated AIPL1 leads to the deactivation of NUB1 under hypoxic conditions, resulting in cell cycle arrest in breast cancer cells. 2) Low cytoplasmic NUB1 expression is significantly associated with poorer overall survival, particularly in ER-negative breast cancer patients, indicating its potential as a prognostic biomarker. 3) NUB1’s role in preventing cell cycle arrest is crucial, with its absence linked to the upregulation of p21 and p27 and poorer survival outcomes in breast cancer. Current prognostic biomarkers fall short in stratifying Oestrogen receptor (ER)-negative breast cancer patients regarding tumour progression risk at diagnosis. The role of AIPL1 in activating its tumour suppressor client protein, NEDD8 Ultimate Buster-1 (NUB1) remains unknown in cancer. Our study demonstrated how downregulated AIPL1 results in the deactivated NUB1 protein under hypoxic conditions. We examined the AIPL1-NUB1 pathwayin vitro using cell lines i.e. MCF-7, MDA-MB-231, RCC4 etc. NUB1 expression was assessed using Oncomine, and cBioPortal was performed to assess NUB1′s prognostic significance in human cancers. In the John Radcliffe Hospital cohort (n = 122), immunohistochemistry analysis revealed downregulated AIPL1 (Log2 fold change=-0.28; p < 0.001) and upregulated NUB1 transcripts (Log2 fold change=0.59; p < 0.001) compared to adjacent normal tissues. In severe chronic hypoxia, multimerised AIPL1 localisedin the cytoplasm while NUB1 protein migrated to the nucleus, where the absence of NUB1 nuclear localisation led to cell cycle arrest. Biopsies showed that patients with lower cytoplasmic NUB1 expression (n = 57) had poorer overall survival compared to those with higher cytoplasmic expression (n = 57), HR=1.78; 95 % CI=1.01–3.35, p = 0.048. Low NUB1 protein levels in both normoxic and hypoxic conditions were associated with cell cycle arrest and upregulation ofp21 and p27 in breast cancer cell lines, correlating significantly withpoorer survival outcomes in all breast cancer and ER-negative breast cancer patients. [Display omitted]
Current prognostic biomarkers fall short in stratifying Oestrogen receptor (ER)-negative breast cancer patients regarding tumour progression risk at diagnosis. The role of AIPL1 in activating its tumour suppressor client protein, NEDD8 Ultimate Buster-1 (NUB1) remains unknown in cancer. Our study demonstrated how downregulated AIPL1 results in the deactivated NUB1 protein under hypoxic conditions. We examined the AIPL1-NUB1 pathwayin vitro using cell lines i.e. MCF-7, MDA-MB-231, RCC4 etc. NUB1 expression was assessed using Oncomine, and cBioPortal was performed to assess NUB1's prognostic significance in human cancers. In the John Radcliffe Hospital cohort (n = 122), immunohistochemistry analysis revealed downregulated AIPL1 (Log2 fold change=-0.28; p < 0.001) and upregulated NUB1 transcripts (Log2 fold change=0.59; p < 0.001) compared to adjacent normal tissues. In severe chronic hypoxia, multimerised AIPL1 localisedin the cytoplasm while NUB1 protein migrated to the nucleus, where the absence of NUB1 nuclear localisation led to cell cycle arrest. Biopsies showed that patients with lower cytoplasmic NUB1 expression (n = 57) had poorer overall survival compared to those with higher cytoplasmic expression (n = 57), HR=1.78; 95 % CI=1.01-3.35, p = 0.048. Low NUB1 protein levels in both normoxic and hypoxic conditions were associated with cell cycle arrest and upregulation ofp21 and p27 in breast cancer cell lines, correlating significantly withpoorer survival outcomes in all breast cancer and ER-negative breast cancer patients.Current prognostic biomarkers fall short in stratifying Oestrogen receptor (ER)-negative breast cancer patients regarding tumour progression risk at diagnosis. The role of AIPL1 in activating its tumour suppressor client protein, NEDD8 Ultimate Buster-1 (NUB1) remains unknown in cancer. Our study demonstrated how downregulated AIPL1 results in the deactivated NUB1 protein under hypoxic conditions. We examined the AIPL1-NUB1 pathwayin vitro using cell lines i.e. MCF-7, MDA-MB-231, RCC4 etc. NUB1 expression was assessed using Oncomine, and cBioPortal was performed to assess NUB1's prognostic significance in human cancers. In the John Radcliffe Hospital cohort (n = 122), immunohistochemistry analysis revealed downregulated AIPL1 (Log2 fold change=-0.28; p < 0.001) and upregulated NUB1 transcripts (Log2 fold change=0.59; p < 0.001) compared to adjacent normal tissues. In severe chronic hypoxia, multimerised AIPL1 localisedin the cytoplasm while NUB1 protein migrated to the nucleus, where the absence of NUB1 nuclear localisation led to cell cycle arrest. Biopsies showed that patients with lower cytoplasmic NUB1 expression (n = 57) had poorer overall survival compared to those with higher cytoplasmic expression (n = 57), HR=1.78; 95 % CI=1.01-3.35, p = 0.048. Low NUB1 protein levels in both normoxic and hypoxic conditions were associated with cell cycle arrest and upregulation ofp21 and p27 in breast cancer cell lines, correlating significantly withpoorer survival outcomes in all breast cancer and ER-negative breast cancer patients.
•1) The study identified that downregulated AIPL1 leads to the deactivation of NUB1 under hypoxic conditions, resulting in cell cycle arrest in breast cancer cells. 2) Low cytoplasmic NUB1 expression is significantly associated with poorer overall survival, particularly in ER-negative breast cancer patients, indicating its potential as a prognostic biomarker. 3) NUB1’s role in preventing cell cycle arrest is crucial, with its absence linked to the upregulation of p21 and p27 and poorer survival outcomes in breast cancer. Current prognostic biomarkers fall short in stratifying Oestrogen receptor (ER)-negative breast cancer patients regarding tumour progression risk at diagnosis. The role of AIPL1 in activating its tumour suppressor client protein, NEDD8 Ultimate Buster-1 (NUB1) remains unknown in cancer. Our study demonstrated how downregulated AIPL1 results in the deactivated NUB1 protein under hypoxic conditions. We examined the AIPL1-NUB1 pathwayin vitro using cell lines i.e. MCF-7, MDA-MB-231, RCC4 etc. NUB1 expression was assessed using Oncomine, and cBioPortal was performed to assess NUB1′s prognostic significance in human cancers. In the John Radcliffe Hospital cohort (n = 122), immunohistochemistry analysis revealed downregulated AIPL1 (Log2 fold change=-0.28; p < 0.001) and upregulated NUB1 transcripts (Log2 fold change=0.59; p < 0.001) compared to adjacent normal tissues. In severe chronic hypoxia, multimerised AIPL1 localisedin the cytoplasm while NUB1 protein migrated to the nucleus, where the absence of NUB1 nuclear localisation led to cell cycle arrest. Biopsies showed that patients with lower cytoplasmic NUB1 expression (n = 57) had poorer overall survival compared to those with higher cytoplasmic expression (n = 57), HR=1.78; 95 % CI=1.01–3.35, p = 0.048. Low NUB1 protein levels in both normoxic and hypoxic conditions were associated with cell cycle arrest and upregulation ofp21 and p27 in breast cancer cell lines, correlating significantly withpoorer survival outcomes in all breast cancer and ER-negative breast cancer patients. Image, graphical abstract
ArticleNumber 102106
Author Hu, Jianting
Zois, Christos E.
Acuto, Oreste
Pezzella, Francesco
Turley, Helen
Buffa, Francesca
Tan, Ka-Liong
Harris, Adrian L.
Leek, Russell
Haider, Syed
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  email: francesco.pezzella@ndcls.ox.ac.uk
  organization: Tumour Pathology Laboratory, Nuffield Division of Clinical Laboratory Sciences, Radcliffe Department of Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
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Cites_doi 10.1038/nn.3367
10.1074/jbc.M407871200
10.1038/nature11412
10.1038/ncomms11479
10.1126/science.1059817
10.1038/sj.bjc.6605574
10.1016/j.bbrc.2005.09.014
10.1038/71732
10.1074/jbc.M108636200
10.1016/j.molcel.2008.08.021
10.1016/j.cell.2015.09.033
10.2353/ajpath.2006.051067
10.1074/jbc.M004847200
10.1128/MCB.16.9.4691
10.1074/jbc.M100920200
10.1038/ng1532
10.1186/1471-2407-3-31
10.1016/j.prp.2020.153002
10.1158/0008-5472.CAN-03-3620
10.1073/pnas.211566398
10.1016/j.tibs.2008.01.005
10.1111/j.1365-2559.1991.tb00229.x
10.1038/sj.onc.1203985
10.6000/1929-2279.2013.02.03.5
10.1093/hmg/11.7.823
10.1074/jbc.M110.188706
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Keywords Immunohistochemistry
Biomarkers
NUB1
Oestrogen receptor
Language English
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References Wu, Chen, Pan (bib0029) 2000; 275
Adaikalavan, R.
Tanji, Tanaka, Kamitani (bib0013) 2005; 337
Pereira (bib0025) 2016; 7
Anon (bib0026) 2012; 490
Dyrskjot (bib0007) 2004; 64
Ramasamy (bib0002) 2009
Tsuchiya, Iseda, Hino (bib0005) 1996; 56
Kito, Yeh, Kamitani (bib0012) 2001; 276
Lenburg (bib0008) 2003; 3
2009., Oxford.
Tanji (bib0017) 2006; 169
Chen (bib0004) 1996; 16
Basso (bib0006) 2005; 37
Ramaswamy (bib0009) 2001; 98
van der Spuy (bib0016) 2002; 11
Elston, Ellis (bib0022) 1991; 19
Kamitani (bib0011) 2001; 276
Ivan (bib0031) 2001; 292
in
Groettrup (bib0014) 2008; 33
Ciriello (bib0027) 2015; 163
Ryu (bib0020) 2011; 286
Yao, Lu (bib0033) 2015; 5
Zhang (bib0018) 2020; 216
Saha, Deshaies (bib0021) 2008; 32
Hosono (bib0019) 2010; 102
Lu (bib0032) 2013; 16
Calderwood (bib0001) 2013; 2013
van der Spuy, Cheetham (bib0010) 2004; 279
Sohocki (bib0015) 2000; 24
Schoenfeld (bib0030) 2000; 19
Hu (bib0003) 2013; 2
Lu (10.1016/j.tranon.2024.102106_bib0032) 2013; 16
Lenburg (10.1016/j.tranon.2024.102106_bib0008) 2003; 3
Ryu (10.1016/j.tranon.2024.102106_bib0020) 2011; 286
Dyrskjot (10.1016/j.tranon.2024.102106_bib0007) 2004; 64
Kito (10.1016/j.tranon.2024.102106_bib0012) 2001; 276
van der Spuy (10.1016/j.tranon.2024.102106_bib0016) 2002; 11
Hosono (10.1016/j.tranon.2024.102106_bib0019) 2010; 102
Ramaswamy (10.1016/j.tranon.2024.102106_bib0009) 2001; 98
Groettrup (10.1016/j.tranon.2024.102106_bib0014) 2008; 33
Tanji (10.1016/j.tranon.2024.102106_bib0017) 2006; 169
Saha (10.1016/j.tranon.2024.102106_bib0021) 2008; 32
Calderwood (10.1016/j.tranon.2024.102106_bib0001) 2013; 2013
Anon (10.1016/j.tranon.2024.102106_bib0026) 2012; 490
Ciriello (10.1016/j.tranon.2024.102106_bib0027) 2015; 163
Hu (10.1016/j.tranon.2024.102106_bib0003) 2013; 2
Yao (10.1016/j.tranon.2024.102106_bib0033) 2015; 5
Basso (10.1016/j.tranon.2024.102106_bib0006) 2005; 37
Elston (10.1016/j.tranon.2024.102106_bib0022) 1991; 19
Sohocki (10.1016/j.tranon.2024.102106_bib0015) 2000; 24
Pereira (10.1016/j.tranon.2024.102106_bib0025) 2016; 7
van der Spuy (10.1016/j.tranon.2024.102106_bib0010) 2004; 279
Ivan (10.1016/j.tranon.2024.102106_bib0031) 2001; 292
Kamitani (10.1016/j.tranon.2024.102106_bib0011) 2001; 276
Schoenfeld (10.1016/j.tranon.2024.102106_bib0030) 2000; 19
Chen (10.1016/j.tranon.2024.102106_bib0004) 1996; 16
Tanji (10.1016/j.tranon.2024.102106_bib0013) 2005; 337
Zhang (10.1016/j.tranon.2024.102106_bib0018) 2020; 216
10.1016/j.tranon.2024.102106_bib0028
Ramasamy (10.1016/j.tranon.2024.102106_bib0002) 2009
Tsuchiya (10.1016/j.tranon.2024.102106_bib0005) 1996; 56
Wu (10.1016/j.tranon.2024.102106_bib0029) 2000; 275
40221214 - Transl Oncol. 2025 May;55:102354. doi: 10.1016/j.tranon.2025.102354.
References_xml – volume: 102
  start-page: 873
  year: 2010
  end-page: 882
  ident: bib0019
  article-title: NUB1, an interferon-inducible protein, mediates anti-proliferative actions and apoptosis in renal cell carcinoma cells through cell-cycle regulation
  publication-title: Br. J. Cancer
– volume: 216
  year: 2020
  ident: bib0018
  article-title: Overexpression of negative regulator of ubiquitin-like proteins 1 (NUB1) inhibits proliferation and invasion of gastric cancer cells through upregulation of p27Kip1 and inhibition of epithelial-mesenchymal transition
  publication-title: Pathol. Res. Pract.
– volume: 56
  start-page: 2881
  year: 1996
  end-page: 2885
  ident: bib0005
  article-title: Identification of a novel protein (VBP-1) binding to the von Hippel-Lindau (VHL) tumor suppressor gene product
  publication-title: Cancer Res.
– volume: 337
  start-page: 116
  year: 2005
  end-page: 120
  ident: bib0013
  article-title: Interaction of NUB1 with the proteasome subunit S5a
  publication-title: Biochem. Biophys. Res. Commun.
– volume: 98
  start-page: 15149
  year: 2001
  end-page: 15154
  ident: bib0009
  article-title: Multiclass cancer diagnosis using tumor gene expression signatures
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
– reference: Adaikalavan, R.,
– reference: , in
– volume: 286
  start-page: 6963
  year: 2011
  end-page: 6970
  ident: bib0020
  article-title: Hypoxia-inducible factor alpha subunit stabilization by NEDD8 conjugation is reactive oxygen species-dependent
  publication-title: J. Biol. Chem.
– volume: 16
  start-page: 4691
  year: 1996
  end-page: 4699
  ident: bib0004
  article-title: A new member of the hsp90 family of molecular chaperones interacts with the retinoblastoma protein during mitosis and after heat shock
  publication-title: Mol. Cell. Biol.
– volume: 292
  start-page: 464
  year: 2001
  end-page: 468
  ident: bib0031
  article-title: HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing
  publication-title: Science
– volume: 19
  start-page: 5851
  year: 2000
  end-page: 5857
  ident: bib0030
  article-title: The von Hippel-Lindau tumor suppressor gene protects cells from UV-mediated apoptosis
  publication-title: Oncogene
– reference: . 2009., Oxford.
– volume: 16
  start-page: 562
  year: 2013
  end-page: 570
  ident: bib0032
  article-title: Identification of NUB1 as a suppressor of mutant Huntington toxicity via enhanced protein clearance
  publication-title: Nat. Neurosci.
– volume: 275
  start-page: 32317
  year: 2000
  end-page: 32324
  ident: bib0029
  article-title: Conjugation of Nedd8 to CUL1 enhances the ability of the ROC1-CUL1 complex to promote ubiquitin polymerization
  publication-title: J. Biol. Chem.
– volume: 3
  start-page: 31
  year: 2003
  ident: bib0008
  article-title: Previously unidentified changes in renal cell carcinoma gene expression identified by parametric analysis of microarray data
  publication-title: BMC Cancer
– volume: 33
  start-page: 230
  year: 2008
  end-page: 237
  ident: bib0014
  article-title: Activating the ubiquitin family: UBA6 challenges the field
  publication-title: Trend. Biochem. Sci.
– volume: 169
  start-page: 553
  year: 2006
  end-page: 565
  ident: bib0017
  article-title: NUB1 suppresses the formation of Lewy body-like inclusions by proteasomal degradation of synphilin-1
  publication-title: Am. J. Pathol.
– volume: 24
  start-page: 79
  year: 2000
  end-page: 83
  ident: bib0015
  article-title: Mutations in a new photoreceptor-pineal gene on 17p cause Leber congenital amaurosis
  publication-title: Nat. Genet.
– volume: 490
  start-page: 61
  year: 2012
  end-page: 70
  ident: bib0026
  article-title: Comprehensive molecular portraits of human breast tumours
  publication-title: Nature
– volume: 2
  start-page: 194
  year: 2013
  end-page: 210
  ident: bib0003
  article-title: TRAP1 is involved in cell cycle regulated by retinoblastoma susceptibility gene (RB1) in early hypoxia and has variable expression patterns in human tumors
  publication-title: J. Can. Res. Update.
– volume: 37
  start-page: 382
  year: 2005
  end-page: 390
  ident: bib0006
  article-title: Reverse engineering of regulatory networks in human B cells
  publication-title: Nat. Genet.
– volume: 276
  start-page: 20603
  year: 2001
  end-page: 20609
  ident: bib0012
  article-title: NUB1, a NEDD8-interacting protein, is induced by interferon and down-regulates the NEDD8 expression
  publication-title: J. Biol. Chem.
– volume: 2013
  year: 2013
  ident: bib0001
  article-title: Molecular cochaperones: tumor growth and cancer treatment
  publication-title: Scientifica. (Cairo).
– volume: 7
  start-page: 11479
  year: 2016
  ident: bib0025
  article-title: The somatic mutation profiles of 2,433 breast cancers refines their genomic and transcriptomic landscapes
  publication-title: Nat. Commun.
– volume: 11
  start-page: 823
  year: 2002
  end-page: 831
  ident: bib0016
  article-title: The Leber congenital amaurosis gene product AIPL1 is localized exclusively in rod photoreceptors of the adult human retina
  publication-title: Hum. Mol. Genet.
– volume: 279
  start-page: 48038
  year: 2004
  end-page: 48047
  ident: bib0010
  article-title: The Leber congenital amaurosis protein AIPL1 modulates the nuclear translocation of NUB1 and suppresses inclusion formation by NUB1 fragments
  publication-title: J. Biol. Chem.
– volume: 163
  start-page: 506
  year: 2015
  end-page: 519
  ident: bib0027
  article-title: Comprehensive molecular portraits of invasive lobular breast cancer
  publication-title: Cell
– volume: 32
  start-page: 21
  year: 2008
  end-page: 31
  ident: bib0021
  article-title: Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation
  publication-title: Mol. Cell.
– volume: 5
  start-page: 129
  year: 2015
  end-page: 136
  ident: bib0033
  article-title: NUB1 suppression of huntington toxicity: mechanistic insights. Research and Reports in Biochemistry
  publication-title: Res. Rep. Biochem.
– volume: 64
  start-page: 4040
  year: 2004
  end-page: 4048
  ident: bib0007
  article-title: in situ
  publication-title: Cancer Res.
– volume: 276
  start-page: 46655
  year: 2001
  end-page: 46660
  ident: bib0011
  article-title: Targeting of NEDD8 and its conjugates for proteasomal degradation by NUB1
  publication-title: J. Biol. Chem.
– start-page: 152
  year: 2009
  ident: bib0002
  article-title: Increasing Statistical Power and Generalizability in Genomic Microarray Research
– volume: 19
  start-page: 403
  year: 1991
  end-page: 410
  ident: bib0022
  article-title: Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up
  publication-title: Histopathology
– ident: 10.1016/j.tranon.2024.102106_bib0028
– volume: 16
  start-page: 562
  issue: 5
  year: 2013
  ident: 10.1016/j.tranon.2024.102106_bib0032
  article-title: Identification of NUB1 as a suppressor of mutant Huntington toxicity via enhanced protein clearance
  publication-title: Nat. Neurosci.
  doi: 10.1038/nn.3367
– volume: 2013
  year: 2013
  ident: 10.1016/j.tranon.2024.102106_bib0001
  article-title: Molecular cochaperones: tumor growth and cancer treatment
  publication-title: Scientifica. (Cairo).
– volume: 279
  start-page: 48038
  issue: 46
  year: 2004
  ident: 10.1016/j.tranon.2024.102106_bib0010
  article-title: The Leber congenital amaurosis protein AIPL1 modulates the nuclear translocation of NUB1 and suppresses inclusion formation by NUB1 fragments
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M407871200
– volume: 490
  start-page: 61
  issue: 7418
  year: 2012
  ident: 10.1016/j.tranon.2024.102106_bib0026
  article-title: Comprehensive molecular portraits of human breast tumours
  publication-title: Nature
  doi: 10.1038/nature11412
– volume: 7
  start-page: 11479
  year: 2016
  ident: 10.1016/j.tranon.2024.102106_bib0025
  article-title: The somatic mutation profiles of 2,433 breast cancers refines their genomic and transcriptomic landscapes
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms11479
– volume: 292
  start-page: 464
  issue: 5516
  year: 2001
  ident: 10.1016/j.tranon.2024.102106_bib0031
  article-title: HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing
  publication-title: Science
  doi: 10.1126/science.1059817
– volume: 102
  start-page: 873
  issue: 5
  year: 2010
  ident: 10.1016/j.tranon.2024.102106_bib0019
  article-title: NUB1, an interferon-inducible protein, mediates anti-proliferative actions and apoptosis in renal cell carcinoma cells through cell-cycle regulation
  publication-title: Br. J. Cancer
  doi: 10.1038/sj.bjc.6605574
– volume: 337
  start-page: 116
  issue: 1
  year: 2005
  ident: 10.1016/j.tranon.2024.102106_bib0013
  article-title: Interaction of NUB1 with the proteasome subunit S5a
  publication-title: Biochem. Biophys. Res. Commun.
  doi: 10.1016/j.bbrc.2005.09.014
– volume: 24
  start-page: 79
  issue: 1
  year: 2000
  ident: 10.1016/j.tranon.2024.102106_bib0015
  article-title: Mutations in a new photoreceptor-pineal gene on 17p cause Leber congenital amaurosis
  publication-title: Nat. Genet.
  doi: 10.1038/71732
– volume: 276
  start-page: 46655
  issue: 49
  year: 2001
  ident: 10.1016/j.tranon.2024.102106_bib0011
  article-title: Targeting of NEDD8 and its conjugates for proteasomal degradation by NUB1
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M108636200
– volume: 32
  start-page: 21
  issue: 1
  year: 2008
  ident: 10.1016/j.tranon.2024.102106_bib0021
  article-title: Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation
  publication-title: Mol. Cell.
  doi: 10.1016/j.molcel.2008.08.021
– volume: 163
  start-page: 506
  issue: 2
  year: 2015
  ident: 10.1016/j.tranon.2024.102106_bib0027
  article-title: Comprehensive molecular portraits of invasive lobular breast cancer
  publication-title: Cell
  doi: 10.1016/j.cell.2015.09.033
– volume: 169
  start-page: 553
  issue: 2
  year: 2006
  ident: 10.1016/j.tranon.2024.102106_bib0017
  article-title: NUB1 suppresses the formation of Lewy body-like inclusions by proteasomal degradation of synphilin-1
  publication-title: Am. J. Pathol.
  doi: 10.2353/ajpath.2006.051067
– volume: 275
  start-page: 32317
  issue: 41
  year: 2000
  ident: 10.1016/j.tranon.2024.102106_bib0029
  article-title: Conjugation of Nedd8 to CUL1 enhances the ability of the ROC1-CUL1 complex to promote ubiquitin polymerization
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M004847200
– volume: 16
  start-page: 4691
  issue: 9
  year: 1996
  ident: 10.1016/j.tranon.2024.102106_bib0004
  article-title: A new member of the hsp90 family of molecular chaperones interacts with the retinoblastoma protein during mitosis and after heat shock
  publication-title: Mol. Cell. Biol.
  doi: 10.1128/MCB.16.9.4691
– volume: 276
  start-page: 20603
  issue: 23
  year: 2001
  ident: 10.1016/j.tranon.2024.102106_bib0012
  article-title: NUB1, a NEDD8-interacting protein, is induced by interferon and down-regulates the NEDD8 expression
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M100920200
– volume: 37
  start-page: 382
  issue: 4
  year: 2005
  ident: 10.1016/j.tranon.2024.102106_bib0006
  article-title: Reverse engineering of regulatory networks in human B cells
  publication-title: Nat. Genet.
  doi: 10.1038/ng1532
– volume: 5
  start-page: 129
  issue: 5
  year: 2015
  ident: 10.1016/j.tranon.2024.102106_bib0033
  article-title: NUB1 suppression of huntington toxicity: mechanistic insights. Research and Reports in Biochemistry
  publication-title: Res. Rep. Biochem.
– volume: 56
  start-page: 2881
  issue: 13
  year: 1996
  ident: 10.1016/j.tranon.2024.102106_bib0005
  article-title: Identification of a novel protein (VBP-1) binding to the von Hippel-Lindau (VHL) tumor suppressor gene product
  publication-title: Cancer Res.
– start-page: 152
  year: 2009
  ident: 10.1016/j.tranon.2024.102106_bib0002
– volume: 3
  start-page: 31
  year: 2003
  ident: 10.1016/j.tranon.2024.102106_bib0008
  article-title: Previously unidentified changes in renal cell carcinoma gene expression identified by parametric analysis of microarray data
  publication-title: BMC Cancer
  doi: 10.1186/1471-2407-3-31
– volume: 216
  issue: 8
  year: 2020
  ident: 10.1016/j.tranon.2024.102106_bib0018
  article-title: Overexpression of negative regulator of ubiquitin-like proteins 1 (NUB1) inhibits proliferation and invasion of gastric cancer cells through upregulation of p27Kip1 and inhibition of epithelial-mesenchymal transition
  publication-title: Pathol. Res. Pract.
  doi: 10.1016/j.prp.2020.153002
– volume: 64
  start-page: 4040
  issue: 11
  year: 2004
  ident: 10.1016/j.tranon.2024.102106_bib0007
  article-title: Gene expression in the urinary bladder: a common carcinoma in situ gene expression signature exists disregarding histopathological classification
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-03-3620
– volume: 98
  start-page: 15149
  issue: 26
  year: 2001
  ident: 10.1016/j.tranon.2024.102106_bib0009
  article-title: Multiclass cancer diagnosis using tumor gene expression signatures
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.211566398
– volume: 33
  start-page: 230
  issue: 5
  year: 2008
  ident: 10.1016/j.tranon.2024.102106_bib0014
  article-title: Activating the ubiquitin family: UBA6 challenges the field
  publication-title: Trend. Biochem. Sci.
  doi: 10.1016/j.tibs.2008.01.005
– volume: 19
  start-page: 403
  issue: 5
  year: 1991
  ident: 10.1016/j.tranon.2024.102106_bib0022
  article-title: Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up
  publication-title: Histopathology
  doi: 10.1111/j.1365-2559.1991.tb00229.x
– volume: 19
  start-page: 5851
  issue: 51
  year: 2000
  ident: 10.1016/j.tranon.2024.102106_bib0030
  article-title: The von Hippel-Lindau tumor suppressor gene protects cells from UV-mediated apoptosis
  publication-title: Oncogene
  doi: 10.1038/sj.onc.1203985
– volume: 2
  start-page: 194
  issue: 3
  year: 2013
  ident: 10.1016/j.tranon.2024.102106_bib0003
  article-title: TRAP1 is involved in cell cycle regulated by retinoblastoma susceptibility gene (RB1) in early hypoxia and has variable expression patterns in human tumors
  publication-title: J. Can. Res. Update.
  doi: 10.6000/1929-2279.2013.02.03.5
– volume: 11
  start-page: 823
  issue: 7
  year: 2002
  ident: 10.1016/j.tranon.2024.102106_bib0016
  article-title: The Leber congenital amaurosis gene product AIPL1 is localized exclusively in rod photoreceptors of the adult human retina
  publication-title: Hum. Mol. Genet.
  doi: 10.1093/hmg/11.7.823
– volume: 286
  start-page: 6963
  issue: 9
  year: 2011
  ident: 10.1016/j.tranon.2024.102106_bib0020
  article-title: Hypoxia-inducible factor alpha subunit stabilization by NEDD8 conjugation is reactive oxygen species-dependent
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M110.188706
– reference: 40221214 - Transl Oncol. 2025 May;55:102354. doi: 10.1016/j.tranon.2025.102354.
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Snippet •1) The study identified that downregulated AIPL1 leads to the deactivation of NUB1 under hypoxic conditions, resulting in cell cycle arrest in breast cancer...
Current prognostic biomarkers fall short in stratifying Oestrogen receptor (ER)-negative breast cancer patients regarding tumour progression risk at diagnosis....
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StartPage 102106
SubjectTerms Biomarkers
Immunohistochemistry
NUB1
Oestrogen receptor
Original Research
Title Low cytoplasmic NUB1 protein exerts hypoxic cell death with poorer prognosis in oestrogen receptor negative breast cancer patients
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https://dx.doi.org/10.1016/j.tranon.2024.102106
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